Analyze Diet
Antioxidants (Basel, Switzerland)2019; 8(11); 567; doi: 10.3390/antiox8110567

Redox Regulation and Oxidative Stress: The Particular Case of the Stallion Spermatozoa.

Abstract: Redox regulation and oxidative stress have become areas of major interest in spermatology. Alteration of redox homeostasis is recognized as a significant cause of male factor infertility and is behind the damage that spermatozoa experience after freezing and thawing or conservation in a liquid state. While for a long time, oxidative stress was just considered an overproduction of reactive oxygen species, nowadays it is considered as a consequence of redox deregulation. Many essential aspects of spermatozoa functionality are redox regulated, with reversible oxidation of thiols in cysteine residues of key proteins acting as an "on-off" switch controlling sperm function. However, if deregulation occurs, these residues may experience irreversible oxidation and oxidative stress, leading to malfunction and ultimately death of the spermatozoa. Stallion spermatozoa are "professional producers" of reactive oxygen species due to their intense mitochondrial activity, and thus sophisticated systems to control redox homeostasis are also characteristic of the spermatozoa in the horse. As a result, and combined with the fact that embryos can easily be collected in this species, horses are a good model for the study of redox biology in the spermatozoa and its impact on the embryo.
Publication Date: 2019-11-19 PubMed ID: 31752408PubMed Central: PMC6912273DOI: 10.3390/antiox8110567Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
  • Journal Article
  • Review

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

This research article provides an overview of the role of redox regulation and oxidative stress in the function and preservation of stallion spermatoa, and its implications for male infertility.

Concept of Redox Homeostasis and Oxidative Stress in Spermatology

  • Redox regulation and oxidative stress have emerged as important areas of study in spermatology, the scientific study of sperm cells and their function.
  • Disturbance of redox homeostasis (the balance of oxidation and reduction reactions in the body) is seen as a significant reason behind male infertility.
  • This imbalance also causes damage to sperm cells through processes like freezing and thawing or during preservation in a liquid state.

Reversible and Irreversible Oxidation Impact on Sperm Function

  • Much of how sperm cells function is determined by redox regulation. This includes reversible oxidation of thiols in cysteine residues – chemicals found in key proteins – which control sperm function like an “on-off” switch.
  • If redox homeostasis is disrupted, irreversible oxidation may occur, causing oxidative stress. This can lead to the malfunctions and death of sperm cells.

Stallion Spermatozoa as Reactive Oxygen Species Producers

  • Stallion spermatozoa produce a large amount of reactive oxygen species (ROS) due to their high mitochondrial activity. Mitochondria are the powerhouses of cells, generating most of the cell’s supply of adenosine triphosphate (ATP), which is used as a source of chemical energy.
  • Because of this intense activity, stallion spermatozoa also have intricate systems to balance redox homeostasis.

Horses as a Model for Redox Biology Studies

  • Given these characteristics, combined with the ability to easily collect embryos from horses, this species offers a good model for studying the impact of redox biology on sperm cells and embryos.

Cite This Article

APA
Peña FJ, O'Flaherty C, Ortiz Rodríguez JM, Martín Cano FE, Gaitskell-Phillips GL, Gil MC, Ortega Ferrusola C. (2019). Redox Regulation and Oxidative Stress: The Particular Case of the Stallion Spermatozoa. Antioxidants (Basel), 8(11), 567. https://doi.org/10.3390/antiox8110567

Publication

ISSN: 2076-3921
NlmUniqueID: 101668981
Country: Switzerland
Language: English
Volume: 8
Issue: 11
PII: 567

Researcher Affiliations

Peña, Fernando J
  • Laboratory of Equine Reproduction and Equine Spermatology, Veterinary Teaching Hospital, University of Extremadura, 10003 Cáceres, Spain.
O'Flaherty, Cristian
  • Departments of Surgery (Urology Division) and Pharmacology and Therapeutics, Faculty of Medicine, McGill University, Montréal, QC H4A 3J1, Canada.
Ortiz Rodríguez, José M
  • Laboratory of Equine Reproduction and Equine Spermatology, Veterinary Teaching Hospital, University of Extremadura, 10003 Cáceres, Spain.
Martín Cano, Francisco E
  • Laboratory of Equine Reproduction and Equine Spermatology, Veterinary Teaching Hospital, University of Extremadura, 10003 Cáceres, Spain.
Gaitskell-Phillips, Gemma L
  • Laboratory of Equine Reproduction and Equine Spermatology, Veterinary Teaching Hospital, University of Extremadura, 10003 Cáceres, Spain.
Gil, María C
  • Laboratory of Equine Reproduction and Equine Spermatology, Veterinary Teaching Hospital, University of Extremadura, 10003 Cáceres, Spain.
Ortega Ferrusola, Cristina
  • Laboratory of Equine Reproduction and Equine Spermatology, Veterinary Teaching Hospital, University of Extremadura, 10003 Cáceres, Spain.

Grant Funding

  • AGL2017-83149-R / Ministerio de Ciencia, Innovaciu00f3n y Universidades
  • IB16030 and GR18008 / Consejeru00eda de Empleo Empresa e Innovaciu00f3n del Gobierno de Extremadura

Conflict of Interest Statement

The authors declare that there is no conflict of interest that may affect the impartiality of the information presented in this paper. “The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results”.

