Connective tissue growth factor induces collagen I expression in human lung fibroblasts through the Rac1/MLK3/JNK/AP-1 pathway

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1833, Issue 12, 2013, Pages 2823-2833

  Lin, Chien Huang ^a   Yu, Ming Chih ^a,b   Tung, Wan Hsuan ^a   Chen, Tzu Ting ^a   Yu, Chung Chi ^a   Weng, Chih Ming ^a   Tsai, Yan Jyu ^a   Bai, Kua Jen ^a,b   Hong, Chuang Ye ^b   Chien, Ming Hsien ^a,b   Chen, Bing Chang ^a  

^a TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^b TAIPEI MEDICAL UNIVERSITY   (Taiwan)

Author keywords

Collagen I; Connective tissue growth factor; Fibroblasts; Lung fibrosis; Signal transduction

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; COLLAGEN TYPE 1; CONNECTIVE TISSUE GROWTH FACTOR; MIXED LINEAGE KINASE 3; PROCOLLAGEN; RAC1 PROTEIN; SMALL INTERFERING RNA; STRESS ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR AP 1;

ARTICLE; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; LUNG FIBROBLAST; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION;

EID: 84882805566     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2013.07.016     Document Type: Article

References (53)

1. Oglesby I.K., McElvaney N.G., Greene C.M. MicroRNAs in inflammatory lung disease-master regulators or target practice?. Respir. Res. 2010, 11:148. 10.1186/1465-9921-11-148.
2. Mozaffarian A., Brewer A.W., Trueblood E.S., Luzina I.G., Todd N.W., Atamas S.P., Arnett H.A. Mechanisms of oncostatin M-induced pulmonary inflammation and fibrosis. J. Immunol. 2008, 181:7243-7253.
3. Olson A.L., Swigris J.J. Idiopathic pulmonary fibrosis: diagnosis and epidemiology. Clin. Chest Med. 2012, 33:41-50.
4. Roche W.R., Beasley R., Williams J.H., Holgate S.T. Subepithelial fibrosis in the bronchi of asthmatics. Lancet 1989, 1:520-524.
5. Gelse K., Poschl E., Aigner T. Collagens-structure, function, and biosynthesis. Adv. Drug Deliv. Rev. 2003, 55:1531-1546.
6. Zhang H.Y., Gharaee-Kermani M., Zhang K., Karmiol S., Phan S.H. Lung fibroblast α-smooth muscle actin expression and contractile phenotype in bleomycin-induced pulmonary fibrosis. Am. J. Pathol. 1996, 148:527-537.
7. Zhang J., Feng M.X., Qu J.M. Low dose theophylline showed an inhibitory effect on the production of IL-6 and IL-8 in primary lung fibroblast from patients with COPD. Mediat. Inflamm. 2012, 2012:492901.
8. Lin Q., Fang L.P., Zhou W.W., Liu X.M. Rosiglitazone inhibits migration, proliferation, and phenotypic differentiation in cultured human lung fibroblasts. Exp. Lung Res. 2010, 36:120-128.
9. Leask A., Holmes A., Black C.M., Abraham D.J. Connective tissue growth factor gene regulation. Requirements for its induction by transforming growth factor-β2 in fibroblasts. J. Biol. Chem. 2003, 278:13008-13015.
10. Yu C.C., Hsu M.J., Kuo M.L., Chen R.F., Chen M.C., Bai K.J., Yu M.C., Chen B.C., Lin C.H. Thrombin-induced connective tissue growth factor expression in human lung fibroblasts requires the ASK1/JNK/AP-1 pathway. J. Immunol. 2009, 182:7916-7927.
11. Moussad E.E., Brigstock D.R. Connective tissue growth factor: what's in a name?. Mol. Genet. Metab. 2000, 71:276-292.
12. Robinson P.M., Blalock T.D., Yuan R., Lewin A.S., Schultz G.S. Hammerhead ribozyme-mediated knockdown of mRNA for fibrotic growth factors: transforming growth factor-β1 and connective tissue growth factor. Methods Mol. Biol. 2012, 820:117-132.
13. Ohnishi H., Oka T., Kusachi S., Nakanishi T., Takeda K., Nakahama M., Doi M., Murakami T., Ninomiya Y., Takigawa M., Tsuji T. Increased expression of connective tissue growth factor in the infarct zone of experimentally induced myocardial infarction in rats. J. Mol. Cell. Cardiol. 1998, 30:2411-2422.
14. Kennedy L., Liu S., Shi-Wen X., Chen Y., Eastwood M., Sabetkar M., Carter D.E., Lyons K.M., Black C.M., Abraham D.J., Leask A. CCN2 is necessary for the function of mouse embryonic fibroblasts. Exp. Cell Res. 2007, 313:952-964.
15. Ponticos M., Holmes A.M., Shi-wen X., Leoni P., Khan K., Rajkumar V.S., Hoyles R.K., Bou-Gharios G., Black C.M., Denton C.P., Abraham D.J., Leask A., Lindahl G.E. Pivotal role of connective tissue growth factor in lung fibrosis: MAPK-dependent transcriptional activation of type I collagen. Arthritis Rheum. 2009, 60:2142-2155.
