Acid-sensing ion channel 3 decreases phosphorylation of extracellular signal-regulated kinases and induces synoviocyte cell death by increasing intracellular calcium

Arthritis Research and Therapy

Volumn 16, Issue 3, 2014, Pages

  Gong, Weiyi ^a,b   Kolker, Sandra J ^b   Usachev, Yuriy ^b   Walder, Roxanne Y ^b   Boyle, David L ^c   Firestein, Gary S ^c   Sluka, Kathleen A ^b  

^a FUJIAN MEDICAL UNIVERSITY   (China)

^b UNIVERSITY OF IOWA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; ACID SENSING ION CHANNEL; ACID SENSING ION CHANNEL 1; ACID SENSING ION CHANNEL 3; CALCIUM; COLLAGENASE 3; INTERLEUKIN 1BETA; INTERLEUKIN 6; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHOPROTEIN PHOSPHATASE 2A; STROMELYSIN; UNCLASSIFIED DRUG; ACCN3 PROTEIN, MOUSE; MATRIX METALLOPROTEINASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CALCIUM CELL LEVEL; CELL ASSAY; CELL DEATH; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; FIBROBLAST LIKE SYNOVIOCYTE; FLUORESCENCE IMAGING; GENE EXPRESSION; INFLAMMATION; LIVE DEAD ASSAY; MALE; MOUSE; NONHUMAN; PH; PROTEIN EXPRESSION; PROTEIN FUNCTION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RHEUMATOID ARTHRITIS; SYNOVIOCYTE; WESTERN BLOTTING; ANIMAL; C57BL MOUSE; CELL CULTURE; CYTOLOGY; DRUG EFFECTS; GENETICS; HUMAN; INTRACELLULAR SPACE; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; PHOSPHORYLATION; SYNOVIUM;

ACID SENSING ION CHANNELS; ANIMALS; ARTHRITIS, RHEUMATOID; BLOTTING, WESTERN; CALCIUM; CELL DEATH; CELLS, CULTURED; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GENE EXPRESSION; HUMANS; HYDROGEN-ION CONCENTRATION; INTERLEUKIN-1BETA; INTERLEUKIN-6; INTRACELLULAR SPACE; MALE; MATRIX METALLOPROTEINASES; MICE, INBRED C57BL; MICE, KNOCKOUT; PHOSPHORYLATION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SYNOVIAL MEMBRANE;

EID: 84904269909     PISSN: 14786354     EISSN: 14786362     Source Type: Journal    
DOI: 10.1186/ar4577     Document Type: Article

References (45)

