Research resource: Gene profiling of G protein-coupled receptors in the arcuate nucleus of the female

Molecular Endocrinology

Volumn 28, Issue 8, 2014, Pages 1362-1380

  Rønnekleiv, Oline K ^a,b   Fang, Yuan ^a,c   Zhang, Chunguang ^a   Nestor, Casey C ^a   Mao, Peizhong ^a,b   Kelly, Martin J ^a,b  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^c Hangzhou Derlead Bio Tech Co Ltd   (China)

Author keywords

[No Author keywords available]

Indexed keywords

EXENDIN 4; G PROTEIN COUPLED RECEPTOR; GLUCAGON LIKE PEPTIDE 1 RECEPTOR; MESSENGER RNA; PROOPIOMELANOCORTIN; TRANSCRIPTOME;

ADULT; ANIMAL CELL; ARCUATE NUCLEUS; ARTICLE; CONDUCTANCE; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; GENE EXPRESSION PROFILING; IN VITRO STUDY; MALE; MOUSE; NERVE CELL; NONHUMAN; POTASSIUM CONDUCTANCE; PRIORITY JOURNAL; PROTEIN BINDING; QUANTITATIVE ANALYSIS; RECEPTOR GENE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WHOLE CELL PATCH CLAMP; ANIMAL; C57BL MOUSE; CELL CULTURE; CYTOLOGY; GENETICS; METABOLISM;

ANIMALS; ARCUATE NUCLEUS OF HYPOTHALAMUS; CELLS, CULTURED; FEMALE; GENE EXPRESSION PROFILING; MICE, INBRED C57BL; NEURONS; PRO-OPIOMELANOCORTIN; RECEPTORS, G-PROTEIN-COUPLED; TRANSCRIPTOME;

EID: 84905266259     PISSN: 08888809     EISSN: 19449917     Source Type: Journal    
DOI: 10.1210/me.2014-1103     Document Type: Article

References (120)

