- About this Journal ·
- Abstracting and Indexing ·
- Aims and Scope ·
- Article Processing Charges ·
- Articles in Press ·
- Author Guidelines ·
- Bibliographic Information ·
- Citations to this Journal ·
- Contact Information ·
- Editorial Board ·
- Editorial Workflow ·
- Free eTOC Alerts ·
- Publication Ethics ·
- Reviewers Acknowledgment ·
- Submit a Manuscript ·
- Subscription Information ·
- Table of Contents
Advances in Virology
Volume 2012 (2012), Article ID 674360, 8 pages
Elevated VEGF Levels in Pulmonary Edema Fluid and PBMCs from Patients with Acute Hantavirus Pulmonary Syndrome
1Department of Molecular Genetics and Microbiology, Stony Brook University, Stony Brook, NY 11794-5222, USA
2Lovelace Respiratory Research Institute, 2425 Ridgecrest Dr. Albuquerque, NM 87108, USA
Received 23 May 2012; Accepted 11 July 2012
Academic Editor: Amiya K. Banerjee
Copyright © 2012 Irina Gavrilovskaya et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
- F. Koster, K. Foucar, B. Hjelle et al., “Rapid presumptive diagnosis of hantavirus cardiopulmonary syndrome by peripheral blood smear review,” American Journal of Clinical Pathology, vol. 116, no. 5, pp. 665–672, 2001.
- F. Koster and E. R. Mackow, “Pathogenesis of the hantavirus pulmonary syndrome,” Future Virology, vol. 7, no. 1, pp. 41–51, 2012.
- S. T. Nichol, C. F. Spiropoulou, S. Morzunov et al., “Genetic identification of a hantavirus associated with an outbreak of acute respiratory illness,” Science, vol. 262, no. 5135, pp. 914–917, 1993.
- C. Schmaljohn and B. Hjelle, “Hantaviruses: a global disease problem,” Emerging Infectious Diseases, vol. 3, no. 2, pp. 95–104, 1997.
- S. R. Zaki, P. W. Greer, L. M. Coffield et al., “Hantavirus pulmonary syndrome: pathogenesis of an emerging infectious disease,” American Journal of Pathology, vol. 146, no. 3, pp. 552–579, 1995.
- J. S. Duchin, F. T. Koster, C. J. Peters et al., “Hantavirus pulmonary syndrome: a clinical description of 17 patients with a newly recognized disease,” New England Journal of Medicine, vol. 330, no. 14, pp. 949–955, 1994.
- K. B. Nolte, R. M. Feddersen, K. Foucar et al., “Hantavirus pulmonary syndrome in the United States: a pathological description of a disease caused by a new agent,” Human Pathology, vol. 26, no. 1, pp. 110–120, 1995.
- M. Kanerva, J. Mustonen, and A. Vaheri, “Pathogenesis of puumala and other hantavirus infections,” Reviews in Medical Virology, vol. 8, no. 2, pp. 67–86, 1998.
- E. D. Kilpatrick, M. Terajima, F. T. Koster, M. D. Catalina, J. Cruz, and F. A. Ennis, “Role of specific CD8+ T cells in the severity of a fulminant zoonotic viral hemorrhagic fever, hantavirus pulmonary syndrome,” Journal of Immunology, vol. 172, no. 5, pp. 3297–3304, 2004.
- T. Krakauer, J. W. Leduc, and H. Krakauer, “Serum levels of tumor necrosis factor-α, interleukin-1, and interleukin-6 in hemorrhagic fever with renal syndrome,” Viral Immunology, vol. 8, no. 2, pp. 75–79, 1995.
- E. R. Mackow and I. N. Gavrilovskaya, “Hantavirus regulation of endothelial cell functions,” Thrombosis and Haemostasis, vol. 102, no. 6, pp. 1030–1041, 2009.
- P. Maes, J. Clement, P. H. P. Groeneveld, P. Colson, T. W. J. Huizinga, and M. Van Ranst, “Tumor necrosis factor-α genetic predisposing factors can influence clinical severity in nephropathia epidemica,” Viral Immunology, vol. 19, no. 3, pp. 558–564, 2006.
- M. Mori, A. L. Rothman, I. Kurane et al., “High levels of cytokine-producing cells in the lung tissues of patients with fatal hantavirus pulmonary syndrome,” Journal of Infectious Diseases, vol. 179, no. 2, pp. 295–302, 1999.
- J. B. Sundstrom, L. K. McMullan, C. F. Spiropoulou et al., “Hantavirus infection induces the expression of RANTES and IP-10 without causing increased permeability in human lung microvascular endothelial cells,” Journal of Virology, vol. 75, no. 13, pp. 6070–6085, 2001.
