The Impact of Reproductive Technologies on Stallion Mitochondrial Function

Reproduction in Domestic Animals

Volumn 50, Issue 4, 2015, Pages 529-537

  Pena F J ^a,b   Plaza Davila, M ^a   Ball, Ba ^b   Squires, E L ^b   Martin Munoz P ^a   Ortega Ferrusola, C ^a   Balao da Silva, C ^a  

^a UNIVERSITY OF EXTREMADURA   (Spain)

^b UNIVERSITY OF KENTUCKY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MAMMALIA;

REACTIVE OXYGEN METABOLITE;

ADVERSE EFFECTS; ANIMAL; APOPTOSIS; CELL SEPARATION; CELL SURVIVAL; CRYOPRESERVATION; FERTILIZATION; HORSE; INFERTILITY THERAPY; MALE; MITOCHONDRION; OSMOLARITY; OXIDATIVE STRESS; PHYSIOLOGY; PROCEDURES; SEX SELECTION; SPERM PRESERVATION; SPERMATOZOON; ULTRASTRUCTURE; VETERINARY;

ANIMALS; APOPTOSIS; CELL SEPARATION; CELL SURVIVAL; CRYOPRESERVATION; FERTILIZATION; HORSES; MALE; MITOCHONDRIA; OSMOLAR CONCENTRATION; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; REPRODUCTIVE TECHNIQUES; SEMEN PRESERVATION; SEX PRESELECTION; SPERMATOZOA;

EID: 84936986302     PISSN: 09366768     EISSN: 14390531     Source Type: Journal    
DOI: 10.1111/rda.12551     Document Type: Review

References (113)

1. Agarwal A, Virk G, Ong C, du Plessis SS, 2014: Effect of oxidative stress on male reproduction. World J Mens Health 32, 1-17.
2. Aitken RJ, Curry BJ, 2011: 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 14, 367-381.
3. Aitken RJ, Koppers AJ, 2011: Apoptosis and DNA damage in human spermatozoa. Asian J Androl 13, 36-42.
4. Aitken RJ, De Iuliis GN, Gibb Z, Baker MA, 2012a: The Simmet lecture: new horizons on an old landscape-oxidative stress, DNA damage and apoptosis in the male germ line. Reprod Domest Anim 47(Suppl 4), 7-14.
5. Aitken RJ, Gibb Z, Mitchell LA, Lambourne SR, Connaughton HS, De Iuliis GN, 2012b: 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 87, 110-118.
6. Aitken RJ, Whiting S, De Iuliis GN, McClymont S, Mitchell LA, Baker MA, 2012c: Electrophilic aldehydes generated by sperm metabolism activate mitochondrial reactive oxygen species generation and apoptosis by targeting succinate dehydrogenase. J Biol Chem 287, 33048-33060.
7. Aitken RJ, Finnie JM, Muscio L, Whiting S, Connaughton HS, Kuczera L, Rothkirch TB, De Iuliis GN, 2014: Potential importance of transition metals in the induction of DNA damage by sperm preparation media. Hum Reprod 29, 2136-2147.
8. Alessi DR, Deak M, Casamayor A, Caudwell FB, Morrice N, Norman DG, Gaffney P, Reese CB, MacDougall CN, Harbison D, Ashworth A, Bownes M, 1997: 3-Phosphoinositide-dependent protein kinase-1 (PDK1): structural and functional homology with the Drosophila DSTPK61 kinase. Curr Biol 7, 776-789.
9. Amaral A, Lourenco B, Marques M, Ramalho-Santos J, 2013: Mitochondria functionality and sperm quality. Reproduction 146, R163-R174.
10. Auger J, Leonce S, Jouannet P, Ronot X, 1993: Flow cytometric sorting of living, highly motile human spermatozoa based on evaluation of their mitochondrial activity. J Histochem Cytochem 41, 1247-1251.
11. Balao da Silva CM, Ortega Ferrusola C, Morillo Rodriguez A, Gallardo Bolanos JM, Plaza Davila M, Morrell JM, Rodriguez Martinez H, Tapia JA, Aparicio IM, Pena FJ, 2013a: Sex sorting increases the permeability of the membrane of stallion spermatozoa. Anim Reprod Sci, 138, 241-251.
