Syndecan-1-mediated cell spreading requires signaling by αvβ3 integrins in human breast carcinoma cells

Experimental Cell Research

Volumn 286, Issue 2, 2003, Pages 219-232

  Beauvais, DeannaLee M ^a   Rapraeger, Alan C ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Adhesion; Carcinoma; Integrin; Proteoglycan; Syndecan

Indexed keywords

BETA1 INTEGRIN; BETA3 INTEGRIN; FIBRINOGEN; MANGANESE; MONOCLONAL ANTIBODY; PROTEIN; SYNDECAN 1; SYNDECAN 4; UNCLASSIFIED DRUG;

ARTICLE; BREAST CARCINOMA; CANCER CELL; CELL ADHESION; CELL SPREADING; HUMAN; HUMAN CELL; LIGAND BINDING; METASTASIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

MURINAE;

EID: 0037622031     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0014-4827(03)00126-5     Document Type: Article

References (78)

1. Roskelley C.D., Srebrow A., Bissell M.J. A hierarchy of ECM-mediated signalling regulates tissue-specific gene expression. Curr. Opin. Cell Biol. 7:1995;736-747.
2. Miranti C.K., Brugge J.S. Sensing the environment a historical perspective on integrin signal transduction . Nature Cell Biol. 4:2002;E83-E90.
3. Bernfield M., Gotte M., Park P.W., Reizes O., Fitzgerald M.L., Lincecum J., Zako M. Functions of cell surface heparan sulfate proteoglycans. Annu. Rev. Biochem. 68:1999;729-777.
4. Rapraeger A.C., Ott V.L. Molecular interactions of the syndecan core proteins. Curr. Opin. Cell Biol. 10:1998;620-628.
5. Rapraeger A.C. Syndecan-regulated receptor signaling. J. Cell Biol. 149:2000;995-998.
6. Couchman J.R., Chen L., Woods A. Syndecans and cell adhesion. Int. Rev. Cytol. 207:2001;113-150.
7. Klass C.M., Couchman J.R., Woods A. Control of extracellular matrix assembly by syndecan-2 proteoglycan. J. Cell Sci. 113:2000;493-506.
8. Woods A., Couchman J.R. Syndecan-4 and focal adhesion function. Curr. Opin. Cell Biol. 13:2001;578-583.
9. McFall A.J., Rapraeger A.C. Identification of an adhesion site within the syndecan-4 extracellular protein domain. J. Biol. Chem. 272:1997;12901-12904.
10. McFall A.J., Rapraeger A.C. Characterization of the high affinity cell-binding domain in the cell surface proteoglycan syndecan-4. J. Biol. Chem. 273:1998;28270-28276.
11. Woods A., Couchman J.R., Johansson S., Hook M. Adhesion and cytoskeletal organisation of fibroblasts in response to fibronectin fragments. EMBO J. 5:1986;665-670.
12. Izzard C.S., Radinsky R., Culp L.A. Substratum contacts and cytoskeletal reorganization of BALB/c 3T3 cells on a cell-binding fragment and heparin-binding fragments of plasma fibronectin. Exp. Cell Res. 165:1986;320-336.
13. Streeter H.B., Rees D.A. Fibroblast adhesion to RGDS shows novel features compared with fibronectin. J. Cell Biol. 105:1987;507-515.
14. Singer I.I., Kawka D.W., Scott S., Mumford R.A., Lark M.W. The fibronectin cell attachment sequence Arg-Gly-Asp-Ser promotes focal contact formation during early fibroblast attachment and spreading. J. Cell Biol. 104:1987;573-584.
15. Woods A., Couchman J.R. Syndecan 4 heparan sulfate proteoglycan is a selectively enriched and widespread focal adhesion component. Mol. Biol. Cell. 5:1994;183-192.
16. Saoncella S., Echtermeyer F., Denhez F., Nowlen J.K., Mosher D.F., Robinson S.D., Hynes R.O., Goetinck P.F. Syndecan-4 signals cooperatively with integrins in a Rho-dependent manner in the assembly of focal adhesions and actin stress fibers. Proc. Natl. Acad. Sci. USA. 96:1999;2805-2810.
