The Evolutionary Pathway to Virulence of an RNA Virus
Open accessAbstract
Paralytic polio once afflicted almost half a million children each year. The attenuated oral polio vaccine (OPV) has enabled world-wide vaccination efforts, which resulted in nearly complete control of the disease. However, poliovirus eradication is hampered globally by epidemics of vaccine-derived polio. Here, we describe a combined theoretical and experimental strategy that describes the molecular events leading from OPV to virulent strains. We discover that similar evolutionary events occur in most epidemics. The mutations and the evolutionary trajectories driving these epidemics are replicated using a simple cell-based experimental setup where the rate of evolution is intentionally accelerated. Furthermore, mutations accumulating during epidemics increase the replication fitness of the virus in cell culture and increase virulence in an animal model. Our study uncovers the evolutionary strategies by which vaccine strains become pathogenic and provides a powerful framework for rational design of safer vaccine strains and for forecasting virulence of viruses. VIDEO ABSTRACT.
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Recombination events downstream of nucleotide 5000 leading to acquisition of the non-structural coding region of WT PV3 are often observed in vivo in vaccinees that receive trivalent OPV.
“This event is often observed in vivo in vaccinees that receive trivalent OPV (tOPV) (Korotkova et al., 2017, Stern et al., 2017).”
From Engineering the Live-Attenuated Polio Vaccine to Prevent Reversion to Virulence (2020) · cites this paper as Stern et al., 2017
The Results section on vaccinees reports type 2 viruses recombinant with OPV1 in the P2 or P3 regions 14 days after trivalent OPV vaccination. The Conclusions likewise say the non-structural region is frequently replaced with OPV1-derived sequence, not wild-type PV3 sequence. The cited passages do not establish a breakpoint downstream of nucleotide 5000. (LLM, conf=0.88)
Checked by a reasoning model — may be wrong.
Experimental — accuracy not yet measuredSoon after vaccination, the majority of vaccinees shed polioviruses with a high frequency of mutations that increase domV stability, indicating that domV structural stability is under strong positive selection in the human gut.
“Soon after vaccination, the majority of vaccinees shed polioviruses with a high frequency of such mutations (Evans et al., 1985, Stern et al., 2017), indicating that the structural stability of domV is under strong positive selection in the human gut.”
From Engineering the Live-Attenuated Polio Vaccine to Prevent Reversion to Virulence (2020) · cites this paper as Stern et al., 2017
The Results section (‘Next generation sequencing of vaccinees confirms rapid emergence of gate-keeper mutations’; page unavailable) reports that all three gate-keeper mutations were at high frequencies in viruses excreted by all eleven vaccinees studied 14 days after vaccination. The paper interprets their rapid emergence as a fitness advantage, but our copy does not establish that these mutations increase domain V structural stability or that selection specifically favors that stability in the human gut. (LLM, conf=0.86)
Experimental — accuracy not yet measuredRecombination of an OPV strain with co-circulating enterovirus C species allowed the Sabin2 domV to be replaced by that of a WT co-circulating enterovirus to provide a thermostable structure, thereby restoring viral fitness.
“Recombination of an OPV strain with co-circulating enterovirus C species allowed the Sabin2 domV to be replaced by that of a WT co-circulating enterovirus to provide a thermostable structure, thereby restoring viral fitness (Burns et al., 2013, Stern et al., 2017).”
From Engineering the Live-Attenuated Polio Vaccine to Prevent Reversion to Virulence (2020) · cites this paper as Stern et al., 2017
The Results report that recombination with co-circulating HEV-C strains replaced the OPV2 5′ UTR in 397 of 424 sequences; they do not identify domain V specifically. The Conclusions link recombination to improved fitness and report that OPV2–HEV-C chimeras had elevated fitness at higher temperatures, but do not say that replacement of domain V provided a thermostable structure. (LLM, conf=0.85)
Experimental — accuracy not yet measuredIn all type 2 lineages in current outbreaks, the 481 A-to-G mutation preceded all other events leading to cVDPV virulence, suggesting its role as a gate-keeper in the reversion process.
“In all type 2 lineages in current outbreaks, the 481 A-to-G mutation preceded all other events leading to cVDPVs virulence (Stern et al., 2017), suggesting its role as a “gate-keeper” in the reversion process, similar to driver mutations in cancer evolution (Curigliano, 2018, Reddy et al., 2017, Temko et al., 2017).”