12. Balao da Silva CM, Spinaci M, Bucci D, Giaretta E, Pena FJ, Mari G, Galeati G, 2013b: Effect of sex sorting on stallion spermatozoa: Heterologous oocyte binding, tyrosine phosphorylation and acrosome reaction assay. Anim Reprod Sci 141, 68-74.
13. Balao da Silva C, Ortega Ferrusola C, Gallardo Bolanos J, Plaza Davila M, Martin-Munoz P, Morrell J, Rodriguez Martinez H, Pena F, 2014: Effect of overnight staining on the quality of flow cytometric sorted stallion sperm: comparison with tradtitional protocols. Reprod Domest Anim 49, 1021-1027.
14. Ball BA, 2008: Oxidative stress, osmotic stress and apoptosis: impacts on sperm function and preservation in the horse. Anim Reprod Sci 107, 257-267.
15. Ball BA, Gravance CG, Medina V, Baumber J, Liu IK, 2000: Catalase activity in equine semen. Am J Vet Res 61, 1026-1030.
16. Barroso G, Taylor S, Morshedi M, Manzur F, Gavino F, Oehninger S, 2006: Mitochondrial membrane potential integrity and plasma membrane translocation of phosphatidylserine as early apoptotic markers: a comparison of two different sperm subpopulations. Fertil Steril 85, 149-154.
17. Bathgate R, 2008: Functional integrity of sex-sorted, frozen-thawed boar sperm and its potential for artificial insemination. Theriogenology 70, 1234-1241.
18. Becker WMKL, Hardin J, 2003: The world of the cell Benjamin Cummings San Francisco.
19. Bolanos JM, Moran AM, da Silva CM, Davila MP, Munoz PM, Aparicio IM, Tapia JA, Ferrusola CO, Pena FJ, 2014: During cooled storage the extender influences processed autophagy marker light chain 3 (LC3B) of stallion spermatozoa. Anim Reprod Sci 145, 40-46.
20. Bravo MM, Aparicio IM, Garcia-Herreros M, Gil MC, Pena FJ, Garcia-Marin LJ, 2005: Changes in tyrosine phosphorylation associated with true capacitation and capacitation-like state in boar spermatozoa. Mol Reprod Dev 71, 88-96.
21. Bravo A, Treulen F, Uribe P, Boguen R, Felmer R, Villegas JV, 2014: Effect of mitochondrial calcium uniporter blocking on human spermatozoa. Andrologia doi:10.1111/and.12314 [Epub ahead of print].
22. Breitbart H, Levinshal T, Cohen N, Friedmann H, Lubart R, 1996: Changes in calcium transport in mammalian sperm mitochondria and plasma membrane irradiated at 633 nm (HeNe laser). J Photochem Photobiol, B 34, 117-121.
23. Brum AM, Sabeur K, Ball BA, 2008: Apoptotic-like changes in equine spermatozoa separated by density-gradient centrifugation or after cryopreservation. Theriogenology 69, 1041-1055.
24. Buchanan BR, Seidel GE Jr, McCue PM, Schenk JL, Herickhoff LA, Squires EL, 2000: Insemination of mares with low numbers of either unsexed or sexed spermatozoa. Theriogenology, 53, 1333-1344.
25. Cardone MH, Roy N, Stennicke HR, Salvesen GS, Franke TF, Stanbridge E, Frisch S, Reed JC, 1998: Regulation of cell death protease caspase-9 by phosphorylation. Science 282, 1318-1321.
26. Caselles AB, Miro-Moran A, Morillo Rodriguez A, Gallardo Bolanos JM, Ortega-Ferrusola C, Salido GM, Pena FJ, Tapia JA, Aparicio IM, 2014: Identification of apoptotic bodies in equine semen. Reprod Domest Anim, 49, 254-262.
27. Chipuk JE, Bouchier-Hayes L, Green DR, 2006: Mitochondrial outer membrane permeabilization during apoptosis: the innocent bystander scenario. Cell Death Differ 13, 1396-1402.
28. Costello S, Michelangeli F, Nash K, Lefievre L, Morris J, Machado-Oliveira G, Barratt C, Kirkman-Brown J, Publicover S, 2009: Ca2+-stores in sperm: their identities and functions. Reproduction 138, 425-437.
