Analyze Diet
Journal of proteome research2021; 20(5); 2435-2446; doi: 10.1021/acs.jproteome.0c00932

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.

Abstract: Although cryopreservation is widely used in animal breeding, the technique is still suboptimal. The population of spermatozoa surviving the procedure experiences changes attributed to alteration in their redox regulation. In order to expand our knowledge regarding this particular aspect, the proteome in fresh and frozen thawed aliquots of equine spermatozoa was studied to identify the proteins most severely affected by the procedure. If alteration of redox regulation is a major factor explaining cryodamage, proteins participating in redox regulation should be principally affected. Using a split sample design, 30 ejaculates from 10 different stallions were analyzed as fresh spermatozoa, and another aliquot from the same ejaculate was analyzed as a frozen thawed sample. The proteome was studied under both conditions using UHPLC-MS/MS and bioinformatic analysis conducted to identify discriminant variables between both conditions. Data are available through the ProteomeXchange Consortium with identifier PXD022236. The proteins most significantly reduced were Aldo-keto reductase family 1 member B (p = 2.2 × 10-17) and Superoxide dismutase (Cu-Zn) (p = 4.7 × 10-14). This is the first time that SOD1 has been identified as a discriminating variable using bioinformatic analysis, where it was one of the most highly significantly different proteins seen between fresh and frozen thawed semen. This finding strongly supports the theory that alteration in redox regulation and oxidative stress is a major factor involved in cryodamage and suggests that control of redox regulation should be a major target to improve current cryopreservation procedures.
Publication Date: 2021-03-03 PubMed ID: 33656888PubMed Central: PMC8562871DOI: 10.1021/acs.jproteome.0c00932Google 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
  • Research Support
  • Non-U.S. Gov't

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.

The research article investigates the impact of cryopreservation on stallion spermatozoa, revealing that Superoxide Dismutase (Cu-Zn) (SOD1) and Aldo-Keto-Reductase Family 1 Member b (AKR1B1) are the proteins most significantly affected by the procedure.

Research Objective and Methodology

  • The research aims to expand understanding of changes in the proteome (a set of proteins expressed by a genome, cell, tissue or organism) in stallion spermatozoa due to cryopreservation, a widely used but still suboptimal technique in animal breeding. The particular focus is on proteins related to redox regulation as these are likely to be most affected by cryodamage.
  • The procedure involves analysing 30 ejaculates from 10 different stallions, both as fresh spermatozoa and as another aliquot from the same ejaculate after undergoing cryopreservation. This split sample design allows for direct comparison of changes caused by this process.
  • Analysis of the proteome in these conditions was performed using Ultra High Performance Liquid Chromatography-Tandem Mass Spectrometry (UHPLC-MS/MS). Following this, bioinformatic procedures were used to identify the proteins showing the most significant changes between fresh and frozen semen.

Research Findings

  • The study found that Superoxide Dismutase (Cu-Zn) (SOD1) and Aldo-Keto-Reductase Family 1 Member b (AKR1B1) were the proteins most significantly reduced by cryopreservation. This is the first time that SOD1 has been identified as significantly different between fresh and frozen semen using bioinformatic analysis.
  • These findings suggest that alterations in redox regulation, which involves the control of oxidation and reduction reactions in a cell, and resultant oxidative stress are major factors contributing to cryodamage. This implies that to improve cryopreservation procedures, research should target control of redox regulation.

Concluding Remarks

  • This study provides new insight into the impact of cryopreservation on stallion spermatozoa at the proteomic level. In particular, it highlights the key role of proteins associated with redox regulation in explaining the damaging effects of freezing-thawing techniques on spermatozoa viability.
  • The findings here can guide future research and development efforts in animal breeding techniques, particularly improvements in spermatozoa cryopreservation.

