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Fuel/Energy Sources of Spermatozoa

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Male Infertility

Abstract

Spermatozoa consume energy in the form of intracellular adenosine triphosphate (ATP) generated by its fuel machinery. Energy is required to facilitate sperm functions, from sperm motility and hyperactivation to capacitation and acrosome reaction, all of which are crucial for the success of fertilization. Glycolysis and oxidative phosphorylation are the two metabolic pathways known to generate energy in spermatozoa. However, the cellular mechanism and signaling pathways that spermatozoa predominantly utilize to generate the energy it requires to achieve successful fertilization are not fully elucidated. Oxidative phosphorylation occurs in the mitochondria and is a more efficient pathway for ATP production compared to glycolysis. Mitochondrial respiration is reported to be the primary source of energy for sperm motility, yet the diffusion potential of ATP from the mitochondria downwards of the entire flagellar length is inadequate to support sperm motility. On the other hand, glycolysis, which takes place in the sperm head and tail, is the main source of ATP along the flagellum. Although inhibition of the glycolysis process does not appear to disrupt sperm function and motility, it is uncertain whether such motility is sustainable over an extended time period or if it is vigorous enough for fertilization to occur effectively. This chapter provides an overview of sperm energy metabolism, which is supported by the unique anatomical and physiological characteristics in spermatozoa as well as the coordination between the Sertoli cells and spermatogonial cells during energy production in spermatozoa. Energy utilization during each sperm process and the consequence of fuel depletion on sperm function are also described. Understanding the intricacies of sperm energy metabolism would help improve the in vitro sperm storage media and contribute toward the development of non-hormonal contraceptives.

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References

  1. du Plessis SS, et al. Oxidative phosphorylation versus glycolysis: what fuel do spermatozoa use? Asian J Androl. 2015;17(2):230–5.

    Article  CAS  PubMed  Google Scholar 

  2. Berg JM, et al. Biochemistry. 8th ed. New York: W. H. Freeman and Company; 2015.

    Google Scholar 

  3. Erecinska M, Wilson DF. On the mechanism of regulation of cellular respiration. The dependence of respiration on the cytosolic [ATP], [ADP] and [PI]. Adv Exp Med Biol. 1977;94:271–8.

    Article  CAS  PubMed  Google Scholar 

  4. Kim YH, et al. Compartmentalization of a unique ADP/ATP carrier protein SFEC (sperm flagellar energy carrier, AAC4) with glycolytic enzymes in the fibrous sheath of the human sperm flagellar principal piece. Dev Biol. 2007;302(2):463–76.

    Article  CAS  PubMed  Google Scholar 

  5. Piomboni P, et al. The role of mitochondria in energy production for human sperm motility. Int J Androl. 2012;35(2):109–24.

    Article  CAS  PubMed  Google Scholar 

  6. Gnaiger E. Bioenergetics at low oxygen: dependence of respiration and phosphorylation on oxygen and adenosine diphosphate supply. Respir Physiol. 2001;128(3):277–97.

    Article  CAS  PubMed  Google Scholar 

  7. Mishro MM, Ramya T. Fuel/energy sources of spermatozoa. In: Parekattil SJ, Agarwal A, editors. Male infertility: contemporary clinical approaches, andrology, art & antioxidants. New York: Springer-Verlag; 2012. p. 209–23.

    Chapter  Google Scholar 

  8. Rees JM, Ford WC, Hull MG. Effect of caffeine and of pentoxifylline on the motility and metabolism of human spermatozoa. J Reprod Fertil. 1990;90(1):147–56.

    Article  CAS  PubMed  Google Scholar 

  9. Inaba K. Sperm flagella: comparative and phylogenetic perspectives of protein components. Mol Hum Reprod. 2011;17(8):524–38.

    Article  CAS  PubMed  Google Scholar 

  10. Mukai C, Travis AJ. What sperm can teach us about energy production. Reprod Domest Anim. 2012;47(Suppl 4):164–9.

    Article  PubMed  PubMed Central  Google Scholar 

  11. Turner RM. Tales from the tail: what do we really know about sperm motility? J Androl. 2003;24(6):790–803.

    Article  PubMed  Google Scholar 

  12. Rajender S, Rahul P, Mahdi AA. Mitochondria, spermatogenesis and male infertility. Mitochondrion. 2010;10(5):419–28.

    Article  CAS  PubMed  Google Scholar 

  13. Ramalho-Santos J, et al. Mitochondrial functionality in reproduction: from gonads and gametes to embryos and embryonic stem cells. Hum Reprod Update. 2009;15(5):553–72.

    Article  CAS  PubMed  Google Scholar 

  14. Ferramosca A, et al. Mitochondrial respiratory efficiency is positively correlated with human sperm motility. Urology. 2012;79(4):809–14.

