Dobrava and Tula hantaviruses from Central Europe: molecular evolution and pathogenic relevanceBoris Klempa1.11.11.2231.345307#242604#2531.41.4.11.4.261.4.371.4.41.581.61.6.191011121.6.21314289#3511.715605#6491617181.81920399#3161.921222.2.12223399#3162.22.2.12.2.22.3242.4252.52.5.12.5.2262.5.3272.6282.7292.8302.92.9.12.9.2312.102.11323.3.13233604#4713.23.2.134353.2.236373.2.33839451#333416#3253.2.4404142552#3343.2.54344945#3143.33.3.1454647433#3983.3.24849573#374503.43.4.1513.4.252533.4.35455604#36156604#2533.4.43.4.557583.53.5.13.5.25960255#19961556#441506#4813.66263643.73.7.13.7.1.13.7.1.2653.7.2666768554#6594.4.1694.270512#173714.3724.473744.5757677784.679804.78182834.8844.985864.1087884.1189REFERENCESAbbreviationsAcknowledgementList of PublicationsCommunications to Scientific MeetingsSelbständigkeitserklärungenContentsHelp REFERENCES Antoniadis, A., Stylianakis, A., Papa, A., Alexiou-Daniel, S., Lampropoulos, A., Nichol, S. T., Peters, C. J. and Spiropoulou, C. F. (1996). Direct genetic detection of Dobrava virus in Greek and Albanian patients with hemorrhagic fever with renal syndrome. J Infect Dis, 174,407-410. Arikawa, J., Lapenotiere, H. F., Iacono-Connors, L., Wang, M. L. and Schmaljohn, C. S. (1990). Coding properties of the S and the M genome segments of Sapporo rat virus: comparison to other causative agents of hemorrhagic fever with renal syndrome. Virology, 176,114-125. Arikawa, J., Schmaljohn, A. L., Dalrymple, J. M. and Schmaljohn, C. S. (1989). Characterization of Hantaan virus envelope glycoprotein antigenic determinants defined by monoclonal antibodies. J Gen Virol, 70,615-624. Avsic-Zupanc, T., Nemirov, K., Petrovec, M., Trilar, T., Poljak, M., Vaheri, A. and Plyusnin, A. (2000). Genetic analysis of wild-type Dobrava hantavirus in Slovenia: co-existence of two distinct genetic lineages within the same natural focus. J Gen Virol, 81,1747-1755. Avsic-Zupanc, T., Petrovec, M., Furlan, P., Kaps, R., Elgh, F. and Lundkvist, Å. (1999). Hemorrhagic fever with renal syndrome in the Dolenjska region of Slovenia--a 10-year survey. Clin Infect Dis, 28,860-865. Avsic-Zupanc, T., Toney, A., Anderson, K., Chu, Y. K. and Schmaljohn, C. S. (1995). Genetic and antigenic properties of Dobrava virus: a unique member of the Hantavirus genus, family Bunyaviridae. J Gen Virol, 76,2801-2808. Avsic-Zupanc, T., Xiao, S. Y., Stojanovic, R., Gligic, A., van der, G. G. and Leduc, J. W. (1992). Characterization of Dobrava virus: a Hantavirus from Slovenia, Yugoslavia. J Med Virol, 38,132-137. Barome, P. O., Monnerot, M. and Gautun, J. C. (1998). Intrageneric phylogeny of Acomys (rodentia, muridae) using mitochondrial gene cytochrome b. Mol Phylogenet Evol, 9,560-566. Beaty, B. J. and Calisher, C. H. (1991). Bunyaviridae--natural history. In D. Kolakofsky (Ed.), Bunyaviridae (pp. 27-78.).

Berlin

: Springer-Verlag. Bowen, M. D., Gelbmann, W., Ksiazek, T. G., Nichol, S. T. and Nowotny, N. (1997). Puumala virus and two genetic variants of Tula virus are present in Austrian rodents. J Med Virol, 53,174-181. Brummer-Korvenkontio, M., Vaheri, A., Hovi, T., von Bonsdorff, C. H., Vuorimies, J., Manni, T., Penttinen, K., Oker-Blom, N. and Lahdevirta, J. (1980). Nephropathia epidemica: detection of antigen in bank voles and serologic diagnosis of human infection. J Infect Dis, 141,131-134. Brus Sjolander, K., Golovljova, I., Vasilenko, V., Plyusnin, A. and Lundkvist, Å. (2002). Serological divergence of Dobrava and Saaremaa hantaviruses : evidence for two distinct serotypes. Epidemiol Infect, 128,99-103. Carey, D. E., Reuben, R., Panicker, K. N., Shope, R. E. and Myers, R. M. (1971). Thottapalayam virus: a presuptive arbovirus isolated from a shrew in India. Indian J Med Res, 59, 1758-1760. Casals, J., Henderson, B. E., Hoogstraal, H., Johnson, K. M. and Shelokov, A. (1970). A review of Soviet viral hemorrhagic fevers, 1969. J Infect Dis, 122,437-453. Chare, E. R., Gould, E. A. and Holmes, E. C. (2003). Phylogenetic analysis reveals a low rate of homologous recombination in negative-sense RNA viruses. J Gen Virol, 84, 2691-2703. Chizhikov, V. E., Spiropoulou, C. F., Morzunov, S. P., Monroe, M. C., Peters, C. J. and Nichol, S. T. (1995). Complete genetic characterization and analysis of isolation of Sin Nombre virus. J Virol, 69,8132-8136. Chomczynski, P. and Sacchi, N. (1987). Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem, 162,156-159. Dayhoff, M. O., Schwartz, R. M. and Orcutt, B. C. (1978). A model of evolutionary change in proteins. In M.O.Dayhoff (Eds.), Atlas of protein sequence and structure (pp. 345-352.).

