Autophagy and apoptosis have a role in the survival or death of stallion spermatozoa during conservation in refrigeration

PLoS ONE

Volumn 7, Issue 1, 2012, Pages

  Bolaños, Juan M Gallardo ^a   Morán, Álvaro Miró ^a   da Silva, Carolina M Balao ^a   Rodríguez, Antolín Morillo ^a   Dávila, María Plaza ^a   Aparicio, Inés M ^a   Tapia, José A ^a   Ferrusola, Cristina Ortega ^a   Peña, Fernando J ^a  

^a UNIVERSITY OF EXTREMADURA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; CASPASE 7; PHOSPHATIDYLSERINE; TUMOR NECROSIS FACTOR; TUMOR NECROSIS FACTOR RECEPTOR 1; TUMOR NECROSIS FACTOR RECEPTOR 2;

ANIMAL CELL; APOPTOSIS; ARTICLE; AUTOPHAGY; CELL MEMBRANE; CELL MEMBRANE PERMEABILITY; CELL SURVIVAL; CENTRIFUGATION; CONTROLLED STUDY; CRYOPRESERVATION; EJACULATION; ENZYME ACTIVITY; FLOW CYTOMETRY; FREEZING; LIPID PEROXIDATION; MALE; MALE GENITAL TRACT PARAMETERS; MITOCHONDRIAL MEMBRANE POTENTIAL; NONHUMAN; PHOSPHOLIPID TRANSFER; SEMEN ANALYSIS; SPERM PRESERVATION; SPERM QUALITY; SPERMATOZOON MOTILITY; STALLION; WESTERN BLOTTING;

EID: 84856266647     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0030688     Document Type: Article

References (61)

