Endocrinology, Vol 137, 5191-5196, Copyright © 1996 by Endocrine Society

ARTICLES

Regulation of endothelin-1 expression in the bovine corpus luteum: elevation by prostaglandin F 2 alpha

E Girsh, W Wang, R Mamluk, F Arditi, A Friedman, RA Milvae and R Meidan
Department of Animal Science, Section of Reproduction, The Hebrew University of Jerusalem, Rehovot, Israel.

Prostaglandin F2alpha (PGF2alpha) has been recognized as the physiological luteolysin in ruminants and other species for more than three decades; however, the mechanisms involved in its action are poorly understood. We previously have shown that endothelin-1 (ET-1) mediates, at least in part, the action of PGF2alpha, and the current study examines the effect of PGF2alpha on the expression of ET-1 in bovine corpus luteum (CL). Endothelins (ETs) were extracted from CL, collected at various times of the estrous cycle, and highest levels were found during luteolysis. The expression of prepro-ET-1 was also highest in regressing CL, suggesting that PGF2alpha may have elevated ET-1 expression. This was confirmed by demonstrating that administration of PGF2alpha to heifers at midcycle elevated luteal ET-1 expression. Levels were induced as soon as 2 h after PGF2alpha treatment and 24 h later were 7-fold higher than preinjection levels. Endothelial cells isolated from bovine CL produced ET-1, and addition of PGF2alpha, oxytocin (OT), and vasopressin-augmented ET biosynthesis. Induction of ET-1 expression by PGF2alpha in these cells was evident after a short incubation time (15-90 min). Taken together, these data suggest that stimulation of luteal ET-1 expression by PGF2alpha may be achieved by several nonmutually exclusive mechanisms: 1) by acting directly on luteal endothelial cells; 2) indirectly, via OT release from large luteal cells; and 3) by causing hypoxia in the CL (as a result of ET-1-induced vasoconstriction). The latter mechanism may serve to augment ET-1 secretion in a positive-feedback process.

This article has been cited by other articles:

				K. Shirasuna, S. Watanabe, T. Asahi, M. P B Wijayagunawardane, K. Sasahara, C. Jiang, M. Matsui, M. Sasaki, T. Shimizu, J. S Davis, et al. Prostaglandin F2{alpha} increases endothelial nitric oxide synthase in the periphery of the bovine corpus luteum: the possible regulation of blood flow at an early stage of luteolysis Reproduction, April 1, 2008; 135(4): 527 - 539. [Abstract] [Full Text] [PDF]

				M. D. Doerr, M. P. Goravanahally, J. D. Rhinehart, E. K. Inskeep, and J. A. Flores Effects of Endothelin Receptor Type-A and Type-B Antagonists on Prostaglandin F2alpha-Induced Luteolysis of the Sheep Corpus Luteum Biol Reprod, April 1, 2008; 78(4): 688 - 696. [Abstract] [Full Text] [PDF]

				S. Erdmann, A. Ricken, C. Merkwitz, I. Struman, R. Castino, K. Hummitzsch, F. Gaunitz, C. Isidoro, J. Martial, and K. Spanel-Borowski The expression of prolactin and its cathepsin D-mediated cleavage in the bovine corpus luteum vary with the estrous cycle Am J Physiol Endocrinol Metab, November 1, 2007; 293(5): E1365 - E1377. [Abstract] [Full Text] [PDF]

				C. Boiti, M. Maranesi, C. Dall'Aglio, L. Pascucci, G. Brecchia, A. Gobbetti, and M. Zerani Vasoactive Peptides in the Luteolytic Process Activated by PGF2alpha in Pseudopregnant Rabbits at Different Luteal Stages Biol Reprod, July 1, 2007; 77(1): 156 - 164. [Abstract] [Full Text] [PDF]

				K. Shirasuna, T. Shimizu, K.-G. Hayashi, K. Nagai, M. Matsui, and A. Miyamoto Positive Association, in Local Release, of Luteal Oxytocin with Endothelin 1 and Prostaglandin F2alpha During Spontaneous Luteolysis in the Cow: A Possible Intermediatory Role for Luteolytic Cascade Within the Corpus Luteum Biol Reprod, June 1, 2007; 76(6): 965 - 970. [Abstract] [Full Text] [PDF]

				M. J Cannon, J. S Davis, and J. L Pate The class II major histocompatibility complex molecule BoLA-DR is expressed by endothelial cells of the bovine corpus luteum Reproduction, May 1, 2007; 133(5): 991 - 1003. [Abstract] [Full Text] [PDF]

				D. H. Townson Immune cell-endothelial cell interactions in the bovine corpus luteum Integr. Comp. Biol., December 1, 2006; 46(6): 1055 - 1059. [Abstract] [Full Text] [PDF]

				M. Rosiansky-Sultan, E. Klipper, K. Spanel-Borowski, and R. Meidan Inverse Relationship between Nitric Oxide Synthases and Endothelin-1 Synthesis in Bovine Corpus Luteum: Interactions at the Level of Luteal Endothelial Cell Endocrinology, November 1, 2006; 147(11): 5228 - 5235. [Abstract] [Full Text] [PDF]

