Improved throughput traction microscopy reveals pivotal role for matrix stiffness in fibroblast contractility and TGF-β responsiveness

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 303, Issue 3, 2012, Pages

  Marinkovic, Aleksandar ^a   Mih, Justin D ^a   Park, Jin Ah ^a   Liu, Fei ^a   Tschumperlin, Daniel J ^a  

^a HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

Extracellular matrix; Fibrosis; Forces; Lung; Rigidity

Indexed keywords

POLYACRYLAMIDE; SMAD2 PROTEIN; SMAD3 PROTEIN; TRANSFORMING GROWTH FACTOR BETA1;

ARTICLE; CONTROLLED STUDY; EXTRACELLULAR MATRIX; FETUS; HIGH THROUGHPUT TRACTION MICROSCOPY; HUMAN; HUMAN CELL; HYDROGEL; LUNG COMPLIANCE; LUNG FIBROBLAST; MEASUREMENT; MICROSCOPY; MYOFIBROBLAST; PRIORITY JOURNAL; RIGIDITY;

CELLS, CULTURED; EXTRACELLULAR MATRIX; FETUS; FIBROBLASTS; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; LUNG; MICROSCOPY; PHOSPHORYLATION; PULMONARY FIBROSIS; SIGNAL TRANSDUCTION; SMAD2 PROTEIN; SMAD3 PROTEIN; TRACTION; TRANSFORMING GROWTH FACTOR BETA;

EID: 84864744748     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00108.2012     Document Type: Article

References (72)

