Nitric oxide is essential for optimal meiotic maturation of murine cumulus-oocyte complexes in vitro

Molecular Reproduction and Development

Volumn 55, Issue 4, 2000, Pages 412-421

  Jablonka Shariff, AlbinaD ^a   Olson, Lisa M ^a,b  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b MONSANTO COMPANY   (United States)

Author keywords

Endothelial nitric oxide synthase; In vitro; Meiosis; Mice; Nitric oxide; Oocyte

Indexed keywords

N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE; NITRIC OXIDE SYNTHASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CUMULUS OOPHORUS; ENDOTHELIUM; FEMALE; MEIOSIS; METAPHASE; MOUSE; NONHUMAN; OOCYTE DEVELOPMENT; OOCYTE MATURATION; OVARY FOLLICLE; PRIORITY JOURNAL;

ANIMALS; CELL SURVIVAL; CELLS, CULTURED; CHROMOSOME ABERRATIONS; ENDOTHELIUM; ENZYME INHIBITORS; FEMALE; ISOENZYMES; MEIOSIS; MICE; NG-NITROARGININE METHYL ESTER; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; OOCYTES; ORGAN SIZE; OVARIAN FOLLICLE; OVARY; STEROIDS;

ANIMALIA; MURINAE;

EID: 0034010659     PISSN: 1040452X     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1098-2795(200004)55:4<412::AID-MRD9>3.0.CO;2-W     Document Type: Article

References (42)

