A tale of two endothelins: the rise and fall of the corpus luteum
Magdalena Szymanska A B , Raghavendra Basavaraja A C and Rina Meidan A *A
B Present address:
C Present address:
Abstract
Endothelins are small 21 amino acid peptides that interact with G-protein-coupled receptors. They are highly conserved across species and play important roles in vascular biology as well as in disease development and progression. Endothelins, mainly endothelin-1 and endothelin-2, are intricately involved in ovarian function and metabolism. These two peptides differ only in two amino acids but are encoded by different genes, which suggests an independent regulation and a cell-specific mode of expression. This review aims to comprehensively discuss the distinct regulation and roles of endothelin-1 and endothelin-2 regarding corpus luteum function throughout its life span.
Keywords: corpus luteum, endothelin-1, endothelin-2, hypoxia, interferon tau, PCOS, prostaglandin F2 alpha, sirtuin 1.
References
Adams JM, Difazio LT, Rolandelli RH, Lujan JJ, Hasko G, Csoka B, Selmeczy Z, Nemeth ZH (2009) HIF-1: a key mediator in hypoxia. Acta Physiologica Hungarica 96(1), 19-28.
| Crossref | Google Scholar | PubMed |
Antoniazzi AQ, Webb BT, Romero JJ, Ashley RL, Smirnova NP, Henkes LE, Bott RC, Oliveira JF, Niswender GD, Bazer FW, Hansen TR (2013) Endocrine delivery of interferon tau protects the corpus luteum from prostaglandin F2 alpha-induced luteolysis in ewes. Biology of Reproduction 88(6), 144.
| Crossref | Google Scholar | PubMed |
Apa R, Miceli F, de Feo D, Mastrandrea ML, Mancuso S, Napolitano M, Lanzone A (1998a) Endothelin-1 inhibits basal and human chorionic gonadotrophin-stimulated progesterone production. Human Reproduction 13(9), 2425-2429.
| Crossref | Google Scholar | PubMed |
Apa R, Miceli F, de Feo D, Pierro E, Ayala G, Mancuso S, Napolitano M, Lanzone A (1998b) Endothelin-1: expression and role in human corpus luteum. American Journal of Reproductive Immunology 40(5), 370-376.
| Crossref | Google Scholar | PubMed |
Arai H, Hori S, Aramori I, Ohkubo H, Nakanishi S (1990) Cloning and expression of a cDNA encoding an endothelin receptor. Nature 348(6303), 730-732.
| Crossref | Google Scholar | PubMed |
Aramori I, Nakanishi S (1992) Coupling of two endothelin receptor subtypes to differing signal transduction in transfected Chinese hamster ovary cells. Journal of Biological Chemistry 267(18), 12468-12474.
| Crossref | Google Scholar | PubMed |
Arinami T, Ishikawa M, Inoue A, Yanagisawa M, Masaki T, Yoshida MC, Hamaguchi H (1991) Chromosomal assignments of the human endothelin family genes: the endothelin-1 gene (EDN1) to 6p23-p24, the endothelin-2 gene (EDN2) to 1p34, and the endothelin-3 gene (EDN3) to 20q13.2-q13.3. American Journal of Human Genetics 48(5), 990-996.
| Google Scholar | PubMed |
Balen AH, Morley LC, Misso M, Franks S, Legro RS, Wijeyaratne CN, Stener-Victorin E, Fauser BCJM, Norman RJ, Teede H (2016) The management of anovulatory infertility in women with polycystic ovary syndrome: an analysis of the evidence to support the development of global WHO guidance. Human Reproduction Update 22(6), 687-708.
| Crossref | Google Scholar | PubMed |
Banecki KMRM, Dora KA (2023) Endothelin-1 in health and disease. International Journal of Molecular Sciences 24(14), 11295.
| Crossref | Google Scholar | PubMed |
Basavaraja R, Przygrodzka E, Pawlinski B, Gajewski Z, Kaczmarek MM, Meidan R (2017) Interferon-tau promotes luteal endothelial cell survival and inhibits specific luteolytic genes in bovine corpus luteum. Reproduction 154(5), 559-568.
| Crossref | Google Scholar | PubMed |
Basavaraja R, Madusanka ST, Drum JN, Shrestha K, Farberov S, Wiltbank MC, Sartori R, Meidan R (2019) Interferon-tau exerts direct prosurvival and antiapoptotic actions in luteinized bovine granulosa cells. Scientific Reports 9(1), 14682.
| Crossref | Google Scholar | PubMed |
Basavaraja R, Madusanka ST, Shrestha K, Przygrodzka E, Kaczmarek MM, Meidan R (2020) Pentraxin-3 mediates prosurvival actions of interferon tau in bovine luteinized granulosa cells. Reproduction 160(4), 603-612.
| Crossref | Google Scholar | PubMed |
Basavaraja R, Drum JN, Sapuleni J, Bibi L, Friedlander G, Kumar S, Sartori R, Meidan R (2021) Downregulated luteolytic pathways in the transcriptome of early pregnancy bovine corpus luteum are mimicked by interferon-tau in vitro. BMC Genomics 22(1), 452.
| Crossref | Google Scholar | PubMed |
Bazer FW, Spencer TE, Thatcher WW (2012) Growth and development of the ovine conceptus. Journal of Animal Science 90(1), 159-170.
| Crossref | Google Scholar | PubMed |
Bazer FW, Ying W, Wang X, Dunlap KA, Zhou B, Johnson GA, Wu G (2015) The many faces of interferon tau. Amino Acids 47(3), 449-460.
| Crossref | Google Scholar | PubMed |
Beindorff N, Nagai K, Shirasuna K, Herzog K, Hoeffmann K, Sasaki M, Bollwein H, Miyamoto A (2010) Vascular changes in the corpus luteum during early pregnancy in the cow. Journal of Reproduction and Development 56(2), 263-270.
