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Bank vole immunoheterogeneity may limit Nephropatia Epidemica emergence in a French non-endemic region

Published online by Cambridge University Press:  21 September 2017

A. DUBOIS ,
G. CASTEL ,
S. MURRI ,
C. PULIDO ,
J.-B. PONS ,
L. BENOIT ,
A. LOISEAU ,
L. LAKHDAR ,
M. GALAN  and
P. MARIANNEAU
...Show all authors
A. DUBOIS
Affiliation:
CBGP, INRA, CIRAD, IRD, Montpellier SupAgro, Univ. Montpellier, Montpellier, France ANSES, Unité de Virologie, Laboratoire de Lyon, France
G. CASTEL
Affiliation:
CBGP, INRA, CIRAD, IRD, Montpellier SupAgro, Univ. Montpellier, Montpellier, France
S. MURRI
Affiliation:
ANSES, Unité de Virologie, Laboratoire de Lyon, France
C. PULIDO
Affiliation:
ANSES, Plateforme d'Expérimentation Animale, Laboratoire de Lyon, France
J.-B. PONS
Affiliation:
Univ Lyon, LabEx ECOFECT Ecoevolutionary Dynamics of Infectious Diseases, Villeurbanne Lyon, France
L. BENOIT
Affiliation:
CBGP, CIRAD, INRA, IRD, Montpellier SupAgro, Univ. Montpellier, Montpellier, France
A. LOISEAU
Affiliation:
CBGP, INRA, CIRAD, IRD, Montpellier SupAgro, Univ. Montpellier, Montpellier, France
L. LAKHDAR
Affiliation:
ANSES, Plateforme d'Expérimentation Animale, Laboratoire de Lyon, France
M. GALAN
Affiliation:
CBGP, INRA, CIRAD, IRD, Montpellier SupAgro, Univ. Montpellier, Montpellier, France
P. MARIANNEAU
Affiliation:
ANSES, Unité de Virologie, Laboratoire de Lyon, France
N. CHARBONNEL*
Affiliation:
CBGP, INRA, CIRAD, IRD, Montpellier SupAgro, Univ. Montpellier, Montpellier, France
*
*Corresponding author. N. Charbonnel, Centre de Biologie pour la Gestion des Populations, Montferrier sur Lez, France. E-mail: nathalie.charbonnel@inra.fr
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Summary

Ecoevolutionary processes affecting hosts, vectors and pathogens are important drivers of zoonotic disease emergence. In this study, we focused on nephropathia epidemica (NE), which is caused by Puumala hantavirus (PUUV) whose natural reservoir is the bank vole, Myodes glareolus. We questioned the possibility of NE emergence in a French region that is considered to be NE-free but that is adjacent to a NE-endemic region. We first confirmed the epidemiology of these two regions and we demonstrated the absence of spatial barriers that could have limited dispersal, and consequently, the spread of PUUV into the NE-free region. We next tested whether regional immunoheterogeneity could impact PUUV chances to circulate and persist in the NE-free region. We showed that bank voles from the NE-free region were sensitive to experimental PUUV infection. We observed high levels of immunoheterogeneity between individuals and also between regions. Antiviral gene expression (Tnf and Mx2) reached higher levels in bank voles from the NE-free region. During experimental infections, anti-PUUV antibody production was higher in bank voles from the NE-endemic region. These results indicated a lower susceptibility to PUUV for bank voles from this NE-free region, which might limit PUUV persistence and therefore, the risk of NE.

Keywords

Myodes glareolusrodentPuumala hantaviruspopulation geneticsexperimental infectionsecoimmunology.
Type
Research Article
Information
Parasitology , Volume 145 , Issue 3 , March 2018 , pp. 393 - 407
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Copyright © Cambridge University Press 2017 

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Footnotes

†

These authors contributed equally to this work.