    Article  PubMed  Google Scholar 

  15. Calvin HI. Comparative labelling of rat epididymal spermatozoa by intratesticularly administered 65ZnCl2 and [35S]cysteine. J Reprod Fertil. 1981;61(1):65–73.

    Article  CAS  PubMed  Google Scholar 

  16. Ho HC, Suarez SS. Characterization of the intracellular calcium store at the base of the sperm flagellum that regulates hyperactivated motility. Biol Reprod. 2003;68(5):1590–6.

    Article  CAS  PubMed  Google Scholar 

  17. Storey BT. Mammalian sperm metabolism: oxygen and sugar, friend and foe. Int J Dev Biol. 2008;52(5–6):427–37.

    Article  CAS  PubMed  Google Scholar 

  18. Fouquet JP, et al. Differential distribution of glutamylated tubulin during spermatogenesis in mammalian testis. Cell Motil Cytoskeleton. 1994;27(1):49–58.

    Article  CAS  PubMed  Google Scholar 

  19. Zhao Y, Buhr MM. Localization of various ATPases in fresh and cryopreserved bovine spermatozoa. Anim Reprod Sci. 1996;44(3):139–48.

    Article  CAS  Google Scholar 

  20. Jorgensen PL, Hakansson KO, Karlish SJ. Structure and mechanism of Na,K-ATPase: functional sites and their interactions. Annu Rev Physiol. 2003;65:817–49.

    Article  CAS  PubMed  Google Scholar 

  21. Sanchez G, et al. The Na,K-ATPase alpha4 isoform from humans has distinct enzymatic properties and is important for sperm motility. Mol Hum Reprod. 2006;12(9):565–76.

    Article  CAS  PubMed  Google Scholar 

  22. Jimenez T, et al. Na,K-ATPase alpha4 isoform is essential for sperm fertility. Proc Natl Acad Sci U S A. 2011;108(2):644–9.

    Article  PubMed  Google Scholar 

  23. Da Costa R, et al. Cadmium inhibits motility, activities of plasma membrane Ca(2+)-ATPase and axonemal dynein-ATPase of human spermatozoa. Andrologia. 2016;48(4):464–9.

    Article  CAS  PubMed  Google Scholar 

  24. Schuh K, et al. Plasma membrane Ca2+ ATPase 4 is required for sperm motility and male fertility. J Biol Chem. 2004;279(27):28220–6.

    Article  CAS  PubMed  Google Scholar 

  25. Williams KM, Ford WC. Effects of Ca-ATPase inhibitors on the intracellular calcium activity and motility of human spermatozoa. Int J Androl. 2003;26(6):366–75.

    Article  CAS  PubMed  Google Scholar 

  26. Freitas MJ, et al. TCTEX1D4 interactome in human testis: unraveling the function of dynein light chain in spermatozoa. OMICS. 2014;18(4):242–53.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Lestari SW, et al. Sperm Na(+), K(+)-ATPase alpha4 and plasma membrane Ca(2+)-ATPase (PMCA) 4 regulation in asthenozoospermia. Syst Biol Reprod Med. 2017;63(5):294–302.

    Article  CAS  PubMed  Google Scholar 

  28. Storey BT, Kayne FJ. Properties of pyruvate kinase and flagellar ATPase in rabbit spermatozoa: relation to metabolic strategy of the sperm cell. J Exp Zool. 1980;211(3):361–7.

    Article  CAS  PubMed  Google Scholar 

  29. Halangk W, Troger U, Bohnensack R. Quantification of aerobic energy turnover in epididymal bull spermatozoa. Biochim Biophys Acta. 1990;1015(2):243–7.

    Article  CAS  PubMed  Google Scholar 

  30. Krisfalusi M, et al. Multiple glycolytic enzymes are tightly bound to the fibrous sheath of mouse spermatozoa. Biol Reprod. 2006;75(2):270–8.

    Article  CAS  PubMed  Google Scholar 

  31. Millan JL, et al. Epitopes of human testis-specific lactate dehydrogenase deduced from a cDNA sequence. Proc Natl Acad Sci U S A. 1987;84(15):5311–5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. McCarrey JR, Thomas K. Human testis-specific PGK gene lacks introns and possesses characteristics of a processed gene. Nature. 1987;326(6112):501–5.

    Article  CAS  PubMed  Google Scholar 

  33. Welch JE, et al. Human glyceraldehyde 3-phosphate dehydrogenase-2 gene is expressed specifically in spermatogenic cells. J Androl. 2000;21(2):328–38.