1. Ailenberg M, Tung PS, Fritz IB. Transforming growth factor-beta elicits shape changes and increases contractility of testicular peritubular cells. Biol Reprod 42: 499-509, 1990.
2. Annes JP, Chen Y, Munger JS, Rifkin DB. Integrin alphaVbeta6-mediated activation of latent TGF-beta requires the latent TGF-beta binding protein-1. J Cell Biol 165: 723-734, 2004.
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. Balaban NQ, Schwarz US, Riveline D, Goichberg P, Tzur G, Sabanay I, Mahalu D, Safran S, Bershadsky A, Addadi L, Geiger B. Force and focal adhesion assembly: a close relationship studied using elastic mi-cropatterned substrates. Nat Cell Biol 3: 466-472, 2001.
5. Brown RA, Sethi KK, Gwanmesia I, Raemdonck D, Eastwood M, Mudera V. Enhanced fibroblast contraction of 3D collagen lattices and integrin expression by TGF-beta1 and -beta3: mechanoregulatory growth factors? Exp Cell Res 274: 310-322, 2002.
6. Buscemi L, Ramonet D, Klingberg F, Formey A, Smith-Clerc J, Meister JJ, Hinz B. The single-molecule mechanics of the latent TGF-beta1 complex. Curr Biol 21: 2046-2054, 2011.
7. Butler JP, Tolic-Norrelykke IM, Fabry B, Fredberg JJ. Traction fields, moments, and strain energy that cells exert on their surroundings. Am J Physiol Cell Physiol 282: C595-C605, 2002.
8. Califano JP, and Reinhart-King CA. Substrate stiffness and cell area predict cellular traction stresses in single cells and cells in contact. Cell Mol Bioeng 3: 68-75, 2010.
9. Cavalcanti-Adam EA, Volberg T, Micoulet A, Kessler H, Geiger B, Spatz JP. Cell spreading and focal adhesion dynamics are regulated by spacing of integrin ligands. Biophys J 92: 2964-2974, 2007.
10. Chen J, Li H, SundarRaj N, Wang JH. Alpha-smooth muscle actin expression enhances cell traction force. Cell Motil Cytoskeleton 64: 248-257, 2007.
11. Chen JH, Chen WL, Sider KL, Yip CY, Simmons CA. beta-catenin mediates mechanically regulated, transforming growth factor-beta1-in-duced myofibroblast differentiation of aortic valve interstitial cells. Arte-rioscler Thromb Vasc Biol 31: 590-597, 2011.
12. Conidi A, Cazzola S, Beets K, Coddens K, Collart C, Cornelis F, Cox L, Joke D, Dobreva MP, Dries R, Esguerra C, Francis A, Ibrahimi A, Kroes R, Lesage F, Maas E, Moya I, Pereira PN, Stappers E, Stryjew-ska A, van den Berghe V, Vermeire L, Verstappen G, Seuntjens E, Umans L, Zwijsen A, Huylebroeck D. Few Smad proteins and many Smad-interacting proteins yield multiple functions and action modes in TGFbeta/BMP signaling in vivo. Cytokine Growth Factor Rev 22: 287-300, 2011.
13. Crider BJ, Risinger GM Jr, Haaksma CJ, Howard EW, Tomasek JJ. Myocardin-related transcription factors A and B are key regulators of TGF-beta1-induced fibroblast to myofibroblast differentiation. J Invest Dermatol 131: 2378-2385, 2011.
14. Dembo M, Wang YL. Stresses at the cell-to-substrate interface during locomotion of fibroblasts. Biophys J 76: 2307-2316, 1999.
15. Discher DE, Janmey P, Wang YL. Tissue cells feel and respond to the stiffness of their substrate. Science 310: 1139-1143, 2005.
16. 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.
17. Dupont S, Morsut L, Aragona M, Enzo E, Giulitti S, Cordenonsi M, Zanconato F, Le Digabel J, Forcato M, Bicciato S, Elvassore N, Piccolo S. Role of YAP/TAZ in mechanotransduction. Nature 474: 179-183, 2011.
18. Eickelberg O, Kohler E, Reichenberger F, Bertschin S, Woodtli T, Erne P, Perruchoud AP, Roth M. Extracellular matrix deposition by primary human lung fibroblasts in response to TGF-fj1 and TGF-fj3. Am J Physiol Lung Cell Mol Physiol 276: L814-L824, 1999.
19. Feng XH, Derynck R. Specificity and versatility in tgf-beta signaling through Smads. Ann Rev Cell Dev Biol 21: 659-693, 2005.
20. Finesmith TH, Broadley KN, Davidson JM. Fibroblasts from wounds of different stages of repair vary in their ability to contract a collagen gel in response to growth factors. J Cell Physiol 144: 99-107, 1990.
21. Fujimura T, Hotta M, Kitahara T, Takema Y. Loss of contraction force in dermal fibroblasts with aging due to decreases in myosin light chain phosphorylation enzymes. Arch Pharmacol Res (Seoul) 34: 1015-1022, 2011.
