YAP/TAZ are mechanoregulators of TGF-b-smad signaling and renal fibrogenesis

Journal of the American Society of Nephrology

Volumn 27, Issue 10, 2016, Pages 3117-3128

  Szeto, Stephen G ^a,b   Narimatsu, Masahiro ^c   Lu, Mingliang ^a   He, Xiaolin ^a   Sidiqi, Ahmad M ^a,b   Tolosa, Monica F ^a,d   Chan, Lauren ^a   De Freitas, Krystale ^a   Bialik, Janne Folke ^a   Majumder, Syamantak ^a   Boo, Stellar ^e   Hinz, Boris ^e   Dan, Qinghong ^a   Advani, Andrew ^a,b   John, Rohan ^f   Wrana, Jeffrey L ^c   Kapus, Andras ^a,b   Yuen, Darren A ^a,b,d  

^a ST MICHAEL'S HOSPITAL   (Canada)

^b Institute of Medical Science   (Canada)

^c ST MICHAEL'S HOSPITAL   (Canada)

^d Graduate Studies Office   (Canada)

^e Division of Oral Biology   (Canada)

^f UNIVERSITY HEALTH NETWORK   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN; SMAD PROTEIN; SMAD2 PROTEIN; SMAD3 PROTEIN; TRANSCRIPTIONAL COACTIVATOR WITH PDZ BINDING MOTIF; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; VERTEPORFIN; YES ASSOCIATED PROTEIN; PHOSPHOPROTEIN; SIGNAL TRANSDUCING ADAPTOR PROTEIN; SMAD2 PROTEIN, MOUSE; SMAD3 PROTEIN, MOUSE; TAZ PROTEIN, MOUSE; TRANSCRIPTION FACTOR; YAP PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL GROWTH; CELL SURFACE; CELLULAR DISTRIBUTION; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CYTOSOL; DISEASE COURSE; EXTRACELLULAR MATRIX; FIBROBLAST; FIBROGENESIS; IMMUNOBLOTTING; IMMUNOFLUORESCENCE; IN SITU HYBRIDIZATION; IN VIVO STUDY; KIDNEY; KIDNEY FIBROSIS; MALE; MOUSE; MYOFIBROBLAST; NONHUMAN; NRK-49F CELL LINE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; URETER OBSTRUCTION; ANIMAL; C57BL MOUSE; FIBROSIS; PATHOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; FIBROSIS; KIDNEY; MALE; MICE; MICE, INBRED C57BL; PHOSPHOPROTEINS; SIGNAL TRANSDUCTION; SMAD2 PROTEIN; SMAD3 PROTEIN; TRANSCRIPTION FACTORS; TRANSFORMING GROWTH FACTOR BETA;

EID: 84983475728     PISSN: 10466673     EISSN: 15333450     Source Type: Journal    
DOI: 10.1681/ASN.2015050499     Document Type: Article

References (54)

