The MSP receptor regulates α6β4 and α3β1 integrins via 14-3-3 proteins in keratinocyte migration

Developmental Cell

Volumn 5, Issue 2, 2003, Pages 257-271

  Santoro, Massimo M ^a,b   Gaudino, Giovanni ^a   Marchisio, Pier Carlo ^b  

^a UNIVERSITY OF EASTERN PIEDMONT   (Italy)

^b VITA SALUTE SAN RAFFAELE UNIVERSITY   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA6 INTEGRIN; BETA1 INTEGRIN; BETA4 INTEGRIN; GROWTH FACTOR RECEPTOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; KALININ; MACROPHAGE ACTIVATING FACTOR; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN 14 3 3; SYNAPTOPHYSIN; TYROSINE;

ARTICLE; BINDING SITE; CELL ADHESION; CELL MIGRATION; CELL SPREADING; CELL STRUCTURE; CELLULAR DISTRIBUTION; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME ACTIVATION; HEMIDESMOSOME; HUMAN; HUMAN CELL; KERATINOCYTE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; WOUND HEALING;

1-PHOSPHATIDYLINOSITOL 3-KINASE; 14-3-3 PROTEINS; BINDING SITES; CELL ADHESION MOLECULES; CELL LINE; CELL MOVEMENT; ENZYME ACTIVATION; HEPATOCYTE GROWTH FACTOR; HUMANS; INTEGRIN ALPHA3BETA1; INTEGRIN ALPHA6BETA4; KERATINOCYTES; NF-KAPPA B; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN KINASE C; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTOR PROTEIN-TYROSINE KINASES; SERINE; SIGNAL TRANSDUCTION; TWO-HYBRID SYSTEM TECHNIQUES; TYROSINE 3-MONOOXYGENASE; WOUND HEALING;

EID: 0042679580     PISSN: 15345807     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1534-5807(03)00201-6     Document Type: Article

References (45)

