• 1.

    Bushar G, Sagripanti JL, 1997. Molecular characteristics of Junin virus. J Virol Methods 63: 2735.

  • 2.

    de Bracco MME, Rimoldi MT, Cossio PM, Rabinovich A, Maiztegui JI, Carballal G, Arana RM, 1978. Argentine hemorrhagic fever. N Engl J Med 299: 216221.

  • 3.

    Molteni HD, Guarinos HC, Petrillo CO, Jaschek F, 1961. Clinico-statistical study of 338 patients with epidemic hemorrhagic fever in the northwest of the province of Buenos Aires. Sem Med 118: 839855.

    • Search Google Scholar
    • Export Citation
  • 4.

    Nguyen TH, Nguyen TL, Lei HY, Lin YS, Le BL, Huang KJ, Lin CF, Do QH, Vu TQ, Lam TM, Yeh TM, Huang JH, Liu CC, Halstead SB, 2006. Volume replacement in infants with dengue hemorrhagic fever/dengue shock syndrome. Am J Trop Med Hyg 74: 684691.

    • Search Google Scholar
    • Export Citation
  • 5.

    Levis SC, Saavedra MC, Ceccoli C, Falcoff E, Feuillade MR, Enria DA, Maiztegui JI, Falcoff R, 1984. Endogenous interferon in Argentine hemorrhagic fever. J Infect Dis 149: 428433.

    • Search Google Scholar
    • Export Citation
  • 6.

    Marta RF, Montero VS, Hack CE, Sturk A, Maiztegui JI, Molinas FC, 1999. Proinflammatory cytokines and elastase-alpha-1-antitrypsin in Argentine hemorrhagic fever. Am J Trop Med Hyg 60: 8589.

    • Search Google Scholar
    • Export Citation
  • 7.

    Andrews BS, Theofilopoulos AN, Peters CJ, Loskutoff DJ, Brandt WE, Dixon FJ, 1978. Replication of dengue and junin viruses in cultured rabbit and human endothelial cells. Infect Immun 20: 776781.

    • Search Google Scholar
    • Export Citation
  • 8.

    Lukashevich IS, Maryankova R, Vladyko AS, Nashkevich N, Koleda S, Djavani M, Horejsh D, Voitenok NN, Salvato MS, 1999. Lassa and Mopeia virus replication in human monocytes/macrophages and in endothelial cells: different effects on IL-8 and TNF-alpha gene expression. J Med Virol 59: 552560.

    • Search Google Scholar
    • Export Citation
  • 9.

    Hippenstiel S, Suttorp N, 2003. Interaction of pathogens with the endothelium. Thromb Haemost 89: 1824.

  • 10.

    Peters CJ, Zaki SR, 2002. Role of the endothelium in viral hemorrhagic fevers. Crit Care Med 30: S268S273.

  • 11.

    Breviario F, Caveda L, Corada M, Martin-Padura I, Navarro P, Golay J, Introna M, Gulino D, Lampugnani MG, Dejana E, 1995. Functional properties of human vascular endothelial cadherin (7B4/cadherin-5), an endothelium-specific cadherin. Arterioscler Thromb Vasc Biol 15: 12291239.

    • Search Google Scholar
    • Export Citation
  • 12.

    Dejana E, Orsenigo F, Lampugnani MG, 2008. The role of adherens junctions and VE-cadherin in the control of vascular permeability. J Cell Sci 121: 21152122.

    • Search Google Scholar
    • Export Citation
  • 13.

    Taddei A, Giampietro C, Conti A, Orsenigo F, Breviario F, Pirazzoli V, Potente M, Daly C, Dimmeler S, Dejana E, 2008. Endothelial adherens junctions control tight junctions by VE-cadherin-mediated upregulation of claudin-5. Nat Cell Biol 10: 923934.

    • Search Google Scholar
    • Export Citation
  • 14.