Washington D.C.

: National Biomedical Research Foundation. de Carvalho, N., Sallberg, M., Hultgren, C. and Lundkvist, Å. (2001). T-helper and humoral responses to Puumala hantavirus nucleocapsid protein: identification of T-helper epitopes in a mouse model. J Gen Virol, 82,129-138. Dekonenko, A., Yakimenko, V., Ivanov, A., Morozov, V., Nikitin, P., Khasanova, S., Dzagurova, T., Tkachenko, E. and Schmaljohn, C. S. (2003). Genetic similarity of Puumala viruses found in Finland and western Siberia and of the mitochondrial DNA of their rodent hosts suggests a common evolutionary origin. Infect Genet Evol, 3, 245-257. Dornetzhuber, V., Griesbach, S. and Schmidt, K. (1960). Dalsie letalne pripady hemoragickej nefrozo-nefritidy na Slovensku. Bratisl Lek Listy, 40,418-425. Ebihara, H., Yoshimatsu, K., Ogino, M., Araki, K., Ami, Y., Kariwa, H., Takashima, I., Li, D. and Arikawa, J. (2000). 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, 74,9245-9255. Elgh, F., Linderholm, M., Wadell, G., Tarnvik, A. and Juto, P. (1998). Development of humoral cross-reactivity to the nucleocapsid protein of heterologous hantaviruses in nephropathia epidemica. FEMS Immunol Med Microbiol, 22,309-315. Elliott, R. M., Bouloy, M., Calisher, C. H., Goldbach, R., Moyer, J. T., Nichol, S. T., Pettersson, R., Plyusnin, A. and Schmaljohn, C. S. (1999). Bunyaviridae. In M. H. V. van Regenmortel, C. M. Fauquet, D. H. L. Bishop, E. B. Carsten, M. K. Estes, S. M. Lemon, J. Maniloff, M. A. Mayo, D. J. McGeoch, C. R. Pringle and R. B. Wickner (Eds.), Virus Taxonomy: VIIth report of the International Committee on Taxonomy of Viruses (pp. 599-631.).

San Diego, California

: Academic Press. Escutenaire, S., Chalon, P., De Jaegere, F., Karelle-Bui, L., Mees, G., Brochier, B., Rozenfeld, F. and Pastoret, P. P. (2002). Behavioral, physiologic, and habitat influences on the dynamics of Puumala virus infection in bank voles (Clethrionomys glareolus). Emerg Infect Dis, 8,930-936. Felsenstein, J. PHYLIP (Phylogeny Inference Package), version 3.5c. 1993.

Seattle, Washington, USA

. Flick, K., Hooper, J.W., Schmaljohn, C.S., Petterson, R.F., Feldmann, H. and Flick, R. (2003). Rescue of Hantaan virus minigenomes. Virology, 306, 219-224. Geraghty, D. E. (2002). Genetic diversity and genomics of the immune response. Immunol Rev, 190, 5-8. Gott, P., Stohwasser, R., Schnitzler, P., Darai, G. and Bautz, E. K. (1993). RNA binding of recombinant nucleocapsid proteins of hantaviruses. Virology, 194,332-337. Gott, P., Zoller, L., Darai, G. and Bautz, E. K. (1997). A major antigenic domain of hantaviruses is located on the aminoproximal site of the viral nucleocapsid protein. Virus Genes, 14,31-40. Hall, T. A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis for Windows 95/98/NT. Nucl Acids Symp Ser, 41, 95-98. Heider, H., Ziaja, B., Priemer, C., Lundkvist, Å., Neyts, J., Krüger, D. H. and Ulrich, R. (2001). A chemiluminescence detection method of hantaviral antigens in neutralisation assays and inhibitor studies. J Virol Methods, 96,17-23. Henderson, W. W., Monroe, M. C., St Jeor, S. C., Thayer, W. P., Rowe, J. E., Peters, C. J. and Nichol, S. T. (1995). Naturally occurring Sin Nombre virus genetic reassortants. Virology, 214,602-610. Heyman, P., Klingstrom, J., De Jaegere, F., Leclercq, G., Rozenfeld, F., Escutenaire, S., Vandenvelde, C., Zizi, M., Plyusnin, A. and Lundkvist, Å. (2002). Tula hantavirus in Belgium. Epidemiol Infect, 128,251-256. Hilleman, M. R. (2002). Realities and enigmas of human viral influenza: pathogenesis, epidemiology and control. Vaccine, 20, 3068-3087. Hjelle, B., Chavez-Giles, F., Torrez-Martinez, N., Yates, T., Sarisky, J., Webb, J. and Ascher, M. (1994). Genetic identification of a novel hantavirus of the harvest mouse Reithrodontomys megalotis. J Virol, 68,6751-6754. Hjelle, B., Krolikowski, J., Torrez-Martinez, N., Chavez-Giles, F., Vanner, C. and Laposata, E. (1995). Phylogenetically distinct hantavirus implicated in a case of hantavirus pulmonary syndrome in the northeastern United States. J Med Virol, 46,21-27. Hjelle, B. and Yates, T. (2001). Modeling hantavirus maintenance and transmission in rodent communities. In C. S. Schmaljohn and S. T. Nichol (Eds.), Hantaviruses (pp. 77-90.).

