Framework to function: Mechanosensitive regulators of gene transcription

Cellular and Molecular Biology Letters

Volumn 21, Issue 1, 2016, Pages

  Finch Edmondson, Megan ^a,b   Sudol, Marius ^a,b  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

Actin; Epithelial mesenchymal transition; Mechanotransduction; MRTF; Myocardin; TAZ; YAP; catenin

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; CYTOSKELETON PROTEIN; MYOCARDIN RELATED TRANSCRIPTION FACTOR; MYOCARDIN RELATED TRANSCRIPTION FACTOR A; MYOCARDIN RELATED TRANSCRIPTION FACTOR B; PROTEIN; SERUM RESPONSE FACTOR; TAZ PROTEIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; YES ASSOCIATED PROTEIN; ACTIN; MYOCARDIN; NUCLEAR PROTEIN; TRANSACTIVATOR PROTEIN;

ALPHA SMA GENE; BIOPHYSICS; CELL DIFFERENTIATION; CELL INTERACTION; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; CYTOPLASM; EPITHELIAL MESENCHYMAL TRANSITION; FIBROSIS; GENE ACTIVATION; GENE EXPRESSION; GENE TARGETING; GENETIC TRANSCRIPTION; HUMAN; MALIGNANT NEOPLASM; MOLECULAR DYNAMICS; MRTF GENE; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; PROTEIN STRUCTURE; REGULATOR GENE; REVIEW; SRF GENE; TAZ GENE; YAP GENE; ANIMAL; MECHANOTRANSDUCTION;

ACTINS; ANIMALS; EPITHELIAL-MESENCHYMAL TRANSITION; HUMANS; MECHANOTRANSDUCTION, CELLULAR; NUCLEAR PROTEINS; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 85009259856     PISSN: 14258153     EISSN: 16891392     Source Type: Journal    
DOI: 10.1186/s11658-016-0028-7     Document Type: Review

References (150)

1. Bustelo XR, Sauzeau V, Berenjeno IM. GTP-binding proteins of the Rho/Rac family: regulation, effectors and functions in vivo. Bioessays. 2007;29:356-70.
2. Olson EN, Nordheim A. Linking actin dynamics and gene transcription to drive cellular motile functions. Nat Rev Mol Cell Biol. 2010;11:353-65.
3. Miralles F, Posern G, Zaromytidou AI, Treisman R. Actin Dynamics Control SRF Activity by Regulation of Its Coactivator MAL. Cell. 2003;113:329-42.
4. Xu YZ, Kanagaratham C, Radzioch D. Exploring Secrets of Nuclear Actin Involvement in the Regulation of Gene Transcription and Genome Organization. In: Najman S, editor. Current Frontiers and Perspectives in Cell Biology. Rijeka: InTech; 2012. p. 181-210.
5. Treisman R. Identification of a Protein-Binding Site That Mediates Transcriptional Response of the c-fos Gene to Serum Factors. Cell. 1986;46:567-74.
6. Cen B, Selvaraj A, Burgess RC, Hitzler JK, Ma Z, Morris SW, Prywes R. Megakaryoblastic Leukemia 1, a Potent Transcriptional Coactivator for Serum Response Factor (SRF), Is Required for Serum Induction of SRF Target Genes. Mol Cell Biol. 2003;23:6597-608.
7. Wang DZ, Chang PS, Wang Z, Sutherland L, Richardson JA, Small E, Krieg PA, Olson EN. Activation of Cardiac Gene Expression by Myocardin, a Transcriptional Cofactor for Serum Response Factor. Cell. 2001;105:851-62.
8. Wang DZ, Li S, Hockemeyer D, Sutherland L, Wang Z, Schratt G, Richardson JA, Nordheim A, Olson EN. Potentiation of serum response factor activity by a family of myocardin-related transcription factors. Proc Natl Acad Sci U S A. 2002;99:14855-60.
9. Li S, Wang DZ, Wang Z, Richardson JA, Olson EN. The serum response factor coactivator myocardin is required for vascular smooth muscle development. Proc Natl Acad Sci U S A. 2003;100:9366-70.
10. Li S, Chang S, Qi X, Richardson JA, Olson EN. Requirement of a myocardin-related transcription factor for development of mammary myoepithelial cells. Mol Cell Biol. 2006;26:5797-808.
11. Sun Y, Boyd K, Xu W, Ma J, Jackson CW, Fu A, Shillingford JM, Robinson GW, Hennighausen L, Hitzler JK, Ma Z, Morris SW. Acute Myeloid Leukemia-Associated Mkl1 (Mrtf-a) Is a Key Regulator of Mammary Gland Function. Mol Cell Biol. 2006;26:5809-26.
