Reservoir host immune responses to emerging zoonotic viruses

Cell

Volumn 160, Issue 1-2, 2015, Pages 20-35

  Mandl, Judith N ^a,g   Ahmed, Rafi ^b   Barreiro, Luis B ^c   Daszak, Peter ^d   Epstein, Jonathan H ^d   Virgin, Herbert W ^e   Feinberg, Mark B ^f  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF MONTREAL   (Canada)

^d ECOHEALTH ALLIANCE   (United States)

^e WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f MERCK RESEARCH LABORATORIES   (United States)

^g MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CORONAVIRUS; COST; DISEASE ASSOCIATION; EBOLA VIRUS; HANTAVIRUS; HENIPAVIRUS; HOST; HOST RESISTANCE; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS; IMMUNE RESPONSE; IMMUNOLOGY; INFLUENZA VIRUS A; INNATE IMMUNITY; METABOLISM; NONHUMAN; PATHOGENESIS; PHYSIOLOGY; PRIORITY JOURNAL; VIRUS; VIRUS INFECTION; VIRUS REPLICATION; VIRUS TRANSMISSION; ZOONOSIS; ZOONOTIC VIRUS; ANIMAL; COMMUNICABLE DISEASE; DISEASE CARRIER; HOST PATHOGEN INTERACTION; TRANSMISSION; VIRAL PHENOMENA AND FUNCTIONS; VIROLOGY;

ANIMALIA; EBOLA VIRUS; INFLUENZA A VIRUS;

ANIMALS; COMMUNICABLE DISEASES, EMERGING; DISEASE RESERVOIRS; HOST-PATHOGEN INTERACTIONS; HUMANS; VIRUS DISEASES; VIRUS PHYSIOLOGICAL PHENOMENA; ZOONOSES;

EID: 84920948384     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2014.12.003     Document Type: Review

References (126)

1. R. Ahmed, R.S. Simon, M. Matloubian, S.R. Kolhekar, P.J. Southern, and D.M. Freedman Genetic analysis of in vivo-selected viral variants causing chronic infection: importance of mutation in the L RNA segment of lymphocytic choriomeningitis virus J. Virol. 62 1988 3301 3308
2. W. Al-Herz, A. Bousfiha, J.L. Casanova, T. Chatila, M.E. Conley, C. Cunningham-Rundles, A. Etzioni, J.L. Franco, H.B. Gaspar, and S.M. Holland Primary immunodeficiency diseases: an update on the classification from the international union of immunological societies expert committee for primary immunodeficiency Front. Immunol. 5 2014 162
3. R. Antia, R.R. Regoes, J.C. Koella, and C.T. Bergstrom The role of evolution in the emergence of infectious diseases Nature 426 2003 658 661
4. J. Ayllon, and A. Garcia-Sastre The NS1 protein: A multitasking virulence factor Curr. Top. Microbiol. Immunol. 386 2015 73 107
5. E. Bailes, F. Gao, F. Bibollet-Ruche, V. Courgnaud, M. Peeters, P.A. Marx, B.H. Hahn, and P.M. Sharp Hybrid origin of SIV in chimpanzees Science 300 2003 1713
6. M.L. Baker, T. Schountz, and L.F. Wang Antiviral immune responses of bats: a review Zoonoses Public Health 60 2013 104 116
7. D.L. Barber, E.J. Wherry, D. Masopust, B. Zhu, J.P. Allison, A.H. Sharpe, G.J. Freeman, and R. Ahmed Restoring function in exhausted CD8 T cells during chronic viral infection Nature 439 2006 682 687
8. M.R. Barber, J.R. Aldridge Jr., R.G. Webster, and K.E. Magor Association of RIG-I with innate immunity of ducks to influenza Proc. Natl. Acad. Sci. USA 107 2010 5913 5918
9. L.B. Barreiro, and L. Quintana-Murci From evolutionary genetics to human immunology: how selection shapes host defence genes Nat. Rev. Genet. 11 2010 17 30
10. L.B. Barreiro, J.C. Marioni, R. Blekhman, M. Stephens, and Y. Gilad Functional comparison of innate immune signaling pathways in primates PLoS Genet. 6 2010 e1001249
