Molecular networks underlying myofibroblast fate and fibrosis

Journal of Molecular and Cellular Cardiology

Volumn 97, Issue , 2016, Pages 153-161

  Stempien Otero, April ^a   Kim, Deok Ho ^b   Davis, Jennifer ^a,b  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^b University of Washington   (United States)

Author keywords

Actin cytoskeleton; Differentiation; Fibrosis; Mitogen activated protein kinases; Myofibroblast; RNA binding proteins; TGF ; TRP channels

Indexed keywords

CALCINEURIN; CALCIUM ION; MITOGEN ACTIVATED PROTEIN KINASE P38; MYOCARDIN RELATED TRANSCRIPTION FACTOR; RHO KINASE; RNA BINDING PROTEIN; ROCK1 PROTEIN; ROCK2 PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTOME; TRANSFORMING GROWTH FACTOR BETA; TRANSIENT RECEPTOR POTENTIAL CHANNEL 6; UNCLASSIFIED DRUG; BIOLOGICAL MARKER;

ACTIN FILAMENT; CALCIUM SIGNALING; CELL FATE; CELL FUNCTION; CELL HETEROGENEITY; CELL POPULATION; HEART MUSCLE FIBROSIS; HUMAN; INTRACELLULAR SIGNALING; MECHANOTRANSDUCTION; MOLECULAR DYNAMICS; MOLECULAR PATHOLOGY; MYOFIBROBLAST; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; REGULATORY MECHANISM; REVIEW; STEM CELL; TRANSCRIPTION REGULATION; ANIMAL; CELL DIFFERENTIATION; CYTOLOGY; FIBROSIS; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; PHENOTYPE; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; BIOMARKERS; CELL DIFFERENTIATION; FIBROSIS; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORKS; HUMANS; MYOFIBROBLASTS; PHENOTYPE; SIGNAL TRANSDUCTION;

EID: 84969697684     PISSN: 00222828     EISSN: 10958584     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2016.05.002     Document Type: Review

References (124)

1. Bruder O., Wagner A., Jensen C.J., Schneider S., Ong P., Kispert E.M., et al. Myocardial scar visualized by cardiovascular magnetic resonance imaging predicts major adverse events in patients with hypertrophic cardiomyopathy. J. Am. Coll. Cardiol. 2010, 56:875-887.
2. Elliott P.M., Poloniecki J., Dickie S., Sharma S., Monserrat L., Varnava A., et al. Sudden death in hypertrophic cardiomyopathy: identification of high risk patients. J. Am. Coll. Cardiol. 2000, 36:2212-2218.
3. Maron B.J., Olivotto I., Spirito P., Casey S.A., Bellone P., Gohman T.E., et al. Epidemiology of hypertrophic cardiomyopathy-related death: revisited in a large non-referral-based patient population. Circulation 2000, 102:858-864.
4. O'Hanlon R., Grasso A., Roughton M., Moon J.C., Clark S., Wage R., et al. Prognostic significance of myocardial fibrosis in hypertrophic cardiomyopathy. J. Am. Coll. Cardiol. 2010, 56:867-874.
5. Hinz B., Phan S.H., Thannickal V.J., Galli A., Bochaton-Piallat M.L., Gabbiani G. The myofibroblast: one function, multiple origins. Am. J. Pathol. 2007, 170:1807-1816.
6. Tomasek J.J., Gabbiani G., Hinz B., Chaponnier C., Brown R.A. Myofibroblasts and mechano-regulation of connective tissue remodelling. Nat. Rev. Mol. Cell Biol. 2002, 3:349-363.
7. Gabbiani G. The myofibroblast in wound healing and fibrocontractive diseases. J. Pathol. 2003, 200:500-503.
8. Sun Y., Weber K.T. Infarct scar: a dynamic tissue. Cardiovasc. Res. 2000, 46:250-256.
9. Hinz B. Tissue stiffness, latent TGF-beta1 activation, and mechanical signal transduction: implications for the pathogenesis and treatment of fibrosis. Curr. Rheumatol. Rep. 2009, 11:120-126.
