Role of extracellular proton-sensing OGR1 in regulation of insulin secretion and pancreatic β-cell functions

Endocrine Journal

Volumn 61, Issue 2, 2014, Pages 101-110

  Mogi, Chihiro ^a   Nakakura, Takashi ^a   Okajima, Fumikazu ^a  

^a GUNMA UNIVERSITY   (Japan)

Author keywords

Insulin secretion; OGR1; Pancreatic cell; Proton sensing GPCRs

Indexed keywords

CALCIUM ION; G PROTEIN COUPLED RECEPTOR; GLUCOSE; INSULIN; ION CHANNEL; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN OGR1; PROTON; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; VANILLOID RECEPTOR 1;

BLOOD PH; CALCIUM TRANSPORT; CELL DIFFERENTIATION; CELL PH; CIRCULATION; EXTRACELLULAR MATRIX; GLUCOSE METABOLISM; HORMONE ACTION; HORMONE SYNTHESIS; HUMAN; IN VITRO STUDY; IN VIVO STUDY; INSULIN RELEASE; INSULIN SENSITIVITY; MICROENVIRONMENT; NONHUMAN; PANCREAS ISLET BETA CELL; PANCREAS ISLET CELL FUNCTION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN METABOLISM; PROTON TRANSPORT; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; CELL DIFFERENTIATION; FEMALE; GLUCOSE; HYDROGEN-ION CONCENTRATION; INSULIN; INSULIN-SECRETING CELLS; ISOXAZOLES; MICE; RATS; RECEPTORS, G-PROTEIN-COUPLED; TRPV CATION CHANNELS;

EID: 84896863727     PISSN: 09188959     EISSN: 13484540     Source Type: Journal    
DOI: 10.1507/endocrj.EJ13-0380     Document Type: Review

References (74)

