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BioMed research international2016; 2016; 9380609; doi: 10.1155/2016/9380609

The Impact of Sperm Metabolism during In Vitro Storage: The Stallion as a Model.

Abstract: In vitro sperm storage is a necessary part of many artificial insemination or in vitro fertilization regimes for many species, including the human and the horse. In many situations spermatozoa are chilled to temperatures between 4 and 10°C for the purpose of restricting the metabolic rate during storage, in turn, reducing the depletion of ATP and the production of detrimental by-products such as reactive oxygen species (ROS). Another result of lowering the temperature is that spermatozoa may be "cold shocked" due to lipid membrane phase separation, resulting in reduced fertility. To overcome this, a method of sperm storage must be developed that will preclude the need to chill spermatozoa. If a thermally induced restriction-of-metabolic-rate strategy is not employed, ATP production must be supported while ameliorating the deleterious effects of ROS. To achieve this end, an understanding of the nature of energy production by the spermatozoa of the species of interest is essential. Human spermatozoa depend predominantly on glycolytic ATP production, producing significantly less ROS than oxidative phosphorylation, with the more efficient pathway predominantly employed by stallion spermatozoa. This review provides an overview of the implications of sperm metabolism for in vitro sperm storage, with a focus on ambient temperature storage in the stallion.
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Publication Date: 2016-01-12 PubMed ID: 26881234PubMed Central: PMC4737440DOI: 10.1155/2016/9380609Google Scholar: Lookup
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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 is an investigation into the effects of sperm metabolism during in vitro storage, using the stallion as a model. It specifically looks at the implications of sperm metabolism on the storage process and provides insights into the possibilities of ambient temperature storage.

Objective of the Research

  • The main objective is to understand the impact of sperm metabolism on its in vitro storage process. The researchers particularly wanted to find a storage method that would eliminate the need to chill spermatozoa, which can lead to ineffective fertility due to ‘cold shock’.

The Process of In Vitro Storage

  • During the in vitro storage, spermatozoa are typically chilled to temperatures between 4 and 10 °C. This procedure is conducted to reduce the metabolic rate of the sperm, minimizing ATP (Adenosine Triphosphate) depletion and the production of harmful by-products like reactive oxygen species (ROS).
  • However, lowering temperatures can cause a “cold shock” to the spermatoa due to lipid membrane phase separation, resulting in reduced fertility. Thus, there is a need for a storage method that does not require the sperm to be chilled.

The Need for Understanding Energy Production

  • If a method is to be developed that does not involve chilling the spermatozoa, it becomes essential to understand the system of energy production in the spermatozoa of the related species.
  • In humans, spermatozoa are mostly dependent on glycolytic ATP production, which produces significantly less reactive oxygen species compared to oxidative phosphorylation – the pathway more commonly used by stallion spermatozoa. Understanding these paths can aid in developing an improved storage method.

Implications for Ambient Temperature Storage

  • The study also evaluates the possibilities for storing spermatozoa at ambient temperatures, which could potentially solve some of the challenges associated with chilled storage.
  • A deeper understanding of sperm metabolism will help to identify the best conditions and methods for ambient temperature storage, which could have significant implications for artificial insemination or in vitro fertilization procedures.

Cite This Article

APA
Gibb Z, Aitken RJ. (2016). The Impact of Sperm Metabolism during In Vitro Storage: The Stallion as a Model. Biomed Res Int, 2016, 9380609. https://doi.org/10.1155/2016/9380609

Publication

BioMed research international
ISSN: 2314-6141
NlmUniqueID: 101600173
Country: United States
Language: English
Volume: 2016
Pages: 9380609

Researcher Affiliations

Gibb, Zamira
  • Priority Research Centre for Reproductive Science, Discipline of Biological Sciences, Faculty of Science and IT, University of Newcastle, Callaghan, NSW 2308, Australia.
Aitken, Robert J
  • Priority Research Centre for Reproductive Science, Discipline of Biological Sciences, Faculty of Science and IT, University of Newcastle, Callaghan, NSW 2308, Australia.

