VEGFR2 and Src kinase inhibitors suppress Andes virus-induced endothelial cell permeability

Journal of Virology

Volumn 85, Issue 5, 2011, Pages 2296-2303

  Gorbunova, Elena E ^a   Gavrilovskaya, Irina N ^a   Pepini, Timothy ^a   Mackow, Erich R ^a  

^a STONY BROOK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINO 7 TERT BUTYL 5 (4 METHYLPHENYL)PYRAZOLO[3,4 D]PYRIMIDINE; BOSUTINIB; DASATINIB; GSK VEG10003; PAZOPANIB; PROTEIN TYROSINE KINASE; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; VASCULAR ENDOTHELIAL CADHERIN; VASCULOTROPIN RECEPTOR 2;

ANDES VIRUS; ARTICLE; BLEEDING; BLOOD VESSEL PERMEABILITY; CAPILLARY PERMEABILITY; CELL JUNCTION; CELL MEMBRANE PERMEABILITY; COMPETITIVE INHIBITION; CONTROLLED STUDY; DRUG EFFICACY; ENDOTHELIUM CELL; FOOD AND DRUG ADMINISTRATION; HANTAVIRUS; HANTAVIRUS PULMONARY SYNDROME; HUMAN; HUMAN CELL; IC 50; LUNG EDEMA; NEUROLOGIC DISEASE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN TARGETING; REGULATORY MECHANISM; RNA VIRUS;

CELL LINE; DOWN-REGULATION; ENDOTHELIAL CELLS; HANTAVIRUS; HANTAVIRUS PULMONARY SYNDROME; HUMANS; PERMEABILITY; PROTEIN KINASE INHIBITORS; RNA INTERFERENCE; SRC-FAMILY KINASES; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

ANDES VIRUS; HANTAVIRUS;

EID: 79551692297     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02319-10     Document Type: Article

References (98)

