Akt1 mediates α-smooth muscle actin expression and myofibroblast differentiation via myocardin and serum response factor

Journal of Biological Chemistry

Volumn 288, Issue 46, 2013, Pages 33483-33493

  Abdalla, Maha ^a,b   Goc, Anna ^a,b   Segar, Lakshman ^a,b   Somanath, Payaningal R ^a,b,c  

^a UNIVERSITY OF GEORGIA   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c MEDICAL COLLEGE OF GEORGIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CONTRACTILE FORCE; GENE TRANSCRIPTION FACTORS; MAMMALIAN TARGET; MOUSE EMBRYONIC FIBROBLASTS; SERUM RESPONSE FACTORS; SMOOTH MUSCLE ACTINS; SUSTAINED ACTIVATION; THERAPEUTIC TARGETS;

BODY FLUIDS; CELL CULTURE; FIBROBLASTS; MUSCLE;

PROTEINS;

ALPHA SMOOTH MUSCLE ACTIN; FIBRONECTIN; MYOCARDIN; PROTEIN AKT1; PROTEIN KINASE B; SERUM RESPONSE FACTOR; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME INACTIVATION; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; MOUSE; MYOFIBROBLAST; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; SIGNAL TRANSDUCTION;

AKT; DIFFERENTIATION; FIBRONECTIN; FIBROSIS; MYOCARDIN; MYOFIBROBLAST; SERUM RESPONSE FACTOR;

ACTINS; ANIMALS; CELL DIFFERENTIATION; GENE EXPRESSION REGULATION; MICE; MICE, KNOCKOUT; MYOFIBROBLASTS; NIH 3T3 CELLS; NUCLEAR PROTEINS; PROTO-ONCOGENE PROTEINS C-AKT; SERUM RESPONSE FACTOR; TRANS-ACTIVATORS; TRANSFORMING GROWTH FACTOR BETA;

EID: 84887842825     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.504290     Document Type: Article

References (51)