10. Hinz B. The myofibroblast: paradigm for a mechanically active cell. J. Biomech. 2010, 43:146-155.
11. Muthusubramaniam L., Zaitseva T., Paukshto M., Martin G., Desai T. Effect of collagen nanotopography on keloid fibroblast proliferation and matrix synthesis: implications for dermal wound healing. Tissue Eng. A 2014, 20:2728-2736.
12. Wang H., Haeger S.M., Kloxin A.M., Leinwand L.A., Anseth K.S. Redirecting valvular myofibroblasts into dormant fibroblasts through light-mediated reduction in substrate modulus. PLoS One 2012, 7.
13. Wang H., Tibbitt M.W., Langer S.J., Leinwand L.A., Anseth K.S. Hydrogels preserve native phenotypes of valvular fibroblasts through an elasticity-regulated PI3K/AKT pathway. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:19336-19341.
14. Suzuki J., Isobe M., Aikawa M., Kawauchi M., Shiojima I., Kobayashi N., et al. Nonmuscle and smooth muscle myosin heavy chain expression in rejected cardiac allografts. A study in rat and monkey models. Circulation 1996, 94:1118-1124.
15. Rice N.A., Leinwand L.A. Skeletal myosin heavy chain function in cultured lung myofibroblasts. J. Cell Biol. 2003, 163:119-129.
16. Serini G., Bochaton-Piallat M.L., Ropraz P., Geinoz A., Borsi L., Zardi L., et al. The fibronectin domain ED-A is crucial for myofibroblastic phenotype induction by transforming growth factor-beta1. J. Cell Biol. 1998, 142:873-881.
17. White E.S., Muro A.F. Fibronectin splice variants: understanding their multiple roles in health and disease using engineered mouse models. IUBMB Life 2011, 63:538-546.
18. Hinz B. Masters and servants of the force: the role of matrix adhesions in myofibroblast force perception and transmission. Eur. J. Cell Biol. 2006, 85:175-181.
19. Arslan F., Smeets M.B., Riem Vis P.W., Karper J.C., Quax P.H., Bongartz L.G., et al. Lack of fibronectin-EDA promotes survival and prevents adverse remodeling and heart function deterioration after myocardial infarction. Circ. Res. 2011, 108:582-592.
20. Hinz B. Formation and function of the myofibroblast during tissue repair. J. Investig. Dermatol. 2007, 127:526-537.
21. Hinz B., Pittet P., Smith-Clerc J., Chaponnier C., Meister J.J. Myofibroblast development is characterized by specific cell-cell adherens junctions. Mol. Biol. Cell 2004, 15:4310-4320.
22. Davis J., Burr A.R., Davis G.F., Birnbaumer L., Molkentin J.D. A TRPC6-dependent pathway for myofibroblast transdifferentiation and wound healing in vivo. Dev. Cell 2012, 23:705-715.
23. Acharya A., Baek S.T., Huang G., Eskiocak B., Goetsch S., Sung C.Y., et al. The bHLH transcription factor Tcf21 is required for lineage-specific EMT of cardiac fibroblast progenitors. Development 2012, 139:2139-2149.
24. Moore-Morris T., Guimaraes-Camboa N., Banerjee I., Zambon A.C., Kisseleva T., Velayoudon A., et al. Resident fibroblast lineages mediate pressure overload-induced cardiac fibrosis. J. Clin. Invest. 2014, 124:2921-2934.
25. Furtado M.B., Costa M.W., Pranoto E.A., Salimova E., Pinto A.R., Lam N.T., et al. Cardiogenic genes expressed in cardiac fibroblasts contribute to heart development and repair. Circ. Res. 2014, 114:1422-1434.
26. Ali S.R., Ranjbarvaziri S., Talkhabi M., Zhao P., Subat A., Hojjat A., et al. Developmental heterogeneity of cardiac fibroblasts does not predict pathological proliferation and activation. Circ. Res. 2014, 115:625-635.
