Structures, Functions and Expressions of GnRH and GnRH Receptor in Peripheral Reproductive Organs and Their Regulation by Estradiol-17β
الموضوعات :
اچ.ب. سیفتسی
1
(Department of Animal Science, School of Agriculture, Selçuk University, Konya 42075, Turkey)
الکلمات المفتاحية: GnRH, Ovary, Uterus, estradiol, oviduct,
ملخص المقالة :
Studies have shown that estradiol-17β (E2) regulates gonadotropin-releasing hormone (GnRH) and GnRH receptor expression in hypothalamus and pituitary. Several studies have shown that GnRH and its receptor are also expressed in peripheral reproductive organs and little is known about their regulations. In this study, GnRH and GnRH receptor structures, functions, their peripheral expressions and regulations by E2 were reviewed. Several in vivo and in vitro conducted studies indicate that E2 decreases the expression of GnRH mRNA and regulates GnRH receptor expression in a time dependent manner. Nevertheless, the exact mechanism has not been clearly explained yet.
REFERENCES
Adams B.A., Tello J.A. and Erchegyi J. (2003). Six novel gonadotropin-releasing hormones are encoded as triplets on each of two genes in the protochordate, Ciona intestinalis. Endocrinology. 144, 1907-1919.
Adelman J.P., Mason A.J., Hayflick J.S. and Seeburg P.H. (1986).Isolation of the gene and hypothalamic cDNA for the common precursor of gonadotropin-releasing hormone and prolactin release-inhibiting factor in human and rat. Proc. Nat. Acad. Sci. USA. 83, 179-183.
Albarracin C.T., Kaiser U.B. and Chin W.W. (1994). Isolation and characterization of the 5’-flanking region of the mouse gonadotropin-releasing hormone receptor gene. Endocrinology. 135, 2300-2306.
Amarant T., Fridkin M. and Koch Y. (1982). Luteinizing hormone-releasing hormone and thyrotropin-releasing hormone in human and bovine milk. European J. Biochem. 127, 647-650.
Bahk J.Y., Hyun J.S., Chung S.H., Lee H., Kim M.O., Lee B.H. and Choi W.S. (1995). Stage specific identification of the expression of GnRH mRNA and localization of the GnRH receptor in mature rat and adult human testis. J. Urol. 154, 1958-1961.
Baldwin J.M. (1993). The probable arrangement of the helices in G protein-coupled receptors. EMBO J. 12, 1693-1703.
Ballesteros J.A. and Weinstein H. (1992). Analysis and refinement of criteria for predicting the structure and relative orientations of transmembranal helical domains. Biophys. J. 62, 107-109.
Ballesteros J., Kitanovic S., Guarnieri F., Davies P., Fromme B.J., Konvicka K., Chi L., Millar R.P., Davidson J.S., Weinstein H. and Sealfon S.C. (1998). Functional micro domains in G-protein-coupled receptors. The conserved arginine-cage motif in the gonadotropin-releasing hormone receptor. J. Biol. Chem. 273, 10445-10453.
Balthazart J., Cornil C.A., Charlier T.D., Taziaux M. and Ball G.F. (2009). Estradiol, a key endocrine signal in the sexual differentiation and activation of reproductive behavior in quail. J. Exp. Zool. A Ecol. Genet. Physiol. 311, 323-345.
Bauer-Dantoin A.C. and Jameson J.L. (1995). Gonadotropinreleasing hormone receptor messenger ribonucleic acid expression in the ovary during rat estrous cycle. Endocrinology. 136, 4432-4438.
Borroni R., Blasio A.M.D., Gaffari B., Santorsola R., Busacca M., Vigano P. and Viganali M. (2000). Expression of GnRH receptor gene in human ectopic endometrial cells and inhibition of their proliferation by leuprolide acetate. Mol. Cell. Endocrinol. 159, 37-43.
Brodowska A., Laszczynska M., Starczewski A., Karakiewicz B. and Brodowski J. (2007). The localization of estrogen receptor alpha and its function in the ovaries of postmenopausal women. Folia Histochem. Cytobiol. 45, 325-330.
Burger L.L., Dalkin A.C., Aylor K.W., Haisenleder D.J. and Marshall J.C. (2002). GnRH pulse frequency modulation of gonadotropin subunit gene transcription in normal gonadotropes-assessment by primary transcript assay provides evidence for roles of GnRH and follistatin. Endocrinology. 143, 3243-3249.
Calatayud N.E., Pask A.J., Shaw G., Richings N.M., Osborn S. and Renfree M.B. (2010). Ontogeny of the oestrogen receptors ESR1 and ESR2 during gonadal development in the tammar wallaby, Macropus Eeugenii. Reproduction. 139, 599-611.
