Melatonin prevents capacitation and apoptotic-like changes of ram spermatozoa and increases fertility rate

Journal of Pineal Research

Volumn 48, Issue 1, 2010, Pages 39-46

  Casao, Adriana ^a   Mendoza, Noelia ^a   Pérez Pé, Rosaura ^a   Grasa, Patricia ^a   Abecia, José Alfonso ^a   Forcada, Fernando ^a   Cebrián Pérez, José A ^a   Muino Blanco, Teresa ^a  

^a UNIVERSITY OF ZARAGOZA   (Spain)

Author keywords

Capacitation; IVF; Melatonin; Phosphatidylserine translocation; Ram spermatozoa

Indexed keywords

ANTIOXIDANT; MELATONIN; PHOSPHATIDYLSERINE; REACTIVE OXYGEN METABOLITE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CONTROLLED STUDY; FERTILIZATION IN VITRO; MALE; MALE FERTILITY; NONHUMAN; OOCYTE CLEAVAGE; RAM (SHEEP); SEMINAL PLASMA; SPERM PRESERVATION; SPERMATOZOON CAPACITATION; SPERMATOZOON MOTILITY;

ANIMALS; BIRTH RATE; FEMALE; FERTILITY; FERTILIZATION; MALE; MELATONIN; SHEEP; SPERM CAPACITATION; SPERMATOZOA;

EID: 71549139176     PISSN: 07423098     EISSN: 1600079X     Source Type: Journal    
DOI: 10.1111/j.1600-079X.2009.00722.x     Document Type: Article

References (69)

