Suppression of the GnRH pulse generator by neurokinin B involves a κ-opioid receptor-dependent mechanism

Endocrinology

Volumn 153, Issue 10, 2012, Pages 4894-4904

  Grachev, P ^a   Li, X F ^a   Kinsey Jones, J S ^a   Di Domenico, A L ^a   Millar, R P ^b,c,d   Lightman, S L ^e   O'Byrne, Kevin ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c UNIVERSITY OF PRETORIA   (South Africa)

^d UNIVERSITY OF CAPE TOWN   (South Africa)

^e UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

3,4 DICHLORO N METHYL N [2 (1 PYRROLIDINYL)CYCLOHEXYL]BENZENEACETAMIDE; DYNORPHIN A; G PROTEIN COUPLED RECEPTOR 54; GONADORELIN; KAPPA OPIATE RECEPTOR; KAPPA OPIATE RECEPTOR ANTAGONIST; KISSPEPTIN; LUTEINIZING HORMONE; NEUROKININ B; NOR BINALTORPHIMINE; SENKTIDE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARCUATE NUCLEUS; ARTICLE; CONTROLLED STUDY; DOSE RESPONSE; DOWN REGULATION; DRUG EFFECT; FEMALE; GENE EXPRESSION REGULATION; HORMONE DETERMINATION; IN VIVO STUDY; NEUROPHARMACOLOGY; NONHUMAN; OVARIECTOMY; PRIORITY JOURNAL; PULSE GENERATOR; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; VAGINA CYTOLOGY;

ANIMALS; ARCUATE NUCLEUS; ESTRADIOL; ESTROUS CYCLE; GONADOTROPIN-RELEASING HORMONE; KISSPEPTINS; LUTEINIZING HORMONE; NEUROKININ B; PEPTIDE FRAGMENTS; PREOPTIC AREA; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, G-PROTEIN-COUPLED; RECEPTORS, NEUROKININ-3; RECEPTORS, OPIOID, KAPPA; SUBSTANCE P;

EID: 84866747269     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2012-1574     Document Type: Article

References (42)