1. 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.
2. 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.
3. Lyons DJ, Horjales-Araujo E, Broberger C. Synchronized network oscillations in rat tuberoinfundibular dopamine neurons: switch to tonic discharge by thyrotropin-releasing hormone. Neuron. 2010; 65:217-229.
4. Lehman MN, Ladha Z, Coolen LM, et al. Neuronal plasticity and seasonal reproduction in sheep. Eur J Neurosci. 2010;32:2152-2164.
5. Ohkura S, Takase K, Matsuyama S, et al. Gonadotrophin-releasing hormone pulse generator activity in the hypothalamus of the goat. J Neuroendocrinol. 2009;21:813-821.
6. Rønnekleiv OK, Bosch MA, Zhang C. 17-Oestradiol regulation of gonadotrophin-releasing hormone neuronal excitability. J Neuroendocrinol. 2011;24:122-130.
7. Kelly MJ, Rønnekleiv OK. Membrane-initiated actions of estradiol that regulate reproduction, energy balance and body temperature. Front Neuroendocrinol. 2012;33:376-387.
8. Micevych PE, Kelly MJ. Membrane estrogen receptor regulation of hypothalamic function. Neuroendocrinology. 2012;96:103-110.
9. Kelly MJ, Zhang C, Qiu J, Rønnekleiv OK. Pacemaking kisspeptin neurons. Exp Physiol. 2013;98:1535-1543.
10. Gearing M, Terasawa E. Suppression of luteinizing hormone release by the _1-adrenergic receptor antagonist prazosin in the ovariectomized female rhesus monkey. Am J Primatol. 1991;25: 23-33.
11. Kelly MJ, Qiu J, Wagner EJ, Rønnekleiv OK. Rapid effects of estrogen on G protein-coupled receptor activation of potassium channels in the central nervous system (CNS). J Steroid Biochem Mol Biol. 2002;83:187-193.
12. Ibrahim N, Bosch MA, Smart JL, et al. Hypothalamic proopiomelanocortin neurons are glucose-responsive and express KATP channels. Endocrinology. 2003;144:1331-1340.
13. Cone RD. Anatomy and regulation of the central melanocortin system. Nat Neurosci. 2005;8:571-578.
14. 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.
15. Qiu J, Xue C, Bosch MA, et al. Serotonin 5-hydroxytryptamine2c receptor signaling in hypothalamic POMC neurons: role in energy homeostasis in females. Mol Pharmacol. 2007;72:885-896.
16. 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.
17. Pennock RL, Hentges ST. Differential expression and sensitivity of presynaptic and postsynaptic opioid receptors regulating hypothalamic proopiomelanocortin neurons. J Neurosci. 2011;31:281-288.
18. 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 1_-estradiol. Am J Physiol Endocrinol Metab. 2013;305:E632-E640.
19. Regard JB, Sato IT, Coughlin SR. Anatomical profiling of g protein- coupled receptor expression. Cell. 2008;135:561-571.
20. Allen Institute for Brain Science. Allen Brain Atlas. Seattle, WA: Allen Institute for Brain Science; 2011.
21. Civelli O. Orphan GPCRs and neuromodulation. Neuron. 2012; 76:12-21.
22. Civelli O, Reinscheid RK, Zhang Y, Wang Z, Fredriksson R, Schiöth HB. G protein-coupled receptor deorphanizations. Annu Rev Pharmacol Toxicol. 2013;53:127-146.
23. Allen JA, Roth BL. Strategies to discover unexpected targets for drugs active at G protein-coupled receptors. Annu Rev Pharmacol Toxicol. 2011;51:117-144.
24. Kelly MJ, Loose MD, Rønnekleiv OK. Estrogen suppresses _-opioid- and GABAB-mediated hyperpolarization of hypothalamic arcuate neurons. J Neurosci. 1992;12:2745-2750.
25. Lagrange AH, Wagner EJ, Rønnekleiv OK, Kelly MJ. Estrogen rapidly attenuates a GABAB response in hypothalamic neurons. Neuroendocrinology. 1996;64:114-123.
26. Wagner EJ, Bosch MA, Kelly MJ, Rønnekleiv OK. A powerful GABAB receptor-mediated inhibition of GABAergic neurons in arcuate nucleus. NeuroReport. 1999;10:2681-2687.
27. 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.
28. Zheng SX, Bosch MA, Rønnekleiv OK. Mu-opioid receptor mRNA expression in identified hypothalamic neurons. J Comp Neurol. 2005;487:332-344.
29. Bosch MA, Hou J, Fang Y, Kelly MJ, Rønnekleiv OK. 17-Estradiol regulation of themRNAexpression of T-type calcium channel subunits: role of estrogen receptor _and estrogen receptor. J Comp Neurol. 2009;512:347-358.
