Regulation of gonadotropin-releasing hormone in nonhypothalamic tissues

Seminars in Reproductive Medicine

Volumn 25, Issue 5, 2007, Pages 326-336

  Kim, Helen H ^a   Mui, Keeley L ^a   Nikrodhanond, Amisra A ^a   Tamayo, Niña Carmela R ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

Breast; Gene regulation; Gonadotropin releasing hormone (GnRH); Ovary; Placenta; Prostate; Testes; Tissue specific expression

Indexed keywords

ESTRADIOL; ESTROGEN; GLUCOCORTICOID; GONADORELIN;

BREAST; FEMALE GENITAL SYSTEM; GENE CONTROL; GENE STRUCTURE; HORMONAL REGULATION; HORMONE ACTION; HORMONE RELEASE; HUMAN; HYPOTHALAMUS; IMMUNOREACTIVITY; MALE GENITAL SYSTEM; NONHUMAN; OVARY; PLACENTA; PROSTATE; PROTEIN BINDING; REPRODUCTION; REVIEW; TESTIS; TRANSCRIPTION REGULATION;

ANIMALS; BREAST; FEMALE; GENE EXPRESSION REGULATION; GENITALIA, MALE; GONADOTROPIN-RELEASING HORMONE; HUMANS; HYPOTHALAMUS; MALE; MAMMARY GLANDS, ANIMAL; OVARY; PLACENTA; REPRODUCTION; TRANSCRIPTION, GENETIC;

EID: 34548314192     PISSN: 15268004     EISSN: None     Source Type: Journal    
DOI: 10.1055/s-2007-984738     Document Type: Review

References (131)

1. Cheng CK, Leung PC. Molecular biology of gonadotropin-releasing hormone (GnRH)-I, GnRH-II, and their receptors in humans. Endocr Rev 2005;26:283-306
2. Harrison GS, Wierman ME, Nett TM, Glode LM. Gonadotropin-releasing hormone and its receptor in normal and malignant cells. Endocr Relat Cancer 2004;11:725-748
3. Limonta P, Moretti RM, Marelli MM, Motta M. The biology of gonadotropin hormone-releasing hormone: role in the control of tumor growth and progression in humans. Front Neuroendocrinol 2003;24:279-295
4. Gore AC. Multiple GnRH Molecules Phylogeny and Evolution. In: Gore AC, ed. GnRH: the Master Molecule of Reproduction. Norwell, MA: Kluwer Academic; 2002
5. Fernald RD, White RB. Gonadotropin-releasing hormone genes: phylogeny, structure, and functions. Front Neuroendocrinol 1999;20:224-240
6. Givens ML, Kurotani R, Rave-Harel N, Miller NL, Mellon PL. Phylogenetic footprinting reveals evolutionarily conserved regions of the gonadotropin-releasing hormone gene that enhance cell-specific expression. Mol Endocrinol 2004; 18:2950-2966
7. Eraly SA, Mellon PL. Regulation of gonadotropin-releasing hormone transcription by protein kinase C is mediated by evolutionarily conserved promoter-proximal elements. Mol Endocrinol 1995;9:848-859
8. Belsham DD, Lovejoy DA. Gonadotropin-releasing hormone: gene evolution, expression, and regulation. Vitam Horm 2005;71:59-94
9. Chandran UR, DeFranco DB. Regulation of gonadotropin-releasing hormone gene transcription. Behav Brain Res 1999;105:29-36
10. Seeburg PH, Adelman JP. Characterization of cDNA for precursor of human luteinizing hormone releasing hormone. Nature 1984;311:666-668
11. Gibbons JM Jr, Mitnick M, Chieffo V. In vitro biosynthesis of TSH- and LH-releasing factors by the human placenta. Am J Obstet Gynecol 1975;121:127-131
12. Khodr GS, Siler-Khodr TM. Placental luteinizing hormone-releasing factor and its synthesis. Science 1980; 207: 315-317
13. Khodr G, Siler-Khodr TM. The effect of luteinizing hormone-releasing factor on human chorionic gonadotropin secretion. Fertil Steril 1978;30:301-304
14. Siler-Khodr TM, Khodr GS. Dose response analysis of gnRH stimulation of hCG release from human term placenta. Biol Reprod 1981;25:353-358
