Endothelial cell migration on RGD-peptide-containing PEG hydrogels in the presence of sphingosine 1-phosphate

Biophysical Journal

Volumn 94, Issue 1, 2008, Pages 273-285

  Wacker, Bradley K ^a   Alford, Shannon K ^a   Scott, Evan A ^a   Thakur, Meghna Das ^b,c   Longmore, Gregory D ^b,c   Elbert, Donald L ^a  

^a WASHINGTON UNIVERSITY IN ST LOUIS   (United States)

^b WASHINGTON UNIVERSITY   (United States)

^c WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARGINYLGLYCYLASPARTIC ACID; BETA1 INTEGRIN; BETA3 INTEGRIN; MACROGOL; SPHINGOSINE 1 PHOSPHATE;

ARTICLE; CELL ADHESION; CELL MIGRATION; CELL MOTILITY; CELL SIZE; CONTROLLED STUDY; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; HYDROGEL; PROTEIN BINDING; PROTEIN FUNCTION; SHEAR STRESS; STOCHASTIC MODEL;

EID: 37749039764     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.107.109074     Document Type: Article

References (88)

1. Bjornsson, T. D., M. Dryjski, J. Tluczek, R. Mennie, J. Ronan, T. N. Mellin, and K. A. Thomas. 1991. Acidic fibroblast growth factor promotes vascular repair. Proc. Natl. Acad. Sci. USA. 88:8651-8655.
2. Luscher, T. F., F. C. Tanner, M. R. Tschudi, and G. Noll. 1993. Endothelial dysfunction in coronary artery disease. Annu. Rev. Med. 44:395-418.
3. Strauss, B. H., R. J. Chisholm, F. W. Keeley, A. I. Gotlieb, R. A. Logan, and P. W. Armstrong. 1994. Extracellular matrix remodeling after balloon angioplasty injury in a rabbit model of restenosis. Circ. Res. 75:650-658.
4. Okura, H., S. Shimodozono, M. Hayase, H. N. Bonneau, P. G. Yock, and P. J. Fitzgerald. 2002. Impact of deep vessel wall injury and vessel stretching on subsequent arterial remodeling after balloon angioplasty: a serial intravascular ultrasound study. Am. Heart J. 144:323-328.
5. Wilensky, R. L., K. L. March, I. Gradus-Pizlo, G. Sandusky, N. Fineberg, and D. R. Hathaway. 1995. Vascular injury, repair, and restenosis after percutaneous transluminal angioplasty in the atherosclerotic rabbit. Circulation. 92:2995-3005.
6. Fischman, D. L., M. B. Leon, D. S. Baim, R. A. Schatz, M. P. Savage, I. Penn, K. Detre, L. Veltri, D. Ricci, M. Nobuyoshi, M. Cleman, R. Heuser, B. Almond, P. S. Teirstein, R. D. Fish, A. Colombo, J. Brinker, J. Moses, A. Shaknovich, J. Hirshfeld, S. Bailey, S. Ellis, R. Rake, and S. Goldberg. 1994. A randomized comparison of coronary-stent placement and balloon angioplasty in the treatment of coronary artery disease. N. Engl. J. Med. 331:496-501.
7. Serruys, P. W., P. de Jaegere, F. Kiemeneij, C. Macaya, W. Rutsch, G. Heyndrickx, H. Emanuelsson, J. Marco, V. Legrand, P. Materne, J. Belardi, U. Sigwart, A. Colombo, J. J. Goy, P. V. D. Heuvel, J. Delcan, and M. Morel. 1994. A comparison of balloon-expandable-stent implantation with balloon angioplasty in patients with coronary artery disease. N. Engl. J. Med. 331:489-495.
8. Chen, M. S., J. M. John, D. P. Chew, D. S. Lee, S. G. Ellis, and D. L. Bhatt. 2006. Bare metal stent restenosis is not a benign clinical entity. Am. Heart J. 151:1260-1264.
9. Liistro, F., G. Falsini, P. Angioli, K. Ducci, and L. Bolognese. 2006. Late acute thrombosis after implantation of sirolimus-eluting stent to treat in-stent restenosis. Acute Card. Care. 8:116-118.
10. Shuchman, M. 2006. Trading restenosis for thrombosis? New questions about drug-eluting stents. N. Engl. J. Med. 355:1949-1952.
11. Brewster, L., E. M. Brey, M. Addis, L. Xue, V. Husak, J. Ellinger, C. C. Haudenschild, and H. P. Greisler. 2006. Improving endothelial healing with novel chimeric mitogens. Am. J. Surg. 192:589-593.
12. Carnevale, K., K. Ouriel, Y. Gabriel, D. Clair, J. F. Bena, M. B. Silva, and T. P. Sarac. 2006. Biological coating for arterial stents: the next evolutionary change in stents. J. Endovasc. Ther. 13:164-174.
