Biomechanical regulation of mesenchymal cell function

Current Opinion in Rheumatology

Volumn 25, Issue 1, 2013, Pages 92-100

  Tschumperlin, Daniel J ^a   Liu, Fei ^a   Tager, Andrew M ^b  

^a HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

Extracellular matrix; fibrosis; mechanotransduction; stiffness

Indexed keywords

BETA CATENIN; FOCAL ADHESION KINASE; PROTEIN TAZ; PROTEIN YAP; SMAD PROTEIN; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; WNT PROTEIN;

ANGIOGENESIS; BIOMECHANICS; CELL ACTIVATION; EXTRACELLULAR MATRIX; FIBROSIS; HYPERTROPHIC SCAR; MESENCHYME CELL; MYOFIBROBLAST; PRIORITY JOURNAL; REVIEW;

ANIMALS; CICATRIX, HYPERTROPHIC; EXTRACELLULAR MATRIX; FIBROSIS; HUMANS; MECHANOTRANSDUCTION, CELLULAR; MESENCHYMAL STROMAL CELLS; MYOFIBROBLASTS; WOUND HEALING;

EID: 84871248579     PISSN: 10408711     EISSN: 15316963     Source Type: Journal    
DOI: 10.1097/BOR.0b013e32835b13cd     Document Type: Review

References (72)

