Polioviruses with Natural Recombinant Genomes Isolated from Vaccine-Associated Paralytic Poliomyelitis
Abstract
To determine how oral poliovirus vaccine (Sabin) strains evolve during replication in humans and to confirm the etiology of vaccine-associated paralytic poliomyelitis (VAPP), we examined 70 vaccine-derived strains isolated from VAPP cases. Two distant sequences of the poliovirus genome were targeted for a double restriction fragment length polymorphism assay (RFLP) of reverse-transcribed genomic segments amplified by PCR, an extension of the method that we described previously (Balanant et al., 1991). One (RFLP-1) was a 480-long nucleotide sequence coding for the N-terminal part of the VP1 capsid polypeptide, situated in the 5' third of the viral genome (nucleotides 2401-2880). The other (RFLP-3D1) was a 291-long nucleotide sequence coding for a part of the viral polymerase, situated near the 3' end of the genome (nucleotides 6086-6376). Strain-specific restriction profiles could be generated for different field isolates by using three restriction enzymes in each case: HaeIII, DdeI, and HpaII for RFLP-1 and HaeIII, DdeI and RsaI for RFLP-3D1. With few exceptions, the vaccine-specific RFLP profiles were found to be conserved in both regions during replication of these viruses in humans. Thus, RFLP could be used as a marker so as to identify the origin of viral isolates at both ends of their genome. Whether viral isolates were vaccine-derived was determined by using strain-specific monoclonal antibodies and RFLP-1. Among the 70 isolates, 21 of the 43 type 2 strains and 15 of the 22 type 3 strains had a recombinant genome. None of the 5 type 1 Sabin-derived isolates was found to be recombinant. Both intertypic vaccine/vaccine and vaccine/non-vaccine recombinants were detected. Partial nucleotide sequencing confirmed the RFLP results in all cases that were investigated. In one case, it was possible to predict the recombination junction site from the restriction profiles. This site was more precisely localized by sequencing. The C6203 > U nucleotide substitution, which is suspected to contribute to the reversion toward neurovirulence of the attenuated Sabin 1 strain, was detected in almost all the recombinant genomes containing Sabin 1-specific sequences at the 3' extremity. This mutation was detected by identification of the modified RsaI profile in the RFLP-3D1. The results presented in this paper suggest that recombination, alone or together with mutation, might be one of the mechanisms of the reversion toward neurovirulence of attenuated vaccine strains and of the natural evolution of poliovirus.
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Many isolates from VAPP cases, AFP cases with incidental isolation of vaccine-related virus, and healthy OPV recipients are vaccine/vaccine recombinants.
“Many isolates from VAPP cases, AFP cases with incidental isolation of vaccine-related virus (much more frequent thanVAPPcases),andhealthyOPVrecipients are vaccine/vaccine recombinants (18, 33, 59, 91, 106).”
From VACCINE-DERIVED POLIOVIRUSES AND THE ENDGAME STRATEGY FOR GLOBAL POLIO ERADICATION (2005) · cites this paper as [59]
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VACCINE-DERIVED POLIOVIRUSES AND THE ENDGAME STRATEGY FOR GLOBAL POLIO ERADICATION
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A Natural Intergenotypic Recombinant of Hepatitis C Virus Identified in St. Petersburg
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“The recombination breakpoints for nonsegmented plus-strand RNA viruses, such as polioviruses and other picornaviruses, as well as members of the family Flaviviridae, are often located in the part of the genome encoding the first nonstructural protein but are sometimes in genes encoding structural proteins (usually env…”
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“Both intra- and intertypic recombination have been shown to occur among poliovirus vaccine strains (5, 18, 28, 37) and between polioviruses and other, unidentified, donor strains FIG.”
BackgroundEvidence of recombination among enteroviruses
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“Recombination has been shown to occur between PVs of vaccine and wild-type origin (2, 8 ). The evidence supports a model of homologous recombination by strand switching (copy choice) (14, 19).”
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“Other genomic regions that do not encode serotype-specific determinants are more conserved across serotypes and may evolve or undergo recombination (122, 127, 281) independently of virus serotype.”
