Metal-Stimulated Interleukin-6 Production Through a Proton-Sensing Receptor, Ovarian Cancer G Protein-Coupled Receptor 1, in Human Bronchial Smooth Muscle Cells: A Response Inhibited by Dexamethasone

References

• Hirst SJ. Airway smooth muscle as a target in asthma. Clin Exp Allergy. 2000;30(Suppl 1):54–59. doi:10.1046/j.1365-2222.2000.00099.x
   PubMedGoogle Scholar
• Ludwig MG, Vanek M, Guerini D, et al. Proton-sensing G-protein-coupled receptors. Nature. 2003;425:93–98. doi:10.1038/nature01905
   PubMed Web of Science ®Google Scholar
• Saxena H, Deshpande DA, Tiegs BC, et al. The GPCR OGR1 (GPR68) mediates diverse signalling and contraction of airway smooth muscle in response to small reductions in extracellular pH. Br J Pharmacol. 2012;166:981–990. doi:10.1111/j.1476-5381.2011.01807.x
   PubMed Web of Science ®Google Scholar
• Nayak AP, Penn RB. The proton-sensing receptor ovarian cancer G-protein coupled receptor 1 (OGR1) in airway physiology and disease. Curr Opin Pharmacol. 2020;51:1–10. doi:10.1016/j.coph.2020.03.004
   PubMed Web of Science ®Google Scholar
• Huang XP, Karpiak J, Kroeze WK, et al. Allosteric ligands for the pharmacologically dark receptors GPR68 and GPR65. Nature. 2015;527:477–483. doi:10.1038/nature15699
   PubMed Web of Science ®Google Scholar
• Pera T, Deshpande DA, Ippolito M, et al. Biased signaling of the proton-sensing receptor OGR1 by benzodiazepines. FASEB J. 2018;32:862–874. doi:10.1096/fj.201700555R
   PubMedGoogle Scholar
• Nayak AP, Pera T, Deshpande DA, et al. Regulation of ovarian cancer G protein-coupled receptor-1 expression and signaling. Am J Physiol Lung Cell Mol Physiol. 2019;316:L894–L902. doi:10.1152/ajplung.00426.2018
   PubMed Web of Science ®Google Scholar
• 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:L567–577. doi:10.1152/ajplung.00415.2009
   PubMed Web of Science ®Google Scholar
• Kadowaki M, Yamada H, Sato K, et al. Extracellular acidification-induced CXCL8 production through a proton-sensing receptor OGR1 in human airway smooth muscle cells: a response inhibited by dexamethasone. J Inflamm (Lond). 2019;16:4. doi:10.1186/s12950-019-0207-1
   PubMed Web of Science ®Google Scholar
• Matsuzaki S, Ishizuka T, Yamada H, 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
   PubMed Web of Science ®Google Scholar
• Nakajima M, Kawaguchi M, Ota K, et al. IL-17F induces IL-6 via TAK1-NFkappaB pathway in airway smooth muscle cells. Immun Inflamm Dis. 2017;5:124–131. doi:10.1002/iid3.149
   PubMed Web of Science ®Google Scholar
• Ge Q, Moir LM, Trian T, et al. The phosphoinositide 3ʹ-kinase p110delta modulates contractile protein production and IL-6 release in human airway smooth muscle. J Cell Physiol. 2012;227:3044–3052. doi:10.1002/jcp.23046
   PubMed Web of Science ®Google Scholar
• Shan L, Redhu NS, Saleh A, et al. Thymic stromal lymphopoietin receptor-mediated IL-6 and CC/CXC chemokines expression in human airway smooth muscle cells: role of MAPKs (ERK1/2, p38, and JNK) and STAT3 pathways. J Immunol. 2010;184:7134–7143. doi:10.4049/jimmunol.0902515
   PubMed Web of Science ®Google Scholar
• Henness S, Johnson CK, Ge Q, et al. IL-17A augments TNF-alpha-induced IL-6 expression in airway smooth muscle by enhancing mRNA stability. J Allergy Clin Immunol. 2004;114:958–964. doi:10.1016/j.jaci.2004.06.023
   PubMed Web of Science ®Google Scholar
• Oltmanns U, Chung KF, Walters M, et al. Cigarette smoke induces IL-8, but inhibits eotaxin and RANTES release from airway smooth muscle. Respir Res. 2005;6:74. doi:10.1186/1465-9921-6-74
   PubMed Web of Science ®Google Scholar
• Pang L, Knox AJ. Bradykinin stimulates IL-8 production in cultured human airway smooth muscle cells: role of cyclooxygenase products. J Immunol. 1998;161:2509–2515.