Berlin

: Springer-Verlag. Hoffmann, R. S. and Koeppl, J. W. (

1985

). Zoogeography. In R. H. Tamarin (Ed.), Biology of New World Microtus (pp. 84-115.). American Society of Mammalogists. Holmes, E. C. (2003). Molecular clocks and the puzzle of RNA virus origins. J Virol, 77, 3893-3897. Horling, J., Chizhikov, V., Lundkvist, Å., Jonsson, M., Ivanov, L., Dekonenko, A., Niklasson, B., Dzagurova, T., Peters, C. J., Tkachenko, E. and Nichol, S. (1996). Khabarovsk virus: a phylogenetically and serologically distinct hantavirus isolated from Microtus fortis trapped in far-east Russia. J Gen Virol, 77,687-694. Horling, J., Lundkvist, Å., Persson, K., Mullaart, M., Dzagurova, T., Dekonenko, A., Tkachenko, E. and Niklasson, B. (1995). Detection and subsequent sequencing of Puumala virus from human specimens by PCR. J Clin Microbiol, 33,277-282. Huckenbeck, W., Scheil, H. G., Schmidt, H. D., Efremovska, L. and Xirotiris, N. (2001). Population genetic studies in the Balkans. II. DNA-STR-systems. Anthropol Anz, 59, 213-225. Hughes, A. L. and Friedman, R. (2000). Evolutionary diversification of protein-coding genes of hantaviruses. Mol Biol Evol, 17,1558-1568. Hungnes, O., Jonassen, T. O., Jonassen, C. M. and Grinde, B. (2000). Molecular epidemiology of viral infections. Acta Pathol Microbiol Immunol Scandinav, 108, 81-97. Isegawa, Y., Tanishita, O., Ueda, S. and Yamanishi, K. (1994). Association of serine in position 1124 of Hantaan virus glycoprotein with virulence in mice. J Gen Virol, 75,3273-3278. Jenison, S., Yamada, T., Morris, C., Anderson, B., Torrez-Martinez, N., Keller, N. and Hjelle, B. (1994). Characterization of human antibody responses to four corners hantavirus infections among patients with hantavirus pulmonary syndrome. J Virol, 68,3000-3006. Jonsson, C. B. and Schmaljohn, C. S. (2001). Replication of hantaviruses. In C. S. Schmaljohn and S. T. Nichol (Eds.), Hantaviruses (pp. 15-32.). Berlin: Springer-Verlag. Kallio-Kokko, H., Vapalahti, O., Lundkvist, Å. and Vaheri, A. (1998). Evaluation of Puumala virus IgG and IgM enzyme immunoassays based on recombinant baculovirus-expressed nucleocapsid protein for early nephropathia epidemica diagnosis. Clin Diagn Virol, 10,83-90. Kanerva, M., Mustonen, J. and Vaheri, A. (1998). Pathogenesis of Puumala and other hantavirus infections. Rev Med Virol, 8,67-86. Klempa, B., Meisel, H., Rath, S., Bartel, J., Ulrich, R. and Krüger , D.H. (2003a). Occurrence of renal and pulmonary syndrome in a region of Northeast Germany where Tula hantavirus circulates. J Clin Microbiol, 41, 4894-4897. Klempa, B., Schmidt, H. A., Ulrich, R., Kaluz, S., Labuda, M., Meisel, H., Hjelle, B. and Krüger, D. H. (2003b). Genetic interaction between distinct Dobrava hantavirus subtypes in Apodemus agrarius and A. flavicollis in nature. J Virol, 77,804-809. Klempa, B., Schütt, M., Auste, B., Labuda, M., Ulrich, R., Meisel, H. and Krüger, D.H. (2004). First molecular identification of human Dobrava virus infection in Central Europe. J Clin Microbiol, 42, 1322-1325. Klempa, B., Ulrich, R., Meisel, H., Krüger, D.H., Schmidt, H.A., Kaluz, S., Labuda, M., Hjelle, B. (2003c). Genetic Interaction between Dobrava and Saaremaa Hantaviruses: Now or Millions of Years Ago? (Authors' Reply). J Virol, 77, 7157-7158. Klingstrom, J., Heyman, P., Escutenaire, S., Sjolander, K. B., De Jaegere, F., Henttonen, H. and Lundkvist, Å. (2002). Rodent host specificity of European hantaviruses : evidence of Puumala virus interspecific spillover. J Med Virol, 68,581-588. Koh, H. S., Lee, W. J. and Kocher, T. D. (2000). The genetic relationships of two subspecies of striped field mice, Apodemus agrarius coreae and Apodemus agrarius chejuensis. Heredity, 85,30-36. Kratochvil, J. (1962). Notiz zur Ergänzung der Verbreitung von Apodemus agrarius und A. microps in der Tschechoslowakei. Zoologicke listy, 11, 15-26. Kraus, A. A., Raftery, M. J., Giese, T., Ulrich, R., Zawatsky, R., Hippenstiel, S., Suttorp, N., Krüger, D. H. and Schönrich, G. (2004). Differential antiviral response of endothelial cells after infection with pathogenic and nonpathogenic hantaviruses. J Virol, 78, 6143-6150. Krüger, D. H., Ulrich, R. and Lundkvist, Å. (2001). Hantavirus infections and their prevention. Microbes Infect, 3,1129-1144. Lee, H. W., Baek, L. J. and