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RNA Viruses: A Case Study of the Biology of Emerging Infectious Diseases

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  • Authors: Mark E. J. Woolhouse1, Kyle Adair2, Liam Brierley3
  • Editors: Ronald M. Atlas4, Stanley Maloy6
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Centre for Immunity, Infection & Evolution, University of Edinburgh, Edinburgh EH9 3JT, United Kingdom; 2: Centre for Immunity, Infection & Evolution, University of Edinburgh, Edinburgh EH9 3JT, United Kingdom; 3: Centre for Immunity, Infection & Evolution, University of Edinburgh, Edinburgh EH9 3JT, United Kingdom; 4: University of Louisville, Louisville, KY; 5: San Diego State University, San Diego, CA; 6: University of Louisville, Louisville, KY; 7: San Diego State University, San Diego, CA;
  • Source: microbiolspec October 2013 vol. 1 no. 1 doi:10.1128/microbiolspec.OH-0001-2012
  • Received 14 June 2012 Accepted 23 May 2013 Published 25 October 2013
  • Mark E. J. Woolhouse, mark.woolhouse@ed.ac.uk
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  • Abstract:

    There are 180 currently recognized species of RNA virus that can infect humans, and on average, 2 new species are added every year. RNA viruses are routinely exchanged between humans and other hosts (particularly other mammals and sometimes birds) over both epidemiological and evolutionary time: 89% of human-infective species are considered zoonotic and many of the remainder have zoonotic origins. Some viruses that have crossed the species barrier into humans have persisted and become human-adapted viruses, as exemplified by the emergence of HIV-1. Most, however, have remained as zoonoses, and a substantial number have apparently disappeared again. We still know relatively little about what determines whether a virus is able to infect, transmit from, and cause disease in humans, but there is evidence that factors such as host range, cell receptor usage, tissue tropisms, and transmission route all play a role. Although systematic surveillance for potential new human viruses in nonhuman hosts would be enormously challenging, we can reasonably aspire to much better knowledge of the diversity of mammalian and avian RNA viruses than exists at present.

  • Citation: J. Woolhouse M, Adair K, Brierley L. 2013. RNA Viruses: A Case Study of the Biology of Emerging Infectious Diseases. Microbiol Spectrum 1(1):OH-0001-2012. doi:10.1128/microbiolspec.OH-0001-2012.

