Mechanosignaling through YAP and TAZ drives fibroblast activation and fibrosis

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 308, Issue 4, 2015, Pages L344-L357

  Liu, Fei ^a   Lagares, David ^b   Choi, Kyoung Moo ^c   Stopfer, Lauren ^c   Marinković, Aleksandar ^a   Vrbanac, Vladimir ^b   Probst, Clemens K ^b   Hiemer, Samantha E ^d   Sisson, Thomas H ^e   Horowitz, Jeffrey C ^e   Rosas, Ivan O ^f   Fredenburgh, Laura E ^f   Feghali Bostwick, Carol ^g   Varelas, Xaralabos ^d   Tager, Andrew M ^b   Tschumperlin, Daniel J ^a,c  

^a HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c MAYO GRADUATE SCHOOL   (United States)

^d BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^f BRIGHAM AND WOMEN S HOSPITAL   (United States)

^g MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

Extracellular matrix; Hippo; Idiopathic pulmonary fibrosis; Mechanotransduction; Plasminogen activator inhibitor 1

Indexed keywords

MUTANT PROTEIN; PLASMINOGEN ACTIVATOR INHIBITOR 1; TRANSCRIPTION FACTOR; TRANSCRIPTIONAL COACTIVATOR WIH PDZ BINDING MOTIF; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; YES ASSOCIATED PROTEIN; PHOSPHOPROTEIN; PROTEASE NEXIN I; SERPINE1 PROTEIN, HUMAN; SERPINE2 PROTEIN, MOUSE; SIGNAL TRANSDUCING ADAPTOR PROTEIN; TAZ PROTEIN, HUMAN; TAZ PROTEIN, MOUSE; YAP PROTEIN, MOUSE; YAP1 (YES-ASSOCIATED) PROTEIN, HUMAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL FUNCTION; CELL IMMORTALIZATION; CELL NUCLEUS; CLINICAL ARTICLE; CONTROLLED STUDY; EXTRACELLULAR MATRIX; FEEDBACK SYSTEM; FIBROBLAST CULTURE; FIBROGENESIS; FIBROSING ALVEOLITIS; HUMAN; HUMAN CELL; HUMAN TISSUE; LUNG FIBROBLAST; LUNG FIBROSIS; LUNG PARENCHYMA; MALE; MECHANOTRANSDUCTION; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RIGIDITY; SPINDLE CELL; 3T3 CELL LINE; ANIMAL; BIOSYNTHESIS; CLINICAL TRIAL; FEMALE; FIBROBLAST; GENE SILENCING; GENETICS; LUNG; METABOLISM; MUTATION; NONOBESE DIABETIC MOUSE; PATHOLOGY;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; FEMALE; FIBROBLASTS; GENE KNOCKDOWN TECHNIQUES; HUMANS; LUNG; MALE; MECHANOTRANSDUCTION, CELLULAR; MICE; MICE, INBRED NOD; MUTATION; NIH 3T3 CELLS; PHOSPHOPROTEINS; PLASMINOGEN ACTIVATOR INHIBITOR 1; PULMONARY FIBROSIS; SERPIN E2; TRANSCRIPTION FACTORS; TRANSFORMING GROWTH FACTOR BETA;

EID: 84922967715     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00300.2014     Document Type: Article

References (64)

