Galanin activates g protein gated inwardly rectifying potassium channels and suppresses kisspeptin-10 activation of gnrh neurons

Endocrinology

Volumn 157, Issue 8, 2016, Pages 3197-3212

  Constantin, Stephanie ^a   Wray, Susan ^a  

^a NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AR M 1896; CALCIUM; CYCLIC AMP; G PROTEIN COUPLED INWARDLY RECTIFYING POTASSIUM CHANNEL; GALANIN; GALANIN 1 16; GALANIN RECEPTOR 1; GALANIN RECEPTOR 2; GALANIN RECEPTOR 3; GONADORELIN; KISSPEPTIN 10; M 1145; M 617; OPIATE AGONIST; UNCLASSIFIED DRUG; KISS1 PROTEIN, HUMAN; KISSPEPTIN;

ADULT; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BIOASSAY; CALCIUM SIGNALING; CELL ACTIVATION; CELLS; EMBRYO; EXPLANT; FEMALE; HORMONE RELEASE; INTRACELLULAR SIGNALING; MOUSE; MOUSE EMBRYO; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; AGONISTS; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL CULTURE; CYTOLOGY; DRUG EFFECTS; HYPOTHALAMUS; MAMMALIAN EMBRYO; METABOLISM; PREGNANCY;

ANIMALS; CALCIUM SIGNALING; CELLS, CULTURED; EMBRYO, MAMMALIAN; FEMALE; G PROTEIN-COUPLED INWARDLY-RECTIFYING POTASSIUM CHANNELS; GALANIN; GONADOTROPIN-RELEASING HORMONE; HYPOTHALAMUS; KISSPEPTINS; MICE; NEURONS; PREGNANCY;

EID: 84982840841     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2016-1064     Document Type: Article

References (80)