    CAS  PubMed  Google Scholar 

  34. Kuravsky ML, et al. Testis-specific glyceraldehyde-3-phosphate dehydrogenase: origin and evolution. BMC Evol Biol. 2011;11:160.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Muronetz VI, et al. Sperm-specific Glyceraldehyde-3-phosphate dehydrogenase – an evolutionary Acquisition of Mammals. Biochemistry (Mosc). 2015;80(13):1672–89.

    Article  CAS  Google Scholar 

  36. Edwards YH, Grootegoed JA. A sperm-specific enolase. J Reprod Fertil. 1983;68(2):305–10.

    Article  CAS  PubMed  Google Scholar 

  37. Gillis BA, Tamblyn TM. Association of bovine sperm aldolase with sperm subcellular components. Biol Reprod. 1984;31(1):25–35.

    Article  CAS  PubMed  Google Scholar 

  38. Mori C, et al. Mouse spermatogenic cell-specific type 1 hexokinase (mHk1-s) transcripts are expressed by alternative splicing from the mHk1 gene and the HK1-S protein is localized mainly in the sperm tail. Mol Reprod Dev. 1998;49(4):374–85.

    Article  CAS  PubMed  Google Scholar 

  39. Miki K, et al. Glyceraldehyde 3-phosphate dehydrogenase-S, a sperm-specific glycolytic enzyme, is required for sperm motility and male fertility. Proc Natl Acad Sci U S A. 2004;101(47):16501–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Kobayashi T, et al. Localization and physiological implication of aldose reductase and sorbitol dehydrogenase in reproductive tracts and spermatozoa of male rats. J Androl. 2002;23(5):674–83.

    CAS  PubMed  Google Scholar 

  41. King TE, Mann T. Sorbitol metabolism in spermatozoa. Proc R Soc Lond B Biol Sci. 1959;151:226–43.

    Article  Google Scholar 

  42. Frenette G, Thabet M, Sullivan R. Polyol pathway in human epididymis and semen. J Androl. 2006;27(2):233–9.

    Article  CAS  PubMed  Google Scholar 

  43. Mann T. Studies on the metabolism of semen: 3. Fructose as a normal constituent of seminal plasma. Site of formation and function of fructose in semen. Biochem J. 1946;40:481–91.

    CAS  PubMed  PubMed Central  Google Scholar 

  44. Peterson RN, Freund M. Metabolism of human spermatozoa. In: Hafez ESE, editor. Human semen and fertility regulation in men. St Louis: Mosby; 1975. p. 176–86.

    Google Scholar 

  45. Westhoff D, Kamp G. Glyceraldehyde 3-phosphate dehydrogenase is bound to the fibrous sheath of mammalian spermatozoa. J Cell Sci. 1997;110(Pt 15):1821–9.

    CAS  PubMed  Google Scholar 

  46. Goldberg E, et al. Cytochrome c: immunofluorescent localization of the testis-specific form. Science. 1977;196(4293):1010–2.

    Article  CAS  PubMed  Google Scholar 

  47. Narisawa S, et al. Testis-specific cytochrome c-null mice produce functional sperm but undergo early testicular atrophy. Mol Cell Biol. 2002;22(15):5554–62.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Huttemann M, Jaradat S, Grossman LI. Cytochrome c oxidase of mammals contains a testes-specific isoform of subunit VIb – the counterpart to testes-specific cytochrome c? Mol Reprod Dev. 2003;66(1):8–16.

    Article  CAS  PubMed  Google Scholar 

  49. Blanco A, Zinkham WH. Lactate dehydrogenases in human testes. Science. 1963;139(3555):601–2.

    Article  CAS  PubMed  Google Scholar 

  50. Goldberg E. Lactic and malic dehydrogenases in human spermatozoa. Science. 1963;139(3555):602–3.

    Article  CAS  PubMed  Google Scholar 

  51. Bradley MP, et al. Cloning, sequencing, and characterization of LDH-C4 from a fox testis cDNA library. Mol Reprod Dev. 1996;44(4):452–9.

    Article  CAS  PubMed  Google Scholar 

  52. Rato L, et al. Metabolic regulation is important for spermatogenesis. Nat Rev Urol. 2012;9(6):330–8.

    Article  CAS  PubMed  Google Scholar 

  53. Oliveira PF, et al. Intracellular pH regulation in human Sertoli cells: role of membrane transporters. Reproduction. 2009;137(2):353–9.

    Article  CAS  PubMed  Google Scholar 

  54. Rato L, et al. Tubular fluid secretion in the seminiferous epithelium: ion transporters and aquaporins in Sertoli cells. J Membr Biol. 2010;236(2):215–24.

    Article  CAS  PubMed  Google Scholar 

  55. Boussouar F, Benahmed M. Lactate and energy metabolism in male germ cells. Trends Endocrinol Metab. 2004;15(7):345–50.

