Skip to main content
The Journal of Clinical Investigation logoLink to The Journal of Clinical Investigation
. 1994 Jan;93(1):180–187. doi: 10.1172/JCI116943

Gonadotropin stimulates ovarian renin-angiotensin system in the rabbit.

Y Yoshimura 1, N Koyama 1, M Karube 1, T Oda 1, M Akiba 1, A Yoshinaga 1, S Shiokawa 1, M Jinno 1, Y Nakamura 1
PMCID: PMC293751  PMID: 8282785

Abstract

The present study was undertaken to assess the role of ovarian renin-angiotensin system (RAS) in the preovulatory cascade induced by gonadotropin exposure. In the in vitro perfused rabbit ovaries, exposure to human chorionic gonadotropin (hCG) enhanced the secretion rate of angiotensin II (Ang II) within 1 h. The secretion rate reached maximal levels at 6 h and then declined thereafter. The intrafollicular Ang II content and renin-like activity were also significantly increased at 2 and 4 h after exposure to hCG, compared with control ovaries perfused with medium alone. The level of intrafollicular Ang II after hCG exposure significantly exceeded the concentration of Ang II in an equivalent volume of plasma. The addition of 1 microM captopril to the perfusate significantly inhibited the secretion rate of Ang II stimulated by hCG; however, captopril affected neither the ovulatory efficiency nor prostaglandin production in ovaries treated with hCG. Captopril significantly inhibited the resumption of meiosis in the ovulated ova and follicular oocytes stimulated by hCG. The administration of 100 micrograms Ang II at 2-h intervals to the perfusate reversed the inhibitory effects of captopril on hCG-induced oocyte maturation. In conclusion, these data indicate that gonadotropin stimulates renin-like activity and Ang II production in the rabbit ovary. Ovarian renin-angiotensin system may play an important role in the process of oocyte maturation after exposure to gonadotropin.