1. Skofitsch G, Jacobowitz DM. Quantitative distribution of galaninlike immunoreactivity in the rat central nervous system. Peptides. 1986;7:609-613.
2. Gentleman SM, Falkai P, Bogerts B, Herrero MT, Polak JM, Roberts GW. Distribution of galanin-like immunoreactivity in the human brain. Brain Res. 1989;505:311-315.
3. Pérez SE, Wynick D, Steiner RA, Mufson EJ. Distribution of galaninergic immunoreactivity in the brain of the mouse. J Comp Neurol. 2001;434:158-185.
4. Kaplan LM, Gabriel SM, Koenig JI, et al. Galanin is an estrogeninducible, secretory product of the rat anterior pituitary. Proc Natl Acad Sci USA. 1988;85:7408-7412.
5. Gabriel SM, Koenig JI, Kaplan LM. Galanin-like immunoreactivity is influenced by estrogen in peripubertal and adult rats. Neuroendocrinology. 1990;51:168-173.
6. Lang R, Gundlach AL, Holmes FE, et al. Physiology, signaling, and pharmacology of galanin peptides and receptors: three decades of emerging diversity. Pharmacol Rev. 2015;67:118-175.
7. Merchenthaler I, Lopez FJ, Negro-Vilar A. Colocalization of galanin and luteinizing hormone-releasing hormone in a subset of preoptic hypothalamic neurons: anatomical and functional correlates. Proc Natl Acad Sci USA. 1990;87:6326-6330.
8. Key S, Wray S. Two olfactory placode derived galanin subpopulations: luteinizing hormone-releasing hormone neurones and vomeronasal cells. J Neuroendocrinol. 2000;12:535-545.
9. Dudas B, Merchenthaler I. Three-dimensional representation of the neurotransmitter systems of the human hypothalamus: inputs of the gonadotrophin hormone-releasing hormone neuronal system. J Neuroendocrinol. 2006;18:79-95.
10. Porteous R, Petersen SL, Yeo SH, et al. Kisspeptin neurons co-express met-enkephalin and galanin in the rostral periventricular region of the female mouse hypothalamus. J Comp Neurol. 2011; 519:3456-3469.
11. Rajendren G, Li X. Galanin synaptic input to gonadotropin-releasing hormone perikarya in juvenile and adult female mice: implications for sexual maturity. Brain Res Dev Brain Res. 2001;131:161-165.
12. Rajendren G, Gibson MJ. A confocal microscopic study of synaptic inputs to gonadotropin-releasing hormone cells in mouse brain: regional differences and enhancement by estrogen. Neuroendocrinology. 2001;73:84-90.
13. Rajendren G. Increased galanin synapses onto activated gonadotropin-releasing hormone neuronal cell bodies in normal female mice and in functional preoptic area grafts in hypogonadal mice. J Neuroendocrinol. 2002;14:435-441.
14. Mitchell V, Bouret S, Prévot V, Jennes L, Beauvillain JC. Evidence for expression of galanin receptor Gal-R1 mRNA in certain gonadotropin releasing hormone neurones of the rostral preoptic area. J Neuroendocrinol. 1999;11:805-812.
15. Dufourny L, Skinner DC. Distribution of galanin receptor 1-immunoreactive neurons in the ovine hypothalamus: colocalization with GnRH. Brain Res. 2005;1054:73-81.
16. Todman MG, Han SK, Herbison AE. Profiling neurotransmitter receptor expression in mouse gonadotropin-releasing hormone neurons using green fluorescent protein-promoter transgenics and microarrays. Neuroscience. 2005;132:703-712.
17. Kalló I, Vida B, Deli L, et al. Co-localisation of kisspeptin with galanin or neurokinin B in afferents to mouse GnRH neurones. J Neuroendocrinol. 2012;24:464-476.
18. Fueshko S, Wray S. LHRH cells migrate on peripherin fibers in embryonic olfactory explant cultures: an in vitro model for neurophilic neuronal migration. Dev Biol. 1994;166:331-348.
19. Klenke U, Taylor-Burds C. Culturing embryonic nasal explants for developmental and physiological study. Curr Protoc Neurosci. 2012;Chapter 3:Unit 3.25.1-16.
20. Kramer PR, Krishnamurthy R, Mitchell PJ, Wray S. Transcription factor activator protein-2 is required for continued luteinizing hormone-releasing hormone expression in the forebrain of developing mice. Endocrinology. 2000;141:1823-1838.