11. E.S. Barton, D.W. White, J.S. Cathelyn, K.A. Brett-McClellan, M. Engle, M.S. Diamond, V.L. Miller, and H.W. Virgin IV Herpesvirus latency confers symbiotic protection from bacterial infection Nature 447 2007 326 329
12. C.M. Beaumier, L.D. Harris, S. Goldstein, N.R. Klatt, S. Whitted, J. McGinty, C. Apetrei, I. Pandrea, V.M. Hirsch, and J.M. Brenchley CD4 downregulation by memory CD4+ T cells in vivo renders African green monkeys resistant to progressive SIVagm infection Nat. Med. 15 2009 879 885
13. A.S. Beignon, K. McKenna, M. Skoberne, O. Manches, I. DaSilva, D.G. Kavanagh, M. Larsson, R.J. Gorelick, J.D. Lifson, and N. Bhardwaj Endocytosis of HIV-1 activates plasmacytoid dendritic cells via Toll-like receptor-viral RNA interactions J. Clin. Invest. 115 2005 3265 3275
14. R. Biek, P.D. Walsh, E.M. Leroy, and L.A. Real Recent common ancestry of Ebola Zaire virus found in a bat reservoir PLoS Pathog. 2 2006 e90
15. J.C. Blackwood, D.G. Streicker, S. Altizer, and P. Rohani Resolving the roles of immunity, pathogenesis, and immigration for rabies persistence in vampire bats Proc. Natl. Acad. Sci. USA 110 2013 20837 20842
16. S.E. Bosinger, Z.P. Johnson, K.A. Folkner, N. Patel, T. Hashempour, S.P. Jochems, P.M. Del Rio Estrada, M. Paiardini, R. Lin, and T.H. Vanderford Intact type I Interferon production and IRF7 function in sooty mangabeys PLoS Pathog. 9 2013 e1003597
17. H.R. Bouma, H.V. Carey, and F.G. Kroese Hibernation: the immune system at rest? J. Leukoc. Biol. 88 2010 619 624
18. A.C. Breed, J. Meers, I. Sendow, K.N. Bossart, J.A. Barr, I. Smith, S. Wacharapluesadee, L. Wang, and H.E. Field The distribution of henipaviruses in Southeast Asia and Australasia: is Wallace's line a barrier to Nipah virus? PLoS ONE 8 2013 e61316
19. J.M. Brenchley, D.A. Price, T.W. Schacker, T.E. Asher, G. Silvestri, S. Rao, Z. Kazzaz, E. Bornstein, O. Lambotte, and D. Altmann Microbial translocation is a cause of systemic immune activation in chronic HIV infection Nat. Med. 12 2006 1365 1371
20. J.F. Brinkworth, E.A. Pechenkina, J. Silver, and S.M. Goyert Innate immune responses to TLR2 and TLR4 agonists differ between baboons, chimpanzees and humans J. Med. Primatol. 41 2012 388 393
21. D.R. Burton, R.L. Stanfield, and I.A. Wilson Antibody vs. HIV in a clash of evolutionary titans Proc. Natl. Acad. Sci. USA 102 2005 14943 14948
22. M.J. Cameron, J.F. Bermejo-Martin, A. Danesh, M.P. Muller, and D.J. Kelvin Human immunopathogenesis of severe acute respiratory syndrome (SARS) Virus Res. 133 2008 13 19
23. G.A. Churchill, D.C. Airey, H. Allayee, J.M. Angel, A.D. Attie, J. Beatty, W.D. Beavis, J.K. Belknap, B. Bennett, W. Berrettini Complex Trait Consortium The Collaborative Cross, a community resource for the genetic analysis of complex traits Nat. Genet. 36 2004 1133 1137
24. R. Dantzer, J.C. O'Connor, G.G. Freund, R.W. Johnson, and K.W. Kelley From inflammation to sickness and depression: when the immune system subjugates the brain Nat. Rev. Neurosci. 9 2008 46 56
25. L.J. Demma, J.M. Logsdon Jr., T.H. Vanderford, M.B. Feinberg, and S.I. Staprans SIVsm quasispecies adaptation to a new simian host PLoS Pathog. 1 2005 e3
26. S.F. Dowell, R. Mukunu, T.G. Ksiazek, A.S. Khan, P.E. Rollin, and C.J. Peters Transmission of Ebola hemorrhagic fever: a study of risk factors in family members, Kikwit, Democratic Republic of the Congo, 1995. Commission de Lutte contre les Epidémies à Kikwit J. Infect. Dis. 179 Suppl 1 1999 S87 S91
