Skip to main content
Log in

Localization of Nitric Oxide-related Substances in the Quail Ovary During Folliculogenesis

  • Published:
The Histochemical Journal Aims and scope Submit manuscript

Abstract

In the present study, nitric oxide (NO)-related substances, namely NO synthase (NOS), L-citrulline, cGMP and nitrotyrosine, have been localized in the quail ovary, using NADPH-diaphorase staining and immunohistochemical methods. The results indicate the presence of the NOS isoforms, showing distinct cell-specific distribution patterns in the quail ovary. Inducible NOS is primarily present in leukocytes, endothelial NOS in granulosa cells, and neuronal NOS in nerve cells, oocytes, interstitial cells and granulosa cells of pre-hierarchal follicles and of the germinal disc region of pre-ovulatory follicles. NOS activity, indicated by the presence of L-citrulline, is observed in oocytes, nerve cells, interstitial cells and a few granulosa cells of pre-hierarchal follicles. Detection of accumulated cGMP indicates that granulosa cells of pre-hierarchal and of pre- and post-ovulatory follicles, the theca interna of pre-ovulatory follicles, and oocytes are main targets of NO. Nitrotyrosine, a marker of peroxynitrite activity, is mainly localized in atretic follicles and in post-ovulatory follicles. lt is concluded that the quail ovary possesses a NO/NOS system, and that NO may be considered as a mediator involved in various ovarian processes, including atresia.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References cited

  • Ahsan S, Lacey M, Whitehead SA (1997) Interactions between interleukin 1β, nitric oxide and prostaglandin E2 in the rat ovary: effects on steroidogenesis. Eur J Endocrinol 137: 293-300.

    Google Scholar 

  • Aoki E, Takeuchi IK, Shoji R (1995) Nitric oxide: an attractive signaling molecule. Acta Histochem Cytochem 28: 97-106.

    Google Scholar 

  • Beckman JS, Ye YZ, Anderson PG, Chen J, Accavitti MA, Tarpey MM, White CR (1994) Extensive nitration of protein tyrosines in human artherosclerosis detected by immunohistochemistry. Biol Chem Hoppe-Seyler 375: 81-88.

    Google Scholar 

  • Behrman HR, Riley JCM, Aten RF (1993) Reactive oxygen species and ovarian function. In Adashi EY, Leung PCK eds. The Ovary. pp. 455-471. New York: Raven Press.

    Google Scholar 

  • Bonello N, McKie K, Jasper M, Andrew L, Ross N, Braybon E, Brännström, M, Norman RJ (1996) Inhibition of nitric oxide: effects on interleukin-1β-enhanced ovulation rate, steroid hormones, and ovarian leukocyte distribution at ovulation in the rat. Biol Reprod 54: 436-455.

    Google Scholar 

  • Brunswig-Spickenheier B, Mukhopadhyay AK (1997) Stimulation of nitric oxide-cyclic guanosine monophosphate pathway in bovine ovarian theca cells by tumor necrosis factor α (TNFα). Is this pathway implicated in the TNFβ-induced inhibition of luteinizing hormone-stimulated protein production? Biol Reprod 57: 700-706.

    Google Scholar 

  • Callebaut M (1973) Correlation between germinal vesicle and oocyte development in the adult Japanese quail (Cotumix cotumix japonica). A cytochemical and autoradiographic study. J Embryol Exp Morph 29: 145-157.

    Google Scholar 

  • Callebaut M (1983) The constituent oocytal layers of the avian germ and the origin of the primordial germ cell yolk. Arch Anat Microsc 72: 199-214.

    Google Scholar 

  • Chalana RK, Guraya SS (1978) Histophysiological studies on the postovulatory follicles of the fowl ovary. Poultry Sci 57: 814-817.

    Google Scholar 

  • Chalana RK, Guraya SS (1979a) Morphological and histochemical observations on the primordial and early growing oocytes of crow (Corvus splendens) and myna (Acridotheres tristis). Poultry Sci 58: 225-231.

    Google Scholar 

  • Chalana RK, Guraya SS (1979b) Seasonal fluctuations and histochemical characteristics of the interstitial cells in the ovary of crow and myna. PAVO 17: 65-70.

    Google Scholar 

  • Chalana RK, Guraya SS (1980) Morphological and histochemical changes in the follicular epithelium during follicular growth in the crow Corvus splendens. Proc Indian Acad Sci 89: 133-140.

    Google Scholar 

  • 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.

    Google Scholar 

  • Eisenhauer KM, Chun S-Y, Minami S, Billig H, Hsueh AJW (1996) Mechanisms of atresia: the hormonal control of apoptosis. In Fillicori M, Flamigni C, eds. Ovary: Regulation, Dysfunction and Treatment, Amsterdam: Elsevier Science Publishers pp. 103-112.

    Google Scholar 

  • Etches RJ, Petitte JN (1990) Reptilian and avian hierarchies: models for the study of ovarian development. J Exp Zool (Suppl. 4): 112-122.

  • Gilbert AB (1965) Innervation of the ovarian follicle of the domestic hen. Q J Exp Physiol 50: 437-445.

    Google Scholar 

  • Grozdanovic Z, Mayer B, Baumgarten HG, Brüning G (1994) Nitric oxide synthase-containing nerve fibers and neurons in the genital tract of the female mouse. Cell Tissue Res 275: 355-360.

    Google Scholar 

  • Hattori M-A, Sakamoto K, Fujihara N, Kojima I (1996) Nitric oxide: a modulator for the epidermal growth factor receptor expression in developing ovarian granulosa cells. Am J Physiol 39: C812-C818.

    Google Scholar 

  • 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.