| Crossref | Google Scholar | PubMed |
Berisha B, Schams D (2005) Ovarian function in ruminants. Domestic Animal Endocrinology 29(2), 305-317.
| Crossref | Google Scholar | PubMed |
Berisha B, Schams D, Miyamoto A (2002) The expression of angiotensin and endothelin system members in bovine corpus luteum during estrous cycle and pregnancy. Endocrine 19(3), 305-312.
| Crossref | Google Scholar | PubMed |
Bharati J, Mohan NH, Kumar S, Gogoi J, Kumar S, Jose B, Punetha M, Borah S, Kumar A, Sarkar M (2021) Transcriptome profiling of different developmental stages of corpus luteum during the estrous cycle in pigs. Genomics 113(1), 366-379.
| Crossref | Google Scholar | PubMed |
Boiti C, Guelfi G, Brecchia G, Dall’Aglio C, Ceccarelli P, Maranesi M, Mariottini C, Zampini D, Gobbetti A, Zerani M (2005) Role of the endothelin-1 system in the luteolytic process of pseudopregnant rabbits. Endocrinology 146(3), 1293-1300.
| Crossref | Google Scholar | PubMed |
Boonyaprakob U, Gadsby JE, Hedgpeth V, Routh PA, Almond GW (2005) Expression and localization of hypoxia inducible factor-1alpha mRNA in the porcine ovary. Canadian Journal of Veterinary Research 69(3), 215-222.
| Google Scholar | PubMed |
Bordone L, Cohen D, Robinson A, Motta MC, van Veen E, Czopik A, Steele AD, Crowe H, Marmor S, Luo J, Gu W, Guarente L (2007) SIRT1 transgenic mice show phenotypes resembling calorie restriction. Aging Cell 6(6), 759-767.
| Crossref | Google Scholar | PubMed |
Cacioppo JA, Oh SW, Kim HY, Cho J, Lin PCP, Yanagisawa M, Ko C (2014) Loss of function of endothelin-2 leads to reduced ovulation and CL formation. PLoS ONE 9(4), e96115.
| Crossref | Google Scholar | PubMed |
Camps C, Buffa FM, Colella S, Moore J, Sotiriou C, Sheldon H, Harris AL, Gleadle JM, Ragoussis J (2008) hsa-miR-210 Is induced by hypoxia and is an independent prognostic factor in breast cancer. Clinical Cancer Research 14(5), 1340-1348.
| Crossref | Google Scholar | PubMed |
Cao LY, Zhang ZQ, Liu PP, Xu DF, Tang L, Fan L, Sun XC, Li JY, Wu QF, Li ZM, Tan J (2022) Aberrant BMP15/HIF-1α/SCF signaling pathway in human granulosa cells is involved in the PCOS related abnormal follicular development. Gynecological Endocrinology 38(11), 971-977.
| Crossref | Google Scholar | PubMed |
Chan SY, Loscalzo J (2010) MicroRNA-210: a unique and pleiotropic hypoxamir. Cell Cycle 9(6), 1072-1083.
| Crossref | Google Scholar | PubMed |
Costine BA, Inskeep EK, Blemings KP, Flores JA, Wilson ME (2007) Mechanisms of reduced luteal sensitivity to prostaglandin F2α during maternal recognition of pregnancy in ewes. Domestic Animal Endocrinology 32(2), 106-121.
| Crossref | Google Scholar | PubMed |
Cuyas E, Verdura S, Llorach-Pares L, Fernandez-Arroyo S, Joven J, Martin-Castillo B, Bosch-Barrera J, Brunet J, Nonell-Canals A, Sanchez-Martinez M, Menendez JA (2018) Metformin is a direct SIRT1-activating compound: computational modeling and experimental validation. Frontiers in Endocrinology 9, 657.
| Crossref | Google Scholar | PubMed |
Davis JS, Rueda BR, Spanel-Borowski K (2003) Microvascular endothelial cells of the corpus luteum. Reproductive Biology and Endocrinology 1, 89.
| Crossref | Google Scholar | PubMed |
Denkova R, Bourneva V, Yaneva E, Baleva K, Nikolov B, Ivanov I, Simeonov K, Timeva T (2002) Potential role of nitric oxide in endothelin-1 provoked inhibition of progesterone secretion by isolated ovarian granulosa cells. Endocrine Regulations 36(1), 19-22.
| Google Scholar | PubMed |
Devlin C, Greco S, Martelli F, Ivan M (2011) miR-210: More than a silent player in hypoxia. IUBMB Life 63(2), 94-100.
| Crossref | Google Scholar | PubMed |
Diskin MG, Morris DG (2008) Embryonic and early foetal losses in cattle and other ruminants. Reproduction in Domestic Animals 43(Suppl 2), 260-267.
| Crossref | Google Scholar | PubMed |
Doerr MD, Goravanahally MP, Rhinehart JD, Inskeep EK, Flores JA (2008) Effects of endothelin receptor type-A and type-B antagonists on prostaglandin F2alpha-induced luteolysis of the sheep corpus luteum. Biology of Reproduction 78(4), 688-696.
| Crossref | Google Scholar | PubMed |
Duncan WC, van den Driesche S, Fraser HM (2008) Inhibition of vascular endothelial growth factor in the primate ovary up-regulates hypoxia-inducible factor-1α in the follicle and corpus luteum. Endocrinology 149(7), 3313-3320.
| Crossref | Google Scholar | PubMed |
Ervin JM, Schütz LF, Spicer LJ (2017) Current status of the role of endothelins in regulating ovarian follicular function: a review. Animal Reproduction Science 186, 1-10.
| Crossref | Google Scholar | PubMed |
Farberov S, Meidan R (2016) Thrombospondin-1 affects bovine luteal function via transforming growth factor-beta1-dependent and independent actions. Biology of Reproduction 94(1), 25.
| Crossref | Google Scholar | PubMed |
Farhat N, Matouk CC, Mamarbachi AM, Marsden PA, Allen BG, Thorin E (2008) Activation of ETB receptors regulates the abundance of ET-1 mRNA in vascular endothelial cells. British Journal of Pharmacology 153(7), 1420-1431.
