Optogenetic stimulation of arcuate nucleus kiss1 neurons reveals a steroid-dependent glutamatergic input to POMC and AgRP neurons in male mice

Molecular Endocrinology

Volumn 30, Issue 6, 2016, Pages 630-644

  Nestor, Casey C ^a   Qiu, Jian ^a   Padilla, Stephanie L ^d   Zhang, Chunguang ^a   Bosch, Martha A ^a   Fan, Wei ^b   Aicher, Sue A ^a   Palmiter, Richard D ^d   Rønnekleiv, Oline K ^a,c   Kelly, Martin J ^a,c  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^c OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^d UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AGOUTI RELATED PROTEIN; ANDROGEN RECEPTOR; G PROTEIN COUPLED RECEPTOR 54; GLUTAMATE DECARBOXYLASE 67; GLUTAMIC ACID; KISSPEPTIN; MESSENGER RNA; METABOTROPIC RECEPTOR AGONIST; PROOPIOMELANOCORTIN; STEROID; TESTOSTERONE; VESICULAR GLUTAMATE TRANSPORTER 2; YELLOW FLUORESCENT PROTEIN; 4 AMINOBUTYRIC ACID; CHANNELRHODOPSIN; GLUTAMIC ACID DERIVATIVE; METABOTROPIC RECEPTOR; METABOTROPIC RECEPTOR 2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARCUATE NUCLEUS; ARTICLE; BRAIN ELECTROPHYSIOLOGY; BRAIN SLICE; CASTRATED MALE; CASTRATION; CONTROLLED STUDY; ENERGY BALANCE; GENE EXPRESSION; GLUTAMATERGIC SYNAPSE; GONADECTOMY; HOMEOSTASIS; MALE; MOUSE; NERVE CELL STIMULATION; NONHUMAN; OPTOGENETICS; PHOTOSTIMULATION; PRIORITY JOURNAL; REPRODUCTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UPREGULATION; VOLTAGE CLAMP TECHNIQUE; ACTION POTENTIAL; AGONISTS; ANIMAL; AXON; C57BL MOUSE; DRUG EFFECTS; GENETICS; LIGHT; METABOLISM; NERVE CELL; RADIATION RESPONSE; ULTRASTRUCTURE;

ACTION POTENTIALS; AGOUTI-RELATED PROTEIN; ANIMALS; ARCUATE NUCLEUS OF HYPOTHALAMUS; AXONS; CASTRATION; CHANNELRHODOPSINS; GAMMA-AMINOBUTYRIC ACID; GLUTAMATES; KISSPEPTINS; LIGHT; MALE; MICE, INBRED C57BL; NEURONS; OPTOGENETICS; PRO-OPIOMELANOCORTIN; RECEPTORS, METABOTROPIC GLUTAMATE; RNA, MESSENGER; STEROIDS; UP-REGULATION; VESICULAR GLUTAMATE TRANSPORT PROTEIN 2;

EID: 84971658661     PISSN: 08888809     EISSN: 19449917     Source Type: Journal    
DOI: 10.1210/me.2016-1026     Document Type: Article

References (82)

1. Seminara SB, Messager S, Chatzidaki EE, et al. The GPR54 gene as a regulator of puberty. N Engl J Med. 2003;349:1614–1627.
2. de Roux N, Genin E, Carel JC, Matsuda F, Chaussain JL, Milgrom E. Hypogonadotropic hypogonadism due to loss of function of the KiSS1-derived peptide receptor GPR54. Proc Natl Acad Sci USA. 2003;100:10972–10976.
3. Mayer C, Boehm U. Female reproductive maturation in the absence of kisspeptin/GPR54 signaling. Nat Neurosci. 2011;14:704–710.
4. de Bond JA, Smith JT. Kisspeptin and energy balance in reproduction. Reproduction. 2014;147:R53–R63.
5. Roa J, Tena-Sempere M. Connecting metabolism and reproduction: roles of central energy sensors and key molecular mediators. Mol Cell Endocrinol. 2014;397:4–14.
