Delayed stress fiber formation mediates pulmonary myofibroblast differentiation in response to TGF-β

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 301, Issue 5, 2011, Pages

  Sandbo, Nathan ^a   Lau, Andrew ^b   Kach, Jacob ^b   Ngam, Caitlyn ^a   Yau, Douglas ^b   Dulin, Nickolai O ^b  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

Author keywords

Actin polymerization; Human lung fibroblasts; Megakaryoblastic leukemia 1 translocation; Serum response factor activation; Transforming growth factor

Indexed keywords

4 (1 AMINOETHYL) N (4 PYRIDYL)CYCLOHEXANECARBOXAMIDE; ALPHA ACTIN; ALPHA SMOOTH MUSCLE ACTIN; CYCLOHEXIMIDE; JASPAMIDE; LATRUNCULIN B; MEGAKARYOBLASTIC LEUKEMIA 1 PROTEIN; MYOCARDIN; PROTEIN INHIBITOR; RHO KINASE; SERUM RESPONSE FACTOR; SMAD PROTEIN; TRANSCRIPTION FACTOR; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; ENZYME ACTIVATION; GENE SILENCING; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; IN VITRO STUDY; MYOFIBROBLAST; PRIORITY JOURNAL; PROTEIN EXPRESSION; PULMONARY MYOFIBROBLAST DIFFERENTIATION; SIGNAL TRANSDUCTION; STRESS FIBER;

ACTINS; ADENOVIRIDAE; BLOTTING, WESTERN; CELL DIFFERENTIATION; DNA-BINDING PROTEINS; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION; GENES, REPORTER; HUMANS; LUCIFERASES; LUNG; MUSCLE, SMOOTH; MYOFIBROBLASTS; ONCOGENE PROTEINS, FUSION; PRIMARY CELL CULTURE; PULMONARY FIBROSIS; REAL-TIME POLYMERASE CHAIN REACTION; RHO-ASSOCIATED KINASES; SERUM RESPONSE FACTOR; SIGNAL TRANSDUCTION; SMAD PROTEINS; STRESS FIBERS; TRANSDUCTION, GENETIC; TRANSFORMING GROWTH FACTOR BETA1;

EID: 80055106592     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00166.2011     Document Type: Article

References (92)

1. Adam PJ, Regan CP, Hautmann MB, Owens GK. Positive- and negative-acting Kruppel-like transcription factors bind a transforming growth factor beta control element required for expression of the smooth muscle cell differentiation marker SM22alpha in vivo. J Biol Chem 275: 37798-37806, 2000.
2. Araya J, Nishimura SL. Fibrogenic reactions in lung disease. Annu Rev Pathol 5: 77-98.
3. Arora PD, Narani N, McCulloch CA. The compliance of collagen gels regulates transforming growth factor-beta induction of alpha-smooth muscle actin in fibroblasts. Am J Pathol 154: 871-882, 1999.
4. Bhowmick NA, Ghiassi M, Bakin A, Aakre M, Lundquist CA, Engel ME, Arteaga CL, Moses HL. Transforming growth factor-beta1 mediates epithelial to mesenchymal transdifferentiation through a RhoA-dependent mechanism. Mol Biol Cell 12: 27-36, 2001.
5. Bogatkevich GS, Tourkina E, Silver RM, Ludwicka-Bradley A. Thrombin differentiates normal lung fibroblasts to a myofibroblast phenotype via the proteolytically activated receptor-1 and a protein kinase C-dependent pathway. J Biol Chem 276: 45184-45192, 2001.
6. Bottinger EP. TGF-beta in renal injury and disease. Semin Nephrol 27: 309-320, 2007.
7. Buckley ST, Medina C, Kasper M, Ehrhardt C. Interplay between RAGE, CD44, and focal adhesion molecules in epithelial-mesenchymal transition of alveolar epithelial cells. Am J Physiol Lung Cell Mol Physiol 300: L548-L559, 2011.