1. Topaloglu AK, Reimann F, Guclu M, Yalin AS, Kotan LD, Porter KM, Serin A, Mungan NO, Cook JR, Ozbek MN, Imamoglu S, Akalin NS, Yuksel B, O'Rahilly S, Semple RK 2009 TAC3 and TACR3 mutations in familial hypogonadotropic hypogonadism reveal a key role for neurokinin B in the central control of reproduction. Nat Genet 41:354-358
2. Knobil E 1990 The GnRH pulse generator. Am J Obstet Gynecol 163:1721-1727
3. Li XF, Kinsey-Jones JS, Cheng Y, Knox AM, Lin Y, Petrou NA, Roseweir A, Lightman SL, Milligan SR, Millar RP, O'Byrne KT 2009 Kisspeptin signalling in the hypothalamic arcuate nucleus regulates GnRH pulse generator frequency in the rat. PLoS One 4:e8334
4. Burke MC, Letts PA, Krajewski SJ, Rance NE 2006 Coexpression of dynorphin and neurokinin B immunoreactivity in the rat hypothalamus: morphologic evidence of interrelated function within the arcuate nucleus. J Comp Neurol 498:712-726 (Pubitemid 44350359)
5. Goodman RL, Lehman MN, Smith JT, Coolen LM, de Oliveira CV, Jafarzadehshirazi MR, Pereira A, Iqbal J, Caraty A, Ciofi P, Clarke IJ 2007 Kisspeptin neurons in the arcuate nucleus of the ewe express both dynorphin A and neurokinin B. Endocrinology 148:5752-5760 (Pubitemid 350146171)
6. Navarro VM, Gottsch ML, Chavkin C, Okamura H, Clifton DK, Steiner RA 2009 Regulation of gonadotropin-releasing hormone secretion by kisspeptin/dynorphin/ neurokinin B neurons in the arcuate nucleus of the mouse. J Neurosci 29:11859-11866
7. Wakabayashi Y, Nakada T, Murata K, Ohkura S, Mogi K, Navarro VM, Clifton DK, Mori Y, Tsukamura H, Maeda K, Steiner RA, Okamura H 2010 Neurokinin B and dynorphin A in kisspeptin neurons of the arcuate nucleus participate in generation of periodic oscillation of neural activity driving pulsatile gonadotropin-releasing hormone secretion in the goat. J Neurosci 30:3124-3132
8. Funes S, Hedrick JA, Vassileva G, Markowitz L, Abbondanzo S, Golovko A, Yang S, Monsma FJ, Gustafson EL 2003 The KiSS-1 receptor GPR54 is essential for the development of the murine reproductive system. Biochem Biophys Res Commun 312:1357-1363 (Pubitemid 37490966)
9. Seminara SB, Messager S, Chatzidaki EE, Thresher RR, Acierno Jr JS, 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 Jr WF, Aparicio SA, Colledge WH 2003 The GPR54 gene as a regulator of puberty. N Engl J Med 349:1614-1627 (Pubitemid 37303886)
10. Mayer C, Boehm U 2011 Female reproductive maturation in the absence of kisspeptin/GPR54 signaling. Nat Neurosci 14:704-710
11. Schulz R, Wilhelm A, Pirke KM, Gramsch C, Herz A 1981 β-Endorphin and dynorphin control serum luteinizing hormone level in immature female rats. Nature 294:757-759 (Pubitemid 12174447)
12. Kinoshita F, Nakai Y, Katakami H, Imura H 1982 Suppressive effect of dynorphin-(1-13) on luteinizing hormone release in conscious castrated rats. Life Sci 30:1915-1919 (Pubitemid 12098885)
13. Goodman RL, Coolen LM, Anderson GM, Hardy SL, Valent M, Connors JM, Fitzgerald ME, Lehman MN 2004 Evidence that dynorphin plays a major role in mediating progesterone negative feedback on gonadotropin-releasing hormone neurons in sheep. Endocrinology 145:2959-2967 (Pubitemid 38686245)
14. Bowe JE, Li XF, Kinsey-Jones JS, Paterson S, Brain SD, Lightman SL, O'Byrne KT 2005 Calcitonin gene-related peptide-induced suppression of luteinizing hormone pulses in the rat: the role of endogenous opioid peptides. J Physiol 566:921-928 (Pubitemid 41122671)
15. Krajewski SJ, Burke MC, Anderson MJ, McMullen NT, Rance NE 2010 Forebrain projections of arcuate neurokinin B neurons demonstrated by anterograde tract-tracing and monosodium glutamate lesions in the rat. Neuroscience 166:680-697
16. Ramaswamy S, Seminara SB, Ali B, Ciofi P, Amin NA, Plant TM 2010 Neurokinin B stimulates GnRH release in the male monkey (Macaca mulatta) and is colocalized with kisspeptin in the arcuate nucleus. Endocrinology 151:4494-4503
17. Ramaswamy S, Seminara SB, Plant TM 2011 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 94:237-245
18. García-Galiano D, van Ingen Schenau D, Leon S, Krajnc-Franken MA, Manfredi-Lozano M, Romero-Ruiz A, Navarro VM, Gaytan F, van Noort PI, Pinilla L, Blomenröhr M, Tena-Sempere M 2012 Kisspeptin signaling is indispensable for neurokinin B, but not glutamate, stimulation of gonadotropin secretion in mice. Endocrinology 153:316-328
19. Navarro VM, Gottsch ML, Wu M, García-Galiano D, Hobbs SJ, Bosch MA, Pinilla L, Clifton DK, Dearth A, Ronnekleiv OK, Braun RE, Palmiter RD, Tena-Sempere M, Alreja M, Steiner RA 2011 Regulation of NKB pathways and their roles in the control of Kiss1 neurons in the arcuate nucleus of the male mouse. Endocrinology 152:4265-4275