29. Danial NN, Gramm CF, Scorrano L, Zhang CY, Krauss S, Ranger AM, Datta SR, Greenberg ME, Licklider LJ, Lowell BB, Gygi SP, Korsmeyer SJ, 2003: BAD and glucokinase reside in a mitochondrial complex that integrates glycolysis and apoptosis. Nature 424, 952-956.
30. Das SC, Isobe N, Yoshimura Y, 2011: Expression of Toll-like receptors and avian beta-defensins and their changes in response to bacterial components in chicken sperm. Poult Sci 90, 417-425.
31. Datta SR, Dudek H, Tao X, Masters S, Fu H, Gotoh Y, Greenberg ME, 1997: Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell 91, 231-241.
32. De Martino C, Floridi A, Marcante ML, Malorni W, Scorza Barcellona P, Bellocci M, Silvestrini B, 1979: Morphological, histochemical and biochemical studies on germ cell mitochondria of normal rats. Cell Tissue Res 196, 1-22.
33. Dramsi S, Scheid MP, Maiti A, Hojabrpour P, Chen X, Schubert K, Goodlett DR, Aebersold R, Duronio V, 2002: Identification of a novel phosphorylation site, Ser-170, as a regulator of bad pro-apoptotic activity. J Biol Chem 277, 6399-6405.
34. Dudkina NV, Sunderhaus S, Boekema EJ, Braun HP, 2008: The higher level of organization of the oxidative phosphorylation system: mitochondrial supercomplexes. J Bioenerg Biomembr 40, 419-424.
35. Edmond AJ, Brinsko SP, Love CC, Blanchard TL, Teague SR, Varner DD, 2012: Effect of centrifugal fractionation protocols on quality and recovery rate of equine sperm. Theriogenology 77, 959-966.
36. Ferramosca A, Focarelli R, Piomboni P, Coppola L, Zara V, 2008: Oxygen uptake by mitochondria in demembranated human spermatozoa: a reliable tool for the evaluation of sperm respiratory efficiency. Int J Androl 31, 337-345.
37. Ford WC, 2006: Glycolysis and sperm motility: does a spoonful of sugar help the flagellum go round? Hum Reprod Update 12, 269-274.
38. Frijters AC, Mullaart E, Roelofs RM, van Hoorne RP, Moreno JF, Moreno O, Merton JS, 2009: What affects fertility of sexed bull semen more, low sperm dosage or the sorting process? Theriogenology 71, 64-67.
39. Fujita Y, Mihara T, Okazaki T, Shitanaka M, Kushino R, Ikeda C, Negishi H, Liu Z, Richards JS, Shimada M, 2011: Toll-like receptors (TLR) 2 and 4 on human sperm recognize bacterial endotoxins and mediate apoptosis. Hum Reprod 26, 2799-2806.
40. Fuller SJ, Whittingham DG, 1997: Capacitation-like changes occur in mouse spermatozoa cooled to low temperatures. Mol Reprod Dev 46, 318-324.
41. Gallardo Bolanos JM, Miro Moran A, Balao da Silva CM, Morillo Rodriguez A, Plaza Davila M, Aparicio IM, Tapia JA, Ortega Ferrusola C, Pena FJ, 2012: Autophagy and apoptosis have a role in the survival or death of stallion spermatozoa during conservation in refrigeration. PLoS One, 7, e30688.
42. Gallardo Bolanos JM, Balao da Silva CM, Martin Munoz P, Morillo Rodriguez A, Plaza Davila M, Rodriguez-Martinez H, Aparicio IM, Tapia JA, Ortega Ferrusola C, Pena FJ, 2014: Phosphorylated AKT preserves stallion sperm viability and motility by inhibiting caspases 3 and 7. Reproduction, 148, 221-235.
43. Gallon F, Marchetti C, Jouy N, Marchetti P, 2006: The functionality of mitochondria differentiates human spermatozoa with high and low fertilizing capability. Fertil Steril 86, 1526-1530.
44. Garcia EM, Vazquez JM, Parrilla I, Calvete JJ, Sanz L, Caballero I, Roca J, Vazquez JL, Martinez EA, 2007: Improving the fertilizing ability of sex sorted boar spermatozoa. Theriogenology 68, 771-778.
