Cx43 contributes to TGF-β signaling to regulate differentiation of cardiac fibroblasts into myofibroblasts

Experimental Cell Research

Volumn 315, Issue 7, 2009, Pages 1190-1199

  Asazuma Nakamura, Yuko ^a   Dai, Ping ^a   Harada, Yoshinori ^a   Jiang, Yan ^a   Hamaoka, Kenji ^a   Takamatsu, Tetsuro ^a  

^a KYOTO PREFECTURAL UNIVERSITY OF MEDICINE   (Japan)

Author keywords

Antisense oligodeoxynucleotides; Cardiac fibroblast; Cardiac myofibroblast; Connexin43; Differentiation; TGF ; SMA

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; ANTISENSE OLIGODEOXYNUCLEOTIDE; CONNEXIN 43; GAP JUNCTION PROTEIN; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL TISSUE; ARTICLE; CELL CULTURE; CELL DIFFERENTIATION; CONTROLLED STUDY; GENE OVEREXPRESSION; HEART MUSCLE CELL; IMMUNOCYTOCHEMISTRY; MYOFIBROBLAST; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; WISTAR RAT;

RATTUS;

ACTINS; ANIMALS; ANIMALS, NEWBORN; CELL DIFFERENTIATION; CONNEXIN 43; FIBROBLASTS; HEART FAILURE; MYOCARDIUM; MYOCYTES, SMOOTH MUSCLE; RATS; RATS, WISTAR; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA;

EID: 63049134111     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2008.12.021     Document Type: Article

References (46)

