An Integrin and Rho GTPase-Dependent Pinocytic Vacuole Mechanism Controls Capillary Lumen Formation in Collagen and Fibrin Matrices

REFERENCES

• Akhtar N, Hotchin NA. (2001). Rac1 Regulates ad-herens junctions through endocytosis of E-Cadherin. Mol Biol Cell 12:847–862.
   PubMed Web of Science ®Google Scholar
• Anderson RG. (1998). The caveolae membrane sys-tem. Annu Rev Biochem 67:199–225.
   PubMed Web of Science ®Google Scholar
• Bauer J, Margolis M, Schreiner C, Edgell CJ, Aziz-khan J, Lazarowski E, Juliano RL. (1992). In vitro model of angiogenesis using a human endothelium-derived permanent cell line: Contributions of in-duced gene expression, G-proteins and integrins. J Cell Physiol 153:437–449.
   PubMed Web of Science ®Google Scholar
• Bayless KJ, Davis GE. (2002). The Cdc42 and Rac1 GTPases are required for capillary lumen formation in three-dimensional extracellular matrices. J Cell Sci 115:1123–1136.
   PubMed Web of Science ®Google Scholar
• Bayless KJ, Salazar R, Davis GE. (2000). RGD-dependent vacuolation and lumen formation ob-served during endothelial cell morphogenesis in three-dimensional fibrin matrices involves the avr33 and (15131 integrins. Am J Pathol 156:1673–1683.
   PubMed Web of Science ®Google Scholar
• Beitel GJ, Krasnow MA. (2000). Genetic control of epithelial tube size in the Drosophila tracheal sys-tem. Development 127:3271–3282.
   PubMed Web of Science ®Google Scholar
• Bell SE, Mavila A, Salazar R, Bayless KJ, Kanagala S, Maxwell SA, Davis GE. (2001). Differential gene expression during capillary morphogenesis in three-dimensional collagen matrices: Regulated expression of novel and known genes involved in basement membrane matrix assembly, cell cycle regulation, cellular differentiation and G-protein signaling. J Cell Sci 114:2755–2773.
   PubMed Web of Science ®Google Scholar
• Bishop AL, Hall A. (2000). Rho GTPases and their effector proteins. Biochem J 348:241–255.
   PubMed Web of Science ®Google Scholar
• Bonanno E, Iurlaro M, Madri JA, Nicosia RF. (2000). Type IV collagen modulates angiogenesis and neovessel survival in the rat aorta model. In Vitro Cell Dev Biol Animal 36:336–340.
   PubMed Web of Science ®Google Scholar
• Bloch W, Forsberg E, Lentini S, Brakebusch C, Mar-tin K, Krell HW, Weidle UH, Addicks K, Fassler R. (1997). Beta 1 integrin is essential for teratoma growth and angiogenesis. J Cell Biol 139:265–278.
   PubMed Web of Science ®Google Scholar
• Brooks PC, Clark RA, Cheresh DA. (1994). Require-ment of vascular integrin avr33 for angiogenesis. Science 264:569–571.
   PubMed Web of Science ®Google Scholar
• Buechner M, Hall DH, Bhatt H, Hedgecock EM. (1999). Cystic canal mutants in Caenorhabditis el-egans are defective in the apical membrane domain of the renal (excretory) cell. Develop Biol 214:227–241.
   PubMedGoogle Scholar
• Cardelli J. (2001). Phagocytosis and macropinocy-tosis in Dictyostelium: Phosphoinositide-based pro-cesses, biochemically distinct. Traffic 2:311–320.
   PubMedGoogle Scholar
• Carmeliet P, Jain RK. (2000). Angiogenesis in can-cer and other diseases. Nature 407:249–257.
   PubMed Web of Science ®Google Scholar
• Carmeliet P, Luttun A. (2001). The emerging role of the bone marrow-derived stem cells in (therapeutic) angiogenesis. Thromb Haemost 86:289–297.
