Uncovering the mysteries of hantavirus infections

Nature Reviews Microbiology

Volumn 11, Issue 8, 2013, Pages 539-550

  Vaheri, Antti ^a   Strandin, Tomas ^a   Hepojoki, Jussi ^a   Sironen, Tarja ^a   Henttonen, Heikki ^b   Mäkelä, Satu ^c,d   Mustonen, Jukka ^c,d  

^a UNIVERSITY OF HELSINKI   (Finland)

^b FINNISH FOREST RESEARCH INSTITUTE   (Finland)

^c TAMPERE UNIVERSITY OF TECHNOLOGY   (Finland)

^d TAMPERE UNIVERSITY HOSPITAL   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY RNA; GUANINE NUCLEOTIDE BINDING PROTEIN; NONSTRUCTURE PROTEIN; RNA DIRECTED RNA POLYMERASE; UNCLASSIFIED DRUG; VIRUS PROTEIN; VIRUS RNA;

ENDOCYTOSIS; HANTAVIRUS; HANTAVIRUS CARDIOPULMONARY SYNDROME; HANTAVIRUS INFECTION; HEADACHE; HEMORRHAGIC FEVER WITH RENAL SYNDROME; HOST CELL; HUMAN; IMMUNE SYSTEM; IMMUNOPATHOLOGY; NONHUMAN; PRIORITY JOURNAL; REVIEW; VIRUS ENTRY; VIRUS GENOME; VIRUS REPLICATION; VIRUS TRANSMISSION;

ANIMALS; CAPILLARY PERMEABILITY; CARRIER STATE; CD8-POSITIVE T-LYMPHOCYTES; ENDOTHELIAL CELLS; GENOME, VIRAL; HANTAVIRUS; HANTAVIRUS INFECTIONS; HUMANS; RECEPTORS, VIRUS; RODENTIA; TRANSCRIPTION, GENETIC; VIRUS INTERNALIZATION; VIRUS REPLICATION;

EID: 84880435410     PISSN: 17401526     EISSN: 17401534     Source Type: Journal    
DOI: 10.1038/nrmicro3066     Document Type: Review

References (133)

1. Vaheri, A., Mills, J. N., Spiropoulou, C. F. & Hjelle, B. in Oxford Textbook of Zoonoses: Biology, Clinical Practice and Public Health Control (eds Palmer, S. R., Lord Soulsby, Torgerson, P. R. & Brown, D. W. G.) 307-322 (Oxford Univ. Press, 2011
2. Vaheri, A. et al. Hantavirus infections in Europe and their impact on public health. Rev. Med. Virol. 23, 35-49 (2013
3. Hjelle, B. & Torres-Pérez, F. Hantaviruses in the Americas and their role as emerging pathogens. Viruses 2, 2259-2286 (2010
4. Jonsson, C. B., Figueiredo, L. T. & Vapalahti, O. A global perspective on hantavirus ecology, epidemiology, and disease. Clin. Microbiol. Rev. 23, 412-441 (2010
5. CDC. Hantavirus pulmonary syndrome in visitors to a national park - Yosemite Valley, California, 2012. Morb. Mortal. Wkly Rep. 61, 952 (2012
6. Schmaljohn, C. S. et al. Antigenic and genetic properties of viruses linked to hemorrhagic fever with renal syndrome. Science 227, 1041-1044 (1985
7. Schmaljohn, C. S. & Nichol, S. T. in Fields Virology (eds Knipe, D. M. & Howley, P. M.) 1741-1790 (Lippincott Williams & Wilkins, 2007
8. Spiropoulou, C. F. in Bunyaviridae. Molecular and Cellular Biology (eds Plyusnin, A. & Elliott, R. M.) 41-60 (Caister Academic Press, 2011
9. Hussein, I. T., Haseeb, A. Haque, A. & Mir, M. A. Recent advances in hantavirus molecular biology and disease. Adv. Appl. Microbiol. 74, 35-75 (2011
10. Jääskeläinen, K. M. et al. Tula and Puumala hantavirus NSs ORFs are functional and the products inhibit activation of the interferon-ß promoter. J. Med. Virol. 79, 1527-1536 (2007
11. Virtanen, J. O., Jääskeläinen, K. M., Djupsjöbacka, J., Vaheri, A. & Plyusnin, A. Tula hantavirus NSs protein accumulates in the perinuclear area in infected and transfected cells. Arch. Virol. 155, 117-121 (2010
12. Rönnberg, T. S. et al. Searching for cellular partners of hantaviral nonstructural protein NSs: The yeast two-hybrid screening of mouse cDNA library and analysis of cellular interactome. PLoS ONE 7, e34307 (2012
