Spontaneous kisspeptin neuron firing in the adult mouse reveals marked sex and brain region differences but no support for a direct role in negative feedback

Endocrinology

Volumn 153, Issue 11, 2012, Pages 5384-5393

  De Croft, Simon ^a   Piet, Richard ^a   Mayer, Christian ^b   Mai, Oliver ^b   Boehm, Ulrich ^b   Herbison, Allan E ^a  

^a UNIVERSITY OF OTAGO   (New Zealand)

^b SAARLAND UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

GONADORELIN; GREEN FLUORESCENT PROTEIN; KISSPEPTIN;

ANIMAL TISSUE; ARCUATE NUCLEUS; ARTICLE; BRAIN ELECTROPHYSIOLOGY; BRAIN REGION; BRAIN SLICE; BRAIN THIRD VENTRICLE; CELL ADHESION; CONTROLLED STUDY; DIESTRUS; ELECTROENCEPHALOGRAM; FEMALE; HYPOTHALAMUS PERIVENTRICULAR NUCLEUS; IMMUNOFLUORESCENCE; MALE; MOUSE; NEGATIVE FEEDBACK; NERVE CELL STIMULATION; NONHUMAN; OVARIECTOMY; PREOPTIC AREA; PRIORITY JOURNAL; PROESTRUS; SEX DIFFERENCE;

ACTION POTENTIALS; ANIMALS; BRAIN; FEEDBACK, PHYSIOLOGICAL; FEMALE; KISSPEPTINS; MALE; MICE; NEURONS; ORGAN SPECIFICITY; SEX CHARACTERISTICS;

EID: 84867834569     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2012-1616     Document Type: Article

References (42)