12. Li J, Zhu X, Chen M, Cheng L, Zhou D, Lu MM, Du K, Epstein JA, Parmacek MS. Myocardin-related transcription factor B is required in cardiac neural crest for smooth muscle differentiation and cardiovascular development. Proc Natl Acad Sci U S A. 2005;102:8916-21.
13. Oh J, Richardson JA, Olson EN. Requirement of myocardin-related transcription factor-B for remodeling of branchial arch arteries and smooth muscle differentiation. Proc Natl Acad Sci U S A. 2005;102:15122-7.
14. Parmacek MS. Myocardin-Related Transcription Factors: Critical Coactivators Regulating Cardiovascular Development and Adaptation. Circ Res. 2007;100:633-44.
15. Posern G, Sotiropoulos A, Treisman R. Mutant Actins Demonstrate a Role for Unpolymerized Actin in Control of Transcription by Serum Response Factor. Mol Biol Cell. 2002;13:4167-78.
16. Kuwahara K, Barrientos T, Pipes GCT, Li S, Olson EN. Muscle-Specific Signaling Mechanism That Links Actin Dynamics to Serum Response Factor. Mol Cell Biol. 2005;25:3173-81.
17. Guettler S, Vartianinen MK, Miralles F, Larijani B, Treisman R. RPEL Motifs Link the Serum Response Factor Cofactor MAL but Not Myocardin to Rho Signaling via Actin Binding. Mol Cell Biol. 2008;28:732-42.
18. Nakamura S, Hayashi K, Iwasaki K, Fujioka T, Equsa H, Yatani H, Sobue K. Nuclear Import Mechanism for Myocardin Family Members and Their Correlation with Vascular Smooth Muscle Cell Phenotype. J Biol Chem. 2010;285:37314-23.
19. Hayashi K, Morita T. Differences in the Nuclear Export Mechanism between Myocardin and Myocardin-related Transcription Factor A. J Biol Chem. 2013;288:5743-55.
20. Sotiropoulos A, Gineitis D, Copeland J, Treisman R. Signal-Regulated Activation of Serum Response Factor Is Mediated by Changes in Actin Dynamics. Cell. 1999;98:159-69.
21. Schratt G, Philippar U, Berger J, Schwarz H, Heindenreich O, Nordheim A. Serum response factor is crucial for actin cytoskeletal organization and focal adhesion assembly in embryonic stem cells. J Cell Biol. 2002;156:737-50.
22. Somogyi K, Rørth P. Evidence for Tension-Based Regulation of Drosophila MAL and SRF during Invasive Cell Migration. Dev Cell. 2004;7:85-93.
23. Zhao XH, Laschinger C, Arora P, Szászi K, Kapus A, McCulloch CA. Force activates smooth muscle α-actin promoter activity through the Rho signaling pathway. J Cell Sci. 2007;120:1801-9.
24. McGee KM, Vartiainen MK, Khaw PT, Treisman R, Bailly M. Nuclear transport of the serum response factor coactivator MRTF-A is downregulated at tensional homeostasis. EMBO Rep. 2011;12:963-70.
25. Thiery JP, Acloque H, Huang RYJ, Nieto MA. Epithelial-Mesenchymal Transitions in Development and Disease. Cell. 2009;139:871-90.
26. Lamouille S, Xu J, Derynck R. Molecular mechanisms of epithelial-mesenchymal transition. Nat Rev Mol Cell Biol. 2014;15:178-96.
27. Morita T, Mayanagi T, Sobue K. Dual roles of myocardin-related transcription factors in epithelial-mesenchymal transition via slug induction and actin remodeling. J Cell Biol. 2007;179:1027-42.
28. Fan L, Sebe A, Péterfi Z, Masszi A, Thirone ACP, Rotstein OD, Nakano H, McCulloch CA, Szászi K, Mucsi I, Kapus A. Cell Contact-dependent Regulation of Epithelial-Myofibroblast Transition via the Rho-Rho Kinase-Phospho-Myosin Pathway. Mol Biol Cell. 2007;18:1083-97.
29. Gomez EW, Chen QK, Gjorevski N, Nelson CM. Tissue Geometry Patterns Epithelial-Mesenchymal Transition Via Intercellular Mechanotransduction. J Cell Biochem. 2010;110:44-51.
30. O'Connor JW, Gomez EW. Cell Adhesion and Shape Regulate TGF-Beta1-Induced Epithelial-Myofibroblast Transition via MRTF-A Signaling. PLoS One. 2013;8:e83188.