Campion C.E., Turzillo A.M. and Clay C.M. (1996). The gene encoding the ovine gonadotropin- releasing hormone (GnRH) receptor: cloning and initial characterization. Gene. 170, 277-280.
Caraty A., Locatelli A. and Martin G.B. (1989). Biphasic response in the secretion of gonadotropin-releasing hormone in ovariectomized ewes injected with oestradiol. J. Endocrinol. 123, 375-382.
Casañ E.M., Raga F. and Polan M.L. (1999). GnRH mRNA and protein expression in human preimplantation embryos. Mol. Hum. Reprod. 5, 234-239.
Casañ E.M., Raga F., Bonilla-Musoles F. and Polan M.L. (2000). Human oviductal gonadotropin-releasing hormone: possible implications in fertilization, early embryonic development, and implantation. J. Clin. Endocrinol. Metab. 85, 1377-1381.
Chen A., Kaganovsky E., Rahimipour S., Ben-Aroya N., Okon E. and Koch Y. (2002). Two forms of gonadotropin-releasing hormone (GnRH) are expressed in human breast tissue and over expressed in breast cancer: a putative mechanism for the antiproliferative effect of GnRH by down-regulation of acidic ribosomal phosphoproteins P1 and P2. Cancer. Res. 62, 1036-1044.
Cheng C.K. and Leung P.C. (2005). Molecular biology of gonadotropin-releasing hormone (GnRH)-I, GnRH-II and their receptors in humans. Endocrine. Rev. 26, 283-306.
Cheon K.W., Lee H.S., Parhar I.S. and Kang I.S. (2001). Expression of the second isoform of gonadotropin-releasing hormone (GnRH-II) in human endometrium throughout the menstrual cycle. Mol. Hum. Reprod. 7, 447-452.
Chongthammakun S. and Terasawa E. (1993). Negative feedback effects of estrogen on luteinizing hormone releasing hormone release occur in pubertal, but not prepubertal, ovariectomized female rhesus monkeys. Endocrinology. 132, 735-743.
Choi K.C., Auersperg N. and Leung P.C. (2001). Expression and antiproliferative effect of a second form of gonadotropin-releasing hormone in normal and neoplastic ovarian surface epithelial cells. J. Clin. Endocrinol. Metab. 86, 5075-5078.
Clayton R.N., Shakespear R.A., Duncan J.A., Marshall J.C., Munson P.J. and Rodbard D. (1979). Radio iodinated nondegradable gonadotropin-releasing hormone analogs: new probes for the investigation of pituitary gonadotropin-releasing hormone receptors. Endocrinology. 105, 1369-1376.
Conn P.M., Huckle W.R., Andrews W.V. and McArdle C.A. (1987). The molecular mechanism of action of gonadotropin hormone-releasing hormone (GnRH) in the pituitary. Recent Prog. Horm. Res.43, 29-68.
Conn P.M. and Crowley W.F.Jr. (1994). Gonadotropin-releasing hormone and its analogs. Annu. Rev. Med. 45, 391-405.
Cui H.X., Zhao S.M., Cheng M.L., Guo L., Ye R.Q., Liu W.Q. and Gao S.Z. (2009). Cloning and expression levels of genes relating to the ovulation rate of the Yunling black goat. Biol. Reprod. 80, 219-226.
Dalkin A.C., Haisenleder D.J., Ortolano G.A., Ellis T.R. and Marshall J.C. (1989). The frequency of gonadotropin-releasing-hormone stimulation differentially regulates gonadotropin subunit messenger ribonucleic acid expression. Endocrinology. 125, 917-924.
Dekel N., Lewysohn O., Ayalon D. and Hazum E. (1988). Receptors of gonadotropin-releasing hormone are present in rat oocyte. Endocrinology. 123, 1205-1207.
Densmore V.S. and Urbanski H.F. (2004). Effect of 17β-estradiol on hypothalamic GnRH-II gene expression in the female rhesus macaque.J. Mol. Endocrinol. 33, 145-153.
Dohlman H.G., Thorner J., Caron M.G. and Lefkowitz R.J. (1991). Model systems for the study of seven transmembrane segment receptors. Annu. Rev. Biochem. 60, 653-688.
Dong K.W., Marcelin K., Hsu M.I., Chiang C.M., Hoffman G. and Roberts J.L. (1998). Expression of gonadotropin-releasing hormone (GnRH) gene in human uterine endometrial tissue. Mol. Hum. Reprod. 4, 893-898.
Donnelly D., Johnson M.S., Blundell T.L. and Saunders J. (1989). An analysis of the periodicity of conserved residues in sequence alignments of G-protein coupled receptors. Implications for the three-dimensional structure. FEBS Lett. 251, 109-116.