17. Oh E.S., Woods A., Couchman J.R. Syndecan-4 proteoglycan regulates the distribution and activity of protein kinase C. J. Biol. Chem. 272:1997;8133-8136.
18. Oh E.S., Woods A., Couchman J.R. Multimerization of the cytoplasmic domain of syndecan-4 is required for its ability to activate protein kinase C. J. Biol. Chem. 272:1997;11805-11811.
19. Oh E.S., Woods A., Lim S.T., Theibert A.W., Couchman J.R. Syndecan-4 proteoglycan cytoplasmic domain and phosphatidylinositol 4,5-bisphosphate coordinately regulate protein kinase C activity. J. Biol. Chem. 273:1998;10624-10629.
20. Baciu P.C., Goetinck P.F. Protein kinase C regulates the recruitment of syndecan-4 into focal contacts. Mol. Biol. Cell. 6:1995;1503-1513.
21. Hansen C.A., Schroering A.G., Carey D.J., Robishaw J.D. Localization of a heterotrimeric G protein gamma subunit to focal adhesions and associated stress fibers. J. Cell Biol. 126:1994;811-819.
22. Carey D.J., Stahl R.C., Cizmeci-Smith G., Asundi V.K. Syndecan-1 expressed in Schwann cells causes morphological transformation and cytoskeletal reorganization and associates with actin during cell spreading. J. Cell Biol. 124:1994;161-170.
23. Carey D.J., Stahl R.C., Tucker B., Bendt K.A., Cizmeci-Smith G. Aggregation-induced association of syndecan-1 with microfilaments mediated by the cytoplasmic domain. Exp. Cell Res. 214:1994;12-21.
24. Liu W., Litwack E.D., Stanley M.J., Langford J.K., Lander A.D., Sanderson R.D. Heparan sulfate proteoglycans as adhesive and anti-invasive molecules. Syndecans and glypican have distinct functions. J. Biol. Chem. 273:1998;22825-22832.
25. Ohtake T., Fujimoto Y., Ikuta K., Saito H., Ohhira M., Ono M., Kohgo Y. Proline-rich antimicrobial peptide, PR-39 gene transduction altered invasive activity and actin structure in human hepatocellular carcinoma cells. Br. J. Cancer. 81:1999;393-403.
26. Lebakken C.S., Rapraeger A.C. Syndecan-1 mediates cell spreading in transfected human lymphoblastoid (Raji) cells. J. Cell Biol. 132:1996;1209-1221.
27. Granes F., Garcia R., Casaroli-Marano R.P., Castel S., Rocamora N., Reina M., Urena J.M., Vilaro S. Syndecan-2 induces filopodia by active cdc42Hs. Exp. Cell Res. 248:1999;439-456.
28. Yamashita Y., Oritani K., Miyoshi E.K., Wall R., Bernfield M., Kincade P.W. Syndecan-4 is expressed by B lineage lymphocytes and can transmit a signal for formation of dendritic processes. J. Immunol. 162:1999;5940-5948.
29. Iba K., Albrechtsen R., Gilpin B., Frohlich C., Loechel F., Zolkiewska A., Ishiguro K., Kojima T., Liu W., Langford J.K., Sanderson R.D., Brakebusch C., Fassler R., Wewer U.M. The cysteine-rich domain of human ADAM 12 supports cell adhesion through syndecans and triggers signaling events that lead to beta1 integrin-dependent cell spreading. J. Cell Biol. 149:2000;1143-1156.
30. Khan M.Y., Jaikaria N.S., Frenz D.A., Villanueva G., Newman S.A. Structural changes in the NH2-terminal domain of fibronectin upon interaction with heparin. Relationship to matrix-driven translocation. J. Biol. Chem. 263:1988;11314-11318.
31. Lebakken C.S., McQuade K.J., Rapraeger A.C. Syndecan-1 signals independently of betal integrins during Raji cell spreading. Exp. Cell Res. 259:2000;315-325.
