Thrombin induces heme oxygenase-1 expression in human synovial fibroblasts through protease-activated receptor signaling pathways

Arthritis Research and Therapy

Volumn 14, Issue 2, 2012, Pages

  Liu, Ju Fang ^a   Hou, Sheng Mou ^a   Tsai, Chun Hao ^b,c   Huang, Chun Yin ^c,d   Yang, Wei Hung ^e,f,g   Tang, Chih Hsin ^c,g  

^a SHIN KONG WU HO SU MEMORIAL HOSPITAL   (Taiwan)

^b CHINA MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

^c CHINA MEDICAL UNIVERSITY   (Taiwan)

^d CHINA MEDICAL UNIVERSITY BEIGANG HOSPITAL   (Taiwan)

^e Taichung Hospital   (Taiwan)

^f NATIONAL CHUNG HSING UNIVERSITY   (Taiwan)

^g CHINA MEDICAL UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

2 [1 (3 DIMETHYLAMINOPROPYL) 3 INDOLYL] 3 (3 INDOLYL)MALEIMIDE; 4 AMINO 7 TERT BUTYL 5 (4 CHLOROPHENYL)PYRAZOLO[3,4 D]PYRIMIDINE; BETA ACTIN; FIBRIN; HEME; HEME OXYGENASE 1; PROTEIN KINASE C DELTA; PROTEIN TYROSINE KINASE; PROTEIN TYROSINE KINASE INHIBITOR; PROTEINASE ACTIVATED RECEPTOR; PROTEINASE ACTIVATED RECEPTOR 1; PROTEINASE ACTIVATED RECEPTOR 3; PROTEINASE ACTIVATED RECEPTOR 4; RECEPTOR PROTEIN; ROTTLERIN; SMALL INTERFERING RNA; THROMBIN; THROMBIN INHIBITOR; TRANSCRIPTION FACTOR NRF2; PROTEASE-ACTIVATED RECEPTOR 3; THROMBIN RECEPTOR;

ANGIOGENESIS; ARTICLE; CELL PROTECTION; CHROMATIN IMMUNOPRECIPITATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; ENZYME ACTIVITY; FIBRIN DEPOSITION; FIBROBLAST; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IN VIVO STUDY; INFLAMMATION; OSTEOARTHRITIS; OXIDATIVE STRESS; PROMOTER REGION; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SYNOVIAL FIBROBLAST; SYNOVIUM; UPREGULATION; WESTERN BLOTTING; CELL CULTURE; ENZYMOLOGY; PHYSIOLOGY; SYNOVIAL FLUID;

CELLS, CULTURED; FIBROBLASTS; HEME OXYGENASE-1; HUMANS; RECEPTOR, PAR-1; RECEPTORS, PROTEINASE-ACTIVATED; RECEPTORS, THROMBIN; SIGNAL TRANSDUCTION; SYNOVIAL FLUID; THROMBIN;

EID: 84860218962     PISSN: 14786354     EISSN: 14786362     Source Type: Journal    
DOI: 10.1186/ar3815     Document Type: Article

References (37)

