Recombination in circulating enteroviruses
Open accessAbstract
Recombination is a well-known phenomenon for enteroviruses. However, the actual extent of recombination in circulating nonpoliovirus enteroviruses is not known. We have analyzed the phylogenetic relationships in four genome regions, VP1, 2A, 3D, and the 5′ nontranslated region (NTR), of 40 enterovirus B strains (coxsackie B viruses and echoviruses) representing 11 serotypes and isolated in 1981 to 2002 in the former Soviet Union states. In the VP1 region, strains of the same serotype expectedly grouped with their prototype strain. However, as early as the 2A region, phylogenetic grouping differed significantly from that in the VP1 region and indicated recombination within the 2A region. Moreover, in the 5′ NTR and 3D region, only 1 strain of 40 grouped with its prototype strain. Instead, we observed a major group in both the 5′ NTR and the 3D region that united most (in the 5′ NTR) or all (in the 3D region) of the strains studied, regardless of the serotype. Subdivision within that major group in the 3D region correlated with the time of virus isolation but not with the serotype. Therefore, we conclude that a majority, if not all, circulating enterovirus B strains are recombinants relative to the prototype strains, isolated mostly in the 1950s. Moreover, the ubiquitous recombination has allowed different regions of the enterovirus genome to evolve independently. Thus, a novel model of enterovirus genetics is proposed: the enterovirus genome is a stable symbiosis of genes, and enterovirus species consist of a finite set of capsid genes responsible for different serotypes and a continuum of nonstructural protein genes that seem to evolve in a relatively independent manner.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Recombination between viral RNA genomes is a well-known phenomenon for enteroviruses.
“Recombination between viral RNA genomes is a well-known phenomenon for enteroviruses [28–31].”
From Recombination between Poliovirus and Coxsackie A Viruses of Species C: A Model of Viral Genetic Plasticity and Emergence (2011) · cites this paper as [28]
Similar evolution processes, involving frequent intertypic recombination, have already been described mostly for HEV-B and PVs.
“Similar evolution processes, involving frequent intertypic recombination, have already been described mostly for HEV-B [46–52] and PVs [5,8,53,54].”
From Co-Circulation and Evolution of Polioviruses and Species C Enteroviruses in a District of Madagascar (2007) · cites this paper as [47]
Enterovirus species consist of a finite set of capsid genes responsible for different serotypes and a continuum of nonstructural protein genes that seem to evolve in a relatively independent manner.
“Lukashev and colleagues [28] proposed that enterovirus species consist of a finite set of capsid genes responsible for different serotypes and a continuum of nonstructural protein genes that seem to evolve in a relatively independent manner.”
From Recombination between Poliovirus and Coxsackie A Viruses of Species C: A Model of Viral Genetic Plasticity and Emergence (2011) · cites this paper as [28]
Cites
Thompson, J. (1997) · Nucleic Acids Research · doi:10.1093/nar/25.24.4876 · Cited by 39,119 · see citing works
PHYLIP-Phylogeny inference package (Version 3.2)
Felsenstein, J. (1989) · Cladistics · Cited by 17,848 · see citing works
Rapid and simple method for purification of nucleic acids
Boom, R., Sol, C. J. A., Salimans, M. M. M., Jansen, C. L., Dillen, P. M. E. W., & van der Noordaa, J. (1990) · Journal of Clinical Microbiology · doi:10.1128/jcm.28.3.495-503.1990 · Cited by 5,273 · see citing works
Oberste, M. S., Maher, K., Kilpatrick, D. R., & Pallansch, M. A. (1999) · Journal of Virology · doi:10.1128/jvi.73.3.1941-1948.1999 · Cited by 854 · see citing works
Enteroviruses : Polioviruses, Coxsackieviruses, Echoviruses, and Newer Enteroviruses
Pallansch, M. (2001) · Medical Entomology and Zoology · Cited by 849 · see citing works
The mechanism of RNA recombination in poliovirus
Kirkegaard, K., & Baltimore, D. (1986) · Cell · doi:10.1016/0092-8674(86)90600-8 · Cited by 499 · see citing works
Genetic recombination with newcastle disease virus, polioviruses, and influenza
Hirst, G. K. (1962) · Cold Spring Harbor Symposia on Quantitative Biology · doi:10.1101/sqb.1962.027.001.028 · Cited by 269 · see citing works
Evidence of recombination among enteroviruses
Santti, J., Hyypiä, T., Kinnunen, L., & Salminen, M. (1999) · Journal of Virology · doi:10.1128/jvi.73.10.8741-8749.1999 · Cited by 259 · see citing works
KLUMP, W. M., Bergmann, I. E., Müller, B., Ameis, D., & Kandolf, R. (1990) · Journal of Virology · doi:10.1128/jvi.64.4.1573-1583.1990 · Cited by 253 · see citing works
Molecular strategy for ‘serotyping’ of human enteroviruses
Caro, V., Guillot, S., Delpeyroux, F., & Crainic, R. (2001) · Journal of General Virology · doi:10.1099/0022-1317-82-1-79 · Cited by 211 · see citing works
Minor, P. D., John, A., Ferguson, M. A. J., & Icenogle, J. P. (1986) · Journal of General Virology · doi:10.1099/0022-1317-67-4-693 · Cited by 203 · see citing works
Jenkins, O. F., Booth, J. D., Minor, P. D., & Almond, J. W. (1987) · Journal of General Virology · doi:10.1099/0022-1317-68-7-1835 · Cited by 202 · see citing works
Natural genetic exchanges between vaccine and wild poliovirus strains in humans.