1. Eghbali M., Czaja M.J., Zeydel M., Weiner F.R., Zern M.A., Seifter S., and Blumenfeld O.O. Collagen chain mRNAs in isolated heart cells from young and adult rats. J. Mol. Cell. Cardiol. 20 (1988) 267-276
2. Kawano H., Do Y.S., Kawano Y., Starnes V., Barr M., Law R.E., and Hsueh W.A. Angiotensin II has multiple profibrotic effects in human cardiac fibroblasts. Circulation 101 (2000) 1130-1137
3. Frangogiannis N.G. The mechanistic basis of infarct healing. Antioxid. Redox. Signal 8 (2006) 1907-1939
4. Serini G., and Gabbiani G. Mechanisms of myofibroblast activity and phenotypic modulation. Exp. Cell Res. 250 (1999) 273-283
5. Gabbiani G. Evolution and clinical implications of the myofibroblast concept. Cardiovasc. Res. 38 (1998) 545-548
6. Desmouliere A., Geinoz A., Gabbiani F., and Gabbiani G. Transforming growth factor-beta 1 induces alpha-smooth muscle actin expression in granulation tissue myofibroblasts and in quiescent and growing cultured fibroblasts. J. Cell Biol. 122 (1993) 103-111
7. Rosenkranz S. TGF-beta1 and angiotensin networking in cardiac remodeling. Cardiovasc. Res. 63 (2004) 423-432
8. Tomasek J.J., McRae J., Owens G.K., and Haaksma C.J. Regulation of alpha-smooth muscle actin expression in granulation tissue myofibroblasts is dependent on the intronic CArG element and the transforming growth factor-beta1 control element. Am. J. Pathol. 166 (2005) 1343-1351
9. Kulkarni A.B., Huh C.G., Becker D., Geiser A., Lyght M., Flanders K.C., Roberts A.B., Sporn M.B., Ward J.M., and Karlsson S. Transforming growth factor beta 1 null mutation in mice causes excessive inflammatory response and early death. Proc. Natl. Acad. Sci. U. S. A. 90 (1993) 770-774
10. Virag J.I., and Murry C.E. Myofibroblast and endothelial cell proliferation during murine myocardial infarct repair. Am. J. Pathol. 163 (2003) 2433-2440
11. Petrov V.V., Fagard R.H., and Lijnen P.J. Stimulation of collagen production by transforming growth factor-beta1 during differentiation of cardiac fibroblasts to myofibroblasts. Hypertension 39 (2002) 258-263
12. Iwano M., Plieth D., Danoff T.M., Xue C., Okada H., and Neilson E.G. Evidence that fibroblasts derive from epithelium during tissue fibrosis. J. Clin. Invest. 110 (2002) 341-350
13. Zeisberg E.M., Tarnavski O., Zeisberg M., Dorfman A.L., McMullen J.R., Gustafsson E., Chandraker A., Yuan X., Pu W.T., Roberts A.B., Neilson E.G., Sayegh M.H., Izumo S., and Kalluri R. Endothelial-to-mesenchymal transition contributes to cardiac fibrosis. Nat. Med. 13 (2007) 952-961
14. Dai P., Nakagami T., Tanaka H., Hitomi T., and Takamatsu T. Cx43 mediates TGF-beta signaling through competitive Smads binding to microtubules. Mol. Biol. Cell 18 (2007) 2264-2273
15. Nakano Y., Oyamada M., Dai P., Nakagami T., Kinoshita S., and Takamatsu T. Connexin43 knockdown accelerates wound healing but inhibits mesenchymal transition after corneal endothelial injury in vivo. Invest. Ophthalmol. Vis. Sci. 49 (2008) 93-104
16. Qiu C., Coutinho P., Frank S., Franke S., Law L.Y., Martin P., Green C.R., and Becker D.L. Targeting connexin43 expression accelerates the rate of wound repair. Curr. Biol. 13 (2003) 1697-1703
17. Tanabe T., Oyamada M., Fujita K., Dai P., Tanaka H., and Takamatsu T. Multiphoton excitation-evoked chromophore-assisted laser inactivation using green fluorescent protein. Nat. Methods 2 (2005) 503-505
18. Gu L., Zhu Y.J., Yang X., Guo Z.J., Xu W.B., and Tian X.L. Effect of TGF-beta/Smad signaling pathway on lung myofibroblast differentiation. Acta Pharmacol. Sin. 28 (2007) 382-391
19. Shao Q., Wang H., McLachlan E., Veitch G.I., and Laird D.W. Down-regulation of Cx43 by retroviral delivery of small interfering RNA promotes an aggressive breast cancer cell phenotype. Cancer Res. 65 (2005) 2705-2711
20. Brouty-Boye D., Kolonias D., Savaraj N., and Lampidis T.J. Alpha-smooth muscle actin expression in cultured cardiac fibroblasts of newborn rat. In Vitro Cell. Dev. Biol. 28A (1992) 293-296
21. Wang J., Chen H., Seth A., and McCulloch C.A. Mechanical force regulation of myofibroblast differentiation in cardiac fibroblasts. Am. J. Physiol. Heart Circ. Physiol. 285 (2003) H1871-1881
22. Dugina V., Fontao L., Chaponnier C., Vasiliev J., and Gabbiani G. Focal adhesion features during myofibroblastic differentiation are controlled by intracellular and extracellular factors. J. Cell. Sci. 114 (2001) 3285-3296
23. Inman G.J., Nicolas F.J., Callahan J.F., Harling J.D., Gaster L.M., Reith A.D., Laping N.J., and Hill C.S. SB-431542 is a potent and specific inhibitor of transforming growth factor-beta superfamily type I activin receptor-like kinase (ALK) receptors ALK4, ALK5, and ALK7. Mol. Pharmacol. 62 (2002) 65-74