1. Bittman E, Karsch F, Hopkins J. Role of the pineal gland in ovine photoperiodism: regulation of seasonal breeding and negative feedback effects of estradiol upon luteinizing hormone secretion. Endocrinology 1983 113 : 329 336.
2. Langford GA, Ainsworth L, Marcus GJ et al. Photoperiod entrainment of testosterone, luteinizing hormone, follicle-stimulating hormone, and prolactin cycles in rams in relation to testis size and semen quality. Biol Reprod 1987 37 : 489 499.
3. Lincoln GA, Lincoln CE, Mcneilly AS. Seasonal cycles in the blood plasma concentration of FSH, inhibin and testosterone, and testicular size in rams of wild, feral and domesticated breeds of sheep. J Reprod Fertil 1990 88 : 623 633.
4. Schanbacher BD, Lunstra DD. Seasonal changes in sexual activity and serum levels of LH and testosterone in Finish Landrace and Suffolk rams. J Anim Sci 1976 43 : 644 650.
5. Avdi M, Banos G, Stefos K et al. Seasonal variation in testicular volume and sexual behavior of Chios and Serres rams. Theriogenology 2004 62 : 275 282.
6. D'occhio MJ, Schanbacher BD, Kinder JE. Profiles of luteinizing hormone, follicle-stimulating hormone, testosterone and prolactin in rams of diverse breeds: effects of contrasting short (8L:16D) and long (16L:8D) photoperiods. Biol Reprod 1984 30 : 1039 1054.
7. Mandiki SNM, Derycke G, Bister JL et al. Influence of season and age on sexual maturation parameters of Texel, Suffolk and Ile-de-France rams: 1. Testicular size, semen quality and reproductive capacity. Small Rumin Res 1998 28 : 67 79.
8. Haresign W. Manipulation of reproduction in sheep. J Reprod Fertil Suppl 1992 45 : 127 139.
9. Chemineau P, Malpaux B, Delgadillo JA et al. Control of sheep and goat reproduction: Use of light and melatonin. Anim Reprod Sci 1992 30 : 157 184.
10. Zúñiga O, Forcada F, Abecia JA. The effect of melatonin implants on the response to the male effect and on the subsequent cyclicity of Rasa Aragonesa ewes implanted in April. Anim Reprod Sci 2002 72 : 165 174.
11. Webster JR, Suttie JM, Veenvliet BA et al. Effect of melatonin implants on secretion of luteinizing hormone in intact and castrated rams. J Reprod Fertil 1991 92 : 21 31.
12. Kaya A, Baspinar N, Yildiz C et al. Influence of melatonin implantation on sperm quality, biochemical composition of the seminal plasma and plasma testosterone levels in rams. Rev Med Vet 2000 151 : 1143 1146.
13. Coyan K, Kaya A, Karaca F et al. The effect of melatonin on sperm quality and testicular size of normospermic and pathospermic rams in the anoestrous season. Wien Tierarztl Monatsschr 1998 85 : 383 388.
14. Rosa HJ, Juniper DT, Bryant MJ. Effects of recent sexual experience and melatonin treatment of rams on plasma testosterone concentration, sexual behaviour and ability to induce ovulation in seasonally anoestrous ewes. J Reprod Fertil 2000 120 : 169 176.
15. Lincoln GA, Ebling FJ. Effect of constant-release implants of melatonin on seasonal cycles in reproduction, prolactin secretion and moulting in rams. J Reprod Fertil 1985 73 : 241 253.
16. Forcada F, Abecia JA, Sierra I. Seasonal changes in oestrus activity and ovulation rate in Rasa Aragonesa ewes maintained at two different body condition levels. Small Rumin Res 1992 8 : 313 324.
17. Palacín I, Abecia JA, Forcada F et al. Effect of exogenous melatonin treatment on out of season ram fertility. Ital J Anim Sci 2008 7 : 199 206.
18. Casao A, Vega S, Palacín I et al. Effects of melatonin implants during non-breeding season on sperm motility and reproductive parameters in Rasa aragonesa rams. Reprod Domest Anim 2009 in press. Doi :.
19. Lincoln GA, Clarke IJ. Refractoriness to a static melatonin signal develops in the pituitary gland for the control of prolactin secretion in the ram. Biol Reprod 1997 57 : 460 467.
20. Shiu SY, Li L, Siu SW et al. Biological basis and possible physiological implications of melatonin receptor-mediated signaling in the rat epididymis. Biol Signals Recept 2000 9 : 172 187.
