Molecular Comparison and Evolutionary Analyses of VP1 Nucleotide Sequences of New African Human Enterovirus 71 Isolates Reveal a Wide Genetic Diversity
Most circulating strains of Human enterovirus 71 (EV-A71) have been classified primarily into three genogroups (A to C) on the basis of genetic divergence between the 1D gene, which encodes the VP1 capsid protein. The aim of the present study was to provide further insights into the diversity of the EV-A71 genogroups following the recent description of highly divergent isolates, in particular those from African countries, including Madagascar. We classified recent EV-A71 isolates by a large comparison of 3,346 VP1 nucleotidic sequences collected from GenBank. Analysis of genetic distances and phylogenetic investigations indicated that some recently-reported isolates did not fall into the genogroups A-C and clustered into three additional genogroups, including one Indian genogroup (genogroup D) and 2 African ones (E and F). Our Bayesian phylogenetic analysis provided consistent data showing that the genogroup D isolates share a recent common ancestor with the members of genogroup E, while the isolates of genogroup F evolved from a recent common ancestor shared with the members of the genogroup B. Our results reveal the wide diversity that exists among EV-A71 isolates and suggest that the number of circulating genogroups is probably underestimated, particularly in developing countries where EV-A71 epidemiology has been poorly studied.
References
[1]
McMinn PC (2012) Recent advances in the molecular epidemiology and control of human enterovirus 71 infection. Curr Opin Virol 2: 199–205. doi: 10.1016/j.coviro.2012.02.009
[2]
Abzug MJ (2009) Enterovirus 71: emergence of the new poliomyelitis. South Afr J Epidemiol Infect 24: 5–8.
[3]
Ooi MH, Wong SC, Lewthwaite P, Cardosa MJ, Solomon T (2010) Clinical features, diagnosis, and management of enterovirus 71. Lancet Neurol 9: 1097–1105. doi: 10.1016/s1474-4422(10)70209-x
[4]
Solomon T, Lewthwaite P, Perera D, Cardosa MJ, McMinn P, et al. (2010) Virology, epidemiology, pathogenesis, and control of enterovirus 71. Lancet Infect Dis 10: 778–790. doi: 10.1016/s1473-3099(10)70194-8
[5]
Li YP, Liang ZL, Xia JL, Wu JY, Wang L, et al.. (2013) Immunogenicity, Safety, and Immune persistence of A Novel Inactivated Human Enterovirus 71 (EV71) Vaccine: A Phase II, Randomized, Double-Blind, Placebo-Controlled trial. J Infect Dis.
[6]
Zhu FC, Meng FY, Li JX, Li XL, Mao QY, et al. (2013) Efficacy, safety, and immunology of an inactivated alum-adjuvant enterovirus 71 vaccine in children in China: a multicentre, randomised, double-blind, placebo-controlled, phase 3 trial. Lancet 381: 2024–2032. doi: 10.1016/s0140-6736(13)61049-1
[7]
Oberste MS, Maher K, Kilpatrick DR, Pallansch MA (1999) Molecular evolution of the human enteroviruses: correlation of serotype with VP1 sequence and application to picornavirus classification. J Virol 73: 1941–1948.
[8]
Kottaridi C, Bolanaki E, Siafakas N, Markoulatos P (2005) Evaluation of seroneutralization and molecular diagnostic methods for echovirus identification. Diagn Microbiol Infect Dis 53: 113–119. doi: 10.1016/j.diagmicrobio.2005.06.016
[9]
Mirand A, Henquell C, Archimbaud C, Ughetto S, Antona D, et al. (2012) Outbreak of hand, foot and mouth disease/herpangina associated with coxsackievirus A6 and A10 infections in 2010, France: a large citywide, prospective observational study. Clin Microbiol Infect 18: E110–118. doi: 10.1111/j.1469-0691.2012.03789.x
[10]
Oberste MS, Maher K, Kilpatrick DR, Flemister MR, Brown BA, et al. (1999) Typing of human enteroviruses by partial sequencing of VP1. J Clin Microbiol 37: 1288–1293.
[11]
Brown BA, Oberste MS, Alexander JP Jr, Kennett ML, Pallansch MA (1999) Molecular epidemiology and evolution of enterovirus 71 strains isolated from 1970 to 1998. J Virol 73: 9969–9975.
[12]
Yu H, Chen W, Chang H, Tang R, Zhao J, et al. (2010) Genetic analysis of the VP1 region of enterovirus 71 reveals the emergence of genotype A in central China in 2008. Virus Genes 41: 1–4. doi: 10.1007/s11262-010-0472-9
[13]
Zhu J, Luo Z, Wang J, Xu Z, Chen H, et al. (2013) Phylogenetic Analysis of Enterovirus 71 Circulating in Beijing, China from 2007 to 2009. PLoS One 8: e56318. doi: 10.1371/journal.pone.0056318
[14]
Deshpande JM, Nadkarni SS, Francis PP (2003) Enterovirus 71 isolated from a case of acute flaccid paralysis in India represents a new genotype. Current Science 84: 1350–1353.
