Increased neurokinin B (Tac2) expression in the mouse arcuate nucleus is an early marker of pubertal onset with differential sensitivity to sex steroid-negative feedback than Kiss1

Endocrinology

Volumn 153, Issue 10, 2012, Pages 4883-4893

  Gill, John C ^a   Navarro, Víctor M ^b   Kwong, Cecilia ^a   Noel, Sekoni D ^a   Martin, Cecilia ^a   Xu, Shuyun ^a   Clifton, Donald K ^c   Carroll, Rona S ^a   Steiner, Robert A ^b,c   Kaiser, Ursula B ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

^c UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ESTRADIOL; FOLLITROPIN; GONADORELIN; KISSPEPTIN; LUTEINIZING HORMONE; MESSENGER RNA; N (ALPHA ETHYLBENZYL) 3 METHYL 2 PHENYL 4 QUINOLINECARBOXAMIDE; NEUROKININ 3 RECEPTOR; NEUROKININ B; SEX HORMONE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARCUATE NUCLEUS; ARTICLE; BRAIN LEVEL; FEMALE; GENE EXPRESSION; HORMONE SENSITIVITY; HYPOGONADISM; IN VIVO STUDY; MOUSE; NEGATIVE FEEDBACK; NONHUMAN; PERINATAL PERIOD; POSTNATAL DEVELOPMENT; PREPUBERTY; PRIORITY JOURNAL; PUBERTY; SIGNAL TRANSDUCTION; WILD TYPE;

ANIMALS; ARCUATE NUCLEUS; ESTRADIOL; FEEDBACK, PHYSIOLOGICAL; FEMALE; GONADOTROPIN-RELEASING HORMONE; KISSPEPTINS; LUTEINIZING HORMONE; MICE; MICE, KNOCKOUT; NEUROKININ B; NEURONS; PROTEIN PRECURSORS; SEXUAL MATURATION; SIGNAL TRANSDUCTION; TACHYKININS;

EID: 84866774663     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2012-1529     Document Type: Article

References (52)

