Direct regulation of GnRH neuron excitability by arcuate nucleus POMC and NPY neuron neuropeptides in female mice

Endocrinology

Volumn 153, Issue 11, 2012, Pages 5587-5599

  Roa, Juan ^a,b,c   Herbison, Allan E ^a  

^a UNIVERSITY OF OTAGO   (New Zealand)

^b INSTITUTO DE SALUD CARLOS III   (Spain)

^c Hospital Universitario Reina Sofia   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERMEDIN; AMPHETAMINE; BETA ENDORPHIN; COCAINE; GONADORELIN; MELANOCORTIN 3 RECEPTOR; MELANOCORTIN 4 RECEPTOR; NEUROPEPTIDE Y; PROOPIOMELANOCORTIN;

ANIMAL CELL; ARCUATE NUCLEUS; ARTICLE; BRAIN ELECTROPHYSIOLOGY; CONTROLLED STUDY; EVOKED RESPONSE; FEMALE; FEMALE FERTILITY; INHIBITION KINETICS; MEMBRANE DEPOLARIZATION; MOLECULAR INTERACTION; MOUSE; NERVE CELL EXCITABILITY; NEUROMODULATION; NONHUMAN; POSTSYNAPTIC POTENTIAL; PRIORITY JOURNAL; PROTEIN SECRETION; RECEPTOR AFFINITY; REGULATORY MECHANISM;

AGOUTI-RELATED PROTEIN; ALPHA-MSH; ANIMALS; ARCUATE NUCLEUS; BETA-ENDORPHIN; ENKEPHALIN, ALA(2)-MEPHE(4)-GLY(5)-; FEMALE; GONADOTROPIN-RELEASING HORMONE; MICE; NERVE TISSUE PROTEINS; NEURONS; NEUROPEPTIDE Y; NEUROTRANSMITTER AGENTS; PEPTIDE FRAGMENTS; PRO-OPIOMELANOCORTIN; RECEPTOR, MELANOCORTIN, TYPE 3; RECEPTOR, MELANOCORTIN, TYPE 4;

EID: 84867764901     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2012-1470     Document Type: Article

References (87)