1. Abe M, Harpel JG, Metz CN, Nunes I, Loskutoff DJ, Rifkin DB. An assay for transforming growth factor-beta using cells transfected with a plasminogen activator inhibitor-1 promoter-luciferase construct. Anal Biochem 216: 276-284, 1994.
2. Aragona M, Panciera T, Manfrin A, Giulitti S, Michielin F, Elvassore N, Dupont S, Piccolo S. A mechanical checkpoint controls multicellular growth through YAP/TAZ regulation by actin-processing factors. Cell 154: 1047-1059, 2013.
3. Balestrini JL, Chaudhry S, Sarrazy V, Koehler A, Hinz B. The mechanical memory of lung myofibroblasts. Integr Biol (Camb) 4: 410-421, 2012.
4. Barry-Hamilton V, Spangler R, Marshall D, McCauley S, Rodriguez HM, Oyasu M, Mikels A, Vaysberg M, Ghermazien H, Wai C, Garcia CA, Velayo AC, Jorgensen B, Biermann D, Tsai D, Green J, Zaffryar-Eilot S, Holzer A, Ogg S, Thai D, Neufeld G, Van Vlasselaer P, Smith V. Allosteric inhibition of lysyl oxidase-like-2 impedes the development of a pathologic microenvironment. Nat Med 16: 1009-1017, 2010.
5. Beacham DA, Amatangelo MD, Cukierman E. Preparation of extracellular matrices produced by cultured and primary fibroblasts. Curr Protoc Cell Biol 10: 19, 2007.
6. Booth AJ, Hadley R, Cornett AM, Dreffs AA, Matthes SA, Tsui JL, Weiss K, Horowitz JC, Fiore VF, Barker TH, Moore BB, Martinez FJ, Niklason LE, White ES. Acellular normal and fibrotic human lung matrices as a culture system for in vitro investigation. Am J Respir Crit Care Med 186: 866-876, 2012.
7. Brown AC, Fiore VF, Sulchek TA, Barker TH. Physical and chemical microenvironmental cues orthogonally control the degree and duration of fibrosis-associated epithelial-to-mesenchymal transitions. J Pathol 229: 25-35, 2013.
8. Butler JP, Nakamura M, Sasaki H, Sasaki T, Takishima T. Poissons’ ratio of lung parenchyma and parenchymal interaction with bronchi. Jpn J Physiol 36: 91-106, 1986.
9. Calvo F, Ege N, Grande-Garcia A, Hooper S, Jenkins RP, Chaudhry SI, Harrington K, Williamson P, Moeendarbary E, Charras G, Sahai E. Mechanotransduction and YAP-dependent matrix remodelling is required for the generation and maintenance of cancer-associated fibroblasts. Nat Cell Biol 15: 637-646, 2013.
10. Chuang-Tsai S, Sisson TH, Hattori N, Tsai CG, Subbotina NM, Hanson KE, Simon RH. Reduction in fibrotic tissue formation in mice genetically deficient in plasminogen activator inhibitor-1. Am J Pathol 163: 445-452, 2003.
11. 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.
12. 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.
13. Esnault C, Stewart A, Gualdrini F, East P, Horswell S, Matthews N, Treisman R. Rho-actin signaling to the MRTF coactivators dominates the immediate transcriptional response to serum in fibroblasts. Genes Dev 28: 943-958, 2014.
14. Friedman SL, Sheppard D, Duffield JS, Violette S. Therapy for fibrotic diseases: nearing the starting line. Sci Transl Med 5: 167sr161, 2013.
15. Georges PC, Hui JJ, Gombos Z, McCormick ME, Wang AY, Uemura M, Mick R, Janmey PA, Furth EE, Wells RG. Increased stiffness of the rat liver precedes matrix deposition: implications for fibrosis. Am J Physiol Gastrointest Liver Physiol 293: G1147-G1154, 2007.
16. Ghosh AK, Vaughan DE. PAI-1 in tissue fibrosis. J Cell Physiol 227: 493-507, 2012.
17. 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.
18. Hardie WD, Glasser SW, Hagood JS. Emerging concepts in the pathogenesis of lung fibrosis. Am J Pathol 175: 3-16, 2009.
19. Hattori N, Mizuno S, Yoshida Y, Chin K, Mishima M, Sisson TH, Simon RH, Nakamura T, Miyake M. The plasminogen activation system reduces fibrosis in the lung by a hepatocyte growth factordependent mechanism. Am J Pathol 164: 1091-1098, 2004.
20. Horowitz JC, Rogers DS, Simon RH, Sisson TH, Thannickal VJ. Plasminogen activation induced pericellular fibronectin proteolysis promotes fibroblast apoptosis. Am J Respir Cell Mol Biol 38: 78-87, 2008.
21. Huang SK, Fisher AS, Scruggs AM, White ES, Hogaboam CM, Richardson BC, Peters-Golden M. Hypermethylation of PTGER2 confers prostaglandin E2 resistance in fibrotic fibroblasts from humans and mice. Am J Pathol 177: 2245-2255, 2010.
