Cited by 1,009Evolution and Genetic DynamicsMathematical and Theoretical Epidemiology and Ecology ModelsRNA and protein synthesis mechanisms

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Viral Quasispecies Evolution

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Domingo, Esteban, Sheldon, Julie, Perales, Celia·2012·Microbiology and Molecular Biology Reviews

DOI 10.1128/mmbr.05023-11PMC PMC3372249

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Abstract

SUMMARY: Evolution of RNA viruses occurs through disequilibria of collections of closely related mutant spectra or mutant clouds termed viral quasispecies. Here we review the origin of the quasispecies concept and some biological implications of quasispecies dynamics. Two main aspects are addressed: (i) mutant clouds as reservoirs of phenotypic variants for virus adaptability and (ii) the internal interactions that are established within mutant spectra that render a virus ensemble the unit of selection. The understanding of viruses as quasispecies has led to new antiviral designs, such as lethal mutagenesis, whose aim is to drive viruses toward low fitness values with limited chances of fitness recovery. The impact of quasispecies for three salient human pathogens, human immunodeficiency virus and the hepatitis B and C viruses, is reviewed, with emphasis on antiviral treatment strategies. Finally, extensions of quasispecies to nonviral systems are briefly mentioned to emphasize the broad applicability of quasispecies theory.

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Impact of Host Cell Line Adaptation on Quasispecies Composition and Glycosylation of Influenza A Virus Hemagglutinin
Rödig, J., Rapp, E., Höper, D. W., Genzel, Y., & Reichl, U. (2011) · PLoS ONE · doi:10.1371/journal.pone.0027989 · Cited by 43
Evolution of sex in RNA viruses
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Quasispecies Heterogeneity of the Carboxy-Terminal Part of the E2 Gene Including the PePHD and Sensitivity of Hepatitis C Virus 1b Isolates to Antiviral Therapy
Sarrazin, C., Bruckner, M., Herrmann, E. M., Rüster, B., Bruch, K., Roth, W. K., & Zeuzem, S. (2001) · Virology · doi:10.1006/viro.2001.1092 · Cited by 43
Prediction of Efficient Virological Response to Pegylated Interferon/Ribavirin Combination Therapy by NS5A Sequences of Hepatitis C Virus and Anti‐NS5A Antibodies in Pre‐Treatment Sera
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Fitness Increase of Memory Genomes in a Viral Quasispecies
Arias, A., Ruiz-Jarabo, C. M., Escarmı́s, C., & Domingo, E. (2004) · Journal of Molecular Biology · doi:10.1016/j.jmb.2004.03.061 · Cited by 42
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Combination of a mutagenic agent with a reverse transcriptase inhibitor results in systematic inhibition of HIV-1 infection
Tàpia, N., Fernández, G., Parera, M., Gómez‐Mariano, G., Clotet, B., Quiñones‐Mateu, M. E., Domingo, E., & Martı́nez, M. Á. (2005) · Virology · doi:10.1016/j.virol.2005.05.008 · Cited by 42
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Molecular Characterization of a Dual Inhibitory and Mutagenic Activity of 5-Fluorouridine Triphosphate on Viral RNA Synthesis. Implications for Lethal Mutagenesis
Agudo, R., Arias, A., Pariente, N., Perales, C., Escarmı́s, C., Jorge, A., Marina, A., & Domingo, E. (2008) · Journal of Molecular Biology · doi:10.1016/j.jmb.2008.07.033 · Cited by 42
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Mutant Viral Polymerase in the Transition of Virus to Error Catastrophe Identifies a Critical Site for RNA Binding
Arias, A., Agudo, R., Ferrer‐Orta, C., Pérez-Luque, R., Airaksinen, A., Brocchi, E., Domingo, E., Verdaguer, N., & Escarmı́s, C. (2005) · Journal of Molecular Biology · doi:10.1016/j.jmb.2005.09.022 · Cited by 42
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Isolation of Fidelity Variants of RNA Viruses and Characterization of Virus Mutation Frequency
