Hantavirus-induced immunity in rodent reservoirs and humans

Immunological Reviews

Volumn 225, Issue 1, 2008, Pages 163-189

  Schönrich, Günther ^a   Rang, Andreas ^a   Lütteke, Nina ^a   Raftery, Martin J ^a   Charbonnel, Nathalie ^b   Ulrich, Rainer G ^c  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b CENTRE DE BIOLOGIE ET DE GESTION DES POPULATIONS   (France)

^c FEDERAL RESEARCH INSTITUTE FOR ANIMAL HEALTH   (Germany)

Author keywords

Cell mediated pathogenesis; Hantavirus cardiopulmonary syndrome; Hantaviruses; Immunopathogenesis; Rodent reservoir; Transmission; Viral hemorrhagic fever

Indexed keywords

BETA3 INTEGRIN; VASCULOTROPIN; VASCULOTROPIN INHIBITOR; VASCULOTROPIN RECEPTOR 2; VERY LATE ACTIVATION ANTIGEN 5; VIRUS GLYCOPROTEIN;

ADAPTIVE IMMUNITY; ANDES VIRUS; APOPTOSIS; ARTIFICIAL VENTILATION; ASH RIVER VIRUS; B LYMPHOCYTE; BAYOU VIRUS; BLACK CREEK CANAL VIRUS; CAMP RIPLEY VIRUS; CAO BANG VIRUS; CARDIOGENIC SHOCK; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL MEMBRANE PERMEABILITY; CELL MOTILITY; CELLULAR IMMUNODEFICIENCY; CYTOTOXIC T LYMPHOCYTE; DENDRITIC CELL; DOBRAVA BELGRADE VIRUS; GEOGRAPHIC DISTRIBUTION; HANTAVIRUS; HANTAVIRUS CARDIOPULMONARY SYNDROME; HEMOCONCENTRATION; HUMAN; HUMORAL IMMUNITY; HYPOTENSION; HYPOXEMIA; IMMUNOGENETICS; IMMUNOPATHOGENESIS; INFECTION SENSITIVITY; INNATE IMMUNITY; ISLA VISTA VIRUS; JEMEZ SPRINGS VIRUS; LEUKOCYTOSIS; MAPORAL VIRUS; MOLECULAR EVOLUTION; NEPHROPATHIA EPIDEMICA; NEW YORK VIRUS; NONHUMAN; PERSISTENT INFECTION; PRIORITY JOURNAL; PROSPECT HILL VIRUS; PROTEIN MOTIF; PUUMALA VIRUS; REGULATORY T LYMPHOCYTE; RESPIRATORY FAILURE; RESPIRATORY TRACT DISEASE; REVIEW; RODENT; SANGASSOU VIRUS; SEEWIS VIRUS; SEOUL VIRUS; SIN NOMBRE VIRUS; SPECIES; T LYMPHOCYTE ACTIVATION; TANGANYA VIRUS; TH1 CELL; TH2 CELL; THAILAND VIRUS; THOTTAPALAYAM VIRUS; THROMBOCYTOPENIA; TULA VIRUS; VASODILATATION; VIRUS CELL INTERACTION; VIRUS GENOME; VIRUS HEMORRHAGIC FEVER; VIRUS IMMUNITY; VIRUS INFECTION; VIRUS MORPHOLOGY; VIRUS PATHOGENESIS; VIRUS REPLICATION; VIRUS STRAIN; VIRUS TRANSMISSION;

ANIMALS; ANTIBODIES, VIRAL; APOPTOSIS; DENDRITIC CELLS; DISEASE RESERVOIRS; HANTAVIRUS; HANTAVIRUS INFECTIONS; HUMANS; IMMUNITY, ACTIVE; IMMUNITY, INNATE; INTEGRINS; RODENTIA; T-LYMPHOCYTE SUBSETS; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 52049112067     PISSN: 01052896     EISSN: 1600065X     Source Type: Journal    
DOI: 10.1111/j.1600-065X.2008.00694.x     Document Type: Review

References (328)

1. Jones KE, et al. Global trends in emerging infectious diseases. Nature 2008 451 : 990 993.
2. Murphy FA. Emerging zoonoses: the challenge for public health and biodefense. Prev Vet Med 2008 86 : 216 223.
3. Peters CJ. Emerging infections: lessons from the viral hemorrhagic fevers. Trans Am Clin Climatol Assoc 2006 117 : 189 197.
4. Vorou RM, Papavassiliou VG, Tsiodras S. Emerging zoonoses and vector-borne infections affecting humans in Europe. Epidemiol Infect 2007 135 : 1231 1247.
5. Johnson KM. Hantaviruses: history and overview. Curr Top Microbiol Immunol 2001 256 : 1 14.
6. Lee HW, Lee PW, Johnson KM. Isolation of the etiologic agent of Korean Hemorrhagic fever. J Infect Dis 1978 137 : 298 308.
7. Brummer-Korvenkontio M, et al. Nephropathia epidemica: detection of antigen in bank voles and serologic diagnosis of human infection. J Infect Dis 1980 141 : 131 134.
8. Lee HW, Baek LJ, Johnson KM. Isolation of Hantaan virus, the etiologic agent of Korean hemorrhagic fever, from wild urban rats. J Infect Dis 1982 146 : 638 644.
9. Lee PW, Amyx HL, Yanagihara R, Gajdusek DC, Goldgaber D, Gibbs CJ Jr. Partial characterization of Prospect Hill virus isolated from meadow voles in the United States. J Infect Dis 1985 152 : 826 829.
10. CDC., 2008.
11. Nichol ST, et al. Genetic identification of a hantavirus associated with an outbreak of acute respiratory illness. Science 1993 262 : 914 917.
12. Schmaljohn C, Hjelle B. Hantaviruses: a global disease problem. Emerg Infect Dis 1997 3 : 95 104.
13. Zavasky DM, Hjelle B, Peterson MC, Denton RW, Reimer L. Acute infection with Sin Nombre hantavirus without pulmonary edema. Clin Infect Dis 1999 29 : 664 666.
14. Childs JE, et al. Serologic and genetic identification of Peromyscus maniculatus as the primary rodent reservoir for a new hantavirus in the southwestern United States. J Infect Dis 1994 169 : 1271 1280.
15. Hjelle B, Glass GE. Outbreak of hantavirus infection in the Four Corners region of the United States in the wake of the 1997-1998 El Nino-southern oscillation. J Infect Dis 2000 181 : 1569 1573.
16. Carey DE, Reuben R, Panicker KN, Shope RE, Myers RM. Thottapalayam virus: a presumptive arbovirus isolated from a shrew in India. Indian J Med Res 1971 59 : 1758 1760.
17. Song JW, Baek LJ, Schmaljohn CS, Yanagihara R. Thottapalayam virus, a prototype shrewborne hantavirus. Emerg Infect Dis 2007 13 : 980 985.
18. Arai S, et al. Hantavirus in northern short-tailed shrew, United States. Emerg Infect Dis 2007 13 : 1420 1423.
19. Arai S, et al. Phylogenetically distinct hantaviruses in the masked shrew (Sorex cinereus) and dusky shrew (Sorex monticolus) in the United States. Am J Trop Med Hyg 2008 78 : 348 351.
20. Klempa B, et al. Novel hantavirus sequences in Shrew, Guinea. Emerg Infect Dis 2007 13 : 520 522.
21. Song JW, et al. Newfound hantavirus in Chinese mole shrew, Vietnam. Emerg Infect Dis 2007 13 : 1784 1787.
22. Wilson DE, Reeder DAM, eds. Mammal Species of the World. A Taxonomic and Geographic Reference, 3rd edn. Baltimore : Johns Hopkins University Press, 2005.
23. Nichol ST, Beaty BJ, Goldbach R, Plyusnin A, Schmaljohn CS, Tesh RB. Family Bunyaviridae. In : Fauquet CM, Mayo MA, Maniloff J, Desselberger U, Ball LA, eds. Virus Taxonomy: VIIIth Report of the International Committee on Taxonomy of Viruses. Amsterdam : Elsevier Academic Press, 2005 : 231 238.
24. Bridgen A, Weber F, Fazakerley JK, Elliott RM. Bunyamwera bunyavirus nonstructural protein NSs is a nonessential gene product that contributes to viral pathogenesis. Proc Natl Acad Sci USA 2001 98 : 664 669.
25. Weber F, Dunn EF, Bridgen A, Elliott RM. The Bunyamwera virus nonstructural protein NSs inhibits viral RNA synthesis in a minireplicon system. Virology 2001 281 : 67 74.