Cite This Article

APA
Gaitskell-Phillips G, Martín-Cano FE, Ortiz-Rodríguez JM, Silva-Rodríguez A, Gil MC, Ortega-Ferrusola C, Peña FJ. (2021). 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, 20(5), 2435-2446. https://doi.org/10.1021/acs.jproteome.0c00932

Publication

ISSN: 1535-3907
NlmUniqueID: 101128775
Country: United States
Language: English
Volume: 20
Issue: 5
Pages: 2435-2446

Researcher Affiliations

Gaitskell-Phillips, Gemma
  • 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.
Ortiz-Rodríguez, José M
  • Laboratory of Equine Reproduction and Equine Spermatology, Veterinary Teaching Hospital, University of Extremadura, 10003 Cáceres, Spain.
Silva-Rodríguez, Antonio
  • Facility of Innovation and Analysis in Animal Source Foodstuffs, University of Extremadura, 10003 Cáceres, Spain.
Gil, Maria 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.
Peña, Fernando J
  • Laboratory of Equine Reproduction and Equine Spermatology, Veterinary Teaching Hospital, University of Extremadura, 10003 Cáceres, Spain.

MeSH Terms

  • Aldehyde Reductase
  • Animals
  • Cryopreservation
  • Horses
  • Male
  • Oxidoreductases
  • Sperm Motility
  • Spermatozoa
  • Superoxide Dismutase / genetics
  • Superoxide Dismutase-1 / genetics
  • Tandem Mass Spectrometry

Conflict of Interest Statement

The authors declare no competingfinancial interest.