1. 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)
2. 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 WH2003 The GPR54 gene as a regulator of puberty. N Engl J Med 349:1614-1627 (Pubitemid 37303886)
3. Clarkson J, Herbison AE 2009 Oestrogen, kisspeptin, GPR54 and the pre-ovulatory luteinising hormone surge. J Neuroendocrinol 21: 305-311
4. 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 26:6687-6694 (Pubitemid 44315230)
5. 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
6. Lehman MN, Coolen LM, Goodman RL 2010 Minireview: kisspeptin/ neurokinin B/dynorphin (KNDy) cells of the arcuate nucleus: a central node in the control of gonadotropin-releasing hormone secretion. Endocrinology 151:3479-3489
7. Popa SM, Clifton DK, Steiner RA 2008 The role of kisspeptins and GPR54in the neuroendocrine regulation of reproduction. Annu Rev Physiol 70:213-238 (Pubitemid 351738178)
8. 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
9. Colledge WH 2009 Kisspeptins and GnRH neuronal signalling. Trends Endocrinol Metab 20:115-121
10. 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
11. Ducret E, Gaidamaka G, Herbison AE 2010 Electrical and morphological characteristics of anteroventral periventricular nucleus kisspeptin and other neurons in the female mouse. Endocrinology 151:2223-2232
12. Gottsch ML, Popa SM, Lawhorn JK, Qiu J, Tonsfeldt KJ, Bosch MA, Kelly MJ, Rønnekleiv OK, Sanz E, McKnight GS, Clifton DK, Palmiter RD, Steiner RA 2011 Molecular properties of Kiss1 neurons in the arcuate nucleus of the mouse. Endocrinology 152:4298-4309
13. Qiu J, Fang Y, Bosch MA, Rønnekleiv OK, Kelly MJ 2011 Guinea pig kisspeptin neurons are depolarized by leptin via activation of TRPC channels. Endocrinology 152:1503-1514
14. Mayer C, Acosta-Martinez M, Dubois SL, Wolfe A, Radovick S, Boehm U, Levine JE 2010 Timing and completion of puberty in female mice depend on estrogen receptor α-signaling in kisspeptin neurons. Proc Natl Acad Sci USA 107:22693-22698
15. Mayer C, Boehm U 2011 Female reproductive maturation in the absence of kisspeptin/GPR54 signaling. Nat Neurosci 14:704-710
16. Porteous R, Petersen SL, Yeo SH, Bhattarai JP, Ciofi P, de Tassigny XD, Colledge WH, Caraty A, Herbison AE 2011 Kisspeptin neurons co-express met-enkephalin and galanin in the rostral periventricular region of the female mouse hypothalamus. J Comp Neurol 519: 3456-3469
17. Franceschini I, Lomet D, Cateau M, Delsol G, Tillet Y, Caraty A 2006 Kisspeptin immunoreactive cells of the ovine preoptic area and arcuate nucleus co-express estrogen receptor α. Neurosci Lett 401: 225-230 (Pubitemid 43729526)
18. Clarkson J, d'Anglemont de Tassigny X, Colledge WH, Caraty A, Herbison AE 2009 Distribution of kisspeptin neurones in the adult female mouse brain. J Neuroendocrinol 21:673-682
19. Paxinos G, Franklin KBJ 2004 The mouse brain in stereotaxic coordinates. San Diego: Academic Press
20. Golde WT, Gollobin P, Rodriguez LL 2005 A rapid, simple, and humane method for submandibular bleeding of mice using a lancet. Lab Anim 34:39-43 (Pubitemid 44662092)
21. 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)
22. Yeo SH, Herbison AE 2011 Projections of arcuate nucleus and rostral periventricular kisspeptin neurons in the adult female mouse brain. Endocrinology 152:2387-2399
23. Wen S, Götze IN, Mai O, Schauer C, Leinders-Zufall T, Boehm U 2011 Genetic identification of GnRH receptor neurons: a new model for studying neural circuits underlying reproductive physiology in the mouse brain. Endocrinology 152:1515-1526
24. Adachi S, Yamada S, Takatsu Y, Matsui H, Kinoshita M, Takase K, Sugiura H, Ohtaki T, Matsumoto H, Uenoyama Y, Tsukamura H, Inoue K, Maeda K 2007 Involvement of anteroventral periventricular metastin/kisspeptin neurons in estrogen positive feedback action on luteinizing hormone release in female rats. J Reprod Dev 53: 367-378 (Pubitemid 46743563)
25. Hoffman GE, Le WW, Franceschini I, Caraty A, Advis JP 2011 Expression of fos and in vivo median eminence release of LHRH identifies an active role for preoptic area kisspeptin neurons in synchronized surges of LH and LHRH in the ewe. Endocrinology 152: 214-222
26. Clarkson J, d'Anglemont de Tassigny X, Moreno AS, Colledge WH, Herbison AE 2008 Kisspeptin-GPR54 signaling is essential for preovulatory gonadotropin-releasing hormone neuron activation and the luteinizing hormone surge. J Neurosci 28:8691-8697
27. Cravo RM, Margatho LO, Osborne-Lawrence S, Donato Jr J, Atkin S, Bookout AL, Rovinsky S, Frazão R, Lee CE, Gautron L, Zigman JM, Elias CF 2011 Characterization of Kiss1 neurons using transgenic mouse models. Neuroscience 173:37-56
28. 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)
29. 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)
30. Clarkson J, Herbison AE 2011 Dual phenotype kisspeptin-dopamine neurones of the rostral periventricular area of the third ventricle project to gonadotrophin-releasing hormone neurones. J Neuroendocrinol 23:293-301
31. Navarro VM, Gottsch ML, Wu M, Garcia-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
32. 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:E1212-E1221
33. Rance NE 2009 Menopause and thehumanhypothalamus: evidence for the role of kisspeptin/neurokinin B neurons in the regulation of estrogen negative feedback. Peptides 30:111-122
34. Ohkura S, Uenoyama Y, Yamada S, Homma T, Takase K, Inoue N, Maeda K, Tsukamura H 2009 Physiological role of metastin/kisspeptin in regulating gonadotropin-releasing hormone (GnRH) secretion in female rats. Peptides 30:49-56
35. Mittelman-Smith MA, Williams H, Krajewski-Hall SJ, Lai J, Ciofi P, McMullen NT, Rance NE 2012 Arcuate kisspeptin/neurokinin B/dynorphin (KNDy) neurons mediate the estrogen suppression of gonadotropin secretion and body weight. Endocrinology 153: 2800-2812
36. Tsukamura H, Homma T, Tomikawa J, Uenoyama Y, Maeda K 2010 Sexual differentiation of kisspeptin neurons responsible for sex difference in gonadotropin release in rats. Ann NY Acad Sci 1200:95-103
37. Roa J, Castellano JM, Navarro VM, Handelsman DJ, Pinilla L, Tena-Sempere M 2009 Kisspeptins and the control of gonadotropin secretion in male and female rodents. Peptides 30:57-66
38. Smith JT, Li Q, Yap KS, Shahab M, Roseweir AK, Millar RP, Clarke IJ 2011 Kisspeptin is essential for the full preovulatory LH surge and stimulates GnRH release from the isolated ovine median eminence. Endocrinology 152:1001-1012
39. Roa J, Vigo E, Castellano JM, Gaytan F, Navarro VM, Aguilar E, Dijcks FA, Ederveen AG, Pinilla L, van Noort PI, Tena-Sempere M 2008 Opposite roles of estrogen receptor (ER)-α and ERβ in the modulation of luteinizing hormone responses to kisspeptin in the female rat: implications for the generation of the preovulatory surge. Endocrinology 149:1627-1637 (Pubitemid 351468345)
40. Williams III WP, Jarjisian SG, Mikkelsen JD, Kriegsfeld LJ 2011 Circadian control of kisspeptin and a gated GnRH response mediate the preovulatory luteinizing hormone surge. Endocrinology 152: 595-606
41. Smarr BL, Morris E, de la Iglesia HO 2012 The dorsomedial suprachiasmatic nucleus times circadian expression of Kiss1 and the luteinizing hormone surge. Endocrinology 153:2839-2850
42. Vida B, Deli L, Hrabovszky E, Kalamatianos T, Caraty A, Coen CW, Liposits Z, Kalló I 2010 Evidence for suprachiasmatic vasopressin neurones innervating kisspeptin neurones in the rostral periventricular area of the mouse brain: regulation by oestrogen. J Neuroendocrinol 22:1032-1039