New insights into the mechanisms of ram sperm protection by seminal plasma proteins

Biology of Reproduction

Volumn 88, Issue 6, 2013, Pages

  Mendoza, Noelia ^a   Casao, Adriana ^a   Pérez Pé, Rosaura ^a   Cebrián Pérez, José A ^a   Muiño Blanco, Teresa ^a  

^a UNIVERSIDAD DE ZARAGOZA   (Spain)

Author keywords

Apoptosis; Capacitation; Refrigeration

Indexed keywords

BETULIC ACID; CARDIOLIPIN; CASPASE 3; CASPASE 7; DNA; PHOSPHATIDYLSERINE; SEMINAL PLASMA PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; CELL VIABILITY; CONTROLLED STUDY; DNA DAMAGE; ENZYME ACTIVATION; ENZYME ACTIVITY; FLOW CYTOMETRY; FREEZING; LOW TEMPERATURE PROCEDURES; MALE; MITOCHONDRIAL MEMBRANE POTENTIAL; NICK END LABELING; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN FUNCTION; RAM (SHEEP); SEMINAL PLASMA; SPERM; SPERMATOZOON CAPACITATION; WESTERN BLOTTING;

APOPTOSIS; CAPACITATION; REFRIGERATION;

ANIMALS; APOPTOSIS; CELL SURVIVAL; MALE; REFRIGERATION; SEMEN PRESERVATION; SEMINAL PLASMA PROTEINS; SHEEP; SPERM CAPACITATION; SPERM MOTILITY; SPERMATOZOA;

EID: 84882279238     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.112.105650     Document Type: Article

References (96)