References

This article includes 208 references
  1. Staub C, Johnson L. Review: Spermatogenesis in the bull.. Animal 2018 Jun;12(s1):s27-s35.
    doi: 10.1017/S1751731118000435pubmed: 29882505google scholar: lookup
  2. Bose R, Sheng K, Moawad AR, Manku G, O'Flaherty C, Taketo T, Culty M, Fok KL, Wing SS. Ubiquitin Ligase Huwe1 Modulates Spermatogenesis by Regulating Spermatogonial Differentiation and Entry into Meiosis.. Sci Rep 2017 Dec 19;7(1):17759.
    doi: 10.1038/s41598-017-17902-0pmc: PMC5736635pubmed: 29259204google scholar: lookup
  3. Gervasi MG, Visconti PE. Molecular changes and signaling events occurring in spermatozoa during epididymal maturation.. Andrology 2017 Mar;5(2):204-218.
    doi: 10.1111/andr.12320pmc: PMC5354101pubmed: 28297559google scholar: lookup
  4. Shiraishi K, Matsuyama H. Gonadotoropin actions on spermatogenesis and hormonal therapies for spermatogenic disorders [Review].. Endocr J 2017 Feb 27;64(2):123-131.
    doi: 10.1507/endocrj.EJ17-0001pubmed: 28100869google scholar: lookup
  5. Kalyanaraman B, Cheng G, Hardy M, Ouari O, Bennett B, Zielonka J. Teaching the basics of reactive oxygen species and their relevance to cancer biology: Mitochondrial reactive oxygen species detection, redox signaling, and targeted therapies.. Redox Biol 2018 May;15:347-362.
    doi: 10.1016/j.redox.2017.12.012pmc: PMC5756055pubmed: 29306792google scholar: lookup
  6. Kalyanaraman B. Teaching the basics of redox biology to medical and graduate students: Oxidants, antioxidants and disease mechanisms.. Redox Biol 2013 Feb 8;1(1):244-57.
    doi: 10.1016/j.redox.2013.01.014pmc: PMC3757692pubmed: 24024158google scholar: lookup
  7. Swegen A, Lambourne SR, Aitken RJ, Gibb Z. Rosiglitazone Improves Stallion Sperm Motility, ATP Content, and Mitochondrial Function.. Biol Reprod 2016 Nov;95(5):107.
    doi: 10.1095/biolreprod.116.142687pubmed: 27683266google scholar: lookup
  8. Gibb Z, Lambourne SR, Aitken RJ. The paradoxical relationship between stallion fertility and oxidative stress.. Biol Reprod 2014 Sep;91(3):77.
    doi: 10.1095/biolreprod.114.118539pubmed: 25078685google scholar: lookup
  9. Davila MP, Muñoz PM, Bolaños JM, Stout TA, Gadella BM, Tapia JA, da Silva CB, Ferrusola CO, Peña FJ. Mitochondrial ATP is required for the maintenance of membrane integrity in stallion spermatozoa, whereas motility requires both glycolysis and oxidative phosphorylation.. Reproduction 2016 Dec;152(6):683-694.
    doi: 10.1530/REP-16-0409pubmed: 27798283google scholar: lookup
  10. Plaza Davila M, Martin Muñoz P, Tapia JA, Ortega Ferrusola C, Balao da Silva C C, Peña FJ. Inhibition of Mitochondrial Complex I Leads to Decreased Motility and Membrane Integrity Related to Increased Hydrogen Peroxide and Reduced ATP Production, while the Inhibition of Glycolysis Has Less Impact on Sperm Motility.. PLoS One 2015;10(9):e0138777.
  11. Darr CR, Varner DD, Teague S, Cortopassi GA, Datta S, Meyers SA. Lactate and Pyruvate Are Major Sources of Energy for Stallion Sperm with Dose Effects on Mitochondrial Function, Motility, and ROS Production.. Biol Reprod 2016 Aug;95(2):34.
    doi: 10.1095/biolreprod.116.140707pubmed: 27335066google scholar: lookup
  12. TOSIC J, WALTON A. Formation of hydrogen peroxide by spermatozoa and its inhibitory effect of respiration.. Nature 1946 Oct 5;158:485.
    doi: 10.1038/158485a0pubmed: 20999112google scholar: lookup
  13. Lee D, Moawad AR, Morielli T, Fernandez MC, O'Flaherty C. Peroxiredoxins prevent oxidative stress during human sperm capacitation.. Mol Hum Reprod 2017 Feb 10;23(2):106-115.
    doi: 10.1093/molehr/gaw081pmc: PMC5388279pubmed: 28025393google scholar: lookup
  14. Liu Y, O'Flaherty C. In vivo oxidative stress alters thiol redox status of peroxiredoxin 1 and 6 and impairs rat sperm quality.. Asian J Androl 2017 Jan-Feb;19(1):73-79.
    doi: 10.4103/1008-682X.170863pmc: PMC5227679pubmed: 26823067google scholar: lookup
  15. O'Flaherty C. Redox regulation of mammalian sperm capacitation.. Asian J Androl 2015 Jul-Aug;17(4):583-90.
    doi: 10.4103/1008-682X.153303pmc: PMC4492048pubmed: 25926608google scholar: lookup
  16. O'Flaherty C, de Souza AR. Hydrogen peroxide modifies human sperm peroxiredoxins in a dose-dependent manner.. Biol Reprod 2011 Feb;84(2):238-47.
  17. de Lamirande E, O'Flaherty C. Sperm activation: role of reactive oxygen species and kinases.. Biochim Biophys Acta 2008 Jan;1784(1):106-15.
    doi: 10.1016/j.bbapap.2007.08.024pubmed: 17920343google scholar: lookup
  18. O'Flaherty C, de Lamirande E, Gagnon C. Positive role of reactive oxygen species in mammalian sperm capacitation: triggering and modulation of phosphorylation events.. Free Radic Biol Med 2006 Aug 15;41(4):528-40.
  19. O'Flaherty C, de Lamirande E, Gagnon C. Reactive oxygen species and protein kinases modulate the level of phospho-MEK-like proteins during human sperm capacitation.. Biol Reprod 2005 Jul;73(1):94-105.
    doi: 10.1095/biolreprod.104.038794pubmed: 15772258google scholar: lookup
  20. O'Flaherty CM, Beorlegui NB, Beconi MT. Reactive oxygen species requirements for bovine sperm capacitation and acrosome reaction.. Theriogenology 1999 Jul 15;52(2):289-301.
    doi: 10.1016/S0093-691X(99)00129-6pubmed: 10734395google scholar: lookup
  21. Fujii S, Sawa T, Nishida M, Ihara H, Ida T, Motohashi H, Akaike T. Redox signaling regulated by an electrophilic cyclic nucleotide and reactive cysteine persulfides.. Arch Biochem Biophys 2016 Apr 1;595:140-6.
    doi: 10.1016/j.abb.2015.11.008pubmed: 27095231google scholar: lookup
  22. Holmström KM, Finkel T. Cellular mechanisms and physiological consequences of redox-dependent signalling.. Nat Rev Mol Cell Biol 2014 Jun;15(6):411-21.
    doi: 10.1038/nrm3801pubmed: 24854789google scholar: lookup
  23. Go YM, Jones DP. The redox proteome.. J Biol Chem 2013 Sep 13;288(37):26512-20.
    doi: 10.1074/jbc.R113.464131pmc: PMC3772199pubmed: 23861437google scholar: lookup
  24. Briehl MM. Oxygen in human health from life to death--An approach to teaching redox biology and signaling to graduate and medical students.. Redox Biol 2015 Aug;5:124-139.
    doi: 10.1016/j.redox.2015.04.002pmc: PMC4412967pubmed: 25912168google scholar: lookup
  25. Zhang L, Wang X, Cueto R, Effi C, Zhang Y, Tan H, Qin X, Ji Y, Yang X, Wang H. Biochemical basis and metabolic interplay of redox regulation.. Redox Biol 2019 Sep;26:101284.
    doi: 10.1016/j.redox.2019.101284pmc: PMC6831867pubmed: 31400697google scholar: lookup
  26. Aitken JB, Naumovski N, Curry B, Grupen CG, Gibb Z, Aitken RJ. Characterization of an L-amino acid oxidase in equine spermatozoa.. Biol Reprod 2015 May;92(5):125.
    doi: 10.1095/biolreprod.114.126052pubmed: 25740544google scholar: lookup
  27. Vernet P, Fulton N, Wallace C, Aitken RJ. Analysis of reactive oxygen species generating systems in rat epididymal spermatozoa.. Biol Reprod 2001 Oct;65(4):1102-13.
    doi: 10.1095/biolreprod65.4.1102pubmed: 11566731google scholar: lookup
  28. Cueto R, Zhang L, Shan HM, Huang X, Li X, Li YF, Lopez J, Yang WY, Lavallee M, Yu C, Ji Y, Yang X, Wang H. Identification of homocysteine-suppressive mitochondrial ETC complex genes and tissue expression profile - Novel hypothesis establishment.. Redox Biol 2018 Jul;17:70-88.
    doi: 10.1016/j.redox.2018.03.015pmc: PMC6006524pubmed: 29679893google scholar: lookup
  29. Ortega-Ferrusola C, Anel-López L, Martín-Muñoz P, Ortíz-Rodríguez JM, Gil MC, Alvarez M, de Paz P, Ezquerra LJ, Masot AJ, Redondo E, Anel L, Peña FJ. Computational flow cytometry reveals that cryopreservation induces spermptosis but subpopulations of spermatozoa may experience capacitation-like changes.. Reproduction 2017 Mar;153(3):293-304.
    doi: 10.1530/REP-16-0539pubmed: 27965398google scholar: lookup
  30. Aitken RJ, Gibb Z, Baker MA, Drevet J, Gharagozloo P. Causes and consequences of oxidative stress in spermatozoa.. Reprod Fertil Dev 2016;28(1-2):1-10.
    doi: 10.1071/RD15325pubmed: 27062870google scholar: lookup
  31. Yeste M, Estrada E, Rocha LG, Marín H, Rodríguez-Gil JE, Miró J. Cryotolerance of stallion spermatozoa is related to ROS production and mitochondrial membrane potential rather than to the integrity of sperm nucleus.. Andrology 2015 Mar;3(2):395-407.
    doi: 10.1111/andr.291pubmed: 25294093google scholar: lookup
  32. Aparicio IM, Espino J, Bejarano I, Gallardo-Soler A, Campo ML, Salido GM, Pariente JA, Peña FJ, Tapia JA. Autophagy-related proteins are functionally active in human spermatozoa and may be involved in the regulation of cell survival and motility.. Sci Rep 2016 Sep 16;6:33647.
    doi: 10.1038/srep33647pmc: PMC5025659pubmed: 27633131google scholar: lookup
  33. Sies H, Berndt C, Jones DP. Oxidative Stress.. Annu Rev Biochem 2017 Jun 20;86:715-748.
  34. Schmidt HH, Stocker R, Vollbracht C, Paulsen G, Riley D, Daiber A, Cuadrado A. Antioxidants in Translational Medicine.. Antioxid Redox Signal 2015 Nov 10;23(14):1130-43.
    doi: 10.1089/ars.2015.6393pmc: PMC4657516pubmed: 26154592google scholar: lookup
  35. Han D, Antunes F, Canali R, Rettori D, Cadenas E. Voltage-dependent anion channels control the release of the superoxide anion from mitochondria to cytosol.. J Biol Chem 2003 Feb 21;278(8):5557-63.
    doi: 10.1074/jbc.M210269200pubmed: 12482755google scholar: lookup
  36. Han D, Antunes F, Daneri F, Cadenas E. Mitochondrial superoxide anion production and release into intermembrane space.. Methods Enzymol 2002;349:271-80.