    Gao X, Kouklis P, Xu N, Minshall RD, Sandoval R, Vogel SM, Malik AB, 2000. Reversibility of increased microvessel permeability in response to VE-cadherin disassembly. Am J Physiol Lung Cell Mol Physiol 279: L1218L1225.

    • Search Google Scholar
    • Export Citation
  • 15.

    Hossain MA, Russell JC, Miknyoczki S, Ruggeri B, Lal B, Laterra J, 2004. Vascular endothelial growth factor mediates vasogenic edema in acute lead encephalopathy. Ann Neurol 55: 660667.

    • Search Google Scholar
    • Export Citation
  • 16.

    Paul R, Zhang ZG, Eliceiri BP, Jiang Q, Boccia AD, Zhang RL, Chopp M, Cheresh DA, 2001. Src deficiency or blockade of Src activity in mice provides cerebral protection following stroke. Nat Med 7: 222227.

    • Search Google Scholar
    • Export Citation
  • 17.

    Angelini DJ, Hyun SW, Grigoryev DN, Garg P, Gong P, Singh IS, Passaniti A, Hasday JD, Goldblum SE, 2006. TNF-alpha increases tyrosine phosphorylation of vascular endothelial cadherin and opens the paracellular pathway through fyn activation in human lung endothelia. Am J Physiol Lung Cell Mol Physiol 291: L1232L1245.

    • Search Google Scholar
    • Export Citation
  • 18.

    Cheung LW, Leung PC, Wong AS, 2010. Cadherin switching and activation of p120 catenin signaling are mediators of gonadotropin-releasing hormone to promote tumor cell migration and invasion in ovarian cancer. Oncogene 29: 24272440.

    • Search Google Scholar
    • Export Citation
  • 19.

    Lampugnani MG, 2010. Endothelial adherens junctions and the actin cytoskeleton: an ‘infinity net’? J Biol 9: 16.

  • 20.

    Harris TJ, Tepass U, 2010. Adherens junctions: from molecules to morphogenesis. Nat Rev Mol Cell Biol 11: 502514.

  • 21.

    Vincent PA, Xiao K, Buckley KM, Kowalczyk AP, 2004. VE-cadherin: adhesion at arm's length. Am J Physiol Cell Physiol 286: C987C997.

  • 22.

    Gomez RM, Pozner RG, Lazzari MA, D'Atri LP, Negrotto S, Chudzinski-Tavassi AM, Berria MI, Schattner M, 2003. Endothelial cell function alteration after Junin virus infection. Thromb Haemost 90: 326333.

    • Search Google Scholar
    • Export Citation
  • 23.

    Enria DA, Barrera Oro JG, 2002. Junin virus vaccines. Curr Top Microbiol Immunol 263: 239261.

  • 24.

    Mahanty S, Bausch DG, Thomas RL, Goba A, Bah A, Peters CJ, Rollin PE, 2001. Low levels of interleukin-8 and interferon-inducible protein–10 in serum are associated with fatal infections in acute lassa fever. J Infect Dis 183: 17131721.

    • Search Google Scholar
    • Export Citation
  • 25.

    Stairs DB, Bayne LJ, Rhoades B, Vega ME, Waldron TJ, Kalabis J, Klein-Szanto A, Lee JS, Katz JP, Diehl JA, Reynolds AB, Vonderheide RH, Rustgi AK, 2011. Deletion of p120-catenin results in a tumor microenvironment with inflammation and cancer that establishes it as a tumor suppressor gene. Cancer Cell 19: 470483.

    • Search Google Scholar
    • Export Citation
  • 26.

    Xiao K, Garner J, Buckley KM, Vincent PA, Chiasson CM, Dejana E, Faundez V, Kowalczyk AP, 2005. p120-Catenin regulates clathrin-dependent endocytosis of VE-cadherin. Mol Biol Cell 16: 51415151.

    • Search Google Scholar
    • Export Citation
  • 27.

