Role of recombination in evolution of enteroviruses
Corresponding Author
Alexander N. Lukashev
Chumakov Institute of Poliomyelitis and Viral Encephalitides RAMS, Moscow, Russia
Russia, 142782, Moscow Region, p/o Institut Poliomielita, Institute of Poliomyelitis and Viral Encephalitides.Search for more papers by this authorCorresponding Author
Alexander N. Lukashev
Chumakov Institute of Poliomyelitis and Viral Encephalitides RAMS, Moscow, Russia
Russia, 142782, Moscow Region, p/o Institut Poliomielita, Institute of Poliomyelitis and Viral Encephalitides.Search for more papers by this authorAbstract
Enteroviruses, members of the Picornaviridae family, comprise a large (over 70 serotypes) group of viruses that are ubiquitous in nature, infect different species and cause a wide range of diseases. Human enteroviruses were recently classified into five species, human enterovirus A–D and poliovirus. Recombination has long been known to be an important property of poliovirus genetics. Recently, several publications demonstrated that recombination is extremely frequent also in non-polio enteroviruses, and allows independent evolution of enterovirus genome fragments even on a microevolutionary scale. Prototype enterovirus strains were shown to have complex phylogenetic relations, and almost all modern enterovirus isolates turned out to be recombinants compared with the prototype strains. Recombination takes place strictly between members of the same species, and usually spares the capsid-encoding genome region. Therefore, it can be concluded that the enterovirus species exist as a worldwide reservoir of genetic material comprising a limited quantity of capsid gene sets defining a finite number of serotypes and a range of non-structural genes that recombine frequently to produce new virus variants. This new model of enterovirus genetics helps to explain the failure of previous attempts to connect serotype and disease profile in non-polio enteroviruses, and seriously questions existing typing approaches that are based solely on the capsid-encoding genome region. It remains to be determined what role recombination plays in the emergence of new enterovirus variants and in the macroevolution of animal enteroviruses and viruses of the picorna-like supergroup. Copyright © 2004 John Wiley & Sons, Ltd.
REFERENCES
- 1 Racaniello VR. Picornaviridae: the viruses and their replication. In Fields Virology, 4th edn, DM Knipe, PM Howley (eds). Lippincott-Raven: Philadelphia, 2001; 685–723.
- 2 Pallansch MA, Roos RP. Enteroviruses: polioviruses, coxsackieviruses, echoviruses and newer enteroviruses. In Fields Virology, 4th edn, DM Knipe, PM Howley (eds). Lippincott-Raven: Philadelphia, 2001; 723–775.
- 3 Akerblom HK, Vaarala O, Hyoty H, Ilonen J, Knip M. Environmental factors in the etiology of type 1 diabetes. Am J Med Genet 2002; 115: 18–29.
- 4 Lashkevich VA, Koroleva GA, Lukashev AN, Denisova EV, Katargina LA. Enterovirus uveitis. Rev Med Virol 2004; 14: 241–254.
- 5 Melnick JL, Rennick V, Hampil B, Schmidt NJ, Ho HH. Lyophilized combination pools of enterovirus equine antisera: Preparation and test procedures for the identification of field strains of 42 enteroviruses. Bull World Health Organ 1973; 48: 263–268.
- 6 Caro V, Guillot S, Delpeyroux F, Crainic R. Molecular strategy for ‘serotyping’ of human enteroviruses. J Gen Virol 2001; 82: 79–91.
- 7 Oberste MS, Maher K, Kilpatrick DR, Flemister MR, Brown BA, Pallansch MA. Typing of human enteroviruses by partial sequencing of VP1. J Clin Microbiol 1999; 37: 1288–1293.
- 8 Ledinko N. Genetic recombination with poliovirus type 1: studies of crosses between a normal horse-serum resistant mutant and several guanidine-resistant mutants of the same strain. Virology 1963; 20: 107–119.
- 9 Hirst GK. Genetic recombination with Newcastle disease virus, polioviruses and influenza. In Cold Spring Harbor Symposia on Quantitative Biology. 1962.
- 10 Sergiescu D, Horodniceanu F, Klein R, Crainic R. Genetic transfer of guanidine resistance from type 2 to type 1 poliovirus. Arch Gesamte Virusforsch 1966; 18: 231–243.