   PubMed Web of Science ®Google Scholar
• Caron E, Hall A. (1998). Identification of two dis-tinct mechanisms of phagocytosis controlled by dif-ferent Rho GTPases. Science 282:1717–1721.
   PubMed Web of Science ®Google Scholar
• Chirnini G, Chavrier P. (2000). Function of Rho family of proteins in actin dynamics during phago-cytosis and engulfment. Nat Cell Biol 2:E191–E196.
   Google Scholar
• Clark ER, Clark EL. (1939). Microscopic observa-tions on the growth of blood capillaries in the living mammal. Am J Anat 64:251–301.
   Google Scholar
• Daub H, Gavaert K, Vandekerchkhove J, Sobel A, Hall A. (2001). Rac/Cdc42 and p65PAK regulate the microtubule - destabilizing protein stathmin through phosphorylation and serine 16. J Biol Chem 276:1677–1680.
   PubMed Web of Science ®Google Scholar
• Davis GE, Bayless KJ, Mavila A. (2002). The mo-lecular basis of endothelial cell morphogenesis in three-dimensional extracellular matrices. Anat Rec 268:252–275.
   PubMedGoogle Scholar
• Davis GE, Black SM, Bayless KJ. (2000). Capillary morphogenesis during endothelial cell invasion of three-dimensional collagen matrices. In Vitro Cell Dev Biol Animal 36:513–519.
   Google Scholar
• Davis GE, Camarillo CW. (1995). Regulation of en-dothelial cell morphogenesis by integrins, mechani-cal forces, and matrix guidance pathways. Exp Cell Res 216:113–123.
   PubMed Web of Science ®Google Scholar
• Davis GE, Camarillo CW. (1996). An a2131 inte-grin- dependent pinocytic mechanism involving intracellular vacuole formation and coalescence regulates capillary lumen and tube formation in three-dimensional collagen matrix. Exp Cell Res 224:39–51.
   PubMed Web of Science ®Google Scholar
• Davis GE, Pintar Allen KA, Salazar R, Maxwell SA. (2001). Matrix metalloproteinase-1 and -9 activa-tion by plasmin regulates a novel endothelial cell-mediated mechanism of collagen gel contraction and capillary tube regression in three-dimensional colla-gen matrices. J Cell Sci 114:917–930.
   PubMed Web of Science ®Google Scholar
• Dharmaawardhane S, Schurman A, Sells MA, Cher-noff J, Schmid SL, Bokoch GM. (2000). Regulation of macropinocytosis by p21-activated kinase-1. Mol Biol Cell 11:3341–3352.
   Google Scholar
• Djonov V, Schmid M, Tschanz SA, Burn i PH. (2000). Intussceptive angiogenesis: Its role in em-bryonic vascular network formation. Circ Res 86: 286–292.
   PubMed Web of Science ®Google Scholar
• Drake CJ, Brandt SJ, Trusk TC, Little CD. (1997). Tal/Scl is expressed in endothelial progenitor cells/ angioblasts and defines a dorsal-to-ventral gradient of vasculogenesis. Dev Biol 192:17–30.
   PubMed Web of Science ®Google Scholar
• Drake CJ, Fleming PA. (2000). Vasculogenesis in the day 6.5 to 9.5 mouse embryo. Blood 95:1671–1679.
   PubMed Web of Science ®Google Scholar
• Drake CJ, Little CD. (1999). VEGF and vascular fusion: Implications for normal and pathological vessels. J Histochem Cytochem 47:1351–1355.
   PubMed Web of Science ®Google Scholar
• Dvorak AM, Feng D. (2001). The vesiculo-vacuolar organelle (VV0): A new endothelial cell permeabil-ity organelle. J Histochem Cytochem 49:419–432.
   PubMed Web of Science ®Google Scholar
• Dyson SE, Jones DG, Kendrick WL. (1976). Some observations on the ultrastructure of developing rat cerebral capillaries. Cell Tissue Res 173:529–542.
   Google Scholar
• Erickson AC, Couchman JR. (2000). Still more complexity in mammalian basement membranes. J Histochem Cytochem 48:1291–1306.
