Antifibrotic properties of c-Ski and its regulation of cardiac myofibroblast phenotype and contractility

American Journal of Physiology - Cell Physiology

Volumn 300, Issue 1, 2011, Pages

  Cunnington, Ryan H ^a   Wang, Baiqiu ^b   Ghavami, Saeid ^a   Bathe, Krista L ^a   Rattan, Sunil G ^a   Dixon, Ian M C ^a  

^a UNIVERSITY OF MANITOBA   (Canada)

^b HD Biosciences   (China)

Author keywords

Cardiac fibrosis; Collagen; Smad2

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; COLLAGEN TYPE 1; ONCOPROTEIN; PROTEIN C SKI; RECEPTOR REGULATED SMAD PROTEIN; RECEPTOR REGULATED SMAD PROTEIN 2; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL FUNCTION; CELL NUCLEUS; CELL SECRETION; CYTOPLASM; FIBROBLAST; GENE OVEREXPRESSION; GENETIC TRANSFECTION; HEART INFARCTION; HEART MUSCLE CELL; MALE; MYOFIBROBLAST; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RAT;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; APOPTOSIS; CELL DIFFERENTIATION; CELL SURVIVAL; FIBROSIS; GENE EXPRESSION REGULATION; MYOCARDIAL CONTRACTION; MYOCARDIUM; MYOFIBROBLASTS; PROTO-ONCOGENE PROTEINS; RATS; SMAD2 PROTEIN; TRANSFORMING GROWTH FACTOR BETA1;

ADENOVIRIDAE;

EID: 78651368993     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00050.2010     Document Type: Article

References (54)