1. Sluka KA, Rasmussen LA, Edgar MM, O'Donnel JM, Walder RY, Kolker SJ, Boyle DL, Firestein GS. Acid sensing ion channel 3 deficiency increases inflammation but decreases pain behavior in arthritis. Arthritis Rheum 2013, 65:1194-1202.
2. Walder RY, Gautam M, Wilson SP, Benson CJ, Sluka KA. Selective Targeting of ASIC3 using miRNAs inhibits primary and secondary hyperalgesia following muscle inflammation. Pain 2011, 152:2348-2356.
3. Walder RY, Rasmussen LA, Rainier JD, Light AR, Wemmie JA, Sluka KA. ASIC1 and ASIC3 play different roles in the development of hyperalgesia after inflammatory muscle injury. J Pain 2010, 11:210-218.
4. Ikeuchi M, Kolker SJ, Sluka KA. Acid-sensing ion channel 3 expression in mouse knee joint afferents and effects of carrageenan-induced arthritis. J Pain 2009, 10:336-342.
5. Sluka KA, Winter OC, Wemmie JA. Acid-sensing ion channels: A new target for pain and CNS diseases. Curr Opin Drug Discov Devel 2009, 12:693-704.
6. Ikeuchi M, Kolker SJ, Burnes LA, Walder RY, Sluka KA. Role of ASIC3 in the primary and secondary hyperalgesia produced by joint inflammation in mice. Pain 2008, 137:662-669.
7. Sluka KA, Radhakrishnan R, Benson CJ, Eshcol JO, Price MP, Babinski K, Audette KM, Yeomans DC, Wilson SP. ASIC3 in muscle mediates mechanical, but not heat, hyperalgesia associated with muscle inflammation. Pain 2007, 129:102-112.
8. Sluka KA, Price MP, Breese NM, Stucky CL, Wemmie JA, Welsh MJ. Chronic hyperalgesia induced by repeated acid injections in muscle is abolished by the loss of ASIC3, but not ASIC1. Pain 2003, 106:229-239.
9. Kolker SJ, Walder RY, Usachev Y, Hillman J, Boyle DL, Firestein GS, Sluka KA. ASIC3 expressed in Type B synoviocytes and chondrocytes modulates hyaluronan expression and release. Ann Rheum Dis 2010, 69:903-909.
10. Goldie I, Nachemson A. Synovial pH in rheumatoid knee joints. II. The effect of local corticosteroid treatment. Acta Orthop Scand 1970, 41:354-362.
11. Goldie I, Nachemson A. Synovial pH in rheumatoid knee-joints. I. The effect of synovectomy. Acta Orthop Scand 1969, 40:634-641.
12. Waldmann R, Champigny G, Lingueglia E, De Weille JR, Heurteaux C, Lazdunski M. H(+)-gated cation channels. Ann NY Acad Sci 1999, 868:67-76.
13. McNearney T, Baethge BA, Cao S, Alam R, Lisse JR, Westlund KN. Excitatory amino acids, TNF-alpha, and chemokine levels in synovial fluids of patients with active arthropathies. Clin Exp Immunol 2004, 137:621-627.
14. Houssiau FA, Devogelaer JP, Van DJ, de Deuxchaisnes CN, Van SJ. Interleukin-6 in synovial fluid and serum of patients with rheumatoid arthritis and other inflammatory arthritides. Arthritis Rheum 1988, 31:784-788.
15. Kaneko S, Satoh T, Chiba J, Ju C, Inoue K, Kagawa J. Interleukin-6 and interleukin-8 levels in serum and synovial fluid of patients with osteoarthritis. Cytokines Cell Mol Ther 2000, 6:71-79.
16. Sweeney SE, Firestein GS. Rheumatoid arthritis: regulation of synovial inflammation. Int J Biochem Cell Biol 2004, 36:372-378.
17. Inoue T, Boyle DL, Corr M, Hammaker D, Davis RJ, Flavell RA, Firestein GS. Mitogen-activated protein kinase kinase 3 is a pivotal pathway regulating p38 activation in inflammatory arthritis. Proc Natl Acad Sci U S A 2006, 103:5484-5489.
18. Han Z, Boyle DL, Chang L, Bennett B, Karin M, Yang L, Manning AM, Firestein GS. c-Jun N-terminal kinase is required for metalloproteinase expression and joint destruction in inflammatory arthritis. J Clin Invest 2001, 108:73-81.
19. Han Z, Chang L, Yamanishi Y, Karin M, Firestein GS. Joint damage and inflammation in c-Jun N-terminal kinase 2 knockout mice with passive murine collagen-induced arthritis. Arthritis Rheum 2002, 46:818-823.
20. Sweeney SE, Firestein GS. Signal transduction in rheumatoid arthritis. Curr Opin Rheumatol 2004, 16:231-237.
21. Han Z, Boyle DL, Aupperle KR, Bennett B, Manning AM, Firestein GS. Jun N-terminal kinase in rheumatoid arthritis. J Pharmacol Exp Ther 1999, 291:124-130.
22. Cha HS, Boyle DL, Inoue T, Schoot R, Tak PP, Pine P, Firestein GS. A novel spleen tyrosine kinase inhibitor blocks c-Jun N-terminal kinase-mediated gene expression in synoviocytes. J Pharmacol Exp Ther 2006, 317:571-578.
23. Hayashi S, Nishiyama T, Miura Y, Fujishiro T, Kanzaki N, Hashimoto S, Matsumoto T, Kurosaka M, Kuroda R. DcR3 induces cell proliferation through MAPK signaling in chondrocytes of osteoarthritis. Osteoarthritis Cartilage 2011, 19:903-910.
24. Philpott KL, Facci L. MAP kinase pathways in neuronal cell death. CNS Neurol Disord Drug Targets 2008, 7:83-97.
