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. 1996 Mar 2;132(6):1209–1221. doi: 10.1083/jcb.132.6.1209

Syndecan-1 mediates cell spreading in transfected human lymphoblastoid (Raji) cells

PMCID: PMC2120752  PMID: 8601596

Abstract

Syndecan-1 is a cell surface proteoglycan containing a highly conserved transmembrane and cytoplasmic domain, and an extracellular domain bearing heparan sulfate glycosaminoglycans. Through these domains, syndecan-1 is proposed to have roles in growth factor action, extracellular matrix adhesion, and cytoskeletal organization that controls cell morphology. To study the role of syndecan-1 in cell adhesion and cytoskeleton reorganization, mouse syndecan-1 cDNA was transfected into human Raji cells, a lymphoblastoid cell line that grows as suspended cells and exhibits little or no endogenous cell surface heparan sulfate. High expressing transfectants (Raji-Sl cells) bind to and spread on immobilized thrombospondin or fibronectin, which are ligands for the heparan sulfate chains of the proteoglycan. This binding and spreading as not dependent on the cytoplasmic domain of the core protein, is mutants expressing core proteins with cytoplasmic deletions maintain the ability to spread. The spreading is mediated through engagement of the syndecan-1 core protein, as the Raji-S 1 cells also bind to and spread on immobilized mAb 281.2, an antibody specific for the ectodomain of the syndecan-1 core protein. Spreading on the antibody is independent of the heparan sulfate glycosaminoglycan chains and can be inhibited by competition with soluble mAb 281.2. The spreading can be inhibited by treatment with cytochalasin D or colchicine. These data suggest that the core protein of syndecan-1 mediates spreading through the formation of a multimolecular signaling complex at the cell surface that signals cytoskeleton reorganization. This complex may form via intramembrane or extracellular interactions with the syndecan core protein.

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Selected References

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  1. Arkett S. A., Dixon S. J., Sims S. M. Lamellipod extension and K+ current in osteoclasts are regulated by different types of G proteins. J Cell Sci. 1994 Feb;107(Pt 2):517–526. [PubMed] [Google Scholar]
  2. Asundi V. K., Carey D. J. Self-association of N-syndecan (syndecan-3) core protein is mediated by a novel structural motif in the transmembrane domain and ectodomain flanking region. J Biol Chem. 1995 Nov 3;270(44):26404–26410. doi: 10.1074/jbc.270.44.26404. [DOI] [PubMed] [Google Scholar]
  3. Ballard L. L., Brown E. J., Holers V. M. Expression of the fibronectin receptor VLA-5 is regulated during human B cell differentiation and activation. Clin Exp Immunol. 1991 May;84(2):336–346. doi: 10.1111/j.1365-2249.1991.tb08170.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bernfield M., Kokenyesi R., Kato M., Hinkes M. T., Spring J., Gallo R. L., Lose E. J. Biology of the syndecans: a family of transmembrane heparan sulfate proteoglycans. Annu Rev Cell Biol. 1992;8:365–393. doi: 10.1146/annurev.cb.08.110192.002053. [DOI] [PubMed] [Google Scholar]
  5. Bershadsky A. D., Vaisberg E. A., Vasiliev J. M. Pseudopodial activity at the active edge of migrating fibroblast is decreased after drug-induced microtubule depolymerization. Cell Motil Cytoskeleton. 1991;19(3):152–158. doi: 10.1002/cm.970190303. [DOI] [PubMed] [Google Scholar]
  6. Boutin E. L., Sanderson R. D., Bernfield M., Cunha G. R. Epithelial-mesenchymal interactions in uterus and vagina alter the expression of the cell surface proteoglycan, syndecan. Dev Biol. 1991 Nov;148(1):63–74. doi: 10.1016/0012-1606(91)90317-v. [DOI] [PubMed] [Google Scholar]
  7. Carey D. J., Evans D. M., Stahl R. C., Asundi V. K., Conner K. J., Garbes P., Cizmeci-Smith G. Molecular cloning and characterization of N-syndecan, a novel transmembrane heparan sulfate proteoglycan. J Cell Biol. 1992 Apr;117(1):191–201. doi: 10.1083/jcb.117.1.191. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. 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. 1994 Jan;124(1-2):161–170. doi: 10.1083/jcb.124.1.161. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. 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. 1994 Sep;214(1):12–21. doi: 10.1006/excr.1994.1228. [DOI] [PubMed] [Google Scholar]
