The endothelial nitric oxide synthase/nitric oxide system is involved in the defective quality of bovine oocytes from low mid-antral follicle count ovaries

Journal of Animal Science

Volumn 89, Issue 8, 2011, Pages 2389-2396

  Tessaro, I ^a   Luciano, A M ^a   Franciosi, F ^a   Lodde, V ^a   Corbani, D ^a   Modina, S C ^a  

^a UNIVERSITY OF MILAN   (Italy)

Author keywords

Cow; Endothelial nitric oxide synthase; Medium antral follicle; Oocyte developmental competence; Vasculature

Indexed keywords

ENDOTHELIAL NITRIC OXIDE SYNTHASE; LECTIN; N ACETYL S NITROSOPENICILLAMINE; NITRIC OXIDE;

ANIMAL; ANIMAL DISEASE; ARTICLE; CATTLE; DRUG EFFECT; EMBRYO CULTURE; FEMALE; FERTILIZATION IN VITRO; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; OOCYTE; OVARY FOLLICLE; PHYSIOLOGY; PROTEIN BINDING; PROTEIN TRANSPORT;

ANIMALS; CATTLE; EMBRYO CULTURE TECHNIQUES; FEMALE; FERTILIZATION IN VITRO; GENE EXPRESSION REGULATION, ENZYMOLOGIC; LECTINS; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE III; OOCYTES; OVARIAN FOLLICLE; PROTEIN BINDING; PROTEIN TRANSPORT; S-NITROSO-N-ACETYLPENICILLAMINE;

BOVINAE;

EID: 80052601608     PISSN: 00218812     EISSN: 15253163     Source Type: Journal    
DOI: 10.2527/jas.2010-3714     Document Type: Article

References (48)