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“Intra- and intertypic recombination has been shown to occur among poliovirus vaccine strains (3, 10 , 21) and between wild polioviruses and other, unidentified donor strains (14, 22).”
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“Then a stochastic increase in fitness (9, 14, 19, 52) and hence in neurovirulence occurred in the M lineage due to either a mutation(s) (not necessarily in the sequenced region) or recombination ( 21 , 22, 39).”
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“Such recombinants between wild-type and vaccine strains of polioviruses, as well as between different enterovirus types belonging to the same species, have been described (Furione et al., 1993 ; Santti et al., 1999 ; Guillot et al., 2000).”
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“Mutations in codons 106 of VP1, 225 of VP3 and 73 of 3Dpol are also found in some strains isolated from VAPP cases (Figure 4) (Furione et al, 1993; Georgescu et al, 1995; Li et al, 1996; Otelea et al, 1993).”
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“It has been reported that RFLP analysis was useful for intratypic differentiation between wild and vaccine strains (2, 10 , 25).”
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“The RFLP developments in the PCR methodology have contributed greatly to these diagnostic demands ( 1 , 4). Their implementation, however, has revealed certain weaknesses that call for definite improvements (31; Georgopoulou et al., unpublished data).”
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Sabin Type 2 Polioviruses with Intertypic Vaccine/Vaccine Recombinant Genomes
Georgopoulou, A., & Markoulatos, P. (2001) · European Journal of Clinical Microbiology & Infectious Diseases · doi:10.1007/s100960100610 · Cited by 32 · see citing works
Karakasiliοtis, I., Markoulatos, P., & Katsorchis, T. (2003) · Molecular and Cellular Probes · doi:10.1016/j.mcp.2003.09.009 · Cited by 33 · see citing works
de Oliveira, L. H., & Struchiner, C. J. (2000) · International Journal of Epidemiology · doi:10.1093/ije/29.4.757 · Cited by 30 · see citing works
Strength in numbers: Mechanisms of viral co-infection
Aguilera, E. R., & Pfeiffer, J. K. (2019) · Virus Research · doi:10.1016/j.virusres.2019.03.003 · Cited by 26 · see citing works
“In fact, individuals infected with circulating vaccine derived polioviruses (cVDPVs) are commonly infected with viruses that have undergone genetic exchange (Cherkasova et al., 2002; Cuervo et al., 2001; Dahourou et al., 2002; Furione et al., 1993; Liu et al., 2000).”
BackgroundSiafakas, N., Markoulatos, P., & Levidiotou-Stefanou, S. (2004) · Molecular and Cellular Probes · doi:10.1016/j.mcp.2004.06.005 · Cited by 29 · see citing works
Skiadopoulos, M. H., Surman, S. R., Riggs, J. M., Collins, P. L., & Murphy, B. R. (2001) · Journal of Virology · doi:10.1128/jvi.75.21.10498-10504.2001 · Cited by 29 · see citing works
Recombination and evolutionary dynamics of human echovirus 6
Cabrerizo, M., Trallero, G., & Peter Simmonds, K. (2013) · Journal of Medical Virology · doi:10.1002/jmv.23741 · Cited by 28 · see citing works
“…to occur between different poliovirus types used in the Sabin live attenuated oral poliovirus vaccine [Minor et al., 1986; Cammack et al., 1988; Furione et al., 1993], this process has been described more recently to occur on natural infection in a wide range of other human EVs [reviewed in…”
BackgroundYan, D., Li, L., Zhu, S., Zhang, Y., An, J., Wang, D., Wen, N., Jorba, J. C., Liu, W. Y., Zhong, G., et al. (2010) · Journal of Clinical Microbiology · doi:10.1128/jcm.00712-10 · Cited by 28 · see citing works
Zhang, Y., Zhu, S., Yan, D., Liu, G., Bai, R., Wang, D., Chen, L., Zhu, H., An, H., Kew, O. M., et al. (2010) · PLoS ONE · doi:10.1371/journal.pone.0015300 · Cited by 29 · see citing works
“The frequency of recombination is about 2%, 53%, and 79% of poliovirus type 1, 2 and 3, respectively, and shows that the frequency depends strongly on the serotype of polioviruses [16].”
