Thromb Haemost 2009; 102(06): 1024-1029
DOI: 10.1160/TH09-06-0357
Theme Issue Article
Schattauer GmbH

The role of the vascular endothelium in arenavirus haemorrhagic fevers

Stefan Kunz
1   Institute of Microbiology, University Hospital Center and University of Lausanne, Lausanne, Switzerland
› Author Affiliations
Further Information

Publication History

Received: 08 June 2009

Accepted after minor revision: 13 August 2009

Publication Date:
28 November 2017 (online)

Summary

Viral haemorrhagic fevers (VHF) caused by arenaviruses are among the most devastating emerging human diseases.The most important pathogen among the arenaviruses is Lassa virus (LASV), the causative agent of Lassa fever that is endemic to West Africa. On the South American continent, the New World arenavirus Junin virus (JUNV), Machupo (MACV), Guanarito (GTOV), and Sabia virus (SABV) have emerged as causative agents of severe VHFs. Clinical and experimental studies on arenavirus VHF have revealed a crucial role of the endothelium in their pathogenesis. However, in contrast to other VHFs, haemorrhages are not a salient feature of Lassa fever and fatal cases do not show overt destruction of vascular tissue.The functional alteration of the vascular endothelium that precede shock and death in fatal Lassa fever may be due to more subtle direct or indirect effects of the virus on endothelial cells. Haemorrhagic disease manifestations and vascular involvement are more pronounced in the VHF caused by the South American haemorrhagic fever viruses. Recent studies on JUNV revealed perturbation of specific endothelial cell function, including expression of cell adhesion molecules, coagulation factors, and vasoactive mediators as a consequence of productive viral infection.These studies provided first possible links to some of the vascular abnormalities observed in patients; however, their relevance in vivo remains to be investigated.