Guillot, S., Caro, V., Cuervo, N., Korotkova, E., Combiescu, M., Persu, A., Aubert-Combiescu, A., Delpeyroux, F., & Crainic, R. (2000) · Journal of Virology · doi:10.1128/jvi.74.18.8434-8443.2000 · Cited by 202 · see citing works
Chang, K. H., Auvinen, P., Hyypiä, T., & Stanway, G. (1989) · Journal of General Virology · doi:10.1099/0022-1317-70-12-3269 · Cited by 167 · see citing works
Genetic recombination with poliovirus type 1
Ledinko, N. (1963) · Virology · doi:10.1016/0042-6822(63)90145-4 · Cited by 163 · see citing works
Repression of viral transcription during herpes simplex virus latency
Preston, C. M. (2000) · Microbiology · doi:10.1099/0022-1317-81-1-1 · Cited by 160 · see citing works
Complete nucleotide sequence of the genome of coxsackievirus B1
Iizuka, N., Shusuke, K., & Nomoto, A. (1987) · Virology · doi:10.1016/0042-6822(87)90436-3 · Cited by 159 · see citing works
Furlone, M., Guillot, S., Otelea, D., Balanant, J., Candrea, A., & Crainic, R. (1993) · Virology · doi:10.1006/viro.1993.1468 · Cited by 148 · see citing works
Genomic Features of Intertypic Recombinant Sabin Poliovirus Strains Excreted by Primary Vaccinees
Cuervo, N. S., Guillot, S., Romanenkova, N., Combiescu, M., Aubert-Combiescu, A., Seghier, M., Caro, V., Crainic, R., & Delpeyroux, F. (2001) · Journal of Virology · doi:10.1128/jvi.75.13.5740-5751.2001 · Cited by 136 · see citing works
Macadam, A. J., Arnold, C., Howlett, J., John, A., Marsden, S., Taffs, F., Reeve, P., Hamada, N., Wareham, K., Almond, J., et al. (1989) · Virology · doi:10.1016/0042-6822(89)90183-9 · Cited by 125 · see citing works
Intertypic genomic rearrangements of poliovirus strains in vaccinees
Cammack, N. C., Phillips, A., Dunn, G., Patel, V., & Minor, P. D. (1988) · Virology · doi:10.1016/0042-6822(88)90113-4 · Cited by 111 · see citing works
Intertypic genomic rearrangements of poliovirus strains in vaccinees
CAMMACK, N., PHILLIPS, A., DUNN, G., PATEL, V, & MINOR, P. (1988) · Virology · doi:10.1016/s0042-6822(88)90113-4 · Cited by 111 · see citing works
Georgescu, M., Delpeyroux, F., Tardy-Panit, M., Balanant, J., Combiescu, M., Aubert-Combiescu, A., Guillot, S., & Crainic, R. (1994) · Journal of Virology · doi:10.1128/jvi.68.12.8089-8101.1994 · Cited by 109 · see citing works
Zhang, G., Wilsden, G., Knowles, N. J., & McCauley, J. W. (1993) · Journal of General Virology · doi:10.1099/0022-1317-74-5-845 · Cited by 106 · see citing works
Natural genetic recombination between co-circulating heterotypic enteroviruses
Oprisan, G., Combiescu, M., Guillot, S., Caro, V., Combiescu, A., Delpeyroux, F., & Crainic, R. (2002) · Journal of General Virology · doi:10.1099/0022-1317-83-9-2193 · Cited by 105 · see citing works
The Complete Nucleotide Sequence of Coxsackievirus A21
Hughes, P. J., North, C., Minor, P. D., & Stanway, G. (1989) · Journal of General Virology · doi:10.1099/0022-1317-70-11-2943 · Cited by 105 · see citing works
Lipskaya, G. Y., Muzychenko, A. R., Kutitova, O. K., Maslova, S. V., Equestre, M., Drozdov, S. G., Bercoff, R. P., & Agol, V. I. (1991) · Journal of Medical Virology · doi:10.1002/jmv.1890350415 · Cited by 97 · see citing works