31. O'Connor JW, Riley PN, Nalluri SM, Ashar PK, Gomez EW. Matrix Rigidity Mediates TGFβ1- Induced Epithelial-Myofibroblast Transition by Controlling Cytoskeletal Organization and MRTF-A Localization. J Cell Physiol. 2015;230:1829-39.
32. 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. 2013;123:1096-108.
33. Tian W, Hao C, Fan Z, Weng X, Qin H, Wu X, Fang M, Chen Q, Shen A, Xu Y. Myocardin related transcription factor A programs epigenetic activation of hepatic stellate cells. J Hepatol. 2015;62:165-74.
34. Liao XH, Wang N, Liu LY, Zheng L, Xing WJ, Zhao DW, Sun XG, Hu P, Dong J, Zhang TC. MRTF-A and STAT3 synergistically promote breast cancer cell migration. Cell Signal. 2014;26:2370-80.
35. Medjkane S, Perez-Sanchez C, Gaggioli C, Sahai E, Treisman R. Myocardin-related transcription factors and SRF are required for cytoskeletal dynamics and experimental metastasis. Nat Cell Biol. 2009;11:257-68.
36. Sampath D, Winneker RC, Zhang Z. Cyr61, a Member of the CCN Family, Is Required for MCF-7 Cell Proliferation: Regulation by 17β-Estradiol and Overexpression in Human Breast Cancer. Endocrinology. 2001;142:2540-8.
37. Cheng X, Yang Y, Fan Z, Yu L, Bai H, Zhou B, Wu X, Xu H, Fang M, Shen A, Chen Q, Xu Y. MKL1 potentiates lung cancer cell migration and invasion by epigenetically activating MMP9 transcription. Oncogene. 2015;34:5570-81.
38. Sienel W, Hellers J, Morresi-Hauf A, Lichtinghagen R, Mutschler W, Jochum M, Klein C, Passlick B, Pantel K. Prognostic impact of matrix metalloproteinase-9 in operable non-small cell lung cancer. Int J Cancer. 2002;103:647-51.
39. Song Z, Liu Z, Sun J, Li CZ, Sun JZ, Xu LY. The MRTF-A/B function as oncogenes in pancreatic cancer. Oncol Rep. 2016;35:127-38.
40. Nakazuru S, Yoshio T, Suemura S, Itoh M, Araki M, Yoshioka C, Ohta M, Sueyoshi Y, Ohta T, Hasegawa H, Morita K, Toyama T, Kuzushita N, Kodama Y, Mano M, Mita E. Poorly differentiated endocrine carcinoma of the pancreas responded to gemcitabine: Case report. World J Gastroenterol. 2010;16:3835-56.
41. Evelyn CR, Wade SM, Wang Q, Wu M, Iñiguez-Lluhí JA, Merajver SD, Neubig RR. CCG-1423: a small-molecule inhibitor of RhoA transcriptional signaling. Mol Cancer Ther. 2007;6:2249-60.
42. Hayashi K, Watanabe B, Nakagawa Y, Minami S, Morita T. RPEL Proteins Are the Molecular Targets for CCG-1423, an Inhibitor of Rho Signaling. PLoS One. 2014;9:e89016.
43. Johnson LA, Rodansky ES, Haak AJ, Larsen SD, Neubig RR, Higgins PDR. Novel Rho/MRTF/SRF Inhibitors Block Matrix-stiffness and TGF-β-Induced Fibrogenesis in Human Colonic Myofibroblasts. Inflamm Bowel Dis. 2014;20:154-65.
44. Yan C, Grimm WA, Garner WL, Qin L, Travis T, Tan N, Han YP. Epithelial to Mesenchymal Transition in Human Skin Wound Healing Is Induced by Tumor Necrosis Factor-α through Bone Morphogenic Protein-2. Am J Pathol. 2010;176:2247-58.
45. 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. 2010;107:294-304.
46. Russell JL, Goetsch SC, Aguilar H, Frantz DE, Schneider JW. Targeting native adult heart progenitors with cardiogenic small-molecules. ACS Chem Biol. 2012;7:1067-76.
47. 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 U S A. 2013;110:16850-5.
48. Chiquet-Ehrismann R, Chiquet M. Tenascins: regulation and putative functions during pathological stress. J Pathol. 2003;200:488-99.
49. Asparuhova MB, Ferralli J, Chiquet M, Chiquet-Ehrismann R. The transcriptional regulator megakaryoblastic leukemia-1 mediates serum response factor-independent activation of tenascin-C transcription by mechanical stress. FASEB J. 2011;25:3477-88.
50. Gurbuz I, Ferralli J, Roloff T, Chiquet-Ehrismann R, Asparuhova MB. SAP domain-dependent Mkl1 signaling stimulates proliferation and cell migration by induction of a distinct gene set indicative of poor prognosis in breast cancer patients. Mol Cancer. 2014;13:1-16.
