Evidence from the agonadal juvenile male rhesus monkey (macaca mulatta) for the view that the action of neurokinin b to trigger gonadotropin-releasing hormone release is upstream from the kisspeptin receptor

Neuroendocrinology

Volumn 94, Issue 3, 2011, Pages 237-245

  Ramaswamy, Suresh ^a   Seminara, Stephanie B ^b   Plant, Tony M ^a  

^a UNIVERSITY OF PITTSBURGH   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

Gonadotropin releasing hormone; Kisspeptin; Kisspeptin receptor; KNDy neurons; Monkey; Neurokinin B

Indexed keywords

G PROTEIN COUPLED RECEPTOR 54; GONADORELIN; KISSPEPTIN 10; NEUROKININ 3 RECEPTOR; NEUROKININ B; SENKTIDE;

ANIMAL EXPERIMENT; ARTICLE; BIOASSAY; CASTRATION; CONTROLLED STUDY; DESENSITIZATION; HORMONE RELEASE; HYPOPHYSIS; HYPOTHALAMUS; MACACA MULATTA; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; SIGNAL TRANSDUCTION;

AGE FACTORS; ANIMALS; GENITALIA, MALE; GONADOTROPIN-RELEASING HORMONE; HUMANS; KISSPEPTINS; LUTEINIZING HORMONE; MACACA MULATTA; MALE; MODELS, ANIMAL; NEUROKININ B; ORCHIECTOMY; RECEPTORS, G-PROTEIN-COUPLED; RECEPTORS, NEUROKININ-3; SIGNAL TRANSDUCTION;

EID: 81355149648     PISSN: 00283835     EISSN: 14230194     Source Type: Journal    
DOI: 10.1159/000329045     Document Type: Article

References (48)