45. Garcia BM, Fernandez LG, Ferrusola CO, Salazar-Sandoval C, Rodriguez AM, Martinez HR, Tapia JA, Morcuende D, Pena FJ, 2011: Membrane lipids of the stallion spermatozoon in relation to sperm quality and susceptibility to lipid peroxidation. Reprod Domest Anim 46, 141-148.
46. Garcia BM, Moran AM, Fernandez LG, Ferrusola CO, Rodriguez AM, Bolanos JM, da Silva CM, Martinez HR, Tapia JA, Pena FJ, 2012: The mitochondria of stallion spermatozoa are more sensitive than the plasmalemma to osmotic-induced stress: role of c-Jun N-terminal kinase (JNK) pathway. J Androl 33, 105-113.
47. Gibb Z, Morris LH, Maxwell WM, Grupen CG, 2011: Use of a defined diluent increases the sex-sorting efficiency of stallion sperm. Theriogenology 75, 610-619.
48. Gibb Z, Butler TJ, Morris LH, Maxwell WM, Grupen CG, 2013: Quercetin improves the postthaw characteristics of cryopreserved sex-sorted and nonsorted stallion sperm. Theriogenology 79, 1001-1009.
49. Gibb Z, Lambourne SR, Aitken RJ, 2014: The paradoxical relationship between stallion fertility and oxidative stress. Biol Reprod 91, 77-87.
50. Gillan L, Evans G, Maxwell WM, 2005: Flow cytometric evaluation of sperm parameters in relation to fertility potential. Theriogenology 63, 445-457.
51. Gonzalez-Fernandez L, Ortega-Ferrusola C, Macias-Garcia B, Salido GM, Pena FJ, Tapia JA, 2009: Identification of protein tyrosine phosphatases and dual-specificity phosphatases in mammalian spermatozoa and their role in sperm motility and protein tyrosine phosphorylation. Biol Reprod 80, 1239-1252.
52. Gonzalez-Fernandez L, Morrell JM, Pena FJ, Macias-Garcia B, 2012: Osmotic shock induces structural damage on equine spermatozoa plasmalemma and mitochondria. Theriogenology 78, 415-422.
53. de Graaf SP, Evans G, Maxwell WM, O'Brien JK, 2006: In vitro characteristics of fresh and frozen-thawed ram spermatozoa after sex sorting and re-freezing. Reprod Fertil Dev 18, 867-874.
54. Holt WV, Van Look KJ, 2004: Concepts in sperm heterogeneity, sperm selection and sperm competition as biological foundations for laboratory tests of semen quality. Reproduction 127, 527-535.
55. Johnson LA, 2000: Sexing mammalian sperm for production of offspring: the state-of-the-art. Anim Reprod Sci 60-61, 93-107.
56. Johnson LA, Welch GR, Rens W, 1999: The Beltsville sperm sexing technology: high-speed sperm sorting gives improved sperm output for in vitro fertilization and AI. J Anim Sci 77(Suppl 2), 213-220.
57. Johnston SD, Satake N, Zee Y, Lopez-Fernandez C, Holt WV, Gosalvez J, 2012: Osmotic stress and cryoinjury of koala sperm: an integrative study of the plasma membrane, chromatin stability and mitochondrial function. Reproduction 143, 787-797.
58. Klingenberg M, 2008: The ADP and ATP transport in mitochondria and its carrier. Biochim Biophys Acta 1778, 1978-2021.
59. Koppers AJ, De Iuliis GN, Finnie JM, McLaughlin EA, Aitken RJ, 2008: Significance of mitochondrial reactive oxygen species in the generation of oxidative stress in spermatozoa. J Clin Endocrinol Metab 93, 3199-3207.
60. Koppers AJ, Garg ML, Aitken RJ, 2010: Stimulation of mitochondrial reactive oxygen species production by unesterified, unsaturated fatty acids in defective human spermatozoa. Free Radic Biol Med 48, 112-119.
61. Koppers AJ, Mitchell LA, Wang P, Lin M, Aitken RJ, 2011: Phosphoinositide 3-kinase signalling pathway involvement in a truncated apoptotic cascade associated with motility loss and oxidative DNA damage in human spermatozoa. Biochem J 436, 687-698.
