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Animals : an open access journal from MDPI2021; 11(11); doi: 10.3390/ani11113248

An Update on Semen Physiology, Technologies, and Selection Techniques for the Advancement of In Vitro Equine Embryo Production: Section I.

Abstract: As the use of assisted reproductive technologies (ART) and in vitro embryo production (IVP) expand in the equine industry, it has become necessary to further our understanding of semen physiology as it applies to overall fertility. This segment of our two-section review will focus on normal sperm parameters, beginning with development and extending through the basic morphology of mature spermatozoa, as well as common issues with male factor infertility in IVP. Ultimately, the relevance of sperm parameters to overall male factor fertility in equine IVP will be assessed.
Publication Date: 2021-11-13 PubMed ID: 34827983PubMed Central: PMC8614440DOI: 10.3390/ani11113248Google Scholar: Lookup
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  • 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 paper discusses an update on the understanding of equine semen physiology, technologies, and selection methods for development in the area of in vitro equine embryo production, with particular emphasis on sperm parameters and fertility.

Objective of the Research

  • The research primarily aims to understand and discuss the knowledge advancements in equine semen physiology, the technologies used, and the selection techniques that contribute to the expansion of in vitro embryo production (IVP) in the equine industry.

Scope of the Research

  • The study provides a comprehensive review in two distinct sections. This abstract discusses the first section, which focuses specifically on standard sperm parameters concerning male fertility in in vitro equine embryo production.
  • This section begins with an exploration of sperm development and extends to the basic morphology, that is the shape and structure, of mature spermatozoa.

Issues Addressed in the Research

  • The problems dealt with in the study are principally related to the male factor infertility in the process of in vitro equine embryo production.
  • The relevance and impact of sperm parameters on male fertility in the mentioned process is an additional issue to be assessed in the research.

Significance of the Research

  • With the increasing dependency on Assisted Reproductive Technologies (ART) in the equine industry, understanding the semen physiology becomes crucial to enhancing overall fertility.
  • The research, in its depth and comprehensive approach to understanding sperm parameters, holds significant relevance as it can offer insights that could potentially enhance equine in vitro embryo production.

Cite This Article

APA
Orsolini MF, Meyers SA, Dini P. (2021). An Update on Semen Physiology, Technologies, and Selection Techniques for the Advancement of In Vitro Equine Embryo Production: Section I. Animals (Basel), 11(11). https://doi.org/10.3390/ani11113248

Publication

ISSN: 2076-2615
NlmUniqueID: 101635614
Country: Switzerland
Language: English
Volume: 11
Issue: 11

Researcher Affiliations

Orsolini, Morgan F
  • Department of Population Health and Reproduction, School of Veterinary Medicine, University of California, Davis, CA 95616, USA.
Meyers, Stuart A
  • Department of Anatomy, Physiology, and Cell Biology, School of Veterinary Medicine, University of California, Davis, CA 95616, USA.
Dini, Pouya
  • Department of Population Health and Reproduction, School of Veterinary Medicine, University of California, Davis, CA 95616, USA.

Conflict of Interest Statement

The authors declare have no conflict of interest.

