1921
Volume 90, Issue 6
  • ISSN: 0002-9637
  • E-ISSN: 1476-1645

Abstract

Abstract.

Junín virus (JUNV) is endemic to the fertile Pampas of Argentina, maintained in nature by the rodent host , 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) 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.

Loading

Article metrics loading...

/content/journals/10.4269/ajtmh.13-0382
2014-06-04
2017-11-24
Loading full text...

Full text loading...

/deliver/fulltext/14761645/90/6/993.html?itemId=/content/journals/10.4269/ajtmh.13-0382&mimeType=html&fmt=ahah

References

  1. Bushar G, Sagripanti JL, , 1997. Molecular characteristics of Junin virus. J Virol Methods 63: 2735.[Crossref]
  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.[Crossref]
  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.
  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.
  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.[Crossref]
  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.
  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.
  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.[Crossref]
  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.[Crossref]
  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.[Crossref]
  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.[Crossref]
  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.[Crossref]
  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.
  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.[Crossref]
  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.[Crossref]
  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.[Crossref]
  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.[Crossref]
  19. Lampugnani MG, , 2010. Endothelial adherens junctions and the actin cytoskeleton: an ‘infinity net’? J Biol 9: 16.[Crossref]
  20. Harris TJ, Tepass U, , 2010. Adherens junctions: from molecules to morphogenesis. Nat Rev Mol Cell Biol 11: 502514.[Crossref]
  21. Vincent PA, Xiao K, Buckley KM, Kowalczyk AP, , 2004. VE-cadherin: adhesion at arm's length. Am J Physiol Cell Physiol 286: C987C997.[Crossref]
  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.[Crossref]
  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.[Crossref]
  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.[Crossref]
  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.[Crossref]
  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.[Crossref]
  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.[Crossref]
  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.[Crossref]
  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.[Crossref]
  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.
  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.[Crossref]
  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.[Crossref]
  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.[Crossref]
  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.[Crossref]
  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.[Crossref]
  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.[Crossref]
  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.[Crossref]
  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.
  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.[Crossref]
  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.[Crossref]
  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.[Crossref]
  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.[Crossref]
  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.[Crossref]
  46. Candurra NA, Lago MJ, Maskin L, Damonte EB, , 1999. Involvement of the cytoskeleton in Junin virus multiplication. J Gen Virol 80: 147156.[Crossref]
  47. Martinez MG, Cordo SM, Candurra NA, , 2008. Involvement of cytoskeleton in Junin virus entry. Virus Res 138: 1725.[Crossref]
  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.[Crossref]
  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.
  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.[Crossref]
  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.[Crossref]
  52. Arroyo AG, Iruela-Arispe ML, , 2010. Extracellular matrix, inflammation, and the angiogenic response. Cardiovasc Res 86: 226235.[Crossref]
  53. Feldmann H, Klenk HD, , 1996. Marburg and Ebola viruses. Adv Virus Res 47: 152.[Crossref]
  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.[Crossref]
  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.[Crossref]
http://instance.metastore.ingenta.com/content/journals/10.4269/ajtmh.13-0382
Loading
/content/journals/10.4269/ajtmh.13-0382
Loading

Data & Media loading...

  • Received : 27 Jun 2013
  • Accepted : 19 Nov 2013

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error