1. Berk M, Desai SY, Heyman HC, Colmenares C. Mice lacking the ski proto-oncogene have defects in neurulation, craniofacial, patterning, and skeletal muscle development. Genes Dev 11: 2029-2039, 1997.
2. Bujak M, Ren G, Kweon HJ, Dobaczewski M, Reddy A, Taffet G, Wang XF, Frangogiannis NG. Essential role of Smad3 in infarct healing and in the pathogenesis of cardiac remodeling. Circulation 116: 2127-2138, 2007.
3. Burstein B, Libby E, Calderone A, Nattel S. Differential behaviors of atrial versus ventricular fibroblasts: a potential role for platelet-derived growth factor in atrial-ventricular remodeling differences. Circulation 117: 1630-1641, 2008.
4. Chang HY, Chi JT, Dudoit S, Bondre C, van de RM, Botstein D, Brown PO. Diversity, topographic differentiation, and positional memory in human fibroblasts. Proc Natl Acad Sci USA 99: 12877-12882, 2002.
5. Claycomb WC, Lanson NA Jr. Proto-oncogene expression in proliferating and differentiating cardiac and skeletal muscle. Biochem J 247: 701-706, 1987.
6. Cleutjens JP, Verluyten MJ, Smits JF, Daemen MJ. Collagen remodeling after myocardial infarction in the rat heart. Am J Pathol 147: 325-338, 1995.
7. Colmenares C, Stavnezer E. Structure and activities of the ski oncogene. Semin Cancer Biol 1: 383-387, 1990.
8. Darby I, Skalli O, Gabbiani G. Alpha-smooth muscle actin is transiently expressed by myofibroblasts during experimental wound healing. Lab Invest 63: 21-29, 1990.
9. Desmouliere A, Geinoz A, Gabbiani F, 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: 103-111, 1993.
10. Desmouliere A, Redard M, Darby I, Gabbiani G. Apoptosis mediates the decrease in cellularity during the transition between granulation tissue and scar. Am J Pathol 146: 56-66, 1995.
11. Dixon IMC, Lee SL, Dhalla NS. Nitrendipine binding in congestive heart failure due to myocardial infarction. Circ Res 66: 782-788, 1990.
12. Dobaczewski M, Bujak M, Li N, Gonzalez-Quesada C, Mendoza LH, Wang XF, Frangogiannis NG. Smad3 signaling critically regulates fibroblast phenotype and function in healing myocardial infarction. Circ Res 107: 418-428, 2010.
13. Evans RA, Tian YC, Steadman R, Phillips AO. TGF-beta1-mediated fibroblast-myofibroblast terminal differentiation-the role of smad proteins. Exp Cell Res 282: 90-100, 2003.
14. Frangogiannis NG, Michael LH, Entman ML. Myofibroblasts in reper-fused myocardial infarcts express the embryonic form of smooth muscle myosin heavy chain (SMemb). Cardiovasc Res 48: 89-100, 2000.
15. Freed DH, Cunnington RH, Dangerfield AL, Sutton JS, Dixon IM. Emerging evidence for the role of cardiotrophin-1 in cardiac repair in the infarcted heart. Cardiovasc Res 65: 782-792, 2005.
16. Ghavami S, Eshraghi M, Kadkhoda K, Mutawe MM, Maddika S, Bay GH, Wesselborg S, Halayko AJ, Klonisch T, Los M. Role of BNIP3 in TNF-induced cell death-TNF upregulates BNIP3 expression. Biochim Biophys Acta 1793: 546-560, 2009.
17. Ghavami S, Eshragi M, Ande SR, Chazin WJ, Klonisch T, Halayko AJ, McNeill KD, Hashemi M, Kerkhoff C, Los M. S100A8/A9 induces autophagy and apoptosis via ROS-mediated cross-talk between mitochondria and lysosomes that involves BNIP3. Cell Res 20: 314-331, 2010.
18. Ghavami S, Kerkhoff C, Chazin WJ, Kadkhoda K, Xiao W, Zuse A, Hashemi M, Eshraghi M, Schulze-Osthoff K, Klonisch T, Los M. S100A8/9 induces cell death via a novel, RAGE-independent pathway that involves selective release of Smac/DIABLO and Omi/HtrA2. Biochim Biophys Acta 1783: 297-311, 2008.
19. Ghavami S, Mutawe MM, Hauff K, Stelmack GL, Schaafsma D, Sharma P, McNeill KD, Hynes TS, Kung SK, Unruh H, Klonisch T, Hatch GM, Los M, Halayko AJ. Statin-triggered cell death in primary human lung mesenchymal cells involves p53-PUMA and release of Smac and Omi but not cytochrome c. Biochim Biophys Acta 1803: 452-467, 2010.