6. Smith JT, Dungan HM, Stoll EA, et al. Differential regulation of KiSS-1 mRNA expression by sex steroids in the brain of the male mouse. Endocrinology. 2005;146:2976–2984.
7. Smith JT, Cunningham MJ, Rissman EF, Clifton DK, Steiner RA. Regulation of Kiss1 gene expression in the brain of the female mouse. Endocrinology. 2005;146:3686–3692.
8. Navarro VM, Gottsch ML, Wu M, et al. Regulation of NKB pathways and their roles in the control of Kiss1 neurons in the arcuate nucleus of the male mouse. Endocrinology. 2011;152:4265–4275.
9. Zhang C, Tonsfeldt KJ, Qiu J, et al. Molecular mechanisms that drive estradiol-dependent burst firing of Kiss1 neurons in the rostral periventricular preoptic area. Am J Physiol Endocrinol Metab. 2013;305:E1384–E1397.
10. Mittelman-Smith MA, Williams H, Krajewski-Hall SJ, et al. Arcuate kisspeptin/neurokinin B/dynorphin (KNDy) neurons mediate the estrogen suppression of gonadotropin secretion and body weight. Endocrinology. 2012;153:2800–2812.
11. Mittelman-Smith MA, Williams H, Krajewski-Hall SJ, McMullen NT, Rance NE. Role for kisspeptin/neurokinin B/dynorphin (KNDy) neurons in cutaneous vasodilatation and the estrogen modulation of body temperature. Proc Natl Acad Sci USA. 2012;109: 19846–19851.
12. Chai JK, Blaha V, Meguid MM, Laviano A, Yang ZJ, Varma M. Use of orchiectomy and testosterone replacement to explore meal number-to-meal size relationship in male rats. Am J Physiol. 1999; 276:R1366–R1373.
13. Wallen WJ, Belanger MP, Wittnich C. Sex hormones and the selective estrogen receptor modulator tamoxifen modulate weekly body weights and food intake in adolescent and adult rats. J Nutr. 2001; 131:2351–2357.
14. Gropp E, Shanabrough M, Borok E, et al. Agouti-related peptideexpressing neurons are mandatory for feeding. Nat Neurosci. 2005; 8:1289–1291.
15. Luquet S, Perez FA, Hnasko TS, Palmiter RD. NPY/AgRP neurons are essential for feeding in adult mice but can be ablated in neonates. Science. 2005;310:683–685.
16. Smith JT, Acohido BV, Clifton DK, Steiner RA. KiSS-1 neurones are direct targets for leptin in the ob/ob mouse. J Neuroendocrinol. 2006;18:298–303.
17. Cravo RM, Margatho LO, Osborne-Lawrence S, et al. Characterization of Kiss1 neurons using transgenic mouse models. Neuroscience. 2011;173:37–56.
18. Qiu J, Fang Y, Bosch MA, Rønnekleiv OK, Kelly MJ. Guinea pig kisspeptin neurons are depolarized by leptin via activation of TRPC channels. Endocrinology. 2011;152:1503–1514.
19. Donato J Jr, Cravo RM, Frazão R, et al. 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. 2011;121: 355–368.
20. Cravo RM, Frazao R, Perello M, et al. Leptin signaling in Kiss1 neurons arises after pubertal development. PLoS One. 2013;8: e58698.
21. Qiu J, Zhang C, Borgquist A, et al. Insulin excites anorexigenic proopiomelanocortin neurons via activation of canonical transient receptor potential channels. Cell Metab. 2014;19:682–693.
22. Lehman MN, Hileman SM, Goodman RL. Neuroanatomy of the kisspeptin signaling system in mammals: comparative and developmental aspects. Adv Exp Med Biol. 2013;784:27–62.
23. Backholer K, Smith JT, Rao A, et al. Kisspeptin cells in the ewe brain respond to leptin and communicate with neuropeptide Y and proopiomelanocortin cells. Endocrinology. 2010;151:2233–2243.
24. Fu LY, van den Pol AN. Kisspeptin directly excites anorexigenic proopiomelanocortin neurons but inhibits orexigenic neuropeptide Y cells by an indirect synaptic mechanism. J Neurosci. 2010;30: 10205–10219.