BackgroundPapaventsis, D. C., Siafakas, N., Markoulatos, P., Papageorgiou, G. T., Kourtis, C., Chatzichristou, E., Economou, C., & Levidiotou, S. (2005) · Applied and Environmental Microbiology · doi:10.1128/aem.71.1.72-79.2005 · Cited by 28 · see citing works
“Moreover, the distinction between nonpolio and polio-like enteroviruses was accurate, something which is extremely important for the eradication of wild-type polioviruses from the environment and for surveillance for vaccine-associated cases of AFP (4, 8, 9 , 10, 11, 13).”
BackgroundMolecular and Biological Basis of Picornavirus Taxonomy
Stanway, G., Hovi, T., Knowles, N. J., & Hyypiä, T. (2014) · ASM Press eBooks · doi:10.1128/9781555817916.ch2 · Cited by 28 · see citing works
Retrospective Characterization of a Vaccine-Derived Poliovirus Type 1 Isolate from Sewage in Greece
Dedepsidis, E., Kyriakopoulou, Z., Pliaka, V., Kottaridi, C., Bolanaki, E., Levidiotou-Stefanou, S., Komiotis, D., & Markoulatos, P. (2007) · Applied and Environmental Microbiology · doi:10.1128/aem.00535-07 · Cited by 27 · see citing works
Hovi, T., Lindholm, N., Savolainen, C., Stenvik, M., & Burns, C. C. (2004) · Journal of General Virology · doi:10.1099/vir.0.19518-0 · Cited by 27 · see citing works
“…in the case of trivalent OPV reci- pients, inter-serotypic recombinations have been frequently 374 Journal of General Virology 85 Downloaded from www.microbiologyresearch.org by IP: 54.70.40.11 On: Tue, 11 Dec 2018 06:01:42 observed (Minor et al., 1986; Lipskaya et al., 1991; Furione et al., 1993).”
BackgroundInfluentialStability of Yellow Fever Virus under Recombinatory Pressure as Compared with Chikungunya Virus
McGee, C. E., Tsetsarkin, K. A., Guy, B., Lang, J., Plante, K. S., Vanlandingham, D. L., & Higgs, S. (2011) · PLoS ONE · doi:10.1371/journal.pone.0023247 · Cited by 25 · see citing works
“Homologous recombination of picornavirus oral polio vaccines is a well documented etiology of vaccine associated paralytic poliomyelitis [61–63].”
BackgroundZhang, Y., Wang, H., Zhu, S., Li, Y., Li, S., Liu, Y., Liu, G., Nishimura, Y., Chen, L., Yan, D., et al. (2009) · Journal of General Virology · doi:10.1099/vir.0.014258-0 · Cited by 25 · see citing works
“Analysis of VAPP infection cases revealed poliovirus recombination with a 50 % involvement of Sabin 2 strains and 67 % of Sabin 3 strains, while Sabin 1 strains were rarely involved (Furione et al., 1993).”
BackgroundGeorgescu, M., Tardy-Panit, M., Guillot, S., Crainic, R., & Delpeyroux, F. (1995) · Journal of Virology · doi:10.1128/jvi.69.9.5278-5286.1995 · Cited by 26 · see citing works
“Nevertheless, it is paradoxical that a 39-terminal fragment of the Sabin 1 genome is frequently found in VAPP intertypic recombinant strain genomes (30 of 62 intertypic VAPP recombinants analyzed) (15, 16, 23, 25, 26).”