21. Giacobini P, Kopin AS, Beart PM, Mercer LD, Fasolo A, Wray S. Cholecystokinin modulates migration of gonadotropin-releasing hormone-1 neurons. J Neurosci. 2004;24:4737-4748.
22. Constantin S, Wray S. Gonadotropin-releasing hormone-1 neuronal activity is independent of hyperpolarization-activated cyclic nucleotide-modulated channels but is sensitive to protein kinase a-dependent phosphorylation. Endocrinology. 2008;149:3500-3511.
23. Liu X, Lee K, Herbison AE. Kisspeptin excites gonadotropin-releasing hormone neurons through a phospholipase C/calcium-dependent pathway regulating multiple ion channels. Endocrinology. 2008;149:4605-4614.
24. Constantin S, Iremonger KJ, Herbison AE. In vivo recordings of GnRH neuron firing reveal heterogeneity and dependence upon GABAA receptor signaling. J Neurosci. 2013;33:9394-9401.
25. Constantin S, Caligioni CS, Stojilkovic S, Wray S. Kisspeptin-10 facilitates a plasma membrane-driven calcium oscillator in gonadotropin-releasing hormone-1 neurons. Endocrinology. 2009;150: 1400-1412.
26. Jasoni CL, Romanò N, Constantin S, Lee K, Herbison AE. Calcium dynamics in gonadotropin-releasing hormone neurons. Front Neuroendocrinol. 2010;31:259-269.
27. Constantin S, Wray S. Gonadotropin-releasing hormone-1 neuronal activity is independent of cyclic nucleotide-gated channels. Endocrinology. 2008;149:279-290.
28. Constantin S, Caraty A, Wray S, Duittoz AH. Development of go-nadotropin-releasing hormone-1 secretion in mouse nasal explants. Endocrinology. 2009;150:3221-3227.
29. Lundstrom L, Sollenberg U, Brewer A, et al. A galanin receptor subtype 1 specific agonist. Int J Pept Res Ther. 2005;11:17-27.
30. Runesson J, Saar I, Lundström L, Järv J, Langel U. A novel GalR2-specific peptide agonist. Neuropeptides. 2009;43:187-192.
31. Constantin S, Klenke U, Wray S. The calcium oscillator of GnRH-1 neurons is developmentally regulated. Endocrinology. 2010;151: 3863-3873.
32. Yue HY, Fujita T, Kumamoto E. Biphasic modulation by galanin of excitatory synaptic transmission in substantia gelatinosa neurons of adult rat spinal cord slices. J Neurophysiol. 2011;105:2337-2349.
33. Giacobini P, Wray S. Cholecystokinin directly inhibits neuronal activity of primary gonadotropin-releasing hormone cells through cholecystokinin-1 receptor. Endocrinology. 2007;148:63-71.
34. Meister B, Hulting AL, Uvnäs-Moberg K, Hökfelt T. Galanin stimulates the release of cholecystokinin from nerve fibres in the pituitary neurointermediate lobe. Neuroreport. 1993;4:631-634.
35. Klenke U, Constantin S, Wray S. Neuropeptide Y directly inhibits neuronal activity in a subpopulation of gonadotropin-releasing hormone-1 neurons via Y1 receptors. Endocrinology. 2010;151:2736-2746.
36. Meneses D, Mateos V, Islas G, Barral J. G-protein-coupled inward rectifier potassium channels involved in corticostriatal presynaptic modulation. Synapse. 2015;69:446-452.
37. Bartfai T, Bedecs K, Land T, et al. M-15: high-affinity chimeric peptide that blocks the neuronal actions of galanin in the hippocampus, locus coeruleus, and spinal cord. Proc Natl Acad Sci USA. 1991;88:10961-10965.
38. Constantin S. Physiology of the gonadotrophin-releasing hormone (GnRH) neurone: studies from embryonic GnRH neurones. J Neuroendocrinol. 2011;23:542-553.
39. Constantin S, Piet R, Iremonger K, et al. GnRH neuron firing and response to GABA in vitro depend on acute brain slice thickness and orientation. Endocrinology. 2012;153:3758-3769.
40. Mennicken F, Hoffert C, Pelletier M, Ahmad S, O'Donnell D. Restricted distribution of galanin receptor 3 (GalR3) mRNA in the adult rat central nervous system. J Chem Neuroanat. 2002;24:257-268.
41. O'Donnell D, Ahmad S, Wahlestedt C, Walker P. Expression of the novel galanin receptor subtype GALR2 in the adult rat CNS: distinct distribution from GALR1. J Comp Neurol. 1999;409:469- 481.
