The CO donor CORM-2 inhibits LPS-induced vascular cell adhesion molecule-1 expression and leukocyte adhesion in human rheumatoid synovial fibroblasts

British Journal of Pharmacology

Volumn 171, Issue 12, 2014, Pages 2993-3009

  Chi, Pei Ling ^a   Chuang, Yu Chen ^a   Chen, Yu Wen ^a   Lin, Chih Chung ^b   Hsiao, Li Der ^a   Yang, Chuen Mao ^a  

^a CHANG GUNG UNIVERSITY COLLEGE OF MEDICINE   (Taiwan)

^b CHANG GUNG UNIVERSITY   (Taiwan)

Author keywords

carbon monoxide; leukocyte adhesion; LPS; VCAM 1

Indexed keywords

CARBON MONOXIDE; CARBONYL DERIVATIVE; CORM 2; DIMER; DNA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LIPOPOLYSACCHARIDE; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; MYELOID DIFFERENTIATION FACTOR 88; PROTEIN TYROSINE KINASE; RUTHENIUM COMPLEX; TOLL LIKE RECEPTOR 4; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR AP 1; TRANSCRIPTION FACTOR RELA; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 6; UNCLASSIFIED DRUG; VASCULAR CELL ADHESION MOLECULE 1; ANTIRHEUMATIC AGENT; MYD88 PROTEIN, HUMAN; ORGANOMETALLIC COMPOUND; RELA PROTEIN, HUMAN; TLR4 PROTEIN, HUMAN; TRICARBONYLDICHLORORUTHENIUM (II) DIMER;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL INFILTRATION; CHROMATIN IMMUNOPRECIPITATION; COMPLEX FORMATION; CONTROLLED STUDY; DOWN REGULATION; FIBROBLAST; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNOCOMPETENT CELL; IMMUNOHISTOCHEMISTRY; INFLAMMATION; LEUKOCYTE ADHERENCE; MOUSE; NONHUMAN; ONCOGENE C FOS; ONCOGENE C JUN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DNA BINDING; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RHEUMATOID ARTHRITIS; SYNOVIUM; ANIMAL; BINDING SITE; CELL ADHESION; CELL CULTURE; COCULTURE; DRUG EFFECTS; ENZYME ACTIVATION; GENETICS; INSTITUTE FOR CANCER RESEARCH MOUSE; LEUKOCYTE; METABOLISM; PATHOLOGY; PHOSPHORYLATION; SIGNAL TRANSDUCTION; TIME;

ANIMALS; ANTIRHEUMATIC AGENTS; ARTHRITIS, RHEUMATOID; BINDING SITES; CARBON MONOXIDE; CELL ADHESION; CELLS, CULTURED; COCULTURE TECHNIQUES; DOWN-REGULATION; ENZYME ACTIVATION; FIBROBLASTS; HUMANS; LEUKOCYTES; LIPOPOLYSACCHARIDES; MICE, INBRED ICR; MITOGEN-ACTIVATED PROTEIN KINASES; MYELOID DIFFERENTIATION FACTOR 88; ORGANOMETALLIC COMPOUNDS; PHOSPHORYLATION; PROMOTER REGIONS, GENETIC; SIGNAL TRANSDUCTION; SRC-FAMILY KINASES; SYNOVIAL MEMBRANE; TIME FACTORS; TNF RECEPTOR-ASSOCIATED FACTOR 6; TOLL-LIKE RECEPTOR 4; TRANSCRIPTION FACTOR AP-1; TRANSCRIPTION FACTOR RELA; VASCULAR CELL ADHESION MOLECULE-1;

EID: 84901412712     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/bph.12680     Document Type: Article

References (64)