1. Rance NE, Young 3rd WS 1991 Hypertrophy and increased gene expression of neurons containing neurokinin-B and substance-P messenger ribonucleic acids in the hypothalami of postmenopausal women. Endocrinology 128:2239-2247
2. Akesson TR, Sternini C, Micevych PE 1991 Continuous estrogen decreases neurokinin B expression in the rat arcuate nucleus. Mol Cell Neurosci 2:299-304 (Pubitemid 121006162)
3. Seminara SB, Kaiser UB 2005 New gatekeepers of reproduction: GPR54 and its cognate ligand, KiSS-1. Endocrinology 146:1686-1688 (Pubitemid 40396874)
4. 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)
5. Rometo AM, Krajewski SJ, Voytko ML, Rance NE 2007 Hypertrophy and increased kisspeptin gene expression in the hypothalamic infundibular nucleus of postmenopausal women and ovariectomized monkeys. J Clin Endocrinol Metab 92:2744-2750 (Pubitemid 47037385)
6. Hrabovszky E, Ciofi P, Vida B, Horvath MC, Keller E, Caraty A, Bloom SR, Ghatei MA, Dhillo WS, Liposits Z, Kallo I 2010 The kisspeptin system of the human hypothalamus: sexual dimorphism and relationship with gonadotropin- releasing hormone and neurokinin B neurons. Eur J Neurosci 31:1984-1998
7. 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
8. Xu J, Kirigiti MA, Grove KL, Smith MS 2009 Regulation of food intake and gonadotropin-releasing hormone/luteinizing hormone during lactation: role of insulin and leptin. Endocrinology 150:4231-4240
9. 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
10. 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
11. 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
12. Smith JT, Dungan HM, Stoll EA, Gottsch ML, Braun RE, Eacker SM, Clifton DK, Steiner RA 2005 Differential regulation of KiSS-1 mRNA expression by sex steroids in the brain of the male mouse. Endocrinology 146:2976-2984 (Pubitemid 41002804)
13. Rance NE, Krajewski SJ, Smith MA, Cholanian M, Dacks PA 2010 Neurokinin B and the hypothalamic regulation of reproduction. Brain Res 1364:116-128
14. Smith JT, Cunningham MJ, Rissman EF, Clifton DK, Steiner RA 2005 Regulation of Kiss1 gene expression in the brain of the female mouse. Endocrinology 146:3686-3692 (Pubitemid 41175732)
15. Herbison AE 2008 Estrogen positive feedback to gonadotropin-releasing hormone (GnRH) neurons in the rodent: the case for the rostral periventricular area of the third ventricle (RP3V). Brain Res Rev 57:277-287 (Pubitemid 351381764)
16. Clarkson J, Herbison AE 2006 Postnatal development of kisspeptin neurons in mouse hypothalamus; sexual dimorphism and projections to gonadotropin- releasing hormone neurons. Endocrinology 147:5817-5825 (Pubitemid 44833498)
17. Kauffman AS, Gottsch ML, Roa J, Byquist AC, Crown A, Clifton DK, Hoffman GE, Steiner RA, Tena-Sempere M 2007 Sexual differentiation of Kiss1 gene expression in the brain of the rat. Endocrinology 148:1774-1783 (Pubitemid 46457121)
18. Gill JC, Wang O, Kakar S, Martinelli E, Carroll RS, Kaiser UB 2010 Reproductive hormone-dependent and -independent contributions to developmental changes in kisspeptin in GnRH-deficient hypogonadal mice. PLoS One 5:e11911
19. 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
20. 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 2010 TAC3 and TACR3 defects cause hypothalamic congenital hypogonadotropic hypogonadism in humans. J Clin Endocrinol Metab 95:2287-2295
21. Gianetti E, Tusset C, Noel SD, Au MG, Dwyer AA, Hughes VA, Abreu AP, Carroll J, Trarbach E, Silveira LF, Costa EM, de Mendonça BB, de Castro M, Lofrano A, Hall JE, Bolu E, Ozata M, Quinton R, Amory JK, Stewart SE, Arlt W, Cole TR, Crowley WF, Kaiser UB, Latronico AC, Seminara SB 2010 TAC3/TACR3 mutations reveal preferential activation of gonadotropin-releasing hormone release by neurokinin B in neonatal life followed by reversal in adulthood. J Clin Endocrinol Metab 95:2857-2867
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. 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
24. 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
25. 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)
26. 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
27. Charlton H 2004 Neural transplantation in hypogonadal (hpg) mice - physiology and neurobiology. Reproduction 127:3-12 (Pubitemid 38220122)
28. Han SK, Gottsch ML, Lee KJ, Popa SM, Smith JT, Jakawich SK, Clifton DK, Steiner RA, Herbison AE 2005 Activation of gonadotropin-releasing hormone neurons by kisspeptin as a neuroendocrine switch for the onset of puberty. J Neurosci 25:11349-11356 (Pubitemid 43083709)