13. Van Belle, E., L. Maillard, F. O. Tio, and J. M. Isner. 1997. Accelerated endothelialization by local delivery of recombinant human vascular endothelial growth factor reduces in-stent intimal formation. Biochem. Biophys. Res. Commun. 235:311-316.
14. English, D., Z. Welch, A. T. Kovala, K. Harvey, O. V. Volpert, D. N. Brindley, and J. G. Garcia. 2000. Sphingosine 1-phosphate released from platelets during clotting accounts for the potent endothelial cell chemotactic activity of blood serum and provides a novel link between hemostasis and angiogenesis. FASEB J. 14:2255-2265.
15. Wacker, B. K., E. A. Scott, M. M. Kaneda, S. K. Alford, and D. L. Elbert. 2006. Delivery of sphingosine 1-phosphate from poly(ethylene glycol) hydrogels. Biomacromolecules. 7:1335-1343.
16. McVerry, B. J., and J. G. Garcia. 2005. In vitro and in vivo modulation of vascular barrier integrity by sphingosine 1-phosphate: mechanistic insights. Cell. Signal. 17:131-139.
17. Allende, M. L., T. Yamashita, and R. L. Proia. 2003. G-protein-coupled receptor S1P1 acts within endothelial cells to regulate vascular maturation. Blood. 102:3665-3667.
18. Paik, J. H., A. Skoura, S. S. Chae, A. E. Cowan, D. K. Han, R. L. Proia, and T. Hla. 2004. Sphingosine 1-phosphate receptor regulation of N-cadherin mediates vascular stabilization. Genes Dev. 18:2392-2403.
19. Tamama, K., H. Tomura, K. Sato, E. Malchinkhuu, A. Damirin, T. Kimura, A. Kuwabara, M. Murakami, and F. Okajima. 2005. Highdensity lipoprotein inhibits migration of vascular smooth muscle cells through its sphingosine 1-phosphate component. Atherosclerosis. 178:19-23.
20. DiMilla, P. A., K. Barbee, and D. A. Lauffenburger. 1991. Mathematical model for the effects of adhesion and mechanics on cell migration speed. Biophys. J. 60:15-37.
21. DiMilla, P. A., J. A. Stone, J. A. Quinn, S. M. Albelda, and D. A. Lauffenburger. 1993. Maximal migration of human smooth muscle cells on fibronectin and type IV collagen occurs at an intermediate attachment strength. J. Cell Biol. 122:729-737.
22. Goodman, S. L., G. Risse, and K. von der Mark. 1989. The E8 subfragment of laminin promotes locomotion of myoblasts over extracellular matrix. J. Cell Biol. 109:799-809.
23. Huttenlocher, A., M. H. Ginsberg, and A. F. Horwitz. 1996. Modulation of cell migration by integrin-mediated cytoskeletal linkages and ligand-binding affinity. J. Cell Biol. 134:1551-1562.
24. Palecek, S. P., J. C. Loftus, M. H. Ginsberg, D. A. Lauffenburger, and A. F. Horwitz. 1997. Integrin-ligand binding properties govern cell migration speed through cell-substratum adhesiveness. Nature. 385:537-540.
25. Bayless, K. J., and G. E. Davis. 2003. Sphingosine-1-phosphate markedly induces matrix metalloproteinase and integrin-dependent human endothelial cell invasion and lumen formation in three-dimensional collagen and fibrin matrices. Biochem. Biophys. Res. Commun. 312:903-913.
26. Endo, A., K. Nagashima, H. Kurose, S. Mochizuki, M. Matsuda, and N. Mochizuki. 2002. Sphingosine 1-phosphate induces membrane ruffling and increases motility of human umbilical vein endothelial cells via vascular endothelial growth factor receptor and CrkII. J. Biol. Chem. 277:23747-23754.
27. Kimura, T., T. Watanabe, K. Sato, J. Kon, H. Tomura, K. Tamama, A. Kuwabara, T. Kanda, I. Kobayashi, H. Ohta, M. Ui, and F. Okajima. 2000. Sphingosine 1-phosphate stimulates proliferation and migration of human endothelial cells possibly through the lipid receptors, Edg-1 and Edg-3. Biochem. J. 348:71-76.
28. Lee, H., E. J. Goetzl, and S. An. 2000. Lysophosphatidic acid and sphingosine 1-phosphate stimulate endothelial cell wound healing. Am. J. Physiol. Cell Physiol. 278:C612-C618.