MeSH Terms

  • Animals
  • Cold Temperature
  • Fertilization in Vitro
  • Horses
  • Humans
  • Male
  • Reactive Oxygen Species / metabolism
  • Semen Preservation
  • Sperm Motility / physiology
  • Spermatozoa / metabolism

References

This article includes 85 references
  1. Kosova G, Abney M, Ober C. Heritability of reproductive fitness traits in a human population. Proceedings of the National Academy of Sciences of the United States of America 2010;107(1):1772–1778.
    doi: 10.1073/pnas.0906196106pmc: PMC2868280pubmed: 19822755google scholar: lookup
  2. Nath L C, Anderson G A, McKinnon A O. Reproductive efficiency of Thoroughbred and Standardbred horses in north-east Victoria. Australian Veterinary Journal 2010;88(5):169–175.
    doi: 10.1111/j.1751-0813.2010.00565.xpubmed: 20529022google scholar: lookup
  3. Squires E, Barbacini S, Matthews P. Retrospective study of factors affecting fertility of fresh, cooled and frozen semen. Equine Veterinary Education 2006;18(2):96–99.
  4. Pagl R, Aurich J E, Müller-Schlösser F, Kankofer M, Aurich C. Comparison of an extender containing defined milk protein fractions with a skim milk-based extender for storage of equine semen at 5°C. Theriogenology 2006;66(5):1115–1122.
    doi: 10.1016/j.theriogenology.2006.03.006pubmed: 16620943google scholar: lookup
  5. Aurich J, Aurich C. Developments in European horse breeding and consequences for veterinarians in equine reproduction. Reproduction in Domestic Animals 2006;41(4):275–279.
    doi: 10.1111/j.1439-0531.2006.00719.xpubmed: 16869881google scholar: lookup
  6. Jane M M. Artificial insemination: current and future trends. Artificial Insemination in Farm Animals 2011;1:1–13.
  7. Flesch F M, Gadella B M. Dynamics of the mammalian sperm plasma membrane in the process of fertilization. Biochimica et Biophysica Acta (BBA)—Reviews on Biomembranes 2000;1469(3):197–235.
    doi: 10.1016/s0304-4157(00)00018-6pubmed: 11063883google scholar: lookup
  8. Miller D, Brinkworth M, Iles D. Paternal DNA packaging in spermatozoa: more than the sum of its parts? DNA, histones, protamines and epigenetics. Reproduction 2010;139(2):287–301.
    doi: 10.1530/rep-09-0281pubmed: 19759174google scholar: lookup
  9. Bucci D, Rodriguez-Gil J E, Vallorani C, Spinaci M, Galeati G, Tamanini C. GLUTs and mammalian sperm metabolism. Journal of Andrology 2011;32(4):348–355.
    doi: 10.2164/jandrol.110.011197pubmed: 21088231google scholar: lookup
  10. Vernet P, Aitken R J, Drevet J R. Antioxidant strategies in the epididymis. Molecular and Cellular Endocrinology 2004;216(1):31–39.
    doi: 10.1016/j.mce.2003.10.069pubmed: 15109742google scholar: lookup
  11. Aitken R J, Curry B J. 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. Antioxidants and Redox Signaling 2011;14(3):367–381.
    doi: 10.1089/ars.2010.3186pubmed: 20522002google scholar: lookup
  12. Storey B T. Mammalian sperm metabolism: oxygen and sugar, friend and foe. International Journal of Developmental Biology 2008;52(5-6):427–437.
    doi: 10.1387/ijdb.072522bspubmed: 18649255google scholar: lookup
  13. Kasahara M, Hinkle P C. Reconstitution and purification of the D-glucose transporter from human erythrocytes. The Journal of Biological Chemistry 1977;252(20):7384–7390.
    pubmed: 903365
  14. Angulo C, Rauch M C, Droppelmann A. Hexose transporter expression and function in mammalian spermatozoa: cellular localization and transport of hexoses and vitamin C. Journal of Cellular Biochemistry 1998;71(2):189–203.
    doi: 10.1002/(sici)1097-4644(19981101)71:2lt;189::aid-jcb5>3.0.co;2-rpubmed: 9779818google scholar: lookup
  15. Mueckler M, Caruso C, Baldwin S A. Sequence and structure of a human glucose transporter. Science 1985;229(4717):941–945.
    doi: 10.1126/science.3839598pubmed: 3839598google scholar: lookup
  16. Bucci D, Isani G, Spinaci M. Comparative immunolocalization of GLUTs 1, 2, 3 and 5 in boar, stallion and dog spermatozoa. Reproduction in Domestic Animals 2010;45(2):315–322.
    doi: 10.1111/j.1439-0531.2008.01307.xpubmed: 19055550google scholar: lookup
  17. Gibb Z, Lambourne S R, Aitken R J. The paradoxical relationship between stallion fertility and oxidative stress. Biology of Reproduction 2014;91(3, article 77).