21. Van Vuuren RJ, Pitout MJ, Van Aswegen CH et al. Putative melatonin receptor in human spermatozoa. Clin Biochem 1992 25 : 125 127.
22. Luboshitzky R, Shen-Orr Z, Herer P. Seminal plasma melatonin and gonadal steroids concentrations in normal men. Arch Androl 2002 48 : 225 232.
23. Misztal T, Romanowicz K, Barcikowski B. Melatonin - a modulator of the GnRH/LH axis in sheep. Reprod Biol 2002 2 : 267 275.
24. Yeung CH, Weinbauer GF, Cooper TG. Effect of acute androgen withdrawal by GnRH antagonist on epididymal sperm motility and morphology in the cynomolgus monkey. J Androl 1999 20 : 72 79.
25. Bastias MC, Kamijo H, Pavlou SN. Sperm motion parameters after suppression of spermatogenesis with a gonadotropin-releasing hormone antagonist plus testosterone supplementation. Fertil Steril 1993 59 : 1261 1265.
26. Fujinoki M. Melatonin-enhanced hyperactivation of hamster sperm. Reproduction 2008 136 : 533 541.
27. Casao A, Luna C, Serrano E et al. Quantification of melatonin and oxidized proteins and lipids in ram semen in breeding and non-breeding season. In : XIII Jornadas sobre Producción Animal, AIDA. Aida eds., AIDA, Zaragoza, Spain, 2009 pp. 723 725.
28. Sheikheldin MA, Howland BE, Palmer WM. Seasonal profiles of melatonin in adult rams. J Pineal Res 1992 12 : 58 63.
29. Ronnberg L, Kauppila A, Leppaluoto J et al. Circadian and seasonal variation in human preovulatory follicular fluid melatonin concentration. J Clin Endocrinol Metab 1990 71 : 492 496.
30. Tamura H, Takasaki A, Miwa I et al. Oxidative stress impairs oocyte quality and melatonin protects oocytes from free radical damage and improves fertilization rate. J Pineal Res 2008 44 : 280 287.
31. Tricoire H, Locatelli A, Chemineau P et al. Melatonin enters the cerebrospinal fluid through the pineal recess. Endocrinology 2002 143 : 84 90.
32. Tan D, Manchester LC, Reiter RJ et al. High physiological levels of melatonin in the bile of mammals. Life Sci 1999 65 : 2523 2529.
33. Tan D-X, Manchester LC, Reiter RJ et al. Identification of highly elevated levels of melatonin in bone marrow: its origin and significance. Biochim Biophys Acta 1999 1472 : 206 214.
34. Karagiannidis A, Varsakeli S, Alexopoulos C et al. Seasonal variation in semen characteristics of Chios and Friesian rams in Greece. Small Rumin Res 2000 37 : 125 130.
35. Ollero M, Muino-Blanco T, Lopez-Perez MJ et al. Viability of ram spermatozoa in relation to the abstinence period and successive ejaculations. Int J Androl 1996 19 : 287 292.
36. Ishizuka B, Kuribayashi Y, Murai K et al. The effect of melatonin on in vitro fertilization and embryo development in mice. J Pineal Res 2000 28 : 48 51.
37. Verstegen J, Iguer-Ouada M, Onclin K. Computer assisted semen analyzers in andrology research and veterinary practice. Theriogenology 2002 57 : 149 179.
38. Harrison RA, Vickers SE. Use of fluorescent probes to assess membrane integrity in mammalian spermatozoa. J Reprod Fertil 1990 88 : 343 352.
39. Grasa P, Cebrian-Perez JA, Muino-Blanco T. Signal transduction mechanisms involved in in vitro ram sperm capacitation. Reproduction 2006 132 : 721 732.
40. Gillan L, Evans G, Maxwell WM. Capacitation status and fertility of fresh and frozen-thawed ram spermatozoa. Reprod Fertil Dev 1997 9 : 481 487.
41. Marti E, Perez-Pe R, Colas C et al. Study of apoptosis-related markers in ram spermatozoa. Anim Reprod Sci 2008 106 : 113 132.
42. Wani NA, Wani GM, Khan MZ et al. Effect of different factors on the recovery rate of oocytes for in vitro maturation and in vitro fertilization procedures in sheep. Small Rumin Res 1999 34 : 71 76.
43. Wani NA, Wani GM, Khan MZ et al. Effect of oocyte harvesting techniques on in vitro maturation and in vitro fertilization in sheep. Small Rumin Res 2000 36 : 63 67.
44. Tervit HR, Whittingham DG. Succesful culture in vitro of sheep and cattle ova. J Reprod Fertil 1972 30 : 493 497.
