β1 Integrin Establishes Endothelial Cell Polarity and Arteriolar Lumen Formation via a Par3-Dependent Mechanism

Developmental Cell

Volumn 18, Issue 1, 2010, Pages 39-51

  Zovein, Ann C ^a   Luque, Alfonso ^a   Turlo, Kirsten A ^a   Hofmann, Jennifer J ^a   Yee, Kathleen M ^a   Becker, Michael S ^a   Fassler, Reinhard ^b   Mellman, Ira ^c   Lane, Timothy F ^d   Iruela Arispe, M Luisa ^a,d  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^c GENENTECH INC   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

DEVBIO

Indexed keywords

BETA1 INTEGRIN; CELL ADHESION MOLECULE; PROTEINASE ACTIVATED RECEPTOR 3; PARD3 PROTEIN, MOUSE;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTERIOLE; ARTERY ENDOTHELIUM; ARTICLE; CELL POLARITY; CELLULAR DISTRIBUTION; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; ENDOTHELIUM CELL; FEMALE; GENE EXPRESSION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; ANIMAL; CELL ADHESION; CELL DIFFERENTIATION; CELL SHAPE; CYTOLOGY; DISEASE MODEL; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOUSE MUTANT; PHYSIOLOGY; PRENATAL DEVELOPMENT; SIGNAL TRANSDUCTION;

ANIMALS; ANTIGENS, CD29; ARTERIOLES; CELL ADHESION; CELL ADHESION MOLECULES; CELL DIFFERENTIATION; CELL POLARITY; CELL SHAPE; DISEASE MODELS, ANIMAL; ENDOTHELIAL CELLS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MICE; MICE, KNOCKOUT; NEOVASCULARIZATION, PHYSIOLOGIC; SIGNAL TRANSDUCTION;

EID: 74249091561     PISSN: 15345807     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.devcel.2009.12.006     Document Type: Article

References (40)