29. Gottsch ML, Cunningham MJ, Smith JT, Popa SM, Acohido BV, Crowley WF, Seminara S, Clifton DK, Steiner RA 2004 A role for kisspeptins in the regulation of gonadotropin secretion in the mouse. Endocrinology 145:4073-4077 (Pubitemid 39120554)
30. 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 GA, Hay DW 2000 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 295:373-381
31. Nwaneshiudu CA, Unterwald EM 2009 Blockade of neurokinin-3 receptors modulates dopamine-mediated behavioral hyperactivity. Neuropharmacology 57:295-301
32. Nordquist RE, Ballard TM, Algeyer B, Pauly-Evers M, Ozmen L, Spooren W 2010 Pharmacological characterization of senktide-induced tail whips. Neuropharmacology 58:259-267
33. Michael SD, Kaplan SB, Macmillan BT 1980 Peripheral plasma concentrations of LH, FSH, prolactin and GH from birth to puberty in male and female mice. J Reprod Fertil 59:217-222 (Pubitemid 10088034)
34. Porter KL, Chanda S, Wang HQ, Gaido KW, Smart RC, Robinette CL 2002 17β-estradiol is a hormonal regulator of mirex tumor promotion sensitivity in mice. Toxicol Sci 69:42-48
35. 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)
36. de Roux N, Genin E, Carel JC, Matsuda F, Chaussain JL, Milgrom E 2003 Hypogonadotropic hypogonadism due to loss of function of the KiSS1-derived peptide receptor GPR54. Proc Natl Acad Sci USA 100:10972-10976 (Pubitemid 37140137)
37. Roa J, Navarro VM, Tena-Sempere M 2011 Kisspeptins in reproductive biology: consensus knowledge and recent developments. Biol Reprod 85:650-660
38. 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 2009 Hypogonadotropic hypogonadism due to a novel missense mutation in the first extracellular loop of the neurokinin B receptor. J Clin Endocrinol Metab 94:3633-3639
39. Francou B, Bouligand J, Voican A, Amazit L, Trabado S, Fagart J, Meduri G, Brailly-Tabard S, Chanson P, Lecomte P, Guiochon- Mantel A, Young J 2011 Normosmic congenital hypogonadotropic hypogonadism due toTAC3/TACR3 mutations: characteriaztion of neuroendocrine phenotypes and novel mutations. PLoS One 6:e25614
40. Topaloglu AK, Semple RK 2011 Neurokinin B signalling in the human reproductive axis. Mol Cell Endocrinol 346:57-64
41. Kauffman AS 2010 Coming of age in the kisspeptin era: sex differences, development, and puberty. Mol Cell Endocrinol 324:51-63
42. 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 2004 Tachykinin NK3-receptor deficiency does not inhibit pulmonary eosinophilia in allergic mice. Pharmacol Res 50:611-615 (Pubitemid 39388972)
43. Yang JJ, Caligioni CS, Chan YM, Seminara SB 2012 Uncovering novel reproductive defects in neurokinin B receptor null mice: closing the gap between mice and men. Endocrinology 153:1498-1508
44. Gill JC, Wadas B, Chen P, Portillo W, Reyna A, Jorgensen E, Mani S, Schwarting GA, Moenter SM, Tobet S, Kaiser UB 2008 The gonadotropin-releasing hormone (GnRH) neuronal population is normal in size and distribution in GnRH-deficient and GnRH receptor-mutant hypogonadal mice. Endocrinology 149:4596-4604
45. Dellovade TL, Merchenthaler I 2004 Estrogen regulation of neurokinin B gene expression in the mouse arcuate nucleus is mediated by estrogen receptor α. Endocrinology 145:736-742 (Pubitemid 38183816)
46. Kauffman AS, Navarro VM, Kim J, Clifton D, Steiner RA 2009 Sex differences in the regulation of Kiss1/NKB neurons in juvenile mice: implications for the timing of puberty. Am J Physiol Endocrinol Metab 297:1212-1221
47. Navarro VM, Ruiz-Pino F, Sánchez-Garrido MA, García-Galiano D, Hobbs SJ, Manfredi-Lozano M, León S, Sangiao-Alvarellos S, Castellano JM, Clifton DK, Pinilla L, Steiner RA, Tena-Sempere M 2012 Role of neurokinin B in the control of female puberty and its modulation by metabolic status. J Neurosci 32:2388-2397
48. Pintado CO, Pinto FM, Pennefather JN, Hidalgo A, Baamonde A, Sanchez T, Candenas ML 2003 A role for tachykinins in female mouse and rat reproductive function. Biol Reprod 69:940-946 (Pubitemid 37064623)
49. Almeida TA, Rojo J, Nieto PM, Pinto FM, Hernandez M, Martin JD, Candenas ML 2004 Tachykinins and tachykinin receptors: structure and activity relationships. Curr Med Chem 11:2045-2081 (Pubitemid 38967729)
50. 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
51. 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
52. Harris-Warrick RM, Johnson BR 2010 Checks and balances in neuromodulation. Front Behav Neurosci 4:47