CCM1-ICAP-1 complex controls β1 integrin-dependent endothelial contractility and fibronectin remodeling

Journal of Cell Biology

Volumn 202, Issue 3, 2013, Pages 545-561

  Faurobert, Eva ^a,b,c   Rome, Claire ^a,c   Lisowska, Justyna ^a,b,c   Manet Dupé, Sandra ^a,b,c   Boulday, Gwénola ^d   Malbouyres, Marilyne ^g   Balland, Martial ^c,h   Bouin, Anne Pascale ^a,b,c   Kéramidas, Michelle ^a,c   Bouvard, Daniel ^a,b,c   Coll, Jean Luc ^a,c   Ruggiero, Florence ^g   Tournier Lasserve, Elisabeth ^d,e,f   Albiges Rizo, Corinne ^a,b,c  

^a INSTITUT ALBERT BONNIOT   (France)

^b CNRS   (France)

^c UNIV GRENOBLE ALPES   (France)

^d INSERM   (France)

^e UNIVERSITÉ PARIS DESCARTES   (France)

^f SAINT LOUIS HOSPITAL   (France)

^g Univ Lyon 1   (France)

^h LIPHY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BETA1 INTEGRIN; CEREBRAL CAVERNOUS MALFORMATION 1 PROTEIN; CEREBRAL CAVERNOUS MALFORMATION 2 PROTEIN; FIBRONECTIN; ICAP 1 PROTEIN; PROTEIN INHIBITOR; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD VESSEL COMPLIANCE; BLOOD VESSEL PERMEABILITY; CAVERNOUS HEMANGIOMA; CELL JUNCTION; CELL TENSION; COMPLEX FORMATION; CONTROLLED STUDY; ENDOTHELIUM CELL; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; KNOCKOUT MOUSE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; TENSION; TISSUE REPAIR; VASCULAR ENDOTHELIUM;

ANIMALS; ANTIGENS, CD29; CELL ADHESION; CELLS, CULTURED; FIBRONECTINS; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; MICE, INBRED STRAINS; MICE, KNOCKOUT; MICROTUBULE-ASSOCIATED PROTEINS; MODELS, BIOLOGICAL; PROTO-ONCOGENE PROTEINS;

EID: 84884217926     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201303044     Document Type: Article

References (80)