    Herron CR, Lowery AM, Hollister PR, Reynolds AB, Vincent PA, 2011. p120 regulates endothelial permeability independently of its NH2 terminus and Rho binding. Am J Physiol Heart Circ Physiol 300: H36H48.

    • Search Google Scholar
    • Export Citation
  • 28.

    Klavinskis LS, Oldstone MB, 1989. Lymphocytic choriomeningitis virus selectively alters differentiated but not housekeeping functions: block in expression of growth hormone gene is at the level of transcriptional initiation. Virology 168: 232235.

    • Search Google Scholar
    • Export Citation
  • 29.

    Bureau JF, Le Goff S, Thomas D, Parlow AF, de la Torre JC, Homann D, Brahic M, Oldstone MB, 2001. Disruption of differentiated functions during viral infection in vivo. V. Mapping of a locus involved in susceptibility of mice to growth hormone deficiency due to persistent lymphocytic choriomeningitis virus infection. Virology 281: 6166.

    • Search Google Scholar
    • Export Citation
  • 30.

    Wright TJ, Leach L, Shaw PE, Jones P, 2002. Dynamics of vascular endothelial-cadherin and beta-catenin localization by vascular endothelial growth factor-induced angiogenesis in human umbilical vein cells. Exp Cell Res 280: 159168.

    • Search Google Scholar
    • Export Citation
  • 31.

    Dejana E, Lampugnani MG, Martinez-Estrada O, Bazzoni G, 2000. The molecular organization of endothelial junctions and their functional role in vascular morphogenesis and permeability. Int J Dev Biol 44: 743748.

    • Search Google Scholar
    • Export Citation
  • 32.

    Cheung LW, Leung PC, Wong AS, 2010. Cadherin switching and activation of p120 catenin signaling are mediators of gonadotropin-releasing hormone to promote tumor cell migration and invasion in ovarian cancer. Oncogene 29: 24272440.

    • Search Google Scholar
    • Export Citation
  • 33.

    Weis S, Shintani S, Weber A, Kirchmair R, Wood M, Cravens A, McSharry H, Iwakura A, Yoon Y-s, Himes N, Burstein D, Doukas J, Soll R, Losordo D, Cheresh D, 2004. Src blockade stabilizes a Flk/cadherin complex, reducing edema and tissue injury following myocardial infarction. J Clin Invest 113: 885894.

    • Search Google Scholar
    • Export Citation
  • 34.

    Gorbunova EE, Gavrilovskaya IN, Pepini T, Mackow ER, 2011. VEGFR2 and Src kinase inhibitors suppress Andes virus-induced endothelial cell permeability. J Virol 85: 22962303.

    • Search Google Scholar
    • Export Citation
  • 35.

    Shrivastava-Ranjan P, Rollin PE, Spiropoulou CF, 2010. Andes virus disrupts the endothelial cell barrier by induction of vascular endothelial growth factor and downregulation of VE-cadherin. J Virol 84: 1122711234.

    • Search Google Scholar
    • Export Citation
  • 36.

    Sathupan P, Khongphattanayothin A, Srisai J, Srikaew K, Poovorawan Y, 2007. The role of vascular endothelial growth factor leading to vascular leakage in children with dengue virus infection. Ann Trop Paediatr 27: 179184.

    • Search Google Scholar
    • Export Citation
  • 37.

    Iyer S, Ferreri DM, DeCocco NC, Minnear FL, Vincent PA, 2004. VE-cadherin-p120 interaction is required for maintenance of endothelial barrier function. Am J Physiol Lung Cell Mol Physiol 286: L1143L1153.

    • Search Google Scholar
    • Export Citation
  • 38.

    Maruo N, Morita I, Shirao M, Murota S, 1992. IL-6 increases endothelial permeability in vitro. Endocrinology 131: 710714.

  • 39.