Dubois E.A., Zandbergen M.A., Peute J. and Goos H.J. (2002). Evolutionary development of three gonadotropin-releasing hormone (GnRH) systems invertebrates. Brain. Res. Bull. 57, 413-418.
Eidne K.A., Flanagan C.A. and Millar R.P. (1985). Gonadotropin-releasing hormone binding sites in human breast carcinoma. Science. 229(4717), 989-991.
Ekholm C., Hillensjo T. and Isaksson O. (1981). Gonadotropin-releasing hormone agonists stimulate oocyte meiosis and ovulation in hypophysectomized rats. Endocrinology. 108, 2022-2024.
Emons G., Muller V., Ortmann O. and Schulz K.D. (1998). Effects of LHRH-analogues on mitogenic signal transduction in cancer cells. J. Steroid Biochem. Mol. Biol. 65, 199-206.
Evans N.P., Dahl G.E., Glover B.H. and Karsch F.J. (1994). Central regulation of pulsatile gonadotropin-releasing hormone (GnRH) secretion by estradiol during the period leading up to the preovulatory GnRH surge in the ewe. Endocrinology. 134, 1806-1811.
Evans N.P., Dahl G.E., Mauger D. and Karsch F.J. (1995). Estradiol induces both qualitative and quantitative changes in the pattern of gonadotropin-releasing hormone secretion during the presurge period in the ewe. Endocrinology. 136, 1603-1609.
Fan N.C., Peng C., Krisinger J. and Leung P. (1995). The human gonadotropin-releasing hormone receptor gene: complete structure including multiple protomers, transcription sites, and polyadenylation signals. Mol. Cell. Endocrinol. 107, l-8
Ferguson S.S. (2001). Evolving concepts in G-protein-coupled receptor endocytosis: the role in receptor desensitization and signalling. Pharmacol. Rev. 53, 1-24.
Flanagan C.A., Becker I.I., Davidson J.S., Wakefield I.K., Zhou W., Sealfon S.C. and Millar R.P. (1994). Glutamate 301 of the mouse gonadotropin-releasing hormone receptor confers specificity for arginine 8 of mammalian gonadotropin-releasing hormone. J. Biol. Chem. 269, 22636-22641.
Flanagan C.A., Millar R.P. and Illing N. (1997). Advances in understanding gonadotrophin-releasing hormone receptor structure and ligand interactions. Rev. Reprod. 2, 113-120.
Funston R.N. and Seidel G.E.Jr. (1995). Gonadotropin-releasing hormone increases cleavage rates of bovine oocytes fertilized in vitro. Biol. Reprod. 53, 541-545.
Grundker C., Volker P. and Emons G. (2001). Antiproliferative signalling of luteinising hormone-releasing hormone in human endometrial and ovarian cancer cells through G protein alpha(I)-mediated activation of phosphotyrosine phosphatase. Endocrinology. 142, 2369-2380.
Haisenleder D.J., Ortolano G.A., Yasin M., Dalkin A.C. and Marshall J.C. (1993). Regulation of gonadotropin subunit messenger ribonucleic acid expression by gonadotropin-releasing hormone pulse amplitude in vitro. Endocrinology. 132, 1292-1296.
Hanyaloglu A.C., Vrecl M., Kroeger K.M., Miles L.E., Qian H., Thomas W.G. and Eidne K.A. (2001). Casein kinase II sites in the intracellular C-terminal domain of the thyrotropin-releasing hormone receptor and chimeric gonadotrophin-releasing hormone receptors contribute to beta-arrestin-dependent internalization. J. Biol. Chem. 276, 18066-18074.
Harris G.W. (1948). Neural control of the pituitary gland. Physiol. Rev. 28, 139-179.
Harrison G.C., WiermanM.E., Nett T.M. and Glode L.M. (2004). Gonadotropin-releasing hormone and its receptor in normal and malignant cells. Endocrinol. Relat. Cancer. 11, 725-748.
Hasegawa Y., Miyamoto K., Igarashi M., Chino N. and Sakakibara S. (1984). Biological properties of chicken luteinizing hormone-releasing hormone. gonadotropin release from rat and chicken cultured anterior pituitary cells and radioligand analysis. Endocrinology. 114, 1441-1447.
Harwood J.P., Clayton R.N. and Catt K.J. (1980). Ovarian gonadotropin-releasing hormone receptors. I. Properties and inhibition of luteal cell function. Endocrinology. 107, 407-413.
Heding A., Vrecl M., Bogerd J., McGregor A., Sellar R., Taylor P.L. and Eidne K.A. (1998). Gonadotropin-releasing hormone receptors with intracellular carboxyl-terminal tails undergo acute desensitization of total inositol phosphate production and exhibit accelerated internalization kinetics. J. Biol. Chem. 273, 11472-11477.
