Evidence that down regulation of hypothalamic KiSS-1 expression is involved in the negative feedback action of testosterone to regulate luteinising hormone secretion in the adult male rhesus monkey (Macaca mulatta)

Journal of Neuroendocrinology

Volumn 19, Issue 6, 2007, Pages 432-438

  Shibata, M ^a   Friedman, R L ^a   Ramaswamy, S ^a   Plant, T M ^a,b  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF OCCUPATIONAL AND ENVIRONMENTAL HEALTH   (Japan)

Author keywords

GPR54; KiSS 1; Kisspeptin; LH; Monkey

Indexed keywords

FOLLITROPIN; G PROTEIN COUPLED RECEPTOR 54; GONADORELIN; KISSPEPTIN; LUTEINIZING HORMONE; MESSENGER RNA; RIBONUCLEASE; TESTOSTERONE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CASTRATION; CONTROLLED STUDY; DOWN REGULATION; HORMONE ACTION; HORMONE RELEASE; HYPOTHALAMUS; MALE; NEGATIVE FEEDBACK; NEUROBIOLOGY; NONHUMAN; PREOPTIC AREA; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; RHESUS MONKEY; SIGNAL TRANSDUCTION;

ANIMALS; DOWN-REGULATION; FEEDBACK, BIOCHEMICAL; FOLLICLE STIMULATING HORMONE; GONADOTROPIN-RELEASING HORMONE; HYPOTHALAMUS; LUTEINIZING HORMONE; MACACA MULATTA; MALE; NERVE TISSUE PROTEINS; PITUITARY GLAND; RECEPTORS, G-PROTEIN-COUPLED; RNA, MESSENGER; SIGNAL TRANSDUCTION; TESTOSTERONE;

EID: 34248677312     PISSN: 09538194     EISSN: 13652826     Source Type: Journal    
DOI: 10.1111/j.1365-2826.2007.01549.x     Document Type: Article

References (42)