Beaucourt, S. M., Bordería, A. V., Coffey, L. L., Gnädig, N. F., Sanz-Ramos, M., Beeharry, Y., & Vignuzzi, M. (2011) · Journal of Visualized Experiments · doi:10.3791/2953 · Cited by 42
Synthesis and Antiviral Evaluation of a Mutagenic and Non-Hydrogen Bonding Ribonucleoside Analogue: 1-β- d -Ribofuranosyl-3-nitropyrrole
Harki, D. A., Graci, J. D., Korneeva, V. S., Ghosh, S., Hong, Z., Cameron, C. E., & Peterson, B. R. (2002) · Biochemistry · doi:10.1021/bi026120w · Cited by 42
A model for the generation of multiple A to G transitions in the human respiratory syncytial virus genome: predicted RNA secondary structures as substrates for adenosine deaminases that act on RNA
Martínez, I., & Melero, J. A. (2002) · Journal of General Virology · doi:10.1099/0022-1317-83-6-1445 · Cited by 42
Virus population dynamics, fitness variations and the control of viral disease: an update
Domingo, E., Más, A., Yuste, E., Pariente, N., Sierra, S., Gutiérrez‐Rivas, M., & Menéndez‐Arias, L. (2001) · Birkhäuser Basel eBooks · doi:10.1007/978-3-0348-8308-5_2 · Cited by 41
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Contingent Neutrality in Competing Viral Populations
Quer, J., Hershey, C. L., Domingo, E., Holland, J. J., & Novella, I. S. (2001) · Journal of Virology · doi:10.1128/jvi.75.16.7315-7320.2001 · Cited by 41
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Quasispecies Spatial Models for RNA Viruses with Different Replication Modes and Infection Strategies
Josep Sardanyés, A., & Elena, S. F. (2011) · PLoS ONE · doi:10.1371/journal.pone.0024884 · Cited by 41
Mechanism of HBV genome variability and replication of HBV mutants
Tong, S. (2005) · Journal of Clinical Virology · doi:10.1016/s1386-6532(05)80023-x · Cited by 41
Antigenic properties and population stability of a foot-and-mouth disease virus with an altered Arg-Gly-Asp receptor-recognition motif
Ruiz-Jarabo, C. M., Sevilla, N., Dávila, M., Gómez‐Mariano, G., Baranowski, É., & Domingo, E. (1999) · Journal of General Virology · doi:10.1099/0022-1317-80-8-1899 · Cited by 41
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Hepatitis B virus: origin and evolution
Jazayeri, S. M., Alavian, S. M., & Carman, W. F. (2009) · Journal of Viral Hepatitis · doi:10.1111/j.1365-2893.2009.01193.x · Cited by 41
Reappearance of Founder Virus Sequence in Human Immunodeficiency Virus Type 1-Infected Patients
Karlsson, A. C., Gaines, H., Sällberg, M., Lindbäck, S., & Sönnerborg, A. B. (1999) · Journal of Virology · doi:10.1128/jvi.73.7.6191-6196.1999 · Cited by 40
Fitness Variations and their Impact on the Evolution of Antiretroviral Drug Resistance
Menéndez‐Arias, L., Martı́nez, M. Á., Quiñones‐Mateu, M. E., & Martínez‐Picado, J. (2003) · Current Drug Targets - Infectious Disorders · doi:10.2174/1568005033481033 · Cited by 40
Increased polymerase fidelity of lamivudine-resistant HIV-1 variants does not limit their evolutionary potential
Keulen, W., van Wijk, A., Schuurman, R., Berkhout, B., & Boucher, C. A. (1999) · AIDS · doi:10.1097/00002030-199907300-00011 · Cited by 40
Emergence and selection of HBV variants in an anti-HBe positive patient persistently infected with quasi-species
Alexopoulou, A. A., Karayiannis, P., Hadziyannis, S. J., Aiba, N., & Thomas, H. C. (1997) · Journal of Hepatology · doi:10.1016/s0168-8278(97)80238-3 · Cited by 40
Continued evolution of HIV-1 circulating in blood monocytes with antiretroviral therapy: genetic analysis of HIV-1 in monocytes and CD4+ T cells of patients with discontinued therapy
Llewellyn, N., Zioni, R., Zhu, H., Andrus, T., Xu, Y., Corey, L., & Zhu, T. (2006) · Journal of Leukocyte Biology · doi:10.1189/jlb.0306144 · Cited by 40
Variation of Hepatitis C Virus Hypervariable Region 1 in Immunocompromised Patients
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Viral Quasispecies: Dynamics, Interactions, and Pathogenesis**Dedicated to Manfred Eigen on the occasion of his 80th birthday, for the insights that his pioneer studies have represented for virology.