1. Li Z, Dranoff JA, Chan EP, et al. Transforming growth factor-beta and substrate stiffness regulate portal fibroblast activation in culture. Hepatology 2007; 46:1246-1256.
2. Liu F, Mih JD, Shea BS, et al. Feedbackamplification offibrosisthrough matrix stiffening and COX-2 suppression. J Cell Biol 2010; 190:693-706.
3. Prager-Khoutorsky M, Lichtenstein A, Krishnan R, et al. Fibroblast polarization is a matrix-rigidity-dependent process controlled by focal adhesion mechan-osensing. Nat Cell Biol 2011; 13:1457-1465.
4. Balestrini JL, Chaudhry S, Sarrazy V, et al. The mechanical memory of lung myofibroblasts. Integr Biol (Camb) 2012; 4:410-421.
5. Huang X, Yang N, Fiore VF, et al. Matrix stiffness-induced myofibroblast differentiation is mediated by intrinsic mechanotransduction. Am J Respir Cell Mol Biol 2012; 47:340-348.
6. Chen JH, Chen WL, Sider KL, et al. beta-catenin mediates mechanically regulated, transforming growth factor-beta1-induced myofibroblast differen-tiation of aortic valve interstitial cells. Arterioscler Thromb Vasc Biol 2011; 31:590-597.
7. Galie PA, Westfall MV, Stegemann JP. Reduced serum content and increased matrix stiffness promote the cardiac myofibroblast transition in 3D collagen matrices. Cardiovasc Pathol 2011; 20:325-333.
8. Marinkovic A, Mih JD, Park JA, et al. Improved throughput traction microscopy reveals pivotal role for matrix stiffness in fibroblast contractility and TGF-beta responsiveness. Am J Physiol Lung Cell Mol Physiol 2012; 00:000-000.
9. Leight JL, Wozniak MA, Chen S, et al. Matrix rigidity regulates a switch between TGF-beta1-induced apoptosis and epithelial-mesenchymal transition. Mol Biol Cell 2012; 23:781-791.
10. Olsen AL, Bloomer SA, Chan EP, et al. Hepatic stellate cells require a stiff environment for myofibroblastic differentiation. Am J Physiol Gastrointest Liver Physiol 2011; 301:G110-G118.
11. Heise RL, Stober V, Cheluvaraju C, et al. Mechanical stretch induces epithelial-mesenchymal transition in alveolar epithelia via hyaluronan activation of innate immunity. J Biol Chem 2011; 286:17435-17444.
12. Boudreault F, Tschumperlin DJ. Stretch-induced mitogen-activated protein kinase activation in lung fibroblasts is independent of receptor tyrosine kinases. Am J Respir Cell Mol Biol 2010; 43:64-73.
13. Paterno J, Vial IN, Wong VW, et al. Akt-mediated mechanotransduction in murine fibroblasts during hypertrophic scar formation. Wound Repair Regen 2011; 19:49-58.
14. Maeda T, Sakabe T, Sunaga A, et al. Conversion of mechanical force into TGF-beta-mediated biochemical signals. Curr Biol 2011; 21:933-941.
15. Guo F, Carter DE, Leask A. Mechanical tension increases CCN2/CTGF expression and proliferation in gingival fibroblasts via a TGFbeta-dependent mechanism. PLo S One 2011; 6:e19756.
16. Lu F, Ogawa R, Nguyen DT, et al. Microdeformation of three-dimensional cultured fibroblasts induces gene expression and morphological changes. Ann Plast Surg 2011; 66:296-300.
17. Blaauboer ME, Smit TH, Hanemaaijer R, et al. Cyclic mechanical stretch reduces myofibroblast differentiation of primary lung fibroblasts. Biochem Biophys Res Commun 2011; 404:23-27.
18. Throm Quinlan AM, Sierad LN, Capulli AK, et al. Combining dynamic stretch and tunable stiffness to probe cell mechanobiology in vitro. PLo S One 2011; 6:e23272.
19. Mammoto A, Connor KM, Mammoto T, et al. A mechanosensitive transcrip-tional mechanism that controls angiogenesis. Nature 2009; 457:1103-1108.
20. Rao RR, Peterson AW, Ceccarelli J, et al. Matrix composition regulatesthree-dimensional network formation by endothelial cells and mesenchymal stem cells in collagen/fibrin materials. Angiogenesis 2012; 15:253-264.
21. Huynh J, Nishimura N, Rana K, et al. Age-related intimal stiffening enhances endothelial permeability and leukocyte transmigration. Sci Transl Med 2011; 3:112-122.
22. Stroka KM, Aranda-Espinoza H. Endothelial cell substrate stiffness influences neutrophil transmigration via myosin light chain kinase-dependent cell con-traction. Blood 2011; 118:1632-1640.