26. Schmaljohn CS, Nichol ST. Bunyaviridae. In : Knipe DM, Howley PM, eds. Fields Virology, Vol. 2, 5th edn. Philadelphia : Lippincott Williams & Wilkins, 2007 : 1741 1789.
27. Jaaskelainen KM, et al. Tula and Puumala hantavirus NSs ORFs are functional and the products inhibit activation of the interferon-beta promoter. J Med Virol 2007 79 : 1527 1536.
28. Jaaskelainen KM, Plyusnina A, Lundkvist A, Vaheri A, Plyusnin A. Tula hantavirus isolate with the full-length ORF for nonstructural protein NSs survives for more consequent passages in interferon-competent cells than the isolate having truncated NSs ORF. Virol J 2008 5 : 3.
29. Plyusnin A, Morzunov SP. Virus evolution and genetic diversity of hantaviruses and their rodent hosts. Curr Top Microbiol Immunol 2001 256 : 47 75.
30. Ulrich R, Hjelle B, Pitra C, Kruger DH. Emerging viruses: the case 'hantavirus'. Intervirology 2002 45 : 318 327.
31. Rang A, Heider H, Ulrich R, Kruger DH. A novel method for cloning of non-cytolytic viruses. J Virol Methods 2006 135 : 26 31.
32. Gavrilovskaya IN, Brown EJ, Ginsberg MH, Mackow ER. Cellular entry of hantaviruses which cause hemorrhagic fever with renal syndrome is mediated by beta3 integrins. J Virol 1999 73 : 3951 3959.
33. Schmaljohn CS, Dalrymple JM. Analysis of Hantaan virus RNA: evidence for a new genus of Bunyaviridae. Virology 1983 131 : 482 491.
34. Guerrero CA, Mendez E, Zarate S, Isa P, Lopez S, Arias CF. Integrin alpha(v)beta(3) mediates rotavirus cell entry. Proc Natl Acad Sci USA 2000 97 : 14644 14649.
35. Jackson T, et al. Arginine-glycine-aspartic acid-specific binding by foot-and-mouth disease viruses to the purified integrin alpha(v)beta3 in vitro. J Virol 1997 71 : 8357 8361.
36. Roivainen M, et al. Entry of coxsackievirus A9 into host cells: specific interactions with alpha v beta 3 integrin, the vitronectin receptor. Virology 1994 203 : 357 365.
37. Wickham TJ, Mathias P, Cheresh DA, Nemerow GR. Integrins alpha v beta 3 and alpha v beta 5 promote adenovirus internalization but not virus attachment. Cell 1993 73 : 309 319.
38. Gavrilovskaya IN, Gorbunova EE, Mackow NA, Mackow ER. 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 2008 82 : 5797 5806.
39. Gavrilovskaya IN, Peresleni T, Geimonen E, Mackow ER. Pathogenic hantaviruses selectively inhibit beta3 integrin directed endothelial cell migration. Arch Virol 2002 147 : 1913 1931.
40. Chu JJ, Ng ML. Interaction of West Nile virus with alpha v beta 3 integrin mediates virus entry into cells. J Biol Chem 2004 279 : 54533 54541.
41. Krautkramer E, Zeier M. Hantavirus causing hemorrhagic fever with renal syndrome enters from the apical surface and requires decay-accelerating factor (DAF/CD55). J Virol 2008 82 : 4257 4264.
42. Jin M, et al. Hantaan virus enters cells by clathrin-dependent receptor-mediated endocytosis. Virology 2002 294 : 60 69.
43. Elliott RM, Schmaljohn CS, Collett MS. Bunyaviridae genome structure and gene expression. Curr Top Microbiol Immunol 1991 169 : 91 141.
44. Garcin D, et al. The 5′ ends of Hantaan virus (Bunyaviridae) RNAs suggest a prime-and-realign mechanism for the initiation of RNA synthesis. J Virol 1995 69 : 5754 5762.
45. Lee HW, Cho HJ. Electron microscope appearance of Hantaan virus, the causative agent of Korean haemorrhagic fever. Lancet 1981 1 : 1070 1072.
46. Ravkov EV, Nichol ST, Compans RW. Polarized entry and release in epithelial cells of Black Creek Canal virus, a New World hantavirus. J Virol 1997 71 : 1147 1154.
47. Ravkov EV, Nichol ST, Peters CJ, Compans RW. Role of actin microfilaments in Black Creek Canal virus morphogenesis. J Virol 1998 72 : 2865 2870.
48. Kallio ER, et al. Prolonged survival of Puumala hantavirus outside the host: evidence for indirect transmission via the environment. J Gen Virol 2006 87 : 2127 2134.
49. Douron E, et al. HFRS after a wild rodent bite in the Haute-Savoie-and risk of exposure to Hantaan-like virus in a Paris laboratory. Lancet 1984 1 : 676 677.
50. Padula P, et al. Transmission study of Andes hantavirus infection in wild sigmodontine rodents. J Virol 2004 78 : 11972 11979.
51. Yanagihara R, Amyx HL, Gajdusek DC. Experimental infection with Puumala virus, the etiologic agent of nephropathia epidemica, in bank voles (Clethrionomys glareolus). J Virol 1985 55 : 34 38.
52. Padula PJ, Edelstein A, Miguel SD, Lopez NM, Rossi CM, Rabinovich RD. Epidemic outbreak of Hantavirus pulmonary syndrome in Argentina. Molecular evidence of person to person transmission of Andes virus. Medicina (B Aires) 1998 58 (Suppl. 1) : 27 36.
53. Wells RM, et al. An unusual hantavirus outbreak in southern Argentina: person-to-person transmission? Hantavirus Pulmonary Syndrome Study Group for Patagonia. Emerg Infect Dis 1997 3 : 171 174.
54. Pettersson L, Klingstrom J, Hardestam J, Lundkvist A, Ahlm C, Evander M. Hantavirus RNA in saliva from patients with hemorrhagic fever with renal syndrome. Emerg Infect Dis 2008 14 : 406 411.
55. Jackson AP, Charleston MA. A cophylogenetic perspective of RNA-virus evolution. Mol Biol Evol 2004 21 : 45 57.
56. Herbreteau V, Gonzalez JP, Hugot JP. Implication of phylogenetic systematics of rodent-borne hantaviruses allows understanding of their distribution. Ann NY Acad Sci 2006 1081 : 39 56.
57. Botten J, et al. Shedding and intracage transmission of Sin Nombre hantavirus in the deer mouse (Peromyscus maniculatus) model. J Virol 2002 76 : 7587 7594.
58. Hutchinson KL, Rollin PE, Shieh WJ, Zaki S, Greer PW, Peters CJ. Transmission of Black Creek Canal virus between cotton rats. J Med Virol 2000 60 : 70 76.
59. Kallio ER. Experimental ecology on the interaction between the Puumala hantavirus and its host, the bank vole. 2006. Thesis, University of Jyväskylä.
60. Kariwa H, Fujiki M, Yoshimatsu K, Arikawa J, Takashima I, Hashimoto N. Urine-associated horizontal transmission of Seoul virus among rats. Arch Virol 1998 143 : 15 24.
61. Lee HW, Lee PW, Baek LJ, Song CK, Seong IW. Intraspecific transmission of Hantaan virus, etiologic agent of Korean hemorrhagic fever, in the rodent Apodemus agrarius. Am J Trop Med Hyg 1981 30 : 1106 1112.
62. Bernshtein AD, et al. Dynamics of Puumala hantavirus infection in naturally infected bank voles (Clethrinomys glareolus). Arch Virol 1999 144 : 2415 2428.
63. Easterbrook JD, Kaplan JB, Glass GE, Pletnikov MV, Klein SL. Elevated testosterone and reduced 5-HIAA concentrations are associated with wounding and hantavirus infection in male Norway rats. Horm Behav 2007 52 : 474 481.
64. Hinson ER, Shone SM, Zink MC, Glass GE, Klein SL. Wounding: the primary mode of Seoul virus transmission among male Norway rats. Am J Trop Med Hyg 2004 70 : 310 317.
65. Klein SL, Zink MC, Glass GE. Seoul virus infection increases aggressive behaviour in male Norway rats. Anim Behav 2004 67 : 421 429.
66. Root JJ, Black WC, Calisher CH, Wilson KR, Beaty BJ. Genetic relatedness of deer mice (Peromyscus maniculatus) infected with Sin Nombre virus. Vector Borne Zoonotic Dis 2004 4 : 149 157.
67. Escutenaire S, et al. Behavioral, physiologic, and habitat influences on the dynamics of Puumala virus infection in bank voles (Clethrionomys glareolus). Emerg Infect Dis 2002 8 : 930 936.