1. Abraham, S., N. Kogata, R. Fässler, and R.H. Adams, 2008. Integrin beta1 subunit controls mural cell adhesion, spreading, and blood vessel wall stability. Circ. Res. 102:562-570. http://dx.doi.org/10.1161/CIRCRESAHA .107.167908
2. Albigés-Rizo, C., P. Frachet, and M.R. Block. 1995. Down regulation of talin alters cell adhesion and the processing of the alpha 5 beta 1 integrin. J. Cell Sci. 108:3317-3329.
3. Atienza, J.M., N. Yu, S.L. Kirstein, B. Xi, X. Wang, X. Xu, and Y.A. Abassi. 2006. Dynamic and label-free cell-based assays using the real-time cell electronic sensing system. Assay Drug Dev. Technol. 4:597-607. http:// dx.doi.org/10.1089/adt.2006.4.597
4. Barkan, D., and A.F. Chambers. 2011. β1-integrin: a potential therapeutic target in the battle against cancer recurrence. Clin. Cancer Res. 17:7219-7223. http://dx.doi.org/10.1158/1078-0432.CCR-11-0642
5. Bazzoni, G., D.T. Shih, C.A. Buck, and M.E. Hemler. 1995. Monoclonal antibody 9EG7 defines a novel beta 1 integrin epitope induced by soluble ligand and manganese, but inhibited by calcium. J. Biol. Chem. 270:25570-25577. http://dx.doi.org/10.1074/jbc.270.30.17784
6. Béraud-Dufour, S., R. Gautier, C. Albiges-Rizo, P. Chardin, E. Faurobert, and S. Béraud-Dufour. 2007. Krit 1 interactions with microtubules and membranes are regulated by Rap1 and integrin cytoplasmic domain associated protein-1. FEBS J. 274:5518-5532. http://dx.doi.org/10.1111/j.1742-4658.2007.06068.x
7. Boettner, B., and L. Van Aelst. 2009. Control of cell adhesion dynamics by Rap1 signaling. Curr. Opin. Cell Biol. 21:684-693. http://dx.doi.org/10.1016/ j.ceb.2009.06.004
8. Booth, A.J., S.C. Wood, A.M. Cornett, A.A. Dreffs, G. Lu, A.F. Muro, E.S. White, and D.K. Bishop. 2012. Recipient-derived EDA fibronectin promotes cardiac allograft fibrosis. J. Pathol. 226:609-618. http://dx.doi .org/10.1002/path.3010
9. Borikova, A.L., C.F. Dibble, N. Sciaky, C.M. Welch, A.N. Abell, S. Bencharit, and G.L. Johnson. 2010. Rho kinase inhibition rescues the endothelial cell cerebral cavernous malformation phenotype. J. Biol. Chem. 285:11760-11764. http://dx.doi.org/10.1074/jbc.C109.097220
10. Boulday, G., A. Blécon, N. Petit, F. Chareyre, L.A. Garcia, M. Niwa-Kawakita, M. Giovannini, and E. Tournier-Lasserve. 2009. Tissue-specific conditional CCM2 knockout mice establish the essential role of endothelial CCM2 in angiogenesis: implications for human cerebral cavernous malformations. Dis. Model. Mech. 2:168-177. http://dx.doi.org/10.1242/dmm.001263
11. Boulday, G., N. Rudini, L. Maddaluno, A. Blécon, M. Arnould, A. Gaudric, F. Chapon, R.H. Adams, E. Dejana, and E. Tournier-Lasserve. 2011. Developmental timing of CCM2 loss influences cerebral cavernous malformations in mice. J. Exp. Med. 208:1835-1847. http://dx.doi.org/10.1084/jem.20110571
12. Bouvard, D., L. Vignoud, S. Dupé-Manet, N. Abed, H.N. Fournier, C. Vincent-Monegat, S.F. Retta, R. Fassler, and M.R. Block. 2003. Disruption of focal adhesions by integrin cytoplasmic domain-associated protein-1 alpha. J. Biol. Chem. 278:6567-6574. http://dx.doi.org/10.1074/jbc .M211258200
13. Bouvard, D., A. Millon-Fremillon, S. Dupe-Manet, M.R. Block, and C. Albiges-Rizo. 2006. Unraveling ICAP-1 function: toward a new direction? Eur. J. Cell Biol. 85:275-282. http://dx.doi.org/10.1016/j.ejcb.2005.10.005