   PubMed Web of Science ®Google Scholar
• Folkman J. (1995). Angiogenesis in cancer, vascu-lar, rheumatoid and other disease. Nat Med 1:27–31.
   PubMed Web of Science ®Google Scholar
• Folkman J, Haudenschild C. (1980). Angiogenesis in vitro. Nature 288:551–556.
   PubMed Web of Science ®Google Scholar
• Garrett WS, Chen LM, Kroschewski R, Ebersold M, Turley S, Trombetta S, Galan JE, Mellman I. (2000). Developmental control of endocytosis in dendritic cells by Cdc42. Cell 102:325–334.
   PubMed Web of Science ®Google Scholar
• Geiger B, Bershadsky A, Pankov R, Yamada KM. (2001). Transmembrane crosstalk between the ex-tracellular matrix-cytoskeleton. Nat Rev Mol Cell Biol 2:793–805.
   PubMed Web of Science ®Google Scholar
• Giancotti FG, Ruoslahti E. (1999). Integrin signal-ing. Science 285:1028–1032.
   PubMed Web of Science ®Google Scholar
• Glienke J, Schmitt AO, Pilarsky C, Hinzmann B, Weib B, Rosenthal A, Thierauch KH. (2000). Dif-ferential gene expression by endothelial cells in dis-tinct angiogenic states. Eur J Biochem 267:2820–2830.
   PubMedGoogle Scholar
• Goode BL, Drubin DG, Barnes F. (2000). Func-tional cooperation between the microtubule and ac-tin cytoskeletons. Curr Opin Cell Biol 12:63–71.
   PubMed Web of Science ®Google Scholar
• Greenberg S. (1995). Signal transduction of phago-cy. tosis Trends Cell Biol 5:93–99.
   PubMed Web of Science ®Google Scholar
• Guldner FH, Wolff JR. (1973). Seamless endothelia as indicators of capillaries developed from sprouts. Bibl Anat 12:120–123.
   Google Scholar
• Hall A, Nobes CD. (2000). Rho GTPases: Molecular switches that control the organization and dynamics of the actin cytoskeleton. Phil Trans R Soc Lond B 355:965–970.
   PubMed Web of Science ®Google Scholar
• Hanahan D. (1997). Signaling vascular morphogen-esis and maintenance. Science 277:48–50.
   PubMed Web of Science ®Google Scholar
• Hawes BE, Kil E, Green B, O'Neill K, Fried S, Gra-ziano MP. (2000). The melanin-concentrating hor-mone receptor couples to multiple G proteins to ac-tivate diverse intracellular signaling pathways. En-docrinology 141:4525–4532.
   Google Scholar
• Elan N, Cheung L, Pinter E, Madri JA. (2000). Plate-let-endothelial cell adhesion molecule-1 (CD31), a scaffolding molecule for selected catenin family members whose binding is mediated by different ty- rosine and serine/threonine phosphorylation. J Biol Chem 275:21435–21443.
   Google Scholar
• Inada H, Togashi H, Nakamura Y, Kaibuchi K, Na-gata K, Inagaki M. (1999). Balance between activi-ties of Rho kinase and type 1 protein phosphatase modulates turnover of phosphorylation and dynam-ics of desmin/virnentin filaments. J Biol Chem 274: 34932–34939.
   Google Scholar
• Ingber D, Folkman J. (1988). Inhibition of angio-genesis through modulation of collagen metabolism. Lab Invest 59:44–51.
   PubMed Web of Science ®Google Scholar
• Iruela-Arispe ML, Hasselaar P, Sage EH. (1991). Differential expression of extracellular proteins is correlated with angiogenesis in vitro. Lab Invest 64: 174–186.
   PubMed Web of Science ®Google Scholar
• Isaac DD, Andrew DJ. (1996). Tubulogenesis in Drosophila: A requirement for the trachealess gene product. Genes Dev 10:103–117.
   PubMed Web of Science ®Google Scholar
• Jackson CJ, Jenkins K, Schreiber L. (1992). Possible mechanisms of type I collagen-induced vascular tube. PCS 61:198–204.