References

This article includes 57 references
  1. Aurich J, Kuhl J, Tichy A, Aurich C. Efficiency of Semen Cryopreservation in Stallions. Animals (Basel) 2020, 10 (6), 1033.
    doi: 10.3390/ani10061033pmc: PMC7341245pubmed: 32545785google scholar: lookup
  2. Greiser T, Sieme H, Martinsson G, Distl O. Breed and stallion effects on frozen-thawed semen in warmblood, light and quarter horses. Theriogenology 2020, 142, 8–14.
  3. Mislei B, Bucci D, Malama E, Bollwein H, Mari G. Seasonal changes in ROS concentrations and sperm quality in unfrozen and frozen-thawed stallion semen. Theriogenology 2020, 144, 89–97.
  4. Pena F J, Garcia B M, Samper J C, Aparicio I M, Tapia J A, Ferrusola C O. Dissecting the molecular damage to stallion spermatozoa: the way to improve current cryopreservation protocols?. Theriogenology 2011, 76 (7), 1177–1186.
  5. Agarwal A, Bertolla R P, Samanta L. Sperm proteomics: potential impact on male infertility treatment. Expert Rev. Proteomics 2016, 13 (3), 285–96.
    doi: 10.1586/14789450.2016.1151357pubmed: 26853600google scholar: lookup
  6. Amaral A, Paiva C, Attardo Parrinello C, Estanyol J M, Ballesca J L, Ramalho-Santos J, Oliva R. Identification of proteins involved in human sperm motility using high-throughput differential proteomics. J. Proteome Res. 2014, 13 (12), 5670–84.
    doi: 10.1021/pr500652ypubmed: 25250979google scholar: lookup
  7. Ko E Y. Sperm proteomics: fertility diagnostic testing beyond the semen analysis?. Fertil. Steril. 2014, 101 (6), 1585.
  8. Oliva R, De Mateo S, Castillo J, Azpiazu R, Oriola J, Ballesca J L. Methodological advances in sperm proteomics. Hum. Fertil. (Stockholm, Swed.) 2010, 13 (4), 263–7.
    doi: 10.3109/14647273.2010.516877pubmed: 21117936google scholar: lookup
  9. Aitken R J, Baker M A. The role of proteomics in understanding sperm cell biology. Int. J. Androl. 2008, 31 (3), 295–302.
  10. Swegen A, Curry B J, Gibb Z, Lambourne S R, Smith N D, Aitken R J. Investigation of the stallion sperm proteome by mass spectrometry. Reproduction 2015, 149 (3), 235–44.
    doi: 10.1530/REP-14-0500pubmed: 25504869google scholar: lookup
  11. Martin-Cano F E, Gaitskell-Phillips G, Ortiz-Rodriguez J M, Silva-Rodriguez A, Roman A, Rojo-Dominguez P, Alonso-Rodriguez E, Tapia J A, Gil M C, Ortega-Ferrusola C, Pena F J. Proteomic profiling of stallion spermatozoa suggests changes in sperm metabolism and compromised redox regulation after cryopreservation. J. Proteomics 2020, 221, 103765.
    doi: 10.1016/j.jprot.2020.103765pubmed: 32247875google scholar: lookup
  12. Peris-Frau P, Soler A J, Iniesta-Cuerda M, Martin-Maestro A, Sanchez-Ajofrin I, Medina-Chavez D A, Fernandez-Santos M R, Garcia-Alvarez O, Maroto-Morales A, Montoro V, Garde J J. Sperm Cryodamage in Ruminants: Understanding the Molecular Changes Induced by the Cryopreservation Process to Optimize Sperm Quality. Int. J. Mol. Sci. 2020, 21 (8), 2781.
    doi: 10.3390/ijms21082781pmc: PMC7215299pubmed: 32316334google scholar: lookup
  13. Parrilla I, Perez-Patino C, Li J, Barranco I, Padilla L, Rodriguez-Martinez H, Martinez E A, Roca J. Boar semen proteomics and sperm preservation. Theriogenology 2019, 137, 23–29.
  14. Fu L, An Q, Zhang K, Liu Y, Tong Y, Xu J, Zhou F, Wang X, Guo Y, Lu W, Liang X, Gu Y. Quantitative proteomic characterization of human sperm cryopreservation: using data-independent acquisition mass spectrometry. BMC Urol. 2019, 19 (1), 133.
    doi: 10.1186/s12894-019-0565-2pmc: PMC6916233pubmed: 31842847google scholar: lookup
  15. Perez-Patino C, Barranco I, Li J, Padilla L, Martinez E A, Rodriguez-Martinez H, Roca J, Parrilla I. Cryopreservation Differentially Alters the Proteome of Epididymal and Ejaculated Pig Spermatozoa. Int. J. Mol. Sci. 2019, 20 (7), 1791.
    doi: 10.3390/ijms20071791pmc: PMC6479301pubmed: 30978930google scholar: lookup