| Crossref | Google Scholar | PubMed |
Ferreira-Dias G, Costa AS, Mateus L, Korzekwa A, Redmer DA, Skarzynski DJ (2006) Proliferative processes within the equine corpus luteum may depend on paracrine progesterone actions. Journal of Physiology and Pharmacology 57(Suppl 8), 139-151.
| Google Scholar |
Flores JA, Garmey JC, Lahav M, Veldhuis JD (1999) Mechanisms underlying endothelin’s inhibition of FSH-stimulated progesterone production by ovarian granulosa cells. Molecular and Cellular Endocrinology 156(1–2), 169-178.
| Crossref | Google Scholar | PubMed |
Fraser HM, Wulff C (2003) Angiogenesis in the corpus luteum. Reproductive Biology and Endocrinology 1, 88.
| Crossref | Google Scholar | PubMed |
Fu X, Shi L, Liu P, Jiao Y, Guo S, Chen Q, Zheng Q, Chen X, Wang Y (2023) Expression and clinical significance of HIF-1α in follicular fluid and granulosa cells in infertile PCOS patients. Reproductive Sciences 30(7), 2263-2274.
| Crossref | Google Scholar | PubMed |
Gabler C, Plath-Gabler A, Killian GJ, Berisha B, Schams D (2004) Expression pattern of fibroblast growth factor (FGF) and vascular endothelial growth factor (VEGF) system members in bovine corpus luteum endothelial cells during treatment with FGF-2, VEGF or oestradiol. Reproduction in Domestic Animals 39(5), 321-327.
| Crossref | Google Scholar | PubMed |
Gecaj RM, Schanzenbach CI, Kirchner B, Pfaffl MW, Riedmaier I, Tweedie-Cullen RY, Berisha B (2017) The dynamics of microRNA transcriptome in bovine corpus luteum during its formation, function, and regression. Frontiers in Genetics 8, 213.
| Crossref | Google Scholar |
Girsh E, Dekel N (2002) Involvement of endothelin-1 and its receptors in PGF2α-induced luteolysis in the rat. Molecular Reproduction and Development 63(1), 71-78.
| Crossref | Google Scholar | PubMed |
Girsh E, Greber Y, Meidan R (1995) Luteotrophic and luteolytic interactions between bovine small and large luteal-like cells and endothelial cells. Biology of Reproduction 52(4), 954-962.
| Crossref | Google Scholar | PubMed |
Girsh E, Milvae RA, Wang W, Meidan R (1996a) Effect of endothelin-1 on bovine luteal cell function: role in prostaglandin F2alpha-induced antisteroidogenic action. Endocrinology 137(4), 1306-1312.
| Crossref | Google Scholar | PubMed |
Girsh E, Wang W, Mamluk R, Arditi F, Friedman A, Milvae RA, Meidan R (1996b) Regulation of endothelin-1 expression in the bovine corpus luteum: elevation by prostaglandin F 2 alpha. Endocrinology 137(12), 5191-5196.
| Crossref | Google Scholar | PubMed |
Gram A, Boos A, Kowalewski MP (2017) Cellular localization, expression and functional implications of the utero-placental endothelin system during maintenance and termination of canine gestation. Journal of Reproduction and Development 63(3), 235-245.
| Crossref | Google Scholar | PubMed |
Han Y, Luo H, Wang H, Cai J, Zhang Y (2017) SIRT1 induces resistance to apoptosis in human granulosa cells by activating the ERK pathway and inhibiting NF-κB signaling with anti-inflammatory functions. Apoptosis 22(10), 1260-1272.
| Crossref | Google Scholar | PubMed |
Hansel W, Cain G (1996) The bovine corpus luteum. Theriogenology 45(7), 1265-1266.
| Crossref | Google Scholar | PubMed |
Hansel W, Alila HW, Dowd JP, Milvae RA (1991) Differential origin and control mechanisms in small and large bovine luteal cells. J Reprod Fertil Suppl 43, 77-89.
| Google Scholar | PubMed |
Hansen TR, Henkes LK, Ashley RL, Bott RC, Antoniazzi AQ, Han H (2010) Endocrine actions of interferon-tau in ruminants. Society for Reproduction and Fertility Supplement 67, 325-340.
| Crossref | Google Scholar | PubMed |
Hinckley ST, Milvae RA (2001) Endothelin-1 mediates prostaglandin F(2alpha)-induced luteal regression in the ewe. Biology of Reproduction 64(6), 1619-1623.
| Crossref | Google Scholar | PubMed |
Hohos NM, Cho KJ, Swindle DC, Skaznik-Wikiel ME (2018) High-fat diet exposure, regardless of induction of obesity, is associated with altered expression of genes critical to normal ovulatory function. Molecular and Cellular Endocrinology 470, 199-207.
| Crossref | Google Scholar | PubMed |
Hohos NM, Elliott EM, Giornazi A, Silva E, Rice JD, Skaznik-Wikiel ME (2021) High-fat diet induces an ovulatory defect associated with dysregulated endothelin-2 in mice. Reproduction 161(3), 307-317.
| Crossref | Google Scholar | PubMed |
Hou X, Arvisais EW, Jiang C, Chen DB, Roy SK, Pate JL, Hansen TR, Rueda BR, Davis JS (2008) Prostaglandin F2alpha stimulates the expression and secretion of transforming growth factor B1 via induction of the early growth response 1 gene (EGR1) in the bovine corpus luteum. Molecular Endocrinology 22(2), 403-414.
| Crossref | Google Scholar | PubMed |
Huang X, Ding L, Bennewith KL, Tong RT, Welford SM, Ang KK, Story M, Le QT, Giaccia AJ (2009) Hypoxia-inducible mir-210 regulates normoxic gene expression involved in tumor initiation. Molecular Cell 35(6), 856-867.