8. Chow N, Bell RD, Deane R, Streb JW, Chen J, Brooks A, Van Nostrand W, Miano JM, Zlokovic BV. Serum response factor and myocardin mediate arterial hypercontractility and cerebral blood flow dysregulation in Alzheimer's phenotype. Proc Natl Acad Sci USA 104: 823-828, 2007.
9. Cogan JG, Subramanian SV, Polikandriotis JA, Kelm RJ Jr, Strauch AR. Vascular smooth muscle alpha-actin gene transcription during myofibroblast differentiation requires Sp1/3 protein binding proximal to the MCAT enhancer. J Biol Chem 277: 36433-36442, 2002.
10. Das S, Becker BN, Hoffmann FM, Mertz JE. Complete reversal of epithelial to mesenchymal transition requires inhibition of both ZEB expression and the Rho pathway (Abstract). BMC Cell Biol 10: 94, 2009.
11. Davies SP, Reddy H, Caivano M, Cohen P. Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem J 351: 95-105, 2000.
12. Davis A, Hogarth K, Fernandes D, Solway J, Niu J, Kolenko V, Browning D, Miano JM, Orlov SN, Dulin NO. Functional significance of protein kinase A activation by endothelin-1 and ATP: negative regulation of SRF-dependent gene expression by PKA. Cell Signal 15: 597-604, 2003.
13. Dennler S, Itoh S, Vivien D, ten Dijke P, Huet S, Gauthier JM. Direct binding of Smad3 and Smad4 to critical TGF beta-inducible elements in the promoter of human plasminogen activator inhibitor-type 1 gene. EMBO J 17: 3091-3100, 1998.
14. Derynck R, Zhang YE. Smad-dependent and Smad-independent pathways in TGF-beta family signalling. Nature 425: 577-584, 2003.
15. Desmouliere A, Chaponnier C, Gabbiani G. Tissue repair, contraction, and the myofibroblast. Wound Repair Regen 13: 7-12, 2005.
16. 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.
17. Ding Q, Gladson CL, Wu H, Hayasaka H, Olman MA. Focal adhesion kinase (FAK)-related non-kinase inhibits myofibroblast differentiation through differential MAPK activation in a FAK-dependent manner. J Biol Chem 283: 26839-26849, 2008.
18. Dugina V, Fontao L, Chaponnier C, Vasiliev J, Gabbiani G. Focal adhesion features during myofibroblastic differentiation are controlled by intracellular and extracellular factors. J Cell Sci 114: 3285-3296, 2001.
19. Edlund S, Landstrom M, Heldin CH, Aspenstrom P. Transforming growth factor-beta-induced mobilization of actin cytoskeleton requires signaling by small GTPases Cdc42 and RhoA. Mol Biol Cell 13: 902-914, 2002.
20. Evans JN, Kelley J, Krill J, Low RB, Adler KB. The myofibroblast in pulmonary fibrosis. Chest 83: 97S-98S, 1983.
21. 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.
22. Evelyn CR, Wade SM, Wang Q, Wu M, Iniguez-Lluhi JA, Merajver SD, Neubig RR. CCG-1423: a small-molecule inhibitor of RhoA transcriptional signaling. Mol Cancer Ther 6: 2249-2260, 2007.
23. Fan L, Sebe A, Peterfi Z, Masszi A, Thirone AC, Rotstein OD, Nakano H, McCulloch CA, Szaszi K, Mucsi I, Kapus A. Cell contact-dependent regulation of epithelial-myofibroblast transition via the rho-rho kinasephospho-myosin pathway. Mol Biol Cell 18: 1083-1097, 2007.
24. Feng XH, Derynck R. Specificity and versatility in tgf-beta signaling through Smads. Annu Rev Cell Dev Biol 21: 659-693, 2005.
25. Fouletier-Dilling CM, Bosch P, Davis AR, Shafer JA, Stice SL, Gugala Z, Gannon FH, Olmsted-Davis E. A Novel compound enables high-level adenovirus transduction in the absence of an adenovirus-specific receptor. Human Gene Ther 16: 1287-1297, 2005.
26. Gohla A, Offermanns S, Wilkie TM, Schultz G. Differential involvement of Galpha12 and Galpha13 in receptor-mediated stress fiber formation. J Biol Chem 274: 17901-17907, 1999.
