Pathogenic hantaviruses Andes virus and Hantaan virus induce adherens junction disassembly by directing vascular endothelial cadherin internalization in human endothelial cell

Journal of Virology

Volumn 84, Issue 14, 2010, Pages 7405-7411

  Gorbunova, Elena ^a   Gavrilovskaya, Irina N ^a   Mackow, Erich R ^a  

^a STONY BROOK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOPOIETIN 1; SPHINGOSINE 1 PHOSPHATE; VASCULAR ENDOTHELIAL CADHERIN; VASCULOTROPIN C;

ANDES VIRUS; ARTICLE; CAPILLARY PERMEABILITY; CELL JUNCTION; ENDOTHELIUM CELL; HANTAVIRUS; HUMAN; HYPOXEMIA; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; TULA VIRUS; VIRUS INFECTION;

ADHERENS JUNCTIONS; ANGIOPOIETIN-1; ANTIGENS, CD; CADHERINS; CELLS, CULTURED; ENDOTHELIAL CELLS; HANTAAN VIRUS; HANTAVIRUS; HUMANS; LYSOPHOSPHOLIPIDS; SPHINGOSINE; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

ANDES VIRUS; HANTAAN VIRUS; HANTAVIRUS; TULA VIRUS;

EID: 77953763318     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00576-10     Document Type: Article

References (63)