1. Rousseau JC, Delmas PD. Biological markers in osteoarthritis. Nat Clin Pract Rheumatol 2007, 3:346-356. 10.1038/ncprheum0508, 17538566.
2. Laufer S. Role of eicosanoids in structural degradation in osteoarthritis. Curr Opin Rheumatol 2003, 15:623-627. 10.1097/00002281-200309000-00017, 12960491.
3. Wright B, Rashid A, Leonard L. Scaphoid fracture in a patient with pre-existing scaphotrapezio-trapezoid osteoarthritis. J Hand Surg Eur Vol 2009, 34:818-819. 10.1177/1753193409339119, 20067933.
4. Kirkby KA, Adin CA. Products of heme oxygenase and their potential therapeutic applications. Am J Physiol Renal Physiol 2006, 290:F563-571.
5. Ryter SW, Kim HP, Nakahira K, Zuckerbraun BS, Morse D, Choi AM. Protective functions of heme oxygenase-1 and carbon monoxide in the respiratory system. Antioxid Redox Signal 2007, 9:2157-2173. 10.1089/ars.2007.1811, 17845132.
6. Balla G, Jacob HS, Balla J, Rosenberg M, Nath K, Apple F, Eaton JW, Vercellotti GM. Ferritin: a cytoprotective antioxidant strategem of endothelium. J Biol Chem 1992, 267:18148-18153.
7. Choi BM, Pae HO, Jeong YR, Oh GS, Jun CD, Kim BR, Kim YM, Chung HT. Overexpression of heme oxygenase (HO)-1 renders Jurkat T cells resistant to fas-mediated apoptosis: involvement of iron released by HO-1. Free Radic Biol Med 2004, 36:858-871. 10.1016/j.freeradbiomed.2004.01.004, 15019971.
8. Rushworth SA, Chen XL, Mackman N, Ogborne RM, O'Connell MA. Lipopolysaccharide-induced heme oxygenase-1 expression in human monocytic cells is mediated via Nrf2 and protein kinase C. J Immunol 2005, 175:4408-4415.
9. Aggeli IK, Gaitanaki C, Beis I. Involvement of JNKs and p38-MAPK/MSK1 pathways in H2O2-induced upregulation of heme oxygenase-1 mRNA in H9c2 cells. Cell Signal 2006, 18:1801-1812. 10.1016/j.cellsig.2006.02.001, 16531007.
10. Devesa I, Ferrandiz ML, Terencio MC, Joosten LA, van den Berg WB, Alcaraz MJ. Influence of heme oxygenase 1 modulation on the progression of murine collagen-induced arthritis. Arthritis Rheum 2005, 52:3230-3238. 10.1002/art.21356, 16200597.
11. Guillen M, Megias J, Gomar F, Alcaraz M. Haem oxygenase-1 regulates catabolic and anabolic processes in osteoarthritic chondrocytes. J Pathol 2008, 214:515-522.
12. Smith MD, Triantafillou S, Parker A, Youssef PP, Coleman M. Synovial membrane inflammation and cytokine production in patients with early osteoarthritis. J Rheumatol 1997, 24:365-371.
13. Hasegawa M, Segawa T, Maeda M, Yoshida T, Sudo A. Thrombin-cleaved osteopontin levels in synovial fluid correlate with disease severity of knee osteoarthritis. J Rheumatol 2011, 38:129-134. 10.3899/jrheum.100637, 21041276.
14. Varisco PA, Peclat V, van Ness K, Bischof-Delaloye A, So A, Busso N. Effect of thrombin inhibition on synovial inflammation in antigen induced arthritis. Ann Rheum Dis 2000, 59:781-787. 10.1136/ard.59.10.781, 1753002, 11005778.
15. So AK, Varisco PA, Kemkes-Matthes B, Herkenne-Morard C, Chobaz-Peclat V, Gerster JC, Busso N. Arthritis is linked to local and systemic activation of coagulation and fibrinolysis pathways. J Thromb Haemost 2003, 1:2510-2515. 10.1111/j.1538-7836.2003.00462.x, 14675085.
16. Ohnishi M, Katsuki H, Unemura K, Izumi Y, Kume T, Takada-Takatori Y, Akaike A. Heme oxygenase-1 contributes to pathology associated with thrombin-induced striatal and cortical injury in organotypic slice culture. Brain Res 2010, 1347:170-178.
17. Tang CH, Chiu YC, Tan TW, Yang RS, Fu WM. Adiponectin enhances IL-6 production in human synovial fibroblast via an AdipoR1 receptor, AMPK, p38, and NF-kappa B pathway. J Immunol 2007, 179:5483-5492.
18. Tang CH, Hsu CJ, Fong YC. The CCL5/CCR5 axis promotes interleukin-6 production in human synovial fibroblasts. Arthritis Rheum 2010, 62:3615-3624. 10.1002/art.27755, 20862675.
19. Hsieh MT, Hsieh CL, Lin LW, Wu CR, Huang GS. Differential gene expression of scopolamine-treated rat hippocampus-application of cDNA microarray technology. Life Sci 2003, 73:1007-1016. 10.1016/S0024-3205(03)00372-2, 12818353.
20. Wang YC, Lee PJ, Shih CM, Chen HY, Lee CC, Chang YY, Hsu YT, Liang YJ, Wang LY, Han WH. Damage formation and repair efficiency in the p53 gene of cell lines and blood lymphocytes assayed by multiplex long quantitative polymerase chain reaction. Anal Biochem 2003, 319:206-215. 10.1016/S0003-2697(03)00330-0, 12871714.