    doi: 10.1095/biolreprod.114.118539pubmed: 25078685google scholar: lookup
  18. Ferrusola C O, Fernández L G, Sandoval C S. Inhibition of the mitochondrial permeability transition pore reduces ‘apoptosis like’ changes during cryopreservation of stallion spermatozoa. Theriogenology 2010;74(3):458–465.
    doi: 10.1016/j.theriogenology.2010.02.029pubmed: 20451990google scholar: lookup
  19. Morrell J M, Johannisson A, Dalin A-M, Hammar L, Sandebert T, Rodriguez-Martinez H. Sperm morphology and chromatin integrity in Swedish warmblood stallions and their relationship to pregnancy rates. Acta Veterinaria Scandinavica 2008;50, article 2.
    doi: 10.1186/1751-0147-50-2pmc: PMC2246141pubmed: 18179691google scholar: lookup
  20. Halliwell B, Gutteridge J M C. Free Radicals in Biology and Medicine. 3rd. Oxford, UK: Oxford University Press; 2003.
  21. Ball B A, Vo A T, Baumber J. Generation of reactive oxygen species by equine spermatozoa. American Journal of Veterinary Research 2001;62(4):508–515.
    doi: 10.2460/ajvr.2001.62.508pubmed: 11327456google scholar: lookup
  22. Aitken R J, Clarkson J S. Cellular basis of defective sperm function and its association with the genesis of reactive oxygen species by human spermatozoa. Journal of Reproduction and Fertility 1987;81(2):459–469.
    doi: 10.1530/jrf.0.0810459pubmed: 2828610google scholar: lookup
  23. Jones R, Mann T, Sherins R. Peroxidative breakdown of phospholipids in human spermatozoa, spermicidal properties of fatty acid peroxides, and protective action of seminal plasma. Fertility and Sterility 1979;31(5):531–537.
    pubmed: 446777
  24. Aitken R J, Gibb Z, Mitchell L A, Lambourne S R, Connaughton H S, De Iuliis G N. 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. Biology of Reproduction 2012;87(5, article 110).
    doi: 10.1095/biolreprod.112.102020pubmed: 22933515google scholar: lookup
  25. Ginther O J, Whitmore H L, Squires E L. Characteristics of estrus, diestrus, and ovulation in mares and effects of season and nursing. American Journal of Veterinary Research 1972;33(10):1935–1939.
    pubmed: 4672613
  26. Brinsko S P, Crockett E C, Squires E L. Effect of centrifugation and partial removal of seminal plasma on equine spermatozoal motility after cooling and storage. Theriogenology 2000;54(1):129–136.
    doi: 10.1016/S0093-691X(00)00331-9pubmed: 10990354google scholar: lookup
  27. Batellier F, Vidament M, Fauquant J. Advances in cooled semen technology. Animal Reproduction Science 2001;68(3-4):181–190.
    doi: 10.1016/s0378-4320(01)00155-5pubmed: 11744263google scholar: lookup
  28. Brinsko S P, Van Wagner G S, Graham J K, Squires E L. Motility, morphology and triple stain analysis of fresh, cooled and frozen-thawed stallion spermatozoa. Journal of Reproduction and Fertility. Supplement 2000;(56):111–120.
    pubmed: 20681122
  29. Nallella K P, Sharma R K, Said T M, Agarwal A. Inter-sample variability in post-thaw human spermatozoa. Cryobiology 2004;49(2):195–199.
    doi: 10.1016/j.cryobiol.2004.07.003pubmed: 15351691google scholar: lookup
  30. Bedford S J, Varner D D, Meyers S A. Effects of cryopreservation on the acrosomal status of stallion spermatozoa. Journal of Reproduction and Fertility Supplement 2000;56:133–140.
    pubmed: 20681125
  31. Brum A M, Sabeur K, Ball B A. Apoptotic-like changes in equine spermatozoa separated by density-gradient centrifugation or after cryopreservation. Theriogenology 2008;69(9):1041–1055.
    doi: 10.1016/j.theriogenology.2008.01.014pubmed: 18378291google scholar: lookup
  32. Neild D M, Gadella B M, Chaves M G, Miragaya M H, Colenbrander B, Agüero A. Membrane changes during different stages of a freeze-thaw protocol for equine semen cryopreservation. Theriogenology 2003;59(8):1693–1705.
    doi: 10.1016/S0093-691X(02)01231-1pubmed: 12566145google scholar: lookup
  33. Valcarce D G, Cartón-García F, Riesco M F, Herráez M P, Robles V. Analysis of DNA damage after human sperm cryopreservation in genes crucial for fertilization and early embryo development. Andrology 2013;1(5):723–730.
    doi: 10.1111/j.2047-2927.2013.00116.xpubmed: 23970451google scholar: lookup