29. Lee, O. H., D. J. Lee, Y. M. Kim, Y. S. Kim, H. J. Kwon, K. W. Kim, and Y. G. Kwon. 2000. Sphingosine 1-phosphate stimulates tyrosine phosphorylation of focal adhesion kinase and chemotactic motility of endothelial cells via the G(i) protein-linked phospholipase C pathway. Biochem. Biophys. Res. Commun. 268:47-53.
30. Morales-Ruiz, M., M. J. Lee, S. Zollner, J. P. Gratton, R. Scotland, I. Shiojima, K. Walsh, T. Hla, and W. C. Sessa. 2001. Sphingosine 1-phosphate activates Akt, nitric oxide production, and chemotaxis through a Gi protein/phosphoinositide 3-kinase pathway in endothelial cells. J. Biol. Chem. 276:19672-19677.
31. 1-containing integrins. J. Biol. Chem. 276:11830-11837.
32. Panetti, T. S. 2002. Differential effects of sphingosine 1-phosphate and lysophosphatidic acid on endothelial cells. Biochim. Biophys. Acta. 1582:190-196.
33. Wang, F., J. R. Van Brocklyn, J. P. Hobson, S. Movafagh, Z. Zukowska-Grojec, S. Milstien, and S. Spiegel. 1999. Sphingosine 1-phosphate stimulates cell migration through a G(i)-coupled cell surface receptor. Potential involvement in angiogenesis. J. Biol. Chem. 274:35343-35350.
34. Maheshwari, G., A. Wells, L. G. Griffith, and D. A. Lauffenburger. 1999. Biophysical integration of effects of epidermal growth factor and fibronectin on fibroblast migration. Biophys. J. 76:2814-2823.
35. Shikata, Y., K. G. Birukov, A. A. Birukova, A. Verin, and J. G. Garcia. 2003. Involvement of site-specific FAK phosphorylation in sphingosine-1 phosphate- and thrombin-induced focal adhesion remodeling: role of Src and GIT. FASEB J. 17:2240-2249.
36. Mattie, M., G. Brooker, and S. Spiegel. 1994. Sphingosine-1-phosphate, a putative second messenger, mobilizes calcium from internal stores via an inositol trisphosphate-independent pathway. J. Biol. Chem. 269:3181-3188.
37. 2+ mediates rac activation and adherens junction assembly in endothelial cells. J. Biol. Chem. 280:17320-17328.
38. Giannone, G., P. Ronde, M. Gaire, J. Beaudouin, J. Haiech, J. Ellenberg, and K. Takeda. 2004. Calcium rises locally trigger focal adhesion disassembly and enhance residency of focal adhesion kinase at focal adhesions. J. Biol. Chem. 279:28715-28723.
39. Ren, X. D., W. B. Kiosses, D. J. Sieg, C. A. Otey, D. D. Schlaepfer, and M. A. Schwartz. 2000. Focal adhesion kinase suppresses Rho activity to promote focal adhesion turnover. J. Cell Sci. 113:3673-3678.
40. Pierschbacher, M. D., and E. Ruoslahti. 1984. Cell attachment activity of fibronectin can be duplicated by small synthetic fragments of the molecule. Nature. 309:30-33.
41. Koivunen, E., B. Wang, and E. Ruoslahti. 1995. Phage libraries displaying cyclic peptides with different ring sizes: ligand specificities of the RGD-directed integrins. Biotechnology (N. Y.). 13:265-270.
42. Elbert, D. L., and J. A. Hubbell. 2001. Conjugate addition reactions combined with free-radical cross-linking for the design of materials for tissue engineering. Biomacromolecules. 2:430-441.
43. Liu, J. C., S. C. Heilshorn, and D. A. Tirrell. 2004. Comparative cell response to artificial extracellular matrix proteins containing the RGD and CS5 cell-binding domains. Biomacromolecules. 5:497-504.
44. Reyes, C. D., and A. J. Garcia. 2003. A centrifugation cell adhesion assay for high-throughput screening of biomaterial surfaces. J. Biomed. Mater. Res. A. 67:328-333.
45. Dunn, G. A. 1983. Characterising a kinesis response: time averaged measures of cell speed and directional persistence. Agents Actions Suppl. 12:14-33.
46. Harms, B. D., G. M. Bassi, A. R. Horwitz, and D. A. Lauffenburger. 2005. Directional persistence of EGF-induced cell migration is associated with stabilization of lamellipodial protrusions. Biophys. J. 88:1479-1488.