1. Gabbiani, G., Ryan, G. B., and Majne, G. (1971) Presence of modified fibroblasts in granulation tissue and their possible role in wound contraction. Experientia 27, 549-550
2. Majno, G., Gabbiani, G., Hirschel, B. J., Ryan, G. B., and Statkov, P. R. (1971) Contraction of granulation tissue in vitro. Similarity to smooth muscle. Science 173, 548-550
3. Tomasek, J. J., Gabbiani, G., Hinz, B., Chaponnier, C., and Brown, R. A. (2002) Nature Rev. 3, 349-363
4. Hinz, B., and Gabbiani, G. (2003) Mechanisms of force generation and transmission by myofibroblasts. Curr. Opin. Biotechnol. 14, 538-546
5. Hinz, B. (2007) Formation and function of the myofibroblast during tissue repair. J. Invest. Dermatol. 127, 526-537
6. Hinz, B., Phan, S. H., Thannickal, V. J., Prunotto, M., Desmoulière, A., Varga, J., De Wever, O., Mareel, M., and Gabbiani, G. (2012) Recent developments in myofibroblast biology. Paradigms for connective tissue remodeling. Am. J. Pathol. 180, 1340-1355
7. Hinz, B., Celetta, G., Tomasek, J. J., Gabbiani, G., and Chaponnier, C. (2001) α-Smooth muscle actin expression up-regulates fibroblast contractile activity. Mol. Biol. Cell 12, 2730-2741
8. Zhang, H. Y., and Phan, S. H. (1999) Inhibition of myofibroblast apoptosis by transforming growth factor β1. Am. J. Respir. Cell Mol. Biol. 21, 658-665
9. Darby, I. A., and Hewitson, T. D. (2007) Fibroblast differentiation in wound healing and fibrosis. Int. Rev. Cytol. 257, 143-179
10. Phan, S. H. (2002) The myofibroblast in pulmonary fibrosis. Chest 122, 286S-289S
11. Thannickal, V. J., Lee, D. Y., White, E. S., Cui, Z., Larios, J. M., Chacon, R., Horowitz, J. C., Day, R. M., and Thomas, P. E. (2003) Myofibroblast differentiation by transforming growth factor-β1 is dependent on cell adhesion and integrin signaling via focal adhesion kinase. J. Biol. Chem. 278, 12384-12389
12. Desmoulière, A., Geinoz, A., Gabbiani, F., and Gabbiani, G. (1993) Transforming growth factor-β 1 induces α-smooth muscle actin expression in granulation tissue myofibroblasts and in quiescent and growing cultured fibroblasts. J. Cell Biol. 122, 103-111
13. Rønnov-Jessen, L., and Petersen, O. W. (1993) Induction of α-smooth muscle actin by transforming growth factor-β1 in quiescent human breast gland fibroblasts. Implications for myofibroblast generation in breast neoplasia. Lab. Invest. 68, 696-707
14. Mattey, D. L., Dawes, P. T., Nixon, N. B., and Slater, H. (1997) Transforming growth factor β1 and interleukin 4 induced α-smooth muscle actin expression and myofibroblast-like differentiation in human synovial fibroblasts in vitro. Modulation by basic fibroblast growth factor. Ann. Rheum. Dis. 56, 426-431
15. Maltseva, O., Folger, P., Zekaria, D., Petridou, S., and Masur, S. K. (2001) Fibroblast growth factor reversal of the corneal myofibroblast phenotype. Invest. Ophthalmol. Vis. Sci. 42, 2490-2495
16. Zhao, X. H., Laschinger, C., Arora, P., Szászi, K., Kapus, A., and McCulloch, C. A. (2007) Force activates smooth muscle α-actin promoter activity through the Rho signaling pathway. J. Cell Sci. 120, 1801-1809
17. Akhmetshina, A., Dees, C., Pileckyte, M., Szucs, G., Spriewald, B. M., Zwerina, J., Distler, O., Schett, G., and Distler, J. H. (2008) Rho-associated kinases are crucial for myofibroblast differentiation and production of extracellular matrix in scleroderma fibroblasts. Arthritis Rheum. 58, 2553-2564
18. Wang, D. Z., Li, S., Hockemeyer, D., Sutherland, L., Wang, Z., Schratt, G., Richardson, J. A., Nordheim, A., and Olson, E. N. (2002) Potentiation of serum response factor activity by a family of myocardin-related transcription factors. Proc. Natl. Acad. Sci. U. S. A. 99, 14855-14860