1. Adjei, A. A. 2007. Novel small-molecule inhibitors of the vascular endothelial growth factor receptor. Clin. Lung Cancer 8(Suppl. 2):S74-S78. (Pubitemid 46569721)
2. Aleshin, A., and R. S. Finn. 2010. SRC: a century of science brought to the clinic. Neoplasia 12:599-607.
3. Bain, J., et al. 2007. The selectivity of protein kinase inhibitors: a further update. Biochem. J. 408:297-315.
4. Basu, A., and U. C. Chaturvedi. 2008. Vascular endothelium: the battlefield of dengue viruses. FEMS Immunol. Med. Microbiol. 53:287-299.
5. Berger, M. M., et al. 2005. Hypoxia impairs systemic endothelial function in individuals prone to high-altitude pulmonary edema. Am. J. Respir. Crit. Care Med. 172:763-767.
6. 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.
7. Bustamante, E. A., H. Levy, and S. Q. Simpson. 1997. Pleural fluid characteristics in hantavirus pulmonary syndrome. Chest 112:1133-1136.
8. Chang, B., M. Crowley, M. Campen, and F. Koster. 2007. Hantavirus cardiopulmonary syndrome. Semin. Respir. Crit. Care Med. 28:193-200.
9. Corada, M., et al. 1999. Vascular endothelial-cadherin is an important determinant of microvascular integrity in vivo. Proc. Natl. Acad. Sci. U. S. A. 96:9815-9820.
10. 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.
11. 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.
12. Duchin, J. S., et al. 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.
13. Dvorak, H. F. 2006. Discovery of vascular permeability factor (VPF). Exp. Cell Res. 312:522-526. (Pubitemid 43290329)
14. 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.
15. Dvorak, H. F., et al. 1991. Distribution of vascular permeability factor (vascular endothelial growth factor) in tumors: concentration in tumor blood vessels. J. Exp. Med. 174:1275-1278.
16. Eliceiri, B. P., et al. 1999. Selective requirement for Src kinases during VEGF-induced angiogenesis and vascular permeability. Mol. Cell 4:915-924. (Pubitemid 30054898)
17. Enria, D., et al. 1996. Hantavirus pulmonary syndrome in Argentina. Possibility of person to person transmission. Medicina 56:709-711.
18. Forsythe, J. A., et al. 1996. Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol. Cell. Biol. 16:4604-4613.
19. Galeno, H., et al. 2002. First human isolate of Hantavirus (Andes virus) in the Americas. Emerg. Infect. Dis. 8:657-661.
20. Gamble, J. R., et al. 2000. Angiopoietin-1 is an antipermeability and antiinflammatory agent in vitro and targets cell junctions. Circ. Res. 87:603-607.
21. Garcia, J. G., et al. 2001. Sphingosine 1-phosphate promotes endothelial cell barrier integrity by Edg-dependent cytoskeletal rearrangement. J. Clin. Invest. 108:689-701.
22. Gavard, J. 2009. Breaking the VE-cadherin bonds. FEBS Lett. 583:1-6.
23. 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.
24. 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.
25. Gavrilovskaya, I. N., E. J. Brown, M. H. Ginsberg, and E. R. Mackow. 1999. Cellular entry of hantaviruses which cause hemorrhagic fever with renal syndrome is mediated by beta3 integrins. J. Virol. 73:3951-3959.
26. Gavrilovskaya, I. N., 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.
27. 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.
28. Gavrilovskaya, I. N., T. Peresleni, E. Geimonen, and E. R. Mackow. 2002. Pathogenic hantaviruses selectively inhibit beta3 integrin directed endothelial cell migration. Arch. Virol. 147:1913-1931.
29. 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.
30. Geimonen, E., et al. 2002. Pathogenic and nonpathogenic hantaviruses differentially regulate endothelial cell responses. Proc. Natl. Acad. Sci. U. S. A. 99:13837-13842.
31. Gorbunova, E., I. N. Gavrilovskaya, and E. R. Mackow. 2010. Pathogenic hantaviruses Andes virus and Hantaan virus induce adherens junction disassembly by directing vascular endothelial cadherin internalization in human endothelial cells. J. Virol. 84:7405-7411.