    Arendt BK, Velazquez-Dones A, Tschumper RC, Howell KG, Ansell SM, Witzig TE, Jelinek DF, 2002. Interleukin 6 induces monocyte chemoattractant protein-1 expression in myeloma cells. Leukemia 16: 21422147.

    • Search Google Scholar
    • Export Citation
  • 40.

    Biswas P, Delfanti F, Bernasconi S, Mengozzi M, Cota M, Polentarutti N, Mantovani A, Lazzarin A, Sozzani S, Poli G, 1998. Interleukin-6 induces monocyte chemotactic protein-1 in peripheral blood mononuclear cells and in the U937 cell line. Blood 91: 258265.

    • Search Google Scholar
    • Export Citation
  • 41.

    Clifton DR, Rydkina E, Huyck H, Pryhuber G, Freeman RS, Silverman DJ, Sahni SK, 2005. Expression and secretion of chemotactic cytokines IL-8 and MCP-1 by human endothelial cells after Rickettsia rickettsii infection: regulation by nuclear transcription factor NF-kappaB. Int J Med Microbiol 295: 267278.

    • Search Google Scholar
    • Export Citation
  • 42.

    Lee YR, Liu MT, Lei HY, Liu CC, Wu JM, Tung YC, Lin YS, Yeh TM, Chen SH, Liu HS, 2006. MCP-1, a highly expressed chemokine in dengue haemorrhagic fever/dengue shock syndrome patients, may cause permeability change, possibly through reduced tight junctions of vascular endothelium cells. J Gen Virol 87: 36233630.

    • Search Google Scholar
    • Export Citation
  • 43.

    Tieu BC, Lee C, Sun H, Lejeune W, Recinos A 3rd, Ju X, Spratt H, Guo DC, Milewicz D, Tilton RG, Brasier AR, 2009. An adventitial IL-6/MCP1 amplification loop accelerates macrophage-mediated vascular inflammation leading to aortic dissection in mice. J Clin Invest 119: 36373651.

    • Search Google Scholar
    • Export Citation
  • 44.

    Rübe C, Wilfert F, Palm J, König J, Burdak-Rothkamm S, Liu L, Schuck A, Willich N, Rübe C, 2004. Irradiation induces a biphasic expression of pro-inflammatory cytokines in the lung. Strahlenther Onkol 180: 442448.

    • Search Google Scholar
    • Export Citation
  • 45.

    Hebda PA, Piltcher OB, Swarts JD, Alper CM, Zeevi A, Doyle WJ, 2002. Cytokine profiles in a rat model of otitis media with effusion caused by eustachian tube obstruction with and without Streptococcus pneumoniae infection. Laryngoscope 112: 16571662.

    • Search Google Scholar
    • Export Citation
  • 46.

    Candurra NA, Lago MJ, Maskin L, Damonte EB, 1999. Involvement of the cytoskeleton in Junin virus multiplication. J Gen Virol 80: 147156.

  • 47.

    Martinez MG, Cordo SM, Candurra NA, 2008. Involvement of cytoskeleton in Junin virus entry. Virus Res 138: 1725.

  • 48.

    Pozner RG, Ure AE, Jaquenod de Giusti C, D'Atri LP, Italiano JE, Torres O, Romanowski V, Schattner M, Gomez RM, 2010. Junin virus infection of human hematopoietic progenitors impairs in vitro proplatelet formation and platelet release via a bystander effect involving type I IFN signaling. PLoS Pathog 6: e1000847.

    • Search Google Scholar
    • Export Citation
  • 49.

    Elsner B, Schwarz E, Mando OG, Maiztegui J, Vilches A, 1973. Pathology of 12 fatal cases of Argentine hemorrhagic fever. Am J Trop Med Hyg 22: 229236.

    • Search Google Scholar
    • Export Citation
  • 50.

    Riviere Y, Gresser I, Guillon JC, Tovey MG, 1977. Inhibition by anti-interferon serum of lymphocytic choriomeningitis virus disease in suckling mice. Proc Natl Acad Sci USA 74: 21352139.