   PubMed Web of Science ®Google Scholar
• Wuyts WA, Vanaudenaerde BM, Dupont LJ, et al. Interleukin-17–induced interleukin-8 release in human airway smooth muscle cells: role for mitogen-activated kinases and nuclear factor-kappaB. J Heart Lung Transplant. 2005;24:875–881. doi:10.1016/j.healun.2004.05.003
   PubMed Web of Science ®Google Scholar
• McWhinnie R, Pechkovsky DV, Zhou D, et al. Endothelin-1 induces hypertrophy and inhibits apoptosis in human airway smooth muscle cells. Am J Physiol Lung Cell Mol Physiol. 2007;292:L278–286. doi:10.1152/ajplung.00111.2006
   PubMed Web of Science ®Google Scholar
• Zhong H, Belardinelli L, Maa T, et al. A 2B adenosine receptors increase cytokine release by bronchial smooth muscle cells. Am J Respir Cell Mol Biol. 2004;30:118–125. doi:10.1165/rcmb.2003-0118OC
   PubMed Web of Science ®Google Scholar
• Lin CC, Lee IT, Yang YL, et al. Induction of COX-2/PGE(2)/IL-6 is crucial for cigarette smoke extract-induced airway inflammation: role of TLR4-dependent NADPH oxidase activation. Free Radic Biol Med. 2010;48:240–254. doi:10.1016/j.freeradbiomed.2009.10.047
   PubMed Web of Science ®Google Scholar
• Hollins F, Kaur D, Yang W, et al. Human airway smooth muscle promotes human lung mast cell survival, proliferation, and constitutive activation: cooperative roles for CADM1, stem cell factor, and IL-6. J Immunol. 2008;181:2772–2780. doi:10.4049/jimmunol.181.4.2772
   PubMed Web of Science ®Google Scholar
• Dodge IL, Carr MW, Cernadas M, et al. IL-6 production by pulmonary dendritic cells impedes Th1 immune responses. J Immunol. 2003;170:4457–4464. doi:10.4049/jimmunol.170.9.4457
   PubMed Web of Science ®Google Scholar
• Doganci A, Sauer K, Karwot R, et al. Pathological role of IL-6 in the experimental allergic bronchial asthma in mice. Clin Rev Allergy Immunol. 2005;28:257–270. doi:10.1385/CRIAI:28:3:257
   PubMed Web of Science ®Google Scholar
• Neveu WA, Allard JB, Dienz O, et al. IL-6 is required for airway mucus production induced by inhaled fungal allergens. J Immunol. 2009;183:1732–1738. doi:10.4049/jimmunol.0802923
   PubMed Web of Science ®Google Scholar
• Yokoyama A, Kohno N, Fujino S, et al. Circulating interleukin-6 levels in patients with bronchial asthma. Am J Respir Crit Care Med. 1995;151:1354–1358. doi:10.1164/ajrccm.151.5.7735584
   PubMed Web of Science ®Google Scholar
• Neveu WA, Allard JL, Raymond DM, et al. Elevation of IL-6 in the allergic asthmatic airway is independent of inflammation but associates with loss of central airway function. Respir Res. 2010;11:28. doi:10.1186/1465-9921-11-28
   PubMed Web of Science ®Google Scholar
• Zhang JG, Chen XJ, Liu T, et al. FOXP3(+) associated with the pro-inflammatory regulatory T and T helper 17 effector cells in asthma patients. Exp Ther Med. 2016;12:2753–2758. doi:10.3892/etm.2016.3662
   PubMed Web of Science ®Google Scholar
• Tillie-Leblond I, Pugin J, Marquette CH, et al. Balance between proinflammatory cytokines and their inhibitors in bronchial lavage from patients with status asthmaticus. Am J Respir Crit Care Med. 1999;159:487–494. doi:10.1164/ajrccm.159.2.9805115
   PubMed Web of Science ®Google Scholar
• Dixon AE, Shade DM, Cohen RI, et al. Effect of obesity on clinical presentation and response to treatment in asthma. J Asthma. 2006;43:553–558. doi:10.1080/02770900600859123
   PubMed Web of Science ®Google Scholar
• Virchow JC, Kroegel C, Walker C, et al. Inflammatory determinants of asthma severity: mediator and cellular changes in bronchoalveolar lavage fluid of patients with severe asthma. J Allergy Clin Immunol. 1996;98(5 Pt 2):S27–S33; discussion S33–S40. doi:10.1016/S0091-6749(96)70014-3
   PubMed Web of Science ®Google Scholar
• Bruckner HC. Extrinsic asthma in a tungsten carbide worker. J Occup Med. 1967;9:518–519. doi:10.1097/00043764-196710000-00006
   PubMedGoogle Scholar
• Weissman DN, Lewis DM. Is specific antibody determination diagnostic for asthma attributable to low-molecular-weight agents? Occup Med. 2000;15:385–398.