1. Plant TM, Dubey AK. Evidence from the rhesus monkey (Macaca mulatta) for the view that negative feedback control of luteinizing hormone secretion by the testis is mediated by a deceleration of hypothalamic gonadotropin-releasing hormone pulse frequency. Endocrinology 1984; 115: 2145-2153.
2. Plant TM. Gonadal regulation of hypothalamic gonadotropin-releasing hormone release in primates. Endocrine Rev 1986; 7: 75-88.
3. Grumbach MM. Pubertal maturation in aromatase deficiency and resistance to estrogen. In: Bourguignon JP, Plant TM, eds. The Onset of Puberty in Perspective. Amsterdam: Elsevier, 2000: 247-267.
4. Rhen T, Cidlowski JA. Steroid hormone action. In: Strauss JF III, Barbieri RL, eds. Yen and Jaffe's Reproductive Endocrinology. Physiology, Pathophysiology, and Clinical Management, 5th edn. Philadelphia, PA: Elsevier, 2004: 155-174.
5. Herbison AE, Skinner DC, Robinson JE, King IS. Androgen receptor-immunoreactive cells in ram hypothalamus: Distribution and co-localization patterns with gonadotropin-releasing hormone, somatostatin and tyrosine hydroxylase. Neuroendocrinology 1996; 63: 120-131.
6. Herbison AE. Physiology of the gonadotropin-releasing hormone neuronal network. In: Neill JD, ed. Knobil and Neill's Physiology of Reproduction, 3rd edn. San Diego, CA: Elsevier, 2006: 1415-1482.
7. Scott CJ, Tilbrook AJ, Rawson JA, Clarke IJ. Gonadal steroid receptors in the regulation of GnRH secretion in farm animals. Anim Reprod Sci 2000; 60-61: 313-326.
8. de Roux N, Genin E, Carel JC, Matsuda F, Chaussain JL, Milgrom E. Hypogonadotropic hypogonadism due to loss of function of the KiSS1-derived peptide receptor GPR54. Proc Natl Acad Sci USA 2003; 100: 10972-10976.
9. Seminara SB, Messager S, Chatzidaki EE, Thresher RR, Acierno JS, Jr Shagoury JK, Bo-Abbas Y, Kuohung W, Schwinof KM, Hendrick AG, Zahn D, Dixon J, Kaiser UB, Slaugenhaupt SA, Gusella JF, O'Rahilly S, Carlton MBL, Crowley WF, Jr Aparicio SAJR, Colledge WH. The GPR54 gene as a regulator of puberty. N Engl J Med 2003; 349: 1589-1592.
10. Funes S, Hendrick JA, Vassileva G, Markowitz L, Abbondanzo S, Golovko A, Yang S, Monsma FJ, Gustafson EL. The KiSS-1 receptor GPR54 is essential for the development of the murine reproductive system. Biochem Biophys Res Commun 2003; 312: 1357-1363.
11. Ohtaki T, Shintani Y, Honda S, Matsumoto H, Hori A, Kanehashi K, Terao Y, Kumano S, Takatsu Y, Masuda Y, Ishibashi Y, Watanabe T, Asada M, Yamada T, Suenaga M, Kitada C, Usuki S, Kurokawa T, Onada H, Nishimura O, Fujino M. Metastasis suppressor gene KiSS -1 encodes peptide ligand of a G-protein-coupled receptor. Nature 2001; 411: 613-617.
12. Muir AI, Chamberlain L, Elshourbagy NA, Michalovich D, Moore DJ, Calamari A, Szekeres PG, Sarau HM, Chambers JK, Murdock P, Steplewski K, Shabon U, Miller JE, Middleton SE, Darker JG, Larminie CGC, Wilson S, Bergsma DJ, Emson P, Faull R, Philpott KL, Harrison DC. AXOR12, a novel human G protein-coupled receptor, activated by the peptide KiSS -1. J Biol Chem 2001; 276: 28969-28975.
13. Kotani M, Detheux M, Vandenbogaerde A, Communi D, Vanderwinden JM, Le Poul E, Brezillon S, Tyldesley R, Suarez-Huerta N, Vandeputt F, Blanpain C, Schiffmann SN, Vassart G, Parmentier M. The metastasis suppressor gene KiSS -1 encodes kisspeptins, the natural ligands of the orphan G protein-coupled receptor GPR54. J Biol Chem 2001; 276: 34631-34636.
14. Lee JH, Miele ME, Hicks DJ, Phillips KK, Trent JM, Weissman BE, Welch DR. KiSS-1, a novel human malignant melanoma metastis-suppressor gene. J Natl Cancer Inst 1996; 88: 1731-1736.
15. Gottsch ML, Cunningham MJ, Smith JT, Popa SM, Acohido BV, Crowley WF, Seminara S, Clifton DK, Steiner RA. A role for kisspeptins in the regulation of gonadotropin secretion in the mouse. Endocrinology 2004; 145: 4073-4077.
16. Shahab M, Mastronardi C, Seminara SB, Crowley WF, Ojeda SR, Plant TM. Increased hypothalamic GPR54 signaling: A potential mechanism for initiation of puberty in primates. Proc Natl Acad Sci USA 2005; 102: 2129-2134.
17. Franceschini I, Lomet D, Cateau M, Delsol G, Tillet Y, Caraty A. Kisspeptin immunoreactive cells of the ovine preoptic area and arcuate nucleus co-express estrogen receptor alpha. Neurosci Lett 2006; 401: 225-230.
18. Irwig MS, Fraley GS, Smith JT, Acohido BV, Popa SM, Cunningham MJ, Gottsch ML, Clifton DK, Steiner RA. Kisspeptin activation of gonadotropin releasing hormone neurons and regulation of KiSS-1 mRNA in the male rat. Neuroendocrinology 2004; 80: 264-272.
19. Messager S, Chatzidaki EE, Ma D, Hendrick AG, Zahn D, Dixon J, Thresher RR, Malinge I, Lomet D, Carlton MB, Colledge WH, Caraty A, Aparicio SA. Kisspeptin directly stimulates gonadotropin-releasing hormone release via G protein-coupled receptor 54. Proc Natl Acad Sci USA 2005; 102: 1761-1766.
20. Han SK, Gottsch ML, Lee KJ, Popa SM, Smith JT, Jakawich SK, Clifton DK, Steiner RA, Herbison AE. Activation of gonadotropin-releasing hormone neurons by kisspeptin as a neuroendocrine switch for the onset of puberty. J Neurosci 2005; 25: 11349-11356.