1. Ayers P, Dixon C (2012) Simple acid-base tutorial. JPEN J Parenter Enteral Nutr 36: 18-23.
2. Yajima M, Ui M (1975) Carbohydrate metabolism and its response to catecholamines as modified in alkalotic rat. Am J Physiol 228: 1046-1052.
3. Yajima M, Ui M (1975) Hydrocortisone restoration of the pH-dependent metabolic responses to catecholamines. Am J Physiol 228: 1053-1059.
4. Ohta M, Nelson D, Nelson J, Meglasson MD, Erecinska M (1991) Relationships between energy level and insulin secretion in isolated rat islets of Langerhans. A study at various pH values. Biochem Pharmacol 42: 593-598.
5. Hyder A, Laue C, Schrezenmeir J (2001) Effect of extracellular pH on insulin secretion and glucose metabolism in neonatal and adult rat pancreatic islets. Acta Diabetol 38: 171-178.
6. Juntti-Berggren L, Arkhammar P, Nilsson T, Rorsman P, Berggren PO (1991) Glucose-induced increase in cytoplasmic pH in pancreatic beta-cells is mediated by Na+/ H+ exchange, an effect not dependent on protein kinase C. J Biol Chem 266: 23537-23541.
7. Stiernet P, Nenquin M, Moulin P, Jonas JC, Henquin JC (2007) Glucose-induced cytosolic pH changes in betacells and insulin secretion are not causally related: studies in islets lacking the Na+/H+ exchangeR NHE1. J Biol Chem 282: 24538-24546.
8. Best L, Bone EA, Meats JE, Tomlinson S (1988) Is intracellular pH a coupling factor in nutrient-stimulated pancreatic islets? J Mol Endocrinol 1: 33-38.
9. Gunawardana SC, Sharp GW (2002) Intracellular pH plays a critical role in glucose-induced time-dependent potentiation of insulin release in rat islets. Diabetes 51: 105-113.
10. Gunawardana SC, Rocheleau JV, Head WS, Piston DW (2004) Nutrient-stimulated insulin secretion in mouse islets is critically dependent on intracellular pH. BMC Endocr Disord 4: 1.
11. Nabe K, Fujimoto S, Shimodahira M, Kominato R, Nishi Y et al. (2006) Diphenylhydantoin suppresses glucose-induced insulin release by decreasing cytoplasmic H+ concentration in pancreatic islets. Endocrinology 147: 2717-2727.
12. Misler S, Gillis K, Tabcharani J (1989) Modulation of gating of a metabolically regulated, ATP-dependent K+ channel by intracellular pH in B cells of the pancreatic islet. J Membr Biol 109: 135-143.
13. Xu H, Cui N, Yang Z, Wu J, Giwa LR et al. (2001) Direct activation of cloned K(atp) channels by intracellular acidosis. J Biol Chem 276: 12898-12902.
14. Xu H, Wu J, Cui N, Abdulkadir L, Wang R et al. (2001) Distinct histidine residues control the acid-induced activation and inhibition of the cloned K(ATP) channel. J Biol Chem 276: 38690-38696.
15. Morales-Lazaro SL, Simon SA, Rosenbaum T (2013) The role of endogenous molecules in modulating pain through transient receptor potential vanilloid 1 (TRPV1). J Physiol 591: 3109-3121.
16. Wemmie JA, Taugher RJ, Kreple CJ (2013) Acid-sensing ion channels in pain and disease. Nat Rev Neurosci 14: 461-471.
17. Ho KW, Ward NJ, Calkins DJ (2012) TRPV1: a stress response protein in the central nervous system. Am J Neurodegener Dis 1: 1-14.
18. Zsombok A (2013) Vanilloid receptors--do they have a role in whole body metabolism? Evidence from TRPV1. J Diabetes Complications 27: 287-292.
19. Ludwig MG, Vanek M, Guerini D, Gasser JA, Jones CE et al. (2003) Proton-sensing G-protein-coupled receptors. Nature 425: 93-98.
20. Wang JQ, Kon J, Mogi C, Tobo M, Damirin A et al. (2004) TDAG8 is a proton-sensing and psychosinesensitive G-protein-coupled receptor. J Biol Chem 279: 45626-45633.
21. Liu JP, Nakakura T, Tomura H, Tobo M, Mogi C et al (2010) Each one of certain histidine residues in G-protein-coupled receptor GPR4 is critical for extracellular proton-induced stimulation of multiple G-proteinsignaling pathways. Pharmacol Res 61: 499-505.
22. Tominaga M, Tominaga T (2005) Structure and function of TRPV1. Pflugers Arch 451: 143-150.
23. Banner KH, Igney F, Poll C (2011) TRP channels: emerging targets for respiratory disease. Pharmacol Ther 130: 371-384.
24. Lee LY, Gu Q, Xu F, Hong JL (2013) Acid-sensing by airway afferent nerves. Pulm Pharmacol Ther 26: 491-497
25. Uchida K, Tominaga M (2011) The role of thermosensitive TRP (transient receptor potential) channels in insulin secretion. Endocr J 58: 1021-1028.
26. Zhu Z, Luo Z, Ma S, Liu D (2011) TRP channels and their implications in metabolic diseases. Pflugers Arch 461: 211-223.
27. Akiba Y, Kato S, Katsube K, Nakamura M, Takeuchi K et al. (2004) Transient receptor potential vanilloid subfamily 1 expressed in pancreatic islet beta cells modulates insulin secretion in rats. Biochem Biophys Res Commun 321: 219-225.
28. Jabin Fagelskiold A, Kannisto K, Bostrom A, Hadrovic B, Farre C et al. (2012) Insulin-secreting INS-1E cells express functional TRPV1 channels. Islets 4: 56-63.