13. Van Knippenberg, I., Fragkoudis, R. & Elliott, R. M. The transient nature of Bunyamwera orthobunyavirus NSs protein expression: Effects of increased stability of NSs protein on virus replication. PLoS ONE 8, e64137 (2013
14. Hepojoki, J., Strandin, T., Lankinen, H. & Vaheri, A. Hantavirus structure - Molecular interactions behind the scene. J. Gen. Virol. 93, 1631-1644 (2012
15. Huiskonen, J. T. et al. Electron cryo-tomography of Tula hantavirus suggests a unique assembly paradigm for enveloped viruses. J. Virol. 84, 4889-4897 (2010
16. Kallio, E. R. et al. Prolonged survival of Puumala hantavirus outside the host: Evidence for indirect transmission via the environment. J. Gen. Virol. 87, 2127-2134 (2006
17. Mackow, E. R. & Gavrilovskaya, I. N. Hantavirus regulation of endothelial cell functions. Thromb. Haemost. 102, 1030-1041 (2009
18. Takagi, J. & Springer, T. A. Integrin activation and structural rearrangement. Immunol. Rev. 186, 141-163 (2002
19. Gavrilovskaya, I., Shepley, M., Shaw, R., Ginsberg, M. & Mackow E. ß3 integrins mediate the cellular entry of hantaviruses that cause respiratory failure. Proc. Natl Acad. Sci. USA 95, 7074-7079 (1998
20. Mackow, E. R. & Gavrilovskaya, I. N. Cellular receptors and hantavirus pathogenesis. Curr. Top. Microbiol. Immunol. 256, 91-115 (2001
21. Krautkrämer, E. & Zeier, M. Hantavirus causing hemorrhagic fever with renal syndrome enters from the apical surface and requires decay-accelerating factor (DAF/CD55). J. Virol. 82, 4257-4264 (2008
22. Choi, Y. et al. A hantavirus causing hemorrhagic fever with renal syndrome requires gC1qR/p32 for efficient cell binding and infection. Virology 381, 178-183 (2008
23. Jin, M. et al. Hantaan virus enters cells by clathrin-dependent receptor-mediated endocytosis. Virology 294, 60-69 (2002
24. Ramanathan, H. N. & Jonsson, C. B. New and Old World hantaviruses differentially utilized host cytoskeletal components during their life cycles. Virology 374, 138-150 (2008
25. Lozach, P. Y. et al. Entry of bunyaviruses into mammalian cells. Cell Host Microbe 7, 488-499 (2009
26. Ramanathan, H. N. et al. Dynein-dependent transport of the Hantaan virus nucleocapsid protein to the endoplasmic reticulum-Golgi intermediate compartment. J. Virol. 81, 8634-8647 (2007
27. Flick, K. et al. Rescue of Hantaan virus minigenomes. Virology 306, 219-224 (2003
28. Boyloy, M., Plotch, S. J. & Krug, R. M. Globin mRNAs are primers for the transcription of influenza viral RNA in vitro. Proc. Natl Acad. Sci. USA 75, 4886-4890 (1978
29. Mir, M. A., Duran, W. A., Hjelle, B. L., Ye, C. & Panganiban, A. T. Storage of cellular 5' mRNA caps in P bodies for viral cap-snatching. Proc. Natl Acad. Sci. USA 105, 19294-19299 (2008
30. Heinemann, P., Schmidt-Chanasit, J. & Günther, S. The N terminus of Andes virus L protein suppresses mRNA and protein expression in mammalian cells. J. Virol. 87, 6975-6985 (2013
31. Reguera, J., Weber, F. & Cusack, S. Bunyaviridae RNA polymerases (L protein) have an N terminal, influenza-like endonuclease domain, essential for viral cap-dependent transcription. PLoS Pathog. 6, e1001101 (2010
32. 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. 69, 5754-5766 (1995
33. Fontana, J., López-Montero, N., Elliott, R. M., Fernández, J. J. & Risco, C. The unique architecture of Bunyamwera virus factories around the Golgi complex. Cell. Microbiol. 10, 2012-2028 (2008