1. Akira S, Takeda K, (2004). Toll-like receptor signaling. Nat Rev Immunol 4: 499-511.
2. Alexander SPH, Benson HE, Faccenda E, Pawson AJ, Sharman JL, Spedding M, et al (2013). The Concise Guide to PHARMACOLOGY 2013/14: Catalytic Receptors. Br J Pharmacol 170, 1676-1705.
3. Basta G, Lazzerini G, Del TS, Ratto GM, Schmidt AM, De CR, (2005). At least 2 distinct pathways generating reactive oxygen species mediate vascular cell adhesion molecule-1 induction by advanced glycation end products. Arterioscler Thromb Vasc Biol 25: 1401-1407.
4. Carpenter S, O'Neill LA, (2009). Recent insights into the structure of Toll-like receptors and post-translational modifications of their associated signaling proteins. Biochem J 422: 1-10.
5. Carter RA, Wicks IP, (2001). Vascular cell adhesion molecule 1 (CD106): a multifaceted regulator of joint inflammation. Arthritis Rheum 44: 985-994.
6. Carter RA, Campbell KI, O'Donnel KL, Wicks IP, (2002). Vascular cell adhesion molecule-1 (VCAM-1) blockade in collagen-induced arthritis reduces joint involvement and alters B cell trafficking. Clin Exp Immunol 128: 44-51.
7. Cheng SE, Lee IT, Lin CC, Kou YR, Yang CM, (2010). Cigarette smoke particle-phase extract induces HO-1 expression in human tracheal smooth muscle cells: role of the c-Src/NADPH oxidase/MAPK/Nrf2 signaling pathway. Free Radic Biol Med 48: 1410-1422.
8. Chi PL, Luo SF, Hsieh HL, Lee IT, Hsiao LD, Chen YL, et al. (2011). cPLA2 induction by IL-1β via the MyD88-dependent and cooperation of p300, Akt, and NF-κB pathway in human rheumatoid arthritis synovial fibroblasts. Arthritis Rheum 63: 2905-2917.
9. Choi BM, Pae HO, Kim YM, Chung HT, (2003). Nitric oxide-mediated cytoprotection of hepatocytes from glucose deprivation-induced cytotoxicity: involvement of heme oxygenase-1. Hepatology 37: 810-823.
10. Collins T, Read MA, Neish AS, Whitley MZ, Thanos D, Maniatis T, (1995). Transcriptional regulation of endothelial cell adhesion molecules: NF-κB and cytokine-inducible enhancers. FASEB J 9: 899-909.
11. Conde de la Rosa L, Vrenken TE, Hannivoort RA, Buist-Homana M, Havingaa R, Slebosb DJ, et al. (2008). Carbon monoxide blocks oxidative stress-induced hepatocyte apoptosis via inhibition of the p54 JNK isoform. Free Radic Biol Med 44: 1323-1333.
12. Fernandez-Pisonero I, Duenas AI, Barreiro O, Montero O, Sanchez-Madrid F, Garcia-Rodriguez G, (2012). Lipopolysaccharide and sphingosine-1-phosphate cooperate to induce inflammatory molecules and leukocyte adhesion in endothelial cells. J Immunol 189: 5402-5410.
13. Funakoshi-Tago M, Tago K, Sonoda Y, Tominaga S, Kasahara T, (2003). TRAF6 and C-SRC induce synergistic AP-1 activation via PI3-kinase-AKT-JNK pathway. Eur J Biochem 270: 1257-1268.
14. Garcia-Arnandis I, Guillen MI, Gomar F, Castejon MA, Alcaraz MJ, (2011). Control of cell migration and inflammatory mediators production by CORM-2 in osteoarthritic synoviocytes. PLoS ONE 6: e24591.
15. Gobert AP, Verriere T, de Sablet T, Peek RM Jr, Chaturvedi R, Wilson KT, (2013). Haem oxygenase-1 inhibits phosphorylation of the Helicobacter pylori oncoprotein CagA in gastric epithelial cells. Cell Microbiol 15: 145-156.