15. Miyake A, Sakumoto T, Aono T, Kawamura Y, Maeda T, Kurachi K. Changes in luteinizing hormone-releasing hormone in human placenta throughout pregnancy. Obstet Gynecol 1982;60:444-449
16. Currie AJ, Fraser HM, Sharpe RM. Human placental receptors for luteinizing hormone releasing hormone. Biochem Biophys Res Commun 1981;99:332-338
17. Belisle S, Guevin JF, Bellabarba D, Lehoux JG. Luteinizing hormone-releasing hormone binds to enriched human placental membranes and stimulates in vitro the synthesis of bioactive human chorionic gonadotropin. J Clin Endocrinol Metab 1984;59:119-126
18. Wolfahrt S, Kleine B, Rossmanith WG. Detection of gonadotrophin releasing hormone and its receptor mRNA in human placental trophoblasts using in-situ reverse transcription-polymerase chain reaction. Mol Hum Reprod 1998;4:999-1006
19. Rice GE, Smirnis M. Identification of luteinizing hormone releasing hormone-like immunoactivity in ovine cotyledons. Regul Pept 1990;27:51-59
20. Gautron JP, Pattou E, Kordon C. Occurrence of higher molecular forms of LHRH in fractionated extracts from rat hypothalamus, cortex and placenta. Mol Cell Endocrinol 1981;24:1-15
21. Nowak RA, Bahr JM. Secretion of a gonadotrophin-releasing hormone- (GnRH-)like factor by the rabbit fetal placenta in vitro. Placenta 1987;8:299-304
22. Gohar J, Mazor M, Leiberman JR. GnRH in pregnancy. Arch Gynecol Obstet 1996;259:1-6
23. Bercu BB, Hyashi A, Poth M, Alexandrova M, Soloff MS, Donahoe PK. Luteinizing hormone-releasing hormone-induced delay of parturition. Endocrinology 1980;107:504-508
24. Kang IS, Koong MK, Forman J, Siler-Khodr TM. Dose-related action of gonadotropin-releasing hormone on basal prostanoid production from the human term placenta. Am J Obstet Gynecol 1991;165:1771-1776
25. Chou CS, Beristain AG, MacCalman CD, Leung PC. Cellular localization of gonadotropin-releasing hormone (GnRH) I and GnRH II in first-trimester human placenta and decidua. J Clin Endocrinol Metab 2004;89:1459-1466
26. Chou CS, Zhu H, MacCalman CD, Leung PC. Regulatory effects of gonadotropin-releasing hormone (GnRH) I and GnRH II on the levels of matrix metalloproteinase (MMP)-2, MMP-9, and tissue inhibitor of metalloproteinases-1 in primary cultures of human extravillous cytotrophoblasts. J Clin Endocrinol Metab 2003;88:4781-4790
27. Chou CS, MacCalman CD, Leung PC. Differential effects of gonadotropin-releasing hormone I and II on the urokinase-type plasminogen activator/plasminogen activator inhibitor system in human decidual stromal cells in vitro. J Clin Endocrinol Metab 2003;88:3806-3815
28. Chou CS, Tai CJ, MacCalman CD, Leung PC. Dose-dependent effects of gonadotropin releasing hormone on matrix metalloproteinase (MMP)-2, and MMP-9 and tissue specific inhibitor of metalloproteinases-1 messenger ribonucleic acid levels in human decidual Stromal cells in vitro. J Clin Endocrinol Metab 2003;88:680-688
29. Radovick S, Wondisford FE, Nakayama Y, Yamada M, Cutler GB Jr, Weintraub BD. Isolation and characterization of the human gonadotropin-releasing hormone gene in the hypothalamus and placenta. Mol Endocrinol 1990;4:476-480
30. Dong KW, Yu KL, Roberts JL. Identification of a major up-stream transcription start site for the human progonadotropin-releasing hormone gene used in reproductive tissues and cell lines. Mol Endocrinol 1993;7:1654-1666