27. J.D. Easterbrook, and S.L. Klein Immunological mechanisms mediating hantavirus persistence in rodent reservoirs PLoS Pathog. 4 2008 e1000172
28. J.H. Epstein, M.L. Baker, C. Zambrana-Torrelio, D. Middleton, J.A. Barr, E. Dubovi, V. Boyd, B. Pope, S. Todd, and G. Crameri Duration of Maternal Antibodies against Canine Distemper Virus and Hendra Virus in Pteropid Bats PLoS ONE 8 2013 e67584
29. R. Feuer, J.D. Boone, D. Netski, S.P. Morzunov, and S.C. St Jeor Temporal and spatial analysis of Sin Nombre virus quasispecies in naturally infected rodents J. Virol. 73 1999 9544 9554
30. N. Figueiredo, A. Chora, H. Raquel, N. Pejanovic, P. Pereira, B. Hartleben, A. Neves-Costa, C. Moita, D. Pedroso, and A. Pinto Anthracyclines induce DNA damage response-mediated protection against severe sepsis Immunity 39 2013 874 884
31. H. Frebel, V. Nindl, R.A. Schuepbach, T. Braunschweiler, K. Richter, J. Vogel, C.A. Wagner, D. Loffing-Cueni, M. Kurrer, B. Ludewig, and A. Oxenius Programmed death 1 protects from fatal circulatory failure during systemic virus infection of mice J. Exp. Med. 209 2012 2485 2499
32. T.W. Geisbert, and P.B. Jahrling Exotic emerging viral diseases: progress and challenges Nat. Med. 10 Suppl 2004 S110 S121
33. T.W. Geisbert, H. Feldmann, and C.C. Broder Animal challenge models of henipavirus infection and pathogenesis Curr. Top. Microbiol. Immunol. 359 2012 153 177
34. S.K. Gire, A. Goba, K.G. Andersen, R.S. Sealfon, D.J. Park, L. Kanneh, S. Jalloh, M. Momoh, M. Fullah, and G. Dudas Genomic surveillance elucidates Ebola virus origin and transmission during the 2014 outbreak Science 345 2014 1369 1372
35. B.B. Gowen, J.D. Hoopes, M.H. Wong, K.H. Jung, K.C. Isakson, L. Alexopoulou, R.A. Flavell, and R.W. Sidwell TLR3 deletion limits mortality and disease severity due to Phlebovirus infection J. Immunol. 177 2006 6301 6307
36. B.H. Hahn, G.M. Shaw, K.M. De Cock, and P.M. Sharp AIDS as a zoonosis: scientific and public health implications Science 287 2000 607 614
37. K. Halpin, P.L. Young, H.E. Field, and J.S. Mackenzie Isolation of Hendra virus from pteropid bats: a natural reservoir of Hendra virus J. Gen. Virol. 81 2000 1927 1932
38. K. Halpin, A.D. Hyatt, R. Fogarty, D. Middleton, J. Bingham, J.H. Epstein, S.A. Rahman, T. Hughes, C. Smith, H.E. Field, P. Daszak Henipavirus Ecology Research Group Pteropid bats are confirmed as the reservoir hosts of henipaviruses: a comprehensive experimental study of virus transmission Am. J. Trop. Med. Hyg. 85 2011 946 951
39. S.A. Handley, L.B. Thackray, G. Zhao, R. Presti, A.D. Miller, L. Droit, P. Abbink, L.F. Maxfield, A. Kambal, and E. Duan Pathogenic simian immunodeficiency virus infection is associated with expansion of the enteric virome Cell 151 2012 253 266
40. K.M. Hastie, S. Bale, C.R. Kimberlin, and E.O. Saphire Hiding the evidence: two strategies for innate immune evasion by hemorrhagic fever viruses Curr. Opin. Virol. 2 2012 151 156
41. M.M. Herbst, J. Prescott, A.D. Palmer, and T. Schountz Sequence and expression analysis of deer mouse interferon-gamma, interleukin-10, tumor necrosis factor, and lymphotoxin-alpha Cytokine 17 2002 203 213
42. E.C. Holmes, and A.J. Drummond The evolutionary genetics of viral emergence Curr. Top. Microbiol. Immunol. 315 2007 51 66