    Article  CAS  PubMed  Google Scholar 

  56. Erkkila K, et al. Lactate inhibits germ cell apoptosis in the human testis. Mol Hum Reprod. 2002;8(2):109–17.

    Article  CAS  PubMed  Google Scholar 

  57. Scheepers A, Joost HG, Schurmann A. The glucose transporter families SGLT and GLUT: molecular basis of normal and aberrant function. JPEN J Parenter Enteral Nutr. 2004;28(5):364–71.

    Article  CAS  PubMed  Google Scholar 

  58. Jutte NH, et al. FSH stimulation of the production of pyruvate and lactate by rat Sertoli cells may be involved in hormonal regulation of spermatogenesis. J Reprod Fertil. 1983;68(1):219–26.

    Article  CAS  PubMed  Google Scholar 

  59. Oonk RB, Grootegoed JA, van der Molen HJ. Comparison of the effects of insulin and follitropin on glucose metabolism by Sertoli cells from immature rats. Mol Cell Endocrinol. 1985;42(1):39–48.

    Article  CAS  PubMed  Google Scholar 

  60. Oliveira PF, et al. Effect of insulin deprivation on metabolism and metabolism-associated gene transcript levels of in vitro cultured human Sertoli cells. Biochim Biophys Acta. 2012;1820(2):84–9.

    Article  CAS  PubMed  Google Scholar 

  61. Alves MG, et al. Hormonal control of Sertoli cell metabolism regulates spermatogenesis. Cell Mol Life Sci. 2013;70(5):777–93.

    Article  CAS  PubMed  Google Scholar 

  62. Dias TR, et al. Glucose transport and metabolism in Sertoli cell: relevance for male fertility. Curr Chem Biol. 2013;7(3):282–93.

    Article  CAS  Google Scholar 

  63. Oonk RB, Grootegoed JA. Identification of insulin receptors on rat Sertoli cells. Mol Cell Endocrinol. 1987;49(1):51–62.

    Article  CAS  PubMed  Google Scholar 

  64. Hall PF, Mita M. Influence of follicle-stimulating hormone on glucose transport by cultured Sertoli cells. Biol Reprod. 1984;31(5):863–9.

    Article  CAS  PubMed  Google Scholar 

  65. Blok LJ, et al. Follicle-stimulating hormone regulates androgen receptor mRNA in Sertoli cells. Mol Cell Endocrinol. 1989;63(1–2):267–71.

    Article  CAS  PubMed  Google Scholar 

  66. Blok LJ, et al. Transient down-regulation of androgen receptor messenger ribonucleic acid (mRNA) expression in Sertoli cells by follicle-stimulating hormone is followed by up-regulation of androgen receptor mRNA and protein. Endocrinology. 1992;131(3):1343–9.

    Article  CAS  PubMed  Google Scholar 

  67. Borland K, et al. The actions of insulin-like growth factors I and II on cultured Sertoli cells. Endocrinology. 1984;114(1):240–6.

    Article  CAS  PubMed  Google Scholar 

  68. Skinner MK, Griswold MD. Secretion of testicular transferrin by cultured Sertoli cells is regulated by hormones and retinoids. Biol Reprod. 1982;27(1):211–21.

    Article  CAS  PubMed  Google Scholar 

  69. Guma FC, et al. Effect of FSH and insulin on lipogenesis in cultures of Sertoli cells from immature rats. Braz J Med Biol Res. 1997;30(5):591–7.

    Article  CAS  PubMed  Google Scholar 

  70. Oliveira PF, et al. Influence of 5alpha-dihydrotestosterone and 17beta-estradiol on human Sertoli cells metabolism. Int J Androl. 2011;34(6 Pt 2):e612–20.

    Article  CAS  PubMed  Google Scholar 

  71. Simoes VL, et al. Regulation of apoptotic signaling pathways by 5alpha-dihydrotestosterone and 17beta-estradiol in immature rat Sertoli cells. J Steroid Biochem Mol Biol. 2013;135:15–23.

    Article  CAS  PubMed  Google Scholar 

  72. Palmero S, Maggiani S, Fugassa E. Nuclear triiodothyronine receptors in rat Sertoli cells. Mol Cell Endocrinol. 1988;58(2–3):253–6.

    Article  CAS  PubMed  Google Scholar 

  73. Nehar D, et al. Interleukin 1alpha stimulates lactate dehydrogenase a expression and lactate production in cultured porcine Sertoli cells. Biol Reprod. 1998;59(6):1425–32.

    Article  CAS  PubMed  Google Scholar 

  74. Grataroli R, Boussouar F, Benahmed M. Role of sphingosine in the tumor necrosis factor alpha stimulatory effect on lactate dehydrogenase a expression and activity in porcine Sertoli cells. Biol Reprod. 2000;63(5):1473–81.

