Adhesion-mediated cytoskeletal remodeling is controlled by the direct scaffolding of Src from FAK complexes to lipid rafts by SSeCKS/AKAP12 (original) (raw)

• Iiizumi M, Liu W, Pai SK, Furuta E, Watabe K . Drug development against metastasis-related genes and their pathways: a rationale for cancer therapy. Biochim Biophys Acta 2008; 1786: 87–104.
  CAS PubMed PubMed Central Google Scholar
• Frame MC . Newest findings on the oldest oncogene; how activated src does it. J Cell Sci 2004; 117: 989–998.
  Article CAS PubMed Google Scholar
• Bild AH, Parker JS, Gustafson AM, Acharya CR, Hoadley KA, Anders C et al. An integration of complementary strategies for gene-expression analysis to reveal novel therapeutic opportunities for breast cancer. Breast Cancer Res 2009; 11: R55.
  Article PubMed PubMed Central Google Scholar
• Kumar A, White TA, Mackenzie AP, Clegg N, Lee C, Dumpit RF et al. Exome sequencing identifies a spectrum of mutation frequencies in advanced and lethal prostate cancers. Proc Natl Acad Sci USA 2011; 108: 17087–17092.
  Article CAS PubMed PubMed Central Google Scholar
• Sturge J, Caley MP, Waxman J . Bone metastasis in prostate cancer: emerging therapeutic strategies. Nat Rev Clin Oncol 2011; 8: 357–368.
  Article CAS PubMed Google Scholar
• Gelman IH . Src-family tyrosine kinases as therapeutic targets in advanced cancer. Front Biosci 2011; E3: 801–807.
  Article CAS Google Scholar
• Trevino JG, Summy JM, Lesslie DP, Parikh NU, Hong DS, Lee FY et al. Inhibition of SRC expression and activity inhibits tumor progression and metastasis of human pancreatic adenocarcinoma cells in an orthotopic nude mouse model. Am J Pathol 2006; 168: 962–972.
  Article CAS PubMed PubMed Central Google Scholar
• Eliceiri BP, Paul R, Schwartzberg PL, Hood JD, Leng J, Cheresh DA . Selective requirement for Src kinases during VEGF-induced angiogenesis and vascular permeability. Mol Cell 1999; 4: 915–924.
  Article CAS PubMed Google Scholar
• Hiscox S, Morgan L, Green T, Nicholson RI . Src as a therapeutic target in anti-hormone/anti-growth factor-resistant breast cancer. Endocr Relat Cancer 2006; 13 (Suppl 1): S53–S59.
  Article CAS PubMed Google Scholar
• Ischenko I, Camaj P, Seeliger H, Kleespies A, Guba M, De Toni EN et al. Inhibition of Src tyrosine kinase reverts chemoresistance toward 5-fluorouracil in human pancreatic carcinoma cells: an involvement of epidermal growth factor receptor signaling. Oncogene 2008; 27: 7212–7222.
  Article CAS PubMed Google Scholar
• Yoshida T, Okamoto I, Okamoto W, Hatashita E, Yamada Y, Kuwata K et al. Effects of Src inhibitors on cell growth and epidermal growth factor receptor and MET signaling in gefitinib-resistant non-small cell lung cancer cells with acquired MET amplification. Cancer Sci 2010; 101: 167–172.
  Article CAS PubMed Google Scholar
• Martin GS . The hunting of the Src. Nat Rev Mol Cell Biol 2001; 2: 467–475.
  Article CAS PubMed Google Scholar
• Bos JL . Ras oncogenes in human cancer: a review. Cancer Res 1989; 49: 4682–4689.
  CAS PubMed Google Scholar
• Milligan G, Parenti M, Magee AI . The dynamic role of palmitoylation in signal transduction. TIBS 1995; 20: 181–186.
  CAS PubMed Google Scholar
• Resh MD . Myristylation and palmitylation of src family members: the fats of the matter. Cell 1994; 76: 411–414.