| Crossref | Google Scholar | PubMed |
Hubbard BP, Sinclair DA (2013) Measurement of sirtuin enzyme activity using a substrate-agnostic fluorometric nicotinamide assay. Methods in Molecular Biology 1077, 167-177.
| Crossref | Google Scholar | PubMed |
Hughes CK, Maalouf SW, Liu WS, Pate JL (2019) Molecular profiling demonstrates modulation of immune cell function and matrix remodeling during luteal rescue. Biology of Reproduction 100(6), 1581-1596.
| Crossref | Google Scholar | PubMed |
Hughes CHK, Inskeep EK, Pate JL (2020) Temporal changes in the corpus luteum during early pregnancy reveal regulation of pathways that enhance steroidogenesis and suppress luteolytic mechanisms. Biology of Reproduction 103(1), 70-84.
| Crossref | Google Scholar | PubMed |
Hunter AR, Turner AJ (2006) Expression and localization of endothelin-converting enzyme-1 isoforms in human endothelial cells. Experimental Biology and Medicine 231(6), 718-722.
| Google Scholar | PubMed |
Imai S, Armstrong CM, Kaeberlein M, Guarente L (2000) Transcriptional silencing and longevity protein Sir2 is an NAD-dependent histone deacetylase. Nature 403(6771), 795-800.
| Crossref | Google Scholar | PubMed |
Imbar T, Klipper E, Greenfield C, Hurwitz A, Haimov-Kochman R, Meidan R (2012) Altered endothelin expression in granulosa-lutein cells of women with polycystic ovary syndrome. Life Sciences 91(13–14), 703-709.
| Crossref | Google Scholar | PubMed |
Inoue A, Yanagisawa M, Kimura S, Kasuya Y, Miyauchi T, Goto K, Masaki T (1989) The human endothelin family: three structurally and pharmacologically distinct isopeptides predicted by three separate genes. Proceedings of the National Academy of Sciences 86(8), 2863-2867.
| Crossref | Google Scholar | PubMed |
Isberg V, Mordalski S, Munk C, Rataj K, Harpsøe K, Hauser AS, Vroling B, Bojarski AJ, Vriend G, Gloriam DE (2016) GPCRdb: an information system for G protein-coupled receptors. Nucleic Acids Res 44(D1), D356-D364.
| Crossref | Google Scholar | PubMed |
Joo HY, Yun M, Jeong J, Park ER, Shin HJ, Woo SR, Jung JK, Kim YM, Park JJ, Kim J, Lee KH (2015) SIRT1 deacetylates and stabilizes hypoxia-inducible factor-1α (HIF-1α) via direct interactions during hypoxia. Biochemical and Biophysical Research Communications 462(4), 294-300.
| Crossref | Google Scholar | PubMed |
Kawanabe Y, Okamoto Y, Nozaki K, Hashimoto N, Miwa S, Masaki T (2002) Molecular mechanism for endothelin-1-induced stress-fiber formation: analysis of G proteins using a mutant endothelin(A) receptor. Molecular Pharmacology 61(2), 277-284.
| Crossref | Google Scholar | PubMed |
Kedzierski RM, Yanagisawa M (2001) Endothelin system: the double-edged sword in health and disease. Annual Review of Pharmacology and Toxicology 41, 851-876.
| Crossref | Google Scholar | PubMed |
Kelly TJ, Souza AL, Clish CB, Puigserver P (2011) A hypoxia-induced positive feedback loop promotes hypoxia-inducible factor 1alpha stability through miR-210 suppression of glycerol-3-phosphate dehydrogenase 1-like. Molecular and Cellular Biology 31(13), 2696-2706.
| Crossref | Google Scholar | PubMed |
Kim J, Bagchi IC, Bagchi MK (2009) Signaling by hypoxia-inducible factors is critical for ovulation in mice. Endocrinology 150(7), 3392-3400.
| Crossref | Google Scholar | PubMed |
Kisliouk T, Podlovni H, Spanel-Borowski K, Ovadia O, Zhou QY, Meidan R (2005) Prokineticins (endocrine gland-derived vascular endothelial growth factor and BV8) in the bovine ovary: expression and role as mitogens and survival factors for corpus luteum-derived endothelial cells. Endocrinology 146(9), 3950-3958.
| Crossref | Google Scholar | PubMed |
Kitamura K, Shiraishi N, Singer WD, Handlogten ME, Tomita K, Miller RT (1999) Endothelin-B receptors activate Galpha13. American Journal of Physiology 276(4), C930-C937.
| Crossref | Google Scholar | PubMed |
Kliem H, Welter H, Kraetzl WD, Steffl M, Meyer HHD, Schams D, Berisha B (2007) Expression and localisation of extracellular matrix degrading proteases and their inhibitors during the oestrous cycle and after induced luteolysis in the bovine corpus luteum. Reproduction 134(3), 535-547.
| Crossref | Google Scholar | PubMed |
Klipper E, Levit A, Mastich Y, Berisha B, Schams D, Meidan R (2010) Induction of endothelin-2 expression by luteinizing hormone and hypoxia: possible role in bovine corpus luteum formation. Endocrinology 151, 1914-1922.
| Crossref | Google Scholar | PubMed |
Ko C, Gieske MC, Al-Alem L, Hahn Y, Su W, Gong MC, Iglarz M, Koo Y (2006) Endothelin-2 in ovarian follicle rupture. Endocrinology 147(4), 1770-1779.
| Crossref | Google Scholar | PubMed |
Kowalczyk A, Kleniewska P, Kolodziejczyk M, Skibska B, Goraca A (2015) The role of endothelin-1 and endothelin receptor antagonists in inflammatory response and sepsis. Archivum Immunologiae et Therapiae Experimentalis 63(1), 41-52.
| Crossref | Google Scholar | PubMed |
Kowalewski MP (2014) Luteal regression vs. prepartum luteolysis: regulatory mechanisms governing canine corpus luteum function. Reproductive Biology 14(2), 89-102.