30. Zhang C, Tonsfeldt KJ, Qiu J, Bosch MA, Kobayashi K, Steiner RA, Kelly MJ, Rønnekleiv OK. 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.
31. Bosch MA, Xue C, Rønnekleiv OK. Kisspeptin expression in guinea pig hypothalamus: effects of 17-estradiol. J Comp Neurol. 2012;520:2143-2162.
32. Zhang C, Bosch MA, Rick EA, Kelly MJ, Rønnekleiv OK. 17- Estradiol regulation of T-type calcium channels in gonadotropinreleasing hormone neurons. J Neurosci. 2009;29:10552-10562.
33. Qiu J, Fang Y, Rønnekleiv OK, Kelly MJ. Leptin excites proopiomelanocortin neurons via activation of TRPC channels. J Neurosci. 2010;30:1560-1565.
34. Bosch MA, Tonsfeldt KJ, Rønnekleiv OK. mRNA expression of ion channels in GnRH neurons: subtype-specific regulation by 17-estradiol. Mol Cell Endocrinol. 2013;367:85-97.
35. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2CT method. Methods. 2001;25:402-408.
36. Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acid Res. 2001;29:2002-2007.
37. Taylor S. A MIQE case study-effect of RNA sample quality and reference gene stability on gene expression data. Bio-Rad Tech Bull. 2011;6245.
38. Turton MD, O'Shea D, Gunn I, et al. A role for glucagon-like peptide-1 in the central regulation of feeding. Nature. 1996;379: 69-72.
39. Göke R, Fehmann HC, Linn T, et al. Exendin-4 is a high potency agonist and truncated exendin-(9-39)-amide an antagonist at the glucagon-like peptide 1-(7-36)-amide receptor of insulin-secreting beta-cells. J Biol Chem. 1993;268:19650-19655.
40. Dalvi PS, Nazarians-Armavil A, Purser MJ, Belsham DD. Glucagon- like peptide-1 receptor agonist, exendin-4, regulates feedingassociated neuropeptides in hypothalamic neurons in vivo and in vitro. Endocrinology. 2012;153:2208-2222.
41. Van Pett K, Viau V, Bittencourt JC, et al. Distribution of mRNAs encoding CRF receptors in brain and pituitary of rat and mouse. J Comp Neurol. 2000;428:191-212.
42. Lagrange AH, Rønnekleiv OK, Kelly MJ. The potency of _-opioid hyperpolarization of hypothalamic arcuate neurons is rapidly attenuated by 17α-estradiol. J Neurosci. 1994;14:6196-6204.
43. Unnerstall JR, Kopajtic TA, Kuhar MJ. Distribution of α2 agonist binding sites in the rat and human central nervous system: analysis of some functional, anatomic correlates of the pharmacologic effects of clonidine and related adrenergic agents. Brain Res. 1984; 319:69-101.
44. Condon TP, Rønnekleiv OK, Kelly MJ. Estrogen modulation of the α1-adrenergic response of hypothalamic neurons. Neuroendocrinology 1989;50:51-58.
45. King PR, Gundlach AL, Louis WJ. Quantitative autoradiographic localization in rat brain of α2-adrenergic and non-adrenergic I-receptor binding sites labelled by [3H]rilmenidine. Brain Res. 1995; 675:264-278.
46. Acosta-Martinez M, Fiber JM, Brown RD, Etgen AM. Localization of α1B-adrenergic receptor in female rat brain regions involved in stress and neuroendocrine function. Neurochem Int. 1999;35:383-391.
47. Gundlah C, Pecins-Thompson M, Schutzer WE, Bethea CL. Ovarian steroid effects on serotonin 1A, 2A and 2C receptor mRNA in macaque hypothalamus. Mol Brain Res. 1999;63:325-339.
48. Etgen AM. Estrogen regulation of neurotransmitter and growth factor signaling in the brain. In: Pfaff DW, ed. Hormones, Brain and Behavior. 3rd ed. San Diego, CA: Academic Press; 2002:381-440.
49. Kishi T, Elmquist JK. Body weight is regulated by the brain: a link between feeding and emotion. Mol Psychiatry. 2005;10:132-146.
50. Smith SM, True C, Grove KL. The neuroendocrine basis of lactation- induced suppression of GnRH: role of kisspeptin and leptin. Brain Res. 2010;1364:139-152.
51. 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.
52. Allen LG, Crowley WR, Kalra SP. Interactions between neuropeptide Y and adrenergic systems in the stimulation of luteinizing hormone release in steroid-primed ovariectomized rats. Endocrinology. 1987;121:1953-1959.
