Role of cell surface heparan sulfate proteoglycans in endothelial cell migration and mechanotransduction

Journal of Cellular Physiology

Volumn 203, Issue 1, 2005, Pages 166-176

  Moon, James J ^a   Matsumoto, Melissa ^a   Patel, Shyam ^a   Lee, Luke ^a   Guan, Jun Lin ^b   Li, Song ^a  

^a University of California at Berkeley   (United States)

^b Department of Obstetrics Gynecology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL SURFACE PROTEIN; FIBRONECTIN; FOCAL ADHESION KINASE; HEPARIN LYASE; PROTEOHEPARAN SULFATE;

ARTICLE; BINDING AFFINITY; CELL ADHESION; CELL MIGRATION; CELL SURFACE; ENDOTHELIUM CELL; ENZYME PHOSPHORYLATION; FOCAL ADHESION; MECHANOTRANSDUCTION; PRIORITY JOURNAL; PROTEIN INTERACTION; SHEAR STRESS; STRESS FIBER;

ANIMALS; AORTA; CATTLE; CELL ADHESION; CELL MOVEMENT; CELLS, CULTURED; ENDOTHELIUM, VASCULAR; FOCAL ADHESION PROTEIN-TYROSINE KINASES; HEPARAN SULFATE PROTEOGLYCANS; MECHANOTRANSDUCTION, CELLULAR; MEMBRANE PROTEINS; PERFUSION; PHOSPHORYLATION; POLYSACCHARIDE-LYASES; PROTEIN-TYROSINE KINASES; STRESS FIBERS; STRESS, MECHANICAL;

EID: 14744281839     PISSN: 00219541     EISSN: None     Source Type: Journal    
DOI: 10.1002/jcp.20220     Document Type: Article

References (71)