- M. Temonen, J. Mustonen, H. Helin, A. Pasternack, A. Vaheri, and H. Holthöfer, “Cytokines, adhesion molecules, and cellular infiltration in nephropathia epidemica kidneys: an immunohistochemical study,” Clinical Immunology and Immunopathology, vol. 78, no. 1, pp. 47–55, 1996.
- S. F. Khaiboullina, D. M. Netski, P. Krumpe, and S. C. S. Jeor, “Effects of tumor necrosis factor alpha on Sin Nombre virus infection in vitro,” Journal of Virology, vol. 74, no. 24, pp. 11966–11971, 2000.
- I. N. Gavrilovskaya, E. E. Gorbunova, and E. R. Mackow, “Pathogenic hantaviruses direct the adherence of quiescent platelets to infected endothelial cells,” Journal of Virology, vol. 84, no. 9, pp. 4832–4839, 2010.
- I. N. Gavrilovskaya, E. E. Gorbunova, N. A. Mackow, and E. R. Mackow, “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,” Journal of Virology, vol. 82, no. 12, pp. 5797–5806, 2008.
- I. N. Gavrilovskaya, T. Peresleni, E. Geimonen, and E. R. Mackow, “Pathogenic hantaviruses selectively inhibit β3 integrin directed endothelial cell migration,” Archives of Virology, vol. 147, no. 10, pp. 1913–1931, 2002.
- T. Raymond, E. Gorbunova, I. N. Gavrilovskaya, and E. R. Mackow, “Pathogenic hantaviruses bind plexin-semaphorin-integrin domains present at the apex of inactive, bent αvβ3 integrin conformers,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 4, pp. 1163–1168, 2005.
- S. D. Robinson, L. E. Reynolds, L. Wyder, D. J. Hicklin, and K. M. Hodivala-Dilke, “β3-integrin regulates vascular endothelial growth factor-A-dependent permeability,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 24, no. 11, pp. 2108–2114, 2004.
- B. Chang, M. Crowley, M. Campen, and F. Koster, “Hantavirus cardiopulmonary syndrome,” Seminars in Respiratory and Critical Care Medicine, vol. 28, no. 2, pp. 193–200, 2007.
- E. Geimonen, S. Neff, T. Raymond, S. S. Kocer, I. N. Gavrilovskaya, and E. R. Mackow, “Pathogenic and nonpathogenic hantaviruses differentially regulate endothelial cell responses,” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 21, pp. 13837–13842, 2002.
- E. Gorbunova, I. N. Gavrilovskaya, and E. R. Mackow, “Pathogenic hantaviruses Andes virus and Hantaan virus induce adherens junction disassembly by directing vascular endothelial cadherin internalization in human endothelial cell,” Journal of Virology, vol. 84, no. 14, pp. 7405–7411, 2010.
- S. F. Khaiboullina, A. A. Rizvanov, E. Otteson, A. Miyazato, J. Maciejewski, and S. S. Jeor, “Regulation of cellular gene expression in endothelial cells by Sin Nombre and Prospect Hill viruses,” Viral Immunology, vol. 17, no. 2, pp. 234–251, 2004.
- R. Yanagihara and D. J. Silverman, “Experimental infection of human vascular endothelial cells by pathogenic and nonpathogenic hantaviruses,” Archives of Virology, vol. 111, no. 3-4, pp. 281–286, 1990.
- K. M. Hodivala-Dilke, K. P. McHugh, D. A. Tsakiris et al., “β3-integrin-deficient mice are a model for Glanzmann thrombasthenia showing placental defects and reduced survival,” Journal of Clinical Investigation, vol. 103, no. 2, pp. 229–238, 1999.
- A. R. Reynolds, L. E. Reynolds, T. E. Nagel et al., “Elevated Flk1 (vascular endothelial growth factor receptor 2) signaling mediates enhanced angiogenesis in β3-integrin-deficient mice,” Cancer Research, vol. 64, no. 23, pp. 8643–8650, 2004.
- I. N. Gavrilovskaya, M. Shepley, R. Shaw, M. H. Ginsberg, and E. R. Mackow, “β3 integrins mediate the cellular entry of hantaviruses that cause respiratory failure,” Proceedings of the National Academy of Sciences of the United States of America, vol. 95, no. 12, pp. 7074–7079, 1998.