  10. Condeelis J. Life at the leading edge: the formation of cell protrusions. Annu Rev Cell Biol. 1993;9:411–444. doi: 10.1146/annurev.cb.09.110193.002211. [DOI] [PubMed] [Google Scholar]
  11. David G., Bernfield M. R. Collagen reduces glycosaminoglycan degradation by cultured mammary epithelial cells: possible mechanism for basal lamina formation. Proc Natl Acad Sci U S A. 1979 Feb;76(2):786–790. doi: 10.1073/pnas.76.2.786. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. 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. 1992 Aug;118(4):961–969. doi: 10.1083/jcb.118.4.961. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Drake S. L., Klein D. J., Mickelson D. J., Oegema T. R., Furcht L. T., McCarthy J. B. Cell surface phosphatidylinositol-anchored heparan sulfate proteoglycan initiates mouse melanoma cell adhesion to a fibronectin-derived, heparin-binding synthetic peptide. J Cell Biol. 1992 Jun;117(6):1331–1341. doi: 10.1083/jcb.117.6.1331. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Elenius K., Mättä A., Salmivirta M., Jalkanen M. Growth factors induce 3T3 cells to express bFGF-binding syndecan. J Biol Chem. 1992 Mar 25;267(9):6435–6441. [PubMed] [Google Scholar]
  15. Filardo E. J., Brooks P. C., Deming S. L., Damsky C., Cheresh D. A. Requirement of the NPXY motif in the integrin beta 3 subunit cytoplasmic tail for melanoma cell migration in vitro and in vivo. J Cell Biol. 1995 Jul;130(2):441–450. doi: 10.1083/jcb.130.2.441. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Gould S. E., Upholt W. B., Kosher R. A. Syndecan 3: a member of the syndecan family of membrane-intercalated proteoglycans that is expressed in high amounts at the onset of chicken limb cartilage differentiation. Proc Natl Acad Sci U S A. 1992 Apr 15;89(8):3271–3275. doi: 10.1073/pnas.89.8.3271. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Graham I. L., Anderson D. C., Holers V. M., Brown E. J. Complement receptor 3 (CR3, Mac-1, integrin alpha M beta 2, CD11b/CD18) is required for tyrosine phosphorylation of paxillin in adherent and nonadherent neutrophils. J Cell Biol. 1994 Nov;127(4):1139–1147. doi: 10.1083/jcb.127.4.1139. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. 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. 1994 Aug;126(3):811–819. doi: 10.1083/jcb.126.3.811. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Iida J., Meijne A. M., Spiro R. C., Roos E., Furcht L. T., McCarthy J. B. Spreading and focal contact formation of human melanoma cells in response to the stimulation of both melanoma-associated proteoglycan (NG2) and alpha 4 beta 1 integrin. Cancer Res. 1995 May 15;55(10):2177–2185. [PubMed] [Google Scholar]
  20. Jalkanen M., Elenius K., Salmivirta M. Syndecan--a cell surface proteoglycan that selectively binds extracellular effector molecules. Adv Exp Med Biol. 1992;313:79–85. doi: 10.1007/978-1-4899-2444-5_8. [DOI] [PubMed] [Google Scholar]
  21. Jalkanen M., Nguyen H., Rapraeger A., Kurn N., Bernfield M. Heparan sulfate proteoglycans from mouse mammary epithelial cells: localization on the cell surface with a monoclonal antibody. J Cell Biol. 1985 Sep;101(3):976–984. doi: 10.1083/jcb.101.3.976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Kato M., Saunders S., Nguyen H., Bernfield M. Loss of cell surface syndecan-1 causes epithelia to transform into anchorage-independent mesenchyme-like cells. Mol Biol Cell. 1995 May;6(5):559–576. doi: 10.1091/mbc.6.5.559. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Kim C. W., Goldberger O. A., Gallo R. L., Bernfield M. Members of the syndecan family of heparan sulfate proteoglycans are expressed in distinct cell-, tissue-, and development-specific patterns. Mol Biol Cell. 1994 Jul;5(7):797–805. doi: 10.1091/mbc.5.7.797. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Koda J. E., Rapraeger A., Bernfield M. Heparan sulfate proteoglycans from mouse mammary epithelial cells. Cell surface proteoglycan as a receptor for interstitial collagens. J Biol Chem. 1985 Jul 5;260(13):8157–8162. [PubMed] [Google Scholar]