68. Botten J, et al. Experimental infection model for Sin Nombre hantavirus in the deer mouse (Peromyscus maniculatus). Proc Natl Acad Sci USA 2000 97 : 10578 10583.
69. Hjelle B, Yates T. Modeling hantavirus maintenance and transmission in rodent communities. Curr Top Microbiol Immunol 2001 256 : 77 90.
70. Klingstrom J, et al. Rodent host specificity of European hantaviruses: evidence of Puumala virus interspecific spillover. J Med Virol 2002 68 : 581 588.
71. Monroe MC, et al. Genetic diversity and distribution of Peromyscus-borne hantaviruses in North America. Emerg Infect Dis 1999 5 : 75 86.
72. Plyusnin A, et al. Sequences of wild Puumala virus genes show a correlation of genetic variation with geographic origin of the strains. J Gen Virol 1994 75 (Part 2) : 405 409.
73. Zou Y, et al. Genetic characterization of hantaviruses isolated from Guizhou, China: evidence for spillover and reassortment in nature. J Med Virol 2008 80 : 1033 1041.
74. Escutenaire S, Pastoret PP, Sjolander KB, Heyman P, Brochier B, Lundkvist A. Evidence of Puumala hantavirus infection in red foxes (Vulpes vulpes) in Belgium. Vet Rec 2000 147 : 365 366.
75. Essbauer S, et al. A new Puumala hantavirus subtype in rodents associated with an outbreak of Nephropathia epidemica in South-East Germany in 2004. Epidemiol Infect 2006 134 : 1333 1344.
76. Kimmig P, et al. Epidemiology of hantaviruses in Baden-Wurttemberg. Gesundheitswesen 2001 63 : 107 112.
77. Vahlenkamp M, Muller T, Tackmann K, Loschner U, Schmitz H, Schreiber M. The muskrat (Ondatra zibethicus) as a new reservoir for Puumala-like hantavirus strains in Europe. Virus Res 1998 57 : 139 150.
78. Hjelle B, et al. Genetic identification of a novel hantavirus of the harvest mouse Reithrodontomys megalotis. J Virol 1994 68 : 6751 6754.
79. Hjelle B, Anderson B, Torrez-Martinez N, Song W, Gannon WL, Yates TL. Prevalence and geographic genetic variation of hantaviruses of New World harvest mice (Reithrodontomys): identification of a divergent genotype from a Costa Rican Reithrodontomys mexicanus. Virology 1995 207 : 452 459.
80. Rawlings JA, et al. Cocirculation of multiple hantaviruses in Texas, with characterization of the small (S) genome of a previously undescribed virus of cotton rats (Sigmodon hispidus). Am J Trop Med Hyg 1996 55 : 672 679.
81. Rowe JE, et al. Coexistence of several novel hantaviruses in rodents indigenous to North America. Virology 1995 213 : 122 130.
82. Song W, et al. Isla Vista virus: a genetically novel hantavirus of the California vole Microtus californicus. J Gen Virol 1995 76 (Part 12) : 3195 3199.
83. Torrez-Martinez N, et al. Bayou virus-associated hantavirus pulmonary syndrome in Eastern Texas: identification of the rice rat, Oryzomys palustris, as reservoir host. Emerg Infect Dis 1998 4 : 105 111.
84. Ahlm C, et al. Serologic evidence of Puumala virus infection in wild moose in northern Sweden. Am J Trop Med Hyg 2000 62 : 106 111.
85. Leighton FA, Artsob HA, Chu MC, Olson JG. A serological survey of rural dogs and cats on the southwestern Canadian prairie for zoonotic pathogens. Can J Public Health 2001 92 : 67 71.
86. Malecki TM, Jillson GP, Thilsted JP, Elrod J, Torrez-Martinez N, Hjelle B. Serologic survey for hantavirus infection in domestic animals and coyotes from New Mexico and northeastern Arizona. J Am Vet Med Assoc 1998 212 : 970 973.
87. Kanerva M, Mustonen J, Vaheri A. Pathogenesis of Puumala and other hantavirus infections. Rev Med Virol 1998 8 : 67 86.
88. Kruger DH, Ulrich R, Lundkvist AA. Hantavirus infections and their prevention. Microbes Infect 2001 3 : 1129 1144.
89. Peters CJ, Simpson GL, Levy H. Spectrum of hantavirus infection: hemorrhagic fever with renal syndrome and hantavirus pulmonary syndrome. Annu Rev Med 1999 50 : 531 545.
90. Enria DA, Briggiler AM, Pini N, Levis S. Clinical manifestations of New World hantaviruses. Curr Top Microbiol Immunol 2001 256 : 117 134.
91. Mertz GJ, Hjelle B, Crowley M, Iwamoto G, Tomicic V, Vial PA. Diagnosis and treatment of new world hantavirus infections. Curr Opin Infect Dis 2006 19 : 437 442.
92. Linderholm M, Elgh F. Clinical characteristics of hantavirus infections on the Eurasian continent. Curr Top Microbiol Immunol 2001 256 : 135 151.
93. Lee M. Coagulopathy in patients with hemorrhagic fever with renal syndrome. J Korean Med Sci 1987 2 : 201 211.
94. Lee M, et al. Coagulopathy in hemorrhagic fever with renal syndrome (Korean hemorrhagic fever). Rev Infect Dis 1989 11 (Suppl. 4) : S877 S883.
95. Lee M, Lee JS, Kim BK. Disseminated intravascular coagulation in Korean hemorrhagic fever. Bibl Haematol 1983 49 : 181 199.
96. Cohen MS, Kwei HE, Chin CC, Ge HC. CNS manifestations of epidemic hemorrhagic fever. An advanced manifestation of disease associated with poor prognosis. Arch Intern Med 1983 143 : 2070 2072.
97. Lee JS. Clinical features of hemorrhagic fever with renal syndrome in Korea. Kidney Int 1991 35 (Suppl.) : S88 S93.
98. Mustonen J, Brummer-Korvenkontio M, Hedman K, Pasternack A, Pietila K, Vaheri A. Nephropathia epidemica in Finland: a retrospective study of 126 cases. Scand J Infect Dis 1994 26 : 7 13.
99. Settergren B. Clinical aspects of nephropathia epidemica (Puumala virus infection) in Europe: a review. Scand J Infect Dis 2000 32 : 125 132.
100. Nemirov K, et al. Isolation and characterization of Dobrava hantavirus carried by the striped field mouse (Apodemus agrarius) in Estonia. J Gen Virol 1999 80 (Part 2) : 371 379.
101. Kontkanen M, Puustjarvi T, Lahdevirta J. Myopic shift and its mechanism in nephropathia epidemica or Puumala virus infection. Br J Ophthalmol 1994 78 : 903 906.
102. Ahlm C, et al. Central nervous system and ophthalmic involvement in nephropathia epidemica (European type of haemorrhagic fever with renal syndrome). J Infect 1998 36 : 149 155.
103. Parssinen O, Klemetti A, Rossi-Rautiainen E, Forslund T. Ophthalmic manifestations of epidemic nephropathy. Acta Ophthalmol (Copenh) 1993 71 : 114 118.
104. Kanerva M, Paakkala A, Mustonen J, Paakkala T, Lahtela J, Pasternack A. Pulmonary involvement in nephropathia epidemica: radiological findings and their clinical correlations. Clin Nephrol 1996 46 : 369 378.
105. Linderholm M, Billstrom A, Settergren B, Tarnvik A. Pulmonary involvement in nephropathia epidemica as demonstrated by computed tomography. Infection 1992 20 : 263 266.
106. French GR, Foulke RS, Brand OA, Eddy GA, Lee HW, Lee PW. Korean hemorrhagic fever: propagation of the etiologic agent in a cell line of human origin. Science 1981 211 : 1046 1048.
107. Pensiero MN, Sharefkin JB, Dieffenbach CW, Hay J. Hantaan virus infection of human endothelial cells. J Virol 1992 66 : 5929 5936.
108. Raftery MJ, Kraus AA, Ulrich R, Kruger DH, Schonrich G. Hantavirus infection of dendritic cells. J Virol 2002 76 : 10724 10733.
109. Temonen M, Vapalahti O, Holthofer H, Brummer-Korvenkontio M, Vaheri A, Lankinen H. Susceptibility of human cells to Puumala virus infection. J Gen Virol 1993 74 (Part 3) : 515 518.
110. Yanagihara R, et al. Propagation of nephropathia epidemica virus in cell culture. Lancet 1984 1 : 1013.
111. Yanagihara R, Silverman DJ. Experimental infection of human vascular endothelial cells by pathogenic and nonpathogenic hantaviruses. Arch Virol 1990 111 : 281 286.