Domingo, E., Escarmı́s, C., Menéndez‐Arias, L., Perales, C., Herrera, M., Novella, I. S., & Holland, J. J. (2008) · Elsevier eBooks · doi:10.1016/b978-0-12-374153-0.00004-7 · Cited by 40
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Shared paramyxoviral glycoprotein architecture is adapted for diverse attachment strategies
Bowden, T. A., Crispin, M., Jones, E. Y., & Stuart, D. I. (2010) · Biochemical Society Transactions · doi:10.1042/bst0381349 · Cited by 39
Transitions in Understanding of RNA Viruses: A Historical Perspective
Holland, J. J. (2006) · Springer eBooks · doi:10.1007/3-540-26397-7_14 · Cited by 39
Hepatitis B Virus: Significance of Naturally Occurring Mutants
Blum, H. E. (1993) · Intervirology · doi:10.1159/000150294 · Cited by 39
Human Rhinovirus Type 54 Infection via Heparan Sulfate Is Less Efficient and Strictly Dependent on Low Endosomal pH
Khan, A. G., Pichler, J., Rosemann, A., & Blaas, D. (2007) · Journal of Virology · doi:10.1128/jvi.02160-06 · Cited by 39
Continuum of Change in RNA Virus Genomes
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Fidelity analysis of HIV‐1 reverse transcriptase mutants with an altered amino‐acid sequence at residues Leu74, Glu89, Tyr115, Tyr183 and Met184
Jonckheere, H., Clercq, E. D., & Anné, J. (2000) · European Journal of Biochemistry · doi:10.1046/j.1432-1327.2000.01272.x · Cited by 38
Counteracting Quasispecies Adaptability: Extinction of a Ribavirin-Resistant Virus Mutant by an Alternative Mutagenic Treatment
Perales, C., Agudo, R., & Domingo, E. (2009) · PLoS ONE · doi:10.1371/journal.pone.0005554 · Cited by 38
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Hepatitis C virus superinfection of liver grafts: a detailed analysis of early exclusion of non-dominant virus strains
Ramírez, S., Pérez‐del‐Pulgar, S., Carrión, J. A., Coto‐Llerena, M., Mensa, L., Dragun, J., García‐Valdecasas, J. C., Navasa, M., & Forns, X. (2010) · Journal of General Virology · doi:10.1099/vir.0.018929-0 · Cited by 38
HIV-1 acquires resistance to two classes of antiviral drugs through homologous recombination
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Synchronous Loss of Quasispecies Memory in Parallel Viral Lineages: A Deterministic Feature of Viral Quasispecies
Ruiz-Jarabo, C. M., Miller, E. L., Gómez‐Mariano, G., & Domingo, E. (2003) · Journal of Molecular Biology · doi:10.1016/j.jmb.2003.08.054 · Cited by 38
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Minor HIV-1 Variants with the K103N Resistance Mutation during Intermittent Efavirenz-Containing Antiretroviral Therapy and Virological Failure
Delobel, P., Saliou, A., Nicot, F., Dubois, M., Trancart, S., Tangre, P., Aboulker, J.-P., Taburet, A., Molina, J., Massip, P., et al. (2011) · PLoS ONE · doi:10.1371/journal.pone.0021655 · Cited by 38
Error threshold in RNA quasispecies models with complementation
Josep Sardanyés, A., & Elena, S. F. (2010) · Journal of Theoretical Biology · doi:10.1016/j.jtbi.2010.05.018 · Cited by 38
Stochastic extinction of viral infectivity through the action of defectors
Iranzo, J., & Manrubia, S. C. (2008) · Europhysics Letters (EPL) · doi:10.1209/0295-5075/85/18001 · Cited by 38
A single amino acid substitution in the transmembrane envelope glycoprotein of feline immunodeficiency virus alters cellular tropism