1. Kerr JF, Wyllie AH, Currie AR. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer 1972; 26:239-257.
2. Brenner C, Kroemer G. Apoptosis. Mitochondria-the death signal integrators. Science 2000; 289:1150-1151.
3. Wajant H. The Fas signaling pathway: more than a paradigm. Science 2002; 296:1635-1636.
4. Fulda S. Betulinic acid for cancer treatment and prevention. Int J Mol Sci 2008; 9:1096-1107.
5. Wick W, Grimmel C, Wagenknecht B, Dichgans J, Weller M. Betulinic acid-induced apoptosis in glioma cells: a sequential requirement for new protein synthesis, formation of reactive oxygen species, and caspase processing. J Pharmacol Exp Ther 1999; 289:1306-1312.
6. Aitken RJ, Koppers AJ. Apoptosis and DNA damage in human spermatozoa. Asian J Androl 2011; 13:36-42.
7. Kierszenbaum AL. Apoptosis during spermatogenesis: the thrill of being alive. Mol Reprod Dev 2001; 58:1-3.
8. Paasch U, Grunewald S, Agarwal A, Glandera HJ. Activation pattern of caspases in human spermatozoa. Fertil Steril 2004; 81(suppl 1):802-809. 9. Sakkas D, Seli E, Manicardi GC, Nijs M, Ombelet W, Bizzaro D. The presence of abnormal spermatozoa in the ejaculate: did apoptosis fail. Human Fertil (Cambridge) 2004; 7:99-103.
9. Sakkas D, Seli E, Manicardi GC, Nijs M, Ombelet W, Bizzaro D. The presence of abnormal spermatozoa in the ejaculate: did apoptosis fail. Human Fertil (Cambridge) 2004; 7:99-103.
10. Kurosaka K, Takahashi M, Watanabe N, Kobayashi Y. Silent cleanup of very early apoptotic cells by macrophages. J Immunol 2003; 171: 4672-4679.
11. Oehninger S, Morshedi M, Weng S, Taylor S, Duran E, Beebe S. Presence and significance of somatic cell apoptosis markers in human ejaculated spermatozoa. Reprod Biomed Online 2003; 7:469-476.
12. Gosalvez J, Lopez-Fernandez C, Fernandez JL, Gouraud A, Holt WV. Relationships between the dynamics of iatrogenic DNA damage and genomic design in mammalian spermatozoa from eleven species. Mol Reprod Dev 2011; 78:951-961.
13. Kotwicka M, Jendraszak M, Jedrzejczak P. Phosphatidylserine membrane translocation in human spermatozoa: topography in membrane domains and relation to cell vitality. J Membrane Biol 2011; 240:165-170.
14. Martinez-Pastor F, Fernandez-Santos MR, del Olmo E, Dominguez- Rebolledo AE, Esteso MC, Montoro V, Garde JJ. Mitochondrial activity and forward scatter vary in necrotic, apoptotic and membrane-intact spermatozoan subpopulations. Reprod Fertil Dev 2008; 20:547-556.
15. Sakkas D, Mariethoz E, St John JC. Abnormal sperm parameters in humans are indicative of an abortive apoptotic mechanism linked to the Fas-mediated pathway. Exp Cell Res 1999; 251:350-355.
16. Said T, Agarwal A, Grunewald S, Rasch M, Baumann T, Kriegel C, Li L, Glander HJ, Thomas AJ Jr, Paasch U. Selection of nonapoptotic spermatozoa as a new tool for enhancing assisted reproduction outcomes: an in vitro model. Biol Reprod 2006; 74:530-537.
17. Anzar M, He L, Buhr MM, Kroetsch TG, Pauls KP. Sperm apoptosis in fresh and cryopreserved bull semen detected by flow cytometry and its relationship with fertility. Biol Reprod 2002; 66:354-360.
18. Pérez-Pé R, Mendoza N, Casao A, Quintin F, Sevilla E, Lavina A, Cebrián-Pérez JA, Muino-Blanco T. Relationship between apoptosisrelated parameters and in vivo fertility with refrigerated ram semen. Reprod Domest Anim 2010; 45:103-103.
19. Trzcinska M, Bryla M, Smorag Z. Apoptotic-like changes in the spermatozoa of fresh and stored boar semen and the quality of embryos produced in vivo. Anim Reprod Sci 2011; 124:90-97.
20. Muller K, Pomorski T, Muller P, Zachowski A, Herrmann A. Proteindependent translocation of aminophospholipids and asymmetric transbilayer distribution of phospholipids in the plasma membrane of ram sperm cells. Biochemistry 1994; 33:9968-9974.