    pubmed: 11912916doi: 10.1016/s0076-6879(02)49341-xgoogle scholar: lookup
  37. Han D, Williams E, Cadenas E. Mitochondrial respiratory chain-dependent generation of superoxide anion and its release into the intermembrane space.. Biochem J 2001 Jan 15;353(Pt 2):411-6.
    doi: 10.1042/bj3530411pmc: PMC1221585pubmed: 11139407google scholar: lookup
  38. Vieceli Dalla Sega F, Zambonin L, Fiorentini D, Rizzo B, Caliceti C, Landi L, Hrelia S, Prata C. Specific aquaporins facilitate Nox-produced hydrogen peroxide transport through plasma membrane in leukaemia cells.. Biochim Biophys Acta 2014 Apr;1843(4):806-14.
    doi: 10.1016/j.bbamcr.2014.01.011pubmed: 24440277google scholar: lookup
  39. Mubarakshina Borisova MM, Kozuleva MA, Rudenko NN, Naydov IA, Klenina IB, Ivanov BN. Photosynthetic electron flow to oxygen and diffusion of hydrogen peroxide through the chloroplast envelope via aquaporins.. Biochim Biophys Acta 2012 Aug;1817(8):1314-21.
    doi: 10.1016/j.bbabio.2012.02.036pubmed: 22421105google scholar: lookup
  40. Bienert GP, Møller AL, Kristiansen KA, Schulz A, Møller IM, Schjoerring JK, Jahn TP. Specific aquaporins facilitate the diffusion of hydrogen peroxide across membranes.. J Biol Chem 2007 Jan 12;282(2):1183-92.
    doi: 10.1074/jbc.M603761200pubmed: 17105724google scholar: lookup
  41. Li TK. The glutathione and thiol content of mammalian spermatozoa and seminal plasma.. Biol Reprod 1975 Jun;12(5):641-6.
    doi: 10.1095/biolreprod12.5.641pubmed: 1220831google scholar: lookup
  42. Wong JL, Créton R, Wessel GM. The oxidative burst at fertilization is dependent upon activation of the dual oxidase Udx1.. Dev Cell 2004 Dec;7(6):801-14.
    doi: 10.1016/j.devcel.2004.10.014pubmed: 15572124google scholar: lookup
  43. Wong JL, Wessel GM. Free-radical crosslinking of specific proteins alters the function of the egg extracellular matrix at fertilization.. Development 2008 Feb;135(3):431-40.
    doi: 10.1242/dev.015503pubmed: 18094022google scholar: lookup
  44. Chapman JC, Michael SD. Proposed mechanism for sperm chromatin condensation/decondensation in the male rat.. Reprod Biol Endocrinol 2003 Feb 11;1:20.
    doi: 10.1186/1477-7827-1-20pmc: PMC151792pubmed: 12646056google scholar: lookup
  45. Herrero MB, de Lamirande E, Gagnon C. Nitric oxide is a signaling molecule in spermatozoa.. Curr Pharm Des 2003;9(5):419-25.
    doi: 10.2174/1381612033391720pubmed: 12570819google scholar: lookup
  46. Roselli M, Buonomo O, Piazza A, Guadagni F, Vecchione A, Brunetti E, Cipriani C, Amadei G, Nieroda C, Greiner JW, Casciani CU. Novel clinical approaches in monoclonal antibody-based management in colorectal cancer patients: radioimmunoguided surgery and antigen augmentation.. Semin Surg Oncol 1998 Dec;15(4):254-62.
  47. Maciel VL Jr, Caldas-Bussiere MC, Marín DFD, Paes de Carvalho CS, Quirino CR, Leal ACMS. Nitric oxide impacts bovine sperm capacitation in a cGMP-dependent and cGMP-independent manner.. Reprod Domest Anim 2019 Dec;54(12):1612-1620.
    doi: 10.1111/rda.13570pubmed: 31549441google scholar: lookup
  48. Maciel VL Jr, Caldas-Bussiere MC, Silveira V, Reis RS, Rios AFL, Paes de Carvalho CS. l-arginine alters the proteome of frozen-thawed bovine sperm during in vitro capacitation.. Theriogenology 2018 Oct 1;119:1-9.
  49. Staicu FD, Lopez-Úbeda R, Romero-Aguirregomezcorta J, Martínez-Soto JC, Matás Parra C. Regulation of boar sperm functionality by the nitric oxide synthase/nitric oxide system.. J Assist Reprod Genet 2019 Aug;36(8):1721-1736.
    doi: 10.1007/s10815-019-01526-6pmc: PMC6707978pubmed: 31325069google scholar: lookup
  50. Ortega Ferrusola C, González Fernández L, Macías García B, Salazar-Sandoval C, Morillo Rodríguez A, Rodríguez Martinez H, Tapia JA, Peña FJ. Effect of cryopreservation on nitric oxide production by stallion spermatozoa.. Biol Reprod 2009 Dec;81(6):1106-11.
    doi: 10.1095/biolreprod.109.078220pubmed: 19605785google scholar: lookup
  51. O'Flaherty C, Matsushita-Fournier D. Reactive oxygen species and protein modifications in spermatozoa.. Biol Reprod 2017 Oct 1;97(4):577-585.
    doi: 10.1093/biolre/iox104pubmed: 29025014google scholar: lookup
  52. Luque GM, Dalotto-Moreno T, Martín-Hidalgo D, Ritagliati C, Puga Molina LC, Romarowski A, Balestrini PA, Schiavi-Ehrenhaus LJ, Gilio N, Krapf D, Visconti PE, Buffone MG. Only a subpopulation of mouse sperm displays a rapid increase in intracellular calcium during capacitation.. J Cell Physiol 2018 Dec;233(12):9685-9700.
    doi: 10.1002/jcp.26883pmc: PMC6185779pubmed: 29953592google scholar: lookup
  53. Alvau A, Battistone MA, Gervasi MG, Navarrete FA, Xu X, Sánchez-Cárdenas C, De la Vega-Beltran JL, Da Ros VG, Greer PA, Darszon A, Krapf D, Salicioni AM, Cuasnicu PS, Visconti PE. The tyrosine kinase FER is responsible for the capacitation-associated increase in tyrosine phosphorylation in murine sperm.. Development 2016 Jul 1;143(13):2325-33.
    doi: 10.1242/dev.136499pmc: PMC4958327pubmed: 27226326google scholar: lookup
  54. Stival C, Puga Molina Ldel C, Paudel B, Buffone MG, Visconti PE, Krapf D. Sperm Capacitation and Acrosome Reaction in Mammalian Sperm.. Adv Anat Embryol Cell Biol 2016;220:93-106.
    doi: 10.1007/978-3-319-30567-7_5pubmed: 27194351google scholar: lookup
  55. Stival C, La Spina FA, Baró Graf C, Arcelay E, Arranz SE, Ferreira JJ, Le Grand S, Dzikunu VA, Santi CM, Visconti PE, Buffone MG, Krapf D. Src Kinase Is the Connecting Player between Protein Kinase A (PKA) Activation and Hyperpolarization through SLO3 Potassium Channel Regulation in Mouse Sperm.. J Biol Chem 2015 Jul 24;290(30):18855-64.
    doi: 10.1074/jbc.M115.640326pmc: PMC4513139pubmed: 26060254google scholar: lookup
  56. Escoffier J, Navarrete F, Haddad D, Santi CM, Darszon A, Visconti PE. Flow cytometry analysis reveals that only a subpopulation of mouse sperm undergoes hyperpolarization during capacitation.. Biol Reprod 2015 May;92(5):121.
  57. Visconti PE, Krapf D, de la Vega-Beltrán JL, Acevedo JJ, Darszon A. Ion channels, phosphorylation and mammalian sperm capacitation.. Asian J Androl 2011 May;13(3):395-405.
    doi: 10.1038/aja.2010.69pmc: PMC3739340pubmed: 21540868google scholar: lookup
  58. Boerke A, Brouwers JF, Olkkonen VM, van de Lest CH, Sostaric E, Schoevers EJ, Helms JB, Gadella BM. Involvement of bicarbonate-induced radical signaling in oxysterol formation and sterol depletion of capacitating mammalian sperm during in vitro fertilization.. Biol Reprod 2013 Jan;88(1):21.
    doi: 10.1095/biolreprod.112.101253pubmed: 23115269google scholar: lookup
  59. Aitken RJ. The capacitation-apoptosis highway: oxysterols and mammalian sperm function.. Biol Reprod 2011 Jul;85(1):9-12.
    doi: 10.1095/biolreprod.111.092528pubmed: 21490245google scholar: lookup
  60. Zerbinati C, Caponecchia L, Puca R, Ciacciarelli M, Salacone P, Sebastianelli A, Pastore A, Palleschi G, Petrozza V, Porta N, Rago R, Carbone A, Iuliano L. Mass spectrometry profiling of oxysterols in human sperm identifies 25-hydroxycholesterol as a marker of sperm function.. Redox Biol 2017 Apr;11:111-117.
    doi: 10.1016/j.redox.2016.11.008pmc: PMC5133663pubmed: 27912195google scholar: lookup
  61. Brouwers JF, Boerke A, Silva PF, Garcia-Gil N, van Gestel RA, Helms JB, van de Lest CH, Gadella BM. Mass spectrometric detection of cholesterol oxidation in bovine sperm.. Biol Reprod 2011 Jul;85(1):128-36.
    doi: 10.1095/biolreprod.111.091207pubmed: 21415139google scholar: lookup
  62. Leemans B, Stout TAE, De Schauwer C, Heras S, Nelis H, Hoogewijs M, Van Soom A, Gadella BM. Update on mammalian sperm capacitation: how much does the horse differ from other species?. Reproduction 2019 May;157(5):R181-R197.
    doi: 10.1530/REP-18-0541pubmed: 30721132google scholar: lookup
  63. Battistone MA, Da Ros VG, Salicioni AM, Navarrete FA, Krapf D, Visconti PE, Cuasnicú PS. Functional human sperm capacitation requires both bicarbonate-dependent PKA activation and down-regulation of Ser/Thr phosphatases by Src family kinases.. Mol Hum Reprod 2013 Sep;19(9):570-80.
    doi: 10.1093/molehr/gat033pmc: PMC3749807pubmed: 23630234google scholar: lookup
  64. Chávez JC, Hernández-González EO, Wertheimer E, Visconti PE, Darszon A, Treviño CL. Participation of the Cl-/HCO(3)- exchangers SLC26A3 and SLC26A6, the Cl- channel CFTR, and the regulatory factor SLC9A3R1 in mouse sperm capacitation.. Biol Reprod 2012 Jan;86(1):1-14.
  65. Salicioni AM, Platt MD, Wertheimer EV, Arcelay E, Allaire A, Sosnik J, Visconti PE. Signalling pathways involved in sperm capacitation.. Soc Reprod Fertil Suppl 2007;65:245-59.
    pubmed: 17644966
  66. Hernández-González EO, Sosnik J, Edwards J, Acevedo JJ, Mendoza-Lujambio I, López-González I, Demarco I, Wertheimer E, Darszon A, Visconti PE. Sodium and epithelial sodium channels participate in the regulation of the capacitation-associated hyperpolarization in mouse sperm.. J Biol Chem 2006 Mar 3;281(9):5623-33.
    doi: 10.1074/jbc.M508172200pubmed: 16407190google scholar: lookup
  67. Lefièvre L, Jha KN, de Lamirande E, Visconti PE, Gagnon C. Activation of protein kinase A during human sperm capacitation and acrosome reaction.. J Androl 2002 Sep-Oct;23(5):709-16.
    pubmed: 12185106
  68. Visconti PE, Stewart-Savage J, Blasco A, Battaglia L, Miranda P, Kopf GS, Tezón JG. Roles of bicarbonate, cAMP, and protein tyrosine phosphorylation on capacitation and the spontaneous acrosome reaction of hamster sperm.. Biol Reprod 1999 Jul;61(1):76-84.