62. de Lamirande E, Gagnon C, 1993: Human sperm hyperactivation in whole semen and its association with low superoxide scavenging capacity in seminal plasma. Fertil Steril 59, 1291-1295.
63. de Lamirande E, Gagnon C, 2002: The extracellular signal-regulated kinase (ERK) pathway is involved in human sperm function and modulated by the superoxide anion. Mol Hum Reprod 8, 124-135.
64. de Lamirande E, Gagnon C, 2003: Redox control of changes in protein sulfhydryl levels during human sperm capacitation. Free Radic Biol Med 35, 1271-1285.
65. de Lamirande E, Lamothe G, 2009: Reactive oxygen-induced reactive oxygen formation during human sperm capacitation. Free Radic Biol Med 46, 502-510.
66. de Lamirande E, Jiang H, Zini A, Kodama H, Gagnon C, 1997: Reactive oxygen species and sperm physiology. Rev Reprod 2, 48-54.
67. Leahy T, Gadella BM, 2011: Sperm surface changes and physiological consequences induced by sperm handling and storage. Reproduction 142, 759-778.
68. Leahy T, Marti JI, Mendoza N, Perez-Pe R, Muino-Blanco T, Cebrian-Perez JA, Evans G, Maxwell WM, 2010: High pre-freezing dilution improves post-thaw function of ram spermatozoa. Anim Reprod Sci 119, 137-146.
69. Leahy T, Marti JI, Crossett B, Evan G, Maxwell WM, 2011: Two-dimensional polyacrylamide gel electrophoresis of membrane proteins from flow cytometrically sorted ram sperm. Theriogenology 75, 962-971.
70. Lizcano JM, Morrice N, Cohen P, 2000: Regulation of BAD by cAMP-dependent protein kinase is mediated via phosphorylation of a novel site, Ser155. Biochem J 349, 547-557.
71. Luo SM, Schatten H, Sun QY, 2013: Sperm mitochondria in reproduction: good or bad and where do they go? J Genet Genomics 40, 549-556.
72. Macias Garcia B, Gonzalez Fernandez L, Morrell JM, Ortega Ferrusola C, Tapia JA, Rodriguez Martinez H, Pena FJ, 2009a: Single-layer centrifugation through colloid positively modifies the sperm subpopulation structure of frozen-thawed stallion spermatozoa. Reprod Domest Anim 44, 523-526.
73. Macias Garcia B, Morrell JM, Ortega-Ferrusola C, Gonzalez-Fernandez L, Tapia JA, Rodriguez-Martinez H, Pena FJ, 2009b: Centrifugation on a single layer of colloid selects improved quality spermatozoa from frozen-thawed stallion semen. Anim Reprod Sci 114, 193-202.
74. Macias Garcia B, Ortega Ferrusola C, Aparicio IM, Miro-Moran A, Morillo Rodriguez A, Gallardo Bolanos JM, Gonzalez Fernandez L, Balao da Silva CM, Rodriguez Martinez H, Tapia JA, Pena FJ, 2012: Toxicity of glycerol for the stallion spermatozoa: effects on membrane integrity and cytoskeleton, lipid peroxidation and mitochondrial membrane potential. Theriogenology, 77, 1280-1289.
75. Macias-Garcia B, Gonzalez-Fernandez L, Gallardo-Bolanos JM, Pena FJ, Johannisson A, Morrell JM, 2012: Androcoll-E large selects a subset of live stallion spermatozoa capable of producing ROS. Anim Reprod Sci 132, 74-82.
76. Martin G, Sabido O, Durand P, Levy R, 2004: Cryopreservation induces an apoptosis-like mechanism in bull sperm. Biol Reprod 71, 28-37.
77. Mazur P, Koshimoto C, 2002: Is intracellular ice formation the cause of death of mouse sperm frozen at high cooling rates? Biol Reprod 66, 1485-1490.
78. Mendoza N, Casao A, Perez-Pe R, Cebrian-Perez JA, Muino-Blanco T, 2013: New insights into the mechanisms of ram sperm protection by seminal plasma proteins. Biol Reprod 88, 149-159.