  34. Mazur P, Cole K W. Roles of unfrozen fraction, salt concentration, and changes in cell volume in the survival of frozen human erythrocytes. Cryobiology 1989;26(1):1–29.
    doi: 10.1016/0011-2240(89)90030-8pubmed: 2924590google scholar: lookup
  35. Pegg D E, Diaper M P. The ‘unfrozen fraction’ hypothesis of freezing injury to human erythrocytes: a critical examination of the evidence. Cryobiology 1989;26(1):30–43.
    doi: 10.1016/0011-2240(89)90031-xpubmed: 2924591google scholar: lookup
  36. Pegg D E. Principles of cryopreservation. Methods in Molecular Biology 2007;368:39–57.
    doi: 10.1007/978-1-59745-362-2_3pubmed: 18080461google scholar: lookup
  37. Hammerstedt R H, Graham J K, Nolan J P. Cryopreservation of mammalian sperm: what we ask them to survive. Journal of Andrology 1990;11(1):73–88.
    pubmed: 2179184
  38. Morris G J, Faszer K, Green J E, Draper D, Grout B W W, Fonseca F. Rapidly cooled horse spermatozoa: loss of viability is due to osmotic imbalance during thawing, not intracellular ice formation. Theriogenology 2007;68(5):804–812.
    doi: 10.1016/j.theriogenology.2007.06.009pubmed: 17645937google scholar: lookup
  39. Sardoy M C, Carretero M I, Neild D M. Evaluation of stallion sperm DNA alterations during cryopreservation using toluidine blue. Animal Reproduction Science 2008;107(3-4):349–350.
    doi: 10.1016/j.anireprosci.2008.05.126google scholar: lookup
  40. Klewitz J, Hagen C, Behrendt D, Martinsson G, Sieme H. Effect of multiple freezing of stallion semen on sperm quality and fertility. Animal Reproduction Science 2008;107(3-4):327–328.
    doi: 10.1016/j.anireprosci.2008.05.104google scholar: lookup
  41. Burnaugh L, Ball B A, Sabeur K, Thomas A D, Meyers S A. Osmotic stress stimulates generation of superoxide anion by spermatozoa in horses. Animal Reproduction Science 2010;117(3-4):249–260.
    doi: 10.1016/j.anireprosci.2009.05.014pubmed: 19553037google scholar: lookup
  42. Darin-Bennett A, White I G. Influence of the cholesterol content of mammalian spermatozoa on susceptibility to cold-shock. Cryobiology 1977;14(4):466–470.
    doi: 10.1016/0011-2240(77)90008-6pubmed: 560945google scholar: lookup
  43. Colenbrander B, Gadella B M, Stout T A E. The predictive value of semen analysis in the evaluation of stallion fertility. Reproduction in Domestic Animals 2003;38(4):305–311.
    doi: 10.1046/j.1439-0531.2003.00451.xpubmed: 12887569google scholar: lookup
  44. Bosh K A, Powell D, Shelton B, Zent W. Reproductive performance measures among Thoroughbred mares in central Kentucky, during the 2004 mating season. Equine Veterinary Journal 2009;41(9):883–888.
    doi: 10.2746/042516409x456068pubmed: 20383986google scholar: lookup
  45. Holt W V. Basic aspects of frozen storage of semen. Animal Reproduction Science 2000;62(1–3):3–22.
    doi: 10.1016/s0378-4320(00)00152-4pubmed: 10924818google scholar: lookup
  46. Rota A, Calicchio E, Nardoni S. Presence and distribution of fungi and bacteria in the reproductive tract of healthy stallions. Theriogenology 2011;76(3):464–470.
    doi: 10.1016/j.theriogenology.2011.02.023pubmed: 21529914google scholar: lookup
  47. Aurich C, Spergser J. Influence of bacteria and gentamicin on cooled-stored stallion spermatozoa. Theriogenology 2007;67(5):912–918.
    doi: 10.1016/j.theriogenology.2006.11.004pubmed: 17141306google scholar: lookup
  48. Ortega-Ferrusola C, González-Fernández L, Muriel A. Does the microbial flora in the ejaculate affect the freezeability of stallion sperm?. Reproduction in Domestic Animals 2009;44(3):518–522.
    doi: 10.1111/j.1439-0531.2008.01267.xpubmed: 19655428google scholar: lookup
  49. Varner D D, Scanlan C M, Thompson J A. Bacteriology of preserved stallion semen and antibiotics in semen extenders. Theriogenology 1998;50(4):559–573.
    doi: 10.1016/S0093-691X(98)00161-7pubmed: 10732147google scholar: lookup
  50. Gibb Z, Butler T J, Morris L H A, Maxwell W M C, Grupen C G. Quercetin improves the postthaw characteristics of cryopreserved sex-sorted and nonsorted stallion sperm. Theriogenology 2013;79(6):1001–1009.
    doi: 10.1016/j.theriogenology.2012.06.032pubmed: 23453253google scholar: lookup