   Google Scholar
• Kaibuchi K, Kuroda S, Amano M. (1999). Regula-tion of the cytoskeleton and cell adhesion by the Rho family GTPases in mammalian cells. Ann Rev Bio-chem 68:459–468.
   PubMed Web of Science ®Google Scholar
• Kahn J, Mehraban F, Ingle G, Xin X, Bryant JE, Vehar G, Schoenfeld J, Grimaldi CJ, Peale F, Drak-sharapu A, Lewin DA, Gerritsen ME. (2000). Gene expression profiling in an in vitro model of angio-genesis. Am J Pathol 156:1887–1900.
   PubMed Web of Science ®Google Scholar
• Kim S, Bell K, Mousa SA, Varner JA. (2000). Regu-lation of angiogenesis in vivo by ligation of integrin alpha5beta1 with the central cell-binding domain of fibronectin. Am J Pathol 156:1345–1362.
   PubMed Web of Science ®Google Scholar
• Kiosses WB, Daniels RH, Otey C, Bokoch GM, Schwartz MA. (1999). A role for p21-activated ki-nase in endothelial cell migration. J Cell Biol 147: 831–843.
   PubMed Web of Science ®Google Scholar
• Konerding MA, van Ackern C, Steinberg F, Streffer C. (1992). Combined morphological approaches in the study of network formation in tumor angiogen-esis. In: Steiner R, Weisz PB, Langer R, editors. An-giogenesis. Basel, Switzerland: Birkhauser Verlag/ Switzerland, 40–58.
   Google Scholar
• Lefebvre O, Sorokin L, Kedinger M, Simon-Assmann P. (1999). Developmental expression and cellular origin of the larninin alpha2, alpha4, and alpha5 chains in the intestine. Dev Biol 210:135–150.
   PubMedGoogle Scholar
• Lin HH, Yang TP, Jiang ST, Yang HY, Tang MJ. (1999). Bc1-2 overexpression prevents apoptosis-induced Madin-Darby canine kidney simple epithe-lial cyst formation. Kidney Int 55:168–178.
   PubMedGoogle Scholar
• Lipschutz JH, Guo W, O'Brien LE, Nguyen YH, Novick P, Mostov KE. (2000). Exocyst is involved in cystogenesis and tubulogenesis and acts by modu-lating synthesis and delivery of basolateral plasma membrane and secretory proteins. Mol Biol Cell 11: 4259–4275.
   Google Scholar
• Maragoudakis ME, Sarmonika M, Panoutsacopou-lou M. (1988). Inhibition of basement membrane synthesis prevents angiogenesis. J Pharmacol Exp Ther 244:729–733.
   PubMed Web of Science ®Google Scholar
• Meriane M, Mary S, Comunale F, Vifnal E, Fort P, Gauthier-Rouviere C. (2000). Cdc42Hs and Rac1 GTPases induce collapse of the virnentin intermedi-ate filament network. J Biol Chem 275:33046–33052.
   Google Scholar
• Metzger RJ, Krasnow MA. (1999). Genetic control of branching morphogenesis. Science 284:1635–1639.
   PubMed Web of Science ®Google Scholar
• Meyer GT, Matthias LJ, Noack L, Vadas MA, Gamble JR. (1997). Lumen formation during angio-genesis in vitro involves phagocytic activity, forma-tion and secretion of vacuoles, cell death, and cap-illary tube remodelling by different populations of endothelial cells. Anat Rec 249:327–340.
   PubMedGoogle Scholar
• Miner JH, Cunningham J, Sanes JR. (1998). Roles for larninin in embryogenesis: exencephaly, syndac-tyly, and placentopathy in mice lacking the larninin alpha5 chain. J Cell Biol 143:1713–1723.
   PubMed Web of Science ®Google Scholar
• Montesano R. (1992). Regulation of angiogenesis in vitro. Eur J Clin Invest 22:504–515.