| Crossref | Google Scholar | PubMed |
Laemmle A, Lechleiter A, Roh V, Schwarz C, Portmann S, Furer C, Keogh A, Tschan MP, Candinas D, Vorburger SA, Stroka D (2012) Inhibition of SIRT1 impairs the accumulation and transcriptional activity of HIF-1α protein under hypoxic conditions. PLoS ONE 7(3), e33433.
| Crossref | Google Scholar | PubMed |
Lee J, McCracken JA, Banu SK, Rodriguez R, Nithy TK, Arosh JA (2010) Transport of prostaglandin F(2α) pulses from the uterus to the ovary at the time of luteolysis in ruminants is regulated by prostaglandin transporter-mediated mechanisms. Endocrinology 151(7), 3326-3335.
| Crossref | Google Scholar | PubMed |
Levy N, Gordin M, Mamluk R, Yanagisawa M, Smith MF, Hampton JH, Meidan R (2001) Distinct cellular localization and regulation of endothelin-1 and endothelin-converting enzyme-1 expression in the bovine corpus luteum: implications for luteolysis. Endocrinology 142(12), 5254-5260.
| Crossref | Google Scholar | PubMed |
Lim JH, Lee YM, Chun YS, Chen J, Kim JE, Park JW (2010) Sirtuin 1 modulates cellular responses to hypoxia by deacetylating hypoxia-inducible factor 1alpha. Molecular Cell 38(6), 864-878.
| Crossref | Google Scholar | PubMed |
Mamluk R, Levy N, Rueda B, Davis JS, Meidan R (1999) Characterization and regulation of type A endothelin receptor gene expression in bovine luteal cell types. Endocrinology 140(5), 2110-2116.
| Crossref | Google Scholar | PubMed |
Mann GE, Lamming GE, Robinson RS, Wathes DC (1999) The regulation of interferon-tau production and uterine hormone receptors during early pregnancy. Journal of Reproduction and Fertility. Supplements 54, 317-328.
| Google Scholar | PubMed |
March WA, Moore VM, Willson KJ, Phillips DIW, Norman RJ, Davies MJ (2010) The prevalence of polycystic ovary syndrome in a community sample assessed under contrasting diagnostic criteria. Human Reproduction 25(2), 544-551.
| Crossref | Google Scholar | PubMed |
Mares SE, Zimbelman RG, Casida LE (1962) Variation in progesterone content of the bovine corpus luteum of the estrual cycle. Journal of Animal Science 21, 266-271.
| Crossref | Google Scholar |
Martínez-Díaz I, Martos N, Llorens-Cebrià C, Álvarez FJ, Bedard PW, Vergara A, Jacobs-Cachá C, Soler MJ (2023) Endothelin receptor antagonists in kidney disease. International Journal of Molecular Sciences 24(4), 3427.
| Crossref | Google Scholar |
Meidan R (2017) ‘The life cycle of the corpus luteum.’ 1st edn. (Springer International Publishing: Cham) 10.1007/978-3-319-43238-0
Meidan R, Girsh E (1997) Role of endothelial cells in the steroidogenic activity of the bovine corpus luteum. Semin Reprod Endocrinol 15(4), 371-382.
| Crossref | Google Scholar | PubMed |
Meidan R, Levy N (2007) The ovarian endothelin network: an evolving story. Trends in Endocrinology & Metabolism 18(10), 379-385.
| Crossref | Google Scholar | PubMed |
Meidan R, Szymanska M (2023) Divergent roles of sirtuin 1 in human granulosa-lutein cells: similarities to human chorionic gonadotropin. Biology of Reproduction 108(5), 720-730.
| Crossref | Google Scholar | PubMed |
Meidan R, Girsh E, Blum O, Aberdam E (1990) In vitro differentiation of bovine theca and granulosa cells into small and large luteal-like cells: morphological and functional characteristics. Biology of Reproduction 43(6), 913-921.
| Crossref | Google Scholar | PubMed |
Meidan R, Levy N, Kisliouk T, Podlovny L, Rusiansky M, Klipper E (2005) The yin and yang of corpus luteum-derived endothelial cells: balancing life and death. Domestic Animal Endocrinology 29(2), 318-328.
| Crossref | Google Scholar | PubMed |
Meidan R, Klipper E, Zalman Y, Yalu R (2013) The role of hypoxia-induced genes in ovarian angiogenesis. Reproduction, Fertility and Development 25(2), 343-350.
| Crossref | Google Scholar | PubMed |
Meidan R, Girsh E, Mamluk R, Levy N, Farberov S (2017) Luteolysis in ruminants: past concepts, new insights, and persisting challenges. In ‘The life cycle of the corpus luteum by Rina Meidan’. (Ed. R Meidan) pp. 159–182. (Springer International Publishing) 10.1007/978-3-319-43238-0_9
Merlo A, de Quiros SB, Secades P, Zambrano I, Balbin M, Astudillo A, Scola B, Aristegui M, Suarez C, Chiara MD (2012) Identification of a signaling axis HIF-1α/microRNA-210/ISCU independent of SDH mutation that defines a subgroup of head and neck paragangliomas. Journal of Clinical Endocrinology and Metabolism 97(11), E2194-E2200.
| Crossref | Google Scholar | PubMed |
Miyamoto A, Kobayashi S, Arata S, Ohtani M, Fukui Y, Schams D (1997) Prostaglandin F2 alpha promotes the inhibitory action of endothelin-1 on the bovine luteal function in vitro. Journal of Endocrinology 152(2), R7-R11.
| Crossref | Google Scholar | PubMed |
Miyamoto A, Shirasuna K, Shimizu T, Bollwein H, Schams D (2010) Regulation of corpus luteum development and maintenance: specific roles of angiogenesis and action of prostaglandin F2alpha. Society of Reproduction and Fertility Supplement 67, 289-304.