1. LeBleu VS, Taduri G, O'Connell J, Teng Y, Cooke VG, Woda C, Sugimoto H, Kalluri R: Origin and function of myofibroblasts in kidney fibrosis. Nat Med 19: 1047-1053, 2013
2. Attisano L,Wrana JL: Signal transduction by the TGF-beta superfamily. Science 296: 1646-1647, 2002
3. Shi Y, Massagué J: Mechanisms of TGF-beta signaling from cell membrane to the nucleus. Cell 113: 685-700, 2003
4. Leask A, Abraham DJ: TGF-beta signaling and the fibrotic response. FASEB J 18: 816-827, 2004
5. Olsen AL, Bloomer SA, Chan EP, Gaça MD, Georges PC, Sackey B, Uemura M, Janmey PA, Wells RG: Hepatic stellate cells require a stiff environment for myofibroblastic differentiation. Am J Physiol Gastrointest Liver Physiol 301: G110-G118, 2011
6. Wells RG: Tissue mechanics and fibrosis. Biochim Biophys Acta 1832: 884-890, 2013
7. 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, ThaiD,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
8. 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
9. Salameh N, Larrat B, Abarca-Quinones J, Pallu S, DorvilliusM, Leclercq I, Fink M, Sinkus R, Van Beers BE: Early detection of steatohepatitis in fatty rat liver by using MR elastography. Radiology 253: 90-97, 2009
10. Perepelyuk M, Terajima M, Wang AY, Georges PC, Janmey PA, Yamauchi M, Wells RG: Hepatic stellate cells and portal fibroblasts are themajor cellular sources of collagens and lysyl oxidases in normal liver and early after injury. Am J Physiol Gastrointest Liver Physiol 304: G605-G614, 2013
11. 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
12. 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
13. Liu F, Mih JD, Shea BS, Kho AT, Sharif AS, Tager AM, Tschumperlin DJ: Feedback amplification of fibrosis throughmatrix stiffening and COX-2 suppression. J Cell Biol 190: 693-706, 2010
14. Beyer TA, Weiss A, Khomchuk Y, Huang K, Ogunjimi AA, Varelas X, Wrana JL: Switch enhancers interpret TGF-b and Hippo signaling to control cell fate in human embryonic stem cells. Cell Reports 5: 1611-1624, 2013
15. 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
16. 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-b-SMAD pathway. Dev Cell 19: 831-844, 2010
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. 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
19. Liu-Chittenden Y, Huang B, Shim JS, Chen Q, Lee SJ, Anders RA, Liu JO, Pan D: Genetic and pharmacological disruption of the TEAD-YAP complex suppresses the oncogenic activity of YAP. Genes Dev 26: 1300-1305, 2012
20. 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
21. Hinz B, Mastrangelo D, Iselin CE, Chaponnier C, Gabbiani G: Mechanical tension controls granulation tissue contractile activity and myofibroblast differentiation. Am J Pathol 159: 1009-1020, 2001
22. Fan L, Sebe A, Péterfi Z, Masszi A, Thirone AC, Rotstein OD, Nakano H, McCulloch CA, Szászi 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
23. Masszi A, Speight P, Charbonney E, Lodyga M, Nakano H, Szászi K, Kapus A: Fate-determining mechanisms in epithelial-myofibroblast transition: Major inhibitory role for Smad3. J Cell Biol 188: 383-399, 2010
24. Speight P, Nakano H, Kelley TJ, Hinz B, Kapus A: Differential topical susceptibility to TGFb in intact and injured regions of the epithelium: Key role in myofibroblast transition. Mol Biol Cell 24: 3326-3336, 2013
25. Zhao B,Wei X, LiW, Udan RS, YangQ, KimJ, 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
26. Swift J, Ivanovska IL, Buxboim A, Harada T, Dingal PC, Pinter J, Pajerowski JD, Spinler KR, Shin JW, TewariM, Rehfeldt F, Speicher DW, Discher DE: Nuclear lamin-A scales with tissue stiffness and enhances matrix-directed differentiation. Science 341: 1240104, 2013
27. Umale S, Deck C, BourdetN,Dhumane P, Soler L, Marescaux J,Willinger R: Experimental mechanical characterization of abdominal organs: Liver, kidney & spleen. J Mech Behav Biomed Mater 17: 22-33, 2013
28. Nicolle S, Vezin P, Palierne JF: A strain-hardening bi-power law for the nonlinearbehaviourofbiological soft tissues.JBiomech43: 927-932, 2010
29. Arndt R, Schmidt S, Loddenkemper C, Grünbaum M, Zidek W, van der Giet M, Westhoff TH: Noninvasive evaluation of renal allograft fibrosis by transient elastography-A pilot study. Transpl Int 23: 871-877, 2010
30. Michels S, Schmidt-Erfurth U: Photodynamic therapy with verteporfin: A new treatment in ophthalmology. Semin Ophthalmol 16: 201-206, 2001
31. Zhao B, Li L, Tumaneng K, Wang CY, Guan KL: A coordinated phosphorylation by Lats and CK1 regulates YAP stability through SCF(beta-TRCP). Genes Dev 24: 72-85, 2010
32. Liu CY, Zha ZY, Zhou X, Zhang H, HuangW, Zhao D, Li T, Chan SW, Lim CJ, Hong W, Zhao S, Xiong Y, Lei QY, Guan KL: The hippo tumor pathway promotes TAZ degradation by phosphorylating a phosphodegron and recruiting the SCFbeta-TrCP E3 ligase. J Biol Chem 285: 37159-37169, 2010