- 11 Cooper PD, Geissler E, Tannock GA. Attempts to extend the genetic map of poliovirus temperature-sensitive mutants. J Gen Virol 1975; 29: 109–120.
- 12 Cooper PD. A genetic map of poliovirus temperature-sensitive mutants. Virology 1968; 35: 584–596.
- 13 Romanova LI, Tolskaya EA, Kolesnikova MS, Agol VI. Biochemical evidence for intertypic genetic recombination of polioviruses. FEBS Lett 1980; 118: 109–112.
- 14 Tolskaya EA, Romanova LA, Kolesnikova MS, Agol VI. Intertypic recombination in poliovirus: genetic and biochemical studies. Virology 1983; 124: 121–132.
- 15 Romanova LA, Blinov VM, Tolskaya EA, et al. The primary structure of crossover regions of intertypic poliovirus recombinants: a model of recombination between RNA genomes. Virology 1986; 155: 202–213.
- 16 Tolskaya EA, Romanova LA, Blinov VM, et al. Studies on the recombination between RNA genomes of poliovirus: the primary structure and nonrandom distribution of crossover regions in the genomes of intertypic poliovirus recombinants. Virology 1987; 161: 54–61.
- 17 Agol VI, Drozdov SG, Grachev VP, et al. Recombinants between attenuated and virulent strains of poliovirus type 1: derivation and characterization of recombinants with centrally located crossover points. Virology 1985; 143: 467–477.
- 18 Agol VI, Grachev VP, Drosdov SG, et al. Construction and properties of intertypic poliovirus recombinants: first approximation mapping of the major determinants of neurovirulence. Virology 1984; 136: 41–55.
- 19 Agol VI, Drosdov SG, Frolova MP, et al. Neurovirulence of the intertypic poliovirus recombinant v3/a1-25: characterization of strains isolated from the spinal cord of diseased monkeys and evaluation of contribution of the 3'-half of the genome. J Gen Virol 1985; 65: 309–316.
- 20 Tang RS, Barton DJ, Flanegan JB, Kirkegaard K. Poliovirus RNA recombination in cell-free extracts. RNA 1997; 3: 624–633.
- 21 Duggal R, Cuconati A, Gromeier M, Wimmer E. Genetic recombination of poliovirus in a cell-free system. Proc Natl Acad Sci USA 1997; 94: 13786–13791.
- 22 Jarvis TC, Kirkegaard K. Poliovirus RNA recombination: mechanistic studies in the absence of selection. EMBO J 1992; 11: 3135–3145.
- 23 Kirkegaard K, Baltimore D. The mechanism of RNA recombination in poliovirus. Cell 1986; 47: 433–443.
- 24 King AM. Preferred sites of recombination in poliovirus RNA: an analysis of 40 intertypic cross-over sequences. Nucleic Acids Res 1988; 16: 11705–11723.
- 25 Pilipenko EV, Gmyl AP, Agol VI. A model for rearrangements in RNA genomes. Nucleic Acid Res 1995; 23: 1870–1875.
- 26 Arnold JJ, Cameron CE. Poliovirus RNA-dependent RNA polymerase (3Dpol) is sufficient for template switching in vitro. J Biol Chem 1999; 274: 2706–2716.
- 27 Gmyl AP, Belousov EV, Maslova SV, Khitrina EV, Chetverin AB, Agol VI. Nonreplicative RNA recombination in poliovirus. J Virol 1999; 73: 8958–8965.
- 28 Gmyl AP, Korshenko SA, Belousov EV, Khitrina EV, Agol VI. Nonreplicative homologous RNA recombination: promiscuous joining of RNA pieces? RNA 2003; 9: 1221–1231.
- 29 Georgescu M-M, Delpeyroux F, Crainic R. Tripartite organization of a natural type 2 vaccine/nonvaccine recombinant poliovirus. J Gen Virol 1995; 76: 2343–2348.
- 30 Martin J, Samoilovich E, Dunn G, et al. Isolation of an intertypic poliovirus capsid recombinant from a child with vaccine-associated paralytic poliomyelitis. J Virol 2002; 76: 10921–10928.
