Proton-sensing ovarian cancer G protein-coupled receptor 1 on dendritic cells is required for airway responses in a murine asthma model

PLoS ONE

Volumn 8, Issue 11, 2013, Pages

  Aoki, Haruka ^a,b   Mogi, Chihiro ^a   Hisada, Takeshi ^b   Nakakura, Takashi ^a   Kamide, Yosuke ^b   Ichimonji, Isao ^a   Tomura, Hideaki ^a   Tobo, Masayuki ^a   Sato, Koichi ^a   Tsurumaki, Hiroaki ^a,b   Dobashi, Kunio ^a   Mori, Tetsuya ^c   Harada, Akihiro ^d   Yamada, Masanobu ^b   Mori, Masatomo ^b   Ishizuka, Tamotsu ^e   Okajima, Fumikazu ^a  

^a GUNMA UNIVERSITY   (Japan)

^b GUNMA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c TAKASAKI UNIVERSITY OF HEALTH AND WELFARE   (Japan)

^d OSAKA UNIVERSITY   (Japan)

^e UNIVERSITY OF FUKUI   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; CHEMOKINE RECEPTOR CCR7; CYTOKINE; G PROTEIN COUPLED RECEPTOR; IMMUNOGLOBULIN E; MESSENGER RNA; OVALBUMIN; OVARIAN CANCER G PROTEIN COUPLED RECEPTOR 1; UNCLASSIFIED DRUG;

AIRWAY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTHMA; CELL MIGRATION; CONTROLLED STUDY; DENDRITIC CELL; EOSINOPHILIA; GENE EXPRESSION; GOBLET CELL; IN VITRO STUDY; LYMPH NODE; METAPLASIA; MOUSE; NONHUMAN; RESPIRATORY TRACT ALLERGY; RESPIRATORY TRACT INFLAMMATION; TH2 CELL;

ADOPTIVE TRANSFER; ANIMALS; ASTHMA; BRONCHIAL HYPERREACTIVITY; CALCIUM; CELL MOVEMENT; DENDRITIC CELLS; FEMALE; GENE EXPRESSION REGULATION; GOBLET CELLS; IMMUNOGLOBULIN E; LUNG; LYMPH NODES; MICE; MICE, KNOCKOUT; OVALBUMIN; PULMONARY EOSINOPHILIA; RECEPTORS, CCR7; RECEPTORS, G-PROTEIN-COUPLED; SIGNAL TRANSDUCTION; TH1-TH2 BALANCE; TH2 CELLS;

EID: 84893198734     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0079985     Document Type: Article

References (36)