1. Albuquerque ML, Flozak AS. 2001. Patterns of living β-actin movement in wounded human coronary artery endothelial cells exposed to shear stress. Exp Cell Res 270(2):223-234.
2. Albuquerque ML, Waters CM, Savla U, Schnaper HW, Flozak AS. 2000. Shear stress enhances human endothelial cell wound closure in vitro. Am J Physiol Heart Circ Physiol 279(1):H293-H302.
3. Ando J, Nomura H, Kamiya A. 1987. The effect of fluid shear stress on the migration and proliferation of cultured endothelial cells. Microvasc Res 33(1):62-70.
4. Bernfield M, Gotte M, Park PW, Reizes O, Fitzgerald ML, Lincecum J, Zako M. 1999. Functions of cell surface heparan sulfate proteoglycans. Annu Rev Biochem 68:729-777.
5. Beyth RJ, Culp LA. 1984. Complementary adhesive responses of human skin fibroblasts to the cell-binding domain of fibronectin and the heparan sulfate-binding protein, platelet factor-4. Exp Cell Res 155(2):537-548.
6. Boardman KC, Swartz MA. 2003. Interstitial flow as a guide for lymphangiogenesis. Circ Res 92(7):801-808.
7. Branemark PI. 1965. Capillary form and function. The microcirculation of granulation tissue. Bibl Anat 7:9-28.
8. Burridge K, Turner CE, Romer LH. 1992. Tyrosine phosphorylation of paxillin and pp125FAK accompanies cell adhesion to extracellular matrix: A role in cytoskeletal assembly. J Cell Biol 119(4):893-903.
9. Cary LA, Han DC, Polte TR, Hanks SK, Guan JL. 1998. Identification of p130Cas as a mediator of focal adhesion kinase-promoted cell migration. J Cell Biol 140(1):211-221.
10. Cary LA, Han DC, Guan JL. 1999. Integrin-mediated signal transduction pathways. Histol Histopathol 14(3):1001-1009.
11. Chen Q, Kinch MS, Lin TH, Burridge K, Juliano RL. 1994. Integrin-mediated cell adhesion activates mitogen-activated protein kinases. J Biol Chem 269(43):26602-26605.
12. Couchman JR, Woods A. 1999. Syndecan-4 and integrins: Combinatorial signaling in cell adhesion. J Cell Sci 112(Pt 20):3415-3420.
13. De Cat B, David G. 2001. Developmental roles of the glypicans. Semin Cell Dev Biol 12(2):117-125.
14. Echtermeyer F, Streit M, Wilcox-Adelman S, Saonceila S, Denhez F, Detmar M, Goetinck P. 2001. Delayed wound repair and impaired angiogenesis in mice lacking syndecan-4. J Clin Invest 107(2):R9-R14.
15. Florian JA, Kosky JR, Ainslie K, Pang Z, Dull RO, Tarbell JM. 2003. Heparan sulfate proteoglycan is a mechanosensor on endothelial cells. Circ Res 93(10):e136-e42.
16. Fransson LA, Carlstedt I, Coster L, Malmstrom A. 1986. The functions of the heparan sulphate proteoglycans. Ciba Found Symp 124:125-142.
17. Hsu PP, Li S, Li YS, Usami S, Ratcliffe A, Wang X, Chien S. 2001. Effects of flow patterns on endothelial cell migration into a zone of mechanical denudation. Biochem Biophys Res Commun 285(3):751-759.
18. Hu YL, Li S, Miao H, Tsou TC, del Pozo MA, Chien S. 2002. Roles of microtubule dynamics and small GTPase rac in endothelial cell migration and lamellipodium formation under flow. J Vasc Res 39(6):465-476.
19. Iivanainen E, Kahari VM, Heino J, Elenius K. 2003. Endothelial cell-matrix interactions. Microsc Res Tech 60(1):13-22.
20. Ishiguro K, Kadomatsu K, Kojima T, Muramatsu H, Tsuzuki S, Nakamura E, Kusugami K, Saito H, Muramatsu T. 2000. Syndecan-4 deficiency impairs focal adhesion formation only under restricted conditions. J Biol Chem 275(8):5249-5252.
21. Jarvelainen H, Wight TN. 2002. Vascular proteoglycans. In: Garg HG, Roughley PJ, Hales CA, editors. Proteoglycans and lung disease. New York: Marcel Dekker. pp 291-321.
22. Jeong J, Han I, Lim Y, Kim J, Park I, Woods A, Couchman JR, Oh ES. 2001. Rat embryo fibroblasts require both the cell-binding and the heparin-binding domains of fibronectin for survival. Biochem J 356(Pt 2):531-537.
23. Kapila YL, Wang S, Johnson PW. 1999. Mutations in the heparin binding domain of fibronectin in cooperation with the V region induce decreases in pp125(FAK) levels plus proteoglycan-mediated apoptosis via caspases. J Biol Chem 274(43):30906-30913.
24. Karumanchi SA, Jha V, Ramchandran R, Karihaloo A, Tsiokas L, Chan B, Dhanabal M, Hanai JI, Venkataraman G, Shriver Z, Keiser N, Kalluri R, Zeng H, Mukhopadhyay D, Chen RL, Lander AD, Hagihara K, Yamaguchi Y, Sasisekharan R, Cantley L, Sukhatme VP. 2001. Cell surface glypicans are low-affinity endostatin receptors. Mol Cell 7(4):811-822.