51. Sudol M. Yes-associated protein (YAP65) is a proline-rich phosphoprotein that binds to the SH3 domain of the Yes proto-oncogene product. Oncogene. 1994;9:2145-52.
52. Kanai F, Marignani PA, Sarassova 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. 2000;19:6778-91.
53. Pan D. The Hippo Signaling Pathway in Development and Cancer. Dev Cell. 2010;19:491-505.
54. Yu FX, Zhao B, Guan KL. Hippo Pathway in Organ Size Control, Tissue Homeostasis, and Cancer. Cell. 2015;163:811-28.
55. Zhao B, Wei X, Li W, Udan RS, Yang Q, Kim J, Xie J, Ikemoue 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. 2007;21:2747-61.
56. Chan EH, Nousianien M, Chalamalasetty RB, Schafer A, Nigg EA, Sillje HHW. The Ste20-like kinase Mst2 activates the human large tumor suppressor kinase Lats1. Oncogene. 2005;24:2076-86.
57. Wu S, Huang JB, Dong JX, Pan DJ. hippo Encodes a Ste-20 Family Protein Kinase that Restricts Cell Proliferation and Promotes Apoptosis in Conjunction with salvador and warts. Cell. 2003;114:445-56.
58. Lei QY, Zhang HB, 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. 2008;28:2426-36.
59. Oka T, Mazack V, Sudol M. Mst2 and Lats Kinases Regulate Apoptotic Function of Yes Kinase-associated Protein (YAP). J Biol Chem. 2008;283:27534-46.
60. Zhang J, Smolen GA, Haber DA. Negative Regulation of YAP by LATS1 Underscores Evolutionary Conservation of the Drosophila Hippo Pathway. Cancer Res. 2008;68:2789-94.
61. Dong J, Feldmann G, Huang J, Wu S, Zhang N, Comerford SA, Gayyed MF, Anders RA, Maitra A, Pan D. Elucidation of a Universal Size-Control Mechanism in Drosophila and Mammals. Cell. 2007;130:1120-33.
62. Liu CY, Zha ZY, Zhou X, Zhang H, Huang W, 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 SCF-βTrCP E3 Ligase. J Biol Chem. 2010;285:37159-69.
63. 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. 2010;24:72-85.
64. Gaspar P, Tapon N. Sensing the local environment: actin architecture and Hippo signalling. Curr Opin Cell Biol. 2014;31:74-83.
65. Low BC, Pan CQ, Shivashankar GV, Bershadsky A, Sudol M, Sheetz M. YAP/TAZ as mechanosensors and mechanotransducers in regulating organ size and tumor growth. FEBS Lett. 2014;588:2663-70.
66. Wada KI, Itoga K, Okano T, Yonemura S, Sasaki H. Hippo pathway regulation by cell morphology and stress fibers. Development. 2011;138:3907-14.
67. 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. 2011;474:179-83.
68. 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. 2013;154:1047-59.
69. 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. 2012;150:780-91.
70. Miller E, Yang J, DeRan M, Wu C, Su AI, Bonamy GMC, Liu J, Peters EC, Wu X. Identification of Serum-Derived Sphingosine-1-Phosphate as a Small Molecule Regulator of YAP. Chem Biol. 2012;19:955-62.
71. Zhao B, Li L, Wang L, Wang CY, Yu J, Guan KL. Cell detachment activates the Hippo pathway via cytoskeleton reorganization to induce anoikis. Genes Dev. 2012;26:54-68.
72. Sansores-Garcia L, Bossuyt W, Wada K, Yonemura S, Tao C, Sasaki H, Halder G. Modulating F-actin organization induces organ growth by affecting the Hippo pathway. EMBO J. 2011;30:2325-35.
73. Fernández BG, Gaspar P, Brás-Pereira C, Jezowska B, Rebelo SR, Janody F. Actin-Capping Protein and the Hippo pathway regulate Factin and tissue growth in Drosophila. Development. 2011;138:2337-46.
74. Zheng Y, Wang W, Liu B, Deng H, Uster E, Pan D. Identification of Happyhour/MAP4K as Alternative Hpo/Mst-like Kinases in the Hippo Kinase Cascade. Dev Cell. 2015;34:642-55.
75. Rauskolb C, Sun S, Sun G, Pan Y, Irvine KD. Cytoskeletal Tension inhibits Hippo signaling through an Ajuba-Warts complex. Cell. 2014;158:143-56.
76. Codelia VA, Sun G, Irvine KD. Regulation of YAP by Mechanical Strain through Jnk and Hippo Signaling. Curr Biol. 2014;24:2012-7.