27. Pinto A.R., Ilinykh A., Ivey M.J., Kuwabara J.T., D'Antoni M., Debuque R.J., et al. Revisiting cardiac cellular composition. Circ. Res. 2015.
28. Crawford J.R., Haudek S.B., Cieslik K.A., Trial J., Entman M.L. Origin of developmental precursors dictates the pathophysiologic role of cardiac fibroblasts. J. Cardiovasc. Transl. Res. 2012, 5:749-759.
29. Haudek S.B., Cheng J., Du J., Wang Y., Hermosillo-Rodriguez J., Trial J., et al. Monocytic fibroblast precursors mediate fibrosis in angiotensin-II-induced cardiac hypertrophy. J. Mol. Cell. Cardiol. 2010, 49:499-507.
30. Haudek S.B., Trial J., Xia Y., Gupta D., Pilling D., Entman M.L. Fc receptor engagement mediates differentiation of cardiac fibroblast precursor cells. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:10179-10184.
31. Haudek S.B., Xia Y., Huebener P., Lee J.M., Carlson S., Crawford J.R., et al. Bone marrow-derived fibroblast precursors mediate ischemic cardiomyopathy in mice. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:18284-18289.
32. Moeller A., Gilpin S.E., Ask K., Cox G., Cook D., Gauldie J., et al. Circulating fibrocytes are an indicator of poor prognosis in idiopathic pulmonary fibrosis. Am. J. Respir. Crit. Care Med. 2009, 179:588-594.
33. Kalluri R., Weinberg R.A. The basics of epithelial-mesenchymal transition. J. Clin. Invest. 2009, 119:1420-1428.
34. Zeisberg E.M., Kalluri R. Origins of cardiac fibroblasts. Circ. Res. 2010, 107:1304-1312.
35. Zeisberg E.M., Tarnavski O., Zeisberg M., Dorfman A.L., McMullen J.R., Gustafsson E., et al. Endothelial-to-mesenchymal transition contributes to cardiac fibrosis. Nat. Med. 2007, 13:952-961.
36. Zhou B., Honor L.B., He H., Ma Q., Oh J.H., Butterfield C., et al. Adult mouse epicardium modulates myocardial injury by secreting paracrine factors. J. Clin. Invest. 2011, 121:1894-1904.
37. Kisseleva T., Cong M., Paik Y., Scholten D., Jiang C., Benner C., et al. Myofibroblasts revert to an inactive phenotype during regression of liver fibrosis. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:9448-9453.
38. Snider P., Standley K.N., Wang J., Azhar M., Doetschman T., Conway S.J. Origin of cardiac fibroblasts and the role of periostin. Circ. Res. 2009, 105:934-947.
39. Davis J., Molkentin J.D. Myofibroblasts: trust your heart and let fate decide. J. Mol. Cell. Cardiol. 2014, 70:9-18.
40. Takeda N., Manabe I., Uchino Y., Eguchi K., Matsumoto S., Nishimura S., et al. Cardiac fibroblasts are essential for the adaptive response of the murine heart to pressure overload. J. Clin. Invest. 2010, 120:254-265.
41. Oka T., Xu J., Kaiser R.A., Melendez J., Hambleton M., Sargent M.A., et al. Genetic manipulation of periostin expression reveals a role in cardiac hypertrophy and ventricular remodeling. Circ. Res. 2007, 101:313-321.
42. Shimazaki M., Nakamura K., Kii I., Kashima T., Amizuka N., Li M., et al. Periostin is essential for cardiac healing after acute myocardial infarction. J. Exp. Med. 2008, 205:295-303.
43. Davis J., Salomonis N., Ghearing N., Lin S.C., Kwong J.Q., Mohan A., et al. MBNL1-mediated regulation of differentiation RNAs promotes myofibroblast transformation and the fibrotic response. Nat. Commun. 2015, 6:10084.