32. Hallin, G. W., et al. 1996. Cardiopulmonary manifestations of hantavirus pulmonary syndrome. Crit. Care Med. 24:252-258.
33. Hegedus, C., et al. 2009. Interaction of nilotinib, dasatinib and bosutinib with ABCB1 and ABCG2: implications for altered anti-cancer effects and pharmacological properties. Br. J. Pharmacol. 158:1153-1164.
34. 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.
35. Hooper, J. W., T. Larsen, D. M. Custer, and C. S. Schmaljohn. 2001. A lethal disease model for hantavirus pulmonary syndrome. Virology 289:6-14.
36. Huggins, J. W., et al. 1991. Prospective, double-blind, concurrent, placebo-controlled clinical trial of intravenous ribavirin therapy of hemorrhagic fever with renal syndrome. J. Infect. Dis. 164:1119-1127.
37. Iwamoto, F. M., et al. 2010. Phase II trial of pazopanib (GW786034), an oral multi-targeted angiogenesis inhibitor, for adults with recurrent glioblastoma (North American Brain Tumor Consortium Study 06-02). Neuro Oncol. 12:855-861.
38. Jain, R. K., and L. L. Munn. 2000. Leaky vessels? Call Ang1! Nat. Med. 6:131-132.
39. Johnson, F. M., et al. 2010. Phase 1 pharmacokinetic and drug-interaction study of dasatinib in patients with advanced solid tumors. Cancer 116:1582-1591.
40. Jones, C. A., et al. 2008. Robo4 stabilizes the vascular network by inhibiting pathologic angiogenesis and endothelial hyperpermeability. Nat. Med. 14:448-453.
41. Jonsson, C. B., J. Hooper, and G. Mertz. 2008. Treatment of hantavirus pulmonary syndrome. Antiviral Res. 78:162-169.
42. Kaner, R. J., et al. 2000. Lung overexpression of the vascular endothelial growth factor gene induces pulmonary edema. Am. J. Respir. Cell Mol. Biol. 22:657-664.
43. Kantarjian, H., E. Jabbour, J. Grimley, and P. Kirkpatrick. 2006. Dasatinib. Nat. Rev. Drug Discov. 5:717-718.
44. Khaiboullina, S. F., D. M. Netski, P. Krumpe, and S. C. St. Jeor. 2000. Effects of tumor necrosis factor alpha on Sin Nombre virus infection in vitro. J. Virol. 74:11966-11971.
45. Kim, M. P., S. I. Park, S. Kopetz, and G. E. Gallick. 2009. Src family kinases as mediators of endothelial permeability: effects on inflammation and metastasis. Cell Tissue Res. 335:249-259.
46. Kortekaas, J., O. Ergonul, and R. J. Moormann. 2010. Interventions against West Nile virus, Rift Valley fever virus, and Crimean-Congo hemorrhagic fever virus: where are we? Vector Borne Zoonotic Dis. 10:709-718.
47. Koster, F., et al. 2001. Rapid presumptive diagnosis of hantavirus cardiopulmonary syndrome by peripheral blood smear review. Am. J. Clin. Pathol. 116:665-672.
48. Kourembanas, S., et al. 1998. Hypoxic responses of vascular cells. Chest 114:25S-28S.
49. Krakauer, T., J. W. Leduc, J. C. Morrill, A. O. Anderson, and H. Krakauer. 1994. Serum levels of alpha and gamma interferons in hemorrhagic fever with renal syndrome. Viral Immunol. 7:97-101. (Pubitemid 24348469)
50. Kumar, R., et al. 2007. Pharmacokinetic-pharmacodynamic correlation from mouse to human with pazopanib, a multikinase angiogenesis inhibitor with potent antitumor and antiangiogenic activity. Mol. Cancer Ther. 6:2012-2021.
51. Lahdevirta, J. 1982. Clinical features of HFRS in Scandinavia as compared with East Asia. Scand. J. Infect. Dis. Suppl. 36:93-95.
52. Lamalice, L., F. Le Boeuf, and J. Huot. 2007. Endothelial cell migration during angiogenesis. Circ. Res. 100:782-794.
53. Lampugnani, M. G., and E. Dejana. 2007. Adherens junctions in endothelial cells regulate vessel maintenance and angiogenesis. Thromb. Res. 120(Suppl. 2):S1-S6.
54. Lee, H. W. 1982. Hemorrhagic fever with renal syndrome (HFRS). Scand. J. Infect. Dis. Suppl. 36:82-85.