31. Wong B C, Wang X, Oehninger S, Gibbons WE, Dong KW. Estrogen down-regulates GnRH gene expression in human placental cytotrophoblast cells. Mol Cell Endocrinol 2004;213:199-210
32. Dong KW, Yu KL, Chen ZG, Chen YD, Roberts JL. Characterization of multiple promoters directing tissue-specific expression of the human gonadotropin-releasing hormone gene. Endocrinology 1997;138:2754-2762
33. Wolfe A, Kim HH, Tobet S, Stafford DE, Radovick S. Identification of a discrete promoter region of the human GnRH gene that is sufficient for directing neuron-specific expression: a role for POU homeodomain transcription factors. Mol Endocrinol 2002;16:435-449
34. Clark ME, Mellon PL. The POU homeodomain transcription factor Oct-1 is essential for activity of the gonadotropin-releasing hormone neuron-specific enhancer. Mol Cell Biol 1995;15:6169-6177
35. Dong KW, Zheng HM, Wen ZY, Chen ZG. The POU homeodomain protein Oct-1 binds Cis-regulatory element essential for the human GnRH upstream promoter activity in JEG-3 cells. J Clin Endocrinol Metab 2001;86:2838-2844
36. Chen ZG, Chou CS, Hsu MI, Dong KW. Glucocorticoids modulate human gonadotrophin releasing hormone upstream promoter activity in transfected human placental cells (JEG-3). Mol Hum Reprod 1998;4:93-99
37. Radovick S, Ticknor CM, Nakayama Y, et al. Evidence for direct estrogen regulation of the human gonadotropin-releasing hormone gene. J Clin Invest 1991;88:1649-1655
38. Wierman ME, Kepa JK, Sun W, Gordon DF, Wood WM. Estrogen negatively regulates rat gonadotropin releasing hormone (rGnRH) promoter activity in transfected placen3 tal cells. Mol Cell Endocrinol 1992;86:1-10
39. Dong KW, Chen ZG, Cheng KW, Yu KL. Evidence for estrogen receptor-mediated regulation of human gonadotropin-releasing hormone promoter activity in human placental cells. Mol Cell Endocrinol 1996;117:241-246
40. Chen Z, Zheng H, Dong KW. Identification of negative and positive estrogen response elements in human GnRH upstream promoter in the placental JEG-3 cells. Mol Cell Endocrinol 2001;184:125-134
41. Janssens RM, Brus L, Cahill DJ, Huirne JA, Schoemaker J, Lambalk CB. Direct ovarian effects and safety aspects of GnRH agonists and antagonists. Hum Reprod Update 2000;6:505-518
42. Kang SK, Choi KC, Yang HS, Leung PC. Potential role of gonadotrophin-releasing hormone (GnRH)-I and GnRH-II in the ovary and ovarian cancer. Endocr Relat Cancer 2003;10:169-177
43. Takekida S, Deguchi J, Samoto T, Matsuo H, Maruo T. Comparative analysis of the effects of gonadotropin-releasing hormone agonist on the proliferative activity, apoptosis, and steroidogenesis in cultured porcine granulosa cells at varying stages of follicular growth. Endocrine 2000;12:61-67
44. Saragueta PE, Lanuza GM, Baranao JL. Inhibitory effect of gonadotrophin-releasing hormone (GnRH) on rat granulosa cell deoxyribonucleic acid synthesis. Mol Reprod Dev 1997;47:170-174
45. Billig H, Furuta I, Hsueh AJ. Gonadotropin-releasing hormone directly induces apoptotic cell death in the rat ovary: biochemical and in situ detection of deoxyribonucleic acid fragmentation in granulosa cells. Endocrinology 1994; 134:245-252