    Article  CAS  PubMed  Google Scholar 

  75. Riera MF, et al. Regulation of lactate production and glucose transport as well as of glucose transporter 1 and lactate dehydrogenase a mRNA levels by basic fibroblast growth factor in rat Sertoli cells. J Endocrinol. 2002;173(2):335–43.

    Article  CAS  PubMed  Google Scholar 

  76. Alves MG, et al. Diabetes, insulin-mediated glucose metabolism and Sertoli/blood-testis barrier function. Tissue Barriers. 2013;1(2):e23992.

    Article  PubMed  PubMed Central  Google Scholar 

  77. Hunter RH. Fallopian tube physiology: preliminaries to monospermic fertilization and cellular events post-fertilization. Ernst Schering Res Found Workshop. 2005;52:245–61.

    Article  Google Scholar 

  78. Wassarman PM. Mammalian fertilization: molecular aspects of gamete adhesion, exocytosis, and fusion. Cell. 1999;96(2):175–83.

    Article  CAS  PubMed  Google Scholar 

  79. Paoli D, et al. Mitochondrial membrane potential profile and its correlation with increasing sperm motility. Fertil Steril. 2011;95(7):2315–9.

    Article  CAS  PubMed  Google Scholar 

  80. Inaba K. Molecular architecture of the sperm flagella: molecules for motility and signaling. Zool Sci. 2003;20(9):1043–56.

    Article  CAS  Google Scholar 

  81. Gunes S, et al. Microtubular dysfunction and male infertility. World J Mens Health. 2018;36 https://doi.org/10.5534/wjmh.180066.

  82. Shingyoji C, et al. Effect of beat frequency on the velocity of microtubule sliding in reactivated sea urchin sperm flagella under imposed head vibration. J Exp Biol. 1995;198(Pt 3):645–53.

    CAS  PubMed  Google Scholar 

  83. Burgess SA, et al. Dynein structure and power stroke. Nature. 2003;421(6924):715–8.

    Article  CAS  PubMed  Google Scholar 

  84. Serohijos AW, et al. A structural model reveals energy transduction in dynein. Proc Natl Acad Sci U S A. 2006;103(49):18540–5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Kamp G, et al. Regulatory properties of 6-phosphofructokinase and control of glycolysis in boar spermatozoa. Reproduction. 2007;133(1):29–40.

    Article  CAS  PubMed  Google Scholar 

  86. Adam DE, Wei J. Mass transport of ATP within the motile sperm. J Theor Biol. 1975;49(1):125–45.

    Article  CAS  PubMed  Google Scholar 

  87. Wang X, et al. Alterations in mitochondria membrane potential and oxidative stress in infertile men: a prospective observational study. Fertil Steril. 2003;80(Suppl 2):844–50.

    Article  PubMed  Google Scholar 

  88. Luft R. The development of mitochondrial medicine. Biochim Biophys Acta. 1995;1271(1):1–6.

    Article  CAS  PubMed  Google Scholar 

  89. Tombes RM, Shapiro BM. Enzyme termini of a phosphocreatine shuttle. Purification and characterization of two creatine kinase isozymes from sea urchin sperm. J Biol Chem. 1987;262(33):16011–9.

    CAS  PubMed  Google Scholar 

  90. Oberholzer M, et al. Trypanosomes and mammalian sperm: one of a kind? Trends Parasitol. 2007;23(2):71–7.

    Article  PubMed  Google Scholar 

  91. Rodriguez-Gil JE. Mammalian sperm energy resources management and survival during conservation in refrigeration. Reprod Domest Anim. 2006;41(Suppl 2):11–20.

    Article  PubMed  Google Scholar 

  92. Mukai C, Okuno M. Glycolysis plays a major role for adenosine triphosphate supplementation in mouse sperm flagellar movement. Biol Reprod. 2004;71(2):540–7.

    Article  CAS  PubMed  Google Scholar 

  93. Odet F, et al. Expression of the gene for mouse lactate dehydrogenase C (Ldhc) is required for male fertility. Biol Reprod. 2008;79(1):26–34.

    Article  CAS  PubMed  Google Scholar 

  94. Hung PH, et al. Sperm mitochondrial integrity is not required for hyperactivated motility, zona binding, or acrosome reaction in the rhesus macaque. Biol Reprod. 2008;79(2):367–75.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Hereng TH, et al. Exogenous pyruvate accelerates glycolysis and promotes capacitation in human spermatozoa. Hum Reprod. 2011;26(12):3249–63.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Yanagimachi R. Fertility of mammalian spermatozoa: its development and relativity. Zygote. 1994;2(4):371–2.