16. Higashiyama H, Saito I, Hayashi Y, Miyasaka N, (1995). In situ hybridization study of vascular cell adhesion molecule-1 messenger RNA expression in rheumatoid synovium. J Autoimmun 8: 947-957.
17. Iademarco MF, McQuillan JJ, Rosen GD, Dean DC, (1992). Characterization of the promoter for vascular cell adhesion molecule-1 (VCAM-1). J Biol Chem 267: 16323-16329.
18. Kaizu T, Nakao A, Tsung A, Toyokawa H, Sahai R, Geller DA, et al. (2005). Carbon monoxide inhalation ameliorates cold ischemia/reperfusion injury after rat liver transplantation. Surgery 138: 229-235.
19. Kilkenny C, Browne W, Cuthill IC, Emerson M, Altman DG, (2010). Animal research: Reporting in vivo experiments: the ARRIVE guidelines. Br J Pharmacol 160: 1577-1579.
20. Kim H, Jung Y, Shin BS, Kim H, Song H, Bae SH, et al. (2010). Redox regulation of lipopolysaccharide-mediated sulfiredoxin induction, which depends on both AP-1 and Nrf2. J Biol Chem 285: 34419-34428.
21. Kobayashi S, Momohara S, Kamatani N, Okamoto H, (2008). Molecular aspects of rheumatoid arthritis: role of environmental factors. FEBS J 275: 4456-4462.
22. Lee IT, Wang SW, Lee CW, Chang CC, Lin CC, Luo SF, et al. (2008). Lipoteichoic acid induces HO-1 expression via the TLR2/MyD88/c-Src/NADPH oxidase pathway and Nrf2 in human tracheal smooth muscle cells. J Immunol 181: 5098-5110.
23. Lee IT, Luo SF, Lee CW, Wang SW, Lin CC, Chang CC, et al. (2009). Overexpression of HO-1 protects against TNF-α-mediated airway inflammation by down-regulation of TNFR1-dependent oxidative stress. Am J Pathol 175: 519-532.s
24. Lee IT, Shih RH, Lin CC, Chen JT, Yang CM, (2012). Role of TLR4/NADPH oxidase/ROS-activated p38 MAPK in VCAM-1 expression induced by lipopolysaccharide in human renal mesangial cells. Cell Commun Signal 10: 33.
25. Lee TS, Chau LY, (2002). Heme oxygenase-1 mediates the anti-inflammatory effect of interleukin-10 in mice. Nat Med 8: 240-246.
26. Lin CC, Lee IT, Yang YL, Lee CW, Kou YR, Yang CM, (2010). 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 48: 240-254.
27. Lin CW, Shen SC, Hou WC, Yang LY, Chen YC, (2008a). Heme oxygenase-1 inhibits breast cancer invasion via suppressing the expression of matrix metalloproteinase-9. Mol Cancer Ther 7: 1195-1206.
28. Lin WN, Luo SF, Lee CW, Wang CC, Wang JS, Yang CM, (2007). Involvement of MAPKs and NF-κB in LPS-induced VCAM-1 expression in human tracheal smooth muscle cells. Cell Signal 19: 1258-1267.
29. Lin WN, Luo SF, Wu CB, Lin CC, Yang CM, (2008b). Lipopolysaccharide induces VCAM-1 expression and neutrophil adhesion to human tracheal smooth muscle cells: involvement of Src/EGFR/PI3-K/Akt pathway. Toxicol Appl Pharmacol 228: 256-268.
30. Lin WN, Luo SF, Lin CC, Hsiao LD, Yang CM, (2009). Differential involvement of PKC-dependent MAPKs activation in lipopolysaccharide-induced AP-1 expression in human tracheal smooth muscle cells. Cell Signal 21: 1385-1395.
31. Luo SF, Fang RY, Hsieh HL, Chi PL, Lin CC, Hsiao LD, et al. (2010). Involvement of MAPKs and NF-κB in tumor necrosis factor alpha-induced vascular cell adhesion molecule 1 expression in human rheumatoid arthritis synovial fibroblasts. Arthritis Rheum 62: 105-116.
32. Lyss G, Knorre A, Schmidt TJ, Pahl HL, Merfort I, (1998). The anti-inflammatory sesquiterpene lactone helenalin inhibits the transcription factor NF-κB by directly targeting p65. J Biol Chem 273: 33508-33516.