  Article CAS PubMed Google Scholar
• Cross FR, Garber EA, Pellman D, Hanafusa H . A short sequence in the p60src N terminus is required for p60src myristylation and membrane association and for cell transformation. Mol Cell Biol 1984; 4: 1834–1842.
  Article CAS PubMed PubMed Central Google Scholar
• Aoki M, Batista O, Bellacosa A, Tsichlis P, Vogt PK . The akt kinase: molecular determinants of oncogenicity. Proc Natl Acad Sci USA 1998; 95: 14950–14955.
  Article CAS PubMed PubMed Central Google Scholar
• Song KS, Sargiacomo M, Galbiati F, Parenti M, Lisanti MP . Targeting of a Gα subunit (Gi1α) and c-Src tyrosine kinase to caveolae membranes: clarifying the role of N- myristoylation. Cell Mol Biol 1997; 43: 293–303.
  CAS PubMed Google Scholar
• Wanaski SP, Ng BK, Glaser M . Caveolin scaffolding region and the membrane binding region of src form lateral membrane domains. Biochemistry 2003; 42: 42–56.
  Article CAS PubMed Google Scholar
• Sverdlov M, Shajahan AN, Minshall RD . Tyrosine phosphorylation-dependence of caveolae-mediated endocytosis. J Cell Mol Med 2007; 11: 1239–1250.
  Article CAS PubMed PubMed Central Google Scholar
• Patra SK . Dissecting lipid raft facilitated cell signaling pathways in cancer. Biochim Biophys Acta 2008; 1785: 182–206.
  CAS PubMed Google Scholar
• Nethe M, Hordijk PL . A model for phospho-caveolin-1-driven turnover of focal adhesions. Cell Adh Migr 2011; 5: 59–64.
  Article PubMed PubMed Central Google Scholar
• Gelman IH . Emerging Roles for SSeCKS/Gravin/AKAP12 in the control of cell proliferation, cancer malignancy, and barriergenesis. Genes Cancer 2010; 1: 1147–1156.
  Article CAS PubMed PubMed Central Google Scholar
• Yan X, Walkiewicz M, Carlson J, Leiphon L, Grove B . Gravin dynamics regulates the subcellular distribution of PKA. Exp Cell Res 2009; 315: 1247–1259.
  Article CAS PubMed PubMed Central Google Scholar
• Su B, Zheng Q, Vaughan MM, Bu Y, Gelman IH . SSeCKS metastasis-suppressing activity in MatLyLu prostate cancer cells correlates with VEGF inhibition. Cancer Res 2006; 66: 5599–5607.
  Article CAS PubMed Google Scholar
• Brunton VG, Avizienyte E, Fincham VJ, Serrels B, Metcalf CA, Sawyer TK et al. Identification of Src-specific phosphorylation site on focal adhesion kinase: dissection of the role of Src SH2 and catalytic functions and their consequences for tumor cell behavior. Cancer Res 2005; 65: 1335–1342.
  Article CAS PubMed Google Scholar
• Li SW, Couet J, Lisanti MP . Src tyrosine kinases, Gα subunits, and H-Ras share a common membrane-anchored scaffolding protein, caveolin—caveolin binding negatively regulates the auto-activation of Src tyrosine kinases. J Biol Chem 1996; 271: 29182–29190.
  Article CAS PubMed Google Scholar
• Su B, Bu Y, Engelberg D, Gelman IH . SSeCKS/Gravin/AKAP12 inhibits cancer cell invasiveness and chemotaxis by suppressing a protein kinase C- Raf/MEK/ERK pathway. J Biol Chem 2010; 285: 4578–4586.
  Article CAS PubMed Google Scholar
• Pollard TD, Borisy GG . Cellular motility driven by assembly and disassembly of actin filaments. Cell 2003; 112: 453–465.
  Article CAS PubMed Google Scholar
• Xia W, Unger P, Miller L, Nelson J, Gelman IH . The _Src_-suppressed C kinase substrate, SSeCKS, is a potential metastasis inhibitor in prostate cancer. Cancer Res 2001; 61: 5644–5651.