21. Thompson EL, Patterson M, Murphy KG, Smith KL, Dhillo WS, Todd JF, Ghatei MA, Bloom SR. Central and peripheral administration of kisspeptin-10 stimulates the hypothalamic-pituitary-gonadal axis. J Neuroendocrinol 2004; 16: 850-858.
22. Navarro VM, Castellano JM, Fernández-Fernández R, Barreiro ML, Roa J, Sanchez-Criado JE, Aguilar E, Dieguez C, Pinilla L, Tena-Sempere M. Characterization of the potent LH releasing activity of KiSS-1 peptide, the natural ligand of GPR54. Endocrinology 2005; 146: 156-163.
23. Navarro VM, Castellano JM, Fernandez-Fernandez R, Barreiro ML, Roa J, Sanchez-Criado JE, Aguilar E, Dieguez C, Pinilla L, Tena-Sempere M. Developmental and hormonally regulated messenger ribonucleic acid expression of KiSS-1 and its putative receptor, GPR54, in rat hypothalamus and potent luteinizing hormone-releasing activity of KiSS-1 peptide. Endocrinology 2004; 145: 4565-4574.
24. Smith JT, Cunningham MJ, Rissman EF, Clifton DK, Steiner RA. Regulation of Kiss1 gene expression in the brain of the female mouse. Endocrinology 2005; 146: 3686-3692.
25. Smith JT, Dungan HM, Stoll EA, Gottsch ML, Braun RE, Eacker SM, Clifton DK, Steiner RA. Differential regulation of KiSS-1 mRNA expression by sex steroids in the brain of the male mouse. Endocrinology 2005; 146: 2976-2984.
26. Gottsch ML, Clifton DK, Steiner RA. Kisspeptin-GPR54 signaling in the neuroendocrine reproductive axis. Mol Cel Endocrinol 2006; 254-255: 91-96.
27. Marshall GR, Ramaswamy S, Plant TM. Gonadotropin independent proliferation of the pale type A spermatogonia in the adult rhesus monkey (Macaca mulatta). Biol Reprod 2005; 73: 222-229.
28. Ramaswamy S, Pohl CR, McNeilly AS, Winters SJ, Plant TM. The time course of follicle-stimulating hormone suppression by recombinant human inhibin A in the adult male rhesus monkey (Macaca mulatta). Endocrinology 1998; 139: 3409-3415.
29. El Majdoubi M, Ramaswamy S, Sahu A, Plant TM. Effects of orchidectomy on levels of the mRNAs encoding gonadotropin-releasing hormone and other hypothalamic peptides in the adult male rhesus monkey (Macaca mulatta). J Neuroendocrinol 2000; 12: 167-176.
30. Plant TM. Time courses of concentrations of circulating gonadotropin, prolactin, testosterone, and cortisol in adult male rhesus monkeys (Macaca mulatta) throughout the 24 h light-dark cycle. Biol Reprod 1981; 25: 244-252.
31. Kauffman AS, Gottsch ML, Roa J, Byquist AC, Crown A, Clifton DK, Hoffman GE, Steiner RA, Tena-Sempere M. Sexual differentiation of KiSS-1 gene expression in the brain of the rat. Endocrinology 2007; January 4 [Epub ahead of print]: 10.1210/en.2006-1540.
32. Paxionos G, Huang XF, Toga AW. The Rhesus Monkey Brain in Stereotaxic Coordinates. San Diego: Academic Press 2000.
33. Winters SJ, Troen P, Plant TM. Relationship between testosterone binding globulin and the failure of androgens to suppress serum gonadotropin concentrations in long-term castrated adult male rhesus monkeys (Macaca mulatta). J Steroid Biochem 1981; 14 (1223-1227): 1981.
34. Resko JA, Pereyra-Martinez AC, Stadelman HL, Roselli CE. Cellular observations and hormonal correlates of feedback control of luteinizing hormone secretion by testosterone in long-term castrated male rhesus monkeys. Biol Reprod 2000; 63: 872-878.
35. Hileman SM, Lubbers LS, Petersen SL, Kuehl DE, Scott CJ, Jackson GL. Influence of testosterone on LHRH release, LHRH mRNA and proopiomelanocortin mRNA in the male sheep. J Neuroendocrinol 1996; 8: 113-121.
36. Sagrillo CA, Grattan DR, McCarthy MM, Selmanoff M. Hormonal and neurotransmitter regulation of GnRh gene expression and related reproductive behaviors. Behav Genet 1996; 26: 241-277.
37. Spratt DP, Herbison AE. Regulation of preoptic area gonadotropin-releasing hormone (GnRH) mRNA expression by gonadal steroids in the long-term gonadectomized male rat. Mol Brain Res 1997; 47: 125-133.
38. Adams LA, Vician L, Clifton DK, Steiner RA. Testosterone regulates pro-opiomelanocortin gene expression in the primate brain. Endocrinology 1991; 128: 1881-1886.
39. Sagrillo CA, Selmanoff M. Castration decreases single cell levels of mRNA encoding glutamic acid decarboxylase in the diagonal band of broca and the sexually dimorphic nucleus of the preoptic area. J Neuroendocrinol 1997; 9: 699-706.
40. Mitsushima D, Hei DL, Terasawa E. γ-Aminobutyric acid is an inhibitory neurotransmitter restricting the release of luteinizing the release of luteinizing hormone-releasing hormone before the onset of puberty. Proc Natl Acad Sci USA 1994; 91: 395-399.
41. Ferreira SA, Scott CJ, Kuehl DE, Jackson GL. Differential regulation of luteinizing hormone release by γ-aminobutyric acid receptor subtypes in the arcuate-ventromedial region of the castrated ram. Endocrinology 1996; 137: 3453-34760.
42. Veldhuis JD, Rogol AD, Samojlik E, Ertel NH. Role of endogenous opiates in the expression of negative feedback action of androgens and estrogens on pulsatile properties of luteinizing hormone secretion in man. J Clin Invest 1984; 74: 47-55.