G protein-coupled pH-sensing receptor OGR1 is a regulator of intestinal inflammation

Inflammatory Bowel Diseases

Volumn 21, Issue 6, 2015, Pages 1269-1281

  De Vallière, Cheryl ^a   Wang, Yu ^a,b   Eloranta, Jyrki J ^a   Vidal, Solange ^c   Clay, Ieuan ^c   Spalinger, Marianne R ^a   Tcymbarevich, Irina ^a   Terhalle, Anne ^a   Ludwig, Marie Gabrielle ^c   Suply, Thomas ^c   Fried, Michael ^a   Kullak Ublick, Gerd A ^a   Frey Wagner, Isabelle ^a   Scharl, Michael ^a   Seuwen, Klaus ^c   Wagner, Carsten A ^b   Rogler, Gerhard ^a  

^a UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^b UNIVERSITY OF ZURICH   (Switzerland)

^c NOVARTIS PHARMA AG   (Switzerland)

Author keywords

animal model; GPCR; IBD; microarrays; OGR1; pH sensing receptors

Indexed keywords

G PROTEIN COUPLED RECEPTOR; LIPOPOLYSACCHARIDE; MITOGEN ACTIVATED PROTEIN KINASE; OGR1 PROTEIN; PROTEIN KINASE B; REGULATOR PROTEIN; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; GPR68 PROTEIN, HUMAN; GPR68 PROTEIN, MOUSE; IL10 PROTEIN, MOUSE; INTERLEUKIN 10;

ACTIN FILAMENT; ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ARTICLE; BONE MARROW CELL; CELL ACTIVATION; CELL ADHESION; COLITIS; CONTROLLED STUDY; ENTERITIS; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; HUMAN TISSUE; IMMUNE RESPONSE; INTESTINE MUCOSA; KNOCKOUT MOUSE; MACROPHAGE; MONOCYTE; MOUSE; NONHUMAN; PERITONEUM MACROPHAGE; PH; PRIORITY JOURNAL; PROMOTER REGION; REAL TIME POLYMERASE CHAIN REACTION; RECEPTOR UPREGULATION; RECTUM PROLAPSE; ACID BASE BALANCE; ANIMAL; CELL LINE; FEMALE; INFLAMMATORY BOWEL DISEASE; INTESTINE; MALE; METABOLISM; PATHOLOGY; PHYSIOLOGY;

ACID-BASE EQUILIBRIUM; ANIMALS; CELL LINE; FEMALE; HUMANS; INFLAMMATORY BOWEL DISEASES; INTERLEUKIN-10; INTESTINAL MUCOSA; INTESTINES; MACROPHAGES, PERITONEAL; MALE; MICE; MICE, KNOCKOUT; RECEPTORS, G-PROTEIN-COUPLED;

EID: 84929863936     PISSN: 10780998     EISSN: 15364844     Source Type: Journal    
DOI: 10.1097/MIB.0000000000000375     Document Type: Article

References (63)