34. Ravkov, E. V. & Compans, R. W. Hantavirus nucleocapsid protein is expressed as a membrane-associated protein in the perinuclear region. J. Virol. 75, 1808-1815 (2001
35. Kukkonen, S. K. J., Vaheri, A. & Plyusnin, A. Tula hantavirus L protein is a 250 kDa peripheral membrane-associated protein. J. Gen. Virol. 85, 1181-1189 (2004
36. Kaukinen, P., Vaheri, A. & Plyusnin, A. Hantavirus nucleocapsid protein: A multifunctional molecule with both house-keeping and ambassadorial duties. Arch. Virol. 150, 1693-1713 (2005
37. Ariza, A. et al. Nucleocapsid protein structures from orthobunyaviruses reveal insight into ribonucleoprotein architecture and RNA polymerization. Nucleic Acids Res. 17, 1-15 (2013
38. Ferron, F. et al. The hexamer structure of the Rift Valley Fever virus nucleoprotein suggests a mechanism for its assembly into ribonucleoprotein complexes. PLoS Pathog. 20117, e1002030 (2011
39. Hepojoki, J., Strandin, T., Vaheri, A. & Lankinen, H. Interactions and oligomerization of hantavirus glycoproteins. J. Virol. 84, 227-242 (2010
40. Hepojoki, J. et al. Cytoplasmic tails of hantavirus glycoproteins interact with the nucleocapsid protein. J. Gen. Virol. 92, 1189-1198 (2010
41. Strandin, T. et al. The cytoplasmic tail of hantavirus Gn interacts with RNA. Virology 418, 12-20 (2011
42. Piper, M. E., Sorenson, D. R. & Gerrard, S. R. Efficient cellular release of Rift Valley Fever virus requires genomic RNA. PLoS ONE 6, e18070 (2011
43. Strandin, T., Hepojoki, J. & Vaheri, A. Cytoplasmic tails of bunyavirus Gn glycoproteins - could they act as matrix protein surrogates? Virology 437, 73-80 (2013
44. Zheng, W. & Tao, Y. J. Structure and assembly of influenza A virus ribonucleoprotein complex. FEBS Lett. 587, 1206-1214 (2013
45. Terasaki, K., Murakami, S., Lokugamage, K. G. & Makino, S. Mechanism of tripartite RNA genome packaging in Rift Valley fever virus. Proc. Natl Acad. Sci. USA 108, 804-809 (2011
46. Rowe, R. K., Suszko, J. W. & Pekosz, A. Roles for the recycling endosome, Rab8, and Rab11 in hatavirus release from epithelial cells. Virology 382, 239-249 (2008
47. Meyer, B. J. & Schmaljohn, C. S. Persistent hantavirus infections: Characteristics and mechanisms. Trends Microbiol. 8, 61-67 (2000
48. Henttonen, H. et al. Recent discoveries of new hantaviruses widen their range and question their origins. Ann. N. Y. Acad. Sci. 1149, 84-89 (2008
49. Kallio, E. R. et al. Endemic hantavirus infection impairs the winter survival of its rodent host. Ecology 88, 1911-1916 (2007
50. Luis, A. D., Douglass, R. J., Hudson, P. J., Mills, J. N. & Bjørnstad, O. N. Sin Nombre hantavirus decreases survival of male deer mice. Oecologia 169, 431-439 (2012
51. Spengler, J. R. et al. Experimental Andes virus infection in deer mice: Characteristics of infection and clearance in a heterologous rodent host. PLoS ONE 8, e55310 (2013
52. Olsson, G. E., Leirs, H. & Henttonen, H. Hantaviruses and their hosts in Europe: Reservoirs here and there, but not everywhere? Vector Borne Zoonotic Dis. 10, 546-561 (2010
53. Gavrilovskaya, I. N. et al. Features of circulation of hemorrhagic fever with renal syndrome (HFRS) virus among small mammals in the European U.S.S.R. Arch. Virol. 75, 313-316 (1983