  25. Kozma R., Ahmed S., Best A., Lim L. The Ras-related protein Cdc42Hs and bradykinin promote formation of peripheral actin microspikes and filopodia in Swiss 3T3 fibroblasts. Mol Cell Biol. 1995 Apr;15(4):1942–1952. doi: 10.1128/mcb.15.4.1942. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Lagenaur C., Lemmon V. An L1-like molecule, the 8D9 antigen, is a potent substrate for neurite extension. Proc Natl Acad Sci U S A. 1987 Nov;84(21):7753–7757. doi: 10.1073/pnas.84.21.7753. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Leppä S., Mali M., Miettinen H. M., Jalkanen M. Syndecan expression regulates cell morphology and growth of mouse mammary epithelial tumor cells. Proc Natl Acad Sci U S A. 1992 Feb 1;89(3):932–936. doi: 10.1073/pnas.89.3.932. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Liebersbach B. F., Sanderson R. D. Expression of syndecan-1 inhibits cell invasion into type I collagen. J Biol Chem. 1994 Aug 5;269(31):20013–20019. [PubMed] [Google Scholar]
  29. Mali M., Andtfolk H., Miettinen H. M., Jalkanen M. Suppression of tumor cell growth by syndecan-1 ectodomain. J Biol Chem. 1994 Nov 11;269(45):27795–27798. [PubMed] [Google Scholar]
  30. Marynen P., Zhang J., Cassiman J. J., Van den Berghe H., David G. Partial primary structure of the 48- and 90-kilodalton core proteins of cell surface-associated heparan sulfate proteoglycans of lung fibroblasts. Prediction of an integral membrane domain and evidence for multiple distinct core proteins at the cell surface of human lung fibroblasts. J Biol Chem. 1989 Apr 25;264(12):7017–7024. [PubMed] [Google Scholar]
  31. McLean I. W., Nakane P. K. Periodate-lysine-paraformaldehyde fixative. A new fixation for immunoelectron microscopy. J Histochem Cytochem. 1974 Dec;22(12):1077–1083. doi: 10.1177/22.12.1077. [DOI] [PubMed] [Google Scholar]
  32. Miettinen H. M., Edwards S. N., Jalkanen M. Analysis of transport and targeting of syndecan-1: effect of cytoplasmic tail deletions. Mol Biol Cell. 1994 Dec;5(12):1325–1339. doi: 10.1091/mbc.5.12.1325. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Neumann E., Schaefer-Ridder M., Wang Y., Hofschneider P. H. Gene transfer into mouse lyoma cells by electroporation in high electric fields. EMBO J. 1982;1(7):841–845. doi: 10.1002/j.1460-2075.1982.tb01257.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Nobes C. D., Hall A. Rho, rac, and cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia. Cell. 1995 Apr 7;81(1):53–62. doi: 10.1016/0092-8674(95)90370-4. [DOI] [PubMed] [Google Scholar]
  35. Numa F., Hirabayashi K., Tsunaga N., Kato H., O'Rourke K., Shao H., Stechmann-Lebakken C., Varani J., Rapraeger A., Dixit V. M. Elevated levels of syndecan-1 expression confer potent serum-dependent growth in human 293T cells. Cancer Res. 1995 Oct 15;55(20):4676–4680. [PubMed] [Google Scholar]
  36. PULVERTAFT J. V. A STUDY OF MALIGNANT TUMOURS IN NIGERIA BY SHORT-TERM TISSUE CULTURE. J Clin Pathol. 1965 May;18:261–273. doi: 10.1136/jcp.18.3.261. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Pierce A., Lyon M., Hampson I. N., Cowling G. J., Gallagher J. T. Molecular cloning of the major cell surface heparan sulfate proteoglycan from rat liver. J Biol Chem. 1992 Feb 25;267(6):3894–3900. [PubMed] [Google Scholar]
  38. Polliack A., Gamliel H., Ben Bassat H., Gurfel D., Leizerowitz R., Minowada J. Surface morphology and membrane phenotype of cultured human leukemia-lymphoma cells. A scanning electron microscopic study of 36 cell lines. Cancer. 1983 Jan 1;51(1):72–79. doi: 10.1002/1097-0142(19830101)51:1<72::aid-cncr2820510117>3.0.co;2-z. [DOI] [PubMed] [Google Scholar]
  39. Rapraeger A. C., Bernfield M. Heparan sulfate proteoglycans from mouse mammary epithelial cells. A putative membrane proteoglycan associates quantitatively with lipid vesicles. J Biol Chem. 1983 Mar 25;258(6):3632–3636. [PubMed] [Google Scholar]
