The molecular evolution of the most dangerous emerging virus infections

N Popov; T Kolotova

Автор(и)

N Popov Mechnikov Institute of Microbiology and Immunology,
T Kolotova Mechnikov Institute of Microbiology and Immunolog,

Ключові слова:

emerging viruses, four stage of the emergence, natural reservoir, recombination, reassotment, mutagenesis, HIV-1, HIV-2, SIV, SARS-CoV, virus Ebola, influenza virus A

Анотація

In this paper we reviewed what is known about the emerging viruses, the hosts that they originate in, and the molecular events that drive their emergence. When a pathogen crosses over from animals to humans, or an existing human disease suddenly increases in incidence, the infectious disease is said to be ‘emerging’. Most of the emerging pathogens originate from nonhuman animal species which has been termed natural reservoirs. The number of emerging infectious diseases has increased over the last few decades, driven by both anthropogenic and environmental factors such as population growth, urbanization, global travel and trade, intensification of livestock production. Now it has been believed that the emergence process may include four steps. On the first step the exposure of the humans to a novel virus occures. On the second step the subset of the viruses overcome the cross-species barrier. Host shifts have resulted in multiple human pandemics, such as HIV from chimps the H1N1, ‘‘spanish flu’’ from birds, SARS-CoV and virus Ebola from bats. Then some viruses enables to transmit from one human to another. And on the last step the viruses that are sufficiently transmissible between humans cause outbreaks and become endemic in human populations without the requirement of a natural reservoir. This review aims to discuss the molecular mechanisms that govern virus cross-species transmission and following stage, using the emergence of HIV, SARS-CoV, virus Ebola and influenza virus A as the models.Populations of many viruses harbour abundant genetic variability due to a combination of high mutation, recombination or reassortation rates and large population sizes. Mutations and recombinations has been associated with the increases in virulence, the evasion of host immunity and the evolution of resistance to antivirals. Genetic alterations in one species may results in the acquisition of variations that allow them to overcome cross species barriers and infect new hosts. Really, many recently emerged human diseases are caused by viruses that display active recombination or reassortment. The continual shuffling of genes of influenza A represents a example of the key role of reassortment for the new virus emergence. Available data demonstrate the possible origin of SARS-CoV from recombination of different bat SL-CoVs viruses strains. However in other cases the emergence of a specific virus cannot be directly attributed to its ability to recombine. For example, although SIV recombines at a high rate in natural reservoirs, there is no evidence that recombination assisted the cross-species transfer of the virus from the chimpanzee into humans. But mutagenesis and recombination actively shape the further molecular history of HIV in humans. Also it is not proved that recombination precede the cross-species jump of the Ebola virus. In summary, the available data suggest that although recombination, reassortment and mutagenesis is sometimes directly involved to the process of cross-species transmission, it is not a necessary precursor to successful viral emergence. Further investigations are required to reveal the role of genetic change in the history of virus emergence. We believethat comprehensive description of molecular evolution of new viruses has led to a better understanding of the causes and predictability of infection emergence.

Посилання

Stern, D.L. Is Genetic Evolution Predictable? [Text]/ D. L. Stern, V. Orgogozo // Science. – 2009. – V.323. – P. 746-751.

Neverov, A. D. Coordinated Evolution of Influenza A Surface Proteins [Text] / A. D. Neverov, S. Kryazhimskiy, J. B. Plotkin, G. A. Bazykin // PLoS Genet. -- 2015. – V. 11. – N. 8. -- e1005404.

Longdon, B. The evolution and genetics of virus host shifts [Text] / B. Longdon, M. A. Brockhurst, C. A. Russell, J. J. Welch, F. M. Jiggins // PLoS Pathog. -- 2014. – V. 10. – N. 11. -- e1004395.

Peters, C.J. Emerging viral diseases [Text] / C. J. Peters // Fields Virology. -- 5th. ed. – Lappincott, Williams, Wilkins. -- Philadelphia, --2007. – P. 605–625.