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Detection of Human Immunodeficiency Virus (HIV) Type 1 M184V and K103N Minority Variants in Patients with Primary HIV Infection
Toni, T. D., Asahchop, E. L., Moisi, D. D., Ntemgwa, M. L., Oliveira, M., Masquelier, B., BRENNER, B. G., & Wainberg, M. A. (2009) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.01494-08 · Cited by 38
The Picornaviruses
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HIV Infection-Related Premature Immunosenescence: High Rates of Immune Exhaustion After Short Time of Infection
Ferrando‐Martínez, S., Ruíz-Mateos, E., Romero-Sánchez, M. C., Muñoz‐Fernández, M. Á., Viciana, P., Genebat, M., & Leal, M. (2011) · Current HIV Research · doi:10.2174/157016211797636008 · Cited by 37
Monitoring Sequence Space as a Test for the Target of Selection in Viruses
Perales, C., Martı́n, V., Ruiz-Jarabo, C. M., & Domingo, E. (2004) · Journal of Molecular Biology · doi:10.1016/j.jmb.2004.10.066 · Cited by 37
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Sequence and Phenotypic Analysis for Resistance Monitoring in Hepatitis C Virus Drug Development: Recommendations From the HCV DRAG
Kwong, A. D., Nájera, I., Bechtel, J. T., Bowden, S., Fitzgibbon, J. E., Harrington, P. R., Kempf, D. J., Kieffer, T. L., Koletzki, D., Kukolj, G., et al. (2011) · Gastroenterology · doi:10.1053/j.gastro.2011.01.029 · Cited by 37
Tempo and mode of inhibitor–mutagen antiviral therapies: A multidisciplinary approach
Iranzo, J., Perales, C., Domingo, E., & Manrubia, S. C. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1110489108 · Cited by 37
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PAQ: Partition Analysis of Quasispecies
Baccam, P., Thompson, R. J., Fedrigo, O. D., Carpenter, S. L., & Cornette, J. L. (2001) · Bioinformatics · doi:10.1093/bioinformatics/17.1.16 · Cited by 37
Multidrug‐Resistant Variants of HIV Type 1 (HIV‐1) Can Exist in Cells as Defective Quasispecies and Be Rescued by Superinfection with Other Defective HIV‐1 Variants
Quan, Y., Liang, C., BRENNER, B. G., & Wainberg, M. A. (2009) · The Journal of Infectious Diseases · doi:10.1086/606117 · Cited by 37
Genetic consequences of a bottleneck and spatial genetic structure in the triggerplant Stylidium coroniforme (Stylidiaceae)
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Treatment of lethal pichinde virus infections in weanling LVG/Lak hamsters with ribavirin, ribamidine, selenazofurin, and ampligen
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Beneficial Effects of Population Bottlenecks in an RNA Virus Evolving at Increased Error Rate
Cases‐González, C. E., Arribas, M., Domingo, E., & Lázaro, E. (2008) · Journal of Molecular Biology · doi:10.1016/j.jmb.2008.10.014 · Cited by 36
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Mutability of prions
Li, J., Mahal, S. P., Demczyk, C. A., & Weissmann, C. (2011) · EMBO Reports · doi:10.1038/embor.2011.191 · Cited by 36
Evolution of the hypervariable region of hepatitis C virus
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Preexisting drug-resistance mutations reveal unique barriers to resistance for distinct antivirals
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Topology of evolving, mutagenized viral populations: quasispecies expansion, compression, and operation of negative selection