46. Zhao S, Saito H, Wang X, Saito T, Kaneko T, Hiroi M. Effects of gonadotropin-releasing hormone agonist on the incidence of apoptosis in porcine and human granulosa cells. Gynecol Obstet Invest 2000;49:52-56
47. Goto T, Endo T, Henmi H, et al. Gonadotropin-releasing hormone agonist has the ability to induce increased matrix metalloproteinase (MMP)-2 and membrane type 1-MMP expression in corpora lutea, and structural luteolysis in rats. J Endocrinol 1999;161:393-402
48. Tilly JL, LaPolt PS, Hsueh AJ. Hormonal regulation of follicle-stimulating hormone receptor messenger ribonucleic acid levels in cultured rat granulosa cells. Endocrinology 1992;130:1296-1302
49. Hsueh AJ, Erickson GF. Extrapituitary action of gonadotropin-releasing hormone: direct inhibition ovarian steroidogenesis. Science 1979;204:854-855
50. Vaananen JE, Tong BL, Vaananen CM, Chan IH, Yuen BH, Leung PC. Interaction of prostaglandin F2alpha and gonadotropin-releasing hormone on progesterone and estradiol production in human granulosa-luteal cells. Biol Reprod 1997;57:1346-1353
51. Leung PC, Cheng CK, Zhu XM. Multi-factorial role of GnRH-I and GnRH-II in the human ovary. Mol Cell Endocrinol 2003;202:145-153
52. Piquette GN, LaPolt PS, Oikawa M, Hsueh AJ. Regulation of luteinizing hormone receptor messenger ribonucleic acid levels by gonadotropins, growth factors, and gonadotropin-releasing hormone in cultured rat granulosa cells. Endocrinology 1991;128:2449-2456
53. Lynch JP, Lala DS, Peluso JJ, Luo W, Parker KL, White BA. Steroidogenic factor 1, an orphan nuclear receptor, regulates the expression of the rat aromatase gene in gonadal tissues. Mol Endocrinol 1993;7:776-786
54. Sridaran R, Philip GH, Li H, et al. GnRH agonist treatment decreases progesterone synthesis, luteal peripheral benzodiazepine receptor mRNA, ligand binding and steroidogenic acute regulatory protein expression during pregnancy. J Mol Endocrinol 1999;22:45-54
55. Clayton RN, Harwood JP, Catt KJ. Gonadotropin-releasing hormone analogue binds to luteal cells and inhibits progesterone production. Nature 1979;282:90-92
56. Macdonald GJ, Beattie CW. Pregnancy failure in hypophysectomized rats following LH-RH administration. Life Sci 1979;24:1103-1110
57. Jones PB, Hsueh AJ. Direct inhibitory effect of gonadotropin-releasing hormone upon luteal luteinizing hormone receptor and steroidogenesis in hypophysectomized rats. Endocrinology 1980;107:1930-1936
58. Corbin A, Bex FJ. Luteinizing hormone releasing hormone agonists induce ovulation in hypophysectomized proestrous rats: direct ovarian effect. Life Sci 1981;29:185-192
59. Ekholm C, Hillensjo T, Isaksson O. Gonadotropin releasing hormone agonists stimulate oocyte meiosis and ovulation in hypophysectomized rats. Endocrinology 1981; 108:2022-2024
60. Wong WY, Richards JS. Induction of prostaglandin H synthase in rat preovulatory follicles by gonadotropin-releasing hormone. Endocrinology 1992;130:3512-3521
61. Morris JK, Richards JS. Hormone induction of luteinization and prostaglandin endoperoxide synthase-2 involves multiple cellular signaling pathways. Endocrinology 1993;133: 770-779
62. Natraj U, Richards JS. Hormonal regulation, localization, and functional activity of the progesterone receptor in granulosa cells of rat preovulatory follicles. Endocrinology 1993;133:761-769