Heding A., Vrecl M., Hanyaloglu A.C., Sellar R., Taylor P.L. and Eidne K.A. (2000). The rat gonadotrophin releasing hormone receptor internalizes via a beta-arrestin-independent, but dynamindependent, pathway: addition of a carboxyl-terminal tail confers beta-arrestin dependency. Endocrinology. 141, 299-306.
Hillensjo T. and LeMaire W.J. (1980). Gonadotropin-releasing hormone agonists stimulate meiotic maturation of follicle-enclosed rat oocytes in vitro. Nature. 287, 145-146.
Hsueh A.J. and Jones P.B. (1981). Extra pituitary actions of gonadotropin-releasing hormone. Endocrinol. Rev. 2, 437-461.
Hsueh A.J. and Schaeffer J.M. (1985). Gonadotropin-releasing hormone as a paracrine hormone and neurotransmitter in extra-pituitary sites. J. Steroid. Biochem. 23, 757-764.
Hułas-Stasiak M. and Gawron A. (2007). Immunohistochemical localization of estrogen receptors ERalpha and ERbeta in the spiny mouse (Acomys cahirinus) ovary during postnatal development. J. Mol. Histol. 38, 25-32.
Ikeda M., Taga M., Sakakibara H., Minaguchi H., Ginsburg E. and Vonderhaar B.K. (1996). Gene expression of gonadotropin-releasing hormone in early pregnant rat and steroid hormone exposed mouse uteri. J. Endocrinol. Invest. 19, 708-713.
Ikeda M., Taga M., Kurogi K. and Minaguchi H. (1997). Gene expression of gonadotropin-releasing hormone, but not its receptor, in human endometrium and decidua. Mol. Cell. Endocrinol. 135, 165-168.
Illing N., Troskie B.E., Nahorniak C.S., Hapgood J.P., Peter R.E. and Millar R.P. (1999). Two gonadotropin-releasing hormone receptor subtypes with distinct ligand selectivity and differential distribution in brain and pituitary in the goldfish (Carassius autatus). Proc. Natl. Acad. Sci. USA. 96, 2526-253.
Imai A., Ohno T., Iida K., Fuseya T., Furui T. and Tamaya T. (1994). Presence of gonadotropin-releasing hormone receptor and its messenger ribonucleic acid in endometrial carcinoma and endometrium. Gynecol. Oncol. 55, 144-148.
Imai A. and Tamaya T. (2000). GnRH receptor and apoptotic signalling. Vitam. Horm. 59, 1-33.
Jennes L. Stumpf W.E. and Conn P.M. (1983). Intracellular pathways of electron-opaque gonadotrophin releasing hormone derivatives bound by cultured gonadotrophs. Endocrinology. 113, 1683-1689.
Jennes L., Coy D. and Conn P.M. (1986). Receptor-mediated uptake of GnRH agonist and antagonists by cultured gonadotrophs: evidence for differential intracellular routing. Peptides. 7, 459-463.
Jones P.B., Conn P.M., Marian J. and Hsueh A.J. (1980). Binding of gonadotropin-releasing hormone agonist to rat ovarian granulosa cells. Life Sci. 27, 2125-2132.
Juengel J.L., Heath D.A., Quirke L.D. and McNatty K.P. (2006). Oestrogen receptor alpha and beta androgen receptor and progesterone receptor mRNA and protein localisation within the developing ovary and in small growing follicles of sheep. Reproduction. 131, 81-92.
Kang S., Cheng K., Nathwani P., Choi K. and Leung P. (2000). Autocrine role of gonadotropin-releasing hormone and its receptor in ovarian cancer cell growth. Endocrinology. 13, 297-304.
Kaiser U.B., Conn P.M. and Chin W.W. (1997). Studies of gonadotropin-releasing hormone (GnRH) action using GnRH receptor-expressing pituitary cell lines. Endocrinol. Rev. 18, 46-70.
Kakar S.S., Musgrove L.C., DevorD.C., Sellers J.C. and Neill J.D. (1992). Cloning, sequencing, and expression of human gonadotropin-releasing hormone (GnRH) receptor. Biochem. Biophys. Res. Commun. 189, 289-295.
Katzenellenbogen J.A. and Katzenellenbogen B.S. (1996). Nuclear hormone receptors: ligand activated regulators of transcription and diverse cell responses. Chem. Biol. 3, 529-536.
Khodr G.S. and Siler-Khodr T.M. (1978). Localization of luteinizing hormone-releasing factor in the human placenta. Fertil. Steril. 29, 523-526.
