Endothelial adhesion molecules in the development of the vascular tree: The garden of forking paths

Current Opinion in Cell Biology

Volumn 11, Issue 5, 1999, Pages 573-581

  Bazzoni, Gianfranco ^a   Dejana, Elisabetta ^a,b   Lampugnani, Maria Grazia ^a  

^a MARIO NEGRI INSTITUTE FOR PHARMACOLOGICAL RESEARCH   (Italy)

^b UNIVERSITY OF INSUBRIA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CADHERIN; CATENIN; CELL ADHESION MOLECULE; CELL SURFACE RECEPTOR; INTEGRIN;

ANGIOGENESIS; CELL ADHESION; ENDOTHELIUM CELL; EXTRACELLULAR MATRIX; MORPHOGENESIS; PRIORITY JOURNAL; REVIEW;

EID: 0032845468     PISSN: 09550674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0955-0674(99)00023-X     Document Type: Review

References (94)

1. Borges JL Ficciones. 1956;Blaneta, Buenos Aires.
2. Soldi R, Mitola S, Strasly M, Defilippi P, Tarone G, Bussolino F Role of αvβ3 integrin in the activation of vascular endothelial growth factor receptor-2. EMBO J. 18:1999;882-892. This paper, together with [3-5], reports interesting descriptions of functional crosstalk between integrin-based adhesion and receptor tyrosine kinases.
3. Schneller M, Vuori K, Ruoslahti E αvβ3 integrin associates with activated insulin and PDGFβ receptors and potentiates the biological activity of PDGF. EMBO J. 16:1997;5600-5607.
4. Senger DR, Ledbetter SR, Claffey KP, Papadopoulos-Sergiou A, Peruzzi CA, Detmar M Stimulation of endothelial cell migration by vascular permeability factor/vascular endothelial growth factor through cooperative mechanisms involving the αvβ3 integrin, osteopontin, and thrombin. Am J Pathol. 149:1996;293-305.
5. Woodard AS, Garcia-Cardena G, Leong M, Madri JA, Sessa WC, Languino LR The synergistic activity of αvβ3 integrin and PDGF receptor increases cell migration. J Cell Sci. 111:1998;469-478.
6. Berdichevsky F, Gilbert C, Shearer M, Taylor-Papadimitriou J Collagen-induced rapid morphogenesis of human mammary epithelial cells: the role of the α2β1 integrin. J Cell Sci. 102:1992;437-446.
7. Kreidberg JA, Donovan MJ, Goldstein SL, Rennke H, Shepherd K, Jones RC, Jaenisch R α3β1 integrin has a crucial role in kidney and lung organogenesis. Development. 122:1996;3537-3547.
8. Muller U, Wang D, Denda S, Meneses JJ, Pedersen RA, Reichardt LF Integrin α8β1 is critically important for epithelial-mesenchymal interactions during kidney morphogenesis. Cell. 88:1997;603-613.
9. Kubota Y, Kleinman HK, Martin GR, Lawley TJ Role of laminin and basement membrane in the morphological differentiation of human endothelial cells into capillary-like structures. J Cell Biol. 107:1988;1589-1598.
10. Bauer J, Margolis M, Schreiner C, Edgell CJ, Azizkhan J, Lazarowski E, Juliano RL In vitro model of angiogenesis using a human endothelium-derived permanent cell line: contributions of induced gene expression, G-proteins, and integrins. J Cell Physiol. 153:1992;437-449.
11. Klein S, Giancotti FG, Presta M, Albelda SM, Buck CA, Rifkin DB Basic fibroblast growth factor modulates integrin expression in microvascular endothelial cells. Mol Biol Cell. 4:1993;973-982.
12. Grant DS, Tashiro KI, Segui-Real B, Yamada Y, Martin GR, Kleinman HK Two different laminin domains mediate the differentiation of human endothelial cells into capillary-like structures in vitro. Cell. 58:1989;933-943.
13. Georges-Labouesse E, Messaddeq N, Yehia G, Cadalbert L, Dierich A, Le Meur M Absence of integrin α6 leads to epidermolysis bullosa and neonatal death in mice. Nat Genet. 13:1996;370-373.
14. Hodivala-Dilke KM, DiPersio CM, Kreidberg JA, Hynes RO Novel roles for α3β1 integrin as a regulator of cytoskeletal assembly and as a trans-dominant inhibitor of integrin receptor function in mouse keratinocytes. J Cell Biol. 142:1998;1357-1369. This work, together with that described in [15], provides convincing experimental evidence for the 'trans-dominant inhibition' of integrin function, whereby binding of one integrin may inhibit the function of other target integrins. This form of crosstalk between integrins might explain why anti-integrin blocking reagents can sometimes bring about broader effects than expected and lead to potential overestimation of the biologic role of individual integrins.