25. Koo LY, Irvine DJ, Mayes AM, Lauffenburger DA, Griffith LG. 2002. Co-regulation of cell adhesion by nanoscale RGD organization and mechanical stimulus. J Cell Sci 115(Pt 7):1423-1433.
26. Lauffenburger DA, Horwitz AF. 1996. Cell migration: A physically integrated molecular process. Cell 84(3):359-369.
27. LeBaron HG, Esko JD, Woods A, Johansson S, Hook M. 1988. Adhesion of glycosaminoglycan-deficient chinese hamster ovary cell mutants to fibronectin substrata. J Cell Biol 106(3):945-952.
28. Li S, Chen BP, Azuma N, Hu YL, Wu SZ, Sumpio BE, Shyy JY, Chien S. 1999. Distinct roles for the small GTPases Cdc42 and Rho in endothelial responses to shear stress. J Clin Invest 103(8):1141-1150.
29. Li S, Butler P, Wang Y, Hu Y, Han DC, Usami S, Guan JL, Chien S. 2002. The role of the dynamics of focal adhesion kinase in the mechanotaxis of endothelial cells. Proc Natl Acad Sci USA 99(6):3546-3551.
30. Linhardt RJ, Turnbull JE, Wang HM, Loganathan D, Gallagher JT. 1990. Examination of the substrate specificity of heparin and heparan sulfate lyases. Biochemistry 29(10):2611-2617.
31. Longley RL, Woods A, Fleetwood A, Cowling GJ, Gallagher JT, Couchman JR. 1999. Control of morphology, cytoskeleton and migration by syndecan-4. J Cell Sci 112(Pt 20):3421-3431.
32. Luft JH. 1966. Fine structures of capillary and endocapillary layer as revealed by ruthenium red. Fed Proc 25(6):1773-1783.
33. Magnusson MK, Mosher DF. 1998. Fibronectin: Structure, assembly, and cardiovascular implications. Arterioscler Thromb Vasc Biol 18(9):1363-1370.
34. Marcum JA, Rosenberg RD. 1987. Anticoagulantly active heparan sulfate proteoglycan and the vascular endothelium. Semin Thromb Hemost 13(4):464-474.
35. Masuda M, Fujiwara K. 1993. The biased lamellipodium development and microtubule organizing center position in vascular endothelial cells migrating under the influence of fluid flow. Biol Cell 77(3):237-245.
36. Mathur AB, Truskey GA, Reichert WM. 2003. Synergistic effect of high-affinity binding and flow preconditioning on endothelial cell adhesion. J Biomed Mater Res 64A(1):155-163.
37. Mertens G, Cassiman JJ, Van den Berghe H, Vermylen J, David G. 1992. Cell surface heparan sulfate proteoglycans from human vascular endothelial cells. Core protein characterization and antithrombin III binding properties. J Biol Chem 267(28):20435-20443.
38. Mochizuki S, Vink H, Hiramatsu O, Kajita T, Shigeto F, Spaan JA, Kajiya F. 2003. Role of hyaluronic acid glycosaminoglycans in shear-induced endothelium-derived nitric oxide release. Am J Physiol Heart Circ Physiol 285(2):H722-H726.
39. Mohri H. 1997. Interaction of fibronectin with integrin receptors: Evidence by use of synthetic peptides. Peptides 18(6):899-907.
40. Moldovan NI, Goldschmidt-Clermont PJ, Parker-Thornburg J, Shapiro SD, Kolattukudy PE. 2000. Contribution of monocytes/macrophages to compensatory neovascularization: The drilling of metalloelastase-positive tunnels in ischemic myocardium. Circ Res 87(5):378-384.
41. Moyano JV, Carnemolla B, Albar JP, Leprini A, Gaggero B, Zardi L, Garcia-Pardo A. 1999. Cooperative role for activated α4 β1 integrin and chondroitin sulfate proteoglycans in cell adhesion to the heparin III domain of fibronectin. Identification of a novel heparin and cell binding sequence in repeat III5. J Biol Chem 274(1):135-142.
42. Rapraeger AC. 1993. The coordinated regulation of heparan sulfate, syndecans and cell behavior. Curr Opin Cell Biol 5(5):844-853.
43. Rapraeger AC, Krufka A, Olwin BB. 1991. Requirement of heparan sulfate for bFGF-mediated fibroblast growth and myoblast differentiation. Science 252(5013):1705-1708.
44. Romberger DJ. 1997. Fibronectin. Int J Biochem Cell Biol 29(7):939-943.
45. Ruoslahti E, Engvall E. 1997. Integrins and vascular extracellular matrix assembly. J Clin Invest 100(Suppl 11):S53-S56.
46. Ruoslahti E, Pierschbacher MD. 1987. New perspectives in cell adhesion: RGD and integrins. Science 238(4826):491-497.
47. Saksela O, Moscatelli D, Sommer A, Rifkin DB. 1988. Endothelial cell-derived heparan sulfate binds basic fibroblast growth factor and protects it from proteolytic degradation. J Cell Biol 107(2):743-751.
48. Saoncella S, Echtermeyer F, Denhez F, Nowlen JK, Mosher DF, Robinson SD, Hynes RO, Goetinck PF. 1999. 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(6):2805-2810.