55. Levis, S., J. Rowe, S. Morzunov, D. Enria, and S. St. Jeor. 1997. New hantaviruses causing hantavirus pulmonary syndrome in central America. Lancet 349:998-999.
56. London, N. R., K. J. Whitehead, and D. Y. Li. 2009. Endogenous endothelial cell signaling systems maintain vascular stability. Angiogenesis 12:149-158.
57. Lopez, N., P. Padula, C. Rossi, M. E. Lazaro, and M. T. Franze-Fernandez. 1996. Genetic identification of a new hantavirus causing severe pulmonary syndrome in Argentina. Virology 220:223-226.
58. Mackow, E. R., and I. N. Gavrilovskaya. 2009. Hantavirus regulation of endothelial cell functions. Thromb. Haemost. 102:1030-1041.
59. Manalo, D. J., et al. 2005. Transcriptional regulation of vascular endothelial cell responses to hypoxia by HIF-1. Blood 105:659-669. (Pubitemid 40070750)
60. Markowska, A. I., F. T. Liu, and N. Panjwani. 2010. Galectin-3 is an important mediator of VEGF- and bFGF-mediated angiogenic response. J. Exp. Med. 207:1981-1993.
61. Matthys, V. S., E. E. Gorbunova, I. N. Gavrilovskaya, and E. R. Mackow. 2010. Andes virus recognition of human and Syrian hamster beta3 integrins is determined by an L33P substitution in the PSI domain. J. Virol. 84:352-360.
62. McVerry, B. J., and J. G. Garcia. 2004. Endothelial cell barrier regulation by sphingosine 1-phosphate. J. Cell. Biochem. 92:1075-1085.
63. Morgan, M. R., M. J. Humphries, and M. D. Bass. 2007. Synergistic control of cell adhesion by integrins and syndecans. Nat. Rev. Mol. Cell Biol. 8:957-969.
64. Mukhopadhyay, D., et al. 1995. Hypoxic induction of human vascular endothelial growth factor expression through c-Src activation. Nature 375:577-581.
65. Nam, S., et al. 2005. Action of the Src family kinase inhibitor, dasatinib (BMS-354825), on human prostate cancer cells. Cancer Res. 65:9185-9189. (Pubitemid 41507982)
66. Nolte, K. B., et al. 1995. Hantavirus pulmonary syndrome in the United States: a pathological description of a disease caused by a new agent. Hum. Pathol. 26:110-120.
67. Paddock, C. D., et al. 2006. Fatal hemorrhagic fever caused by West Nile virus in the United States. Clin. Infect. Dis. 42:1527-1535.
68. Padula, P. J., et al. 1998. Hantavirus pulmonary syndrome outbreak in Argentina: molecular evidence for person-to-person transmission of Andes virus. Virology 241:323-330. (Pubitemid 28384205)
69. Pepini, T., E. E. Gorbunova, I. Gavrilovskaya, J. E. Mackow, and E. R. Mackow. 2010. Andes virus regulation of cellular microRNAs contributes to hantavirus-induced endothelial cell permeability. J. Virol. 84:11929-11936.
70. Pham, I., et al. 2002. Hypoxia upregulates VEGF expression in alveolar epithelial cells in vitro and in vivo. Am. J. Physiol. Lung Cell. Mol. Physiol. 283:L1133-L1142.
71. Podar, K., et al. 2006. The small-molecule VEGF receptor inhibitor pazopanib (GW786034B) targets both tumor and endothelial cells in multiple myeloma. Proc. Natl. Acad. Sci. U. S. A. 103:19478-19483.
72. Porkka, K., et al. 2010. Dasatinib 100 mg once daily minimizes the occurrence of pleural effusion in patients with chronic myeloid leukemia in chronic phase and efficacy is unaffected in patients who develop pleural effusion. Cancer 116:377-386.
73. Pulzova, L., M. R. Bhide, and K. Andrej. 2009. Pathogen translocation across the blood-brain barrier. FEMS Immunol. Med. Microbiol. 57:203-213.
74. 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.
75. Reynolds, A. R., et al. 2009. Stimulation of tumor growth and angiogenesis by low concentrations of RGD-mimetic integrin inhibitors. Nat. Med. 15:392-400.
76. Reynolds, A. R., et al. 2004. Elevated Flk1 (vascular endothelial growth factor receptor 2) signaling mediates enhanced angiogenesis in beta3-integrin-deficient mice. Cancer Res. 64:8643-8650. (Pubitemid 39552078)
