p66^Shc Couples Mechanical Signals to RhoA through Focal Adhesion Kinase-Dependent Recruitment of p115-RhoGEF and GEF-H1

REFERENCES

• Matthews BD, Overby DR, Mannix R, Ingber DE. 2006. Cellular adaptation to mechanical stress: role of integrins, Rho, cytoskeletal tension and mechanosensitive ion channels. J Cell Sci 119:508–518. http://dx.doi.org/10.1242/jcs.02760.
   PubMedGoogle Scholar
• McBeath R, Pirone DM, Nelson CM, Bhadriraju K, Chen CS. 2004. Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment. Dev Cell 6:483–495. http://dx.doi.org/10.1016/S1534-5807(04)00075-9.
   PubMed Web of Science ®Google Scholar
• Ewald AJ, Brenot A, Duong M, Chan BS, Werb Z. 2008. Collective epithelial migration and cell rearrangements drive mammary branching morphogenesis. Dev Cell 14:570–581. http://dx.doi.org/10.1016/j.devcel.2008.03.003.
   PubMed Web of Science ®Google Scholar
• Farge E. 2003. Mechanical induction of Twist in the Drosophila foregut/stomodeal primordium. Curr Biol 13:1365–1377. http://dx.doi.org/10.1016/S0960-9822(03)00576-1.
   PubMed Web of Science ®Google Scholar
• Harden N, Ricos M, Ong YM, Chia W, Lim L. 1999. Participation of small GTPases in dorsal closure of the Drosophila embryo: distinct roles for Rho subfamily proteins in epithelial morphogenesis. J Cell Sci 112(Pt 3):273–284.
   PubMedGoogle Scholar
• Moore KA, Polte T, Huang S, Shi B, Alsberg E, Sunday ME, Ingber DE. 2005. Control of basement membrane remodeling and epithelial branching morphogenesis in embryonic lung by Rho and cytoskeletal tension. Dev Dyn 232:268–281. http://dx.doi.org/10.1002/dvdy.20237.
   PubMedGoogle Scholar
• Nakaya Y, Sukowati EW, Wu Y, Sheng G. 2008. RhoA and microtubule dynamics control cell-basement membrane interaction in EMT during gastrulation. Nat Cell Biol 10:765–775. http://dx.doi.org/10.1038/ncb1739.
   PubMedGoogle Scholar
• Zhao XH, Laschinger C, Arora P, Szaszi K, Kapus A, McCulloch CA. 2007. Force activates smooth muscle alpha-actin promoter activity through the Rho signaling pathway. J Cell Sci 120:1801–1809. http://dx.doi.org/10.1242/jcs.001586.
   PubMedGoogle Scholar
• Pelicci G, Lanfrancone L, Grignani F, McGlade J, Cavallo F, Forni G, Nicoletti I, Pawson T, Pelicci PG. 1992. A novel transforming protein (SHC) with an SH2 domain is implicated in mitogenic signal transduction. Cell 70:93–104. http://dx.doi.org/10.1016/0092-8674(92)90536-L.
   PubMed Web of Science ®Google Scholar
• Rozakis-Adcock M, McGlade J, Mbamalu G, Pelicci G, Daly R, Li W, Batzer A, Thomas S, Brugge J, Pelicci PG, Schlessinger J, Pawson T. 1992. Association of the Shc and Grb2/Sem5 SH2-containing proteins is implicated in activation of the Ras pathway by tyrosine kinases. Nature 360:689–692. http://dx.doi.org/10.1038/360689a0.
   PubMed Web of Science ®Google Scholar
• Nicholson PR, Empereur S, Glover HR, Dilworth SM. 2001. ShcA tyrosine phosphorylation sites can replace ShcA binding in signalling by middle T-antigen. EMBO J 20:6337–6346. http://dx.doi.org/10.1093/emboj/20.22.6337.
   PubMedGoogle Scholar
• Ong SH, Dilworth S, Hauck-Schmalenberger I, Pawson T, Kiefer F. 2001. ShcA and Grb2 mediate polyoma middle T antigen-induced endothelial transformation and Gab1 tyrosine phosphorylation. EMBO J 20:6327–6336. http://dx.doi.org/10.1093/emboj/20.22.6327.
   PubMedGoogle Scholar
• Wary KK, Mainiero F, Isakoff SJ, Marcantonio EE, Giancotti FG. 1996. The adaptor protein Shc couples a class of integrins to the control of cell cycle progression. Cell 87:733–743. http://dx.doi.org/10.1016/S0092-8674(00)81392-6.