References

REFERENCES

Aars, J., Dallas, J. F., Piertney, S. B., Marshall, F., Gow, J. L., Telfer, S. and Lambin, X. (2006). Widespread gene flow and high genetic variability in populations of water voles Arvicola terrestris in patchy habitats. Molecular Ecology 15, 1455–1466.Google Scholar
Behnke, J. M., Barnard, C. J., Bajer, A., Bray, D., Dinmore, J., Frake, K., Osmond, J., Race, T. and Sinski, E. (2001). Variation in the helminth community structure in bank voles (Clethrionomys glareolus) from three comparable localities in the Mazury Lake District region of Poland. Parasitology 123, 401–414.Google Scholar
Beldomenico, P. M., Telfer, S., Gebert, S., Lukomski, L., Bennett, M. and Begon, M. (2008). Poor condition and infection: a vicious circle in natural populations. Proceedings of the Royal Society B-Biological Sciences 275, 1753–1759.CrossRefGoogle ScholarPubMed
Benjamini, Y. and Hochberg, Y. (1995). Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society: Series B 57, 289–300.Google Scholar
Bernshtein, A. D., Apekina, N. S., Mikhailova, T. V., Myasnikov, Y. A., Khlyap, L. A., Korotkov, Y. S. and Gavrilovskaya, I. N. (1999). Dynamics of Puumala hantavirus infection in naturally infected bank voles (Clethrinomys glareolus). Archives of Virology 144, 2415–2428.CrossRefGoogle ScholarPubMed
Berthier, K., Galan, M., Foltete, J. C., Charbonnel, N. and Cosson, J. F. (2005). Genetic structure of the cyclic fossorial water vole (Arvicola terrestris): landscape and demographic influences. Molecular Ecology 14, 2861–2871.CrossRefGoogle ScholarPubMed
Berthier, K., Charbonnel, N., Galan, M., Chaval, Y. and Cosson, J. F. (2006). Migration and maintenance of genetic variability in cyclic vole populations: a spatio-temporal study. Molecular Ecology 15, 2665–2676.CrossRefGoogle Scholar
Bowie, A. G. and Haga, I. R. (2005). The role of Toll-like receptors in the host response to viruses. Molecular Immunology 42, 859–867.Google Scholar
Bradley, J. R. (2008). TNF-mediated inflammatory disease. Journal of Pathology 214, 149–160.Google Scholar
Brummer-Korvenkotio, M., Henttonen, H. and Vaheri, A. (1982). Hemorrhagic fever with renal syndrome in Finland: ecology and virology of Nephropathia Epidemica. Scandinavian Journal of Infectious Diseases 36, 88–89.Google Scholar
Bryja, J., Charbonnel, N., Berthier, K., Galan, M. and Cosson, J. F. (2007). Density-related changes in selection pattern for major histocompatibility complex genes in fluctuating populations of voles. Molecular Ecology 16, 5084–5097.Google Scholar
Campbell, C. L., Torres-Perez, F., Acuna-Retamar, M. and Schountz, T. (2015) Transcriptome markers of viral persistence in naturally-infected Andes Virus (Bunyaviridae) seropositive long-tailed pygmy rice rats. PLoS ONE 10, e0122935.Google Scholar
Castel, G., Couteaudier, M., Sauvage, F., Pons, J. B., Murri, S., Plyusnina, A., Pontier, D., Cosson, J. F., Plyusnin, A., Marianneau, P. and Tordo, N. (2015). Complete genome and phylogeny of Puumala hantavirus isolates circulating in France. Viruses 7, 5476–5488.CrossRefGoogle ScholarPubMed
Charbonnel, N., Pagès, M., Sironen, T., Henttonen, H., Vapalahti, O., Mustonen, J. and Vaheri, A. (2014). Immunogenetic factors affecting susceptibility of humans and rodents to hantaviruses and the clinical course of hantaviral disease in humans. Viruses 6, 2214–2241.CrossRefGoogle ScholarPubMed
Daszak, P., Cunningham, A. A. and Hyatt, A. D. (2000). Emerging infectious diseases of wildlife – threats to biodiversity and human health. Science 287, 443–449.CrossRefGoogle ScholarPubMed