15. Diaz-Gonzalez F, Forsyth J, Steiner B, Ginsberg MH Trans-dominant inhibition of integrin function. Mol Biol Cell. 7:1996;1939-1951.
16. Eliceiri BP, Cheresh DA The role of αv integrins during angiogenesis: insights into potential mechanisms of action and clinical development. J Clin Invest. 103:1999;1227-1230. A concise and up-to-date review about the role of αvβ3 integrin in angiogenesis with a discussion of the basis for potential pharmacological interventions.
17. Brooks PC, Clark RA, Cheresh DA Requirement of vascular integrin αvβ3 for angiogenesis. Science. 264:1994;569-571.
18. Hammes HP, Brownlee M, Jonczyk A, Sutter A, Preissner KT Subcutaneous injection of a cyclic peptide antagonist of vitronectin receptor-type integrins inhibits retinal neovascularization. Nat Med. 2:1996;529-533.
19. Drake CJ, Cheresh DA, Little CD An antagonist of integrin αvβ3 prevents maturation of blood vessels during embryonic neovascularization. J Cell Sci. 108:1995;2655-2661.
20. Friedlander M, Brooks PC, Shaffer RW, Kincaid CM, Varner JA, Cheresh DA Definition of two angiogenic pathways by distinct αv integrins. Science. 270:1995;1500-1502.
21. Storgard CM, Stupack DG, Jonczyk A, Goodman SL, Fox RI, Cheresh DA Decreased angiogenesis and arthritic disease in rabbits treated with an αvβ3 antagonist. J Clin Invest. 103:1999;47-54.
22. Leavesley DI, Schwartz MA, Rosenfeld M, Cheresh DA Integrin β1- and β3-mediated endothelial cell migration is triggered through distinct signaling mechanisms. J Cell Biol. 121:1993;163-170.
23. Brooks PC, Stromblad S, Sanders LC, von Schalscha TL, Aimes RT, Stetler Stevenson WG, Quigley JP, Cheresh DA Localization of matrix metalloproteinase MMP-2 to the surface of invasive cells by interaction with integrin αvβ3. Cell. 85:1996;683-693.
24. Stromblad S, Becker JC, Yebra M, Brooks PC, Cheresh DA Suppression of p53 activity and p21WAF1/CIP1 expression by vascular cell integrin αvβ3 during angiogenesis. J Clin Invest. 98:1996;426-433.
25. Brooks PC, Montgomery AM, Rosenfeld M, Reisfeld RA, Hu T, Klier G, Cheresh DA Integrin αvβ3 antagonists promote tumor regression by inducing apoptosis of angiogenic blood vessels. Cell. 79:1994;1157-1164.
26. Bader BL, Rayburn H, Crowley D, Hynes RO Extensive vasculogenesis, angiogenesis, and organogenesis precede lethality in mice lacking all αv integrins. Cell. 95:1998;507-519. The surprising observation that null mutation of the αv integrin gene allows extensive vasculogenesis and angiogenesis requires re-evaluation of the importance of αv-based integrins during vascular development.
27. Lampugnani MG, Dejana E Interendothelial junctions: structure, signalling and functional roles. Curr Opin Cell Biol. 9:1997;674-682.
28. Ben-Ze'ev A, Geiger B Differential molecular interactions of β-catenin and plakoglobin in adhesion, signaling and cancer. Curr Opin Cell Biol. 10:1998;629-639.
29. Newman PJ Switched at birth: a new family for PECAM-1. J Clin Invest. 103:1999;5-9.
30. Stevenson BR, Keon BH The tight junction: morphology to molecules. Annu Rev Cell Dev Biol. 14:1998;89-109.
31. Bach TL, Barsigian C, Chalupowicz DG, Busler D, Yaen CH, Grant DS, Martinez J VE-cadherin mediates endothelial cell capillary tube formation in fibrin and collagen gels. Exp Cell Res. 238:1998;324-334.
32. Matsumura T, Wolff K, Petzelbauer P Endothelial cell tube formation depends on cadherin 5 and CD31 interactions with filamentous actin. J Immunol. 158:1997;3408-3416.