  51. de Oliveira R A, Wolf C A, de Oliveira Viu M A, Gambarini M L. Addition of glutathione to an extender for frozen equine semen. Journal of Equine Veterinary Science 2013;33(12):1148–1152.
    doi: 10.1016/j.jevs.2013.05.001google scholar: lookup
  52. Franco J S V, Chaveiro A, da Silva F M. Effect of freezing rates and supplementation of α-tocopherol in the freezing extender in equine sperm cryosurvival. Journal of Equine Veterinary Science 2014;34(8):992–997.
    doi: 10.1016/j.jevs.2014.05.007google scholar: lookup
  53. de Oliveira R A, Wolf C A, Viu M A D, Gambarini M L. Cooling of equine semen at 16 degrees C for 36 h with the addition of cysteine in different concentrations. Pferdeheilkunde 2015;31:27–32.
  54. da Silva C M B, MacÍas-García B, Miró-Morán A. Melatonin reduces lipid peroxidation and apoptotic-like changes in stallion spermatozoa. Journal of Pineal Research 2011;51(2):172–179.
    doi: 10.1111/j.1600-079x.2011.00873.xpubmed: 21486367google scholar: lookup
  55. Giaretta E, Bucci D, Mari G. Is resveratrol effective in protecting stallion cooled semen?. Journal of Equine Veterinary Science 2014;34(11-12):1307–1312.
    doi: 10.1016/j.jevs.2014.09.011google scholar: lookup
  56. Baumber J, Ball B A, Linfor J J. Assessment of the cryopreservation of equine spermatozoa in the presence of enzyme scavengers and antioxidants. American Journal of Veterinary Research 2005;66(5):772–779.
    doi: 10.2460/ajvr.2005.66.772pubmed: 15934604google scholar: lookup
  57. Thomson L K, Fleming S D, Aitken R J, De Iuliis G N, Zieschang J-A, Clark A M. Cryopreservation-induced human sperm DNA damage is predominantly mediated by oxidative stress rather than apoptosis. Human Reproduction 2009;24(9):2061–2070.
    doi: 10.1093/humrep/dep214pubmed: 19525298google scholar: lookup
  58. Moubasher A E, El Din A M E, Ali M E, El-Sherif W T, Gaber H D. Catalase improves motility, vitality and DNA integrity of cryopreserved human spermatozoa. Andrologia 2013;45(2):135–139.
    doi: 10.1111/j.1439-0272.2012.01310.xpubmed: 22591546google scholar: lookup
  59. Banihani S, Agarwal A, Sharma R, Bayachou M. Cryoprotective effect of l-carnitine on motility, vitality and DNA oxidation of human spermatozoa. Andrologia 2014;46(6):637–641.
    doi: 10.1111/and.12130pubmed: 23822772google scholar: lookup
  60. Lisboa F, Hartwig F, Freitas-Dell'Aqua C, Hartwig F, Papa F, Dell’aqua J. Improvement of cooled equine semen by addition of carnitines. Journal of Equine Veterinary Science 2014;34(1):p. 48.
    doi: 10.1016/j.jevs.2013.10.028google scholar: lookup
  61. Lisboa F L, Hartwig F P, Maziero R R D, Monteiro G A, Papa F O, Dell'aqua J A. Use of L-carnitine and acetyl-L-carnitine in cooled-stored stallion semen. Journal of Equine Veterinary Science 2012;32(8):493–494.
  62. Banihani S, Sharma R, Bayachou M, Sabanegh E, Agarwal A. Human sperm DNA oxidation, motility and viability in the presence of l-carnitine during in vitro incubation and centrifugation. Andrologia 2012;44(1):505–512.
    doi: 10.1111/j.1439-0272.2011.01216.xpubmed: 21950483google scholar: lookup
  63. Gibb Z, Lambourne S R, Quadrelli J, Smith N D, Aitken R J. L-carnitine and pyruvate are prosurvival factors during the storage of stallion spermatozoa at room temperature. Biology of Reproduction 2015;93(4, article 104).
    doi: 10.1095/biolreprod.115.131326pubmed: 26316064google scholar: lookup
  64. Littarru G P, Tiano L. Bioenergetic and antioxidant properties of coenzyme Q10: recent developments. Molecular Biotechnology 2007;37(1):31–37.
    doi: 10.1007/s12033-007-0052-ypubmed: 17914161google scholar: lookup
  65. Srinivasan V, Spence D W, Pandi-Perumal S R, Brown G M, Cardinali D P. Melatonin in mitochondrial dysfunction and related disorders. International Journal of Alzheimer's Disease 2011;2011:16.
    doi: 10.4061/2011/326320pmc: PMC3100547pubmed: 21629741google scholar: lookup
  66. Shimizu T, Johnson K A. Kinetic evidence for multiple dynein ATPase sites. The Journal of Biological Chemistry 1983;258(22):3841–3846.
    pubmed: 6227618
  67. de Lamirande E, Jiang H, Zini A, Kodama H, Gagnon C. Reactive oxygen species and sperm physiology. Reviews of Reproduction 1997;2(1):48–54.
    doi: 10.1530/ror.0.0020048pubmed: 9414465google scholar: lookup