1. Rigby SL, Brinsko SP, Cochran M, Blanchard TL, Love CC, et al. (2001) Advances in cooled semen technologies: seminal plasma and semen extender. Anim Reprod Sci 68: 171-180.
2. Moran DM, Jasko DJ, Squires EL, Amann RP, (1992) Determination of temperature and cooling rate which induce cold shock in stallion spermatozoa. Theriogenology 38: 999-1012.
3. Chantler E, Abraham-Peskir JV, Little S, McCann C, Medenwaldt R, (2000) Effect of cooling on the motility and function of human spermatozoa. Cryobiology 41: 125-134.
4. Drobnis EZ, Crowe LM, Berger T, Anchordoguy TJ, Overstreet JW, et al. (1993) Cold shock damage is due to lipid phase transitions in cell membranes: a demonstration using sperm as a model. J Exp Zool 265: 432-437.
5. White IG, (1993) Lipids and calcium uptake of sperm in relation to cold shock and preservation: a review. Reprod Fertil Develop 5: 639-658.
6. Windsor DP, White IG, Selley ML, Swan MA, (1993) Effects of the lipid peroxidation product (E)-4-hydroxy-2-nonenal on ram sperm function. J Reprod Fertil 99: 359-366.
7. Moran JM, Madejon L, Ortega Ferrusola C, Peña FJ, (2008) Nitric oxide induces caspase activity in boar spermatozoa. Theriogenology 70: 91-96.
8. Purdy PH, Tharp N, Stewart T, Spiller SF, Blackburn HD, (2010) Implications of the pH and temperature of diluted, cooled boar semen on fresh and frozen-thawed sperm motility characteristics. Theriogenology 74: 1304-1310.
9. Halangk W, Bohnensack R, Kunz W, (1980) [Relation between intactness and adenine nucleotide pattern of ejaculated bull spermatozoa]. Acta biologica et medica Germanica 39: 791-808.
10. Ortega-Ferrusola C, Gonzalez-Fernandez L, Muriel A, Macias-Garcia B, Rodriguez-Martinez H, et al. (2009) Does the microbial flora in the ejaculate affect the freezeability of stallion sperm? Reprod Domest Anim 44: 518-522.
11. 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. Bioch J 436: 687-698.
12. 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.
13. Holt WV, (2011) Does apoptosis hold the key to long-term sperm storage mechanisms in vivo? Mol Reprod Develop 78: 464-465.
14. Barth S, Glick D, Macleod KF, (2010) Autophagy: assays and artifacts. J Pathol 221: 117-124.
15. Glick D, Barth S, Macleod KF, (2010) Autophagy: cellular and molecular mechanisms. J Pathol 221: 3-12.
16. Ortega-Ferrusola C, Sotillo-Galan Y, Varela-Fernandez E, Gallardo-Bolanos JM, Muriel A, et al. (2008) Detection of "apoptosis-like" changes during the cryopreservation process in equine sperm. J Androl 29: 213-221.
17. Ortega Ferrusola C, Gonzalez Fernandez L, Morrell JM, Salazar Sandoval C, Macias Garcia B, et al. (2009) 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.
18. Said TM, Gaglani A, Agarwal A, (2010) Implication of apoptosis in sperm cryoinjury. Reprod Biomed Online 21: 456-462.
19. Martin G, Sabido O, Durand P, Levy R, (2004) Cryopreservation induces an apoptosis-like mechanism in bull sperm. Biol Reprod 71: 28-37.
20. Johannisson A, Morrell JM, Thoren J, Jonsson M, Dalin AM, et al. (2009) Colloidal centrifugation with Androcoll-E prolongs stallion sperm motility, viability and chromatin integrity. Anim Reprod Sci 116: 119-128.
21. Macias Garcia B, Gonzalez Fernandez L, Morrell JM, Ortega Ferrusola C, Tapia JA, et al. (2009) Single-layer centrifugation through colloid positively modifies the sperm subpopulation structure of frozen-thawed stallion spermatozoa. Reprod Domest Anim 44: 523-526.
22. Morrell JM, Rodriguez-Martinez H, Johannisson A, (2010) Single layer centrifugation of stallion spermatozoa consistently selects the most robust spermatozoa from the rest of the ejaculate in a large sample size. Equine Veterinary Journal 42: 579-585.
23. Macias Garcia B, Morrell JM, Ortega-Ferrusola C, Gonzalez-Fernandez L, Tapia JA, et al. (2009) Centrifugation on a single layer of colloid selects improved quality spermatozoa from frozen-thawed stallion semen. Anim Reprod Sci 114: 193-202.
24. Nuñez-Martinez I, Moran JM, Peña FJ, (2007) Sperm indexes obtained using computer-assisted morphometry provide a forecast of the freezability of canine sperm. Int J Androl 30: 182-189.
25. Peña FJ, Saravia F, Johannisson A, Walgren M, Rodriguez-Martinez H, (2005) A new and simple method to evaluate early membrane changes in frozen-thawed boar spermatozoa. Int J Androl 28: 107-114.
26. Peña 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.
27. Grunewald S, Sharma R, Paasch U, Glander HJ, Agarwal A, (2009) Impact of caspase activation in human spermatozoa. Micro Res Tech 72: 878-888.
28. Balao da Silva CM, Macias-Garcia B, Miro-Moran A, Gonzalez-Fernandez L, Morillo-Rodriguez A, et al. (2011) Melatonin reduces lipid peroxidation and apoptotic-like changes in stallion spermatozoa. J Pineal Res 51: 172-179.
29. Ortega Ferrusola C, Gonzalez Fernandez L, Macias Garcia B, Salazar-Sandoval C, Morillo Rodriguez A, et al. (2009) Effect of cryopreservation on nitric oxide production by stallion spermatozoa. Biol Reprod 81: 1106-1111.
30. Peña FJ, Johannisson A, Wallgren M, Rodriguez Martinez H, (2003) Antioxidant supplementation in vitro improves boar sperm motility and mitochondrial membrane potential after cryopreservation of different fractions of the ejaculate. Anim Reprod Sci 78: 85-98.