77. Reynolds, L. E., et al. 2002. Enhanced pathological angiogenesis in mice lacking beta3 integrin or beta3 and beta5 integrins. Nat. Med. 8:27-34.
78. Rini, B. I. 2009. Vascular endothelial growth factor-targeted therapy in metastatic renal cell carcinoma. Cancer 115:2306-2312.
79. 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.
80. Rusnak, J. M., et al. 2009. Experience with intravenous ribavirin in the treatment of hemorrhagic fever with renal syndrome in Korea. Antiviral Res. 81:68-76.
81. Sanchez, T., et al. 2003. Phosphorylation and action of the immunomodulator FTY720 inhibits vascular endothelial cell growth factor-induced vascular permeability. J. Biol. Chem. 278:47281-47290.
82. Schmaljohn, C. 2001. Bunyaviridae and their replication, p. 1581-1602. In D. M. Knipe et al. (ed.), Fields virology, 4th ed., vol. 1. Lipppincott Williams & Wilkins, Philadelphia, PA.
83. Schmaljohn, C., and B. Hjelle. 1997. Hantaviruses: a global disease problem. Emerg. Infect. Dis. 3:95-104.
84. Shrivastava-Ranjan, P., P. E. Rollin, and C. F. Spiropoulou. 2010. Andes virus disrupts the endothelial cell barrier by induction of vascular endothelial growth factor and downregulation of VE-cadherin. J. Virol. 84:11227-11234.
85. Sleijfer, S., et al. 2009. Pazopanib, a multikinase angiogenesis inhibitor, in patients with relapsed or refractory advanced soft tissue sarcoma: a phase II study from the European organisation for research and treatment of cancersoft tissue and bone sarcoma group (EORTC study 62043). J. Clin. Oncol. 27:3126-3132.
86. Sonpavde, G., T. E. Hutson, and C. N. Sternberg. 2008. Pazopanib, a potent orally administered small-molecule multitargeted tyrosine kinase inhibitor for renal cell carcinoma. Expert Opin. Invest. Drugs 17:253-261.
87. Sundstrom, J. B., et al. 2001. Hantavirus infection induces the expression of RANTES and IP-10 without causing increased permeability in human lung microvascular endothelial cells. J. Virol. 75:6070-6085. (Pubitemid 32553138)
88. Tamura, M., H. Asada, K. Kondo, M. Takahashi, and K. Yamanishi. 1987. Effects of human and murine interferons against hemorrhagic fever with renal syndrome (HFRS) virus (Hantaan virus). Antiviral Res. 8:171-178. (Pubitemid 18032859)
89. Tang, N., et al. 2004. Loss of HIF-1alpha in endothelial cells disrupts a hypoxia-driven VEGF autocrine loop necessary for tumorigenesis. Cancer Cell 6:485-495. (Pubitemid 39469984)
90. Thurston, G., et al. 2000. Angiopoietin-1 protects the adult vasculature against plasma leakage. Nat. Med. 6:460-463.
91. Thurston, G., et al. 1999. Leakage-resistant blood vessels in mice transgenically overexpressing angiopoietin-1. Science 286:2511-2514. (Pubitemid 30026340)
92. Verma, S., M. Kumar, U. Gurjav, S. Lum, and V. R. Nerurkar. 2010. Reversal of West Nile virus-induced blood-brain barrier disruption and tight junction proteins degradation by matrix metalloproteinases inhibitor. Virology 397:130-138.
93. Vultur, A., et al. 2008. SKI-606 (bosutinib), a novel Src kinase inhibitor, suppresses migration and invasion of human breast cancer cells. Mol. Cancer Ther. 7:1185-1194.
94. Wahl-Jensen, V., et al. 2007. Temporal analysis of Andes virus and Sin Nombre virus infections of Syrian hamsters. J. Virol. 81:7449-7462. (Pubitemid 47047833)
95. Weis, S., et al. 2004. Src blockade stabilizes a Flk/cadherin complex, reducing edema and tissue injury following myocardial infarction. J. Clin. Invest. 113:885-894.
96. Weis, S. M., and D. A. Cheresh. 2005. Pathophysiological consequences of VEGF-induced vascular permeability. Nature 437:497-504.
97. Wu-Hsieh, B. A., Y. T. Yen, and H. C. Chen. 2009. Dengue hemorrhage in a mouse model. Ann. N. Y. Acad. Sci. 1171(Suppl. 1):E42-E47.
98. Zaki, S., et al. 1995. Hantavirus pulmonary syndrome: pathogenesis of an emerging infectious disease. Am. J. Pathol. 146:552-579.