    doi: 10.1095/biolreprod61.1.76pubmed: 10377034google scholar: lookup
  69. O'Flaherty C, de Lamirande E, Gagnon C. Phosphorylation of the Arginine-X-X-(Serine/Threonine) motif in human sperm proteins during capacitation: modulation and protein kinase A dependency.. Mol Hum Reprod 2004 May;10(5):355-63.
    doi: 10.1093/molehr/gah046pubmed: 14997001google scholar: lookup
  70. O'Flaherty C, Beorlegui N, Beconi MT. Participation of superoxide anion in the capacitation of cryopreserved bovine sperm.. Int J Androl 2003 Apr;26(2):109-14.
  71. Freitas MJ, Vijayaraghavan S, Fardilha M. Signaling mechanisms in mammalian sperm motility.. Biol Reprod 2017 Jan 1;96(1):2-12.
    doi: 10.1095/biolreprod.116.144337pubmed: 28395326google scholar: lookup
  72. González-Fernández L, Ortega-Ferrusola C, Macias-Garcia B, Salido GM, Peña FJ, Tapia JA. Identification of protein tyrosine phosphatases and dual-specificity phosphatases in mammalian spermatozoa and their role in sperm motility and protein tyrosine phosphorylation.. Biol Reprod 2009 Jun;80(6):1239-52.
    doi: 10.1095/biolreprod.108.073486pubmed: 19211810google scholar: lookup
  73. Denu JM, Tanner KG. Specific and reversible inactivation of protein tyrosine phosphatases by hydrogen peroxide: evidence for a sulfenic acid intermediate and implications for redox regulation.. Biochemistry 1998 Apr 21;37(16):5633-42.
    doi: 10.1021/bi973035tpubmed: 9548949google scholar: lookup
  74. Frijhoff J, Dagnell M, Godfrey R, Ostman A. Regulation of protein tyrosine phosphatase oxidation in cell adhesion and migration.. Antioxid Redox Signal 2014 May 1;20(13):1994-2010.
    doi: 10.1089/ars.2013.5643pubmed: 24111825google scholar: lookup
  75. Ozkosem B, Feinstein SI, Fisher AB, O'Flaherty C. Advancing age increases sperm chromatin damage and impairs fertility in peroxiredoxin 6 null mice.. Redox Biol 2015 Aug;5:15-23.
    doi: 10.1016/j.redox.2015.02.004pmc: PMC4371547pubmed: 25796034google scholar: lookup
  76. Jeong W, Bae SH, Toledano MB, Rhee SG. Role of sulfiredoxin as a regulator of peroxiredoxin function and regulation of its expression.. Free Radic Biol Med 2012 Aug 1;53(3):447-56.
  77. Wood ZA, Schröder E, Robin Harris J, Poole LB. Structure, mechanism and regulation of peroxiredoxins.. Trends Biochem Sci 2003 Jan;28(1):32-40.
    doi: 10.1016/S0968-0004(02)00003-8pubmed: 12517450google scholar: lookup
  78. Wood ZA, Poole LB, Karplus PA. Peroxiredoxin evolution and the regulation of hydrogen peroxide signaling.. Science 2003 Apr 25;300(5619):650-3.
    doi: 10.1126/science.1080405pubmed: 12714747google scholar: lookup
  79. Scherz-Shouval R, Shvets E, Fass E, Shorer H, Gil L, Elazar Z. Reactive oxygen species are essential for autophagy and specifically regulate the activity of Atg4.. EMBO J 2007 Apr 4;26(7):1749-60.
    doi: 10.1038/sj.emboj.7601623pmc: PMC1847657pubmed: 17347651google scholar: lookup
  80. Gualtieri R, Mollo V, Duma G, Talevi R. Redox control of surface protein sulphhydryls in bovine spermatozoa reversibly modulates sperm adhesion to the oviductal epithelium and capacitation.. Reproduction 2009 Jul;138(1):33-43.
    doi: 10.1530/REP-08-0514pubmed: 19439561google scholar: lookup
  81. Gualtieri R, Iaccarino M, Mollo V, Prisco M, Iaccarino S, Talevi R. Slow cooling of human oocytes: ultrastructural injuries and apoptotic status.. Fertil Steril 2009 Apr;91(4):1023-34.
  82. Talevi R, Zagami M, Castaldo M, Gualtieri R. Redox regulation of sperm surface thiols modulates adhesion to the fallopian tube epithelium.. Biol Reprod 2007 Apr;76(4):728-35.
    doi: 10.1095/biolreprod.106.056028pubmed: 17229933google scholar: lookup
  83. Ortiz-Rodriguez JM, Martín-Cano FE, Ortega-Ferrusola C, Masot J, Redondo E, Gázquez A, Gil MC, Aparicio IM, Rojo-Domínguez P, Tapia JA, Rodriguez-Martínez H, Peña FJ. The incorporation of cystine by the soluble carrier family 7 member 11 (SLC7A11) is a component of the redox regulatory mechanism in stallion spermatozoa†.. Biol Reprod 2019 Jul 1;101(1):208-222.
    doi: 10.1093/biolre/ioz069pubmed: 30998234google scholar: lookup
  84. Ball BA, Gravance CG, Medina V, Baumber J, Liu IK. Catalase activity in equine semen.. Am J Vet Res 2000 Sep;61(9):1026-30.
    doi: 10.2460/ajvr.2000.61.1026pubmed: 10976731google scholar: lookup
  85. Baumber J, Ball BA. Determination of glutathione peroxidase and superoxide dismutase-like activities in equine spermatozoa, seminal plasma, and reproductive tissues.. Am J Vet Res 2005 Aug;66(8):1415-9.
    doi: 10.2460/ajvr.2005.66.1415pubmed: 16173486google scholar: lookup
  86. Brummer M, Hayes S, Dawson KA, Lawrence LM. Measures of antioxidant status of the horse in response to selenium depletion and repletion.. J Anim Sci 2013 May;91(5):2158-68.
    doi: 10.2527/jas.2012-5794pubmed: 23463557google scholar: lookup
  87. LEONE E. Ergothioneine in the equine ampullar secretion.. Nature 1954 Aug 28;174(4426):404-5.
    doi: 10.1038/174404b0pubmed: 13194007google scholar: lookup
  88. Mann T. Biochemistry of stallion semen.. J Reprod Fertil Suppl 1975 Oct;(23):47-52.
    pubmed: 1060826
  89. Ortega Ferrusola C, González Fernández L, Morrell JM, Salazar Sandoval C, Macías García B, Rodríguez-Martinez H, Tapia JA, Peña FJ. Lipid peroxidation, assessed with BODIPY-C11, increases after cryopreservation of stallion spermatozoa, is stallion-dependent and is related to apoptotic-like changes.. Reproduction 2009 Jul;138(1):55-63.
    doi: 10.1530/REP-08-0484pubmed: 19380427google scholar: lookup
  90. Fernandez MC, O'Flaherty C. Peroxiredoxin 6 is the primary antioxidant enzyme for the maintenance of viability and DNA integrity in human spermatozoa.. Hum Reprod 2018 Aug 1;33(8):1394-1407.
    doi: 10.1093/humrep/dey221pmc: PMC6070098pubmed: 29912414google scholar: lookup
  91. Moawad AR, Fernandez MC, Scarlata E, Dodia C, Feinstein SI, Fisher AB, O'Flaherty C. Deficiency of peroxiredoxin 6 or inhibition of its phospholipase A(2) activity impair the in vitro sperm fertilizing competence in mice.. Sci Rep 2017 Oct 11;7(1):12994.
    doi: 10.1038/s41598-017-13411-2pmc: PMC5636886pubmed: 29021631google scholar: lookup
  92. Neagu VR, García BM, Sandoval CS, Rodríguez AM, Ferrusola CO, Fernández LG, Tapia JA, Peña FJ. Freezing dog semen in presence of the antioxidant butylated hydroxytoluene improves postthaw sperm membrane integrity.. Theriogenology 2010 Mar 15;73(5):645-50.
  93. Efrat M, Stein A, Pinkas H, Breitbart H, Unger R, Birk R. Paraoxonase 1 (PON1) attenuates sperm hyperactivity and spontaneous acrosome reaction.. Andrology 2019 Jan;7(1):24-30.
    doi: 10.1111/andr.12552pubmed: 30225889google scholar: lookup
  94. Barranco I, Tvarijonaviciute A, Perez-Patiño C, Alkmin DV, Ceron JJ, Martinez EA, Rodriguez-Martinez H, Roca J. The activity of paraoxonase type 1 (PON-1) in boar seminal plasma and its relationship with sperm quality, functionality, and in vivo fertility.. Andrology 2015 Mar;3(2):315-20.
    doi: 10.1111/andr.309pubmed: 25598515google scholar: lookup
  95. Barranco I, Roca J, Tvarijonaviciute A, Rubér M, Vicente-Carrillo A, Atikuzzaman M, Ceron JJ, Martinez EA, Rodriguez-Martinez H. Measurement of activity and concentration of paraoxonase 1 (PON-1) in seminal plasma and identification of PON-2 in the sperm of boar ejaculates.. Mol Reprod Dev 2015 Jan;82(1):58-65.
    doi: 10.1002/mrd.22444pubmed: 25487823google scholar: lookup
  96. Lazaros LA, Xita NV, Hatzi EG, Kaponis AI, Stefos TJ, Plachouras NI, Makrydimas GV, Sofikitis NV, Zikopoulos KA, Georgiou IA. Association of paraoxonase gene polymorphisms with sperm parameters.. J Androl 2011 Jul-Aug;32(4):394-401.
    doi: 10.2164/jandrol.110.010348pubmed: 21127310google scholar: lookup
  97. Verit FF, Verit A, Ciftci H, Erel O, Celik H. Paraoxonase-1 activity in subfertile men and relationship to sperm parameters.. J Androl 2009 Mar-Apr;30(2):183-9.
    doi: 10.2164/jandrol.108.004929pubmed: 18930907google scholar: lookup
  98. Moradi MN, Karimi J, Khodadadi I, Amiri I, Karami M, Saidijam M, Vatannejad A, Tavilani H. Evaluation of the p53 and Thioredoxin reductase in sperm from asthenozoospermic males in comparison to normozoospermic males.. Free Radic Biol Med 2018 Feb 20;116:123-128.
  99. Emelyanov AV, Fyodorov DV. Thioredoxin-dependent disulfide bond reduction is required for protamine eviction from sperm chromatin.. Genes Dev 2016 Dec 15;30(24):2651-2656.
    doi: 10.1101/gad.290916.116pmc: PMC5238724pubmed: 28031247google scholar: lookup
  100. Tirmarche S, Kimura S, Dubruille R, Horard B, Loppin B. Unlocking sperm chromatin at fertilization requires a dedicated egg thioredoxin in Drosophila.. Nat Commun 2016 Nov 23;7:13539.
    doi: 10.1038/ncomms13539pmc: PMC5122968pubmed: 27876811google scholar: lookup
  101. Su D, Novoselov SV, Sun QA, Moustafa ME, Zhou Y, Oko R, Hatfield DL, Gladyshev VN. Mammalian selenoprotein thioredoxin-glutathione reductase. Roles in disulfide bond formation and sperm maturation.. J Biol Chem 2005 Jul 15;280(28):26491-8.
    doi: 10.1074/jbc.M503638200pubmed: 15901730google scholar: lookup
  102. Miranda-Vizuete A, Tsang K, Yu Y, Jiménez A, Pelto-Huikko M, Flickinger CJ, Sutovsky P, Oko R. Cloning and developmental analysis of murid spermatid-specific thioredoxin-2 (SPTRX-2), a novel sperm fibrous sheath protein and autoantigen.. J Biol Chem 2003 Nov 7;278(45):44874-85.
    doi: 10.1074/jbc.M305475200pubmed: 12909633google scholar: lookup