  68. Kamp G, Büsselmann G, Lauterwein J. Spermatozoa: models for studying regulatory aspects of energy metabolism. Cellular and Molecular Life Sciences 1996;52:487–494.
    pubmed: 8641386
  69. Silver I A, Erecińska M. Energetic demands of the Na+/K+ ATPase in mammalian astrocytes. Glia 1997;21(1):35–45.
    doi: 10.1002/(sici)1098-1136(199709)21:1<35::aid-glia4>3.0.co;2-0pubmed: 9298845google scholar: lookup
  70. Gülçin I. Antioxidant and antiradical activities of l-carnitine. Life Sciences 2006;78(8):803–811.
    doi: 10.1016/j.lfs.2005.05.103pubmed: 16253281google scholar: lookup
  71. Peluso G, Barbarisi A, Savica V. Carnitine: an osmolyte that plays a metabolic role. Journal of Cellular Biochemistry 2000;80(1):1–10.
    doi: 10.1002/1097-4644(20010101)80:1<1::aid-jcb10>3.0.co;2-wpubmed: 11029749google scholar: lookup
  72. 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):235–244.
    doi: 10.1530/REP-14-0500pubmed: 25504869google scholar: lookup
  73. Li K, Li W, Huang Y-F, Shang X-J. Level of free L-carnitine in human seminal plasma and its correlation with semen quality. National Journal of Andrology 2007;13(2):143–146.
    pubmed: 17345771
  74. Matalliotakis I, Koumantaki Y, Evageliou A, Matalliotakis G, Goumenou A, Koumantakis E. L-carnitine levels in the seminal plasma of fertile and infertile men: correlation with sperm quality. International Journal of Fertility and Women's Medicine 2000;45(3):236–240.
    pubmed: 10929687
  75. Golan R, Weissenberg R, Lewin L M. Carnitine and acetylcarnitine in motile and immotile human spermatozoa. International Journal of Andrology 1984;7(6):484–494.
    doi: 10.1111/j.1365-2605.1984.tb00805.xpubmed: 6526513google scholar: lookup
  76. Jeulin C, Lewin L M. Role of free L-carnitine and acetyl-L-carnitine in post-gonadal maturation of mammalian spermatozoa. Human Reproduction Update 1996;2(2):87–102.
    doi: 10.1093/humupd/2.2.87pubmed: 9079406google scholar: lookup
  77. Lewin L M, Shalev D P, Weissenberg R, Soffer Y. Carnitine and acylcarnitines in semen from azoospermic patients. Fertility and Sterility 1981;36(2):214–218.
    pubmed: 6114878
  78. Stradaioli G, Sylla L, Zelli R. Seminal carnitine and acetylcarnitine content and carnitine acetyltransferase activity in young Maremmano stallions. Animal Reproduction Science 2000;64(3-4):233–245.
    doi: 10.1016/s0378-4320(00)00201-3pubmed: 11121899google scholar: lookup
  79. Brooks D E. Carnitine in the male reproductive tract and its relation to the metabolism of the epididymis and spermatozoa. In: McGarry J. D., Frenkel R. A., editors. Carnitine Biosynthesis Metabolism and Function. New York, NY, USA: Academic Press; 1980. pp. 219–235.
  80. Hinton B T, Setchell B P. Concentration and uptake of carnitine in the rat epididymis. A micropuncture study. In: Frenkel R. A., McGarry J. D., editors. Carnitine Biosynthesis, Metabolism and Function. New York, NY, USA: Academic Press; 1980. p. p. 237.
  81. Stradaioli G, Sylla L, Zelli R, Chiodi P, Monaci M. Effect of L-carnitine administration on the seminal characteristics of oligoasthenospermic stallions. Theriogenology 2004;62(3-4):761–777.
    doi: 10.1016/j.theriogenology.2003.11.018pubmed: 15226028google scholar: lookup
  82. Lee Y H. Functional maturation of mouse epididymal spermatozoa [Ph.D. thesis]. Callaghan, Australia: The University of Newcastle; 2008.
  83. Dello Russo C, Gavrilyuk V, Weinberg G. Peroxisome proliferator-activated receptor gamma thiazolidinedione agonists increase glucose metabolism in astrocytes. Journal of Biological Chemistry 2003;278(8):5828–5836.
    doi: 10.1074/jbc.m208132200pubmed: 12486128google scholar: lookup
  84. Vazquez A, Liu J, Zhou Y, Oltvai Z N. Catabolic efficiency of aerobic glycolysis: the Warburg effect revisited. BMC Systems Biology 2010;4, article 58.
    doi: 10.1186/1752-0509-4-58pmc: PMC2880972pubmed: 20459610google scholar: lookup
  85. Brunmair B, Staniek K, Gras F. Thiazolidinediones, like metformin, inhibit respiratory complex I—a common mechanism contributing to their antidiabetic actions?. Diabetes 2004;53(4):1052–1059.
    doi: 10.2337/diabetes.53.4.1052pubmed: 15047621google scholar: lookup