1. Aitken A. 14-3-3 and its possible role in co-ordinating multiple signalling pathways Trends Cell Biol. 6 1996 341-347
2. Alt A. Ohba M. Li L. Gartsbein M. Belanger A. Denning M.F. Kuroki T. Yuspa S.H. Tennenbaum T. Protein kinase Cδ-mediated phosphorylation of α6β4 is associated with reduced integrin localization to the HD and decreased keratinocyte attachment Cancer Res. 61 2001 4591-4598
3. Banu N. Price D.J. London R. Deng B. Mark M. Godowski P.J. Avraham H. Modulation of megakaryocytopoiesis by human macrophage-stimulating protein, the ligand for the RON receptor J. Immunol. 156 1996 2933-2940
4. Biffo S. Sanvito F. Costa S. Preve L. Pignatelli R. Spinardi R. Marchisio P.C. Isolation of a novel β 4 integrin-binding protein (p27(BBP)) highly expressed in epithelial cells J. Biol. Chem. 272 1997 30314-30321
5. Borradori L. Sonnenberg A. Structure and function of HDs: more than simple adhesion complexes J. Invest. Dermatol. 112 1999 411-418
6. Colognato H. Yurchenco P.D. Form and function: the laminin family of heterotrimers Dev. Dyn. 218 2000 213-234
7. Conejo R. de Alvaro C. Benito M. Cuadrado A. Lorenzo M. Insulin restores differentiation of Ras-transformed C2C12 myoblasts by inducing NF-κB through an AKT/P70S6K/p38-MAPK pathway Oncogene 21 2002 3739-3753
8. Cowin A.J. Kallincos N. Hatzirodos N. Robertson J.G. Pickering K.J. Couper J. Belford D.A. Hepatocyte growth factor and macrophage-stimulating protein are upregulated during excisional wound repair in rats Cell Tissue Res. 306 2001 239-250
9. Danilkovitch A. Donley S. Skeel A. Leonard E.J. Two independent signaling pathways mediate the antiapoptotic action of macrophage-stimulating protein on epithelial cells Mol. Cell. Biol. 20 2000 2218-2227
10. Dans M. Gagnoux-Palacios L. Bòaikie P. Klein S. Mariotti A. Giancotti F.G. Tyrosine phosphorylation of the β4 integrin cytoplasmic domain mediates Shc signaling to extracellular signal-regulated kinase and antagonizes formation of HDs J. Biol. Chem. 276 2001 1494-1502
11. Diaz-Gonzalez F. Forsyth J. Steiner B. Ginsberg M.H. Trans-dominant inhibition of integrin function Mol. Biol. Cell 7 1996 1939-1951
12. Follenzi A. Naldini L. HIV-based vectors: preparation and use Methods Mol. Med. 69 2002 259-274
13. Fuchs E. Dowling J. Segre J. Lo S.H. Yu Q.C. Integrators of epidermal growth and differentiation: distinct function for β1 and β4 integrins Curr. Opin. Genet. Dev. 7 1997 672-682
14. Gagnoux-Palacios L. Allegra M. Spirito F. Pommeret O. Romero C. Ortonne J.P. Meneguzzi G. The short arm of the laminin γ2 chain plays a pivotal role in the incorporation of laminin-5 into the extracellular matrix and in cell adhesion J. Cell Biol. 153 2001 835-849
15. Gaudino G. Follenzi A. Naldini L. Collesi C. Santoro M. Gallo K.A. Godowski P.J. Comoglio P.M. RON is a heterodimeric tyrosine kinase receptor activated by HGF homologue MSP EMBO J. 13 1994 3524-3532
16. Giancotti F.G. Ruoslahti E. Integrin signaling Science 285 1999 1028-1032
17. Goldfinger L.E. Hopkinson S.B. deHart G.W. Collawn S. Couchman J.R. Jones J.C. The α3 laminin subunit, α6β4 and α3β1 integrin coordinately regulate wound healing in cultured epithelial cells and the skin J. Cell Sci. 112 1999 2615-2629
18. Hintermann E. Bilban M. Sharabi A. Quaranta V. Inhibitory role of α6β4-associated erbB-2 and phosphoinositide 3-kinase in keratinocyte haptotactic migration dependent on α3β1 integrin J. Cell Biol. 153 2001 465-478
19. Hodivala-Dilke K.M. DiPersio C.M. Kreidberg J.A. Hynes R.O. Novel roles for α3β1 integrin as a regulator of cytoskeletal assembly and as a trans-dominant inhibitor of integrin receptor function in mouse keratinocytes J. Cell Biol. 142 1998 1357-1369
20. Kay B.K. Williamson M.P. Sudol M. The importance of being proline: the interaction of proline-rich motifs in signaling proteins with their cognate domains FASEB J. 14 2000 231-241
21. Kreidberg J.A. Functions of α3β1 integrin Curr. Opin. Cell Biol. 12 2000 548-553