   PubMed Web of Science ®Google Scholar
• Montesano R, Matsumoto K, Nakamura T, Orci L. (1991). Identification of a fibroblast-derived epithe-lial morphogen as hepatocyte growth factor. Cell 67: 901–908.
   PubMed Web of Science ®Google Scholar
• Montesano R, Orci L. (1985). Tumor-promoting phorbol esters induce angiogenesis in vitro. Cell 42: 469–477.
   PubMed Web of Science ®Google Scholar
• Montesano R, Orci L. (1987). Phorbol ester induces cultured endothelial cells to invade a fibrin matrix in the presence of fibrinolytic inhibitors. J Cell Physiol 132:509–516.
   PubMedGoogle Scholar
• Montesano R, Orci L. (1988). Intracellular dia-phragmed fenestrae in cultured capillary endothelial cells. J Cell Sci 89:441–447.
   Google Scholar
• Montesano R, Soriano JV, Pepper MS, Orci L. (1997). Induction of epithelial branching tubulo-genesis in vitro. J Cell Physiol 173:152–161.
   Google Scholar
• Morrissette NS, Gold ES, Guo J, Hamerman JA, Ozinsky A, Bedian V, Aderem AA. (1999). Isolation and characterization of monoclonal antibodies di-rected against novel components of macrophage phagosomes. J Cell Sci 112:4705–4713.
   Google Scholar
• Nicosia RF, Madri JA. (1987). The microvascular extracellular matrix: Developmental changes during angiogenesis in the aortic ring-plasma clot model. Am J Pathol 128:78–90.
   PubMed Web of Science ®Google Scholar
• Nicosia RF, Ottinetti A. (1990). Growth of mi-crovessels in serum-free matrix culture of rat aorta: A quantitative assay of angiogenesis in vitro. Lab Invest 63:115–122.
   PubMed Web of Science ®Google Scholar
• Nicosia RF, Tchao R, Leighton J. (1982). Histotypic angiogenesis in vitro: Light microscopic, ultrastruc- tural, and radioautographic studies. In Vitro 18: 538–549.
   PubMedGoogle Scholar
• Nobes CD, Hall A. (1995). Rho, Rac, and Cdc42 GTPases regulate the assembly of multirnolecular focal complexes associated with actin stress fibers, larnellipodia, and filopodia. Cell 81:53–62.
   PubMed Web of Science ®Google Scholar
• Noden D. (1990). Origins and assembly of avian embryonic blood vessels. Ann. NY Acad. Sci. 588: 236–249.
   Google Scholar
• O'Brien LE, Zegers MMP, Mostov KE. (2002). Building epithelial architecture: Insights from three-dimensional culture models. Nat Rev Mol Cell Biol 3:531–537.
   PubMed Web of Science ®Google Scholar
• Palazzo AF, Cook TA, Alberts AS, Gundersen GG. (2001). mDia mediates Rho-regulated formation and orientation of stable microtubules. Nat Cell Biol 3:723–729.
   PubMedGoogle Scholar
• Patan S. (2000). Vasculogenesis and angiogenesis as mechanisms of vascular network formation, growth and remodeling. J Neurooncol 50:1–15.
   PubMed Web of Science ®Google Scholar
• Pollack AL, Barth AT, Altschuler Y, Nelson WJ, Mostov KE. (1997). Dynamics of beta-catenin in-teractions with APC protein regulate epithelial tu-bulogenesis J Cell Biol 137:1651–1662.
   Google Scholar
• Prehoda KE, Scott JA, Mullins RD, Lim WA. (2000). Integration of multiple signals through co-operative regulation of the N-WASP-Arp2/3 com-plex. Science 290:801–806.
   PubMed Web of Science ®Google Scholar
• Reinhard M, Jarchau T, Walter U. (2001). Actin-based motility: stop and go with Ena/VASP pro-teins. Trends Biochem Sci 26:243–249.
   PubMed Web of Science ®Google Scholar
• Ridley AJ. (2001). Rho proteins: Linking signaling with membrane trafficking. Traffic 2:303–310.
   Google Scholar
• Ridley AJ. (2001). Rho family proteins: coordinat-ing cell responses. Trends Cell Biol 11:471–477.