43. A. Iwasaki A virological view of innate immune recognition Annu. Rev. Microbiol. 66 2012 177 196
44. B. Jacquelin, V. Mayau, B. Targat, A.S. Liovat, D. Kunkel, G. Petitjean, M.A. Dillies, P. Roques, C. Butor, and G. Silvestri Nonpathogenic SIV infection of African green monkeys induces a strong but rapidly controlled type I IFN response J. Clin. Invest. 119 2009 3544 3555
45. A.M. Jamieson, L. Pasman, S. Yu, P. Gamradt, R.J. Homer, T. Decker, and R. Medzhitov Role of tissue protection in lethal respiratory viral-bacterial coinfection Science 340 2013 1230 1234
46. V. Jeney, S. Ramos, M.L. Bergman, I. Bechmann, J. Tischer, A. Ferreira, V. Oliveira-Marques, C.J. Janse, S. Rebelo, and S. Cardoso Control of disease tolerance to malaria by nitric oxide and carbon monoxide Cell Rep. 8 2014 126 136
47. C. Jin, J. Henao-Mejia, and R.A. Flavell Innate immune receptors: key regulators of metabolic disease progression Cell Metab. 17 2013 873 882
48. K.E. Jones, N.G. Patel, M.A. Levy, A. Storeygard, D. Balk, J.L. Gittleman, and P. Daszak Global trends in emerging infectious diseases Nature 451 2008 990 993
49. E. Jourdain, G. Gunnarsson, J. Wahlgren, N. Latorre-Margalef, C. Bröjer, S. Sahlin, L. Svensson, J. Waldenström, A. Lundkvist, and B. Olsen Influenza virus in a natural host, the mallard: experimental infection data PLoS ONE 5 2010 e8935
50. W.B. Karesh, A. Dobson, J.O. Lloyd-Smith, J. Lubroth, M.A. Dixon, M. Bennett, S. Aldrich, T. Harrington, P. Formenty, and E.H. Loh Ecology of zoonoses: natural and unnatural histories Lancet 380 2012 1936 1945
51. J.C. Kash, T.M. Tumpey, S.C. Proll, V. Carter, O. Perwitasari, M.J. Thomas, C.F. Basler, P. Palese, J.K. Taubenberger, and A. García-Sastre Genomic analysis of increased host immune and cell death responses induced by 1918 influenza virus Nature 443 2006 578 581
52. A. Kaur, R.M. Grant, R.E. Means, H. McClure, M. Feinberg, and R.P. Johnson Diverse host responses and outcomes following simian immunodeficiency virus SIVmac239 infection in sooty mangabeys and rhesus macaques J. Virol. 72 1998 9597 9611
53. B.F. Keele, J.H. Jones, K.A. Terio, J.D. Estes, R.S. Rudicell, M.L. Wilson, Y. Li, G.H. Learn, T.M. Beasley, and J. Schumacher-Stankey Increased mortality and AIDS-like immunopathology in wild chimpanzees infected with SIVcpz Nature 460 2009 515 519
54. D.J. Kominsky, E.L. Campbell, and S.P. Colgan Metabolic shifts in immunity and inflammation J. Immunol. 184 2010 4062 4068
55. C. Kornfeld, M.J.Y. Ploquin, I. Pandrea, A. Faye, R. Onanga, C. Apetrei, V. Poaty-Mavoungou, P. Rouquet, J. Estaquier, and L. Mortara Antiinflammatory profiles during primary SIV infection in African green monkeys are associated with protection against AIDS J. Clin. Invest. 115 2005 1082 1091
56. T. Kuiken, B. Riteau, R.A. Fouchier, and G.F. Rimmelzwaan Pathogenesis of influenza virus infections: the good, the bad and the ugly Curr. Opin. Virol. 2 2012 276 286
57. R. Le Goffic, V. Balloy, M. Lagranderie, L. Alexopoulou, N. Escriou, R. Flavell, M. Chignard, and M. Si-Tahar Detrimental contribution of the Toll-like receptor (TLR)3 to influenza A virus-induced acute pneumonia PLoS Pathog. 2 2006 e53
58. M.N. Lee, C. Ye, A.C. Villani, T. Raj, W. Li, T.M. Eisenhaure, S.H. Imboywa, P.I. Chipendo, F.A. Ran, and K. Slowikowski Common genetic variants modulate pathogen-sensing responses in human dendritic cells Science 343 2014 1246980