27. Guettler S, Vartiainen MK, Miralles F, Larijani B, Treisman R. RPEL motifs link the serum response factor cofactor MAL but not myocardin to Rho signaling via actin binding. Mol Cell Biol 28: 732-742, 2008.
28. Halder SK, Beauchamp RD, Datta PK. A specific inhibitor of TGF-beta receptor kinase, SB-431542, as a potent antitumor agent for human cancers. Neoplasia 7: 509-521, 2005.
29. Hardie WD, Glasser SW, Hagood JS. Emerging concepts in the pathogenesis of lung fibrosis. Am J Pathol 175: 3-16, 2009.
30. Hashimoto S, Gon Y, Takeshita I, Matsumoto K, Maruoka S, Horie T. Transforming growth Factor-beta1 induces phenotypic modulation of human lung fibroblasts to myofibroblast through a c-Jun-NH2-terminal kinase-dependent pathway. Am J Respir Crit Care Med 163: 152-157, 2001.
31. Hinson JS, Medlin MD, Lockman K, Taylor JM, Mack CP. Smooth muscle cell-specific transcription is regulated by nuclear localization of the myocardin-related transcription factors. Am J Physiol Heart Circ Physiol 292: H1170-H1180, 2007.
32. Hinz B. Masters and servants of the force: the role of matrix adhesions in myofibroblast force perception and transmission. Eur J Cell Biol 85: 175-181, 2006.
33. Hinz B, Dugina V, Ballestrem C, Wehrle-Haller B, Chaponnier C. Alpha-smooth muscle actin is crucial for focal adhesion maturation in myofibroblasts. Mol Biol Cell 14: 2508-2519, 2003.
34. Hinz B, Phan SH, Thannickal VJ, Galli A, Bochaton-Piallat ML, Gabbiani G. The Myofibroblast. One Function Multiple Origins. Am J Pathol 170: 1807-1816, 2007.
35. Hogarth DK, Sandbo N, Taurin S, Kolenko V, Miano JM, Dulin NO. Dual role of PKA in phenotypic modulation of vascular smooth muscle cells by extracellular ATP. Am J Physiol Cell Physiol 287: C449-C456, 2004.
36. Hu B, Wu Z, Liu T, Ullenbruch MR, Jin H, Phan SH. Gut-enriched Kruppel-like factor interaction with Smad3 inhibits myofibroblast differentiation. Am J Respir Cell Mol Biol 36: 78-84, 2007.
37. Hu B, Wu Z, Phan SH. Smad3 mediates transforming growth factorbeta-induced alpha-smooth muscle actin expression. Am J Respir Cell Mol Biol 29: 397-404, 2003.
38. Ishizaki T, Uehata M, Tamechika I, Keel J, Nonomura K, Maekawa M, Narumiya S. Pharmacological properties of Y-27632, a specific inhibitor of rho-associated kinases. Mol Pharmacol 57: 976-983, 2000.
39. Jester JV, Huang J, Barry-Lane PA, Kao WW, Petroll WM, Cavanagh HD. Transforming growth factor(beta)-mediated corneal myofibroblast differentiation requires actin and fibronectin assembly. Invest Ophthalmol Vis Sci 40: 1959-1967, 1999.
40. Katoh K, Kano Y, Fujiwara K. Isolation and in vitro contraction of stress fibers. Methods Enzymol 325: 369-380, 2000.
41. Khan R, Sheppard R. Fibrosis in heart disease: understanding the role of transforming growth factor-beta in cardiomyopathy, valvular disease and arrhythmia. Immunology 118: 10-24, 2006.
42. Kono Y, Nishiuma T, Nishimura Y, Kotani Y, Okada T, Nakamura S, Yokoyama M. Sphingosine kinase 1 regulates differentiation of human and mouse lung fibroblasts mediated by TGF-beta1. Am J Respir Cell Mol Biol 37: 395-404, 2007.
