Characterization of imidazopyridine compounds as negative allosteric modulators of proton-sensing GPR4 in extracellular acidification-induced responses

PLoS ONE

Volumn 10, Issue 6, 2015, Pages

  Tobo, Ayaka ^a   Tobo, Masayuki ^a   Nakakura, Takashi ^a   Ebara, Masashi ^a   Tomura, Hideaki ^a   Mogi, Chihiro ^a   Im, Dong Soon ^b   Murata, Naoya ^a   Kuwabara, Atsushi ^a   Ito, Saki ^c   Fukuda, Hayato ^c   Arisawa, Mitsuhiro ^c   Shuto, Satoshi ^c   Nakaya, Michio ^d   Kurose, Hitoshi ^d   Sato, Koichi ^a   Okajima, Fumikazu ^a  

^a GUNMA UNIVERSITY   (Japan)

^b Pusan National University   (South Korea)

^c HOKKAIDO UNIVERSITY   (Japan)

^d KYUSHU UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP; G PROTEIN COUPLED RECEPTOR; G PROTEIN COUPLED RECEPTOR 40; G2A RECEPTOR; IMIDAZOPYRIDINE DERIVATIVE; MESSENGER RNA; OVARIAN CANCER G PROTEIN COUPLED RECEPTOR 1; PSYCHOSINE; RHO FACTOR; T CELL DEATH ASSOCIATED GENE 8; UNCLASSIFIED DRUG; IMIDAZOLE DERIVATIVE; PROTEIN BINDING; PROTON; PYRIDINE DERIVATIVE;

ACIDIFICATION; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; HUMAN; HUMAN CELL; INTERNALIZATION; INTRACELLULAR SIGNALING; PH; PROTEIN FUNCTION; SERUM RESPONSIVE ELEMENT; ALLOSTERISM; AMINO ACID SUBSTITUTION; ANIMAL; CHEMISTRY; CHO CELL LINE; CRICETULUS; DRUG EFFECTS; GENETICS; HAMSTER; HEK293 CELL LINE; METABOLISM; UMBILICAL VEIN ENDOTHELIAL CELL;

ALLOSTERIC REGULATION; AMINO ACID SUBSTITUTION; ANIMALS; CHO CELLS; CRICETINAE; CRICETULUS; HEK293 CELLS; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; IMIDAZOLES; PROTEIN BINDING; PROTONS; PYRIDINES; RECEPTORS, G-PROTEIN-COUPLED;

EID: 84935507594     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0129334     Document Type: Article

References (45)