33. McGrath J, Drummond G, McLachlan E, Kilkenny C, Wainwright C, (2010). Guidelines for reporting experiments involving animals: the ARRIVE guidelines. Br J Pharmacol 160: 1573-1576.
34. McMurray RW, (1996). Adhesion molecules in autoimmune disease. Semin Arthritis Rheum 25: 215-233.
35. Megias J, Busserolles J, Alcaraz MJ, (2007). The carbon monoxide-releasing molecule CORM-2 inhibits the inflammatory response induced by cytokines in Caco-2 cells. Br J Pharmacol 150: 977-986.
36. Morel JC, Park CC, Zhu K, Kumar P, Ruth JH, Koch AE, (2002). Signal transduction pathways involved in rheumatoid arthritis synovial fibroblast interleukin-18-induced vascular cell adhesion molecule-1 expression. J Biol Chem 277: 34679-34691.
37. Morse D, Pischke SE, Zhou Z, Davis RJ, Flavell RA, Loop T, et al. (2003). Suppression of inflammatory cytokine production by carbon monoxide involves the JNK pathway and AP-1. J Biol Chem 278: 36993-36998.
38. Motterlini R, (2007). Carbon monoxide-releasing molecules (CO-RMs): vasodilatory, anti-ischaemic and anti-inflammatory activities. Biochem Soc Trans 35: 1142-1146.
39. Motterlini R, Otterbein LE, (2010). The therapeutic potential of carbon monoxide. Nat Rev Drug Discov 9: 728-743.
40. Motterlini R, Clark JE, Foresti R, Sarathchandra P, Mann BE, Green CJ, (2002). Carbon monoxide-releasing molecules: characterization of biochemical and vascular activities. Circ Res 90: E17-E24.
41. Nakao A, Moore BA, Murase N, Liu F, Zuckerbraun BS, Bach FH, et al. (2003). Immunomodulatory effects of inhaled carbon monoxide on rat syngeneic small bowel graft motility. Gut 52: 1278-1285.
42. Neumann E, Lefevre S, Zimmermann B, Gay S, Muller-Ladner U, (2010). Rheumatoid arthritis progression mediated by activated synovial fibroblasts. Trends Mol Med 16: 458-468.
43. Okamoto H, Hoshi D, Kiire A, Yamanaka H, Kamatani N, (2008). Molecular targets of rheumatoid arthritis. Inflamm Allergy Drug Targets 7: 53-66.
44. O'Neill LA, (2008). The interleukin-1 receptor/Toll-like receptor superfamily: 10 years of progress. Immunol Rev 226: 10-18.
45. Otterbein LE, Bach FH, Alam J, Soares M, Tao LH, Wysk M, et al. (2000). Carbon monoxide has anti-inflammatory effects involving the mitogen-activated protein kinase pathway. Nat Med 6: 422-428.
46. Reddy SP, Mossman BT, (2002). Role and regulation of activator protein-1 in toxicant-induced responses of the lung. Am J Physiol Lung Cell Mol Physiol 283: L1161-L1178.
47. Rego D, Kumar A, Nilchi L, Wright K, Huang S, Kozlowski M, (2011). IL-6 production is positively regulated by two distinct Src homology domain 2-containing tyrosine phosphatase-1 (SHP-1)-dependent CCAAT/enhancer-binding protein beta and NF-κB pathways and an SHP-1-independent NF-κB pathway in lipopolysaccharide-stimulated bone marrow-derived macrophages. J Immunol 186: 5443-5456.
48. Rosenstein ED, Greenwald RA, Kushner LJ, Weissmann G, (2004). Hypothesis: the humoral immune response to oral bacteria provides a stimulus for the development of rheumatoid arthritis. Inflammation 28: 311-318.
49. Ryter SW, Otterbein LE, Morse D, Choi AM, (2002). Heme oxygenase/carbon monoxide signaling pathways: regulation and functional significance. Mol Cell Biochem 234-235: 249-263.