19. Fan, L., Sebe, A., Péterfi, Z., Masszi, A., Thirone, A. C., Rotstein, O. D., Nakano, H., McCulloch, C. A., Szászi, K., Mucsi, I., and Kapus, A. (2007) Cell contact-dependent regulation of epithelial-myofibroblast transition via the rho-rho kinase-phosphomyosin pathway. Mol. Biol. Cell 18, 1083-1097
20. Miralles, F., Posern, G., Zaromytidou, A. I., and Treisman, R. (2003) Actin dynamics control SRF activity by regulation of its coactivator MAL. Cell 113, 329-342
21. Jeon, E. S., Moon, H. J., Lee, M. J., Song, H. Y., Kim, Y. M., Bae, Y. C., Jung, J. S., and Kim, J. H. (2006) Sphingosylphosphorylcholine induces differentiation of human mesenchymal stem cells into smooth-muscle-like cells through a TGF-β-dependent mechanism. J. Cell Sci. 119, 4994-5005
22. Qiu, P., Feng, X. H., and Li, L. (2003) Interaction of Smad3 and SRFassociated complex mediates TGF-β1 signals to regulate SM22 transcription during myofibroblast differentiation. J. Mol. Cell. Cardiol. 35, 1407-1420
23. Sandbo, N., Qin, Y., Taurin, S., Hogarth, D. K., Kreutz, B., and Dulin, N. O. (2005) Regulation of serum response factor-dependent gene expression by proteasome inhibitors. Mol. Pharmacol. 67, 789-797
24. Sandbo, N., Lau, A., Kach, J., Ngam, C., Yau, D., and Dulin, N. O. (2011) Delayed stress fiber formation mediates pulmonary myofibroblast differentiation in response to TGF-β. Am. J. Physiol. Lung Cell. Mol. Physiol. 301, L656-666
25. Wang, D., Chang, P. S., Wang, Z., Sutherland, L., Richardson, J. A., Small, E., Krieg, P. A., and Olson, E. N. (2001) Activation of cardiac gene expression by myocardin, a transcriptional cofactor for serum response factor. Cell 105, 851-862
26. Small, E. M., Thatcher, J. E., Sutherland, L. B., Kinoshita, H., Gerard, R. D., Richardson, J. A., Dimaio, J. M., Sadek, H., Kuwahara, K., and Olson, E. N. (2010) Myocardin-related transcription factor-α controls myofibroblast activation and fibrosis in response to myocardial infarction. Circ. Res. 107, 294-304
27. Liu, Z. P., Wang, Z., Yanagisawa, H., and Olson, E. N. (2005) Phenotypic modulation of smooth muscle cells through interaction of Foxo4 and myocardin. Dev. Cell 9, 261-270
28. Chen, J., Somanath, P. R., Razorenova, O., Chen, W. S., Hay, N., Bornstein, P., and Byzova, T. V. (2005) Akt1 regulates pathological angiogenesis, vascular maturation and permeability in vivo. Nat. Med. 11, 1188-1196
29. Somanath, P. R., and Byzova, T. V. (2009) 14-3-3β-Rac1-p21 activated kinase signaling regulates Akt1-mediated cytoskeletal organization, lamellipodia formation and fibronectin matrix assembly. J. Cell. Physiol. 218, 394-404
30. Somanath, P. R., Kandel, E. S., Hay, N., and Byzova, T. V. (2007) Akt1 signaling regulates integrin activation, matrix recognition, and fibronectin assembly. J. Biol. Chem. 282, 22964-22976
31. Goc, A., Choudhary, M., Byzova, T. V., and Somanath, P. R. (2011) TGF β- and bleomycin-induced extracellular matrix synthesis is mediated through Akt and mammalian target of rapamycin (mTOR). J. Cell. Physiol. 226, 3004-3013
32. Shi-Wen, X., Chen, Y., Denton, C. P., Eastwood, M., Renzoni, E. A., Bou- Gharios, G., Pearson, J. D., Dashwood, M., du Bois, R. M., Black, C. M., Leask, A., and Abraham, D. J. (2004) Endothelin-1 promotes myofibroblast induction through the ETA receptor via a rac/phosphoinositide 3-kinase/ Akt-dependent pathway and is essential for the enhanced contractile phenotype of fibrotic fibroblasts. Mol. Biol. Cell 15, 2707-2719
33. Jun, J. B., Kuechle, M., Min, J., Shim, S. C., Kim, G., Montenegro, V., Korn, J. H., and Elkon, K. B. (2005) Scleroderma fibroblasts demonstrate enhanced activation of Akt (protein kinase B) in situ. J. Investig. Dermatol. 124, 298-303
34. Guo, W., Shan, B., Klingsberg, R. C., Qin, X., and Lasky, J. A. (2009) Abrogation of TGF-β1-induced fibroblast-myofibroblast differentiation by histone deacetylase inhibition. Am. J. Physiol. Lung Cell Mol. Physiol. 297, L864-870