16. Wang Q., Usinger W., Nichols B., Gray J., Xu L., Seeley T.W., Brenner M., Guo G., Zhang W., Oliver N., Lin A., Yeowell D. Cooperative interaction of CTGF and TGF-β in animal models of fibrotic disease. Fibrogenesis Tissue Repair 2011, 4:4. 10.1186/1755-1536-4-4.
17. Tao L., Liu J., Li Z., Dai X., Li S. Role of the JAK-STAT pathway in proliferation and differentiation of human hypertrophic scar fibroblasts induced by connective tissue growth factor. Mol. Med. Rep. 2010, 3:941-945.
18. Aumailley M., Gayraud B. Structure and biological activity of the extracellular matrix. J. Mol. Med. 1998, 76:253-265.
19. Goodwin A., Jenkins G. Role of integrin-mediated TGF-β activation in the pathogenesis of pulmonary fibrosis. Biochem. Soc. Trans. 2009, 37:849-854.
20. Blaauboer M.E., Emson C.L., Verschuren L., van Erk M., Turner S.M., Everts V., Hanemaaijer R., Stoop R. Novel combination of collagen dynamics analysis and transcriptional profiling reveals fibrosis-relevant genes and pathways. Matrix Biol. 2013, 10.1016/j.matbio.2013.04.005.
21. Ihn H., Yamane K., Kubo M., Tamaki K. Blockade of endogenous transforming growth factor β signaling prevents up-regulated collagen synthesis in scleroderma fibroblasts: association with increased expression of transforming growth factor β receptors. Arthritis Rheum. 2001, 44:474-480.
22. Chen S.J., Yuan W.H., Mori Y., Levenson A., Trojanowska M., Varga J. Stimulation of type I collagen transcription in human skin fibroblasts by TGF-β: involvement of Smad 3. J. Invest. Dermatol. 1999, 112:49-57.
23. Tang H.T., Cheng D.S., Jia Y.T., Ben D.F., Ma B., Lv K.Y., Wei D., Sheng Z.Y., Xia F. Angiotensin II induces type I collagen gene expression in human dermal fibroblasts through an AP-1/TGF-β1-dependent pathway. Biochem. Biophys. Res. Commun. 2009, 385:418-423.
24. Jin S., Ray R.M., Johnson L.R. Rac1 mediates intestinal epithelial cell apoptosis via JNK. Am. J. Physiol. Gastrointest. Liver Physiol. 2006, 291:G1137-G1147.
25. Teramoto H., Coso O.A., Miyata H., Igishi T., Miki T., Gutkind J.S. Signaling from the small GTP-binding proteins Rac1 and Cdc42 to the c-Jun N-terminal kinase/stress-activated protein kinase pathway. A role for mixed lineage kinase 3/protein-tyrosine kinase 1, a novel member of the mixed lineage kinase family. J. Biol. Chem. 1996, 271:27225-27228.
26. Linseman D.A., Loucks F.A. Diverse roles of Rho family GTPases in neuronal development, survival, and death. Front. Biosci. 2008, 13:657-676.
27. Zhang Y., Chadee D.N. Inhibition of Cdc42-mediated activation of mixed lineage kinase 3 by the tumor suppressor protein merlin. Small Gtpases 2010, 1:183-186.
28. Gallo K.A., Johnson G.L. Signalling: mixed-lineage kinase control of JNK and p38 MAPK pathways. Nat. Rev. Mol. Cell Biol. 2002, 3:663-672.
29. Kyriakis J.M., Avruch J. Mammalian mitogen-activated protein kinase signal transduction pathways activated by stress and inflammation. Physiol. Rev. 2001, 81:807-869.
30. Chadee D.N., Kyriakis J.M. MLK3 is required for mitogen activation of B-Raf, ERK and cell proliferation. Nat. Cell Biol. 2004, 6:770-776.
31. Zhang Q.G., Wang R., Han D., Dong Y., Brann D.W. Role of Rac1 GTPase in JNK signaling and delayed neuronal cell death following global cerebral ischemia. Brain Res. 2009, 1265:138-147.
32. Engers R., Springer E., Kehren V., Simic T., Young D.A., Beier J., Klotz L.O., Clark I.M., Sies H., Gabbert H.E. Rac upregulates tissue inhibitor of metalloproteinase-1 expression by redox-dependent activation of extracellular signal-regulated kinase signaling. FEBS J. 2006, 273:4754-4769.
33. Lin C.H., Cheng H.W., Hsu M.J., Chen M.C., Lin C.C., Chen B.C. c-Src mediates thrombin-induced NF-κB activation and IL-8/CXCL8 expression in lung epithelial cells. J. Immunol. 2006, 177:3427-3438.
34. Liu S., Kapoor M., Shi-wen X., Kennedy L., Denton C.P., Glogauer M., Abraham D.J., Leask A. Role of Rac1 in a bleomycin-induced scleroderma model using fibroblast-specific Rac1-knockout mice. Arthritis Rheum. 2008, 58:2189-2195.