Khodr G.S. and Siler-Khodr T.M. (1980). Placental LRF and its synthesis. Science. 207, 315-317.
King J.A. and Millar R.P. (1995). Evolutionary aspects of gonadotropin-releasing hormone and its receptor. Cell. Mol. Neurobiol. 15, 5-23.
Kochman K. and Domański E. (1969). Studies on purification of the hypothalamic substances responsible for the release of gonadotropins from the pituitary gland. Acta. Physiol. Pol. 20, 441-453.
Khosravi S. and Leung P.C. (2003). Differential regulation of gonadotropin-releasing hormone (GnRH)I and GnRHII messenger ribonucleic acid by gonadal steroids in human granulosa luteal cells. J. Clin. Endocrinol. Metab. 88, 663-672.
Knapczyk-Stwora K., Durlej M., Duda M., Czernichowska-Ferreira K., Tabecka-Lonczynska A. and Slomczynska M. (2011). Expression of oestrogen receptor α and oestrogen receptor β in the uterus of the pregnant swine. Reprod. Domest. Anim. 46, 1-7.
Kottler M.L, Bergametti F., Carre M.C., Morice S., Decoret E., Lagarde J.P., Starzec A. and Counis R. (1999). Tissue-specific pattern of variant transcripts of the human gonadotropin-releasing hormone receptor gene. European J. Endocrinol. 140, 561-569.
Latimer V.S., Kohama S.G., Garyfallou V.T. and Urbanski H.F. (2001). A developmental increase in the expression of messenger ribonucleic acid encoding a second form of gonadotropin-releasing hormone in the rhesus macaque hypothalamus. J. Clin. Endocrinol. Metab. 86, 324-329.
Lefkowitz R.J., Hausdorff W.P. and Caron M.G. (1990). Role of phosphorylation in desensitization of the b-adrenoceptor. Trends. Pharmacol. Sci. 11, 190-194.
Lescheid D.W., Terasawa E., Abler L.A., Urbanski H.F., Warby C.M., Millar R.P. and SherwoodN.M. (1997). A second form of gonadotropin releasing hormone (GnRH) with characteristics of chicken GnRHII is present in the primate brain. Endocrinology. 138, 5618-5629.
Laugier C., Courion C., Pageaux J.F., Fanidi A., Dumas M.Y., Sandoz D., Nemoz G., Prigent A.F. and Pacheco H. (1988). Effect of estrogen on adenosine 3¢ 5', cyclic monophosphate in quail oviduct: possible involvement in estradiol-activated growth. Endocrinology. 122, 158-164.
Levine J.E. and Ramirez V.D. (1980). In vivo release of luteinizing hormone-releasing hormone estimated with push-pull cannulae from the mediabasal hypothalami of ovariectomized, steroid-primed rats. Endocrinology. 107, 1782-1790.
Li W.I., Jialo S. and Chin P.P. (1993). Immunoreactive gonadotropin-releasing hormone in procine reproductive tissues. Peptides. 14, 543-549.
Lien R.J., Cain J.R. and Forrest D.W. (1985). The influence of exogenous estradiol on bobwhite quail (Colinus virginianus) reproductive systems. Comp. Biochem. Physiol. Comp. Physiol. 80, 433-436.
Limonta P., Moretti R.M., Marelli M.M., Dondi D., Parenti M. and Motta M. (1999). The luteinizing hormone-releasing hormone receptor in human prostate cancer cells: messenger ribonucleic acid expression, molecular size and signal transduction pathway. Endocrinology. 140, 5250-5256.
Limonta P., Marelli M.M. and Moretti R.M. (2001). LHRH analogues as anticancer agents: pituitary and extra pituitary sites of action. Expert. Opin. Invest. Drug. 10, 709-720.
Lin L.S., Roberts V.J. and Yen S.S. (1995). Expression of human gonadotropin-releasing hormone receptor gene in the placenta and its functional relationship to human chorionic gonadotropin secretion. J. Clin. Endocrinol. Metab. 80, 580-585.
McCann S.M., Taleisnik S. and Friedman K.M. (1960). LH-releasing activity in hypothalamus extracts. Proc. Soc. Exp. Biol. Med. 104, 432-434.
Millar R.P. and King J.A. (1983). Synthesis, luteinizing hormone-releasing activity and receptor binding of chicken hypothalamic luteinizing hormone-releasing hormone. Endocrinology. 113, 1364-1369.
Millar R.P., Flanagan C.A., Milton R.C. and King J.A. (1989). Chimeric analogues of vertebrate gonadotropin-releasing hormones comprising substitutions of the variant amino acids in positions 5, 7 and 8. Characterization of requirements for receptor binding and gonadotropin release in mammalian and avian pituitary gonadotropes. J. Biol. Chem. 264, 21007-21013.