1. Lambrecht BN, Hammad H (2009) Biology of lung dendritic cells at the origin of asthma. Immunity 31: 412-424. doi:10.1016/j.immuni. 2009.08.008. PubMed: 19766084.
2. Holgate ST (2012) Innate and adaptive immune responses in asthma. Nat Med 18: 673-683. doi:10.1038/nm.2731. PubMed: 22561831.
3. Hunt JF, Fang K, Malik R, Snyder A, Malhotra N et al. (2000) Endogenous airway acidification. Implications for asthma pathophysiology. Am J Respir Crit Care Med 161: 694-699. doi:10.1164/ajrccm.161.3.9911005. PubMed: 10712309. (Pubitemid 30171718)
4. Ricciardolo FL, Gaston B, Hunt J (2004) Acid stress in the pathology of asthma. J Allergy Clin Immunol 113: 610-619. doi:10.1016/j.jaci.2003.12.034. PubMed: 15100663. (Pubitemid 38530413)
5. Kodric M, Shah AN, Fabbri LM, Confalonieri M (2007) An investigation of airway acidification in asthma using induced sputum: a study of feasibility and correlation. Am J Respir Crit Care Med 175: 905-910. doi:10.1164/rccm.200607- 940OC. PubMed: 17290044. (Pubitemid 46684700)
6. Lardner A (2001) The effects of extracellular pH on immune function. J Leukoc Biol 69: 522-530. PubMed: 11310837.
7. Lee LY, Gu Q (2009) Role of TRPV1 in inflammation-induced airway hypersensitivity. Curr Opin Pharmacol 9: 243-249. doi:10.1016/j.coph.2009.02. 002. PubMed: 19269247.
8. Ludwig MG, Vanek M, Guerini D, Gasser JA, Jones CE et al. (2003) Proton-sensing G-protein-coupled receptors. Nature 425: 93-98. doi:10.1038/nature01905. PubMed: 12955148. (Pubitemid 37101724)
9. Wang JQ, Kon J, Mogi C, Tobo M, Damirin A et al. (2004) TDAG8 is a proton-sensing and psychosine-sensitive G-protein-coupled receptor. J Biol Chem 279: 45626-45633. doi:10.1074/jbc.M406966200. PubMed: 15326175. (Pubitemid 39491550)
10. 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-protein-signaling pathways. Pharmacol Res 61: 499-505. doi:10.1016/j.phrs.2010.02.013. PubMed: 20211729.
11. Tomura H, Mogi C, Sato K, Okajima F (2005) Proton-sensing and lysolipid-sensitive G-protein-coupled receptors: a novel type of multifunctional receptors. Cell Signal 17: 1466-1476. doi:10.1016/j.cellsig.2005.06.002. PubMed: 16014326. (Pubitemid 41253986)
12. Meyer zu Heringdorf D, Jakobs KH (2007) Lysophospholipid receptors: signalling, pharmacology and regulation by lysophospholipid metabolism. Biochim Biophys Acta 1768: 923-940. doi:10.1016/j.bbamem.2006.09.026. PubMed: 17078925. (Pubitemid 46452543)
13. Okajima F (2013) Regulation of inflammation by extracellular acidification and proton-sensing GPCRs. Cell Signal (. (2013)) PubMed: 23917207.
14. 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-L577. doi:10.1152/ajplung.00415.2009. PubMed: 20656891.
15. Matsuzaki S, Ishizuka T, Yamada H, Kamide Y, Hisada T et al. (2011) Extracellular acidification induces connective tissue growth factor production through proton-sensing receptor OGR1 in human airway smooth muscle cells. Biochem Biophys Res Commun 413: 499-503. doi:10.1016/j.bbrc.2011.08.087. PubMed: 21907704.
16. 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. doi:10.1111/j.1476-5381.2011.01807.x. PubMed: 22145625.
17. 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. doi:10.1359/jbmr.080236. PubMed: 18302504. (Pubitemid 351915735)
18. 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-H742. doi:10.1152/ajpheart.00977.2009. PubMed: 20622109.
19. Liu C, Li Q, Zhou X, Kolosov VP, Perelman JM (2013) Regulator of G-protein signaling 2 inhibits acid-induced mucin5AC hypersecretion in human airway epithelial cells. Respir Physiol Neurobiol 185: 265-271. doi:10.1016/j.resp.2012.10.003. PubMed: 23063741.
20. 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. doi:10.4049/jimmunol.0803466. PubMed: 19234222.
21. 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. doi:10.1016/j.cellimm.2009.05.008. PubMed: 19539899.
22. 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. doi:10.1210/en.2012-1164. PubMed: 22733973.
23. Aoki H, Hisada T, Ishizuka T, Utsugi M, Kawata T et al. (2008) Resolvin E1 dampens airway inflammation and hyperresponsiveness in a murine model of asthma. Biochem Biophys Res Commun 367: 509-515. doi:10.1016/j.bbrc.2008.01.012. PubMed: 18190790.
24. Hamelmann E, Schwarze J, Takeda K, Oshiba A, Larsen GL et al. (1997) Noninvasive measurement of airway responsiveness in allergic mice using barometric plethysmography. Am J Respir Crit Care Med 156: 766-775. doi:10.1164/ajrccm.156.3.9606031. PubMed: 9309991. (Pubitemid 27396413)
25. Takeda K, Hamelmann E, Joetham A, Shultz LD, Larsen GL et al. (1997) Development of eosinophilic airway inflammation and airway hyperresponsiveness in mast cell-deficient mice. J Exp Med 186: 449-454. doi:10.1084/jem.186.3.449. PubMed: 9236197. (Pubitemid 27332903)
26. Paruchuri S, Tashimo H, Feng C, Maekawa A, Xing W et al. (2009) Leukotriene E4-induced pulmonary inflammation is mediated by the P2Y12 receptor. J Exp Med 206: 2543-2555. doi:10.1084/jem.20091240. PubMed: 19822647.
27. Lee KS, Lee HK, Hayflick JS, Lee YC, Puri KD (2006) Inhibition of phosphoinositide 3-kinase delta attenuates allergic airway inflammation and hyperresponsiveness in murine asthma model. FASEB J 20: 455-465. doi:10.1096/fj.05-5045com. PubMed: 16507763. (Pubitemid 44933322)
28. Koya T, Takeda K, Kodama T, Miyahara N, Matsubara S et al. (2006) RANTES (CCL5) regulates airway responsiveness after repeated allergen challenge. Am J Respir Cell Mol Biol 35: 147-154. doi:10.1165/rcmb.2005-0394OC. PubMed: 16528011. (Pubitemid 44175313)
29. Tsuchiya K, Siddiqui S, Risse PA, Hirota N, Martin JG. (2012) The presence of LPS in OVA inhalations affects airway inflammation and AHR but not remodeling in a rodent model of asthma. Am J Physiol Lung Cell Mol Physiol 303: L54-L63. doi:10.1152/ajplung.00208.2011. PubMed: 22523281.
30. Miyahara N, Ohnishi H, Matsuda H, Miyahara S, Takeda K et al. (2008) Leukotriene B4 receptor 1 expression on dendritic cells is required for the development of Th2 responses and allergen-induced airway hyperresponsiveness. J Immunol 181: 1170-1178. PubMed: 18606670.
31. Lomask M (2006) Further exploration of the Penh parameter. Exp Toxicol Pathol 57 Suppl 2: 13-20. doi:10.1016/j.etp.2006.02.014. PubMed: 16638630.
32. Adler A, Cieslewicz G, Irvin CG (2004) Unrestrained plethysmography is an unreliable measure of airway responsiveness in BALB/c and C57BL/6 mice. J Appl Physiol 97: 286-292. doi:10.1152/japplphysiol.00821.2003. PubMed: 15033965. (Pubitemid 38802530)
33. Bates J, Irvin C, Brusasco V, Drazen J, Fredberg J et al. (2004) The use and misuse of Penh in animal models of lung disease. Am J Respir Cell Mol Biol 31: 373-374. doi:10.1165/ajrcmb.31.3.1. PubMed: 15317683. (Pubitemid 39180309)
34. 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. doi:10.1254/jphs.FP0050599. PubMed: 16210776. (Pubitemid 41524454)
35. Müller T, Robaye B, Vieira RP, Ferrari D, Grimm M et al. (2010) The purinergic receptor P2Y2 receptor mediates chemotaxis of dendritic cells and eosinophils in allergic lung inflammation. Allergy 65: 1545-1553. doi:10.1111/j.1398-9995.2010.02426.x. PubMed: 20880147.
36. 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. doi:10.1182/blood-2009-05-220681. PubMed: 19641187.