  103. Yu Y, Oko R, Miranda-Vizuete A. Developmental expression of spermatid-specific thioredoxin-1 protein: transient association to the longitudinal columns of the fibrous sheath during sperm tail formation.. Biol Reprod 2002 Nov;67(5):1546-54.
    doi: 10.1095/biolreprod.102.004838pubmed: 12390887google scholar: lookup
  104. Kuribayashi Y, Gagnon C. Effect of catalase and thioredoxin addition to sperm incubation medium before in vitro fertilization on sperm capacity to support embryo development.. Fertil Steril 1996 Dec;66(6):1012-7.
    doi: 10.1016/S0015-0282(16)58699-3pubmed: 8941071google scholar: lookup
  105. Ozkosem B, Feinstein SI, Fisher AB, O'Flaherty C. Absence of Peroxiredoxin 6 Amplifies the Effect of Oxidant Stress on Mobility and SCSA/CMA3 Defined Chromatin Quality and Impairs Fertilizing Ability of Mouse Spermatozoa.. Biol Reprod 2016 Mar;94(3):68.
  106. O'Flaherty C. Peroxiredoxins: hidden players in the antioxidant defence of human spermatozoa.. Basic Clin Androl 2014;24:4.
    doi: 10.1186/2051-4190-24-4pmc: PMC4349611pubmed: 25780579google scholar: lookup
  107. Ortega-Ferrusola C, Martin Muñoz P, Ortiz-Rodriguez JM, Anel-López L, Balao da Silva C, Álvarez M, de Paz P, Tapia JA, Anel L, Silva-Rodríguez A, Aitken RJ, Gil MC, Gibb Z, Peña FJ. Depletion of thiols leads to redox deregulation, production of 4-hydroxinonenal and sperm senescence: a possible role for GSH regulation in spermatozoa†.. Biol Reprod 2019 Apr 1;100(4):1090-1107.
    doi: 10.1093/biolre/ioy241pubmed: 30418487google scholar: lookup
  108. Keil M, Wetterauer U, Heite HJ. Glutamic acid concentration in human semen--its origin and significance.. Andrologia 1979 Sep-Oct;11(5):385-91.
  109. Muñoz PM, Ferrusola CO, Lopez LA, Del Petre C, Garcia MA, de Paz Cabello P, Anel L, Peña FJ. Caspase 3 Activity and Lipoperoxidative Status in Raw Semen Predict the Outcome of Cryopreservation of Stallion Spermatozoa.. Biol Reprod 2016 Sep;95(3):53.
    doi: 10.1095/biolreprod.116.139444pubmed: 27417910google scholar: lookup
  110. Martin Muñoz P, Ortega Ferrusola C, Vizuete G, Plaza Dávila M, Rodriguez Martinez H, Peña FJ. Depletion of Intracellular Thiols and Increased Production of 4-Hydroxynonenal that Occur During Cryopreservation of Stallion Spermatozoa Lead to Caspase Activation, Loss of Motility, and Cell Death.. Biol Reprod 2015 Dec;93(6):143.
    doi: 10.1095/biolreprod.115.132878pubmed: 26536905google scholar: lookup
  111. Aitken RJ, Baker MA, Nixon B. Are sperm capacitation and apoptosis the opposite ends of a continuum driven by oxidative stress?. Asian J Androl 2015 Jul-Aug;17(4):633-9.
    doi: 10.4103/1008-682X.153850pmc: PMC4492056pubmed: 25999358google scholar: lookup
  112. Brand MD. Mitochondrial generation of superoxide and hydrogen peroxide as the source of mitochondrial redox signaling.. Free Radic Biol Med 2016 Nov;100:14-31.
  113. Goncalves RL, Bunik VI, Brand MD. Production of superoxide/hydrogen peroxide by the mitochondrial 2-oxoadipate dehydrogenase complex.. Free Radic Biol Med 2016 Feb;91:247-55.
  114. Samanta L, Agarwal A, Swain N, Sharma R, Gopalan B, Esteves SC, Durairajanayagam D, Sabanegh E. Proteomic Signatures of Sperm Mitochondria in Varicocele: Clinical Use as Biomarkers of Varicocele Associated Infertility.. J Urol 2018 Aug;200(2):414-422.
    doi: 10.1016/j.juro.2018.03.009pubmed: 29530785google scholar: lookup
  115. Lu X, Zhang Y, Bai H, Liu J, Li J, Wu B. Mitochondria-targeted antioxidant MitoTEMPO improves the post-thaw sperm quality.. Cryobiology 2018 Feb;80:26-29.
  116. Amaral S, S Tavares R, Baptista M, Sousa MI, Silva A, Escada-Rebelo S, Paiva CP, Ramalho-Santos J. Mitochondrial Functionality and Chemical Compound Action on Sperm Function.. Curr Med Chem 2016;23(31):3575-3606.
  117. Gibb Z, Lambourne SR, Quadrelli J, Smith ND, Aitken RJ. L-carnitine and pyruvate are prosurvival factors during the storage of stallion spermatozoa at room temperature.. Biol Reprod 2015 Oct;93(4):104.
    doi: 10.1095/biolreprod.115.131326pubmed: 26316064google scholar: lookup
  118. Peña FJ, Plaza Davila M, Ball BA, Squires EL, Martin Muñoz P, Ortega Ferrusola C, Balao da Silva C. The Impact of Reproductive Technologies on Stallion Mitochondrial Function.. Reprod Domest Anim 2015 Aug;50(4):529-37.
    doi: 10.1111/rda.12551pubmed: 26031351google scholar: lookup
  119. Jones DP. Disruption of mitochondrial redox circuitry in oxidative stress.. Chem Biol Interact 2006 Oct 27;163(1-2):38-53.
    doi: 10.1016/j.cbi.2006.07.008pubmed: 16970935google scholar: lookup
  120. Rico-Leo EM, Moreno-Marín N, González-Rico FJ, Barrasa E, Ortega-Ferrusola C, Martín-Muñoz P, Sánchez-Guardado LO, Llano E, Alvarez-Barrientos A, Infante-Campos A, Catalina-Fernández I, Hidalgo-Sánchez M, de Rooij DG, Pendás AM, Peña FJ, Merino JM, Fernández-Salguero PM. piRNA-associated proteins and retrotransposons are differentially expressed in murine testis and ovary of aryl hydrocarbon receptor deficient mice.. Open Biol 2016 Dec;6(12).
    doi: 10.1098/rsob.160186pmc: PMC5204120pubmed: 28003471google scholar: lookup
  121. Losano JDA, Angrimani DSR, Ferreira Leite R, Simões da Silva BDC, Barnabe VH, Nichi M. Spermatic mitochondria: role in oxidative homeostasis, sperm function and possible tools for their assessment.. Zygote 2018 Aug;26(4):251-260.
    doi: 10.1017/S0967199418000242pubmed: 30223916google scholar: lookup
  122. Amaral A, Lourenço B, Marques M, Ramalho-Santos J. Mitochondria functionality and sperm quality.. Reproduction 2013;146(5):R163-74.
    doi: 10.1530/REP-13-0178pubmed: 23901129google scholar: lookup
  123. Vakifahmetoglu-Norberg H, Ouchida AT, Norberg E. The role of mitochondria in metabolism and cell death.. Biochem Biophys Res Commun 2017 Jan 15;482(3):426-431.
    doi: 10.1016/j.bbrc.2016.11.088pubmed: 28212726google scholar: lookup
  124. du Plessis SS, Agarwal A, Mohanty G, van der Linde M. Oxidative phosphorylation versus glycolysis: what fuel do spermatozoa use?. Asian J Androl 2015 Mar-Apr;17(2):230-5.
    doi: 10.4103/1008-682X.135123pmc: PMC4650467pubmed: 25475660google scholar: lookup
  125. Amaral A, Paiva C, Attardo Parrinello C, Estanyol JM, Ballescà JL, Ramalho-Santos J, Oliva R. Identification of proteins involved in human sperm motility using high-throughput differential proteomics.. J Proteome Res 2014 Dec 5;13(12):5670-84.
    doi: 10.1021/pr500652ypubmed: 25250979google scholar: lookup
  126. Amaral A, Castillo J, Estanyol JM, Ballescà JL, Ramalho-Santos J, Oliva R. Human sperm tail proteome suggests new endogenous metabolic pathways.. Mol Cell Proteomics 2013 Feb;12(2):330-42.
    doi: 10.1074/mcp.M112.020552pmc: PMC3567857pubmed: 23161514google scholar: lookup
  127. Klingenberg M. The ADP and ATP transport in mitochondria and its carrier.. Biochim Biophys Acta 2008 Oct;1778(10):1978-2021.
    doi: 10.1016/j.bbamem.2008.04.011pubmed: 18510943google scholar: lookup
  128. Ortega Ferrusola C, Anel-López L, Ortiz-Rodriguez JM, Martin Muñoz P, Alvarez M, de Paz P, Masot J, Redondo E, Balao da Silva C, Morrell JM, Rodriguez Martinez H, Tapia JA, Gil MC, Anel L, Peña FJ. Stallion spermatozoa surviving freezing and thawing experience membrane depolarization and increased intracellular Na().. Andrology 2017 Nov;5(6):1174-1182.
    doi: 10.1111/andr.12419pubmed: 28973824google scholar: lookup
  129. Moscatelli N, Lunetti P, Braccia C, Armirotti A, Pisanello F, De Vittorio M, Zara V, Ferramosca A. Comparative Proteomic Analysis of Proteins Involved in Bioenergetics Pathways Associated with Human Sperm Motility.. Int J Mol Sci 2019 Jun 19;20(12).
    doi: 10.3390/ijms20123000pmc: PMC6627292pubmed: 31248186google scholar: lookup
  130. Ferramosca A, Zara V. Bioenergetics of mammalian sperm capacitation.. Biomed Res Int 2014;2014:902953.
    doi: 10.1155/2014/902953pmc: PMC3984864pubmed: 24791005google scholar: lookup
  131. Piomboni P, Focarelli R, Stendardi A, Ferramosca A, Zara V. The role of mitochondria in energy production for human sperm motility.. Int J Androl 2012 Apr;35(2):109-24.
  132. Bucci D, Rodriguez-Gil JE, Vallorani C, Spinaci M, Galeati G, Tamanini C. GLUTs and mammalian sperm metabolism.. J Androl 2011 Jul-Aug;32(4):348-55.
    doi: 10.2164/jandrol.110.011197pubmed: 21088231google scholar: lookup
  133. Marin S, Chiang K, Bassilian S, Lee WN, Boros LG, Fernández-Novell JM, Centelles JJ, Medrano A, Rodriguez-Gil JE, Cascante M. Metabolic strategy of boar spermatozoa revealed by a metabolomic characterization.. FEBS Lett 2003 Nov 20;554(3):342-6.
    doi: 10.1016/S0014-5793(03)01185-2pubmed: 14623091google scholar: lookup
  134. Asghari A, Marashi SA, Ansari-Pour N. A sperm-specific proteome-scale metabolic network model identifies non-glycolytic genes for energy deficiency in asthenozoospermia.. Syst Biol Reprod Med 2017 Apr;63(2):100-112.
    doi: 10.1080/19396368.2016.1263367pubmed: 28085499google scholar: lookup
  135. Swegen A, Curry BJ, Gibb Z, Lambourne SR, Smith ND, Aitken RJ. Investigation of the stallion sperm proteome by mass spectrometry.. Reproduction 2015 Mar;149(3):235-44.
    doi: 10.1530/REP-14-0500pubmed: 25504869google scholar: lookup
  136. Qiu JH, Li YW, Xie HL, Li Q, Dong HB, Sun MJ, Gao WQ, Tan JH. Effects of glucose metabolism pathways on sperm motility and oxidative status during long-term liquid storage of goat semen.. Theriogenology 2016 Aug;86(3):839-49.
  137. Miraglia E, Lussiana C, Viarisio D, Racca C, Cipriani A, Gazzano E, Bosia A, Revelli A, Ghigo D. The pentose phosphate pathway plays an essential role in supporting human sperm capacitation.. Fertil Steril 2010 May 1;93(7):2437-40.
