Galanin inhibits GLP-1 and GIP secretion via the GAL1 receptor in enteroendocrine L and K cells

British Journal of Pharmacology

Volumn 173, Issue 5, 2016, Pages 888-898

  Psichas, Arianna ^a   Glass, Leslie L ^a   Sharp, Stephen J ^b   Reimann, Frank ^a   Gribble, Fiona M ^a  

^a MEDICAL RESEARCH COUNCIL   (United Kingdom)

^b MRC EPIDEMIOLOGY UNIT   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP; G PROTEIN COUPLED INWARDLY RECTIFYING POTASSIUM CHANNEL; G PROTEIN COUPLED INWARDLY RECTIFYING POTASSIUM CHANNEL 1; G PROTEIN COUPLED INWARDLY RECTIFYING POTASSIUM CHANNEL 4; GALANIN; GALANIN RECEPTOR 1; GASTRIC INHIBITORY POLYPEPTIDE; GLUCAGON LIKE PEPTIDE 1; GLUCAGON LIKE PEPTIDE 1 RECEPTOR; INCRETIN; UNCLASSIFIED DRUG; GUANINE NUCLEOTIDE EXCHANGE FACTOR; MESSENGER RNA; RAPGEF4 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL LINE; CONTROLLED STUDY; EMBRYO; ENZYME INHIBITION; FEMALE; GENE EXPRESSION; HORMONE RELEASE; K CELL LINE; L CELL LINE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SECRETION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; CELL CULTURE; DRUG EFFECTS; ENTEROENDOCRINE CELL; GENETICS; MALE; METABOLISM; SECRETION (PROCESS); TRANSGENIC MOUSE;

ANIMALS; CELLS, CULTURED; CYCLIC AMP; ENTEROENDOCRINE CELLS; FEMALE; GALANIN; GASTRIC INHIBITORY POLYPEPTIDE; GLUCAGON-LIKE PEPTIDE 1; GUANINE NUCLEOTIDE EXCHANGE FACTORS; MALE; MICE, INBRED C57BL; MICE, TRANSGENIC; RECEPTOR, GALANIN, TYPE 1; RNA, MESSENGER;

EID: 84958787122     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/bph.13407     Document Type: Article

References (54)