				A. R. Liptak, B. T. Sullivan, L. E. Henkes, M. P.B. Wijayagunawardane, A. Miyamoto, J. S. Davis, B. R. Rueda, and D. H. Townson Cooperative Expression of Monocyte Chemoattractant Protein 1 Within the Bovine Corpus Luteum: Evidence of Immune Cell-Endothelial Cell Interactions in a Coculture System Biol Reprod, May 1, 2005; 72(5): 1169 - 1176. [Abstract] [Full Text] [PDF]

				C. Boiti, G. Guelfi, G. Brecchia, C. Dall'Aglio, P. Ceccarelli, M. Maranesi, C. Mariottini, D. Zampini, A. Gobbetti, and M. Zerani Role of the Endothelin-1 System in the Luteolytic Process of Pseudopregnant Rabbits Endocrinology, March 1, 2005; 146(3): 1293 - 1300. [Abstract] [Full Text] [PDF]

				E. Choudhary, A. Sen, E. K. Inskeep, and J. A. Flores Developmental Sensitivity of the Bovine Corpus Luteum to Prostaglandin F2{alpha} (PGF2{alpha}) and Endothelin-1 (ET-1): Is ET-1 a Mediator of the Luteolytic Actions of PGF2{alpha} or a Tonic Inhibitor of Progesterone Secretion? Biol Reprod, March 1, 2005; 72(3): 633 - 642. [Abstract] [Full Text] [PDF]

				K. Shirasuna, H. Asaoka, T. J. Acosta, M. P.B. Wijayagunawardane, M. Ohtani, M. Hayashi, M. Matsui, and A. Miyamoto Real-Time Relationships in Intraluteal Release among Prostaglandin F2{alpha}, Endothelin-1, and Angiotensin II During Spontaneous Luteolysis in the Cow Biol Reprod, November 1, 2004; 71(5): 1706 - 1711. [Abstract] [Full Text] [PDF]

				E. Klipper, T. Gilboa, N. Levy, T. Kisliouk, K. Spanel-Borowski, and R. Meidan Characterization of endothelin-1 and nitric oxide generating systems in corpus luteum-derived endothelial cells Reproduction, October 1, 2004; 128(4): 463 - 473. [Abstract] [Full Text] [PDF]

				K. Shirasuna, H. Asaoka, T. J Acosta, M. P B Wijayagunawardane, M. Ohtani, K.-G. Hayashi, M. Matsui, and A. Miyamoto Real-time dynamics of prostaglandin F2{alpha} release from uterus and corpus luteum during spontaneous luteolysis in the cow Reproduction, August 1, 2004; 128(2): 189 - 195. [Abstract] [Full Text] [PDF]

				A. Sen, J. Browning, E. K. Inskeep, P. Lewis, and J. A. Flores Expression and Activation of Protein Kinase C Isozymes by Prostaglandin F2{alpha} in the Early- and Mid-Luteal Phase Bovine Corpus Luteum Biol Reprod, February 1, 2004; 70(2): 379 - 384. [Abstract] [Full Text] [PDF]

				M Ohtani, S Takase, M P B Wijayagunawardane, M Tetsuka, and A Miyamoto Local interaction of prostaglandin F2{alpha} with endothelin-1 and tumor necrosis factor-{alpha} on the release of progesterone and oxytocin in ovine corpora lutea in vivo: a possible implication for a luteolytic cascade Reproduction, January 1, 2004; 127(1): 117 - 124. [Abstract] [Full Text] [PDF]

				D. J. Skarzynski, J. J. Jaroszewski, M. M. Bah, K. M. Deptula, B. Barszczewska, B. Gawronska, and W. Hansel Administration of a Nitric Oxide Synthase Inhibitor Counteracts Prostaglandin F2-Induced Luteolysis in Cattle Biol Reprod, May 1, 2003; 68(5): 1674 - 1681. [Abstract] [Full Text] [PDF]

				N. Levy, M. Gordin, M. F. Smith, O. U. Bolden-Tiller, and R. Meidan Hormonal Regulation and Cell-Specific Expression of Endothelin-Converting Enzyme 1 Isoforms in Bovine Ovarian Endothelial and Steroidogenic Cells Biol Reprod, April 1, 2003; 68(4): 1361 - 1368. [Abstract] [Full Text] [PDF]

				V. A. Cavicchio, J. K. Pru, B. S. Davis, J. S. Davis, B. R. Rueda, and D. H. Townson Secretion of Monocyte Chemoattractant Protein-1 by Endothelial Cells of the Bovine Corpus Luteum: Regulation by Cytokines But Not Prostaglandin F2{alpha} Endocrinology, September 1, 2002; 143(9): 3582 - 3589. [Abstract] [Full Text] [PDF]

				T. J. Acosta, N. Yoshizawa, M. Ohtani, and A. Miyamoto Local Changes in Blood Flow Within the Early and Midcycle Corpus Luteum after Prostaglandin F2{alpha} Injection in the Cow Biol Reprod, March 1, 2002; 66(3): 651 - 658. [Abstract] [Full Text] [PDF]