References

This article includes 159 references
  1. Katila T. Sperm-uterine interactions. .
  2. Holt W.V, Van Look K.J.W. Concepts in sperm heterogeneity, sperm selection and sperm competition as biological foundations for laboratory tests of semen quality. Reproduction 2004;127:527–535.
    doi: 10.1530/rep.1.00134pubmed: 15129008google scholar: lookup
  3. Amann R. Spermatogenesis in the stallion: A review. J. Equine Vet. Sci. 1981;1:131–139.
  4. Johnson L, Blanchard T, Varner D, Scrutchfield W. Factors affecting spermatogenesis in the stallion. Theriogenology 1997;48:1199–1216.
    doi: 10.1016/S0093-691X(97)00353-1pubmed: 16728209google scholar: lookup
  5. Vasconcelos A.B, Santana M.A, Santos A.M.C, Santoro M.M, Lagares M.A. Metabolic evaluation of cooled equine spermatozoa. Andrologia 2010;42:106–111.
  6. Meyers S, Bulkeley E, Foutouhi A. Sperm mitochondrial regulation in motility and fertility in horses. Reprod. Domest. Anim. 2019;54:22–28.
    doi: 10.1111/rda.13461pubmed: 31512320google scholar: lookup
  7. Brito L.F. Evaluation of Stallion Sperm Morphology. Clin. Tech. Equine Pract. 2007;6:249–264.
  8. Veeramachaneni D.R, Moeller C.L, Sawyer H.R. Sperm Morphology in Stallions: Ultrastructure as a Functional and Diagnostic Tool. Vet. Clin. N. Am. Equine Pract. 2006;22:683–692.
    doi: 10.1016/j.cveq.2006.08.001pubmed: 17129796google scholar: lookup
  9. Meyers S. Equine sperm-oocyte interaction: The role of sperm surface hyaluronidase. Anim. Reprod. Sci. 2001;68:291–303.
    doi: 10.1016/S0378-4320(01)00166-Xpubmed: 11744273google scholar: lookup
  10. Thomas A, Meyers S, Ball B. Capacitation-like changes in equine spermatozoa following cryopreservation. Theriogenology 2006;65:1531–1550.
  11. Graham J.K. Methods for Induction of Capacitation and the Acrosome Reaction of Stallion Spermatozoa. Vet. Clin. N. Am. Equine Pract. 1996;12:111–117.
    doi: 10.1016/S0749-0739(17)30298-5pubmed: 8726453google scholar: lookup
  12. Ball B.A, Vo A.T, Baumber J. Generation of reactive oxygen species by equine spermatozoa. Am. J. Vet. Res. 2001;62:508–515.
    doi: 10.2460/ajvr.2001.62.508pubmed: 11327456google scholar: lookup
  13. Moore A, Squires E, Graham J. Effect of seminal plasma on the cryopreservation of equine spermatozoa. Theriogenology 2005;63:2372–2381.
  14. Guasti P, Souza F, Scott C, Papa P, Camargo L, Schmith R, Monteiro G, Hartwig F, Papa F. Equine seminal plasma and sperm membrane: Functional proteomic assessment. Theriogenology 2020;156:70–81.
  15. Al-Essawe E.M, Wallgren M, Wulf M, Aurich C, Macías-García B, Sjunnesson Y, Morrell J.M. Seminal plasma influences the fertilizing potential of cryopreserved stallion sperm. Theriogenology 2018;115:99–107.
  16. Clermont Y. Kinetics of spermatogenesis in mammals: Seminiferous epithelium cycle and spermatogonial renewal. Physiol. Rev. 1972;52:198–236.
    doi: 10.1152/physrev.1972.52.1.198pubmed: 4621362google scholar: lookup
  17. Swierstra E.E, Pickett B.W, Gebauer M.R. Spermatogenesis and duration of transit of spermatozoa through the excurrent ducts of stallions. J. Reprod. Fertil. Suppl. 1975;23:53–57.
    pubmed: 1060837
  18. Johnson L. Spermatogenesis. 1991. pp. 173–219.
  19. Wong C, Cheng C.Y. The Blood-Testis Barrier: Its Biology, Regulation, and Physiological Role in Spermatogenesis. Curr. Top. Dev. Biol. 2005;71:263–296.
    doi: 10.1016/s0070-2153(05)71008-5pubmed: 16344108google scholar: lookup
  20. Zirkin B.R, Papadopoulos V. Leydig cells: Formation, function, and regulation†. Biol. Reprod. 2018;99:101–111.
    doi: 10.1093/biolre/ioy059pmc: PMC6044347pubmed: 29566165google scholar: lookup
  21. Huhtaniemi I, Teerds K. Leydig cells. 2018. pp. 30–38.
  22. Griswold M.D. The central role of Sertoli cells in spermatogenesis. Semin. Cell Dev. Biol. 1998;9:411–416.
    doi: 10.1006/scdb.1998.0203pubmed: 9813187google scholar: lookup
  23. Johnson L, Thompson D.L. Age-Related and Seasonal Variation in the Sertoli Cell Population, Daily Sperm Production and Serum Concentrations of Follicle-Stimulating Hormone, Luteinizing Hormone and Testosterone in Stallions. Biol. Reprod. 1983;29:777–789.
    doi: 10.1095/biolreprod29.3.777pubmed: 6414546google scholar: lookup
  24. França L.R, Hess R.A, Dufour J.M, Hofmann M.-C, Griswold M.D. The Sertoli cell: One hundred fifty years of beauty and plasticity. Andrology 2016;4:189–212.
    doi: 10.1111/andr.12165pmc: PMC5461925pubmed: 26846984google scholar: lookup
  25. Johnson L, Tatum M.E. Temporal Appearance of Seasonal Changes in Numbers of Sertoli Cells, Leydig Cells, and Germ Cells in Stallions. Biol. Reprod. 1989;40:994–999.
    doi: 10.1095/biolreprod40.5.994pubmed: 2765623google scholar: lookup
  26. Pickett B, Voss J. Management of shuttle stallions for maximum reproductive efficiency—Part 1. J. Equine Vet. Sci. 1998;18:212–227.
  27. Griswold M.D. Spermatogenesis: The Commitment to Meiosis. Physiol. Rev. 2016;96:1–17.
    doi: 10.1152/physrev.00013.2015pmc: PMC4698398pubmed: 26537427google scholar: lookup
