Relevance of endothelial junctions in leukocyte extravasation and vascular permeability

Annals of the New York Academy of Sciences

Volumn 1257, Issue 1, 2012, Pages 184-192

  Vestweber, Dietmar ^a  

^a MAX PLANCK INSTITUTE FOR MOLECULAR BIOMEDICINE   (Germany)

Author keywords

Endothelial junctions; Inflammation; Vascular permeability; VE cadherin

Indexed keywords

ALPHA CATENIN; BETA CATENIN; CD31 ANTIGEN; CD99 ANTIGEN; CHEMOKINE; CYTOKINE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 1BETA; PROTEIN TYROSINE KINASE; PROTEIN TYROSINE PHOSPHATASE; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; VASCULAR ENDOTHELIAL CADHERIN;

BLOOD VESSEL PERMEABILITY; BLOOD VESSEL WALL; CELL HOMING; CELL INTERACTION; DIAPEDESIS; ENDOTHELIUM CELL; EXTRAVASATION; HUMAN; IMMUNOSURVEILLANCE; IN VIVO STUDY; INFLAMMATION; LEUKOCYTE; LEUKOCYTE ADHERENCE; LEUKOCYTE MIGRATION; LYMPHOCYTE; MONOCYTE; NEUTROPHIL; NONHUMAN; REVIEW; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIUM;

EID: 84861986064     PISSN: 00778923     EISSN: 17496632     Source Type: Book Series    
DOI: 10.1111/j.1749-6632.2012.06558.x     Document Type: Review

References (62)

