Endocrinology, Vol 130, 3095-3097, Copyright © 1992 by Endocrine Society

ARTICLES

Interleukin-1 stimulates ovarian prostaglandin biosynthesis: evidence for heterologous contact-independent cell-cell interaction

E Kokia, A Hurwitz, E Ricciarelli, C Tedeschi, CE Resnick, MD Mitchell and EY Adashi
Department of Obstetrics/Gynecology, University of Maryland School of Medicine, Baltimore 21201.

An increasing body of information now suggests the existence of a complete intraovarian IL-1 system replete with ligands, receptor, and receptor antagonist. Since IL-1 is an established mediator of inflammation and since ovulation may constitute an inflammatory-like reaction, consideration may be given to the possibility that IL-1 may play an intermediary role in the ovulatory process. To further assess the above hypothesis, we have set out to determine whether IL-1 is capable of promoting ovarian prostaglandin biosynthesis, an established component of the ovulatory cascade. Cultured whole ovarian dispersates from immature (25 day old) rats constitutively elaborated major prostaglandin species (PGE2 greater than PGF2 alpha) in a cell density- dependent fashion. Treatment with IL-1 produced dose-dependent increments in prostaglandin (PGE2 greater than PGF2 alpha) accumulation as compared with untreated controls. Comparable cellular densities of untreated or IL-1 beta-treated whole ovarian dispersates elaborated substantially more PGE2 as compared with isolated granulosa or theca- interstitial cell preparations suggesting a requirement for cell-cell interaction. Indeed, cell contact-dependent reconstitution experiments involving isolated granulosa and theca-interstitial cells at a projected physiologic ratio of 4:1 revealed synergistic interactions in the elaboration of PGE2 under both basal and IL-1 beta-treated circumstances. Identical results were obtained for cell contact- independent heterologous (but not homologous) coculture experiments. Taken together, our present findings reveal optimal basal and IL-1- stimulated ovarian prostaglandin (PGE2 greater than PGF2 alpha) biosynthesis to require heterologous, contact-independent, presumably humorally-mediated, cell-cell interaction. These observations along with the demonstration of the gonadotropin-dependent preovulatory induction of ovarian IL-1 beta gene expression provide strong support for the view that IL-1 may be the centerpiece of an intraovarian regulatory loop concerned with the promotion of the preovulatory cascade.

This article has been cited by other articles:

				S O'Leary, M J Jasper, S A Robertson, and D T Armstrong Seminal plasma regulates ovarian progesterone production, leukocyte recruitment and follicular cell responses in the pig Reproduction, July 1, 2006; 132(1): 147 - 158. [Abstract] [Full Text] [PDF]

				T. E. Curry Jr. and K. G. Osteen The Matrix Metalloproteinase System: Changes, Regulation, and Impact throughout the Ovarian and Uterine Reproductive Cycle Endocr. Rev., August 1, 2003; 24(4): 428 - 465. [Abstract] [Full Text] [PDF]

				A. Martoriati, G. Duchamp, and N. Gerard In Vivo Effect of Epidermal Growth Factor, Interleukin-1{beta}, and Interleukin-1RA on Equine Preovulatory Follicles Biol Reprod, May 1, 2003; 68(5): 1748 - 1754. [Abstract] [Full Text] [PDF]

				A. Martoriati, A.-C. Lalmanach, G. Goudet, and N. Gerard Expression of Interleukin-1 (IL-1) System Genes in Equine Cumulus-Oocyte Complexes and Influence of IL-1{beta} During In Vitro Maturation Biol Reprod, August 1, 2002; 67(2): 630 - 636. [Abstract] [Full Text] [PDF]

				J. Saito, M. Ando, D. Sussman, H. Negishi, G. King, and E. Y. Adashi Interleukin 1 Upregulates Ovarian Prostaglandin Endoperoxide Synthase-2 Expression: Evidence for Prostaglandin-Dependent/Ceramide-Independent Transcriptional Stimulation and for Message Stabilization Biol Reprod, December 1, 2001; 65(6): 1759 - 1765. [Abstract] [Full Text] [PDF]

				K. W. Chung, M. Ando, and E. Y. Adashi Periovulatory and Interleukin (IL)-1--Dependent Reglation of IL-6 in the Immature Rat Ovary: A Specific IL-1 Receptor-Mediated Eicosanoid-Dependent Effect Reproductive Sciences, September 1, 2000; 7(5): 301 - 308. [Abstract] [PDF]

				E. Levitas, D. Chamoun, L. C. Udoff, M. Ando, C. E. Resnick, and E. Y. Adashi Periovulatory and Interleukin-1{beta}-Dependent Up-Regulation of Intraovarian Vascular Endothelial Growth Factor (VEGF) in the Rat: Potential Role for VEGF in the Promotion of Periovulatory Angiogenesis and Vascular Permeability Reproductive Sciences, January 1, 2000; 7(1): 51 - 60. [Abstract] [PDF]

