Fibronectin fibrillogenesis regulates three-dimensional neovessel formation

Genes and Development

Volumn 22, Issue 9, 2008, Pages 1231-1243

  Zhou, Xiaoming ^a   Rowe, R Grant ^a   Hiraoka, Nobuaki ^a   George, Jerry P ^b   Wirtz, Denis ^b   Mosher, Deane F ^c   Virtanen, Ismo ^d   Chernousov, Michael A ^e   Weiss, Stephen J ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b Johns Hopkins University   (United States)

^c UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^d UNIVERSITY OF HELSINKI   (Finland)

^e WEIS CENTER FOR RESEARCH   (United States)

Author keywords

Actomyosin; Angiogenesis; Endothelial cells; Extracellular matrix; Fibronectin

Indexed keywords

FIBRONECTIN; LIGAND; MYOSIN ADENOSINE TRIPHOSPHATASE;

ANGIOGENESIS; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOSKELETON; ENDOTHELIUM CELL; FIBER; HUMAN; HUMAN CELL; HUMAN TISSUE; NEOVASCULARIZATION (PATHOLOGY); NONHUMAN; PRIORITY JOURNAL; PROTEIN POLYMERIZATION; REGULATORY MECHANISM; VISCOELASTICITY;

CELL ADHESION; CELL CULTURE TECHNIQUES; CELLS, CULTURED; COLLAGEN TYPE I; CYTOSKELETON; ENDOTHELIAL CELLS; EXTRACELLULAR MATRIX; FIBRIN; FIBRONECTINS; GREEN FLUORESCENT PROTEINS; HEPATOCYTE GROWTH FACTOR; HUMANS; IMMUNOBLOTTING; MICROSCOPY, CONFOCAL; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; MYOSINS; NEOVASCULARIZATION, PHYSIOLOGIC; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; PROTEIN FOLDING; RECOMBINANT FUSION PROTEINS; TRANSFECTION; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VINCULIN;

EID: 43249124148     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.1643308     Document Type: Article

References (73)