21. Jha R, Agarwal A, Mahfouz R, Paasch U, Grunewald S, Sabanegh E, Yadav SP, Sharma R. Determination of Poly (ADP-ribose) polymerase (PARP) homologues in human ejaculated sperm and its correlation with sperm maturation. Fertil Steril 2009; 91:782-790.
22. Martin G, Sabido O, Durand P, Levy R. Phosphatidylserine externalization in human sperm induced by calcium ionophore A23187: relationship with apoptosis, membrane scrambling and the acrosome reaction. Hum Reprod 2005; 20:3459-3468.
23. Martí E, Pérez-Pé R, Colás C, Muino-Blanco T, Cebrián-Pérez JA. Study of apoptosis-related markers in ram spermatozoa. Anim Reprod Sci 2008; 106:113-132.
24. Marti E, Perez-Pe R, Muino-Blanco T, Cebrián-Perez JA. Comparative study of four different sperm washing methods using apoptotic markers in ram spermatozoa. J Androl 2006; 27:746-753.
25. Ortega-Ferrusola C, Sotillo-Galan Y, Varela-Fernandez E, Gallardo-Bolanos JM, Muriel A, Gonzalez-Fernandez L, Tapia JA, Pena FJ. Detection of "apoptosis-like" changes during the cryopreservation process in equine sperm. J Androl 2008; 29:213-221.
26. Grunewald S, Baumann T, Paasch U, Glander HJ. Capacitation and acrosome reaction in nonapoptotic human spermatozoa. Ann N Y Acad Sci 2006; 1090:138-146.
27. Martin G, Sabido O, Durand P, Levy R. Cryopreservation induces an apoptosis-like mechanism in bull sperm. Biol Reprod 2004; 71:28-37.
28. Ortega Ferrusola C, Gonzalez Fernandez L, Salazar Sandoval C, Macias Garcia B, Rodriguez Martinez H, Tapia JA, Pena FJ. Inhibition of the mitochondrial permeability transition pore reduces "apoptosis like" changes during cryopreservation of stallion spermatozoa. Theriogenology 2010; 74:458-465.
29. Paasch U, Grunewald S, Dathe S, Glander HJ. Mitochondria of human spermatozoa are preferentially susceptible to apoptosis. Ann N Y Acad Sci 2004; 1030:403-409.
30. Pena FJ, Johannisson A, Wallgren M, Rodriguez-Martinez H. Assessment of fresh and frozen-thawed boar semen using an Annexin-V assay: a new method of evaluating sperm membrane integrity. Theriogenology 2003; 60:677-689.
31. Holt WV. Fundamental aspects of sperm cryobiology: the importance of species and individual differences. Theriogenology 2000; 53:47-58.
32. Del Valle I, Mendoza N, Casao A, Cebrian-Perez JA, Perez-Pe R, Muino-Blanco T. Significance of non-conventional parameters in the evaluation of cooling-induced damage to ram spermatozoa diluted in three different media. Reprod Domest Anim 2010; 45:e260-e268.
33. Holt WV, North RD. Partially irreversible cold-induced lipid phase transitions in mammalian sperm plasma membrane domains: freezefracture study. J Exp Zool 1984; 230:473-483.
34. Leahy T, Gadella BM. Capacitation and capacitation-like sperm surface changes induced by handling boar semen. Reprod Domest Anim 2011; 46: 7-13.
35. Pérez-Pé R, Grasa P, Fernandez-Juan M, Peleato ML, Cebrián-Pérez JA, Muino-Blanco T. Seminal plasma proteins reduce protein tyrosine phosphorylation in the plasma membrane of cold-shocked ram spermatozoa. Mol Reprod Dev 2002; 61:226-233.
36. Maxwell WM, Watson PF. Recent progress in the preservation of ram semen. Anim Reprod Sci 1996; 42:55-65.
37. Rodriguez-Martinez H, Kvist U, Ernerudh J, Sanz L, Calvete JJ. Seminal plasma proteins: what role do they play. Am J Reprod Immunol 2011; 66: 11-22.
38. Caballero I, Parrilla I, Alminana C, del Olmo D, Roca J, Martinez EA, Vazquez JM. Seminal plasma proteins as modulators of the sperm function and their application in sperm biotechnologies. Reprod Domest Anim 2012; 47:12-21.