From Engineering the Live-Attenuated Polio Vaccine to Prevent Reversion to Virulence (2020) · cites this paper as Stern et al., 2017
The Results section (“A probabilistic evolutionary model”) says A481G was one of three gate-keeper substitutions that preceded the later waves of events in lineages with enough phylogenetic resolution. It does not say A481G preceded every other event in all lineages; the vaccinee-sequencing Results say A481G was *usually* first among the three gate-keepers. The paper also describes the analyzed outbreaks, not necessarily all current outbreaks. (LLM, conf=0.87)
Experimental — accuracy not yet measuredThermoresistant variants of Sabin2 also display a significant increase in virulence.
“These thermoresistant variants also display a significant increase in virulence (Macadam et al., 2006, Stern et al., 2017).”
From Engineering the Live-Attenuated Polio Vaccine to Prevent Reversion to Virulence (2020) · cites this paper as Stern et al., 2017
The Results section reports that all three gate-keeper mutations were adaptive in cell culture at 39.5°C. In the mouse virulence experiments, however, only A481G alone and the combination of all three significantly increased virulence; the other individual mutations did not. The claim overgeneralizes the virulence finding to the thermoresistant variants as a group. (LLM, conf=0.86)
Experimental — accuracy not yet measured
In the mouse neurovirulence test, nOPV2 recovered from vaccinees maintained its attenuation phenotype, in contrast to the current vaccine containing Sabin2.
“Strikingly, in the mouse neurovirulence test, the redesigned nOPV2 recovered from vaccinees maintained its attenuation phenotype (Van Damme et al., 2019), in contrast to the current vaccine containing Sabin2 (Stern et al., 2017).”
From Engineering the Live-Attenuated Polio Vaccine to Prevent Reversion to Virulence (2020) · cites this paper as Stern et al., 2017
The Results section reports that gatekeeper mutations increased the virulence of conventional OPV2 in mice, and the Conclusions note that these mutations were present in viruses excreted by vaccinees. This supports the contrast with Sabin2, which is the part attributed to Stern et al., but the paper tested engineered mutants rather than virus recovered from vaccinees in the mouse test. The nOPV2 finding is attributed to Van Damme et al., not to this source. (LLM, conf=0.86)
Experimental — accuracy not yet measuredMutation U459C (nucleotide 398 in Sabin2) was identified as a secondary adaptive mutation in cVDPV2 isolates and vaccinee isolates.
“Mutation U459C (nucleotide 398 in Sabin2) was identified as a secondary adaptive mutation in cVDPV2 isolates and vaccinee isolates (Stern et al., 2017).”
From Engineering the Live-Attenuated Polio Vaccine to Prevent Reversion to Virulence (2020) · cites this paper as Stern et al., 2017
The Results sections on parallel substitutions and vaccinees identify U398C as an adaptive gate-keeper mutation in cVDPV2 lineages and report it at high frequency in viruses from vaccinees. Our copy does not establish that U459C is another numbering of U398C, and it calls U398C a gate-keeper rather than a secondary adaptive mutation. Page numbers are unavailable in our copy. (LLM, conf=0.82)
Experimental — accuracy not yet measuredBy 14 days post-vaccination, most Sabin2 vaccinees excrete virus mutants that lost the attenuation allele entirely in domV.
“Indeed, by 14 days post-vaccination, most Sabin2 vaccinees excrete virus mutants that lost the attenuation allele entirely in domV (Figures 7A and 7B) (Stern et al., 2017).”
From Engineering the Live-Attenuated Polio Vaccine to Prevent Reversion to Virulence (2020) · cites this paper as Stern et al., 2017
The Results section, “Next generation sequencing of vaccinees confirms rapid emergence of gate-keeper mutations” (page unavailable), reports that the A481G attenuation reversion was present at high frequency in viruses excreted 14 days after vaccination by all 11 vaccinees studied. High frequency does not establish that the attenuation allele was lost entirely, which is the unsupported part of the claim. (LLM, conf=0.84)
Experimental — accuracy not yet measuredThree specific codon positions are involved in reversion of OPV strains, two in the 5′ UTR region and one in the VP1 region.
“A number of studies have identified three specific codon positions that are involved in this reversion, two in the 5′ UTR region and one in the VP1 region [82,83].”
From The Fight against Poliovirus Is Not Over (2023) · cites this paper as [82]
A single A-to-G mutation at position 481 increases temperature tolerance and makes the virus more neurovirulent.