1. Alexander SPH, Davenport AP, Kelly E, Marrion N, Peters JA, Benson HE, et al., (2015a). The Concise Guide to PHARMACOLOGY 2015/16: G Protein-Coupled Receptors. Br J Pharmacol 172: 5744-5869.
2. Alexander SPH, Catterall WA, Kelly E, Marrion N, Peters JA, Benson HE, et al., (2015b). The Concise Guide to PHARMACOLOGY 2015/16: Voltage-gated ion channels. Br J Pharmacol 172: 5904-5941.
3. Anselmi L, Stella SL Jr, Brecha NC, Sternini C, (2009). Galanin inhibition of voltage-dependent Ca(2+) influx in rat cultured myenteric neurons is mediated by galanin receptor 1. J Neurosci Res 87: 1107-1114.
4. Bauer F, Zintel A, Kenny M, Calder D, Ghatei M, Bloom S, (1989). Inhibitory effect of galanin on postprandial gastrointestinal motility and gut hormone release in humans. Gastroenterology 97: 260-264.
5. Bohorquez DV, Samsa LA, Roholt A, Medicetty S, Chandra R, Liddle RA, (2014). An enteroendocrine cell-enteric glia connection revealed by 3D electron microscopy. PLoS One 9 e89881.
6. Bohorquez DV, Shahid RA, Erdmann A, Kreger AM, Wang Y, Calakos N, et al., (2015). Neuroepithelial circuit formed by innervation of sensory enteroendocrine cells. J Clin Invest 125: 782-786.
7. Campbell J, Drucker D, (2013). Pharmacology, physiology, and mechanisms of incretin hormone action. Cell Metab 17: 819-837.
8. Chan KW, Sui JL, Vivaudou M, Logothetis DE, (1996). Control of channel activity through a unique amino acid residue of a G protein-gated inwardly rectifying K+ channel subunit. Proc Natl Acad Sci U S A 93: 14193-14198.
9. Chang C, Chey W, Coy D, Chang T, (1995). Galanin inhibits cholecystokinin secretion in STC-1 cells. Biochem Biophys Res Commun 216: 20-25.
10. Counts SE, McGuire SO, Sortwell CE, Crawley JN, Collier TJ, Mufson EJ, (2002). Galanin inhibits tyrosine hydroxylase expression in midbrain dopaminergic neurons. J Neurochem 83: 442-451.
11. Curtis MJ, Bond RA, Spina D, Ahluwalia A, Alexander SP, Giembycz MA, et al., (2015). Experimental design and analysis and their reporting: New guidance for publication in BJP. Br J Pharmacol 172: 3461-3471.
12. de Weille JR, Fosset M, Schmid-Antomarchi H, Lazdunski M, (1989). Galanin inhibits dopamine secretion and activates a potassium channel in pheochromocytoma cells. Brain Res 485: 199-203.
13. Dumoulin V, Dakka T, Plaisancie P, Chayvialle JA, Cuber JC, (1995). Regulation of glucagon-like peptide-1-(7-36) amide, peptide YY, and neurotensin secretion by neurotransmitters and gut hormones in the isolated vascularly perfused rat ileum. Endocrinology 136: 5182-5188.
14. Duprat F, Lesage F, Guillemare E, Fink M, Hugnot JP, Bigay J, et al., (1995). Heterologous multimeric assembly is essential for K+ channel activity of neuronal and cardiac G-protein-activated inward rectifiers. Biochem Biophys Res Commun 212: 657-663.
15. Friedlander RS, Moss CE, Mace J, Parker HE, Tolhurst G, Habib AM, et al., (2011). Role of phosphodiesterase and adenylate cyclase isozymes in murine colonic glucagon-like peptide 1 secreting cells. Br J Pharmacol 163: 261-271.
16. Fuxe K, Marcellino D, Rivera A, Diaz-Cabiale Z, Filip M, Gago B, et al., (2008). Receptor-receptor interactions within receptor mosaics. Impact on neuropsychopharmacology. Brain Res Rev 58: 415-452.
17. Fuxe K, Borroto-Escuela DO, Romero-Fernandez W, Tarakanov AO, Calvo F, Garriga P, et al., (2012). On the existence and function of galanin receptor heteromers in the central nervous system. Front Endocrinol 3: 127.
18. Habert-Ortoli E, Amiranoff B, Loquet I, Laburthe M, Mayaux J, (1994). Molecular cloning of a functional human galanin receptor. Proc Natl Acad Sci U S A 91: 9780-9783.
19. Habib AM, Richards P, Cairns LS, Rogers GJ, Bannon CA, Parker HE, et al., (2012). Overlap of endocrine hormone expression in the mouse intestine revealed by transcriptional profiling and flow cytometry. Endocrinology 153: 3054-3065.
20. Herrmann-Rinke C, Voge A, Hess M, Goke B, (1995). Regulation of glucagon-like peptide-1 secretion from rat ileum by neurotransmitters and peptides. J Endocrinol 147: 25-31.
21. Herrmann-Rinke C, Hörsch D, McGregor G, Göke B, (1996). Galanin is a potent inhibitor of glucagon-like peptide-1 secretion from rat ileum. Peptides 17: 571-576.
22. Howard AD, Tan C, Shiao LL, Palyha OC, McKee KK, Weinberg DH, et al., (1997). Molecular cloning and characterization of a new receptor for galanin. FEBS Lett 405: 285-290.
23. Huang CL, Slesinger PA, Casey PJ, Jan YN, Jan LY, (1995). Evidence that direct binding of G beta gamma to the GIRK1 G protein-gated inwardly rectifying K+ channel is important for channel activation. Neuron 15: 1133-1143.
24. Huber P, (1967). The behavior of maximum likelihood estimates under nonstandard conditions. Proc Fifth Berkeley Symp on Math Statist and Prob 1: 221-233.
25. Jin W, Lu Z, (1999b). Synthesis of a stable form of tertiapin: A high-affinity inhibitor for inward-rectifier K+ channels. Biochemistry 38: 14286-14293.
26. Jin W, Klem AM, Lewis JH, Lu Z, (1999a). Mechanisms of inward-rectifier K+ channel inhibition by tertiapin-Q. Biochemistry 38: 14294-14301.
27. Kaplan L, Spindel E, Isselbacher K, Chin W, (1988). Tissue-specific expression of the rat galanin gene. Proc Natl Acad Sci U S A 85: 1065-1069.
28. Kaufmann K, Romaine I, Days E, Pascual C, Malik A, Yang L, et al., (2013). ML297 (VU0456810), the first potent and selective activator of the GIRK potassium channel, displays antiepileptic properties in mice. ACS chemical neuroscience 4: 1278-1286.