  138. Andò S, Aquila S. Arguments raised by the recent discovery that insulin and leptin are expressed in and secreted by human ejaculated spermatozoa.. Mol Cell Endocrinol 2005 Dec 21;245(1-2):1-6.
    doi: 10.1016/j.mce.2005.09.011pubmed: 16274924google scholar: lookup
  139. Urner F, Sakkas D. Involvement of the pentose phosphate pathway and redox regulation in fertilization in the mouse.. Mol Reprod Dev 2005 Apr;70(4):494-503.
    doi: 10.1002/mrd.20222pubmed: 15685628google scholar: lookup
  140. Williams AC, Ford WC. Functional significance of the pentose phosphate pathway and glutathione reductase in the antioxidant defenses of human sperm.. Biol Reprod 2004 Oct;71(4):1309-16.
    doi: 10.1095/biolreprod.104.028407pubmed: 15189835google scholar: lookup
  141. Urner F, Sakkas D. A possible role for the pentose phosphate pathway of spermatozoa in gamete fusion in the mouse.. Biol Reprod 1999 Mar;60(3):733-9.
    doi: 10.1095/biolreprod60.3.733pubmed: 10026124google scholar: lookup
  142. Evdokimov VV, Barinova KV, Turovetskii VB, Muronetz VI, Schmalhausen EV. Low Concentrations of Hydrogen Peroxide Activate the Antioxidant Defense System in Human Sperm Cells.. Biochemistry (Mosc) 2015 Sep;80(9):1178-85.
    doi: 10.1134/S0006297915090084pubmed: 26555470google scholar: lookup
  143. Ford WC, Whittington K, Williams AC. Reactive oxygen species in human sperm suspensions: production by leukocytes and the generation of NADPH to protect sperm against their effects.. Int J Androl 1997;20 Suppl 3:44-9.
    pubmed: 9466185
  144. Ortiz-Rodriguez JM, Balao da Silva C, Masot J, Redondo E, Gazquez A, Tapia JA, Gil C, Ortega-Ferrusola C, Peña FJ. Rosiglitazone in the thawing medium improves mitochondrial function in stallion spermatozoa through regulating Akt phosphorylation and reduction of caspase 3.. PLoS One 2019;14(7):e0211994.
  145. Volpe CMO, Villar-Delfino PH, Dos Anjos PMF, Nogueira-Machado JA. Cellular death, reactive oxygen species (ROS) and diabetic complications.. Cell Death Dis 2018 Jan 25;9(2):119.
    doi: 10.1038/s41419-017-0135-zpmc: PMC5833737pubmed: 29371661google scholar: lookup
  146. Allaman I, Bélanger M, Magistretti PJ. Methylglyoxal, the dark side of glycolysis.. Front Neurosci 2015;9:23.
    doi: 10.3389/fnins.2015.00023pmc: PMC4321437pubmed: 25709564google scholar: lookup
  147. Nevin C, McNeil L, Ahmed N, Murgatroyd C, Brison D, Carroll M. Investigating the Glycating Effects of Glucose, Glyoxal and Methylglyoxal on Human Sperm.. Sci Rep 2018 Jun 13;8(1):9002.
    doi: 10.1038/s41598-018-27108-7pmc: PMC5998133pubmed: 29899461google scholar: lookup
  148. Chen MC, Lin JA, Lin HT, Chen SY, Yen GC. Potential effect of advanced glycation end products (AGEs) on spermatogenesis and sperm quality in rodents.. Food Funct 2019 Jun 19;10(6):3324-3333.
    doi: 10.1039/C9FO00240Epubmed: 31095144google scholar: lookup
  149. Karimi J, Goodarzi MT, Tavilani H, Khodadadi I, Amiri I. Relationship between advanced glycation end products and increased lipid peroxidation in semen of diabetic men.. Diabetes Res Clin Pract 2011 Jan;91(1):61-6.
    doi: 10.1016/j.diabres.2010.09.024pubmed: 20970866google scholar: lookup
  150. Aquila S, Gentile M, Middea E, Catalano S, Andò S. Autocrine regulation of insulin secretion in human ejaculated spermatozoa.. Endocrinology 2005 Feb;146(2):552-7.
    doi: 10.1210/en.2004-1252pubmed: 15550513google scholar: lookup
  151. Sangeeta S, Arangasamy A, Kulkarni S, Selvaraju S. Role of amino acids as additives on sperm motility, plasma membrane integrity and lipid peroxidation levels at pre-freeze and post-thawed ram semen.. Anim Reprod Sci 2015 Oct;161:82-8.
  152. Lahnsteiner F. The role of free amino acids in semen of rainbow trout Oncorhynchus mykiss and carp Cyprinus carpio.. J Fish Biol 2009 Sep;75(4):816-33.
  153. Koppula P, Zhang Y, Zhuang L, Gan B. Amino acid transporter SLC7A11/xCT at the crossroads of regulating redox homeostasis and nutrient dependency of cancer.. Cancer Commun (Lond) 2018 Apr 25;38(1):12.
    doi: 10.1186/s40880-018-0288-xpmc: PMC5993148pubmed: 29764521google scholar: lookup
  154. Breda CNS, Davanzo GG, Basso PJ, Saraiva Câmara NO, Moraes-Vieira PMM. Mitochondria as central hub of the immune system.. Redox Biol 2019 Sep;26:101255.
    doi: 10.1016/j.redox.2019.101255pmc: PMC6598836pubmed: 31247505google scholar: lookup
  155. Bromfield EG, Aitken RJ, Anderson AL, McLaughlin EA, Nixon B. The impact of oxidative stress on chaperone-mediated human sperm-egg interaction.. Hum Reprod 2015 Nov;30(11):2597-613.
    doi: 10.1093/humrep/dev214pubmed: 26345691google scholar: lookup
  156. Gharagozloo P, Aitken RJ. The role of sperm oxidative stress in male infertility and the significance of oral antioxidant therapy.. Hum Reprod 2011 Jul;26(7):1628-40.
    doi: 10.1093/humrep/der132pubmed: 21546386google scholar: lookup
  157. Aitken RJ, De Iuliis GN, Finnie JM, Hedges A, McLachlan RI. Analysis of the relationships between oxidative stress, DNA damage and sperm vitality in a patient population: development of diagnostic criteria.. Hum Reprod 2010 Oct;25(10):2415-26.
    doi: 10.1093/humrep/deq214pubmed: 20716559google scholar: lookup
  158. Aitken RJ, Baker MA. Oxidative stress, sperm survival and fertility control.. Mol Cell Endocrinol 2006 May 16;250(1-2):66-9.
    doi: 10.1016/j.mce.2005.12.026pubmed: 16412557google scholar: lookup
  159. Thomson LK, Fleming SD, Aitken RJ, De Iuliis GN, Zieschang JA, Clark AM. Cryopreservation-induced human sperm DNA damage is predominantly mediated by oxidative stress rather than apoptosis.. Hum Reprod 2009 Sep;24(9):2061-70.
    doi: 10.1093/humrep/dep214pubmed: 19525298google scholar: lookup
  160. García BM, Moran AM, Fernández LG, Ferrusola CO, Rodriguez AM, Bolaños JM, da Silva CM, Martínez HR, Tapia JA, Peña FJ. The mitochondria of stallion spermatozoa are more sensitive than the plasmalemma to osmotic-induced stress: role of c-Jun N-terminal kinase (JNK) pathway.. J Androl 2012 Jan-Feb;33(1):105-13.
    doi: 10.2164/jandrol.110.011957pubmed: 21436310google scholar: lookup
  161. Peña FJ, Ball BA, Squires EL. A New Method for Evaluating Stallion Sperm Viability and Mitochondrial Membrane Potential in Fixed Semen Samples.. Cytometry B Clin Cytom 2018 Mar;94(2):302-311.
    doi: 10.1002/cyto.b.21506pubmed: 28033647google scholar: lookup
  162. Balao da Silva CM, Ortega Ferrusola C, Morillo Rodriguez A, Gallardo Bolaños JM, Plaza Dávila M, Morrell JM, Rodriguez Martínez H, Tapia JA, Aparicio IM, Peña FJ. Sex sorting increases the permeability of the membrane of stallion spermatozoa.. Anim Reprod Sci 2013 May;138(3-4):241-51.
  163. Rodríguez AM, Ferrusola CO, García BM, Morrell JM, Martínez HR, Tapia JA, Peña FJ. Freezing stallion semen with the new Cáceres extender improves post thaw sperm quality and diminishes stallion-to-stallion variability.. Anim Reprod Sci 2011 Aug;127(1-2):78-83.
  164. Ortega Ferrusola C, González Fernández L, Salazar Sandoval C, Macías García B, Rodríguez Martínez H, Tapia JA, Peña FJ. Inhibition of the mitochondrial permeability transition pore reduces "apoptosis like" changes during cryopreservation of stallion spermatozoa.. Theriogenology 2010 Aug;74(3):458-65.
  165. Ortega-Ferrusola C, Gil MC, Rodríguez-Martínez H, Anel L, Peña FJ, Martín-Muñoz P. Flow cytometry in Spermatology: A bright future ahead.. Reprod Domest Anim 2017 Dec;52(6):921-931.
    doi: 10.1111/rda.13043pubmed: 28815751google scholar: lookup
  166. Gallardo Bolaños JM, Miró Morán Á, Balao da Silva CM, Morillo Rodríguez A, Plaza Dávila M, Aparicio IM, Tapia JA, Ortega Ferrusola C, Peña FJ. Autophagy and apoptosis have a role in the survival or death of stallion spermatozoa during conservation in refrigeration.. PLoS One 2012;7(1):e30688.
  167. Guéraud F, Atalay M, Bresgen N, Cipak A, Eckl PM, Huc L, Jouanin I, Siems W, Uchida K. Chemistry and biochemistry of lipid peroxidation products.. Free Radic Res 2010 Oct;44(10):1098-124.
    doi: 10.3109/10715762.2010.498477pubmed: 20836659google scholar: lookup
  168. Uchida K. Lipid peroxidation and redox-sensitive signaling pathways.. Curr Atheroscler Rep 2007 Sep;9(3):216-21.
    doi: 10.1007/s11883-007-0022-7pubmed: 18241616google scholar: lookup
  169. Uchida K. Cellular response to bioactive lipid peroxidation products.. Free Radic Res 2000 Dec;33(6):731-7.
    doi: 10.1080/10715760000301251pubmed: 11237095google scholar: lookup
  170. Macías García B, González Fernández L, Ortega Ferrusola C, Morillo Rodríguez A, Gallardo Bolaños JM, Rodríguez Martinez H, Tapia JA, Morcuende D, Peña FJ. Fatty acids and plasmalogens of the phospholipids of the sperm membranes and their relation with the post-thaw quality of stallion spermatozoa.. Theriogenology 2011 Mar 15;75(5):811-8.
  171. García BM, Fernández LG, Ferrusola CO, Salazar-Sandoval C, Rodríguez AM, Martinez HR, Tapia JA, Morcuende D, Peña FJ. Membrane lipids of the stallion spermatozoon in relation to sperm quality and susceptibility to lipid peroxidation.. Reprod Domest Anim 2011 Feb;46(1):141-8.
  172. Martín Muñoz P, Anel-López L, Ortiz-Rodríguez JM, Álvarez M, de Paz P, Balao da Silva C, Rodríguez Martinez H, Gil MC, Anel L, Peña FJ, Ortega Ferrusola C. Redox cycling induces spermptosis and necrosis in stallion spermatozoa while the hydroxyl radical (OH•) only induces spermptosis.. Reprod Domest Anim 2018 Feb;53(1):54-67.