1. Xu Y. Sphingosylphosphorylcholine and lysophosphatidylcholine: G protein-coupled receptors and receptor-mediated signal transduction. Biochim Biophys Acta. 2002; 1582: 81-88. PMID: 12069813
2. Tomura H, Mogi C, Sato K, Okajima F. Proton-sensing and lysolipid-sensitive G-protein-coupled receptors: a novel type of multi-functional receptors. Cell Signal. 2005; 17: 1466-1476. PMID: 16014326
3. Seuwen K, Ludwig MG, Wolf RM. Receptors for protons or lipid messengers or both? J Recept Signal Transduct Res. 2006; 26: 599-610. PMID: 17118800
4. Ludwig MG, Vanek M, Guerini D, Gasser JA, Jones CE, Junker U, et al. Proton-sensing G-protein-coupled receptors. Nature. 2003; 425: 93-98. PMID: 12955148
5. Okajima F. Regulation of inflammation by extracellular acidification and proton-sensing GPCRs. Cell Signal. 2013; 25: 2263-2271. doi: 10.1016/j.cellsig.2013.07.022 PMID: 23917207
6. Wang JQ, Kon J, Mogi C, Tobo M, Damirin A, Sato K, et al. TDAG8 is a proton-sensing and psychosine-sensitive G-protein-coupled receptor. J Biol Chem. 2004; 279: 45626-45633. PMID: 15326175
7. Liu JP, Nakakura T, Tomura H, Tobo M, Mogi C, Damirin A, et al. 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. 2010; 61: 499-505. doi: 10.1016/j.phrs.2010.02.013 PMID: 20211729
8. Murakami N, Yokomizo T, Okuno T, Shimizu T. G2A is a proton-sensing G-protein-coupled receptor antagonized by lysophosphatidylcholine. J Biol Chem. 2004; 279: 42484-42491. PMID: 15280385
9. Radu CG, Nijagal A, McLaughlin J, Wang L, Witte ON. 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. 2005; 102: 1632-1637. PMID: 15665078
10. Kabarowski JH. G2A and LPC: regulatory functions in immunity. Prostaglandins Other Lipid Mediat. 2009; 89: 73-81. doi: 10.1016/j.prostaglandins.2009.04.007 PMID: 19383550
11. Obinata H, Izumi T. G2A as a receptor for oxidized free fatty acids. Prostaglandins Other Lipid Mediat. 2009; 89: 66-72. doi: 10.1016/j.prostaglandins.2008.11.002 PMID: 19063986
12. Lardner A. The effects of extracellular pH on immune function. J Leukoc Biol. 2001; 69: 522-530. PMID: 11310837
13. Justus CR, Dong L, Yang LV. Acidic tumor microenvironment and pH-sensing G protein-coupled receptors. Front Physiol. 2014; 4: 354.
14. Aoki H, Mogi C, Okajima F. Ionotropic and metabotropic proton-sensing receptors involved in airway inflammation in allergic asthma. Mediators Inflamm. 2014; 2014: 712962. doi: 10.1155/2014/712962 PMID: 25197168
15. Tomura H, Wang JQ, Liu JP, Komachi M, Damirin A, Mogi C, et al. Cyclooxygenase-2 expression and prostaglandin E2 production in response to acidic pH through OGR1 in a human osteoblastic cell line. J Bone Miner Res. 2008; 23: 1129-1139. doi: 10.1359/jbmr.080236 PMID: 18302504
16. Tomura H, Wang JQ, Komachi M, Damirin A, Mogi C, Tobo 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. PMID: 16087674
17. Liu JP, Komachi M, Tomura H, Mogi C, Damirin A, Tobo M, et al. 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. 2010; 299: H731-742. doi: 10.1152/ajpheart.00977.2009 PMID: 20622109
18. Ichimonji I, Tomura H, Mogi C, Sato K, Aoki H, Hisada T, et al. 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. 2010; 299: L567-577. doi: 10.1152/ajplung.00415.2009 PMID: 20656891
19. Matsuzaki S, Ishizuka T, Yamada H, Kamide Y, Hisada T, Ichimonji I, et al. Extracellular acidification induces connective tissue growth factor production through proton-sensing receptor OGR1 in human airway smooth muscle cells. Biochem Biophys Res Commun. 2011; 413: 499-503. doi: 10.1016/j.bbrc.2011.08.087 PMID: 21907704
20. Aoki H, Mogi C, Hisada T, Nakakura T, Kamide Y, Ichimonji I, et al. Proton-sensing ovarian cancer G protein-coupled receptor 1 on dendritic cells is required for airway responses in a murine asthma model. PLoS One. 2013; 8: e79985. doi: 10.1371/journal.pone.0079985 PMID: 24244587
21. Chen A, Dong L, Leffler NR, Asch AS, Witte ON, Yang LV. Activation of GPR4 by acidosis increases endothelial cell adhesion through the cAMP/Epac pathway. PLoS One. 2011; 6: e27586. doi: 10.1371/journal.pone.0027586 PMID: 22110680
22. Dong L, Li Z, Leffler NR, Asch AS, Chi JT, Yang LV. Acidosis activation of the proton-sensing GPR4 receptor stimulates vascular endothelial cell inflammatory responses revealed by transcriptome analysis. PLoS One. 2013; 8: e61991. doi: 10.1371/journal.pone.0061991 PMID: 23613998
23. Saki M, Nonaka H, Miyaji H, Takahashi C, Manabe H, Hiura N, et al. Preventive and/or therapeutic agent for neutrophil inflammation disease. International patent application No. PCT/JP2004/005930 or international patent publication 2004; No. WO2004/093912 A1, pp. 1-156.