33. Vittet D, Buchou T, Schweitzer A, Dejana E, Huber P Targeted null-mutation in the vascular endothelial-cadherin gene impairs the organization of vascular-like structures in embryoid bodies. Proc Natl Acad Sci USA. 94:1997;6273-6278.
34. Carmeliet P, Lampugnani MG, Moons L, Breviario F, Bono F, Balconi G, Compernolle V, Spagnuolo R, Dewerchin M, Zanetti Aet al. Targeted deficiency or cytosolic truncation of the VE-cadherin gene in mice impairs VEGF-mediated endothelial survival and angiogenesis. Cell. 98:1999;147-157.
35. Torres M, Stoykova A, Huber O, Chowdhury K, Bonaldo P, Butz S, Kemler R, Gruss P An α-E-catenin gene trap mutation defines its function in preimplantation development. Proc Natl Acad Sci USA. 94:1997;901-906.
36. Haegel H, Larue L, Ohsugi M, Fedorov L, Herrenknecht K, Kemler R Lack of β-catenin affects mouse development at gastrulation. Development. 121:1995;3529-3537.
37. Ruiz P, Brinkmann V, Ledermann B, Behrend M, Grund C, Vogel F, Birchmeier C, Gunthert U, Franke WW, Birchmeier W Targeted mutation of plakoglobin in mice reveals essential functions of desmosomes in the embryonic heart. J Cell Biol. 135:1996;215-225.
38. Navarro P, Ruco L, Dejana E Differential localization of VE- and N-cadherin in human endothelial cells. VE-cadherin competes with N-cadherin for junctional localization. J Cell Biol. 140:1998;1475-1484.
39. Radice GL, Rayburn H, Matsunami H, Knudsen KA, Takeichi M, Hynes RO Developmental defects in mouse embryos lacking N-cadherin. Dev Biol. 181:1997;64-78.
40. Risau W Mechanisms of angiogenesis. Nature. 386:1997;671-674.
41. DeLisser HM, Christofidou-Solomidou M, Strieter RM, Burdick MD, Robinson CS, Wexler RS, Kerr JS, Garlanda C, Merwin JR, Madri JA, Albelda SM Involvement of endothelial PECAM-1/CD31 in angiogenesis. Am J Pathol. 151:1997;671-677.
42. Duncan GS, Andrew DP, Takimoto H, Kaufman SA, Yoshida HS, Luis de la Pompa J, Elia A, Wakeham A, Karan-Tamir B, Senaldi G Genetic evidence for functional redundancy of platelet/endothelial cell adhesion molecule-1 (PECAM-1): CD31-deficient mice reveal PECAM-1-dependent and PECAM-1-independent functions. J Immunol. 162:1999;3022-3030.
43. Pece NB, Wrana JL, Letarte M Endoglin is an accessory protein that interacts with the signaling receptors complex of multiple members of the transforming growth factor-β superfamily. J Biol Chem. 274:1999;584-594.
44. McAllister KA, Grogg KM, Johnson DW, Gallione CJ, Jackson CE, Helmbold EA, Markel DS, McKinnon WC, Murrell J Endoglin, a TGF-β binding protein of endothelial cells, is the gene for hereditary haemorrhagic telangiectasia type 1. Nat Genet. 8:1994;345-351.
45. Pasquale EB The Eph family of receptors. Curr Opin Cell Biol. 9:1997;608-615.
46. ••].
47. ••] comprehensively comment on the subject of ephrin/Eph and endothelial morphogenesis.
48. ••].
49. Pandey A, Shao H, Marks RM, Polverini PJ, Dixit VM Role of B61, the ligand for the Eck receptor tyrosine kinase, in TNF-α-induced angiogenesis. Science. 268:1995;567-569.
50. Stein E, Lane AA, Cerretti DP, Schoecklmann HO, Schroff AD, Van Etten RL, Daniel TO Eph receptors discriminate specific ligand oligomers to determine alternative signaling complexes, attachment, and assembly responses. Genes Dev. 12:1998;667-678.
51. Daniel TO, Stein E, Cerretti DP, St John PL, Robert B, Abrahamson DR ELK and LERK-2 in developing kidney and microvascular endothelial assembly. Kidney Int Suppl. 57:1996;S73-S81.
52. Bohme B, VandenBos T, Cerretti DP, Park LS, Holtrich U, Strebhardt K Cell-cell adhesion mediated by binding of membrane-anchored ligand LERK-2 to the EPH-related receptor human embryonal kinase 2 promotes tyrosine kinase activity. J Biol Chem. 271:1996;24747-24752.
53. Huynh-Do U, Stein E, Lane AA, Liu H, Cerretti DP, Daniel TO Surface densities of ephrin-B1 determine EphB1-coupled activation of cell attachment through αvβ3 and α5β1 integrins. EMBO J. 18:1999;2165-2173.