14. Bouvard, D., A. Aszodi, G. Kostka, M.R. Block, C. Albigés-Rizo, and R. Fässler. 2007. Defective osteoblast function in ICAP-1-deficient mice. Development. 134:2615-2625. http://dx.doi.org/10.1242/dev.000877
15. Brunner, M., A. Millon-Frémillon, G. Chevalier, I.A. Nakchbandi, D. Mosher, M.R. Block, C. Albigés-Rizo, and D. Bouvard. 2011. Osteoblast mineralization requires beta1 integrin/ICAP-1-dependent fibronectin deposition. J. Cell Biol. 194:307-322. http://dx.doi.org/10.1083/jcb.201007108
16. Brütsch, R., S.S. Liebler, J. Wüstehube, A. Bartol, S.E. Herberich, M.G. Adam, A. Telzerow, H.G. Augustin, and A. Fischer. 2010. Integrin cytoplasmic domain-associated protein-1 attenuates sprouting angiogenesis. Circ. Res. 107:592-601. http://dx.doi.org/10.1161/CIRCRESAHA.110.217257
17. Burute, M., and M. Thery. 2012. Spatial segregation between cell-cell and cell-matrix adhesions. Curr. Opin. Cell Biol. 24:628-636. http://dx.doi .org/10.1016/j.ceb.2012.07.003
18. Chan, A.C., D.Y. Li, M.J. Berg, and K.J. Whitehead. 2010. Recent insights into cerebral cavernous malformations: animal models of CCM and the human phenotype. FEBS J. 277:1076-1083. http://dx.doi.org/10.1111/ j.1742-4658.2009.07536.x
19. Chan, A.C., S.G. Drakos, O.E. Ruiz, A.C. Smith, C.C. Gibson, J. Ling, S.F. Passi, A.N. Stratman, A. Sacharidou, M.P. Revelo, et al. 2011. Mutations in 2 distinct genetic pathways result in cerebral cavernous malformations in mice. J. Clin. Invest. 121:1871-1881. http://dx.doi .org/10.1172/JCI44393
20. Chang, D.D., C. Wong, H. Smith, and J. Liu. 1997. ICAP-1, a novel beta1 integrin cytoplasmic domain-associated protein, binds to a conserved and functionally important NPXY sequence motif of beta1 integrin. J. Cell Biol. 138:1149-1157. http://dx.doi.org/10.1083/jcb.138.5.1149
21. Clark, K., R. Pankov, M.A. Travis, J.A. Askari, A.P. Mould, S.E. Craig, P. Newham, K.M. Yamada, and M.J. Humphries. 2005. A specific alpha5beta1-integrin conformation promotes directional integrin translocation and fibronectin matrix formation. J. Cell Sci. 118:291-300. http://dx.doi.org/10.1242/jcs.01623
22. Clatterbuck, R.E., C.G. Eberhart, B.J. Crain, and D. Rigamonti. 2001. Ultrastructural and immunocytochemical evidence that an incompetent blood-brain barrier is related to the pathophysiology of cavernous malformations. J. Neurol. Neurosurg. Psychiatry. 71:188-192. http://dx.doi.org/10.1136/jnnp.71.2.188
23. Colombelli, J., A. Besser, H. Kress, E.G. Reynaud, P. Girard, E. Caussinus, U. Haselmann, J.V. Small, U.S. Schwarz, and E.H. Stelzer. 2009. Mechanosensing in actin stress fibers revealed by a close correlation between force and protein localization. J. Cell Sci. 122:1665-1679. http:// dx.doi.org/10.1242/jcs.042986
24. Cunningham, K., Y. Uchida, E. O'Donnell, E. Claudio, W. Li, K. Soneji, H. Wang, Y.S. Mukouyama, and U. Siebenlist. 2011. Conditional deletion of Ccm2 causes hemorrhage in the adult brain: a mouse model of human cerebral cavernous malformations. Hum. Mol. Genet. 20:3198-3206. http://dx.doi.org/10.1093/hmg/ddr225
25. DuFort, C.C., M.J. Paszek, and V.M. Weaver. 2011. Balancing forces: architectural control of mechanotransduction. Nat. Rev. Mol. Cell Biol. 12:308-319. http://dx.doi.org/10.1038/nrm3112
26. Edgell, C.J., C.C. McDonald, and J.B. Graham. 1983. Permanent cell line expressing human factor VIII-related antigen established by hybridization. Proc. Natl. Acad. Sci. USA. 80:3734-3737. http://dx.doi.org/10.1073/pnas.80.12.3734