Ojosnegros, S., Agudo, R., Sierra, M., Briones, C., Sierra, S., López, C. G., Domingo, E., & Cristina, J. (2008) · BMC Evolutionary Biology · doi:10.1186/1471-2148-8-207 · Cited by 35
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Rapid viral quasispecies evolution: implications for vaccine and drug strategies
Novella, I. S., Domingo, E., & Holland, J. J. (1995) · Molecular Medicine Today · doi:10.1016/s1357-4310(95)91551-6 · Cited by 35
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Negative Effect of Genetic Bottlenecks on the Adaptability of Vesicular Stomatitis Virus
Novella, I. S. (2003) · Journal of Molecular Biology · doi:10.1016/j.jmb.2003.12.002 · Cited by 35
The 30th anniversary of quasispecies
Domingo, E., & Wain–Hobson, S. (2009) · EMBO Reports · doi:10.1038/embor.2009.61 · Cited by 35
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Noninfectious Retrovirus Particles Drive the Apobec3/Rfv3 Dependent Neutralizing Antibody Response
Smith, D. S., Guo, K., Barrett, B. S., Heilman, K. J., Evans, L. H., Hasenkrug, K. J., Greene, W. C., & Santiago, M. L. (2011) · PLoS Pathogens · doi:10.1371/journal.ppat.1002284 · Cited by 34
HIV Quasispecies Dynamics during Pro-Active Treatment Switching: Impact on Multi-Drug Resistance and Resistance Archiving in Latent Reservoirs
von Kleist, M., Menz, S., Stocker, H., Arastéh, K., Schütte, C., & Huisinga, W. (2011) · PLoS ONE · doi:10.1371/journal.pone.0018204 · Cited by 34
Nucleoside-analog resistance mutations in HIV-1 reverse transcriptase and their influence on polymerase fidelity and viral mutation rates
Rezende, L. F., & Prasad, V. R. (2004) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2004.02.025 · Cited by 34
Novel Mutations in a Tissue Culture-Adapted Hepatitis C Virus Strain Improve Infectious-Virus Stability and Markedly Enhance Infection Kinetics
Pokrovskii, M. V., Bush, C. O., Beran, R. K. F., Robinson, M. F., Cheng, G., Tirunagari, N., Fenaux, M., Greenstein, A. E., Zhong, W., Delaney, W. E., et al. (2011) · Journal of Virology · doi:10.1128/jvi.01760-10 · Cited by 34
Hepatitis C Virus Quasi‐Species Dynamics Predict Progression of Fibrosis after Liver Transplantation
Arenas, J. I., Gallegos-Orozco, J. F., Laskus, T., Wilkinson, J., Khatib, A., Fasola, C. G., Adair, D. M., Radkowski, M., Kibler, K. V., Nowicki, M., et al. (2004) · The Journal of Infectious Diseases · doi:10.1086/386338 · Cited by 34
Use of substituted and tandem‐repeated peptides to probe the relevance of the highly conserved RGD tripeptide in the immune response against foot‐and‐mouth disease virus
Novella, I. S., Borrego, B., Mateu, M. G., Domingo, E., Giralt, E., & Andreu, D. (1993) · FEBS Letters · doi:10.1016/0014-5793(93)80883-v · Cited by 33
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5-Fluorouracil in Lethal Mutagenesis of Foot-And-Mouth Disease Virus
Agudo, R., Arias, A., & Domingo, E. (2009) · Future Medicinal Chemistry · doi:10.4155/fmc.09.26 · Cited by 33
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Current Nucleos(t)ide Analogue Therapy for Chronic Hepatitis B
Kim, S. S., Cheong, J. Y., & Cho, S. W. (2011) · Gut and Liver · doi:10.5009/gnl.2011.5.3.278 · Cited by 33
Initial Fitness Recovery of HIV-1 Is Associated with Quasispecies Heterogeneity and Can Occur without Modifications in the Consensus Sequence
Bordería, A. V., Lorenzo-Redondo, R., Pernas, M., Casado, C., Alvaro, T., Domingo, E., & López‐Galíndez, C. (2010) · PLoS ONE · doi:10.1371/journal.pone.0010319 · Cited by 33