32. David G., van der Schueren B., Marynen P., Cassiman J.J., van den Berghe H. Molecular cloning of amphiglycan, a novel integral membrane heparan sulfate proteoglycan expressed by epithelial and fibroblastic cells. J. Cell Biol. 118:1992;961-969.
33. Adams J.C., Kureishy N., Taylor A.L. A role for syndecan-1 in coupling fascin spike formation by thrombospondin-1. J. Cell Biol. 152:2001;1169-1182.
34. Woods A., Couchman J.R. Protein kinase C involvement in focal adhesion formation. J. Cell Sci. 101:1992;277-290.
35. Vuori K., Ruoslahti E. Activation of protein kinase C precedes alpha 5 beta 1 integrin-mediated cell spreading on fibronectin. J. Biol. Chem. 268:1993;21459-21462.
36. van der Pluijm G., Vloedgraven H., Papapoulos S., Lowick C., Grzesik W., Kerr J., Robey P.G. Attachment characteristics and involvement of integrins in adhesion of breast cancer cell lines to extracellular bone matrix components. Lab. Invest. 77:1997;665-675.
37. Humphries M.J. Integrin structure. Biochem. Soc. Trans. 28:2000;311-339.
38. Fernandez C., Clark K., Burrows L., Schofield N.R., Humphries M.J. Regulation of the extracellular ligand binding activity of integrins. Front. Biosci. 3:1998;D684-D700.
39. Takada Y., Puzon W. Identification of a regulatory region of integrin beta 1 subunit using activating and inhibiting antibodies. J. Biol. Chem. 268:1993;17597-17601.
40. Mould A.P., Akiyama S.K., Humphries M.J. The inhibitory anti-beta1 integrin monoclonal antibody 13 recognizes an epitope that is attenuated by ligand occupancy. Evidence for allosteric inhibition of integrin function. J. Biol. Chem. 271:1996;20365-20374.
41. Chandrasekaran S., Guo N.H., Rodrigues R.G., Kaiser J., Roberts D.D. Pro-adhesive and chemotactic activities of thrombospondin-1 for breast carcinoma cells are mediated by alpha3beta1 integrin and regulated by insulin-like growth factor-1 and CD98. J. Biol. Chem. 274:1999;11408-11416.
42. Berdichevsky F., Gilbert C., Shearer M., Taylor-Papadimitriou J. Collagen-induced rapid morphogenesis of human mammary epithelial cells the role of the alpha 2 beta 1 integrin . J. Cell Sci. 102:1992;437-446.
43. Zhang X.P., Puzon-McLaughlin W., Irie A., Kovach N., Prokopishyn N.L., Laferte S., Takeuchi K., Tsuji T., Takada Y. Alpha 3 beta 1 adhesion to laminin-5 and invasin critical and differential role of integrin residues clustered at the boundary between alpha 3 N-terminal repeats 2 and 3 . Biochemistry. 38:1999;14424-14431.
44. Burrows L., Clark K., Mould A.P., Humphries M.J. Fine mapping of inhibitory anti-alpha5 monoclonal antibody epitopes that differentially affect integrin-ligand binding. Biochem. J. 344:(Pt 2):1999;527-533.
45. Hangan D., Morris V.L., Boeters L., von Ballestrem C., Uniyal S., Chan B.M. An epitope on VLA-6 (alpha6beta1) integrin involved in migration but not adhesion is required for extravasation of murine melanoma B16F1 cells in liver. Cancer Res. 57:1997;3812-3817.
46. Smith J.W., Piotrowicz R.S., Mathis D. A mechanism for divalent cation regulation of beta 3-integrins. J. Biol. Chem. 269:1994;960-967.
47. Yamagata M., Suzuki S., Akiyama S.K., Yamada K.M., Kimata K. Regulation of cell-substrate adhesion by proteoglycans immobilized on extracellular substrates. J. Biol. Chem. 264:1989;8012-8018.