Johnson, K. M. (1982). Isolation of Hantaan virus, the etiologic agent of Korean hemorrhagic fever, from wild urban rats. J Infect Dis, 146,638-644. Lee, H. W., Lee, P. W. and Johnson, K. M. (1978). Isolation of the etiologic agent of Korean Hemorrhagic fever. J Infect Dis, 137,298-308. Lee, H. W. and van der Groen, G. (1989). Hemorrhagic fever with renal syndrome. Prog Med Virol, 36, 62-102. Li, D., Schmaljohn, A. L., Anderson, K. and Schmaljohn, C. S. (1995). Complete nucleotide sequences of the M and S segments of two hantavirus isolates from California: evidence for reassortment in nature among viruses related to hantavirus pulmonary syndrome. Virology, 206,973-983. Liang, M., Li, D., Xiao, S. Y., Hang, C., Rossi, C. A. and Schmaljohn, C. S. (1994). Antigenic and molecular characterization of hantavirus isolates from China. Virus Res, 31,219-233. Lin, M., Tseng, H. K., Trejaut, J. A., Lee, H. L., Loo, J. H., Chu, C. C., Chen, P. J., Su, Y. W., Lim, K. H., Tsai, Z. U., Lin, R. Y., Lin, R. S. and Huang, C. H. (2003). Association of HLA class I with severe acute respiratory syndrome coronavirus infection. BMC Med Genet, 4, 9. Lole, K. S., Bollinger, R. C., Paranjape, R. S., Gadkari, D., Kulkarni, S. S., Novak, N. G., Ingersoll, R., Sheppard, H. W. and Ray, S. C. (1999). Full-length human immunodeficiency virus type 1 genomes from subtype C-infected seroconverters in India, with evidence of intersubtype recombination. J Virol, 73,152-160. Lundkvist, Å., Apekina, N., Myasnikov, Y., Vapalahti, O., Vaheri, A. and Plyusnin, A. (1997a). Dobrava hantavirus outbreak in Russia. Lancet, 350, 781-782. Lundkvist, Å., Cheng, Y., Sjolander, K. B., Niklasson, B., Vaheri, A. and Plyusnin, A. (1997b). 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, 71,9515-9523. Lundkvist, Å., Fatouros, A. and Niklasson, B. (1991). Antigenic variation of European haemorrhagic fever with renal syndrome virus strains characterized using bank vole monoclonal antibodies. J Gen Virol, 72,2097-2103. Lundkvist, Å., Hukic, M., Horling, J., Gilljam, M., Nichol, S. and Niklasson, B. (1997c). Puumala and Dobrava viruses cause hemorrhagic fever with renal syndrome in Bosnia-Herzegovina: evidence of highly cross-neutralizing antibody responses in early patient sera. J Med Virol , 53,51-59. Lundkvist, Å., Lindegren, G., Brus Sjölander, K., Mavtchoutko, V., Vene, S., Plyusnin, A., Kalnina, V. (2002a). Hantavirus infections in Latvia. Eur J Clin Microbiol Infect Dis, 21, 626-629. Lundkvist, Å., Meisel, H., Koletzki, D., Lankinen, H., Cifire, F., Geldmacher, A., Sibold, C., Gott, P., Vaheri, A., Krüger, D. H. and Ulrich, R. (2002b). Mapping of B-cell epitopes in the nucleocapsid protein of Puumala hantavirus. Viral Immunol, 15,177-192. Lundkvist, Å., Vasilenko, V., Golovljova, I., Plyusnin, A. and Vaheri, A. (1998). Human Dobrava hantavirus infections in Estonia. Lancet, 352, 369. Mäkelä, S., Mustonen, J., Ala-Houhala, I., Hurme, M., Partanen, J., Vapalahti, O., Vaheri, A. and Pasternack, A. (2002). 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, 186, 843-846. Mackow, E. R. and Gavrilovskaya, I. N. (2001). Cellular receptors and hantavirus pathogenesis. In C. S. Schmaljohn and S. T. Nichol (Eds.), Hantaviruses (pp. 91-115.). Berlin: Springer-Verlag. Martin, Y., Gerlach, G., Schlotterer, C. and Meyer, A. (2000). Molecular phylogeny of European muroid rodents based on complete cytochrome b sequences. Mol Phylogenet Evol, 16,37-47. Meisel, H., Lundkvist, Å., Gantzer, K., Bar, W., Sibold, C. and Krüger, D. H. (1998). First case of infection with hantavirus Dobrava in Germany. Eur J Clin Microbiol Infect Dis, 17,884-885. Mertz, G. J., Hjelle, B. L. and Bryan, R. T. (1997). Hantavirus infection. Adv Intern Med, 42, 369-421. Michaux, J. R., Chevret, P., Filippucci, M. G. and Macholan, M. (2002). Phylogeny of the genus Apodemus with a special emphasis on the subgenus Sylvaemus using the nuclear IRBP gene and two mitochondrial markers: cytochrome b and 12S rRNA. Mol Phylogenet Evol, 23,123-136. Montgomery, W. I. (1999). Apodemus flavicollis. In A. J. Mitchell-Jones, G. Amori, W. Bogdanovicz, B. Krystufek, P. J. H. Rejinders, F. Spitzenberger, M. Stubbe, J. B. M. Thissen, V. Vohralik and J. Zima (Eds.), The Atlas of European Mammals (pp. 270-271.).