Taylor, L. Н. Risk factors for human disease emergence [Text]/ L. H. Taylor, S. M. Latham, M. E. J. Woolhouse // Phil. Trans. R. Soc. Lond. B. – 2001. -- V. 356. – P. 983–989.

Woolhouse, M. Chase-Topping Human viruses: discovery and emergence [Text] / M. Woolhouse, F. Scott, Z. Hudson, R. Howey // Phil. Trans. R. Soc. B. – 2012. -- V.367. – P. 2864–2871.

Keele, B.F. Increased mortality and AIDS-like immunopathology in wild chimpanzees infected with SIVcpz [Text]/ B. F. Keele, J. H. Jones, K. A. Terio, J. D. Estes, R. S. Rudicell, [et al.] // Nature. – 2009. – V. 460. – P. 515–519.

Lederer, S. Transcriptional profiling in pathogenic and non-pathogenic SIV infections reveals significant distinctions in kinetics and tissue compartmentalization [Text]/ S. Lederer, D. Favre, K. A. Walters, S. Proll, B. Kanwar, [et al.] // PLoS Pathog. – 2009. -- V. 5 -- e1000296.

Holmes, E.C. Viral evolution and the emergence of SARS coronavirus [Text]/ E.C. Holmes, A. Rambaut, // Phil. Trans. R. Soc. Lond. B. – 2004. – V. 359. – P. 1059–1065.

Cohen, J. As swine flu circles globe, scientists grapple with basic questions [Text] / J. Cohen, M. Enserink // Science – V. 2009 . – V. 324. – P. 572–573.

Longdon, B. The Causes and Consequences of Changes in Virulence following Pathogen Host Shifts [Text] / B. Longdon, J. D. Hadfield, J. P. Day, S. C. Smith, J. E. McGonigle, [et al.] // PLoS Pathog. – 2015. – V.11. – N. 3. -- e1004728.

Merson, M.H. The history and challenge of HIV prevention [Text] / M. H. Merson, J. O’Malley, D. Serwadda, C. Apisuk // Lancet. – 2008 – V. 372. – P. 475–488.

Delaugerre, C. HIV-1 group N: Travelling beyond Cameroon [Text] / C. Delaugerre, F. De Oliveira, C. Lascoux-Combe, J. C. Plantier, F. Simon // Lancet. – 2011. – P. 378. – P. 1894.

Peeters, M. Geographical distribution of HIV-1 group O viruses in Africa [Text] / M. Peeters, A. Gueye, S. Mboup, [et al.] // AIDS. – 1997. -- V. 11. – P. 493–498.

Kluge, S.F. Nef proteins of epidemic HIV-1 group O strains antagonize human tetherin [Text] / S. F. Kluge, K. Mack, S. S. Iyer [et al.] // Cell Host Microbe. – 2014. -- V. 16. – P. 639–650.

Plantier, J-C. A new human immunodeficiency virus derived from gorillas [Text] / J-C. Plantier, M. Leoz, J. E. Dickerson, [et al.] // Nat. Med. – 2009. – V. 15. -- V. 871–872.

Vallari, A. Confirmation of putative HIV-1 group P in Cameroon [Text] / A. Vallari, Holzmayer V, Harris B, [et al.] // J. Virol. 2011. – V. 85. – P. 1403–1407.

Worobey M. Direct evidence of extensive diversity of HIV-1 in Kinshasa by 1960 [Text] / M. Worobey, M. Gemmel, D. E. Teuwen , [et al.] // Nature. – 2008. – V.455. -- P. 661–664.

Faria, N.R. HIV epidemiology. The early spread and epidemic ignition of HIV-1 in human populations [Text] / N. R. Faria, A. Rambaut, M. A. Suchard [et al.] // Science – 2014. – V.346. – P. 56–66.

Bailes, E. Hybrid origin of SIV in chimpanzees [Text] / E. Bailes, F. Gao, F. Bibollet-Ruche [et al.] // Science. – 2003. – V. 300.-- P. 1713.