77. Kaunas R, Usami S, Chien S. Regulation of stretch-induced JNK activation by stress fiber orientation. Cell Signal. 2006;18:1924-31.
78. Hirata H, Tatsumi H, Sokabe M. Mechanical forces facilitate actin polymerization at focal adhesions in a zyxin-dependent manner. J Cell Sci. 2008;121:2795-804.
79. Rauskolb C, Pan G, Reddy BVVG, Oh H, Irvine KD. Zyxin Links Fat Signaling to the Hippo Pathway. PLoS Biol. 2011;9:e1000624.
80. Hirota T, Morisaki T, Nishiyama Y, Marumoto T, Tada K, Hara T, Masuko N, Inagaki M, Hatakeyama K, Saya H. Zyxin, a Regulator of Actin Filament Assembly, Targets the Mitotic Apparatus by Interacting with h-warts/LATS1 Tumor Suppressor. J Cell Biol. 2000;149:1073-86.
81. Gaspar P, Holder MV, Aerne BL, Janody F, Tapon N. Zyxin Antagonizes the FERM Protein Expanded to Couple F-Actin and Yorkie-Dependent Organ Growth. Curr Biol. 2015;25:679-89.
82. Visser-Grieve S, Zhou Z, She YM, Huang H, Cyr TD, Xu T, Yang X. LATS1 tumor suppressor is a novel actin-binding protein and negative regulator of actin polymerization. Cell Res. 2011;21:1513-6.
83. Das A, Fischer RS, Pan D, Waterman CM. YAP nuclear localization in the absence of cell-cell contact is mediated by a filamentous actin-dependent, myosin II- and phospho-YAP independent pathway during ECM mechanosensing. J Biol Chem. 2016;291:6096-110.
84. Adler JJ, Johnson DE, Heller BL, Bringman LR, Ranahan WP, Conwell MD, Sun Y, Hudmon A, Wells CD. Serum deprivation inhibits the transcriptional co-activator YAP and cell growth via phosphorylation of the 130-kDa isoform of Angiomotin by the LATS1/2 protein kinases. Proc Natl Acad Sci U S A. 2013;110:17368-73.
85. Chan SW, Lim CJ, Chong YF, Pobbati AV, Huang C, Hong W. Hippo Pathway-independent Restriction of TAZ and YAP by Angiomotin. J Biol Chem. 2011;286:7018-26.
86. Mana-Capelli S, Paramasivan M, Dutta S, McCollum D. Angiomotins link F-actin architecture to Hippo pathway signaling. Mol Biol Cell. 2014;25:1676-85.
87. Dai X, She P, Chi F, Feng Y, Liu H, Jin D, Zhao Y, Guo X, Jiang D, Guan KL, Zhong TP, Zhao B. Phosphorylation of angiomotin by Lats1/2 kinases inhibits F-actin binding, cell migration, and angiogenesis. J Biol Chem. 2013;288:34041-51.
88. Bennett V, Baines AJ. Spectrin and Ankyrin-Based Pathways: Metazoan Inventions for Integrating Cells Into Tissues. Physiol Rev. 2001;81:1353-92.
89. Deng H, Wang W, Yu J, Zheng Y, Qing Y, Pan D. Spectrin regulates Hippo signaling by modulating cortical actomyosin activity. Elife. 2015;4:e06567.
90. Fletcher GC, Elbediwy A, Khanal I, Ribeiro PS, Tapon N, Thompson BJ. The Spectrin cytoskeleton regulates the Hippo signalling pathway. EMBO J. 2015;34:940-54.
91. Wong KKL, Li W, An Y, Duan Y, Li Z, Kang Y, Yan Y. β-Spectrin Regulates the Hippo Signaling Pathway and Modulates the Basal Actin Network. J Biol Chem. 2015;290:6397-407.
92. Sun M, Spill F, Zaman MH. A Computational Model of YAP/TAZ Mechanosensing. Biophys J. 2016;110:2540-50.
93. Cui Y, Hameed FM, Yang B, Lee K, Pan CQ, Park S, Sheetz M. Cyclic stretching of soft substrates induces spreading and growth. Nat Commun. 2015;6:6333.
94. Nishioka N, Inoue K, Adachi K, Kiyonari H, Ota M, Ralston A, Yabuta N, Hirahara S, Stephenson RO, Ogonuki N, Makita R, Kurihara H, Morin-Kensicki EM, Nojima H, Rossant J, Nakao K, Niwa H, Sasaki H. The Hippo signaling pathway components Lats and Yap pattern Tead4 activity to distinguish mouse trophectoderm from inner cell mass. Dev Cell. 2009;16:398-410.