London, UK

: Academic Press. Morzunov, S. P., Feldmann, H., Spiropoulou, C. F., Semenova, V. A., Rollin, P. E., Ksiazek, T. G., Peters, C. J. and Nichol, S. T. (1995). A newly recognized virus associated with a fatal case of hantavirus pulmonary syndrome in Louisiana. J Virol, 69,1980-1983. Mustonen, J., Partanen, J., Kanerva, M., Pietila, K., Vapalahti, O., Pasternack, A. and Vaheri, A. (1996). Genetic susceptibility to severe course of nephropathia epidemica caused by Puumala hantavirus. Kidney Int, 49, 217-221. Mustonen, J., Partanen, J., Kanerva, M., Pietila, K., Vapalahti, O., Pasternack, A. and Vaheri, A. (1998). Association of HLA B27 with benign clinical course of nephropathia epidemica caused by Puumala hantavirus. Scand J Immunol, 47, 277-279. Nemirov, K., Henttonen, H., Vaheri, A. and Plyusnin, A. (2002). Phylogenetic evidence for host switching in the evolution of hantaviruses carried by Apodemus mice. Virus Res, 90,207-215. Nemirov, K., Lundkvist, Å., Vaheri, A., Plyusnin, A. (2003a). 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, 77, 8793-8800. Nemirov, K., Vapalahti, O., Lundkvist, Å., Vasilenko, V., Golovljova, I., Plyusnina, A., Niemimaa, J., Laakkonen, J., Henttonen, H., Vaheri, A. and Plyusnin, A. (1999). Isolation and characterization of Dobrava hantavirus carried by the striped field mouse (Apodemus agrarius) in Estonia. J Gen Virol, 80,371-379. Nemirov, K., Vapalahti, O., Papa, A., Plyusnina, A., Lundkvist, Å., Antoniadis, A., Vaheri, A., Plyusnin, A. (2003b). Genetic characterization of new Dobrava hantavirus isolate from Greece. J Med Virol. 69, 408-416. Nichol, S. T. (1999). Genetic analysis of hantaviruses and their host relationships. In J. F. Saluz and B. Dodet (Eds.), Emergence and Control of Rodent-borne Viral Diseases (pp. 99-109.).