Millar R.P. (2003). GnRH-II and type-II GnRH receptors. Trends. Endocrinol. Metabol. 14, 35-43.
Millar R.P., Lu Z.L., Pawson A.J., Flanagan C.A., Morgan K. and Maudsley S.R. (2004). Gonadotropin-releasing hormone receptors. Endocrinol. Rev. 25, 235-275.
Millar R.P., Pawson A.J., Morgan K., Rissman E.F. and Lu Z.L. (2008). Diversity of actions of GnRHs mediated by ligand-induced selective signaling. Front. Neuroendocrinol. 29, 17-35.
Miller W.R., Scott W.N., Morris R., Fraser H.M. and Sharpe R.M. (1985). Growth of human breast cancer cells inhibited by a luteinizing hormone-releasing hormone agonist. Nature. 313, 231-233.
Minaretzis D., Jakubowski M., Mortola J.F. and Pavlou S.N. (1995). Gonadotropin-releasing hormone receptor gene expression in human ovary and granulosa-lutein cells. J. Clin. Endocrinol. Metab. 80, 430-434.
Moenter S.M., Caraty A. and Karsch F.J. (1990). The estradiol-induced surge of gonadotropin-releasing hormone in the ewe. Endocrinology. 127, 1375-1384.
Morales P. (1998). Gonadotropin-releasing hormone increases ability of the spermatozoa to bind to the human zona pellucida. Biol. Reprod. 59, 426-430.
Morales P., Kerr B., Oliva C., Pizarro E. and Kong M. (1999). Gonadotropin-releasing hormone antagonist inhibits sperm binding to human zona pellucida. Hum. Reprod. 14, 2069-2074.
Moumni M., Kottler M.L. and Counis R. (1994). Nucleotide sequence analysis of mRNA predicts that rat pituitary and gonadal gonadotropin-releasing hormone receptor proteins have identical primary structure. Biochem. Biophys. Res. Commun. 200, 1359-1366.
Naor Z., Harris D. and Shacham S. (1998). Mechanism of GnRH receptor signaling: combinatorial cross-talk of Ca2+ and protein kinase C. Front. Neuroendocrinol. 19, 1-19.
Nathwani P.S., Kang S.K., Cheng K.W., Choi K.C. and Leung P.C. (2000). Regulation of gonadotropin-releasing hormone and its receptor gene expression by 17beta-estradiol in cultured human granulosa-luteal cells. Endocrinology. 141, 1754-1763.
Neill J.D., Duck L.W., Sellers J.C. and Musgrove L.C. (2001). A gonadotropin releasing hormone (GnRH) receptor specific for GnRH-II in primates. Biochem. Biophys. Res. Commun. 282, 1012-1018.
Neill J.D. (2002). GnRH and GnRH receptor genes in the human genome. Endocrinology. 143, 737-743.
Oikawa M., Dargan C., Ny T. and Hsueh A.J. (1990). Expression of gonadotropin-releasing hormone and prothymosin-alpha messenger ribonucleic acid in the ovary. Endocrinology. 127, 2350-2356.
Olofsson J.I., Conti C.C. and Leung P.C.K. (1995). Homologous and heterologous regulation of gonadotropin-releasing hormone receptor gene expression in preovulatory rat granulosa cells. Endocrinology. 136, 974-980.
Okada A., Ohta Y., Inoue S., Hiroi H., Muramatsu M. and Iguchi T. (2003). Expression of estrogen, progesterone and androgen receptors in the oviduct of developing, cycling and pre-implantation rats. J. Mol. Endocrinol. 30, 301-315.
Okrasa S., Skowronski M.T., Staszkiewicz J., Kotwica G., Łakomy M. and Zięcik A.J. (2003). The effects of estradiol on β-endorphin, GnRH and galanin content in the oviduct and the uterus of ovariectomized gilts. Reprod. Biol. 3, 63-80.
Peng C., FanN.C., Ligier M. and Vaananen J. (1994). Expression and regulation of GnRH and GnRH receptor mRNA in human granulosa luteal cells. Endocrinology. 135, 1740-1746.
Petersen S.L., McCrone S., Keller M. and Shores S. (1995). Effects of estrogen and progesterone on luteinizing hormone-releasing hormone messenger ribonucleic acid levels: consideration of temporal and neuroanatomical variables. Endocrinology. 136, 3604-3610.
Pieper D.R., Richards J.S. and Marshall J.C. (1981). Ovarian gonadotropin-releasing hormone (GnRH) receptors: characterization, distribution, and induction by GnRH. Endocrinology. 108, 1148-1155.