35. Wang M.J., Huang H.Y., Chen W.F., Chang H.F., Kuo J.S. Glycogen synthase kinase-3β inactivation inhibits tumor necrosis factor-α production in microglia by modulating nuclear factor κB and MLK3/JNK signaling cascades. J. Neuroinflammation 2010, 7:99. 10.1186/1742-2094-7-99.
36. Leung I.W., Lassam N. The kinase activation loop is the key to mixed lineage kinase-3 activation via both autophosphorylation and hematopoietic progenitor kinase 1 phosphorylation. J. Biol. Chem. 2001, 276:1961-1967.
37. Tapon N., Nagata K., Lamarche N., Hall A. A new rac target POSH is an SH3-containing scaffold protein involved in the JNK and NF-κB signalling pathways. EMBO J. 1998, 17:1395-1404.
38. Tournier C., Whitmarsh A.J., Cavanagh J., Barrett T., Davis R.J. Mitogen-activated protein kinase kinase 7 is an activator of the c-Jun NH2-terminal kinase. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:7337-7342.
39. Kook S.H., Hwang J.M., Park J.S., Kim E.M., Heo J.S., Jeon Y.M., Lee J.C. Mechanical force induces type I collagen expression in human periodontal ligament fibroblasts through activation of ERK/JNK and AP-1. J. Cell. Biochem. 2009, 106:1060-1067.
40. Worrall J.A., Mason J.M. Thermodynamic analysis of Jun-Fos coiled coil peptide antagonists. FEBS J. 2011, 278:663-672.
41. Vanden Bush T.J., Bishop G.A. CDK-mediated regulation of cell functions via c-Jun phosphorylation and AP-1 activation. PLoS One 2011, 6:e19468.
42. Frazier K., Williams S., Kothapalli D., Klapper H., Grotendorst G.R. Stimulation of fibroblast cell growth, matrix production, and granulation tissue formation by connective tissue growth factor. J. Invest. Dermatol. 1996, 107:404-411.
43. Arnould T., Kim E., Tsiokas L., Jochimsen F., Grüning W., Chang J.D., Walz G. The polycystic kidney disease 1 gene product mediates protein kinase C α-dependent and c-Jun N-terminal kinase-dependent activation of the transcription factor AP-1. J. Biol. Chem. 1998, 273:6013-6018.
44. Choi S.S., Sicklick J.K., Ma Q., Yang L., Huang J., Qi Y., Chen W., Li Y.X., Goldschmidt-Clermont P.J., Diehl A.M. Sustained activation of Rac1 in hepatic stellate cells promotes liver injury and fibrosis in mice. Hepatology 2006, 44:1267-1267.
45. Gupta S., Barrett T., Whitmarsh A.J., Cavanagh J., Sluss H.K., Derijard B., Davis R.J. Selective interaction of JNK protein kinase isoforms with transcription factors. EMBO J. 1996, 15:2760-2770.
46. Roy S.K., Shuman J.D., Platanias L.C., Shapiro P.S., Reddy S.P., Johnson P.F., Kalvakolanu D.V. A role for mixed lineage kinases in regulating transcription factor CCAAT/enhancer-binding protein-β-dependent gene expression in response to interferon-γ. J. Biol. Chem. 2005, 280:24462-24471.
47. Hehner S.P., Hofmann T.G., Ushmorov A., Dienz O., Wing-Lan Leung I., Lassam N., Scheidereit C., Dröge W., Schmitz M.L. Mixed-lineage kinase 3 delivers CD3/CD28-derived signals into the IκB kinase complex. Mol. Cell. Biol. 2000, 20:2556-2568.
48. Ip Y.T., Davis R.J. Signal transduction by the c-Jun N-terminal kinase (JNK): from inflammation to development. Curr. Opin. Cell Biol. 1998, 10:205-219.
49. Tengku-Muhammad T.S., Hughes T.R., Foka P., Cryer A., Ramji D.P. Cytokine-mediated differential regulation of macrophage activator protein-1 genes. Cytokine 2000, 12:720-726.
50. Rahman I., MacNee W. Regulation of redox glutathione levels and gene transcription in lung inflammation: therapeutic approaches. Free Radic. Biol. Med. 2000, 28:1405-1420.
51. Hisatomi K., Mukae H., Sakamoto N., Ishimatsu Y., Kakugawa T., Hara S., Fujita H., Nakamichi S., Oku H., Urata Y., Kubota H., Nagata K., Kohno S. Pirfenidone inhibits TGF-β1-induced over-expression of collagen type I and heat shock protein 47 in A549 cells. BMC Pulm. Med. 2012, 12:24.
52. Ruiz P.A., Jarai G. Discoidin domain receptors regulate the migration of primary human lung fibroblasts through collagen matrices. Fibrogenesis Tissue Repair 2012, 5:3.
53. Bonniaud P., Margetts P.J., Kolb M., Haberberger T., Kelly M., Robertson J., Gauldie J. Adenoviral gene transfer of connective tissue growth factor in the lung induces transient fibrosis. Am. J. Respir. Crit. Care Med. 2003, 168:770-778.