63. Ny T, Liu YX, Ohlsson M, Jones PB, Hsueh AJ. Regulation of tissue-type plasminogen activator activity and messenger RNA levels by gonadotropin- releasing hormone in cultured rat granulosa cells and cumulus-oocyte complexes. J Biol Chem 1987;262:11790-11793
64. Hillensjo T, LeMaire WJ. Gonadotropin releasing hormone agonists stimulate meiotic maturation of follicle-enclosed rat oocytes in vitro. Nature 1980;287:145-146
65. Magnusson C, LeMaire WJ. A gonadotrophin-releasing hormone agonist stimulates oxygen consumption and maturation of follicle-enclosed rat oocytes in vitro. Acta Physiol Scand 1981;111:377-379
66. Yoshimura Y, Nakamura Y, Ando M, Shiokawa S, Koyama N, Nanno T. Direct effect of gonadotropin-releasing hormone agonists on the rabbit ovarian follicle. Fertil Steril 1992;57:1091-1097
67. Schirman-Hildesheim TD, Bar T, Ben-Aroya N, Koch Y. Differential gonadotropin-releasing hormone (GnRH) and GnRH receptor messenger ribonucleic acid expression patterns in different tissues of the female rat across the estrous cycle. Endocrinology 2005;146:3401-3408
68. Reeves JJ, Seguin C, Lefebvre FA, Kelly PA, Labrie F. Similar luteinizing hormone-releasing hormone binding sites in rat anterior pituitary and ovary. Proc Natl Acad Sci U S A 1980;77:5567-5571
69. Jones PB, Conn PM, Marian J, Hsueh AJ. Binding of gonadotropin releasing hormone agonist to rat ovarian granulosa cells. Life Sci 1980;27:2125-2132
70. Seguin C, Pelletier G, Dube D, Labrie F. Distribution of luteinizing hormone-releasing hormone receptors in the rat ovary. Regul Pept 1982;4:183-190
71. Olofsson JI, Conti CC, Leung PC. Homologous and heterologous regulation of gonadotropin-releasing hormone receptor gene expression in preovulatory rat granulosa cells. Endocrinology 1995;136:974-980
72. Minaretzis D, Jakubowski M, Mortola JF, Pavlou SN. Gonadotropin-releasing hormone receptor gene expression in human ovary and granulosa-lutein cells. J Clin Endocrinol Metab 1995;80:430-434
73. Kang SK, Choi KC, Cheng KW, Nathwani PS, Auersperg N, Leung PC. Role of gonadotropin-releasing hormone as an autocrine growth factor in human ovarian surface epithelium. Endocrinology 2000;141:72-80
74. Ramakrishnappa N, Rajamahendran R, Lin YM, Leung PC. GnRH in non-hypothalamic reproductive tissues. Anim Reprod Sci 2005;88:95-113
75. Bull P, Morales P, Huyser C, Socias T, Castellon EA. Expression of GnRH receptor in mouse and rat testicular germ cells. Mol Hum Reprod 2000;6:582-586
76. Moumni M, Kottler ML, Counis R. Nucleotide sequence analysis of mRNAs predicts that rat pituitary and gonadal gonadotropin-releasing hormone receptor proteins have identical primary structure. Biochem Biophys Res Commun 1994;200:1359-1366
77. Peng C, Fan NC, Ligier M, Vaananen J, Leung PC. Expression and regulation of gonadotropin-releasing hormone (GnRH) and GnRH receptor messenger ribonucleic acids in human granulosa-luteal cells. Endocrinology 1994;135:1740-1746
78. Hsueh AJ, Jones PB. Extrapituitary actions of gonadotropin-releasing hormone. Endocr Rev 1981;2:437-461
79. Nett TM, Akbar AM, Niswender GD. Serum levels of luteinizing hormone and gonadotropin-releasing hormone in cycling, castrated and anestrous ewes. Endocrinology 1974;94:713-718
80. Oikawa M, Dargan C, Ny T, Hsueh AJ. Expression of gonadotropin-releasing hormone and prothymosin-alpha messenger ribonucleic acid in the ovary. Endocrinology 1990;127:2350-2356