Deter, J., Chaval, Y., Galan, M., Gauffre, B., Morand, S., Henttonen, H., Laakkonen, J., Voutilainen, L., Charbonnel, N. and Cosson, J. F. (2008 a). Kinship, dispersal and hantavirus transmission in bank and common voles. Archives of Virology 153, 435–444.Google Scholar
Deter, J., Chaval, Y., Galan, M., Henttonen, H., Laakkonen, J., Voutilainen, L., Ribas Salvador, A., Bryja, J., Morand, S., Cosson, J. F. and Charbonnel, N. (2008 b). Association between the DQA MHC class II gene and Puumala virus infection in the specific reservoir Myodes glareolus . Infection Genetics Evolution 8, 450–458.Google Scholar
Di Ciccio, T. J. and Efron, B. (1996). Bootstrap confidence intervals. Statistical Science 11, 189–228.Google Scholar
Dubois, A., Castel, G., Murri, S., Pulido, C., Pons, J. B., Benoit, L., Loiseau, A., Lakhdar, L., Galan, M., Charbonnel, N. and Marianneau, P. (2017 a). Experimental infections of wild bank voles (Myodes glareolus) from Nephropatia Epidemica endemic and non-endemic regions revealed slight differences in Puumala virological course and immunological responses. Virus Research 253, 67–72.Google Scholar
Dubois, A., Galan, M., Guivier, E., Henttonen, H., Voutilainen, L., Razzauti, M., Gauffre, B., Marianneau, P., Cosson, J. F. and Charbonnel, N. (2017 b). Microevolution of bank voles (Myodes glareolus) at neutral and immune related genes during a multi-annual complete dynamic cycle: consequences for Puumala hantavirus epidemiology. Infection Genetics Evolution 49, 318–329.Google Scholar
Easterbrook, J. D. and Klein, S. L. (2008). Seoul virus enhances regulatory and reduces proinflammatory responses in male Norway rats. Journal of Medical Virology 80, 1308–1318.Google Scholar
Excoffier, L. and Lischer, H. E. L. (2010). Arlequin suite ver 3·5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources 10, 564–567.CrossRefGoogle ScholarPubMed
Friberg, I. M., Lowe, A., Ralli, C., Bradley, J. E. and Jackson, J. A. (2011). Temporal anomalies in immunological gene expression in a time series of wild mice: signature of an epidemic? PloS ONE 5, e20070.CrossRefGoogle Scholar
Gascuel, F., Choisy, M., Duplantier, J. M., Debarre, F. and Brouat, C. (2013). Host resistance, population structure and the long-term persistence of bubonic plague: contributions of a modelling approach in the Malagasy focus. Plos Computational Biology 9, e1003039.CrossRefGoogle ScholarPubMed
Gavrilovskaya, I. N., Chumakov, M. P., Apekina, N. S., Ryltseva, E. V., Martiyanova, L. I., Gorbachkova, E. A., Bernshtein, A. D., Zakharova, M. A. and Boiko, V. A. (1983). Adaptation to laboratory and wild animals of the haemorrhagic fever with renal syndrome virus present in the foci of European U.S.S.R. Archives of Virology 77, 87–90.Google Scholar
Guivier, E., Galan, M., Ribas Salvador, A., Xuéreb, A., Chaval, Y., Olsson, G., Essbauer, S., Henttonen, H., Voutilainen, L., Cosson, J. F. and Charbonnel, N. (2010). Tnf-α expression and promoter sequences reflect the balance of tolerance/resistance to Puumala virus infection in European bank vole populations. Infection Genetics Evolution 10, 1208–1217.Google Scholar
Guivier, E., Galan, M., Chaval, Y., Xuereb, A., Ribas Salvador, A., Poulle, M. L., Charbonnel, N. and Cosson, J. F. (2011). Landscape genetics highlights the role of bank vole metapopulation dynamics in the epidemiology of Puumala hantavirus . Molecular Ecology 20, 3569–3583.Google Scholar