1. Ley, K. et al. 2007. Getting to the site of inflammation: the leukocyte adhesion cascade updated. Nat. Rev. Immunol. 7: 678-689.
2. Kvietys, P.R. & M. Sandig. 2001. Neutrophil diapedesis: paracellular or transcellular. News Physiol. Sci. 16: 15-19.
3. Muller, W.A. 2001. Migration of leukocytes across endothelial junctions: some concepts and controversies. Microcirculation 8: 181-193.
4. Muller, W.A. 2003. Leukocyte-endothelial-cell interactions in leukocyte transmigration and the inflammatory response. Trends Immunol. 24: 326-333.
5. Carman, C.V. & T.A. Springer. 2004. A transmigratory cup in leukocyte diapedesis both through individual vascular endothelial cells and between them. J. Cell Biol. 167: 377-388.
6. Carman, C.V. et al. 2007. Transcellular diapedesis is initiated by invasive podosomes. Immunity 26: 784-797.
7. Carman, C.V. & T.A. Springer. 2008. Trans-cellular migration: cell-cell contacts get intimate. Curr. Opin. Cell Biol. 20: 1-8.
8. Yang, L. et al. 2005. ICAM-1 regulates neutrophil adhesion and transcellular migration of TNF-alpha-activated vascular endothelium under flow. Blood 106: 584-592.
9. Millan, J.L. et al. 2006. Lymphocyte transcellular migration occurs through recruitment of endothelial ICAM-1 to caveola- and F-actin-rich domains. Nat. Cell Biol. 8: 113-123.
10. Feng, D. et al. 2002. Ultrastructural studies define soluble macromolecular, particulate, and cellular transendothelial cell pathways in venules, lymphatic vessels, and tumor-associated microvessels in man and animals. Microsc. Res. Tech. 57: 289-326.
11. Wittchen, E.S. et al. 2005. Rap1 GTPase inhibits leukocyte transmigration by promoting endothelial barrier function. J. Biol. Chem. 280: 11675-11682.
12. Vestweber, D. 2007. Adhesion and signaling molecules controlling the transmigration of leukocytes through endothelium. Immunol. Rev. 218: 178-196.
13. Muller, W.A. 2011. Mechanisms of leukocyte transendothelial migration. Annu. Rev. Pathol. 6: 323-344.
14. Mamdouh, Z., A. Mikhailov & W.A. Muller. 2009. Transcellular migration of leukocytes is mediated by the endothelial lateral border recycling compartment. J. Exp. Med. 206: 2795-2808.
15. Schoefl, G.I. 1972. The migration of lymphocytes across the vascular endothelium in lymphoid tissue. A reexamination. J. Exp. Med. 136: 568-588.
16. Marchesi, V. 1961. The site of leukocyte emigration during inflammation. Q. J. Exp. Physiol. Cogn. Med. Sci. 46: 115-118.
17. Anderson, A.O. & N.D. Anderson. 1976. Lymphocyte emigration from high endothelial venules in rat lymph nodes. Immunology 31: 731-748.
18. Feng, D. et al. 1998. Neutrophils emigrate from venules by a transendothelial cell pathway in response to FMLP. J. Exp. Med. 187: 903-915.
19. Hoshi, O. & T. Ushiki. 1999. Scanning electron microscopic studies on the route of neutrophil extravasation in the mouse after exposure to the chemotactic peptide N-formyl-methionyl-leucyl-phenylalanine (fMLP). Arch. Histol. Cytol. 62: 253-260.
20. Farr, A.G. & P.P.H. DeBruyn. 1975. The mode of lymphocyte migration through postcapillary venule endothelium in lymph node. Am. J. Anat. 143: 55-92.
21. Marchesi, V.T. & J.L. Gowans. 1964. The migration of lymphocytes through the endothelium of venules in lymph nodes: an electron microscope study. Proc. R. Soc. Lond. B. Biol. Sci. 159: 283-290.
22. Fujita, S. et al. 1991. An ultrastructural study of in vivo interactions between lymphocytes and endothelial cells in the pathogenesis of the vascular leak syndrome induced by interleukin-2. Cancer 68: 2169-2174.
23. Wolburg, H., K. Wolburg-Buchholz & B. Engelhardt. 2005. Diapedesis of mononuclear cells across cerebral venules during experimental autoimmune encephalomyelitis leaves tight junctions intact. Acta Neuropathol. (Berl). 109: 181-190.
24. Hurley, J. & N. Xeros. 1961. Electron microscopic observation on the emigration of leukocytes. Austral. J. Exp. Biol. Med. Sci. 39: 609-624.
25. Chamberlain, J.K. & M.A. Lichtman. 1978. Marrow cell egress: specificity of the site of penetration into the sinus. Blood 52: 959-968.
26. Woodfin, A. et al. 2011. The junctional adhesion molecule JAM-C regulates polarized transendothelial migration of neutrophils in vivo. Nat. Immunol. 12: 761-769.
27. Riethmuller, C., I. Nasdala & D. Vestweber. 2008. Nano-surgery at the leukocyte-endothelial docking site. Pflugers Arch. (Eur. J. Physiol.). 456: 71-81.
28. Schulte, D. et al. 2011. Stabilizing the VE-cadherin-catenin complex blocks leukocyte extravasation and vascular permeability. EMBO J 30: 4157-4170.
29. Gotsch, U. et al. 1997. VE-cadherin antibody accelerates neutrophil recruiment in vivo. J. Cell Sci. 110: 583-588.
30. Corada, M. et al. 1999. Vascular endothelial-cadherin is an important determinant of microvascular integrity in vivo. Proc. Natl. Acad. Sci. USA 96: 9815-9820.
31. Monaghan-Benson, E. & K. Burridge. 2009. The regulation of vascular endothelial growth factor-induced microvascular permeability requires Rac and reactive oxygen species. J. Biol. Chem. 284: 25602-25611.
32. Nagafuchi, A., S. Ishihara & S. Tsukita. 1994. The roles of catenins in the cadherin-mediated cell adhesion: functional analysis of E-cadherin-alpha catenin fusion molecules. J. Cell Biol. 127: 235-245.
33. Ozawa, M. & R. Kemler. 1998. Altered cell adhesion activity by pervanadate due to the dissociation of alpha-catenin from the E-cadherin-catenin complex. J. Biol. Chem. 273: 6166-6170.