   PubMed Web of Science ®Google Scholar
• Wary KK, Mariotti A, Zurzolo C, Giancotti FG. 1998. A requirement for caveolin-1 and associated kinase Fyn in integrin signaling and anchorage-dependent cell growth. Cell 94:625–634. http://dx.doi.org/10.1016/S0092-8674(00)81604-9.
   PubMed Web of Science ®Google Scholar
• Cowan KJ, Law DA, Phillips DR. 2000. Identification of Shc as the primary protein binding to the tyrosine-phosphorylated beta 3 subunit of alpha IIbbeta 3 during outside-in integrin platelet signaling. J Biol Chem 275:36423–36429. http://dx.doi.org/10.1074/jbc.M004068200.
   PubMedGoogle Scholar
• Deshmukh L, Gorbatyuk V, Vinogradova O. 2010. Integrin {beta}3 phosphorylation dictates its complex with the Shc phosphotyrosine-binding (PTB) domain. J Biol Chem 285:34875–34884. http://dx.doi.org/10.1074/jbc.M110.159087.
   PubMedGoogle Scholar
• Migliaccio E, Mele S, Salcini AE, Pelicci G, Lai KM, Superti-Furga G, Pawson T, Di Fiore PP, Lanfrancone L, Pelicci PG. 1997. Opposite effects of the p52shc/p46shc and p66shc splicing isoforms on the EGF receptor-MAP kinase-fos signalling pathway. EMBO J 16:706–716. http://dx.doi.org/10.1093/emboj/16.4.706.
   PubMed Web of Science ®Google Scholar
• Xi G, Shen X, Clemmons DR. 2010. p66shc inhibits insulin-like growth factor-I signaling via direct binding to Src through its polyproline and Src homology 2 domains, resulting in impairment of Src kinase activation. J Biol Chem 285:6937–6951. http://dx.doi.org/10.1074/jbc.M109.069872.
   PubMed Web of Science ®Google Scholar
• Natalicchio A, Laviola L, De Tullio C, Renna LA, Montrone C, Perrini S, Valenti G, Procino G, Svelto M, Giorgino F. 2004. Role of the p66Shc isoform in insulin-like growth factor I receptor signaling through MEK/Erk and regulation of actin cytoskeleton in rat myoblasts. J Biol Chem 279:43900–43909. http://dx.doi.org/10.1074/jbc.M403936200.
   PubMed Web of Science ®Google Scholar
• Lee MK, Smith SM, Banerjee MM, Li C, Minoo P, Volpe MV, Nielsen HC. 2014. The p66Shc adapter protein regulates the morphogenesis and epithelial maturation of fetal mouse lungs. Am J Physiol Lung Cell Mol Physiol 306:L316–L325. http://dx.doi.org/10.1152/ajplung.00062.2013.
   PubMedGoogle Scholar
• Favetta LA, Madan P, Mastromonaco GF, St John EJ, King WA, Betts DH. 2007. The oxidative stress adaptor p66Shc is required for permanent embryo arrest in vitro. BMC Dev Biol 7:132. http://dx.doi.org/10.1186/1471-213X-7-132.
   PubMedGoogle Scholar
• Ma Z, Myers DP, Wu RF, Nwariaku FE, Terada LS. 2007. p66Shc mediates anoikis through RhoA. J Cell Biol 179:23–31. http://dx.doi.org/10.1083/jcb.200706097.
   PubMed Web of Science ®Google Scholar
• Ma Z, Liu Z, Wu RF, Terada LS. 2010. p66Shc restrains Ras hyperactivation and suppresses metastatic behavior. Oncogene 29:5559–5567. http://dx.doi.org/10.1038/onc.2010.326.
   PubMed Web of Science ®Google Scholar
• Wang YL, Pelham RJ, Jr. 1998. Preparation of a flexible, porous polyacrylamide substrate for mechanical studies of cultured cells. Methods Enzymol 298:489–496. http://dx.doi.org/10.1016/S0076-6879(98)98041-7.
   PubMed Web of Science ®Google Scholar
• Guilluy C, Swaminathan V, Garcia-Mata R, O'Brien ET, Superfine R, Burridge K. 2011. The Rho GEFs LARG and GEF-H1 regulate the mechanical response to force on integrins. Nat Cell Biol 13:724–729. http://dx.doi.org/10.1038/ncb2254.