| Crossref | Google Scholar | PubMed |
Monaco CF, Davis JS (2023) Mechanisms of angioregression of the corpus luteum. Frontiers in Physiology 14, 1254943.
| Crossref | Google Scholar | PubMed |
Mondal M, Schilling B, Folger J, Steibel JP, Buchnick H, Zalman Y, Ireland JJ, Meidan R, Smith GW (2011) Deciphering the luteal transcriptome: potential mechanisms mediating stage-specific luteolytic response of the corpus luteum to prostaglandin F2α alpha. Physiol Genomics 43(8), 447-456.
| Crossref | Google Scholar | PubMed |
Montrezor LH, Piccinato CA, Collares CVA, Vireque AA, Silva AAM (2015) Effects of angiotensin II, atrial natriuretic peptide and endothelin-1 on proliferation and steroidogenic output of bovine granulosa cells cultured in a chemically defined system. Animal Reproduction Science 152, 8-16.
| Crossref | Google Scholar | PubMed |
Morita Y, Wada-Hiraike O, Yano T, Shirane A, Hirano M, Hiraike H, Koyama S, Oishi H, Yoshino O, Miyamoto Y, Sone K, Oda K, Nakagawa S, Tsutsui K, Taketani Y (2012) Resveratrol promotes expression of SIRT1 and StAR in rat ovarian granulosa cells: an implicative role of SIRT1 in the ovary. Reproductive Biology and Endocrinology 10, 14.
| Crossref | Google Scholar | PubMed |
Muller L, Valdenaire O, Barret A, Korth P, Pinet F, Corvol P, Tougard C (2000) Expression of the endothelin-converting enzyme-1 isoforms in endothelial cells. Journal of Cardiovascular Pharmacology 36(Supplement 1), S15-S18.
| Crossref | Google Scholar |
Muller L, Barret A, Etienne E, Meidan R, Valdenaire O, Corvol P, Tougard C (2003) Heterodimerization of endothelin-converting enzyme-1 isoforms regulates the subcellular distribution of this metalloprotease. Journal of Biological Chemistry 278(1), 545-555.
| Crossref | Google Scholar | PubMed |
Murphy BD, Gevry N, Ruiz-Cortes T, Cote F, Downey BR, Sirois J (2001) Formation and early development of the corpus luteum in pigs. Reproduction Supplement 58, 47-63.
| Google Scholar | PubMed |
Nishimura R, Okuda K (2010) Hypoxia is important for establishing vascularization during corpus luteum formation in cattle. Journal of Reproduction and Development 56(1), 110-116.
| Crossref | Google Scholar | PubMed |
Niswender GD, Juengel JL, Silva PJ, Rollyson MK, McIntush EW (2000) Mechanisms controlling the function and life span of the corpus luteum. Physiological Reviews 80, 1-29.
| Crossref | Google Scholar | PubMed |
Ohtani M, Kobayashi S, Miyamoto A, Hayashi K, Fukui Y (1998) Real-time relationships between intraluteal and plasma concentrations of endothelin, oxytocin, and progesterone during prostaglandin F2alpha-induced luteolysis in the cow. Biology of Reproduction 58(1), 103-108.
| Crossref | Google Scholar | PubMed |
Oliveira LJ, Barreto RSN, Perecin F, Mansouri-Attia N, Pereira FTV, Meirelles FV (2012) Modulation of maternal immune system during pregnancy in the cow. Reproduction in Domestic Animals 47(Suppl 1), 384-393.
| Crossref | Google Scholar | PubMed |
O’Shea JD, Rodgers RJ, D’Occhio MJ (1989) Cellular composition of the cyclic corpus luteum of the cow. Reproduction 85(2), 483-487.
| Crossref | Google Scholar | PubMed |
Palanisamy GS, Cheon YP, Kim J, Kannan A, Li Q, Sato M, Mantena SR, Sitruk-Ware RL, Bagchi MK, Bagchi IC (2006) A novel pathway involving progesterone receptor, endothelin-2, and endothelin receptor B controls ovulation in mice. Molecular Endocrinology 20(11), 2784-2795.
| Crossref | Google Scholar | PubMed |
Park SJ, Ahmad F, Um JH, Brown AL, Xu X, Kang H, Ke H, Feng X, Ryall J, Philp A, Schenk S, Kim MK, Sartorelli V, Chung JH (2017) Specific Sirt1 activator-mediated improvement in glucose homeostasis requires Sirt1-independent activation of AMPK. EBioMedicine 18, 128-138.
| Crossref | Google Scholar | PubMed |
Patil K, Hinduja I, Mukherjee S (2021) Alteration in angiogenic potential of granulosa-lutein cells and follicular fluid contributes to luteal defects in polycystic ovary syndrome. Human Reproduction 36(4), 1052-1064.
| Crossref | Google Scholar | PubMed |
Patwardhan VV, Lanthier A (1980) Concentration of prostaglandins PGE and PGF, estrone, estradiol, and progesterone in human corpora lutea. Prostaglandins 20(6), 963-969.
| Crossref | Google Scholar | PubMed |
Pocock R (2011) Invited review: decoding the microRNA response to hypoxia. Pflugers Arch 461(3), 307-315.
| Crossref | Google Scholar | PubMed |
Pokharel K, Peippo J, Weldenegodguad M, Honkatukia M, Li MH, Kantanen J (2020) Gene expression profiling of corpus luteum reveals important insights about early pregnancy in domestic sheep. Genes 11(4), 415.
| Crossref | Google Scholar |
Przygrodzka E, Kaczmarek MM, Kaczynski P, Ziecik AJ (2016) Steroid hormones, prostanoids, and angiogenic systems during rescue of the corpus luteum in pigs. Reproduction 151(2), 135-147.