79. Mitchell P, 1967: Proton current flow in mitochondrial systems. Nature 214, 1327-1328.
80. Mizrahi R, Breitbart H, 2014: Mitochondrial PKA mediates sperm motility. Biochim Biophys Acta 1840, 3402-3412.
81. Morrell JM, Garcia BM, Pena FJ, Johannisson A, 2011: Processing stored stallion semen doses by Single Layer Centrifugation. Theriogenology 76, 1424-1432.
82. Olson GE, Winfrey VP, 1990: Mitochondria-cytoskeleton interactions in the sperm midpiece. J Struct Biol 103, 13-22.
83. Olson GE, Winfrey VP, 1992: Structural organization of surface domains of sperm mitochondria. Mol Reprod Dev 33, 89-98.
84. Ortega Ferrusola C, Gonzalez Fernandez L, Macias Garcia B, Salazar-Sandoval C, Morillo Rodriguez A, Rodriguez Martinez H, Tapia JA, Pena FJ, 2009a: Effect of cryopreservation on nitric oxide production by stallion spermatozoa. Biol Reprod 81, 1106-1111.
85. Ortega Ferrusola C, Gonzalez Fernandez L, Morrell JM, Salazar Sandoval C, Macias Garcia B, Rodriguez-Martinez H, Tapia JA, Pena FJ, 2009b: Lipid peroxidation, assessed with BODIPY-C11, increases after cryopreservation of stallion spermatozoa, is stallion-dependent and is related to apoptotic-like changes. Reproduction 138, 55-63.
86. Ortega Ferrusola C, Gonzalez Fernandez L, Salazar Sandoval C, Macias Garcia B, Rodriguez Martinez H, Tapia JA, Pena FJ, 2010: Inhibition of the mitochondrial permeability transition pore reduces "apoptosis like" changes during cryopreservation of stallion spermatozoa. Theriogenology 74, 458-465.
87. Ortega-Ferrusola C, Sotillo-Galan Y, Varela-Fernandez E, Gallardo-Bolanos JM, Muriel A, Gonzalez-Fernandez L, Tapia JA, Pena FJ, 2008: Detection of "apoptosis-like" changes during the cryopreservation process in equine sperm. J Androl 29, 213-221.
88. Ortega-Ferrusola C, Garcia BM, Gallardo-Bolanos JM, Gonzalez-Fernandez L, Rodriguez-Martinez H, Tapia JA, Pena FJ, 2009: Apoptotic markers can be used to forecast the freezeability of stallion spermatozoa. Anim Reprod Sci 114, 393-403.
89. Pena FJ, Johannisson A, Wallgren M, Rodriguez-Martinez H, 2003: Assessment of fresh and frozen-thawed boar semen using an Annexin-V assay: a new method of evaluating sperm membrane integrity. Theriogenology 60, 677-689.
90. Peña FJ, Garcia BM, Samper JC, Aparicio IM, Tapia JA, Ferrusola CO, 2011: Dissecting the molecular damage to stallion spermatozoa: the way to improve current cryopreservation protocols? Theriogenology 76, 1177-1186.
91. Petyim S, Neungton C, Thanaboonyawat I, Laokirkkiat P, Choavaratana R, 2014: Sperm preparation before freezing improves sperm motility and reduces apoptosis in post-freezing-thawing sperm compared with post-thawing sperm preparation. J Assist Reprod Genet 31, 1673-1680.
92. Pommer AC, Rutllant J, Meyers SA, 2002: The role of osmotic resistance on equine spermatozoal function. Theriogenology 58, 1373-1384.
93. Prince FP, Buttle KF, 2004: Mitochondrial structure in steroid-producing cells: three-dimensional reconstruction of human Leydig cell mitochondria by electron microscopic tomography. Anat Rec A Discov Mol Cell Evol Biol 278, 454-461.
94. Pujianto DA, Curry BJ, Aitken RJ, 2010: Prolactin exerts a prosurvival effect on human spermatozoa via mechanisms that involve the stimulation of Akt phosphorylation and suppression of caspase activation and capacitation. Endocrinology 151, 1269-1279.
95. Ramalho-Santos J, Varum S, Amaral S, Mota PC, Sousa AP, Amaral A, 2009: Mitochondrial functionality in reproduction: from gonads and gametes to embryos and embryonic stem cells. Hum Reprod Update 15, 553-572.