Full text

PDF
187

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Anderson P. W., Malarkey W. B., Salk J., Kletsky O. A., Hsueh W. A. The effect of angiotensin-converting enzyme inhibition on prolactin responses in normal and hyperprolactinemic subjects. J Clin Endocrinol Metab. 1989 Sep;69(3):518–522. doi: 10.1210/jcem-69-3-518. [DOI] [PubMed] [Google Scholar]
  2. Armstrong D. T., Grinwich D. L., Moon Y. S., Zamecnik J. Inhibition of ovulation in rabbits by intrafollicular injection of indomethacin and prostaglandin F antiserum. Life Sci. 1974 Jan 1;14(1):129–140. doi: 10.1016/0024-3205(74)90252-5. [DOI] [PubMed] [Google Scholar]
  3. Beardwell C. G. Radioimmunoassay of arginine vasopressin in human plasma. J Clin Endocrinol Metab. 1971 Aug;33(2):254–260. doi: 10.1210/jcem-33-2-254. [DOI] [PubMed] [Google Scholar]
  4. Brentjens J. R., Matsuo S., Andres G. A., Caldwell P. R., Zamboni L. Gametes contain angiotensin converting enzyme (kininase II). Experientia. 1986 Apr 15;42(4):399–402. doi: 10.1007/BF02118626. [DOI] [PubMed] [Google Scholar]
  5. Cornwallis C. M., Skinner S. L., Nayudu P. L., Lopata A., Thatcher R. L., Yeung S. P., Whitworth J. A. Follicular fluid renin concentration and IVF outcome. Hum Reprod. 1990 May;5(4):413–417. doi: 10.1093/oxfordjournals.humrep.a137113. [DOI] [PubMed] [Google Scholar]
  6. Culler M. D., Tarlatzis B. C., Lightman A., Fernandez L. A., Decherney A. H., Negro-Vilar A., Naftolin F. Angiotensin II-like immunoreactivity in human ovarian follicular fluid. J Clin Endocrinol Metab. 1986 Mar;62(3):613–615. doi: 10.1210/jcem-62-3-613. [DOI] [PubMed] [Google Scholar]
  7. Daud A. I., Bumpus F. M., Husain A. Characterization of angiotensin I-converting enzyme (ACE)-containing follicles in the rat ovary during the estrous cycle and effects of ACE inhibitor on ovulation. Endocrinology. 1990 Jun;126(6):2927–2935. doi: 10.1210/endo-126-6-2927. [DOI] [PubMed] [Google Scholar]
  8. Daud A. I., Bumpus F. M., Husain A. Evidence for selective expression of angiotensin II receptors on atretic follicles in the rat ovary: an autoradiographic study. Endocrinology. 1988 Jun;122(6):2727–2734. doi: 10.1210/endo-122-6-2727. [DOI] [PubMed] [Google Scholar]
  9. Dharmarajan A. M., Yoshimura Y., Sueoka K., Atlas S. J., Dubin N. H., Ewing L. L., Zirkin B. R., Wallach E. E. Progesterone secretion by corpora lutea of the isolated perfused rabbit ovary during pseudopregnancy. Biol Reprod. 1988 Jun;38(5):1137–1143. doi: 10.1095/biolreprod38.5.1137. [DOI] [PubMed] [Google Scholar]
  10. Fernandez L. A., Tarlatzis B. C., Rzasa P. J., Caride V. J., Laufer N., Negro-Vilar A. F., DeCherney A. H., Naftolin F. Renin-like activity in ovarian follicular fluid. Fertil Steril. 1985 Aug;44(2):219–223. doi: 10.1016/s0015-0282(16)48740-6. [DOI] [PubMed] [Google Scholar]
  11. Ferris T. F., Weir E. K. Effect of captopril on uterine blood flow and prostaglandin E synthesis in the pregnant rabbit. J Clin Invest. 1983 Apr;71(4):809–815. doi: 10.1172/JCI110834. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Ganong W. F. The brain renin-angiotensin system. Annu Rev Physiol. 1984;46:17–31. doi: 10.1146/annurev.ph.46.030184.000313. [DOI] [PubMed] [Google Scholar]
  13. Glorioso N., Atlas S. A., Laragh J. H., Jewelewicz R., Sealey J. E. Prorenin in high concentrations in human ovarian follicular fluid. Science. 1986 Sep 26;233(4771):1422–1424. doi: 10.1126/science.3529392. [DOI] [PubMed] [Google Scholar]
  14. Hamada Y., Wright K. H., Wallach E. E. In vitro reversal of indomethacin-blocked ovulation by prostaglandin F2alpha. Fertil Steril. 1978 Dec;30(6):702–706. [PubMed] [Google Scholar]
  15. Howard R. B., Pucell A. G., Bumpus F. M., Husain A. Rat ovarian renin: characterization and changes during the estrous cycle. Endocrinology. 1988 Nov;123(5):2331–2340. doi: 10.1210/endo-123-5-2331. [DOI] [PubMed] [Google Scholar]
  16. Husain A., Bumpus F. M., De Silva P., Speth R. C. Localization of angiotensin II receptors in ovarian follicles and the identification of angiotensin II in rat ovaries. Proc Natl Acad Sci U S A. 1987 Apr;84(8):2489–2493. doi: 10.1073/pnas.84.8.2489. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Ichikawa F., Yoshimura Y., Oda T., Shiraki M., Maruyama K., Kawakami S., Nakamura Y., Fukushima M. The effects of lipoxygenase products on progesterone and prostaglandin production by human corpora lutea. J Clin Endocrinol Metab. 1990 Apr;70(4):849–855. doi: 10.1210/jcem-70-4-849. [DOI] [PubMed] [Google Scholar]