 
  • References

  • 1 Geisbert TW, Jahrling PB. Exotic emerging viral diseases: progress and challenges. Nat Med 2004; 10 (Suppl. 12) S110-121.
  • 2 Peters CJ. Human infection with arenaviruses in the Americas. Curr Top Microbiol Immunol 2002; 262: 65-74.
  • 3 Delgado S, Erickson BR, Agudo R. et al. Chapare virus, a newly discovered arenavirus isolated from a fatal hemorrhagic fever case in Bolivia. PLoS Pathog 2008; 04: e1000047.
  • 4 Briese T, Paweska JT, McMullan LK. et al. Genetic detection and characterization of Lujo virus, a new hemorrhagic fever-associated arenavirus from southern Africa. PLoS Pathog 2009; 05: e1000455.
  • 5 Borio L, Inglesby T, Peters CJ. et al. Hemorrhagic fever viruses as biological weapons: medical and public health management. Jama 2002; 287: 2391-2405.
  • 6 Oldstone MB. Biology and Pathogenesis of Lymphocytic Choriomeningitis Virus Infection. In: Oldstone MB. editor. Arenaviruses; 2002: 83-118.
  • 7 Buchmeier MJ, de la Torre JC, Peters CJ. Arenaviridae: the viruses and their replication. In: Knipe DL, Howley PM. editors. Fields Virology. 4th ed. Lippincott-Raven: Philadelphia; 2007: 1791-1828.
  • 8 Charrel RN, de Lamballerie X, Emonet S. Phylogeny of the genus Arenavirus. Curr Opin Microbiol 2008; 11: 362-368.
  • 9 Charrel RN, Feldmann H, Fulhorst CF. et al. Phylogeny of New World arenaviruses based on the complete coding sequences of the small genomic segment identified an evolutionary lineage produced by intrasegmental recombination. Biochem Biophys Res Commun 2002; 296: 1118-1124.
  • 10 Charrel RN, Lemasson JJ, Garbutt M. et al. New insights into the evolutionary relationships between arenaviruses provided by comparative analysis of small and large segment sequences. Virology 2003; 317: 191-196.
  • 11 Archer AM, Rico-Hesse R, Garcia JB. et al. High genetic divergence and recombination in Arenaviruses from the Americas. Virology 2002; 304: 274-281.
  • 12 Clegg JC. Molecular phylogeny of the arenaviruses. Curr Top Microbiol Immunol 2002; 262: 1-24.
  • 13 McCormick JB, Fisher-Hoch SP. Lassa fever. Curr Top Microbiol Immunol 2002; 262: 75-109.
  • 14 Richmond JK, Baglole DJ. Lassa fever: epidemiology, clinical features, and social consequences. BMJ 2003; 327: 1271-1275.
  • 15 Buckley SM, Casals J. Lassa fever, a new virus disease of man from West. 3. Isolation and characterization of the virus. Africa. Am J Trop Med Hyg 1970; 19: 680-691.
  • 16 Buckley SM, Casals J, Downs WG. Isolation and antigenic characterization of Lassa virus. Nature 1970; 227: 174.
  • 17 Monath TP, Newhouse VF, Kemp GE. et al. Lassa virus isolation from Mastomys natalensis rodents during an epidemic in Sierra Leone. Science 1974; 185: 263-265.
  • 18 Keenlyside RA, McCormick JB, Webb PA. et al. Case-control study of Mastomys natalensis and humans in Lassa virus-infected households in Sierra Leone. Am J Trop Med Hyg 1983; 32: 829-837.
  • 19 Carey DE, Kemp GE, White HA. et al. Lassa fever. Epidemiological aspects of the 1970 epidemic, Jos, Nigeria. Trans R Soc Trop Med Hyg 1972; 66: 402-408.
  • 20 White HA. Lassa fever. A study of 23 hospital cases. Trans R Soc Trop Med Hyg 1972; 66: 390-401.
  • 21 Monath TP. Lassa fever. Trop Doct 1973; 03: 155-161.
  • 22 Fisher-Hoch SP, Tomori O, Nasidi A. et al. Review of cases of nosocomial Lassa fever in Nigeria: the high price of poor medical practice. BMJ 1995; 311: 857-859.
  • 23 McCormick JB, King IJ, Webb PA. et al. A case-control study of the clinical diagnosis and course of Lassa fever. J Infect Dis 1987; 155: 445-455.
  • 24 Cummins D, McCormick JB, Bennett D. et al. Acute sensorineural deafness in Lassa fever. Jama 1990; 264: 2093-2096.
  • 25 Johnson KM, McCormick JB, Webb PA. et al. Clinical virology of Lassa fever in hospitalized patients. J Infect Dis 1987; 155: 456-464.
  • 26 Walker DH, McCormick JB, Johnson KM. et al. Pathologic and virologic study of fatal Lassa fever in man. Am J Pathol 1982; 107: 349-356.
  • 27 McCormick JB, Walker DH, King IJ. et al. Lassa virus hepatitis: a study of fatal Lassa fever in humans. Am J Trop Med Hyg 1986; 35: 401-407.
  • 28 Fisher-Hoch S, McCormick JB, Sasso D. et al. Hematologic dysfunction in Lassa fever. J Med Virol 1988; 26: 127-135.
  • 29 Cummins D, Fisher-Hoch SP, Walshe KJ. et al. A plasma inhibitor of platelet aggregation in patients with Lassa fever. Br J Haematol 1989; 72: 543-548.
  • 30 Lukashevich IS, Maryankova R, Vladyko AS. et al. 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 1999; 59: 552-560.
  • 31 Fisher-Hoch SP, Mitchell SW, Sasso DR. et al. Physiological and immunologic disturbances associated with shock in a primate model of Lassa fever. J Infect Dis 1987; 155: 465-474.
  • 32 Aleksandrowicz P, Wolf K, Falzarano D. et al. Viral haemorrhagic fever and vascular alterations. Hamostaseologie 2008; 28: 77-84.
  • 33 Schnittler HJ, Feldmann H. Viral haemorrhagic fever--a vascular disease?. Thromb Haemost 2003; 89: 967-972.