   Google Scholar
• Zhou MM, Ravichandran KS, Olejniczak EF, Petros AM, Meadows RP, Sattler M, Harlan JE, Wade WS, Burakoff SJ, Fesik SW. 1995. Structure and ligand recognition of the phosphotyrosine binding domain of Shc. Nature 378:584–592. http://dx.doi.org/10.1038/378584a0.
   PubMedGoogle Scholar
• Lietha D, Cai X, Ceccarelli DF, Li Y, Schaller MD, Eck MJ. 2007. Structural basis for the autoinhibition of focal adhesion kinase. Cell 129:1177–1187. http://dx.doi.org/10.1016/j.cell.2007.05.041.
   PubMed Web of Science ®Google Scholar
• Iwanicki MP, Vomastek T, Tilghman RW, Martin KH, Banerjee J, Wedegaertner PB, Parsons JT. 2008. FAK, PDZ-RhoGEF and ROCKII cooperate to regulate adhesion movement and trailing-edge retraction in fibroblasts. J Cell Sci 121:895–905. http://dx.doi.org/10.1242/jcs.020941.
   PubMedGoogle Scholar
• Medley QG, Buchbinder EG, Tachibana K, Ngo H, Serra-Pages C, Streuli M. 2003. Signaling between focal adhesion kinase and trio. J Biol Chem 278:13265–13270. http://dx.doi.org/10.1074/jbc.M300277200.
   PubMed Web of Science ®Google Scholar
• Garcia-Mata R, Wennerberg K, Arthur WT, Noren NK, Ellerbroek SM, Burridge K. 2006. Analysis of activated GAPs and GEFs in cell lysates. Methods Enzymol 406:425–437. http://dx.doi.org/10.1016/S0076-6879(06)06031-9.
   PubMed Web of Science ®Google Scholar
• Khamdaeng T, Luo J, Vappou J, Terdtoon P, Konofagou EE. 2012. Arterial stiffness identification of the human carotid artery using the stress-strain relationship in vivo. Ultrasonics 52:402–411. http://dx.doi.org/10.1016/j.ultras.2011.09.006.
   PubMed Web of Science ®Google Scholar
• Riley WA, Barnes RW, Evans GW, Burke GL. 1992. Ultrasonic measurement of the elastic modulus of the common carotid artery. The Atherosclerosis Risk in Communities (ARIC) Study. Stroke 23:952–956.
   PubMed Web of Science ®Google Scholar
• 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. 2011. Role of YAP/TAZ in mechanotransduction. Nature 474:179–183. http://dx.doi.org/10.1038/nature10137.
   PubMed Web of Science ®Google Scholar
• Chen KD, Li YS, Kim M, Li S, Yuan S, Chien S, Shyy JY. 1999. Mechanotransduction in response to shear stress. Roles of receptor tyrosine kinases, integrins, and Shc. J Biol Chem 274:18393–18400.
   Google Scholar
• Liu Y, Sweet DT, Irani-Tehrani M, Maeda N, Tzima E. 2008. Shc coordinates signals from intercellular junctions and integrins to regulate flow-induced inflammation. J Cell Biol 182:185–196. http://dx.doi.org/10.1083/jcb.200709176.
   PubMedGoogle Scholar
• Hardy WR, Li L, Wang Z, Sedy J, Fawcett J, Frank E, Kucera J, Pawson T. 2007. Combinatorial ShcA docking interactions support diversity in tissue morphogenesis. Science 317:251–256. http://dx.doi.org/10.1126/science.1140114.
   PubMedGoogle Scholar
• Vanderlaan RD, Hardy WR, Kabir MG, Pasculescu A, Jones N, deTombe PP, Backx PH, Pawson T. 2011. The ShcA phosphotyrosine docking protein uses distinct mechanisms to regulate myocyte and global heart function. Circ Res 108:184–193. http://dx.doi.org/10.1161/CIRCRESAHA.110.233924.
   PubMedGoogle Scholar
• Dubash AD, Wennerberg K, Garcia-Mata R, Menold MM, Arthur WT, Burridge K. 2007. A novel role for Lsc/p115 RhoGEF and LARG in regulating RhoA activity downstream of adhesion to fibronectin. J Cell Sci 120:3989–3998. http://dx.doi.org/10.1242/jcs.003806.
   PubMedGoogle Scholar
• Scott DW, Tolbert CE, Burridge K. 2016. Tension on JAM-A activates RhoA via GEF-H1 and p115 RhoGEF. Mol Biol Cell 27:1420–1430. http://dx.doi.org/10.1091/mbc.E15-12-0833.