    doi: 10.1111/rda.13052pubmed: 28833663google scholar: lookup
  173. Hall SE, Aitken RJ, Nixon B, Smith ND, Gibb Z. Electrophilic aldehyde products of lipid peroxidation selectively adduct to heat shock protein 90 and arylsulfatase A in stallion spermatozoa.. Biol Reprod 2017 Jan 1;96(1):107-121.
    doi: 10.1095/biolreprod.116.145292pubmed: 28395341google scholar: lookup
  174. Bromfield EG, Aitken RJ, McLaughlin EA, Nixon B. Proteolytic degradation of heat shock protein A2 occurs in response to oxidative stress in male germ cells of the mouse.. Mol Hum Reprod 2017 Feb 10;23(2):91-105.
    doi: 10.1093/molehr/gaw074pubmed: 27932549google scholar: lookup
  175. Gibb Z, Lambourne SR, Curry BJ, Hall SE, Aitken RJ. Aldehyde Dehydrogenase Plays a Pivotal Role in the Maintenance of Stallion Sperm Motility.. Biol Reprod 2016 Jun;94(6):133.
    doi: 10.1095/biolreprod.116.140509pubmed: 27103446google scholar: lookup
  176. Moazamian R, Polhemus A, Connaughton H, Fraser B, Whiting S, Gharagozloo P, Aitken RJ. Oxidative stress and human spermatozoa: diagnostic and functional significance of aldehydes generated as a result of lipid peroxidation.. Mol Hum Reprod 2015 Jun;21(6):502-15.
    doi: 10.1093/molehr/gav014pubmed: 25837702google scholar: lookup
  177. Baker MA, Weinberg A, Hetherington L, Villaverde AI, Velkov T, Baell J, Gordon CP. Defining the mechanisms by which the reactive oxygen species by-product, 4-hydroxynonenal, affects human sperm cell function.. Biol Reprod 2015 Apr;92(4):108.
    doi: 10.1095/biolreprod.114.126680pubmed: 25673561google scholar: lookup
  178. Aitken RJ, Baker MA. Causes and consequences of apoptosis in spermatozoa; contributions to infertility and impacts on development.. Int J Dev Biol 2013;57(2-4):265-72.
    doi: 10.1387/ijdb.130146japubmed: 23784837google scholar: lookup
  179. Aitken RJ, Smith TB, Lord T, Kuczera L, Koppers AJ, Naumovski N, Connaughton H, Baker MA, De Iuliis GN. On methods for the detection of reactive oxygen species generation by human spermatozoa: analysis of the cellular responses to catechol oestrogen, lipid aldehyde, menadione and arachidonic acid.. Andrology 2013 Mar;1(2):192-205.
  180. Aurich C, Ortega Ferrusola C, Peña Vega FJ, Schrammel N, Morcuende D, Aurich J. Seasonal changes in the sperm fatty acid composition of Shetland pony stallions.. Theriogenology 2018 Feb;107:149-153.
  181. Zimniak P. Relationship of electrophilic stress to aging.. Free Radic Biol Med 2011 Sep 15;51(6):1087-105.
  182. Martínez-Pastor F, Mata-Campuzano M, Alvarez-Rodríguez M, Alvarez M, Anel L, de Paz P. Probes and techniques for sperm evaluation by flow cytometry.. Reprod Domest Anim 2010 Jun;45 Suppl 2:67-78.
  183. Aitken RJ, Gibb Z, Mitchell LA, Lambourne SR, Connaughton HS, De Iuliis GN. Sperm motility is lost in vitro as a consequence of mitochondrial free radical production and the generation of electrophilic aldehydes but can be significantly rescued by the presence of nucleophilic thiols.. Biol Reprod 2012 Nov;87(5):110.
    doi: 10.1095/biolreprod.112.102020pubmed: 22933515google scholar: lookup
  184. Bromfield EG, McLaughlin EA, Aitken RJ, Nixon B. Heat Shock Protein member A2 forms a stable complex with angiotensin converting enzyme and protein disulfide isomerase A6 in human spermatozoa.. Mol Hum Reprod 2016 Feb;22(2):93-109.
    doi: 10.1093/molehr/gav073pubmed: 26676989google scholar: lookup
  185. Aitken RJ, Flanagan HM, Connaughton H, Whiting S, Hedges A, Baker MA. Involvement of homocysteine, homocysteine thiolactone, and paraoxonase type 1 (PON-1) in the etiology of defective human sperm function.. Andrology 2016 Mar;4(2):345-60.
    doi: 10.1111/andr.12157pubmed: 26825875google scholar: lookup
  186. Teperek M, Simeone A, Gaggioli V, Miyamoto K, Allen GE, Erkek S, Kwon T, Marcotte EM, Zegerman P, Bradshaw CR, Peters AH, Gurdon JB, Jullien J. Sperm is epigenetically programmed to regulate gene transcription in embryos.. Genome Res 2016 Aug;26(8):1034-46.
    doi: 10.1101/gr.201541.115pmc: PMC4971762pubmed: 27034506google scholar: lookup
  187. Valcarce DG, Cartón-García F, Riesco MF, Herráez MP, Robles V. Analysis of DNA damage after human sperm cryopreservation in genes crucial for fertilization and early embryo development.. Andrology 2013 Sep;1(5):723-30.
  188. Valcarce DG, Cartón-García F, Herráez MP, Robles V. Effect of cryopreservation on human sperm messenger RNAs crucial for fertilization and early embryo development.. Cryobiology 2013 Aug;67(1):84-90.
  189. Kopeika J, Thornhill A, Khalaf Y. The effect of cryopreservation on the genome of gametes and embryos: principles of cryobiology and critical appraisal of the evidence.. Hum Reprod Update 2015 Mar-Apr;21(2):209-27.
    doi: 10.1093/humupd/dmu063pubmed: 25519143google scholar: lookup
  190. Rex AS, Aagaard J, Fedder J. DNA fragmentation in spermatozoa: a historical review.. Andrology 2017 Jul;5(4):622-630.
    doi: 10.1111/andr.12381pmc: PMC5601286pubmed: 28718529google scholar: lookup
  191. Evenson DP, Kasperson K, Wixon RL. Analysis of sperm DNA fragmentation using flow cytometry and other techniques.. Soc Reprod Fertil Suppl 2007;65:93-113.
    pubmed: 17644957
  192. Lhomme J, Constant JF, Demeunynck M. Abasic DNA structure, reactivity, and recognition.. Biopolymers 1999;52(2):65-83.
  193. Belmont P, Jourdan M, Demeunynck M, Constant JF, Garcia J, Lhomme J, Carez D, Croisy A. Abasic site recognition in DNA as a new strategy to potentiate the action of anticancer alkylating drugs?. J Med Chem 1999 Dec 16;42(25):5153-9.
    doi: 10.1021/jm9901428pubmed: 10602700google scholar: lookup
  194. Greenberg MM. Looking beneath the surface to determine what makes DNA damage deleterious.. Curr Opin Chem Biol 2014 Aug;21:48-55.
    doi: 10.1016/j.cbpa.2014.03.018pmc: PMC4149920pubmed: 24762292google scholar: lookup
  195. San Pedro JM, Greenberg MM. 5,6-Dihydropyrimidine peroxyl radical reactivity in DNA.. J Am Chem Soc 2014 Mar 12;136(10):3928-36.
    doi: 10.1021/ja412562ppmc: PMC3980663pubmed: 24579910google scholar: lookup
  196. Greenberg MM. Abasic and oxidized abasic site reactivity in DNA: enzyme inhibition, cross-linking, and nucleosome catalyzed reactions.. Acc Chem Res 2014 Feb 18;47(2):646-55.
    doi: 10.1021/ar400229dpmc: PMC3944396pubmed: 24369694google scholar: lookup
  197. Balao da Silva CM, Ortega-Ferrusola C, Morrell JM, Rodriguez Martínez H, Peña FJ. Flow Cytometric Chromosomal Sex Sorting of Stallion Spermatozoa Induces Oxidative Stress on Mitochondria and Genomic DNA.. Reprod Domest Anim 2016 Feb;51(1):18-25.
    doi: 10.1111/rda.12640pubmed: 26592367google scholar: lookup
  198. Vorilhon S, Brugnon F, Kocer A, Dollet S, Bourgne C, Berger M, Janny L, Pereira B, Aitken RJ, Moazamian A, Gharagozloo P, Drevet J, Pons-Rejraji H. Accuracy of human sperm DNA oxidation quantification and threshold determination using an 8-OHdG immuno-detection assay.. Hum Reprod 2018 Apr 1;33(4):553-562.
    doi: 10.1093/humrep/dey038pubmed: 29579272google scholar: lookup
  199. Li Z, Yang J, Huang H. Oxidative stress induces H2AX phosphorylation in human spermatozoa.. FEBS Lett 2006 Nov 13;580(26):6161-8.
    doi: 10.1016/j.febslet.2006.10.016pubmed: 17064697google scholar: lookup
  200. Garolla A, Cosci I, Bertoldo A, Sartini B, Boudjema E, Foresta C. DNA double strand breaks in human spermatozoa can be predictive for assisted reproductive outcome.. Reprod Biomed Online 2015 Jul;31(1):100-7.
    doi: 10.1016/j.rbmo.2015.03.009pubmed: 25985994google scholar: lookup
  201. Castillo J, Jodar M, Oliva R. The contribution of human sperm proteins to the development and epigenome of the preimplantation embryo.. Hum Reprod Update 2018 Sep 1;24(5):535-555.
    doi: 10.1093/humupd/dmy017pubmed: 29800303google scholar: lookup
  202. Aitken RJ, Curry BJ. Redox regulation of human sperm function: from the physiological control of sperm capacitation to the etiology of infertility and DNA damage in the germ line.. Antioxid Redox Signal 2011 Feb 1;14(3):367-81.
    doi: 10.1089/ars.2010.3186pubmed: 20522002google scholar: lookup
  203. Burruel V, Klooster KL, Chitwood J, Ross PJ, Meyers SA. Oxidative damage to rhesus macaque spermatozoa results in mitotic arrest and transcript abundance changes in early embryos.. Biol Reprod 2013 Sep;89(3):72.
  204. McCarthy MJ, Baumber J, Kass PH, Meyers SA. Osmotic stress induces oxidative cell damage to rhesus macaque spermatozoa.. Biol Reprod 2010 Mar;82(3):644-51.
  205. Ortiz-Rodriguez JM, Ortega-Ferrusola C, Gil MC, Martín-Cano FE, Gaitskell-Phillips G, Rodríguez-Martínez H, Hinrichs K, Álvarez-Barrientos A, Román Á, Peña FJ. Transcriptome analysis reveals that fertilization with cryopreserved sperm downregulates genes relevant for early embryo development in the horse.. PLoS One 2019;14(6):e0213420.
  206. Jodar M. Sperm and seminal plasma RNAs: what roles do they play beyond fertilization?. Reproduction 2019 Oct;158(4):R113-R123.
    doi: 10.1530/REP-18-0639pubmed: 31063972google scholar: lookup
  207. Zhou D, Suzuki T, Asami M, Perry ACF. Caput Epididymidal Mouse Sperm Support Full Development.. Dev Cell 2019 Jul 1;50(1):5-6.
    doi: 10.1016/j.devcel.2019.05.012pubmed: 31265812google scholar: lookup
  208. Morielli T, O'Flaherty C. Oxidative stress impairs function and increases redox protein modifications in human spermatozoa.. Reproduction 2015 Jan;149(1):113-23.
    doi: 10.1530/REP-14-0240pmc: PMC5489333pubmed: 25385721google scholar: lookup