35. He, Z., Zhu, Y., and Jiang, H. (2009) Toll-like receptor 4 mediates lipopolysaccharide- induced collagen secretion by phosphoinositide 3-kinase- Akt pathway in fibroblasts during acute lung injury. J. Recept. Signal. Transduct. Res. 29, 119-125
36. Horowitz, J. C., Rogers, D. S., Sharma, V., Vittal, R., White, E. S., Cui, Z., and Thannickal, V. J. (2007) Combinatorial activation of FAK and AKT by transforming growth factor-β1 confers an anoikis-resistant phenotype to myofibroblasts. Cell. Signal. 19, 761-771
37. Wang, Z., Wang, D. Z., Pipes, G. C., and Olson, E. N. (2003) Myocardin is a master regulator of smooth muscle gene expression. Proc. Natl. Acad. Sci. U.S.A. 100, 7129-7134
38. Stenmark, K. R., Fagan, K. A., and Frid, M. G. (2006) Hypoxia-induced pulmonary vascular remodeling. Cellular and molecular mechanisms. Circ. Res. 99, 675-691
39. Short, M., Nemenoff, R. A., Zawada, W. M., Stenmark, K. R., and Das, M. (2004) Hypoxia induces differentiation of pulmonary artery adventitial fibroblasts into myofibroblasts. Am. J. Physiol. Cell Physiol. 286, C416-425
40. Abdalla, M., Goc, A., and Somanath, P. R. (2012) NOVA Publisher Chapter 7
41. Nicholson, A. G., Fulford, L. G., Colby, T. V., du Bois, R. M., Hansell, D. M., and Wells, A. U. (2002) The relationship between individual histologic features and disease progression in idiopathic pulmonary fibrosis. Am. J. Respir. Crit. Care Med. 166, 173-177
42. Meyer-Ter-Vehn, T., Gebhardt, S., Sebald, W., Buttmann, M., Grehn, F., Schlunck, G., and Knaus, P. (2006) p38 inhibitors prevent TGF-β-induced myofibroblast transdifferentiation in human tenon fibroblasts. Invest. Ophthalmol. Vis. Sci. 47, 1500-1509
43. White, E. S., Atrasz, R. G., Hu, B., Phan, S. H., Stambolic, V., Mak, T. W., Hogaboam, C. M., Flaherty, K. R., Martinez, F. J., Kontos, C. D., and Toews, G. B. (2006) Negative regulation of myofibroblast differentiation by PTEN (phosphatase and tensin homolog deleted on chromosome 10). Am. J. Respir. Crit. Care Med. 173, 112-121
44. Sandbo, N., Kregel, S., Taurin, S., Bhorade, S., and Dulin, N. O. (2009) Critical role of serum response factor in pulmonary myofibroblast differentiation induced by TGF-β. Am. J. Respir. Cell Mol. Biol. 41, 332-338
45. Anderson, S., DiCesare, L., Tan, I., Leung, T., and SundarRaj, N. (2004) Rho-mediated assembly of stress fibers is differentially regulated in corneal fibroblasts and myofibroblasts. Exp. Cell Res. 298, 574-583
46. Pipes, G. C., Creemers, E. E., and Olson, E. N. (2006) The myocardin family of transcriptional coactivators. Versatile regulators of cell growth, migration, and myogenesis. Genes Dev. 20, 1545-1556
47. Greenberg, R. S., Bernstein, A. M., Benezra, M., Gelman, I. H., Taliana, L., and Masur, S. K. (2006) FAK-dependent regulation of myofibroblast differentiation. FASEB J. 20, 1006-1008
48. Kohan, M., Muro, A. F., White, E. S., and Berkman, N. (2010) EDA-containing cellular fibronectin induces fibroblast differentiation through binding to α4β7 integrin receptor and MAPK/Erk 1/2-dependent signaling. FASEB J. 24, 4503-4512
49. Blaustein, M., Pelisch, F., Tanos, T., Muñoz, M. J., Wengier, D., Quadrana, L., Sanford, J. R., Muschietti, J. P., Kornblihtt, A. R., Cáceres, J. F., Coso,O. A., and Srebrow, A. (2005) Concerted regulation of nuclear and cytoplasmic activities of SR proteins by AKT. Nat. Struct. Mol. Biol. 12,1037-1044
50. White, E. S., Sagana, R. L., Booth, A. J., Yan, M., Cornett, A. M., Bloomheart, C. A., Tsui, J. L., Wilke, C. A., Moore, B. B., Ritzenthaler, J. D., Roman, J., and Muro, A. F. (2010) Control of fibroblast fibronectin expression and alternative splicing via the PI3K/Akt/mTOR pathway. Exp. Cell Res. 316, 2644-2653
51. Karni, R., Hippo, Y., Lowe, S. W., and Krainer, A. R. (2008) The splicingfactor oncoprotein SF2/ASF activates mTORC1. Proc. Natl. Acad. Sci. U.S.A. 105, 15323-15327