| Crossref | Google Scholar | PubMed |
Puissegur MP, Mazure NM, Bertero T, Pradelli L, Grosso S, Robbe-Sermesant K, Maurin T, Lebrigand K, Cardinaud B, Hofman V, Fourre S, Magnone V, Ricci JE, Pouyssegur J, Gounon P, Hofman P, Barbry P, Mari B (2011) miR-210 is overexpressed in late stages of lung cancer and mediates mitochondrial alterations associated with modulation of HIF-1 activity. Cell Death & Differentiation 18(3), 465-478.
| Crossref | Google Scholar | PubMed |
Reynolds LP, Grazul-Bilska AT, Redmer DA (2000) Angiogenesis in the corpus luteum. Endocrine 12(1), 1-9.
| Crossref | Google Scholar | PubMed |
Roberts RM, Chen Y, Ezashi T, Walker AM (2008) Interferons and the maternal-conceptus dialog in mammals. Seminars in Cell & Developmental Biology 19(2), 170-177.
| Crossref | Google Scholar | PubMed |
Romero JJ, Antoniazzi AQ, Smirnova NP, Webb BT, Yu F, Davis JS, Hansen TR (2013) Pregnancy-associated genes contribute to antiluteolytic mechanisms in ovine corpus luteum. Physiological Genomics 45(22), 1095-1108.
| Crossref | Google Scholar | PubMed |
Romero JJ, Antoniazzi AQ, Nett TM, Ashley RL, Webb BT, Smirnova NP, Bott RC, Bruemmer JE, Bazer FW, Anthony RV, Hansen TR (2015) Temporal release, paracrine and endocrine actions of ovine conceptus-derived interferon-tau during early pregnancy. Biology of Reproduction 93(6), 146.
| Crossref | Google Scholar | PubMed |
Russell W (1975) Luteolysis induced in pigtail monkeys (Macaca nemestrina) with prostaglandin f 2 alpha, ICI 80996 and ICI 81008. Prostaglandins 10(1), 163-183.
| Crossref | Google Scholar | PubMed |
Sakurai T, Yanagisawa M, Takuwa Y, Miyazaki H, Kimura S, Goto K, Masaki T (1990) Cloning of a cDNA encoding a non-isopeptide-selective subtype of the endothelin receptor. Nature 348(6303), 732-735.
| Crossref | Google Scholar | PubMed |
Sapuleni J, Szymanska M, Meidan R (2022) Diverse actions of sirtuin-1 on ovulatory genes and cell death pathways in human granulosa cells. Reproductive Biology and Endocrinology 20(1), 104.
| Crossref | Google Scholar | PubMed |
Semenza GL (2007) Hypoxia-inducible factor 1 (HIF-1) pathway. Science’s STKE 2007(407), cm8.
| Crossref | Google Scholar |
Shah KB, Tripathy S, Suganthi H, Rudraiah M (2014) Profiling of luteal transcriptome during prostaglandin F2-alpha treatment in buffalo cows: analysis of signaling pathways associated with luteolysis. PLoS ONE 9(8), e104127.
| Crossref | Google Scholar | PubMed |
Shirasuna K, Asaoka H, Acosta TJ, Wijayagunawardane MPB, Ohtani M, Hayashi KG, Matsui M, Miyamoto A (2004) Real-time dynamics of prostaglandin F2alpha release from uterus and corpus luteum during spontaneous luteolysis in the cow. Reproduction 128(2), 189-195.
| Crossref | Google Scholar | PubMed |
Shiratsuki S, Hara T, Munakata Y, Shirasuna K, Kuwayama T, Iwata H (2016) Low oxygen level increases proliferation and metabolic changes in bovine granulosa cells. Molecular and Cellular Endocrinology 437, 75-85.
| Crossref | Google Scholar | PubMed |
Shrestha K, Onasanya AE, Eisenberg I, Wigoda N, Yagel S, Yalu R, Meidan R, Imbar T (2018) miR-210 and GPD1L regulate EDN2 in primary and immortalized human granulosa-lutein cells. Reproduction 155(2), 197-205.
| Crossref | Google Scholar | PubMed |
Silvia WJ, Lewis GS, McCracken JA, Thatcher WW, Wilson L, Jr. (1991) Hormonal regulation of uterine secretion of prostaglandin F2 alpha during luteolysis in ruminants. Biology of Reproduction 45(5), 655-663.
| Crossref | Google Scholar | PubMed |
Skarzynski DJ, Piotrowska-Tomala KK, Lukasik K, Galvão A, Farberov S, Zalman Y, Meidan R (2013) Growth and regression in bovine corpora lutea: regulation by local survival and death pathways. Reproduction in Domestic Animals 48(Suppl 1), 25-37.
| Crossref | Google Scholar | PubMed |
Spencer TE, Bazer FW (1996) Ovine interferon tau suppresses transcription of the estrogen receptor and oxytocin receptor genes in the ovine endometrium. Endocrinology 137(3), 1144-1147.
| Crossref | Google Scholar | PubMed |
Sugino N, Okuda K (2007) Species-related differences in the mechanism of apoptosis during structural luteolysis. Journal of Reproduction and Development 53(5), 977-986.
| Crossref | Google Scholar | PubMed |
Szymanska M, Manthe S, Shrestha K, Girsh E, Harlev A, Kisliouk T, Meidan R (2021a) Sirtuin-1 inhibits endothelin-2 expression in human granulosa-lutein cells via hypoxia inducible factor 1 alpha and epigenetic modifications. Biology of Reproduction 104(2), 387-398.
| Crossref | Google Scholar | PubMed |
Szymanska M, Shrestha K, Girsh E, Harlev A, Eisenberg I, Imbar T, Meidan R (2021b) Reduced endothelin-2 and hypoxic signaling pathways in granulosa-lutein cells of PCOS women. International Journal of Molecular Sciences 22(15), 8216.
| Crossref | Google Scholar | PubMed |
Takigawa M, Sakurai T, Kasuya Y, Abe Y, Masaki T, Goto K (1995) Molecular identification of guanine-nucleotide-binding regulatory proteins which couple to endothelin receptors. European Journal of Biochemistry 228(1), 102-108.