54. Winning RS, Scales JB, Sargent TD Disruption of cell adhesion in Xenopus embryos by Pagliaccio, an Eph-class receptor tyrosine kinase. Dev Biol. 179:1996;309-319.
55. Stein E, Cerretti DP, Daniel TO Ligand activation of ELK receptor tyrosine kinase promotes its association with Grb10 and Grb2 in vascular endothelial cells. J Biol Chem. 271:1996;23588-23593.
56. Pandey A, Lazar DF, Saltiel AR, Dixit VM Activation of the Eck receptor protein tyrosine kinase stimulates phosphatidylinositol 3-kinase activity. J Biol Chem. 269:1994;30154-30157.
57. Greenwald I LIN-12/Notch signaling: lessons from worms and flies. Genes Dev. 12:1998;1751-1762.
58. Zimrin AB, Pepper MS, McMahon GA, Nguyen F, Montesano RM, Maciag T An antisense oligonucleotide to the notch ligand jagged enhances fibroblast growth factor-induced angiogenesis in vitro. J Biol Chem. 271:1996;32499-32502.
59. Uyttendaele H, Marazzi G, Wu G, Yan Q, Sassoon D, Kitajewski J Notch4/int-3, a mammary proto-oncogene, is an endothelial cell-specific mammalian Notch gene. Development. 122:1996;2251-2259.
60. Uyttendaele H, Soriano JV, Montesano R, Kitajewski J Notch4 and Wnt-1 proteins function to regulate branching morphogenesis of mammary epithelial cells in an opposing fashion. Dev Biol. 196:1998;204-217.
61. Hidai C, Zupancic T, Penta K, Mikhail A, Kawana M, Quatermous EE, Aoka Y, Fukagawa M, Matsui Y, Platika D Cloning and characterization of developmental endothelial locus-1: an embryonic endothelial cell protein that binds the αvβ3 integrin receptor. Genes Dev. 12:1998;21-33.
62. Penta K, Varner JA, Liaw L, Hidai C, Schatzman R, Quertermous T Del1 induces integrin signaling and angiogenesis by ligation of αvβ3. J Biol Chem. 274:1999;11101-11109. The potential role of the endothelial-specific protein Del1 as a unique autocrine angiogenic factor is discussed here, with a particular reference to previous findings (see [61]).
63. Edelman GM, Jones FS Outside and downstream of the homeobox. J Biol Chem. 268:1993;20683-20686.
64. Boudreau N, Andrews C, Srebrow A, Ravanpay A, Cheresh DA Induction of the angiogenic phenotype by Hox D3. J Cell Biol. 139:1997;257-264.
65. Boudreau N, Bissell MJ Extracellular matrix signaling: integration of form and function in normal and malignant cells. Curr Opin Cell Biol. 10:1998;640-646.
66. Toker A, Cantley LC Signalling through the lipid products of phosphoinositide-3-OH kinase. Nature. 387:1997;673-676.
67. Derman MP, Cunha MJ, Barros EJ, Nigam SK, Cantley LG HGF-mediated chemotaxis and tubulogenesis require activation of the phosphatidylinositol 3-kinase. Am J Physiol. 268:1995;F1211-F1217.
68. Khwaja A, Lehmann K, Marte BM, Downward J Phosphoinositide 3 kinase induces scattering and tubulogenesis in epithelial cells through a novel pathway. J Biol Chem. 273:1998;18793-18801. A detailed analysis of the molecular pathways signaling tubulogenesis and scattering in epithelial cells downstream PI3K. The discussion offers stimulating comments and speculations about the outcomes of different molecular effectors in terms of cellular physiology.
69. Khwaja A, Rodriguez-Viciana P, Wennstrom S, Warne PH, Downward J Matrix adhesion and Ras transformation both activate a phosphoinositide 3-OH kinase and protein kinase B/Akt cellular survival pathway. EMBO J. 16:1997;2783-2793.
70. Chen HC, Guan JL Association of focal adhesion kinase with its potential substrate phosphatidylinositol 3-kinase. Proc Natl Acad Sci USA. 91:1994;10148-10152.
71. Weidner KM, Di Cesare S, Sachs M, Brinkmann V, Behrens J, Birchmeier W Interaction between Gab1 and the c-Met receptor tyrosine kinase is responsible for epithelial morphogenesis. Nature. 384:1996;173-176.
72. •].
73. Fournier TM, Kamikura D, Teng K, Park M Branching tubulogenesis but not scatter of Madin-Darby canine kidney cells requires a functional Grb2 binding site in the Met receptor tyrosine kinase. J Biol Chem. 271:1996;22211-22217.