Amsterdam

: Elsevier. Nichol, S. T., Spiropoulou, C. F., Morzunov, S., Rollin, P. E., Ksiazek, T. G., Feldmann, H., Sanchez, A., Childs, J., Zaki, S. and Peters, C. J. (1993). Genetic identification of a hantavirus associated with an outbreak of acute respiratory illness. Science, 262,914-917. Olsson, G. E., White, N., Ahlm, C., Elgh, F., Verlemyr, A. C., Juto, P. and Palo, R. T. (2002). Demographic factors associated with hantavirus infection in bank voles (Clethrionomys glareolus). Emerg Infect Dis, 8,924-929. Padula, P. J., Edelstein, A., Miguel, S. D., Lopez, N. M., Rossi, C. M. and Rabinovich, R. D. (1998). Hantavirus pulmonary syndrome outbreak in Argentina: molecular evidence for person-to-person transmission of Andes virus. Virology, 241,323-330. Papa, A., Johnson, A. M., Stockton, P. C., Bowen, M. D., Spiropoulou, C. F., Alexiou-Daniel, S., Ksiazek, T. G., Nichol, S. T. and Antoniadis, A. (1998). Retrospective serological and genetic study of the distribution of hantaviruses in Greece. J Med Virol, 55,321-327. Papa, A., Nemirov, K., Henttonen, H., Niemimaa, J., Antoniadis, A., Vaheri, A., Plyusnin, A. and Vapalahti, O. (2001). Isolation of Dobrava virus from Apodemus flavicollis in Greece. J Clin Microbiol, 39,2291-2293. Parrington, M. A. and Kang, C. Y. (1990). Nucleotide sequence analysis of the S genomic segment of Prospect Hill virus: comparison with the prototype Hantavirus. Virology, 175,167-175. Plyusnin, A. (2002). Genetics of hantaviruses : implications to taxonomy. Arch Virol, 147,665-682. Plyusnin, A., Cheng, Y., Vapalahti, O., Pejcoch, M., Unar, J., Jelinkova, Z., Lehvaslaiho, H., Lundkvist, Å. and Vaheri, A. (1995). Genetic variation in Tula hantaviruses : sequence analysis of the S and M segments of strains from Central Europe. Virus Res, 39,237-250. Plyusnin, A., Horling, J., Kanerva, M., Mustonen, J., Cheng, Y., Partanen, J., Vapalahti, O., Kukkonen, S. K., Niemimaa, J., Henttonen, H., Niklasson, B., Lundkvist, Å. and Vaheri, A. (1997a). Puumala hantavirus genome in patients with nephropathia epidemica: correlation of PCR positivity with HLA haplotype and link to viral sequences in local rodents. J Clin Microbiol, 35,1090-1096. Plyusnin, A., Krüger, D. H. and Lundkvist, Å. (2001a). Hantavirus infections in Europe. Adv Virus Res, 57, 105-136. Plyusnin, A., Kukkonen, S. K., Plyusnina, A., Vapalahti, O. and Vaheri, A. (2002). Transfection-mediated generation of functionally competent Tula hantavirus with recombinant S RNA segment. EMBO J, 21,1497-1503. Plyusnin, A. and Morzunov, S. P. (2001b). Virus evolution and genetic diversity of hantaviruses and their rodent hosts. In C. S. Schmaljohn and S. T. Nichol (Eds.), Hantaviruses (pp. 47-75.).

Berlin

: Springer-Verlag. Plyusnin, A., Mustonen, J., Asikainen, K., Plyusnina, A., Niemimaa, J., Henttonen, H. and Vaheri, A. (1999a). Analysis of Puumala hantavirus genome in patients with nephropathia epidemica and rodent carriers from the sites of infection. J Med Virol, 59,397-405. Plyusnin, A., Nemirov, K., Apekina, N., Plyusnina, A., Lundkvist, Å. and Vaheri, A. (1999b). Dobrava hantavirus in Russia. Lancet, 353,207. Plyusnin, A., Vapalahti, O., Lankinen, H., Lehvaslaiho, H., Apekina, N., Myasnikov, Y., Kallio-Kokko, H., Henttonen, H., Lundkvist, Å. and Brummer-Korvenkontio, M. (1994). Tula virus: a newly detected hantavirus carried by European common voles. J Virol, 68,7833-7839. Plyusnin, A., Vaheri, A. and Lundkvist, Å. (2003). Genetic interaction between Dobrava and Saaremaa viruses: now or millions of years ago? J Virol, 77, 7156-7157. Plyusnin, A., Vapalahti, O. and Vaheri, A. (1996). Hantaviruses: genome structure, expression and evolution. J Gen Virol, 77,2677-2687. Plyusnin, A., Vapalahti, O., Vasilenko, V., Henttonen, H. and Vaheri, A. (1997b). Dobrava hantavirus in Estonia: does the virus exist throughout Europe? Lancet, 349,1369- 1370. Pringle, C. R. (1991). The Bunyaviridae and their genetics--an overview. In D. Kolakofsky (Ed.), Bunyviridae (pp. 1-25.).