25. Gottsch ML, Popa SM, Lawhorn JK, et al. Molecular properties of Kiss1 neurons in the arcuate nucleus of the mouse. Endocrinology. 2011;152:4298–4309.
26. Madisen L, Mao T, Koch H, et al. A toolbox of Cre-dependent optogenetic transgenic mice for light-induced activation and silencing. Nat Neurosci. 2012;15:793–802.
27. Cowley MA, Smart JL, Rubinstein M, et al. Leptin activates anorexigenic POMC neurons through a neural network in the arcuate nucleus. Nature. 2001;411:480–484.
28. van den Pol AN, Yao Y, Fu LY, et al. Neuromedin B and gastrinreleasing peptide excite arcuate nucleus neuropeptide Y neurons in a novel transgenic mouse expressing strong Renilla green fluorescent protein in NPY neurons. J Neurosci. 2009;29:4622–4639.
29. Atasoy D, Betley JN, Su HH, Sternson SM. Deconstruction of a neural circuit for hunger. Nature. 2012;488:172–117.
30. Gore BB, Soden ME, Zweifel LS. Manipulating gene expression in projection-specific neuronal populations using combinatorial viral approaches. Curr Protoc Neurosci. 2013;65:1–20.
31. Saunders A, Johnson CA, Sabatini BL. Novel recombinant adenoassociated viruses for Cre activated and inactivated transgene expression in neurons. Front Neural Circuits. 2012;6:47.
32. Bosch MA, Tonsfeldt KJ, Rønnekleiv OK. mRNAexpression of ion channels in GnRH neurons: subtype-specific regulation by 17β- estradiol. Mol Cell Endocrinol. 2013;367:85–97.
33. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(– ∆ ∆ C(T)) method. Methods. 2001;25:402–408.
34. Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acid Res. 2001;29:2002–2007.
35. Silverman MB, Hermes SM, Zadina JE, Aicher SA. μ-Opioid receptor is present in dendritic targets of endomorphin-2 axon terminals in the nuclei of the solitary tract. Neuroscience. 2005;135:887–896.
36. Todd AJ, Hughes DI, Polgár E, et al. The expression of vesicular glutamate transporters VGLUT1 and VGLUT2 in neurochemically defined axonal populations in the rat spinal cord with emphasis on the dorsal horn. Eur J Neurosci. 2016;17:13–27.
37. Bulloch K, Miller MM, Gal-Toth J, et al. CD11c/EYFP transgene illuminates a discrete network of dendritic cells within the embryonic, neonatal, adult, and injured mouse brain. J Comp Neurol. 2008;508:687–710.
38. Qiu J, Bosch MA, Tobias SC, et al. Rapid signaling of estrogen in hypothalamic neurons involves a novel G-protein-coupled estrogen receptor that activates protein kinase C. J Neurosci. 2003;23: 9529–9540.
39. Qiu J, Nestor CC, Padilla SL, Palmiter RD, Rønnekleiv OK, Kelly MJ. High frequency-induced peptide release governs the synchronization of the arcuate kisspeptin neurons. Annual Meeting of the Society for Neuroscience, Chicago, IL. 2015 (Program 613.24/ Poster S19).
40. Cousin MA, Robinson PJ. Ca(2+) influx inhibits dynamin and arrests synaptic vesicle endocytosis at the active zone. J Neurosci. 2000;20:949–957.
41. Petreanu L, Mao T, Sternson SM, Svoboda K. The subcellular organization of neocortical excitatory connections. Nature. 2009; 457:1142–1145.
42. Smith AW, Bosch MA, Wagner EJ, Rønnekleiv OK, Kelly MJ. The membrane estrogen receptor ligand STX rapidly enhances GABAergic signaling in NPY/AgRP neurons: role in mediating the anorexigenic effects of 17β-estradiol. Am J Physiol Endocrinol Metab. 2013;305:E632–E640.
43. Qiu J, Bosch MA, Tobias SC, et al. A G protein-coupled estrogen receptor is involved in hypothalamic control of energy homeostasis. J Neurosci. 2006;26:5649–5655.