1. Abramoff, M. D., P. J. Magelhaes, and S. J. Ram. 2004. Image processing with ImageJ. Biophotonics International 11:36-42.
2. Alviggi, C., P. Humaidan, C. M. Howles, D. Tredway, and S. G. Hillier. 2009. Biological versus chronological ovarian age: Implications for assisted reproductive technology. Reprod. Biol. Endocrinol. 7:101.
3. Basini, G., M. Baratta, N. Ponderato, S. Bussolati, and C. Tamanini. 1998. Is nitric oxide an autocrine modulator of bovine granulosa cell function? Reprod. Fertil. Dev. 10:471-478.
4. Bilodeau-Goeseels, S. 2007. Effects of manipulating the nitric oxide/cyclic GMP pathway on bovine oocyte meiotic resumption in vitro. Theriogenology 68:693-701.
5. Borini, A., A. Maccolini, A. Tallarini, M. A. Bonu, R. Sciajno, and C. Flamigni. 2001. Perifollicular vascularity and its relationship with oocyte maturity and IVF outcome. Ann. N. Y. Acad. Sci. 943:64-67.
6. Bu, S., G. Xia, Y. Tao, L. Lei, and B. Zhou. 2003. Dual effects of nitric oxide on meiotic maturation of mouse cumulus cell-enclosed oocytes in vitro. Mol. Cell. Endocrinol. 207:21-30.
7. Bu, S., H. Xie, Y. Tao, J. Wang, and G. Xia. 2004. Nitric oxide influences the maturation of cumulus cell-enclosed mouse oocytes cultured in spontaneous maturation medium and hypoxanthinesupplemented medium through different signaling pathways. Mol. Cell. Endocrinol. 223:85-93.
8. Coccia, M. E., and F. Rizzello. 2008. Ovarian reserve. Ann. N. Y. Acad. Sci. 1127:27-30.
9. Cushman, R. A., M. F. Allan, L. A. Kuehn, W. M. Snelling, A. S. Cupp, and H. C. Freetly. 2009. Evaluation of antral follicle count and ovarian morphology in crossbred beef cows: Investigation of influence of stage of the estrous cycle, age, and birth weight. J. Anim. Sci. 87:1971-1980.
10. Erickson, B. H., R. A. Reynolds, and R. L. Murphree. 1976. Ovarian characteristics and reproductive performance of the aged cow. Biol. Reprod. 15:555-560.
11. Gandolfi, F., A. M. Luciano, S. Modina, A. Ponzini, P. Pocar, D. T. Armstrong, and A. Lauria. 1997. The in vitro developmental competence of bovine oocytes can be related to the morphology of the ovary. Theriogenology 48:1153-1160.
12. Goud, A. P., P. T. Goud, M. P. Diamond, and H. M. Abu-Soud. 2005. Nitric oxide delays oocyte aging. Biochemistry 44:11361-11368.
13. Grazul-Bilska, A. T., C. Navanukraw, M. L. Johnson, D. A. Arnold, L. P. Reynolds, and D. A. Redmer. 2006. Expression of endothelial nitric oxide synthase in the ovine ovary throughout the estrous cycle. Reproduction 132:579-587.
14. Grazul-Bilska, A. T., C. Navanukraw, M. L. Johnson, K. A. Vonnahme, S. P. Ford, L. P. Reynolds, and D. A. Redmer. 2007. Vascularity and expression of angiogenic factors in bovine dominant follicles of the first follicular wave. J. Anim. Sci. 85:1914-1922.
15. Gross, S. S., and M. S. Wolin. 1995. Nitric oxide: Pathophysiological mechanisms. Annu. Rev. Physiol. 57:737-769.
16. Hanafy, K. A., J. S. Krumenacker, and F. Murad. 2001. NO, nitrotyrosine, and cyclic GMP in signal transduction. Med. Sci. Monit. 7:801-819.
17. Ireland, J. J., A. E. Zielak-Steciwko, F. Jimenez-Krassel, J. Folger, A. Bettegowda, D. Scheetz, S. Walsh, F. Mossa, P. G. Knight, G. W. Smith, P. Lonergan, and A. C. Evans. 2009. Variation in the ovarian reserve is linked to alterations in intrafollicular estradiol production and ovarian biomarkers of follicular differentiation and oocyte quality in cattle. Biol. Reprod. 80:954-964.
18. Ireland, J. L., D. Scheetz, F. Jimenez-Krassel, A. P. Themmen, F. Ward, P. Lonergan, G. W. Smith, G. I. Perez, A. C. Evans, and J. J. Ireland. 2008. Antral follicle count reliably predicts number of morphologically healthy oocytes and follicles in ovaries of young adult cattle. Biol. Reprod. 79:1219-1225.
19. Jablonka-Shariff, A., and L. M. Olson. 1997. Hormonal regulation of nitric oxide synthases and their cell-specific expression during follicular development in the rat ovary. Endocrinology 138:460-468.
20. Kim, H., C. Moon, M. Ahn, Y. Lee, H. Kim, S. Kim, T. Ha, Y. Jee, and T. Shin. 2005. Expression of nitric oxide synthase isoforms in the porcine ovary during follicular development. J. Vet. Sci. 6:97-101.
21. Lazzari, G., I. Tessaro, G. Crotti, C. Galli, S. Hoffmann, S. Bremer, and C. Pellizzer. 2008. Development of an in vitro test battery for assessing chemical effects on bovine germ cells under the ReProTect umbrella. Toxicol. Appl. Pharmacol. 233:360-370.
22. Luciano, A. M., F. Franciosi, V. Lodde, D. Corbani, G. Lazzari, G. Crotti, C. Galli, C. Pellizzer, S. Bremer, M. Weimer, and S. C. Modina. 2010. Transferability and inter-laboratory variability assessment of the in vitro bovine oocyte maturation (IVM) test within ReProTect. Reprod. Toxicol. 30:81-88.
23. Luciano, A. M., V. Lodde, M. S. Beretta, S. Colleoni, A. Lauria, and S. Modina. 2005. Developmental capability of denuded bovine oocyte in a co-culture system with intact cumulus-oocyte complexes: Role of cumulus cells, cyclic adenosine 3',5'-monophosphate, and glutathione. Mol. Reprod. Dev. 71:389-397.
24. Lussier, J. G., P. Matton, and J. J. Dufour. 1987. Growth rates of follicles in the ovary of the cow. J. Reprod. Fertil. 81:301-307.