44. Qian L., Huang Y., Spencer C.I., Foley A., Vedantham V., Liu L., et al. In vivo reprogramming of murine cardiac fibroblasts into induced cardiomyocytes. Nature 2012, 485:593-598.
45. VanDusen N.J., Vincentz J.W., Firulli B.A., Howard M.J., Rubart M., Firulli A.B. Loss of Hand2 in a population of Periostin lineage cells results in pronounced bradycardia and neonatal death. Dev. Biol. 2014, 388:149-158.
46. Chu P.Y., Mariani J., Finch S., McMullen J.R., Sadoshima J., Marshall T., et al. Bone marrow-derived cells contribute to fibrosis in the chronically failing heart. Am. J. Pathol. 2010, 176:1735-1742.
47. Ieronimakis N., Hays A.L., Janebodin K., Mahoney W.M., Duffield J.S., Majesky M.W., et al. Coronary adventitial cells are linked to perivascular cardiac fibrosis via TGFbeta1 signaling in the mdx mouse model of Duchenne muscular dystrophy. J. Mol. Cell. Cardiol. 2013, 63:122-134.
48. Kramann R., Schneider R.K., DiRocco D.P., Machado F., Fleig S., Bondzie P.A., et al. Perivascular Gli1+ progenitors are key contributors to injury-induced organ fibrosis. Cell Stem Cell 2015, 16:51-66.
49. Chang H.Y., Chi J.T., Dudoit S., Bondre C., van de Rijn M., Botstein D., et al. Diversity, topographic differentiation, and positional memory in human fibroblasts. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:12877-12882.
50. Wipff P.J., Rifkin D.B., Meister J.J., Hinz B. Myofibroblast contraction activates latent TGF-beta1 from the extracellular matrix. J. Cell Biol. 2007, 179:1311-1323.
51. Leask A., Abraham D.J. TGF-beta signaling and the fibrotic response. FASEB J. 2004, 18:816-827.
52. Hecker L., Vittal R., Jones T., Jagirdar R., Luckhardt T.R., Horowitz J.C., et al. NADPH oxidase-4 mediates myofibroblast activation and fibrogenic responses to lung injury. Nat. Med. 2009, 15:1077-1081.
53. Bonniaud P., Kolb M., Galt T., Robertson J., Robbins C., Stampfli M., et al. Smad3 null mice develop airspace enlargement and are resistant to TGF-beta-mediated pulmonary fibrosis. J. Immunol. 2004, 173:2099-2108.
54. Dobaczewski M., Bujak M., Li N., Gonzalez-Quesada C., Mendoza L.H., Wang X.F., et al. Smad3 signaling critically regulates fibroblast phenotype and function in healing myocardial infarction. Circ. Res. 2010, 107:418-428.
55. Lal H., Ahmad F., Zhou J., Yu J.E., Vagnozzi R.J., Guo Y., et al. Cardiac fibroblast glycogen synthase kinase-3beta regulates ventricular remodeling and dysfunction in ischemic heart. Circulation 2014, 130:419-430.
56. Koitabashi N., Danner T., Zaiman A.L., Pinto Y.M., Rowell J., Mankowski J., et al. Pivotal role of cardiomyocyte TGF-beta signaling in the murine pathological response to sustained pressure overload. J. Clin. Invest. 2011, 121:2301-2312.
57. Watkins S.J., Jonker L., Arthur H.M. A direct interaction between TGFbeta activated kinase 1 and the TGFbeta type II receptor: implications for TGFbeta signalling and cardiac hypertrophy. Cardiovasc. Res. 2006, 69:432-439.
58. Yu L., Hebert M.C., Zhang Y.E. TGF-beta receptor-activated p38 MAP kinase mediates Smad-independent TGF-beta responses. EMBO J. 2002, 21:3749-3759.