Keele, B.F. Chimpanzee reservoirs of pandemic and nonpandemic HIV-1 [Text] / B. F. Keele, F. Van Heuverswyn, Y. Li, [et al.] // Science. -- 2006. – V. 313. – P. 523–526.

Van Heuverswyn, F. Human immunodeficiency viruses: SIV infection in wild gorillas [Text] / F. Van Heuverswyn, Y. Li, C. Neel, [et al.] // Nature. – 2006. – V. 444. – P.164.

D'arc, M. Origin of the HIV-1 group O epidemic in western lowland gorillas [Text] / M. D'arc, A. Ayouba, A. Esteban, [et al.] // Proc. Nat.l Acad. Sci. U S A. – 2015. -- V.112. – E1343-1352.

Reeves, J. D. Human Immunodeficiency Virus Type 2 [Text] / J. D. Reeves, R. W. Doms // J. Gen. Virol. 2002. – V. 83. – P. 1253–1265.

Demma, L.J. SIV quasispecies adaptation to a simian new host [Text] / L. J. Demma, J. M. J. Logsdon, T. H. Vanderford, M. B. Feinberg, S. I. Staprans // PLoS Path. – 2005. – P. 1. -- e3.

Demma, L.J. Evolution of the uniquely adaptable lentiviral envelope in a natural reservoir host [Text] / L. J. Demma, T. H. Vanderford, J. M. Logsdon, M. B. Feinberg, S. I. Staprans // Retrovirology– 2006. – V. 203. – P. 19.

Wain, L.V. Adaptation of HIV-1 to its human host [Text] / L. V. Wain, E. Bailes, F. Bibollet-Ruche, [et al.] // Mol. Biol. Evol. – 2007. -- V. 24. -- P. 1853–1860.

Bibollet-Ruche, F. Efficient SIVcpz replication in human lymphoid tissue requires viral matrix protein adaptation [Text] / F. Bibollet-Ruche, A. Heigele, B. F. Keele, [et al.] // J. Clin. Invest. – 2012 – V. 122. – P. 1644–1652.

Li, H. High Multiplicity Infection by HIV-1 in men who have sex with men [Text] / H. Li, K. J. Bar, S. Wang, J. M. Decker, [et al.] // PLoS Pathog.-- 2010. – V. 6. -- e1000890.

Streeck, H. Immune-driven recombination and loss of control after HIV superinfection [Text] / H. Streeck,; B. Li, A. F. Poon, A. Schneidewind, A. D. Gladden, [et al.] // J. Exp. Med. – 2008. – V. 205. – P. 1789–1796.

Gundlach, B.R. Evidence for recombination of live, attenuated immunodeficiency virus vaccine with challenge virus to a more virulent strain [Text] / B. R. Gundlach, M. G. Lewis, S. Sopper, T. Schnell, J. Sodroski, [et al.] // J. Virol. – 2000. – V. 74, 3537–3542.

Kalish, M.L. Central African hunters exposed to simian immunodeficiency virus [Text] / M. L. Kalish, N. D. Wolfe, C. D. Ndongmo, J. McNicholl, K. E. Robbins, [et al.] // Emerg. Infect. Dis. 2005. – V. 11. – P. 1928–1930.

Chitnis, A. Origin of HIV Type 1 in Colonial French Equatorial Africa? [Text] / A. Chitnis, D. Rawls, J. Moore // AIDS Research and Human Retroviruses –2000. – V. 16. – P. 5–8.

Olsen, B. Global patterns of influenza a virus in wild birds [Text] / B. Olsen, V. J. Munster, A. Wallensten, J. Waldenstrom, A. D. Osterhaus, [et al.] // Science. – 2006 .—V.312. – P. 384–388.

Taubenberger, J.K. 1918 Influenza: the mother of all pandemics [Text] / J. K. Taubenberger, D. M. Morens // Emerg. Infec. Dis. – 2006. – V. 12. – P. 15–22.

Kilbourne, E.D. Influenza pandemics of the 20th century [Text] / E. D. Kilbourne // Emerg. Infect. Dis. –2006. – V.12. – P. 9–14.