    Article  CAS  PubMed  Google Scholar 

  97. Buffone MG, et al. Capacitation-associated protein tyrosine phosphorylation and membrane fluidity changes are impaired in the spermatozoa of asthenozoospermic patients. Reproduction. 2005;129(6):697–705.

    Article  CAS  PubMed  Google Scholar 

  98. Ho HC, Granish KA, Suarez SS. Hyperactivated motility of bull sperm is triggered at the axoneme by Ca2+ and not cAMP. Dev Biol. 2002;250(1):208–17.

    Article  CAS  PubMed  Google Scholar 

  99. de Lamirande E, Leclerc P, Gagnon C. Capacitation as a regulatory event that primes spermatozoa for the acrosome reaction and fertilization. Mol Hum Reprod. 1997;3(3):175–94.

    Article  PubMed  Google Scholar 

  100. Kirichok Y, Navarro B, Clapham DE. Whole-cell patch-clamp measurements of spermatozoa reveal an alkaline-activated Ca2+ channel. Nature. 2006;439(7077):737–40.

    Article  CAS  PubMed  Google Scholar 

  101. Toshimori K, Higashi R, Oura C. Distribution of intramembranous particles and filipin-sterol complexes in mouse sperm membranes: polyene antibiotic filipin treatment. Am J Anat. 1985;174(4):455–70.

    Article  CAS  PubMed  Google Scholar 

  102. Suarez SS, Dai X. Intracellular calcium reaches different levels of elevation in hyperactivated and acrosome-reacted hamster sperm. Mol Reprod Dev. 1995;42(3):325–33.

    Article  CAS  PubMed  Google Scholar 

  103. Kota V, et al. Role of glycerol-3-phosphate dehydrogenase 2 in mouse sperm capacitation. Mol Reprod Dev. 2010;77(9):773–83.

    Article  CAS  PubMed  Google Scholar 

  104. Harper CV, Publicover SJ. Reassessing the role of progesterone in fertilization – compartmentalized calcium signalling in human spermatozoa? Hum Reprod. 2005;20(10):2675–80.

    Article  CAS  PubMed  Google Scholar 

  105. Roveri A, et al. Phospholipid hydroperoxide glutathione peroxidase of rat testis. Gonadotropin dependence and immunocytochemical identification. J Biol Chem. 1992;267(9):6142–6.

    CAS  PubMed  Google Scholar 

  106. Mitra K, Shivaji S. Proteins implicated in sperm capacitation. Indian J Exp Biol. 2005;43(11):1001–15.

    CAS  PubMed  Google Scholar 

  107. Hoshi K, Tsukikawa S, Sato A. Importance of Ca2+, K+ and glucose in the medium for sperm penetration through the human zona pellucida. Tohoku J Exp Med. 1991;165(2):99–104.

    Article  CAS  PubMed  Google Scholar 

  108. Ruiz-Pesini E, et al. The role of the mitochondrion in sperm function: is there a place for oxidative phosphorylation or is this a purely glycolytic process? Curr Top Dev Biol. 2007;77:3–19.

    Article  CAS  PubMed  Google Scholar 

  109. Nichol R, et al. Concentrations of energy substrates in oviductal fluid and blood plasma of pigs during the peri-ovulatory period. J Reprod Fertil. 1992;96(2):699–707.

    Article  CAS  PubMed  Google Scholar 

  110. Hutson SM, Van Dop C, Lardy HA. Mitochondrial metabolism of pyruvate in bovine spermatozoa. J Biol Chem. 1977;252(4):1309–15.

    CAS  PubMed  Google Scholar 

  111. Fraser LR, Lane MR. Capacitation- and fertilization-related alterations in mouse sperm oxygen consumption. J Reprod Fertil. 1987;81(2):385–93.

    Article  CAS  PubMed  Google Scholar 

  112. Stendardi A, et al. Evaluation of mitochondrial respiratory efficiency during in vitro capacitation of human spermatozoa. Int J Androl. 2011;34(3):247–55.

    Article  CAS  PubMed  Google Scholar 

  113. Cosson MP, Cosson J, Billard R. Synchronous triggering of trout sperm is followed by an invariable set sequence of movement parameters whatever the incubation medium. Cell Motil Cytoskeleton. 1991;20(1):55–68.

    Article  CAS  PubMed  Google Scholar 

  114. Cosson J. Frenetic activation of fish spermatozoa flagella entails short-term motility, portending their precocious decadence. J Fish Biol. 2010;76(1):240–79.

    Article  CAS  PubMed  Google Scholar 

  115. Dreanno C, et al. 1H-NMR and (31)P-NMR analysis of energy metabolism of quiescent and motile turbot (Psetta maxima) spermatozoa. J Exp Zool. 2000;286(5):513–22.