  28. Yoshida S, Sukeno M, Nakagawa T, Ohbo K, Nagamatsu G, Suda T, Nabeshima Y.-I. The first round of mouse spermatogenesis is a distinctive program that lacks the self-renewing spermatogonia stage. Development 2006;133:1495–1505.
    doi: 10.1242/dev.02316pubmed: 16540512google scholar: lookup
  29. Evans E, Hogarth C, Mitchell D, Griswold M. Riding the spermatogenic wave: Profiling gene expression within neonatal germ and sertoli cells during a synchronized initial wave of spermatogenesis in mice. Biol. Reprod. 2014;90:108.
  30. De Rooij D.G, Russell L.D. All you wanted to know about spermatogonia but were afraid to ask. J. Androl. 2000;21:776–798.
    pubmed: 11105904
  31. De Rooij D.G, Griswold M.D. Questions About Spermatogonia Posed and Answered Since 2000. J. Androl. 2012;33:1085–1095.
    doi: 10.2164/jandrol.112.016832pubmed: 22879526google scholar: lookup
  32. Johnson L. Seasonal Differences in Equine Spermatocytogenesis. Biol. Reprod. 1991;44:284–291.
    doi: 10.1095/biolreprod44.2.284pubmed: 2009330google scholar: lookup
  33. Steger K. Transcriptional and translational regulation of gene expression in haploid spermatids. Anat. Embryol. 1999;199:471–487.
    doi: 10.1007/s004290050245pubmed: 10350128google scholar: lookup
  34. Druart X, de Graaf S. Seminal plasma proteomes and sperm fertility. Anim. Reprod. Sci. 2018;194:33–40.
  35. Pesch S, Bergmann M. Structure of mammalian spermatozoa in respect to viability, fertility and cryopreservation. Micron. 2006;37:597–612.
    doi: 10.1016/j.micron.2006.02.006pubmed: 16621580google scholar: lookup
  36. Gravance C, Champion Z, Liu I, Casey P. Sperm head morphometry analysis of ejaculate and dismount stallion semen samples. Anim. Reprod. Sci. 1997;47:149–155.
    doi: 10.1016/S0378-4320(96)01634-Xpubmed: 9233514google scholar: lookup
  37. Casey P, Gravance C, Davis R, Chabot D, Liu I. Morphometric differences in sperm head dimensions of fertile and subfertile stallions. Theriogenology 1997;47:575–582.
    doi: 10.1016/S0093-691X(97)00015-0pubmed: 16728009google scholar: lookup
  38. Bedford J. Mammalian Fertilization Misread? Sperm Penetration of the Eutherian Zona Pellucida Is Unlikely to be a Lytic Event. Biol. Reprod. 1998;59:1275–1287.
    doi: 10.1095/biolreprod59.6.1275pubmed: 9828168google scholar: lookup
  39. Foster J.A, Gerton G.L. The Acrosomal Matrix. Adv. Anat. Embryol. Cell. Biol. 2016;220:15–33.
    doi: 10.1007/978-3-319-30567-7_2pmc: PMC5112175pubmed: 27194348google scholar: lookup
  40. López M.L, De Souza W. Distribution of filipin-sterol complexes in the plasma membrane of stallion spermatozoa during the epididymal maturation process. Mol. Reprod. Dev. 1991;28:158–168.
    doi: 10.1002/mrd.1080280209pubmed: 2007029google scholar: lookup
  41. Jones R. Plasma membrane composition and organisation during maturation of spermatozoa in the epididymis. 2002. pp. 405–416.
  42. Flesch F, Gadella B.M. Dynamics of the mammalian sperm plasma membrane in the process of fertilization. Biochim. Biophys. Acta (BBA)-Rev. Biomembr. 2000;1469:197–235.
    doi: 10.1016/S0304-4157(00)00018-6pubmed: 11063883google scholar: lookup
  43. Schroter S, Osterhoff C, McArdle W, Ivell R. The glycocalyx of the sperm surface. Hum. Reprod. Updat. 1999;5:302–313.
    doi: 10.1093/humupd/5.4.302pubmed: 10465522google scholar: lookup
  44. Ma X, Pan Q, Feng Y, Choudhury B.P, Ma Q, Gagneux P, Ma F. Sialylation Facilitates the Maturation of Mammalian Sperm and Affects Its Survival in Female Uterus. Biol. Reprod. 2016;94:123.
  45. Scott T.W, Voglmayr J.K, Setchell B.P. Lipid composition and metabolism in testicular and ejaculated ram spermatozoa. Biochem. J. 1967;102:456–461.
    doi: 10.1042/bj1020456pmc: PMC1270266pubmed: 6029604google scholar: lookup
  46. Poulos A, Darin-Bennett A, White I. The phospholipid-bound fatty acids and aldehydes of mammalian spermatozoa. Comp. Biochem. Physiol. Part B Comp. Biochem. 1973;46:541–549.
    doi: 10.1016/0305-0491(73)90094-1pubmed: 4754770google scholar: lookup
  47. Aveldaño M.I, Rotstein N.P, Vermouth N.T. Lipid remodelling during epididymal maturation of rat spermatozoa. Enrichment in plasmenylcholines containing long-chain polyenoic fatty acids of the n-9 series. Biochem. J. 1992;283:235–241.
    doi: 10.1042/bj2830235pmc: PMC1131019pubmed: 1567371google scholar: lookup
  48. Rana A.P, Majumder G.C, Misra S, Ghosh A. Lipid changes of goat sperm plasma membrane during epididymal maturation. Biochim. Biophys. Acta (BBA)-Biomembr. 1991;1061:185–196.
    doi: 10.1016/0005-2736(91)90284-Fpubmed: 1998692google scholar: lookup
  49. Retamal C, Urzúa J, Lorca C, López M.L, Alves E.W. Changes in the plasma membrane proteins of stallion spermatozoa during maturation in the epididymis. J. Submicrosc. Cytol. Pathol. 2000;32:229–239.
    pubmed: 11085212
  50. López M, Olea N, Retamal C. Post-testicular changes in the density and distribution of intramembrane particles of stallion sperm surface domains. Anim. Reprod. Sci. 2007;100:204–210.