1. Aird, W. C. 2004. Endothelium as an organ system. Crit. Care Med. 32:S271-S279.
2. Berger, M. M., C. Hesse, C. Dehnert, H. Siedler, P. Kleinbongard, H. J. Bardenheuer, M. Kelm, P. Bartsch, and W. E. Haefeli. 2005. Hypoxia impairs systemic endothelial function in individuals prone to high-altitude pulmonary edema. Am. J. Respir. Crit. Care Med. 172:763-767.
3. Borges, E., Y. Jan, and E. Ruoslahti. 2000. Platelet-derived growth factor receptor beta and vascular endothelial growth factor receptor 2 bind to the beta 3 integrin through its extracellular domain. J. Biol. Chem. 275:39867-39873.
4. Bustamante, E. A., H. Levy, and S. Q. Simpson. 1997. Pleural fluid characteristics in hantavirus pulmonary syndrome. Chest 112:1133-1136. (Pubitemid 27446346)
5. Byzova, T. V., C. K. Goldman, N. Pampori, K. A. Thomas, A. Bett, S. J. Shattil, and E. F. Plow. 2000. A mechanism for modulation of cellular responses to VEGF: activation of the integrins. Mol. Cell 6:851-860.
6. Calvete, J. J. 1999. Platelet integrin GPIIb/IIIa: structure-function correlations. An update and lessons from other integrins. Proc. Soc. Exp. Biol. Med. 222:29-38.
7. Chang, B., M. Crowley, M. Campen, and F. Koster. 2007. Hantavirus cardiopulmonary syndrome. Semin. Respir. Crit. Care Med. 28:193-200.
8. Coller, B. S., and S. J. Shattil. 2008. The GPIIb/IIIa (integrin alphaIIbbeta3) odyssey: a technology-driven saga of a receptor with twists, turns, and even a bend. Blood 112:3011-3025.
9. Dehler, M., E. Zessin, P. Bartsch, and H. Mairbaurl. 2006. Hypoxia causes permeability oedema in the constant-pressure perfused rat lung. Eur. Respir. J. 27:600-606.
10. Dejana, E., F. Orsenigo, and M. G. Lampugnani. 2008. The role of adherens junctions and VE-cadherin in the control of vascular permeability. J. Cell Sci. 121:2115-2122.
11. Duchin, J. S., F. T. Koster, C. J. Peters, G. L. Simpson, B. Tempest, S. R. Zaki, T. G. Ksiazek, P. E. Rollin, S. Nichol, E. T. Umland, R. L. Moolenaar, S. E. Reef, K. B. Nolte, M. M. Gallaher, J. C. Butler, R. F. Breiman, and H. S. Group. 1994. Hantavirus pulmonary syndrome: a clinical description of 17 patients with a newly recognized disease. The Hantavirus Study Group. N. Engl. J. Med. 330:949-955.
12. Dvorak, H. F. 2006. Discovery of vascular permeability factor (VPF). Exp. Cell Res. 312:522-526.
13. Dvorak, H. F., L. F. Brown, M. Detmar, and A. M. Dvorak. 1995. Vascular permeability factor/vascular endothelial growth factor, microvascular hyperpermeability, and angiogenesis. Am. J. Pathol. 146:1029-1039.
14. Dvorak, H. F., T. M. Sioussat, L. F. Brown, B. Berse, J. A. Nagy, A. Sotrel, E. J. Manseau, L. Van de Water, and D. R. Senger. 1991. Distribution of vascular permeability factor (vascular endothelial growth factor) in tumors: concentration in tumor blood vessels. J. Exp. Med. 174:1275-1278.
15. Forsythe, J. A., B. H. Jiang, N. V. Iyer, F. Agani, S. W. Leung, R. D. Koos, and G. L. Semenza. 1996. Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol. Cell. Biol. 16:4604-4613.
16. Gamble, J. R., J. Drew, L. Trezise, A. Underwood, M. Parsons, L. Kasminkas, J. Rudge, G. Yancopoulos, and M. A. Vadas. 2000. Angiopoietin-1 is an antipermeability and anti-inflammatory agent in vitro and targets cell junctions. Circ. Res. 87:603-607.
17. Gavard, J., and J. S. Gutkind. 2006. VEGF controls endothelial-cell permeability by promoting the beta-arrestin-dependent endocytosis of VE-cadherin. Nat. Cell Biol. 8:1223-1234.
18. Gavard, J., V. Patel, and J. S. Gutkind. 2008. Angiopoietin-1 prevents VEGF-induced endothelial permeability by sequestering Src through mDia. Dev. Cell 14:25-36.
19. Gavrilovskaya, I., E. E. Gorbunova, and E. R. Mackow. 2010. Pathogenic hantaviruses direct the adherence of quiescent platelets to infected endothelial cells. J. Virol. 84:4832-4839.
20. Gavrilovskaya, I., T. Peresleni, E. Geimonen, and E. Mackow. 2002. Pathogenic hantaviruses selectively inhibit beta3 integrin directed endothelial cell migration. Arch. Virol. 147:1913-1931.
21. 3 integrins. J. Virol. 73:3951-3959.