1. 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 MB, Crowley WF Jr, Apaicio SA, Colledge WH: The GPR54 gene as a regulator of puberty. N Engl J Med 2003; 349: 1614-1627. (Pubitemid 37303886)
2. De Roux N, Genin E, Carel JC, Matsuda F, Chaussain JL, Milgrom E: Hypogonadotropic hypogonadism due to loss of function of the KiSS-1-derived peptide receptor GPR54. Proc Natl Acad Sci USA 2003; 100: 10972-10976. (Pubitemid 37140137)
3. Topaloglu AK, Reimann F, Guclu M, Yalin AS, Kotan LD, Porter KM, Serin A, Mungan NL, Cook JR, Ozbek MN, Imamoglu S, Akalin NS, Yuksel B, O'Rahilly S, Semple RK: TAC3 and TACR3 mutations in familial hypogonadotropic hypogonadism reveal a key role for neurokinin B in the central control of reproduction. Nat Genet 2009; 41: 354-358.
4. Guran T, Tolhurst G, Bereket A, Rocha N, Porter K, Turan S, Gribble FM, Kotan LD, Akcay T, Atay Z, Canan H, Serin A, O'Rahilly S, Reimann F, Semple RK, Topaloglu AK: Hypogonadotropic hypogonadism due to a novel missense mutation in the first extracellular loop of the neurokinin B receptor. J Clin Endocrinol Metab 2009; 94: 3633-3639.
5. Young J, Bouligand J, Francou B, Raffin-Sanson ML, Gaillez S, Jeanpierre M, Grynberg M, Kamenicky P, Chanson P, Brailly-Tabard S, Guiochon-Mantel A: TAC3 and TACR3 defects cause hypothalamic congenital hypogonadotropic hypogonadism in humans. J Clin Endocrinol Metab 2010; 95: 2287-2295.
6. Goodman RL, Lehman MN, Smith JT, Coolen LM, de Oliveira CVR, Jafarzadehshirazi MR, Pereira A, Iqbal J, Caraty A, Ciofi P, Clarke IJ: Kisspeptin neurons in the arcuate nucleus of the ewe express both dynorphin A and neurokinin B. Endocrinology 2007; 148: 5752-5760. (Pubitemid 350146171)
7. Navarro VM, Gottsch ML, Chavkin C, Okamura H, Clifton DK, Steiner RA: Regulation of gonadotropin-releasing hormone secretion by kisspeptin/dynorphin/ neurokinin B neurons in the arcuate nucleus of the mouse. J Neurosci 2009; 29: 11859-11866.
8. Cheng G, Coolen LM, Padmanabhan V, Goodman RL, Lehman MN: The kisspeptin/neurokinin B/dynorphin (KNDy) cell population of the arcuate nucleus: sex differences and effects of prenatal testosterone in sheep. Endocrinology 2010; 151: 301-311.
9. Ramaswamy S, Seminara SB, Ali B, Ciofi P, Amin NA, Plant TM: Neurokinin B stimulates GnRH release in the male monkey (Macaca mulatta) and is colocalized with kisspeptin in the arcuate nucleus. Endocrinology 2010; 151: 4494-4503.
10. Hrabovszky E, Ciofi P, Vida B, Horvath MC, Keller E, Caraty A, Bloom SR, Ghatei MA, Dhillo WS, Liposits Z, Kallo I: The kisspeptin system of the human hypothalamus: sexual dimorphism and relationship with gonadotropin-releasing hormone and neurokinin B neurons. Eur J Neurosci 2010; 31: 1984-1998.
11. Foradori CD, Amstalden M, Goodman RL, Lehman MN: Colocalization of dynorphin A and neurokinin B immunoreactivity in the arcuate nucleus and median eminence of the sheep. J Neuroendocrinol 2006; 18: 534-541. (Pubitemid 43821725)
12. Wakabayashi Y, Nakada T, Murata K, Ohkura S, Mogi K, Navarro VM, Clifton DK, Mori Y, Tsukamura H, Maeda KI, Steiner RA, Okamura H: Neurokinin B and dynorphin A in kisspeptin neurons of the arcuate nucleus participate in generation of periodic oscillations of neural activity driving pulsatile gonadotropin-releasing hormone secretion in the goat. J Neurosci 2010; 30: 3124-3132.
13. Lehman MN, Merkley CM, Coolen LM, Goodman RL: Anatomy of the kisspeptin neural network in mammals. Brain Res 2010; 1364: 90-102.
14. Plant TM, Krey LC, Moossy J, McCormach JT, Hess DL, Knobil E: The arcuate nucleus and the control of gonadotropin and prolactin secretion in the female rhesus monkey. Endocrinology 1978; 102: 52-62. (Pubitemid 8277609)
15. 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. (Pubitemid 40262023)