   PubMed Web of Science ®Google Scholar
• Schlaepfer DD, Jones KC, Hunter T. 1998. Multiple Grb2-mediated integrin-stimulated signaling pathways to ERK2/mitogen-activated protein kinase: summation of both c-Src- and focal adhesion kinase-initiated tyrosine phosphorylation events. Mol Cell Biol 18:2571–2585. http://dx.doi.org/10.1128/MCB.18.5.2571.
   PubMed Web of Science ®Google Scholar
• Barberis L, Wary KK, Fiucci G, Liu F, Hirsch E, Brancaccio M, Altruda F, Tarone G, Giancotti FG. 2000. Distinct roles of the adaptor protein Shc and focal adhesion kinase in integrin signaling to ERK. J Biol Chem 275:36532–36540. http://dx.doi.org/10.1074/jbc.M002487200.
   PubMedGoogle Scholar
• Gu J, Tamura M, Pankov R, Danen EH, Takino T, Matsumoto K, Yamada KM. 1999. Shc and FAK differentially regulate cell motility and directionality modulated by PTEN. J Cell Biol 146:389–403. http://dx.doi.org/10.1083/jcb.146.2.389.
   PubMed Web of Science ®Google Scholar
• Schaller MD. 2010. Cellular functions of FAK kinases: insight into molecular mechanisms and novel functions. J Cell Sci 123:1007–1013. http://dx.doi.org/10.1242/jcs.045112.
   PubMed Web of Science ®Google Scholar
• Chan SW, Lim CJ, Guo K, Ng CP, Lee I, Hunziker W, Zeng Q, Hong W. 2008. A role for TAZ in migration, invasion, and tumorigenesis of breast cancer cells. Cancer Res 68:2592–2598. http://dx.doi.org/10.1158/0008-5472.CAN-07-2696.
   PubMed Web of Science ®Google Scholar
• Tian Y, Kolb R, Hong JH, Carroll J, Li D, You J, Bronson R, Yaffe MB, Zhou J, Benjamin T. 2007. TAZ promotes PC2 degradation through a SCFbeta-Trcp E3 ligase complex. Mol Cell Biol 27:6383–6395. http://dx.doi.org/10.1128/MCB.00254-07.
   PubMedGoogle Scholar
• Zhou Z, Hao Y, Liu N, Raptis L, Tsao MS, Yang X. 2011. TAZ is a novel oncogene in non-small cell lung cancer. Oncogene 30:2181–2186. http://dx.doi.org/10.1038/onc.2010.606.
   PubMed Web of Science ®Google Scholar
• Zhao B, Li L, Wang L, Wang CY, Yu J, Guan KL. 2012. Cell detachment activates the Hippo pathway via cytoskeleton reorganization to induce anoikis. Genes Dev 26:54–68. http://dx.doi.org/10.1101/gad.173435.111.
   PubMed Web of Science ®Google Scholar
• Li X, Xu Z, Du W, Zhang Z, Wei Y, Wang H, Zhu Z, Qin L, Wang L, Niu Q, Zhao X, Girard L, Gong Y, Ma Z, Sun B, Yao Z, Minna JD, Terada LS, Liu Z. 2014. Aiolos promotes anchorage independence by silencing p66(Shc) transcription in cancer cells. Cancer Cell 25:575–589. http://dx.doi.org/10.1016/j.ccr.2014.03.020.
   PubMed Web of Science ®Google Scholar
• Glaven JA, Whitehead IP, Nomanbhoy T, Kay R, Cerione RA. 1996. Lfc and Lsc oncoproteins represent two new guanine nucleotide exchange factors for the Rho GTP-binding protein. J Biol Chem 271:27374–27381. http://dx.doi.org/10.1074/jbc.271.44.27374.
   PubMed Web of Science ®Google Scholar
• Jaiswal M, Gremer L, Dvorsky R, Haeusler LC, Cirstea IC, Uhlenbrock K, Ahmadian MR. 2011. Mechanistic insights into specificity, activity, and regulatory elements of the regulator of G-protein signaling (RGS)-containing Rho-specific guanine nucleotide exchange factors (GEFs) p115, PDZ-RhoGEF (PRG), and leukemia-associated RhoGEF (LARG). J Biol Chem 286:18202–18212. http://dx.doi.org/10.1074/jbc.M111.226431.
   PubMed Web of Science ®Google Scholar
• Nimnual AS, Yatsula BA, Bar-Sagi D. 1998. Coupling of Ras and Rac guanosine triphosphatases through the Ras exchanger Sos. Science 279:560–563. http://dx.doi.org/10.1126/science.279.5350.560.
   PubMed Web of Science ®Google Scholar