27. Engvall, E., and E. Ruoslahti. 1977. Binding of soluble form of fibroblast surface protein, fibronectin, to collagen. Int. J. Cancer. 20:1-5. http://dx.doi .org/10.1002/ijc.2910200102
28. Faurobert, E., and C. Albiges-Rizo. 2010. Recent insights into cerebral cavernous malformations: a complex jigsaw puzzle under construction. FEBS J. 277:1084-1096. http://dx.doi.org/10.1111/j.1742-4658.2009.07537.x
29. Gaggioli, C., S. Hooper, C. Hidalgo-Carcedo, R. Grosse, J.F. Marshall, K. Harrington, and E. Sahai. 2007. Fibroblast-led collective invasion of carcinoma cells with differing roles for RhoGTPases in leading and following cells. Nat. Cell Biol. 9:1392-1400. http://dx.doi.org/10.1038/ncb1658
30. Glading, A., J. Han, R.A. Stockton, and M.H. Ginsberg. 2007. KRIT-1/CCM1 is a Rap1 effector that regulates endothelial cell cell junctions. J. Cell Biol. 179:247-254. http://dx.doi.org/10.1083/jcb.200705175
31. Goetz, J.G., S. Minguet, I. Navarro-Lérida, J.J. Lazcano, R. Samaniego, E. Calvo, M. Tello, T. Osteso-Ibáñez, T. Pellinen, A. Echarri, et al. 2011. Biomechanical remodeling of the microenvironment by stromal caveolin-1 favors tumor invasion and metastasis. Cell. 146:148-163. http://dx.doi.org/10.1016/j.cell.2011.05.040
32. Guilluy, C., V. Swaminathan, R. Garcia-Mata, E.T. O'Brien, R. Superfine, and K. Burridge. 2011. The Rho GEFs LARG and GEF-H1 regulate the mechanical response to force on integrins. Nat. Cell Biol. 13:722-727. http:// dx.doi.org/10.1038/ncb2254
33. Hilder, T.L., M.H. Malone, S. Bencharit, J. Colicelli, T.A. Haystead, G.L. Johnson, and C.C. Wu. 2007. Proteomic identification of the cerebral cavernous malformation signaling complex. J. Proteome Res. 6:4343-4355. http://dx.doi.org/10.1021/pr0704276
34. 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. http://dx.doi.org/10.1083/jcb.134.6.1551
35. Huveneers, S., and E.H. Danen. 2009. Adhesion signaling -crosstalk between integrins, Src and Rho. J. Cell Sci. 122:1059-1069. http://dx.doi.org/10.1242/jcs.039446
36. Huveneers, S., H. Truong, R. Fässler, A. Sonnenberg, and E.H. Danen. 2008. Binding of soluble fibronectin to integrin alpha5 beta1 -link to focal adhesion redistribution and contractile shape. J. Cell Sci. 121:2452-2462. http://dx.doi.org/10.1242/jcs.033001
37. Hynes, R.O. 2002. Integrins: bidirectional, allosteric signaling machines. Cell. 110:673-687. http://dx.doi.org/10.1016/S0092-8674(02)00971-6
38. Khan, M.M., C. Gandhi, N. Chauhan, J.W. Stevens, D.G. Motto, S.R. Lentz, and A.K. Chauhan. 2012. Alternatively-spliced extra domain A of fibronectin promotes acute inflammation and brain injury after cerebral ischemia in mice. Stroke. 43:1376-1382. http://dx.doi.org/10.1161/STROKEAHA.111.635516
39. Kleaveland, B., X. Zheng, J.J. Liu, Y. Blum, J.J. Tung, Z. Zou, S.M. Sweeney, M. Chen, L. Guo, M.M. Lu, et al. 2009. Regulation of cardiovascular development and integrity by the heart of glass-cerebral cavernous malformation protein pathway. Nat. Med. 15:169-176. http://dx.doi.org/10.1038/nm.1918
40. Krishnan, R., D.D. Klumpers, C.Y. Park, K. Rajendran, X. Trepat, J. van Bezu, V.W. van Hinsbergh, C.V. Carman, J.D. Brain, J.J. Fredberg, et al. 2011. Substrate stiffening promotes endothelial monolayer disruption through enhanced physical forces. Am. J. Physiol. Cell Physiol. 300:C146-C154. http://dx.doi.org/10.1152/ajpcell.00195.2010