53. Clark JT, Gist RS, Kalra SP, Kalra PS. Alpha2-adrenoceptor blockade attenuates feeding behavior induced by neuropeptide Y and epinephrine. Physiol Behav. 1988;43:417-422.
54. Pralong FP, Gonzales C, Voirol MJ, et al. The neuropeptide Y Y1 receptor regulates leptin-mediated control of energy homeostasis and reproductive functions. FASEB J. 2002;16:712-714.
55. Fetissov SO, Byrne LC, Hassani H, Ernfors P, Hökfelt T. Characterization of neuropeptide Y Y2 and Y5 receptor expression in the mouse hypothalamus. J Comp Neurol. 2004;470:256-265.
56. Guy J, Pelletier G. Neuronal interactions between neuropeptide Y (NPY) and catecholaminergic systems in the rat arcuate nucleus as shown by dual immunocytochemistry. Peptides. 1988;9:567-570.
57. Horvath TL, Naftolin F, Kalra SP, Leranth C. Neuropeptide-Y innervation of _-endorphin-containing cells in the rat mediobasal hypothalamus: a light and electron microscopic double immunostaining analysis. Endocrinology. 1992;131:2461-2467.
58. Lagrange AH, Rønnekleiv OK, Kelly MJ. Estradiol-17 and -opioid peptides rapidly hyperpolarize GnRH neurons: A cellular mechanism of negative feedback? Endocrinology. 1995;136: 2341-2344.
59. Roa J, Herbison AE. Direct regulation of GnRH neuron excitability by arcuate nucleus POMC and NPY neuron neuropeptides in female mice. Endocrinology. 2012;153:5587-5599.
60. Chen AS, Marsh DJ, Trumbauer ME, et al. Inactivation of the mouse melanocortin-3 receptor results in increased fat mass and reduced lean body mass. Nat Genet. 2000;26:97-102.
61. Lee Y-S, Poh LK, Loke KY. A novel melanocortin 3 receptor gene (MC3R) mutation associated with severe obesity. J Clin Endocrinol Metab. 2002;87:1423-1426.
62. Farooqi IS, Keogh JM, Yeo GS, Lank EJ, Cheetham T, O'Rahilly S. Clinical spectrum of obesity and mutations in the melanocortin 4 receptor gene. N Engl J Med. 2003;348:1085-1095.
63. Gantz I, Konda Y, Tashiro T, et al. Molecular cloning of a novel melanocortin receptor. J Biol Chem. 1993;268:8246-8250.
64. Roselli-Rehfuss L, Mountjoy KG, Robbins LS, et al. Identification of a receptor for α melanotropin and other proopiomelanocortin peptides in the hypothalamus and limbic system. Proc Natl Acad Sci USA. 1993;90:8856-8860.
65. Mountjoy KG, Mortrud MT, Low MJ, Simerly RB, Cone RD. Localization of the melanocortin-4 receptor (MC4-R) in neuroendocrine and autonomic control circuits in the brain. Mol Endocrinol. 1994;8:1298-1308.
66. Beck B. Neuropeptide Y in normal eating and in genetic and dietary- induced obesity. Phil Trans R Soc B Biol Sci. 2006;361: 1159-1185.
67. Ramachandrappa S, Gorrigan RJ, Clark AJL, Chan LF. The melanocortin receptors and their accessory proteins. Front Endocrinol (Lausanne). 2013;4:9.
68. Holst JJ. The physiology of glucagon-like peptide 1. Physiol Rev. 2007;87:1409-1439.
69. Munroe DG, Gupta AK, Kooshesh F, et al. Prototypic G proteincoupled receptor for the intestinotrophic factor glucagon-like peptide 2. Proc Natl Acad Sci USA. 1999;96:1569-1573.
70. Qui 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.
71. Szayna M, Doyle ME, Betkey JA, et al. Exendin-4 decelerates food intake, weight gain, and fat deposition in Zucker rats. Endocrinology. 2000;141:1936-1941.
72. Tang-Christensen M, Larsen PJ, Thulesen J, Rømer J, Vrana N. The proglucagon-derived peptide, glucagon-like peptide-2, is a neurotransmitter involved in the regulation of food intake. Nat. Med. 2000;6:802-807.
73. Guan X, Shi X, Li X, et al. GLP-2 receptor in POMC neurons suppresses feeding behavior and gastric motility. Am J Physiol Endocrinol Metab. 2012;303:E853-E864.
74. Lovshin J, Estall J, Yusta B, Brown TJ, Drucker DJ. Glucagon-like peptide (GLP)-2 action in the murine central nervous system is enhanced by elimination of GLP-1 receptor signaling. J Biol Chem. 2001;276:21489-21499.
75. Herbison AE, de Tassigny Xd, Doran J, Colledge WH. Distribution and postnatal development of Gpr54 gene expression in mouse brain and gonadotropin-releasing hormone neurons. Endocrinology. 2010;151:312-321.