96. Roca J, Martinez-Alborcia MJ, Gil MA, Parrilla I, Martinez EA, 2013: Dead spermatozoa in raw semen samples impair in vitro fertilization outcomes of frozen-thawed spermatozoa. Fertil Steril 100, 875-881.
97. Samper JC, Peña FJ, Plough TA, 2012: Commercial breeding with sexed stallion sperm: reality of fiction? J Equine Vet Sci 32, 471-474.
98. Schlame M, Ren M, Xu Y, Greenberg ML, Haller I, 2005: Molecular symmetry in mitochondrial cardiolipins. Chem Phys Lipids 138, 38-49.
99. da Silva CM, Macias-Garcia B, Miro-Moran A, Gonzalez-Fernandez L, Morillo-Rodriguez A, Ortega-Ferrusola C, Gallardo-Bolanos JM, Stilwell G, Tapia JA, Pena FJ, 2011: Melatonin reduces lipid peroxidation and apoptotic-like changes in stallion spermatozoa. J Pineal Res 51, 172-179.
100. Smith TB, Dun MD, Smith ND, Curry BJ, Connaughton HS, Aitken RJ, 2013: The presence of a truncated base excision repair pathway in human spermatozoa that is mediated by OGG1. J Cell Sci 126, 1488-1497.
101. Sousa AP, Amaral A, Baptista M, Tavares R, Caballero Campo P, Caballero Peregrin P, Freitas A, Paiva A, Almeida-Santos T, Ramalho-Santos J, 2011: Not all sperm are equal: functional mitochondria characterize a subpopulation of human sperm with better fertilization potential. PLoS One 6, e18112.
102. Spinaci M, Volpe S, Bernardini C, de Ambrogi M, Tamanini C, Seren E, Galeati G, 2006: Sperm sorting procedure induces a redistribution of Hsp70 but not Hsp60 and Hsp90 in boar spermatozoa. J Androl 27, 899-907.
103. Stowe DF, Camara AK, 2009: Mitochondrial reactive oxygen species production in excitable cells: modulators of mitochondrial and cell function. Antioxid Redox Signal 11, 1373-1414.
104. Thompson WE, Ramalho-Santos J, Sutovsky P, 2003: Ubiquitination of prohibitin in mammalian sperm mitochondria: possible roles in the regulation of mitochondrial inheritance and sperm quality control. Biol Reprod 69, 254-260.
105. Ursini F, Heim S, Kiess M, Maiorino M, Roveri A, Wissing J, Flohe L, 1999: Dual function of the selenoprotein PHGPx during sperm maturation. Science 285, 1393-1396.
106. Vadnais ML, Lin AM, Gerton GL, 2014: Mitochondrial fusion protein MFN2 interacts with the mitostatin-related protein MNS1 required for mouse sperm flagellar structure and function. Cilia 3, 5-25.
107. Vazquez JM, Parrilla I, Roca J, Gil MA, Cuello C, Vazquez JL, Martinez EA, 2009: Sex-sorting sperm by flow cytometry in pigs: issues and perspectives. Theriogenology 71, 80-88.
108. Voet DJG, Voet JG, Pratt CW, 2006: Fundamentals of Biochemistry, 2nd edn. John Wiley and Sons, New York.
109. Willoughby CE, Mazur P, Peter AT, Critser JK, 1996: Osmotic tolerance limits and properties of murine spermatozoa. Biol Reprod 55, 715-727.
110. Yang E, Zha J, Jockel J, Boise LH, Thompson CB, Korsmeyer SJ, 1995: Bad, a heterodimeric partner for Bcl-XL and Bcl-2, displaces Bax and promotes cell death. Cell 80, 285-291.
111. Yeste M, Estrada E, Rocha LG, Marin H, Rodriguez-Gil JE, Miro J, 2015: Cryotolerance of stallion spermatozoa is related to ROS production and mitochondrial membrane potential rather than to the integrity of sperm nucleus. Andrology 3, 395-407.
112. Yu F, Sugawara T, Maier CM, Hsieh LB, Chan PH, 2005: Akt/Bad signaling and motor neuron survival after spinal cord injury. Neurobiol Dis 20, 491-499.
113. Zini A, De Lamirande E, Gagnon C, 1995: Low levels of nitric oxide promote human sperm capacitation in vitro. J Androl 16, 424-431.