48. Makabe T., Saiki I., Murata J., Ohdate Y., Kawase Y., Taguchi Y., Shimojo T., Kimizuka F., Kato I., Azuma I. Modulation of haptotactic migration of metastatic melanoma cells by the interaction between heparin and heparin-binding domain of fibronectin. J. Biol. Chem. 265:1990;14270-14276.
49. Hayashi K., Madri J.A., Yurchenco P.D. Endothelial cells interact with the core protein of basement membrane perlecan through beta 1 and beta 3 integrins an adhesion modulated by glycosaminoglycan . J. Cell Biol. 119:1992;945-959.
50. Iida J., Meijne A.M., Oegema T.R. Jr., Yednock T.A., Kovach N.L., Furcht L.T., McCarthy J.B. A role of chondroitin sulfate glycosaminoglycan binding site in alpha4beta1 integrin-mediated melanoma cell adhesion. J. Biol. Chem. 273:1998;5955-5962.
51. Shimizu Y., Van Seventer G.A., Siraganian R., Wahl L., Shaw S. Dual role of the CD44 molecule in T cell adhesion and activation. J. Immunol. 143:1989;2457-2463.
52. Eisenmann K.M., McCarthy J.B., Simpson M.A., Keely P.J., Guan J.L., Tachibana K., Lim L., Manser E., Furcht L.T., Iida J. Melanoma chondroitin sulphate proteoglycan regulates cell spreading through Cdc42, Ack-1 and p130cas. Nature Cell Biol. 1:1999;507-513.
53. Baciu P.C., Saoncella S., Lee S.H., Denhez F., Leuthardt D., Goetinck P.F. Syndesmos, a protein that interacts with the cytoplasmic domain of syndecan-4, mediates cell spreading and actin cytoskeletal organization. J. Cell Sci. 113:2000;315-324.
54. Wilcox-Adelman S.A., Denhez F., Goetinck P.F. Syndecan-4 modulates focal adhesion kinase phosphorylation. J. Biol. Chem. 277:2002;32970-32977.
55. Horowitz A., Murakami M., Gao Y., Simons M. Phosphatidylinositol-4,5-bisphosphate mediates the interaction of syndecan-4 with protein kinase C. Biochemistry. 38:1999;15871-15877.
56. Adams J.C., Schwartz M.A. Stimulation of fascin spikes by thrombospondin-1 is mediated by the GTPases Rac and Cdc42. J. Cell Biol. 150:2000;807-822.
57. Loftus J.C., Liddington R.C. New insights into integrin-ligand interaction. J. Clin. Invest. 100:1997;S77-S81.
58. Lin E.C., Ratnikov B.I., Tsai P.M., Gonzalez E.R., McDonald S., Pelletier A.J., Smith J.W. Evidence that the integrin beta3 and beta5 subunits contain a metal ion-dependent adhesion site-like motif but lack an I domain. J. Biol. Chem. 272:1997;14236-14243.
59. Mould A.P., Askari J.A., Barton S., Kline A.D., McEwan P.A., Craig S.E., Humphries M.J. Integrin activation involves a conformational change in the alpha 1 helix of the beta subunit A-domain. J. Biol. Chem. 277:2002;19800-19805.
60. Masumoto A., Hemler M.E. Multiple activation states of VLA-4. Mechanistic differences between adhesion to CS1/fibronectin and to vascular cell adhesion molecule-1. J. Biol. Chem. 268:1993;228-234.
61. Masumoto A., Hemler M.E. Mutation of putative divalent cation sites in the alpha 4 subunit of the integrin VLA-4 distinct effects on adhesion to CS1/fibronectin, VCAM-1, and invasin . J. Cell. Biol. 123:1993;245-253.
62. Michishita M., Videm V., Arnaout M.A. A novel divalent cation-binding site in the A domain of the beta 2 integrin CR3 (CD11b/CD18) is essential for ligand binding. Cell. 72:1993;857-867.