22. Gavrilovskaya, I. N., E. E. Gorbunova, N. A. Mackow, and E. R. Mackow. 2008. Hantaviruses direct endothelial cell permeability by sensitizing cells to the vascular permeability factor VEGF, while angiopoietin 1 and sphingosine 1-phosphate inhibit hantavirus-directed permeability. J. Virol. 82: 5797-5806.
23. Gavrilovskaya, I. N., M. Shepley, R. Shaw, M. H. Ginsberg, and E. R. Mackow. 1998. Beta3 integrins mediate the cellular entry of hantaviruses that cause respiratory failure. Proc. Natl. Acad. Sci. U. S. A. 95:7074-7079.
24. Hodivala-Dilke, K. M., K. P. McHugh, D. A. Tsakiris, H. Rayburn, D. Crowley, M. Ullman-Cullere, F. P. Ross, B. S. Coller, S. Teitelbaum, and R. O. Hynes. 1999. Beta3-integrin-deficient mice are a model for Glanzmann thrombasthenia showing placental defects and reduced survival. J. Clin. Invest. 103:229-238.
25. Holmes, K., O. L. Roberts, A. M. Thomas, and M. J. Cross. 2007. Vascular endothelial growth factor receptor-2: structure, function, intracellular signalling and therapeutic inhibition. Cell. Signal. 19:2003-2012.
26. Hynes, R. O., B. L. Bader, and K. Hodivala-Dilke. 1999. Integrins in vascular development. Braz. J. Med. Biol. Res. 32:501-510.
27. Igarashi, J., P. A. Erwin, A. P. Dantas, H. Chen, and T. Michel. 2003. VEGF induces S1P1 receptors in endothelial cells: implications for cross-talk between sphingolipid and growth factor receptors. Proc. Natl. Acad. Sci. U. S. A. 100:10664-10669.
28. Jain, R. K., and L. L. Munn. 2000. Leaky vessels? Call Ang1! Nat. Med. 6:131-132.
29. Kaner, R. J., J. V. Ladetto, R. Singh, N. Fukuda, M. A. Matthay, and R. G. Crystal. 2000. Lung overexpression of the vascular endothelial growth factor gene induces pulmonary edema. Am. J. Respir. Cell Mol. Biol. 22:657-664.
30. Kevil, C. G., D. K. Payne, E. Mire, and J. S. Alexander. 1998. Vascular permeability factor/vascular endothelial cell growth factor-mediated permeability occurs through disorganization of endothelial junctional proteins. J. Biol. Chem. 273:15099-15103.
31. Lahdevirta, J. 1982. Clinical features of HFRS in Scandinavia as compared with East Asia. Scand. J. Infect. Dis. Suppl. 36:93-95.
32. Lampugnani, M. G., and E. Dejana. 2007. Adherens junctions in endothelial cells regulate vessel maintenance and angiogenesis. Thromb. Res. 120(Suppl. 2):S1-S6.
33. Lampugnani, M. G., and E. Dejana. 2007. The control of endothelial cell functions by adherens junctions. Novartis Found. Symp. 283:4-13.
34. Lampugnani, M. G., F. Orsenigo, M. C. Gagliani, C. Tacchetti, and E. Dejana. 2006. Vascular endothelial cadherin controls VEGFR-2 internalization and signaling from intracellular compartments. J. Cell Biol. 174:593-604.
35. Luo, B. H., J. Karanicolas, L. D. Harmacek, D. Baker, and T. A. Springer. 2009. Rationally designed integrin beta3 mutants stabilized in the high affinity conformation. J. Biol. Chem. 284:3917-3924.
36. Mackow, E. R., and I. N. Gavrilovskaya. 2001. Cellular receptors and hantavirus pathogenesis. Curr. Top. Microbiol. Immunol. 256:91-115.
37. Mahabeleshwar, G. H., W. Feng, K. Reddy, E. F. Plow, and T. V. Byzova. 2007. Mechanisms of integrin-vascular endothelial growth factor receptor cross-activation in angiogenesis. Circ. Res. 101:570-580.
38. Manalo, D. J., A. Rowan, T. Lavoie, L. Natarajan, B. D. Kelly, S. Q. Ye, J. G. Garcia, and G. L. Semenza. 2005. Transcriptional regulation of vascular endothelial cell responses to hypoxia by HIF-1. Blood 105:659-669. (Pubitemid 40070750)
39. 3 integrins is determined by an L33P substitution in the PSI domain. J. Virol. 84:352-360.
40. McVerry, B. J., and J. G. Garcia. 2004. Endothelial cell barrier regulation by sphingosine 1-phosphate. J. Cell. Biochem. 92:1075-1085.
41. Nawroth, R., G. Poell, A. Ranft, S. Kloep, U. Samulowitz, G. Fachinger, M. Golding, D. T. Shima, U. Deutsch, and D. Vestweber. 2002. VE-PTP and VE-cadherin ectodomains interact to facilitate regulation of phosphorylation and cell contacts. EMBO J. 21:4885-4895.
42. Nolte, K. B., R. M. Feddersen, K. Foucar, S. R. Zaki, F. T. Koster, D. Madar, T. L. Merlin, P. J. McFeeley, E. T. Umland, and R. E. Zumwalt. 1995. Hantavirus pulmonary syndrome in the United States: a pathological description of a disease caused by a new agent. Hum. Pathol. 26:110-120.