Citations

This article has been cited 19 times.
  1. Shamhari A', Jefferi NES, Abd Hamid Z, Budin SB, Idris MHM, Taib IS. The Role of Promyelocytic Leukemia Zinc Finger (PLZF) and Glial-Derived Neurotrophic Factor Family Receptor Alpha 1 (GFRα1) in the Cryopreservation of Spermatogonia Stem Cells.. Int J Mol Sci 2023 Jan 18;24(3).
    doi: 10.3390/ijms24031945pubmed: 36768269google scholar: lookup
  2. Zargari F, Rahaman MS, KazemPour R, Hajirostamlou M. Arsenic, Oxidative Stress and Reproductive System.. J Xenobiot 2022 Jul 18;12(3):214-222.
    doi: 10.3390/jox12030016pubmed: 35893266google scholar: lookup
  3. Catalán J, Yánez-Ortiz I, Tvarijonaviciute A, González-Aróstegui LG, Rubio CP, Barranco I, Yeste M, Miró J. Seminal Plasma Antioxidants Are Related to Sperm Cryotolerance in the Horse.. Antioxidants (Basel) 2022 Jun 28;11(7).
    doi: 10.3390/antiox11071279pubmed: 35883774google scholar: lookup
  4. Palacin-Martinez C, Alvarez M, Montes-Garrido R, Neila-Montero M, Anel-Lopez L, de Paz P, Anel L, Riesco MF. Frequency of Semen Collection Affects Ram Sperm Cryoresistance.. Animals (Basel) 2022 Jun 8;12(12).
    doi: 10.3390/ani12121492pubmed: 35739829google scholar: lookup
  5. Capela L, Leites I, Romão R, Lopes-da-Costa L, Pereira RMLN. Impact of Heat Stress on Bovine Sperm Quality and Competence.. Animals (Basel) 2022 Apr 9;12(8).
    doi: 10.3390/ani12080975pubmed: 35454222google scholar: lookup
  6. Yánez-Ortiz I, Catalán J, Delgado-Bermúdez A, Carluccio A, Miró J, Yeste M. Addition of Reduced Glutathione (GSH) to Freezing Medium Reduces Intracellular ROS Levels in Donkey Sperm.. Vet Sci 2021 Dec 2;8(12).
    doi: 10.3390/vetsci8120302pubmed: 34941829google scholar: lookup
  7. Yánez-Ortiz I, Catalán J, Mateo-Otero Y, Dordas-Perpinyà M, Gacem S, Yeste N, Bassols A, Yeste M, Miró J. Extracellular Reactive Oxygen Species (ROS) Production in Fresh Donkey Sperm Exposed to Reductive Stress, Oxidative Stress and NETosis.. Antioxidants (Basel) 2021 Aug 27;10(9).
    doi: 10.3390/antiox10091367pubmed: 34572999google scholar: lookup
  8. Zhu Z, Zeng Y, Zeng W. Cysteine improves boar sperm quality via glutathione biosynthesis during the liquid storage.. Anim Biosci 2022 Feb;35(2):166-176.
    doi: 10.5713/ab.21.0151pubmed: 34445846google scholar: lookup
  9. Pintus E, Ros-Santaella JL. Impact of Oxidative Stress on Male Reproduction in Domestic and Wild Animals.. Antioxidants (Basel) 2021 Jul 20;10(7).
    doi: 10.3390/antiox10071154pubmed: 34356386google scholar: lookup
  10. Bazzano M, Laus F, Spaterna A, Marchegiani A. Use of nutraceuticals in the stallion: Effects on semen quality and preservation.. Reprod Domest Anim 2021 Jul;56(7):951-957.
    doi: 10.1111/rda.13934pubmed: 33772909google scholar: lookup
  11. Gaitskell-Phillips G, Martín-Cano FE, Ortiz-Rodríguez JM, Silva-Rodríguez A, Gil MC, Ortega-Ferrusola C, Peña FJ. In Stallion Spermatozoa, Superoxide Dismutase (Cu-Zn) (SOD1) and the Aldo-Keto-Reductase Family 1 Member b (AKR1B1) Are the Proteins Most Significantly Reduced by Cryopreservation.. J Proteome Res 2021 May 7;20(5):2435-2446.
    doi: 10.1021/acs.jproteome.0c00932pubmed: 33656888google scholar: lookup
  12. Riesco MF, Alvarez M, Anel-Lopez L, Neila-Montero M, Palacin-Martinez C, Montes-Garrido R, Boixo JC, de Paz P, Anel L. Multiparametric Study of Antioxidant Effect on Ram Sperm Cryopreservation-From Field Trials to Research Bench.. Animals (Basel) 2021 Jan 23;11(2).
    doi: 10.3390/ani11020283pubmed: 33498656google scholar: lookup
  13. Catalán J, Papas M, Trujillo-Rojas L, Blanco-Prieto O, Bonilla-Correal S, Rodríguez-Gil JE, Miró J, Yeste M. Red LED Light Acts on the Mitochondrial Electron Chain of Donkey Sperm and Its Effects Depend on the Time of Exposure to Light.. Front Cell Dev Biol 2020;8:588621.
    doi: 10.3389/fcell.2020.588621pubmed: 33365309google scholar: lookup
  14. Bubenickova F, Postlerova P, Simonik O, Sirohi J, Sichtar J. Effect of Seminal Plasma Protein Fractions on Stallion Sperm Cryopreservation.. Int J Mol Sci 2020 Sep 3;21(17).
    doi: 10.3390/ijms21176415pubmed: 32899253google scholar: lookup
  15. F Riesco M, Anel-Lopez L, Neila-Montero M, Palacin-Martinez C, Montes-Garrido R, Alvarez M, de Paz P, Anel L. ProAKAP4 as Novel Molecular Marker of Sperm Quality in Ram: An Integrative Study in Fresh, Cooled and Cryopreserved Sperm.. Biomolecules 2020 Jul 14;10(7).
    doi: 10.3390/biom10071046pubmed: 32674525google scholar: lookup
  16. Kumaresan A, Das Gupta M, Datta TK, Morrell JM. Sperm DNA Integrity and Male Fertility in Farm Animals: A Review.. Front Vet Sci 2020;7:321.
    doi: 10.3389/fvets.2020.00321pubmed: 32637425google scholar: lookup
  17. O'Flaherty C. Reactive Oxygen Species and Male Fertility.. Antioxidants (Basel) 2020 Mar 29;9(4).
    doi: 10.3390/antiox9040287pubmed: 32235383google scholar: lookup
  18. Marzano G, Moscatelli N, Di Giacomo M, Martino NA, Lacalandra GM, Dell'Aquila ME, Maruccio G, Primiceri E, Chiriacò MS, Zara V, Ferramosca A. Centrifugation Force and Time Alter CASA Parameters and Oxidative Status of Cryopreserved Stallion Sperm.. Biology (Basel) 2020 Jan 27;9(2).
    doi: 10.3390/biology9020022pubmed: 32012799google scholar: lookup
  19. Aitken RJ, Drevet JR. The Importance of Oxidative Stress in Determining the Functionality of Mammalian Spermatozoa: A Two-Edged Sword.. Antioxidants (Basel) 2020 Jan 27;9(2).
    doi: 10.3390/antiox9020111pubmed: 32012712google scholar: lookup