1. Crown A, Clifton DK, Steiner RA 2007 Neuropeptide signaling in the integration of metabolism and reproduction. Neuroendocrinology 86:175-182 (Pubitemid 350073605)
2. Roa J, García-Galiano D, Castellano JM, Gaytan F, Pinilla L, Tena-Sempere M 2010 Metabolic control of puberty onset: new players, new mechanisms. Mol Cell Endocrinol 324:87-94
3. Group ECW 2006 Nutrition and reproduction in women. Hum Reprod Update 12:193-207
4. Wade GN, Jones JE 2004 Neuroendocrinology of nutritional infertility. Am J Physiol Regul Integr Comp Physiol 287:R1277-R1296 (Pubitemid 39532210)
5. Pralong FP 2010 Insulin and NPY pathways and the control of GnRHfunction and puberty onset. Mol Cell Endocrinol 324:82-86
6. Quennell JH, Mulligan AC, Tups A, Liu X, Phipps SJ, Kemp CJ, Herbison AE, Grattan DR, Anderson GM 2009 Leptin indirectly regulates gonadotropin-releasing hormone neuronal function. Endocrinology 150:2805-2812
7. Louis GW, Greenwald-Yarnell M, Phillips R, Coolen LM, Lehman MN,Myers JrMG 2011 Molecular mapping of the neural pathways linking leptin to the neuroendocrine reproductive axis. Endocrinology 152:2302-2310
8. Divall SA, Williams TR, Carver SE, Koch L, Brüning JC, Kahn CR, Wondisford F, Radovick S, Wolfe A 2010 Divergent roles of growth factors in the GnRH regulation of puberty in mice. J Clin Invest 120:2900-2909
9. Donato Jr J, Cravo RM, Frazão R, Gautron L, Scott MM, Lachey J, Castro IA, Margatho LO, Lee S, Lee C, Richardson JA, Friedman J, Chua Jr S, Coppari R, Zigman JM, Elmquist JK, Elias CF 2011 Leptin's effect on puberty in mice is relayed by the ventral premammillary nucleus and does not require signaling in Kiss1 neurons. J Clin Invest 121:355-368
10. Donato Jr J, Silva RJ, Sita LV, Lee S, Lee C, Lacchini S, Bittencourt JC, Franci CR, Canteras NS, Elias CF 2009 The ventral premammillary nucleus links fasting-induced changes in leptin levels and coordinated luteinizing hormone secretion. J Neurosci 29:5240-5250
11. Leshan RL, Louis GW, Jo YH, Rhodes CJ, Münzberg H, Myers Jr MG 2009 Direct innervation of GnRH neurons by metabolic- and sexual odorant-sensing leptin receptor neurons in the hypothalamic ventral premammillary nucleus. J Neurosci 29:3138-3147
12. Schwartz MW 2001 Brain pathways controlling food intake and body weight. Exp Biol Med 226:978-981
13. van de Wall E, Leshan R, Xu AW, Balthasar N, Coppari R, Liu SM, Jo YH, MacKenzie RG, Allison DB, Dun NJ, Elmquist J, Lowell BB, Barsh GS, de Luca C, Myers Jr MG, Schwartz GJ, Chua Jr SC 2008 Collective and individual functions of leptin receptor modulated neurons controlling metabolism and ingestion. Endocrinology 149:1773-1785 (Pubitemid 351468315)
14. Balthasar N, Coppari R,McMinnJ, Liu SM, Lee CE, Tang V, Kenny CD, McGovern RA, Chua Jr SC, Elmquist JK, Lowell BB 2004 Leptin receptor signaling in POMC neurons is required for normal body weight homeostasis. Neuron 42:983-991.
15. Hill JW, Elias CF, Fukuda M, Williams KW, Berglund ED, Holland WL, Cho YR, Chuang JC, Xu Y, Choi M, Lauzon D, Lee CE, Coppari R, Richardson JA, Zigman JM, Chua S, Scherer PE, Lowell BB, Brüning JC, Elmquist JK 2010 Direct insulin and leptin action on pro-opiomelanocortin neurons is required for normal glucose homeostasis and fertility. Cell Metab 11:286-297
16. Wintermantel TM, Campbell RE, Porteous R, Bock D, Gröne HJ, Todman MG, Korach KS, Greiner E, Pérez CA, Schütz G, Herbison AE 2006 Definition of estrogen receptor pathway critical for estrogen positive feedback to gonadotropin-releasing hormone neurons and fertility. Neuron 52:271-280 (Pubitemid 44548337)
17. Turi GF, Liposits Z, Moenter SM, Fekete C, Hrabovszky E 2003 Origin of neuropeptide Y-containing afferents to gonadotropin-releasing hormone neurons in male mice. Endocrinology 144:4967-4974 (Pubitemid 37378411)