41. Lampugnani, M.G., F. Orsenigo, N. Rudini, L. Maddaluno, G. Boulday, F. Chapon, and E. Dejana. 2010. CCM1 regulates vascular-lumen organization by inducing endothelial polarity. J. Cell Sci. 123:1073-1080. http://dx.doi.org/10.1242/jcs.059329
42. Larsen, M., V.V. Artym, J.A. Green, and K.M. Yamada. 2006. The matrix reorganized: extracellular matrix remodeling and integrin signaling. Curr. Opin. Cell Biol. 18:463-471. http://dx.doi.org/10.1016/j.ceb.2006.08.009
43. Lebrin, F., S. Srun, K. Raymond, S. Martin, S. van den Brink, C. Freitas, C. Breant, T. Mathivet, B. Larrivee, J.-L. Thomas, et al. 2010. Thalidomide stimulates vessel maturation and reduces epistaxis in individuals with hereditary hemorrhagic telangiectasia. Nat. Med. 16:420-428.
44. Lemmon, C.A., C.S. Chen, and L.H. Romer. 2009. Cell traction forces direct fibronectin matrix assembly. Biophys. J. 96:729-738. http://dx.doi.org/10.1016/j.bpj.2008.10.009
45. Liu, W., K.M. Draheim, R. Zhang, D.A. Calderwood, and T.J. Boggon. 2013. Mechanism for KRIT1 release of ICAP1-mediated suppression of integrin activation. Mol. Cell. 49:719-729. http://dx.doi.org/10.1016/j.molcel.2012.12.005
46. Maruthamuthu, V., B. Sabass, U.S. Schwarz, and M.L. Gardel. 2011. Cell-ECM traction force modulates endogenous tension at cell-cell contacts. Proc. Natl. Acad. Sci. USA. 108:4708-4713. http://dx.doi.org/10.1073/pnas.1011123108
47. McDonald, D.A., R. Shenkar, C. Shi, R.A. Stockton, A.L. Akers, M.H. Kucherlapati, R. Kucherlapati, J. Brainer, M.H. Ginsberg, I.A. Awad, and D.A. Marchuk. 2011. A novel mouse model of cerebral cavernous malformations based on the two-hit mutation hypothesis recapitulates the human disease. Hum. Mol. Genet. 20:211-222. http://dx.doi.org/10.1093/hmg/ddq433
48. McDonald, D.A., C. Shi, R. Shenkar, R.A. Stockton, F. Liu, M.H. Ginsberg, D.A. Marchuk, and I.A. Awad. 2012. Fasudil decreases lesion burden in a murine model of cerebral cavernous malformation disease. Stroke. 43:571-574. http://dx.doi.org/10.1161/STROKEAHA.111.625467
49. Mehta, D., and A.B. Malik. 2006. Signaling mechanisms regulating endothelial permeability. Physiol. Rev. 86:279-367. http://dx.doi.org/10.1152/physrev .00012.2005
50. Mettouchi, A. 2012. The role of extracellular matrix in vascular branching morphogenesis. Cell Adhes. Migr. 6:528-534. http://dx.doi.org/10.4161/cam.22862
51. Millon-Frémillon, A., D. Bouvard, A. Grichine, S. Manet-Dupé, M.R. Block, C. Albiges-Rizo, A. Millon-Frémillon, and S. Manet-Dupé. 2008. Cell adaptive response to extracellular matrix density is controlled by ICAP-1-dependent beta1-integrin affinity. J. Cell Biol. 180:427-441. http://dx.doi .org/10.1083/jcb.200707142
52. Pagenstecher, A., S. Stahl, U. Sure, and U. Felbor. 2009. A two-hit mechanism causes cerebral cavernous malformations: complete inactivation of CCM1, CCM2 or CCM3 in affected endothelial cells. Hum. Mol. Genet. 18:911-918.
53. Papusheva, E., and C.-P. Heisenberg. 2010. Spatial organization of adhesion: force-dependent regulation and function in tissue morphogenesis. EMBO J. 29:2753-2768. http://dx.doi.org/10.1038/emboj.2010.182
54. Parsons, J.T., A.R. Horwitz, and M.A. Schwartz. 2010. Cell adhesion: integrating cytoskeletal dynamics and cellular tension. Nat. Rev. Mol. Cell Biol. 11:633-643. http://dx.doi.org/10.1038/nrm2957