Dawood, F.S. Emergence of a novel swine-origin influenza A (H1N1) virus in humans [Text] / F. S. Dawood, S. Jain, L. Finelli, [et al.] // N. Engl. J. Med. – 2009. – V. 360. – P. 2605–2615.

Taubenberger, J.K. Characterization of the 1918 influenza virus polymerase genes [Text] / J. K. Taubenberger, A. H. Reid, R. M. Lourens, R. Wang, G. Jin, T.G. Fanning // Nature. -- 2005. – V.437. – P. 889–893.

Tumpey, T.M. Characterization of the reconstructed 1918 Spanish influenza pandemic virus [Text] / T. M. Tumpey, C. F. Basler, P. V.Aguilar, H. Zeng, A. Solorzano, [et al.] // Science. -- 2005. – V. 310. – P. 77–80.

Worobey, M. Genesis and pathogenesis of the 1918 pandemic H1N1 influenza A virus [Text] / M. Worobey, G.-Z. Han, A. Rambaut // Proc. Natl. Acad. Sci. U S A. – 2014 – V. 111. – P.8107-8112.

Scholtissek, C. On the origin of the human influenza virus subtypes H2N2 and H3N2 [Text] / C. Scholtissek, W. Rohde, V. von Hoyningen, R. Rott // Virology. – 1978. – V. 87. – P. 13–20.

Garten, R.J. Antigenic and genetic characteristics of swine-origin A(H1N1) influenza viruses circulating in humans [Text] / R. J. Garten, C. T. Davis, C. A. Russell, [et al.] // Science. –2009. – V. 325 – P.197–201.

de Jong, J.C. A pandemic warning? [Text] / J. C. de Jong, E. C. Claas, A. D. Osterhaus, R. G. Webster, W. L. Lim // Nature. – 1997. – V. 389. – P. 554.

Wang, H. Probable limited person-to-person transmission of highly pathogenic avian influenza A (H5N1) virus in China [Text] / H. Wang, Z. Feng, Y. Shu [et al.] // Lancet. – 2008. – V. 371. – P. 1427–1434.

Hatchette, T.F. Influenza A viruses in feral Canadian ducks: extensive reassortment in nature [Text] / T. F. Hatchette, D. Walker, C. Johnson, A. Baker, S. P. Pryor, R. G.Webster // J. Gen. Virol. – 2004. -- V. 85. -- Pt 8. – P. 2327–2337.

Schrauwen, E.J. Host adaptation and transmission of influenza A viruses in mammals [Text] / E. J. Schrauwen, R. A.Fouchier // Emerg. Microbes. Infect. – 2014. – V. 3. – e.9.

Lam, T.T. The genesis and source of the H7N9 influenza viruses causing human infections in China [Text] / T. T. Lam, J. Wang, Y. Shen [et al.] // Nature. – 2013. – V. 502. – P. 241–244.

Cleri, D. J. Severe acute respiratory syndrome (SARS) [Text] / D. J. Cleri, A. J. Ricketti, J. R. Vernaleo // Infect. Dis. Clin. North. Am. – 2010. – V. 24. – P.175–202.

Song, H.D. Cross-host evolution of severe acute respiratory syndrome coronavirus in palm civet and human [Text] / H. D. Song, C. C. Tu, G. W. Zhang, S. Y. Wang, K. Zheng, L. C. Lei, [et al.] // Proc. Natl. Acad. Sci. U S A. – 2005. – V. 102. – P.2430–2435.

Zheng, B. J. SARS-related virus predating SARS outbreak, Hong Kong [Text] / B. J. Zheng, K. H. Wong, J. Zhou, K. L. Wong, B. W. Young, L. W. Lu, S. S. Lee. // Emerg. Infect. Dis.-- 2004. -- V. 10. – P.176–178.

Guan, Y. Isolation and characterization of viruses related to the SARS coronavirus from animals in southern China [Text] / Y. Guan, B. Zheng, Y. He, X. Liu, Z. Zhuang, [et al.] // Science.—2003. – V. 302. – P. 276–278.