43. Olsson, A. K., A. Dimberg, J. Kreuger, and L. Claesson-Welsh. 2006. VEGF receptor signalling - in control of vascular function. Nat. Rev. Mol. Cell Biol. 7:359-371.
44. Pensiero, M. N., J. B. Sharefkin, C. W. Dieffenbach, and J. Hay. 1992. Hantaan virus infection of human endothelial cells. J. Virol. 66:5929-5936.
45. Pizurki, L., Z. Zhou, K. Glynos, C. Roussos, and A. Papapetropoulos. 2003. Angiopoietin-1 inhibits endothelial permeability, neutrophil adherence and IL-8 production. Br. J. Pharmacol. 139:329-336.
46. Raymond, T., E. Gorbunova, I. N. Gavrilovskaya, and E. R. Mackow. 2005. Pathogenic hantaviruses bind plexin-semaphorin-integrin domains present at the apex of inactive, bent alphavbeta3 integrin conformers. Proc. Natl. Acad. Sci. U. S. A. 102:1163-1168.
47. Reynolds, L. E., L. Wyder, J. C. Lively, D. Taverna, S. D. Robinson, X. Huang, D. Sheppard, R. O. Hynes, and K. M. Hodivala-Dilke. 2002. Enhanced pathological angiogenesis in mice lacking beta3 integrin or beta3 and beta5 integrins. Nat. Med. 8:27-34.
48. Robinson, S. D., L. E. Reynolds, L. Wyder, D. J. Hicklin, and K. M. Hodivala- Dilke. 2004. Beta3-integrin regulates vascular endothelial growth factor-A-dependent permeability. Arterioscler. Thromb. Vasc. Biol. 24:2108-2114.
49. Schaphorst, K. L., E. Chiang, K. N. Jacobs, A. Zaiman, V. Natarajan, F. Wigley, and J. G. Garcia. 2003. Role of sphingosine-1 phosphate in the enhancement of endothelial barrier integrity by platelet-released products. Am. J. Physiol. Lung Cell. Mol. Physiol. 285:L258-L267.
50. Schmaljohn, C., and B. Hjelle. 1997. Hantaviruses: a global disease problem. Emerg. Infect. Dis. 3:95-104.
51. Soldi, R., S. Mitola, M. Strasly, P. Defilippi, G. Tarone, and F. Bussolino. 1999. Role of alphavbeta3 integrin in the activation of vascular endothelial growth factor receptor-2. EMBO J. 18:882-892. (Pubitemid 29082268)
52. Stenmark, K. R., K. A. Fagan, and M. G. Frid. 2006. Hypoxia-induced pulmonary vascular remodeling: cellular and molecular mechanisms. Circ. Res. 99:675-691.
53. Takagi, J., B. M. Petre, T. Walz, and T. A. Springer. 2002. Global conformational rearrangements in integrin extracellular domains in outside-in and inside-out signaling. Cell 110:599-611. (Pubitemid 35247840)
54. Thurston, G., C. Suri, K. Smith, J. McClain, T. N. Sato, G. D. Yancopoulos, and D. M. McDonald. 1999. Leakage-resistant blood vessels in mice transgenically overexpressing angiopoietin-1. Science 286:2511-2514.
55. Valbuena, G., and D. H. Walker. 2006. The endothelium as a target for infections. Annu. Rev. Pathol. 1:171-198.
56. Voelkel, N. F., R. W. Vandivier, and R. M. Tuder. 2006. Vascular endothelial growth factor in the lung. Am. J. Physiol. Lung Cell. Mol. Physiol. 290:L209-L221.
57. Wallez, Y., I. Vilgrain, and P. Huber. 2006. Angiogenesis: the VE-cadherin switch. Trends Cardiovasc. Med. 16:55-59.
58. Wang, Y., G. Jin, H. Miao, J. Y. Li, S. Usami, and S. Chien. 2006. Integrins regulate VE-cadherin and catenins: dependence of this regulation on Src, but not on Ras. Proc. Natl. Acad. Sci. U. S. A. 103:1774-1779.
59. Wang, Y., S. Pampou, K. Fujikawa, and L. Varticovski. 2004. Opposing effect of angiopoietin-1 on VEGF-mediated disruption of endothelial cell-cell interactions requires activation of PKC beta. J. Cell. Physiol. 198:53-61.
60. Weis, S. M., and D. A. Cheresh. 2005. Pathophysiological consequences of VEGF-induced vascular permeability. Nature 437:497-504.
61. Yanagihara, R., and D. J. Silverman. 1990. Experimental infection of human vascular endothelial cells by pathogenic and nonpathogenic hantaviruses. Arch. Virol. 111:281-286.
62. Zaki, S., P. Greer, L. Coffield, C. Goldsmith, K. Nolte, K. Foucar, R. Feddersen, R. Zumwalt, G. Miller, P. Rollin, T. Ksiazek, S. Nichol, and C. Peters. 1995. Hantavirus pulmonary syndrome: pathogenesis of an emerging infectious disease. Am. J. Pathol. 146:552-579.
63. Zanetti, A., M. G. Lampugnani, G. Balconi, F. Breviario, M. Corada, L. Lanfrancone, and E. Dejana. 2002. Vascular endothelial growth factor induces SHC association with vascular endothelial cadherin: a potential feedback mechanism to control vascular endothelial growth factor receptor-2 signaling. Arterioscler. Thromb. Vasc. Biol. 22:617-622.