16. Plant TM, Ramaswamy S, DiPietro MJ: Repetitive activation of hypothalamic G protein-coupled receptor 54 with intravenous pulses of kisspeptin in the juvenile monkey (Macaca mulatta) elicits a sustained train of gonadotropin-releasing hormone discharges. Endocrinology 2006; 147: 1007-1013. (Pubitemid 43113020)
17. Roseweir AK, Kauffman AS, Smith JT, Guerriero KA, Morgan K, Pielecka-Fortuna J, Pineda R, Gottsch ML, Tena-Sempere M, Moenter SM, Terasawa E, Clarke IJ, Steiner RA, Millar RP: Discovery of potent kisspeptin antagonists delineate physiological mechanisms of gonadotropin regulation. J Neurosci 2009; 29: 3920-3929.
18. Dhillo WS, Chaudhri OB, Patterson M, Thompson EL, Murphy KG, Badman MK, McGowan BM, Amber V, Patel S, Ghatei MA, Bloom SR: Kisspeptin-54 stimulates the hypothalamic-pituitary gonadal axis in human males. J Clin Endocrinol Metab 2005; 90: 6609-6615. (Pubitemid 41759323)
19. Dhillo WS, Chaudhri OB, Thompson EL, Murphy KG, Patterson M, Ramachandran R, Nijher GK, Amber V, Kokkinos A, Donaldson M, Ghatei MA, Bloom SR: Kisspeptin-54 stimulates gonadotropin release most potently during the preovulatory phase of the menstrual cycle in women. J Clin Endocrinol Metab 2007; 92: 3958-3966. (Pubitemid 47607647)
20. Oakley AE, Clifton DK, Steiner RA: Kisspeptin signaling in the brain. Endocr Rev 2009; 30: 713-743.
21. Navarro VM, Tena-Sempere M: Kisspeptins and the neuroendocrine control of reproduction. Front Biosci (Schol Ed) 2011; 3: 267-275.
22. 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. (Pubitemid 40209241)
23. 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. (Pubitemid 40187012)
24. 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. (Pubitemid 43083709)
25. Pielecka-Fortuna J, Chu Z, Moenter SM: Kisspeptin acts directly and indirectly to increase gonadotropin-releasing hormone neuron activity and its effects are modulated by estradiol. Endocrinology 2008; 149: 1979-1986. (Pubitemid 351468349)
26. Liu X, Lee K, Herbison AE: Kisspeptin excites gonadotropin-releasing hormone neurons through a phospholipase C/calcium-dependent pathway regulating multiple ion channels. Endocrinology 2008; 149: 4605-4614.
27. Zhang C, Roepke TA, Kelly MJ, Ronnekleiv OK: Kisspeptin depolarizes gonadotropinreleasing hormone neurons through activation of TRPC-like cationic channels. J Neurosci 2008; 28: 4423-4434.
28. Kung TT, Crawley Y, Jones H, Luo B, Gilchrest H, Greenfeder S, Anthes JC, Lira S, Wiekowski M, Cook DN, Hey JA, Egan RW, Chapman RW: Tachykinin NK3-receptor deficiency does not inhibit pulmonary eosinophilia in allergic mice. Pharmacol Res 2004; 50: 611-615. (Pubitemid 39388972)
29. Sandoval-Guzmán T, Rance NE: Central injection of senktide, an NK3 receptor agonist, or neuropeptide Y inhibits LH secretion and induces different patterns of Fos expression in the rat hypothalamus. Brain Res 2004; 1026: 307-312. (Pubitemid 39361561)
30. Corander MP, Challis BG, Thompson EL, Jovanovic Z, Loraine Tung YC, Rimmington D, Huhtaniemi IT, Murphy KG, Topaloglu AK, Yeo GS, O'Rahilly S, Dhillo WS, Semple RK, Coll AP: A study of the effects of neurokinin B upon gonadotropin release in male rodents. J Neuroendocrinol 2010; 22: 181-187.
31. Navarro VM, Castellano JM, McConkey SM, Pineda R, Ruiz-Pino F, Pinilla L, Clifton DK, Tena-Sempere M, Steiner RA: Interactions between kisspeptin and neurokinin B in the control of GnRH secretion in the female rat. Am J Physiol Endocrinol Metab 2011; 300:E202-E210.
32. Billings HJ, Connors JM, Altman SN, Hileman SM, Holaskova I, Lehman ML, Mc-Manus CJ, Nestor CC, Jacobs BH, Goodman RL: Neurokinin B acts via the neurokinin-3 receptor in the retrochiasmatic area to stimulate luteinizing hormone secretion in sheep. Endocrinology 2010; 151: 3836-3846.