18. Leranth C, MacLusky NJ, Shanabrough M, Naftolin F 1988 Immunohistochemical evidence for synaptic connections between pro-opiomelanocortin-immunoreactive axons and LH-RH neurons in the preoptic area of the rat. Brain Res 449:167-176
19. Xu J, Kirigiti MA, Cowley MA, Grove KL, Smith MS 2009 Suppression of basal spontaneous gonadotropin-releasing hormone neuronal activity during lactation: role of inhibitory effects of neuropeptide Y. Endocrinology 150:333-340
20. Spergel DJ, Krüth U, Hanley DF, Sprengel R, Seeburg PH 1999 GABA- and glutamate-activated channels in green fluorescent protein-tagged gonadotropin-releasing hormone neurons in transgenic mice. J Neurosci 19:2037-2050 (Pubitemid 29133382)
21. 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)
22. Hill RP, Wheeler P, MacNeil S, Haycock JW 2005 α-Melanocyte stimulating hormone cytoprotective biology in human dermal fibroblast cells. Peptides 26:1150-1158 (Pubitemid 40798071)
23. Korotkova TM, Brown RE, Sergeeva OA, Ponomarenko AA, Haas HL 2006 Effects of arousal- and feeding-related neuropeptides on dopaminergic and GABAergic neurons in the ventral tegmental area of the rat. Eur J Neurosci 23:2677-2685 (Pubitemid 43801459)
24. Lebrethon MC, Vandersmissen E, Gérard A, Parent AS, Bourguignon JP 2000 Cocaine and amphetamine-regulated-transcript peptide mediation of leptin stimulatory effect on the rat gonadotropin-releasing hormone pulse generator in vitro. J Neuroendocrinol 12:383-385 (Pubitemid 30223983)
25. Wayne NL, Kuwahara K 2007 β-Endorphin alters electrical activity of gonadotropin releasing hormone neurons located in the terminal nerve of the teleost medaka (Oryzias latipes). GenCompEndocrinol 150:41-47 (Pubitemid 44854883)
26. Pennock RL, Hentges ST 2011 Differential expression and sensitivity of presynaptic and postsynaptic opioid receptors regulating hypothalamic proopiomelanocortin neurons. J Neurosci 31:281-288
27. Krasnow S, Steiner R 2006 Physiological mechanisms integrating metabolism and reproduction. In: Neill JD, ed. Knobil and Neill's physiology of reproduction. 3rd ed. St. Louis: Elservier; 2553-2625
28. Mountjoy K 2010 Distribution and function of melanocortin receptors within the brain. In: Catania A, ed. Melanocortins: multiple actions and therapeutic potential.NewYork: Landes Bioscience and Springer Science+Business Media; 29-48
29. Fu LY, van den Pol AN 2008 Agouti-related peptide and MC3/4 receptor agonists both inhibit excitatory hypothalamic ventromedial nucleus neurons. J Neurosci 28:5433-5449
30. Smith MA, Hisadome K, Al-Qassab H, Heffron H, Withers DJ, Ashford ML 2007 Melanocortins and agouti-related protein modulate the excitability of two arcuate nucleus neuron populations by alteration of resting potassium conductances. J Physiol 578:425-438 (Pubitemid 46092207)
31. Sosulina L, Schwesig G, Seifert G, Pape HC 2008 Neuropeptide Y activates a G-protein-coupled inwardly rectifying potassium current and dampens excitability in the lateral amygdala. Mol Cell Neurosci 39:491-498
32. Cabrele C, Langer M, Bader R, Wieland HA, Doods HN, Zerbe O, Beck-Sickinger AG 2000 The first selective agonist for the neuropeptide YY5 receptor increases food intake in rats. J Biol Chem 275:36043-36048
33. Kalra SP, Fuentes M, Fournier A, Parker SL, Crowley WR 1992 Involvement of the Y-1 receptor subtype in the regulation of luteinizing hormone secretion by neuropeptide Y in rats. Endocrinology 130:3323-3330
34. Leupen SM, Besecke LM, Levine JE 1997 Neuropeptide Y Y1-receptor stimulation is required for physiological amplification of pre-ovulatory luteinizing hormone surges. Endocrinology 138:2735-2739 (Pubitemid 27258500)