1. Ambesi, A., Klein, R.M., Pumiglia, K.M., and McKeown-Longo, P.J. 2005. Anastellin, a fragment of the first type III repeat of fibronectin, inhibits extracellular signal-regulated kinase and causes G(1) arrest in human microvessel endothelial cells. Cancer Res. 65: 148-156.
2. Baneyx, G., Baugh, L., and Vogel, V. 2002. Fibronectin extension and unfolding within cell matrix fibrils controlled by cytoskeletal tension. Proc. Natl. Acad. Sci. 99: 5139-5143.
3. Beningo, K.A., Dembo, M., and Wang, Y.L. 2004. Responses of fibroblasts to anchorage of dorsal extracellular matrix receptors. Proc. Natl. Acad. Sci. 101: 18024-18029.
4. Ben-Ze'ev, A., Farmer, S.R., and Penman, S. 1980. Protein synthesis requires cell-surface contact while nuclear events respond to cell shape in anchorage-dependent fibroblasts. Cell 21: 365-372.
5. Bershadsky, A., Kozlov, M., and Geiger, B. 2006. Adhesion-mediated mechanosensitivity: A time to experiment, and a time to theorize. Curr. Opin. Cell Biol. 18: 472-481.
6. Bourdoulous, S., Orend, G., MacKenna, D.A., Pasqualini, R., and Ruoslahti, E. 1998. Fibronectin matrix regulates activation of RHO and CDC42 GTPases and cell cycle progression. J. Cell Biol. 143: 267-276.
7. Cai, Y., Biais, N., Giannone, G., Tanase, M., Jiang, G., Hofman, J.M., Wiggins, C.H., Silberzan, P., Buguin, A., Ladoux, B., et al. 2006. Nonmuscle myosin IIA-dependent force inhibits cell spreading and drives F-actin flow. Biophys. J. 91: 3907-3920.
8. Carmeliet, P. 2005. Angiogenesis in life, disease and medicine. Nature 438: 932-936.
9. Cavalcanti-Adam, E.A., Volberg, T., Micoulet, A., Kessler, H., Geiger, B., and Spatz, J.P. 2007. Cell spreading and focal adhesion dynamics are regulated by spacing of integrin ligands. Biophys. J. 92: 2964-2974.
10. Chen, C.S., Mrksich, M., Huang, S., Whitesides, G.M., and Ingber, D.E. 1997. Geometric control of cell life and death. Science 276: 1425-1428.
11. Chernousov, M.A., Fogerty, F.J., Koteliansky, V.E., and Mosher, D.F. 1991. Role of the I-9 and III-1 modules of fibronectin in formation of an extracellular fibronectin matrix. J. Biol. Chem. 266: 10851-10858.
12. Christopher, R.A., Kowalczyk, A.P., and McKeown-Longo, P.J. 1997. Localization of fibronectin matrix assembly sites on fibroblasts and endothelial cells. J. Cell Sci. 110: 569-581.
13. Chun, T.H., Sabeh, F., Ota, I., Murphy, H., McDonagh, K.T., Holmbeck, K., Birkedal-Hansen, H., Allen, E.D., and Weiss, S.J. 2004. MT1-MMP-dependent neovessel formation within the confines of the three-dimensional extracellular matrix. J. Cell Biol. 167: 757-767.
14. Chun, T.H., Hotary, K.B., Sabeh, F., Saltiel, A.R., Allen, E.D., and Weiss, S.J. 2006. A pericellular collagenase directs the 3-dimensional development of white adipose tissue. Cell 125: 577-591.
15. Clark, R.A., Quinn, J.H., Winn, H.J., Lanigan, J.M., Dellepella, P., and Colvin, R.B. 1982. Fibronectin is produced by blood vessels in response to injury. J. Exp. Med. 156: 646-651.
16. Clark, K., Langeslag, M., Figdor, C.G., and van Leeuwen, F.N. 2007. Myosin II and mechanotransduction: A balancing act. Trends Cell Biol. 17: 178-186.
17. Corbett, S.A. and Schwarzbauer, J.E. 1999. Requirements for α(5)β(1) integrin-mediated retraction of fibronectin-fibrin matrices. J. Biol. Chem. 274: 20943-20948.
18. Corson, L.B., Yamanaka, Y., Lai, K.M., and Rossant, J. 2003. Spatial and temporal patterns of ERK signaling during mouse embryogenesis. Development 130: 4527-4537.
19. Davidson, L.A., Keller, R., and DeSimone, D.W. 2004. Assembly and remodeling of the fibrillar fibronectin extracellular matrix during gastrulation and neurulation in Xenopus laevis. Dev. Dyn. 231: 888-895.
20. Debnath, J. and Brugge, J.S. 2005. Modelling glandular epithelial cancers in three-dimensional cultures. Nat. Rev. Cancer 5: 675-688.
21. Deroanne, C.F., Colige, A.C., Nusgens, B.V., and Lapiere, C.M. 1996. Modulation of expression and assembly of vinculin during in vitro fibrillar collagen-induced angiogenesis and its reversal. Exp. Cell Res. 224: 215-223.
22. Deroanne, C.F., Lapiere, C.M., and Nusgens, B.V. 2001. In vitro tubulogenesis of endothelial cells by relaxation of the coupling extracellular matrix-cytoskeleton. Cardiovasc. Res. 49: 647-658.
23. Discher, D.E., Janmey, P., and Wang, Y.L. 2005. Tissue cells feel and respond to the stiffness of their substrate. Science 310: 1139-1143.