  16. Panner Selvam M K, Agarwal A, Pushparaj P N. Altered Molecular Pathways in the Proteome of Cryopreserved Sperm in Testicular Cancer Patients before Treatment. Int. J. Mol. Sci. 2019, 20 (3), 677.
    doi: 10.3390/ijms20030677pmc: PMC6387327pubmed: 30764484google scholar: lookup
  17. Pini T, Rickard J P, Leahy T, Crossett B, Druart X, de Graaf S P. Cryopreservation and egg yolk medium alter the proteome of ram spermatozoa. J. Proteomics 2018, 181, 73–82.
    doi: 10.1016/j.jprot.2018.04.001pubmed: 29627624google scholar: lookup
  18. Bogle O A, Kumar K, Attardo-Parrinello C, Lewis S E, Estanyol J M, Ballesca J L, Oliva R. Identification of protein changes in human spermatozoa throughout the cryopreservation process. Andrology 2017, 5 (1), 10–22.
    doi: 10.1111/andr.12279pubmed: 27860400google scholar: lookup
  19. Morrell J M, Garcia B M, Pena F J, Johannisson A. Processing stored stallion semen doses by Single Layer Centrifugation. Theriogenology 2011, 76 (8), 1424–32.
  20. Ortega-Ferrusola C, Garcia B M, Gallardo-Bolanos J M, Gonzalez-Fernandez L, Rodriguez-Martinez H, Tapia J A, Pena F J. Apoptotic markers can be used to forecast the freezeability of stallion spermatozoa. Anim. Reprod. Sci. 2009, 114 (4), 393–403.
  21. Hall S E, Aitken R J, Nixon B, Smith N D, Gibb Z. Electrophilic aldehyde products of lipid peroxidation selectively adduct to heat shock protein 90 and arylsulfatase A in stallion spermatozoa. Biol. Reprod. 2017, 96 (1), 107–121.
    pubmed: 28395341
  22. Ortega Ferrusola C, Anel-Lopez L, Ortiz-Rodriguez J M, Martin Munoz P, Alvarez M, de Paz P, Masot J, Redondo E, Balao da Silva C, Morrell J M, Rodriguez Martinez H, Tapia J A, Gil M C, Anel L, Pena F J. Stallion spermatozoa surviving freezing and thawing experience membrane depolarization and increased intracellular Na(). Andrology 2017, 5 (6), 1174–1182.
    doi: 10.1111/andr.12419pubmed: 28973824google scholar: lookup
  23. Adams G P, Ratto M H, Collins C W, Bergfelt D R. Artificial insemination in South American camelids and wild equids. Theriogenology 2009, 71 (1), 166–75.
  24. Hodge K, Have S T, Hutton L, Lamond A I. Cleaning up the masses: exclusion lists to reduce contamination with HPLC-MS/MS. J. Proteomics 2013, 88, 92–103.
    doi: 10.1016/j.jprot.2013.02.023pmc: PMC3714598pubmed: 23501838google scholar: lookup
  25. Fontes M, Soneson C. The projection score--an evaluation criterion for variable subset selection in PCA visualization. BMC Bioinf. 2011, 12, 307.
    doi: 10.1186/1471-2105-12-307pmc: PMC3167802pubmed: 21798031google scholar: lookup
  26. Bourgon R, Gentleman R, Huber W. Independent filtering increases detection power for high-throughput experiments. Proc. Natl. Acad. Sci. U. S. A. 2010, 107 (21), 9546–51.
    doi: 10.1073/pnas.0914005107pmc: PMC2906865pubmed: 20460310google scholar: lookup
  27. Eisen M B, Spellman P T, Brown P O, Botstein D. Cluster analysis and display of genome-wide expression patterns. Proc. Natl. Acad. Sci. U. S. A. 1998, 95 (25), 14863–8.
    doi: 10.1073/pnas.95.25.14863pmc: PMC24541pubmed: 9843981google scholar: lookup
  28. Rios-Soto L, Avitia-Dominguez C, Sierra-Campos E, Valdez-Solana M, Cisneros-Martinez J, Palacio-Gastellum M G, Tellez-Valencia A. Virtual Screening, Molecular Dynamics and ADME-Tox Tools for Finding Potential Inhibitors of Phosphoglycerate Mutase 1 from Plasmodium falciparum. Curr. Top. Med. Chem. 2018, 18 (18), 1610–1617.
  29. Jia X, Han Q, Lu Z. Analyzing the similarity of samples and genes by MG-PCC algorithm, t-SNE-SS and t-SNE-SG maps. BMC Bioinf. 2018, 19 (1), 512.
    doi: 10.1186/s12859-018-2495-5pmc: PMC6296107pubmed: 30558536google scholar: lookup
  30. Tamhane A C, Hochberg Y, Dunnett C W. Multiple test procedures for dose finding. Biometrics 1996, 52 (1), 21–37.
    doi: 10.2307/2533141pubmed: 8934584google scholar: lookup