  51. Gervasi M.G, Visconti P.E. Molecular changes and signaling events occurring in spermatozoa during epididymal maturation. Andrology 2017;5:204–218.
    doi: 10.1111/andr.12320pmc: PMC5354101pubmed: 28297559google scholar: lookup
  52. Cuasnicú P.S, Cohen D.J, Ellerman D.A, Busso D, Da Ros V.G, Morgenfeld M.M. Changes in specific sperm proteins during epididymal maturation. 2002. pp. 389–403.
  53. Sullivan R, Saez F. Epididymosomes, prostasomes, and liposomes: Their roles in mammalian male reproductive physiology. Reproduction 2013;146:R21–R35.
    doi: 10.1530/REP-13-0058pubmed: 23613619google scholar: lookup
  54. Sharma U, Conine C.C, Shea J.M, Boskovic A, Derr A.G, Bing X.Y, Belleannee C, Kucukural A, Serra R.W, Sun F. Biogenesis and function of tRNA fragments during sperm maturation and fertilization in mammals. Science 2016;351:391–396.
    doi: 10.1126/science.aad6780pmc: PMC4888079pubmed: 26721685google scholar: lookup
  55. Belleannée C. Extracellular microRNAs from the epididymis as potential mediators of cell-to-cell communication. Asian J. Androl. 2015;17:730–736.
    doi: 10.4103/1008-682X.155532pmc: PMC4577581pubmed: 26178395google scholar: lookup
  56. Păunescu T.G, Shum W.W, Huynh C, Lechner L, Goetze B, Brown D, Breton S, Unescu T.G.P. High-resolution helium ion microscopy of epididymal epithelial cells and their interaction with spermatozoa. Mol. Hum. Reprod. 2014;20:929–937.
    doi: 10.1093/molehr/gau052pmc: PMC4172170pubmed: 25015675google scholar: lookup
  57. Saez F, Frenette G, Sullivan R. Epididymosomes and Prostasomes: Their Roles in Posttesticular Maturation of the Sperm Cells. J. Androl. 2003;24:149–154.
  58. Eickhoff R, Baldauf C, Koyro H.-W, Wennemuth G, Suga Y, Seitz J, Henkel R, Meinhardt A. Influence of macrophage migration inhibitory factor (MIF) on the zinc content and redox state of protein-bound sulphydryl groups in rat sperm: Indications for a new role of MIF in sperm maturation. Mol. Hum. Reprod. 2004;10:605–611.
    doi: 10.1093/molehr/gah075pubmed: 15169922google scholar: lookup
  59. Frenette G, Lessard C, Sullivan R. Polyol pathway along the bovine epididymis. Mol. Reprod. Dev. 2004;69:448–456.
    doi: 10.1002/mrd.20170pubmed: 15457514google scholar: lookup
  60. Murta D.D.M, Batista M, Silva E, Trindade A, Henrique D, Duarte A, Lopes-Da-Costa L. Notch signaling in the epididymal epithelium regulates sperm motility and is transferred at a distance within epididymosomes. Andrology 2016;4:314–327.
    doi: 10.1111/andr.12144pubmed: 26825631google scholar: lookup
  61. Krapf D, Ruan Y.C, Wertheimer E.V, Battistone M.A, Pawlak J, Sanjay A, Pilder S.H, Cuasnicu P, Breton S, Visconti P.E. cSrc is necessary for epididymal development and is incorporated into sperm during epididymal transit. Dev. Biol. 2012;369:43–53.
    doi: 10.1016/j.ydbio.2012.06.017pmc: PMC3424100pubmed: 22750823google scholar: lookup
  62. Joshi C.S, Suryawanshi A.R, Khan S.A, Balasinor N.H, Khole V.V. Liprin α3: A putative estrogen regulated acrosomal protein. Histochem. Cell Biol. 2012;139:535–548.
    doi: 10.1007/s00418-012-1044-ypubmed: 23124857google scholar: lookup
  63. Oh J, Woo J.-M, Choi E, Kim T, Cho B.-N, Park Z.Y, Kim Y.C, Kim D.H, Cho C. Molecular, biochemical, and cellular characterization of epididymal ADAMs, ADAM7 and ADAM28. Biochem. Biophys. Res. Commun. 2005;331:1374–1383.
    doi: 10.1016/j.bbrc.2005.04.067pubmed: 15883027google scholar: lookup
  64. Caballero J, Frenette G, D’Amours O, Belleannée C, Lacroix-Pepin N, Robert C, Sullivan R. Bovine sperm raft membrane associated Glioma Pathogenesis-Related 1-like protein 1 (GliPr1L1) is modified during the epididymal transit and is potentially involved in sperm binding to the zona pellucida. J. Cell. Physiol. 2012;227:3876–3886.
    doi: 10.1002/jcp.24099pubmed: 22552861google scholar: lookup
  65. Gibbs G.M, Lo J.C.Y, Nixon B, Jamsai D, O’Connor A.E, Rijal S, Sanchez-Partida L.G, Hearn M.T.W, Bianco D.M, O’Bryan M.K. Glioma Pathogenesis-Related 1-Like 1 Is Testis Enriched, Dynamically Modified, and Redistributed during Male Germ Cell Maturation and Has a Potential Role in Sperm-Oocyte Binding. Endocrinology 2010;151:2331–2342.
    doi: 10.1210/en.2009-1255pubmed: 20219979google scholar: lookup
  66. Frenette G, Sullivan R. Prostasome-like particles are involved in the transfer of P25b from the bovine epididymal fluid to the sperm surface. Mol. Reprod. Dev. 2001;59:115–121.
    doi: 10.1002/mrd.1013pubmed: 11335953google scholar: lookup
  67. Dias A.J, Maia M.S, A Retamal C, López M.L. Identification and partial characterization of α-1,4-glucosidase activity in equine epididymal fluid. Theriogenology 2004;61:1545–1558.
  68. Tecle E, Gagneux P. Sugar-coated sperm: Unraveling the functions of the mammalian sperm glycocalyx. Mol. Reprod. Dev. 2015;82:635–650.
    doi: 10.1002/mrd.22500pmc: PMC4744710pubmed: 26061344google scholar: lookup
  69. Ishijima S.A, Okuno M, Mohri H. Zeta potential of human X- and Y-bearing sperm. Int. J. Androl. 1991;14:340–347.