BackgroundInfluentialSelf-citationKorotkova, E., Laassri, M., Zagorodnyaya, T., Petrovskaya, S., Rodionova, E., Cherkasova, E., Gmyl, A., Ivanova, O., Eremeeva, T., Lipskaya, G., et al. (2017) · Viruses · doi:10.3390/v9110353 · Cited by 23 · see citing works
Genomic Analysis of Recombinant Sabin Clinical Isolates
Paximadi, E., Karakasiliοtis, I., Mamuris, Z., Stathopoulos, C., Krikelis, V., & Markoulatos, P. (2006) · Virus Genes · doi:10.1007/s11262-005-6877-1 · Cited by 24 · see citing works
Impact of the Microbiota on Viral Infections
Campbell, D. E., Li, Y., Ingle, H., & Baldridge, M. T. (2023) · Annual Review of Virology · doi:10.1146/annurev-virology-111821-115754 · Cited by 22 · see citing works
Poliovirus vaccine strains in sewage and river water in South Africa
Pavlov, D. N. (2006) · Canadian Journal of Microbiology · doi:10.1139/w06-026 · Cited by 22 · see citing works
“1991), and restriction fragment length polymorphism analysis (Furione et al. 1993), which allow inter- and intra-typic differentiation (Georgopoulou et al.”
MethodBlomqvist, S., Savolainen‐Kopra, C., Paananen, A., Bassioni, L. E., Nasr, E. M. E. M., Firstova, L., Zamiatina, N. A., Kutateladze, T., & Roivainen, M. (2010) · Virus Research · doi:10.1016/j.virusres.2010.05.006 · Cited by 22 · see citing works
Comparison of poliovirus recombinants: accumulation of point mutations provides further advantages
Savolainen‐Kopra, C., Samoilovich, E., Kahelin, H., Hiekka, A., Hovi, T., & Roivainen, M. (2009) · Journal of General Virology · doi:10.1099/vir.0.010942-0 · Cited by 21 · see citing works
Random selection: a model for poliovirus infection of the central nervous system.
Georgescu, M. M., Ozden, S., Crainic, R., & Balanant, J. (1997) · Journal of General Virology · doi:10.1099/0022-1317-78-8-1819 · Cited by 21 · see citing works
“(Furione et al., 1993) or the recombination site (Georgescu et al.”
Self-citationKapusinszky, B., Molnár, Z., Szomor, K. N., & Berencsi, G. (2009) · FEMS Immunology & Medical Microbiology · doi:10.1111/j.1574-695x.2009.00621.x · Cited by 20 · see citing works
“Among vaccine-related viruses isolated from children given or indirectly exposed to tOPV, recombination is most frequently found among the type 3 isolates, the large majority of which are vaccine/vaccine recombinants (Furione et al., 1993).”
BackgroundHomologous recombination in bovine pestiviruses
Jones, L. R., & Weber, E. L. (2004) · Infection Genetics and Evolution · doi:10.1016/j.meegid.2004.04.004 · Cited by 19 · see citing works
Nagendrakumar, S. B., Madhanmohan, M., Rangarajan, P. N., & Srinivasan, V. A. (2009) · Journal of Biosciences · doi:10.1007/s12038-009-0011-9 · Cited by 19 · see citing works
Domingo, E., Menéndez‐Arias, L., & Holland, J. J. (1997) · Reviews in Medical Virology · doi:10.1002/(sici)1099-1654(199707)7:2 · Cited by 133 · see citing works
Circulation of a type 1 recombinant vaccine-derived poliovirus strain in a limited area in Romania
Combiescu, M., Guillot, S., Persu, A., Băicuş, A., Pițigoi, D., Balanant, J., Oprişan, G., Crainic, R., Delpeyroux, F., & Aubert-Combiescu, A. (2006) · Archives of Virology · doi:10.1007/s00705-006-0884-y · Cited by 18 · see citing works
“virus horse antisera and were confirmed with monotype specific antisera [17, 22].”