| Crossref | Google Scholar | PubMed |
Talbott H, Hou X, Qiu F, Zhang P, Guda C, Yu F, Cushman RA, Wood JR, Wang C, Cupp AS, Davis JS (2017) Early transcriptome responses of the bovine midcycle corpus luteum to prostaglandin F2α includes cytokine signaling. Molecular and Cellular Endocrinology 452, 93-109.
| Crossref | Google Scholar | PubMed |
Tang BL (2016) Sirt1 and the Mitochondria. Molecules and Cells 39(2), 87-95.
| Crossref | Google Scholar | PubMed |
Tatone C, Di Emidio G, Vitti M, Di Carlo M, Santini S, Jr., D’Alessandro AM, Falone S, Amicarelli F (2015) Sirtuin functions in female fertility: possible role in oxidative stress and aging. Oxidative Medicine and Cellular Longevity 2015, 659687.
| Crossref | Google Scholar | PubMed |
Tesone M, Stouffer RL, Borman SM, Hennebold JD, Molskness TA (2005) Vascular endothelial growth factor (VEGF) production by the monkey corpus luteum during the menstrual cycle: isoform-selective messenger RNA expression in vivo and hypoxia-regulated protein secretion in vitro. Biology of Reproduction 73(5), 927-934.
| Crossref | Google Scholar | PubMed |
Tocci P, Cianfrocca R, Di Castro V, Rosano L, Sacconi A, Donzelli S, Bonfiglio S, Bucci G, Vizza E, Ferrandina G, Scambia G, Tonon G, Blandino G, Bagnato A (2019) β-arrestin1/YAP/mutant p53 complexes orchestrate the endothelin A receptor signaling in high-grade serous ovarian cancer. Nature Communications 10(1), 3196.
| Crossref | Google Scholar | PubMed |
van den Driesche S, Myers M, Gay E, Thong KJ, Duncan WC (2008) HCG up-regulates hypoxia inducible factor-1 alpha in luteinized granulosa cells: implications for the hormonal regulation of vascular endothelial growth factor A in the human corpus luteum. Molecular Human Reproduction 14(8), 455-464.
| Crossref | Google Scholar | PubMed |
Vazquez MJ, Toro CA, Castellano JM, Ruiz-Pino F, Roa J, Beiroa D, Heras V, Velasco I, Dieguez C, Pinilla L, Gaytan F, Nogueiras R, Bosch MA, Rønnekleiv OK, Lomniczi A, Ojeda SR, Tena-Sempere M (2018) SIRT1 mediates obesity- and nutrient-dependent perturbation of pubertal timing by epigenetically controlling Kiss1 expression. Nature Communications 9(1), 4194.
| Crossref | Google Scholar | PubMed |
Watanabe S, Shirasuna K, Matsui M, Yamamoto D, Berisha B, Schams D, Miyamoto A (2006) Effect of intraluteal injection of endothelin type A receptor antagonist on PGF2alpha-induced luteolysis in the cow. Journal of Reproduction and Development 52(4), 551-559.
| Crossref | Google Scholar | PubMed |
Yalu R, Oyesiji AE, Eisenberg I, Imbar T, Meidan R (2015) HIF1A-dependent increase in endothelin 2 levels in granulosa cells: role of hypoxia, LH/cAMP, and reactive oxygen species. Reproduction 149(1), 11-20.
| Crossref | Google Scholar | PubMed |
Yanagisawa M, Inoue A, Ishikawa T, Kasuya Y, Kimura S, Kumagaye S, Nakajima K, Watanabe TX, Sakakibara S, Goto K (1988) Primary structure, synthesis, and biological activity of rat endothelin, an endothelium-derived vasoconstrictor peptide. Proceedings of the National Academy of Sciences 85(18), 6964-6967.
| Crossref | Google Scholar | PubMed |
Yanagisawa H, Yanagisawa M, Kapur RP, Richardson JA, Williams SC, Clouthier DE, de Wit D, Emoto N, Hammer RE (1998) Dual genetic pathways of endothelin-mediated intercellular signaling revealed by targeted disruption of endothelin converting enzyme-1 gene. Development 125(5), 825-836.
| Crossref | Google Scholar | PubMed |
Zalman Y, Klipper E, Farberov S, Mondal M, Wee G, Folger JK, Smith GW, Meidan R (2012) Regulation of angiogenesis-related prostaglandin f2alpha-induced genes in the bovine corpus luteum. Biology of Reproduction 86(3), 92.
| Crossref | Google Scholar | PubMed |
Zhai Z, Tang M, Yang Y, Lu M, Zhu WG, Li T (2017) Identifying human SIRT1 substrates by integrating heterogeneous information from various sources. Scientific Reports 7(1), 4614.
| Crossref | Google Scholar | PubMed |
Zhang J, Zhang Z, Wu Y, Chen L, Luo Q, Chen J, Huang X, Cheng Y, Wang Z (2012) Regulatory effect of hypoxia-inducible factor-1α on hCG-stimulated endothelin-2 expression in granulosa cells from the PMSG-treated rat ovary. Journal of Reproduction and Development 58(6), 678-684.
| Crossref | Google Scholar | PubMed |
Zhang S, Spiegelman NA, Lin H (2019) Global profiling of sirtuin deacylase substrates using a chemical proteomic strategy and validation by fluorescent labeling. Methods in Molecular Biology 2009, 137-147.
| Crossref | Google Scholar | PubMed |
Ziecik AJ, Przygrodzka E, Jalali BM, Kaczmarek MM (2018) Regulation of the porcine corpus luteum during pregnancy. Reproduction 156(3), R57-R67.
| Crossref | Google Scholar | PubMed |
Zorrilla LM, Sriperumbudur R, Gadsby JE (2010) Endothelin-1, endothelin converting enzyme-1 and endothelin receptors in the porcine corpus luteum. Domestic Animal Endocrinology 38(2), 75-85.
| Crossref | Google Scholar | PubMed |