   Google Scholar
• Ridley AJ, Hall A. (1992). The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors. Cell 70:389–399.
   PubMed Web of Science ®Google Scholar
• Ridley AJ, Paterson HF, Johnston CL, Diekmann D, Hall A. (1992). The small GTP-binding protein rac regulates growth factor-induced membrane ruffling. Cell 70:401–410.
   PubMed Web of Science ®Google Scholar
• Risau W, Flamme I. (1995). Vasculogenesis. Annu Rev Cell Dev Biol 11:73–91.
   PubMed Web of Science ®Google Scholar
• Rohatgi R, Ma L, Miki H, Lopez M, Kirchhausen T, Takenawa T, Kirschner MW. (1999). The interac-tion between N-WASP and the Arp2/3 complex links Cdc42-dependent signals to actin assembly. Cell 97:221–231.
   PubMed Web of Science ®Google Scholar
• Rupp PA, Little CD. (2001). Integrins in vascular development. Circ Res 89:566–572.
   PubMed Web of Science ®Google Scholar
• Salazar R, Bell SE, Davis GE. (1999). Coordinate induction of the actin cytoskeletal regulatory pro-teins gelsolin, vasodilator-stimulated phosphopro-tein, and profilin during capillary morphogenesis in vitro. Exp Cell Res 249:22–32.
   Google Scholar
• Sarnakovlis C, Hacohen N, Manning G, Sutherland DC, Guillemin K, Krasnow MA. (1996). Develop-ment of the Drosophila tracheal system occurs by a series of morphologically distinct but genetically coupled branching events. Development 122:1395–1407.
   Google Scholar
• Sastry SK, Burridge K. (2000). Focal adhesions: A nexus for intracellular signaling and cytoskeletal dy-arnics. Exp Cell Res 261:25–36.
   PubMed Web of Science ®Google Scholar
• Schwartz M, Shattil S. (2000). Signaling networks linking integrins and Rho family GTPases. Trends Biochem Sci 25:388–391.
   PubMed Web of Science ®Google Scholar
• Senger DR. (1996). Molecular framework for angio-genesis: a complex web of interactions between ex-travasated plasma proteins and endothelial cell pro-teins induced by angiogenic cytokines. Am J Pathol 149:1–7.
   PubMed Web of Science ®Google Scholar
• Senger DR, Claffey KP, Benes JE, Perruzzi CA, Ser-giou AP, Detrnar M. (1997). Angiogenesis promoted by vascular endothelial growth factor: Regulation through alphalbetal and alpha2betal integrins. Proc Natl Acad Sci USA 94:13612–13617.
   Google Scholar
• Senger DR, Perruzzi CA, Streit M, Koteliansky YE, deFougerolles AR, Detmar M. (2002). The alpha(1) beta(1) and alpha(2) beta(1) integrins provide criti-cal support for vascular endothelial growth factor signaling, endothelial cell migration, and tumor an-giogenesis. Am J Pathol 160:195–204.
   PubMed Web of Science ®Google Scholar
• Sephel GC, Kennedy R, Kudravi S. (1996). Expres-sion of capillary basement membrane components during sequential phases of wound angiogenesis. Matrix Biol 15:263–279.
   Google Scholar
• Settleman J. (2001). Rac 'n Rho: The music that shapes a developing embryo. Dev Cell 1:321–331.
   PubMed Web of Science ®Google Scholar
• Shattil SJ, Ginsberg M H. (1997). Integrin signaling in vascular biology. J Clin Invest 100:591–S95.
   Google Scholar
• Soleirnani M, Burnham CE. (2001). Na+:HC 03- co-transporters (NBC): Cloning and characterization. J Membr Biol 183:71–84.
   Google Scholar
• Speidel CC. (1933). Studies of living nerves: Activi-ties of arneboid growth cones, sheath cells and my-elin segments, as revealed by prolonged observation of individual nerve fibers in frog tadpoles. Am J Anat 52:1–75.