  70. Esfahani M.H.N, Deemeh M.R, Tavalaee M, Sekhavati M.H, Gourabi H. Zeta Sperm Selection Improves Pregnancy Rate and Alters Sex Ratio in Male Factor Infertility Patients: A Double-Blind, Randomized Clinical Trial. Int. J. Fertil. Steril. 2016;10:253–260.
    doi: 10.22074/IJFS.2016.4917pmc: PMC4948079pubmed: 27441060google scholar: lookup
  71. Chan P.J, Jacobson J.D, Corselli J.U, Patton W.C. A simple zeta method for sperm selection based on membrane charge. Fertil. Steril. 2006;85:481–486.
  72. Ohshima H, Kondo T. Electrophoresis of large colloidal particles with surface charge layers. Position of the slipping plane and surface layer thickness. Colloid Polym. Sci. 1986;264:1080–1084.
    doi: 10.1007/BF01410326google scholar: lookup
  73. Clogston J.D, Patri A.K. Zeta potential measurement. 2011. pp. 63–70.
  74. Veres I. Negative electrical charge of the surface of bull sperm. Mikroskopie 1968;23:166–169.
    pubmed: 5753481
  75. Yanagimachi R, Noda Y.D, Fujimoto M, Nicolson G.L. The distribution of negative surface charges on mammalian spermatozoa. Am. J. Anat. 1972;135:497–519.
    doi: 10.1002/aja.1001350405pubmed: 4674031google scholar: lookup
  76. Schröter S, Derr P, Conradt H.S, Nimtz M, Hale G, Kirchhoff C. Male-specific Modification of Human CD52. J. Biol. Chem. 1999;274:29862–29873.
    doi: 10.1074/jbc.274.42.29862pubmed: 10514467google scholar: lookup
  77. Calzada L, Salazar E.L, Pedrón N. Presence and Chemical Composition of Glycoproteic Layer on Human Spermatozoa. Arch. Androl. 1994;33:87–92.
    doi: 10.3109/01485019408987808pubmed: 7818376google scholar: lookup
  78. Simon L, Ge S.-Q, Carrell D.T. Sperm Selection Based on Electrostatic Charge. Methods Mol. Biol. 2012;927:269–278.
    doi: 10.1007/978-1-62703-038-0_25pubmed: 22992922google scholar: lookup
  79. Zeng Y, Clark E.N, Florman H.M. Sperm Membrane Potential: Hyperpolarization during Capacitation Regulates Zona Pellucida-Dependent Acrosomal Secretion. Dev. Biol. 1995;171:554–563.
    doi: 10.1006/dbio.1995.1304pubmed: 7556936google scholar: lookup
  80. Love C.C, Varner D.D, Thompson J.A. Intra- and inter-stallion variation in sperm morphology and their relationship with fertility. J. Reprod. Fertil. Suppl. 2000;56:93–100.
    pubmed: 20681120
  81. Varner D.D, Johnson L. From a sperm’s eye view—Revisiting our perception of this intriguing cell. 2007; Proceedings of the 53rd Annual Convention of the American Association of Equine Practitioners; Orlando, FL, USA. 1–5 December 2007; pp. 104–177.
  82. Ramalho-Santos J, Amaral S. Mitochondria and mammalian reproduction. Mol. Cell. Endocrinol. 2013;379:74–84.
    doi: 10.1016/j.mce.2013.06.005pubmed: 23769709google scholar: lookup
  83. Sousa A.P, Amaral A, Baptista M, Tavares R, Campo P.C, Peregrín P.C, Freitas A, Paiva A, Almeida-Santos T, Ramalho-Santos J. Not All Sperm Are Equal: Functional Mitochondria Characterize a Subpopulation of Human Sperm with Better Fertilization Potential. PLoS ONE 2011;6:e18112.
  84. Gallon F, Marchetti C, Jouy N, Marchetti P. The functionality of mitochondria differentiates human spermatozoa with high and low fertilizing capability. Fertil. Steril. 2006;86:1526–1530.
  85. Marchetti P, Ballot C, Jouy N, Thomas P, Marchetti C. Influence of mitochondrial membrane potential of spermatozoa on in vitro fertilisation outcome. Andrologia 2011;44:136–141.
  86. Mannella C.A. Structure and dynamics of the mitochondrial inner membrane cristae. Biochim. Biophys. Acta BBA Mol. Cell Res. 2006;1763:542–548.
    doi: 10.1016/j.bbamcr.2006.04.006pubmed: 16730811google scholar: lookup
  87. Gibb Z, Lambourne S.R, Aitken R.J. The Paradoxical Relationship Between Stallion Fertility and Oxidative Stress. Biol. Reprod. 2014;91:77.
    doi: 10.1095/biolreprod.114.118539pubmed: 25078685google scholar: lookup
  88. Saraste M. Oxidative Phosphorylation at the fin de siècle. Science 1999;283:1488–1493.
    doi: 10.1126/science.283.5407.1488pubmed: 10066163google scholar: lookup
  89. Moraes C.R, Meyers S. The sperm mitochondrion: Organelle of many functions. Anim. Reprod. Sci. 2018;194:71–80.
  90. Wolken G.G, Arriaga E.A. Simultaneous Measurement of Individual Mitochondrial Membrane Potential and Electrophoretic Mobility by Capillary Electrophoresis. Anal. Chem. 2014;86:4217–4226.
    doi: 10.1021/ac403849xpmc: PMC4018156pubmed: 24673334google scholar: lookup
  91. Darr C.R, Varner D.D, Teague S, Cortopassi G.A, Datta S, Meyers S.A. Lactate and Pyruvate Are Major Sources of Energy for Stallion Sperm with Dose Effects on Mitochondrial Function, Motility, and ROS Production. Biol. Reprod. 2016;95:34.
    doi: 10.1095/biolreprod.116.140707pubmed: 27335066google scholar: lookup
  92. Davila M.P, Muñoz P.M, Tapia J.A, Ortega-Ferrusola C, Balao da Silva C.C, Peña F.J. 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:e0138777.
  93. Darr C.R, Cortopassi G.A, Datta S, Varner D.D, Meyers S.A. Mitochondrial oxygen consumption is a unique indicator of stallion spermatozoal health and varies with cryopreservation media. Theriogenology 2016;86:1382–1392.