Blomqvist, S., Bruu, A., Stenvik, M., & Hovi, T. (2003) · Journal of General Virology · doi:10.1099/vir.0.18708-0 · Cited by 94 · see citing works
Molecular epidemiology and evolution of coxsackievirus A9
Santti, J., Harvala, H., Kinnunen, L., & Hyypiä, T. (2000) · Microbiology · doi:10.1099/0022-1317-81-5-1361 · Cited by 91 · see citing works
Kopecká, H., Brown, B. A., & Pallansch, M. A. (1995) · Virus Research · doi:10.1016/0168-1702(95)00055-u · Cited by 66 · see citing works
Ryan, M. D., Jenkins, O. F., Hughes, P. J., Brown, A. E., Knowles, N. J., Booth, D., Minor, P. D., & Almond, J. W. (1990) · Journal of General Virology · doi:10.1099/0022-1317-71-10-2291 · Cited by 66 · see citing works
Tripartite genome organization of a natural type 2 vaccine/nonvaccine recombinant poliovirus
Georgescu, M., Delpeyroux, F., & Crainic, R. (1995) · Journal of General Virology · doi:10.1099/0022-1317-76-9-2343 · Cited by 64 · see citing works
Genetic recombination in wild-type poliovirus
Dahourou, G., Guillot, S., Gall, O. L., & Crainic, R. (2002) · Journal of General Virology · doi:10.1099/0022-1317-83-12-3103 · Cited by 63 · see citing works
Molecular analysis of the echovirus 18 prototype
Andersson, P. O., Edman, K., & Lindberg, A. (2002) · Virus Research · doi:10.1016/s0168-1702(02)00019-9 · Cited by 57 · see citing works
Dahllund, L., Nissinen, L. M., Pulli, T., et al. (1995) · Virus Research · doi:10.1016/0168-1702(94)00104-k · Cited by 47 · see citing works
Zimmermann, H., Eggers, H. J., & Nelsen‐Salz, B. (1996) · Virus Genes · doi:10.1007/bf00572953 · Cited by 47 · see citing works
Duggal, R., & Wimmer, E. (1999) · Virology · doi:10.1006/viro.1999.9703 · Cited by 32 · see citing works
Lukashev, A. N., Lashkevich, V. A., Koroleva, G. A., et al. (2003) · Virology · doi:10.1016/s0042-6822(02)00058-2 · Cited by 31 · see citing works
Self-citationChua, B. H., McMinn, P. C., Lam, S. K., et al. (2001) · Journal of General Virology · doi:10.1099/0022-1317-82-11-2629 · Cited by 30 · see citing works
Martino, T. A., Tellier, R., Petric, M., et al. (1999) · Virus Research · doi:10.1016/s0168-1702(99)00081-7 · Cited by 27 · see citing works
Echovirus 5: infectious transcripts and complete nucleotide sequence from uncloned cDNA
Lindberg, A., Johansson, S., & Andersson, A. (1999) · Virus Research · doi:10.1016/s0168-1702(98)00127-0 · Cited by 16 · see citing works
Construction of a Recombinant cDNA of Echovirus 6 That Established a Persistent in Vitro infection
Gratsch, T. E., & Righthand, V. F. (1994) · Virology · doi:10.1006/viro.1994.1299 · Cited by 15 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Enteroviruses as agents of emerging infectious diseases
Palacios, G., & Oberste, M. (2005) · Journal of Neurovirology · doi:10.1080/13550280591002531 · Cited by 223 · see citing works
Circulation of type 1 vaccine-derived poliovirus in the philippines in 2001
Shimizu, H., Thorley, B., Paladin, F. J., Brussen, K. A., Stambos, V., Yuen, L., Utama, A., Tano, Y., Arita, M., Yoshida, H., et al. (2004) · Journal of Virology · doi:10.1128/jvi.78.24.13512-13521.2004 · Cited by 146 · see citing works
Combelas, N., Holmblat, B., Joffret, M.-L., Colbère-Garapin, F., & Delpeyroux, F. (2011) · Viruses · doi:10.3390/v3081460 · Cited by 135 · see citing works