24. van Veen A.A., van Rijen H.V., and Opthof T. Cardiac gap junction channels: modulation of expression and channel properties. Cardiovasc. Res. 51 (2001) 217-229
25. Miragoli M., Gaudesius G., and Rohr S. Electrotonic modulation of cardiac impulse conduction by myofibroblasts. Circ. Res. 98 (2006) 801-810
26. Louault C., Benamer N., Faivre J.F., Potreau D., and Bescond J. Implication of connexins 40 and 43 in functional coupling between mouse cardiac fibroblasts in primary culture. Biochim. Biophys. Acta (2008)
27. Tomasek J.J., Gabbiani G., Hinz B., Chaponnier C., and Brown R.A. Myofibroblasts and mechano-regulation of connective tissue remodelling. Nat. Rev. Mol. Cell Biol. 3 (2002) 349-363
28. Leask A. TGFbeta, cardiac fibroblasts, and the fibrotic response. Cardiovasc. Res. 74 (2007) 207-212
29. Verrecchia F., and Mauviel A. Control of connective tissue gene expression by TGF beta: role of Smad proteins in fibrosis. Curr. Rheumatol. Rep. 4 (2002) 143-149
30. Shi Y., and Massague J. Mechanisms of TGF-beta signaling from cell membrane to the nucleus. Cell 113 (2003) 685-700
31. Shi-wen X., Stanton L.A., Kennedy L., Pala D., Chen Y., Howat S.L., Renzoni E.A., Carter D.E., Bou-Gharios G., Stratton R.J., Pearson J.D., Beier F., Lyons K.M., Black C.M., Abraham D.J., and Leask A. CCN2 is necessary for adhesive responses to transforming growth factor-beta1 in embryonic fibroblasts. J. Biol. Chem. 281 (2006) 10715-10726
32. Liu S., Xu S.W., Kennedy L., Pala D., Chen Y., Eastwood M., Carter D.E., Black C.M., Abraham D.J., and Leask A. FAK is required for TGFbeta-induced JNK phosphorylation in fibroblasts: implications for acquisition of a matrix-remodeling phenotype. Mol. Biol. Cell 18 (2007) 2169-2178
33. Roy S., Khanna S., Rink T., Radtke J., Williams W.T., Biswas S., Schnitt R., Strauch A.R., and Sen C.K. P21waf1/cip1/sdi1 as a central regulator of inducible smooth muscle actin expression and differentiation of cardiac fibroblasts to myofibroblasts. Mol. Biol. Cell 18 (2007) 4837-4846
34. Lenga Y., Koh A., Perera A.S., McCulloch C.A., Sodek J., and Zohar R. Osteopontin expression is required for myofibroblast differentiation. Circ. Res. 102 (2008) 319-327
35. Li P., Wang D., Lucas J., Oparil S., Xing D., Cao X., Novak L., Renfrow M.B., and Chen Y.F. Atrial natriuretic peptide inhibits transforming growth factor beta-induced Smad signaling and myofibroblast transformation in mouse cardiac fibroblasts. Circ. Res. 102 (2008) 185-192
36. Peters N.S., Coromilas J., Severs N.J., and Wit A.L. Disturbed connexin43 gap junction distribution correlates with the location of reentrant circuits in the epicardial border zone of healing canine infarcts that cause ventricular tachycardia. Circulation 95 (1997) 988-996
37. Matsushita T., Oyamada M., Fujimoto K., Yasuda Y., Masuda S., Wada Y., Oka T., and Takamatsu T. Remodeling of cell-cell and cell-extracellular matrix interactions at the border zone of rat myocardial infarcts. Circ. Res. 85 (1999) 1046-1055
38. Camelliti P., Devlin G.P., Matthews K.G., Kohl P., and Green C.R. Spatially and temporally distinct expression of fibroblast connexins after sheep ventricular infarction. Cardiovasc. Res. 62 (2004) 415-425
39. Dewald O., Ren G., Duerr G.D., Zoerlein M., Klemm C., Gersch C., Tincey S., Michael L.H., Entman M.L., and Frangogiannis N.G. Of mice and dogs: species-specific differences in the inflammatory response following myocardial infarction. Am. J. Pathol. 164 (2004) 665-677
40. Frangogiannis N.G., Ren G., Dewald O., Zymek P., Haudek S., Koerting A., Winkelmann K., Michael L.H., Lawler J., and Entman M.L. Critical role of endogenous thrombospondin-1 in preventing expansion of healing myocardial infarcts. Circulation 111 (2005) 2935-2942
41. Bujak M., and Frangogiannis N.G. The role of TGF-beta signaling in myocardial infarction and cardiac remodeling. Cardiovasc. Res. 74 (2007) 184-195
42. Verrecchia F., Chu M.L., and Mauviel A. Identification of novel TGF-beta/Smad gene targets in dermal fibroblasts using a combined cDNA microarray/promoter transactivation approach. J. Biol. Chem. 276 (2001) 17058-17062
43. Bujak M., Ren G., Kweon H.J., Dobaczewski M., Reddy A., Taffet G., Wang X.F., and Frangogiannis N.G. Essential role of Smad3 in infarct healing and in the pathogenesis of cardiac remodeling. Circulation 116 (2007) 2127-2138
44. Flanders K.C. Smad3 as a mediator of the fibrotic response. Int. J. Exp. Pathol. 85 (2004) 47-64
45. Gabbiani G., Chaponnier C., and Huttner I. Cytoplasmic filaments and gap junctions in epithelial cells and myofibroblasts during wound healing. J. Cell Biol. 76 (1978) 561-568
46. Kim T.Y., Kim W.I., Smith R.E., and Kay E.D. Role of p27(Kip1) in cAMP- and TGF-beta2-mediated antiproliferation in rabbit corneal endothelial cells. Invest. Ophthalmol. Vis. Sci. 42 (2001) 3142-3149