- 31 Blomquist S, Bruu AL, Stenvik M, Hovi T. Characterization of a recombinant type 3/type 2 poliovirus isolated from a healthy vaccinee and containing a chimeric capsid protein VP1. J Gen Virol 2003; 84: 573–580.
- 32 Duggal R, Wimmer E. Genetic recombination of poliovirus in vitro and in vivo: temperature-dependent alteration of crossover sites. Virology 1999; 258: 30–41.
- 33 Cammack N, Phillips A, Dunn G, Patel V, Minor PD. Intertypic genomic rearrangements of poliovirus strains in vaccinees. Virology 1988; 167: 507–514.
- 34 Minor PD, John A, Ferguson M, Icenogle JP. Antigenic and molecular evolution of the vaccine strain of type 3 poliovirus during the period of excretion by primary vaccinee. J Gen Virol 1986; 67: 693–706.
- 35 Cuervo N, Guillot S, Romanenkova N, et al. Genomic features of intertypic recombinant Sabin poliovirus strains excreted by primary vaccinees. J Virol 2001; 75: 5740–5751.
- 36 Furione M, Guillot S, Otelea D, Balanant J, Candrea A, Crainic R. Polioviruses with natural recombinant genomes isolated from vaccine-associated paralytic poliomyelitis. Virology 1993; 196: 199–208.
- 37 Lipskaya GI, Muzychenko AR, Kutitova OK, et al. Frequent isolation of intertypic poliovirus recombinants with serotype 2 specificity from vaccine-associated polio cases. J Med Virol 1991; 35: 290–296.
- 38 Georgopoulou A, Markoulatos P. Sabin type 2 polioviruses with intertypic vaccine/vaccine recombinant genomes. Eur J Clin Microbiol Infect Dis 2001; 20: 792–799.
- 39 Macadam AJ, Arnold C, Howlett J, et al. Reversion of the attenuated and temperature-sensitive phenotypes of the Sabin type 3 strain of poliovirus in vaccinees. Virology 1989; 172: 408–414.
- 40 Guillot S, Caro V, Cuervo N, et al. Natural genetic exchanges between vaccine and wild poliovirus strains in humans. J Virol 2000; 74: 8434–8443.
- 41 Li J, Zhang LB, Yoneyama T, et al. Genetic basis of the neurovirulence of type 1 polioviruses isolated from vaccine-associated paralytic patients. Arch Virol 1996; 141: 1047–1054.
- 42 Liu HM, Zheng DP, Zhang LB, Oberste MS, Kew OM, Pallansch MA. Serial recombination during circulation of type 1 wild-vaccine recombinant polioviruses in China. J Virol 2003; 77: 10994–11005.
- 43 Cherkasova E, Laassri M, Chizhikov V, et al. Microarray analysis of evolution of RNA viruses: evidence of circulation of virulent highly divergent vaccine-derived polioviruses. Proc Natl Acad Sci USA 2003; 100: 9398–9403.
- 44 Rico-Hesse R, Pallansch MA, Nottay BK, Kew OM. Geographic distribution of wild poliovirus type 1 genotypes. Virology 1987; 160: 311–322.
- 45 Dahourou G, Guillot S, Le Gall O, Crainic R. Genetic recombination on wild-type poliovirus. J Gen Virol 2002; 38: 3103–3110.
- 46 Hughes PJ, North C, Minor PD, Stanway G. The complete nucleotide sequence of coxsackievirus A21. J Gen Virol 1989; 70: 2943–2952.
- 47 Andersson P, Edman K, Lindberg AM. Molecular analysis of the echovirus 18 prototype: evidence of interserotypic recombination with echovirus 9. Virus Res 2002; 85: 71–83.
- 48 Santti J, Hyypia T, Kinnunen L, Salminen M. Evidence of recombination among enteroviruses. J Virol 1999; 73: 8741–8749.
- 49 Brown B, Oberste MS, Maher K, Pallansch MA. Complete genomic sequencing shows that polioviruses and members of human enterovirus species C are closely related in the noncapsid coding region. J Virol 2003; 77: 8973–8984.