76. 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.
77. 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.
78. 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.
79. 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.
80. Seminara SB, Messager S, Chatzidaki EE, et al. The GPR54 gene as a regulator of puberty. N Engl J Med. 2003;349:1614-1627.
81. d'Anglemont de Tassigny X, Fagg LA, Dixon JP, et al. Hypogonadotropic hypogonadism in mice lacking a functional Kiss1 gene. Proc Natl Acad Sci USA. 2007;104:10714-10719.
82. Topaloglu AK, Reimann F, Guclu M, et al. TAC3 and TACR3 mutations in familial hypogonadotropic hypogonadism reveal a key role for Neurokinin B in the central control of reproduction. Nat Genet. 2009;41:354-358.
83. Guran T, Tolhurst G, Bereket A, et al. Hypogonadotropic hypogonadism due to a novel missense mutation in the first extracellular loop of the neurokinin B receptor. J Clinl Endocrinol Metab. 2009;94:3633-3639.
84. Topaloglu AK, Tello JA, Kotan LD, et al. Inactivating KISS1 mutation and hypogonadotropic hypogonadism. N Engl J Med. 2012;366:629-635.
85. Rønnekleiv OK, Kelly MJ, Eskay RL. Distribution of immunoreactive substance P neurons in the hypothalamus and pituitary of the rhesus monkey. J Comp Neurol. 1984;224:51-59.
86. de Croft S, Boehm U, Herbison AE. Neurokinin B activates arcuate kisspeptin neurons through multiple tachykinin receptors in the male mouse. Endocrinology. 2013;154:2750-2760.
87. Halls ML, van der Westhuizen ET, Bathgate RA, Summers RJ. Relaxin family peptide receptors-former orphans reunite with their parent ligands to activate multiple signalling pathways. Br J Pharmacol. 2007;150:677-691.
88. McGowan BM, Stanley SA, White NE, et al. Hypothalamic mapping of orexigenic action and Fos-like immunoreactivity following relaxin-3 administration in male Wistar rats. Am J Physiol Endocrinol Metab. 2007;292:E913-E919.
89. Otsubo H, Onaka T, Suzuki H, et al. Centrally administered relaxin- 3 induces Fos expression in the osmosensitive areas in rat brain and facilitates water intake. Peptides. 2010;31:1124-1130.
90. Smith CM, Shen PJ, Banerjee A, et al. Distribution of relaxin-3 and RXFP3 within arousal, stress, affective, and cognitive circuits of mouse brain. J Comp Neurol. 2010;518:4016-4045.
91. Becskei C, Riediger T, Zünd D, Wookey P, Lutz TA. Immunohistochemical mapping of calcitonin receptors in the adult rat brain. Brain Res. 2004;1030:221-233.
92. Lerner UH. Deletions of genes encoding calcitonin/α-CGRP, amylin and calcitonin receptor have given new and unexpected insights into the function of calcitonin receptors and calcitonin receptorlike receptors in bone. J Musculoskelet Neuronal Interact. 2006; 6:87-95.
93. Tavares E, Maldonado R, Miñano FJ. Aminoprocalcitonin-mediated suppression of feeding involves the hypothalamic melanocortin system. Am J Physiol Endocrinol Metab. 2013;304:E1251-E1262.
94. Yamada M, Iwabuchi T, Takahashi K, et al. Identification and expression of frizzled-3 protein in rat frontal cortex after antidepressant and electroconvulsive treatment. J Pharmacol Sci. 2005; 99:239-246.
95. Liu C, Wang Y, Smallwood PM, Nathans J. An essential role for Frizzled5 in neuronal survival in the parafascicular nucleus of the thalamus. J Neurosci. 2008;28:5641-5653.
96. Schulte G, Bryja V. The frizzled family of unconventional G-protein- coupled receptors. Trends Pharmacol Sci. 2007;28:518-525.
97. Gordon MD, Nusse R. Wnt signaling: multiple pathways, multiple receptors, and multiple transcription factors. J Biol Chem. 2006; 281:22429-22433.
98. Kohn AD, Moon RT. Wnt and calcium signaling: _-catenin-independent pathways. Cell Calcium. 2005;38:439-446.
99. Filardo EJ, Thomas P. GPR30: a seven-transmembrane-spanning estrogen receptor that triggers EGF release. Trends Endocrinol Metab. 2005;16:362-367.