33. Krajewski SJ, Anderson MJ, Iles-Shih L, Chen KJ, Urbanski HF, Rance NE: Morphologic evidence that neurokinin B modulates gonadotropin-releasing hormone secretion via neurokinin 3 receptors in the rat median eminence. J Comp Neurol 2005; 489: 372-386. (Pubitemid 41026235)
34. Rance NE, Krajewski SJ, Smith MA, Cholanian M, Dacks PA: Neurokinin B and the hypothalamic regulation of reproduction. Brain Res 2010; 1364: 116-128.
35. Amstalden M, Coolen LM, Hemmerle AM, Billings HJ, Connors JM, Goodman RL, Lehman MN: Neurokinin 3 receptor immunoreactivity in the septal region, preoptic area and hypothalamus of the female sheep: colocalisation in neurokinin B cells of the arcuate nucleus but not in gonadotrophin-releasing hormone neurones. J Neuroendocrinol 2010; 22: 1-12.
36. Maeda KI, Ohkura S, Uenoyama Y, Wakabayashi Y, Oka Y, Tsukamura H, Okamura H: Neurobiological mechanisms underlying GnRH pulse generation by the hypothalamus. Brian Res 2010; 1364: 103-115.
37. Burke MC, Letts PA, Krajewski SJ, Rance NE: Coexpression of dynorphin and neurokinin B immunoreactivity in the rat hypothalamus: morphologic evidence of interrelated function within the arcuate nucleus. J Comp Neurol 2006; 498: 712-726. (Pubitemid 44350359)
38. Plant TM, Witchel SF: Puberty in non-human primates and humans; in Neill JD (ed): Knobil and Neill's Physiology of Reproduction. New York, Elsevier, 2006, vol 2, pp 2177-2230.
39. Almeida TA, Rojo J, Nieto PM, Pinto FM, Hernandez M, Martín JD, Candenas ML: Tachykinins and tachykinin receptors: structure and activity relationships. Curr Med Chem 2004; 11: 2045-2081. (Pubitemid 38967729)
40. Sarau HM, Griswold DE, Bush B, Potts W, Sandhu P, Lundberg D, Foley JJ, Schmidt DB, Webb EF, Martin LD, Legos JJ, Whitmore RG, Barone FC, Medhurst AD, Luttmann MA, Giardina GAM, Hay DWP: Nonpeptide tachykinin receptor antagonists. II. Pharmacological and pharmacokinetic profile of SB-222200, a central nervous system penetrant, potent and selective NK-3 receptor antagonist. J Pharmacol Exp Ther 2000; 295: 373-381.
41. Seminara SB, Dipietro MJ, Ramaswamy S, Crowley WF Jr, Plant TM: Continuous human metastin 45-54 infusion desensitizes G protein-coupled receptor 54-induced gonadotropin-releasing hormone release monitored indirectly in the juvenile male Rhesus monkey (Macaca mulatta) : a finding with therapeutic implications. Endocrinology 2006; 147: 2122-2126.
42. Suter KJ, Pohl CR, Plant TM: The pattern and tempo of the pubertal reaugmentation of open-loop pulsatile gonadotropin-releasing hormone release assessed indirectly in the male rhesus monkey (Macaca mulatta) . Endocrinology 1998; 139: 2774-2783. (Pubitemid 28512386)
43. Gay VL, Plant TM: N-methyl-D, L-aspartate elicits hypothalamic gonadotropin-releasing hormone release in prepubertal male rhesus monkeys (Macaca mulatta) . Endocrinology 1987; 120: 2289-2296. (Pubitemid 17084899)
44. Plant TM: A study of the role of the postnatal testes in determining the ontogeny of gonadotropin secretion in the male rhesus monkey (Macaca mulatta) . Endocrinology 1985; 116: 1341-1350. (Pubitemid 15078148)
45. 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. (Pubitemid 30098898)
46. Caligioni CS, Yang J, Seminara SB: The stimulatory effect of neurokinin B on GnRH/LH release in female mice is dependent on kisspeptin (abstract 633.3); in Annu Meet Soc Neurosci, San Diego, 2010.
47. Todman MG, Han S-K, Herbison AE: Profiling neurotransmitter receptor expression in mouse gonadotropin-releasing hormone neurons using green fluorescent proteinpromoter transgenics and microarrays. Neuroscience 2005; 132: 703-712.
48. Belchez PE, Plant TM, Nakai Y, Keogh EJ, Knobil E: Hypophysial responses to continuous and intermittent delivery of hypothalamic gonadotropin-releasing hormone. Science 1978; 202: 631-633. (Pubitemid 9055618)