54. Hardestam, J. et al. Puumala hantavirus excretion kinetics in bank voles (Myodes glareolus). Emerg. Infect. Dis. 14, 1209-1215 (2008
55. Botten, J. et al. Shedding and intracage transmission of Sin Nombre hantavirus in the deer mouse (Peromyscus maniculatus) model. J. Virol. 76, 7587-7594 (2002
56. Voutilainen, L. Interactions between Puumala hantavirus and its host, the bank vole, in the boreal zone. Thesis, Univ. Helsinki (2013
57. Easterbrook, J. D. & Klein, S. L. Immunological mechanisms mediating hantavirus persistence in rodent reservoirs. PLoS Pathog. 4, e1000172 (2008
58. Easterbrook, J. D., Zink, M. C. & Klein, S. L. Regulatory T cells enhance persistence of the zoonotic pathogen Seoul virus in its reservoir host. Proc. Natl Acad. Sci. USA 104, 15502-15507 (2007
59. Schountz, T. et al. Regulatory T cell-like responses in deer mice persistently infected with Sin Nombre virus. Proc. Natl Acad. Sci. USA 104, 15496-15501 (2007
60. Guivier, E. et al. TNF a expression and promoter sequences reflect the balance of tolerance/resistance to Puumala hantavirus infection in European bank vole populations. Infect. Genet. Evol. 10, 1208-1217 (2010
61. Au, R. Y., Jedlicka, A. E., Li, W., Pekosz, A. & Klein, S. L. Seoul virus suppresses NF ?B mediated inflammatory responses of antigen presenting cells from Norway rats. Virology 400, 115-127 (2010
62. Li, W. & Klein, S. L. Seoul virus-infected rat lung endothelial cells and alveolar macrophages differ in their ability to support virus replication and induce regulatory T cell phenotypes. J. Virol. 86, 11845-11855 (2012
63. Matthys, V. & Mackow, E. R. Hantavirus regulation of type I interferon responses. Adv. Virol. 2012, 524024 (2012
64. Martinez, V. P. et al. Person-to person transmission of Andes virus. Emerg. Infect. Dis. 11, 1848-1853 (2005
65. Sinisalo, M. et al. Headache and low platelets in a patient with acute leukemia. J. Clin. Virol. 48, 159-161 (2010
66. Van Loock, F., Thomas, I., Clement, J., Ghoos, S. & Colson, P. A case-control study after a hantavirus infection outbreak in the south of Belgium: Who is at risk? Clin. Infect. Dis. 28, 834-839 (1999
67. Vapalahti, K., Virtala, A. M., Vaheri, A. & Vapalahti, O. Case-control study on Puumala virus infection: Smoking is a risk factor. Epidemiol. Infect. 138, 576-584 (2010
68. Vapalahti, O. et al. Hantavirus infections in Europe. Lancet Infect. Dis. 3, 653-661 (2003
69. Peters, C. J. & Khan, A. S. Hantavirus pulmonary syndrome: The new American hemorrhagic fever. Clin. Infect. Dis. 34, 1224-1231 (2002
70. Bi, Z., Formenty, P. B. H. & Roth, C. E. Hantavirus infection: A review and global update. J. Infect. Dev. Ctries 2, 3-23 (2008
71. Kruger, D. H., Schönrich, G. & Klempa, B. Human pathogenic hantaviruses and prevention of infection. Hum. Vaccin. 7, 685-693 (2011
72. Duchin, J. S. et al. Hantavirus pulmonary syndrome: A clinical description of 17 patients with a newly recognized disease. N. Engl. J. Med. 330, 949-955 (1994
73. MacNeil, A., Nichol, S. T. & Spiropoulou, C. F. Hantavirus pulmonary syndrome. Virus Res. 162, 138-147 (2011
74. Knust, B., Macnell, A. & Rollin, P. E. Hantavirus pulmonary syndrome clinical findings: Evaluation a surveillance case definition. Vector Borne Zoonotic Dis. 12, 393-399 (2012
75. Simpson, S. Q., Spikes, L., Patel, S. & Faruqi, I. Hantavirus pulmonary syndrome. Infect. Dis. North Am. 24, 159-173 (2010