100. Funakoshi T, Yanai A, Shinoda K, Kawano MM, Mizukami Y. G protein-coupled receptor 30 is an estrogen receptor in the plasma membrane. Biochem Biophys Res Commun. 2006;346:904-910.
101. Filardo E, Quinn J, Pang Y, et al. Activation of the novel estrogen receptor G protein-coupled receptor 30 (GPR30) at the plasma membrane. Endocrinology. 2007;148:3236-3245.
102. Filardo EJ, Thomas P. Minireview: G protein-coupled estrogen receptor-1, GPER-1: its mechanism of action and role in female reproductive cancer, renal and vascular physiology. Endocrinology. 2012;153:2953-2962.
103. Noel SD, Keen KL, Baumann DI, Filardo EJ, Terasawa E. Involvement of G protein-coupled receptor 30 (GPR30) in rapid action of estrogen in primate LHRH neurons. Mol Endocrinol. 2009;23: 349-359.
104. Kenealy BP, Keen KL, Rønnekleiv OK, Terasawa E. STX, a novel nonsteroidal estrogenic compound, induces rapid action in primate GnRH neuronal calcium dynamics and peptide release. Endocrinology. 2011;152:182-191.
105. Qiu J, Rønnekleiv OK, Kelly MJ. Modulation of hypothalamic neuronal activity through a novel G-protein-coupled estrogen membrane receptor. Steroids. 2008;73:985-991.
106. Micevych P, Dewing P. Membrane-initiated estradiol signaling regulating sexual receptivity. Front Endocrinol (Lausanne). 2011; 2:26.
107. Reppert SM, Weaver DR, Edisawa T, Mahle CD, Kolakowski LF Jr. Cloning of a melatonin-related receptor from human pituitary. FEBS Lett. 1996;386:219-224.
108. Sidibe A, Mullier A, Chen P, et al. Expression of the orphan GPR50 protein in rodent and human dorsomedial hypothalamus, tanycytes and median eminence. J Pineal Res. 2010;48:263-269.
109. Batailler M, Mullier A, Sidibe A, et al. Neuroanatomical distribution of the orphan GPR50 receptor in adult sheep and rodent brains. J Neuroendocrinol. 2012;24:798-808.
110. Bechtold DA, Sidibe A, Saer BR, et al. A role for the melatoninrelated receptor GPR50 in leptin signaling, adaptive thermogenesis, and torpor. Curr Biol. 2012;22:70-77.
111. Tarttelin EE, Kirschner LS, Bellingham J, et al. Cloning and characterization of a novel orphan G-protein-coupled receptor localized to human chromosome 2p16. Biochem Biophys Res Commun. 1999;260:174-180.
112. Liu B, Hassan Z, Amisten S, et al. The novel chemokine receptor, G-protein-coupled receptor 75, is expressed by islets and is coupled to stimulation of insulin secretion and improved glucose homeostasis. Diabetologia. 2013;56:2467-2476.
113. Ignatov A, Robert J, Gregory-Evans C, Schaller HC. RANTES stimulates Ca2 mobilization and inositol trisphosphate (IP3) formation in cells transfected with G protein-coupled receptor 75. Br J Pharmacol. 2006;149:490-497.
114. Thaler JP, Schwartz MW. Minireview: Inflammation and obesity pathogenesis: the hypothalamus heats up. Endocrinology. 2010; 151:4109-1415.
115. Luo R, Jeong SJ, Jin Z, Strokes N, Li S, Piao X. G protein-coupled receptor 56 and collagen III, a receptor-ligand pair, regulates cortical development and lamination. Proc Natl Acad Sci USA. 2011; 108:12925-12930.
116. Singer K, Luo R, Jeong SJ, Piao X. GPR56 and the developing cerebral cortex: cells, matrix, and neuronal migration. Mol Neurobiol. 2013;47:186-196.
117. Davenport AP, Alexander SP, Sharman JL, et al. International Union of Basic and Clinical Pharmacology. LXXXVIII. G proteincoupled receptor list: recommendations for new pairings with cognate ligands. Pharmacol Rev. 2013;65:967-986.
118. Duman JG, Tzeng CP, Tu YK, et al. The adhesion-GPCR BAI1 regulates synaptogenesis by controlling the recruitment of the Par3/Tiam1 polarity complex to synaptic sites. J Neurosci. 2013; 33:6964-6978.
119. Stephenson JR, Paavola KJ, Schaefer SA, Kaur B, Van Meir EG, Hall RA. Brain-specific angiogenesis inhibitor-1 signaling, regulation, and enrichment in the postsynaptic density. J Biol Chem. 2013;288:22248-22256.
120. Stephenson JR, Purcell RH, Hall RA. The BAI subfamily of adhesion GPCRs: synaptic regulation and beyond. Trends Pharmacol Sci. 2014;35:208-215.