  31. Viskoper R J, Laszt A, Oren S, Hochberg Y, Villa Y, Drexler I, Bregman L, Mishal J. The antihypertensive effect of atenolol and bopindolol in the elderly. Netherlands J. Med. 1989, 35 (3–4), 185–191.
    pubmed: 2574832
  32. Raudvere U, Kolberg L, Kuzmin I, Arak T, Adler P, Peterson H, Vilo J. g:Profiler: a web server for functional enrichment analysis and conversions of gene lists (2019 update). Nucleic Acids Res. 2019, 47 (W1), W191–W198.
    doi: 10.1093/nar/gkz369pmc: PMC6602461pubmed: 31066453google scholar: lookup
  33. Cook N L, Masterson K R, Battaglia D, Beck R, Metcalf E S. Dimethyl sulfoxide and glycerol as cryoprotectant agents of stallion semen: effects on blastocyst rates following intracytoplasmic sperm injection of IVM equine oocytes. Reprod., Fertil. Dev. 2020, 32 (3), 253–258.
    doi: 10.1071/RD19266pubmed: 32172784google scholar: lookup
  34. Ortega-Ferrusola C, Macias Garcia B, Suarez Rama V, Gallardo-Bolanos J M, Gonzalez-Fernandez L, Tapia J A, Rodriguez-Martinez H, Pena F J. Identification of sperm subpopulations in stallion ejaculates: changes after cryopreservation and comparison with traditional statistics. Reprod. Domest. Anim. 2009, 44 (3), 419–23.
  35. Martinez I N, Moran J M, Pena F J. Two-step cluster procedure after principal component analysis identifies sperm subpopulations in canine ejaculates and its relation to cryoresistance. J. Androl. 2006, 27 (4), 596–603.
    doi: 10.2164/jandrol.05153pubmed: 16582416google scholar: lookup
  36. Martin Munoz P, Anel-Lopez L, Ortiz-Rodriguez J M, Alvarez M, de Paz P, Balao da Silva C, Rodriguez Martinez H, Gil M C, Anel L, Pena F J, Ortega Ferrusola C. Redox cycling induces spermptosis and necrosis in stallion spermatozoa while the hydroxyl radical (OH*) only induces spermptosis. Reprod Domest Anim 2018, 53 (1), 54–67.
    doi: 10.1111/rda.13052pubmed: 28833663google scholar: lookup
  37. Munoz P M, Ferrusola C O, Lopez L A, Del Petre C, Garcia M A, de Paz Cabello P, Anel L, Pena F J. Caspase 3 Activity and Lipoperoxidative Status in Raw Semen Predict the Outcome of Cryopreservation of Stallion Spermatozoa. Biol. Reprod. 2016, 95 (3), 53.
    doi: 10.1095/biolreprod.116.139444pubmed: 27417910google scholar: lookup
  38. Perez-Riverol Y, Csordas A, Bai J, Bernal-Llinares M, Hewapathirana S, Kundu D J, Inuganti A, Griss J, Mayer G, Eisenacher M, Perez E, Uszkoreit J, Pfeuffer J, Sachsenberg T, Yilmaz S, Tiwary S, Cox J, Audain E, Walzer M, Jarnuczak A F, Ternent T, Brazma A, Vizcaino J A. The PRIDE database and related tools and resources in 2019: improving support for quantification data. Nucleic Acids Res. 2019, 47 (D1), D442–D450.
    doi: 10.1093/nar/gky1106pmc: PMC6323896pubmed: 30395289google scholar: lookup
  39. Mazur P, Koshimoto C. Is intracellular ice formation the cause of death of mouse sperm frozen at high cooling rates?. Biol. Reprod. 2002, 66 (5), 1485–90.
    doi: 10.1095/biolreprod66.5.1485pubmed: 11967214google scholar: lookup
  40. Koshimoto C, Mazur P. Effects of cooling and warming rate to and from −70 degrees C, and effect of further cooling from −70 to −196 degrees C on the motility of mouse spermatozoa. Biol. Reprod. 2002, 66 (5), 1477–84.
    doi: 10.1095/biolreprod66.5.1477pubmed: 11967213google scholar: lookup
  41. Ortiz-Rodriguez J M, Martin-Cano F E, Ortega-Ferrusola C, Masot J, Redondo E, Gazquez A, Gil M C, Aparicio I M, Rojo-Dominguez P, Tapia J A, Rodriguez-Martinez H, Pena F J. 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, 101 (1), 208–222.
    doi: 10.1093/biolre/ioz069pubmed: 30998234google scholar: lookup
  42. Roca J, Perez-Patino C, Barranco I, Padilla L C, Martinez E A, Rodriguez-Martinez H, Parrilla I. Proteomics in fresh and preserved pig semen: Recent achievements and future challenges. Theriogenology 2020, 150, 41–47.
  43. Campos-Shimada L B, Hideo Gilglioni E, Fernandes Garcia R, Rizato Martins-Maciel E, Luiza Ishii-Iwamoto E, Luzia Salgueiro-Pagadigorria C. Superoxide dismutase: a review and a modified protocol for activities measurements in rat livers. Arch. Physiol. Biochem. 2018, 1–8.