Guivier, E., Galan, M., Henttonen, H., Cosson, J. F. and Charbonnel, N. (2014). Landscape features and helminth co-infection shape bank vole immunoheterogeneity, with consequences for Puumala virus epidemiology. Heredity 112, 274–281.Google Scholar
Hardestam, J., Karlsson, M., Falk, K. I., Olsson, G., Klingström, J. and Lundkvist, A. (2008). Puumala hantavirus excretion kinetics in bank voles (Myodes glareolus). Emerging Infectious Diseases 14, 1209–1215.Google Scholar
Hayward, A. D., Nussey, D. H., Wilson, A. J., Berenos, C., Pilkington, J. G., Watt, K. A., Pemberton, J. M. and Graham, A. L. (2014). Natural selection on individual variation in tolerance of gastrointestinal nematode infection. PLos Biology 12, e1001917.CrossRefGoogle ScholarPubMed
Heil, F., Hemmi, H., Hochrein, H., Ampenberger, F., Kirschning, C., Akira, S., Lipford, G., Wagner, H. and Bauer, S. (2004). Species-specific recognition of single-stranded RNA via toll-like receptor 7 and 8. Science 303, 1526–1529.Google Scholar
Henttonen, H., Buchy, P., Suputtamongkol, Y., Jittapalapong, S., Herbreteau, V., Laakkonen, J., Chaval, Y., Galan, M., Dobigny, G., Charbonnel, N., Michaux, J., Cosson, J. F., Morand, S. and Hugot, J. P. (2008). Recent discoveries of new hantaviruses widen their range and question their origins. In Animal Biodiversity and Emerging Diseases: Prediction and Prevention, Vol. 1149 (ed. Sparagano, O. A. E., Maillard, J. C. and Figueroa, J. V.), pp. 84–89. Blackwell Publishing, Oxford.Google Scholar
Heyman, P., Ceianu, C. S., Christova, I., Tordo, N., Beersma, M., Joao Alves, M., Lundkvist, A., Hukic, M., Papa, A., Tenorio, A., Zelena, H., Essbauer, S., Visontai, I., Golovljova, I., Connell, J., Nicoletti, L., Van Esbroeck, M., Gjeruldsen Dudman, S., Aberle, S. W., Avsic-Zupanc, T., Korukluoglu, G., Nowakowska, A., Klempa, B., Ulrich, R. G., Bino, S., Engler, O., Opp, M. and Vaheri, A. (2011). A five-year perspective on the situation of haemorrhagic fever with renal syndrome and status of the hantavirus reservoirs in Europe, 2005–2010. Eurosurveillance 16, 1–8.Google Scholar
Heyman, P., Thoma, B. R., Marie, J. L., Cochez, C. and Essbauer, S. S. (2012). In search for factors that drive hantavirus epidemics. Frontiers in Physiology 3, 237.Google Scholar
Hirsch, I., Caux, C., Hasan, U., Bendriss-Vermare, N. and Olive, D. (2010). Impaired Toll-like receptor 7 and 9 signaling: from chronic viral infections to cancer. Trends in Immunology 31, 391–397.CrossRefGoogle ScholarPubMed
Jackson, J. A., Begon, M., Birtles, R., Paterson, S., Friberg, I. M., Hall, A., Ralli, C., Turner, A., Zawadzka, M. and Bradley, J. E. (2011). The analysis of immunological profiles in wild animals: a case study on immunodynamics in the field vole, Microtus agrestis . Molecular Ecology 20, 893–909.Google Scholar
Jackson, J. A., Hall, A. J., Friberg, I. M., Ralli, C., Lowe, A., Zawadzka, M., Turner, A. K., Stewart, A., Birtles, R. J., Paterson, S., Bradley, J. E. and Begon, M. (2014). An immunological marker of tolerance to infection in wild rodents. PLos Biology 12, e1001901.CrossRefGoogle ScholarPubMed
Jameson, L. H., Logue, C. H., Atkinson, B., Baker, B., Galbraith, S. E., Carroll, M. W., Brooks, T. and Hewson, R. (2013). The continued emergence of hantaviruses: isolation of a Seoul virus implicated in human disease, United Kingdom, October 2012. Eurosurveillance 18, 1–4.CrossRefGoogle ScholarPubMed
Jin, H. K., Yoshimatsu, K., Takada, A., Ogino, M., Asano, A., Arikawa, J. and Watanabe, T. (2001). Mouse Mx2 protein inhibits hantavirus but not influenza virus replication. Archives of Virology 146, 41–49.Google Scholar