59. Zhang Y.E. Non-Smad pathways in TGF-beta signaling. Cell Res. 2009, 19:128-139.
60. Akhurst R.J., Hata A. Targeting the TGFbeta signalling pathway in disease. Nat. Rev. Drug Discov. 2012, 11:790-811.
61. Bakin A.V., Rinehart C., Tomlinson A.K., Arteaga C.L. p38 mitogen-activated protein kinase is required for TGFbeta-mediated fibroblastic transdifferentiation and cell migration. J. Cell Sci. 2002, 115:3193-3206.
62. Meyer-Ter-Vehn T., Gebhardt S., Sebald W., Buttmann M., Grehn F., Schlunck G., et al. p38 inhibitors prevent TGF-beta-induced myofibroblast transdifferentiation in human tenon fibroblasts. Invest. Ophthalmol. Vis. Sci. 2006, 47:1500-1509.
63. Meyer-Ter-Vehn T., Katzenberger B., Han H., Grehn F., Schlunck G. Lovastatin inhibits TGF-beta-induced myofibroblast transdifferentiation in human tenon fibroblasts. Invest. Ophthalmol. Vis. Sci. 2008, 49:3955-3960.
64. Sato M., Shegogue D., Gore E.A., Smith E.A., McDermott P.J., Trojanowska M. Role of p38 MAPK in transforming growth factor beta stimulation of collagen production by scleroderma and healthy dermal fibroblasts. J. Investig. Dermatol. 2002, 118:704-711.
65. Stambe C., Atkins R.C., Tesch G.H., Masaki T., Schreiner G.F., Nikolic-Paterson D.J. The role of p38alpha mitogen-activated protein kinase activation in renal fibrosis. J. Am. Soc. Nephrol. 2004, 15:370-379.
66. Vepachedu R., Gorska M.M., Singhania N., Cosgrove G.P., Brown K.K., Alam R. Unc119 regulates myofibroblast differentiation through the activation of Fyn and the p38 MAPK pathway. J. Immunol. 2007, 179:682-690.
67. Wang J., Chen H., Seth A., McCulloch C.A. Mechanical force regulation of myofibroblast differentiation in cardiac fibroblasts. Am. J. Physiol. Heart Circ. Physiol. 2003, 285:H1871-H1881.
68. Wang J., Fan J., Laschinger C., Arora P.D., Kapus A., Seth A., et al. Smooth muscle actin determines mechanical force-induced p38 activation. J. Biol. Chem. 2005, 280:7273-7284.
69. Liu Q., Busby J.C., Molkentin J.D. Interaction between TAK1-TAB1-TAB2 and RCAN1-calcineurin defines a signalling nodal control point. Nat. Cell Biol. 2009, 11:154-161.
70. Zhang D., Gaussin V., Taffet G.E., Belaguli N.S., Yamada M., Schwartz R.J., et al. TAK1 is activated in the myocardium after pressure overload and is sufficient to provoke heart failure in transgenic mice. Nat. Med. 2000, 6:556-563.
71. Kim S.I., Kwak J.H., Zachariah M., He Y., Wang L., Choi M.E. TGF-beta-activated kinase 1 and TAK1-binding protein 1 cooperate to mediate TGF-beta1-induced MKK3-p38 MAPK activation and stimulation of type I collagen. Am. J. Phys. Renal Phys. 2007, 292:F1471-F1478.
72. Wang L., Ma R., Flavell R.A., Choi M.E. Requirement of mitogen-activated protein kinase kinase 3 (MKK3) for activation of p38alpha and p38delta MAPK isoforms by TGF-beta 1 in murine mesangial cells. J. Biol. Chem. 2002, 277:47257-47262.
73. Kompa A.R., See F., Lewis D.A., Adrahtas A., Cantwell D.M., Wang B.H., et al. Long-term but not short-term p38 mitogen-activated protein kinase inhibition improves cardiac function and reduces cardiac remodeling post-myocardial infarction. J. Pharmacol. Exp. Ther. 2008, 325:741-750.
74. See F., Thomas W., Way K., Tzanidis A., Kompa A., Lewis D., et al. p38 mitogen-activated protein kinase inhibition improves cardiac function and attenuates left ventricular remodeling following myocardial infarction in the rat. J. Am. Coll. Cardiol. 2004, 44:1679-1689.