24. Eliceiri, B.P., Klemke, R., Stromblad, S., and Cheresh, D.A. 1998. Integrin αvβ3 requirement for sustained mitogen-activated protein kinase activity during angiogenesis. J. Cell Biol. 140: 1255-1263.
25. Engler, A., Bacakova, L., Newman, C., Hategan, A., Griffin, M., and Discher, D. 2004. Substrate compliance versus ligand density in cell on gel responses. Biophys. J. 86: 617-628.
26. Engler, A.J., Sen, S., Sweeney, H.L., and Discher, D.E. 2006. Matrix elasticity directs stem cell lineage specification. Cell 126: 677-689.
27. Even-Ram, S., Doyle, A.D., Conti, M.A., Matsumoto, K., Adelstein, R.S., and Yamada, K.M. 2007. Myosin IIA regulates cell motility and actomyosin-microtubule crosstalk. Nat. Cell Biol. 9: 299-309.
28. Folkman, J. and Moscona, A. 1978. Role of cell shape in growth control. Nature 273: 345-349.
29. Francis, S.E., Goh, K.L., Hodivala-Dilke, K., Bader, B.L., Stark, M., Davidson, D., and Hynes, R.O. 2002. Central roles of α5β1 integrin and fibronectin in vascular development in mouse embryos and embryoid bodies. Arterioscler. Thromb. Vasc. Biol. 22: 927-933.
30. Galbraith, C.G., Yamada, K.M., and Galbraith, J.A. 2007. Polymerizing actin fibers position integrins primed to probe for adhesion sites. Science 315: 992-995.
31. Geiger, B., Bershadsky, A., Pankov, R., and Yamada, K.M. 2001. Transmembrane crosstalk between the extracellular matrix-cytoskeleton crosstalk. Nat. Rev. Mol. Cell Biol. 2: 793-805.
32. George, E.L., Georges-Labouesse, E.N., Patel-King, R.S., Rayburn, H., and Hynes, R.O. 1993. Defects in mesoderm, neural tube and vascular development in mouse embryos lacking fibronectin. Development 119: 1079-1091.
33. Georges, P.C. and Janmey, P.A. 2005. Cell type-specific response to growth on soft materials. J. Appl. Physiol. 98: 1547-1553.
34. Gui, L., Wojciechowski, K., Gildner, C.D., Nedelkovska, H., and Hocking, D.C. 2006. Identification of the heparin-binding determinants within fibronectin repeat III1: Role in cell spreading and growth. J. Biol. Chem. 281: 34816-34825.
35. Halliday, N.L. and Tomasek, J.J. 1995. Mechanical properties of the extracellular matrix influence fibronectin fibril assembly in vitro. Exp. Cell Res. 217: 109-117.
36. Hiraoka, N., Allen, E., Apel, I.J., Gyetko, M.R., and Weiss, S.J. 1998. Matrix metalloproteinases regulate neovascularization by acting as pericellular fibrinolysins. Cell 95: 365-377.
37. Hoang, M.V., Whelan, M.C., and Senger, D.R. 2004. Rho activity critically and selectively regulates endothelial cell organization during angiogenesis. Proc. Natl. Acad. Sci. 101: 1874-1879.
38. Hocking, D.C., Sottile, J., and Langenbach, K.J. 2000. Stimulation of integrin-mediated cell contractility by fibronectin polymerization. J. Biol. Chem. 275: 10673-10682.
39. Hotary, K.B., Allen, E.D., Brooks, P.C., Datta, N.S., Long, M.W., and Weiss, S.J. 2003. Membrane type I matrix metalloproteinase usurps tumor growth control imposed by the three-dimensional extracellular matrix. Cell 114: 33-45.
40. Huang, S., Chen, C.S., and Ingber, D.E. 1998. Control of cyclin D1, p27(Kip1), and cell cycle progression in human capillary endothelial cells by cell shape and cytoskeletal tension. Mol. Biol. Cell 9: 3179-3193.
41. Hynes, R.O. 2002. A reevaluation of integrins as regulators of angiogenesis. Nat. Med. 8: 918-921.
42. Hynes, R.O. and Zhao, Q. 2000. The evolution of cell adhesion. J. Cell Biol. 150: F89-F96. doi: 10.1083/jcb.150.2.F89.
43. Ingber, D.E. 2006. Cellular mechanotransduction: Putting all the pieces together again. FASEB J. 20: 811-827.
44. Jain, R.K. 2003. Molecular regulation of vessel maturation. Nat. Med. 9: 685-693.
45. Kim, S., Bell, K., Mousa, S.A., and Varner, J.A. 2000. Regulation of angiogenesis in vivo by ligation of integrin α5β1 with the central cell-binding domain of fibronectin. Am. J. Pathol. 156: 1345-1362.
46. Korff, T. and Augustin, H.G. 1998. Integration of endothelial cells in multicellular spheroids prevents apoptosis and induces differentiation. J. Cell Biol. 143: 1341-1352.
47. Larsen, M., Artym, V.V., Green, J.A., and Yamada, K.M. 2006. The matrix reorganized: Extracellular matrix remodeling and integrin signaling. Curr. Opin. Cell Biol. 18: 463-471.
48. Lee, J.S., Panorchan, P., Hale, C.M., Khatau, S.B., Kole, T.P., Tseng, Y., and Wirtz, D. 2006. Ballistic intracellular nanorheology reveals ROCK-hard cytoplasmic stiffening response to fluid flow. J. Cell Sci. 119: 1760-1768.
49. Mao, Y. and Schwarzbauer, J.E. 2005. Fibronectin fibrillogenesis, a cell-mediated matrix assembly process. Matrix Biol. 24: 389-399.