35. Besecke LM, Wolfe AM, Pierce ME, Takahashi JS, Levine JE 1994 Neuropeptide Y stimulates luteinizing hormone-releasing hormone release from superfused hypothalamic GT1-7 cells. Endocrinology 135:1621-1627 (Pubitemid 24307542)
36. Raposinho PD, Broqua P, Pierroz DD, Hayward A, Dumont Y, Quirion R, Junien JL, Aubert ML 1999 Evidence that the inhibition of luteinizing hormone secretion exerted by central administration of neuropeptideY(NPY) in the rat is predominantly mediated by the NPY-Y5 receptor subtype. Endocrinology 140:4046-4055 (Pubitemid 30647100)
37. Browning KN, Travagli RA 2003 Neuropeptide Y and peptide YY inhibit excitatory synaptic transmission in the rat dorsal motor nucleus of the vagus. J Physiol 549:775-785 (Pubitemid 36889768)
38. Michel MC, Beck-Sickinger A, Cox H, Doods HN, Herzog H, Larhammar D, Quirion R, Schwartz T, Westfall T 1998 XVI. international union of pharmacology recommendations for the nomenclature of neuropeptide Y, peptide YY, and pancreatic polypeptide receptors. Pharmacol Rev 50:143-150 (Pubitemid 28158845)
39. Rhim H, Kinney GA, Emmerson PJ, Miller RJ 1997 Regulation of neurotransmission in the arcuate nucleus of the rat by different neuropeptide Y receptors. J Neurosci 17:2980-2989 (Pubitemid 27175812)
40. Hahn TM, Breininger JF, Baskin DG, Schwartz MW 1998 Coexpression of Agrp and NPY in fasting-activated hypothalamic neurons. Nat Neurosci 1:271-272 (Pubitemid 128652670)
41. Ollmann MM, Wilson BD, Yang YK, Kerns JA, Chen Y, Gantz I, Barsh GS 1997 Antagonism of central melanocortin receptors in vitro and in vivo by agouti-related protein. Science 278:135-138 (Pubitemid 27446294)
42. Cone RD 2005 Anatomy and regulation of the central melanocortin system. Nat Neurosci 8:571-578 (Pubitemid 40594196)
43. Herbison AE 2006 Physiology of the gonadotropin-releasing hormone neuronal network. In: Neill J, ed. The physiology of reproduction. San Diego: Elsevier; 1415-1482
44. Coll AP, Farooqi IS, Challis BG, Yeo GS, O'Rahilly S 2004 Proopiomelanocortin and energy balance: insights from human and murine genetics. J Clin Endocrinol Metab 89:2557-2562 (Pubitemid 38766331)
45. Hentges ST, Otero-Corchon V, Pennock RL, King CM, Low MJ 2009 Proopiomelanocortin expression in both GABA and glutamate neurons. J Neurosci 29:13684-13690
46. Simonian SX, Spratt DP, Herbison AE 1999 Identification and characterization of estrogen receptor α-containing neurons projecting to the vicinity of the gonadotropin-releasing hormone perikarya in the rostral preoptic area of the rat. J Comp Neurol 411:346-358 (Pubitemid 29343404)
47. Chen WP, Witkin JW, Silverman AJ 1989 β-Endorphin and gonadotropin-releasing hormone synaptic input to gonadotropin-releasing hormone neurosecretory cells in the male rat. J Comp Neurol 286:85-95 (Pubitemid 19201153)
48. Lagrange AH, Rønnekleiv OK, Kelly MJ 1995 Estradiol-17β and μ-opioid peptides rapidly hyperpolarize GnRH neurons: a cellular mechanism of negative feedback? Endocrinology 136:2341-2344
49. Sannella MI, Petersen SL 1997 Dual label in situ hybridization studies provide evidence that luteinizing hormone-releasing hormone neurons do not synthesize messenger ribonucleic acid for μ, κ, or δ opiate receptors. Endocrinology 138:1667-1672 (Pubitemid 27137120)
50. Mitchell V, Prevot V, Jennes L, Aubert JP, Croix D, Beauvillain JC 1997 Presence of μ and κ opioid receptor mRNAs in galanin but not in GnRH neurons in the female rat. Neuroreport 8:3167-3172 (Pubitemid 27421752)
51. Israel DD, Sheffer-Babila S, de Luca C, Jo YH, Liu SM, Xia Q, Spergel DJ, Dun SL, Dun NJ, Chua Jr SC 2012 Effects of leptin and melanocortin signaling interactions on pubertal development and reproduction. Endocrinology 153:2408-2419