76. Rasmuson, J. et al. Time to revise the paradigm of hantavirus pulmonary syndrome caused by European hantavirus. Eur. J. Clin. Microbiol. Infect. Dis. 30, 685-690 (2011
77. Klempa, B. et al. Complex evolution and epidemiology of Dobrava-Belgrade hantavirus: Definition of genotypes and their characteristics. Arch. Virol. 158, 521-529 (2013
78. Vaheri, A., Vapalahti, O. & Plyusnin, A. How to diagnose hantavirus infections and detect them in rodents and insectivores. Rev. Med. Virol. 18, 277-288 (2008
79. Outinen, T. K. et al. Plasma cell-free DNA levels are elevated in acute Puumala hantavirus infection. PLoS ONE 7, e31455 (2012
80. Kanerva, M., Mustonen, J. & Vaheri, A. Pathogenesis of Puumala and other hantavirus infections. Rev. Med. Virol. 8, 67-86 (1998
81. Zaki, S. R. et al. Hantavirus pulmonary syndrome. Pathogenesis of an emerging infectious disease. Am. J. Pathol. 146, 552-579 (1995
82. Kanerva, M. et al. Pulmonary involvement in nephropathia epidemica: Radiological findings and their clinical correlations. Clin. Nephrol. 46, 369-378 (1996
83. Shrivastava-Ranjan, P., Rollin, P. E. & Spiropoulou, C. F. Andes virus disrupts the endothelial cell barrier by induction of vascular endothelial growth factor and downregulation of VE cadherin. J. Virol. 84, 11227-11234 (2010
84. Gavrilovskaya, I., Gorbunova, E., Koster, F. & Mackow, E. Elevated VEGF levels in pulmonary edema fluid and PBMCs from patients with acute hantavirus pulmonary syndrome. Adv. Virol. 2012, 674360 (2012
85. Gavrilovskaya, I. N., Gorbunova, E. E. & Mackow, E. R. Pathogenic hantaviruses direct the adherence of quiescent platelets to infected endothelial cells. J. Virol. 84, 4832-4839 (2010
86. Laine, O. et al. Platelet ligands and ADAMTS13 during Puumala hantavirus infection and associated thrombocytopenia. Blood Coagul. Fibrinolysis 22, 468-472 (2011
87. Laine, O. et al. Enhanced thrombin formation and fibrinolysis during acute Puumala hantavirus infection. Thromb. Res. 126, 154-158 (2010
88. Krautkrämer, E., Grouls, S., Stein, N., Reiser, J. & Zeier, M. Pathogenic Old World hantaviruses infect renal glomerular and tubular cells and induce disassembling of cell to cell contacts. J. Virol. 85, 9811-9823 (2011
89. Valdivieso, F. et al. Neutralizing antibodies in survivors of Sin Nombre and Andes hantavirus infection. Emerg. Infect. Dis. 12, 166-168 (2006
90. Terajima, M. & Ennis, F. A. T cells and pathogenesis of hantavirus cardiopulmonary syndrome and hemorrhagic fever with renal syndrome. Viruses 3, 1059-1073 (2011
91. Rasmuson, J. et al. Presence of activated airway T lymphocytes in human Puumala hantavirus disease. Chest 140, 715-722 (2011
92. 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. 179, 1988-1995 (2007
93. Van Epps, H. L. et al. Long-lived memory T lymphocyte responses after hantavirus infection. J. Exp. Med. 196, 579-588 (2002
94. Manigold, T. et al. Highly differentiated, resting Gn specific memory CD8+ T cells persist years after infection by Andes hantavirus. PLoS Pathog. 6, e1000779 (2010
95. Akira, S., Hirano, T. Taga, T. & Kishimoto, T. Biology of multifunctional cytokines: IL 6 and related molecules (IL 1 and TNF). FASEB J. 4, 2860-2867 (1990
96. Borges, A. A. et al. Role of mixed Th1 and Th2 serum cytokines on pathogenesis and prognosis of hantavirus pulmonary syndrome. Microbes Infect. 10, 1150-1157 (2008