43. Kuhn C, McDonald JA. The roles of the myofibroblast in idiopathic pulmonary fibrosis. Ultrastructural and immunohistochemical features of sites of active extracellular matrix synthesis. Am J Pathol 138: 1257-1265, 1991.
44. Leask A, Abraham DJ. TGF-beta signaling and the fibrotic response. FASEB J 18: 816-827, 2004.
45. Lee J, Moon HJ, Lee JM, Joo CK. Smad3 regulates Rho signaling via NET1 in the transforming growth factor-beta-induced epithelial-mesenchymal transition of human retinal pigment epithelial cells. J Biol Chem 285: 26618-26627, 2010.
46. Leung T, Chen XQ, Manser E, Lim L. The p160 RhoA-binding kinase ROK alpha is a member of a kinase family and is involved in the reorganization of the cytoskeleton. Mol Cell Biol 16: 5313-5327, 1996.
47. Lockman K, Hinson JS, Medlin MD, Morris D, Taylor JM, Mack CP. Sphingosine 1-phosphate stimulates smooth muscle cell differentiation and proliferation by activating separate serum response factor co-factors. J Biol Chem 279: 42422-42430, 2004.
48. Mack CP, Somlyo AV, Hautmann M, Somlyo AP, Owens GK. Smooth muscle differentiation marker gene expression is regulated by RhoAmediated actin polymerization. J Biol Chem 276: 341-347, 2001.
49. Masszi A, Di Ciano C, Sirokmany G, Arthur WT, Rotstein OD, Wang J, McCulloch CA, Rosivall L, Mucsi I, Kapus A. Central role for Rho in TGF-β1-induced alpha-smooth muscle actin expression during epithelial-mesenchymal transition. Am J Physiol Renal Physiol 284: F911-F924, 2003.
50. Medlin MD, Staus DP, Dubash AD, Taylor JM, Mack CP. Sphingosine 1-phosphate receptor 2 signals through leukemia-associated RhoGEF (LARG), to promote smooth muscle cell differentiation. Arterioscler Thromb Vasc Biol 30: 1779-1786.
51. Miralles F, Posern G, Zaromytidou AI, Treisman R. Actin dynamics control SRF activity by regulation of its coactivator MAL. Cell 113: 329-342, 2003.
52. Morin P, Wickman G, Munro J, Inman GJ, Olson MF. Differing contributions of LIMK and ROCK to TGFbeta-induced transcription, motility and invasion. Eur J Cell Biol 90: 13-25, 2011.
53. Morita T, Mayanagi T, Sobue K. Reorganization of the actin cytoskeleton via transcriptional regulation of cytoskeletal/focal adhesion genes by myocardin-related transcription factors (MRTFs/MAL/MKLs). Exp Cell Res 313: 3432-3445, 2007.
54. Moustakas A, Stournaras C. Regulation of actin organisation by TGFbeta in H-ras-transformed fibroblasts. J Cell Sci 112: 1169-1179, 1999.
55. Noble PW, Homer RJ. Back to the future: historical perspective on the pathogenesis of idiopathic pulmonary fibrosis. Am J Respir Cell Mol Biol 33: 113-120, 2005.
56. Paterson HF, Self AJ, Garrett MD, Just I, Aktories K, Hall A. Microinjection of recombinant p21rho induces rapid changes in cell morphology. J Cell Biol 111: 1001-1007, 1990.
57. Phan SH. Fibroblast phenotypes in pulmonary fibrosis. Am J Respir Cell Mol Biol 29: S87-92, 2003.
58. Phan SH. Role of the myofibroblast in pulmonary fibrosis. Kidney Int Suppl 54: S46-S48, 1996.
59. Powell DW, Mifflin RC, Valentich JD, Crowe SE, Saada JI, West I. Myofibroblast. I. Paracrine cells important in health and disease. Am J Physiol Cell Physiol 277: C1-C9, 1999.
60. Qiu P, Feng XH, Li L. Interaction of Smad3 and SRF-associated complex mediates TGF-beta1 signals to regulate SM22 transcription during myofibroblast differentiation. J Mol Cell Cardiol 35: 1407-1420, 2003.