29. Razavi R, Chan Y, Afifiyan FN, Liu XJ, Wan X et al. (2006) TRPV1+ sensory neurons control beta cell stress and islet inflammation in autoimmune diabetes. Cell 127: 1123-1135.
30. Motter AL, Ahern GP (2008) TRPV1-null mice are protected from diet-induced obesity. FEBS Lett 582: 2257-2262.
31. Wang P, Yan Z, Zhong J, Chen J, Ni Y et al. (2012) Transient receptor potential vanilloid 1 activation enhances gut glucagon-like peptide-1 secretion and improves glucose homeostasis. Diabetes 61: 2155-2165.
32. Lingueglia E (2007) Acid-sensing ion channels in sensory perception. J Biol Chem 282: 17325-17329.
33. Wu WL, Cheng CF, Sun WH, Wong CW, Chen CC (2012) Targeting ASIC3 for pain, anxiety, and insulin resistance. Pharmacol Ther 134: 127-138.
34. Huang SJ, Yang WS, Lin YW, Wang HC, Chen CC (2008) Increase of insulin sensitivity and reversal of age-dependent glucose intolerance with inhibition of ASIC3. Biochem Biophys Res Commun 371: 729-734.
35. Noda M, Yamashita S, Takahashi N, Eto K, Shen LM et al. (2002) Switch to anaerobic glucose metabolism with NADH accumulation in the beta-cell model of mitochondrial diabetes. Characteristics of betaHC9 cells deficient in mitochondrial DNA transcription. J Biol Chem 277: 41817-41826.
36. Petersen KF, Befroy D, Dufour S, Dziura J, Ariyan C et al. (2003) Mitochondrial dysfunction in the elderly: possible role in insulin resistance. Science 300: 1140-1142.
37. Tomura H, Mogi C, Sato K, Okajima F (2005) Protonsensing and lysolipid-sensitive G-protein-coupled receptors: a novel type of multi-functional receptors. Cell Signal 17: 1466-1476.
38. Meyerzu Heringdorf D, Jakobs KH (2007) Lysophospholipid receptors: signalling, pharmacology and regulation by lysophospholipid metabolism. Biochim Biophys Acta 1768: 923-940.
39. Okajima F (2013) Regulation of inflammation by extracellular acidification and proton-sensing GPCRs. Cell Signal 25: 2263-2271.
40. Murakami N, Yokomizo T, Okuno T, Shimizu T (2004) G2A is a proton-sensing G-protein-coupled receptor antagonized by lysophosphatidylcholine. J Biol Chem 279: 42484-42491.
41. Radu CG, Nijagal A, McLaughlin J, Wang L, Witte ON (2005) Differential proton sensitivity of related G protein-coupled receptors T cell death-associated gene 8 and G2A expressed in immune cells. Proc Natl Acad Sci U S A 102: 1632-1637.
42. Komarova SV, Pereverzev A, Shum JW, Sims SM, Dixon SJ (2005) Convergent signaling by acidosis and receptor activator of NF-kappaB ligand (RANKL) on the calcium/calcineurin/NFAT pathway in osteoclasts. Proc Natl Acad Sci U S A 102: 2643-2648.
43. Tomura H, Wang JQ, Liu JP, Komachi M, Damirin A et al. (2008) Cyclooxygenase-2 expression and prostaglandin E2 production in response to acidic pH through OGR1 in a human osteoblastic cell line. J Bone Miner Res 23: 1129-1139.
44. Wang J, Sun Y, Tomura H, Okajima F (2012) Ovarian cancer G-protein-coupled receptor 1 induces the expression of the pain mediator prostaglandin E2 in response to an acidic extracellular environment in human osteoblast-like cells. Int J Biochem Cell Biol 44: 1937-1941.
45. Tomura H, Wang JQ, Komachi M, Damirin A, Mogi C et al. (2005) Prostaglandin I(2) production and cAMP accumulation in response to acidic extracellular pH through OGR1 in human aortic smooth muscle cells. J Biol Chem 280: 34458-34464.
46. Liu JP, Komachi M, Tomura H, Mogi C, Damirin A et al. (2010) Ovarian cancer G protein-coupled receptor 1-dependent and-independent vascular actions to acidic pH in human aortic smooth muscle cells. Am J Physiol Heart Circ Physiol 299: H731-742.
47. Ichimonji I, Tomura H, Mogi C, Sato K, Aoki H et al. (2010) Extracellular acidification stimulates IL-6 production and Ca(2+) mobilization through proton-sensing OGR1 receptors in human airway smooth muscle cells. Am J Physiol Lung Cell Mol Physiol 299: L567-577.
48. Matsuzaki S, Ishizuka T, Yamada H, Kamide Y, Hisada T et al. (2011) Extracellular acidification induces connective tissue growth factor production through protonsensing receptor OGR1 in human airway smooth mus cle cells. Biochem Biophys Res Commun 413: 499-503.
49. Saxena H, Deshpande DA, Tiegs BC, Yan H, Battafarano RJ et al. (2012) The GPCR OGR1 (GPR68) mediates diverse signalling and contraction of airway smooth muscle in response to small reductions in extracellular pH. Br J Pharmacol 166: 981-990.
50. Kottyan LC, Collier AR, Cao KH, Niese KA, Hedgebeth M et al. (2009) Eosinophil viability is increased by acidic pH in a cAMP-and GPR65-dependent manner. Blood 114: 2774-2782.