24. Taracido IC, Harrington EM, Hersperger R, Lattmann R, Miltz W, Weigand K. Imidazo pyridine dereivatives. United States patent application 2009; No. 12/468,706, pp.1-50.
25. Fukunaga S, Setoguchi S, Hirasawa A, Tsujimoto G. Monitoring ligand-mediated internalization of G protein-coupled receptor as a novel pharmacological approach. Life Sci. 2006; 80: 17-23. PMID: 16978657
26. Tobo M, Tomura H, Mogi C, Wang JQ, Liu JP, Komachi M, et al. Previously postulated "ligand-independent" signaling of GPR4 is mediated through proton-sensing mechanisms. Cell Signal. 2007; 19: 1745-1753. PMID: 17462861
27. KimuraT. Saki M Nonaka H Miyaji H Takahashi C Manabe H Hiura Net alPreventive And/or Therapeutic Agent for Neutrophil Inflammation DiseaseInternational patent application No. PCT/JP2004/005930 or international patent publication, WO20042004093912A11-156
28. SatoK., KuwabaraA., TomuraH., IshiwaraM., KobayashiI., et al. Sphingosine 1-phosphate may be a major component of plasma lipoproteins responsible for the cytoprotective actions in human umbilical vein endothelial cells.J Biol Chem2001; 276: 31780-31785. PMID: 11427538
29. Kotake M, Sato K, Mogi C, Tobo M, Aoki H, Ishizuka T, et al. Acidic pH increases cGMP accumulation through the OGR1/phospholipase C/Ca(2+)/neuronal NOS pathway in N1E-115 neuronal cells. Cell Signal. 2014; 26: 2326-2332. doi: 10.1016/j.cellsig.2014.07.010 PMID: 25025574
30. Kimura T, Tomura H, Sato K, Ito M, Matsuoka I, Im DS, et al. Mechanism and role of high density lipoprotein-induced activation of AMP-activated protein kinase in endothelial cells. J Biol Chem. 2010; 285: 4387-4397. doi: 10.1074/jbc.M109.043869 PMID: 20018878
31. Jin Y, Sato K, Tobo A, Mogi C, Tobo M, Murata N, et al. Inhibition of interleukin-1beta production by extracellular acidification through the TDAG8/cAMP pathway in mouse microglia. J Neurochem. 2014; 129: 683-695. doi: 10.1111/jnc.12661 PMID: 24447140
32. Shukla AK, Xiao K, Lefkowitz RJ. Emerging paradigms of beta-arrestin-dependent seven transmembrane receptor signaling. Trends Biochem Sci. 2011; 36: 457-469. doi: 10.1016/j.tibs.2011.06.003 PMID: 21764321
33. Suzuki K. Twenty five years of the "psychosine hypothesis": a personal perspective of its history and present status. Neurochem Res. 1998; 23: 251-259. PMID: 9482237
34. Kanazawa T, Nakamura S, Momoi M, Yamaji T, Takematsu H, Yano H, et al. Inhibition of cytokinesis by a lipid metabolite, psychosine. J Cell Biol. 2000; 149: 943-950. PMID: 10811833
35. Li Y, Sands MS. Experimental Therapies in the Murine Model of Globoid Cell Leukodystrophy. Pediatr Neurol. 2014; 51: 600-606. doi: 10.1016/j.pediatrneurol.2014.08.003 PMID: 25240259
36. Voccoli V, Tonazzini I, Signore G, Caleo M, Cecchini M. Role of extracellular calcium and mitochondrial oxygen species in psychosine-induced oligodendrocyte cell death. Cell Death Dis. 2014; 5: e1529. doi: 10.1038/cddis.2014.483 PMID: 25412308
37. Mogi C, Tomura H, Tobo M, Wang JQ, Damirin A, Kon J, 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. PMID: 16210776
38. Im DS, Heise CE, Nguyen T, O'Dowd BF, Lynch KR. Identification of a molecular target of psychosine and its role in globoid cell formation. J Cell Biol. 2001; 153: 429-434. PMID: 11309421
39. Engers DW, Lindsley CW. Allosteric modulation of Class C GPCRs: a novel approach for the treatment of CNS disorders. Drug Discov Today Technol. 2014; 10: e269-276.
40. Bernat V, Admas TH, Brox R, Heinemann FW, Tschammer N. Boronic acids as probes for investigation of allosteric modulation of the chemokine receptor CXCR3. ACS Chem Biol. 2014; 9: 2664-2677. doi: 10.1021/cb500678c PMID: 25233453
41. Roettger BF, Ghanekar D, Rao R, Toledo C, Yingling J, Pinon D, et al. Antagonist-stimulated internalization of the G protein-coupled cholecystokinin receptor. Mol Pharmacol. 1997; 51: 357-362. PMID: 9058588
42. Bhowmick N, Narayan P, Puett D. The endothelin subtype A receptor undergoes agonist- and antagonist-mediated internalization in the absence of signaling. Endocrinology. 1998; 139: 3185-3192. PMID: 9645692
43. Pfeiffer R, Kirsch J, Fahrenholz F. Agonist and antagonist-dependent internalization of the human vasopressin V2 receptor. Exp Cell Res. 1998; 244: 327-339. PMID: 9770376
44. Willins DL, Alsayegh L, Berry SA, Backstrom JR, Sanders-Bush E, Friedman L, et al. Serotonergic antagonist effects on trafficking of serotonin 5-HT2A receptors in vitro and in vivo. Ann N Y Acad Sci. 1998; 861: 121-127. PMID: 9928248
45. Navarro A, Zapata R, Canela EI, Mallol J, Lluis C, Franco R. Epidermal growth factor (EGF)-induced up-regulation and agonist- and antagonist-induced desensitization and internalization of A1 adenosine receptors in a pituitary-derived cell line. Brain Res. 1999; 816: 47-57. PMID: 9878686