59. J.O. Lloyd-Smith, D. George, K.M. Pepin, V.E. Pitzer, J.R. Pulliam, A.P. Dobson, P.J. Hudson, and B.T. Grenfell Epidemic dynamics at the human-animal interface Science 326 2009 1362 1367
60. S.P. Luby, M. Rahman, M.J. Hossain, L.S. Blum, M.M. Husain, E. Gurley, R. Khan, B.N. Ahmed, S. Rahman, and N. Nahar Foodborne transmission of Nipah virus, Bangladesh Emerg. Infect. Dis. 12 2006 1888 1894
61. A.D. Luis, D.T. Hayman, T.J. O'Shea, P.M. Cryan, A.T. Gilbert, J.R. Pulliam, J.N. Mills, M.E. Timonin, C.K. Willis, and A.A. Cunningham A comparison of bats and rodents as reservoirs of zoonotic viruses: are bats special? Proc. Biol. Sci. 280 2013 20122753
62. J.S. Mackenzie, and M. Jeggo Reservoirs and vectors of emerging viruses Curr. Opin. Virol. 3 2013 170 179
63. J.N. Mandl, A.P. Barry, T.H. Vanderford, N. Kozyr, R. Chavan, S. Klucking, F.J. Barrat, R.L. Coffman, S.I. Staprans, and M.B. Feinberg Divergent TLR7 and TLR9 signaling and type I interferon production distinguish pathogenic and nonpathogenic AIDS virus infections Nat. Med. 14 2008 1077 1087
64. J.N. Mandl, R. Akondy, B. Lawson, N. Kozyr, S.I. Staprans, R. Ahmed, and M.B. Feinberg Distinctive TLR7 signaling, type I IFN production, and attenuated innate and adaptive immune responses to yellow fever virus in a primate reservoir host J. Immunol. 186 2011 6406 6416
65. H.D. Marston, G.K. Folkers, D.M. Morens, and A.S. Fauci Emerging viral diseases: confronting threats with new technologies Sci. Transl. Med. 6 2014 53ps10
66. O. Martinez, L.W. Leung, and C.F. Basler The role of antigen-presenting cells in filoviral hemorrhagic fever: gaps in current knowledge Antiviral Res. 93 2012 416 428
67. V.D. Menachery, A.J. Eisfeld, A. Schafer, L. Josset, A.C. Sims, S. Proll, S. Fan, C. Li, G. Neumann, and S.C. Tilton Pathogenic influenza viruses and coronaviruses utilize similar and contrasting approaches to control interferon-stimulated gene responses Mbio. 5 2014 e01174 e01214
68. C.U. Meteyer, D. Barber, and J.N. Mandl Pathology in euthermic bats with white nose syndrome suggests a natural manifestation of immune reconstitution inflammatory syndrome Virulence 3 2012 583 588
69. D.J. Middleton, C.J. Morrissy, B.M. van der Heide, G.M. Russell, M.A. Braun, H.A. Westbury, K. Halpin, and P.W. Daniels Experimental Nipah virus infection in pteropid bats (Pteropus poliocephalus) J. Comp. Pathol. 136 2007 266 272
70. F. Miedema, M.D. Hazenberg, K. Tesselaar, D. van Baarle, R.J. de Boer, and J.A. Borghans Immune activation and collateral damage in AIDS pathogenesis Front. Immunol. 4 2013 298
71. J. Misasi, and N.J. Sullivan Camouflage and misdirection: the full-on assault of ebola virus disease Cell 159 2014 477 486
72. S. Moir, T.W. Chun, and A.S. Fauci Pathogenic mechanisms of HIV disease Annu. Rev. Pathol. 6 2011 223 248
73. J.L. Mokili, F. Rohwer, and B.E. Dutilh Metagenomics and future perspectives in virus discovery Curr. Opin. Virol. 2 2012 63 77
74. S.S. Morse, J.A. Mazet, M. Woolhouse, C.R. Parrish, D. Carroll, W.B. Karesh, C. Zambrana-Torrelio, W.I. Lipkin, and P. Daszak Prediction and prevention of the next pandemic zoonosis Lancet 380 2012 1956 1965
75. M.B. Oldstone, and H. Rosen Cytokine storm plays a direct role in the morbidity and mortality from influenza virus infection and is chemically treatable with a single sphingosine-1-phosphate agonist molecule Curr. Top. Microbiol. Immunol. 378 2014 129 147