23. Krishnan R, Klumpers DD, Park CY, et al. Substrate stiffening promotes endothelial monolayer disruption through enhanced physical forces. Am J Physiol Cell Physiol 2011; 300:C146-C154.
24. Engler AJ, Sen S, Sweeney HL, Discher DE. Matrix elasticity directs stem cell lineage specification. Cell 2006; 126:677-689.
25. Dupont S, Morsut L, Aragona M, et al. Role of YAP/TAZ in mechano transduction. Nature 2011; 474:179-183.
26. Park JS, Chu JS, Tsou AD, et al. The effect of matrix stiffness on the differentiation of mesenchymal stem cells in response to TGF-beta. Biomaterials 2011; 32:3921-3930.
27. Guvendiren M, Burdick JA. Stiffening hydrogels to probeshort-and long-term cellular responses to dynamic mechanics. Nat Commun 2012; 3:792.
28. Fu J, Wang YK, Yang MT, et al. Mechanical regulation of cell function with geometrically modulated elastomericsubstrates. Nat Methods 2010; 7:733-736.
29. Munger JS, Sheppard D. Cross talk among TGF-beta signaling pathways, integrins, and the extracellular matrix. Cold Spring Harb Perspect Biol 2011; 3:a005017.
30. Munger JS, Huang X, Kawakatsu H, et al. The integrin alphavbeta6 bindsand activates latent TGF beta 1: a mechanism for regulating pulmonary inflamma-tion and fibrosis. Cell 1999; 96:319-328.
31. Wipff PJ, Rifkin DB, Meister JJ, Hinz B. Myofibroblast contraction activates latent TGF-beta1 from the extracellular matrix. J Cell Biol 2007; 179:1311-1323.
32. Buscemi L, Ramonet D, Klingberg F, et al. The single-molecule mechanics of the latent TGF-beta1 complex. Curr Biol 2011; 21:2046-2054.
33. Shi M, Zhu J, Wang R, et al. Latent TGF-beta structure and activation. Nature 2011; 474:343-349.
34. Moore SW, Roca-Cusachs P, Sheetz MP. Stretchy proteins on stretchy substrates: the important elements of integrin-mediated rigidity sensing. Dev Cell 2010; 19:194-206.
35. Patla I, Volberg T, Elad N, et al. Dissecting the molecular architecture of integrin adhesion sites by cryo-electron tomography. Nat Cell Biol 2010; 12:909-915.
36. Eyckmans J, Boudou T, Yu X, Chen CS. A hitchhiker's guide to mechan-obiology. Dev Cell 2011; 21:35-47.
37. Goldmann WH. Mechanotransduction and focal adhesions. Cell Biol Inter-national 2012; 36:649-652.
38. Wang HB, Dembo M, Hanks SK, Wang Y. Focal adhesion kinase is involved in mechanosensing during fibroblast migration. Proc Natl Acad Sci USA 2001; 98:11295-11300.
39. Wong VW, Rustad KC, Akaishi S, et al. Focal adhesion kinase links mechan-ical forceto skin fibrosis via inflammatory signaling. Nat Med 2012; 18:148-152.
40. Aarabi S, Bhatt KA, Shi Y, et al. Mechanical load initiates hypertrophic scar formation through decreased cellular apoptosis. Faseb J 2007; 21:3250-3261.
41. Olson EN, Nordheim A. Linking actin dynamicsand genetranscription todrive cellular motile functions. Nat Rev Mol Cell Biol 2010; 11:353-365.
42. Sotiropoulos A, Gineitis D, Copeland J, Treisman R. Signal-regulated activa-tion of serum response factor is mediated by changes in actin dynamics. Cell 1999; 98:159-169.
43. Miralles F, Posern G, Zaromytidou AI, Treisman R. Actin dynamics control SRF activity by regulation of its coactivator MAL. Cell 2003; 113:329-342.
44. Small EM, Thatcher JE, Sutherland LB, et al. Myocardin-related transcription factor-a controls myofibroblast activation and fibrosis in response to myo-cardial infarction. Circ Res 2010; 107:294-304.
45. Lam AP, Gottardi CJ. beta-catenin signaling: a novel mediator of fibrosis and potential therapeutic target. Curr Opin Rheumatol 2011; 23:562-567.
46. Beyer C, Schramm A, Akhmetshina A, et al. beta-catenin is acentral mediator of pro-fibrotic Wnt signaling in systemic sclerosis. Ann Rheum Dis 2012; 71:761-767.
47. Samuel MS, Lopez JI, Mc Ghee EJ, et al. Actomyosin-mediated cellulartension drives increased tissue stiffness and beta-catenin activation to induce epidermal hyperplasia and tumor growth. Cancer Cell 2011; 19:776-791.
48. Charbonney E, Speight P, Masszi A, et al. beta-catenin and Smad3 regulate the activity and stability of myocardin-related transcription factor during epithelial-myofibroblasttransition. Mol Biol Cell 2011; 22:4472-4485.