  40. Rapraeger A. C. The coordinated regulation of heparan sulfate, syndecans and cell behavior. Curr Opin Cell Biol. 1993 Oct;5(5):844–853. doi: 10.1016/0955-0674(93)90034-n. [DOI] [PubMed] [Google Scholar]
  41. Rapraeger A., Jalkanen M., Bernfield M. Cell surface proteoglycan associates with the cytoskeleton at the basolateral cell surface of mouse mammary epithelial cells. J Cell Biol. 1986 Dec;103(6 Pt 2):2683–2696. doi: 10.1083/jcb.103.6.2683. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Rapraeger A., Jalkanen M., Endo E., Koda J., Bernfield M. The cell surface proteoglycan from mouse mammary epithelial cells bears chondroitin sulfate and heparan sulfate glycosaminoglycans. J Biol Chem. 1985 Sep 15;260(20):11046–11052. [PubMed] [Google Scholar]
  43. Reisman D., Sugden B. trans activation of an Epstein-Barr viral transcriptional enhancer by the Epstein-Barr viral nuclear antigen 1. Mol Cell Biol. 1986 Nov;6(11):3838–3846. doi: 10.1128/mcb.6.11.3838. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Richardson A., Parsons J. T. Signal transduction through integrins: a central role for focal adhesion kinase? Bioessays. 1995 Mar;17(3):229–236. doi: 10.1002/bies.950170309. [DOI] [PubMed] [Google Scholar]
  45. Ridley A. J., Hall A. The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors. Cell. 1992 Aug 7;70(3):389–399. doi: 10.1016/0092-8674(92)90163-7. [DOI] [PubMed] [Google Scholar]
  46. Ridley A. J., Paterson H. F., Johnston C. L., Diekmann D., Hall A. The small GTP-binding protein rac regulates growth factor-induced membrane ruffling. Cell. 1992 Aug 7;70(3):401–410. doi: 10.1016/0092-8674(92)90164-8. [DOI] [PubMed] [Google Scholar]
  47. Ridley R. C., Xiao H., Hata H., Woodliff J., Epstein J., Sanderson R. D. Expression of syndecan regulates human myeloma plasma cell adhesion to type I collagen. Blood. 1993 Feb 1;81(3):767–774. [PubMed] [Google Scholar]
  48. Rincon J., Prieto J., Patarroyo M. Expression of integrins and other adhesion molecules in Epstein-Barr virus-transformed B lymphoblastoid cells and Burkitt's lymphoma cells. Int J Cancer. 1992 May 28;51(3):452–458. doi: 10.1002/ijc.2910510319. [DOI] [PubMed] [Google Scholar]
  49. Salmivirta M., Elenius K., Vainio S., Hofer U., Chiquet-Ehrismann R., Thesleff I., Jalkanen M. Syndecan from embryonic tooth mesenchyme binds tenascin. J Biol Chem. 1991 Apr 25;266(12):7733–7739. [PubMed] [Google Scholar]
  50. Sanderson R. D., Bernfield M. Molecular polymorphism of a cell surface proteoglycan: distinct structures on simple and stratified epithelia. Proc Natl Acad Sci U S A. 1988 Dec;85(24):9562–9566. doi: 10.1073/pnas.85.24.9562. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Sanderson R. D., Lalor P., Bernfield M. B lymphocytes express and lose syndecan at specific stages of differentiation. Cell Regul. 1989 Nov;1(1):27–35. doi: 10.1091/mbc.1.1.27. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Sanderson R. D., Sneed T. B., Young L. A., Sullivan G. L., Lander A. D. Adhesion of B lymphoid (MPC-11) cells to type I collagen is mediated by integral membrane proteoglycan, syndecan. J Immunol. 1992 Jun 15;148(12):3902–3911. [PubMed] [Google Scholar]
  53. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Saunders S., Bernfield M. Cell surface proteoglycan binds mouse mammary epithelial cells to fibronectin and behaves as a receptor for interstitial matrix. J Cell Biol. 1988 Feb;106(2):423–430. doi: 10.1083/jcb.106.2.423. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Saunders S., Jalkanen M., O'Farrell S., Bernfield M. Molecular cloning of syndecan, an integral membrane proteoglycan. J Cell Biol. 1989 Apr;108(4):1547–1556. doi: 10.1083/jcb.108.4.1547. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Stanley M. J., Liebersbach B. F., Liu W., Anhalt D. J., Sanderson R. D. Heparan sulfate-mediated cell aggregation. Syndecans-1 and -4 mediate intercellular adhesion following their transfection into human B lymphoid cells. J Biol Chem. 1995 Mar 10;270(10):5077–5083. doi: 10.1074/jbc.270.10.5077. [DOI] [PubMed] [Google Scholar]
  57. Stossel T. P. From signal to pseudopod. How cells control cytoplasmic actin assembly. J Biol Chem. 1989 Nov 5;264(31):18261–18264. [PubMed] [Google Scholar]