    Google Scholar 

  • Jarrett WA, Price GT, Lynn VJ, Burden HW (1994) NADPH diaphorase-positive neurons innervating the rat ovary. Neurosci Lett 177: 47-49.

    Google Scholar 

  • Lin AW, Chang CC, McCormick CC (1996) Molecular cloning and expression of an avian macrophage nitric-oxide synthase cDNA and the analysis of the genomic 5′-flanking region. J Biol Chem 271: 11911-11919.

    Google Scholar 

  • Majewski M, Sienkiewicz W, Kaleczye J, Mayer B, Czaja K, Lakomy M (1995) The distribution and co-localization of immunoreactivity to nitric oxide synthase, vasoactive intestinal polypeptide and substance P within nerve fibres supplying bovine and porcine female genital organs. Cell Tissue Res 281: 445-464.

    Google Scholar 

  • Matsumi H, Yano T, Koji T, Ogura T, Tsutsumi O, Taketani Y, Esumi H (1998) 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: 67-72.

    Google Scholar 

  • Moeremans M, Daneels G, De Raeymaeker M, De Wever B, De Mey J (1987) The use of colloidal metal particles in protein blotting. Electrophoresis 8: 403-409.

    Google Scholar 

  • Nakos G, Gossrau R (1994) When NADPH diaphorase (NADPHd) works in the presence of formaldehyde, the enzyme appears to visualize selectively cells with constitutive nitric oxide synthase (NOS). Acta Histochem 96: 335-343.

    Google Scholar 

  • Nathan C, Xie Q-W (1994) Nitric oxide synthases: roles, tolls, and controls. Cell 78: 915-918.

    Google Scholar 

  • Norton AJ, Jordan S, Yeomans P (1994) Brief, high-temperature heat denaturation (pressure cooking): a simple and effective method of antigen retrieval for routinely processed tissues. J Pathol 173: 371-379.

    Google Scholar 

  • Olson LM, Jones-Burton CM, Jablonka-Shariff A (1996) Nitric oxide decreases estradiol synthesis of rat luteinized ovarian cells: possible role for nitric oxide in functional luteal regression. Endocrinology 137: 3531-3539.

    Google Scholar 

  • Oribe T, Fujii S (1978) Innervation of the mature follicular membrane of the domestic hen. Bull Hiroshima Agr 6: 63-71.

    Google Scholar 

  • Parshad RK, Guraya SS (1984) Histoenzymological differences in the envelope of white and stages of rapid-growing yellow follicles in the ovary of the crow (Corvus splendens). Proc Indian Acad Sci (Anim Sci) 93: 91-95.

    Google Scholar 

  • Petrusz P, Merchenthaler I, Weinberg RJ, Grossman G, Ordronneau P (1993) Characterization of an antiserum to citrulline for use in immunocytochemistry. J Histochem Cytochem 41: 1126.

    Google Scholar 

  • Powers RW, Chen L, Russell PT, Larsen WJ (1995) Gonadotropin-stimulated regulation of blood-follicle barrier is mediated by nitric oxide. Am J Physiol 269: E290-E298.

    Google Scholar 

  • Puchtler H, Sweat Waldrop F, Meloan SN, Terry MS, Conner HM (1970) Methacarn (methanol-Carnoy) fixation. Practical and theoretical considerations. Histochemie 21: 97-116.

    Google Scholar 

  • Scherer-Singler U, Vincent SR, Kimura H, McGeer EG (1983) Demonstration of a unique population of neurons with NADPH-diaphorase histochemistry. J Neurosci Methods 9: 229-234.

    Google Scholar 

  • Shukovski L, Tsafriri A (1994) The involvement of nitric oxide in the ovulatory process in the rat. Endocrinology 135: 2287-2290.

    Google Scholar 

  • Srivastava V, Jones BJ, Dookwah H, Hiney JK, Dees WL (1997) Ovarian nitric oxide synthase (NOS) gene expression during peripubertal development. Life Sci 61: 1507-1516.

    Google Scholar 

  • Sung Y-Y, Hotchkiss JH, Austic RE, Dietert RR (1991) L-Arginine-dependent production of a reactive nitrogen intermediate by macrophages of a uricotelic species. J Leukocyte Biol 50: 49-56.

    Google Scholar 

  • Tamir H, Ratner S (1963a) Enzymes of arginine metabolism in chicks. Arch Biochem Biophys 102: 249-258.

    Google Scholar 

  • Tamir H, Ratner S (1963b) A study of ornithine, citrulline and arginine synthesis in growing chicks. Arch Biochem Biophys 102: 259-269.

    Google Scholar 

  • Van Voorhis BJ, Moore K, Strijbos PJLM, Nelson S, Baylis SA, Grzybicki D, Weiner CP (1995) Expression and localization of inducible and endothelial nitric oxide synthase in the rat ovary. Effects of gonadotropin stimulation in vivo. J Clin Invest 96: 2719-2726.

    Google Scholar 

  • 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.

    Google Scholar 

  • Yoshimura Y, Tischkau SA, Bahr JM (1994) Destruction of the germinal disc region of an immature preovulatory follicle suppresses follicular maturation and ovulation. Biol Reprod 51: 222-233.

    Google Scholar 

  • Yun H-Y, Dawson VL, Dawson TM (1996) Neurobiology of nitric oxide. Crit Rev Neurobiol 10: 291-316.

    Google Scholar 

  • Zackrisson U, Mikuni M, Wallin A, Delbro D, Hedin L, Brännström M (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.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

van Nassauw, L., Tao, L. & Harrisson, F. Localization of Nitric Oxide-related Substances in the Quail Ovary During Folliculogenesis. Histochem J 31, 443–454 (1999). https://doi.org/10.1023/A:1003755825772

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1003755825772

Keywords

Navigation