45. Brzezinski A, Seibel MM, Lynch HJ et al. Melatonin in human preovulatory follicular fluid. J Clin Endocrinol Metab 1987 64 : 865 867.
46. Kokolis N, Theodosiadou E, Tsantarliotou M et al. The effect of melatonin implants on blood testosterone and acrosin activity in spermatozoa of the ram. Andrologia 2000 32 : 107 114.
47. Tsantarliotou MP, Kokolis NA, Smokovitis A. Melatonin administration increased plasminogen activator activity in ram spermatozoa. Theriogenology 2008 69 : 458 465.
48. Liu Y-X. Involvement of plasminogen activator and plasminogen activator inhibitor type 1 in spermatogenesis, sperm capacitation, and fertilization. Semin Thromb Hemost 2007 33 : 029 040.
49. Tan DX, Chen LD, Poeggeler B et al. Melatonin: a potent, endogenous hydroxyl radical scavenger. Endocr J 1993 1 : 57 60.
50. Peyrot F, Ducrocq C. Potential role of tryptophan derivatives in stress responses characterized by the generation of reactive oxygen and nitrogen species. J Pineal Res 2008 45 : 235 246.
51. Cervantes M, Morali G, Letechipia-Vallejo G. Melatonin and ischemia-reperfusion injury of the brain. J Pineal Res 2008 45 : 1 7.
52. Manda K, Ueno M, Anzai K. Melatonin mitigates oxidative damage and apoptosis in mouse cerebellum induced by high-LET 56Fe particle irradiation. J Pineal Res 2008 44 : 189 196.
53. De Lamirande E, Gagnon C. Human sperm hyperactivation and capacitation as parts of an oxidative process. Free Radic Biol Med 1993 14 : 157 166.
54. Drevet JR. The antioxidant glutathione peroxidase family and spermatozoa: A complex story. Mol Cell Endocrinol 2006 250 : 70 79.
55. Benitez-King G, Huerto-Delgadillo L, Anton-Tay F. Binding of 3H-melatonin to calmodulin. Life Sci 1993 53 : 201 207.
56. Pozo D, Reiter RJ, Calvo JR et al. Inhibition of cerebellar nitric oxide synthase and cyclic GMP production by melatonin via complex formation with calmodulin. J Cell Biochem 1997 65 : 430 442.
57. Si Y, Olds-Clarke P. Evidence for the involvement of calmodulin in mouse sperm capacitation. Biol Reprod 2000 62 : 1231 1239.
58. Bendahmane M, Lynch C, Tulsiani DRP. Calmodulin signals capacitation and triggers the agonist-induced acrosome reaction in mouse spermatozoa. Arch Biochem Biophys 2001 390 : 1 8.
59. Tulsiani DR, Zeng HT, Abou-Haila A. Biology of sperm capacitation: evidence for multiple signalling pathways. Soc Reprod Fertil Suppl 2007 63 : 257 272.
60. Sainz RM, Mayo JC, Rodriguez C et al. Melatonin and cell death: differential actions on apoptosis in normal and cancer cells. Cell Mol Life Sci 2003 60 : 1407 1426.
61. Jou MJ, Peng TI, Yu PZ et al. Melatonin protects against common deletion of mitochondrial DNA-augmented mitochondrial oxidative stress and apoptosis. J Pineal Res 2007 43 : 389 403.
62. Guneli E, Tugyan K, Ozturk H et al. Effect of melatonin on testicular damage in streptozotocin-induced diabetes rats. Eur Surg Res 2008 40 : 354 360.
63. Huang F, Ning H, Xin Q-Q et al. Melatonin pretreatment attenuates 2-bromopropane-induced testicular toxicity in rats. Toxicology 2009 256 : 75 82.
64. Chandra J, Samali A, Orrenius S. Triggering and modulation of apoptosis by oxidative stress. Free Radic Biol Med 2000 29 : 323 333.
65. Choi J, Park SM, Lee E et al. Anti-apoptotic effect of melatonin on preimplantation development of porcine parthenogenetic embryos. Mol Reprod Dev 2008 75 : 1127 1135.
66. Reiter RJ, Tan DX, Osuna C et al. Actions of melatonin in the reduction of oxidative stress - a review. J Biomed Sci 2000 7 : 444 458.
67. Rao MV, Gangadharan B. Antioxidative potential of melatonin against mercury induced intoxication in spermatozoa in vitro. Toxicol Vitro 2008 22 : 935 942.
68. Radogna F, Paternoster L, Albertini MC et al. Melatonin antagonizes apoptosis via receptor interaction in U937 monocytic cells. J Pineal Res 2007 43 : 154 162.
69. Dubocovich ML, Markowska M. Functional MT1 and MT2 melatonin receptors in mammals. Endocrine 2005 27 : 101 110.