75. Liu T., Warburton R.R., Guevara O.E., Hill N.S., Fanburg B.L., Gaestel M., et al. Lack of MK2 inhibits myofibroblast formation and exacerbates pulmonary fibrosis. Am. J. Respir. Cell Mol. Biol. 2007, 37:507-517.
76. Sousa A.M., Liu T., Guevara O., Stevens J., Fanburg B.L., Gaestel M., et al. Smooth muscle alpha-actin expression and myofibroblast differentiation by TGFbeta are dependent upon MK2. J. Cell. Biochem. 2007, 100:1581-1592.
77. 2+ signals confer fibrogenesis in human atrial fibrillation. Circ. Res. 2010, 106:992-1003.
78. Adapala R.K., Thoppil R.J., Luther D.J., Paruchuri S., Meszaros J.G., Chilian W.M., et al. TRPV4 channels mediate cardiac fibroblast differentiation by integrating mechanical and soluble signals. J. Mol. Cell. Cardiol. 2013, 54:45-52.
79. Rahaman S.O., Grove L.M., Paruchuri S., Southern B.D., Abraham S., Niese K.A., et al. TRPV4 mediates myofibroblast differentiation and pulmonary fibrosis in mice. J. Clin. Invest. 2014, 124:5225-5238.
80. 2+ channels and regulation of calcium microdomains. Cell Calcium 2006, 40:495-504.
81. Wang J.H., Thampatty B.P., Lin J.S., Im H.J. Mechanoregulation of gene expression in fibroblasts. Gene 2007, 391:1-15.
82. Kessler D., Dethlefsen S., Haase I., Plomann M., Hirche F., Krieg T., et al. Fibroblasts in mechanically stressed collagen lattices assume a "synthetic" phenotype. J. Biol. Chem. 2001, 276:36575-36585.
83. Georges P.C., Hui J.J., Gombos Z., McCormick M.E., Wang A.Y., Uemura M., et al. Increased stiffness of the rat liver precedes matrix deposition: implications for fibrosis. Am. J. Phys.Gastrointest. Liver Physiol. 2007, 293:G1147-G1154.
84. Sandbo N., Dulin N. Actin cytoskeleton in myofibroblast differentiation: ultrastructure defining form and driving function. Transl. Res. 2011, 158:181-196.
85. Yang C., Tibbitt M.W., Basta L., Anseth K.S. Mechanical memory and dosing influence stem cell fate. Nat. Mater. 2014, 13:645-652.
86. Biela S.A., Su Y., Spatz J.P., Kemkemer R. Different sensitivity of human endothelial cells, smooth muscle cells and fibroblasts to topography in the nano-micro range. Acta Biomater. 2009, 5:2460-2466.
87. Kim D.H., Han K., Gupta K., Kwon K.W., Suh K.Y., Levchenko A. Mechanosensitivity of fibroblast cell shape and movement to anisotropic substratum topography gradients. Biomaterials 2009, 30:5433-5444.
88. Chaterji S., Kim P., Choe S.H., Tsui J.H., Lam C.H., Ho D.S., et al. Synergistic effects of matrix nanotopography and stiffness on vascular smooth muscle cell function. Tissue Eng. A 2014, 20:2115-2126.
89. Clarke S.A., Richardson W.J., Holmes J.W. Modifying the mechanics of healing infarcts: is better the enemy of good?. J. Mol. Cell Cardiol. 2015.
90. Janmey P.A., Wells R.G., Assoian R.K., McCulloch C.A. From tissue mechanics to transcription factors. Differentiation 2013, 86:112-120.
91. Olson E.N., Nordheim A. Linking actin dynamics and gene transcription to drive cellular motile functions. Nat. Rev. Mol. Cell Biol. 2010, 11:353-365.
92. Porter K.E., Turner N.A., O'Regan D.J., Balmforth A.J., Ball S.G. Simvastatin reduces human atrial myofibroblast proliferation independently of cholesterol lowering via inhibition of RhoA. Cardiovasc. Res. 2004, 61:745-755.