44. Herman MA, Ackermann F, Trimbuch T, Rosenmund C. Vesicular glutamate transporter expression level affects synaptic vesicle release probability at hippocampal synapses in culture. J Neurosci. 2014;34:11781–11791.
45. Zucker RS, Regehr WG. Short-term synaptic plasticity. Annu Rev Phys. 2002;64:355–405.
46. Niswender CM, Conn PJ. Metabotropic glutamate receptors: physiology, pharmacology, and disease. Annu Rev Pharmacol Toxicol. 2010;50:295–322.
47. Goodman RL, Lehman MN, Smith JT, et al. Kisspeptin neurons in the arcuate nucleus of the ewe express both dynorphin A and neurokinin B. Endocrinology. 2007;148:5752–5760.
48. 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.
49. Wakabayashi Y, Nakada T, Murata K, et al. Nuerokinin 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. 2010;30:3124–3132.
50. Nestor CC, Briscoe AM, Davis SM, Valent M, Goodman RL, Hileman SM. Evidence of a role for kisspeptin and neurokinin B in puberty of female sheep. Endocrinology. 2012;153:2756–2765.
51. Yeo SH, Herbison AE. Projections of arcuate nucleus and rostral periventricular kisspeptin neurons in the adult female mouse brain. Endocrinology. 2011;152:2387–2399.
52. Yip SH, Boehm U, Herbison AE, Campbell RE. Conditional viral tract tracing delineates the projections of the distinct kisspeptin neuron populations to gonadotropin-releasing hormone (GnRH) neurons in the mouse. Endocrinology. 2015;156:2582–2594.
53. van den Pol AN, Wuarin JP, Dudek FE. Glutamate, the dominant excitatory transmitter in neuroendocrine regulation. Science. 1990; 250:1276–1278.
54. Pinto S, Roseberry AG, Liu H, et al. Rapid rewiring of arcuate nucleus feeding circuits by leptin. Science. 2004;304:110–115.
55. Sternson SM, Shepherd GM, Friedman JM. Topographic mapping of VMH-› arcuate nucleus microcircuits and their reorganization by fasting. Nat Neurosci. 2005;8:1356–1363.
56. Tong Q, Ye CP, Jones JE, Elmquist JK, Lowell BB. Synaptic release of GABA by AgRP neurons is required for normal regulation of energy balance. Nat Neurosci. 2008;11:998–1000.
57. Belousov AB, Van den Pol AN. Local synaptic release of glutamate from neurons in the rat hypothalamic arcuate nucleus. J Physiol (Lond). 1997;499:747–761.
58. Hentges ST, Nishiyama M, Overstreet LS, Stenzel-Poore M, Williams JT, Low MJ. GABA release from proopiomelanocortin neurons. J Neurosci. 2004;24:1578–1583.
59. Hentges ST, Otero-Corchon V, Pennock RL, King CM, Low MJ. Proopiomelanocortin expression in both GABA and glutamate neurons. J Neurosci. 2009;29:13684–13690.
60. Dicken MS, Tooker RE, Hentges ST. Regulation of GABA and glutamate release from proopiomelanocortin neuron terminals in intact hypothalamic networks. J Neurosci. 2012;32:4042–4048.
61. + current. Proc Natl Acad Sci USA. 2007;104:11453–11458.
62. Westphalen RI, Desai KM, Hemmings HC Jr. Presynaptic inhibition of the release of multiple major central nervous system neurotransmitter types by the inhaled anaesthetic isoflurane. Br J Anaesth. 2013;110:592–599.
63. Krashes MJ, Shah BP, Madara JC, et al. An excitatory paraventricular nucleus to AgRP neuron circuit that drives hunger. Nature. 2014;507:238–242.
64. Maccaferri G, Roberts JD, Szucs P, Cottingham CA, Somogyi P. Cell surface domain specific postsynaptic currents evoked by identified GABAergic neurones in rat hippocampus in vitro. J Physiol. 2000;524(pt 1):91–116.