61. Ridley AJ, Hall A. Distinct patterns of actin organization regulated by the small GTP-binding proteins Rac and Rho. Cold Spring Harb Symp Quant Biol 57: 661-671, 1992.
62. Rodriguez-Pascual F, Redondo-Horcajo M, Lamas S. Functional cooperation between Smad proteins and activator protein-1 regulates transforming growth factor-beta-mediated induction of endothelin-1 expression. Circ Res 92: 1288-1295, 2003.
63. Sandbo N, Kregel S, Taurin S, Bhorade S, Dulin NO. Critical role of serum response factor in pulmonary myofibroblast differentiation induced by TGF-beta. Am J Respir Cell Mol Biol 41: 332-338, 2009.
64. Sandbo N, Qin Y, Taurin S, Hogarth DK, Kreutz B, Dulin NO. Regulation of serum response factor-dependent gene expression by proteasome inhibitors. Mol Pharmacol 67: 789-797, 2005.
65. Selman M, King TE, Pardo A. Idiopathic pulmonary fibrosis: prevailing and evolving hypotheses about its pathogenesis and implications for therapy. Ann Intern Med 134: 136-151, 2001.
66. Selman M, Pardo A. Idiopathic pulmonary fibrosis: an epithelial/fibroblastic cross-talk disorder (Abstract). Respir Res 3: 3, 2002.
67. Selman M, Thannickal VJ, Pardo A, Zisman DA, Martinez FJ, Lynch JP 3rd. Idiopathic pulmonary fibrosis: pathogenesis and therapeutic approaches. Drugs 64: 405-430, 2004.
68. Serini G, Gabbiani G. Mechanisms of myofibroblast activity and phenotypic modulation. Exp Cell Res 250: 273-283, 1999.
69. Shen X, Li J, Hu PP, Waddell D, Zhang J, Wang XF. The activity of guanine exchange factor NET1 is essential for transforming growth factor-beta-mediated stress fiber formation. J Biol Chem 276: 15362-15368, 2001.
70. Shi-wen X, Parapuram SK, Pala D, Chen Y, Carter DE, Eastwood M, Denton CP, Abraham DJ, Leask A. Requirement of transforming growth factor beta-activated kinase 1 for transforming growth factor beta-induced alpha-smooth muscle actin expression and extracellular matrix contraction in fibroblasts. Arthritis Rheum 60: 234-241, 2009.
71. Skalli O, Gabbiani F, Gabbiani G. Action of general and alpha-smooth muscle-specific actin antibody microinjection on stress fibers of cultured smooth muscle cells. Exp Cell Res 187: 119-125, 1990.
72. Small EM, Thatcher JE, Sutherland LB, Kinoshita H, Gerard RD, Richardson JA, Dimaio JM, Sadek H, Kuwahara K, Olson EN. Myocardin-related transcription factor-a controls myofibroblast activation and fibrosis in response to myocardial infarction. Circ Res 107: 294-304, 2000.
73. Smith PC, Caceres M, Martinez J. Induction of the myofibroblastic phenotype in human gingival fibroblasts by transforming growth factorbeta1: role of RhoA-ROCK and c-Jun N-terminal kinase signaling pathways. J Periodontal Res 41: 418-425, 2006.
74. Sotiropoulos A, Gineitis D, Copeland J, Treisman R. Signal-regulated activation of serum response factor is mediated by changes in actin dynamics. Cell 98: 159-169, 1999.
75. Spencer JA, Misra RP. Expression of the serum response factor gene is regulated by serum response factor binding sites. J Biol Chem 271: 16535-16543, 1996.
76. Spencer JA, Misra RP. Expression of the SRF gene occurs through a Ras/Sp/SRF-mediated-mechanism in response to serum growth signals. Oncogene 18: 7319-7327, 1999.
77. Subramanian SV, Polikandriotis JA, Kelm RJ Jr, David JJ, Orosz CG, Strauch AR. Induction of vascular smooth muscle alpha-actin gene transcription in transforming growth factor beta1-activated myofibroblasts mediated by dynamic interplay between the Pur repressor proteins and Sp1/Smad coactivators. Mol Biol Cell 15: 4532-4543, 2004.