49. Rauskolb C, Pan G, Reddy BV, et al. Zyxin links fat signaling to the hippo pathway. PLo S Biol 2011; 9:e1000624.
50. Sansores-Garcia L, Bossuyt W, Wada K, et al. Modulating F-actin organiza-tion induces organ growth by affecting the Hippo pathway. EMBO J 2011; 30:2325-2335.
51. Wada K, Itoga K, Okano T, et al. Hippo pathway regulation by cell morphology and stressfibers. Development 2011; 138:3907-3914.
52. Hong JH, Hwang ES, Mc Manus MT, et al. TAZ, a transcriptional modulator of mesenchymal stem cell differentiation. Science 2005; 309:1074-1078.
53. Varelas X, Sakuma R, Samavarchi-Tehrani P, et al. TAZ controls Smad nucleocytoplasmic shuttling and regulates human embryonic stem-cell self-renewal. Nat Cell Biol 2008; 10:837-848.
54. Varelas X, Samavarchi-Tehrani P, Narimatsu M, et al. The Crumbs complex couples cell density sensing to Hippo-dependent control of the TGF-beta-SMAD pathway. Dev Cell 2010; 19:831-844.
55. Aragon E, Goerner N, Zaromytidou AI, et al. A Smad action turnover switch operated by WW domain readers of a phosphoserine code. Genes Dev 2011; 25:1275-1288.
56. Alarcon C, Zaromytidou AI, Xi Q, et al. Nuclear CDKs drive Smad transcrip-tional activation and turnover in BMP and TGF-beta pathways. Cell 2009; 139:757-769.
57. Heallen T, Zhang M, Wang J, et al. Hippo pathway inhibits Wnt signaling to restrain cardiomyocyte proliferation and heartsize. Science 2011; 332:458-461.
58. Varelas X, Miller BW, Sopko R, et al. The Hippo pathway regulates Wnt/beta-catenin signaling. Dev Cell 2010; 18:579-591.
59. Hinz B, Phan SH, Thannickal VJ, et al. Recent developments in myofibroblast biology: paradigms for connective tissue remodeling. Am J Pathol 2012; 180:1340-1355.
60. Wynn TA. Common and unique mechanisms regulate fibrosis in various fibroproliferative diseases. J Clin Invest 2007; 117:524-529.
61. Kolb MR, Gauldie J. Idiopathic pulmonary fibrosis: the matrix is the message. Am J Respir Crit Care Med 2011; 184:627-629.
62. Barry-Hamilton V, Spangler R, Marshall D, et al. Allosteric inhibition of lysyl oxidase-like-2 impedes the development of a pathologic microenvironment Nat Med 2010; 16:1009-1017.
63. Shweke N, Boulos N, Jouanneau C, et al. Tissuetransglutaminasecontributesto interstitial renal fibrosis by favoring accumulation of fibrillar collagen through TGF-beta activation and cell infiltration. Am J Pathol 2008; 173:631-642.
64. Olsen KC, Sapinoro RE, Kottmann RM, et al. Transglutaminase 2 and its role in pulmonary fibrosis. Am J Respir Crit Care Med 2011; 184:699-707.
65. Wong VW, Akaishi S, Longaker MT, Gurtner GC. Pushing back: wound mechanotransduction in repair and regeneration. J Invest Dermatol 2011; 131:2186-2196.
66. Bond JE, Ho TQ, Selim MA, et al. Temporal spatial expression and function of nonmuscle myosin II isoforms IIA and IIB in scar remodeling. Lab Invest 2011; 91:499-508.
67. Lagares D, Busnadiego O, Garcia-Fernandez RA, et al. Inhibition of focal adhesion kinase prevents experimental lung fibrosis and myofibroblast for-mation. Arthritis Rheum 2012; 64:1653-1664.
68. Wong VW, Paterno J, Sorkin M, et al. Mechanical force prolongs acute inflammation via T-cell-dependent pathways during scar formation. FASEB J 2011; 25:4498-4510.
69. Gurtner GC, Dauskardt RH, Wong VW, et al. Improving cutaneous scar formation by controlling the mechanical environment: large animal and phase I studies. Ann Surg 2011; 254:217-225.
70. Kuo JC, Han X, Hsiao CT, et al. Analysis of the myosin-II-responsive focal adhesion proteome reveals a role for beta-Pix in negative regulation of focal adhesion maturation. Nat Cell Biol 2011; 13:383-393.
71. Gilbert PM, Havenstrite KL, Magnusson KE, et al. Substrate elasticity reg-ulates skeletal muscle stem cell self-renewal in culture. Science 2010; 329:1078-1081.
72. Mih JD, Sharif AS, Liu F, et al. A multiwell platform for studying stiffness-dependent cell biology. PLo S One 2011; 6:e19929.