97. Linderholm, M., Ahlm, C., Settergren, B., Waage, A. & Tärnvik, A. Elevated plasma levels of tumor necrosis factor (TNF)-a, soluble TNF receptors, interleukin (IL)-6, and IL 10 in patients with hemorrhagic fever with renal syndrome. J. Infect. Dis. 173, 38-43 (1996
98. Outinen, T. K. et al. The severity of Puumala hantavirus induced nephropathia epidemica can be better evaluated using plasma interleukin 6 than C reactive protein determinations. BMC Infect. Dis. 10, 132 (2010
99. Sadeghi, M. et al. Cytokine expression during early and late phase of acute Puumala hantavirus infection. BMC Immunol. 12, 65 (2011
100. Mäkelä, S. et al. Urinary excretion of interleukin 6 correlates with proteinuria in acute Puumala hantavirus-induced nephritis. Am. J. Kidney Dis. 43, 809-816 (2004
101. Prescott, J. et al. The adaptive immune response does not influence hantavirus disease or persistence in Syrian hamster. Immunology http://dx.doi.org/10.1111/imm.12116 (2013
102. Tsukada, H. et al. Ligation of endothelial avß3 integrin increases capillary hydraulic conductivity in single microvessels of rat lung. J. Clin. Invest. 91, 103-109 (1995
103. Bossi, F. et al. Platelet-activating factor and kinin-dependent vascular leakage as a novel functional activity of the soluble terminal complement complex. J. Immunol. 173, 6921-6927 (2004
104. Paakkala, A., Mustonen, J., Viander, M., Huhtala, H. & Pasternack, A. Complement activation in nephropathia epidemica caused by Puumala hantavirus. Clin. Nephrol. 53, 424-431 (2000
105. Sane, J. et al. Complement activation in Puumala hantavirus infection correlates with disease severity. Ann. Med. 44, 468-475 (2012
106. Mantovani, A., Garlanda, C. & Bottazzi, B. Pentraxin 3, a non-redundant soluble pattern recognition receptor involved in innate immunity. Vaccine 21 (Suppl. 2), S43-S47 (2003
107. Outinen, T. K. et al. High pentraxin 3 plasma levels associate with thrombocytopenia in acute Puumala hantavirus-induced nephropathia epidemica. Eur. J. Clin. Microbiol. Infect. Dis. 31, 957-963 (2012
108. Hepojoki, J. et al. Acute hantavirus infection induces the production of galectin 3 binding protein (90K/Mac 2BP). Abstract O3 6. IX International Conference on HFRS, HPS & Hantaviruses. (2013
109. Mellor, A. L. & Munn, D. H. IDO expression by dendritic cells: Tolerance and tryphophan catabolism. Nature Rev. Immunol. 4, 762-774 (2004
110. Outinen, T. K. et al. High activity of indoleamine 2,3 dioxygenase is associated with renal insufficiency in Puumala hantavirus induced nephropathia epidemica. J. Med. Virol. 83, 731-737 (2011
111. Klingström, J. et al. Loss of cell membrane integrity in Puumala hantavirus-infected patients correlates with levels of epithelial cell apoptosis and perforin. J. Virol. 80, 8279-8282 (2006
112. Groen, J. et al. Hantavirus antigen detection in kidney biopsies from patients with nephropathia epidemica. Clin. Nephrol. 46, 379-383 (1996
113. Ala-Houhala, I. et al. Increased glomerular permeability in patients with nephropathia epidemica caused by Puumala hantavirus. Nephrol. Dial. Transplant. 17, 246-252 (2002
114. Gupta, S. et al. Hantavirus-infection confers resistance to cytotoxic lymphocyte-mediated apoptosis. PLoS Pathog. 9, e1003272 (2013