  94. Nijs M, Vanderzwalmen P, Vandamme B, Segal-Bertin G, Lejeune B, Segal L, van Roosendaal E, Schoysman R. Andrology: Fertilizing ability of immotile spermatozoa after intracytoplasmic sperm injection. Hum. Reprod. 1996;11:2180–2185.
  95. Gaddum-Rosse P. Some observations on sperm transport through the uterotubal junction of the rat. Am. J. Anat. 1981;160:333–341.
    doi: 10.1002/aja.1001600309pubmed: 6894349google scholar: lookup
  96. Fraser L.R, Quinn P.J. A glycolytic product is obligatory for initiation of the sperm acrosome reaction and whiplash motility required for fertilization in the mouse. Reproduction 1981;61:25–35.
    doi: 10.1530/jrf.0.0610025pubmed: 7452624google scholar: lookup
  97. Turner R.M. Tales from the tail: What do we really know about sperm motility?. J. Androl. 2003;24:790–803.
  98. Amann R.P, Waberski D. Computer-assisted sperm analysis (CASA): Capabilities and potential developments. Theriogenology 2014;81:5–17.e3.
  99. Jasko D.J, Little T.V, Lein D.H, Foote R.H. Comparison of spermatozoal movement and semen characteristics with fertility in stallions: 64 cases (1987–1988). J. Am. Vet. Med. Assoc. 1992;200:979–985.
    pubmed: 1577655
  100. Hurtgen J.P. Evaluation of the Stallion for Breeding Soundness. Vet. Clin. N. Am. Equine Pract. 1992;8:149–165.
    doi: 10.1016/S0749-0739(17)30472-8pubmed: 1576547google scholar: lookup
  101. Voss J.L, Pickett B.W, Squires E.L. Stallion spermatozoal morphology and motility and their relationships to fertility. J. Am. Vet. Med. Assoc. 1981;178:287–289.
    pubmed: 7228787
  102. Johnson S, Nguyen V, Coder D. Assessment of Cell Viability. Curr. Protoc. Cytom. 2013;64:9.2.1–9.2.26.
    doi: 10.1002/0471142956.cy0902s64pubmed: 23546778google scholar: lookup
  103. Garner D.L, Johnson L.A. Viability Assessment of Mammalian Sperm Using SYBR-14 and Propidium Iodide. Biol. Reprod. 1995;53:276–284.
    doi: 10.1095/biolreprod53.2.276pubmed: 7492679google scholar: lookup
  104. Pintado B, de la Fuente J, Roldan E.R. Permeability of boar and bull spermatozoa to the nucleic acid stains propidium iodide or Hoechst 33258, or to eosin: Accuracy in the assessment of cell viability. J. Reprod. Fertil. 2000;118:145–152.
    doi: 10.1530/jrf.0.1180145pubmed: 10793636google scholar: lookup
  105. Glazar A.I. Assessment of Sperm Plasma Membrane Integrity and Viability: Propidium Iodide/SYBR-14. Equine Reprod. Proced. 2014:476–477.
  106. Baumber J, Ball B.A, Gravance C.G, Medina V, Davies-Morel M.C.G. The effect of reactive oxygen species on equine sperm motility, viability, acrosomal integrity, mitochondrial membrane potential, and membrane lipid peroxidation. J. Androl. 2000;21:895–902.
    pubmed: 11105916
  107. Gravance C, Garner D, Baumber J, Ball B. Assessment of equine sperm mitochondrial function using JC-1. Theriogenology 2000;53:1691–1703.
    doi: 10.1016/S0093-691X(00)00308-3pubmed: 10968415google scholar: lookup
  108. O’Connell M, McClure N, Lewis S.E.M. The effects of cryopreservation on sperm morphology, motility and mitochondrial function. Hum. Reprod. 2002;17:704–709.
    doi: 10.1093/humrep/17.3.704pubmed: 11870124google scholar: lookup
  109. Glazar A.I, McCue P.M. Assessment of Sperm Mitochondrial Function. Equine Reprod. Proced. 2021:637–638.
  110. Baumber J. Changes in Membrane Lipid Order with Capacitation in Rhesus Macaque (Macaca mulatta) Spermatozoa. J. Androl. 2006;27:578–587.
    doi: 10.2164/jandrol.05135pubmed: 16582419google scholar: lookup
  111. Brum A, Sabeur K, Ball B. Apoptotic-like changes in equine spermatozoa separated by density-gradient centrifugation or after cryopreservation. Theriogenology 2008;69:1041–1055.
  112. Cheng F.-P, Gadella B.M, Voorhout W.F, Fazeli A, Bevers M.M, Colenbrander B. Progesterone-Induced Acrosome Reaction in Stallion Spermatozoa Is Mediated by a Plasma Membrane Progesterone Receptor. Biol. Reprod. 1998;59:733–742.
    doi: 10.1095/biolreprod59.4.733pubmed: 9746720google scholar: lookup
  113. Cheng F.P, Fazeli A, Voorhout W.F, Marks A, Bevers M.M, Colenbrander B. Use of peanut agglutinin to assess the acrosomal status and the zona pellucida-induced acrosome reaction in stallion spermatozoa. J. Androl. 1996;17:674–682.
    pubmed: 9016398
  114. Franken D.R. How accurate is sperm morphology as an indicator of sperm function?. Andrologia 2014;47:720–723.
    doi: 10.1111/and.12324pubmed: 25130990google scholar: lookup
  115. Dariš B, Goropevšek A, Hojnik N, Vlaisavljević V. Sperm morphological abnormalities as indicators of DNA fragmentation and fertilization in ICSI. Arch. Gynecol. Obstet. 2009;281:363–367.
    doi: 10.1007/s00404-009-1140-ypubmed: 19504115google scholar: lookup
  116. Oumaima A, Tesnim A, Zohra H, Amira S, Ines Z, Sana C, Intissar G, Lobna E, Ali J, Meriem M. Investigation on the origin of sperm morphological defects: Oxidative attacks, chromatin immaturity, and DNA fragmentation. Environ. Sci. Pollut. Res. 2018;25:13775–13786.
