Nitric oxide regulates steroid synthesis by bovine antral granulosa cells in a chemically defined medium

Animal Reproduction Science

Volumn 110, Issue 3-4, 2009, Pages 222-236

  Faes, M R ^a   Caldas Bussiere, M C ^a   Viana, K S ^a   Dias, B L ^a   Costa, F R ^a   Escocard, R M ^a  

^a UNIVERSIDADE ESTADUAL DO NORTE FLUMINENSE DARCY RIBEIRO   (Brazil)

Author keywords

17 Estradiol; Cattle; cGMP; Granulosa cells; Nitric oxide; Progesterone

Indexed keywords

1H (1,2,4)OXADIAZOLO(4,3 A)QUINOXALIN 1 ONE; 1H-(1,2,4)OXADIAZOLO(4,3-A)QUINOXALIN-1-ONE; CYCLIC GMP; ENZYME INHIBITOR; ESTRADIOL; NITRATE; NITRIC OXIDE; NITRIC OXIDE DONOR; NITROPRUSSIDE SODIUM; OXADIAZOLE DERIVATIVE; PROGESTERONE; QUINOXALINE DERIVATIVE;

ANIMAL; ARTICLE; BIOSYNTHESIS; CATTLE; CELL CYCLE; CELL SURVIVAL; DOSE RESPONSE; DRUG ANTAGONISM; DRUG EFFECT; FEMALE; GRANULOSA CELL; METABOLISM; PHYSIOLOGY;

ANIMALS; CATTLE; CELL CYCLE; CELL SURVIVAL; CYCLIC GMP; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME INHIBITORS; ESTRADIOL; FEMALE; GRANULOSA CELLS; NITRATES; NITRIC OXIDE; NITRIC OXIDE DONORS; NITROPRUSSIDE; OXADIAZOLES; PROGESTERONE; QUINOXALINES;

BOS; BOVINAE;

EID: 57049174508     PISSN: 03784320     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.anireprosci.2008.01.018     Document Type: Article

References (61)