Jegouic, S., Joffret, M.-L., Blanchard, C., Riquet, F. B., Perret, C., Pelletier, I., Colbere-Garapin, F., Rakoto-Andrianarivelo, M., & Delpeyroux, F. (2009) · PLoS Pathogens · doi:10.1371/journal.ppat.1000412 · Cited by 116 · see citing works
High Frequency and Diversity of Species C Enteroviruses in Cameroon and Neighboring Countries
Sadeuh-Mba, S. A., Bessaud, M., Massenet, D., Joffret, M.-L., Endegue, M.-C., Njouom, R., Reynes, J.-M., Rousset, D., & Delpeyroux, F. (2013) · Journal of Clinical Microbiology · doi:10.1128/jcm.02119-12 · Cited by 108 · see citing works
Transmission networks and population turnover of echovirus 30
Leitch, E. C. M., Bendig, J., Cabrerizo, M., Cardosa, J., Hyypiä, T., Ivanova, O. E., Kelly, A., Kroes, A. C. M., Lukashev, A., MacAdam, A., et al. (2009) · Journal of Virology · doi:10.1128/jvi.02109-08 · Cited by 109 · see citing works
Self-citationBrown, D. M., Hixon, A. M., Oldfield, L. M., Zhang, Y., Novotny, M., Wang, W., Das, S. R., Shabman, R. S., Tyler, K. L., & Scheuermann, R. H. (2018) · mBio · doi:10.1128/mbio.01954-18 · Cited by 105 · see citing works
Arita, M., Zhu, S.-L., Yoshida, H., Yoneyama, T., Miyamura, T., & Shimizu, H. (2005) · Journal of Virology · doi:10.1128/jvi.79.20.12650-12657.2005 · Cited by 95 · see citing works
Co-Circulation and Evolution of Polioviruses and Species C Enteroviruses in a District of Madagascar
Rakoto-Andrianarivelo, M., Guillot, S., Iber, J., Balanant, J., Blondel, B., Riquet, F., Martin, J., Kew, O., Randriamanalina, B., Razafinimpiasa, L., et al. (2007) · PLoS Pathogens · doi:10.1371/journal.ppat.0030191 · Cited by 96 · see citing works
Zhang, T., Du, J., Xue, Y., Su, H., Yang, F., & Jin, Q. (2013) · PLoS ONE · doi:10.1371/journal.pone.0067157 · Cited by 51 · see citing works
- Authors
- Lukashev, A. N., Lashkevich, V. A., Ivanova, O. E., Koroleva, G. A., Hinkkanen, A. E., & Ilonen, J.
- Affiliations
- Åbo Akademi University (FI)
- Chumakov Institute of Poliomyelitis and Viral Encephalitides (RU)
- University of Turku (FI)
- Corresponding author
- Lukashev, Alexander N.
- Venue
- Journal of Virology
- Publisher
- American Society for Microbiology
- Published
- 2003-10
- Volume
- 77
- Issue
- 19
- Pages
- 10423-10431
- ISSN
- 0022-538X (ISSN-L)
- 1098-5514
- PMC
- PMC228507
- OpenAlex
- W2150044147
- Cited by
- 170
- References
- 42
- Citations by year
- 2026: 1 · 2025: 2 · 2024: 4 · 2023: 3 · 2022: 2 · 2021: 4 · 2020: 5 · 2019: 7 · 2018: 10 · 2017: 3 · 2016: 8 · 2015: 5 · 2014: 11 · 2013: 9 · 2012: 8
- FWCI
- 5.48
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- Journal of Virology (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Viral Infections and Immunology Research
- Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Animal Virus Infections Studies
- Keywords
- enterovirus B, recombination, Coxsackie B virus, echovirus, phylogenetic analysis, VP1, 5' untranslated region, serotype evolution, nonstructural protein gene, coat protein gene, former Soviet Union
- MeSH terms
- Enterovirus, Humans, Phylogeny, Recombination, Genetic, Viremia, 5' Untranslated Regions
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review