1. Alva J.A., Zovein A.C., Monvoisin A., Murphy T., Salazar A., Harvey N.L., Carmeliet P., and Iruela-Arispe M.L. VE-cadherin-Cre-recombinase transgenic mouse: a tool for lineage analysis and gene deletion in endothelial cells. Dev. Dyn. 235 (2006) 759-767
2. Carlson T.R., Hu H., Braren R., Kim Y.H., and Wang R.A. Cell-autonomous requirement for β1 integrin in endothelial cell adhesion, migration and survival during angiogenesis in mice. Development 135 (2008) 2193-2202
3. Davis G.E., Koh W., and Stratman A.N. Mechanisms controlling human endothelial lumen formation and tube assembly in three-dimensional extracellular matrices. Birth Defects Res. C Embryo Today 81 (2007) 270-285
4. Desai R.A., Gao L., Raghavan S., Liu W.F., and Chen C.S. Cell polarity triggered by cell-cell adhesion via E-cadherin. J. Cell Sci. 122 (2009) 905-911
5. Desclozeaux M., Venturato J., Wylie F.G., Kay J.G., Joseph S.R., Le H.T., and Stow J.L. Active Rab11 and functional recycling endosome are required for E-cadherin trafficking and lumen formation during epithelial morphogenesis. Am. J. Physiol. 295 (2008) C545-C556
6. Downs K.M. Florence Sabin and the mechanism of blood vessel lumenization during vasculogenesis. Microcirculation 10 (2003) 5-25
7. Drake C.J., Davis L.A., and Little C.D. Antibodies to β1-integrins cause alterations of aortic vasculogenesis, in vivo. Dev. Dyn. 193 (1992) 83-91
8. Folkman J., and Haudenschild C. Angiogenesis in vitro. Nature 288 (1980) 551-556
9. Giancotti F.G., and Ruoslahti E. Integrin signaling. Science 285 (1999) 1028-1032
10. Hellstrom M., Phng L.K., Hofmann J.J., Wallgard E., Coultas L., Lindblom P., Alva J., Nilsson A.K., Karlsson L., Gaiano N., et al. Dll4 signalling through Notch1 regulates formation of tip cells during angiogenesis. Nature 445 (2007) 776-780
11. Hynes R.O. Integrins: bidirectional, allosteric signaling machines. Cell 110 (2002) 673-687
12. Hynes R.O., and Bader B.L. Targeted mutations in integrins and their ligands: their implications for vascular biology. Thromb. Haemost. 78 (1997) 83-87
13. Iden S., Rehder D., August B., Suzuki A., Wolburg-Buchholz K., Wolburg H., Ohno S., Behrens J., Vestweber D., and Ebnet K. A distinct PAR complex associates physically with VE-cadherin in vertebrate endothelial cells. EMBO Rep. 7 (2006) 1239-1246
14. Iruela-Arispe M.L., and Davis G.E. Cellular and molecular mechanisms of vascular lumen formation. Dev. Cell 16 (2009) 222-231
15. Jaffe A.B., Kaji N., Durgan J., and Hall A. Cdc42 controls spindle orientation to position the apical surface during epithelial morphogenesis. J. Cell Biol. 183 (2008) 625-633
16. Kamei M., Saunders W.B., Bayless K.J., Dye L., Davis G.E., and Weinstein B.M. Endothelial tubes assemble from intracellular vacuoles in vivo. Nature 442 (2006) 453-456
17. Koh W., Mahan R.D., and Davis G.E. Cdc42- and Rac1-mediated endothelial lumen formation requires Pak2, Pak4 and Par3, and PKC-dependent signaling. J. Cell Sci. 121 (2008) 989-1001
18. Koh W., Sachidanandam K., Stratman A.N., Sacharidou A., Mayo A.M., Murphy E.A., Cheresh D.A., and Davis G.E. Formation of endothelial lumens requires a coordinated PKCε-, Src-, Pak- and Raf-kinase-dependent signaling cascade downstream of Cdc42 activation. J. Cell Sci. 122 (2009) 1812-1822
19. Lee S., Chen T.T., Barber C.L., Jordan M.C., Murdock J., Desai S., Ferrara N., Nagy A., Roos K.P., and Iruela-Arispe M.L. Autocrine VEGF signaling is required for vascular homeostasis. Cell 130 (2007) 691-703
20. Lei L., Liu D., Huang Y., Jovin I., Shai S.Y., Kyriakides T., Ross R.S., and Giordano F.J. Endothelial expression of β1 integrin is required for embryonic vascular patterning and postnatal vascular remodeling. Mol. Cell. Biol. 28 (2008) 794-802
21. Lubarsky B., and Krasnow M.A. Tube morphogenesis: making and shaping biological tubes. Cell 112 (2003) 19-28
22. Martin-Belmonte F., Gassama A., Datta A., Yu W., Rescher U., Gerke V., and Mostov K. PTEN-mediated apical segregation of phosphoinositides controls epithelial morphogenesis through Cdc42. Cell 128 (2007) 383-397
23. Meder D., Shevchenko A., Simons K., and Fullekrug J. Gp135/podocalyxin and NHERF-2 participate in the formation of a preapical domain during polarization of MDCK cells. J. Cell Biol. 168 (2005) 303-313
24. Monvoisin A., Alva J.A., Hofmann J.J., Zovein A.C., Lane T.F., and Iruela-Arispe M.L. VE-cadherin-CreERT2 transgenic mouse: a model for inducible recombination in the endothelium. Dev. Dyn. 235 (2006) 3413-3422
25. Potocnik A.J., Brakebusch C., and Fassler R. Fetal and adult hematopoietic stem cells require β1 integrin function for colonizing fetal liver, spleen, and bone marrow. Immunity 12 (2000) 653-663
26. Raghavan S., Bauer C., Mundschau G., Li Q., and Fuchs E. Conditional ablation of β1 integrin in skin. Severe defects in epidermal proliferation, basement membrane formation, and hair follicle invagination. J. Cell Biol. 150 (2000) 1149-1160
27. Rupp P.A., and Little C.D. Integrins in vascular development. Circ. Res. 89 (2001) 566-572
28. Santiago-Martinez E., Soplop N.H., Patel R., and Kramer S.G. Repulsion by Slit and Roundabout prevents Shotgun/E-cadherin-mediated cell adhesion during Drosophila heart tube lumen formation. J. Cell Biol. 182 (2008) 241-248
29. Schenkel A.R., Mamdouh Z., Chen X., Liebman R.M., and Muller W.A. CD99 plays a major role in the migration of monocytes through endothelial junctions. Nat. Immunol. 3 (2002) 143-150
30. Sfakianos J., Togawa A., Maday S., Hull M., Pypaert M., Cantley L., Toomre D., and Mellman I. Par3 functions in the biogenesis of the primary cilium in polarized epithelial cells. J. Cell Biol. 179 (2007) 1133-1140
31. Shutter J.R., Scully S., Fan W., Richards W.G., Kitajewski J., Deblandre G.A., Kintner C.R., and Stark K.L. Dll4, a novel Notch ligand expressed in arterial endothelium. Genes Dev. 14 (2000) 1313-1318
32. Soriano P. Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat. Genet. 21 (1999) 70-71
33. Srinivas S., Watanabe T., Lin C.S., William C.M., Tanabe Y., Jessell T.M., and Costantini F. Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Dev. Biol. 1 (2001) 4
34. Stenmark H. Rab GTPases as coordinators of vesicle traffic. Nat. Rev. Mol. Cell Biol. 10 (2009) 513-525
35. Stephens L.E., Sutherland A.E., Klimanskaya I.V., Andrieux A., Meneses J., Pedersen R.A., and Damsky C.H. Deletion of β 1 integrins in mice results in inner cell mass failure and peri-implantation lethality. Genes Dev. 9 (1995) 1883-1895
36. Strilic B., Kucera T., Eglinger J., Hughes M.R., McNagny K.M., Tsukita S., Dejana E., Ferrara N., and Lammert E. The molecular basis of vascular lumen formation in the developing mouse aorta. Dev. Cell 17 (2009) 505-515
37. Stupack D.G., and Cheresh D.A. ECM remodeling regulates angiogenesis: endothelial integrins look for new ligands. Sci. STKE 2002 (2002) pe7
38. Suzuki A., and Ohno S. The PAR-aPKC system: lessons in polarity. J. Cell Sci. 119 (2006) 979-987
39. Tanjore H., Zeisberg E.M., Gerami-Naini B., and Kalluri R. β1 integrin expression on endothelial cells is required for angiogenesis but not for vasculogenesis. Dev. Dyn. 237 (2008) 75-82
40. Yamanaka T., Horikoshi Y., Sugiyama Y., Ishiyama C., Suzuki A., Hirose T., Iwamatsu A., Shinohara A., and Ohno S. Mammalian Lgl forms a protein complex with PAR-6 and aPKC independently of PAR-3 to regulate epithelial cell polarity. Curr. Biol. 13 (2003) 734-743