1. Anteby E.Y., Hurwitz A., Korach O., Revel A., Simon A., Finci-Yeheskel Z., Mayer M., and Laufer N. Human follicular nitric oxide pathway: relationship to follicular size, oestradiol concentrations and ovarian blood flow. Hum. Reprod. 11 (1996) 1947-1951
2. Basini G., Baratta M., Ponderato N., Bussolati S., and Tamanini C. Is nitric oxide an autocrine modulator of bovine granulosa cell function?. Reprod. Fertil. Dev. 10 (1998) 471-478
3. Basini G., Grasselli F., Ponderato N., Bussolati S., and Tamanini C. Lipid hydroperoxide and cGMP are not involved in nitric oxide inhibition of steroidogenesis in bovine granulosa cells. Reprod. Fertil. Dev. 12 (2000) 289-295
4. Beckmann M.W., Polacek D., Seung L., and Schreiber J.R. Human ovarian granulosa cell culture: determination of blood cell contamination and evaluation of possible culture purification steps. Fertil. Steril. 56 (1991) 881-887
5. Blondin P., Dufour M., and Sirard M.A. Analysis of atresia in bovine follicles using different methods: flow cytometry, enzyme-linked immunosorbent assay, and classic histology. Biol. Reprod. 54 (1996) 631-637
6. Bonello N., McKie K., Jasper M., Andrew L., Ross N., Braybon E., Brännstrom M., and Norman R.J. Inhibition of nitric oxide: effects on interleukin-1β-enhanced ovulation rate, steroid hormones, and ovarian leukocyte distribution at ovulation in rat. Biol. Reprod. 54 (1996) 436-445
7. Burney S., Tamir S., Gal A., and Tannenbaum S.R. A mechanistic analysis of nitric oxide-induced celluar toxicity. Nitric Oxide 1 (1997) 130-144
8. Chun S.Y., Eisenhauer K.M., Kubo M., and Hsueh A.J.W. Interleukin-1β suppresses apoptosis in rat ovarian follicles by increasing nitric oxide production. Endocrinology 136 (1995) 3120-3127
9. Clementi E., Brown G.C., Foxwell N., and Moncada S. On mechanism by which vascular endothelial cells regulate their oxygen consumption. Proc. Natl. Acad. Sci. U.S.A. 96 (1999) 1559-1562
10. Conti M., Nemoz G., Sette C., and Vicini E. Recent progress in understanding the hormonal regulation of phosphodiesterases. Endocr. Rev. 16 (1995) 370-389
11. Craven P.A., and DeRubertis F.R. Restoration of the responsiveness of purified guanylate cyclase to nitrosoguanidine, nitric oxide, and related activators by heme and hemeproteins. Evidence for involvement of the paramagnetic nitrosyl-heme complex in enzyme activation. J. Biol. Chem. 253 (1978) 8433-8443
12. Denninger J.W., and Marletta M.A. Guanylate cyclase and the NO/cGMP signaling pathway. Biochem. Biophys. Acta 5 (1999) 339-350
13. Draijer R.J., Atsma D.E., van der Laarse A., and van Hinsberg V.W. cGMP and nitric oxide modulate thrombin-induced endothelial permeability. Regulation via different pathways in human aortic and umbilical vein endothelial cells. Circulation Res. 76 (1995) 199-208
14. Ellman C., Corbett J.A., Misko T.P., McDaniel M., and Beckerman K.P. Nitric oxide mediates interleukin-1-induced cellular cytotoxicity in rat ovary: potential role for nitric oxide in the ovulatory process. J. Clin. Invest. 92 (1993) 3053-3056
15. Grasselli F., Ponderato N., Basini G., and Tamanini C. Nitric oxide synthase expression and nitric oxide/cyclic GMP pathway in swine granulosa cells. Dom. Anim. Endocr. 20 (2001) 241-252
16. Grimes R.W., Matton P., and Ireland J.J. A comparison of histological and non-histological and non-histological indices of atresia and follicular function. Biol. Reprod. 37 (1987) 82-88
17. Gutierrez C.G., Campbell B.K., and Webb R. Development of a long-term bovine granulosa cell culture system: induction and maintenance of estradiol production, response to follicle-stimulating hormone, and morphological characterisics. Biol. Reprod. 56 (1997) 608-616
18. Hanafy K.A., Krumenacker J.S., and Murad F. NO, nitrotyrosine, and cyclic GMP in signal transduction. Med. Sci. Monitor 7 (2001) 801-819
19. Hanke C.J., Drewtt J.G., Myers C.R., and Campbell W.B. Nitric oxide inhibits aldosterone synthesis by a guanylyl cyclase-independent effect. Endocrinology 139 (1998) 4053-4060