95. Stephenson RO, Rossant J, Tam PP. Intercellular interactions, position, and polarity in establishing blastocyst cell lineages and embryonic axes. Cold Spring Harb Perspect Biol. 2012;4:a008235.
96. Kono K, Tamashiro DAA, Alarcon VB. Inhibition of RHO-ROCK signaling enhances ICM and suppresses TE characteristics through activation of Hippo signaling in the mouse blastocyst. Dev Biol. 2014;394:142-55.
97. Porazinski S, Wang H, Asaoka Y, Behrndt M, Miyamoto T, Morita H, Hata S, Sasaki T. YAP is essential for tissue tension to ensure vertebrate 3D body shape. Nature. 2015;521:217-21.
98. Thompson DW. On Growth and Form. United Kingdom: Cambridge University Press; 1917.
99. Musah S, Wrighton PJ, Zaltsman Y, Zhong X, Zorn S, Parlato MB, Hsiao C, Palecek SP, Chang Q, Murphy WL, Kiessling LL. Substratum-induced differentiation of human pluripotent stem cells reveals the coactivator YAP is a potent regulator of neuronal specification. Proc Natl Acad Sci U S A. 2014;111:13805-910.
100. Sun Y, Yong KMA, Villa-Diaz LG, Zhang X, Chen W, Philson R, Weng S, Xu H, Krebsback PH, Fu J. Hippo/YAP-mediated rigidity-dependent motor neuron differentiation of human pluripotent stem cells. Nat Mater. 2014;13:599-604.
101. 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. 2008;10:837-48.
102. Engler AJ, Sen S, Sweeney HL, Discher DE. Matrix Elasticity Directs Stem Cell Lineage Specification. Cell. 2006;126:677-89.
103. Chen Z, Luo Q, Lin C, Song G. Simulated microgravity inhibits osteogenic differentiation of mesenchymal stem cells through down regulating the transcriptional co-activator TAZ. Biochem Biophys Res Commun. 2015;468:21-6.
104. Liu F, Lagares D, Choi KM, Stopfer L, Marinković 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. 2015;308:L344-57.
105. 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. 2015;63:679-88.
106. Xing F, Saidou J, Watabe K. Cancer associated fibroblasts (CAFs) in tumor microenvironment. Front Biosci. 2010;15:166-79.
107. Calvo F, Ege N, Grande-Garcia A, Hooper S, Jenkins RP, Chaudhry SI, Harrington K, Williamson P, Moeendarbary E, Charras G, Sahai E. Mechano-transduction and YAP-dependent matrix remodelling is required for the generation and maintenance of cancer associated fibroblasts. Nat Cell Biol. 2013;15:637-46.
108. Acerbi I, Cassereau L, Dean I, Shi Q, Au A, Park C, Chen YY, Liphardt J, Hwang ES, Weaver VM. Human Breast Cancer Invasion and Aggression Correlates with ECM Stiffening and Immune Cell Infiltration. Integr Biol (Camb). 2015;7:1120-34.
109. Lai D, Ho KC, Hao Y, Yang X. Taxol Resistance in Breast Cancer Cells Is Mediated by the Hippo Pathway Component TAZ and Its Downstream Transcriptional Targets Cyr61 and CTGF. Cancer Res. 2011;71:2728-38.
110. Cordenonsi M, Zanconato F, Azzolin L, Forcato M, Rosato A, Frasson C, Inui M, Montagner M, Parenti AR, Poletti A, Daidone MG, Dupont S, Basso G, Bicciato S, Piccolo S. The Hippo Transducer TAZ Confers Cancer Stem Cell-Related Traits on Breast Cancer Cells. Cell. 2011;147:759-72.
111. Bartucci M, Dattilo R, Moriconi C, Pagliuca A, Mottolese M, Federici G, Di Benedetto A, Todaro M, Stassi G, Sperati F, Amabile MI, Pilozzi E, Patrizii M, Biffoni M, Maugeri-Saccà M, Piccolo S, De Maria R. TAZ is required for metastatic activity and chemoresistance of breast cancer stem cells. Oncogene. 2015;34:681-90.
112. Lee KW, Lee SS, Kim SB, Sohn BH, Lee HS, Jang HJ, Park YY, Kopetz S, Kim SS, Oh SC, Lee JS. Significant Association of Oncogene YAP1 with Poor Prognosis and Cetuximab Resistance in Colorectal Cancer Patients. Clin Cancer Res. 2015;21:357-64.
113. Kim MH, Kim J, Hong H, Lee SH, Lee JK, Jung E, Kim J. Actin remodeling confers BRAF inhibitor resistance to melanoma cells through YAP/TAZ activation. EMBO J. 2016;35:462-78.