1. Albertini DF. 1992. Cytoplasmic microtubular dynamics and chromatin organization during mammalian oogenesis and oocyte maturation. Mut Res 296:57-68.
2. Anteby EY, Hurwitz A, Korach O, Revel A, Simon A, Finci-Yeheskel Z, Mayer M, Laufer N. 1996. Human follicular nitric oxide pathway: relationship to follicular size, oestradiol concentration and ovarian blood flow. Hum Reprod 11:1947-1951.
3. Bonello N, McKie K, Jasper M, Andrew L, Ross N, Braybon E, Brannstrom M, Norman RJ. 1996. Inhibition of nitric oxide: effects of interleukin-1β-enhanced ovulation rate, steroid hormones, and ovarian leukocyte distribution at ovulation in the rat. Biol Reprod 54:436-445.
4. Bredt DS, Hwang PM, Glatt CE, Lowenstein C, Reed RR, Snyder SH. 1991. Cloned and expressed nitric oxide synthase structurally resembles cytochrome P-450 reductase. Nature 351:714-718.
5. Brower PT, Schultz RM. 1982. Intercellular communication between granulosa cells and mouse oocytes: existence and possible nutritional role during oocyte growth. Dev Biol 90:144-153.
6. Chun S-Y, Eisenhauer KM, Kubo M, Hsueh AJW. 1995. Interleukin-1β suppresses apoptosis in rat ovarian follicles by increasing nitric oxide production. Endocrinology 136:3120-3127.
7. Dail WG, Sanborn CR, Ratner A. 1980. Immunocytochemical localization of cyclic AMP and cyclic GMP in rat ovarian tissue. Biol Reprod 22:281-288.
8. Downs SM, Mastropolo AM. 1997. Culture conditions affect meiotic regulation in cumulus cell-enclosed mouse oocytes. Mol Reprod Dev 46:551-566.
9. Ellman C, Corbet JA, Misko TP, McDaniel M, Beckerman KP. 1993. Nitric oxide mediates interleukin-1β induced cellular cytotoxicity: a potential role for nitric oxide in the ovulatory process. J Cin Invest 92:3053-3056.
10. Eppig JJ. 1991. Intercommunication between mammalian oocytes and companion somatic cells. BioEssays 13:569-574.
11. Fukuda AI, Breuel KF. 1997. Effect of nitric oxide synthase inhibitor on in vivo embryonic development and implantation of mouse embryos. Biol Reprod 56:189(abstr. 427).
12. Fukuda AI, Hubbard TE, Breuel KF. 1996. Production of nitric oxide from mouse embryo and effect of nitrite on mouse embryonic development. Biol Reprod 54:173(abstr. 456).
13. Hellstrom WJ, Bell M, Wang R, Sikka SC. 1994. Effects of sodium nitropruside on sperm motility, viability, and lipid peroxidation. Fertil Steril 61:1117-1122.
14. Huang PL, Huang Z, Mashimo H, Bloch KD, Moskowitz MA, Bevan JA, Fishman MC. 1995. Hypertension in mice lacking the gene for endothelial nitric oxide synthase. Nature 377:239-242.
15. Hubbard CJ, Price J. 1988. The effects of follicle-stimulating hormone and cyclic guanosine 3′,5′-monophosphate and cyclic adenosine 3′,5′-monophosphate-phosphodiesterase and resumption of meiosis in hamster cumulus-oocyte complexes. Biol Reprod 39:829-838.
16. Jablonka-Shariff A, Olson LM. 1997. Hormonal regulation of nitric oxide synthases and their cell-specific expression during follicular development in the rat ovary. Endocrinology 138:460-468.
17. Jablonka-Shariff A, Olson LM. 1998. The role of nitric oxide in oocyte meiotic maturation and ovulation: meiotic abnormalities of endothelial nitric oxide synthase knock-out mouse oocytes. Endocrinology 139:2944-2954.
18. Jablonka-Shariff A, Basuray R, Olson LM. 1999a. Inhibitors of nitric oxide synthase influence oocyte maturation in rats. J Soc Gynecol Invest 6:95-101.
19. Jablonka-Shariff A, Ravi S, Beltsos AN, Murphy LL, Olson LM. 1999b. Abnormal estrous cyclicity after disruption of endothelial and inducible nitric oxide synthase in mice. Biol Reprod 61:171-177.
20. Lamas S, Marsden PA, Li GK, Tempst P, Michel T. 1992. Endothelial nitric oxide synthase: molecular cloning and characterization of a distinct constitutive enzyme isoform. Proc Natl Acad Sci USA 89:6348-6352.
21. Lim JM, Hansel W. 1998. Improved development of in vitro-derived bovine embryos by using of a nitric oxide scavenger in a cumulus-granulosa cell coculture system. Mol Reprod Dev 50:45-53.
22. Moncada S, Palmer RM, Higgs EA. 1991. Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmacal Rev 43:109-142.
23. Nathan C. 1992. Nitric oxide as a secretory product of mammalian cells. FASEB J 6:3051-3064.
24. Olson LM, Jones-Burton CM, Jablonka-Shariff A. 1996. Nitric oxide decreases estradiol synthesis in rat luteal cells in vitro: possible role for nitric oxide in functional luteal regression. Endocrinology 137: 3531-3539.
25. Olson LM, Jablonka-Shariff A, Beltsos AN. 1999. Ovarian nitric oxide: a modulator of ovulation and oocyte maturation. In: Adashi FY, editor. Ovulation: evolving scientific and clinical concepts. New York: Springer-Verlag Inc. (in press).
26. Peluso JJ, Hutz R, England-Charlesworth C. 1982. Development of preovulatory follicles and oocytes during the oestrus cycle of mature and aged rats. Acta Endocrinol 100:434-443.
27. Powers RW, Chambers C, Larsen WJ. 1996. Diabetes-mediated decreases in ovarians superoxide dismutase activity are related to blood-follicle barrier and ovulation defects. Endocrinology 137:3101-3110.
28. Purcell TL, Given R, Chwalisz K, Garfield RE. 1999. Nitric oxide synthase distribution during implantation in the mouse. Mol Hum Reprod 5:467-475.
29. Schmidt HHHW, Lohmann SM, Walter U. 1993. The nitric oxide and cGMP signal transduction system: regulation and mechanism of action. Biochim Biophys Acta 1178:153-175.
30. Schroeder AC, Eppig JJ. 1984. The developmental capacity of mouse oocytes that matured spontaneously in vitro is normal. Dev Biol 104:831-840.
31. Schultz RM. 1986. Molecular aspects of mammalian oocyte growth and maturation. In: Rossant J, Pedersen R, editors. Experimental approaches to mammalian embryonic development. New York: Cambridge University Press, p 195-237.
32. Shukovski L, Tsafriri A. 1994. The involvement of nitric oxide in the ovulatory process in the rat. Endocrinology 135:2287-2290.
33. Sorensen RA, Wassarman PM. 1976. Relationship between growth and meiotic maturation of the mouse oocyte. Dev Biol 50:531-536.
34. Steel RGD, Torrie JH. 1980. Principles and procedures of statistics: a biometrical approach. New York: McGraw-Hill. p 137-171.
35. Tornell J, Braanstrom M, Hillensjo T. 1984. Different effects of cyclic nucleotide derivatives upon the rat oocyte-cumulus complex in vitro. Acta Physiol Scand 122:507-513.
36. Tornell J, Billig H, Hillensjo T. 1991. Regulation of oocyte maturation by changes in ovarian levels of cyclic nucleotides. Hum Reprod 6:411-422.
37. Van Voorhis BJ, Dunn MS, Snyder GD, Weiner CP. 1994. Nitric oxide: an autocrine regulator of human granulosa-luteal cell steroidogenesis. Endocrinology 135:1799-1806.
38. Wassarman PM. 1988. The mammalian ovum. In: Knobil E, Neill JD, editors. The physiology of reproduction. Vol. 1. New York: Raven Press, p 69-102.
39. Wolin MS, Wood KS, Ignarro LJ. 1982. Guanylate cyclase from bovine lung: a kinetic analysis of the regulation of unpurified soluble enzyme by protoporphyrin IX, heme, and nitrosyl-heme. J Biol Chem 257:11312-11320.
40. Yamauchi J, Miyazaki T, Iwasaki S, Kishi I, Kuroshima M, Tei C, Yoshimura Y. 1997. Effects of nitric oxide on ovulation and ovarian steroidogenesis and prostaglandin production in the rabbit. Endocrinology 138:3630-3637.
41. Xie Q, Cho HJ, Calaycay J, Mumford RA, Swiderek KM, Lee TD, Ding A, Troso T, Nathan C. 1992. Cloning and characterization of inducible nitric oxide synthase from mouse macrophages. Science 256:225-228.
42. Zini A, De Lamirande E, Gangon C. 1995. Low level of nitric oxide promote human sperm capacitation in vitro. J Androl 16:424-431.