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Fitness Distributions in Exponentially Growing Asexual Populations
Manrubia, S. C., Lázaro, E., Pérez‐Mercader, J., Escarmı́s, C., & Domingo, E. (2003) · Physical Review Letters · doi:10.1103/physrevlett.90.188102 · Cited by 33
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Genetic and catalytic efficiency structure of an HCV protease quasispecies†
Franco, S., Parera, M., Aparicio, E., Clotet, B., & Martı́nez, M. Á. (2007) · Hepatology · doi:10.1002/hep.21623 · Cited by 33
Liver Transplantation With Hepatitis C Virus–Infected Graft: Interaction Between Donor and Recipient Viral Strains
Fan, X., Lang, D. M., Xu, Y., Lyra, A. C., Yusim, K., Everhart, J. E., Korber, B., Perelson, A. S., & Bisceglie, A. M. D. (2003) · Hepatology · doi:10.1053/jhep.2003.50264 · Cited by 33
Biological Effect of Muller's Ratchet: Distant Capsid Site Can Affect Picornavirus Protein Processing
Escarmı́s, C., Perales, C., & Domingo, E. (2009) · Journal of Virology · doi:10.1128/jvi.00538-09 · Cited by 33
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Effect of Bottlenecking on Evolution of the Nonstructural Protein 3 Gene of Hepatitis C Virus during Sexually Transmitted Acute Resolving Infection
Quer, J., Esteban, J. I., Cos, J., Sauleda, S., Ocaña, L., Martell, M., Otero, T., Cubero, M., Palou, E., Murillo, P., et al. (2005) · Journal of Virology · doi:10.1128/jvi.79.24.15131-15141.2005 · Cited by 33
Fitness Ranking of Individual Mutants Drives Patterns of Epistatic Interactions in HIV-1
Martínez, J. P., Bocharov, G. A., Ignatovich, A., Reiter, J., Dittmar, M. T., Wain–Hobson, S., & Meyerhans, A. (2011) · PLoS ONE · doi:10.1371/journal.pone.0018375 · Cited by 32
Positive Selection of Core 70Q Variant Genotype 1b Hepatitis C Virus Strains Induced by Pegylated Interferon and Ribavirin
Kurbanov, F., Tanaka, Y., Matsuura, K., Sugauchi, F., Elkady, A., Khan, A., Hasegawa, I., Ohno, T., Tokuda, H., & Mizokami, M. (2010) · The Journal of Infectious Diseases · doi:10.1086/652500 · Cited by 32
A comparison of pyrosequencing and neuraminidase inhibition assays for the detection of oseltamivir-resistant pandemic influenza A(H1N1) 2009 viruses
Deng, Y., Caldwell, N., Hurt, A. C., Shaw, T., Kelso, A., Chidlow, G. R., Williams, S. H., Smith, D. W., & Barr, I. (2011) · Antiviral Research · doi:10.1016/j.antiviral.2011.02.014 · Cited by 32
Hepatitis B virus drug resistance to current nucleos(t)ide analogs: Mechanisms and mutation sites
Deng, L., & Tang, H. (2011) · Hepatology Research · doi:10.1111/j.1872-034x.2011.00873.x · Cited by 32
Lethal Mutagenesis of Foot-and-Mouth Disease Virus Involves Shifts in Sequence Space
Perales, C., Henry, M., Domingo, E., Wain–Hobson, S., & Vartanian, J. (2011) · Journal of Virology · doi:10.1128/jvi.00716-11 · Cited by 32
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The Replication Cycle of RNA Bacteriophages
Valentine, R. C., Ward, R. L., & Strand, M. (1969) · Advances in virus research · doi:10.1016/s0065-3527(08)60873-8 · Cited by 31
Air sampling for respiratory disease agents in army recruits
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Epistasis among Deleterious Mutations in the HIV-1 Protease
Parera, M., Pérez‐Álvarez, N., Clotet, B., & Martı́nez, M. Á. (2009) · Journal of Molecular Biology · doi:10.1016/j.jmb.2009.07.015 · Cited by 31