81. Clayton RN, Eccleston L, Gossard F, Thalbard JC, Morel G. Rat granulosa cells express the gonadotrophin-releasing hormone gene: evidence from in-situ hybridization histochemistry. J Mol Endocrinol 1992;9:189-195
82. Nathwani PS, Kang SK, Cheng KW, Choi KC, Leung PC. Regulation of gonadotropin-releasing hormone and its receptor gene expression by 17beta-estradiol in cultured human granulosa-luteal cells. Endocrinology 2000;141: 1754-1763
83. Chen ZG, Yu KL, Zheng HM, Dong KW. Estrogen receptor-mediated repression of gonadotropin-releasing hormone (GnRH) promoter activity in transfected CHOK1 cells. Mol Cell Endocrinol 1999;158:131-142
84. Goubau S, Bond CT, Adelmaln JP, et al. Partial characterization of the gonadotropin-releasing hormone (GNRH) gene transcript in the rat ovary. Endocrinology 1992;130: 3098-3100
85. Kim HH, Wolfe A, Smith GR, Tobet SA, Radovick S. Promoter sequences targeting tissue-specific gene expression of hypothalamic and ovarian gonadotropin-releasing hormone in vivo. J Biol Chem 2002;277:5194-5202
86. Kim HH, Wolfe A, Cohen RN, et al. In vivo identification of a 107-base pair promoter element mediating neuron-specific expression of mouse gonadotropin-releasing hormone. Mol Endocrinol 2007;21:457-471
87. Lawson MA, Macconell LA, Kim J, Powl BT, Nelson SB, Mellon PL. Neuron-specific expression in vivo by defined transcription regulatory elements of the GnRH gene. Endocrinology 2002;143:1404-1412
88. Wolfe AM, Wray S, Westphal H, Radovick S. Cell-specific expression of the human gonadotropin-releasing hormone gene in transgenic animals. J Biol Chem 1996;271:20018-20023
89. Baram T, Koch Y, Hazum E, Fridkin M. Gonadotropin-releasing hormone in milk. Science 1977;198:300-302
90. Palmon A, Ben Aroya N, Tel-Or S, Burstein Y, Fridkin M, Koch Y. The gene for the neuropeptide gonadotropin-releasing hormone is expressed in the mammary gland of lactating rats. Proc Natl Acad Sci USA 1994;91:4994-4996
91. Ikeda M, Taga M, Sakakibara H, Minaguchi H, Vonderhaar BK. Detection of messenger RNA for gonadotropin-releasing hormone (GnRH) but not for GnRH receptors in mouse mammary glands. Biochem Biophys Res Commun 1995;207:800-806
92. Amarant T, Fridkin M, Koch Y. Luteinizing hormone-releasing hormone and thyrotropin-releasing hormone in human and bovine milk. Eur J Biochem 1982;127:647-650
93. Smith SS, Ojeda SR. Maternal modulation of infantile ovarian development and available ovarian luteinizing hormone-releasing hormone (LHRH) receptors via milk LHRH. Endocrinology 1984;115:1973-1983
94. Levi LN, Ben-Aroya N, Tel-Or S, Palmon A, Burstein Y, Koch Y. Expression of the gene for the receptor of gonadotropin-releasing hormone in the rat mammary gland. FEBS Lett 1996;379:186-190
95. Kakar SS, Grizzle WE, Neill JD. The nucleotide sequences of human GnRH receptors in breast and ovarian tumors are identical with that found in pituitary. Mol Cell Endocrinol 1994;106:145-149
96. Seppala M, Wahlstrom T. Identification of luteinizing hormone-releasing factor and alpha subunit of glycoprotein hormones in ductal carcinoma of the mammary gland. Int J Cancer 1980;26:267-268
97. Harris N, Dutlow C, Eidne K, Dong KW, Roberts J, Millar R. Gonadotropin-releasing hormone gene expression in MDA-MB-231 and ZR-75-1 breast carcinoma cell lines. Cancer Res 1991;51:2577-2581