  CAS PubMed Google Scholar
• Lin X, Gelman IH . Re-expression of the major protein kinase C substrate, SSeCKS, suppresses v-_src-_induced morphological transformation and tumorigenesis. Cancer Res 1997; 57: 2304–2312.
  CAS PubMed Google Scholar
• Xia W, Gelman IH . Mitogen- and FAK-regulated tyrosine phosphorylation of the SSeCKS scaffolding protein modulates its actin-binding properties. Exp Cell Res 2002; 277: 139–151.
  Article CAS PubMed Google Scholar
• Damsky CH, Werb Z . Signal transduction by integrin receptors for extracellular matrix: cooperative processing of extracellular information. Curr Opin Cell Biol 1992; 4: 772–781.
  Article CAS PubMed Google Scholar
• Mizejewski GJ . Role of integrins in cancer: survey of expression patterns. Proc Soc Exp Biol Med 1999; 222: 124–138.
  Article CAS PubMed Google Scholar
• Yilmaz M, Christofori G . EMT, the cytoskeleton, and cancer cell invasion. Cancer Metastasis Rev 2009; 28: 15–33.
  Article PubMed Google Scholar
• Playford MP, Schaller MD . The interplay between Src and integrins in normal and tumor biology. Oncogene 2004; 23: 7928–7946.
  Article CAS PubMed Google Scholar
• Kumar CC . Signaling by integrin receptors. Oncogene 1998; 17: 1365–1373.
  Article CAS PubMed Google Scholar
• MacCalman CD, Brodt P, Doublet JD, Jednak R, Elhilali MM, Bazinet M et al. The loss of E-cadherin mRNA transcripts in rat prostatic tumors is accompanied by increased expression of mRNA transcripts encoding fibronectin and its receptor. Clin Exp Metastasis 1994; 12: 101–107.
  Article CAS PubMed Google Scholar
• Mitra SK, Schlaepfer DD . Integrin-regulated FAK-Src signaling in normal and cancer cells. Curr Opin Cell Biol 2006; 18: 516–523.
  Article CAS PubMed Google Scholar
• Brunton VG, Frame MC . Src and focal adhesion kinase as therapeutic targets in cancer. Curr Opin Pharmacol 2008; 8: 427–432.
  Article CAS PubMed Google Scholar
• Zhao J, Guan JL . Signal transduction by focal adhesion kinase in cancer. Cancer Metastasis Rev 2009; 28: 35–49.
  Article PubMed Google Scholar
• Schaller MD, Borgman CA, Parsons JT . Autonomous expression of a noncatalytic domain of the focal adhesion-associated protein tyrosine kinase pp125FAK. Mol Cell Biol 1993; 13: 785–791.
  Article CAS PubMed PubMed Central Google Scholar
• Ilic D, Furuta Y, Kanazawa S, Takeda N, Sobue K, Nakatsuji N et al. Reduced cell motility and enhanced focal adhesion contact formation in cells from FAK-deficient mice. Nature 1995; 377: 539–544.
  Article CAS PubMed Google Scholar
• Schlaepfer DD, Hauck CR, Sieg DJ . Signaling through focal adhesion kinase. Prog Biophys Mol Biol 1999; 71: 435–478.
  Article CAS PubMed Google Scholar
• Sieg DJ, Hauck CR, Schlaepfer DD . Required role of focal adhesion kinase (FAK) for integrin-stimulated cell migration. J Cell Sci 1999; 112 (Pt 16): 2677–2691.
  CAS PubMed Google Scholar
• Richardson A, Malik RK, Hildebrand JD, Parsons JT . Inhibition of cell spreading by expression of the C-terminal domain of focal adhesion kinase (FAK) is rescued by coexpression of Src or catalytically inactive FAK: a role for paxillin tyrosine phosphorylation. Mol Cell Biol 1997; 17: 6906–6914.