42. Chambers G, Whitelaw CM, Robinson JE, Evans NP. Distribution of galanin receptor-2 immunoreactive neurones in the ovine hypothalamus: no evidence for involvement in the control of gonadotrophin-releasing hormone secretion. J Neuroendocrinol. 2007;19: 966-973.
43. Couse JF, Yates MM, Walker VR, Korach KS. Characterization of the hypothalamic-pituitary-gonadal axis in estrogen receptor (ER) Null mice reveals hypergonadism and endocrine sex reversal in females lacking ERβ but not ERβ. Mol Endocrinol. 2003;17:1039-1053.
44. Cheong RY, Porteous R, Chambon P, Abrahám I, Herbison AE. Effects of neuron-specific estrogen receptor (ER)α β and ERβ deletion on the acute estrogen negative feedback mechanism in adult female mice. Endocrinology. 2014;155:1418-1427.
45. Herbison AE, Pape JR. New evidence for estrogen receptors in gonadotropin-releasing hormone neurons. Front Neuroendocrinol. 2001;22:292-308.
46. Sharifi N, Reuss AE, Wray S. Prenatal LHRH neurons in nasal explant cultures express estrogen receptor β transcript. Endocrinology. 2002;143:2503-2507.
47. Irwig MS, Fraley GS, Smith JT, et al. Kisspeptin activation of gonadotropin releasing hormone neurons and regulation of KiSS-1 mRNA in the male rat. Neuroendocrinology. 2004;80:264-272.
48. 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.
49. Han SK, Gottsch ML, Lee KJ, et al. Activation of gonadotropinreleasing hormone neurons by kisspeptin as a neuroendocrine switch for the onset of puberty. J Neurosci. 2005;25:11349-11356.
50. Poulain P, Decrocq N, Mitchell V. Direct inhibitory action of galanin on hypothalamic arcuate nucleus neurones expressing galanin receptor Gal-r1 mRNA. Neuroendocrinology. 2003;78:105-117.
51. Badie-Mahdavi H, Lu X, Behrens MM, Bartfai T. Role of galanin receptor 1 and galanin receptor 2 activation in synaptic plasticity associated with 3,5-cyclic AMP response element-binding protein phosphorylation in the dentate gyrus: studies with a galanin receptor 2 agonist and galanin receptor 1 knockout mice. Neuroscience. 2005;133:591- 604.
52. Andreis PG, Malendowicz LK, Rebuffat P, Spinazzi R, Ziolkowska A, Nussdorfer GG. Galanin enhances corticosterone secretion from dispersed rat adrenocortical cells through the activation of GAL-R1 and GAL-R2 receptors coupled to the adenylate cyclase-dependent signaling cascade. Int J Mol Med. 2007;19:149-155.
53. Lopez FJ, Negro-Vilar A. Galanin stimulates luteinizing hormonereleasing hormone secretion from arcuate nucleus-median eminence fragments in vitro: involvement of an β-adrenergic mechanism. Endocrinology. 1990;127:2431-2436.
54. Tarasov KV, Tarasova YS, Crider DG, Anisimov SV, Wobus AM, Boheler KR. Galanin and galanin receptors in embryonic stem cells: accidental or essential? Neuropeptides. 2002;36:239-245.
55. Jones M, Perumal P, Vrontakis M. Presence of galanin-like immunoreactivity in mesenchymal and neural crest origin tissues during embryonic development in the mouse. Anat Rec (Hoboken). 2009; 292:481-487.
56. Wynick D, Bacon A. Targeted disruption of galanin: new insights from knock-out studies. Neuropeptides. 2002;36:132-144.
57. Keimpema E, Zheng K, Barde SS, et al. GABAergic terminals are a source of galanin to modulate cholinergic neuron development in the neonatal forebrain. Cereb Cortex. 2014;24:3277-3288.
58. Shi TJ, Hua XY, Lu X, et al. Sensory neuronal phenotype in galanin receptor 2 knockout mice: focus on dorsal root ganglion neurone development and pain behaviour. Eur J Neurosci. 2006;23:627-636.
59. Jungnickel SR, Yao M, Shen PJ, Gundlach AL. Induction of galanin receptor-1 (GalR1) expression in external granule cell layer of postnatal mouse cerebellum. J Neurochem. 2005;92:1452-1462.
