TAZ activation drives fibroblast spheroid growth, expression of profibrotic paracrine signals, and context-dependent ECM gene expression

American Journal of Physiology - Cell Physiology

Volumn 312, Issue 3, 2017, Pages C277-C285

  Jorgenson, Amy J ^a   Choi, Kyoung Moo ^a   Sicard, Delphine ^a   Smith, Karry M J ^a   Hiemer, Samantha E ^b   Varelas, Xaralabos ^b   Tschumperlin, Daniel J ^a  

^a MAYO GRADUATE SCHOOL   (United States)

^b BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Collagen; Extracellular matrix; Fibrosis; Hippo; Stiffness

Indexed keywords

COL1A1 PROTEIN; COL1A2 PROTEIN; COL3A1 PROTEIN; CONNECTIVE TISSUE GROWTH FACTOR; DOXYCYCLINE; ENDOTHELIN 1; FIBRILLAR COLLAGEN; FIBRONECTIN; FN1 PROTEIN; MYOCARDIN; PLASMINOGEN ACTIVATOR INHIBITOR 1; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR TAZ4SA; TRANSFORMING GROWTH FACTOR BETA1; TUMOR PROTEIN; UNCLASSIFIED DRUG; SCLEROPROTEIN; TAZ PROTEIN, HUMAN;

3T3 CELL LINE; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; EXTRACELLULAR MATRIX; FIBROBLAST; FIBROBLAST CULTURE; GENE EXPRESSION; GENETIC CODE; GENETIC ENHANCEMENT; HUMAN; HUMAN CELL; HYDROGEL; MOLECULAR SIZE; MOLECULAR STABILITY; PARACRINE SIGNALING; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RIGIDITY; TUMOR GROWTH; TUMOR MICROENVIRONMENT; TUMOR SPHEROID; ANIMAL; CELL CULTURE; FIBROSIS; METABOLISM; MOUSE; MULTICELLULAR SPHEROID; NIH 3T3 CELL LINE; PATHOLOGY; TRANSCRIPTION INITIATION;

ANIMALS; CELL PROLIFERATION; CELLS, CULTURED; EXTRACELLULAR MATRIX; EXTRACELLULAR MATRIX PROTEINS; FIBROBLASTS; FIBROSIS; MICE; NIH 3T3 CELLS; PARACRINE COMMUNICATION; SPHEROIDS, CELLULAR; TRANSCRIPTION FACTORS; TRANSCRIPTIONAL ACTIVATION;

EID: 85014589873     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00205.2016     Document Type: Article

References (36)