Wu, D. Civets are equally susceptible to experimental infection by two different severe acute respiratory syndrome coronavirus isolates [Text] / D. Wu, C. Tu, C. Xin, H. Xuan, Q. Meng, Y. [et al.] // J. Virol. -- 2005. – V.79. – P. 2620–2625.

Liang, G. Laboratory diagnosis of four recent sporadic cases of community-acquired SARS, Guangdong province, China [Text] / G. Liang, Q. Chen, J. Xu, Y. Liu, W. Lim, J. S. Peiris, L. J. Anderson, [et al.] // Emerg. Infect. Dis. --2004. – 10. – P.1774–1781.

Kan, B. Molecular evolution analysis and geographic investigation of severe acute respiratory syndrome coronavirus-like virus in palm civets at an animal market and on farms [Text] / B. Kan, M. Wang, H. Jing, H. Xu, X. Jiang, M. Yan, [et al.] // J. Virol. – 2005. –V.79. – P.11892–11900.

Poon, L.L. Identification of a novel coronavirus in bats [Text] / L. L. Poon, D. K. Chu, K. H. Chan, O. K. Wong, T. M. Ellis, Y. H. Leung, [et al.] // J. Virol. – 2005. – V. 79. -- P. 2001–2009.

Li, W. Bats are natural reservoirs of SARS-like coronaviruses [Text] / W. Li, Z. Shi, M. Yu, W. Ren, C. Smith, J. H. Epstein, [et al.] // Science. – 2005. -- V.310. -- P. 676–679.

Ge, X.Y. Isolation and characterization of a bat SARS-like coronavirus that uses the ACE2 receptor [Text] / X. Y. Ge, J. L. Li, X. L. Yang, A. A. Chmura, G. Zhu, [et al.] // Nature.—2013. – V.503. – P. 535–538.

Graham, R. L. Recombination, reservoirs, and the modular spike: mechanisms of coronavirus cross-species transmission [Text] / R. L. Graham, R. S. Baric // J. Virol.-- 2010. – V. 84. – P. 3134–3146.

Li, F. Structure of SARS coronavirus spike receptor-binding domain complexed with receptor [Text] / F. Li, W. Li, M. Farzan, S. C. Harrison. // Science. --2005. – V. 309. – P. 1864–1868.

Bolles, M. SARS-CoV and emergent coronaviruses: viral determinants of interspecies transmission [Text] / M. Bolles, E. Donaldson, R. Baric // Curr. Opin. Virol. – 2011. – V. 6. -- Р. 624-634.

Lau, S.K. Severe Acute Respiratory Syndrome (SARS) coronavirus ORF8 protein is acquired from SARS-related coronavirus from greater horseshoe bats through recombination [Text] / S. K. Lau, Y. Feng, H. Chen, H. K. Luk, W. H. Yang, [et al.] // J. Virol. – 2015. – V. 89. -- 10532–10547.

Oostra, M. The 29-nucleotide deletion present in human but not in animal severe acute respiratory syndrome coronaviruses disrupts the functional expression of open reading frame 8 [Text] / M. Oostra, C. A. de Haan, P. J. Rottier // J. Virol. –2007. -- V. 81. -- Р.13876–13888.

Paessler, S. Pathogenesis of the viral hemorrhagic fevers [Text] / S. Paessler, D. H. Walker // Annu. Rev. Pathol. – 2013. – V. 8. – P.411–440.

Lefebvre, A. Case fatality rates of Ebola virus diseases: a meta-analysis of World Health Organization data [Text] / A. Lefebvre, C. Fiet, C. Belpois-Duchamp, M. Tiv, K. Astruc, [et al.] // Med. Mal. Infect. -- 2014 – V. 44. – P. 412–416.

Leroy, E.M. Human asymptomatic Ebola infection and strong inflammatory response [Text] / E. M. Leroy, S. Baize, V. E. Volchkov, S. P. Fisher-Hoch, M. C. Georges-Courbot, [et al.] // Lancet. -2000 -- V.355. – P. 2210–2215.