29. Krapivinsky G, Gordon EA, Wickman K, Velimirovic B, Krapivinsky L, Clapham DE, (1995). The G-protein-gated atrial K+ channel IKACh is a heteromultimer of two inwardly rectifying K(+)-channel proteins. Nature 374: 135-141.
30. Lang R, Gundlach AL, Kofler B, (2007). The galanin peptide family: Receptor pharmacology, pleiotropic biological actions, and implications in health and disease. Pharmacol Ther 115: 177-207.
31. Lang R, Gundlach AL, Holmes FE, Hobson SA, Wynick D, Hokfelt T, et al., (2015). Physiology, signaling, and pharmacology of galanin peptides and receptors: Three decades of emerging diversity. Pharmacol Rev 67: 118-175.
32. Logothetis DE, Kurachi Y, Galper J, Neer EJ, Clapham DE, (1987). The beta gamma subunits of GTP-binding proteins activate the muscarinic K+ channel in heart. Nature 325: 321-326.
33. Lundstrom L, Sollenberg U, Brewer A, Kouya PF, Zheng K, Xu X-J, et al., (2005). A galanin receptor subtype 1 specific agonist. Int J Pept Res Ther 11: 17-27.
34. Lüscher C, Slesinger P, (2010). Emerging roles for G protein-gated inwardly rectifying potassium (GIRK) channels in health and disease. Nat Rev Neurosci 11: 301-315.
35. Moreno E, Vaz SH, Cai NS, Ferrada C, Quiroz C, Barodia SK, et al., (2011). Dopamine-galanin receptor heteromers modulate cholinergic neurotransmission in the rat ventral hippocampus. J Neuroscience 31: 7412-7423.
36. Moss CE, Marsh WJ, Parker HE, Ogunnowo-Bada E, Riches CH, Habib AM, et al., (2012). Somatostatin receptor 5 and cannabinoid receptor 1 activation inhibit secretion of glucose-dependent insulinotropic polypeptide from intestinal K cells in rodents. Diabetologia 55: 3094-3103.
37. Nikolaev VO, Bunemann M, Hein L, Hannawacker A, Lohse MJ, (2004). Novel single chain cAMP sensors for receptor-induced signal propagation. J Biol Chem 279: 37215-37218.
38. Parker E, Izzarelli D, Nowak H, Mahle C, Iben L, Wang J, et al., (1995). Cloning and characterization of the rat GALR1 galanin receptor from Rin14B insulinoma cells. Brain Res Mol Brain Res 34: 179-189.
39. Parker H, Habib A, Rogers G, Gribble F, Reimann F, (2009). Nutrient-dependent secretion of glucose-dependent insulinotropic polypeptide from primary murine K cells. Diabetologia 52: 289-298.
40. Parsons RL, Mulvaney JM, Merriam LA, (1998). Galanin activates an inwardly rectifying potassium conductance and inhibits a voltage-dependent calcium conductance in mudpuppy parasympathetic neurons. Ann N Y Acad Sci 863: 156-169.
41. Pawson AJ, Sharman JL, Benson HE, Faccenda E, Alexander SPH, Buneman OP, et al., NC-IUPHAR (2014) The IUPHAR/BPS Guide to PHARMACOLOGY: An expert-driven knowledge base of drug targets and their ligands. Nucl. Acids Res 42: D1098-1106.
42. Pfaffinger PJ, Martin JM, Hunter DD, Nathanson NM, Hille B, (1985). GTP-binding proteins couple cardiac muscarinic receptors to a K channel. Nature 317: 536-538.
43. Plaisancie P, Bernard C, Chayvialle JA, Cuber JC, (1994). Regulation of glucagon-like peptide-1-(7-36) amide secretion by intestinal neurotransmitters and hormones in the isolated vascularly perfused rat colon. Endocrinology 135: 2398-2403.
44. Proks P, de Wet H, Ashcroft FM, (2013). Molecular mechanism of sulphonylurea block of K(ATP) channels carrying mutations that impair ATP inhibition and cause neonatal diabetes. Diabetes 62: 3909-3919.
45. Psichas A, Reimann F, Gribble FM, (2015). Gut chemosensing mechanisms. J Clin Invest 125: 908-917.
46. Reimann F, Habib A, Tolhurst G, Parker H, Rogers G, Gribble F, (2008). Glucose sensing in L cells: A primary cell study. Cell Metab 8: 532-539.
47. Reuveny E, Slesinger PA, Inglese J, Morales JM, Iniguez-Lluhi JA, Lefkowitz RJ, et al., (1994). Activation of the cloned muscarinic potassium channel by G protein beta gamma subunits. Nature 370: 143-146.
48. Saifia S, Chevrier AM, Bosshard A, Cuber JC, Chayvialle JA, Abello J, (1998). Galanin inhibits glucagon-like peptide-1 secretion through pertussis toxin-sensitive G protein and ATP-dependent potassium channels in rat ileal L-cells. J Endocrinol 157: 33-41.
49. Smith K, Walker M, Artymyshyn R, Bard J, Borowsky B, Tamm J, et al., (1998). Cloned human and rat galanin GALR3 receptors. Pharmacology and activation of G-protein inwardly rectifying K+ channels. J Biol Chem 273: 23321-23326.
50. Spauschus A, Lentes KU, Wischmeyer E, Dissmann E, Karschin C, Karschin A, (1996). A G-protein-activated inwardly rectifying K+ channel (GIRK4) from human hippocampus associates with other GIRK channels. J Neuroscience 16: 930-938.
51. Tatemoto K, Rökaeus A, Jörnvall H, McDonald T, Mutt V, (1983). Galanin-a novel biologically active peptide from porcine intestine. FEBS Lett 164: 124-128.
52. Wang S, He C, Hashemi T, Bayne M, (1997a). Cloning and expressional characterization of a novel galanin receptor. Identification of different pharmacophores within galanin for the three galanin receptor subtypes. J Biol Chem 272: 31949-31952.
53. Wang S, He C, Maguire MT, Clemmons AL, Burrier RE, Guzzi MF, et al., (1997b). Genomic organization and functional characterization of the mouse GalR1 galanin receptor. FEBS Lett 411: 225-230.
54. Wickman KD, Iniguez-Lluhl JA, Davenport PA, Taussig R, Krapivinsky GB, Linder ME, et al., (1994). Recombinant G-protein beta gamma-subunits activate the muscarinic-gated atrial potassium channel. Nature 368: 255-257.