22. Fukamizu H, Grinnell F. Spatial organization of extracellular matrix and fibroblast activity: effects of serum, transforming growth factor beta, and fibronectin. Exp Cell Res 190: 276-282, 1990.
23. Gabbiani G. The myofibroblast in wound healing and fibrocontractive diseases. J Pathol 200: 500-503, 2003.
24. Galbraith CG, Yamada KM, Sheetz MP. The relationship between force and focal complex development. J Cell Biol 159: 695-705, 2002.
25. Georges PC, Janmey PA. Cell type-specific response to growth on soft materials. J Appl Physiol 98: 1547-1553, 2005.
26. Goffin JM, Pittet P, Csucs G, Lussi JW, Meister JJ, Hinz B. Focal adhesion size controls tension-dependent recruitment of alpha-smooth muscle actin to stress fibers. J Cell Biol 172: 259-268, 2006.
27. Grinnell F, Ho CH. Transforming growth factor beta stimulates fibro-blast-collagen matrix contraction by different mechanisms in mechanically loaded and unloaded matrices. Exp Cell Res 273: 248-255, 2002.
28. Harris AK, Stopak D, Wild P. Fibroblast traction as a mechanism for collagen morphogenesis. Nature 290: 249-251, 1981.
29. Hinz B. Tissue stiffness, latent TGF-beta1 activation, and mechanical signal transduction: implications for the pathogenesis and treatment of fibrosis. Curr Rheumatol Rep 11: 120-126, 2009.
30. 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.
31. 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.
32. Hinz B, Gabbiani G. Mechanisms of force generation and transmission by myofibroblasts. Curr Opin Biotechnol 14: 538-546, 2003.
33. 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.
34. Kobayashi T, Liu X, Kim HJ, Kohyama T, Wen FQ, Abe S, Fang Q, Zhu YK, Spurzem JR, Bitterman P, Rennard SI. TGF-beta1 and serum both stimulate contraction but differentially affect apoptosis in 3D collagen gels. Respir Res 6: 141, 2005.
35. Kobayashi T, Liu X, Wen FQ, Kohyama T, Shen L, Wang XQ, Hashimoto M, Mao L, Togo S, Kawasaki S, Sugiura H, Kamio K, Rennard SI. Smad3 mediates TGF-beta1-induced collagen gel contraction by human lung fibroblasts. Biochem Biophys Res Commun 339: 290-295, 2006.
36. Kolodney MS, Elson EL. Correlation of myosin light chain phosphorylation with isometric contraction of fibroblasts. J Biol Chem 268: 23850-23855, 1993.
37. 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.
38. Lauffenburger DA, Horwitz AF. Cell migration: a physically integrated molecular process. Cell 84: 359-369, 1996.
39. Liu F, Mih JD, Shea BS, Kho AT, Sharif AS, Tager AM, Tschump-erlin DJ. Feedback amplification of fibrosis through matrix stiffening and COX-2 suppression. J Cell Biol 190: 693-706, 2010.
40. Lo CM, Wang HB, Dembo M, Wang YL. Cell movement is guided by the rigidity of the substrate. Biophys J 79: 144-152, 2000.
41. Madri JA, Pratt BM, Tucker AM. Phenotypic modulation of endothelial cells by transforming growth factor-beta depends upon the composition and organization of the extracellular matrix. J Cell Biol 106: 1375-1384, 1988.
42. Massague J, Gomis RR. The logic of TGFbeta signaling. FEBS Lett 580: 2811-2820, 2006.
43. Mih JD, Sharif AS, Liu F, Marinkovic A, Symer MM, Tschumperlin DJ. A multiwell platform for studying stiffness-dependent cell biology. PloS One 6: e19929, 2011.
44. 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.
45. Moore SW, Roca-Cusachs P, Sheetz MP. Stretchy proteins on stretchy substrates: the important elements of integrin-mediated rigidity sensing. Dev Cell 19: 194-206, 2010.
46. Numaguchi Y, Huang S, Polte TR, Eichler GS, Wang N, Ingber DE. Caldesmon-dependent switching between capillary endothelial cell growth and apoptosis through modulation of cell shape and contractility. Angio-genesis 6: 55-64, 2003.
47. Otsu N. A threshold selection method from gray-level histograms. IEEE Trans Syst Man Cybern 9: 62-66, 1979.
48. Paszek MJ, Zahir N, Johnson KR, Lakins JN, Rozenberg GI, Gefen A, Reinhart-King CA, Margulies SS, Dembo M, Boettiger D, Hammer DA, Weaver VM. Tensional homeostasis and the malignant phenotype. Cancer Cell 8: 241-254, 2005.
49. Patla I, Volberg T, Elad N, Hirschfeld-Warneken V, Grashoff C, Fassler R, Spatz JP, Geiger B, Medalia O. Dissecting the molecular architecture of integrin adhesion sites by cryo-electron tomography. Nat Cell Biol 12: 909-915, 2010.