34. Yamada, S. et al. 2005. Deconstructing the cadherin-catenin-actin complex. Cell 123: 889-901.
35. Drees, F. et al. 2005. Alpha-catenin is a molecular switch that binds E-cadherin-beta-catenin and regulates actin-filament assembly. Cell 123: 903-915.
36. Allingham, M.J., J.D. van Buul & K. Burridge. 2007. ICAM-1-mediated, Src- and Pyk2-dependent vascular endothelial cadherin tyrosine phosphorylation is required for leukocyte transendothelial migration. J. Immunol. 179: 4053-4064.
37. Turowski, P. et al. 2008. Phosphorylation of vascular endothelial cadherin controls lymphocyte emigration. J. Cell Sci. 121: 29-37.
38. Adam, A.P. et al. 2010. SRC-induced tyrosine phosphorylation of VE-cadherin is not sufficient to decrease barrier function of endothelial monolayers. J. Biol. Chem. 285: 7045-7055.
39. van Buul, J.D. et al. 2005. Proline-rich tyrosine kinase 2 (Pyk2) mediates vascular endothelial-cadherin-based cell-cell adhesion by regulating beta-catenin tyrosine phosphorylation. J. Biol. Chem. 280: 21129-21136.
40. van Wetering, S. et al. 2003. VCAM-1-mediated Rac signaling controls endothelial cell-cell contacts and leukocyte transmigration. Am. J. Physiol. Cell Physiol. 285: C343-352.
41. Martinelli, R. et al. 2009. ICAM-1-mediated endothelial nitric oxide synthase activation via calcium and AMP-activated protein kinase is required for transendothelial lymphocyte migration. Mol. Biol. Cell 20: 995-1005.
42. Shaw, S.K. et al. 2001. Real-time imaging of vascular endothelial-cadherin during leukocyte transmigration across endothelium. J. Immunol. 167: 2323-2330.
43. Sumagin, R. & I.H. Sarelius. 2010. Intercellular adhesion molecule-1 enrichment near tricellular endothelial junctions is preferentially associated with leukocyte transmigration and signals for reorganization of these junctions to accommodate leukocyte passage. J. Immunol. 184: 5242-5252.
44. Strey, A. et al. 2002. Endothelial Rho signaling is required for monocyte transendothelial migration. FEBS Letters 517: 261-266.
45. Saito, H. et al. 1998. Endothelial myosin light chain kinase regulates neutrophil migration across human umbilical vein endothelial cell monolayer. J. Immunol. 161: 1533-1540.
46. Saito, H. et al. 2002. Endothelial Rho and Rho kinase regulate neutrophil migration via endothelial myosin light chain phosphorylation. J. Leuk. Biol. 72: 829-836.
47. Garcia, J.G. et al. 1998. Adherent neutrophils activate endothelial myosin light chain kinase: role in transendothelial migration. J. Appl. Physiol. 84: 1817-1821.
48. Stroka, K.M. & H. Aranda-Espinoza. 2011. Endothelial cell substrate stiffness influences neutrophil transmigration via myosin light chain kinase-dependent cell contraction. Blood 118: 1632-1640.
49. Bertuglia, S. & A. Colantuoni. 2000. Protective effects of leukopenia and tissue plasminogen activator in microvascular ischemia-reperfusion injury. Am. J. Physiol. Heart Circ. Physiol. 278: H755-H761.
50. Sumagin, R., E. Lomakina & I.H. Sarelius. 2008. Leukocyte-endothelial cell intercations are linked to vascular permeability via ICAM-1-mediated signaling. Am. J. Physiol. Heart Circ. Physiol. 295.
51. Baluk, P. et al. 1998. Endothelial gaps and adherent leukocytes in allergen-induced early- and late-phase plasma leakage in rat airways. Am. J. Pathol. 152: 1463-1476.
52. Kim, M.H., F.R. Curry & S.I. Simon. 2009. Dynamics of neutrophil extravasation and vascular permeability are uncoupled during aseptic cutaneous wounding. Am. J. Physiol. Cell Physiol. 296: C848-C856.
53. He, P. 2010. Leukocyte/endothelium intercations and microvessel permeability: coupled or uncoupled? Cardiovasc. Res. 87: 281-290.
54. Phillipson, M. et al. 2008. Endothelial domes encapsulate adherent neutrophils and minimize increases in vascular permeability in paracellular and transcellular emigration. PLoS ONE 3: e1649.
55. Fachinger, G., U. Deutsch & W. Risau. 1999. Functional interaction of vascular endothelial-protein-tyrosine phosphatase with the angiopoietin receptor Tie-2. Oncogene 18: 5948-5953.
56. Baumer, S. et al. 2006. Vascular endothelial cell specific phospho-tyrosine phosphatase (VE-PTP) activity is required for blood vessel development. Blood 107: 4754-4762.
57. Nawroth, R. et al. 2002. VE-PTP and VE-cadherin ectodomains interact to facilitate regulation of phosphorylation and cell contacts. EMBO J. 21: 4885-4895.
58. Nottebaum, A.F. et al. 2008. VE-PTP maintains the endothelial barrier via plakoglobin and becomes dissociated from VE-cadherin by leukocytes and by VEGF. J. Exp. Med. 205: 2929-2945.
59. Ukropec, J.A. et al. 2000. SHP2 association with VE-cadherin complexes in human endothelial cells is regulated by thrombin. J. Biol. Chem. 275: 5983-5986.
60. Grinnell, K.L., B. Casserly & E.O. Harrington. 2010. Role of protein tyrosine phosphatase SHP2 in barrier function of pulmonary endothelium. Am. J. Physiol. Lung Cell Mol. Physiol. 298: L361-370.
61. Sui, X.F. et al. 2005. Receptor protein tyrosine phosphatase micro regulates the paracellular pathway in human lung microvascular endothelia. Am. J. Pathol. 166: 1247-1258.
62. Broermann, A. et al. 2011. Dissociation of VE-PTP from VE-cadherin is required for leukocyte extravasation and for VEGF-induced vascular permeability in vivo. J. Exp. Med. 208: 2393-2401.