Radovick S., Wondisford F.E., Nakayama Y., Yamada M., Cutler G.B. and Weintraub B.D. (1990). Isolation and characterization of the human gonadotropin-releasing hormone gene in the hypothalamus and placenta. Mol. Endocrinol. 4, 476-480.
Raga F., Casañ E.M., Kruessel J.S., Wen Y., Huang H.Y., Nezhat C. and Polan M.L. (1998). Quantitative gonadotropin-releasing hormone gene expression and immunohistochemical localization in human endometrium throughout the menstrual cycle. Biol. Reprod. 59, 661-669.
Raga F., Casañ E.M., Wen Y., Huang H.Y., Bonilla-Musoles F. and Polan M.L. (1999). Independent regulation of matrix metalloproteinase-9, tissue inhibitor of metalloproteinase-1 (TIMP-1), and TIMP-3 in human endometrial stromal cells by gonadotropin-releasing hormone: implications in early human implantation. J. Clin. Endocrinol. Metab. 84, 636-642.
Ramakrishnappa N., Rajamahendran R., Lin Y.M. and Leung P.C.K. (2005). GnRH in non hypothalamic reproductive tissues. Anim. Reprod. Sci. 88, 95-113.
Rance N.E. and Uswandi S.V. (1996). Gonadotropin-releasing hormone gene expression is increased in the medial basal hypothalamus of postmenopausal women. J. Clin. Endocrinol. Metab. 81, 3540-3546.
Reeves J.J., Seguin C., Lefebvre F.A., Kelly P.A. and Labrie F. (1980). Similar luteinizing hormone-releasing hormone binding sites in rat anterior pituitary and ovary. Proc. Natl. Acad. Sci. USA. 77, 5567-5571.
Reinhart J., Xiao S., Arora K.K. and Catt K.J. (1997). Structural organization and characterization of the protomer region of the rat gonadotropin-releasing hormone receptor gene. Mol. Cell. Endocrinol. 130, 1-12.
Roch G.J., Busby E.R. and SherwoodN.M. (2011). Evolution of GnRH: diving deeper. Gen. Comp. Endocrinol. 171, 1-16.
Sağsöz H., Akbalik M.E., Saruhan B.G. and Ketani M.A. (2011). Localization of estrogen receptor α and progesterone receptor β in bovine cervix and vagina during the follicular and luteal phases of the sexual cycle. Biotech. Histochem. 86, 262-271.
Sarkar D.K., Chiappa S.A., Fink G. and SherwoodN.M. (1976). Gonadotropin-releasing hormone surge in pro-oestrous rats. Nature. 264, 461-463.
Sarkar D.K. and Fink G. (1980). Luteinizing hormone releasing factor in pituitary stalk plasma from long-term ovariectomized rats: effects of steroids. J. Endocrinol. 86, 511-524.
Schally A.V., Arimura A., Baba Y., Nair R.M., Matsuo H., Redding T.W. and Debeljuk L. (1971). Isolation and properties of the FSH and LH-releasing hormone. Biochem. Biophys. Res. Commun. 43, 393-399.
Schally A.V. (1999). LH-RH analogues: I. Their impact on reproductive medicine. Gynecol. Endocrinol. 13, 401-409.
Schally A.V. and Nagy A. (1999). Cancer chemotherapy based on targeting of cytotoxic peptide conjugates to their receptors on tumors. European J. Endocrinol. 141, 1-14.
Schertler G.F. and Villa C. (1993). Projection structure of rhodopsin. Nature. 362, 770-772.
Schmid S.L., McNiven M.A. and De Camilli P. (1998). Dynamin and its partners: a progress report. Curr. Opin. Cell. Biol. 10, 504-512.
SealfonS.C., Weinstein H. and Millar R.P. (1997). Molecular mechanisms of ligand interaction with the gonadotropin relea-sing hormone receptor. Endocr. Rev. 18, 180-205.
Sengupta A., Baker T., Chakrabarti N., Whittaker J.A. and Sridaran R. (2007). Localization of immunoreactive gonadotropin-releasing hormone and relative expression of its mRNA in the oviduct during pregnancy in rats. J. Histochem. Cytochem. 55, 525-534.
Siler-Khodr T.M. and Khodr G.S. (1979). Extrahypothalamic luteinizing hormone-releasing factor (LRF): release of immunoreactive LRF in vitro. Fertil. Steril. 32, 294-296.
Siler-Khodr T.M. and Grayson M. (2001). Action of chicken-II GnRH on the human placenta. J. Clin. Endocrinol. Metab. 86, 804-810.
Simoni R.D., Hill R.L. and Vaughan M. (2002). The discovery of estrone, estriol and estradiol and the biochemical study of reproduction: The work of Edward Adelbert Doisy. J. Biol. Chem. 277, 17.