Switching between raltegravir resistance pathways analyzed by deep sequencing
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Viral suppression of multiple escape mutants by de novo CD8+T cell responses in a human immunodeficiency virus-1 Infected elite suppressor
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Subpopulations of Equine Infectious Anemia Virus Rev Coexist In Vivo and Differ in Phenotype
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HIV-1 dual/mixed tropic isolates show different genetic and phenotypic characteristics and response to maraviroc in vitro
Svicher, V., Balestra, E., Cento, V., Sarmati, L., Dori, L., Vandenbroucke, I., D’Arrigo, R., Buonomini, A. R., Marck, H. G. V., Surdo, M., et al. (2011) · Antiviral Research · doi:10.1016/j.antiviral.2011.02.005 · Cited by 31
Vaccination as a strategy to reduce the emergence of amantadine- and rimantadine-resistant strains of A/Chick/Pennsylvania/83 (H5N2) influenza virus
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Viral quasispecies profiles as the result of the interplay of competition and cooperation
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Foot-and-Mouth Disease Virus Exhibits an Altered Tropism in the Presence of Specific Immunoglobulins, Enabling Productive Infection and Killing of Dendritic Cells
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The Impact of Rapid Evolution of Hepatitis Viruses
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Within-Host Dynamics of the Hepatitis C Virus Quasispecies Population in HIV-1/HCV Coinfected Patients
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Persistence of foot-and-mouth disease virus in cell culture revisited: implications for contingency in evolution
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See all 1,009

Authors: Domingo, E., Sheldon, J., & Perales, C.
Affiliations: Consejo Superior de Investigaciones Científicas (ES)
ORCID: Domingo, Esteban
Sheldon, Julie
Perales, Celia
Venue: Microbiology and Molecular Biology Reviews
Publisher: American Society for Microbiology
Published: 2012-06
Volume: 76
Issue: 2
Pages: 159-216
ISSN: 1092-2172 (ISSN-L)
1098-5557
DOI: 10.1128/mmbr.05023-11
PMC: PMC3372249
OpenAlex: W2073918065
Cited by: 1,009
References: 888
Citations by year: 2026: 51 · 2025: 38 · 2024: 56 · 2023: 55 · 2022: 58 · 2021: 130 · 2020: 104 · 2019: 96 · 2018: 76 · 2017: 76 · 2016: 77 · 2015: 75 · 2014: 63 · 2013: 38 · 2012: 15
FWCI: 7.47
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: journals.asm.org/non-commercial-tdm-license (tdm)
Locations: Microbiology and Molecular Biology Reviews (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
DIGITAL.CSIC (Spanish National Research Council (CSIC)) (submittedVersion)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
Physical Sciences › Mathematics › Applied Mathematics › Mathematical and Theoretical Epidemiology and Ecology Models
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA and protein synthesis mechanisms
Keywords: viral quasispecies, RNA viruses, units of selection, lethal mutagenesis, antiviral strategies, HIV, hepatitis B virus, hepatitis C virus
MeSH terms: Hepatitis B virus, HIV, Humans, RNA Viruses, Selection, Genetic, Virus Diseases, Genome, Viral, Evolution, Molecular

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