    doi: 10.1007/s11356-018-1417-4pubmed: 29508198google scholar: lookup
  117. Kruger T.F, Acosta A.A, Simmons K.F, Swanson R.J, Matta J.F, Oehninger S. Predictive value of abnormal sperm morphology in in vitro fertilization. Fertil. Steril. 1988;49:112–117.
    doi: 10.1016/S0015-0282(16)59660-5pubmed: 3335257google scholar: lookup
  118. Oehninger S, Mahony M, Özgür K, Kolm P, Kruger T, Franken D. Clinical significance of human sperm-zona pellucida binding. Fertil. Steril. 1997;67:1121–1127.
    doi: 10.1016/S0015-0282(97)81449-5pubmed: 9176454google scholar: lookup
  119. Love C. Relationship between sperm motility, morphology and the fertility of stallions. Theriogenology 2011;76:547–557.
  120. Hirohashi N, Yanagimachi R. Sperm acrosome reaction: Its site and role in fertilization†. Biol. Reprod. 2018;99:127–133.
    doi: 10.1093/biolre/ioy045pubmed: 29462288google scholar: lookup
  121. Yanagimachi R, Hamana K, Hafez E.S.E. The movement of golden hamster spermatozoa before and after capacitation. Reproduction 1970;23:193–196.
    doi: 10.1530/jrf.0.0230193pubmed: 5472441google scholar: lookup
  122. Leemans B, Stout T.A.E, De Schauwer C, Heras S, Nelis H, Hoogewijs M, Van Soom A, Gadella B.M. Update on mammalian sperm capacitation: How much does the horse differ from other species?. Reproduction 2019;157:R181–R197.
    doi: 10.1530/REP-18-0541pubmed: 30721132google scholar: lookup
  123. Cheng F.P, Fazeli A, Voorhout W.F, Tremoleda J.L, Bevers M.M, Colenbrander B. Progesterone in mare follicular fluid induces the acrosome reaction in stallion spermatozoa and enhances In Vitro binding to the zona pellucida. Int. J. Androl. 2002;21:57–66.
  124. McPartlin L, Littell J, Mark E, Nelson J, Travis A, Bedford-Guaus S. A defined medium supports changes consistent with capacitation in stallion sperm, as evidenced by increases in protein tyrosine phosphorylation and high rates of acrosomal exocytosis. Theriogenology 2008;69:639–650.
  125. Meyers S.A, Overstreet J.W, Liu I.K, Drobnis E.Z. Capacitation in vitro of stallion spermatozoa: Comparison of progesterone-induced acrosome reactions in fertile and subfertile males. J. Androl. 1995;16:47–54.
    pubmed: 7768752
  126. Mortimer D, Camenzind A. The role of follicular fluid in inducing the acrosome reaction of human spermatozoa incubated in vitro. Hum. Reprod. 1989;4:169–174.
  127. Sun T.T, Chung C.M, Chan H.C. Acrosome reaction in the cumulus oophorus revisited: Involvement of a novel sperm-released factor NYD-SP8. Protein Cell 2011;2:92–98.
    doi: 10.1007/s13238-011-1022-5pmc: PMC4875259pubmed: 21380641google scholar: lookup
  128. Siiteri J.E, Dandekar P, Meizel S. Human sperm acrosome reaction-initiating activity associated with the human cumulus oophorus and mural granulosa cells. J. Exp. Zool. 1988;246:71–80.
    doi: 10.1002/jez.1402460110pubmed: 3385373google scholar: lookup
  129. Leemans B, Gadella B.M, Stout T.A.E, De Schauwer C, Nelis H, Hoogewijs M, Van Soom A. Why doesn’t conventional IVF work in horses. Reproduction 2016;152:R233–R245.
    doi: 10.1530/REP-16-0420pubmed: 27651517google scholar: lookup
  130. Brucker C. The human sperm acrosome reaction: Physiology and regulatory mechanisms. An update. Hum. Reprod. Updat. 1995;1:51–62.
    doi: 10.1093/humupd/1.1.51pubmed: 9080206google scholar: lookup
  131. Esteves S.C. Relationship of in Vitro Acrosome Reaction to Sperm Function: An Update. Open Reprod. Sci. J. 2011;3:72–84.
  132. Avella M.A, Dean J. Fertilization with acrosome-reacted mouse sperm: Implications for the site of exocytosis. Proc. Natl. Acad. Sci. USA 2011;108:19843–19844.
    doi: 10.1073/pnas.1118234109pmc: PMC3250142pubmed: 22143800google scholar: lookup
  133. Gahlay G.K, Rajput N. The enigmatic sperm proteins in mammalian fertilization: An overview†. Biol. Reprod. 2020;103:1171–1185.
    doi: 10.1093/biolre/ioaa140pubmed: 32761117google scholar: lookup
  134. Katz D.F, Yanagimachi R, Dresdner R.D. Movement characteristics and power output of guinea-pig and hamster spermatozoa in relation to activation. Reproduction 1978;52:167–172.
    doi: 10.1530/jrf.0.0520167pubmed: 621693google scholar: lookup
  135. Fraser L.R. Sperm capacitation and the acrosome reaction. Hum. Reprod. 1998;13:9–19.
    doi: 10.1093/humrep/13.suppl_1.9pubmed: 9663766google scholar: lookup
  136. Cummins J.M, Yanagimachi R. Development of ability to penetrate the cumulus oophorus by hamster spermatozoa capacitated in vitro, in relation to the timing of the acrosome reaction. Gamete Res. 1986;15:187–212.
    doi: 10.1002/mrd.1120150302google scholar: lookup
  137. Florman H.M, Jungnickel M.K, Sutton K.A. Regulating the acrosome reaction. Int. J. Dev. Biol. 2008;52:503–510.
    doi: 10.1387/ijdb.082696hfpubmed: 18649263google scholar: lookup
  138. Tesarik J, Mendoza C. Alleviation of acrosome reaction prematurity by sperm treatment with egg yolk. Fertil. Steril. 1995;63:153–157.
    doi: 10.1016/S0015-0282(16)57311-7pubmed: 7805906google scholar: lookup