21. Huang HC, Shi GY, Jiang SJ, Shi CS, Wu CM, Yang HY, Wu HL. Thrombomodulin-mediated cell adhesion: involvement of its lectin-like domain. J Biol Chem 2003, 278:46750-46759. 10.1074/jbc.M305216200, 12951323.
22. Tseng CP, Huang CL, Huang CH, Cheng JC, Stern A, Tseng CH, Chiu DT. Disabled-2 small interfering RNA modulates cellular adhesive function and MAPK activity during megakaryocytic differentiation of K562 cells. FEBS Lett 2003, 541:21-27. 10.1016/S0014-5793(03)00281-3, 12706813.
23. Yang WH, Chang JT, Hsu SF, Li TM, Cho DY, Huang CY, Fong YC, Tang CH. Bradykinin enhances cell migration in human chondrosarcoma cells through BK receptor signaling pathways. J Cell Biochem 2010, 109:82-92.
24. Liu JF, Chang CS, Fong YC, Kuo SC, Tang CH. FPipTB, a benzimidazole derivative, induces chondrosarcoma cell apoptosis via endoplasmic reticulum stress and apoptosis signal-regulating kinase 1. Mol Carcinog 2012, 54:315-326.
25. Kitamoto Y, Nakamura E, Kudo S, Tokunaga H, Murakami E, Noguchi K, Imamura T. Thrombin in synovial fluid as a marker of synovial inflammation: a definite measurement by ELISA and correlation with VEGF. Clin Chim Acta 2008, 398:159-160. 10.1016/j.cca.2008.08.009, 18765237.
26. Shin H, Kitajima I, Nakajima T, Shao Q, Tokioka T, Takasaki I, Hanyu N, Kubo T, Maruyama I. Thrombin receptor mediated signals induce expressions of interleukin 6 and granulocyte colony stimulating factor via NF-kappa B activation in synovial fibroblasts. Ann Rheum Dis 1999, 58:55-60. 10.1136/ard.58.1.55, 1752754, 10343541.
27. Chiu YC, Fong YC, Lai CH, Hung CH, Hsu HC, Lee TS, Yang RS, Fu WM, Tang CH. Thrombin-induced IL-6 production in human synovial fibroblasts is mediated by PAR1, phospholipase C, protein kinase C alpha, c-Src, NF-kappa B and p300 pathway. Mol Immunol 2008, 45:1587-1599. 10.1016/j.molimm.2007.10.004, 18062909.
28. Hsieh HL, Sun CC, Wang TS, Yang CM. PKC-delta/c-Src-mediated EGF receptor transactivation regulates thrombin-induced COX-2 expression and PGE(2) production in rat vascular smooth muscle cells. Biochim Biophys Acta 2008, 1783:1563-1575. 10.1016/j.bbamcr.2008.03.016, 18452714.
29. Basu A, Adkins B, Basu C. Down-regulation of caspase-2 by rottlerin via protein kinase C-delta-independent pathway. Cancer Res 2008, 68:2795-2802. 10.1158/0008-5472.CAN-07-6244, 18413747.
30. Hsieh HL, Sun CC, Wang TS, Yang CM. PKC-delta/c-Src-mediated EGF receptor transactivation regulates thrombin-induced COX-2 expression and PGE(2) production in rat vascular smooth muscle cells. Biochim Biophys Acta 2008, 1783:1563-1575. 10.1016/j.bbamcr.2008.03.016, 18452714.
31. Roskoski R. Src kinase regulation by phosphorylation and dephosphorylation. Biochem Biophys Res Commun 2005, 331:1-14. 10.1016/j.bbrc.2005.03.012, 15845350.
32. Surh YJ, Kundu JK, Na HK, Lee JS. Redox-sensitive transcription factors as prime targets for chemoprevention with anti-inflammatory and antioxidative phytochemicals. J Nutr 2005, 135:2993S-3001S.
33. Coughlin SR. Thrombin signalling and protease-activated receptors. Nature 2000, 407:258-264. 10.1038/35025229, 11001069.
34. Berk BC, Taubman MB, Cragoe EJ, Fenton JW, Griendling KK. Thrombin signal transduction mechanisms in rat vascular smooth muscle cells: calcium and protein kinase C-dependent and -independent pathways. J Biol Chem 1990, 265:17334-17340.
35. Leitges M, Elis W, Gimborn K, Huber M. Rottlerin-independent attenuation of pervanadate-induced tyrosine phosphorylation events by protein kinase C-delta in hemopoietic cells. Lab Invest 2001, 81:1087-1095.
36. Yeh M, Gharavi NM, Choi J, Hsieh X, Reed E, Mouillesseaux KP, Cole AL, Reddy ST, Berliner JA. Oxidized phospholipids increase interleukin 8 (IL-8) synthesis by activation of the c-src/signal transducers and activators of transcription (STAT)3 pathway. J Biol Chem 2004, 279:30175-30181. 10.1074/jbc.M312198200, 15143062.
37. Ishii T, Itoh K, Ruiz E, Leake DS, Unoki H, Yamamoto M, Mann GE. Role of Nrf2 in the regulation of CD36 and stress protein expression in murine macrophages: activation by oxidatively modified LDL and 4-hydroxynonenal. Circ Res 2004, 94:609-616. 10.1161/01.RES.0000119171.44657.45, 14752028.