112. Lundkvist A, Cheng Y, Sjolander KB, Niklasson B, Vaheri A, Plyusnin A. Cell culture adaptation of Puumala hantavirus changes the infectivity for its natural reservoir, Clethrionomys glareolus, and leads to accumulation of mutants with altered genomic RNA S segment. J Virol 1997 71 : 9515 9523.
113. Chizhikov VE, Spiropoulou CF, Morzunov SP, Monroe MC, Peters CJ, Nichol ST. Complete genetic characterization and analysis of isolation of Sin Nombre virus. J Virol 1995 69 : 8132 8136.
114. Nemirov K, Lundkvist A, Vaheri A, Plyusnin A. Adaptation of Puumala hantavirus to cell culture is associated with point mutations in the coding region of the L segment and in the noncoding regions of the S segment. J Virol 2003 77 : 8793 8800.
115. Wahl-Jensen V, et al. Temporal analysis of Andes virus and Sin Nombre virus infections of Syrian hamsters. J Virol 2007 81 : 7449 7462.
116. Hooper JW, Larsen T, Custer DM, Schmaljohn CS. A lethal disease model for hantavirus pulmonary syndrome. Virology 2001 289 : 6 14.
117. Campen MJ, Milazzo ML, Fulhorst CF, Obot Akata CJ, Koster F. Characterization of shock in a hamster model of hantavirus infection. Virology 2006 356 : 45 49.
118. Milazzo ML, Eyzaguirre EJ, Molina CP, Fulhorst CF. Maporal viral infection in the Syrian golden hamster: a model of hantavirus pulmonary syndrome. J Infect Dis 2002 186 : 1390 1395.
119. Ebihara H, et al. Pathogenicity of Hantaan virus in newborn mice: genetic reassortant study demonstrating that a single amino acid change in glycoprotein G1 is related to virulence. J Virol 2000 74 : 9245 9255.
120. Wichmann D, et al. Hantaan virus infection causes an acute neurological disease that is fatal in adult laboratory mice. J Virol 2002 76 : 8890 8899.
121. Yanagihara R, Amyx HL, Lee PW, Asher DM, Gibbs CJ Jr., Gajdusek DC. Experimental hantavirus infection in nonhuman primates. Arch Virol 1988 101 : 125 130.
122. Groen J, et al. A macaque model for hantavirus infection. J Infect Dis 1995 172 : 38 44.
123. Klingstrom J, Plyusnin A, Vaheri A, Lundkvist A. Wild-type Puumala hantavirus infection induces cytokines, C-reactive protein, creatinine, and nitric oxide in cynomolgus macaques. J Virol 2002 76 : 444 449.
124. Janeway CA Jr., Medzhitov R. Innate immune recognition. Annu Rev Immunol 2002 20 : 197 216.
125. Janeway CA Jr. Approaching the asymptote evolution and revolution in immunology. Cold Spring Harb Symp Quant Biol 1989 54 (Part 1) : 1 13.
126. Thompson AJ, Locarnini SA. Toll-like receptors, RIG-I-like RNA helicases and the antiviral innate immune response. Immunol Cell Biol 2007 85 : 435 445.
127. Banchereau J, Steinman RM. Dendritic cells and the control of immunity. Nature 1998 392 : 245 252.
128. Mazzoni A, Segal DM. Controlling the Toll road to dendritic cell polarization. J Leukoc Biol 2004 75 : 721 730.
129. Padovan E, Landmann RM, De Libero G. How pattern recognition receptor triggering influences T cell responses: a new look into the system. Trends Immunol 2007 28 : 308 314.
130. Ouyang W, Kolls JK, Zheng Y. The biological functions of T helper 17 cell effector cytokines in inflammation. Immunity 2008 28 : 454 467.
131. Belkaid Y, Rouse BT. Natural regulatory T cells in infectious disease. Nat Immunol 2005 6 : 353 360.
132. Zhou Y. Regulatory T cells and viral infections. Front Biosci 2008 13 : 1152 1170.
133. Kang JI, Park SH, Lee PW, Ahn BY. Apoptosis is induced by hantaviruses in cultured cells. Virology 1999 264 : 99 105.
134. Markotic A, Hensley L, Geisbert T, Spik K, Schmaljohn C. Hantaviruses induce cytopathic effects and apoptosis in continuous human embryonic kidney cells. J Gen Virol 2003 84 : 2197 2202.
135. Hardestam J, Klingström J, Mattsson K, Lundkvist A. HFRS causing hantaviruses do not induce apoptosis in confluent Vero E6 and A-549 cells. J Med Virol 2005 76 : 234 240.
136. Xiong JP, Stehle T, Goodman SL, Arnaout MA. A novel adaptation of the integrin PSI domain revealed from its crystal structure. J Biol Chem 2004 279 : 40252 40254.
137. Raymond T, Gorbunova E, Gavrilovskaya IN, Mackow ER. Pathogenic hantaviruses bind plexin-semaphorin-integrin domains present at the apex of inactive, bent alphavbeta3 integrin conformers. Proc Natl Acad Sci USA 2005 102 : 1163 1168.
138. Hodivala-Dilke KM, et al. Beta3-integrin-deficient mice are a model for Glanzmann thrombasthenia showing placental defects and reduced survival. J Clin Invest 1999 103 : 229 238.
139. Hynes RO. Integrins: bidirectional, allosteric signaling machines. Cell 2002 110 : 673 687.
140. Martinez-Lemus LA, et al. Integrins as unique receptors for vascular control. J Vasc Res 2003 40 : 211 233.
141. Dvorak HF. Discovery of vascular permeability factor (VPF). Exp Cell Res 2006 312 : 522 526.
142. Robinson SD, Reynolds LE, Wyder L, Hicklin DJ, Hodivala-Dilke KM. Beta3-integrin regulates vascular endothelial growth factor-A-dependent permeability. Arterioscler Thromb Vasc Biol 2004 24 : 2108 2114.
143. Soldi R, Mitola S, Strasly M, Defilippi P, Tarone G, Bussolino F. Role of alphavbeta3 integrin in the activation of vascular endothelial growth factor receptor-2. EMBO J 1999 18 : 882 892.
144. Geimonen E, Fernandez I, Gavrilovskaya IN, Mackow ER. Tyrosine residues direct the ubiquitination and degradation of the NY-1 hantavirus G1 cytoplasmic tail. J Virol 2003 77 : 10760 10868.
145. Abram CL, Lowell CA. The expanding role for ITAM-based signaling pathways in immune cells. Sci STKE 2007 2007 : 2.
146. Jakus Z, Fodor S, Abram CL, Lowell CA, Mocsai A. Immunoreceptor-like signaling by beta 2 and beta 3 integrins. Trends Cell Biol 2007 17 : 493 501.
147. Sen N, Sen A, Mackow ER. Degrons at the C terminus of the pathogenic but not the nonpathogenic hantavirus G1 tail direct proteasomal degradation. J Virol 2007 81 : 4323 4330.
148. Borucki MK, et al. Role of maternal antibody in natural infection of Peromyscus maniculatus with Sin Nombre virus. J Virol 2000 74 : 2426 2429.
149. Dohmae K, Koshimizu U, Nishimune Y. In utero and mammary transfer of hantavirus antibody from dams to infant rats. Lab Anim Sci 1993 43 : 557 561.
150. Dohmae K, Nishimune Y. Protection against hantavirus infection by dam's immunity transferred vertically to neonates. Arch Virol 1995 140 : 165 172.
151. Dohmae K, Nishimune Y. Maternal transfer of hantavirus antibodies in rats. Lab Anim Sci 1998 48 : 395 397.
152. Kallio ER, et al. Maternal antibodies postpone hantavirus infection and enhance individual breeding success. Proc Biol Sci 2006 273 : 2771 2776.
153. Pai RK, et al. Absence of infection in a neonate after possible exposure to sin nombre hantavirus in breast milk. Clin Infect Dis 1999 29 : 1577 1579.
154. Childs JE, Glass GE, Korch GW, Leduc JW. Effects of hantaviral infection on survival, growth and fertility in wild rat (Rattus norvegicus) populations of Baltimore, Maryland. J Wildl Dis 1989 25 : 469 476.
155. Lyubsky S, Gavrilovskaya I, Luft B, Mackow E. Histopathology of Peromyscus leucopus naturally infected with pathogenic NY-1 hantaviruses: pathologic markers of HPS viral infection in mice. Lab Invest 1996 74 : 627 633.