  Article CAS PubMed PubMed Central Google Scholar
• Moissoglu K, Gelman IH . v-Src rescues actin-based cytoskeletal architecture and cell motility, and induces enhanced anchorage-independence during oncogenic transformation of FAK-null fibroblasts. J Biol Chem 2003; 278: 47946–47959.
  Article CAS PubMed Google Scholar
• Schlaepfer DD, Hunter T . Evidence for in vivo phosphorylation of the Grb2 SH2-domain binding site on focal adhesion kinase by Src-family protein- tyrosine kinases. Mol Cell Biol 1996; 16: 5623–5633.
  Article CAS PubMed PubMed Central Google Scholar
• Mitra SK, Mikolon D, Molina JE, Hsia DA, Hanson DA, Chi A et al. Intrinsic FAK activity and Y925 phosphorylation facilitate an angiogenic switch in tumors. Oncogene 2006; 25: 5969–5984.
  Article CAS PubMed Google Scholar
• Gelman IH, Gao L . SSeCKS/Gravin/AKAP12 metastasis suppressor inhibits podosome formation via RhoA- and Cdc42-dependent pathways. Mol Cancer Res 2006; 4: 151–158.
  Article CAS PubMed Google Scholar
• Tao J, Wang HY, Malbon CC . Src docks to A-kinase anchoring protein gravin, regulating beta2-adrenergic receptor resensitization and recycling. J Biol Chem 2007; 282: 6597–6608.
  Article CAS PubMed Google Scholar
• Razani B, Woodman SE, Lisanti MP . Caveolae: from cell biology to animal physiology. Pharmacol Rev 2002; 54: 431–467.
  Article CAS PubMed Google Scholar
• Navarro A, Anand-Apte B, Parat MO . A role for caveolae in cell migration. FASEB J 2004; 18: 1801–1811.
  Article CAS PubMed Google Scholar
• Glenney JR . Tyrosine phosphorylation of a 22-kDa protein is correlated with transformation by Rous sarcoma virus. J Biol Chem 1989; 264: 20163–20166.
  CAS PubMed Google Scholar
• Rothberg KG, Heuser JE, Donzell WC, Ying YS, Glenney JR, Anderson RG . Caveolin, a protein component of caveolae membrane coats. Cell 1992; 68: 673–682.
  Article CAS PubMed Google Scholar
• Lin X, Tombler E, Nelson PJ, Ross M, Gelman IH . A novel _src_- and _ras_-suppressed protein kinase C substrate associated with cytoskeletal architecture. J Biol Chem 1996; 271: 28430–28438.
  Article CAS PubMed Google Scholar
• Shaul PW, Anderson RG . Role of plasmalemmal caveolae in signal transduction. Am J Physiol 1998; 275: L843–L851.
  CAS PubMed Google Scholar
• Williams TM, Lisanti MP . Caveolin-1 in oncogenic transformation, cancer, and metastasis. Am J Physiol Cell Physiol 2005; 288: C494–C506.
  Article CAS PubMed Google Scholar
• Seong J, Ouyang M, Kim T, Sun J, Wen PC, Lu S et al. Detection of focal adhesion kinase activation at membrane microdomains by fluorescence resonance energy transfer. Nat Commun 2011; 2: 406.
  Article PubMed Google Scholar
• Seong J, Lu S, Ouyang M, Huang H, Zhang J, Frame MC et al. Visualization of Src activity at different compartments of the plasma membrane by FRET imaging. Chem Biol 2009; 16: 48–57.
  Article CAS PubMed PubMed Central Google Scholar
• Malek RL, Irby RB, Guo QBM, Lee K, Wong S, He M et al. Identification of Src transformation fingerprint in human colon cancer. Oncogene 2002; 21: 7256–7265.
  Article CAS PubMed Google Scholar
• Irby RB, Mao WG, Coppola D, Kang J, Loubeau JM, Trudeau W et al. Activating SRC mutation in a subset of advanced human colon cancers. Nat Genet 1999; 21: 187–190.