Berlin

: Springer-Verlag. Raftery, M. J., Kraus, A. A., Ulrich, R., Krüger, D. H. and Schönrich, G. (2002). Hantavirus infection of dendritic cells. J Virol, 76,10724-10733. Reip, A., Haring, B., Sibold, C., Stohwasser, R., Bautz, E. K., Darai, G., Meisel, H. and Krüger, D. H. (1995). Coding strategy of the S and M genomic segments of a hantavirus representing a new subtype of the Puumala serotype. Arch Virol, 140,2011 -2026. Rodriguez, L. L., Owens, J. H., Peters, C. J. and Nichol, S. T. (1998). Genetic reassortment among viruses causing hantavirus pulmonary syndrome. Virology, 242, 99-106. Salminen, M. O. (2003). Detecting recombination in viral sequences. In M. Salemi and A. M. Vandamme (Eds.), The Phylogenetic Handbook (pp. 348-377.).

Cambridge

: Cambridge University Press. Salminen, M. O., Carr, J. K., Burke, D. S. and McCutchan, F. E. (1995). Identification of breakpoints in intergenotypic recombinants of HIV type 1 by bootscanning. AIDS Res Hum Retroviruses, 11,1423-1425. Sanchez, A. J., Abbott, K. D. and Nichol, S. T. (2001). Genetic identification and characterization of limestone canyon virus, a unique Peromyscus-borne hantavirus. Virology, 286, 345-353. Scharninghausen, J. J., Meyer, H., Pfeffer, M., Davis, D. S. and Honeycutt, R. L. (1999). Genetic evidence of Dobrava virus in Apodemus agrarius in Hungary. Emerg Infect Dis, 5, 468-470. Scheil, H. G., Scheffrahn, W., Schmidt, H. D., Huckenbeck, W., Efremovska, L. and Xirotiris, N. (2001). Population genetic studies in the Balkans. I. Serum proteins. Anthropol Anz, 59, 203-211. Scheil, H. G., Schuhen, S., Huckenbeck, W. and Schmidt, H. D. (2002). Allele frequencies of alpha-1-antitrypsin (PI) in the Balkans. Coll Anthropol, 26, 403-410. Schmaljohn, C. S. and Hjelle, B. (1997). Hantaviruses: a global disease problem. Emerg Infect Dis, 3,95-104. Schmaljohn, C. S., Jennings, G. B., Hay, J. and Dalrymple, J. M. (1986). Coding strategy of the S genome segment of Hantaan virus. Virology, 155, 633-643. Schmaljohn, C. S. and Nichol, S. T. (2001). Hantaviruses.

Berlin

: Springer-Verlag. Schmidt, H. A., Strimmer, K., Vingron, M. and von Haeseler, A. (2002). TREE-PUZZLE: Maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics, 18, 502-504. Schubert, S., Dechend, F., Skawran, B., Krawczak, M. and Schmidtke, J. (2000). Molecular evolution of the murine tspy genes. Cytogenet Cell Genet, 91, 239-242. Schultze, D., Lundkvist, Å., Blauenstein, U. and Heyman, P. (2002). Tula virus infection associated with fever and exanthema after a wild rodent bite. Eur J Clin Microbiol Infect Dis, 21, 304-306. Serizawa, K., Suzuki, H. and Tsuchiya, K. (2000). A phylogenetic view on species radiation in Apodemus inferred from variation of nuclear and mitochondrial genes. Biochem Genet, 38, 27-40. Sibold, C., Meisel, H., Krüger, D. H., Labuda, M., Lysy, J., Kozuch, O., Pejcoch, M., Vaheri, A. and Plyusnin, A. (1999a). Recombination in Tula hantavirus evolution: analysis of genetic lineages from Slovakia. J Virol, 73, 667-675. Sibold, C., Meisel, H., Lundkvist, Å., Schulz, A., Cifire, F., Ulrich, R., Kozuch, O., Labuda, M. and Krüger, D. H. (1999b). Simultaneous occurrence of Dobrava, Puumala, and Tula Hantaviruses in Slovakia. Am J Trop Med Hyg, 61, 409- 411. Sibold, C., Sparr, S., Schulz, A., Labuda, M., Kozuch, O., Lysy, J., Krüger, D. H. and Meisel, H. (1995). Genetic characterization of a new hantavirus detected in Microtus arvalis from Slovakia. Virus Genes, 10, 277-281. Sibold, C., Ulrich, R., Labuda, M., Lundkvist, Å., Martens, H., Schütt, M., Gerke, P., Leitmeyer, K., Meisel, H. and Krüger, D. H. (2001). Dobrava hantavirus causes hemorrhagic fever with renal syndrome in central Europe and is carried by two different Apodemus mice species. J Med Virol, 63, 158-167. Sironen, T., Vaheri, A. and Plyusnin, A. (2001). Molecular evolution of Puumala hantavirus. J Virol, 75,11803-11810. Song, W., Torrez-Martinez, N., Irwin, W., Harrison, F. J., Davis, R., Ascher, M., Jay, M. and Hjelle, B. (1995). Isla Vista virus: a genetically novel hantavirus of the California vole Microtus californicus. J Gen Virol, 76, 3195-3199. Spiropoulou, C. F., Morzunov, S., Feldmann, H., Sanchez, A., Peters, C. J. and Nichol, S. T. (1994). Genome structure and variability of a virus causing hantavirus pulmonary syndrome. Virology, 200, 715-723. Strimmer, K. and von Haeseler, A. (1997). Likelihood-mapping: a simple method to visualize phylogenetic content of a sequence alignment. Proc Natl Acad Sci U S A, 94, 6815-6819. Swofford, D. L. PAUP* (Phylogenetic analysis using parsimony) (* and other methods), version 4. 2002.