  139. Meyers S.A, Liu I.K, Overstreet J.W, Vadas S, Drobnis E.Z. Zona pellucida binding and zona-induced acrosome reactions in horse spermatozoa: Comparisons between fertile and subfertile stallions. Theriogenology 1996;46:1277–1288.
    doi: 10.1016/S0093-691X(96)00299-3pubmed: 16727991google scholar: lookup
  140. Peña F, Martínez H.R, Tapia J, Ferrusola C.O, Fernández L.G, García B.M. Mitochondria in Mammalian Sperm Physiology and Pathology: A Review. Reprod. Domest. Anim. 2009;44:345–349.
  141. Ball B.A. Oxidative stress, osmotic stress and apoptosis: Impacts on sperm function and preservation in the horse. Anim. Reprod. Sci. 2008;107:257–267.
  142. Aitken R, Koppers A.J. Apoptosis and DNA damage in human spermatozoa. Asian J. Androl. 2011;13:36–42.
    doi: 10.1038/aja.2010.68pmc: PMC3739394pubmed: 20802502google scholar: lookup
  143. Sabeur K, Ball B.A. Detection of superoxide anion generation by equine spermatozoa. Am. J. Vet. Res. 2006;67:701–706.
    doi: 10.2460/ajvr.67.4.701pubmed: 16579765google scholar: lookup
  144. Shamsi M.B, Imam S.N, Dada R. Sperm DNA integrity assays: Diagnostic and prognostic challenges and implications in management of infertility. J. Assist. Reprod. Genet. 2011;28:1073–1085.
    doi: 10.1007/s10815-011-9631-8pmc: PMC3224170pubmed: 21904910google scholar: lookup
  145. Esteves S.C, Sharma R.K, Gosálvez J, Agarwal A. A translational medicine appraisal of specialized andrology testing in unexplained male infertility. Int. Urol. Nephrol. 2014;46:1037–1052.
    doi: 10.1007/s11255-014-0715-0pubmed: 24771472google scholar: lookup
  146. Shamsi M.B, Kumar R, Dada R. Evaluation of nuclear DNA damage in human spermatozoa in men opting for assisted reproduction. Indian J. Med. Res. 2008;127:115–123.
    pubmed: 18403788
  147. Sakkas D, Moffatt O, Manicardi G.C, Mariethoz E, Tarozzi N, Bizzaro D. Nature of DNA Damage in Ejaculated Human Spermatozoa and the Possible Involvement of Apoptosis. Biol. Reprod. 2002;66:1061–1067.
    doi: 10.1095/biolreprod66.4.1061pubmed: 11906926google scholar: lookup
  148. Henkel R, Kierspel E, Stalf T, Mehnert C, Menkveld R, Tinneberg H.-R, Schill W.-B, Kruger T.F. Effect of reactive oxygen species produced by spermatozoa and leukocytes on sperm functions in non-leukocytospermic patients. Fertil. Steril. 2005;83:635–642.
  149. Seli E, Gardner D, Schoolcraft W.B, Moffatt O, Sakkas D. Extent of nuclear DNA damage in ejaculated spermatozoa impacts on blastocyst development after in vitro fertilization. Fertil. Steril. 2004;82:378–383.
  150. Baker M.A, Aitken R.J. Reactive oxygen species in spermatozoa: Methods for monitoring and significance for the origins of genetic disease and infertility. Reprod. Biol. Endocrinol. 2005;3:67–69.
    doi: 10.1186/1477-7827-3-67pmc: PMC1315356pubmed: 16313680google scholar: lookup
  151. Cooke M.S, Evans M.D, Dizdaroglu M, Lunec J. Oxidative DNA damage: Mechanisms, mutation, and disease. FASEB J. 2003;17:1195–1214.
    doi: 10.1096/fj.02-0752revpubmed: 12832285google scholar: lookup
  152. Goriely A, McVean G.A.T, Röjmyr M, Ingemarsson B, Wilkie A.O.M. Evidence for Selective Advantage of Pathogenic FGFR2 Mutations in the Male Germ Line. Science 2003;301:643–646.
    doi: 10.1126/science.1085710pubmed: 12893942google scholar: lookup
  153. Tiemann-Boege I, Navidi W, Grewal R, Cohn D, Eskenazi B, Wyrobek A, Arnheim N. The observed human sperm mutation frequency cannot explain the achondroplasia paternal age effect. Proc. Natl. Acad. Sci. USA 2002;99:14952–14957.
    doi: 10.1073/pnas.232568699pmc: PMC137526pubmed: 12397172google scholar: lookup
  154. Giuliani V, Pandolfi C, Santucci R, Pelliccione F, Macerola B, Focarelli R, Rosati F, Della Giovampaola C, Francavilla F. Expression of gp20, a human sperm antigen of epididymal origin, is reduced in spermatozoa from subfertile men. Mol. Reprod. Dev. 2004;69:235–240.
    doi: 10.1002/mrd.20166pubmed: 15293226google scholar: lookup
  155. Ionov M, Gontarek W, Bryszewska M. Zeta potential technique for analyzing semen quality. MethodsX 2020;7:100895.
    doi: 10.1016/j.mex.2020.100895pmc: PMC7182756pubmed: 32346529google scholar: lookup
  156. Kaneko S, Oshio S, Kobayashi T, Iizuka R, Mohri H. Human X- and Y-bearing sperm differ in cell surface sialic acid content. Biochem. Biophys. Res. Commun. 1984;124:950–955.
    doi: 10.1016/0006-291X(84)91050-7pubmed: 6542364google scholar: lookup
  157. Focarelli R, Rosati F, Terrana B. Sialylglycoconjugates Release During In Vitro Capacitation of Human Spermatozoa. J. Androl. 1990;11:97–104.
  158. Levinsky H, Singer R, Malik Z, Sagiv M, Cohen A.M, Servadio C, Allalouf D. Distribution of Sialic Acid in Human Sperm Membranes. Arch. Androl. 1983;10:209–212.
    doi: 10.3109/01485018308987566pubmed: 6882086google scholar: lookup
  159. Velásquez J.G, Canovas S, Barajas P, Marcos J, Jimenez-Movilla M, Gallego R.G, Ballesta J, Avilés M, Coy P. Role of sialic acid in bovine sperm-zona pellucida binding. Mol. Repeod. Dev. 2006;74:617–628.
    doi: 10.1002/mrd.20619pubmed: 17044044google scholar: lookup