Becquart, P. High prevalence of both humoral and cellular immunity to Zaire ebolavirus among rural populations in Gabon [Text] / P. Becquart, N. Wauquier, T. Mahlakoiv, D. Nkoghe, C. Padilla, [et al.] // PLoS One. -- 2010. -- V. 5. – e. 9126.

de La Vega, M-A. Ebolavirus Evolution: Past and Present [Text] / M-A. de La Vega, D. Stein, G. P. Kobinger // PloS Pathog. -- 2015. -- V. 11. – e1005221.

He, B. Filovirus RNA in fruit bats, China [Text] / B. He, Y. Feng, H. Zhang, L. Xu, W. Yang, [et al.] // Emerg. Infect. Diseases-- 2015. -- V.21. –P. 1675–1677.

Negredo, A. Discovery of an ebolavirus-like filovirus in Europe [Text] / A. Negredo, G. Palacios, S. Vazquez-Moron, F. Gonzalez, H. Dopazo, [et al.] // PLoS Pathog. -- 2011. -- V. 7. -- e1002304.

Olival, K.J. Filoviruses in bats: current knowledge and future directions [Text] / K. J. Olival, D. T. Hayman // Viruses. -- 2014. – V. 6 . – P. 1759–1788.

Bermejo, M. Ebola outbreak killed 5000gorillas [Text] / M. Bermejo, J. D. Rodriguez-Teijeiro, G. Illera, A. Barroso, C. Vila, [et al.] // Science. – 2006. -- V.314. – P. 1564.

Lahm, S.A. Morbidity and mortality of wild animals in relation to outbreaks of Ebola haemorrhagic fever in Gabon, 1994–2003 [Text] / S. A. Lahm, M. Kombila, R. Swanepoel, R. F. Barnes // Trans. R. Soc. Trop. Med. Hyg. – 2007. – 101. – P. 64–78.

Pourrut, X. The natural history of Ebola virus in Africa[Text] / X. Pourrut, B. Kumulungui, T. Wittmann, G. Moussavou, A. Delicat, [et al.] // Microbes Infect. – 2005. – V. 7. – P. 1005–1014.

Wittmann, T.J. Isolates of Zaire ebolavirus from wild apes reveal genetic lineage and recombinants [Text] / T. J. Wittmann, R. Biek, A. Hassanin, P. Rouquet, P. Reed, [et al.] // Proc. Natl. Acad. Sci. USA. – 2007. -- V. 104. – P. 17123–17127.

Jun, S.R. Ebolavirus comparative genomics [Text] / S. R. Jun, M. R. Leuze, I. Nookaew, E. C. Uberbacher, M. Land, Q. Zhang, [et al.] // FEMS Microbiol. Rev. – 2015. -- V. 39. – P. 764-778.

Simon-Loriere, E. Distinct lineages of Ebola virus in Guinea during the 2014 West African epidemic [Text] / E. Simon-Loriere, O. Faye, O. Faye, [et al.] // Nature. –2015. – V. 524. -- P. 102–104.

Shabman, R. S. Deep sequencing identifies noncanonical editing of Ebola and Marburg virus RNAS in infected cells [Text] / R. S. Shabman, O. J. Jabado, C. E. Mire, [et al.] // mBio. – 2014. – V. 5. -- e02011.

Park, D.J. Ebola Virus Epidemiology, Transmission, and Evolution during Seven Months in Sierra Leone [Text] / D. J. Park, G. Dudas, S. Wohl, A. Goba, [et al.] // Cell. – 2015. – V. 161. -- P. 1516-1526.

Tong, Y.-G. Genetic diversity and evolutionary dynamics of Ebola virus in Sierra Leone [Text] / Y.-G. Tong, W.-F. Shi, Di Liu, J. Qian, L. Liang, [et al.] China Mobile Laboratory Testing Team in Sierra Leone // Nature. -- 2015. – V. 524. – P. 93-96.