20. Hurwitz A., Finci-Yeheskel Z., Milwidsky A., and Mayer M. Regulation of cycooxygenase activity and progesterone production in the rat corpus luteum by inducible nitric oxide synthase. Reproduction 123 (2002) 663-669
21. Ignarro L.J. Signal transduction mechanism involving nitric oxide. Biochem. Pharm. 41 (1991) 485-490
22. Ireland J.J., Murphee R.L., and Coulson P.B. Accuracy of predicting stages of bovine estrous cycle by gross appearance of the corpus luteum. J. Dairy Sci. 63 (1980) 155-160
23. Ishimaru R.S., Leung K., Hong L.-S., and LaPolt P.S. Inhibitory effects of nitric oxide on estrogen production and cAMP levels in rat granulosa cells cultures. J. Endocrinol. 168 (2001) 249-255
24. Janblonka-Shariff A., and Olson L.M. Hormonal regulation of nitric oxide synthases and their cell-specific expression during follicular development in the rat ovary. Endocrinology 138 (1997) 460-468
25. Keskintepe L., and Brackett B.G. In vitro developmental competence of in vitro-matured bovine oocytes fertilized and cultured in completely defined media. Biol. Reprod. 55 (1996) 333-339
26. Kurtz A., Gotz K.H., Hamann M., and Wagner C. A stimulation of rennin secretion by nitric oxide is mediated by phosphodiesterase3. Proc. Natl. Acad. Sci. U.S.A. 95 (1998) 4743-4747
27. Lapolt P.S., and Hong L.S. Inibitory effects of superoxide dismutase and cyclic guanosina 3′, 5′-monophosphate on estrogen production in cultured rat granulosa cells. Endocrinology 136 (1995) 5533-5539
28. Lapolt S.P., Leung K., Ishimaru R., Tafoya M.A., and Chen Y.J. Roles of cyclic GMP in modulating ovarian functions. Symposium: Genetic Aspects of Follicular and Oocyte Growth. Reprod. Biomed. (2002) 15-23 (Online 6)
29. Li H.Y., Chang S.P., Yuan C.C., and Chao H.T. Nitric oxide induces apoptosis in endometrial epithelial cells in the presence of progesterone: involvement of mitogen-activated protein kinase pathway. Mol. Hum. Reprod. 7 (2001) 755-763
30. Lieberman S., Greenfield N.J., and Wolfson A. A heuristic proposal for understanding steroidogenic process. Endocr. Rev. 5 (1984) 128-148
31. Liu X., Miller M.J., Thomas D.D., and Lancaster J.R. Accelerated reaction of nitric oxide with oxygen within the hydrophobic interior of biological membranes. Proc. Natl. Acad. Sci. U.S.A. 95 (1998) 2175-2179
32. MacFarland R.T., Zelus B.D., and Beavo J.A. High concentrations of a cGMP-stimulated phosphodisterase mediate ANP-induced decreases in cAMP and steroidogenesis in adrenal glomerulosa cells. J. Biol. Chem. 266 (1991) 136-142
33. Matsumi H., Yano T., Koji T., Ogura T., Tsutsumi O., Taketani Y., and Esumi H. Expression and localization of inducible nitric oxide synthase in the rat ovary: a possible involvement of nitric oxide in the follicular development. Biochem. Biophys. Res. Commun. 243 (1998) 67-72
34. Maurer H.R. Towards serum-free, chemical defined media for mammalian cell culture. In: Freshney R.I. (Ed). Animal Cell Culture: A Practical Approach. second ed. (1992), Oxford University Press 15-46
35. McMahon T.J. Nitric oxide in the human respiratory cycle. Nat. Med. 8 (2002) 711-717
36. Mingone C.J., Gupte S.A., Chow J.L., Ahmad M., Abraham N.G., and Wolin M.S. Am. J. Physiol. Lung Cell. Mol. Physiol. 29 (2006) 334-336
37. Mingoti G.Z., Garcia J.M., and Rosa e Silva A.A.M. Steroidogenesis in cumulus cells of bovine cumulus-oocyte-complexus matured in vitro with BSA and different concentrations of steroids. Anim. Reprod. Sci. 69 (2002) 175-186
38. Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. 65 (1983) 55-63
39. Murard F. Cellular signaling with nitric oxide and cyclic GMP. Braz. J. Med. Biol. Res. 32 (1999) 1317-1327
40. Orsi N.M. Embryotoxicity of the nitric oxide donor sodium nitroprusside in preimplantation bovine embryons in vitro. Anim. Reprod. Sci. 91 (2006) 225-236
41. Piccinato C.A., Montrezor L.H., and Rosa e Silva A.A.M. Produção de óxido nítrico: padronização do modelo de cultura das células da granulosa de folículos ovarianos bovinos. Abstracts of the XV Reunião Anual da Sociedade de Transferência de Embriões. Caldas Novas, Brazil. Porto Alegre: Arq. Fac. Vet. UFRGS (2000) 308 pp.