Sunderland, MA, USA

. Swofford, D. L. and Sullivan, J. (2003). Phylogeny inference based on parsimony and other methods using PAUP*. In M. Salemi and A. M. Vandamme (Eds.), The Phylogenetic Handbook (pp. 160-206.).

Cambridge

: Cambridge University Press. Thompson, J. D., Higgins, D. G. and Gibson, T. J. (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucl Acids Res, 22, 4673-4680. Twiddy, S. S. and Holmes, E. C. (2003). The extent of homologous recombination in members of the genus Flavivirus. J Gen Virol, 84, 429-440. Van de Peer, Y. (2003). Phylogeny inference based on distance methods. In M. Salemi and A. M. Vandamme (Eds.), The Phylogenetic Handbook (pp. 101-136.).

Cambridge

: Cambridge University Press. Van Epps, H. L., Schmaljohn, C. S. and Ennis, F. A. (1999). 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, 73, 5301-5308. Vandamme, A. M. (2003). Basic concepts of molecular evolution. In M. Salemi and A. M. Vandamme (Eds.), The Phylogenetic Handbook (pp. 1-23.).

Cambridge

: Cambridge University Press. Vapalahti, O., Lundkvist, Å., Fedorov, V., Conroy, C. J., Hirvonen, S., Plyusnina, A., Nemirov, K., Fredga, K., Cook, J. A., Niemimaa, J., Kaikusalo, A., Henttonen, H., Vaheri, A. and Plyusnin, A. (1999). Isolation and characterization of a hantavirus from Lemmus sibiricus : evidence for host switch during hantavirus evolution. J Virol, 73,5586-5592. Vapalahti, O., Lundkvist, Å., Kukkonen, S. K., Cheng, Y., Gilljam, M., Kanerva, M., Manni, T., Pejcoch, M., Niemimaa, J., Kaikusalo, A., Henttonen, H., Vaheri, A. and Plyusnin, A. (1996). Isolation and characterization of Tula virus, a distinct serotype in the genus Hantavirus, family Bunyaviridae. J Gen Virol, 77, 3063-3067. Vapalahti, O., Lundkvist, Å. and Vaheri, A. (2001). Human immune response, host genetics, and severity of disease. In C. S. Schmaljohn and S. T. Nichol (Eds.), Hantaviruses (pp. 153-169.).

Berlin

: Springer-Verlag. Wang, H., Yoshimatsu, K., Ebihara, H., Ogino, M., Araki, K., Kariwa, H., Wang, Z., Luo, Z., Li, D., Hang, C. and Arikawa, J. (2000). Genetic diversity of hantaviruses isolated in china and characterization of novel hantaviruses isolated from Niviventer confucianus and Rattus rattus. Virology, 278, 332-345. Worobey, M. and Holmes, E. C. (1999). Evolutionary aspects of recombination in RNA viruses. J Gen Virol, 80, 2535-2543. Xiao, S. Y., Diglisic, G., Avsic-Zupanc, T. and Leduc, J. W. (1993). Dobrava virus as a new Hantavirus: evidenced by comparative sequence analysis. J Med Virol, 39, 152-155. Xiao, S. Y., Leduc, J. W., Chu, Y. K. and Schmaljohn, C. S. (1994). Phylogenetic analyses of virus isolates in the genus Hantavirus, family Bunyaviridae. Virology, 198, 205-217. Yoshimatsu, K., Arikawa, J., Tamura, M., Yoshida, R., Lundkvist, Å., Niklasson, B., Kariwa, H., Azuma, I. (1996). Characterization of the nucleocapsid protein of Hantaan virus strain 76-118 using monoclonal antibodies. J Gen Virol. 77, 695-704. Zeller, H. G., Karabatsos, N., Calisher, C. H., Digoutte, J. P., Cropp, C. B., Murphy, F. A. and Shope, R. E. (1989). Electron microscopic and antigenic studies of uncharacterized viruses. II. Evidence suggesting the placement of viruses in the family Bunyaviridae. Arch Virol, 108, 211-227. Zöller, L.G., Yang, S., Gött, P., Bautz, E.K., Darai, G. (1993). A novel m-capture enzyme-linked immunosorbent assay based on recombinant proteins for sensitive and specific diagnosis of hemorrhagic fever with renal syndrome. J Clin Microbiol. 31, 1194-1199.