39. Barrios B, Pérez-Pé R, Gallego M, Tato A, Osada J, Muino-Blanco T, Cebrián-Pérez JA. Seminal plasma proteins revert the cold-shock damage on ram sperm membrane. Biol Reprod 2000; 63:1531-1537.
40. Colas C, Junquera C, Perez-Pe R, Cebrian-Perez JA, Muino-Blanco T. Ultrastructural study of the ability of seminal plasma proteins to protect ram spermatozoa against cold-shock. Microsc Res Tech 2009; 72: 566-572.
41. Maxwell WMC, de Graaf SP, Ghaoui RE-H, Evans G. Seminal plasma effects on sperm handling and female fertility. Soc Reprod Fertil Suppl 2007; 64:13-38.
42. Ollero M, García-López N, Cebrián-Pérez JA, Muino-Blanco T. Surface changes of ram spermatozoa by adsorption of homologous and heterologous seminal plasma proteins revealed by partition in an aqueous two-phase system. Reprod Fertil Dev 1997; 9:381-390.
43. Perez-Pe R, Cebrian-Perez JA, Muino-Blanco T. Semen plasma proteins prevent cold-shock membrane damage to ram spermatozoa. Theriogenology 2001; 56:425-434.
44. Suzuki K, Asano A, Eriksson B, Niwa K, Nagai T, Rodriguez-Martinez H. Capacitation status and in vitro fertility of boar spermatozoa: effects of seminal plasma, cumulus-oocyte-complexes-conditioned medium and hyaluronan. Int J Androl 2002; 25:84-93.
45. Vadnais ML, Roberts KP. Effects of seminal plasma on cooling-induced capacitative changes in boar sperm. J Androl 2007; 28:416-422.
46. Maxwell WMC, Long CR, Johnson LA, Dobrinsky JR, Welch GR. The relationship between membrane status and fertility of boar spermatozoa after flow cytometric sorting in the presence or absence of seminal plasma. Reprod Fertil Dev 1998; 10:433-440.
47. García-López N, Ollero M, Cebrián-Pérez JA, Muino-Blanco T. Reversion of thermic-shock effect on ram spermatozoa by adsorption of seminal plasma proteins revealed by partition in aqueous two-phase systems. J Chrom B 1996; 680:137-143.
48. Maxwell WMC, Evans G, Mortimer ST, Gillan L, Gellatly ES, McPhie CA. Normal fertility in ewes after cervical insemination with frozenthawed spermatozoa supplemented with seminal plasma. Reprod Fertil Dev 1999; 11:123-126.
49. Rozeboom KJ, Troedsson MH, Hodson HH, Shurson GC, Crabo BG. The importance of seminal plasma on the fertility of subsequent artificial inseminations in swine. J Anim Sci 2000; 78:443-448.
50. Alghamdi AS, Foster DN, Troedsson MH. Equine seminal plasma reduces sperm binding to polymorphonuclear neutrophils (PMNs) and improves the fertility of fresh semen inseminated into inflamed uteri. Reproduction 2004; 127:593-600.
51. Perez-Pe R, Muino-Blanco T, Cebrian-Perez JA. Sperm washing method alters the ability of seminal plasma proteins to revert the cold-shock damage on ram sperm membrane. Int J Androl 2001; 24:352-359.
52. Bergeron A, Villemure M, Lazure C, Manjunath P. Isolation and characterization of the major proteins of ram seminal plasma. Mol Reprod Dev 2005; 71:461-470.
53. Jobim MI, Oberst ER, Salbego CG, Wald VB, Horn AP, Mattos RC. BSP A1/A2-like proteins in ram seminal plasma. Theriogenology 2005; 63: 2053-2062.
54. Barrios B, Fernández-Juan M, Muino-Blanco T, Cebrián-Pérez J. Immunocytochemical localization and biochemical characterization of two seminal plasma proteins that protect ram spermatozoa against cold shock. J Androl 2005; 26:539-549.
55. Desnoyers L, Manjunath P. Major proteins of bovine seminal plasma exhibit novel interactions with phospholipid. J Biol Chem 1992; 267: 10149-10155.
56. Ollero M, Muino-Blanco T, López-Pérez MJ, Cebrián-Pérez JA. Viability of ram spermatozoa in relation to the abstinence period and successive ejaculations. Int J Androl 1996; 19:287-292.
57. García-López N, Ollero M, Muino-Blanco T, Cebrian-Perez JA. A dextran swim-up procedure for separation of highly motile and viable ram spermatozoa from seminal plasma. Theriogenology 1996; 46:141-151.