“A single A-to-G mutation at this position results in increased tolerance to temperature and makes the virus more neurovirulent (Macadam et al., 1992, Macadam et al., 1994, Stern et al., 2017).”
From Engineering the Live-Attenuated Polio Vaccine to Prevent Reversion to Virulence (2020) · cites this paper as Stern et al., 2017
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Analytical validity of nanopore sequencing for rapid SARS-CoV-2 genome analysis
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The phylogenomics of evolving virus virulence
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Engineering the Live-Attenuated Polio Vaccine to Prevent Reversion to Virulence
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Self-citationExperimental Design, Population Dynamics, and Diversity in Microbial Experimental Evolution
den Bergh, B. V., Swings, T., Fauvart, M., & Michiels, J. J. (2018) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00008-18 · Cited by 180 · see citing works
Mechanisms and Concepts in RNA Virus Population Dynamics and Evolution
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Self-citationPrecision epidemiology for infectious disease control
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Development of a new oral poliovirus vaccine for the eradication end game using codon deoptimization
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Self-citationMapping the Evolutionary Potential of RNA Viruses
Dolan, P., Whitfield, Z. J., & Andino, R. (2018) · Cell Host & Microbe · doi:10.1016/j.chom.2018.03.012 · Cited by 91 · see citing works
Self-citationType 2 Poliovirus Detection after Global Withdrawal of Trivalent Oral Vaccine
Blake, I. M., Pons-Salort, M., Molodecky, N. A., Diop, O. M., Chenoweth, P., Bandyopadhyay, A. S., Zaffran, M., Sutter, R. W., & Grassly, N. C. (2018) · New England Journal of Medicine · doi:10.1056/nejmoa1716677 · Cited by 79 · see citing works
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Biased Mutation and Selection in RNA Viruses
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Self-citationDetecting rare mutations and DNA damage with sequencing-based methods
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Genetic stabilization of attenuated oral vaccines against poliovirus types 1 and 3
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Pathogenicity and virulence of hepatitis A virus
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Parallel molecular evolution and adaptation in viruses
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Mechanism of Cross-Species Transmission, Adaptive Evolution and Pathogenesis of Hepatitis E Virus
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Key issues review: evolution on rugged adaptive landscapes
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Evolutionary and Structural Overview of Human Picornavirus Capsid Antibody Evasion
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Emergency Services of Viral RNAs: Repair and Remodeling
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Changes in the EV-A71 Genome through Recombination and Spontaneous Mutations: Impact on Virulence
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An overview of viral mutagenesis and the impact on pathogenesis of SARS-CoV-2 variants
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The role of genetic sequencing and analysis in the polio eradication programme
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The Fight against Poliovirus Is Not Over
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“A number of studies have identified three specific codon positions that are involved in this reversion, two in the 5′ UTR region and one in the VP1 region [82,83].”
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Newcastle Disease Virus-Based Vectored Vaccine against Poliomyelitis
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Experimental Evolution to Study Virus Emergence
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Evolution, Ecology, and Zoonotic Transmission of Betacoronaviruses: A Review
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Self-citationIsolation of Vaccine-Like Poliovirus Strains in Sewage Samples From the United Kingdom
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Evaluating stability of attenuated Sabin and two novel type 2 oral poliovirus vaccines in children
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Self-citationEcological and evolutionary perspectives on tick-borne pathogen co-infections
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The unique evolutionary dynamics of the SARS-CoV-2 Delta variantPreprint
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Enterovirus 71 targets the cardiopulmonary system in a robust oral infection mouse model
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Darwin review: the evolution of virulence in human pathogens
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Mapping Attenuation Determinants in Enterovirus-D68