    pubmed: 30372625
  44. Azadmanesh J, Borgstahl G E O. A Review of the Catalytic Mechanism of Human Manganese Superoxide Dismutase. Antioxidants 2018, 7 (2), 25.
    doi: 10.3390/antiox7020025pmc: PMC5836015pubmed: 29385710google scholar: lookup
  45. Rakhit R, Chakrabartty A. Structure, folding, and misfolding of Cu,Zn superoxide dismutase in amyotrophic lateral sclerosis. Biochim. Biophys. Acta, Mol. Basis Dis. 2006, 1762 (11–12), 1025–37.
    doi: 10.1016/j.bbadis.2006.05.004pubmed: 16814528google scholar: lookup
  46. Chen X, Zhu H, Hu C, Hao H, Zhang J, Li K, Zhao X, Qin T, Zhao K, Zhu H, Wang D. Identification of differentially expressed proteins in fresh and frozen-thawed boar spermatozoa by iTRAQ-coupled 2D LC-MS/MS. Reproduction 2014, 147 (3), 321–30.
    doi: 10.1530/REP-13-0313pubmed: 24357664google scholar: lookup
  47. Shen Y, Zhong L, Johnson S, Cao D. Human aldo-keto reductases 1B1 and 1B10: a comparative study on their enzyme activity toward electrophilic carbonyl compounds. Chem.-Biol. Interact. 2011, 191 (1–3), 192–8.
    doi: 10.1016/j.cbi.2011.02.004pmc: PMC3103604pubmed: 21329684google scholar: lookup
  48. Baker M A, Weinberg A, Hetherington L, Villaverde A I, Velkov T, Baell J, Gordon C P. Defining the mechanisms by which the reactive oxygen species by-product, 4-hydroxynonenal, affects human sperm cell function. Biol. Reprod. 2015, 92 (4), 108.
    pubmed: 25673561
  49. Martin Munoz P, Ortega Ferrusola C, Vizuete G, Plaza Davila M, Rodriguez Martinez H, Pena F J. 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, 93 (6), 143.
    pubmed: 26536905
  50. Huang P, Li W, Yang Z, Zhang N, Xu Y, Bao J, Jiang D, Dong X. LYZL6, an acidic, bacteriolytic, human sperm-related protein, plays a role in fertilization. PLoS One 2017, 12 (2), e0171452.
  51. Watson P F. The causes of reduced fertility with cryopreserved semen. Anim. Reprod. Sci. 2000, 60–61, 481–92.
    doi: 10.1016/S0378-4320(00)00099-3pubmed: 10844218google scholar: lookup
  52. Silva J V, Yoon S, De Bock P J, Goltsev A V, Gevaert K, Mendes J F, Fardilha M. Construction and analysis of a human testis/sperm-enriched interaction network: Unraveling the PPP1CC2 interactome. Biochim. Biophys. Acta, Gen. Subj. 2017, 1861 (2), 375–385.
    doi: 10.1016/j.bbagen.2016.11.041pubmed: 27913189google scholar: lookup
  53. Pena F J, O’Flaherty C, Ortiz Rodriguez J M, Martin Cano F E, Gaitskell-Phillips G L, Gil M C, Ortega Ferrusola C. Redox Regulation and Oxidative Stress: The Particular Case of the Stallion Spermatozoa. Antioxidants (Basel) 2019, 8 (11), 567.
    doi: 10.3390/antiox8110567pmc: PMC6912273pubmed: 31752408google scholar: lookup
  54. Wang S, Wang W, Xu Y, Tang M, Fang J, Sun H, Sun Y, Gu M, Liu Z, Zhang Z, Lin F, Wu T, Song N, Wang Z, Zhang W, Yin C. Proteomic characteristics of human sperm cryopreservation. Proteomics 2014, 14 (2–3), 298–310.
    doi: 10.1002/pmic.201300225pubmed: 24259508google scholar: lookup
  55. Willoughby C E, Mazur P, Peter A T, Critser J K. Osmotic tolerance limits and properties of murine spermatozoa. Biol. Reprod. 1996, 55 (3), 715–27.
    doi: 10.1095/biolreprod55.3.715pubmed: 8862792google scholar: lookup
  56. Makeyeva Y, Nicol C, Ledger W L, Ryugo D K. Immunocytochemical Localization of Olfactory-signaling Molecules in Human and Rat Spermatozoa. J. Histochem. Cytochem. 2020, 68 (7), 491–513.
    doi: 10.1369/0022155420939833pmc: PMC7350079pubmed: 32603211google scholar: lookup
  57. Flegel C, Vogel F, Hofreuter A, Schreiner B S, Osthold S, Veitinger S, Becker C, Brockmeyer N H, Muschol M, Wennemuth G, Altmuller J, Hatt H, Gisselmann G. Characterization of the Olfactory Receptors Expressed in Human Spermatozoa. Front. Mol. Biosci. 2015, 2, 73.
    pmc: PMC4703994pubmed: 26779489