  • 34 Baize S, Kaplon J, Faure C. et al. Lassa virus infection of human dendritic cells and macrophages is productive but fails to activate cells. J Immunol 2004; 172: 2861-2869.
  • 35 Mahanty S, Hutchinson K, Agarwal S. et al. Cutting edge: impairment of dendritic cells and adaptive immunity by Ebola and Lassa viruses. J Immunol 2003; 170: 2797-2801.
  • 36 Mahanty S, Bausch DG, Thomas RL. et al. Low levels of interleukin-8 and interferon-inducible protein-10 in serum are associated with fatal infections in acute Lassa fever. J Infect Dis 2001; 183: 1713-1721.
  • 37 Rojek JM, Spiropoulou CF, Campbell KP. et al. Old World and Clade C New World Arenaviruses Mimic the Molecular Mechanism of Receptor Recognition Used by {alpha}-Dystroglycan’s Host-Derived Ligands. J Virol 2007; 81: 5685-5695.
  • 38 Arribalzaga RA. [New epidemic disease due to unidentified germ: nephrotoxic, leukopenic and enanthematous hyperthermia.]. Dia Med 1955; 27: 1204-1210.
  • 39 Parodi AS, Greenway DJ, Rugiero HR. et al. [Concerning the epidemic outbreak in Junin.]. Dia Med 1958; 30: 2300-2301.
  • 40 Kenyon RH, McKee Jr. KT, Zack PM. et al. Aerosol infection of rhesus macaques with Junin virus. Intervirology 1992; 33: 23-31.
  • 41 Harrison LH, Halsey NA, McKee Jr. KT. et al. Clinical case definitions for Argentine hemorrhagic fever. Clin Infect Dis 1999; 28: 1091-1094.
  • 42 Weissenbacher MC, Laguens RP, Coto CE. Argentine hemorrhagic fever. Curr Top Microbiol Immunol 1987; 134: 79-116.
  • 43 de Bracco MM, Rimoldi MT, Cossio PM. et al. Argentine hemorrhagic fever. Alterations of the complement system and anti-Junin-virus humoral response. N Engl J Med 1978; 299: 216-221.
  • 44 Marta RF, Montero VS, Hack CE. et al. Proinflammatory cytokines and elastase-alpha-1-antitrypsin in Argentine hemorrhagic fever. Am J Trop Med Hyg 1999; 60: 85-89.
  • 45 Heller MV, Marta RF, Sturk A. et al. Early markers of blood coagulation and fibrinolysis activation in Argentine haemorrhagic fever. Thromb Haemost 1995; 73: 368-373.
  • 46 Molinas FC, de Bracco MM, Maiztegui JI. Hemostasis and the complement system in Argentine hemorrhagic fever Rev Infect Dis 1989; 11 (Suppl. 04) S762-70.
  • 47 Johnson KM, Halstead SB, Cohen SN. Hemorrhagic fevers of Southeast Asia and South America: a comparative appraisal. Prog Med Virol 1967; 09: 105-58.
  • 48 Johnson KM, Kuns ML, Mackenzie RB. et al. Isolation of Machupo virus from wild rodent Calomys callosus. Am J Trop Med Hyg 1966; 15: 103-106.
  • 49 Mercado R. Rodent control programmes in areas affected by Bolivian haemorrhagic fever. Bull World Health Organ 1975; 52: 691-696.
  • 50 Salas R, de Manzione N, Tesh RB. et al. Venezuelan haemorrhagic fever. Lancet 1991; 338: 1033-1036.
  • 51 Tesh RB, Jahrling PB, Salas R. et al. Description of Guanarito virus (Arenaviridae: Arenavirus), the etiologic agent of Venezuelan hemorrhagic fever. Am J Trop Med Hyg 1994; 50: 452-459.
  • 52 de Manzione N, Salas RA, Paredes H. et al. Venezuelan hemorrhagic fever: clinical and epidemiological studies of 165 cases. Clin Infect Dis 1998; 26: 308-313.
  • 53 Stinebaugh BJ, Schloeder FX, Johnson KM. et al. Bolivian hemorrhagic fever. A report of four cases. Am J Med 1966; 40: 217-230.
  • 54 Kilgore PE, Peters CJ, Mills JN. et al. Prospects for the control of Bolivian hemorrhagic fever. Emerg Infect Dis 1995; 01: 97-100.
  • 55 Enria DA, Barrera Oro JG. Junin virus vaccines. Curr Top Microbiol Immunol 2002; 263: 239-261.
  • 56 Enria DA, Briggiler AM, Fernandez NJ. et al. Importance of dose of neutralising antibodies in treatment of Argentine haemorrhagic fever with immune plasma. Lancet 1984; 02: 255-256.
  • 57 Enria DA, Maiztegui JI. Antiviral treatment of Argentine hemorrhagic fever. Antiviral Res 1994; 23: 23-31.
  • 58 Maiztegui JI, Fernandez NJ, de Damilano AJ. Efficacy of immune plasma in treatment of Argentine haemorrhagic fever and association between treatment and a late neurological syndrome. Lancet 1979; 02: 1216-1217.
  • 59 Radoshitzky SR, Abraham J, Spiropoulou CF. et al. Transferrin receptor 1 is a cellular receptor for New World haemorrhagic fever arenaviruses. Nature 2007; 446: 92-96.
  • 60 Andrews BS, Theofilopoulos AN, Peters CJ. et al. Replication of dengue and junin viruses in cultured rabbit and human endothelial cells. Infect Immun 1978; 20: 776-781.
  • 61 Gomez RM, Pozner RG, Lazzari MA. et al. Endothelial cell function alteration after Junin virus infection. Thromb Haemost 2003; 90: 326-333.
  • 62 Yun NE, Linde NS, Dziuba N. et al. Pathogenesis of XJ and Romero strains of Junin virus in two strains of guinea pigs. Am J Trop Med Hyg 2008; 79: 275-282.
  • 63 Bockeler M, Stroher U, Seebach J. et al. Breakdown of paraendothelial barrier function during Marburg virus infection is associated with early tyrosine phosphorylation of platelet endothelial cell adhesion molecule-1. J Infect Dis 2007; 196 (Suppl. 02) S337-346.
  • 64 Wahl-Jensen VM, Afanasieva TA, Seebach J. et al. Effects of Ebola virus glycoproteins on endothelial cell activation and barrier function. J Virol 2005; 79: 10442-10450.