42. Rettori V., Gimero M., Lyson K., and McCann S.M. Nitric oxide mediates norepinephrine-induced prostaglandin estradiol release from the hypothalamus. Proc. Natl. Acad. Sci. U.S.A. 89 (1992) 543-546
43. Ricart-Jané D., Llobera M., and López-Tejero D. Anticoagulants and others preanalytical factors interfer in plasma nitrate/nitrite quantification by Griess method. Nitric Oxide 6 (2002) 178-185
44. Richards J.S., Fitzpatrick S.L., and Clemens J.W. Ovarian cell differentiation: a cascade of multiple hormones, cellular signals, and regulates genes. Rec. Prog. Horm. Res. 50 (1995) 23-254
45. +2: their relationship to apoptosis and oncogenesis. FEBS Lett. 325 (1993) 104-107
46. Rouillier P., Matton P., Sirard M.-A., and Guilbault L.A. Follicle-stimulating hormone-induced estradiol and progesterone production by bovine antral and mural granulosa cells cultured in vitro in a completely defined medium. J. Anim. Sci. 74 (1996) 3012-3019
47. Rouillier P., Matton P., Dufour M., Sirard M.-A., and Guilbault L.A. Steroid production, cell proliferation, and apoptosis in cultured bovine antral and mural granulose cells: developmental of an in vitro model to study estradiol production. Mol. Reprod. Dev. 50 (1998) 170-177
48. Sarti P., Lendaro E., Ippoliti R., Bellelli A., Benedetti P.A., and Brunori M. Modulation of mitochondrial respiration by NO: investigation by single cell fluorescence microscopy. FASEB J. 13 (1999) 191-197
49. SAS, 1996. Statistical Analysis System.
50. Sato K., Ozaki K., Oh L., Meguro A., Hatanaka K., Nagai T., Muroi K., and Ozawa K. Nitric oxide plays a critical role in suppression of T-cell proliferation by mesenchymal stem cells. Blood 109 (2007) 228-234
51. Shakil T., and Whitehead S.A. Inhibitory action of peritoneal macrophages on progesterone secretion from co-cultured rat granulose cells. Biol. Reprod. 50 (1994) 1183-1189
52. Sitaramayya A. Calcium-dependent activation of guanylato cyclase by S100b. Adv. Exp. Med. Biol. 514 (2002) 389-398
53. Snyder G.D., Holmes R.W., Bates J.N., and Van Voorhis B.J. Nitric oxide inhibits aromatase activity: mechanisms of action. J. Steroid Biochem. Mol. Biol. 58 (1996) 63-69
54. Strauss III, Schuler L.A., Rosenblum M.F., and Tanaka T. Cholesterol metabolism by ovarian tissue. Adv. Lipid Res. 18 (1981) 99-157
55. Tanner F.C., Meier P., Greutert H., Champion C., Nabel E.G., and Lüscher T.F. Nitric oxide modulates expression of cell cycle regulatory proteins. Acytostatic strategy for inhibition of human vascular smooth muscle cell proliferation. Circulation 101 (2000) 1982-1989
56. Tsafriri A., Chun S.Y., Zhang R., Hsueh A.J., and Conti M. Oocyte maturation involves compartmentalization and opposing changes of cAMP levels in follicular somatic and germ cells: studies using selective phosphodiesterase inhibitors. Dev. Biol. 140 (1996) 307-317
57. Van Voorhis B.J., Dunn M.S., Snyder G.D., and Weiner C.P. Nitric oxide: an autocrine regulator of human granulosa-luteal cell steroidogenesis. Endocrinology 135 (1994) 1779-1806
58. Wang S., Liu Y., Holyoak G.R., and Bunch T.D. The effects of bovine serum albumin and fetal bovine serum on the development of pre- and post-cleavage-stage bovine embryos cultured in modified CR2 and M199 media. Anim. Reprod. Sci. 48 (1997) 37-45
59. Whitehead S., and Lacey M. Inhibitory effect of peritoneal macrophages on progesterone release from co-cultured rat granulosa cells is reversed by dexamethasone: evidence for an action independent of nitric oxide and distal to cyclic adenosine 3′, 5′-monophosphate generation. Biol. Reprod. 54 (1996) 1317-1325
60. Wink D.A., Osawa Y., Darbysbire J.F., Jones C.R., Eshenaur S.C., and Nims R.W. Inhibition of cytochomes P450 by nitric oxide and a nitric oxide-releasing agent. Arch. Biochem. Biophys. 300 (1993) 115-123
61. Yang Z., Simari R.D., Perkins N.D., San H., Gordon D., Nabel G.J., and Nabel E.G. Role of p21 cyclin-dependent kinase inhibitory in limiting intimal cell proliferation in response to arterial injury. Proc. Natl. Acad. Sci. U.S.A. 93 (1996) 7905-7910