- 50 Oberste MS, Maher K, Pallansch MA. Evidence for frequent recombination within species human enterovirus B based on complete genomic sequences of all thirty-seven serotypes. J Virol 2004; 78: 855–867.
- 51 Lukashev AN, Lashkevich VA, Ivanova OE, Koroleva GA, Hinkkanen AE, Ilonen J. Recombination in circulating enteroviruses. J Virol 2003; 77: 10423–10431.
- 52 Kopecka H, Brown B, Pallansch M. Genotypic variation in coxsackievirus B5 isolates from three different outbreaks in the United States. Virus Res 1995; 38: 125–136.
- 53 Santti J, Harvala H, Kinnunen L, Hyypia T. Molecular epidemiology and evolution of coxsackievirus A9. J Gen Virol 2000; 81: 1–12.
- 54 Lukashev AN, Lashkevich VA, Koroleva GA, et al. Molecular epidemiology of enteroviruses causing uveitis and multisystem hemorrhagic disease of infants. Virology 2003; 307: 45–53.
- 55 Lukashev AN, Lashkevich VA, Koroleva GA, Ilonen J, Hinkkanen AE. Recombination in uveitis-causing enterovirus strains. J Gen Virol 2004; 85: 463–470.
- 56 Chevaliez S, Szendroi A, Caro V, et al. Molecular comparison of echovirus 11 strains circulating in Europe during an epidemic of multisystem hemorrhagic disease of infants indicates that evolution generally occurs by recombination. Virology 2004; 325: 56–70.
- 57 Norder H, Bjerregaard L, Magnius LO. Open reading frame sequence of an Asian enterovirus 73 strain reveals that the prototype from California is recombinant. J Gen Virol 2002; 83: 1721–1728.
- 58 Chan Y-F, AbuBakar S. Recombinant human enterovirus 71 in hand, foot and mouth disease patients. Emerg Infect Dis 2004; 10: 1468–1470.
- 59 Chua BH, McMinn PC, Lam SK, Chua KB. Comparison of the complete nucleotide sequence of echovirus 7 strain UMMC and the prototype (Wallace) strain demonstrates a significant genetic drift over time. J Gen Virol 2001; 82: 2629–2639.
- 60 Oprisan G, Combiescu M, Guillot S, et al. Natural genetic recombination between co-circulating heterotypic enteroviruses. J Gen Virol 2002; 83: 2193–2200.
- 61 Lindberg MA, Andersson P, Savolainen C, Mulders MN, Hovi T. Evolution of the genome of human enterovirus B: incongruence between phylogenies of the VP1 and 3CD regions indicates frequent recombination within the species. J Gen Virol 2003; 84: 1223–1235.
- 62 Oberste MS, Penaranda S, Pallansch MA. RNA recombination plays a major role in genomic change during circulation of coxsackie B viruses. J Virol 2004; 78: 2948–2955.
- 63 Palacios G, Casas I, Cisterna D, Trallero G, Tenorio A, Freire C. Molecular epidemiology of echovirus 30: temporal circulation and prevalence of single lineages. J Virol 2002; 76: 4940–4949.
- 64 Savolainen C, Hovi T, Mulders M. Molecular epidemiology of echovirus 30 in Europe: succession of dominant sublineages within a single major genotype. Arch Virol 2001; 146: 521–537.
- 65 Oberste MS, Maher K, Kennett ML, et al. Molecular epidemiology and genetic diversity of echovirus type 30 (E30): genotypes correlate with temporal dynamics of E30 isolation. J Clin Microbiol 1999; 37: 3928–3933.
- 66 Wright PW, Strauss GH, Langford MP. Acute hemorrhagic conjunctivitis. Am Fam Physician 1992; 45: 173–178.
- 67 Bell YC, Semler BL, Ehrenfeld E. Requirements for RNA replication of a poliovirus replicon by coxsackievirus B3 RNA polymerase. J Virol 1999; 73: 9413–9421.
- 68 van Kuppeveld FJ, van den Hurk PJ, van der Vliet W, Galama JM, Melchers WJ. Chimeric coxsackie B3 virus genomes that express hybrid coxsackievirus-poliovirus 2B proteins: functional dissection of structural domains involved in RNA replication. J Gen Virol 1997; 78: 1833–1840.