   PubMedGoogle Scholar
• Walters GI, Robertson AS, Moore VC, et al. Cobalt asthma in metalworkers from an automotive engine valve manufacturer. Occup Med (Lond). 2014;64:358–364. doi:10.1093/occmed/kqu043
   PubMed Web of Science ®Google Scholar
• Shirakawa T, Kusaka Y, Fujimura N, et al. Occupational asthma from cobalt sensitivity in workers exposed to hard metal dust. Chest. 1989;95:29–37. doi:10.1378/chest.95.1.29
   PubMed Web of Science ®Google Scholar
• Kusaka Y, Yokoyama K, Sera Y, et al. Respiratory diseases in hard metal workers: an occupational hygiene study in a factor. Br J Ind Med. 1986;43:474–485. doi:10.1136/oem.43.7.474
   PubMedGoogle Scholar
• Shirakawa T, Kusaka Y, Fujimura N, et al. The existence of specific antibodies to cobalt in hard metal asthma. Clin Allergy. 1988;18:451–460. doi:10.1111/j.1365-2222.1988.tb02895.x
   PubMedGoogle Scholar
• Shirakawa T, Kusaka Y, Morimoto K. Specific IgE antibodies to nickel in workers with known reactivity to cobalt. Clin Exp Allergy. 1992;22:213–218. doi:10.1111/j.1365-2222.1992.tb03075.x
   PubMed Web of Science ®Google Scholar
• Jones MG, Floyd A, Nouri-Aria KT, et al. Is occupational asthma to diisocyanates a non-IgE-mediated disease? J Allergy Clin Immunol. 2006;117:663–669. doi:10.1016/j.jaci.2005.09.053
   PubMed Web of Science ®Google Scholar
• Kusaka Y, Nakano Y, Shirakawa T, et al. Lymphocyte transformation test with cobalt in hard metal asthma. Ind Health. 1989;27:155–163. doi:10.2486/indhealth.27.155
   PubMed Web of Science ®Google Scholar
• Kusaka Y, Nakano Y, Shirakawa T, et al. Lymphocyte transformation test with nickel in hard metal asthma: another sensitizing component of hard metal. Ind Health. 1991;29:153–160. doi:10.2486/indhealth.29.153
   PubMed Web of Science ®Google Scholar
• Anees W, Huggins V, Pavord ID, et al. Occupational asthma due to low molecular weight agents: eosinophilic and non-eosinophilic variants. Thorax. 2002;57:231–236. doi:10.1136/thorax.57.3.231
   PubMed Web of Science ®Google Scholar
• Abe-Ohya R, Ishikawa T, Shiozawa H, et al. Identification of metals from osteoblastic ST-2 cell supernatants as novel OGR1 agonists. J Recept Signal Transduct Res. 2015;35:485–492. doi:10.3109/10799893.2015.1015736
   PubMed Web of Science ®Google Scholar
• Mochimaru Y, Negishi J, Murakami S, et al. Metals differentially activate ovarian cancer G protein-coupled receptor 1 in various species. Zoolog Sci. 2018;35:109–114. doi:10.2108/zs170145
   PubMed Web of Science ®Google Scholar
• Negishi J, Omori Y, Shindo M, et al. Manganese and cobalt activate zebrafish ovarian cancer G-protein-coupled receptor 1 but not GPR4. J Recept Signal Transduct Res. 2017;37:401–408. doi:10.1080/10799893.2017.1298130
   PubMed Web of Science ®Google Scholar
• Okajima F, Sho K, Kondo Y. Inhibition by islet-activating protein, pertussis toxin, of P2-purinergic receptor-mediated iodide efflux and phosphoinositide turnover in FRTL-5 cells. Endocrinology. 1988;123:1035–1043. doi:10.1210/endo-123-2-1035