    Article  CAS  PubMed  Google Scholar 

  116. Cosson J, et al. Marine fish spermatozoa: racing ephemeral swimmers. Reproduction. 2008;136(3):277–94.

    Article  CAS  PubMed  Google Scholar 

  117. Lechtreck KF, Witman GB. Chlamydomonas reinhardtii hydin is a central pair protein required for flagellar motility. J Cell Biol. 2007;176:473–82.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Ginther OJ, Whitmore HL, Squires EL. Characteristics of estrus, diestrus, and ovulation in mares and effects of season and nursing. Am J Vet Res. 1972;33(10):1935–9.

    CAS  PubMed  Google Scholar 

  119. Nallella KP, et al. Inter-sample variability in post-thaw human spermatozoa. Cryobiology. 2004;49(2):195–9.

    Article  PubMed  Google Scholar 

  120. Brum AM, Sabeur K, Ball BA. Apoptotic-like changes in equine spermatozoa separated by density-gradient centrifugation or after cryopreservation. Theriogenology. 2008;69(9):1041–55.

    Article  CAS  PubMed  Google Scholar 

  121. Neild DM, et al. Membrane changes during different stages of a freeze-thaw protocol for equine semen cryopreservation. Theriogenology. 2003;59(8):1693–705.

    Article  CAS  PubMed  Google Scholar 

  122. Valcarce DG, et al. Analysis of DNA damage after human sperm cryopreservation in genes crucial for fertilization and early embryo development. Andrology. 2013;1(5):723–30.

    Article  CAS  PubMed  Google Scholar 

  123. Pegg DE. Principles of cryopreservation. Methods Mol Biol. 2007;368:39–57.

    Article  CAS  PubMed  Google Scholar 

  124. Hammerstedt RH, Graham JK, Nolan JP. Cryopreservation of mammalian sperm: what we ask them to survive. J Androl. 1990;11(1):73–88.

    CAS  PubMed  Google Scholar 

  125. Morris GJ, et al. Rapidly cooled horse spermatozoa: loss of viability is due to osmotic imbalance during thawing, not intracellular ice formation. Theriogenology. 2007;68(5):804–12.

    Article  CAS  PubMed  Google Scholar 

  126. Sardoy MC, Carretero MI, Neild DM. Evaluation of stallion sperm DNA alterations during cryopreservation using toluidine blue. Anim Reprod Sci. 2008;107(3–4):349–50.

    Article  Google Scholar 

  127. Burnaugh L, et al. Osmotic stress stimulates generation of superoxide anion by spermatozoa in horses. Anim Reprod Sci. 2010;117(3–4):249–60.

    Article  CAS  PubMed  Google Scholar 

  128. Rota A, et al. Presence and distribution of fungi and bacteria in the reproductive tract of healthy stallions. Theriogenology. 2011;76(3):464–70.

    Article  CAS  PubMed  Google Scholar 

  129. Aurich C, Spergser J. Influence of bacteria and gentamicin on cooled-stored stallion spermatozoa. Theriogenology. 2007;67(5):912–8.

    Article  CAS  PubMed  Google Scholar 

  130. Ortega-Ferrusola C, et al. Does the microbial flora in the ejaculate affect the freezeability of stallion sperm? Reprod Domest Anim. 2009;44(3):518–22.

    Article  CAS  PubMed  Google Scholar 

  131. Gibb Z, Aitken RJ. The impact of sperm metabolism during in vitro storage: the stallion as a model. Biomed Res Int. 2016;2016:9380609.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  132. Halliwell B, Gutteridge JMC. Free radicals in biology and medicine. 3rd ed. Oxford: Oxford University Press; 2003.

    Google Scholar 

  133. Aitken RJ, Curry BJ. Redox regulation of human sperm function: from the physiological control of sperm capacitation to the etiology of infertility and DNA damage in the germ line. Antioxid Redox Signal. 2011;14(3):367–81.

    Article  CAS  PubMed  Google Scholar 

  134. Aitken RJ, et al. Sperm motility is lost in vitro as a consequence of mitochondrial free radical production and the generation of electrophilic aldehydes but can be significantly rescued by the presence of nucleophilic thiols. Biol Reprod. 2012;87(5):110.

    Article  CAS  PubMed  Google Scholar 

  135. Gibb Z, et al. Quercetin improves the postthaw characteristics of cryopreserved sex-sorted and nonsorted stallion sperm. Theriogenology. 2013;79(6):1001–9.

    Article  CAS  PubMed  Google Scholar 

  136. Baumber J, Ball BA, Linfor JJ. Assessment of the cryopreservation of equine spermatozoa in the presence of enzyme scavengers and antioxidants. Am J Vet Res. 2005;66(5):772–9.

    Article  CAS  PubMed  Google Scholar 

  137. Moubasher AE, et al. Catalase improves motility, vitality and DNA integrity of cryopreserved human spermatozoa. Andrologia. 2013;45(2):135–9.