50. McBeath, R., Pirone, D.M., Nelson, C.M., Bhadriraju, K., and Chen, C.S. 2004. Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment. Dev. Cell 6: 483-495.
51. McKeown-Longo, P.J. and Mosher, D.F. 1985. Interaction of the 70,000-mol-wt amino-terminal fragment of fibronectin with the matrix-assembly receptor of fibroblasts. J. Cell Biol. 100: 364-374.
52. Mercurius, K.O. and Morla, A.O. 1998. Inhibition of vascular smooth muscle cell growth by inhibition of fibronectin matrix assembly. Circ. Res. 82: 548-556.
53. Meshel, A.S., Wei, Q., Adelstein, R.S., and Sheetz, M.P. 2005. Basic mechanism of three-dimensional collagen fibre transport by fibroblasts. Nat. Cell Biol. 7: 157-164.
54. Nelson, C.M. and Bissell, M.J. 2006. Of extracellular matrix, scaffolds, and signaling: Tissue architecture regulates development, homeostasis, and cancer. Annu. Rev. Cell Dev. Biol. 22: 287-309.
55. Neri, D. and Bicknell, R. 2005. Tumour vascular targeting. Nat. Rev. Cancer 5: 436-446.
56. Panorchan, P., Lee, J.S., Kole, T.P., Tseng, Y., and Wirtz, D. 2006. Microrheology and ROCK signaling of human endothelial cells embedded in a 3D matrix. Biophys. J. 91: 3499-3507.
57. Panorchan, P., Lee, J.S.H., Daniels, B.R., Kole, T.P., Tseng, Y., and Wirtz, D. 2007. Probing cellular mechanical responses to stimuli using ballistic intracellular nanorheology. Methods Cell Biol. 83: 115-140.
58. Risau, W. and Lemmon, V. 1988. Changes in the vascular extracellular matrix during embryonic vasculogenesis and angiogenesis. Dev. Biol. 125: 441-450.
59. Solon, J., Levental, I., Sengupta, K., Georges, P.C., and Janmey, P.A. 2007. Fibroblast adaptation and stiffness matching to soft elastic substrates. Biophys. J. 93: 4453-4461.
60. Sottile, J., Hocking, D.C., and Swiatek, P.J. 1998. Fibronectin matrix assembly enhances adhesion-dependent cell growth. J. Cell Sci. 111: 2933-2943.
61. Sottile, J., Hocking, D.C., and Langenbach, K.J. 2000. Fibronectin polymerization stimulates cell growth by RGD-dependent and -independent mechanisms. J. Cell Sci. 113: 4287-4299.
62. Takahashi, S., Leiss, M., Moser, M., Ohashi, T., Kitao, T., Heckmann, D., Pfeifer, A., Kessler, H., Takagi, J., Erickson, H.P., et al. 2007. The RGD motif in fibronectin is essential for development but dispensable for fibril assembly. J. Cell Biol. 178: 167-178.
63. Tan, J.L., Tien, J., Pirone, D.M., Gray, D.S., Bhadriraju, K., and Chen, C.S. 2003. Cells lying on a bed of microneedles: An approach to isolate mechanical force. Proc. Natl. Acad. Sci. 100: 1484-1489.
64. Tomasini-Johansson, B.R., Kaufman, N.R., Ensenberger, M.G., Ozeri, V., Hanski, E., and Mosher, D.F. 2001. A 49-residue peptide from adhesin F1 of Streptococcus pyogenes inhibits fibronectin matrix assembly. J. Biol. Chem. 276: 23430-23439.
65. Tomasini-Johansson, B.R., Annis, D.S., and Mosher, D.F. 2006. The N-terminal 70-kDa fragment of fibronectin binds to cell surface fibronectin assembly sites in the absence of intact fibronectin. Matrix Biol. 25: 282-293.
66. Tseng, Y., Kole, T.P., and Wirtz, D. 2002. Micromechanical mapping of live cells by multiple-particle-tracking microrheology. Biophys. J. 83: 3162-3176.
67. Velling, T., Risteli, J., Wennerberg, K., Mosher, D.F., and Johansson, S. 2002. Polymerization of type I and III collagens is dependent on fibronectin and enhanced by integrins α11β1 and α2β1. J. Biol. Chem. 277: 37377-37381.
68. Vogel, V. and Sheetz, M. 2006. Local force and geometry sensing regulate cell functions. Nat. Rev. Mol. Cell Biol. 7: 265-275.
69. Walpita, D. and Hay, E. 2002. Studying actin-dependent processes in tissue culture. Nat. Rev. Mol. Cell Biol. 3: 137-141.
70. Wu, C., Keivens, V.M., O'Toole, T.E., McDonald, J.A., and Ginsberg, M.H. 1995. Integrin activation and cytoskeletal interaction are essential for the assembly of a fibronectin matrix. Cell 83: 715-724.
71. Yamada, K.M. and Cukierman, E. 2007. Modeling tissue morphogenesis and cancer in 3D. Cell 130: 601-610.
72. Yoneda, A., Ushakov, D., Multhaupt, H.A., and Couchman, J.R. 2007. Fibronectin matrix assembly requires distinct contributions from Rho kinases I and II. Mol. Biol. Cell 18: 66-75.
73. Zhong, C., Chrzanowska-Wodnicka, M., Brown, J., Shaub, A., Belkin, A.M., and Burridge, K. 1998. Rho-mediated contractility exposes a cryptic site in fibronectin and induces fibronectin matrix assembly. J. Cell Biol. 141: 539-551.