20. Greenberg RS, Bernstein AM, Benezra M, Gelman IH, Taliana L, Masur SK. FAK-dependent regulation of myofibroblast differentiation. FASEB J 20: 1006-1008, 2006.
21. Hao J, Wang B, Jones SC, Jassal DS, Dixon IMC. Interaction between angiotensin II and Smad proteins in fibroblasts in failing heart and in vitro. Am J Physiol Heart Circ Physiol 279: H3020-H3030, 2000.
22. Hao J, Ju H, Zhao S, Junaid A, Scammell-LaFleur T, Dixon IM. Elevation of expression of Smads 2, 3, and 4, decorin and TGF-beta in the chronic phase of myocardial infarct scar healing. J Mol Cell Cardiol 31: 667-678, 1999.
23. Hashemi M, Ghavami S, Eshraghi M, Booy EP, Los M. Cytotoxic effects of intra and extracellular zinc chelation on human breast cancer cells. Eur J Pharmacol 557: 9-19, 2007.
24. Hinz B, Celetta G, Tomasek JJ, Gabbiani G, Chaponnier C. Alpha-smooth muscle actin expression upregulates fibroblast contractile activity. Mol Biol Cell 12: 2730-2741, 2001.
25. Kalluri R, Zeisberg M. Fibroblasts in cancer. Nat Rev Cancer 6: 392-401, 2006.
26. Kavsak P, Rasmussen RK, Causing CG, Bonni S, Zhu H, Thomsen GH, Wrana JL. Smad7 binds to Smurf2 to form an E3 ubiquitin ligase that targets the TGF beta receptor for degradation. Mol Cell 6: 1365-1375, 2000.
27. Kuwahara K, Saito Y, Harada M, Ishikawa M, Ogawa E, Miyamoto Y, Hamanaka I, Kamitani S, Kajiyama N, Takahashi N, Nakagawa O, Masuda I, Nakao K. Involvement of cardiotrophin-1 in cardiac myocytenonmyocyte interactions during hypertrophy of rat cardiac myocytes in vitro. Circulation 100: 1116-1124, 1999.
28. Leslie KO, Taatjes DJ, Schwarz J, vonTurkovich M, Low RB. Cardiac myofibroblasts express alpha smooth muscle actin during right ventricular pressure overload in the rabbit. Am J Pathol 139: 207-216, 1991.
29. Liu X, Li P, Chen XY, Zhou YG. c-Ski promotes skin fibroblast proliferation but decreases type I collagen: implications for wound healing and scar formation. Clin Exp Dermatol 35: 417-424, 2009.
30. Lyons GE, Micales BK, Herr MJ, Horrigan SK, Namciu S, Shardy D, Stavnezer E. Protooncogene c-ski is expressed in both proliferating and postmitotic neuronal populations. Dev Dyn 201: 354-365, 1994.
31. Marcelain K, Hayman MJ. The Ski oncoprotein is upregulated and localized at the centrosomes and mitotic spindle during mitosis. Oncogene 24: 4321-4329, 2005.
32. Masur SK, Dewal HS, Dinh TT, Erenburg I, Petridou S. Myofibroblasts differentiate from fibroblasts when plated at low density. Proc Natl Acad Sci USA 93: 4219-4223, 1996.
33. Montesano R, Orci L. Transforming growth factor beta stimulates collagen-matrix contraction by fibroblasts: implications for wound healing. Proc Natl Acad Sci USA 85: 4894-4897, 1988.
34. Nagano Y, Mavrakis KJ, Lee KL, Fujii T, Koinuma D, Sase H, Yuki K, Isogaya K, Saitoh M, Imamura T, Episkopou V, Miyazono K, Miyazawa K. Arkadia induces degradation of SnoN and c-Ski to enhance transforming growth factor-beta signaling. J Biol Chem 282: 20492-20501, 2007.
35. Nagata M, Goto K, Ehata S, Kobayashi N, Saitoh M, Miyoshi H, Imamura T, Miyazawa K, Miyazono K. Nuclear and cytoplasmic c-Ski differently modulate cellular functions. Genes Cells 11: 1267-1280, 2006.
36. Nagata M, Nagata S, Yuki K, Isogaya K, Saitoh M, Miyazono K, Miyazawa K. Identification of a phosphorylation site in c-Ski as serine 515. J Biochem 148: 423-427, 2010.
37. Nakao A, Imamura T, Souchelnytskyi S, Kawabata M, Ishisaki A, Oeda E, Tamaki K, Hanai J, Heldin CH, Miyazono K, ten Dijke P. TGF-beta receptor-mediated signalling through Smad2, Smad3 and Smad4. EMBO J 16: 5353-5362, 1997.