60. Burazin TC, Larm JA, Ryan MC, Gundlach AL. Galanin-R1 and -R2 receptor mRNA expression during the development of rat brain suggests differential subtype involvement in synaptic transmission and plasticity. Eur J Neurosci. 2000;12:2901-2917.
61. Mazarati A, Lu X, Kilk K, Langel U, Wasterlain C, Bartfai T. Galanin type 2 receptors regulate neuronal survival, susceptibility to seizures and seizure-induced neurogenesis in the dentate gyrus. Eur J Neurosci. 2004;19:3235-3244.
62. Papas S, Bourque CW. Galanin inhibits continuous and phasic firing in rat hypothalamic magnocellular neurosecretory cells. J Neurosci. 1997;17:6048-6056.
63. Kennedy ME, Nemec J, Corey S, Wickman K, Clapham DE. GIRK4 confers appropriate processing and cell surface localization to G-protein-gated potassium channels. J Biol Chem. 1999;274:2571-2582.
64. Kubo Y, Adelman JP, Clapham DE, et al. International Union of Pharmacology. LIV. Nomenclature and molecular relationships of inwardly rectifying potassium channels. Pharmacol Rev. 2005;57: 509-526.
65. Kinney GA, Emmerson PJ, Miller RJ. Galanin receptor-mediated inhibition of glutamate release in the arcuate nucleus of the hypothalamus. J Neurosci. 1998;18:3489-3500.
66. Florén A, Land T, Langel U. Galanin receptor subtypes and ligand binding. Neuropeptides. 2000;34:331-337.
67. Webling KE, Runesson J, Bartfai T, Langel U. Galanin receptors and ligands. Front Endocrinol. 2012;3:146.
68. Campos P, Herbison AE. Optogenetic activation of GnRH neurons reveals minimal requirements for pulsatile luteinizing hormone secretion. Proc Natl Acad Sci USA. 2014;111:18387-18392.
69. Messager S, Chatzidaki EE, Ma D, et al. Kisspeptin directly stimulates gonadotropin-releasing hormone release via G protein-coupled receptor 54. Proc Natl Acad Sci USA. 2005;102:1761-1766.
70. Moenter SM. Identified GnRH neuron electrophysiology: a decade of study. Brain Res. 2010;1364:10-24.
71. Sahu A, Crowley WR, Tatemoto K, Balasubramaniam A, Kalra SP. Effects of neuropeptide Y, NPY analog (norleucine4-NPY), galanin and neuropeptide K on LH release in ovariectomized (ovx) and ovx estrogen, progesterone-treated rats. Peptides. 1987;8:921-926.
72. Sahu A, Xu B, Kalra SP. Role of galanin in stimulation of pituitary luteinizing hormone secretion as revealed by a specific receptor antagonist, galantide. Endocrinology. 1994;134:529-536.
73. Tomiæ M, Cesnajaj M, Catt KJ, Stojilkovic SS. Developmental and physiological aspects of Ca2β signaling in agonist-stimulated pituitary gonadotrophs. Endocrinology. 1994;135:1762-1771.
74. Sánchez-Cárdenas C, Hernández-Cruz A. GnRH-Induced [Ca2+]isignalling patterns in mouse gonadotrophs recorded from acute pituitary slices in vitro. Neuroendocrinology. 2010;91:239-255.
75. Duran-Pasten ML, Fiordelisio T. GnRH-induced Ca(2+) signaling patterns and gonadotropin secretion in pituitary gonadotrophs. Functional adaptations to both ordinary and extraordinary physiological demands. Front Endocrinol. 2013;4:127.
76. d'Anglemont de Tassigny X, Fagg LA, Carlton MB, Colledge WH. Kisspeptin can stimulate gonadotropin-releasing hormone (GnRH) release by a direct action at GnRH nerve terminals. Endocrinology. 2008;149:3926-3932.
77. Denef C. Paracrinicity: the story of 30 years of cellular pituitary crosstalk. J Neuroendocrinol. 2008;20:1-70.
78. Jacoby AS, Hort YJ, Constantinescu G, Shine J, Iismaa TP. Critical role for GALR1 galanin receptor in galanin regulation of neuroendocrine function and seizure activity. Brain Res Mol Brain Res. 2002;107:195-200.
79. Hohmann JG, Krasnow SM, Teklemichael DN, Clifton DK, Wynick D, Steiner RA. Neuroendocrine profiles in galanin-overexpressing and knockout mice. Neuroendocrinology. 2003;77:354-366.
80. Fuxe K, Borroto-Escuela D, Fisone G, Agnati LF, Tanganelli S. Understanding the role of heteroreceptor complexes in the central nervous system. Curr Protein Pept Sci. 2014;15:647.