47. Othmer, H. G., S. R. Dunbar, and W. Alt. 1988. Models of dispersal in biological systems. J. Math. Biol. 26:263-298.
48. Smith, L. A., H. Aranda-Espinoza, J. B. Haun, and D. A. Hammer. 2007. Interplay between shear stress and adhesion on neutrophil locomotion. Biophys. J. 92:632-640.
49. Stokes, C. L., D. A. Lauffenburger, and S. K. Williams. 1991. Migration of individual microvessel endothelial cells: stochastic model and parameter measurement. J. Cell Sci. 99:419-430.
50. Rowan, T. H. 1990. Functional Stability Analysis of Numerical Algorithms. University of Texas at Austin, Austin, TX.
51. Deutschman, D. H., J. S. Carstens, R. L. Klepper, W. S. Smith, M. T. Page, T. R. Young, L. A. Gleason, N. Nakajima, and R. A. Sabbadini. 2003. Predicting obstructive coronary artery disease with serum sphingosine-1- phosphate. Am. Heart J. 146:62-68.
52. Murata, N., K. Sato, J. Kon, H. Tomura, M. Yanagita, A. Kuwabara, M. Ui, and F. Okajima. 2000. Interaction of sphingosine 1-phosphate with plasma components, including lipoproteins, regulates the lipid receptor-mediated actions. Biochem. J. 352:809-815.
53. Lee, O. H., Y. M. Kim, Y. M. Lee, E. J. Moon, D. J. Lee, J. H. Kim, K. W. Kim, and Y. G. Kwon. 1999. Sphingosine 1-phosphate induces angiogenesis: its angiogenic action and signaling mechanism in human umbilical vein endothelial cells. Biochem. Biophys. Res. Commun. 264:743-750.
54. Okamoto, H., Y. Yatomi, T. Ohmori, K. Satoh, Y. Matsumoto, and Y. Ozaki. 2000. Sphingosine 1-phosphate stimulates G(i)- and Rho-mediated vascular endothelial cell spreading and migration. Thromb. Res. 99:259-265.
55. Yatomi, Y., T. Ohmori, G. Rile, F. Kazama, H. Okamoto, T. Sano, K. Satoh, S. Kume, G. Tigyi, Y. Igarashi, and Y. Ozaki. 2000. Sphingosine 1-phosphate as a major bioactive lysophospholipid that is released from platelets and interacts with endothelial cells. Blood. 96:3431-3438.
56. Hughes, S. K., B. K. Wacker, M. M. Kaneda, and D. L. Elbert. 2005. Fluid shear stress modulates cell migration induced by sphingosine 1-phosphate and vascular endothelial growth factor. Ann. Biomed. Eng. 33:1003-1014.
57. Hsu, S., R. Thakar, D. Liepmann, and S. Li. 2005. Effects of shear stress on endothelial cell haptotaxis on micropatterned surfaces. Biochem. Biophys. Res. Commun. 337:401-409.
58. Li, S., N. F. Huang, and S. Hsu. 2005. Mechanotransduction in endothelial cell migration. J. Cell. Biochem. 96:1110-1126.
59. Sprague, E. A., J. Luo, and J. C. Palmaz. 2000. Endothelial cell migration onto metal stent surfaces under static and flow conditions. J. Long Term Eff. Med. Implants. 10:97-110.
60. Sprague, E. A., J. Luo, and J. C. Palmaz. 1997. Human aortic endothelial cell migration onto stent surfaces under static and flow conditions. J. Vasc. Interv. Radiol. 8:83-92.
61. Wojciak-Stothard, B., and A. J. Ridley. 2003. Shear stress-induced endothelial cell polarization is mediated by Rho and Rac but not Cdc42 or PI 3-kinases. J. Cell Biol. 161:429-439.
62. Reference deleted in proof.
63. Gupton, S. L., and C. M. Waterman-Storer. 2006. Spatiotemporal feedback between actomyosin and focal-adhesion systems optimizes rapid cell migration. Cell. 125:1361-1374.
64. Sahai, E., and C. J. Marshall. 2003. Differing modes of tumour cell invasion have distinct requirements for Rho/ROCK signalling and extracellular proteolysis. Nat. Cell Biol. 5:711-719.
65. Wang, Y., and P. Dimitrakopoulos. 2006. Nature of the hemodynamic forces exerted on vascular endothelial cells or leukocytes adhering to the surface of blood vessels. Phys. Fluids.:18:087107.
66. 3 integrin expression in normal and atherosclerotic artery. Circ. Res. 77:1129-1135.