[15]
Bessaud M, Pillet S, Ibrahim W, Joffret ML, Pozzetto B, et al. (2012) Molecular Characterization of Human Enteroviruses in the Central African Republic: Uncovering of Wide Diversity and Identification of a New Human Enterovirus A71 Genogroup. J Clin Microbiol 50: 1650–1658. doi: 10.1128/jcm.06657-11
[16]
Sadeuh-Mba SA, Bessaud M, Massenet D, Joffret ML, Endegue MC, et al. (2013) High frequency and diversity of species C enteroviruses in cameroon and neighboring countries. J Clin Microbiol 51: 759–770. doi: 10.1128/jcm.02119-12
[17]
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, et al. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28: 2731–2739. doi: 10.1093/molbev/msr121
[18]
Lole KS, Bollinger RC, Paranjape RS, Gadkari D, Kulkarni SS, et al. (1999) Full-length human immunodeficiency virus type 1 genomes from subtype C-infected seroconverters in India, with evidence of intersubtype recombination. J Virol 73: 152–160.
[19]
Drummond AJ, Ho SY, Phillips MJ, Rambaut A (2006) Relaxed phylogenetics and dating with confidence. PLoS Biol 4: e88. doi: 10.1371/journal.pbio.0040088
[20]
Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7: 214. doi: 10.1186/1471-2148-7-214
[21]
Shapiro B, Rambaut A, Drummond AJ (2006) Choosing appropriate substitution models for the phylogenetic analysis of protein-coding sequences. Mol Biol Evol 23: 7–9. doi: 10.1093/molbev/msj021
[22]
Drummond AJ, Rambaut A, Shapiro B, Pybus OG (2005) Bayesian coalescent inference of past population dynamics from molecular sequences. Mol Biol Evol 22: 1185–1192. doi: 10.1093/molbev/msi103
[23]
Minin VN, Bloomquist EW, Suchard MA (2008) Smooth skyride through a rough skyline: Bayesian coalescent-based inference of population dynamics. Mol Biol Evol 25: 1459–1471. doi: 10.1093/molbev/msn090
[24]
Kass R, A R (1995) Bayes factors and model uncertainly. J Am Stat Assoc 90: 773–795.
Shih SR, Ho MS, Lin KH, Wu SL, Chen YT, et al. (2000) Genetic analysis of enterovirus 71 isolated from fatal and non-fatal cases of hand, foot and mouth disease during an epidemic in Taiwan, 1998. Virus Research 68: 127–136. doi: 10.1016/s0168-1702(00)00162-3
[27]
Bessaud M, Joffret ML, Holmblat B, Razafindratsimandresy R, Delpeyroux F (2011) Genetic relationship between cocirculating Human enteroviruses species C. PLoS One. 6: e24823. doi: 10.1371/journal.pone.0024823
[28]
Bouslama L, Nasri D, Chollet L, Belguith K, Bourlet T, et al. (2007) Natural recombination event within the capsid genomic region leading to a chimeric strain of human enterovirus B. J Virol. 81: 8944–8952. doi: 10.1128/jvi.00180-07
[29]
Lukashev AN, Lashkevich VA, Ivanova OE, Koroleva GA, Hinkkanen AE, et al. (2005) Recombination in circulating Human enterovirus B: independent evolution of structural and non-structural genome regions. J Gen Virol 86: 3281–3290. doi: 10.1099/vir.0.81264-0
[30]
Oberste MS, Penaranda S, Pallansch MA (2004) RNA recombination plays a major role in genomic change during circulation of coxsackie B viruses. J Virol 78: 2948–2955. doi: 10.1128/jvi.78.6.2948-2955.2004
[31]
Simmonds P, Welch J (2006) Frequency and dynamics of recombination within different species of human enteroviruses. J Virol 80: 483–493. doi: 10.1128/jvi.80.1.483-493.2006
[32]
Rao CD, Yergolkar P, Shankarappa KS (2012) Antigenic diversity of enteroviruses associated with nonpolio acute flaccid paralysis, India, 2007–2009. Emerg Infect Dis 18: 1833–1840. doi: 10.3201/eid1811.111457
[33]
Combelas N, Holmblat B, Joffret ML, Colbere-Garapin F, Delpeyroux F (2011) Recombination between poliovirus and coxsackie A viruses of species C: a model of viral genetic plasticity and emergence. Viruses 3: 1460–1484. doi: 10.3390/v3081460
[34]
Lukashev AN (2010) Recombination among picornaviruses. Rev Med Virol 20: 327–337. doi: 10.1002/rmv.660
[35]
Yip CC, Lau SK, Lo JY, Chan KH, Woo PC, et al. (2013) Genetic characterization of EV71 isolates from 2004 to 2010 reveals predominance and persistent circulation of the newly proposed genotype D and recent emergence of a distinct lineage of subgenotype C2 in Hong Kong. Virol J 10: 222. doi: 10.1186/1743-422x-10-222
[36]
Tee KK, Lam TT, Chan YF, Bible JM, Kamarulzaman A, et al. (2010) Evolutionary genetics of human enterovirus 71: origin, population dynamics, natural selection, and seasonal periodicity of the VP1 gene. J Virol 84: 3339–3350. doi: 10.1128/jvi.01019-09
[37]
van der Sanden S, van der Avoort H, Lemey P, Uslu G, Koopmans M (2010) Evolutionary trajectory of the VP1 gene of human enterovirus 71 genogroup B and C viruses. J Gen Virol 91: 1949–1958. doi: 10.1099/vir.0.019695-0
[38]
Mirand A, Schuffenecker I, Henquell C, Billaud G, Jugie G, et al. (2010) Phylogenetic evidence for a recent spread of two populations of human enterovirus 71 in European countries. J Gen Virol 91: 2263–2277. doi: 10.1099/vir.0.021741-0