76. K.J. Olival, J.H. Epstein, L.-F. Wang, H.E. Field, and P. Daszak Are bats unique virus reservoirs? A.A. Aguirre, R.S. Ostfeld, P. Daszak, New Directions in Conservation Medicine Applied Cases of Ecological Health 2013 Oxford University Press New York 195 212
77. L.C. Osborne, L.A. Monticelli, T.J. Nice, T.E. Sutherland, M.C. Siracusa, M.R. Hepworth, V.T. Tomov, D. Kobuley, S.V. Tran, and K. Bittinger Coinfection. Virus-helminth coinfection reveals a microbiota-independent mechanism of immunomodulation Science 345 2014 578 582
78. 4+ T cells are associated with limited CCR5 expression Nat. Med. 17 2011 830 836
79. A. Pandey, K.E. Atkins, J. Medlock, N. Wenzel, J.P. Townsend, J.E. Childs, T.G. Nyenswah, M.L. Ndeffo-Mbah, and A.P. Galvani Strategies for containing Ebola in West Africa Science 346 2014 991 995
80. I. Pandrea, and C. Apetrei Where the wild things are: pathogenesis of SIV infection in African nonhuman primate hosts Curr. HIV/AIDS Rep. 7 2010 28 36
81. U.D. Parashar, L.M. Sunn, F. Ong, A.W. Mounts, M.T. Arif, T.G. Ksiazek, M.A. Kamaluddin, A.N. Mustafa, H. Kaur, and L.M. Ding Case-control study of risk factors for human infection with a new zoonotic paramyxovirus, Nipah virus, during a 1998-1999 outbreak of severe encephalitis in Malaysia J. Infect. Dis. 181 2000 1755 1759
82. E.L. Pearce, and E.J. Pearce Metabolic pathways in immune cell activation and quiescence Immunity 38 2013 633 643
83. J.S. Peiris, Y. Guan, and K.Y. Yuen Severe acute respiratory syndrome Nat. Med. 10 Suppl 2004 S88 S97
84. J.S. Peiris, K.P. Hui, and H.L. Yen Host response to influenza virus: protection versus immunopathology Curr. Opin. Immunol. 22 2010 475 481
85. P. Penaloza-MacMaster, A.O. Kamphorst, A. Wieland, K. Araki, S.S. Iyer, E.E. West, L. O'Mara, S. Yang, B.T. Konieczny, and A.H. Sharpe Interplay between regulatory T cells and PD-1 in modulating T cell exhaustion and viral control during chronic LCMV infection J. Exp. Med. 211 2014 1905 1918
86. D.M. Pigott, N. Golding, A. Mylne, Z. Huang, A.J. Henry, D.J. Weiss, O.J. Brady, M.U. Kraemer, D.L. Smith, and C.L. Moyes Mapping the zoonotic niche of Ebola virus disease in Africa eLife 3 2014
87. J. Pothlichet, and L. Quintana-Murci The genetics of innate immunity sensors and human disease Int. Rev. Immunol. 32 2013 157 208
88. C. Qian, and X. Cao Regulation of Toll-like receptor signaling pathways in innate immune responses Ann. N Y Acad. Sci. 1283 2013 67 74
89. P.L. Quan, C. Firth, J.M. Conte, S.H. Williams, C.M. Zambrana-Torrelio, S.J. Anthony, J.A. Ellison, A.T. Gilbert, I.V. Kuzmin, and M. Niezgoda Bats are a major natural reservoir for hepaciviruses and pegiviruses Proc. Natl. Acad. Sci. USA 110 2013 8194 8199
90. L. Råberg, D. Sim, and A.F. Read Disentangling genetic variation for resistance and tolerance to infectious diseases in animals Science 318 2007 812 814
91. S.A. Rahman, L. Hassan, J.H. Epstein, Z.C. Mamat, A.M. Yatim, S.S. Hassan, H.E. Field, T. Hughes, J. Westrum, M.S. Naim Henipavirus Ecology Research Group Risk Factors for Nipah virus infection among pteropid bats, Peninsular Malaysia Emerg. Infect. Dis. 19 2013 51 60
92. A.L. Rasmussen, A. Okumura, M.T. Ferris, R. Green, F. Feldmann, S.M. Kelly, D.P. Scott, D. Safronetz, E. Haddock, and R. LaCasse Host genetic diversity enables Ebola hemorrhagic fever pathogenesis and resistance Science 346 2014 987 991