1. Hanly EJ, Aurora AA, Shih SP, et al. Peritoneal acidosis mediates immunoprotection in laparoscopic surgery. Surgery. 2007;142:357-364.
2. Mogi C, Tobo M, Tomura H, et al. Involvement of proton-sensing TDAG8 in extracellular acidification-induced inhibition of proinflammatory cytokine production in peritoneal macrophages. J Immunol. 2009; 182:3243-3251.
3. Brokelman WJ, Lensvelt M, Borel Rinkes IH, et al. Peritoneal changes due to laparoscopic surgery. Surg Endosc. 2011;25:1-9.
4. Lardner A. The effects of extracellular pH on immune function. J Leukoc Biol. 2001;69:522-530.
5. Van Heel DA, Udalova IA, De Silva AP, et al. Inflammatory bowel disease is associated with functional TNF polymorphism affecting OCT1/NFkappa B interaction. Gut. 2002;50:A30.
6. Sandborn WJ, Targan SR. Biologic therapy of inflammatory bowel disease. Gastroenterology. 2002;122:1592-1608.
7. Blam ME, Stein RB, Lichtenstein GR. Integrating anti-tumor necrosis factor therapy in inflammatory bowel disease: current and future perspectives. Am J Gastroenterol. 2001;96:1977-1997.
8. Danese S, Colombel JF, Peyrin-Biroulet L, et al. Review article: the role of anti-TNF in the management of ulcerative colitis-past, present and future. Aliment Pharmacol Ther. 2013;37:855-866.
9. Rutgeerts PJ. Review article: efficacy of infliximab in Crohn's disease-induction and maintenance of remission. Aliment Pharmacol Ther. 1999; 13(suppl 4):9-15; discussion 38.
10. van Dullemen HM, van Deventer SJ, Hommes DW, et al. Treatment of Crohn's disease with anti-tumor necrosis factor chimeric monoclonal antibody (cA2). Gastroenterology. 1995;109:129-135.
11. Grivennikov SI, Tumanov AV, Liepinsh DJ, et al. Distinct and nonredundant in vivo functions of TNF produced by t cells and macrophages/neutrophils: protective and deleterious effects. Immunity. 2005; 22:93-104.
12. Neurath MF, Pettersson S, Meyer zum Buschenfelde KH, et al. Local administration of antisense phosphorothioate oligonucleotides to the p65 subunit of NF-kappa B abrogates established experimental colitis in mice. Nat Med. 1996;2:998-1004.
13. Rogler G, Brand K, Vogl D, et al. Nuclear factor kappaB is activated in macrophages and epithelial cells of inflamed intestinal mucosa. Gastroenterology. 1998;115:357-369.
14. Hatoum OA, Binion DG, Gutterman DD. Paradox of simultaneous intestinal ischaemia and hyperaemia in inflammatory bowel disease. Eur J Clin Invest. 2005;35:599-609.
15. Ludwig MG, Vanek M, Guerini D, et al. Proton-sensing G-protein-coupled receptors. Nature. 2003;425:93-98.
16. Seuwen K, Ludwig MG, Wolf RM. Receptors for protons or lipid messengers or both? J Recept Signal Transduct Res. 2006;26:599-610.
17. Mogi C, Tomura H, Tobo M, et al. Sphingosylphosphorylcholine antagonizes proton-sensing ovarian cancer G-protein-coupled receptor 1 (OGR1)-mediated inositol phosphate production and cAMP accumulation. J Pharmacol Sci. 2005;99:160-167.
18. Tomura H, Wang JQ, Komachi M, et al. Prostaglandin I(2) production and cAMP accumulation in response to acidic extracellular pH through OGR1 in human aortic smooth muscle cells. J Biol Chem. 2005;280:34458-34464.
19. Ichimonji I, Tomura H, Mogi C, et al. Extracellular acidification stimulates IL-6 production and Ca2+ mobilization through proton-sensing OGR1 receptors in human airway smooth muscle cells. Am J Physiol Lung Cell Mol Physiol. 2010;299:L567-L577.
20. Palmer CD, Rahman FZ, Sewell GW, et al. Diminished macrophage apoptosis and reactive oxygen species generation after phorbol ester stimulation in Crohn's disease. PLoS One. 2009;4:e7787.