115. Björkström, N. K. et al. Rapid expansion and long-term persistence of elevated NK cell numbers in humans infected with hantavirus. J. Exp. Med. 208, 13-21 (2010
116. Gavrilovskaya, I. N., Gorbunova, E. E., Mackow, N. A. & Mackow, E. R. 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. 82, 5797-5806 (2008
117. Gorbunova, E. E., Gavrilovskaya, I. N., Pepini, T. & Mackow, E. R. VEGFR2 and Src kinase inhibitors suppress Andes virus-induced endothelial cell permeability. J. Virol. 85, 2296-2303 (2010
118. Antonen, J. et al. A severe case of Puumala hantavirus infection successfully treated with bradykinin receptor antagonist icatibant. Scand. J. Infect. Dis. 45, 494-496 (2013
119. Sironen, T. & Plyusnin, A. in Bunyaviridae: Molecular and Cellular Biology (eds Plyusnin, A. & Elliott, R. M.) 61-94 (Caister Academic, 2011
120. Ramsden, C., Holmes, E. C. & Charleston, M. A. Hantavirus evolution in relation to its rodent and insectivore hosts: No evidence for codivergence. Mol. Biol. Evol. 26, 143-153 (2009
121. Blasdell, K., Henttonen, H. & Buchy, P. in New Frontiers of Molecular Epidemiology of Infectious Diseases (eds Morand, S., Beaudeau, F. & Cabaret, J.) 179-216 (Springer, 2012
122. Kanerva, M., Vaheri, A., Mustonen, J. & Partanen, J. High-producer allele of tumour necrosis factor- A is part of the susceptibility MHC haplotype in severe Puumala virus-induced nephropathia epidemica. Scand. J. Infect. Dis. 30, 532-534 (1998
123. Guo, W. P. et al. Phylogeny and origins of hantaviruses harbored by bats, insectivores, and rodents. PLoS Pathog. 9, e1003159 (2013
124. Klempa, B. et al. Occurrence of renal and pulmonary syndrome in a region of Northeast Germany where Tula hantavirus circulates. J. Clin. Microbiol. 41, 4894-4897 (2003
125. 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. 8, 450-458 (2008
126. Mustonen, J. et al. Genetic susceptibility to severe course of nephropathia epidemica caused by Puumala hantavirus. Kidney Int. 49, 217-221 (1996
127. Wang, M. L. et al. Genetic susceptibility to haemorrhagic fever with renal syndrome caused by Hantaan virus in Chinese Han population. Int. J. Immunogenet. 36, 227-229 (2009
128. Korva, M., Saksida, A., Kunilo, S., Vidan Jeras, B. & Avsic-Zupanc, T. HLA-associated hemorrhagic fever with renal syndrome disease progression in Slovenian patients. Clin. Vaccine Immunol. 18, 1435-1440 (2011
129. Mäkelä, S. et al. Human leucocyte antigen-B8 DR3 is a more important risk factor for severe Puumala hantavirus infection than the tumor necrosis factor a(-308) G/A polymorphism. J. Infect. Dis. 186, 843-846 (2002
130. Maes, P., et al. Tumor necrosis factor- A genetic predisposing factors can influence clinical severity in nephropathia epidemica. Viral Immunol. 19, 558-564 (2006
131. Borges, A. A. et al. Association of -308G/A polymorphism in the tumor necrosis factor- A gene promoter with susceptibility to development of hantavirus cardiopulmonary syndrome in the Ribeirão Preto region, Brazil. Arch. Virol. 155, 971-975 (2010
132. Mäkeläa, S. et al. Polymorphism of the cytokine genes in hospitalized patients with Puumala hantavirus infection. Nephrol. Dial. Transplant. 16, 1368-1373 (2001
133. Laine, O. et al. Polymorphism of PAI 1 and platelet GP Ia may associate with impairment of renal function and thrombocytopenia in Puumala hantavirus infection. Thromb. Res. 129, 611-615 (2012