93. T.A. Reese, B.S. Wakeman, H.S. Choi, M.M. Hufford, S.C. Huang, X. Zhang, M.D. Buck, A. Jezewski, A. Kambal, and C.Y. Liu Coinfection. Helminth infection reactivates latent γ-herpesvirus via cytokine competition at a viral promoter Science 345 2014 573 577
94. R.R. Regoes, P.J. McLaren, M. Battegay, E. Bernasconi, A. Calmy, H.F. Günthard, M. Hoffmann, A. Rauch, A. Telenti, J. Fellay Swiss HIV Cohort Study Disentangling human tolerance and resistance against HIV PLoS Biol. 12 2014 e1001951
95. I.G. Rodrigue-Gervais, K. Labbé, M. Dagenais, J. Dupaul-Chicoine, C. Champagne, A. Morizot, A. Skeldon, E.L. Brincks, S.M. Vidal, T.S. Griffith, and M. Saleh Cellular inhibitor of apoptosis protein cIAP2 protects against pulmonary tissue necrosis during influenza virus infection to promote host survival Cell Host Microbe 15 2014 23 35
96. B.T. Rouse, and S. Sehrawat Immunity and immunopathology to viruses: What decides the outcome? Nat. Rev. Immunol. 10 2010 514 526
97. B.A. Roy, and J.W. Kirchner Evolutionary dynamics of pathogen resistance and tolerance Evolution 54 2000 51 63
98. N.G. Sandler, S.E. Bosinger, J.D. Estes, R.T. Zhu, G.K. Tharp, E. Boritz, D. Levin, S. Wijeyesinghe, K.N. Makamdop, and G.Q. del Prete Type I interferon responses in rhesus macaques prevent SIV infection and slow disease progression Nature 511 2014 601 605
99. D. Sauter Counteraction of the multifunctional restriction factor tetherin Front. Microbiol. 5 2014 163
100. D.S. Schneider, and J.S. Ayres Two ways to survive infection: what resistance and tolerance can teach us about treating infectious diseases Nat. Rev. Immunol. 8 2008 889 895
101. J.W. Schoggins, S.J. Wilson, M. Panis, M.Y. Murphy, C.T. Jones, P. Bieniasz, and C.M. Rice A diverse range of gene products are effectors of the type I interferon antiviral response Nature 472 2011 481 485
102. T. Schountz, and J. Prescott Hantavirus immunology of rodent reservoirs: current status and future directions Viruses 6 2014 1317 1335
103. J. Seok, H.S. Warren, A.G. Cuenca, M.N. Mindrinos, H.V. Baker, W. Xu, D.R. Richards, G.P. McDonald-Smith, H. Gao, L. Hennessy Inflammation and Host Response to Injury, Large Scale Collaborative Research Program Genomic responses in mouse models poorly mimic human inflammatory diseases Proc. Natl. Acad. Sci. USA 110 2013 3507 3512
104. Y.Y. Shen, L. Liang, Z.H. Zhu, W.P. Zhou, D.M. Irwin, and Y.P. Zhang Adaptive evolution of energy metabolism genes and the origin of flight in bats Proc. Natl. Acad. Sci. USA 107 2010 8666 8671
105. G. Silvestri, D.L. Sodora, R.A. Koup, M. Paiardini, S.P. O'Neil, H.M. McClure, S.I. Staprans, and M.B. Feinberg Nonpathogenic SIV infection of sooty mangabeys is characterized by limited bystander immunopathology despite chronic high-level viremia Immunity 18 2003 441 452
106. M. Sitkovsky, and D. Lukashev Regulation of immune cells by local-tissue oxygen tension: HIF1 alpha and adenosine receptors Nat. Rev. Immunol. 5 2005 712 721
107. A.R. Sohayati, L. Hassan, S.H. Sharifah, K. Lazarus, C.M. Zaini, J.H. Epstein, N. Shamsyul Naim, H.E. Field, S.S. Arshad, J. Abdul Aziz, P. Daszak Henipavirus Ecology Research Group Evidence for Nipah virus recrudescence and serological patterns of captive Pteropus vampyrus Epidemiol. Infect. 139 2011 1570 1579