   Google Scholar
• St. Croix B, Rago C, Velculescu V, Traverso G, Ro-mans KE, Montgomery E, Lal A, Riggins GJ, Len-gauer C, Vogelstein B, Kinzler KW. (2000). Genes expressed in human tumor endothelium. Science 289:1197–1202.
   PubMed Web of Science ®Google Scholar
• Stromhaug PE, Klionsky DJ. (2001). Approaching the molecular mechanism of autophagy. Traffic 2: 524–531.
   Google Scholar
• Swanson JA, Johnson MT, Beningo K, Post P, Moss-eker M, Araki N. (1999). A contractile activity that closes phagosomes in macrophages. J Cell Sci 112: 307–316.
   Google Scholar
• Swanson JA, Watts C. (1995). Macropinocytosis. Trends Cell Biol 5:424–428.
   PubMed Web of Science ®Google Scholar
• Takai Y, Sasaki T, Matozaki T. (2001). Small GTP-binding proteins. Physiol Rev 81:153–208.
   PubMed Web of Science ®Google Scholar
• Vega-Salas BE, Salas PJI, Rodriguez-Boulan E. (1987). Modulation of the expression of an apical plasma membrane protein of Madin-Darby Canine Kidney epithelial cells: Cell-cell interactions control the appearance of a novel intracellular storage com-partment. J Cell Biol 104:1249–1259.
   Google Scholar
• Vega-Salas BE, Salas PJI, Rodriguez-Boulan E. (1988). Exocytosis of vacuolar apical compartment (VAC): A cell-cell contact controlled mechanism for the establishment of the apical plasma membrane domain in epithelial membrane domain in epithelial cells. J Cell Biol 107:1717–1728.
   PubMedGoogle Scholar
• Vernon RB, Angelo JC, huela-Arispe ML, Lane TF, Sage EH. (1992). Reorganization of basement mem-brane matrices by cellular traction promotes the for-mation of cellular networks in vitro. Lab Invest 66: 536–547.
   PubMed Web of Science ®Google Scholar
• Vernon RB, Sage EH. (1995). Between molecules and morphology: extracellular matrix and the cre-ation of vascular form. Am J Pathol 147:873–883.
   PubMed Web of Science ®Google Scholar
• Vernon RB, Sage EH. (1999). A novel, quantitative model for study of endothelial cell migration and sprout formation within three-dimensional collagen matrices. Micro vasc Res 57:118–133.
   PubMed Web of Science ®Google Scholar
• Wagner RC. (1980). Endothelial cell embryology and growth. Adv Microcirc 9:45–75.
   Google Scholar
• Wojciak-Stothard B, Potempa S, Eichholtz T, Ridley AJ. (2001). Rho and Rac but not Cdc42 regulate endothelial cell permeability. J Cell Sci 114:1343–1355.
   PubMed Web of Science ®Google Scholar
• Wolff JR, Bar T. (1972). 'Seamless' endothelia in brain capillaries during development of the rat's ce-rebral cortex. Brain Res 41:17–24.
   PubMed Web of Science ®Google Scholar
• Yancopoulos GD, Davis S, Gale NW, Rudge JS, Wie-gand SJ, Holash J. (2000). Vascular-specific growth factors and blood vessel formation. Nature 407: 242–248.
   PubMed Web of Science ®Google Scholar
• Yang S, Graham J, Kahn JW, Schwartz EA, Gerrit-sen ME. (1999). Functional roles for PECAM-1 (CD31) and VE-cadherin (CD144) in tube assembly and lumen formation in three-dimensional collagen gels. Am J Pathol 155:887–895.
   PubMed Web of Science ®Google Scholar
• Yeaman C, Grindstaff KK, Nelson WJ. (1999). New perspectives on mechanisms involved in generating epithelial cell polarity. Physiol Rev 79:73–98.
   PubMedGoogle Scholar
• Zerial M, McBride H. (2001). Rab proteins as mem-brane organizers. Nat Rev Mol Cell Biol 2:107–117.
   PubMed Web of Science ®Google Scholar