				S.-i. Kobayashi, T. J. Acosta, T. Ozawa, K. Hayashi, B. Berisha, M. Ohtani, D. Schams, and A. Miyamoto Intraluteal Release of Angiotensin II and Progesterone In Vivo During Corpora Lutea Development in the Cow: Effect of Vasoactive Peptides Biol Reprod, January 1, 2002; 66(1): 174 - 179. [Abstract] [Full Text]

				N. Levy, M. Gordin, R. Mamluk, M. Yanagisawa, M. F. Smith, J. H. Hampton, and R. Meidan Distinct Cellular Localization and Regulation of Endothelin-1 and Endothelin-Converting Enzyme-1 Expression in the Bovine Corpus Luteum: Implications for Luteolysis Endocrinology, December 1, 2001; 142(12): 5254 - 5260. [Abstract] [Full Text] [PDF]

				M. F. Wright, B. Sayre, E. Keith Inskeep, and J. A. Flores Prostaglandin F2{alpha} Regulation of the Bovine Corpus Luteum Endothelin System During the Early and Midluteal Phase Biol Reprod, December 1, 2001; 65(6): 1710 - 1717. [Abstract] [Full Text] [PDF]

				S.T. Hinckley and R.A. Milvae Endothelin-1 Mediates Prostaglandin F2{{alpha}}-Induced Luteal Regression in the Ewe Biol Reprod, June 1, 2001; 64(6): 1619 - 1623. [Abstract] [Full Text]

				F. Miceli, F. Minici, M. G. Pardo, P. Navarra, C. Proto, S. Mancuso, A. Lanzone, and R. Apa Endothelins Enhance Prostaglandin (PGE2 and PGF2{{alpha}}) Biosynthesis and Release by Human Luteal Cells: Evidence of a New Paracrine/Autocrine Regulation of Luteal Function J. Clin. Endocrinol. Metab., February 1, 2001; 86(2): 811 - 817. [Abstract] [Full Text]

				C.-J. Tai, S. K. Kang, K.-C. Choi, C.-R. Tzeng, and P. C. K. Leung Role of Mitogen-Activated Protein Kinase in Prostaglandin F2{{alpha}} Action in Human Granulosa-Luteal Cells J. Clin. Endocrinol. Metab., January 1, 2001; 86(1): 375 - 380. [Abstract] [Full Text]

				J. A. Flores Gene Expression of Endothelin-1 in the Porcine Ovary: Follicular Development Biol Reprod, November 1, 2000; 63(5): 1377 - 1382. [Abstract] [Full Text]

				N. Levy, S.-i. Kobayashi, Z. Roth, D. Wolfenson, A. Miyamoto, and R. Meidan Administration of Prostaglandin F2{alpha} During the Early Bovine Luteal Phase Does Not Alter the Expression of ET-1 and of Its Type A Receptor: A Possible Cause for Corpus Luteum Refractoriness Biol Reprod, August 1, 2000; 63(2): 377 - 382. [Abstract] [Full Text]

				J. J. Jaroszewski and W. Hansel Intraluteal Administration of a Nitric Oxide Synthase Blocker Stimulates Progesterone and Oxytocin Secretion and Prolongs the Life Span of the Bovine Corpus Luteum Experimental Biology and Medicine, May 1, 2000; 224(1): 50 - 55. [Abstract] [Full Text]

				G. D. Niswender, J. L. Juengel, P. J. Silva, M. K. Rollyson, and E. W. McIntush Mechanisms Controlling the Function and Life Span of the Corpus Luteum Physiol Rev, January 1, 2000; 80(1): 1 - 29. [Abstract] [Full Text] [PDF]

				G. G. Nussdorfer, G. P. Rossi, L. K. Malendowicz, and G. Mazzocchi Autocrine-Paracrine Endothelin System in the Physiology and Pathology of Steroid-Secreting Tissues Pharmacol. Rev., September 1, 1999; 51(3): 403 - 438. [Abstract] [Full Text] [PDF]

				R. Mamluk, N. Levy, B. Rueda, J. S. Davis, and R. Meidan Characterization and Regulation of Type A Endothelin Receptor Gene Expression in Bovine Luteal Cell Types Endocrinology, May 1, 1999; 140(5): 2110 - 2116. [Abstract] [Full Text]

				K. Hayashi and A. Miyamoto Angiotensin II Interacts with Prostaglandin F2{alpha} and Endothelin-1 as a Local Luteolytic Factor in the Bovine Corpus Luteum In Vitro Biol Reprod, May 1, 1999; 60(5): 1104 - 1109. [Abstract] [Full Text]

				J. A. McCracken, E. E. Custer, and J. C. Lamsa Luteolysis: A Neuroendocrine-Mediated Event Physiol Rev, April 1, 1999; 79(2): 263 - 323. [Abstract] [Full Text] [PDF]

				J. J. Evans Modulation of Gonadotropin Levels by Peptides Acting at the Anterior Pituitary Gland Endocr. Rev., February 1, 1999; 20(1): 46 - 67. [Abstract] [Full Text]