  58. Sugden B., Marsh K., Yates J. A vector that replicates as a plasmid and can be efficiently selected in B-lymphoblasts transformed by Epstein-Barr virus. Mol Cell Biol. 1985 Feb;5(2):410–413. doi: 10.1128/mcb.5.2.410. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Sun X., Mosher D. F., Rapraeger A. Heparan sulfate-mediated binding of epithelial cell surface proteoglycan to thrombospondin. J Biol Chem. 1989 Feb 15;264(5):2885–2889. [PubMed] [Google Scholar]
  60. Sutherland A. E., Sanderson R. D., Mayes M., Seibert M., Calarco P. G., Bernfield M., Damsky C. H. Expression of syndecan, a putative low affinity fibroblast growth factor receptor, in the early mouse embryo. Development. 1991 Sep;113(1):339–351. doi: 10.1242/dev.113.1.339. [DOI] [PubMed] [Google Scholar]
  61. Takada Y., Huang C., Hemler M. E. Fibronectin receptor structures in the VLA family of heterodimers. Nature. 1987 Apr 9;326(6113):607–609. doi: 10.1038/326607a0. [DOI] [PubMed] [Google Scholar]
  62. Takada Y., Wayner E. A., Carter W. G., Hemler M. E. Extracellular matrix receptors, ECMRII and ECMRI, for collagen and fibronectin correspond to VLA-2 and VLA-3 in the VLA family of heterodimers. J Cell Biochem. 1988 Aug;37(4):385–393. doi: 10.1002/jcb.240370406. [DOI] [PubMed] [Google Scholar]
  63. Thesleff I., Jalkanen M., Vainio S., Bernfield M. Cell surface proteoglycan expression correlates with epithelial-mesenchymal interaction during tooth morphogenesis. Dev Biol. 1988 Oct;129(2):565–572. doi: 10.1016/0012-1606(88)90401-0. [DOI] [PubMed] [Google Scholar]
  64. Trautman M. S., Kimelman J., Bernfield M. Developmental expression of syndecan, an integral membrane proteoglycan, correlates with cell differentiation. Development. 1991 Jan;111(1):213–220. doi: 10.1242/dev.111.1.213. [DOI] [PubMed] [Google Scholar]
  65. Tremble P., Chiquet-Ehrismann R., Werb Z. The extracellular matrix ligands fibronectin and tenascin collaborate in regulating collagenase gene expression in fibroblasts. Mol Biol Cell. 1994 Apr;5(4):439–453. doi: 10.1091/mbc.5.4.439. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Vainio S., Jalkanen M., Thesleff I. Syndecan and tenascin expression is induced by epithelial-mesenchymal interactions in embryonic tooth mesenchyme. J Cell Biol. 1989 May;108(5):1945–1953. doi: 10.1083/jcb.108.5.1945. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Vainio S., Lehtonen E., Jalkanen M., Bernfield M., Saxén L. Epithelial-mesenchymal interactions regulate the stage-specific expression of a cell surface proteoglycan, syndecan, in the developing kidney. Dev Biol. 1989 Aug;134(2):382–391. doi: 10.1016/0012-1606(89)90110-3. [DOI] [PubMed] [Google Scholar]
  68. Wayner E. A., Garcia-Pardo A., Humphries M. J., McDonald J. A., Carter W. G. Identification and characterization of the T lymphocyte adhesion receptor for an alternative cell attachment domain (CS-1) in plasma fibronectin. J Cell Biol. 1989 Sep;109(3):1321–1330. doi: 10.1083/jcb.109.3.1321. [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. Werb Z., Tremble P. M., Behrendtsen O., Crowley E., Damsky C. H. Signal transduction through the fibronectin receptor induces collagenase and stromelysin gene expression. J Cell Biol. 1989 Aug;109(2):877–889. doi: 10.1083/jcb.109.2.877. [DOI] [PMC free article] [PubMed] [Google Scholar]
  70. Woods A., Couchman J. R., Johansson S., Hök M. Adhesion and cytoskeletal organisation of fibroblasts in response to fibronectin fragments. EMBO J. 1986 Apr;5(4):665–670. doi: 10.1002/j.1460-2075.1986.tb04265.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  71. Woods A., Couchman J. R. Syndecan 4 heparan sulfate proteoglycan is a selectively enriched and widespread focal adhesion component. Mol Biol Cell. 1994 Feb;5(2):183–192. doi: 10.1091/mbc.5.2.183. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. Yeaman C., Rapraeger A. C. Post-transcriptional regulation of syndecan-1 expression by cAMP in peritoneal macrophages. J Cell Biol. 1993 Aug;122(4):941–950. doi: 10.1083/jcb.122.4.941. [DOI] [PMC free article] [PubMed] [Google Scholar]

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