				D. Chamoun, M. D. DeMoura, E. Levitas, C. E. Resnick, S. E. Gargosky, R. G. Rosenfeld, T. Matsumoto, and E. Y. Adashi Transcriptional and Posttranscriptional Regulation of Intraovarian Insulin-Like Growth Factor-Binding Proteins by Interleukin-1{beta} (IL-1{beta}): Evidence for IL-1{beta} as an Antiatretic Principal Endocrinology, August 1, 1999; 140(8): 3488 - 3495. [Abstract] [Full Text]

				S. Kol, B. W. Donesky, K. Ruutiainen-Altman, I. Ben-Shlomo, M. Irahara, M. Ando, R. M. Rohan, and E. Y. Adashi Ovarian Interleukin-1 Receptor Antagonist in Rats: Gene Expression, Cellular Localization, Cyclic Variation, and Hormonal Regulation of a Potential Determinant of Interleukin-1 Action Biol Reprod, July 1, 1999; 61(1): 274 - 282. [Abstract] [Full Text]

				B. J. Davis, D. E. Lennard, C. A. Lee, H. F. Tiano, S. G. Morham, W. C. Wetsel, and R. Langenbach Anovulation in Cyclooxygenase-2-Deficient Mice Is Restored by Prostaglandin E2 and Interleukin-1{beta} Endocrinology, June 1, 1999; 140(6): 2685 - 2695. [Abstract] [Full Text]

				M. Irahara, M. Ando, J. Sirois, J. Saito, and E. Y. Adashi Glucocorticoid Receptor-Mediated Post-Ceramide Inhibition of the Interleukin-1ß-Dependent Induction of Ovarian Prostaglandin Endoperoxide Synthase-2 in Rats Biol Reprod, April 1, 1999; 60(4): 946 - 953. [Abstract] [Full Text]

				M. José de los Santos, D. J. Anderson, C. Racowsky, C. Simón, and J. A. Hill Expression of Interleukin-1 System Genes in Human Gametes Biol Reprod, December 1, 1998; 59(6): 1419 - 1424. [Abstract] [Full Text]

				M. Ando, S. Kol, E. Kokia, K. Ruutiainen-Altman, J. Sirois, R. M. Rohan, D. W. Payne, and E. Y. Adashi Rat Ovarian Prostaglandin Endoperoxide Synthase-1 and -2: Periovulatory Expression of Granulosa Cell-Based Interleukin-1-Dependent Enzymes Endocrinology, May 1, 1998; 139(5): 2501 - 2508. [Abstract] [Full Text] [PDF]

				K. Narko, O. Ritvos, and A. Ristimaki Induction of Cyclooxygenase-2 and Prostaglandin F2{alpha} Receptor Expression by Interleukin-1{beta} in Cultured Human Granulosa-Luteal Cells Endocrinology, September 1, 1997; 138(9): 3638 - 3644. [Abstract] [Full Text] [PDF]

				S. Kol, I. Ben-Shlomo, M. Ando, D. W. Payne, and E. Y. Adashi Interleukin-1{beta} Stimulates Ovarian Phospholipase A2 (PLA2) Expression and Activity: Up-Regulation of Both Secretory and Cytosolic PLA2 Endocrinology, January 1, 1997; 138(1): 314 - 321. [Abstract] [Full Text] [PDF]

				S. Kol, K. Ruutiainen-Altman, I. Ben-Shlomo, D. W. Payne, M. Ando, and E. Y. Adashi The Rat Ovarian Phospholipase A2 System: Gene Expression, Cellular Localization, Activity Characterization, and Interleukin-1 Dependence Endocrinology, January 1, 1997; 138(1): 322 - 331. [Abstract] [Full Text] [PDF]

				W. J. Scherzer, K. S. L. Ruutiainen-Altman, L. T. Putowski, S. Kol, E. Y. Adashi, and R. M. Rohan Detection and In Vivo Hormonal Regulation of Rat Ovarian Type I and Type II Interleukin-I Rececptor mRNAs: Increased Expression During the Periovulatory Period Reproductive Sciences, May 1, 1996; 3(3): 131 - 139. [Abstract] [PDF]

				A. Hurwitz, Z. Finci-Yeheskel, M. Dushnik, A. Milwidsky, S. Shimonovitz, S. Yagel, E. Y. Adashi, and M. Mayer Interleukin-1-Mediated Regulation of Plasminogen Activation in Pregnant Mare Serum Gonadotropin-Primed Rat Granulosa Cells Is Independent of Prostaglandin Production Reproductive Sciences, September 1, 1995; 2(5): 691 - 699. [Abstract] [PDF]

				D. W. Payne, C. Shackleton, H. Toms, I. Ben-Shlomo, S. Kol, M. deMoura, J. F. Strauss, and E. Y. Adashi A Novel Nonhepatic Hydroxycholesterol 7alpha-Hydroxylase That Is Markedly Stimulated by Interleukin-1beta J. Biol. Chem., August 11, 1995; 270(32): 18888 - 18896. [Abstract] [Full Text] [PDF]