  18. Itskovitz J., Rubattu S., Rosenwaks Z., Liu H. C., Sealey J. E. Relationship of follicular fluid prorenin to oocyte maturation, steroid levels, and outcome of in vitro fertilization. J Clin Endocrinol Metab. 1991 Jan;72(1):165–171. doi: 10.1210/jcem-72-1-165. [DOI] [PubMed] [Google Scholar]
  19. Itskovitz J., Sealey J. E., Glorioso N., Rosenwaks Z. Plasma prorenin response to human chorionic gonadotropin in ovarian-hyperstimulated women: correlation with the number of ovarian follicles and steroid hormone concentrations. Proc Natl Acad Sci U S A. 1987 Oct;84(20):7285–7289. doi: 10.1073/pnas.84.20.7285. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Kim S., Shinjo M., Fukamizu A., Miyazaki H., Usuki S., Murakami K. Identification of renin and renin messenger RNA sequence in rat ovary and uterus. Biochem Biophys Res Commun. 1987 Jan 15;142(1):169–175. doi: 10.1016/0006-291x(87)90466-9. [DOI] [PubMed] [Google Scholar]
  21. Kobayashi Y., Wright K. H., Santulli R., Wallach E. E. Ovulation and ovum maturation in the rabbit ovary perfused in vitro. Biol Reprod. 1981 Apr;24(3):483–490. doi: 10.1095/biolreprod24.3.483. [DOI] [PubMed] [Google Scholar]
  22. Kuo T. C., Endo K., Dharmarajan A. M., Miyazaki T., Atlas S. J., Wallach E. E. Direct effect of angiotensin II on in-vitro perfused rabbit ovary. J Reprod Fertil. 1991 Jul;92(2):469–474. doi: 10.1530/jrf.0.0920469. [DOI] [PubMed] [Google Scholar]
  23. Lightman A., Tarlatzis B. C., Rzasa P. J., Culler M. D., Caride V. J., Negro-Vilar A. F., Lennard D., DeCherney A. H., Naftolin F. The ovarian renin-angiotensin system: renin-like activity and angiotensin II/III immunoreactivity in gonadotropin-stimulated and unstimulated human follicular fluid. Am J Obstet Gynecol. 1987 Apr;156(4):808–816. doi: 10.1016/0002-9378(87)90336-x. [DOI] [PubMed] [Google Scholar]
  24. Morimoto T., Aoyama M., Gotoh E., Shionoiri H. [A method for radioimmunoassay of plasma angiotensin II using florisil]. Nihon Naibunpi Gakkai Zasshi. 1983 Mar 20;59(3):215–229. doi: 10.1507/endocrine1927.59.3_215. [DOI] [PubMed] [Google Scholar]
  25. Naruse K., Murakoshi M., Osamura R. Y., Naruse M., Toma H., Watanabe K., Demura H., Inagami T., Shizume K. Immunohistological evidence for renin in human endocrine tissues. J Clin Endocrinol Metab. 1985 Jul;61(1):172–177. doi: 10.1210/jcem-61-1-172. [DOI] [PubMed] [Google Scholar]
  26. Nasjletti A., Malik K. U. Relationships between the kallikrein-kinin and prostaglandin systems. Life Sci. 1979 Jul 9;25(2):99–109. doi: 10.1016/0024-3205(79)90380-1. [DOI] [PubMed] [Google Scholar]
  27. Ohkubo H., Nakayama K., Tanaka T., Nakanishi S. Tissue distribution of rat angiotensinogen mRNA and structural analysis of its heterogeneity. J Biol Chem. 1986 Jan 5;261(1):319–323. [PubMed] [Google Scholar]
  28. Pandey K. N., Melner M. H., Parmentier M., Inagami T. Demonstration of renin activity in purified rat Leydig cells: evidence for the existence of an endogenous inactive (latent) form of enzyme. Endocrinology. 1984 Nov;115(5):1753–1759. doi: 10.1210/endo-115-5-1753. [DOI] [PubMed] [Google Scholar]
  29. Pellicer A., Palumbo A., DeCherney A. H., Naftolin F. Blockage of ovulation by an angiotensin antagonist. Science. 1988 Jun 17;240(4859):1660–1661. doi: 10.1126/science.3381087. [DOI] [PubMed] [Google Scholar]
  30. Pucell A. G., Bumpus F. M., Husain A. Rat ovarian angiotensin II receptors. Characterization and coupling to estrogen secretion. J Biol Chem. 1987 May 25;262(15):7076–7080. [PubMed] [Google Scholar]
  31. Pucell A. G., Bumpus F. M., Husain A. Regulation of angiotensin II receptors in cultured rat ovarian granulosa cells by follicle-stimulating hormone and angiotensin II. J Biol Chem. 1988 Aug 25;263(24):11954–11961. [PubMed] [Google Scholar]
  32. Sandberg K., Bor M., Ji H., Markwick A., Millan M. A., Catt K. J. Angiotensin II-induced calcium mobilization in oocytes by signal transfer through gap junctions. Science. 1990 Jul 20;249(4966):298–301. doi: 10.1126/science.2374929. [DOI] [PubMed] [Google Scholar]