21. Campos N, Magro F, Castro AR, et al. Macrophages from IBD patients exhibit defective tumour necrosis factor-alpha secretion but otherwise normal or augmented pro-inflammatory responses to infection. Immunobiology. 2011;216:961-970.
22. Franke A, McGovern DP, Barrett JC, et al. Genome-wide meta-analysis increases to 71 the number of confirmed Crohn's disease susceptibility loci. Nat Genet. 2010;42:1118-1125.
23. Onozawa Y, Komai T, Oda T. Activation of T cell death-associated gene 8 attenuates inflammation by negatively regulating the function of inflammatory cells. Eur J Pharmacol. 2011;654:315-319.
24. Wirtz S, Neurath MF. Mouse models of inflammatory bowel disease. Adv Drug Deliv Rev. 2007;59:1073-1083.
25. Solomon L, Mansor S, Mallon P, et al. The dextran sulphate sodium (DSS) model of colitis: an overview. Comp Clin Pathol. 2010; 19:235-239.
26. Hibi T, Ogata H, Sakuraba A. Animal models of inflammatory bowel disease. J Gastroenterol. 2002;37:409-417.
27. Rogler G, Daig R, Aschenbrenner E, et al. Establishment of long-term primary cultures of human small and large intestinal epithelial cells. Lab Invest. 1998;78:889-890.
28. Mohebbi N, Benabbas C, Vidal S, et al. The proton-activated G protein coupled receptor OGR1 acutely regulates the activity of epithelial proton transport proteins. Cell Physiol Biochem. 2012;29:313-324.
29. Zhang X, Goncalves R, Mosser DM. The isolation and characterization of murine macrophages. Curr Protoc Immunol. 2008; Chapter 14:Unit 141.
30. Bentz S, Pesch T, Wolfram L, et al. Lack of transketolase-like (TKTL) 1 aggravates murine experimental colitis. Am J Physiol Gastrointest Liver Physiol. 2011;300:G598-G607.
31. Fischbeck A, Leucht K, Frey-Wagner I, et al. Sphingomyelin induces cathepsin D-mediated apoptosis in intestinal epithelial cells and increases inflammation in DSS colitis. Gut. 2011;60:55-65.
32. Kauffmann A, Gentleman R, Huber W. arrayQualityMetrics-a bioconductor package for quality assessment of microarray data. Bioinformatics. 2009;25:415-416.
33. Auwerx J. The human leukemia cell line, THP-1: a multifaceted model for the study of monocyte-macrophage differentiation. Experientia. 1991;47: 22-31.
34. Widmann C, Gibson S, Jarpe MB, et al. Mitogen-activated protein kinase: conservation of a three-kinase module from yeast to human. Physiol Rev. 1999;79:143-180.
35. Seger R, Krebs EG. The MAPK signaling cascade. FASEB J. 1995;9:726-735.
36. Cargnello M, Roux PP. Activation and function of the MAPKs and their substrates, the MAPK-activated protein kinases. Microbiol Mol Biol Rev. 2011;75:50-83.
37. Angel P, Karin M. The role of Jun, Fos and the AP-1 complex in cellproliferation and transformation. Biochim Biophys Acta. 1991;1072:129-157.
38. Karin M. The regulation of AP-1 activity by mitogen-activated protein kinases. J Biol Chem. 1995;270:16483-16486.
39. DeFranco AL, Crowley MT, Finn A, et al. The role of tyrosine kinases and map kinases in LPS-induced signaling. Prog Clin Biol Res. 1998;397: 119-136.
40. Englaro W, Bahadoran P, Bertolotto C, et al. Tumor necrosis factor alphamediated inhibition of melanogenesis is dependent on nuclear factor kappa B activation. Oncogene. 1999;18:1553-1559.
41. Kane LP, Shapiro VS, Stokoe D, et al. Induction of NF-kappaB by the Akt/PKB kinase. Curr Biol. 1999;9:601-604.
42. Ozes ON, Mayo LD, Gustin JA, et al. NF-kappaB activation by tumour necrosis factor requires the Akt serine-threonine kinase. Nature. 1999; 401:82-85.
43. Aggarwal BB, Kumar A, Bharti AC. Anticancer potential of curcumin: Preclinical and clinical studies. Anticancer Res. 2003;23:363-398.