    Article  CAS  PubMed  Google Scholar 

  138. Gibb Z, et al. L-carnitine and pyruvate are prosurvival factors during the storage of stallion spermatozoa at room temperature. Biol Reprod. 2015;93(4):104.

    Article  CAS  PubMed  Google Scholar 

  139. Agarwal A, Sengupta P, Durairajanayagam D. Role of L-carnitine in female infertility. Reprod Biol Endocrinol. 2018;16(1):5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  140. Littarru GP, Tiano L. Bioenergetic and antioxidant properties of coenzyme Q10: recent developments. Mol Biotechnol. 2007;37(1):31–7.

    Article  CAS  PubMed  Google Scholar 

  141. Srinivasan V, et al. Melatonin in mitochondrial dysfunction and related disorders. Int J Alzheimers Dis. 2011;2011:326320.

    PubMed  PubMed Central  Google Scholar 

  142. de Lamirande E, et al. Reactive oxygen species and sperm physiology. Rev Reprod. 1997;2(1):48–54.

    Article  PubMed  Google Scholar 

  143. Kamp G, Busselmann G, Lauterwein J. Spermatozoa: models for studying regulatory aspects of energy metabolism. Experientia. 1996;52(5):487–94.

    Article  CAS  PubMed  Google Scholar 

  144. Silver IA, Erecinska M. Energetic demands of the Na+/K+ ATPase in mammalian astrocytes. Glia. 1997;21(1):35–45.

    Article  CAS  PubMed  Google Scholar 

  145. Gulcin I. Antioxidant and antiradical activities of L-carnitine. Life Sci. 2006;78(8):803–11.

    Article  CAS  PubMed  Google Scholar 

  146. Peluso G, et al. Carnitine: an osmolyte that plays a metabolic role. J Cell Biochem. 2000;80(1):1–10.

    Article  CAS  PubMed  Google Scholar 

  147. Swegen A, et al. Investigation of the stallion sperm proteome by mass spectrometry. Reproduction. 2015;149(3):235–44.

    Article  CAS  PubMed  Google Scholar 

  148. Li K, et al. Level of free L-carnitine in human seminal plasma and its correlation with semen quality. Zhonghua Nan Ke Xue. 2007;13(2):143–6.

    CAS  PubMed  Google Scholar 

  149. Brooks DE. Carnitine in the male reproductive tract and its relation to the metabolism of the epididymis and spermatozoa. In: McGarry JD, Frenkel RA, editors. Carnitine biosynthesis metabolism and function. New York: Academic Press; 1980. p. 219–35.

    Chapter  Google Scholar 

  150. Jeulin C, Lewin LM. Role of free L-carnitine and acetyl-L-carnitine in post-gonadal maturation of mammalian spermatozoa. Hum Reprod Update. 1996;2(2):87–102.

    Article  CAS  PubMed  Google Scholar 

  151. Stradaioli G, et al. Effect of L-carnitine administration on the seminal characteristics of oligoasthenospermic stallions. Theriogenology. 2004;62(3–4):761–77.

    Article  CAS  PubMed  Google Scholar 

  152. Mitra A, Richardson RT, O’Rand MG. Analysis of recombinant human semenogelin as an inhibitor of human sperm motility. Biol Reprod. 2010;82(3):489–96.

    Article  CAS  PubMed  Google Scholar 

  153. O’Rand MG, Silva EJ, Hamil KG. Non-hormonal male contraception: a review and development of an Eppin based contraceptive. Pharmacol Ther. 2016;157:105–11.

    Article  CAS  PubMed  Google Scholar 

  154. O’Rand MG, et al. Inhibition of sperm motility in male macaques with EP055, a potential non-hormonal male contraceptive. PLoS One. 2018;13(4):e0195953.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  155. Esposito G, et al. Mice deficient for soluble adenylyl cyclase are infertile because of a severe sperm-motility defect. Proc Natl Acad Sci U S A. 2004;101(9):2993–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  156. Mathew V, Bantwal G. Male contraception. Indian J Endocrinol Metab. 2012;16(6):910–7.

    Article  PubMed  PubMed Central  Google Scholar 

  157. Klein T, Cooper TG, Yeung CH. The role of potassium chloride cotransporters in murine and human sperm volume regulation. Biol Reprod. 2006;75(6):853–8.

    Article  CAS  PubMed  Google Scholar 

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Sengupta, P., Durairajanayagam, D., Agarwal, A. (2020). Fuel/Energy Sources of Spermatozoa. In: Parekattil, S., Esteves, S., Agarwal, A. (eds) Male Infertility. Springer, Cham. https://doi.org/10.1007/978-3-030-32300-4_26

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