114. Niessen CM, Leckband D, Yap AS. Tissue organization by cadherin adhesion molecules: dynamic molecular and cellular mechanisms of morphogenetic regulation. Physiol Rev. 2011;91:691-731.
115. Samuel MS, Lopez JI, McGhee EJ, Croft DR, Strachan D, Timpson P, Munro J, Schröder E, Zhou J, Brunton VG, Barker N, Clevers H, Sansom OJ, Anderson KI, Weaver VM, Olson MF. Actomyosin-mediated cellular tension drives increased tissue stiffness and β-catenin activation to induce interfollicular epidermal hyperplasia and tumor growth. Cancer Cell. 2011;19:776-91.
116. Kumar A, Lnu S, Malya R, Barron D, Moore J, Corry DB, Boriek AM. Mechanical stretch activates nuclear factor-kappaB, activator protein-1, and mitogen-activated protein kinases in lung parenchyma: implications in asthma. FASEB J. 2003;17:1800-11.
117. Sooranna SR, Lee Y, Kim LU, Mohan AR, Bennett PR, Johnson MR. Mechanical stretch activates type 2 cyclooxygenase via activator protein-1 transcription factor in human myometrial cells. Mol Hum Reprod. 2004;10:109-13.
118. Hsieh CY, Hsiao HY, Wu WY, Liu CA, Tsai YC, Chao YJ, Wang DL, Hsieh HJ. Regulation of shear-induced nuclear translocation of the Nrf2 transcription factor in endothelial cells. J Biomed Sci. 2009;16:12.
119. Warboys CM, Amini N, de Luca A, Evans PC. The role of blood flow in determining the sites of atherosclerotic plaques. F1000 Med Rep. 2011;3:5.
120. Hellman NE, Liu Y, Merkel E, Austin C, Le Corre S, Beier DR, Sun Z, Sharma N, Yoder BK, Drummond IA. The zebrafish foxj1a transcription factor regulates cilia function in response to injury and epithelial stretch. Proc Natl Acad Sci U S A. 2010;107:18499-504.
121. Jain N, Iyer KV, Kumar A, Shivashankar GV. Cell geometric constraints induce modular gene-expression patterns via redistribution of HDAC3 regulated by actomyosin contractility. Proc Natl Acad Sci U S A. 2013;110:11349-54.
122. Xie C, Guo Y, Zhu T, Zhang J, Ma PX, Chen YE. Yap1 Protein Regulates Vascular Smooth Muscle Cell Phenotypic Switch by Interaction with Myocardin. J Biol Chem. 2012;287:14598-605.
123. 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. 2015;36:39-49.
124. Liu CY, Chan SW, Guo F, Toloczko A, Cui L, Hong W. MRTF/SRF dependent transcriptional regulation of TAZ in breast cancer cells. Oncotarget. 2016;7:13706-16.
125. Speight P, Kofler M, Szászi K, Kapus A. Context-dependent switch in chemo/mechanotransduction via multilevel crosstalk among cytoskeleton-regulated MRTF and TAZ and TGFβ-regulated Smad3. Nat Commun. 2016;7:11642.
126. Bork P, Sudol M. The WW domain: a signalling site in dystrophin? Trends Biochem Sci. 1995;19:531-3.
127. Chen HI, Sudol M. The WW domain of Yes-associated protein binds a proline-rich ligand that differs from the consensus established for Src homology 3-binding modules. Proc Natl Acad Sci U S A. 1995;92:7819-23.
128. Komuro A, Nagai M, Navin NE, Sudol M. WW Domain-containing Protein YAP Associates with ErbB-4 and Acts as a Co-transcriptional Activator for the Carboxyl-terminal Fragment of ErbB-4 That Translocates to the Nucleus. J Biol Chem. 2003;278:33334-41.
129. Haskins JW, Nguyen DX, Stern DF. Neuregulin 1-activated ERBB4 interacts with YAP to induce Hippo pathway target genes and promote cell migration. Sci Signal. 2014;7:ra116.
130. Giannone G, Sheetz M. Substrate rigidity and force define form through tyrosine phosphatase and kinase pathways. Trends Cell Biol. 2006;16:213-23.
131. Prager-Khoutorsky M, Lichtenstein A, Krishnan R, Rajendran K, Mayo A, Kam Z, Geiger B, Bershadsky AD. Fibroblast polarization is a matrix-rigidity-dependent process controlled by focal adhesion mechanosensing. Nat Cell Biol. 2011;13:1457-65.
132. 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. 2010;188:383-99.