31. Petrunkina AM, Waberski D, Bollwein H, Sieme H, (2010) Identifying non-sperm particles during flow cytometric physiological assessment: a simple approach. Theriogenology 73: 995-1000.
32. Gonzalez-Fernandez L, Ortega-Ferrusola C, Macias-Garcia B, Salido GM, Peña FJ, et al. (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.
33. Ortega Ferrusola C, Gonzalez Fernandez L, Macias Garcia B, Salazar-Sandoval C, Morillo Rodriguez A, et al. (2009) Effect of cryopreservation on nitric oxide production by stallion spermatozoa. Biol Reprod 81: 1106-1111.
34. Chen Y, Klionsky DJ, (2011) The regulation of autophagy- unanswered questions. J Cell Sci 124: 161-170.
35. Yang Z, Klionsky DJ, (2010) Eaten alive: a history of macroautophagy. Nature cell biology 12: 814-822.
36. Sakkas D, Seli E, Bizzaro D, Tarozzi N, Manicardi GC, (2003) Abnormal spermatozoa in the ejaculate: abortive apoptosis and faulty nuclear remodelling during spermatogenesis. Reprod Biomed online 7: 428-432.
37. Yu L, Strandberg L, Lenardo MJ, (2008) The selectivity of autophagy and its role in cell death and survival. Autophagy 4: 567-573.
38. Yu L, Alva A, Su H, Dutt P, Freundt E, et al. (2004) Regulation of an ATG7-beclin 1 program of autophagic cell death by caspase-8. Science 304: 1500-1502.
39. Yu L, Lenardo MJ, Baehrecke EH, (2004) Autophagy and caspases: a new cell death program. Cell cycle 3: 1124-1126.
40. Ortega-Ferrusola C, Garcia BM, Gallardo-Bolanos JM, Gonzalez-Fernandez L, Rodriguez-Martinez H, et al. (2009) Apoptotic markers can be used to forecast the freezeability of stallion spermatozoa. Anim Reprod Sci 114: 393-403.
41. 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.
42. Aitken RJ, Findlay JK, Hutt KJ, Kerr JB, (2011) Apoptosis in the germ line. Reproduction 141: 139-150.
43. Earnshaw WC, Martins LM, Kaufmann SH, (1999) Mammalian caspases: structure, activation, substrates, and functions during apoptosis. Ann Rev Bioch 68: 383-424.
44. Peña FJ, Rodriguez Martinez H, Tapia JA, Ortega Ferrusola C, Gonzalez Fernandez L, et al. (2009) Mitochondria in mammalian sperm physiology and pathology: a review. Reprod Dom Anim 44: 345-349.
45. Peña FJ, Nunez-Martinez I, Moran JM, (2006) Semen technologies in dog breeding: an update. Reprod Dom Anim 41 (Suppl 2): 21-29.
46. Chekeni FB, Elliott MR, Sandilos JK, Walk SF, Kinchen JM, et al. (2010) Pannexin 1 channels mediate 'find-me' signal release and membrane permeability during apoptosis. Nature 467: 863-867.
47. Peña FJ, Saravia F, Johannisson A, Walgren M, Rodriguez-Martinez H, (2005) A new and simple method to evaluate early membrane changes in frozen-thawed boar spermatozoa. Int J Androl 28: 107-114.
48. Elliott MR, Chekeni FB, Trampont PC, Lazarowski ER, Kadl A, et al. (2009) Nucleotides released by apoptotic cells act as a find-me signal to promote phagocytic clearance. Nature 461: 282-286.
49. Anzar M, He L, Buhr MM, Kroetsch TG, Pauls KP, (2002) Sperm apoptosis in fresh and cryopreserved bull semen detected by flow cytometry and its relationship with fertility. Biol Reprod 66: 354-360.
50. Idziorek T, Estaquier J, De Bels F, Ameisen JC, (1995) YOPRO-1 permits cytofluorometric analysis of programmed cell death (apoptosis) without interfering with cell viability. J Immunol Meth 185: 249-258.
51. Martin G, Sabido O, Durand P, Levy R, (2004) Cryopreservation induces an apoptosis-like mechanism in bull sperm. Biol Reprod 71: 28-37.
52. Peña FJ, Saravia F, Johannisson A, Wallgren M, Rodriguez-Martinez H, (2007) Detection of early changes in sperm membrane integrity pre-freezing can estimate post-thaw quality of boar spermatozoa. Anim Reprod Sci 97: 74-83.
53. Martin G, Cagnon N, Sabido O, Sion B, Grizard G, et al. (2007) Kinetics of occurrence of some features of apoptosis during the cryopreservation process of bovine spermatozoa. Hum Reprod 22: 380-388.
54. Aitken RJ, Koppers AJ, (2011) Apoptosis and DNA damage in human spermatozoa. Asian J Androl 13: 36-42.
55. Li MO, Sarkisian MR, Mehal WZ, Rakic P, Flavell RA, (2003) Phosphatidylserine receptor is required for clearance of apoptotic cells. Science 302: 1560-1563.
56. Martinez IN, Moran JM, Peña FJ, (2006) Two-step cluster procedure after principal component analysis identifies sperm subpopulations in canine ejaculates and its relation to cryoresistance. J Androl 27: 596-603.
57. Ortega-Ferrusola C, Macias Garcia B, Suarez Rama V, Gallardo-Bolanos JM, Gonzalez-Fernandez L, et al. (2009) Identification of sperm subpopulations in stallion ejaculates: changes after cryopreservation and comparison with traditional statistics. Reprod Dom Anim 44: 419-423.
58. Paasch U, Sharma RK, Gupta AK, Grunewald S, Mascha EJ, et al. (2004) Cryopreservation and thawing is associated with varying extent of activation of apoptotic machinery in subsets of ejaculated human spermatozoa. Biol Reprod 71: 1828-1837.
59. Paasch U, Grunewald S, Agarwal A, Glandera HJ, (2004) Activation pattern of caspases in human spermatozoa. Fertil Steril 81 (Suppl 1): 802-809.
60. Zhang DW, Shao J, Lin J, Zhang N, Lu BJ, et al. (2009) RIP3, an energy metabolism regulator that switches TNF-induced cell death from apoptosis to necrosis. Science 325: 332-336.
61. Peter AT, Linde-Forsberg C, (2003) Efficacy of the anticaspase agent zVAD-fmk on post-thaw viability of canine spermatozoa. Theriogenology 59: 1525-1532.