Jombart, T., Devillard, S. and Balloux, F. (2010). Discriminant analysis of principal components: a new method for the analysis, of genetically structured populations. BMC Genetics 11, 94.CrossRefGoogle ScholarPubMed
Kallio, E. R., Klingström, J., Gustafsson, E., Manni, T., Vaheri, A., Henttonen, H., Vapalahti, O. and Lundkvist, A. (2006). Prolonged survival of Puumala hantavirus outside the host: evidence for indirect transmission via the environment. Journal of General Virology 87, 2127–2134.Google Scholar
Kanerva, M., Melen, K., Vaheri, A. and Julkunen, I. (1996). Inhibition of Puumala and Tula hantaviruses in vero cells by MxA protein. Virology 224, 55–62.Google Scholar
King, D. A., Peckham, C., Waage, J. K., Brownlie, J. and Woolhouse, M. E. (2006). Epidemiology. Infectious diseases: preparing for the future. Science 313, 1392–1393.CrossRefGoogle ScholarPubMed
Klein, S. L. and Flanagan, K. L. (2016). Sex differences in immune responses. Nature Reviews Immunology 16, 626–638.CrossRefGoogle ScholarPubMed
Klingstrom, J., Heyman, P., Escutenaire, S., Sjolander, K. B., De Jaegere, F., Henttonen, H. and Lundkvist, A. (2002). Rodent host specificity of European hantaviruses: evidence of Puumala virus interspecific spillover. Journal of Medical Virology 68, 581–588.CrossRefGoogle ScholarPubMed
Korpela, H. and Lähdevirta, J. (1978). The role of small rodents and patterns of living in the epidemiology of nephropathia epidemica. Scandinavian Journal of Infectious Diseases 10, 303–305.CrossRefGoogle ScholarPubMed
Korva, M., Duh, D., Saksida, A., Trilar, T. and Avsic-Zupanc, T. (2009). The hantaviral load in tissues of naturally infected rodents. Microbes and Infection 11, 344–351.CrossRefGoogle ScholarPubMed
Kruger, D. H., Ulrich, R. and Lundkvist, Å. (2001). Hantavirus infections and their prevention. Microbes and Infection 3, 1129–1144.CrossRefGoogle ScholarPubMed
Lee, K. A. and Klasing, K. C. (2004). A role for immunology in invasion biology. Trends in Ecology and Evolution 19, 523–529.Google Scholar
Li, Y. L. and Youssoufian, H. (1997). Mxa overexpression reveals a common genetic link in four Fanconi anemia complementation groups. Journal of Clinical Investigation 100, 2873–2880.Google Scholar
Lloyd-Smith, J. O., Cross, P. C., Briggs, C. J., Daugherty, M., Getz, W. M., Latto, J., Sanchez, M. S., Smith, A. B. and Swei, A. (2005). Should we expect population thresholds for wildlife disease? Trends in Ecology & Evolution 20, 511–519.Google Scholar
Loxton, K. C., Lawton, C., Stafford, P. and Holland, C. V. (2016). Reduced helminth parasitism in the introduced bank vole (Myodes glareolus): more parasites lost than gained. International Journal for Parasitology 5, 175–183.Google ScholarPubMed
Lund, J. M., Alexopoulou, L., Sato, A., Karow, M., Adams, N. C., Gale, N. W., Iwasaki, A. and Flavell, R. A. (2004). Recognition of single-stranded RNA viruses by Toll-like receptor 7. Proceedings of the National Academy of Sciences, USA 101, 5598–5603.Google Scholar
Lundkvist, A., Hukic, M., Hörling, J., Gilljam, M., Nichol, S. and Niklasson, B. (1997). Puumala and Dobrava viruses cause hemorrhagic fever with renal syndrome in Bosnia-Herzegovina: evidence of highly cross-neutralizing antibody responses in early patient sera. Journal of Medical Virology 53, 51–59.3.0.CO;2-P>CrossRefGoogle ScholarPubMed
Mace, G., Feyeux, C., Mollard, N., Chantegret, C., Audia, S., Rebibou, J. M., Spagnolo, G., Bour, J. B., Denoyel, G. A., Sagot, P. and Reynes, J. M. (2013). Severe Seoul hantavirus infection in a pregnant woman, France, October 2012. Eurosurveillance 18, 14–17.Google Scholar