52. Wachira SJ, Hughes-Darden CA, Taylor CV, Ochillo R, Robinson TJ 2003 Evidence for the interaction of protein kinase C and melanocortin 3-receptor signaling pathways. Neuropeptides 37:201-210 (Pubitemid 37041012)
53. Konda Y, Gantz I, DelValle J, Shimoto Y, Miwa H, Yamada T 1994 Interaction of dual intracellular signaling pathways activated by the melanocortin-3 receptor. J Biol Chem 269:13162-13166 (Pubitemid 24206079)
54. Daniels D, Patten CS, Roth JD, Yee DK, Fluharty SJ 2003 Melanocortin receptor signaling through mitogen-activated protein kinase in vitro and in rat hypothalamus. Brain Res 986:1-11 (Pubitemid 37272095)
55. Kim CS, Lee SH, Kim RY, Kim BJ, Li SZ, Lee IH, Lee EJ, Lim SK, Bae YS, Lee W, Baik JH 2002 Identification of domains directing specificity of coupling to G-proteins for the melanocortin MC3 and MC4 receptors. J Biol Chem 277:31310-31317 (Pubitemid 34968929)
56. Lacerda AE, Rampe D, Brown AM 1988 Effects of protein kinase C activators on cardiac Ca2+ channels. Nature 335:249-251
57. Butler AA, Cone RD 2002 The melanocortin receptors: lessons from knockout models. Neuropeptides 36:77-84
58. Begriche K, Levasseur PR, Zhang J, Rossi J, Skorupa D, Solt LA, Young B, Burris TP, Marks DL, Mynatt RL, Butler AA 2011 Genetic dissection of the functions of the melanocortin-3 receptor, a seven-transmembrane G-protein-coupled receptor, suggests roles for central and peripheral receptors in energy homeostasis. J Biol Chem 286:40771-40781
59. Sandrock M, Schulz A, Merkwitz C, Schöneberg T, Spanel-Borowski K, Ricken A 2009 A Reduction in corpora lutea number in obese melanocortin-4- receptor-deficient mice. Reprod Biol Endocrinol 7:24
60. Broberger C, Johansen J, Johansson C, Schalling M, Hökfelt T 1998 The neuropeptide Y/agouti gene-related protein (AGRP) brain circuitry in normal, anorectic, and monosodium glutamate-treated mice. Proc Natl Acad Sci USA 95:15043-15048 (Pubitemid 29003753)
61. Marsh DJ, Miura GI, Yagaloff KA, Schwartz MW, Barsh GS, Palmiter RD 1999 Effects of neuropeptide Y deficiency on hypothalamic agouti-related protein expression and responsiveness to melanocortin analogues. Brain Res 848:66-77
62. Pritchard LE, White A 2005 Agouti-related protein: more than a melanocortin-4 receptor antagonist? Peptides 26:1759-1770 (Pubitemid 41354534)
63. Granholm NH, Jeppesen KW, Japs RA 1986 Progressive infertility in female lethal yellow mice (Ay/a; strain C57BL/6J). J Reprod Fertil 76:279-287 (Pubitemid 16149586)
64. Li C, Chen P, Smith MS 1999 Morphological evidence for direct interaction between arcuate nucleus neuropeptide Y (NPY) neurons and gonadotropin-releasing hormone neurons and the possible involvement of NPY Y1 receptors. Endocrinology 140:5382-5390
65. Yulyaningsih E, Zhang L, Herzog H, Sainsbury A 2011 NPY receptors as potential targets for anti-obesity drug development. Br J Pharmacol 163:1170-1202
66. Sullivan SD, Moenter SM 2004 γ-Aminobutyric acid neurons integrate and rapidly transmit permissive and inhibitory metabolic cues to gonadotropin-releasing hormone neurons. Endocrinology 145:1194-1202 (Pubitemid 38281000)
67. Klenke U, Constantin S, Wray S 2010 Neuropeptide Y directly inhibits neuronal activity in a subpopulation of gonadotropin-releasing hormone-1 neurons viaY1receptors. Endocrinology 151:2736-2746
68. Horvath TL, Pu S, Dube MG, Diano S, Kalra SP 2001 A GABA-neuropeptide Y (NPY) interplay in LH release. Peptides 22:473-481 (Pubitemid 32250250)
69. Raposinho PD, Broqua P, Hayward A, Akinsanya K, Galyean R, Schteingart C, Junien J, Aubert ML 2000 Stimulation of the gonadotropic axis by the neuropeptide Y receptor Y1 antagonist/Y4 agonist 1229U91 in the male rat. Neuroendocrinology 71:2-7 (Pubitemid 30045329)