63. Arroyo A.G., Garcia-Pardo A., Sanchez-Madrid F. A high affinity conformational state on VLA integrin heterodimers induced by an anti-beta 1 chain monoclonal antibody. J. Biol. Chem. 268:1993;9863-9868.
64. Pampori N., Hato T., Stupack D.G., Aidoudi S., Cheresh D.A., Nemerow G.R., Shattil S.J. Mechanisms and consequences of affinity modulation of integrin alpha(V)beta(3) detected with a novel patch-engineered monovalent ligand. J. Biol. Chem. 274:1999;21609-21616.
65. Hodivala-Dilke K.M., DiPersio C.M., Kreidberg J.A., Hynes R.O. Novel roles for alpha3beta1 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.
66. Blystone S.D., Slater S.E., Williams M.P., Crow M.T., Brown E.J. A molecular mechanism of integrin crosstalk alphavbeta3 suppression of calcium/calmodulin-dependent protein kinase II regulates alpha5beta1 function . J. Cell Biol. 145:1999;889-897.
67. Kiosses W.B., Shattil S.J., Pampori N., Schwartz M.A. Rac recruits high-affinity integrin alphavbeta3 to lamellipodia in endothelial cell migration. Nature Cell Biol. 3:2001;316-320.
68. Tomatis D., Echtermayer F., Schober S., Balzac F., Retta S.F., Silengo L., Tarone G. The muscle-specific laminin receptor alpha7 beta1 integrin negatively regulates alpha5 beta1 fibronectin receptor function. Exp. Cell Res. 246:1999;421-432.
69. Mackay D.J., Hall A. Rho GTPases. J. Biol. Chem. 273:1998;20685-20688.
70. Brooks P.C., Montgomery A.M., Rosenfeld M., Reisfeld R.A., Hu T., Klier G., Cheresh D.A. Integrin alpha v beta 3 antagonists promote tumor regression by inducing apoptosis of angiogenic blood vessels. Cell. 79:1994;1157-1164.
71. Domanico S.Z., Pelletier A.J., Havran W.L., Quaranta V. Integrin alpha 6A beta 1 induces CD81-dependent cell motility without engaging the extracellular matrix migration substrate. Mol. Biol. Cell. 8:1997;2253-2265.
72. Brassard D.L., Maxwell E., Malkowski M., Nagabhushan T.L., Kumar C.C., Armstrong L. Integrin alpha(v)beta(3)-mediated activation of apoptosis. Exp. Cell Res. 251:1999;33-45.
73. Kuzuya M., Satake S., Ramos M.A., Kanda S., Koike T., Yoshino K., Ikeda S., Iguchi A. Induction of apoptotic cell death in vascular endothelial cells cultured in three-dimensional collagen lattice. Exp. Cell Res. 248:1999;498-508.
74. Stupack D.G., Puente X.S., Boutsaboualoy S., Storgard C.M., Cheresh D.A. Apoptosis of adherent cells by recruitment of caspase-8 to unligated integrins. J. Cell Biol. 155:2001;459-470.
75. Thodeti C.K., Albrechtsen R., Grauslund M., Asmar M., Larsson C., Takada Y., Mercurio A.M., Couchman J.R., Wewer U.M. ADAM12/syndecan-4 signaling promotes beta 1 integrin-dependent cell spreading through protein kinase Calpha and Rho A. J. Biol. Chem. 278:2003;9576-9584.
76. Mould A.P., Akiyama S.K., Humphries M.J. Regulation of integrin alpha 5 beta 1-fibronectin interactions by divalent cations. Evidence for distinct classes of binding sites for Mn2+, Mg2+, and Ca2+. J. Biol. Chem. 270:1995;26270-26277.
77. Hu D.D., Barbas C.F., Smith J.W. An allosteric Ca2+ binding site on the beta3-integrins that regulates the dissociation rate for RGD ligands. J. Biol. Chem. 271:1996;21745-21751.
78. Porter J.C., Hogg N. Integrins take partners cross-talk between integrins and other membrane receptors . Trends Cell Biol. 8:1998;390-396.