BackgroundSelf-citationMechanisms Controlling Virulence Thresholds of Mixed Viral Populations
Lancaster, K. Z., & Pfeiffer, J. K. (2011) · Journal of Virology · doi:10.1128/jvi.00355-11 · Cited by 16 · see citing works
Romanenkova, N. I., Guillot, S., Rozaeva, N. R., Crainic, R., Александровна, Б. М., & Delpeyroux, F. (2006) · Journal of Clinical Microbiology · doi:10.1128/jcm.00017-06 · Cited by 16 · see citing works
Self-citationBoot, H. J., Kasteel, D., Buisman, A., & Kimman, T. G. (2003) · Journal of Virology · doi:10.1128/jvi.77.11.6541-6545.2003 · Cited by 16 · see citing works
Vaccine-associated paralytic poliomyelitis in Brazil, 1989-1995
de Oliveira, L. H., & Struchiner, C. J. (2000) · Revista Panamericana de Salud Pública · doi:10.1590/s1020-49892000000400002 · Cited by 15 · see citing works
Mallet, L., Pelloquin, F., Brigaud, M., Caudrelier, P., Bandet, R., Xueref, C., Fuchs, F., Gibelin, N., Goldman, C., Moulin, J.-C., et al. (1997) · Journal of Medical Virology · doi:10.1002/(sici)1096-9071(199705)52:1 · Cited by 15 · see citing works
Diverse Mechanisms of RNA Recombination
Gmyl, A. P., & Agol, V. I. (2005) · Molecular Biology · doi:10.1007/s11008-005-0069-x · Cited by 14 · see citing works
“This circumstance is probably responsible for the predominance of intertypic recombinants among viruses isolated from rare patients with paralytic poliomyelitis developing as a result of vaccination [139] [140] [141] .”
BackgroundDevaux, C. A., Pontarotti, P., Levasseur, A., Colson, P., & Raoult, D. (2024) · Frontiers in Public Health · doi:10.3389/fpubh.2023.1284337 · Cited by 16 · see citing works
“…RNA recombinations are not site-specific and do not require extensive similarity between the recombining parents at the crossover site with a probable copy choice mechanism for RNA recombination, in which the viral RNA polymerase switches templates during negative strand synthesis (73, 90).”
BackgroundRare adverse events associated with oral poliovirus vaccine in Brazil
Friedrich, F. (1997) · Brazilian Journal of Medical and Biological Research · doi:10.1590/s0100-879x1997000600001 · Cited by 13 · see citing works
“Since the Sabin vaccine strains may increase neurovirulence by genomic modifications during multiplication in the vaccinee and after transmission to contacts, there is also always the possibility of the appearance of neurovirulent strains erived from the Sabin vaccine strains (8,9,11,38,42-44,46-60).”
BackgroundMarturano, J., & Fiore, L. (2002) · Journal of Clinical Microbiology · doi:10.1128/jcm.40.1.316-317.2002 · Cited by 12 · see citing works
Hellen, C. U. T., & Wimmer, E. (2014) · ASM Press eBooks · doi:10.1128/9781555818326.ch2 · Cited by 11 · see citing works
- Authors
- Furlone, M., Guillot, S., Otelea, D., Balanant, J., Candrea, A., & Crainic, R.
- Affiliations
- Institut Pasteur (FR)
- ORCID
- Guillot, Sophie
- Venue
- Virology
- Publisher
- Elsevier BV
- Published
- 1993-09
- Volume
- 196
- Issue
- 1
- Pages
- 199-208
- ISSN
- 0042-6822 (ISSN-L)
- OpenAlex
- W2062555317
- Cited by
- 148
- References
- 0
- Citations by year
- 2024: 1 · 2023: 2 · 2022: 1 · 2020: 2 · 2019: 3 · 2018: 3 · 2017: 2 · 2016: 3 · 2015: 1 · 2014: 7 · 2013: 5 · 2012: 5
- FWCI
- 3.81
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Virology (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Viral Infections and Immunology Research
- Health Sciences › Medicine › Epidemiology › Virology and Viral Diseases
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
- Keywords
- vaccine-associated paralytic poliomyelitis, oral polio vaccine, Sabin strains, vaccine-derived poliovirus, restriction fragment length polymorphism, strain-specific markers, live attenuated vaccine
- MeSH terms
- Base Sequence, DNA, Viral, Humans, Molecular Sequence Data, Paralysis, Poliomyelitis, Poliovirus Vaccine, Oral, Recombination, Genetic, Polymorphism, Restriction Fragment Length, Sequence Homology, Nucleic Acid, Vaccines, Synthetic, Virus Replication, Polymerase Chain Reaction, Genome, Viral, Poliovirus
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