65. Padilla SL, Qiu J, Soden ME, et al. Agouti-related peptide neural circuits mediate adaptive behaviors in the starved state. Nat Neurosci. 2016;19:734–741.
66. Chee MJ, Arrigoni E, Maratos-Flier E. Melanin-concentrating hormone neurons release glutamate for feedforward inhibition of the lateral septum. J Neurosci. 2015;35:3644–3651.
67. Rønnekleiv OK, Fang Y, Zhang C, Nestor CC, Mao P, Kelly MJ. Research resources: gene profiling of G protein-coupled receptors in the arcuate nucleus of the female. Mol Endocrinol. 2014;28: 1362–1380.
68. Nohara K, Zhang Y, Waraich RS, et al. Early-life exposure to testosterone programs the hypothalamic melanocortin system. Endocrinology. 2011;152:1661–1669.
69. Rana K, Fam BC, Clarke MV, Pang TPS, Zajac JD, MacLean HE. Increased adiposity in DNA binding-dependent androgen receptor knockout male mice associated with decreased voluntary activity and not insulin resistance. Am J Physiol. 2011;301: E767–E778.
70. Rowland DL, Perrings TS, Thommes JA. Comparison of androgenic effects on food intake and body weight in adult rats. Physiol Behav. 1980;24:205–209.
71. Chai JK, Blaha V, Meguid MM, Laviano A, Yang ZJ, Varma M. Use of orchiectomy and testosterone replacement to explore meal number-to-meal size relationship in male rats. Am J Physiol. 1999; 276:R1366–R1373.
72. Borgquist A, Meza C, Wagner EJ. The role of AMP-activated protein kinase in the androgenic potentiation of cannabinoid-induced changes in energy homeostasis. Am J Physiol Endocrinol Metab. 2015;308:E482–E495.
73. Anukulkitch C, Rao A, Dunshea FR, Blache D, Lincoln GA, Clarke IJ. Influence of photoperiod and gonadal status on food intake, adiposity and gene expression of hypothalamic appetite regulators in a seasonal mammal. Am J Physiol. 2006;292: R242–R252.
74. Elias CF, Aschkenasi C, Lee C, et al. Leptin differentially regulates NPY and POMC neurons projecting to the lateral hypothalamic area. Neuron. 1999;23:775–786.
75. van den Top M, Lee K, Whyment AD, Blanks AM, Spanswick D. Orexigen-sensitive NPY/AgRP pacemaker neurons in the hypothalamic arcuate nucleus. Nat Neurosci. 2004;7:493–494.
76. Qiu J, Fang Y, Rønnekleiv OK, Kelly MJ. Leptin excites proopiomelanocortin neurons via activation of TRPC channels. J Neurosci. 2010;30:1560–1565.
77. Williams KW, Margatho LO, Lee CE, et al. Segregation of acute leptin and insulin effects in distinct populations of arcuate proopiomelanocortin neurons. J Neurosci. 2010;30:2472–2479.
78. Bauer-Dantoin AC, McDonald JK, Levine JE. Neuropeptide Y potentiates luteinizing hormone (LH)-releasing hormone-stimulated LH surges in pentobarbital-blocked proestrous rats. Endocrinology. 1991;129:402–408.
79. Leupen SM, Levine JE. Role of protein kinase C in facilitation of luteinizing hormone (LH)-releasing hormone-induced LH surges by neuropeptide Y. Endocrinology. 1999;140:3682–3687.
80. Acosta-Martinez M, Horton T, Levine JE. Estrogen receptors in neuropeptide Y neurons: at the crossroads of feeding and reproduction. Trends Endocrinol Metab. 2007;18:48–50.
81. Mills RH, Sohn RK, Micevych PE. Estrogen-induced μ-opioid receptor internalization in the medial preoptic nucleus is mediated via neuropeptide Y-Y1 receptor activation in the arcuate nucleus of female rats. J Neurosci. 2004;24:947–955.
82. Dodd GT, Decherf S, Loh K, et al. Leptin and insulin act on POMC neurons to promote the browning of white fat. Cell. 2015;160:88–104.