67. 3) is implicated, in cooperation with P-selectin and platelet-activating factor, in the adhesion of monocytes to activated endothelial cells. Biochem. J. 304:537-542.
68. Conforti, G., A. Zanetti, S. Colella, M. Abbadini, P. C. Marchisio, R. Pytela, F. Giancotti, G. Tarone, L. R. Languino, and E. Dejana. 1989. Interaction of fibronectin with cultured human endothelial cells: characterization of the specific receptor. Blood. 73:1576-1585.
69. Suzuki, S., W. S. Argraves, H. Arai, L. R. Languino, M. D. Pierschbacher, and E. Ruoslahti. 1987. Amino acid sequence of the vitronectin receptor alpha subunit and comparative expression of adhesion receptor mRNAs. J. Biol. Chem. 262:14080-14085.
70. Urbich, C., D. H. Walter, A. M. Zeiher, and S. Dimmeler. 2000. Laminar shear stress upregulates integrin expression: role in endothelial cell adhesion and apoptosis. Circ. Res. 87:683-689.
71. Tzima, E., M. A. del Pozo, S. J. Shattil, S. Chien, and M. A. Schwartz. 2001. Activation of integrins in endothelial cells by fluid shear stress mediates Rho-dependent cytoskeletal alignment. EMBO J. 20:4639-4647.
72. Brooks, A. R., P. I. Lelkes, and G. M. Rubanyi. 2002. Gene expression profiling of human aortic endothelial cells exposed to disturbed flow and steady laminar flow. Physiol. Genomics. 9:27-41.
73. Diamond, M. S., and T. A. Springer. 1994. The dynamic regulation of integrin adhesiveness. Curr. Biol. 4:506-517.
74. 3 integrin to focal adhesions in endothelial cells: evidence for a role of phosphatidylinositol 3-kinase and Src. Thromb. Haemost. 92:151-161.
75. 3 to lamellipodia in endothelial cell migration. Nat. Cell Biol. 3:316-320.
76. Moon, J. J., M. Matsumoto, S. Patel, L. Lee, J. L. Guan, and S. Li. 2005. Role of cell surface heparan sulfate proteoglycans in endothelial cell migration and mechanotransduction. J. Cell. Physiol. 203:166-176.
77. 5 monoclonal antibody epitopes that differentially affect integrin-ligand binding. Biochem. J. 344:527-533.
78. Geiger, B., A. Bershadsky, R. Pankov, and K. M. Yamada. 2001. Transmembrane crosstalk between the extracellular matrix - cytoskeleton crosstalk. Nat. Rev. Mol. Cell Biol. 2:793-805.
79. Humphries, M. J., M. A. Travis, K. Clark, and A. P. Mould. 2004. Mechanisms of integration of cells and extracellular matrices by integrins. Biochem. Soc. Trans. 32:822-825.
80. Jin, Z. G., H. Ueba, T. Tanimoto, A. O. Lungu, M. D. Frame, and B. C. Berk. 2003. Ligand-independent activation of vascular endothelial growth factor receptor 2 by fluid shear stress regulates activation of endothelial nitric oxide synthase. Circ. Res. 93:354-363.
81. Gloe, T., and U. Pohl. 2002. Laminin binding conveys mechanosensing in endothelial cells. News Physiol. Sci. 17:166-169.
82. 3. J. Biol. Chem. 277:23453-23458.
83. 1. Arterioscler. Thromb. Vasc. Biol. 22:69-75.
84. Shikata, Y., K. G. Birukov, and J. G. Garcia. 2003. S1P induces FA remodeling in human pulmonary endothelial cells: role of Rac, GIT1, FAK, and paxillin. J. Appl. Physiol. 94:1193-1203.
85. Ridley, A. J., M. A. Schwartz, K. Burridge, R. A. Firtel, M. H. Ginsberg, G. Borisy, J. T. Parsons, and A. R. Horwitz. 2003. Cell migration: integrating signals from front to back. Science. 302:1704-1709.
86. Zhan, X., X. Hu, B. Hampton, W. H. Burgess, R. Friesel, and T. Maciag. 1993. Murine cortactin is phosphorylated in response to fibroblast growth factor-1 on tyrosine residues late in the G1 phase of the BALB/c 3T3 cell cycle. J. Biol. Chem. 268:24427-24431.
87. Cory, G. O., and A. J. Ridley. 2002. Cell motility: braking WAVEs. Nature. 418:732-733.
88. Lee, J. F., H. Ozaki, X. Zhan, E. Wang, T. Hla, and M. J. Lee. 2006. Sphingosine-1-phosphate signaling regulates lamellipodia localization of cortactin complexes in endothelial cells. Histochem. Cell Biol. 126:297-304.