25. Asim M, Chaturvedi R, Hoge S, Lewis ND, Singh K, Barry DP, Algood HS, de Sablet T, Gobert AP, Wilson KT. Helicobacter pylori induces ERK-dependent formation of a phospho-c-Fos c-Jun activator protein-1 complex that causes apoptosis in macrophages. J Biol Chem 2010, 285:20343-20357.
26. Hahm ER, Lee J, Singh SV. Role of mitogen-activated protein kinases and Mcl-1 in apoptosis induction by withaferin A in human breast cancer cells. Mol Carcinog 2013, doi:10.1002/mc.22050.
27. Liu WH, Chang LS. Caffeine induces matrix metalloproteinase-2 (MMP-2) and MMP-9 down-regulation in human leukemia U937 cells via Ca2+/ROS-mediated suppression of ERK/c-fos pathway and activation of p38 MAPK/c-jun pathway. J Cell Physiol 2010, 224:775-785.
28. Price MP, McIlwrath SL, Xie J, Cheng C, Qiao J, Tarr DE, Sluka KA, Brennan TJ, Lewin GR, Welsh MJ. The DRASIC Cation Channel contributes to the detection of cutaneous touch and acid stimuli in mice. Neuron 2001, 32:1071-1083.
29. Wemmie JA, Chen J, Askwith CC, Hruska-Hageman AM, Price MP, Nolan BC, Yoder PG, Lamani E, Hoshi T, Freeman JH, Welsh MJ. The acid-activated ion channel ASIC contributes to synaptic plasticity, learning, and memory. Neuron 2002, 34:463-477.
30. Eshcol JO, Harding AM, Hattori T, Costa V, Welsh MJ, Benson CJ. Acid-sensing ion channel 3 (ASIC3) cell surface expression is modulated by PSD-95 within lipid rafts. Am J Physiol Cell Physiol 2008, 295:C732-C739.
31. Boyle DL, Rosengren S, Bugbee W, Kavanaugh A, Firestein GS. Quantitative biomarker analysis of synovial gene expression by real-time PCR. Arthritis Res Ther 2003, 5:R352-R360.
32. Voilley N, de Weille J, Mamet J, Lazdunski M. Nonsteroid anti-inflammatory drugs inhibit both the activity and the inflammation-induced expression of acid-sensing ion channels in nociceptors. J Neurosci 2001, 21:8026-8033.
33. Mamet J, Baron A, Lazdunski M, Voilley N. Proinflammatory mediators, stimulators of sensory neuron excitability via the expression of acid-sensing ion channels. J Neurosci 2002, 22:10662-10670.
34. Kochukov MY, McNearney TA, Fu Y, Westlund KN. Thermosensitive TRP ion channels mediate cytosolic calcium response in human synoviocytes. Am J Physiol Cell Physiol 2006, 291:C424-C432.
35. Hu F, Sun WW, Zhao XT, Cui ZJ, Yang WX. TRPV1 mediates cell death in rat synovial fibroblasts through calcium entry-dependent ROS production and mitochondrial depolarization. Biochem Biophys Res Commun 2008, 369:989-993.
36. Hu F, Yang S, Zhao D, Zhu S, Wang Y, Li J. Moderate extracellular acidification inhibits capsaicin-induced cell death through regulating calcium mobilization, NF-kappaB translocation and ROS production in synoviocytes. Biochem Biophys Res Commun 2012, 424:196-200.
37. Waldmann R, Lazdunski M. H(+)-gated cation channels: neuronal acid sensors in the NaC/DEG family of ion channels. Curr Opin Neurobiol 1998, 8:418-424.
38. Caterina MJ, Leffler A, Tominaga M, Rosen TA, Levine JD, Julius D. The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 1997, 389:816-824.
39. Tominaga M, Caterina MJ, Malmberg AB, Rosen TA, Gilbert H, Skinner K, Raumann BE, Basbaum AI, Julius D. The cloned capsaicin receptor integrates multiple pain-producing stimuli. Neuron 1998, 21:531-543.
40. Christensen BN, Kochukov M, McNearney TA, Taglialatela G, Westlund KN. Proton-sensing G protein-coupled receptor mobilizes calcium in human synovial cells. Am J Physiol Cell Physiol 2005, 289:C601-C608.
41. Christodoulou C, Choy EH. Joint inflammation and cytokine inhibition in rheumatoid arthritis. Clin Exp Med 2006, 6:13-19.
42. Yi JK, Kim HJ, Yu DH, Park SJ, Shin MJ, Yuh HS, Bae KB, Ji YR, Kim NR, Park SJ, Kim JY, Lee HS, Lee SG, Yoon du H, Hyun BH, Kim WU, Ryoo ZY. Regulation of inflammatory responses and fibroblast-like synoviocyte apoptosis by calcineurin-binding protein 1 in mice with collagen-induced arthritis. Arthritis Rheum 2012, 64:2191-2200.
43. Lee SS, Joo YS, Kim WU, Min DJ, Min JK, Park SH, Cho CS, Kim HY. Vascular endothelial growth factor levels in the serum and synovial fluid of patients with rheumatoid arthritis. Clin Exp Rheumatol 2001, 19:321-324.
44. Kong JS, Yoo SA, Kim JW, Yang SP, Chae CB, Tarallo V, De Falco S, Ryu SH, Cho CS, Kim WU. Anti-neuropilin-1 peptide inhibition of synoviocyte survival, angiogenesis, and experimental arthritis. Arthritis Rheum 2010, 62:179-190.
45. Kim WU, Kang SS, Yoo SA, Hong KH, Bae DG, Lee MS, Hong SW, Chae CB, Cho CS. Interaction of vascular endothelial growth factor 165 with neuropilin-1 protects rheumatoid synoviocytes from apoptotic death by regulating Bcl-2 expression and Bax translocation. J Immunol 2006, 177:5727-5735.