156. Netski D, Thran BH, St Jeor SC. Sin Nombre virus pathogenesis in Peromyscus maniculatus. J Virol 1999 73 : 585 591.
157. Kallio ER, et al. Endemic hantavirus infection impairs the winter survival of its rodent host. Ecology 2007 88 : 1911 1916.
158. Villarreal LP, Defilippis VR, Gottlieb KA. Acute and persistent viral life strategies and their relationship to emerging diseases. Virology 2000 272 : 1 6.
159. Meyer BJ, Schmaljohn CS. Persistent hantavirus infections: characteristics and mechanisms. Trends Microbiol 2000 8 : 61 67.
160. Hutchinson KL, Rollin PE, Peters CJ. Pathogenesis of a North American hantavirus, Black Creek Canal virus, in experimentally infected Sigmodon hispidus. Am J Trop Med Hyg 1998 59 : 58 65.
161. Kariwa H, et al. Modes of Seoul virus infections: persistency in newborn rats and transiency in adult rats. Arch Virol 1996 141 : 2327 2338.
162. Botten J, et al. Persistent Sin Nombre virus infection in the deer mouse (Peromyscus maniculatus) model: sites of replication and strand-specific expression. J Virol 2003 77 : 1540 1550.
163. Arikawa J, Takashima I, Hashimoto N, Takahashi K, Yagi K, Hattori K. Epidemiological studies of hemorrhagic fever with renal syndrome (HFRS) related virus infection among urban rats in Hokkaido, Japan. Arch Virol 1986 88 : 231 240.
164. Deter J, et al. Kinship, dispersal and hantavirus transmission in bank and common voles. Arch Virol 2008 153 : 435 444.
165. Mills JN, Ksiazek TG, Peters CJ, Childs JE. Long-term studies of hantavirus reservoir populations in the southwestern United States: a synthesis. Emerg Infect Dis 1999 5 : 135 142.
166. Olsson GE, et al. Demographic factors associated with hantavirus infection in bank voles (Clethrionomys glareolus). Emerg Infect Dis 2002 8 : 924 929.
167. Klein SL, Bird BH, Glass GE. Sex differences in Seoul virus infection are not related to adult sex steroid concentrations in Norway rats. J Virol 2000 74 : 8213 8217.
168. Glass GE, et al. Black Creek canal virus infection in Sigmodon hispidus in southern Florida. Am J Trop Med Hyg 1998 59 : 699 703.
169. Mills JN, et al. Patterns of association with host and habitat: antibody reactive with Sin Nombre virus in small mammals in the major biotic communities of the southwestern United States. Am J Trop Med Hyg 1997 56 : 273 284.
170. Klein SL, Bird BH, Glass GE. Sex differences in immune responses and viral shedding following Seoul virus infection in Norway rats. Am J Trop Med Hyg 2001 65 : 57 63.
171. Klein SL, Cernetich A, Hilmer S, Hoffman EP, Scott AL, Glass GE. Differential expression of immunoregulatory genes in male and female Norway rats following infection with Seoul virus. J Med Virol 2004 74 : 180 190.
172. Klein SL, Marson AL, Scott AL, Ketner G, Glass GE. Neonatal sex steroids affect responses to Seoul virus infection in male but not female Norway rats. Brain Behav Immun 2002 16 : 736 746.
173. Hannah MF, Bajic VB, Klein SL. Sex differences in the recognition of and innate antiviral responses to Seoul virus in Norway rats. Brain Behav Immun 2008 22 : 503 516.
174. Schountz T, et al. Regulatory T cell-like responses in deer mice persistently infected with Sin Nombre virus. Proc Natl Acad Sci USA 2007 104 : 15496 15501.
175. Easterbrook JD, Zink MC, Klein SL. Regulatory T cells enhance persistence of the zoonotic pathogen Seoul virus in its reservoir host. Proc Natl Acad Sci USA 2007 104 : 15502 15507.
176. Zhang XK, Takashima I, Hashimoto N. Characteristics of passive immunity against hantavirus infection in rats. Arch Virol 1989 105 : 235 246.
177. Arikawa J, Yao JS, Yoshimatsu K, Takashima I, Hashimoto N. Protective role of antigenic sites on the envelope protein of Hantaan virus defined by monoclonal antibodies. Arch Virol 1992 126 : 271 281.
178. Schmaljohn CS, Chu YK, Schmaljohn AL, Dalrymple JM. Antigenic subunits of Hantaan virus expressed by baculovirus and vaccinia virus recombinants. J Virol 1990 64 : 3162 3170.
179. Dantas JR Jr., et al. Characterization of glycoproteins of viruses causing hemorrhagic fever with renal syndrome (HFRS) using monoclonal antibodies. Virology 1986 151 : 379 384.
180. Araki K, Yoshimatsu K, Lee BH, Kariwa H, Takashima I, Arikawa J. Hantavirus-specific CD8(+)-T-cell responses in newborn mice persistently infected with Hantaan virus. J Virol 2003 77 : 8408 8417.
181. Araki K, Yoshimatsu K, Lee BH, Kariwa H, Takashima I, Arikawa J. A new model of Hantaan virus persistence in mice: the balance between HTNV infection and CD8(+) T-cell responses. Virology 2004 322 : 318 327.
182. Dohmae K, Okabe M, Nishimune Y. Experimental transmission of hantavirus infection in laboratory rats. J Infect Dis 1994 170 : 1589 1592.
183. Asada H, et al. Role of T lymphocyte subsets in protection and recovery from Hantaan virus infection in mice. J Gen Virol 1987 68 : 1961 1969.
184. Asada H, Tamura M, Kondo K, Dohi Y, Yamanishi K. Cell-mediated immunity to virus causing haemorrhagic fever with renal syndrome: generation of cytotoxic T lymphocytes. J Gen Virol 1988 69 : 2179 2188.
185. Jin HK, et al. Mouse Mx2 protein inhibits hantavirus but not influenza virus replication. Arch Virol 2001 146 : 41 49.
186. Davis IC, Zajac AJ, Nolte KB, Botten J, Hjelle B, Matalon S. Elevated generation of reactive oxygen/nitrogen species in hantavirus cardiopulmonary syndrome. J Virol 2002 76 : 8347 8359.
187. Klingstrom J, et al. Nitric oxide and peroxynitrite have different antiviral effects against hantavirus replication and free mature virions. Eur J Immunol 2006 36 : 2649 2657.
188. de Carvalho NC, Gonzalez DV, Padula P, Bjorling E, Plyusnin A, Lundkvist A. Cross-protection against challenge with Puumala virus after immunization with nucleocapsid proteins from different hantaviruses. J Virol 2002 76 : 6669 6677.
189. Deter J, et al. Association between the DQA MHC class II gene and Puumala virus infection in Myodes glareolus, the bank vole. Infect Genet Evol 2008 8 : 450 458.
190. Schountz T, et al. Cloning and characterization of deer mouse (Peromyscus maniculatus) cytokine and chemokine cDNAs. BMC Immunol 2004 5 : 1.
191. Herbst MM, Prescott J, Palmer AD, Schountz T. Sequence and expression analysis of deer mouse interferon-gamma, interleukin-10, tumor necrosis factor, and lymphotoxin-alpha. Cytokine 2002 17 : 203 213.
192. Haller O, Kochs G, Weber F. The interferon response circuit: induction and suppression by pathogenic viruses. Virology 2006 344 : 119 130.
193. Haller O, Kochs G, Weber F. Interferon, Mx, and viral countermeasures. Cytokine Growth Factor Rev 2007 18 : 425 433.
194. Randall RE, Goodbourn S. Interferons and viruses: an interplay between induction, signalling, antiviral responses and virus countermeasures. J Gen Virol 2008 89 : 1 47.
195. Feuer R, Boone JD, Netski D, Morzunov SP, St Jeor SC. Temporal and spatial analysis of Sin Nombre virus quasispecies in naturally infected rodents. J Virol 1999 73 : 9544 9554.
196. Plyusnin A, et al. Genetic variation of wild Puumala viruses within the
197. Plyusnin A, Cheng Y, Lehvaslaiho H, Vaheri A. Quasispecies in wild-type Tula hantavirus populations. J Virol 1996 70 : 9060 9063.
198. Peebles RS Jr., Graham BS. Viruses, dendritic cells and the lung. Respir Res 2001 2 : 245 249.
199. Marty AM, Jahrling PB, Geisbert TW. Viral hemorrhagic fevers. Clin Lab Med 2006 26 : 345 386, viii.
200. Rinaldo CR Jr., Piazza P. Virus infection of dendritic cells: portal for host invasion and host defense. Trends Microbiol 2004 12 : 337 345.