78. Taurin S, Sandbo N, Yau DM, Sethakorn N, Kach J, Dulin NO. Phosphorylation of myocardin by extracellular signal-regulated kinase. J Biol Chem 284: 33789-33794, 2009.
79. Thannickal VJ, Lee DY, White ES, Cui Z, Larios JM, Chacon R, Horowitz JC, Day RM, Thomas PE. Myofibroblast differentiation by transforming growth factor-beta1 is dependent on cell adhesion and integrin signaling via focal adhesion kinase. J Biol Chem 278: 12384-12389, 2003.
80. Thannickal VJ, Toews GB, White ES, Lynch JP 3rd, Martinez FJ. Mechanisms of pulmonary fibrosis. Annu Rev Med 55: 395-417, 2004.
81. Tomasek JJ, Gabbiani G, Hinz B, Chaponnier C, Brown RA. Myofibroblasts and mechano-regulation of connective tissue remodelling. Nat Rev Mol Cell Biol 3: 349-363, 2002.
82. Tsapara A, Luthert P, Greenwood J, Hill CS, Matter K, Balda MS. The RhoA activator GEF-H1/Lfc is a transforming growth factor-beta target gene and effector that regulates alpha-smooth muscle actin expression and cell migration. Mol Biol Cell 21: 860-870, 2010.
83. Uehata M, Ishizaki T, Satoh H, Ono T, Kawahara T, Morishita T, Tamakawa H, Yamagami K, Inui J, Maekawa M, Narumiya S. Calcium sensitization of smooth muscle mediated by a Rho-associated protein kinase in hypertension. Nature 389: 990-994, 1997.
84. Utsugi M, Dobashi K, Ishizuka T, Masubuchi K, Shimizu Y, Nakazawa T, Mori M. C-Jun-NH2-terminal kinase mediates expression of connective tissue growth factor induced by transforming growth factorbeta1 in human lung fibroblasts. Am J Respir Cell Mol Biol 28: 754-761, 2003.
85. Vardouli L, Moustakas A, Stournaras C. LIM-kinase 2 and cofilin phosphorylation mediate actin cytoskeleton reorganization induced by transforming growth factor-beta. J Biol Chem 280: 11448-11457, 2005.
86. Vardouli L, Vasilaki E, Papadimitriou E, Kardassis D, Stournaras C. A novel mechanism of TGFbeta-induced actin reorganization mediated by Smad proteins and Rho GTPases. Febs J 275: 4074-4087, 2008.
87. Vartiainen MK, Guettler S, Larijani B, Treisman R. Nuclear actin regulates dynamic subcellular localization and activity of the SRF cofactor MAL. Science 316: 1749-1752, 2007.
88. Vaughan MB, Howard EW, Tomasek JJ. Transforming growth factorbeta1 promotes the morphological and functional differentiation of the myofibroblast. Exp Cell Res 257: 180-189, 2000.
89. Wang DZ, Li S, Hockemeyer D, Sutherland L, Wang Z, Schratt G, Richardson JA, Nordheim A, Olson EN. Potentiation of serum response factor activity by a family of myocardin-related transcription factors. Proc Natl Acad Sci USA 99: 14855-14860, 2002.
90. White ES, Lazar MH, Thannickal VJ. Pathogenetic mechanisms in usual interstitial pneumonia/idiopathic pulmonary fibrosis. J Pathol 201: 343-354, 2003.
91. Yamanaka M, Shegogue D, Pei H, Bu S, Bielawska A, Bielawski J, Pettus B, Hannun YA, Obeid L, Trojanowska M. Sphingosine kinase 1 (SPHK1) is induced by transforming growth factor-beta and mediates TIMP-1 up-regulation. J Biol Chem 279: 53994-54001, 2004.
92. Zhao XH, Laschinger C, Arora P, Szaszi K, Kapus A, McCulloch CA. Force activates smooth muscle alpha-actin promoter activity through the Rho signaling pathway. J Cell Sci 120: 1801-1809, 2007.