- E. E. Gorbunova, I. N. Gavrilovskaya, T. Pepini, and E. R. Mackow, “VEGFR2 and Src kinase inhibitors suppress Andes virus-induced endothelial cell permeability,” Journal of Virology, vol. 85, no. 5, pp. 2296–2303, 2011.
- T. Pepini, E. E. Gorbunova, I. N. Gavrilovskaya, J. E. Mackow, and E. R. Mackow, “Andes virus regulation of cellular microRNAs contributes to hantavirus-induced endothelial cell permeability,” Journal of Virology, vol. 84, no. 22, pp. 11929–11936, 2010.
- H. F. Dvorak, L. F. Brown, M. Detmar, and A. M. Dvorak, “Vascular permeability factor/vascular endothelial growth factor, microvascular hyperpermeability, and angiogenesis,” American Journal of Pathology, vol. 146, no. 5, pp. 1029–1039, 1995.
- M. Hanaoka, Y. Droma, A. Naramoto, T. Honda, T. Kobayashi, and K. Kubo, “Vascular endothelial growth factor in patients with high-altitude pulmonary edema,” Journal of Applied Physiology, vol. 94, no. 5, pp. 1836–1840, 2003.
- M. M. Berger, C. Hesse, C. Dehnert et al., “Hypoxia impairs systemic endothelial function in individuals prone to high-altitude pulmonary edema,” American Journal of Respiratory and Critical Care Medicine, vol. 172, no. 6, pp. 763–767, 2005.
- M. Dehler, E. Zessin, P. Bärtsch, and H. Mairbäurl, “Hypoxia causes permeability oedema in the constant-pressure perfused rat lung,” European Respiratory Journal, vol. 27, no. 3, pp. 600–606, 2006.
- H. F. Dvorak, “Vascular permeability to plasma, plasma proteins, and cells: an update,” Current Opinion in Hematology, vol. 17, no. 3, pp. 225–229, 2010.
- K. R. Stenmark, K. A. Fagan, and M. G. Frid, “Hypoxia-induced pulmonary vascular remodeling: cellular and molecular mechanisms,” Circulation Research, vol. 99, no. 7, pp. 675–691, 2006.
- N. Tang, L. Wang, J. Esko et al., “Loss of HIF-1α in endothelial cells disrupts a hypoxia-driven VEGF autocrine loop necessary for tumorigenesis,” Cancer Cell, vol. 6, no. 5, pp. 485–495, 2004.
- R. J. Kaner and R. G. Crystal, “Pathogenesis of high altitude pulmonary edema: does alveolar epithelial lining fluid vascular endothelial growth factor exacerbate capillary leak?” High Altitude Medicine and Biology, vol. 5, no. 4, pp. 399–409, 2004.
- R. J. Kaner, J. V. Ladetto, R. Singh, N. Fukuda, M. A. Matthay, and R. G. Crystal, “Lung overexpression of the vascular endothelial growth factor gene induces pulmonary edema,” American Journal of Respiratory Cell and Molecular Biology, vol. 22, no. 6, pp. 657–664, 2000.
- B. Hjelle, S. Jenison, N. Torrez-Martinez et al., “Rapid and specific detection of Sin Nombre virus antibodies in patients with hantavirus pulmonary syndrome by a strip immunoblot assay suitable for field diagnosis,” Journal of Clinical Microbiology, vol. 35, no. 3, pp. 600–608, 1997.
- G. W. Hallin, S. Q. Simpson, R. E. Crowell et al., “Cardiopulmonary manifestations of hantavirus pulmonary syndrome,” Critical Care Medicine, vol. 24, no. 2, pp. 252–258, 1996.
- M. R. Crowley, R. W. Katz, R. Kessler et al., “Successful treatment of adults with severe Hantavirus pulmonary syndrome with extracorporeal membrane oxygenation,” Critical Care Medicine, vol. 26, no. 2, pp. 409–414, 1998.
- H. F. Dvorak, T. M. Sioussat, L. F. Brown et al., “Distribution of vascular permeability factor (vascular endothelial growth factor) in tumors: concentration in tumor blood vessels,” Journal of Experimental Medicine, vol. 174, no. 5, pp. 1275–1278, 1991.
- E. A. Bustamante, H. Levy, and S. Q. Simpson, “Pleural fluid characteristics in hantavirus pulmonary syndrome,” Chest, vol. 112, no. 4, pp. 1133–1136, 1997.
- H. F. Dvorak, “Discovery of vascular permeability factor (VPF),” Experimental Cell Research, vol. 312, no. 5, pp. 522–526, 2006.