   PubMed Web of Science ®Google Scholar
• Kotake M, Sato K, Mogi C, et al. Acidic pH increases cGMP accumulation through the OGR1/phospholipase C/Ca2+/neuronal NOS pathway in N1E-115 neuronal cells. Cell Signal. 2014;26:2326–2332. doi:10.1016/j.cellsig.2014.07.010
   PubMed Web of Science ®Google Scholar
• Sato K, Mogi C, Mighell AJ, et al. A missense mutation of Leu74Pro of OGR1 found in familial amelogenesis imperfecta actually causes the loss of the pH-sensing mechanism. Biochem Biophys Res Commun. 2020;526:920–926. doi:10.1016/j.bbrc.2020.04.005
   PubMed Web of Science ®Google Scholar
• Perkins ND. Post-translational modifications regulating the activity and function of the nuclear factor kappa B pathway. Oncogene. 2006;25:6717–6730. doi:10.1038/sj.onc.1209937
   PubMed Web of Science ®Google Scholar
• Tomura H, Mogi C, Sato K, et al. Proton-sensing and lysolipid-sensitive G-protein-coupled receptors: a novel type of multi-functional receptors. Cell Signal. 2005;17:1466–1476. doi:10.1016/j.cellsig.2005.06.002
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Aoki H, Mogi C, Okajima F. Ionotropic and metabotropic proton-sensing receptors involved in airway inflammation in allergic asthma. Mediat Inflamm. 2014;2014:712962. doi:10.1155/2014/712962
   PubMed Web of Science ®Google Scholar
• Aoki H, Mogi C, Hisada T, 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
   PubMed Web of Science ®Google Scholar
• Barnes PJ. Glucocorticosteroids: current and future directions. Br J Pharmacol. 2011;163:29–43. doi:10.1111/j.1476-5381.2010.01199.x
   PubMed Web of Science ®Google Scholar
• Hinks TSC, Levine SJ, Brusselle GG. Treatment options in type-2 low asthma. Eur Respir J. 2021;57:2000528. doi:10.1183/13993003.00528-2020
   PubMed Web of Science ®Google Scholar
• Damera G, Tliba O, Panettieri RA. Airway smooth muscle as an immunomodulatory cell. Pulm Pharmacol Ther. 2009;22:353–359. doi:10.1016/j.pupt.2008.12.006
   PubMed Web of Science ®Google Scholar
• Howarth PH, Knox AJ, Amrani Y, et al. Synthetic responses in airway smooth muscle. J Allergy Clin Immunol. 2004;114(2 Suppl):S32–S50. doi:10.1016/j.jaci.2004.04.041
   PubMedGoogle Scholar
• Tliba O, Panettieri RA. Noncontractile functions of airway smooth muscle cells in asthma. Annu Rev Physiol. 2009;71:509–535. doi:10.1146/annurev.physiol.010908.163227
   PubMed Web of Science ®Google Scholar
• Xia YC, Redhu NS, Moir LM, et al. Pro-inflammatory and immunomodulatory functions of airway smooth muscle: emerging concepts. Pulm Pharmacol Ther. 2013;26:64–74. doi:10.1016/j.pupt.2012.05.006
   PubMed Web of Science ®Google Scholar
• Oliver BG, Johnston SL, Baraket M, et al. Increased proinflammatory responses from asthmatic human airway smooth muscle cells in response to rhinovirus infection. Respir Res. 2006;7:71. doi:10.1186/1465-9921-7-71
   PubMed Web of Science ®Google Scholar
• Gosens R, Rieks D, Meurs H, et al. Muscarinic M3 receptor stimulation increases cigarette smoke-induced CXCL8 secretion by human airway smooth muscle cells. Eur Respir J. 2009;34:1436–1443. doi:10.1183/09031936.00045209