  33. Sealey J. E., Atlas S. A., Glorioso N., Manapat H., Laragh J. H. Cyclical secretion of prorenin during the menstrual cycle: synchronization with luteinizing hormone and progesterone. Proc Natl Acad Sci U S A. 1985 Dec;82(24):8705–8709. doi: 10.1073/pnas.82.24.8705. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Sealey J. E., Atlas S. A., Laragh J. H. Prorenin and other large molecular weight forms of renin. Endocr Rev. 1980 Fall;1(4):365–391. doi: 10.1210/edrv-1-4-365. [DOI] [PubMed] [Google Scholar]
  35. Sealey J. E., Cholst I., Glorioso N., Troffa C., Weintraub I. D., James G., Laragh J. H. Sequential changes in plasma luteinizing hormone and plasma prorenin during the menstrual cycle. J Clin Endocrinol Metab. 1987 Jul;65(1):1–5. doi: 10.1210/jcem-65-1-1. [DOI] [PubMed] [Google Scholar]
  36. Speth R. C., Husain A. Distribution of angiotensin-converting enzyme and angiotensin II-receptor binding sites in the rat ovary. Biol Reprod. 1988 Apr;38(3):695–702. doi: 10.1095/biolreprod38.3.695. [DOI] [PubMed] [Google Scholar]
  37. Squires P. M., Kennedy T. G. Evidence for a role for a uterine renin-angiotensin system in decidualization in rats. J Reprod Fertil. 1992 Aug;95(3):791–802. doi: 10.1530/jrf.0.0950791. [DOI] [PubMed] [Google Scholar]
  38. Velletri P. A. Testicular angiotensin I-converting enzyme (E.C. 3.4.15.1). Life Sci. 1985 Apr 29;36(17):1597–1608. doi: 10.1016/0024-3205(85)90362-5. [DOI] [PubMed] [Google Scholar]
  39. Whorton A. R., Young S. L., Data J. L., Barchowsky A., Kent R. S. Mechanism of bradykinin-stimulated prostacyclin synthesis in porcine aortic endothelial cells. Biochim Biophys Acta. 1982 Jul 20;712(1):79–87. doi: 10.1016/0005-2760(82)90087-x. [DOI] [PubMed] [Google Scholar]
  40. Yoshimura Y., Espey L., Hosoi Y., Adachi T., Atlas S. J., Ghodgaonkar R. B., Dubin N. H., Wallach E. E. The effects of bradykinin on ovulation and prostaglandin production by the perfused rabbit ovary. Endocrinology. 1988 Jun;122(6):2540–2546. doi: 10.1210/endo-122-6-2540. [DOI] [PubMed] [Google Scholar]
  41. Yoshimura Y., Karube M., Koyama N., Shiokawa S., Nanno T., Nakamura Y. Angiotensin II directly induces follicle rupture and oocyte maturation in the rabbit. FEBS Lett. 1992 Aug 3;307(3):305–308. doi: 10.1016/0014-5793(92)80701-h. [DOI] [PubMed] [Google Scholar]
  42. Yoshimura Y., Maruyama K., Shiraki M., Kawakami S., Fukushima M., Nakamura Y. Prolactin inhibits plasminogen activator activity in the preovulatory follicles. Endocrinology. 1990 Jan;126(1):631–636. doi: 10.1210/endo-126-1-631. [DOI] [PubMed] [Google Scholar]
  43. Yoshimura Y., Nakamura Y., Oda T., Ando M., Ubukata Y., Koyama N., Karube M., Yamada H. Effects of prolactin on ovarian plasmin generation in the process of ovulation. Biol Reprod. 1992 Mar;46(3):322–327. doi: 10.1095/biolreprod46.3.322. [DOI] [PubMed] [Google Scholar]
  44. Yoshimura Y., Nakamura Y., Oda T., Yamada H., Nanno T., Ando M., Ubukata Y., Suzuki M. Effects of gonadotropin-releasing hormone agonists on meiotic maturation of follicle-enclosed oocytes in rabbits. Biol Reprod. 1990 Dec;43(6):1012–1018. doi: 10.1095/biolreprod43.6.1012. [DOI] [PubMed] [Google Scholar]
  45. Yoshimura Y., Nakamura Y., Shiraki M., Hirota Y., Yamada H., Ando M., Ubukata Y., Suzuki M. Involvement of leukotriene B4 in ovulation in the rabbit. Endocrinology. 1991 Jul;129(1):193–199. doi: 10.1210/endo-129-1-193. [DOI] [PubMed] [Google Scholar]
  46. Yoshimura Y., Santulli R., Atlas S. J., Fujii S., Wallach E. E. The effects of proteolytic enzymes on in vitro ovulation in the rabbit. Am J Obstet Gynecol. 1987 Aug;157(2):468–475. doi: 10.1016/s0002-9378(87)80197-7. [DOI] [PubMed] [Google Scholar]
  47. Yoshimura Y., Wallach E. E. Studies of the mechanism(s) of mammalian ovulation. Fertil Steril. 1987 Jan;47(1):22–34. [PubMed] [Google Scholar]
  48. van Sande M. E., Scharpé S. L., Neels H. M., Van Camp K. O. Distribution of angiotensin converting enzyme in human tissues. Clin Chim Acta. 1985 Apr 30;147(3):255–260. doi: 10.1016/0009-8981(85)90207-4. [DOI] [PubMed] [Google Scholar]

Articles from Journal of Clinical Investigation are provided here courtesy of American Society for Clinical Investigation

RESOURCES