49. Schlaepfer DD, Hanks SK, Hunter T, van der Geer P. 1994. Integrin-mediated signal transduction linked to Ras pathway by GRB2 binding to focal adhesion kinase. Nature 372(6508):786-791.
50. Schlaepfer DD, Hauck CR, Sieg DJ. 1999. Signaling through focal adhesion kinase. Prog Biophys Mol Biol 71(3-4):435-478.
51. Sharma A, Askari JA, Humphries MJ, Jones EY, Stuart DI. 1999. Crystal structure of a heparin- and integrin-binding segment of human fibronectin. EMBO J 18(6):1468-1479.
52. Sheetz MP, Felsenfeld DP, Galbraith CG. 1998. Cell migration: Regulation of force on extracellular-matrix-integrin complexes. Trends Cell Biol 8(2):51-54.
53. Sprague EA, Luo J, Palmaz JC. 1997. Human aortic endothelial cell migration onto stent surfaces under static and flow conditions. J Vasc Interv Radiol 83-92.
54. Squire JM, Chew M, Nneji G, Neal C, Barry J, Michel C. 2001. Quasi-periodic substructure in the microvessel endothelial glycocalyx: A possible explanation for molecular filtering? J Struct Biol 136(3):239-255.
55. Tanaka Y, Fujii K, Hubscher S, Aso M, Takazawa A, Saito K, Ota T, Eto S. 1998. Heparan sulfate proteoglycan on endothelium efficiently induces integrin-mediated T cell adhesion by immobilizing chemokines in patients with rheumatoid synovitis. Arthritis Rheum 41(8):1365-1377.
56. Urbich C, Dernbach E, Reissner A, Vasa M, Zeiher AM, Dimmeler S. 2002. Shear stress-induced endothelial cell migration involves integrin signaling via the fibronectin receptor subunits α5β1. Arterioscler Thromb Vasc Biol 22(1):69-75.
57. Usami S, Chen HH, Zhao Y, Chien S, Skalak R. 1993. Design and construction of a linear shear stress flow chamber. Ann Biomed Eng 21(1):77-83.
58. van Kooten TG, Schakenraad JM, van der Mei HC, Dekker A, Kirkpatrick CJ, Busscher HJ. 1994. Fluid shear induced endothelial cell detachment from glass - Influence of adhesion time and shear stress. Med Eng Phys 16(6):506-512.
59. Vink H, Duling BR. 1996. Identification of distinct luminal domains for macromolecules, erythrocytes, and leukocytes within mammalian capillaries. Circ Res 79(3):581-589.
60. Vuori K, Ruoslahti E. 1995. Tyrosine phosphorylation of p130Cas and cortactin accompanies integrin-mediated cell adhesion to extracellular matrix. J Biol Chem 270(38):22259-22262.
61. Weinbaum S, Zhang X, Han Y, Vink H, Cowin SC. 2003. Mechanotransduction and flow across the endothelial glycocalyx. Proc Natl Acad Sci USA 100(13):7988-7995.
62. Wojciak-Stothard B, Ridley AJ. 2003. Shear stress-induced endothelial cell polarization is mediated by Rho and Rac but not Cdc42 or PI 3-kinases. J Cell Biol 161(2):429-439.
63. Woods A, Couchman JR. 1994. Syndecan 4 heparan sulfate proteoglycan is a selectively enriched and widespread focal adhesion component. Mol Biol Cell 5(2):183-192.
64. Woods A, Couchman JR. 1998. Syndecans: Synergistic activators of cell adhesion. Trends Cell Biol 8(5):189-192.
65. Woods A, Couchman JR, Johansson S, Hook M. 1986. Adhesion and cytoskeletal organisation of fibroblasts in response to fibronectin fragments. EMBO J 5(4):665-670.
66. Woods A, McCarthy JB, Furcht LT, Couchman JR. 1993. A synthetic peptide from the COOH-terminal heparin-binding domain of fibronectin promotes focal adhesion formation. Mol Biol Cell 4(6):605-613.
67. Woods A, Longley RL, Tumova S, Couchman JR. 2000. Syndecan-4 binding to the high affinity heparin-binding domain of fibronectin drives focal adhesion formation in fibroblasts. Arch Biochem Biophys 374(1):66-72.
68. Yamashita Y, Oritani K, Miyoshi EK, Wall R, Bernfield M, Kincade PW. 1999. Syndecan-4 is expressed by B lineage lymphocytes and can transmit a signal for formation of dendritic processes. J Immunol 162(10):5940-5948.
69. Yayon A, Klagsbrun M, Esko JD, Leder P, Ornitz DM. 1991. Cell surface, heparin-like molecules are required for binding of basic fibroblast growth factor to its high affinity receptor. Cell 64(4):841-848.
70. Yoneda J, Saiki I, Igarashi Y, Kobayashi H, Fujii H, Ishizaki Y, Kimizuka F, Kato I, Azuma I. 1995. Role of the heparin-binding domain of chimeric peptides derived from fibronectin in cell spreading and motility. Exp Cell Res 217(1):169-179.
71. Zhu X, Assoian RK. 1995. Integrin-dependent activation of MAP kinase: A link to shape-dependent cell proliferation. Mol Biol Cell 6(3):273-282.