Citations

This article has been cited 23 times.
  1. Strassner FM, Demattio L, Siuda M, Malama E, Muffels G, Bollwein H. Relationships Between Metabolism of Cryopreserved Equine Sperm Determined by the Seahorse Analyzer and Sperm Characteristics Measured by Flow Cytometry and Computer-Assisted Analysis of Motility. Vet Sci 2025 Nov 21;12(12).
    doi: 10.3390/vetsci12121109pubmed: 41472089google scholar: lookup
  2. Graffeo ML, Dunleavy JEM, Houston BJ, O'Bryan MK. Sperm mitochondrial sheath formation - how and why?. Nat Rev Urol 2025 Nov 11;.
    doi: 10.1038/s41585-025-01109-4pubmed: 41219388google 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. Neila-Montero M, Anel-Lopez L, Maside C, Soriano-Úbeda C, Montes-Garrido R, Palacin-Martinez C, Diez-Zavala V, Borragán S, Silva-Rodríguez A, Martín-Cano FE, Anel L, Alvarez M. A Descriptive Study of Brown Bear (Ursus arctos) Sperm Quality and Proteomic Profiles Considering Sperm Origin. Animals (Basel) 2025 Jul 12;15(14).
    doi: 10.3390/ani15142064pubmed: 40723528google scholar: lookup
  5. Graffeo ML, Nguyen J, Parast FY, Dunleavy JEM, Korneev D, Yang H, Okuda H, O'Connor AE, Conrad DF, Nosrati R, Houston BJ, O'Bryan MK. A novel mechanism of sperm midpiece epididymal maturation and the role of CCDC112 in sperm midpiece formation and establishing an optimal flagella waveform. Cell Commun Signal 2025 Jul 1;23(1):319.
    doi: 10.1186/s12964-025-02320-xpubmed: 40598224google scholar: lookup
  6. Takayama E, Takeuchi H, Yajima H, Enomoto S, Sakamoto M, Nishioka M, Tachibana R, Ikeda T, Kondo E. Inexpensive thermal containers and insulation materials prevent deterioration of semen parameters for less than 90 minutes. J Reprod Dev 2025 Jun 6;71(3):185-190.
    doi: 10.1262/jrd.2025-001pubmed: 40189278google scholar: lookup
  7. Lagares MA, Amaral NA, Braga JJ, Alves NC, Freitas MM, Nicolino RR, Wenceslau RR, Anselmo FDR, Oliveira MMDCS, Costa ED, de Almeida FRCL, Stahlberg R. L-Carnitine enhances porcine sperm quality, longevity, and zona pellucida binding in cooled semen. Anim Reprod 2025;22(1):e20230143.
    doi: 10.1590/1984-3143-AR2023-0143pubmed: 40013121google scholar: lookup
  8. Aliabadi E, Nateghian Z, Nasr-Esfahani MH, Tavalaee M, Talaei-Khozani T. Effects of L-carnitine and pentoxifylline on long-term preservation of the human sperms: An experimental study. Int J Reprod Biomed 2024 Nov;22(11):871-882.
    doi: 10.18502/ijrm.v22i11.17820pubmed: 39866588google scholar: lookup
  9. Lord T. Pathophysiological effects of hypoxia on testis function and spermatogenesis. Nat Rev Urol 2025 Jul;22(7):470-488.
    doi: 10.1038/s41585-024-00969-6pubmed: 39762391google scholar: lookup
  10. Pimpa J, Authaida S, Boonkum W, Rerkyusuke S, Janta C, Chankitisakul V. Unveiling the Potential of Aloe vera Gel Supplementation in a Cooling Extender: A Breakthrough in Enhancing Rooster Sperm Quality and Fertility Ability. Animals (Basel) 2024 Aug 6;14(16).
    doi: 10.3390/ani14162290pubmed: 39199824google scholar: lookup
  11. Garriga F, Maside C, Padilla L, Recuero S, Rodríguez-Gil JE, Yeste M. Heat shock protein 70 kDa (HSP70) is involved in the maintenance of pig sperm function throughout liquid storage at 17 °C. Sci Rep 2024 Jun 11;14(1):13383.
    doi: 10.1038/s41598-024-64488-5pubmed: 38862610google scholar: lookup