93. Chan M.W., Chaudary F., Lee W., Copeland J.W., McCulloch C.A. Force-induced myofibroblast differentiation through collagen receptors is dependent on mammalian diaphanous (mDia). J. Biol. Chem. 2010, 285:9273-9281.
94. Akhmetshina A., Dees C., Pileckyte M., Szucs G., Spriewald B.M., Zwerina J., et al. Rho-associated kinases are crucial for myofibroblast differentiation and production of extracellular matrix in scleroderma fibroblasts. Arthritis Rheum. 2008, 58:2553-2564.
95. Sandbo N., Kregel S., Taurin S., Bhorade S., Dulin N.O. Critical role of serum response factor in pulmonary myofibroblast differentiation induced by TGF-beta. Am. J. Respir. Cell Mol. Biol. 2009, 41:332-338.
96. Small E.M., Thatcher J.E., Sutherland L.B., Kinoshita H., Gerard R.D., Richardson J.A., et al. Myocardin-related transcription factor-a controls myofibroblast activation and fibrosis in response to myocardial infarction. Circ. Res. 2010, 107:294-304.
97. Haudek S.B., Gupta D., Dewald O., Schwartz R.J., Wei L., Trial J., et al. Rho kinase-1 mediates cardiac fibrosis by regulating fibroblast precursor cell differentiation. Cardiovasc. Res. 2009, 83:511-518.
98. Luchsinger L.L., Patenaude C.A., Smith B.D., Layne M.D. Myocardin-related transcription factor-A complexes activate type I collagen expression in lung fibroblasts. J. Biol. Chem. 2011, 286:44116-44125.
99. Chai J., Norng M., Tarnawski A.S., Chow J. A critical role of serum response factor in myofibroblast differentiation during experimental oesophageal ulcer healing in rats. Gut 2007, 56:621-630.
100. Yang Y., Zhe X., Phan S.H., Ullenbruch M., Schuger L. Involvement of serum response factor isoforms in myofibroblast differentiation during bleomycin-induced lung injury. Am. J. Respir. Cell Mol. Biol. 2003, 29:583-590.
101. Shiwen X., Stratton R., Nikitorowicz-Buniak J., Ahmed-Abdi B., Ponticos M., Denton C., et al. A role of myocardin related transcription factor-A (MRTF-A) in scleroderma related fibrosis. PLoS One 2015, 10.
102. Huang X., Yang N., Fiore V.F., Barker T.H., Sun Y., Morris S.W., et al. Matrix stiffness-induced myofibroblast differentiation is mediated by intrinsic mechanotransduction. Am. J. Respir. Cell Mol. Biol. 2012, 47:340-348.
103. Small E.M. The actin-MRTF-SRF gene regulatory axis and myofibroblast differentiation. J. Cardiovasc. Transl. Res. 2012, 5:794-804.
104. Wada K., Itoga K., Okano T., Yonemura S., Sasaki H. Hippo pathway regulation by cell morphology and stress fibers. Development 2011, 138:3907-3914.
105. Liu F., Lagares D., Choi K.M., Stopfer L., Marinkovic A., Vrbanac V., et al. Mechanosignaling through YAP and TAZ drives fibroblast activation and fibrosis. Am. J. Phys. Lung Cell. Mol. Phys. 2015, 308:L344-L357.
106. Mannaerts I., Leite S.B., Verhulst S., Claerhout S., Eysackers N., Thoen L.F., et al. The Hippo pathway effector YAP controls mouse hepatic stellate cell activation. J. Hepatol. 2015, 63:679-688.
107. Piersma B., de Rond S., Werker P.M., Boo S., Hinz B., van Beuge M.M., et al. YAP1 is a driver of myofibroblast differentiation in normal and diseased fibroblasts. Am. J. Pathol. 2015, 185:3326-3337.