201. Wu L, KewalRamani VN. Dendritic-cell interactions with HIV: infection and viral dissemination. Nat Rev Immunol 2006 6 : 859 868.
202. Bray M, Geisbert TW. Ebola virus: the role of macrophages and dendritic cells in the pathogenesis of Ebola hemorrhagic fever. Int J Biochem Cell Biol 2005 37 : 1560 1566.
203. Khaiboullina SF, Netski DM, Krumpe P, St Jeor SC. Effects of tumor necrosis factor alpha on Sin Nombre virus infection in vitro. J Virol 2000 74 : 11966 11971.
204. Hippenstiel S, Suttorp N. Interaction of pathogens with the endothelium. Thromb Haemost 2003 89 : 18 24.
205. Zaki SR, et al. Hantavirus pulmonary syndrome. Pathogenesis of an emerging infectious disease. Am J Pathol 1995 146 : 552 579.
206. Sundstrom JB, et al. Hantavirus infection induces the expression of RANTES and IP-10 without causing increased permeability in human lung microvascular endothelial cells. J Virol 2001 75 : 6070 6085.
207. Schnittler HJ, Feldmann H. Viral hemorrhagic fever - a vascular disease? Thromb Haemost 2003 89 : 967 972.
208. Takeuchi O, Akira S. Recognition of viruses by innate immunity. Immunol Rev 2007 220 : 214 224.
209. Unterholzner L, Bowie AG. The interplay between viruses and innate immune signaling: recent insights and therapeutic opportunities. Biochem Pharmacol 2008 75 : 589 602.
210. Kato H, et al. Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 2006 441 : 101 105.
211. Sumpter R, et al. Regulating intracellular antiviral defense and permissiveness to hepatitis C virus RNA replication through a cellular RNA helicase, RIG-I. J Virol 2005 79 : 2689 2699.
212. Yoneyama M, et al. Shared and unique functions of the DExD/H-box helicases RIG-I, MDA5, and LGP2 in antiviral innate immunity. J Immunol 2005 175 : 2851 2858.
213. Yoneyama M, Onomoto K, Fujita T. Cytoplasmic recognition of RNA. Adv Drug Deliv Rev 2008 60 : 841 846.
214. Habjan M, et al. Processing of genome 5′ termini as a strategy of negative-strand RNA viruses to avoid RIG-I-dependent interferon induction. PLoS ONE 2008 3 : e2032.
215. Alff PJ, et al. The pathogenic NY-1 hantavirus G1 cytoplasmic tail inhibits RIG-I- and TBK-1-directed interferon responses. J Virol 2006 80 : 9676 9686.
216. Prescott JB, Hall PR, Bondu-Hawkins VS, Ye C, Hjelle B. Early innate immune responses to Sin Nombre hantavirus occur independently of IFN regulatory factor 3, characterized pattern recognition receptors, and viral entry. J Immunol 2007 179 : 1796 1802.
217. Stetson DB, Medzhitov R. Type I interferons in host defense. Immunity 2006 25 : 373 381.
218. Raftery MJ, Winau F, Giese T, Kaufmann SH, Schaible UE, Schonrich G. Viral danger signals control CD1d de novo synthesis and NKT cell activation. Eur J Immunol 2008 38 : 668 679.
219. Tamura M, Asada H, Kondo K, Takahashi M, Yamanishi K. Effects of human and murine interferons against hemorrhagic fever with renal syndrome (HFRS) virus (Hantaan virus). Antiviral Res 1987 8 : 171 178.
220. Stoltz M, Ahlm C, Lundkvist A, Klingstrom J. Lambda interferon (IFN-lambda) in serum is decreased in hantavirus-infected patients, and in vitro-established infection is insensitive to treatment with all IFNs and inhibits IFN-gamma-induced nitric oxide production. J Virol 2007 81 : 8685 8691.
221. Andersson I, et al. Human MxA protein inhibits the replication of Crimean-Congo hemorrhagic fever virus. J Virol 2004 78 : 4323 4329.
222. Andersson I, Lundkvist A, Haller O, Mirazimi A. Type I interferon inhibits Crimean-Congo hemorrhagic fever virus in human target cells. J Med Virol 2006 78 : 216 222.
223. Bridgen A, Dalrymple DA, Weber F, Elliott RM. Inhibition of Dugbe nairovirus replication by human MxA protein. Virus Res 2004 99 : 47 50.
224. Frese M, Kochs G, Feldmann H, Hertkorn C, Haller O. Inhibition of bunyaviruses, phleboviruses, and hantaviruses by human MxA protein. J Virol 1996 70 : 915 923.
225. Kochs G, Janzen C, Hohenberg H, Haller O. Antivirally active MxA protein sequesters La Crosse virus nucleocapsid protein into perinuclear complexes. Proc Natl Acad Sci USA 2002 99 : 3153 3158.
226. Reichelt M, Stertz S, Krijnse-Locker J, Haller O, Kochs G. Missorting of LaCrosse virus nucleocapsid protein by the interferon-induced MxA GTPase involves smooth ER membranes. Traffic 2004 5 : 772 784.
227. Kanerva M, Melen K, Vaheri A, Julkunen I. Inhibition of Puumala and Tula hantaviruses in Vero cells by MxA protein. Virology 1996 224 : 55 62.
228. Geimonen E, Neff S, Raymond T, Kocer SS, Gavrilovskaya IN, Mackow ER. Pathogenic and nonpathogenic hantaviruses differentially regulate endothelial cell responses. Proc Natl Acad Sci USA 2002 99 : 13837 13842.
229. Khaiboullina SF, Rizvanov AA, Deyde VM, St Jeor SC. Andes virus stimulates interferon-inducible MxA protein expression in endothelial cells. J Med Virol 2005 75 : 267 275.
230. Kim IW, Hwang JY, Kim SK, Kim JK, Park HS. Interferon-stimulated genes response in endothelial cells following Hantaan virus infection. J Korean Med Sci 2007 22 : 987 992.
231. Kraus AA, et al. Differential antiviral response of endothelial cells after infection with pathogenic and nonpathogenic hantaviruses. J Virol 2004 78 : 6143 6150.
232. Spiropoulou CF, Albarino CG, Ksiazek TG, Rollin PE. Andes and Prospect Hill hantaviruses differ in early induction of interferon although both can downregulate interferon signaling. J Virol 2007 81 : 2769 2776.
233. Oelschlegel R, Kruger DH, Rang A. MxA-independent inhibition of Hantaan virus replication induced by type I and type II interferon in vitro. Virus Res 2007 127 : 100 105.
234. Reiss CS, Komatsu T. Does nitric oxide play a critical role in viral infections? J Virol 1998 72 : 4547 4551.
235. Groeneveld PH, Colson P, Kwappenberg KM, Clement J. Increased production of nitric oxide in patients infected with the European variant of hantavirus. Scand J Infect Dis 1995 27 : 453 456.
236. Linderholm M, Groeneveld PH, Tarnvik A. Increased production of nitric oxide in patients with hemorrhagic fever with renal syndrome - relation to arterial hypotension and tumor necrosis factor. Infection 1996 24 : 337 340.
237. Guidotti LG, Chisari FV. Noncytolytic control of viral infections by the innate and adaptive immune response. Annu Rev Immunol 2001 19 : 65 91.
238. Bradley JR. TNF-mediated inflammatory disease. J Pathol 2008 214 : 149 160.
239. Bray M, Mahanty S. Ebola hemorrhagic fever and septic shock. J Infect Dis 2003 188 : 1613 1617.
240. Laskin DL, Pendino KJ. Macrophages and inflammatory mediators in tissue injury. Annu Rev Pharmacol Toxicol 1995 35 : 655 677.
241. Nolte KB, et al. Hantavirus pulmonary syndrome in the United States: a pathological description of a disease caused by a new agent. Hum Pathol 1995 26 : 110 120.
242. Temonen M, Lankinen H, Vapalahti O, Ronni T, Julkunen I, Vaheri A. Effect of interferon-alpha and cell differentiation on Puumala virus infection in human monocyte/macrophages. Virology 1995 206 : 8 15.
243. Nagai T, et al. Isolation of haemorrhagic fever with renal syndrome virus from leukocytes of rats and virus replication in cultures of rat and human macrophages. J Gen Virol 1985 66 (Part 6) : 1271 1278.
244. Cebalo L, Markotic A. Chemokine production predominates in human monocytes infected with Tula virus. Viral Immunol 2007 20 : 206 213.
245. Krakauer T, Leduc JW, Krakauer H. Serum levels of tumor necrosis factor-alpha, interleukin-1, and interleukin-6 in hemorrhagic fever with renal syndrome. Viral Immunol 1995 8 : 75 79.