55. Provenzano, P.P., D.R. Inman, K.W. Eliceiri, S.M. Trier, and P.J. Keely. 2008. Contact guidance mediated three-dimensional cell migration is regulated by Rho/ROCK-dependent matrix reorganization. Biophys. J. 95:5374-5384. http://dx.doi.org/10.1529/biophysj.108.133116
56. Riant, F., F. Bergametti, X. Ayrignac, G. Boulday, and E. Tournier-Lasserve. 2010. Recent insights into cerebral cavernous malformations: the molecular genetics of CCM. FEBS J. 277:1070-1075. http://dx.doi.org/10.1111/j.1742-4658.2009.07535.x
57. Rybak, J.-N., C. Roesli, M. Kaspar, A. Villa, and D. Neri. 2007. The extra-domain A of fibronectin is a vascular marker of solid tumors and metastases. Cancer Res. 67:10948-10957. http://dx.doi.org/10.1158/0008-5472.CAN-07-1436
58. Schwarzbauer, J.E., and D.W. DeSimone. 2011. Fibronectins, their fibrillogenesis, and in vivo functions. Cold Spring Harb. Perspect. Biol. 3. http://dx.doi.org/10.1101/cshperspect.a005041
59. Singh, P., C. Carraher, and J.E. Schwarzbauer. 2010. Assembly of fibronectin extracellular matrix. Annu. Rev. Cell Dev. Biol. 26:397-419. http://dx.doi .org/10.1146/annurev-cellbio-100109-104020
60. Sottile, J., and D.C. Hocking. 2002. Fibronectin polymerization regulates the composition and stability of extracellular matrix fibrils and cell-matrix adhesions. Mol. Biol. Cell. 13:3546-3559. http://dx.doi.org/10.1091/mbc.E02-01-0048
61. Sottile, J., F. Shi, I. Rublyevska, H.Y. Chiang, J. Lust, and J. Chandler. 2007. Fibronectin-dependent collagen I deposition modulates the cell response to fibronectin. Am. J. Physiol. Cell Physiol. 293:C1934-C1946. http://dx.doi.org/10.1152/ajpcell.00130.2007
62. Stockton, R.A., R. Shenkar, I.A. Awad, and M.H. Ginsberg. 2010. Cerebral cavernous malformations proteins inhibit Rho kinase to stabilize vascular integrity. J. Exp. Med. 207:881-896. http://dx.doi.org/10.1084/jem.20091258
63. Stratman, A.N., K.M. Malotte, R.D. Mahan, M.J. Davis, and G.E. Davis. 2009. Pericyte recruitment during vasculogenic tube assembly stimulates endothelial basement membrane matrix formation. Blood. 114:5091-5101. http://dx.doi.org/10.1182/blood-2009-05-222364
64. Theodossiou, T.A., C. Thrasivoulou, C. Ekwobi, and D.L. Becker. 2006. Second harmonic generation confocal microscopy of collagen type I from rat tendon cryosections. Biophys. J. 91:4665-4677. http://dx.doi.org/10 .1529/biophysj.106.093740
65. Tomasini-Johansson, B.R., N.R. Kaufman, M.G. Ensenberger, V. Ozeri, E. Hanski, and D.F. Mosher. 2001. A 49-residue peptide from adhesin F1 of Streptococcus pyogenes inhibits fibronectin matrix assembly. J. Biol. Chem. 276:23430-23439. http://dx.doi.org/10.1074/jbc.M103467200
66. Tseng, Q., I. Wang, E. Duchemin-Pelletier, A. Azioune, N. Carpi, J. Gao, O. Filhol, M. Piel, M. Théry, and M. Balland. 2011. A new micropatterning method of soft substrates reveals that different tumorigenic signals can promote or reduce cell contraction levels. Lab Chip. 11:2231-2240. http://dx.doi.org/10.1039/c0lc00641f
67. Tseng, Q., E. Duchemin-Pelletier, A. Deshiere, M. Balland, H. Guillou, O. Filhol, and M. Théry. 2012. Spatial organization of the extracellular matrix regulates cell-cell junction positioning. Proc. Natl. Acad. Sci. USA. 109:1506-1511. http://dx.doi.org/10.1073/pnas.1106377109
68. Van Obberghen-Schilling, E., R.P. Tucker, F. Saupe, I. Gasser, B. Cseh, and G. Orend. 2011. Fibronectin and tenascin-C: accomplices in vascular morphogenesis during development and tumor growth. Int. J. Dev. Biol. 55:511-525. http://dx.doi.org/10.1387/ijdb.103243eo