20. Navarro VM, Castellano JM, McConkey SM, Pineda R, Ruiz-Pino F, Pinilla L, Clifton DK, Tena-Sempere M, Steiner RA 2011 Interactions between kisspeptin and neurokinin B in the control of GnRH secretion in the female rat. Am J Physiol Endocrinol Metab 300:E202-E210
21. Kinsey-Jones JS, Grachev P, Li XF, Lin YS, Milligan SR, Lightman SL, O'Byrne KT 2012 The inhibitory effects of neurokinin B on GnRH pulse generator frequency in the female rat. Endocrinology 153:307-315
22. Billings HJ, Connors JM, Altman SN, Hileman SM, Holaskova I, Lehman MN, McManus CJ, Nestor CC, Jacobs BH, Goodman RL 2010 Neurokinin B acts via the neurokinin-3 receptor in the retrochiasmatic area to stimulate luteinizing hormone secretion in sheep. Endocrinology 151:3836-3846
23. Sandoval-Guzmán T, Rance NE 2004 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 1026:307-312 (Pubitemid 39361561)
24. Krajewski SJ, Anderson MJ, Iles-Shih L, Chen KJ, Urbanski HF, Rance NE 2005 Morphologic evidence that neurokinin B modulates gonadotropin-releasing hormone secretion via neurokinin 3 receptors in the rat median eminence. J Comp Neurol 489:372-386 (Pubitemid 41026235)
25. Smith JT, Popa SM, Clifton DK, Hoffman GE, Steiner RA 2006 Kiss1 neurons in the forebrain as central processors for generating the preovulatory luteinizing hormone surge. J Neurosci 26:668766-668794
26. Liu X, Porteous R, d'Anglemont de Tassigny X, Colledge WH, Millar R, Petersen SL, Herbison AE 2011 Frequency-dependent recruitment of fast amino acid and slow neuropeptide neurotransmitter release controls gonadotropin-releasing hormone neuron excitability. J Neurosci 31:2421-2430
27. Paxinos G, Watson C 1986 The rat brain in stereotaxic coordinates. 2nd ed. London: Academic Press
28. Cates PS, Forsling ML, O'byrne KT 1999 Stress-induced suppression of pulsatile luteinising hormone release in the female rat: role of vasopressin. J Neuroendocrinol 11:677-683
29. Li XF, Mitchell JC, Wood S, Coen CW, Lightman SL, O'Byrne KT 2003 The effect of oestradiol and progesterone on hypoglycaemic stress-induced suppression of pulsatile luteinizing hormone release and on corticotropin- releasing hormone mRNA expression in the rat. J Neuroendocrinol 15:468-476 (Pubitemid 36582462)
30. Kinsey-Jones JS, Li XF, Knox AM, Wilkinson ES, Zhu XL, Chaudhary AA, Milligan SR, Lightman SL, O'Byrne KT 2009 Down-regulation of hypothalamic kisspeptin and its receptor, Kiss1r, mRNA expression is associated with stress-induced suppression of luteinising hormone secretion in the female rat. J Neuroendocrinol 21:20-29
31. Palkovits M, Brownstein MJ 1988 Maps and guide to microdissection of the rat brain. New York: Elsevier Science
32. Monroe SE, Parlow AF, Midgley Jr AR 1968 Radioimmunoassay for rat luteinizing hormone. Endocrinology 83:1004-1012
33. Van Cauter E 1988 Estimating false-positive and false-negative errors in analyses of hormonal pulsatility. Am J Physiol 254:E786-EE794
34. Rodríguez EM, Blázquez JL, Guerra M 2010 The design of barriers in the hypothalamus allows the median eminence and the arcuate nucleus to enjoy private milieus: the former opens to the portal blood and the latter to the cerebrospinal fluid. Peptides 31:757-776
35. 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 2010 The effects of neurokinin B upon gonadotrophin release in male rodents. J Neuroendocrinol 22:181-187
36. Cagampang FR, Maeda KI, Tsukamura H, Ohkura S, Ota K 1991 Involvement of ovarian steroids and endogenous opioids in the fasting-induced suppression of pulsatile LH release in ovariectomized rats. J Endocrinol 129:321-328
37. Lee JS, Ettinger B, Stanczyk FZ, Vittinghoff E, Hanes V, Cauley JA, Chandler W, Settlage J, Beattie MS, Folkerd E, Dowsett M, Grady D, Cummings SR 2006 Comparison of methods to measure low serum estradiol levels in postmenopausal women. J Clin Endocrinol Metab 91:3791-3797 (Pubitemid 44536845)
38. Kalra SP, Kalra PS 1983 Neural regulation of luteinizing hormone secretion in the rat. Endocr Rev 4:311-351
39. Rance NE 2009 Menopause and the human hypothalamus: evidence for the role of kisspeptin/neurokinin B neurons in the regulation of estrogen negative feedback. Peptides 30:111-122
40. Noritake K Matsuoka T Ohsawa T, Shimomura K, Sanbuissho A, Uenoyama Y, Maeda K, Tsukamura H 2011 Involvement of neurokinin receptors in the control of pulsatile luteinizing hormone secretion in rats. J Reprod Dev 57:409-415
41. Amstalden M, Coolen LM, Hemmerle AM, Billings HJ, Connors JM, Goodman RL, Lehman MN 2010 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 22:1-12
42. Grachev P, Li XF, Lin YS, Hu MH, Elsamani L, Paterson SJ, Millar RP, Lightman SL, O'Byrne KT 2012 GPR54-dependent stimulation of luteinizing hormone secretion by neurokinin B in prepubertal rats. PLoS One 10.1371/journal.pone. 0044344