108. Mitani A., Nagase T., Fukuchi K., Aburatani H., Makita R., Kurihara H. Transcriptional coactivator with PDZ-binding motif is essential for normal alveolarization in mice. Am. J. Respir. Crit. Care Med. 2009, 180:326-338.
109. Lin Z., von Gise A., Zhou P., Gu F., Ma Q., Jiang J., et al. Cardiac-specific YAP activation improves cardiac function and survival in an experimental murine MI model. Circ. Res. 2014, 115:354-363.
110. Xin M., Kim Y., Sutherland L.B., Murakami M., Qi X., McAnally J., et al. Hippo pathway effector Yap promotes cardiac regeneration. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:13839-13844.
111. Garcia J.G., Wang P., Schaphorst K.L., Becker P.M., Borbiev T., Liu F., et al. Critical involvement of p38 MAP kinase in pertussis toxin-induced cytoskeletal reorganization and lung permeability. FASEB J. 2002, 16:1064-1076.
112. Wang J., Zohar R., McCulloch C.A. Multiple roles of alpha-smooth muscle actin in mechanotransduction. Exp. Cell Res. 2006, 312:205-214.
113. Cui X., Zhang X., Yin Q., Meng A., Su S., Jing X., et al. Factin cytoskeleton reorganization is associated with hepatic stellate cell activation. Mol. Med. Rep. 2014, 9:1641-1647.
114. Yu L., Yuan X., Wang D., Barakat B., Williams E.D., Hannigan G.E. Selective regulation of p38beta protein and signaling by integrin-linked kinase mediates bladder cancer cell migration. Oncogene 2014, 33:690-701.
115. Kulkarni A.A., Thatcher T.H., Olsen K.C., Maggirwar S.B., Phipps R.P., Sime P.J. PPAR-gamma ligands repress TGFbeta-induced myofibroblast differentiation by targeting the PI3K/Akt pathway: implications for therapy of fibrosis. PLoS One 2011, 6.
116. Wang E.T., Cody N.A., Jog S., Biancolella M., Wang T.T., Treacy D.J., et al. Transcriptome-wide regulation of pre-mRNA splicing and mRNA localization by muscleblind proteins. Cell 2012, 150:710-724.
117. Besse F., Ephrussi A. Translational control of localized mRNAs: restricting protein synthesis in space and time. Nat. Rev. Mol. Cell Biol. 2008, 9:971-980.
118. Batra R., Charizanis K., Manchanda M., Mohan A., Li M., Finn D.J., et al. Loss of MBNL leads to disruption of developmentally regulated alternative polyadenylation in RNA-mediated disease. Mol. Cell 2014, 56:311-322.
119. Ho T.H., Charlet B.N., Poulos M.G., Singh G., Swanson M.S., Cooper T.A. Muscleblind proteins regulate alternative splicing. EMBO J. 2004, 23:3103-3112.
120. Teplova M., Patel D.J. Structural insights into RNA recognition by the alternative-splicing regulator muscleblind-like MBNL1. Nat. Struct. Mol. Biol. 2008, 15:1343-1351.
121. Lin X., Miller J.W., Mankodi A., Kanadia R.N., Yuan Y., Moxley R.T., et al. Failure of MBNL1-dependent post-natal splicing transitions in myotonic dystrophy. Hum. Mol. Genet. 2006, 15:2087-2097.
122. Miller J.W., Urbinati C.R., Teng-Umnuay P., Stenberg M.G., Byrne B.J., Thornton C.A., et al. Recruitment of human muscleblind proteins to (CUG)(n) expansions associated with myotonic dystrophy. EMBO J. 2000, 19:4439-4448.
123. Kalsotra A., Xiao X., Ward A.J., Castle J.C., Johnson J.M., Burge C.B., et al. A postnatal switch of CELF and MBNL proteins reprograms alternative splicing in the developing heart. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:20333-20338.
124. Han H., Irimia M., Ross P.J., Sung H.K., Alipanahi B., David L., et al. MBNL proteins repress ES-cell-specific alternative splicing and reprogramming. Nature 2013, 498:241-245.