    • Search Google Scholar
    • Export Citation
  • 51.

    Emonet SF, Seregin AV, Yun NE, Poussard AL, Walker AG, de la Torre JC, Paessler S, 2011. Rescue from cloned cDNAs and in vivo characterization of recombinant pathogenic Romero and live-attenuated Candid #1 strains of Junin virus, the causative agent of Argentine hemorrhagic fever disease. J Virol 85: 14731483.

    • Search Google Scholar
    • Export Citation
  • 52.

    Arroyo AG, Iruela-Arispe ML, 2010. Extracellular matrix, inflammation, and the angiogenic response. Cardiovasc Res 86: 226235.

  • 53.

    Feldmann H, Klenk HD, 1996. Marburg and Ebola viruses. Adv Virus Res 47: 152.

  • 54.

    Sundstrom JB, McMullan LK, Spiropoulou CF, Hooper WC, Ansari AA, Peters CJ, Rollin PE, 2001. Hantavirus infection induces the expression of RANTES and IP-10 without causing increased permeability in human lung microvascular endothelial cells. J Virol 75: 60706085.

    • Search Google Scholar
    • Export Citation
  • 55.

    Lee Y-R, Liu M-T, Lei H-Y, Liu C-C, Wu J-M, Tung Y-C, Lin Y-S, Yeh T-M, Chen S-H, Liu H-S, 2006. MCP-1, a highly expressed chemokine in dengue haemorrhagic fever/dengue shock syndrome patients, may cause permeability change, possibly through reduced tight junctions of vascular endothelium cells. J Gen Virol 87: 36233630.

    • Search Google Scholar
    • Export Citation
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 

 

 

 

Endothelial Cell Permeability and Adherens Junction Disruption Induced by Junín Virus Infection

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  • Departments of Pathology and Microbiology and Immunology, University of Texas Medical Branch, Galveston, Texas
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Junín virus (JUNV) is endemic to the fertile Pampas of Argentina, maintained in nature by the rodent host Calomys musculinus, and the causative agent of Argentine hemorrhagic fever (AHF), which is characterized by vascular dysfunction and fluid distribution abnormalities. Clinical as well as experimental studies implicate involvement of the endothelium in the pathogenesis of AHF, although little is known of its role. JUNV has been shown to result in productive infection of endothelial cells (ECs) in vitro with no visible cytopathic effects. In this study, we show that direct JUNV infection of primary human ECs results in increased vascular permeability as measured by electric cell substrate impedance sensing and transwell permeability assays. We also show that EC adherens junctions are disrupted during virus infection, which may provide insight into the role of the endothelium in the pathogenesis of AHF and possibly, other viral hemorrhagic fevers.

Author Notes

* Address correspondence to Heather M. Lander, Sealy Center for Structural Biology and Molecular Biophysics, University of Texas Medical Branch, 301 University Boulevard, Galveston, TX 77555. E-mail: hmlander@utmb.edu

Financial support: This work was supported by the Department of Pathology, University of Texas Medical Branch; National Institutes of Health Biodefense Training Grant T32 AI060549; and the John Sealy Foundation, University of Texas Medical Branch.

Authors' addresses: Heather M. Lander, Sealy Center for Structural Biology and Molecular Biophysics, University of Texas Medical Branch, Galveston, TX, E-mail: hmlander@utmb.edu. Ashley M. Grant, United States Department of Defense, Washington, DC, E-mail: ashleymariegrant@gmail.com. Thomas Albrecht, Department of Microbiology and Immunology, University of Texas Medical Branch, Galveston, TX, E-mail: talbrecht731@yahoo.com. Terence Hill, Department of Microbiology and Immunology, University of Texas Medical Branch, Galveston, TX, E-mail: tehill@utmb.edu. Clarence J. Peters, Department of Microbiology and Immunology, University of Texas Medical Branch, Galveston, TX, E-mail: cjpeters@utmb.edu.

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