   PubMed Web of Science ®Google Scholar
• Iwata S, Ito S, Iwaki M, et al. Regulation of endothelin-1-induced interleukin-6 production by Ca2+ influx in human airway smooth muscle cells. Eur J Pharmacol. 2009;605:15–22. doi:10.1016/j.ejphar.2008.12.045
   PubMed Web of Science ®Google Scholar
• Berair R, Hollins F, Brightling C. Airway smooth muscle hypercontractility in asthma. J Allergy (Cairo). 2013;2013:185971. doi:10.1155/2013/185971
   PubMedGoogle Scholar
• Hudey SN, Ledford DK, Cardet JC. Mechanisms of non-type 2 asthma. Curr Opin Immunol. 2020;66:123–128. doi:10.1016/j.coi.2020.10.002
   PubMed Web of Science ®Google Scholar
• Ferreira MA, Matheson MC, Duffy DL, et al. Identification of IL6R and chromosome 11q13.5 as risk loci for asthma. Lancet. 2011;378:1006–1014. doi:10.1016/S0140-6736(11)60874-X
   PubMed Web of Science ®Google Scholar
• Ullah MA, Revez JA, Loh Z, et al. Allergen-induced IL-6 trans-signaling activates γδ T cells to promote type 2 and type 17 airway inflammation. J Allergy Clin Immunol. 2015;136:1065–1073. doi:10.1016/j.jaci.2015.02.032
   PubMed Web of Science ®Google Scholar
• Chu DK, Al-Garawi A, Llop-Guevara A, et al. Therapeutic potential of anti-IL-6 therapies for granulocytic airway inflammation in asthma. Allergy Asthma Clin Immunol. 2015;11:14. doi:10.1186/s13223-015-0081-1
   PubMed Web of Science ®Google Scholar
• Peters MC, Mauger D, Ross KR, et al. Evidence for exacerbation-prone asthma and predictive biomarkers of exacerbation frequency. Am J Respir Crit Care Med. 2020;202:973–982. doi:10.1164/rccm.201909-1813OC
   PubMed Web of Science ®Google Scholar
• Jevnikar Z, Ostling J, Ax E, et al. Epithelial IL-6 trans-signaling defines a new asthma phenotype with increased airway inflammation. J Allergy Clin Immunol. 2019;143:577–590. doi:10.1016/j.jaci.2018.05.026
   PubMed Web of Science ®Google Scholar
• Holgate ST, Peters-Golden M, Panettieri RA, et al. Roles of cysteinyl leukotrienes in airway inflammation, smooth muscle function, and remodeling. J Allergy Clin Immunol. 2003;111:S18–S34 discussion S34–S36. doi:10.1067/mai.2003.25
   Google Scholar
• Chang PJ, Bhavsar PK, Michaeloudes C, et al. Corticosteroid insensitivity of chemokine expression in airway smooth muscle of patients with severe asthma. J Allergy Clin Immunol. 2012;130:877–885.e5. doi:10.1016/j.jaci.2012.07.017
   PubMed Web of Science ®Google Scholar
• Chang PJ, Michaeloudes C, Zhu J, et al. Impaired nuclear translocation of the glucocorticoid receptor in corticosteroid-insensitive airway smooth muscle in severe asthma. Am J Respir Crit Care Med. 2015;191:54–62. doi:10.1164/rccm.201402-0314OC
   PubMed Web of Science ®Google Scholar
• Chachi L, Abbasian M, Gavrila A, et al. Protein phosphatase 5 mediates corticosteroid insensitivity in airway smooth muscle in patients with severe asthma. Allergy. 2017;72:126–136. doi:10.1111/all.13003
   PubMed Web of Science ®Google Scholar