- I. Pham, T. Uchida, C. Planes et al., “Hypoxia upregulates VEGF expression in alveolar epithelial cells in vitro and in vivo,” American Journal of Physiology-Lung Cellular and Molecular Physiology, vol. 283, no. 5, pp. L1133–L1142, 2002.
- E. Dejana, F. Orsenigo, and M. G. Lampugnani, “The role of adherens junctions and VE-cadherin in the control of vascular permeability,” Journal of Cell Science, vol. 121, no. 13, pp. 2115–2122, 2008.
- J. Gavard and J. S. Gutkind, “VEGF Controls endothelial-cell permeability promoting β-arrestin-dependent Endocytosis VE-cadherin,” Nature Cell Biology, vol. 8, no. 11, pp. 1223–1234, 2006.
- M. G. Lampugnani and E. Dejana, “The control of endothelial cell functions by adherens junctions,” Novartis Foundation Symposium, vol. 283, pp. 4–13, 2007.
- M. G. Lampugnani and E. Dejana, “Adherens junctions in endothelial cells regulate vessel maintenance and angiogenesis,” Thrombosis Research, vol. 120, supplement 2, pp. S1–S6, 2007.
- R. J. Kaner and R. G. Crystal, “Compartmentalization of vascular endothelial growth factor to the epithelial surface of the human lung,” Molecular Medicine, vol. 7, no. 4, pp. 240–246, 2001.
- S. R. Hopkins, J. Garg, D. S. Bolar, J. Balouch, and D. L. Levin, “Pulmonary blood flow heterogeneity during hypoxia and high-altitude pulmonary edema,” American Journal of Respiratory and Critical Care Medicine, vol. 171, no. 1, pp. 83–87, 2005.
- G. Thurston, J. S. Rudge, E. Ioffe et al., “Angiopoietin-1 protects the adult vasculature against plasma leakage,” Nature Medicine, vol. 6, no. 4, pp. 460–463, 2000.
- G. Thurston, C. Suri, K. Smith et al., “Leakage-resistant blood vessels in mice transgenically overexpressing angiopoietin-1,” Science, vol. 286, no. 5449, pp. 2511–2514, 1999.
- Y. Wang, S. Pampou, K. Fujikawa, and L. Varticovski, “Opposing effect of angiopoietin-1 on VEGF-mediated disruption of endothelial cell-cell interactions requires activation of PKCβ,” Journal of Cellular Physiology, vol. 198, no. 1, pp. 53–61, 2004.
- M. Watanabe, J. L. Boyer, and R. G. Crystal, “Genetic delivery of bevacizumab to suppress vascular endothelial growth factor-induced high-permeability pulmonary edema,” Human Gene Therapy, vol. 20, no. 6, pp. 598–610, 2009.
- C. A. Dietl, J. A. Wernly, S. B. Pett et al., “Extracorporeal membrane oxygenation support improves survival of patients with severe Hantavirus cardiopulmonary syndrome,” Journal of Thoracic and Cardiovascular Surgery, vol. 135, no. 3, pp. 579–584, 2008.
- D. Mukhopadhyay, L. Tsiokas, X. M. Zhou, D. Foster, J. S. Brugge, and V. P. Sukhatme, “Hypoxic induction of human vascular endothelial growth factor expression through c-Src activation,” Nature, vol. 375, no. 6532, pp. 577–581, 1995.
- P. Salven, A. Orpana, and H. Joensuu, “Leukocytes and platelets of patients with cancer contain high levels of vascular endothelial growth factor,” Clinical Cancer Research, vol. 5, no. 3, pp. 487–491, 1999.
- J. Zhang, T. Silva, T. Yarovinsky et al., “VEGF blockade inhibits lymphocyte recruitment and ameliorates immune-mediated vascular remodeling,” Circulation Research, vol. 107, no. 3, pp. 408–417, 2010.
- L. B. Ware, R. J. Kaner, R. G. Crystal et al., “VEGF levels in the alveolar compartment do not distinguish between ARDS and hydrostatic pulmonary oedama,” European Respiratory Journal, vol. 26, no. 1, pp. 101–105, 2005.
- R. Xiao, S. Yang, F. Koster, C. Ye, C. Stidley, and B. Hjelle, “Sin Nombre viral RNA load in patients with hantavirus cardiopulmonary syndrome,” Journal of Infectious Diseases, vol. 194, no. 10, pp. 1403–1409, 2006.
- F. Gracia, B. Armien, S. Q. Simpson et al., “Convalescent pulmonary dysfunction following hantavirus pulmonary syndrome in panama and the United States,” Lung, vol. 188, no. 5, pp. 387–391, 2010.