33. Zhang Y, Chang C, Gehling DJ, Hemmati-Brivanlou A, Derynck R: Regulation of Smad degradation and activity by Smurf2, an E3 ubiquitin ligase. Proc Natl Acad Sci U S A 98: 974-979, 2001
34. Gao S, Alarcón C, Sapkota G, Rahman S, Chen PY, Goerner N, Macias MJ, Erdjument-Bromage H, Tempst P, Massagué J: Ubiquitin ligase Nedd4L targets activated Smad2/3 to limit TGF-beta signaling. Mol Cell 36: 457-468, 2009
35. Liu F, Lagares D, Choi KM, Stopfer L, Marinkovic A, Vrbanac V, Probst CK, Hiemer SE, Sisson TH, Horowitz JC, Rosas IO, Fredenburgh LE, Feghali-Bostwick C, Varelas X, Tager AM, Tschumperlin DJ: Mechanosignaling through YAP and TAZ drives fibroblast activation and fibrosis. Am J Physiol Lung Cell Mol Physiol 308: L344-L357, 2015
36. Piersma B, de Rond S,Werker PM, Boo S, Hinz B, van BeugeMM, Bank RA: YAP1 is a driver of myofibroblast differentiation in normal and diseased fibroblasts. Am J Pathol 185: 3326-3337, 2015
37. Mannaerts I, Leite SB, Verhulst S, Claerhout S, Eysackers N, Thoen LF, Hoorens A, Reynaert H, Halder G, van Grunsven LA: The Hippo pathway effector YAP controls mouse hepatic stellate cell activation. J Hepatol 63: 679-688, 2015
38. Zhang H, Ramakrishnan SK, Triner D, Centofanti B,Maitra D, Gyorffy B, Sebolt-Leopold JS, DameMK, Varani J, Brenner DE, Fearon ER,Omary MB, Shah YM: Tumor-selective proteotoxicity of verteporfin inhibits colon cancer progression independently of YAP1. Sci Signal 8: ra98, 2015
39. Donohue E, Balgi AD, Komatsu M, Roberge M: Induction of covalently crosslinked p62 oligomers with reduced binding to polyubiquitinated proteins by the autophagy inhibitor verteporfin. PLoS One 9: e114964, 2014
40. AlarcónC, Zaromytidou AI, Xi Q,Gao S, Yu J, Fujisawa S, Barlas A,Miller AN, Manova-Todorova K, Macias MJ, Sapkota G, Pan D, Massagué J: Nuclear CDKs drive Smad transcriptional activation and turnover in BMP and TGF-beta pathways. Cell 139: 757-769, 2009
41. Aragón E, Goerner N, Zaromytidou AI, Xi Q, Escobedo A, Massagué J, Macias MJ: A Smad action turnover switch operated by WW domain readers of a phosphoserine code. Genes Dev 25: 1275-1288, 2011
42. Luchsinger LL, Patenaude CA, Smith BD, LayneMD: Myocardin-related transcription factor-A complexes activate type I collagen expression in lung fibroblasts. J Biol Chem286: 44116-44125, 2011
43. Sakai N, Chun J, Duffield JS, Wada T, Luster AD, Tager AM: LPA1-induced cytoskeleton reorganization drives fibrosis through CTGFdependent fibroblast proliferation. FASEB J 27: 1830-1846, 2013
44. Rauskolb C, Sun S, Sun G, Pan Y, Irvine KD: Cytoskeletal tension inhibits Hippo signaling through an Ajuba-Warts complex. Cell 158: 143-156, 2014
45. Codelia VA, Sun G, Irvine KD: Regulation of YAP by mechanical strain through Jnk and Hippo signaling. Curr Biol 24: 2012-2017, 2014
46. Fine LG, Norman JT: Chronic hypoxia as a mechanismof progression of chronic kidney diseases: Fromhypothesis to novel therapeutics. Kidney Int 74: 867-872, 2008
47. Tse JR, Engler AJ: Preparation of hydrogel substrates with tunable mechanical properties. Curr Protoc Cell Biol 10: 10.16, 2010
48. Kandow CE, Georges PC, Janmey PA, Beningo KA: Polyacrylamide hydrogels for cell mechanics: Steps toward optimization and alternative uses. Methods Cell Biol 83: 29-46, 2007
49. Godbout C, Follonier Castella L, Smith EA, Talele N, Chow ML, Garonna A, Hinz B: The mechanical environment modulates intracellular calcium oscillation activities of myofibroblasts. PLoS One 8: e64560, 2013
50. Nilsson I, Bahram F, Li X, Gualandi L, Koch S, Jarvius M, Söderberg O, Anisimov A, Kholová I, Pytowski B, BaldwinM, Ylä-Herttuala S, Alitalo K, Kreuger J, Claesson-Welsh L: VEGF receptor 2/-3 heterodimers detected in situ by proximity ligation on angiogenic sprouts. EMBO J 29: 1377-1388, 2010
51. Yuen DA, Connelly KA, Advani A, Liao C, Kuliszewski MA, Trogadis J, Thai K, Advani SL, Zhang Y, Kelly DJ, Leong-Poi H, Keating A,Marsden PA, Stewart DJ, Gilbert RE: Culture-modified bone marrow cells attenuate cardiac and renal injury in a chronic kidney disease rat model via a novel antifibrotic mechanism. PLoS One 5: e9543, 2010
52. Yuen DA, Connelly KA, Zhang Y, Advani SL, Thai K, Kabir G, Kepecs D, Spring C, Smith C, Batruch I, Kosanam H, Advani A, Diamandis E, Marsden PA, Gilbert RE: Early outgrowth cells release soluble endocrine antifibrotic factors that reduce progressive organ fibrosis. Stem Cells 31: 2408-2419, 2013
53. Yuen DA, Kepecs DM, Zhang Y, Advani S, Thai K, Connelly KA, Gilbert RE: Repeated treatment with bone marrow cell secretory products maintains long-term renoprotection in experimental chronic kidney disease: A placebo-controlled trial. Can J Kidney Health Dis 2: 44, 2015
54. Wilkinson DG: RNA detection using non-radioactive in situ hybridization. Curr Opin Biotechnol 6: 20-23, 1995