22. Huang WT, Vayalil PK, Miyata T, Hagood J, Liu RM. Therapeutic value of small molecule inhibitor to plasminogen activator inhibitor-1 for lung fibrosis. Am J Respir Cell Mol Biol 46: 87-95, 2012.
23. Huang X, Yang N, Fiore VF, Barker TH, Sun Y, Morris SW, Ding Q, Thannickal VJ, Zhou Y. Matrix stiffness-induced myofibroblast differentiation is mediated by intrinsic mechanotransduction. Am J Respir Cell Mol Biol 47: 340-348, 2012.
24. Janmey PA, Wells RG, Assoian RK, McCulloch CA. From tissue mechanics to transcription factors. Differentiation 86: 112-120, 2013.
25. Johnson LA, Rodansky ES, Sauder KL, Horowitz JC, Mih JD, Tschumperlin DJ, Higgins PD. Matrix stiffness corresponding to strictured bowel induces a fibrogenic response in human colonic fibroblasts. Inflamm Bowel Dis 19: 891-903, 2013.
26. Jun JI, Lau LF. Taking aim at the extracellular matrix: CCN proteins as emerging therapeutic targets. Nat Rev Drug Discov 10: 945-963, 2011.
27. Kanai F, Marignani PA, Sarbassova D, Yagi R, Hall RA, Donowitz M, Hisaminato A, Fujiwara T, Ito Y, Cantley LC, Yaffe MB. TAZ: a novel transcriptional co-activator regulated by interactions with 14-3-3 and PDZ domain proteins. EMBO J 19: 6778-6791, 2000.
28. Lee H, Dellatore SM, Miller WM, Messersmith PB. Mussel-inspired surface chemistry for multifunctional coatings. Science 318: 426-430, 2007.
29. Lei QY, Zhang H, Zhao B, Zha ZY, Bai F, Pei XH, Zhao S, Xiong Y, Guan KL. TAZ promotes cell proliferation and epithelial-mesenchymal transition and is inhibited by the hippo pathway. Mol Cell Biol 28: 2426-2436, 2008.
30. Li Y, Jiang D, Liang J, Meltzer EB, Gray A, Miura R, Wogensen L, Yamaguchi Y, Noble PW. Severe lung fibrosis requires an invasive fibroblast phenotype regulated by hyaluronan and CD44. J Exp Med 208: 1459-1471, 2011.
31. Li Z, Dranoff JA, Chan EP, Uemura M, Sevigny J, Wells RG. Transforming growth factor-beta and substrate stiffness regulate portal fibroblast activation in culture. Hepatology 46: 1246-1256, 2007.
32. Liu F, Mih JD, Shea BS, Kho AT, Sharif AS, Tager AM, Tschumperlin DJ. Feedback amplification of fibrosis through matrix stiffening and COX-2 suppression. J Cell Biol 190: 693-706, 2010.
33. Liu F, Tschumperlin DJ. Micro-mechanical characterization of lung tissue using atomic force microscopy. J Vis Exp 28: 2911, 2011.
34. Mahoney JE, Mori M, Szymaniak AD, Varelas X, Cardoso WV. The hippo pathway effector yap controls patterning and differentiation of airway epithelial progenitors. Dev Cell 30: 137-150, 2014.
35. Makita R, Uchijima Y, Nishiyama K, Amano T, Chen Q, Takeuchi T, Mitani A, Nagase T, Yatomi Y, Aburatani H, Nakagawa O, Small EV, Cobo-Stark P, Igarashi P, Murakami M, Tominaga J, Sato T, Asano T, Kurihara Y, Kurihara H. Multiple renal cysts, urinary concentration defects, and pulmonary emphysematous changes in mice lacking TAZ. Am J Physiol Renal Physiol 294: F542-F553, 2008.
36. Marinkovic A, Liu F, Tschumperlin DJ. Matrices of physiologic stiffness potently inactivate idiopathic pulmonary fibrosis fibroblasts. Am J Respir Cell Mol Biol 48: 422-430, 2013.
37. Marinkovic A, Mih JD, Park JA, Liu F, Tschumperlin DJ. Improved throughput traction microscopy reveals pivotal role for matrix stiffness in fibroblast contractility and TGF-_ responsiveness. Am J Physiol Lung Cell Mol Physiol 303: L169-L180, 2012.
38. Mauviel A, Nallet-Staub F, Varelas X. Integrating developmental signals: a Hippo in the (path)way. Oncogene 31: 1743-1756, 2012.
39. McDonald JA, Kelley DG, Broekelmann TJ. Role of fibronectin in collagen deposition: Fab’ to the gelatin-binding domain of fibronectin inhibits both fibronectin and collagen organization in fibroblast extracellular matrix. J Cell Biol 92: 485-492, 1982.
40. 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.
41. 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 180: 326-338, 2009.
42. Morin-Kensicki EM, Boone BN, Howell M, Stonebraker JR, Teed J, Alb JG, Magnuson TR, O’Neal W, Milgram SL. Defects in yolk sac vasculogenesis, chorioallantoic fusion, and embryonic axis elongation in mice with targeted disruption of Yap65. Mol Cell Biol 26: 77-87, 2006.