Singh R., Graves M.L., Roskelley C.D., Giritharan G. and Rajamahendran R. (2008). Gonadotropin-releasing hormone receptor gene and protein expression and immunohistochemical localization in bovine uterus and oviducts. Domest. Anim. Endocrinol. 34, 319-326.
Singh P., Krishna A., Sridaran R. and Tsutsui K. (2011). Immunohistochemical localization of GnRH and RFamide-related peptide-3 in the ovaries of mice during the estrous cycle. J. Mol. Histol. 42, 371-381.
Spratt D.P. and Herbison A.E. (1997). Regulation of preoptic area gonadotropin-releasing hormone (GnRH) mRNA expression by gonadal steroids in the long-term gonadectomized male rat. Brain. Res. Mol. Brain. Res. 47, 125-133.
Stojilkovic S.S., Reinhart J. and Catt K.J. (1994). Gonadotropin-releasing hormone receptors: structure and signal transduction pathways. Endocr. Rev. 15, 462-499.
Stojilkovic S.S. and Catt K.J. (1995). Expression and signal transduction pathways of gonadotropin-releasing hormone receptors. Rec. Prog. Horm. Res. 50, 161-205.
Tan L. and Rousseau P. (1982). The chemical identity of the immunoreactive LHRH-like peptide biosynthesized in the human placenta. Biochem. Biophys. Res. Commun. 109, 1061-1071.
Tensen C., Okuzawa K., Blomenröhr M., Rebers F., Leurs R., Bogerd J., Schulz R. and Goos H. (1997). Distinct efficacies for two endogenous ligands on a single cognate gonadoliberin receptor. European J. Biochem. 243, 134-140.
Terasawa E., Kurian J.R., Guerriero K.A., Kenealy B.P., Hutz E.R. and Keen K.L. (2010). Recent Discoveries on the control of GnRH neurons in nonhuman primates. J. Neuroendocrinol. 22, 630-638.
Tesarik J., Hazout A. and Mendoza C. (2004). Enhancement of embryo developmental potential by a single administration of GnRH agonist at the time of implantation. Reproduction. 19, 1176-1180.
Tobin A.B., Totty N.F., Sterlin A.E. and Nahorski S.R. (1997). Stimulus dependent phosphorylation of G-protein-coupled receptors by casein kinase 1 alpha. J. Biol. Chem. 272, 20844-20849.
Turzillo A.M., Nolan T.E. and Nett T.M. (1998). Regulation of gonadotropin-releasing hormone (GnRH) receptor gene expression in sheep: Interaction of GnRH and estradiol. Endocrinology. 139, 4890-4894.
Vrecl M., Anderson L., Hanyaloglu A., McGregor A.M., Groarke A.D., Milligan G., Taylor P.L. and Eidne KA. (1998). Agonist-induced endocytosis and recycling of the gonadotropin-releasing hormone receptor: effect of beta-arrestin on internalization kinetics. Mol. Endocrinol. 12, 1818-1829.
White R.B., Eisen J.A., Kasten T.L. and Fernald R.D. (1998). Second gene for gonadotropin-releasing hormone in humans. Proc. Natl. Acad. Sci. USA. 95, 305-309.
Whitelaw P.F., Eidne K.A., Sellar R., Smyth C.D. and Hillier S.G. (1995). Gonadotropin-releasing hormone receptor ribonucleic acid expression in rat ovary. Endocrinology. 136, 172-179.
Willars G.B., Heding A., Vrecl M., Sellar R., Blomenröhr M., Nahorski S.R. and Eidne K.A. (1999). Lack of a C-terminal tail in the mammalian gonadotropin-releasing hormone receptor confers resistance to agonist-dependent phosphorylation and rapid desensitization. J. Biol. Chem. 274, 30146-30153.
Wray S., Zoeller R.T. and Gainer H. (1989). Differential effects of estrogen on luteinizing hormone-releasing hormone gene expression in slice explant cultures prepared from specific rat forebrain regions. Mol. Endocrinol. 3, 1197-1206.
Zhang J., Ferguson S.S., Barak L.S., Aber M.J., Giros B., Lefkowitz R.J. and Caron M.G. (1997). Molecular mechanisms of G protein-coupled receptor signaling: role of G protein-coupled receptor kinases and arrestins in receptor desensitization and resensitization. Recept. Chan. 5, 193-199.
Zoeller R.T. and Young W.S. (1988). Changes in cellular levels of messenger ribonucleic acid encoding gonadotropin-releasing hormone in the anterior hypothalamus of female rats during the estrous cycle. Endocrinology. 123, 1688-1689.