50. Ryter SW, Alam J, Choi AM, (2006). Heme oxygenase-1/carbon monoxide: from basic science to therapeutic applications. Physiol Rev 86: 583-650.
51. Sawa Y, Ueki T, Hata M, Iwasawa K, Tsuruga E, Kojima H, et al. (2008). LPS-induced IL-6, IL-8, VCAM-1, and ICAM-1 expression in human lymphatic endothelium. J Histochem Cytochem 56: 97-109.
52. Sawle P, Foresti R, Mann BE, Johnson TR, Green CJ, Motterlini R, (2005). Carbon monoxide-releasing molecules (CO-RMs) attenuate the inflammatory response elicited by lipopolysaccharide in RAW264.7 murine macrophages. Br J Pharmacol 145: 800-810.
53. Schwer CI, Mutschler M, Stoll P, Goebel U, Humar M, Hoetzel A, et al. (2010). Carbon monoxide releasing molecule-2 inhibits pancreatic stellate cell proliferation by activating p38 mitogen-activated protein kinase/heme oxygenase-1 signaling. Mol Pharmacol 77: 660-669.
54. Shambharkar PB, Blonska M, Pappu BP, Li H, You Y, Sakurai H, et al. (2007). Phosphorylation and ubiquitination of the IkappaB kinase complex by two distinct signaling pathways. EMBO J 26: 1794-1805.
55. Sheedy FJ, O'Neill LA, (2007). The troll in toll: mal and tram as bridges for TLR2 and TLR4 signaling. J Leukoc Biol 82: 196-203.
56. Soares MP, Seldon MP, Gregoire IP, Vassilevskaia T, Berberat PO, Yu J, et al. (2004). Heme oxygenase-1 modulates the expression of adhesion molecules associated with endothelial cell activation. J Immunol 172: 3553-3563.
57. Stein AB, Bolli R, Dawn B, Sanganalmath SK, Zhu Y, Wang OL, et al. (2012). Carbon monoxide induces a late preconditioning-mimetic cardioprotective and antiapoptotic milieu in the myocardium. J Mol Cell Cardiol 52: 228-236.
58. Sun B, Sun Z, Jin Q, Chen X, (2008a). CO-releasing molecules (CORM-2)-liberated CO attenuates leukocytes infiltration in the renal tissue of thermally injured mice. Int J Biol Sci 4: 176-183.
59. Sun B, Zou X, Chen Y, Zhang P, Shi G, (2008b). Preconditioning of carbon monoxide releasing molecule-derived CO attenuates LPS-induced activation of HUVEC. Int J Biol Sci 4: 270-278.
60. Tak PP, Thurkow EW, Daha MR, Kluin PM, Smeets TJ, Meinders AE, et al. (1995). Expression of adhesion molecules in early rheumatoid synovial tissue. Clin Immunol Immunopathol 77: 236-242.
61. Verstak B, Nagpal K, Bottomley SP, Golenbock DT, Hertzog PJ, Mansell A, (2009). MyD88 adapter-like (Mal)/TIRAP interaction with TRAF6 is critical for TLR2- and TLR4-mediated NF-κB proinflammatory responses. J Biol Chem 284: 24192-24203.
62. Wu CY, Hsieh HL, Jou MJ, Yang CM, (2004). Involvement of p42/p44 MAPK, p38 MAPK, JNK and nuclear factor-κB in interleukin-1β-induced matrix metalloproteinase-9 expression in rat brain astrocytes. J Neurochem 90: 1477-1488.
63. Wu CY, Chi PL, Hsieh HL, Luo SF, Yang CM, (2010). TLR4-dependent induction of vascular adhesion molecule-1 in rheumatoid arthritis synovial fibroblasts: roles of cytosolic phospholipase A(2)alpha/cyclooxygenase-2. J Cell Physiol 223: 480-491.
64. Zhong H, Voll RE, Ghosh S, (1998). Phosphorylation of NF-κB p65 by PKA stimulates transcriptional activity by promoting a novel bivalent interaction with the coactivator CBP/p300. Mol Cell 1: 661-671.