43. Murray LA, Zhang H, Oak SR, Coelho AL, Herath A, Flaherty KR, Lee J, Bell M, Knight DA, Martinez FJ, Sleeman MA, Herzog EL, Hogaboam CM. Targeting IL-13 with tralokinumab attenuates lung fibrosis and epithelial damage in a humanized SCID IPF model. Am J Respir Cell Mol Biol 50: 985-994, 2013.
44. Noble PW, Barkauskas CE, Jiang D. Pulmonary fibrosis: patterns and perpetrators. J Clin Invest 122: 2756-2762, 2012.
45. Parker MW, Rossi D, Peterson M, Smith K, Sikstrom K, White ES, Connett JE, Henke CA, Larsson O, Bitterman PB. Fibrotic extracellular matrix activates a profibrotic positive feedback loop. J Clin Invest 124: 1622-1635, 2014.
46. Pierce EM, Carpenter K, Jakubzick C, Kunkel SL, Flaherty KR, Martinez FJ, Hogaboam CM. Therapeutic targeting of CC ligand 21 or CC chemokine receptor 7 abrogates pulmonary fibrosis induced by the adoptive transfer of human pulmonary fibroblasts to immunodeficient mice. Am J Pathol 170: 1152-1164, 2007.
47. Pilewski JM, Liu L, Henry AC, Knauer AV, Feghali-Bostwick CA. Insulin-like growth factor binding proteins 3 and 5 are overexpressed in idiopathic pulmonary fibrosis and contribute to extracellular matrix deposition. Am J Pathol 166: 399-407, 2005.
48. 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.
49. Tager AM, LaCamera P, Shea BS, Campanella GS, Selman M, Zhao Z, Polosukhin V, Wain J, Karimi-Shah BA, Kim ND, Hart WK, Pardo A, Blackwell TS, Xu Y, Chun J, Luster AD. The lysophosphatidic acid receptor LPA1 links pulmonary fibrosis to lung injury by mediating fibroblast recruitment and vascular leak. Nat Med 14: 45-54, 2008.
50. Trujillo G, Meneghin A, Flaherty KR, Sholl LM, Myers JL, Kazerooni EA, Gross BH, Oak SR, Coelho AL, Evanoff H, Day E, Toews GB, Joshi AD, Schaller MA, Waters B, Jarai G, Westwick J, Kunkel SL, Martinez FJ, Hogaboam CM. TLR9 differentiates rapidly from slowly progressing forms of idiopathic pulmonary fibrosis. Sci Transl Med 2: 57ra82, 2010.
51. 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.
52. Wada K, Itoga K, Okano T, Yonemura S, Sasaki H. Hippo pathway regulation by cell morphology and stress fibers. Development 138: 3907-3914, 2011.
53. 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.
54. 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.
55. Wynn TA, Ramalingam TR. Mechanisms of fibrosis: therapeutic translation for fibrotic disease. Nat Med 18: 1028-1040, 2012.
56. Yagi R, Chen LF, Shigesada K, Murakami Y, Ito Y. A WW domaincontaining yes-associated protein (YAP) is a novel transcriptional coactivator. EMBO J 18: 2551-2562, 1999.
57. Yang C, Tibbitt MW, Basta L, Anseth KS. Mechanical memory and dosing influence stem cell fate. Nat Mater 13: 645-652, 2014.
58. Yu FX, Zhao B, Panupinthu N, Jewell JL, Lian I, Wang LH, Zhao J, Yuan H, Tumaneng K, Li H, Fu XD, Mills GB, Guan KL. Regulation of the Hippo-YAP pathway by G-protein-coupled receptor signaling. Cell 150: 780-791, 2012.
59. Zhao B, Li L, Guan KL. Hippo signaling at a glance. J Cell Sci 123: 4001-4006, 2010.
60. Zhao B, Li L, Lei Q, Guan KL. The Hippo-YAP pathway in organ size control and tumorigenesis: an updated version. Genes Dev 24: 862-874, 2010.
61. Zhao B, Wei X, Li W, Udan RS, Yang Q, Kim J, Xie J, Ikenoue T, Yu J, Li L, Zheng P, Ye K, Chinnaiyan A, Halder G, Lai ZC, Guan KL. Inactivation of YAP oncoprotein by the Hippo pathway is involved in cell contact inhibition and tissue growth control. Genes Dev 21: 2747-2761, 2007.
62. Zhao B, Ye X, Yu J, Li L, Li W, Li S, Lin JD, Wang CY, Chinnaiyan AM, Lai ZC, Guan KL. TEAD mediates YAP-dependent gene induction and growth control. Genes Dev 22: 1962-1971, 2008.
63. Zhao R, Fallon TR, Saladi SV, Pardo-Saganta A, Villoria J, Mou H, Vinarsky V, Gonzalez-Celeiro M, Nunna N, Hariri LP, Camargo F, Ellisen LW, Rajagopal J. YAP tunes airway epithelial size and architecture by regulating the identity, maintenance, and self-renewal of stem cells. Dev Cell 30: 151-165, 2014.
64. Zhou Y, Huang X, Hecker L, Kurundkar D, Kurundkar A, Liu H, Jin TH, Desai L, Bernard K, Thannickal VJ. Inhibition of mechanosensitive signaling in myofibroblasts ameliorates experimental pulmonary fibrosis. J Clin Invest 123: 1096-1108, 2013.