Citations

This article has been cited 9 times.
  1. Wang S, Shi L, Zhang Z, Liu J, Xing J, Yang J, Duan J, Li B, Cao G. NT5C1B Improves Fertility of Boar Spermatozoa by Enhancing Quality and Cryotolerance During Cryopreservation. Animals (Basel) 2025 Dec 8;15(24).
    doi: 10.3390/ani15243530pubmed: 41463814google scholar: lookup
  2. Wang S, Zhang H, Min L, Zhang S, Liu Z, Adetunji AO, Zhu Z. Proteomic and metabolomic profiling reveal alterations in freezing-thawing and fresh drake sperm. Poult Sci 2026 Jan;105(1):106192.
    doi: 10.1016/j.psj.2025.106192pubmed: 41371193google scholar: lookup
  3. Ullah A, Chen W, Shi L, Wang M, Geng M, Na J, Akhtar MF, Khan MZ, Wang C. Challenges and Enhancing Strategies of Equine Semen Preservation: Nutritional and Genetic Perspectives. Vet Sci 2025 Aug 25;12(9).
    doi: 10.3390/vetsci12090807pubmed: 41012733google scholar: lookup
  4. Fan Y, Lv W, Li X, Wanma G, Li J, Xiong X, He X, Wang Y, Yin S, Fu W, He H, Lin Y, Lan D, Xiong Y. Artesunate improves cryopreserved yak sperm quality by activating SOD1 antioxidant pathway. Front Vet Sci 2025;12:1613506.
    doi: 10.3389/fvets.2025.1613506pubmed: 40654506google scholar: lookup
  5. Zhang R, Wang X, Liu R, Mei Y, Miao X, Ma J, Zou L, Zhao Q, Bai X, Dong Y. Proteomics and metabolomics analyses of mechanism underlying bovine sperm cryoinjury. BMC Genomics 2025 Jan 22;26(1):63.
    doi: 10.1186/s12864-025-11258-wpubmed: 39844026google scholar: lookup
  6. Hernández-Avilés C, Ramírez-Agámez L, Weintraub ST, Scoggin CF, Davis BW, Raudsepp T, Varner DD, Love CC. Proteomic analysis of sperm from fertile stallions and subfertile stallions due to impaired acrosomal exocytosis. Sci Rep 2024 May 30;14(1):12446.
    doi: 10.1038/s41598-024-63410-3pubmed: 38816557google scholar: lookup
  7. Egyptien S, Deleuze S, Ledeck J, Ponthier J. Sperm Quality Assessment in Stallions: How to Choose Relevant Assays to Answer Clinical Questions. Animals (Basel) 2023 Oct 6;13(19).
    doi: 10.3390/ani13193123pubmed: 37835729google scholar: lookup
  8. Gaitskell-Phillips G, Martín-Cano FE, Ortiz-Rodríguez JM, Silva-Rodríguez A, da Silva-Álvarez E, Gil MC, Ortega-Ferrusola C, Peña FJ. Dataset of the sperm proteome of stallions with different motility. Data Brief 2022 Dec;45:108578.
    doi: 10.1016/j.dib.2022.108578pubmed: 36131951google scholar: lookup
  9. Mateo-Otero Y, Ribas-Maynou J, Delgado-Bermúdez A, Llavanera M, Recuero S, Barranco I, Yeste M. Aldose Reductase B1 in Pig Sperm Is Related to Their Function and Fertilizing Ability. Front Endocrinol (Lausanne) 2022;13:773249.
    doi: 10.3389/fendo.2022.773249pubmed: 35173684google scholar: lookup