- 69 Dewalt PG, Lawson MA, Colonno RJ, Semler BL. Chimeric picornavirus polyproteins demonstrate a common 3C proteinase substrate specificity. J Virol 1989; 63: 3444–3452.
- 70 Egger D, Bienz K. Recombination of poliovirus RNA proceeds in mixed replication complexes originating from distinct replication start sites. J Virol 2002; 76: 10960–10971.
- 71 Costa-Mattioli M, Di Napoli A, Ferre V, Billaudel S, Perez-Bercoff R, Cristina J. Genetic variability of hepatitis A virus. J Gen Virol 2003; 84: 3191–3201.
- 72 Tosh C, Hemadri D, Sanyal A. Evidence of recombination in the capsid-coding region of type A foot-and-mouth disease virus. J Gen Virol 2002; 83: 2455–2460.
- 73 Tosh C, Mittal M, Sanyal A, Hemadri D, Bandyopadhyay SK. Molecular phylogeny of leader proteinase gene of type A of foot-and-mouth disease virus from India. Arch Virol 2004; 149: 523–536.
- 74 Zhang G, Haydon DT, Knowles NJ, McCauley JW. Molecular evolution of swine vesicular disease virus. J Gen Virol 1999; 80: 639–651.
- 75 Oberste MS, Maher K, Pallansch MA. Molecular phylogeny and proposed classification of the simian picornaviruses. J Virol 2002; 76: 1244–1251.
- 76 Poyry T, Kinnunen L, Hovi T, Hyypia T. Relationships between simian and human enteroviruses. J Gen Virol 1999; 80: 635–638.
- 77 Katayama K, Shirato-Horikoshi H, Kojima S, et al. Phylogenetic analysis of the complete genome of 18 Norwalk-like viruses. Virology 2002; 299: 225–239.
- 78 Vinje J, Green J, Lewis DC, Gallimore CI, Brown DW, Koopmans MP. Genetic polymorphism across regions of the three open reading frames of ‘Norwalk-like viruses’. Arch Virol 2000; 145: 223–241.
- 79 Silbernagel MJ, Mink GI, Zhao RL, Zheng GY. Phenotypic recombination between bean common mosaic and bean common mosaic necrosis potyviruses in vivo. Arch Virol 2001; 146: 1007–1020.
- 80 Glais L, Tribodet M, Kerlan C. Genomic variability in potato potyvirus Y (PVY): evidence that PVY(N)W and PVY(NTN) variants are single to multiple recombinants between PVY(O) and PVY(N) isolates. Arch Virol 2002; 147: 363–378.
- 81 Krause-Sakate R, Fakhfakh H, Peypelut M, et al. A naturally occurring recombinant isolate of lettuce mosaic virus. Arch Virol 2004; 149: 191–197.
- 82 Bousalem M, Dallot S, Fuji S, Natsuaki KT. Origin, world-wide dispersion, bio-geographical diversification, radiation and recombination: an evolutionary history of yam mild mosaic virus (YMMV). Infect Genet Evol 2003; 3: 189–206.
- 83 Tomimura K, Gibbs AJ, Jenner CE, Walsh JA, Ohshima K. The phylogeny of turnip mosaic virus; comparisons of 38 genomic sequences reveal a Eurasian origin and a recent ‘emergence’ in east Asia. Mol Ecol 2003; 12: 2099–2011.
- 84 Paalme V, Gammelgard E, Jarvekulg L, Valkonen JP. In vitro recombinants of two nearly identical potyviral isolates express novel virulence and symptom phenotypes in plants. J Gen Virol 2004; 85: 739–747.
- 85 Gibbs MJ, Weiller GF. Evidence that a plant virus switched hosts to infect a vertebrate and then recombined with a vertebrate-infecting virus. Proc Natl Acad Sci USA 1999; 96: 8022–8027.
- 86 Gromeier M, Wimmer E, Gorbalenya AE. Genetics, pathogenesis and evolution of picornaviruses. In Origin and Evolution of Viruses, E Domingo, R Webster, R Holland (eds). Academic Press: New York, 1999; 287–343.