58. Grasa P, Perez-Pe R, Baguena O, Forcada F, Abecia A, Cebrian-Perez JA, Muino-Blanco T. Ram sperm selection by a dextran/swim-up procedure increases fertilization rates following intrauterine insemination in superovulated ewes. J Androl 2004; 25:982-990.
59. Grunewald S, Paasch U, Said TM, Sharma RK, Glander HJ, Agarwal A. Caspase activation in human spermatozoa in response to physiological and pathological stimuli. Fertil Steril 2005b; 83(suppl 1):1106-1112.
60. Wlodkowic D, Skommer J, Darzynkiewicz Z. Flow cytometry-based apoptosis detection. Methods Mol Biol 2009; 559:19-32.
61. Wlodkowic D, Telford W, Skommer J, Darzynkiewicz Z. Apoptosis and beyond: cytometry in studies of programmed cell death. Methods Cell Biol 2011; 103:55-98.
62. Hernandez-Flores G, Ortiz-Lazareno PC, Lerma-Diaz JM, Dominguez-Rodriguez JR, Jave-Suarez LF, Aguilar-Lemarroy Adel C, de Celis-Carrillo R, del Toro-Arreola S, Castellanos-Esparza YC, Bravo-Cuellar A. Pentoxifylline sensitizes human cervical tumor cells to cisplatin-induced apoptosis by suppressing NF-kappa B and decreased cell senescence. BMC Cancer 2011; 11:483.
63. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970; 227:680-685.
64. Harrison RA, Vickers SE. Use of fluorescent probes to assess membrane integrity in mammalian spermatozoa. J Reprod Fertil 1990; 88:343-352.
65. Castedo M, Ferri K, Roumier T, Metivier D, Zamzami N, Kroemer G. Quantitation of mitochondrial alterations associated with apoptosis. J Immunol Methods 2002; 265:39-47.
66. Del Valle I, Gomez-Duran A, Holt WV, Muino-Blanco T, Cebrian-Perez JA. Soy lecithin interferes with mitochondrial function in frozen-thawed ram spermatozoa. J Androl 2012; 33:717-725.
67. Martinez-Pastor F, Aisen E, Fernandez-Santos MR, Esteso MC, Maroto-Morales A, Garcia-Alvarez O, Garde JJ. Reactive oxygen species generators affect quality parameters and apoptosis markers differently in red deer spermatozoa. Reproduction 2009; 137:225-235.
68. Hallap T, Nagy S, Jaakma U, Johannisson A, Rodriguez-Martinez H. Mitochondrial activity of frozen-thawed spermatozoa assessed by MitoTracker Deep Red 633. Theriogenology 2005; 63:2311-2322.
69. Garcia-Alvarez O, Maroto-Morales A, Ramon M, del Olmo E, Montoro V, Dominguez-Rebolledo AE, Bisbal A, Jimenez-Rabadan P, Perez-Guzman MD, Soler AJ. Analysis of selected sperm by density gradient centrifugation might aid in the estimation of in vivo fertility of thawed ram spermatozoa. Theriogenology 2010; 74:979-988.
70. Pena FJ, Saravia F, Johannisson A, Walgren M, Rodriguez-Martinez H. A new and simple method to evaluate early membrane changes in frozenthawed boar spermatozoa. Int J Androl 2005; 28:107-114.
71. Maftah A, Petit JM, Ratinaud MH, Julien R. 10-N nonyl-acridine orange: a fluorescent probe which stains mitochondria independently of their energetic state. Biochem Biophys Res Commun 1989; 164:185-190.
72. Petit JM, Maftah A, Ratinaud MH, Julien R. 10N-nonyl acridine orange interacts with cardiolipin and allows the quantification of this phospholipid in isolated mitochondria. Eur J Biochem 1992; 209:267-273.
73. Petit JM, Huet O, Gallet PF, Maftah A, Ratinaud MH, Julien R. Direct analysis and significance of cardiolipin transverse distribution in mitochondrial inner membranes. Eur J Biochem 1994; 220:871-879.
74. Li X, Darzynkiewicz Z. Labelling DNA strand breaks with BrdUTP. Detection of apoptosis and cell proliferation. Cell Prolif 1995; 28: 571-579.
75. Ward CR, Storey BT. Determination of the time course of capacitation in mouse spermatozoa using a chlortetracycline fluorescence assay. Dev Biol 1984; 104:287-296.