98. Kottler ML, Starzec A, Carre MC, Lagarde JP, Martin A, Counis R. The genes for gonadotropin-releasing hormone and its receptor are expressed in human breast with fibrocystic disease and cancer. Int J Cancer 1997;71:595-599
99. Chen A, Kaganovsky E, Rahimipour S, Ben-Aroya N, Okon E, Koch Y. Two forms of gonadotropin-releasing hormone (GnRH) are expressed in human breast tissue and overexpressed in breast cancer: a putative mechanism for the antiproliferative effect of GnRH by down-regulation of acidic ribosomal phosphoproteins P1 and P2. Cancer Res 2002;62:1036-1044
100. Grundker C, Huschmand Nia A, Emons G. Gonadotropin-releasing hormone receptor-targeted gene therapy of gynecologic cancers. Mol Cancer Ther 2005;4:225-231
101. Petersen SL, Ottem EN, Carpenter CD. Direct and indirect regulation of gonadotropin-releasing hormone neurons by estradiol. Biol Reprod 2003;69:1771-1778
102. Clayton RN, Katikineni M, Chan V, Dufau ML, Catt KJ. Direct inhibition of testicular function by gonadotropin-releasing hormone: mediation by specific gonadotropin-releasing hormone receptors in interstitial cells. Proc Natl Acad Sci USA 1980;77:4459-4463
103. Lefebvre FA, Reeves JJ, Seguin C, Massicotte J, Labrie F. Specific binding of a potent LHRH agonist in rat testis. Mol Cell Endocrinol 1980;20:127-134
104. Sharpe RM, Fraser HM. Leydig cell receptors for luteinizing hormone releasing hormone and its agonists and their modulation by administration or deprivation of the releasing hormone. Biochem Biophys Res Commun 1980;95:256-262
105. Fasano S, de Leeuw R, Pierantoni R, Chieffi G, van Oordt PG. Characterization of gonadotropin-releasing hormone (GnRH) binding sites in the pituitary and testis of the frog, Rana esculenta. Biochem Biophys Res Commun 1990;168: 923-932
106. Yu KL, He ML, Chik CC, Lin XW, Chang JP, Peter RE. mRNA expression of gonadotropin-releasing hormones (GnRHs) and GnRH receptor in goldfish. Gen Comp Endocrinol 1998;112:303-311
107. Botte MC, Chamagne AM, Carre MC, Counis R, Kottler ML. Fetal expression of GnRH and GnRH receptor genes in rat testis and ovary. J Endocrinol 1998;159:179-189
108. Bahk JY, Hyun JS, Chung SH, et al. Stage specific identification of the expression of GnRH mRNA and localization of the GnRH receptor in mature rat and adult human testis. J Urol 1995;154:1958-1961
109. Tieva A, Stattin P, Wikstrom P, Bergh A, Damber JE. Gonadotropin- releasing hormone receptor expression in the human prostate. Prostate 2001;47:276-284
110. Sharpe RM, Fraser HM. HCG stimulation of testicular LHRH-like activity. Nature 1980;287:642-643
111. Sharpe RM, Fraser HM, Cooper I, Rommerts FF. Sertoli-Leydig cell communication via an LHRH-like factor. Nature 1981;290:785-787
112. Paull WK, Turkelson CM, Thomas CR, Arimura A. Immunohistochemical demonstration of a testicular substance related to luteinizing hormone-releasing hormone. Science 1981;213:1263-1264
113. Azad N, Uddin S, La Paglia N, et al. Luteinizing hormone-releasing hormone (LHRH) in rat prostate: characterization of LHRH peptide, messenger ribonucleic acid expression, and molecular processing of LHRH in intact and castrated male rats. Endocrinology 1993;133:1252-1257