246. Linderholm M, Ahlm C, Settergren B, Waage A, Tarnvik A. Elevated plasma levels of tumor necrosis factor (TNF)-alpha, soluble TNF receptors, interleukin (IL)-6, and IL-10 in patients with hemorrhagic fever with renal syndrome. J Infect Dis 1996 173 : 38 43.
247. Ahmed R, Oldstone MB, Palese P. Protective immunity and susceptibility to infectious diseases: lessons from the 1918 influenza pandemic. Nat Immunol 2007 8 : 1188 1193.
248. Grayson MH, Holtzman MJ. Emerging role of dendritic cells in respiratory viral infection. J Mol Med 2007 85 : 1057 1068.
249. Pohl C, Shishkova J, Schneider-Schaulies S. Viruses and dendritic cells: enemy mine. Cell Microbiol 2007 9 : 279 289.
250. Raftery MJ, Schwab M, Eibert SM, Samstag Y, Walczak H, Schonrich G. Targeting the function of mature dendritic cells by human cytomegalovirus: a multilayered viral defense strategy. Immunity 2001 15 : 997 1009.
251. Muller DB, Raftery MJ, Kather A, Giese T, Schonrich G. Frontline: induction of apoptosis and modulation of c-FLIPL and p53 in immature dendritic cells infected with herpes simplex virus. Eur J Immunol 2004 34 : 941 951.
252. Larsson M, Beignon AS, Bhardwaj N. DC-virus interplay: a double edged sword. Semin Immunol 2004 16 : 147 161.
253. Pollara G, Kwan A, Newton PJ, Handley ME, Chain BM, Katz DR. Dendritic cells in viral pathogenesis: protective or defective? Int J Exp Pathol 2005 86 : 187 204.
254. Bosio CM, et al. Ebola and Marburg viruses replicate in monocyte-derived dendritic cells without inducing the production of cytokines and full maturation. J Infect Dis 2003 188 : 1630 1638.
255. Mahanty S, Hutchinson K, Agarwal S, McRae M, Rollin PE, Pulendran B. Cutting edge: impairment of dendritic cells and adaptive immunity by Ebola and Lassa viruses. J Immunol 2003 170 : 2797 2801.
256. Markotic A, Hensley L, Daddario K, Spik K, Anderson K, Schmaljohn C. Pathogenic hantaviruses elicit different immunoreactions in THP-1 cells and primary monocytes and induce differentiation of human monocytes to dendritic-like cells. Coll Antropol 2007 31 : 1159 1167.
257. Kilpatrick ED, Terajima M, Koster FT, Catalina MD, Cruz J, Ennis FA. Role of specific CD8+T cells in the severity of a fulminant zoonotic viral hemorrhagic fever, hantavirus pulmonary syndrome. J Immunol 2004 172 : 3297 3304.
258. Van Epps HL, et al. Long-lived memory T lymphocyte responses after hantavirus infection. J Exp Med 2002 196 : 579 588.
259. Kaukinen P, Vaheri A, Plyusnin A. Hantavirus nucleocapsid protein: a multifunctional molecule with both housekeeping and ambassadorial duties. Arch Virol 2005 150 : 1693 1713.
260. Van Epps HL, Schmaljohn CS, Ennis FA. Human memory cytotoxic T-lymphocyte (CTL) responses to Hantaan virus infection: identification of virus-specific and cross-reactive CD8(+) CTL epitopes on nucleocapsid protein. J Virol 1999 73 : 5301 5308.
261. Ennis FA, et al. Hantavirus pulmonary syndrome: CD8+ and CD4+ cytotoxic T lymphocytes to epitopes on Sin Nombre virus nucleocapsid protein isolated during acute illness. Virology 1997 238 : 380 390.
262. Terajima M, Hayasaka D, Maeda K, Ennis FA. Immunopathogenesis of hantavirus pulmonary syndrome and hemorrhagic fever with renal syndrome: do CD8+ T cells trigger capillary leakage in viral hemorrhagic fevers? Immunol Lett 2007 113 : 117 120.
263. Hayasaka D, Maeda K, Ennis FA, Terajima M. Increased permeability of human endothelial cell line EA. hy926 induced by hantavirus-specific cytotoxic T lymphocytes. Virus Res 2007 123 : 120 127.
264. Klingstrom J, et al. Loss of cell membrane integrity in Puumala hantavirus-infected patients correlates with levels of epithelial cell apoptosis and perforin. J Virol 2006 80 : 8279 8282.
265. Tuuminen T, et al. Human CD8+T cell memory generation in Puumala hantavirus infection occurs after the acute phase and is associated with boosting of EBV-specific CD8+ memory T cells. J Immunol 2007 179 : 1988 1995.
266. Chen LB, Yang WS. Abnormalities of T cell immunoregulation in hemorrhagic fever with renal syndrome. J Infect Dis 1990 161 : 1016 1019.
267. Huang C, Jin B, Wang M, Li E, Sun C. Hemorrhagic fever with renal syndrome: relationship between pathogenesis and cellular immunity. J Infect Dis 1994 169 : 868 870.
268. Tan LC, et al. A re-evaluation of the frequency of CD8+T cells specific for EBV in healthy virus carriers. J Immunol 1999 162 : 1827 1835.
269. Mullbacher A, Flynn K. Aspects of cytotoxic T cell memory. Immunol Rev 1996 150 : 113 127.
270. Baize S, et al. Defective humoral responses and extensive intravascular apoptosis are associated with fatal outcome in Ebola virus-infected patients. Nat Med 1999 5 : 423 426.
271. Sanchez A, et al. Analysis of human peripheral blood samples from fatal and nonfatal cases of Ebola (Sudan) hemorrhagic fever: cellular responses, virus load, and nitric oxide levels. J Virol 2004 78 : 10370 10377.
272. Vapalahti O, Lundkvist A, Vaheri A. Human immune response, host genetics, and severity of disease. Curr Top Microbiol Immunol 2001 256 : 153 169.
273. Gott P, Zoller L, Darai G, Bautz EK. A major antigenic domain of hantaviruses is located on the aminoproximal site of the viral nucleocapsid protein. Virus Genes 1997 14 : 31 40.
274. Kallio-Kokko H, Lundkvist A, Plyusnin A, Avsic-Zupanc T, Vaheri A, Vapalahti O. Antigenic properties and diagnostic potential of recombinant Dobrava virus nucleocapsid protein. J Med Virol 2000 61 : 266 274.
275. Kallio-Kokko H, Leveelahti R, Brummer-Korvenkontio M, Lundkvist A, Vaheri A, Vapalahti O. Human immune response to Puumala virus glycoproteins and nucleocapsid protein expressed in mammalian cells. J Med Virol 2001 65 : 605 613.
276. Lundkvist A, Vapalahti O, Plyusnin A, Sjolander KB, Niklasson B, Vaheri A. Characterization of Tula virus antigenic determinants defined by monoclonal antibodies raised against baculovirus-expressed nucleocapsid protein. Virus Res 1996 45 : 29 44.
277. Zoller L, et al. Immunoblot analysis of the serological response in hantavirus infections. J Med Virol 1989 27 : 231 237.
278. Maes P, Clement J, Gavrilovskaya I, Van Ranst M. Hantaviruses: immunology, treatment, and prevention. Viral Immunol 2004 17 : 481 497.
279. Bharadwaj M, Nofchissey R, Goade D, Koster F, Hjelle B. Humoral immune responses in the hantavirus cardiopulmonary syndrome. J Infect Dis 2000 182 : 43 48.
280. Valdivieso F, et al. Neutralizing antibodies in survivors of Sin Nombre and Andes hantavirus infection. Emerg Infect Dis 2006 12 : 166 168.
281. Ye C, Prescott J, Nofchissey R, Goade D, Hjelle B. Neutralizing antibodies and Sin Nombre virus RNA after recovery from hantavirus cardiopulmonary syndrome. Emerg Infect Dis 2004 10 : 478 482.
282. Settergren B, Ahlm C, Juto P, Niklasson B. Specific Puumala IgG virus half a century after haemorrhagic fever with renal syndrome. Lancet 1991 338 : 66.
283. Zampieri CA, Sullivan NJ, Nabel GJ. Immunopathology of highly virulent pathogens: insights from Ebola virus. Nat Immunol 2007 8 : 1159 1164.
284. Klein J, Sato A. The HLA system. Second of two parts. N Engl J Med 2000 343 : 782 786.
285. Martin MP, Carrington M. Immunogenetics of viral infections. Curr Opin Immunol 2005 17 : 510 516.
286. Makela S, et al. Human leukocyte antigen-B8-DR3 is a more important risk factor for severe Puumala hantavirus infection than the tumor necrosis factor-alpha(-308) G/A polymorphism. J Infect Dis 2002 186 : 843 846.