Morse, S. S. and Schluederberg, A. (1990). Emerging viruses: the evolution of viruses and viral diseases. Journal of Infectious Diseases 162, 1–7.CrossRefGoogle ScholarPubMed
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). Emerging Infectious Diseases 8, 924–929.CrossRefGoogle ScholarPubMed
Pfaffl, M. W. (2001). A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Research 29, e45.Google Scholar
Plath, K., Mlynarczyk-Evans, S., Nusinow, D. A. and Panning, B. (2002). Xist RNA and the mechanism of X chromosome inactivation. Annual Review of Genetics 36, 233–278.Google Scholar
R Core Team (2013). A language and environment for statistical computing. Austria, Vienna.Google Scholar
Raberg, L., Graham, A. L. and Read, A. F. (2009). Decomposing health: tolerance and resistance to parasites in animals. Philosophical Transactions of the Royal Society B-Biological Sciences 364, 37–49.Google Scholar
Raymond, M. and Rousset, F. (1995). Genepop version 3: population genetics software for exact tests and ecumenicism. Journal of Heredity 86, 248–249.CrossRefGoogle Scholar
Razzauti-Feliu, M., Galan, M., Bernard, M., Maman, S., Klopp, C., Charbonnel, N., Vayssier-Taussat, M., Eloit, M. and Cosson, J. F. (2015). Comparison of next-generation sequencing approaches surveying bacterial pathogens in wildlife. Plos Neglected Tropical Diseases 9, e0003929.Google Scholar
Reynes, J. M., Dutrop, C. M., Carli, D., Levast, M., Fontaine, N., Denoyel, G. A. and Philit, J. B. (2015). Puumala hantavirus infection in Isere: geographic extension of this zoonosis in France. Medecine et Maladies Infectieuses 45, 177–180.CrossRefGoogle ScholarPubMed
Ribas Salvador, A., Guivier, E., Xuereb, A., Chaval, Y., Cadet, P., Poulle, M. L., Sironen, T., Voutilainen, L., Henttonen, H., Cosson, J. F. and Charbonnel, N. (2011). Concomitant influence of helminth infection and landscape on the distribution of Puumala hantavirus in its reservoir. Myodes glareolus . BMC Microbiology 11, 11–30.Google Scholar
Rikalainen, K., Grapputo, A., Knott, E., Koskela, E. and Mappes, T. (2008). A large panel of novel microsatellite markers for the bank vole (Myodes glareolus). Molecular Ecology Resources 8, 1164–1168.CrossRefGoogle ScholarPubMed
Rohfritsch, A., Guivier, E., Galan, M., Chaval, Y. and Charbonnel, N. (2013). Apport de l'immunogénétique à la compréhension des interactions entre le campagnol roussâtre Myodes glareolus et l'hantavirus Puumala. Bulletin de l'académie vétérinaire de France 166, 165–176.Google Scholar
Ruijter, J. M., Ramakers, C., Hoogaars, W. M. H., Karlen, Y., Bakker, O., van den Hoff, M. J. B. and Moorman, A. F. M. (2009). Amplification efficiency: linking baseline and bias in the analysis of quantitative PCR data. Nucleic Acids Research 37, e45.Google Scholar
Schneider, D. S. and Ayres, J. S. (2008). Two ways to survive infection: what resistance and tolerance can teach us about treating infectious diseases. Nature Reviews Immunology 8, 889–895.Google Scholar
Schonrich, G., Rang, A., Lutteke, N., Raftery, M. J., Charbonnel, N. and Ulrich, R. G. (2008). Hantavirus-induced immunity in rodent reservoirs and humans. Immunological Reviews 225, 163–189.Google Scholar
Schountz, T. and Prescott, J. (2014). Hantavirus immunology of rodent reservoirs: current status and future directions. Viruses 6, 1317–1335.Google Scholar