51. Mogi C, Tobo M, Tomura H, Murata N, He XD et al. (2009) Involvement of proton-sensing TDAG8 in extracellular acidification-induced inhibition of proinflammatory cytokine production in peritoneal macrophages. J Immunol 182: 3243-3251.
52. Murata N, Mogi C, Tobo M, Nakakura T, Sato K et al. (2009) Inhibition of superoxide anion production by extracellular acidification in neutrophils. Cell Immunol 259: 21-26.
53. Chen A, Dong L, Leffler NR, Asch AS, Witte ON, Yang LV (2011) Activation of GPR4 by acidosis increases endothelial cell adhesion through the cAMP/Epac pathway. PLoS One 6: e27586.
54. Dong L, Li Z, Leffler NR, Asch AS, Chi JT, Yang LV (2013) Acidosis activation of the proton-sensing GPR4 receptor stimulates vascular endothelial cell inflammatory responses revealed by transcriptome analysis. PLoS One 8: e61991.
55. Yan L, Singh LS, Zhang L, Xu Y (2014) Role of OGR1 in myeloid-derived cells in prostate cancer. Oncogene 33: 157-164.
56. Wyder L, Suply T, Ricoux B, Billy E, Schnell C et al. (2011) Reduced pathological angiogenesis and tumor growth in mice lacking GPR4, a proton sensing receptor. Angiogenesis 14: 533-544.
57. Wike-Hooley JL, Haveman J, Reinhold HS (1984) The relevance of tumour pH to the treatment of malignant disease. Radiother Oncol 2: 343-366.
58. Yang LV, Radu CG, Roy M, Lee S, McLaughlin J et al. (2007) Vascular abnormalities in mice deficient for the G protein-coupled receptor GPR4 that functions as a pH sensor. Mol Cell Biol 27: 1334-1347.
59. Sun X, Yang LV, Tiegs BC, Arend LJ, McGraw DW et al. (2010) Deletion of the pH sensor GPR4 decreases renal acid excretion. J Am Soc Nephrol 21: 1745-1755.
60. Mohebbi N, Benabbas C, Vidal S, Daryadel A, Bourgeois S et al. (2012) The proton-activated G protein coupled receptor OGR1 acutely regulates the activity of epithelial proton transport proteins. Cell Physiol Biochem 29: 313-324.
61. Nakakura T, Mogi C, Tobo M, Tomura H, Sato K et al. (2012) Deficiency of proton-sensing ovarian cancer G protein-coupled receptor 1 attenuates glucose-stimulated insulin secretion. Endocrinology 153: 4171-4180.
62. Mogi C, Tomura H, Tobo M, Wang JQ, Damirin A et al. (2005) Sphingosylphosphorylcholine antagonizes proton-sensing ovarian cancer G-protein-coupled receptor 1 (OGR1)-mediated inositol phosphate production and cAMP accumulation. J Pharmacol Sci 99: 160-167.
63. Urbe S, Dittie AS, Tooze SA (1997) pH-dependent processing of secretogranin II by the endopeptidase PC2 in isolated immature secretory granules. Biochem J 321 (Pt 1): 65-74.
64. Sun-Wada GH, Toyomura T, Murata Y, Yamamoto A, Futai M, Wada Y (2006) The a3 isoform of V-ATPase regulates insulin secretion from pancreatic beta-cells. J Cell Sci 119: 4531-4540.
65. Louagie E, Taylor NA, Flamez D, Roebroek AJ, Bright NA et al. (2008) Role of furin in granular acidification in the endocrine pancreas: identification of the V-ATPase subunit Ac45 as a candidate substrate. Proc Natl Acad Sci U S A 105: 12319-12324.
66. Dechant R, Binda M, Lee SS, Pelet S, Winderickx J, Peter M (2010) Cytosolic pH is a second messenger for glucose and regulates the PKA pathway through V-ATPase. EMBO J 29: 2515-2526.
67. Luckie DB, Wilterding JH, Maleszewski JJ, Hobbs EC, Olson LK (2002) Extracellular acidification parallels insulin secretion in INS-1 and HIT-T15 beta-cell lines. Biochem Biophys Res Commun 293: 1168-1173.
68. Sadek H, Hannack B, Choe E, Wang J, Latif S et al. (2008) Cardiogenic small molecules that enhance myocardial repair by stem cells. Proc Natl Acad Sci U S A 105: 6063-6068.
69. Russell JL, Goetsch SC, Aguilar HR, Coe H, Luo X et al. (2012) Regulated expression of pH sensing G Protein-coupled receptor-68 identified through chemical biology defines a new drug target for ischemic heart disease. ACS Chem Biol 7: 1077-1083.
70. Schneider JW, Gao Z, Li S, Farooqi M, Tang TS et al. (2008) Small-molecule activation of neuronal cell fate. Nat Chem Biol 4: 408-410.
71. Dioum EM, Osborne JK, Goetsch S, Russell J, Schneider JW, Cobb MH (2011) A small molecule differentiation inducer increases insulin production by pancreatic beta cells. Proc Natl Acad Sci U S A 108: 20713-20718.
72. Russell JL, Goetsch SC, Aguilar HR, Frantz DE, Schneider JW (2012) Targeting native adult heart progenitors with cardiogenic small molecules. ACS Chem Biol 7: 1067-1076.
73. Schneider JW, Goetsch SC, Leng X, Ludwig SM, Russell JL et al. (2012) Coupling hippocampal neurogenesis to brain pH through proneurogenic small molecules that regulate proton sensing G protein-coupled receptors. ACS Chem Neurosci 3: 557-568.
74. Zhang L, Li P, Hsu T, Aguilar HR, Frantz DE et al. (2011) Small-molecule blocks malignant astrocyte proliferation and induces neuronal gene expression. Differentiation 81: 233-242.