44. Aggarwal S, Ichikawa H, Takada Y, et al. Curcumin (diferuloylmethane) down-regulates expression of cell proliferation and antiapoptotic and metastatic gene products through suppression of IkappaBalpha kinase and Akt activation. Mol Pharmacol. 2006;69:195-206.
45. Katerelos M, Mudge SJ, Stapleton D, et al. 5-aminoimidazole-4-carboxamide ribonucleoside and AMP-activated protein kinase inhibit signalling through NF-kappaB. Immunol Cell Biol. 2010;88:754-760.
46. Pierce JW, Schoenleber R, Jesmok G, et al. Novel inhibitors of cytokineinduced IkappaBalpha phosphorylation and endothelial cell adhesion molecule expression show anti-inflammatory effects in vivo. J Biol Chem. 1997;272:21096-21103.
47. Kishore N, Sommers C, Mathialagan S, et al. A selective IKK-2 inhibitor blocks NF-kappa B-dependent gene expression in interleukin-1 beta-stimulated synovial fibroblasts. J Biol Chem. 2003;278:32861-32871.
48. Fujioka S, Niu J, Schmidt C, et al. NF-kappaB and AP-1 connection: mechanism of NF-kappaB-dependent regulation of AP-1 activity. Mol Cell Biol. 2004;24:7806-7819.
49. Cartharius K, Frech K, Grote K, et al. MatInspector and beyond: promoter analysis based on transcription factor binding sites. Bioinformatics. 2005; 21:2933-2942.
50. Lum H, Qiao J, Walter RJ, et al. Inflammatory stress increases receptor for lysophosphatidylcholine in human microvascular endothelial cells. Am J Physiol Heart Circ Physiol. 2003;285:H1786-H1789.
51. Haas JG, Baeuerle PA, Riethmuller G, et al. Molecular mechanisms in down-regulation of tumor necrosis factor expression. Proc Natl Acad Sci USA. 1990;87:9563-9567.
52. Ziegler-Heitbrock HW, Blumenstein M, Kafferlein E, et al. In vitro desensitization to lipopolysaccharide suppresses tumour necrosis factor, interleukin-1 and interleukin-6 gene expression in a similar fashion. Immunology. 1992;75:264-268.
53. Pei L, Castrillo A, Tontonoz P. Regulation of macrophage inflammatory gene expression by the orphan nuclear receptor Nur77. Mol Endocrinol. 2006;20:786-794.
54. Esnault C, Stewart A, Gualdrini F, et al. Rho-actin signaling to the MRTF coactivators dominates the immediate transcriptional response to serum in fibroblasts. Genes Dev. 2014;28:943-958.
55. Zhang YQ, Resta S, Jung B, et al. Upregulation of activin signaling in experimental colitis. Am J Physiol Gastrointest Liver Physiol. 2009;297: G768-G780.
56. Sierra-Filardi E, Puig-Kroger A, Blanco FJ, et al. Activin A skews macrophage polarization by promoting a proinflammatory phenotype and inhibiting the acquisition of anti-inflammatory macrophage markers. Blood. 2011;117:5092-5101.
57. Lin Z, Hegarty JP, Cappel JA, et al. Identification of disease-associated DNA methylation in intestinal tissues from patients with inflammatory bowel disease. Clin Genet. 2011;80:59-67.
58. Karatzas PS, Gazouli M, Safioleas M, et al. DNA methylation changes in inflammatory bowel disease. Ann Gastroenterol. 2014;27:125-132.
59. Ng YL, Klopcic B, Lloyd F, et al. Secreted protein acidic and rich in cysteine (SPARC) exacerbates colonic inflammatory symptoms in dextran sodium sulphate-induced murine colitis. PLoS One. 2013;8:e77575.
60. Aljarari NMH. The role of GPCR on various second messenger systems. J Basic Med Allied Sci. 2012:1-7.
61. Anderson CA, Boucher G, Lees CW, et al. Meta-analysis identifies 29 additional ulcerative colitis risk loci, increasing the number of confirmed associations to 47. Nat Genet. 2011;43:246-252.
62. Jostins L, Ripke S, Weersma RK, et al. Host-microbe interactions have shaped the genetic architecture of inflammatory bowel disease. Nature. 2012;491:119-124.
63. Khor B, Gardet A, Xavier RJ. Genetics and pathogenesis of inflammatory bowel disease. Nature. 2011;474:307-317.