76. Grasa P, Cebrián-Perez JA, Muino-Blanco T. Signal transduction mechanisms involved in in vitro ram sperm capacitation. Reproduction 2006; 132:721-732.
77. Gillan L, Evans G, Maxwell WM. Capacitation status and fertility of fresh and frozen-thawed ram spermatozoa. Reprod Fertil Dev 1997; 9:481-487.
78. Pérez-Pé R, Strom-Holst B, Muino-Blanco T, Soderquist L, Rodriguez-Martinez H. Development of a sperm zona pellucida binding assay for ram semen: preliminary results. In: 14th International Congress on Animal Reproduction, ICAR; July 2-6, 2000; Stockholm, Sweden. Page 80.
79. Wani N, Wani G, Khan M, Salahudin S. Effect of oocyte harvesting techniques on in vitro maturation and in vitro fertilization in sheep. Small Rumin Res 2000; 36:63-67.
80. Tervit HR, Whittingham DG, Rowson LE. Successful culture in vitro of sheep and cattle ova. J Reprod Fertil 1972; 30:493-497.
81. Ivanova M, Mollova M. Zona-penetration in vitro test for evaluating boar sperm fertility. Theriogenology 1993; 40:397-410.
82. Marti E, Perez-Pe R, Colas C, Muino-Blanco T, Cebrian-Perez JA. Study of apoptosis-related markers in ram spermatozoa. Anim Reprod Sci 2008; 106:113-132.
83. K Lee J, Richburg JH, Younkin SC, Boekelheide K. The Fas system is a key regulator of germ cell apoptosis in the testis. Endocrinology 1997; 138:2081-2088.
84. Krebs JJR, Hauser H, Carafoli E. Asymmetric distribution of phospholipids in the inner membrane of beef-heart mitochondria. J Biol Chem 1979; 254:5308-5316.
85. Kijas JW, Menzies M, Ingham A. Sequence diversity and rates of molecular evolution between sheep and cattle genes. Anim Genet 2005; 37:171-174.
86. El-Hajj Ghaoui R, Thomson PC, Leahy T, Evans G, Maxwell WM. Autologous whole ram seminal plasma and its vesicle-free fraction improve motility characteristics and membrane status but not in vivo fertility of frozen-thawed ram spermatozoa. Reprod Domest Anim 2007; 42:541-549.
87. Heise A, Kahn W, Volkmann DH, Thompson PN, Gerber D. Influence of seminal plasma on fertility of fresh and frozen-thawed stallion epididymal spermatozoa. Anim Reprod Sci 2010; 118:48-53.
88. Gupta A, Kattal N, Paasch U, Sharma R, Grunewald S, Glander HJ, Agarwal A. Co-existence of mitochondrial and membrane receptor mediated apoptosis machinery in the ejaculated human spermatozoa. In: 28th Annual Meeting of the American Society of Andrology; March 29-April 1, 2003; Phoenix, AZ. Page 32.
89. Twigg J, Irvine DS, Houston P, Fulton N, Michael L, Aitken RJ. Iatrogenic DNA damage induced in human spermatozoa during sperm preparation: protective significance of seminal plasma. Mol Human Reprod 1998; 4:439-445.
90. Muino-Blanco T, Perez-Pe R, Cebrian-Perez JA. Seminal plasma proteins and sperm resistance to stress. Reprod Domest Anim 2008; 43(suppl 4): 18-31.
91. Oehninger S, Mahony M, Ozgur K, Kolm P, Kruger T, Franken D. Clinical significance of human sperm-zona pellucida binding. Fertil Steril 1997; 67:1121-1127.
92. Larsson B, Rodriguez-Martinez H. Can we use in vitro fertilization tests to predict semen fertility. Anim Reprod Sci 2000; 60:327-336.
93. Manjunath P. Gonadotropin-release stimulatory and inhibitory proteins in bull seminal plasma. J Steroid Biochem Mol Biol 1984; 20:1585-1585.
94. Desnoyers L, Manjunath P. Major proteins of bovine seminal plasma exhibit novel interactions with phospholipid. J Biol Chem 1992; 267: 10149-10155.
95. Manjunath P, Therien I. Role of seminal plasma phospholipid-binding proteins in sperm membrane lipid modification that occurs during capacitation. J Reprod Immunol 2002; 53:109-119.
96. Therien I, Bousquet D, Manjunath P. Effect of seminal phospholipidbinding proteins and follicular fluid on bovine sperm capacitation. Biol Reprod 2001; 65:41-51.