133. Charbonney E, Speight P, Masszi A, Nakano H, Kapus A. β-Catenin and Smad3 regulate the activity and stability of myocardin-related transcription factor during epithelial-myofibroblast transition. Mol Biol Cell. 2011;22:4472-85.
134. Benham-Pyle BW, Pruitt BL, Nelson WJ. Mechanical strain induces E-cadherin-dependent Yap1 and β-catenin activation to drive cell cycle entry. Science. 2015;348:1024-7.
135. Kraemer BF, Borst O, Gehring EM, Schoenberger T, Urban B, Ninci E, Seizer P, Schmidt C, Bigalke B, Koch M, Martinovic I, Daub K, Merz T, Schwanitz L, Stellos K, Fiesel F, Schaller M, Lang F, Gawaz M, Lindemann S. PI3 kinase-dependent stimulation of platelet migration by stromal cell-derived factor 1 (SDF-1). J Mol Med. 2010;88:1277-88.
136. Schmidt EM, Münzer P, Borst O, Kraemer BF, Schmid E, Urban B, Lindemann S, Ruth P, Gawaz M, Lang F. Ion channels in the regulation of platelet migration. Biochem Biophys Res Commun. 2011;415:54-60.
137. Yount G, Taft RJ, Luu T, Rachlin K, Moore D, Zhang W. Independent motile microplast formation correlates with glioma cell invasiveness. J Neurooncol. 2007;81:113-21.
138. Chanet S, Martin AC. Mechanical Force Sensing in Tissues. Prog Mol Biol Transl Sci. 2014;126:317-52.
139. Riveline D, Zamir E, Balaban NQ, Schwarz US, Ishizaki T, Narumiya S, Kam Z, Geiger B, Bershadsky AD. Focal contacts as mechanosensors: externally applied local mechanical force induces growth of focal contacts by an mDia1-dependent and ROCK- independent mechanism. J Cell Biol. 2001;153:1175-86.
140. Liu Z, Tan JL, Cohen DM, Yang MT, Sniadecki NJ, Ruiz SA, Nelson CM, Chen CS. Mechanical tugging force regulates the size of cell-cell junctions. Proc Natl Acad Sci U S A. 2010;107:9944-9.
141. Kovács M, Thirumurugan K, Knight PJ, Sellers JR. Load-dependent mechanism of nonmuscle myosin 2. Proc Natl Acad Sci U S A. 2007;104:9994-9.
142. Jégou A, Carlier MF, Romet-Lemonne G. Formin mDia1 senses and generates mechanical forces on actin filaments. Nat Commun. 2013;4:1883.
143. Kuipers AJ, Middelbeek J, van Leeuwen FN. Mechanoregulation of cytoskeletal dynamics by TRP channels. Eur J Cell Biol. 2012;21:834-46.
144. Zanconato F, Forcato M, Battilana G, Azzolin L, Quaranta E, Bodega B, Rosato A, Bicciato S, Cordenonsi M, Piccolo S. Genome-wide association between YAP/TAZ/TEAD and AP-1 at enhancers drives oncogenic growth. Nat Cell Biol. 2015;17:1218-27.
145. Lawrence MS, Stojanov P, Mermel CH, Robinson JT, Garraway LA, Golub TR, Meyerson M, Gabriel SB, Lander ES, Getz G. Discovery and saturation analysis of cancer genes across 21 tumour types. Nature. 2014;505:495-501.
146. Gaffney CJ, Oka T, Mazack V, Hilman D, Gat U, Muramatsu T, Inazawa J, Golden A, Carey DJ, Farooq A, Tromp G, Sudol M. Identification, basic characterization and evolutionary analysis of differentially spliced mRNA isoforms of human YAP1 gene. Gene. 2012;509:215-22.
147. Oka T, Schmitt AP, Sudol M. Opposing roles of angiomotin-like-1 and zona occludens-2 on pro-apoptotic function of YAP. Oncogene. 2012;31:128-34.
148. Finch-Edmondson ML, Strauss RP, Clayton JS, Yeoh GC, Callus BA. Splice variant insertions in the C-terminus impairs YAP's transactivation domain. Biochem Biophys Rep. 2016;6:24-31.
149. Sudol M, Harvey KF. Modularity in the Hippo signaling pathway. Trends Biochem Sci. 2010;35:627-33.
150. Oka T, Remue E, Meerschaert K, Vanloo B, Boucherie C, Gfeller D, Bader GD, Sidhu SS, Vandekerckhove J, Gettemans J, Sudol M. Functional complexes between YAP2 and ZO-2 are PDZ domain-dependent, and regulate YAP2 nuclear localization and signalling. Biochem J. 2010;432:461-72.