50. Peterson LJ, Rajfur Z, Maddox AS, Freel CD, Chen Y, Edlund M, Otey C, Burridge K. Simultaneous stretching and contraction of stress fibers in vivo. Mol Biol Cell 15: 3497-3508, 2004.
51. Polio SR, Rothenberg KE, Stamenovic D, Smith ML. A micropattern-ing and image processing approach to simplify measurement of cellular traction forces. Acta Biomater 8: 82-88, 2012.
52. Regen CM, Horwitz AF. Dynamics of beta 1 integrin-mediated adhesive contacts in motile fibroblasts. J Cell Biol 119: 1347-1359, 1992.
53. Saez A, Buguin A, Silberzan P, Ladoux B. Is the mechanical activity of epithelial cells controlled by deformations or forces? Biophys J 89: L52-L54, 2005.
54. Shi M, Zhu J, Wang R, Chen X, Mi L, Walz T, Springer TA. Latent TGF-beta structure and activation. Nature 474: 343-349, 2011.
55. 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, 2010.
56. Solon J, Levental I, Sengupta K, Georges PC, Janmey PA. Fibroblast adaptation and stiffness matching to soft elastic substrates. Biophys J 93: 4453-4461, 2007.
57. Tan JL, Tien J, Pirone DM, Gray DS, Bhadriraju K, Chen CS. Cells lying on a bed of microneedles: an approach to isolate mechanical force. Proc Natl Acad Sci USA 100: 1484-1489, 2003.
58. Tolic-Norrelykke IM, Butler JP, Chen J, Wang N. Spatial and temporal traction response in human airway smooth muscle cells. Am J Physiol Cell Physiol 283: C1254-C1266, 2002.
59. Tolic-Norrelykke IM, Wang N. Traction in smooth muscle cells varies with cell spreading. J Biomech 38: 1405-1412, 2005.
60. Tomasek JJ, Gabbiani G, Hinz B, Chaponnier C, Brown RA. Myofi-broblasts and mechano-regulation of connective tissue remodelling. Nat Rev Mol Cell Biol 3: 349-363, 2002.
61. Totsukawa G, Yamakita Y, Yamashiro S, Hartshorne DJ, Sasaki Y, Matsumura F. Distinct roles of ROCK (Rho-kinase) and MLCK in spatial regulation of MLC phosphorylation for assembly of stress fibers and focal adhesions in 3T3 fibroblasts. J Cell Biol 150: 797-806, 2000.
62. Tseng Q, Wang I, Duchemin-Pelletier E, Azioune A, Carpi N, Gao J, Filhol O, Piel M, Thery M, Balland M. A new micropatterning method of soft substrates reveals that different tumorigenic signals can promote or reduce cell contraction levels. Lab Chip 11: 2231-2240, 2011.
63. Varelas X, Sakuma R, Samavarchi-Tehrani P, Peerani R, Rao BM, Dembowy J, Yaffe MB, Zandstra PW, Wrana JL. TAZ controls Smad nucleocytoplasmic shuttling and regulates human embryonic stem-cell self-renewal. Nat Cell Biol 10: 837-848, 2008.
64. Varelas X, Samavarchi-Tehrani P, Narimatsu M, Weiss A, Cockburn K, Larsen BG, Rossant J, Wrana JL. The Crumbs complex couples cell density sensing to Hippo-dependent control of the TGF-beta-SMAD pathway. Dev Cell 19: 831-844, 2010.
65. Vicente-Manzanares M, Ma X, Adelstein RS, Horwitz AR. Non-muscle myosin II takes centre stage in cell adhesion and migration. Nat Rev Mol Cell Biol 10: 778-790, 2009.
66. Vollath D. Automatic Focusing by Correlative Methods. J Microsc 147: 279-288, 1987.
67. Weng S, Fu J. Synergistic regulation of cell function by matrix rigidity and adhesive pattern. Biomaterials 32: 9584-9593, 2011.
68. Wipff PJ, Rifkin DB, Meister JJ, Hinz B. Myofibroblast contraction activates latent TGF-beta1 from the extracellular matrix. J Cell Biol 179: 1311-1323, 2007.
69. Wrobel LK, Fray TR, Molloy JE, Adams JJ, Armitage MP, Sparrow JC. Contractility of single human dermal myofibroblasts and fibroblasts. Cell Motil Cytoskeleton 52: 82-90, 2002.
70. Yang MT, Reich DH, Chen CS. Measurement and analysis of traction force dynamics in response to vasoactive agonists. Integr Biol (Camb) 3: 663-674, 2011.
71. Zhang HY, Gharaee-Kermani M, Zhang K, Karmiol S, Phan SH. Lung fibroblast alpha-smooth muscle actin expression and contractile phenotype in bleomycin-induced pulmonary fibrosis. Am J Pathol 148: 527-537, 1996.
72. Zhang K, Rekhter MD, Gordon D, Phan SH. Myofibroblasts and their role in lung collagen gene expression during pulmonary fibrosis. A combined immunohistochemical and in situ hybridization study. Am J Pathol 145: 114-125, 1994.