References

1. Taylor LH, Latham SM, Woolhouse MEJ. 2001. Risk factors for human disease emergence. Philos Trans R Soc Lond B Biol Sci 356:983989.
2. King DA, Peckham C, Waage JK, Brownlie J, Woolhouse MEJ. 2006. Epidemiology. Infectious diseases: preparing for the future. Science 313:13921393.
3. Woolhouse MEJ, Scott FA, Hudson Z, Howey R, Chase-Topping M. 2012. Human viruses: discovery and emergence. Philos Trans R Soc Lond B Biol Sci 367:28642871.
4. Jones KE, Patel NG, Levy MA, Storeygard A, Balk D, Gittleman JL, Daszak P. 2008. Global trends in emerging infectious diseases. Nature 451:990993.
5. Sharp PM, Hahn BH. 2010. The evolution of HIV-1 and the origin of AIDS. Philos Trans R Soc Lond B Biol Sci 365:24872494.
6. Epstein JH, Field HE, Luby S, Pulliam JR, Daszak P. 2006. Nipah virus: impact, origins, and causes of emergence. Curr Infect Dis Rep 8:5963.
7. King AM, Adams MJ, Carstens EB, Lefkowitz EJ (ed). 2012. Virus Taxonomy: Ninth Report of the International Committee for the Taxonomy of Viruses. Elsevier, Amsterdam, The Netherlands.
8. Woolhouse MEJ, Adair K. 2013. The diversity of human RNA viruses. Future Virol 8:159171.
9. Kitchen A, Shackelton LA, Holmes EC. 2011. Family level phylogenies reveal modes of macroevolution in RNA viruses. Proc Natl Acad Sci USA 108:238243.
10. Wolfe ND, Dunavan CP, Diamond J. 2007. Origins of major human infectious diseases. Nature 447:279283.
11. Woolhouse MEJ, Taylor LH, Haydon DT. 2001. Population biology of multihost pathogens. Science 292:11091112.
12. Antia R, Regoes RR, Koella JC, Bergstrom CT. 2003. The role of evolution in the emergence of infectious diseases. Nature 426:658661.
13. Bae SE, Son HS. 2011. Classification of viral zoonosis through receptor pattern analysis. BMC Bioinformatics 12:96. doi:10.1186/1471-2105-12-96.
14. Kuiken T, Holmes EC, McCauley J, Rimmelzwaan GF, Williams CS, Grenfell BT. 2006. Host species barriers to influenza virus infections. Science 312:394397.
15. Blancou J, Aubert MF. 1997. [Transmission of rabies virus: importance of the species barrier]. Bull Acad Natl Med 181:301312. (In French.)
16. Streicker DG, Turmelle AS, Vonhof MJ, Kuzmin IV, McCracken GF, Rupprecht CE. 2010. Host phylogeny constrains cross-species emergence and establishment of rabies virus in bats. Science 329:676679.
17. Woolhouse MEJ, Adair K. 2013. Ecological and taxonomic variation among human RNA viruses. J Clin Virol [Epub ahead of print.] doi:10.1016/j.jcv.2013.02.019.
18. Ebert D, Bull J. 2008. The evolution and expression of virulence, p 153167. In Stearns SC, Koella JC (ed), Evolution in Health and Disease, 2nd ed. Oxford University Press, Oxford, United Kingdom.
19. World Health Organization Multicentre Collaborative Network for Severe Acute Respiratory Syndrome Diagnosis. 2003. A multicentre collaboration to investigate the cause of severe acute respiratory syndrome. Lancet 361:17301733.
20. Morse SS, Mazet JA, Woolhouse M, Parrish CR, Carroll D, Karesh WB, Zambrana-Torrelio C, Lipkin WI, Daszak P. 2012. Prediction and prevention of the next pandemic zoonosis. Lancet 380:19561965.
21. Drexler JF, Corman VM, Mller MA, Maganga GD, Vallo P, Binger T, Gloza-Rausch F, Rasche A, Yordanov S, Seebens A, Oppong S, Adu Sarkodie Y, Pongombo C, Lukashev AN, Schmidt-Chanasit J, Stcker A, Carneiro AJ, Erbar S, Maisner A, Fronhoffs F, Buettner R, Kalko EK, Kruppa T, Franke CR, Kallies R, Yandoko ER, Herrler G, Reusken C, Hassanin A, Krger DH, Matthee S, Ulrich RG, Leroy EM, Drosten C. 2012. Bats host major mammalian paramyxoviruses. Nat Commun 3:796. doi:10.1038/ncomms1796.
22. Ducomble T, Wilking H, Stark K, Takla A, Askar M, Schaade L, Nitsche A, Kurth A. 2012. Lack of evidence for Schmallenberg virus infection in highly exposed persons, Germany, 2012. Emerg Infect Dis 18:13331335.
23. Cotten M, Lam TT, Watson SJ, Palser AL, Petrova V, Grant P, Pybus OG, Rambaut A, Guan Y, Pillay D, Kellam P, Nastouli E. 2013. Full-genome deep sequencing and phylogenetic analysis of novel human betacoronavirus. Emerg Infect Dis 19:736742.
24. Palmarini M. 2007. A veterinary twist on pathogen biology. PLoS Pathog 3:e12. doi:10.1371/journal.ppat.0030012.
25. Woolhouse M, Antia R. 2008. Emergence of new infectious diseases, p 215228. In Stearns SC, Koella JC (ed), Evolution in Health and Disease, 2nd ed. Oxford University Press, Oxford, United Kingdom.
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Figures

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FIGURE 1

A representation of the pathogen pyramid. Each level of the pyramid represents a different degree of interaction between a virus and a human host. Level 1 corresponds to exposure of humans, level 2 to the ability to infect humans, level 3 to the ability to transmit from one human to another, and level 4 to the ability to cause epidemics or persist as an endemic infection. Arrows indicate pathways that viruses may take to reach each level. For example, a level 4 virus may arrive at that state directly, simply by exposure to the virus from a nonhuman reservoir. This is known as an “off-the-shelf” virus. Alternatively, it may initially enter the population as a level 2 or 3 virus—not capable of sustained transmission—but evolve the ability to transmit between humans at a sufficiently high rate to persist within a human population. This is known as a “tailor-made” virus. Adapted from reference 25. doi:10.1128/microbiolspec.OH-0001-2012.f1

Source: microbiolspec October 2013 vol. 1 no. 1 doi:10.1128/microbiolspec.OH-0001-2012
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Image of FIGURE 2

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FIGURE 2

All currently recognized human-infective RNA viruses categorized with respect to their ability to infect and transmit from humans (levels 2, 3, and 4 of the virus pyramid—see Fig. 1) and distinguished in terms of transmission route (green for vector-borne transmission, blue for other routes) and nature of diagnostic evidence (the viruses not in boldface type have only been reported in humans using serology-based methods). doi:10.1128/microbiolspec.OH-0001-2012.f2

Source: microbiolspec October 2013 vol. 1 no. 1 doi:10.1128/microbiolspec.OH-0001-2012
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FIGURE 3

A schematic representation of the relationship between human viruses and viruses from other mammals. Human viruses are depicted as a subset of mammal viruses, only partially protected by a species barrier. There are frequent minor incursions of zoonotic viruses (small arrows), and many of these may not persist in human populations. Occasionally there may be a much more significant event (large arrow) whereby a mammal virus proves capable of establishing itself as a new human virus, perhaps involving adaptation to infect and transmit from humans. doi:10.1128/microbiolspec.OH-0001-2012.f3

Source: microbiolspec October 2013 vol. 1 no. 1 doi:10.1128/microbiolspec.OH-0001-2012
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