25. Malhi, P. S., G. P. Adams, and J. Singh. 2005. Bovine model for the study of reproductive aging in women: Follicular, luteal, and endocrine characteristics. Biol. Reprod. 73:45-53.
26. Mitchell, L. M., C. R. Kennedy, and G. M. Hartshorne. 2004. Expression of nitric oxide synthase and effect of substrate manipulation of the nitric oxide pathway in mouse ovarian follicles. Hum. Reprod. 19:30-40.
27. Modina, S., V. Borromeo, A. M. Luciano, V. Lodde, F. Franciosi, and C. Secchi. 2007. Relationship between growth hormone concentrations in bovine oocytes and follicular fluid and oocyte developmental competence. Eur. J. Histochem. 51:173-180.
28. Monteleone, P., P. Giovanni Artini, G. Simi, E. Casarosa, V. Cela, and A. R. Genazzani. 2008. Follicular fluid VEGF levels directly correlate with perifollicular blood flow in normoresponder patients undergoing IVF. J. Assist. Reprod. Genet. 25:183-186.
29. Nakamura, Y., Y. Yamagata, N. Sugino, H. Takayama, and H. Kato. 2002. Nitric oxide inhibits oocyte meiotic maturation. Biol. Reprod. 67:1588-1592.
30. Nishikimi, A., T. Matsukawa, K. Hoshino, S. Ikeda, Y. Kira, E. F. Sato, M. Inoue, and M. Yamada. 2001. Localization of nitric oxide synthase activity in unfertilized oocytes and fertilized embryos during preimplantation development in mice. Reproduction 122:957-963.
31. Petr, J., R. Rajmon, E. Chmelikova, M. Tomanek, V. Lanska, M. Pribanova, and F. Jilek. 2006. Nitric-oxide-dependent activation of pig oocytes: The role of the cGMP-signalling pathway. Zygote 14:9-16.
32. Petr, J., R. Rajmon, V. Lanska, M. Sedmikova, and F. Jilek. 2005. Nitric oxide-dependent activation of pig oocytes: Role of calcium. Mol. Cell. Endocrinol. 242:16-22.
33. Pinto, C. R., D. L. Paccamonti, B. E. Eilts, C. S. Venugopal, C. R. Short, L. R. Gentry, D. L. Jr. Thompson, and R. A. Godke. 2003. Concentrations of nitric oxide in equine preovulatory follicles before and after administration of human chorionic gonadotropin. Theriogenology 60:819-827.
34. Pires, P. R., N. P. Santos, P. R. Adona, M. M. Natori, K. R. Schwarz, T. H. de Bem, and C. L. Leal. 2009. Endothelial and inducible nitric oxide synthases in oocytes of cattle. Anim. Reprod. Sci. 116:233-243.
35. Rodgers, R. J., and H. F. Irving-Rodgers. 2010. Morphological classification of bovine ovarian follicles. Reproduction 139:309-318.
36. Rosselli, M., P. J. Keller, and R. K. Dubey. 1998. Role of nitric oxide in the biology, physiology and pathophysiology of reproduction. Hum. Reprod. Update 4:3-24.
37. Schwarz, K. R., P. R. Pires, P. R. Adona, T. H. Camara de Bem, and C. L. Leal. 2008. Influence of nitric oxide during maturation on bovine oocyte meiosis and embryo development in vitro. Reprod. Fertil. Dev. 20:529-536.
38. Schwarz, K. R., P. R. Pires, T. H. de Bem, P. R. Adona, and C. L. Leal. 2010. Consequences of nitric oxide synthase inhibition during bovine oocyte maturation on meiosis and embryo development. Reprod. Domest. Anim. 45:75-80.
39. Tao, Y., Z. Fu, M. Zhang, G. Xia, J. Yang, and H. Xie. 2004. Immunohistochemical localization of inducible and endothelial nitric oxide synthase in porcine ovaries and effects of no on antrum formation and oocyte meiotic maturation. Mol. Cell. Endocrinol. 222:93-103.
40. Tatone, C., F. Amicarelli, M. C. Carbone, P. Monteleone, D. Caserta, R. Marci, P. G. Artini, P. Piomboni, and R. Focarelli. 2008. Cellular and molecular aspects of ovarian follicle ageing. Hum. Reprod. Update 14:131-142.
41. Tervit, H. R., D. Whittingham, and L. Rowson. 1972. Successful culture in vitro of sheep and cattle ova. J. Reprod. Fertil. 30:493-497.
42. Thaler, C. D., and D. Epel. 2003. Nitric oxide in oocyte maturation, ovulation, fertilization, cleavage and implantation: A little dab'll do ya. Curr. Pharm. Des. 9:399-409.
43. Van Blerkom, J. 1998. Epigenetic influences on oocyte developmental competence: Perifollicular vascularity and intrafollicular oxygen. J. Assist. Reprod. Genet. 15:226-234.
44. Vandaele, L., B. Mateusen, D. G. Maes, A. de Kruif, and A. Van Soom. 2007. Temporal detection of caspase-3 and -7 in bovine in vitro produced embryos of different developmental capacity. Reproduction 133:709-718.
45. Vassena, R., R. J. Mapletoft, S. Allodi, J. Singh, and G. P. Adams. 2003. Morphology and developmental competence of bovine oocytes relative to follicular status. Theriogenology 60:923-932.
46. Yamagata, Y., Y. Nakamura, N. Sugino, A. Harada, H. Takayama, S. Kashida, and H. Kato. 2002. Alterations in nitrate/nitrite and nitric oxide synthase in preovulatory follicles in gonadotropin-primed immature rat. Endocr. J. 49:219-226.
47. Yang, M. Y., and R. Rajamahendran. 2000. Morphological and biochemical identification of apoptosis in small, medium, and large bovine follicles and the effects of follicle-stimulating hormone and insulin-like growth factor-I on spontaneous apoptosis in cultured bovine granulosa cells. Biol. Reprod. 62:1209-1217.
48. Zackrisson, U., M. Mikuni, A. Wallin, D. Delbro, L. Hedin, and M. Brannstrom. 1996. Cell-specific localization of nitric oxide synthases (NOS) in the rat ovary during follicular development, ovulation and luteal formation. Hum. Reprod. 11:2667-2673.