1. Bertero T, Cottrill KA, Annis S, Bhat B, Gochuico BR, Osorio JC, Rosas I, Haley KJ, Corey KE, Chung RT, Nelson Chau B, Chan SYA. A YAP/TAZ-miR-130/301 molecular circuit exerts systems-level control of fibrosis in a network of human diseases and physiologic conditions. Sci Rep 5: 18277, 2015. doi:10.1038/srep18277.
2. Caliari SR, Perepelyuk M, Cosgrove BD, Tsai SJ, Lee GY, Mauck RL, Wells RG, Burdick JA. Stiffening hydrogels for investigating the dynamics of hepatic stellate cell mechanotransduction during myofibroblast activation. Sci Rep 6: 21387, 2016. doi:10.1038/srep21387.
3. Gumbiner BM, Kim NG. The Hippo-YAP signaling pathway and contact inhibition of growth. J Cell Sci 127: 709–717, 2014. doi:10.1242/jcs. 140103.
4. Jansen KA, Bacabac RG, Piechocka IK, Koenderink GH. Cells actively stiffen fibrin networks by generating contractile stress. Biophys J 105: 2240–2251, 2013. doi:10.1016/j.bpj.2013.10.008.
5. Kopanska KS, Bussonnier M, Geraldo S, Simon A, Vignjevic D, Betz T. Quantification of collagen contraction in three-dimensional cell culture. Methods Cell Biol 125: 353–372, 2015. doi:10.1016/bs.mcb.2014.10.017.
6. Lee WJ, Choi IK, Lee JH, Kim YO, Yun CO. A novel three-dimensional model system for keloid study: organotypic multicellular scar model. Wound Repair Regen 21: 155–165, 2013. doi:10.1111/j.1524-475X.2012.00869.x.
7. 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. doi:10.1128/MCB.01874-07.
8. Leung LY, Tian D, Brangwynne CP, Weitz DA, Tschumperlin DJ. A new microrheometric approach reveals individual and cooperative roles for TGF-α1 and IL-1α in fibroblast-mediated stiffening of collagen gels. FASEB J 21: 2064–2073, 2007. doi:10.1096/fj.06-7510com.
9. Liu CY, Chan SW, Guo F, Toloczko A, Cui L, Hong W. MRTF/SRF dependent transcriptional regulation of TAZ in breast cancer cells. Onco-target 7: 13706–13716, 2016. doi:10.18632/oncotarget.7333.
10. Liu F, Lagares D, Choi KM, Stopfer L, Marinković A, Vrbanac V, Probst CK, Hiemer SE, Sisson TH, Horowitz JC, Rosas IO, Freden-burgh 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. doi:10.1152/ajplung.00300.2014.
11. 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. doi:10.1083/jcb. 201004082.
12. Liu F, Tschumperlin DJ. Micro-mechanical characterization of lung tissue using atomic force microscopy. J Vis Exp 54: e2911, 2011. doi:10. 3791/2911.
13. 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. doi:10.1016/j.jhep.2015.04.011.
14. Marinković 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. doi:10.1165/rcmb.2012-0335OC.
15. Marinković A, Mih JD, Park JA, Liu F, Tschumperlin DJ. Improved throughput traction microscopy reveals pivotal role for matrix stiffness in fibroblast contractility and TGF-α responsiveness. Am J Physiol Lung Cell Mol Physiol 303: L169–L180, 2012. doi:10.1152/ajplung.00108.2012.
16. Mehta G, Hsiao AY, Ingram M, Luker GD, Takayama S. Opportunities and challenges for use of tumor spheroids as models to test drug delivery and efficacy. J Control Release 164: 192–204, 2012. doi:10.1016/j.jconrel.2012.04.045.
17. Meng Z, Moroishi T, Guan KL. Mechanisms of Hippo pathway regulation. Genes Dev 30: 1–17, 2016. doi:10.1101/gad.274027.115.
18. 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. doi:10.1371/journal.pone.0019929.
19. Piccolo S, Dupont S, Cordenonsi M. The biology of YAP/TAZ: hippo signaling and beyond. Physiol Rev 94: 1287–1312, 2014. doi:10.1152/physrev.00005.2014.
20. 19a.Piersma B, Bank RA. Keeping fibroblasts in suspense: TAZ-mediated signaling activates a context-dependent profibrotic phenotype. Focus on “TAZ activation drives fibroblast spheroid growth, expression of profibrotic paracrine signals, and context-dependent ECM gene expression.” Am J Physiol Cell Physiol, 2017. doi:10.1152/ajpcell.00362.2016.
21. Piersma B, Bank RA, Boersema M. Signaling in fibrosis: TGF-α, WNT, and YAP/TAZ converge. Front Med (Lausanne) 2: 59, 2015.
22. Piersma B, de Rond S, Werker PM, Boo S, Hinz B, van Beuge MM, Bank RA. YAP1 is a driver of myofibroblast differentiation in normal and diseased fibroblasts. Am J Pathol 185: 3326–3337, 2015. doi:10.1016/j. ajpath.2015.08.011.
23. Rockey DC, Bell PD, Hill JA. Fibrosis–a common pathway to organ injury and failure. N Engl J Med 372: 1138–1149, 2015. doi:10.1056/NEJMra1300575.
24. Saito A, Nagase T. Hippo and TGF-α interplay in the lung field. Am J Physiol Lung Cell Mol Physiol 309: L756–L767, 2015. doi:10.1152/ajplung.00238.2015.
25. Salmenperä P, Kankuri E, Bizik J, Sirén V, Virtanen I, Takahashi S, Leiss M, Fässler R, Vaheri A. Formation and activation of fibroblast spheroids depend on fibronectin-integrin interaction. Exp Cell Res 314: 3444–3452, 2008. doi:10.1016/j.yexcr.2008.09.004.
26. Salmenperä P, Karhemo PR, Räsänen K, Laakkonen P, Vaheri A. Fibroblast spheroids as a model to study sustained fibroblast quiescence and their crosstalk with tumor cells. Exp Cell Res 345: 17–24, 2016. doi:10.1016/j.yexcr.2016.05.005.
27. Sirén V, Salmenperä P, Kankuri E, Bizik J, Sorsa T, Tervahartiala T, Vaheri A. Cell-cell contact activation of fibroblasts increases the expression of matrix metalloproteinases. Ann Med 38: 212–220, 2006. doi:10. 1080/07853890500494999.
28. Speight P, Kofler M, Szászi K, Kapus A. Context-dependent switch in chemo/mechanotransduction via multilevel crosstalk among cytoskeleton-regulated MRTF and TAZ and TGFα-regulated Smad3. Nat Commun 7: 11642, 2016. doi:10.1038/ncomms11642.
29. Szeto SG, Narimatsu M, Lu M, He X, Sidiqi AM, Tolosa MF, Chan L, De Freitas K, Bialik JF, Majumder S, Boo S, Hinz B, Dan Q, Advani A, John R, Wrana JL, Kapus A, Yuen DA. YAP/TAZ are mechanoregulators of TGF-α-Smad signaling and renal fibrogenesis. J Am Soc Nephrol. 2016. doi:10.1681/ASN.2015050499.
30. Torry DJ, Richards CD, Podor TJ, Gauldie J. Anchorage-independent colony growth of pulmonary fibroblasts derived from fibrotic human lung tissue. J Clin Invest 93: 1525–1532, 1994. doi:10.1172/JCI117131.
31. Tschumperlin DJ. Matrix, mesenchyme, and mechanotransduction. Ann Am Thorac Soc 12, Suppl 1: S24–S29, 2015. doi:10.1513/AnnalsATS. 201407-320MG.
32. Tschumperlin DJ, Liu F, Tager AM. Biomechanical regulation of mesenchymal cell function. Curr Opin Rheumatol 25: 92–100, 2013. doi:10.1097/BOR.0b013e32835b13cd.
33. Velasquez LS, Sutherland LB, Liu Z, Grinnell F, Kamm KE, Schneider JW, Olson EN, Small EM. Activation of MRTF-A-dependent gene expression with a small molecule promotes myofibroblast differentiation and wound healing. Proc Natl Acad Sci USA 110: 16850–16855, 2013. doi:10.1073/pnas.1316764110.
34. Wells RG. The role of matrix stiffness in regulating cell behavior. Hepatology 47: 1394–1400, 2008. doi:10.1002/hep.22193.
35. Wen Q, Janmey PA. Effects of non-linearity on cell-ECM interactions. Exp Cell Res 319: 2481–2489, 2013. doi:10.1016/j.yexcr.2013.05.017.
36. Yu OM, Miyamoto S, Brown JH. Myocardin-related transcription Factor A and yes-associated protein exert dual control in G protein-coupled receptor- and RhoA-mediated transcriptional regulation and cell proliferation. Mol Cell Biol 36: 39–49, 2015. doi:10.1128/MCB.00772-15.