108. L.H. Taylor, S.M. Latham, and M.E.J. Woolhouse Risk factors for human disease emergence Philos. Trans. R. Soc. Lond. B Biol. Sci. 356 2001 983 989
109. A.L. Totura, and R.S. Baric SARS coronavirus pathogenesis: host innate immune responses and viral antagonism of interferon Curr Opin Virol 2 2012 264 275
110. A.S. Turmelle, F.R. Jackson, D. Green, G.F. McCracken, and C.E. Rupprecht Host immunity to repeated rabies virus infection in big brown bats J. Gen. Virol. 91 2010 2360 2366
111. J.H. Verhagen, V.J. Munster, F. Majoor, P. Lexmond, O. Vuong, J.B. Stumpel, G.F. Rimmelzwaan, A.D. Osterhaus, M. Schutten, R. Slaterus, and R.A. Fouchier Avian influenza a virus in wild birds in highly urbanized areas PLoS ONE 7 2012 e38256
112. H.W. Virgin The virome in mammalian physiology and disease Cell 157 2014 142 150
113. H.W. Virgin, E.J. Wherry, and R. Ahmed Redefining chronic viral infection Cell 138 2009 30 50
114. C.M. Wade, E.J. Kulbokas III, A.W. Kirby, M.C. Zody, J.C. Mullikin, E.S. Lander, K. Lindblad-Toh, and M.J. Daly The mosaic structure of variation in the laboratory mouse genome Nature 420 2002 574 578
115. T. Wang, T. Town, L. Alexopoulou, J.F. Anderson, E. Fikrig, and R.A. Flavell Toll-like receptor 3 mediates West Nile virus entry into the brain causing lethal encephalitis Nat. Med. 10 2004 1366 1373
116. B. Weber, S. Schuster, D. Zysset, S. Rihs, N. Dickgreber, C. Schürch, C. Riether, M. Siegrist, C. Schneider, and H. Pawelski TREM-1 deficiency can attenuate disease severity without affecting pathogen clearance PLoS Pathog. 10 2014 e1003900
117. WHO (2014) (http://www.who.int/csr/don/2014-08-27-ebola/en/: World Health Organization).
118. WHO Ebola Response Team Ebola virus disease in West Africa - the first 9 months of the epidemic and forward projections N. Engl. J. Med. 371 2014 1481 1495
119. G.S. Wilkinson, and J.M. South Life history, ecology and longevity in bats Aging Cell 1 2002 124 131
120. N.D. Wolfe, W.M. Switzer, J.K. Carr, V.B. Bhullar, V. Shanmugam, U. Tamoufe, A.T. Prosser, J.N. Torimiro, A. Wright, and E. Mpoudi-Ngole Naturally acquired simian retrovirus infections in central African hunters Lancet 363 2004 932 937
121. N.D. Wolfe, C.P. Dunavan, and J. Diamond Origins of major human infectious diseases Nature 447 2007 279 283
122. M. Woolhouse, F. Scott, Z. Hudson, R. Howey, and M. Chase-Topping Human viruses: discovery and emergence Philos. Trans. R. Soc. Lond. B Biol. Sci. 367 2012 2864 2871
123. A.M. Zaki, S. van Boheemen, T.M. Bestebroer, A.D. Osterhaus, and R.A. Fouchier Isolation of a novel coronavirus from a man with pneumonia in Saudi Arabia N. Engl. J. Med. 367 2012 1814 1820
124. C.A. Zampieri, N.J. Sullivan, and G.J. Nabel Immunopathology of highly virulent pathogens: insights from Ebola virus Nat. Immunol. 8 2007 1159 1164
125. G. Zhang, C. Cowled, Z. Shi, Z. Huang, K.A. Bishop-Lilly, X. Fang, J.W. Wynne, Z. Xiong, M.L. Baker, and W. Zhao Comparative analysis of bat genomes provides insight into the evolution of flight and immunity Science 339 2013 456 460
126. J. Zhao, K. Li, C. Wohlford-Lenane, S.S. Agnihothram, C. Fett, J. Zhao, M.J. Gale Jr., R.S. Baric, L. Enjuanes, and T. Gallagher Rapid generation of a mouse model for Middle East respiratory syndrome Proc. Natl. Acad. Sci. USA 111 2014 4970 4975