38. Namciu S, Lyons GE, Micales BK, Heyman HC, Colmenares C, Stavnezer E. Enhanced expression of mouse c-ski accompanies terminal skeletal muscle differentiation in vivo and in vitro. Dev Dyn 204: 291-300, 1995.
39. Peterson DJ, Ju H, Hao J, Panagia M, Chapman DC, Dixon IM. Expression of Gi-2 alpha and Gs alpha in myofibroblasts localized to the infarct scar in heart failure due to myocardial infarction. Cardiovasc Res 41: 575-585, 1999.
40. Petrov VV, Fagard RH, Lijnen PJ. Transforming growth factor-beta(1) induces angiotensin-converting enzyme synthesis in rat cardiac fibroblasts during their differentiation to myofibroblasts. J Renin Angiotensin Aldosterone Syst 1: 342-352, 2000.
41. Prunier C, Pessah M, Ferrand N, Seo SR, Howe P, Atfi A. The oncoprotein Ski acts as an antagonist of transforming growth factor-beta signaling by suppressing Smad2 phosphorylation. J Biol Chem 278: 26249-26257, 2003.
42. Santiago JJ, Dangerfield AL, Rattan SG, Bathe KL, Cunnington RH, Raizman JE, Bedosky KM, Freed DH, Kardami E, Dixon IM. Cardiac fibroblast to myofibroblast differentiation in vivo and in vitro: expression of focal adhesion components in neonatal and adult rat ventricular myofibroblasts. Dev Dyn 239: 1573-1584, 2010.
43. Serini G, Bochaton-Piallat ML, Ropraz P, Geinoz A, Borsi L, Zardi L, Gabbiani G. The fibronectin domain ED-A is crucial for myofibroblastic phenotype induction by transforming growth factor-beta1. J Cell Biol 142: 873-881, 1998.
44. Smith PK, Krohn RI, Hermanson GT, Mallia AK, Gartner FH, Provenzano MD, Fujimoto EK, Goeke NM, Olson BJ, Klenk DC. Measurement of protein using bicinchoninic acid. Anal Biochem 150: 76-85, 1985.
45. Sutrave P, Copeland TD, Showalter SD, Hughes SH. Characterization of chicken c-ski oncogene products expressed by retrovirus vectors. Mol Cell Biol 10: 3137-3144, 1990.
46. Suzuki H, Yagi K, Kondo M, Kato M, Miyazono K, Miyazawa K. c-Ski inhibits the TGF-beta signaling pathway through stabilization of inactive Smad complexes on Smad-binding elements. Oncogene 23: 5068-5076, 2004.
47. Thum T, Gross C, Fiedler J, Fischer T, Kissler S, Bussen M, Galuppo P, Just S, Rottbauer W, Frantz S, Castoldi M, Soutschek J, Koteliansky V, Rosenwald A, Basson MA, Licht JD, Pena JT, Rouhanifard SH, Muckenthaler MU, Tuschl T, Martin GR, Bauersachs J, Engelhardt S. MicroRNA-21 contributes to myocardial disease by stimulating MAP kinase signalling in fibroblasts. Nature 456: 980-984, 2008.
48. Van den Borne SW, Diez J, Blankesteijn WM, Verjans J, Hofstra L, Narula J. Myocardial remodeling after infarction: the role of myofibroblasts. Nat Rev Cardiol 7: 30-37, 2010.
49. Wang B, Hao J, Jones SC, Yee MS, Roth JC, Dixon IM. Decreased Smad 7 expression contributes to cardiac fibrosis in the infarcted rat heart. Am J Physiol Heart Circ Physiol 282: H1685-H1696, 2002.
50. Wang B, Omar A, Angelovska T, Drobic V, Rattan SG, Jones SC, Dixon IM. Regulation of collagen synthesis by inhibitory Smad7 in cardiac myofibroblasts. Am J Physiol Heart Circ Physiol 293: H1282-H1290, 2007.
51. Wang J, Chen H, Seth A, McCulloch CA. Mechanical force regulation of myofibroblast differentiation in cardiac fibroblasts. Am J Physiol Heart Circ Physiol 285: H1871-H1881, 2003.
52. Wang J, Seth A, McCulloch CA. Force regulates smooth muscle actin in cardiac fibroblasts. Am J Physiol Heart Circ Physiol 279: H2776-H2785, 2000.
53. Willems IE, Havenith MG, De Mey JG, Daemen MJ. The alpha-smooth muscle actin-positive cells in healing human myocardial scars. Am J Pathol 145: 868-75, 1994.
54. Wrana JL. The secret life of Smad4. Cell 136: 13-14, 2009.