  Article CAS PubMed Google Scholar
• Mao WG, Irby R, Coppola D, Fu L, Wloch M, Turner J et al. Activation of c-Src by receptor tyrosine kinases in human colon cancer cells with high metastatic potential. Oncogene 1997; 15: 3083–3090.
  Article CAS PubMed Google Scholar
• Biscardi JS, Tice DA, Parsons SJ . c-Src, receptor tyrosine kinases, and human cancer. Adv Cancer Res 1999; 76: 61–119.
  Article CAS PubMed Google Scholar
• Guo LW, Gao L, Rothschild J, Su B, Gelman IH . Control of protein kinase C activity, phorbol ester-induced cytoskeletal remodeling, and cell survival signals by the scaffolding protein SSeCKS/GRAVIN/AKAP12. J Biol Chem 2011; 286: 38356–38366.
  Article CAS PubMed PubMed Central Google Scholar
• Gelman IH, Lee K, Tombler E, Gordon R, Lin X . Control of cytoskeletal architecture by the _src_-suppressed C kinase substrate, SSeCKS. Cell Motil Cytoskeleton 1998; 41: 1–17.
  Article CAS PubMed Google Scholar
• Yeo MG, Partridge MA, Ezratty EJ, Shen Q, Gundersen GG, Marcantonio EE . Src SH2 arginine 175 is required for cell motility: specific focal adhesion kinase targeting and focal adhesion assembly function. Mol Cell Biol 2006; 26: 4399–4409.
  Article CAS PubMed PubMed Central Google Scholar
• Oneyama C, Hikita T, Enya K, Dobenecker MW, Saito K, Nada S et al. The lipid raft-anchored adaptor protein Cbp controls the oncogenic potential of c-Src. Mol Cell 2008; 30: 426–436.
  Article CAS PubMed Google Scholar
• Del Pozo MA, Balasubramanian N, Alderson NB, Kiosses WB, Grande-Garcia A, Anderson RG et al. Phospho-caveolin-1 mediates integrin-regulated membrane domain internalization. Nat Cell Biol 2005; 7: 901–908.
  Article CAS PubMed PubMed Central Google Scholar
• Humphries MJ. . (1998). Current Protocols in Cell Biology. Bonifacino JS, Dasso M, Harford JB, Lippincott-Schwartz J, Yamada K (eds) Wiley, New York, pp 9.1.1–9.1.11.
  Google Scholar
• Ross SH, Post A, Raaijmakers JH, Verlaan I, Gloerich M, Bos JL . Ezrin is required for efficient Rap1-induced cell spreading. J Cell Sci 2011; 124: 1808–1818.
  Article CAS PubMed Google Scholar
• Ory DS, Neugeboren BA, Mulligan RC . A stable human-derived packaging cell line for production of high titer retrovirus/vesicular stomatitis virus G pseudotypes. Proc Natl Acad Sci USA 1996; 93: 11400–11406.
  Article CAS PubMed PubMed Central Google Scholar
• Bu Y, Gelman IH . v-Src-mediated down-regulation of SSeCKS metastasis suppressor gene promoter by the recruitment of HDAC1 into a USF1-Sp1-Sp3 complex. J Biol Chem 2007; 282: 26725–26739.
  Article CAS PubMed Google Scholar
• Akakura S, Nochajski P, Gao L, Sotomayor P, Matsui S, Gelman IH . Rb-dependent cellular senescence, multinucleation and susceptibility to oncogenic transformation through PKC scaffolding by SSeCKS/AKAP12. Cell Cycle 2010; 9: 4656–4665.
  Article CAS PubMed PubMed Central Google Scholar
• Meng F, Sachs F . Orientation-based FRET sensor for real-time imaging of cellular forces. J Cell Sci 2012; 125: 743–750.
  Article CAS PubMed PubMed Central Google Scholar
• Li S, Seitz R, Lisanti MP . Phosphorylation of caveolin by src tyrosine kinases. The alpha-isoform of caveolin is selectively phosphorylated by v-Src in vivo. J Biol Chem 1996; 271: 3863–3868.
  Article CAS PubMed Google Scholar