Schountz, T., Acuna-Retamar, M., Feinstein, S., Prescott, J., Torres-Perez, F., Podell, B., Peters, S., Ye, C., Black, W. C. and Hjelle, B. (2012). Kinetics of immune responses in deer mice experimentally infected with Sin Nombre Virus. Journal of Virology 86, 10015–10027.Google Scholar
Sommaruga, A. (1997). Geology of the Central Jura and the Molasse Basin. In Institut de Géologie, Vol. PhD, p. 195. Université de Neuchâtel, Neuchâtel, Suisse.Google Scholar
Temonen, M., Mustonen, J., Helin, H., Pasternack, A., Vaheri, A. and Holthofer, H. (1996). Cytokines, adhesion molecules, and cellular infiltration in nephropathia epidemica kidneys: an immunohistochemical study. Clinical Immunology and Immunopathology 78, 47–55.Google Scholar
Tersago, K., Crespin, L., Verhagen, R. and Leirs, H. (2012). Impact of Puumala virus infection on maturation and survival in bank voles: a capture-mark-recapture analysis. Journal of Wildlife Diseases 48, 148–156.Google Scholar
Tollenaere, C., Jacquet, S., Ivanova, S., Loiseau, A., Duplantier, J. M., Streiff, R. and Brouat, C. (2013). Beyond an AFLP genome scan towards the identification of immune genes involved in plague resistance in Rattus rattus from Madagascar. Molecular Ecology 22, 354–367.Google Scholar
Vaheri, A., Strandin, T., Hepojoki, J., Sironen, T., Henttonen, H., Mäkelä, S. and Mustonen, J. (2013). Uncovering the mysteries of hantavirus infections. Nature Reviews Microbiology 11, 539–550.Google Scholar
Vander Wal, E., Garant, D., Calmé, S., Chapman, C. A., Festa-Bianchet, M., Millien, V., Rioux-Paquette, S. and Pelletier, F. (2014). Applying evolutionary concepts to wildlife disease ecology and management. Evolutionary Applications 7, 856–868.CrossRefGoogle ScholarPubMed
Vapalahti, O., Mustonen, J., Lundkvist, A., Henttonen, H., Plyusnin, A. and Vaheri, A. (2003). Hantavirus infections in Europe. Lancet Infectious Diseases 3, 653–661.Google Scholar
Voutilainen, L., Sironen, T., Tonteri, E., Tuiskunen Back, A., Razzauti, M., Karlsson, M., Wahlstrom, M., Niemimaa, J., Henttonen, H. and Lundkvist, A. (2015). Life-long shedding of Puumala hantavirus in wild bank voles (Myodes glareolus). Journal of General Virology 96, 1238–1247.Google Scholar
Voutilainen, L., Kallio, E. R., Niemimaa, J., Vapalahti, O. and Henttonen, H. (2016). Temporal dynamics of Puumala hantavirus infection in cyclic populations of bank voles. Scientific Reports 6, 21323.Google Scholar
Weir, B. and Cockerham, C. (1984). Estimating F-statistics for the analysis of population structure. Evolution 38, 1358–1370.Google Scholar
Wenzel, J., Uerlich, M., Haller, O., Bieber, T. and Tueting, T. (2005). Enhanced type I interferon signaling and recruitment of chemokine receptor CXCR3-expressing lymphocytes into the skin following treatment with the TLR7-agonist imiquimod. Journal of Cutaneous Pathology 32, 257–262.Google Scholar
Wright, S. (1951). The genetical structure of populations. Annals of Eugenics 15, 323–354.Google Scholar
Yanagihara, R., Amyx, H. L. and Gajdusek, D. C. (1985). Experimental infection with Puumala virus, the etiologic agent of nephropathia epidemica, in bank voles (Clethrionomys glareolus). Journal of Virology 55, 34–38.Google Scholar
Zeimes, C. B., Quoilin, S., Henttonen, H., Lyytikaïnen, O., Vapalahti, O., Reynes, J. M., Reusken, C., Swart, A. N., Vainio, K., Hjertqvist, M. and Vanwambeke, S. O. (2015). Landscape and regional environmental analysis of the spatial distribution of hantavirus human cases in Europe. Frontiers in Public Health 3, 1–10.Google Scholar
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