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Self-citationMolodecky, N. A., Jafari, H. S., Safdar, R. M., Ahmed, J., Mahamud, A. S., Bandyopadhyay, A. S., Shukla, H., Quddus, A., Zaffran, M., Sutter, R. W., et al. (2021) · Vaccine · doi:10.1016/j.vaccine.2021.09.037 · Cited by 16 · see citing works
Fitness Barriers Limit Reversion of a Proofreading-Deficient Coronavirus
Graepel, K. W., Agostini, M. L., Lu, X., Sexton, N. R., & Denison, M. R. (2019) · Journal of Virology · doi:10.1128/jvi.00711-19 · Cited by 15 · see citing works
Mucosal vaccines for viral diseases: Status and prospects
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Repeats Mimic Pathogen-Associated Patterns Across a Vast Evolutionary LandscapePreprint
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Monitoring and redirecting virus evolution
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CpG-creating mutations are costly in many human viruses
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Self-citationUnderstanding neurotropic enteric viruses: routes of infection and mechanisms of attenuation
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Emergence of Vaccine-Derived Polioviruses during Ebola Virus Disease Outbreak, Guinea, 2014–2015
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Asymptomatic immunodeficiency-associated vaccine-derived poliovirus infections in two UK children
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Inferring population genetics parameters of evolving viruses using time-series data
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Self-citationNatural and Historical Overview of the Animal Wildlife-Livestock Interface
Vicente, J., Montoro, V., & Vercauteren, K. (2021) · Wildlife research monographs · doi:10.1007/978-3-030-65365-1_2 · Cited by 4 · see citing works
Identification of Evolutionary Trajectories Shared across Human Betacoronaviruses
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A Bayesian Framework for Inferring the Influence of Sequence Context on Point Mutations
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Self-citationAntiviral Development for the Polio Endgame: Current Progress and Future Directions
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Experimental virus evolution in cancer cell monolayers, spheroids, and tissue explants
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Deng, H., Li, Y., He, X., Wang, H., Wang, S., Zhang, H., Zhu, J., Gu, L., Li, R., & Wang, G. (2024) · Journal of Medical Virology · doi:10.1002/jmv.29831 · Cited by 6 · see citing works
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Isolation and Identification of Inter-Species Enterovirus Recombinant Genomes
Bentley, K., Tee, H. K., Pearson, A., Lowry, K., Waugh, S., Jones, S., Chan, Y. F., & Evans, D. J. (2021) · Viruses · doi:10.3390/v13122390 · Cited by 5 · see citing works
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Self-citationHost-virus molecular arms race: RNAi-mediated antiviral defense and viral suppressor of RNAi
Zhang, B., Zhou, X., & Ren, Y. (2025) · Cell Insight · doi:10.1016/j.cellin.2025.100276 · Cited by 4 · see citing works
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- Authors
- Stern, A., Yeh, M. T., Zinger, T., Smith, M., Wright, C., Ling, G., Nielsen, R., Macadam, A., & Andino, R.
- Affiliations
- Tel Aviv University (IL)
- University of California, San Francisco (US)
- National Institute for Biological Standards and Control (GB)
- University of California, Berkeley (US)
- Corresponding author
- Stern, Adi
- Andino, Raul
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 2017-03
- Volume
- 169
- Issue
- 1
- Pages
- 35-46.e19
- ISSN
- 0092-8674 (ISSN-L)
- PMC
- PMC5787669
- OpenAlex
- W2598379945
- Cited by
- 127
- References
- 72
- Citations by year
- 2026: 9 · 2025: 4 · 2024: 10 · 2023: 15 · 2022: 13 · 2021: 20 · 2020: 20 · 2019: 12 · 2018: 17 · 2017: 6 · 2012: 1
- FWCI
- 9.88
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- www.elsevier.com/legal/tdmrep-license (tdm)
- www.elsevier.com/open-access/userlicense/1.0/ (vor, 388 d)
- doi.org/10.15223/policy-017 (stm-asf)
- doi.org/10.15223/policy-037 (stm-asf)
- doi.org/10.15223/policy-012 (stm-asf)
- doi.org/10.15223/policy-029 (stm-asf)
- doi.org/10.15223/policy-004 (stm-asf)
- Locations
- Cell (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- eScholarship (California Digital Library) (submittedVersion, cc-by-nc-nd)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- WIS post-doctoral award
- Rothschild post-doctoral award
- Edmond J. Safra Center for Bioinformatics at Tel-Aviv University
- NSF (CMMI-0941355)
- NIH (R01 GM097115, AI36178, AI40085, P01 AI091575)
- University of California (CCADD
- DARPA Prophecy
- Bill and Melinda Gates Foundation
- 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
- Health Sciences › Medicine › Epidemiology › Virology and Viral Diseases
- Keywords
- poliovirus, vaccine-derived poliovirus, oral polio vaccine, RNA virus evolution, polio epidemic
- MeSH terms
- Animals, Biological Evolution, Phylogeny, Poliomyelitis, Poliovirus Vaccine, Oral, Poliovirus, Mice
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