69. Velling, T., J. Risteli, K. Wennerberg, D.F. Mosher, and S. Johansson. 2002. Polymerization of type I and III collagens is dependent on fibronectin and enhanced by integrins alpha 11beta 1 and alpha 2beta 1. J. Biol. Chem. 277:37377-37381. http://dx.doi.org/10.1074/jbc.M206286200
70. Whitehead, K.J., N.W. Plummer, J.A. Adams, D.A. Marchuk, and D.Y. Li. 2004. Ccm1 is required for arterial morphogenesis: implications for the etiology of human cavernous malformations. Development. 131:1437-1448. http://dx.doi.org/10.1242/dev.01036
71. Whitehead, K.J., A.C. Chan, S. Navankasattusas, W. Koh, N.R. London, J. Ling, A.H. Mayo, S.G. Drakos, C.A. Jones, W. Zhu, et al. 2009. The cerebral cavernous malformation signaling pathway promotes vascular integrity via Rho GTPases. Nat. Med. 15:177-184. http://dx.doi.org/10.1038/nm.1911
72. Wong, J.H., I.A. Awad, and J.H. Kim. 2000. Ultrastructural pathological features of cerebrovascular malformations: a preliminary report. Neurosurgery. 46:1454-1459. http://dx.doi.org/10.1097/00006123-200006000-00027
73. Yadla, S., P.M. Jabbour, R. Shenkar, C. Shi, P.G. Campbell, and I.A. Awad. 2010. Cerebral cavernous malformations as a disease of vascular permeability: from bench to bedside with caution. Neurosurg. Focus. 29:E4. http://dx.doi.org/10.3171/2010.5.FOCUS10121
74. Zawistowski, J.S., I.G. Serebriiskii, M.F. Lee, E.A. Golemis, and D.A. Marchuk. 2002. KRIT1 association with the integrin-binding protein ICAP-1: a new direction in the elucidation of cerebral cavernous malformations (CCM1) pathogenesis. Hum. Mol. Genet. 11:389-396. http://dx.doi.org/10.1093/hmg/11.4.389
75. Zawistowski, J.S., L. Stalheim, M.T. Uhlik, A.N. Abell, B.B. Ancrile, G.L. Johnson, and D.A. Marchuk. 2005. CCM1 and CCM2 protein interactions in cell signaling: implications for cerebral cavernous malformations pathogenesis. Hum. Mol. Genet. 14:2521-2531. http://dx.doi.org/10.1093/hmg/ddi256
76. Zhang, J., R.E. Clatterbuck, D. Rigamonti, D.D. Chang, and H.C. Dietz. 2001. Interaction between krit1 and icap1alpha infers perturbation of integrin beta1-mediated angiogenesis in the pathogenesis of cerebral cavernous malformation. Hum. Mol. Genet. 10:2953-2960. http://dx.doi .org/10.1093/hmg/10.25.2953
77. Zhang, J., S. Basu, D. Rigamonti, H.C. Dietz, and R.E. Clatterbuck. 2008. Krit1 modulates beta 1-integrin-mediated endothelial cell proliferation. Neurosurgery. 63:571-578, discussion :578. http://dx.doi.org/10.1227/01 .NEU.0000325255.30268.B0
78. Zhang, X.A., and M.E. Hemler. 1999. Interaction of the integrin beta1 cytoplasmic domain with ICAP-1 protein. J. Biol. Chem. 274:11-19. http://dx.doi.org/10.1074/jbc.274.1.11
79. Zhou, X., R.G. Rowe, N. Hiraoka, J.P. George, D. Wirtz, D.F. Mosher, I. Virtanen, M.A. Chernousov, and S.J. Weiss. 2008. Fibronectin fibrillogenesis regulates three-dimensional neovessel formation. Genes Dev. 22:1231-1243. http://dx.doi.org/10.1101/gad.1643308
80. Zovein, A.C., A. Luque, K.A. Turlo, J.J. Hofmann, K.M. Yee, M.S. Becker, R. Fassler, I. Mellman, T.F. Lane, and M.L. Iruela-Arispe. 2010. Beta1 integrin establishes endothelial cell polarity and arteriolar lumen formation via a Par3-dependent mechanism. Dev. Cell. 18:39-51. http://dx.doi .org/10.1016/j.devcel.2009.12.006