74. Hordijk PL, ten Klooster JP, van der Kammen RA, Michiels F, Oomen LC, Collard JG Inhibition of invasion of epithelial cells by Tiam1-Rac signaling. Science. 278:1997;1464-1466.
75. Michiels F, Stam JC, Hordijk PL, van der Kammen RA, Ruuls-Van Stalle L, Feltkamp CA, Collard JG Regulated membrane localization of Tiam1, mediated by the NH2-terminal pleckstrin homology domain, is required for Rac-dependent membrane ruffling and C-Jun NH2-terminal kinase activation. J Cell Biol. 137:1997;387-398.
76. •].
77. ••], one can envisage an interplay at the plasma membrane between adhesion molecules at different junctional sites and mitogen-regulated cytoplasmic effectors in determining the 'quiescent versus mophogenic' choice of the cell.
78. Downward J Mechanisms and consequences of activation of protein kinase B/Akt. Curr Opin Cell Biol. 10:1998;262-267.
79. Gerber HP, McMurtrey A, Kowalski J, Yan M, Keyt BA, Ferrara N Vascular endothelial growth factor regulates endothelial cell survival through the phosphatidylinositol 3'-kinase/Akt signal transduction pathway. Requirement for Flk-1/KDR activation. J Biol Chem. 273:1998;30336-30343.
80. Lu PJ, Lu QL, Rughetti A, Taylor-Papadimitriou J Bcl-2 overexpression inhibits cell death and promotes the morphogenesis, but not tumorigenesis of human mammary epithelial cells. J Cell Biol. 129:1995;1363-1378.
81. Bloch W, Forsberg E, Lentini S, Brakebush C, Martin K, Krell HW, Weidle UH, Addicks K, Fassler R β1 integrin is essential for teratoma growth and angiogenesis. J Cell Biol. 139:1997;265-278.
82. Fassler R, Meyer M Consequences of lack of β1 integrin gene expression in mice. Genes Dev. 9:1995;1896-1908.
83. Stephens LE, Sutherland AE, Klimanskaya IV, Andrieux A, Pedersen RA, Damsky CH Deletion of β1 integrins in mice results in inner cell mass failure and peri-implantation lethality. Genes Dev. 9:1995;1883-1895.
84. Hirsch E, Iglesias A, Potocnik AJ, Hartmann U, Fassler R Impaired migration but not differentiation of haematopoietic stem cells in the absence of β1 integrins. Nature. 380:1996;171-175.
85. Senger DR, Claffey KP, Benes JE, Perruzzi CA, Sergiou AP, Detmar M Angiogenesis promoted by vascular endothelial growth factor: regulation through α1β1 and α2β1 integrins. Proc Natl Acad Sci USA. 94:1997;13612-13617.
86. Gardner H, Kreidberg J, Koteliansky V, Jaenisch R Deletion of integrin α1 by homologous recombination permits normal murine development but gives rise to a specific deficit in cell adhesion. Dev Biol. 175:1996;301-313.
87. Enenstein J, Waleh NS, Kramer RH Basic FGF and TGF-beta differentially modulate integrin expression of human microvascular endothelial cells. Exp Cell Res. 203:1992;499-503.
88. Davis GE, Camarillo CW An α2β1 integrin-dependent pinocytic mechanism involving intracellular vacuole formation and coalescence regulates capillary lumen and tube formation in three-dimensional collagen matrix. Exp Cell Res. 224:1996;39-51.
89. Yang JT, Rayburn H, Hynes RO Cell adhesion events mediated by α4 integrins are essential in placental and cardiac development. Development. 121:1995;549-560.
90. Collo G, Pepper MS Endothelial cell integrin α5β1 expression is modulated by cytokines and during migration in vitro. J Cell Sci. 112:1999;569-578.
91. Yang JT, Rayburn H, Hynes RO Embryonic mesodermal defects in α5 integrin-deficient mice. Development. 119:1993;1093-1105.
92. ••]).
93. Defilippi P, Silengo L, Tarone G α6β1 integrin (laminin receptor) is down-regulated by tumor necrosis factor α and interleukin-1 β in human endothelial cells. J Biol Chem. 267:1992;18303-18307.
94. van der Neut R, Calafat J, Niessen CM, Sonnenberg A Epithelial detachment due to absence of hemidesmosomes in integrin β4 null mice. Nat Genet. 13:1996;366-369.