287. Mustonen J, et al. Genetic susceptibility to severe course of nephropathia epidemica caused by Puumala hantavirus. Kidney Int 1996 49 : 217 221.
288. *03 in pediatric patients with nephropathia epidemica caused by Puumala hantavirus. Pediatr Infect Dis J 2004 23 : 959 961.
289. Mustonen J, et al. Association of HLA B27 with benign clinical course of nephropathia epidemica caused by Puumala hantavirus. Scand J Immunol 1998 47 : 277 279.
290. Maes P, Clement J, Groeneveld PH, Colson P, Huizinga TW, Van Ranst M. Tumor necrosis factor-alpha genetic predisposing factors can influence clinical severity in nephropathia epidemica. Viral Immunol 2006 19 : 558 564.
291. Hohler T, Kruger A, Gerken G, Schneider PM, Meyer zum Buschenfelde KH, Rittner C. Tumor necrosis factor alpha promoter polymorphism at position -238 is associated with chronic active hepatitis C infection. J Med Virol 1998 54 : 173 177.
292. Lu LP, et al. Association of -238G/A polymorphism of tumor necrosis factor-alpha gene promoter region with outcomes of hepatitis B virus infection in Chinese Han population. World J Gastroenterol 2004 10 : 1810 1814.
293. Mori M, et al. High levels of cytokine-producing cells in the lung tissues of patients with fatal hantavirus pulmonary syndrome. J Infect Dis 1999 179 : 295 302.
294. Mustonen J, et al. Renal biopsy findings and clinicopathologic correlations in nephropathia epidemica. Clin Nephrol 1994 41 : 121 126.
295. Temonen M, Mustonen J, Helin H, Pasternack A, Vaheri A, Holthofer H. Cytokines, adhesion molecules, and cellular infiltration in nephropathia epidemica kidneys: an immunohistochemical study. Clin Immunol Immunopathol 1996 78 : 47 55.
296. Heider H, et al. A chemiluminescence detection method of hantaviral antigens in neutralisation assays and inhibitor studies. J Virol Methods 2001 96 : 17 23.
297. Lee HW. Hemorrhagic fever with renal syndrome in Korea. Rev Infect Dis 1989 11 (Suppl. 4) : S864 S876.
298. Heyman P, et al. Seoul hantavirus in Europe: first demonstration of the virus genome in wild Rattus norvegicus captured in France. Eur J Clin Microbiol Infect Dis 2004 23 : 711 717.
299. Kim YS, Ahn C, Han JS, Kim S, Lee JS, Lee PW. Hemorrhagic fever with renal syndrome caused by the Seoul virus. Nephron 1995 71 : 419 427.
300. Pilaski J, et al. Haemorrhagic fever with renal syndrome in Germany. Lancet 1991 337 : 111.
301. Cueto GR, Cavia R, Bellomo C, Padula PJ, Suarez OV. Prevalence of hantavirus infection in wild Rattus norvegicus and R. rattus populations of Buenos Aires City, Argentina. Trop Med Int Health 2008 13 : 46 51.
302. Avsic-Zupanc T, Xiao SY, Stojanovic R, Gligic A, van der Groen G, Leduc JW. Characterization of Dobrava virus: a hantavirus from Slovenia, Yugoslavia. J Med Virol 1992 38 : 132 137.
303. Avsic-Zupanc T, Petrovec M, Furlan P, Kaps R, Elgh F, Lundkvist A. Hemorrhagic fever with renal syndrome in the Dolenjska region of Slovenia-a 10-year survey. Clin Infect Dis 1999 28 : 860 865.
304. Klempa B, Stanko M, Labuda M, Ulrich R, Meisel H, Kruger DH. Central European Dobrava hantavirus isolate from a striped field mouse (Apodemus agrarius). J Clin Microbiol 2005 43 : 2756 2763.
305. Klempa B, et al. Hemorrhagic fever with renal syndrome caused by 2 lineages of Dobrava hantavirus, Russia. Emerg Infect Dis 2008 14 : 617 625.
306. Papa A, et al. Retrospective serological and genetic study of the distribution of hantaviruses in Greece. J Med Virol 1998 55 : 321 327.
307. Elwell MR, Ward GS, Tingpalapong M, Leduc JW. Serologic evidence of Hantaan-like virus in rodents and man in Thailand. Southeast Asian J Trop Med Public Health 1985 16 : 349 354.
308. Pattamadilok S, et al. Geographical distribution of hantaviruses in Thailand and potential human health significance of Thailand virus. Am J Trop Med Hyg 2006 75 : 994 1002.
309. Xiao SY, Leduc JW, Chu YK, Schmaljohn CS. Phylogenetic analyses of virus isolates in the genus Hantavirus, family Bunyaviridae. Virology 1994 198 : 205 217.
310. Klempa B, et al. Hantavirus in African wood mouse, Guinea. Emerg Infect Dis 2006 12 : 838 840.
311. Mustonen J, Vapalahti O, Henttonen H, Pasternack A, Vaheri A. Epidemiology of hantavirus infections in Europe. Nephrol Dial Transplant 1998 13 : 2729 2731.
312. Plyusnin A, et al. Tula virus: a newly detected hantavirus carried by European common voles. J Virol 1994 68 : 7833 7839.
313. Scharninghausen JJ, Pfeffer M, Meyer H, Davis DS, Honeycutt RL, Faulde M. Genetic evidence for Tula virus in Microtus arvalis and Microtus agrestis populations in Croatia. Vector Borne Zoonotic Dis 2002 2 : 19 27.
314. Sibold C, et al. Genetic characterization of a new hantavirus detected in Microtus arvalis from Slovakia. Virus Genes 1995 10 : 277 281.
315. Klempa B, Meisel H, Rath S, Bartel J, Ulrich R, Kruger DH. Occurrence of renal and pulmonary syndrome in a region of northeast Germany where Tula hantavirus circulates. J Clin Microbiol 2003 41 : 4894 4897.
316. Hjelle B, et al. Molecular linkage of hantavirus pulmonary syndrome to the white-footed mouse, Peromyscus leucopus: genetic characterization of the M genome of New York virus. J Virol 1995 69 : 8137 8141.
317. Song JW, et al. Isolation of pathogenic hantavirus from white-footed mouse (Peromyscus leucopus). Lancet 1994 344 : 1637.
318. Khan AS, et al. Fatal illness associated with a new hantavirus in Louisiana. J Med Virol 1995 46 : 281 286.
319. Morzunov SP, et al. A newly recognized virus associated with a fatal case of hantavirus pulmonary syndrome in Louisiana. J Virol 1995 69 : 1980 1983.
320. Torrez-Martinez N, Hjelle B. Enzootic of Bayou hantavirus in rice rats (Oryzomys palustris) in 1983. Lancet 1995 346 : 780 781.
321. Ravkov EV, Rollin PE, Ksiazek TG, Peters CJ, Nichol ST. Genetic and serologic analysis of Black Creek Canal virus and its association with human disease and Sigmodon hispidus infection. Virology 1995 210 : 482 489.
322. Rollin PE, et al. Isolation of Black Creek Canal virus, a new hantavirus from Sigmodon hispidus in Florida. J Med Virol 1995 46 : 35 39.
323. Fulhorst CF, Cajimat MN, Utrera A, Milazzo ML, Duno GM. Maporal virus, a hantavirus associated with the fulvous pygmy rice rat (Oligoryzomys fulvescens) in western Venezuela. Virus Res 2004 104 : 139 144.
324. Levis S, et al. Genetic diversity and epidemiology of hantaviruses in Argentina. J Infect Dis 1998 177 : 529 538.
325. Lopez N, Padula P, Rossi C, Lazaro ME, Franze-Fernandez MT. Genetic identification of a new hantavirus causing severe pulmonary syndrome in Argentina. Virology 1996 220 : 223 226.
326. Padula PJ, Edelstein A, Miguel SD, Lopez NM, Rossi CM, Rabinovich RD. Hantavirus pulmonary syndrome outbreak in Argentina: molecular evidence for person-to-person transmission of Andes virus. Virology 1998 241 : 323 330.
327. Song JW, et al. Seewis virus, a genetically distinct hantavirus in the Eurasian common shrew (Sorex araneus). Virol J 2007 4 : 114.
328. Douady CJ, et al. Molecular phylogenetic evidence confirming the Eulipotyphla concept and in support of hedgehogs as the sister group to shrews. Mol Phylogenet Evol 2002 25 : 200 209.