70. Sainsbury A, Schwarzer C, Couzens M, Jenkins A, Oakes SR, Ormandy CJ, Herzog H 2002 Y4 receptor knockout rescues fertility in ob/ob mice. Genes Dev 16:1077-1088 (Pubitemid 34507197)
71. Wang O, Sakihara S, Gudmundsson K, Majzoub J, Leptin is not required for fertility. The Endocrine Society's 94th Annual Meeting and Expo, Houston, 2012
72. Lin S, Lin EJ, Boey D, Lee NJ, Slack K, During MJ, Sainsbury A, Herzog H 2007 Fasting inhibits the growth and reproductive axes via distinct Y2 and Y4 receptor-mediated pathways. Endocrinology 148:2056-2065 (Pubitemid 46997059)
73. Sainsbury A, Shi YC, Zhang L, Aljanova A, Lin Z, Nguyen AD, Herzog H, Lin S 2010 Y4 receptors and pancreatic polypeptide regulate food intake via hypothalamic orexin and brain-derived neurotropic factor dependent pathways. Neuropeptides 44:261-268
74. Yan H, Yang J, Marasco J, Yamaguchi K, Brenner S, Collins F, Karbon W 1996 Cloning and functional expression of cDNAs encoding human and rat pancreatic polypeptide receptors. Proc Natl Acad Sci USA 93:4661-4665 (Pubitemid 26163497)
75. Herde MK, Geist K, Campbell RE, Herbison AE 2011 Gonadotropin-releasing hormone neurons extend complex highly branched dendritic trees outside the blood-brain barrier. Endocrinology 152:3832-3841
76. Roland AV, Moenter SM 2011 Prenatal androgenization of female mice programs an increase in firing activity of gonadotropin-releasing hormone (GnRH) neurons that is reversed by metformin treatment in adulthood. Endocrinology 152:618-628
77. Wu M, Dumalska I, Morozova E, van den Pol A, Alreja M 2009 Melanin-concentrating hormone directly inhibits GnRH neurons and blocks kisspeptin activation, linking energy balance to reproduction. Proc Natl Acad Sci USA 106:17217-17222
78. Blouet C, Jo YH, Li X, Schwartz GJ 2009 Mediobasal hypothalamic leucine sensing regulates food intake through activation of a hypothalamus-brainstem circuit. J Neurosci 29:8302-8311
79. Cowley MA, Smart JL, Rubinstein M, Cerdán MG, Diano S, Horvath TL, Cone RD, Low MJ 2001 Leptin activates anorexigenic POMC neurons through a neural network in the arcuate nucleus. Nature 411:480-484 (Pubitemid 32494394)
80. Schwartz MW, Morton GJ 2002 Obesity: keeping hunger at bay. Nature 418:595-597
81. Minor RK, Chang JW, de Cabo R 2009 Hungry for life: how the arcuate nucleus and neuropeptide Y may play a critical role in mediating the benefits of calorie restriction. Mol Cell Endocrinol 299:79-88
82. Lin S, Boey D, Herzog H 2004 NPY and Y receptors: lessons from transgenic and knockout models. Neuropeptides 38:189-200 (Pubitemid 39161911)
83. Gerald C, Walker MW, Criscione L, Gustafson EL, Batzl-Hartmann C, Smith KE, Vaysse P, Durkin MM, Laz TM, Linemeyer DL, Schaffhauser AO, Whitebread S, Hofbauer KG, Taber RI, Branchek TA, Weinshank RL 1996 A receptor subtype involved in neuropeptide-Y-induced food intake. Nature 382:168-171 (Pubitemid 26242883)
84. Wyss P, Stricker-Krongrad A, Brunner L, Miller J, Crossthwaite A, Whitebread S, Criscione L 1998 The pharmacology of neuropeptide Y (NPY) receptor-mediated feeding in rats characterizes better Y5 than Y1, but not Y2 or Y4 subtypes. Regul Pept 75-76:363-371 (Pubitemid 28477548)
85. Sun L, Miller RJ 1999 Multiple neuropeptide Y receptors regulate K+ and Ca2+ channels in acutely isolated neurons from the rat arcuate nucleus. J Neurophysiol 81:1391-1403 (Pubitemid 29272455)
86. Dumont Y, Gaudreau P, Mazzuferi M, Langlois D, Chabot JG, Fournier A, Simonato M, Quirion R 2005 BODIPY-conjugated neuropeptide Y ligands: new fluorescent tools to tag Y1, Y2, Y4 and Y5 receptor subtypes. Br J Pharmacol 146:1069-1081 (Pubitemid 41785319)
87. Wang YF, Hatton GI 2007 Dominant role of βγ subunits of G-proteins in oxytocin-evoked burst firing. J Neurosci 27:1902-1912