114. Uzbekova S, Lareyre J, Guiguen Y, Ferriere F, Bailhache T, Breton B. Expression of sGnRH mRNA in gonads during rainbow trout gametogenesis. Comp Biochem Physiol B Biochem Mol Biol 2001;129:457-465
115. Soverchia L, Carotti M, Andreu-Vieyra C, et al. Role of gonadotropin-releasing hormone (GnRH) in the regulation of gonadal differentiation in the gilthead seabream (Sparus aurata). Mol Reprod Dev 2007;74:57-67
116. Lau HL, Zhu XM, Leung PC, et al. Detection of mRNA expression of gonadotropin-releasing hormone and its receptor in normal and neoplastic rat prostates. Int J Oncol 2001;19:1193-1201
117. Bahk JY, Hyun JS, Lee H, et al. Expression of gonadotropin-releasing hormone (GnRH) and GnRH receptor mRNA in prostate cancer cells and effect of GnRH on the proliferation of prostate cancer cells. Urol Res 1998;26:259-264
118. Arimura A, Serafini P, Talbot S, Schally AV. Reduction of testicular luteinizing hormone/human chorionic gonadotropin receptors by [D-Trp6]-luteinizing hormone releasing hormone in hypophysectomized rats. Biochem Biophys Res Commun 1979;90:687-693
119. Hsueh AJ, Erickson GF. Extra-pituitary inhibition of testicular function by luteinising hormone releasing hormone. Nature 1979;281:66-67
120. Hsueh AJ, Schaeffer JM. Gonadotropin-releasing hormone as a paracrine hormone and neurotransmitter in extra-pituitary sites. J Steroid Biochem 1985;23:757-764
121. Bambino TH, Schreiber JR, Hsueh AJ. Gonadotropin-releasing hormone and its agonist inhibit testicular luteinizing hormone receptor and steroidogenesis in immature and adult hypophysectomized rats. Endocrinology 1980;107: 908-917
122. Sharpe RM, Cooper I. Stimulatory effect of LHRH and its agonists on Leydig cell steroidogenesis in vitro. Mol Cell Endocrinol 1982;26:141-150
123. Sharpe RM, Doogan DG, Cooper I. Stimulation of Leydig cell testosterone secretion in vitro and in vivo in hypophysectomized rats by an agonist of luteinizing hormone releasing hormone. Biochem Biophys Res Commun 1982;106:1210-1217
124. Andreu-Vieyra CV, Buret AG, Habibi HR. Gonadotropin-releasing hormone induction of apoptosis in the testes of goldfish (Carassius auratus). Endocrinology 2005;146:1588-1596
125. Minucci S, Di Matteo L, Pierantoni R, Varriale B, Rastogi RK, Chieffi G. In vivo and in vitro stimulatory effect of a gonadotropin-releasing hormone analog (HOE 766) on spermatogonial multiplication in the frog, Rana esculenta. Endocrinology 1986;119:731-736
126. Meistrich ML, Kangasniemi M. Hormone treatment after irradiation stimulates recovery of rat spermatogenesis from surviving spermatogonia. J Androl 1997;18:80-87
127. Meistrich ML, Wilson G, Huhtaniemi I. Hormonal treatment after cytotoxic therapy stimulates recovery of spermatogenesis. Cancer Res 1999;59:3557-3560
128. Morales P. Gonadotropin-releasing hormone increases ability of the spermatozoa to bind to the human zona pellucida. Biol Reprod 1998;59:426-430
129. Clayton RN. Gonadotrophin-releasing hormone: its actions and receptors. J Endocrinol 1989;120:11-19
130. Kaiser UB, Conn PM, Chin WW. Studies of gonadotropin-releasing hormone (GnRH) action using GnRH receptor-expressing pituitary cell lines. Endocr Rev 1997; 18:46-70
131. Gupta RK, Flaws JA. Gonadotropin-releasing hormone (GnRH) analogues and the ovary: do GnRH antagonists destroy primordial follicles? Fertil Steril 2005;83:1339-1342