  12. Zhang L, Wang X, Sohail T, Jiang C, Sun Y, Wang J, Sun X, Li Y. Punicalagin Protects Ram Sperm from Oxidative Stress by Enhancing Antioxidant Capacity and Mitochondrial Potential during Liquid Storage at 4 °C. Animals (Basel) 2024 Jan 19;14(2).
    doi: 10.3390/ani14020318pubmed: 38275778google scholar: lookup
  13. Sato T, Sugiyama T, Sekijima T. Mating in the cold. Prolonged sperm storage provides opportunities for forced copulation by male bats during winter. Front Physiol 2023;14:1241470.
    doi: 10.3389/fphys.2023.1241470pubmed: 37745243google scholar: lookup
  14. Li Y, Zhang G, Wen F, Xian M, Guo S, Zhang X, Feng X, Hu Z, Hu J. Glucose Starvation Inhibits Ferroptosis by Activating the LKB1/AMPK Signaling Pathway and Promotes the High Speed Linear Motility of Dairy Goat Sperm. Animals (Basel) 2023 Apr 23;13(9).
    doi: 10.3390/ani13091442pubmed: 37174479google scholar: lookup
  15. Bucci D, Spinaci M, Bustamante-Filho IC, Nesci S. The sperm mitochondria: clues and challenges. Anim Reprod 2022;19(4):e20220131.
    doi: 10.1590/1984-3143-AR2022-0131pubmed: 36819482google scholar: lookup
  16. Chankitisakul V, Boonkum W, Kaewkanha T, Pimprasert M, Ratchamak R, Authaida S, Thananurak P. Fertilizing ability and survivability of rooster sperm diluted with a novel semen extender supplemented with serine for practical use on smallholder farms. Poult Sci 2022 Dec;101(12):102188.
    doi: 10.1016/j.psj.2022.102188pubmed: 36257077google scholar: lookup
  17. Cheng Q, Li L, Jiang M, Liu B, Xian Y, Liu S, Liu X, Zhao W, Li F. Extend the Survival of Human Sperm In Vitro in Non-Freezing Conditions: Damage Mechanisms, Preservation Technologies, and Clinical Applications. Cells 2022 Sep 12;11(18).
    doi: 10.3390/cells11182845pubmed: 36139420google scholar: lookup
  18. Bucci D, Spinaci M, Galeati G, Tamanini C. Different approaches for assessing sperm function. Anim Reprod 2020 May 22;16(1):72-80.
    doi: 10.21451/1984-3143-AR2018-122pubmed: 33299480google scholar: lookup
  19. Fu L, Liu Y, An Q, Zhang J, Tong Y, Zhou F, Lu W, Liang X, Gu Y. Glycolysis metabolic changes in sperm cryopreservation based on a targeted metabolomic strategy. Int J Clin Exp Pathol 2019;12(5):1775-1781.
    pubmed: 31933997
  20. 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 Dec 16;19(1):133.
    doi: 10.1186/s12894-019-0565-2pubmed: 31842847google scholar: lookup
  21. Keshtgar S PhD, Bagheri S MSc, Ebrahimi B MSc. Comparing Human Sperm Quality Preserved at Two Different Temperatures; Effect of Trolox, Coenzyme Q10 and Extracellular Adenosine Triphosphate. Iran J Med Sci 2018 Sep;43(5):541-545.
    pubmed: 30214107
  22. Sommer AP, Jaganathan S, Maduro MR, Hancke K, Janni W, Fecht HJ. Genesis on diamonds II: contact with diamond enhances human sperm performance by 300. Ann Transl Med 2016 Oct;4(20):407.
    doi: 10.21037/atm.2016.08.18pubmed: 27867959google scholar: lookup
  23. Li YJ, Han Z, Ge L, Zhou CJ, Zhao YF, Wang DH, Ren J, Niu XX, Liang CG. C-phycocyanin protects against low fertility by inhibiting reactive oxygen species in aging mice. Oncotarget 2016 Apr 5;7(14):17393-409.
    doi: 10.18632/oncotarget.8165pubmed: 27008700google scholar: lookup
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