22. Mainiero F. Pepe A. Wary K.K. Spinardi L. Mohammidi M. Schlessinger J. Giancotti F.G. Signal transduction by the α6β4 integrin: distinct β4 subunit sites mediate recruitment of Shc/Grb2 and association with the cytoskeleton of HDs EMBO J. 14 1995 4470-4481
23. Mariotti A. Kedeshian P.A. Dans M. Curatola A.M. Gagnoux-Palacios L. Giancotti F.G. EGF-R signaling through Fyn kinase disrupts the function of α6β4 at HDs: role in epithelial cell migration and carcinoma invasion J. Cell Biol. 155 2001 447-458
24. Martin P. Wound healing-aiming for perfect skin regeneration Science 276 1997 75-81
25. Mercurio A.M. Rabinovitz I. Shaw L.M. The α6β4 integrin and epithelial cell migration Curr. Opin. Cell Biol. 13 2001 541-545
26. Miranti C.K. Brugge J. Sensing the environment: a historical perspective on integrin signal transduction Nat. Cell Biol. 4 2002 83-90
27. Muslin A.J. Tanner J.W. Allen P.M. Shaw A.S. Interaction of 14-3-3 with signaling protein is mediated by the recognition of phosphoSer Cell 84 1996 889-897
28. Nanney L.B. Skeel A. Luan J. Polis S. Richmond A. Wang M.H. Leonard E.J. Proteolytic cleavage and activation of pro-macrophage-stimulating protein and upregulation of its receptor in tissue injury J. Invest. Dermatol. 111 1998 573-581
29. Nguyen B.P. Ryan M.C. Gil S.G. Carter W.G. Deposition of laminin 5 epidermal wounds regulates integrin signaling and adhesion Curr. Opin. Cell Biol. 12 2000 554-562
30. Olsen E. Rasmussen H.H. Celis J.E. Identification of proteins that are abnormally regulated in differentiated cultured human keratinocytes Electrophoresis 16 1995 2241-2248
31. Rabinovitz I. Toker A. Mercurio A.M. Protein kinase C-dependent mobilization of the α6β4 integrin from HDs and its association with actin-rich cell protrusions drive the chemotactic migration of carcinoma cells J. Cell Biol. 146 1999 1147-1160
32. Ravanti L. Kahari V.-M. Matrix metalloproteinases in wound repair Int. J. Mol. Med. 6 2000 391-407
33. Romashkova J.A. Makarov S.S. NF-κB is a target of AKT in anti-apoptotic PDGF signalling Nature 401 1999 86-90
34. Santoro M.M. Penengo L. Minetto M. Orecchia S. Cilli M. Gaudino G. Point mutations in the tyrosine kinase domain release the oncogenic and metastatic potential of the Ron receptor Oncogene 17 1998 741-749
35. Shang M. Koshikawa N. Schenk S. Quaranta V. The LG3 modules of laminin-5 harbors a binding site for integrin α3β1 that promotes cell adhesion, spreading and migration J. Biol. Chem. 276 2001 33045-33053
36. Shaw L.M. Rabinovitz I. Wang H.H. Toker A. Mercurio A.M. Activation of phosphoinositide 3-OH kinase by the α6β4 integrin promotes carcinoma invasion Cell 91 1997 949-960
37. Singer A.J. Clark R.A. Cutaneous wound healing N. Engl. J. Med. 341 1999 738-746
38. Skeel A. Leonard E.J. Action and target cell specificity of human macrophage-stimulating protein (MSP) J. Immunol. 152 1994 4618-4623
39. Tzivion G. Shen Y.H. Zhu J. 14-3-3 proteins, bringing new definitions to scaffolding Oncogene 20 2001 6331-6338
40. Wang M.H. Montero-Julian F.A. Dauny I. Leonard E.J. Requirement of phosphatidylinositol-3 kinase for epithelial cell migration activated by human macrophage stimulating protein Oncogene 13 1996 2167-2175
41. Wang M.H. Dlugosz A.A. Sun Y. Suda T. Skeel A. Leonard E.J. Macrophage-stimulating protein induces proliferation and migration of murine keratinocytes Exp. Cell Res. 226 1996 39-46
42. Yaffe M.B. Elia A.E. Phosphoserine/threonine-binding domains Curr. Opin. Cell Biol. 13 2001 131-138
43. Yaffe M.B. Rittinger K. Volinia S. Caron P.R. Aitken A. Leffers H. Gamblin S.J. Smerdon S.J. Cantley L.C. The structural basis for 14-3-3:phosphopeptide binding specificity Cell 91 1997 961-971
44. Yaffe M.B. Leparc G.G. Lai J. Obata T. Volinia S. Cantley L.C. A motif-based profile scanning approach for genome-wide prediction of signaling pathways Nat. Biotechnol. 19 2001 348-353
45. Zhang K. Kramer R.H. Laminin 5 deposition promotes keratinocyte motility Exp. Cell Res. 227 1996 309-322