In vivo mutation rates and the landscape of fitness costs of HIV-1

Virus Evolution

Volumn 3, Issue 1, 2017, Pages

  Zanini, Fabio ^a,b   Puller, Vadim ^a   Brodin, Johanna ^c   Albert, Jan ^c   Neher, Richard A ^a  

^a MAX PLANCK INSTITUTE FOR DEVELOPMENTAL BIOLOGY   (Germany)

^b Stanford University   (United States)

^c KAROLINSKA INSTITUTE   (Sweden)

Author keywords

Evolution; fitness landscape; HIV 1; mutation rate

Indexed keywords

ADENINE; CYTOSINE; GUANINE; INTEGRASE INHIBITOR; NONNUCLEOSIDE REVERSE TRANSCRIPTASE INHIBITOR; RNA DIRECTED DNA POLYMERASE INHIBITOR; THYMINE;

ARTICLE; CONTROLLED STUDY; FITNESS COSTS LANDSCAPE; GENE MUTATION; GENE SEQUENCE; GENETIC REGULATION; GENETIC VARIATION; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; IN VIVO STUDY; LONGITUDINAL STUDY; MICROBIOLOGICAL PARAMETERS; MOLECULAR DYNAMICS; MOLECULAR EVOLUTION; MUTATIONAL ANALYSIS; NONHUMAN; NUCLEIC ACID BASE SUBSTITUTION; RNA STRUCTURE; VIRUS GENE; VIRUS GENOME; VIRUS REPLICATION;

EID: 85032658995     PISSN: None     EISSN: 20571577     Source Type: Journal    
DOI: 10.1093/ve/vex003     Document Type: Article

References (72)

1. Abbotts, J., Bebenek, K., Kunkel, T. A., and Wilson, S. H. (1993) 'Termination of processive synthesis on a natural DNA template is influenced by the sequence of the template-primer stem', Journal of Biological Chemistry, 268: 10312.
2. Abram, M. E., et al. (2010) 'Nature, position, and frequency of mutations made in a single cycle of HIV-1 replication', Journal of Virology, 84: 9864.
3. Acevedo, A., Brodsky, L., and Andino, R. (2014) 'Mutational and fitness landscapes of an RNA virus revealed through population sequencing', Nature, 505: 686.
4. Armitage, A. E., et al. (2012) 'APOBEC3g-Induced Hypermutation of Human Immunodeficiency Virus Type-1 Is Typically a Discrete All or Nothing Phenomenon', PLoS Genet, 8: E1002550.
5. Asquith, B., Edwards, C. T. T., Lipsitch, M., and McLean, A. R. (2006) 'Inefficient cytotoxic T lymphocyte-mediated killing of HIV-1-infected cells in vivo', PLoS Biology, 4: E90.
6. Bar, K. J., et al. (2012) 'Early Low-Titer Neutralizing Antibodies Impede HIV-1 Replication and Select for Virus Escape', PLoS Pathogene, 8: E1002721.
7. Bartha, I., et al. (2013) 'A genome-to-genome analysis of associations between human genetic variation, HIV-1 sequence diversity, and viral control', eLife Sciences, 2: E01123.
8. Barton, J. P., et al. (2016) 'Relative rate and location of intra-host HIV evolution to evade cellular immunity are predictable', Nature Communication, 7: 11660.
9. Brodin, J., et al. (2016) 'Establishment and stability of the latent HIV-1 DNA reservoir', eLife, 5: E18889. ISSN 2050-084X. doi: 10. 7554/eLife. 18889. URL https: //elifesciences. org/content/ 5/e18889v2
10. Carlson, J. M., et al. (2012) 'Phylogenetic Dependency Networks: Inferring Patterns of CTL Escape and Codon Covariation in HIV-1 Gag', Journal of Virology, JVI. 01998
11. Carlson, J. M., et al. (2008) 'Correlates of protective cellular immunity revealed by analysis of population-level immune escape pathways in HIV-1, PLoS Computational Biology, 4: E1000225
12. Chow, Y. K., et al. (1993) 'Use of evolutionary limitations of HIV-1 multidrug resistance to optimize therapy', Nature, 361: 650
13. Cong, M., Heneine, W., and Garcia-Lerma, J. G. (2007) 'The Fitness Cost of Mutations Associated with Human Immunodeficiency Virus Type 1 Drug Resistance Is Modulated by Mutational Interactions', Journal of Virology, 81: 3037
14. Cuevas, J. M., et al. (2015) 'Extremely High Mutation Rate of HIV-1 In Vivo', PLoS Biology, 13: E1002251.
15. Dahirel, V., et al. (2011) 'Coordinate linkage of HIV evolution reveals regions of immunological vulnerability', PNAS, 108: 11530
16. de Visser, J. A. G. M., and Krug, J. (2014) 'Empirical fitness landscapes and the predictability of evolution', Nature Reviews Genetics, 15: 480.
17. Deeks, S. G. (2003) 'Treatment of antiretroviral-drug-resistant HIV-1 infection', Lancet, 362: 2002.
18. Delviks-Frankenberry, K. A., et al. (2016) 'Minimal Contribution of APOBEC3-Induced G-to-A Hypermutation to HIV-1 Recombination and Genetic Variation', PLOS Pathogene, 12: E1005646.
19. Doud, M. B., Ashenberg, O., and Bloom, J. D. (2015) 'Site-Specific Amino Acid Preferences Are Mostly Conserved in Two Closely Related Protein Homologs', Molecular Biologoy and Evolution, 32: 2944.
20. Ferguson, A., et al. (2013) 'Translating HIV Sequences into Quantitative Fitness Landscapes Predicts Viral Vulnerabilities for Rational Immunogen Design', Immunity, 38: 606.
21. Friedrich, T. C., et al. (2004) 'Reversion of CTL escapevariant immunodeficiency viruses in vivo', Nature Medicine, 10: 275.
22. Ganusov, V. V., et al. (2011) 'Fitness costs and diversity of the cytotoxic T lymphocyte (CTL) response determine the rate of CTL escape during acute and chronic phases of HIV infection', Journal of Virology, 85: 10518.
23. Gianella, S., et al. (2011) 'Detection of Minority Resistance during Early HIV-1 Infection: Natural Variation and Spurious Detection rather than Transmission and Evolution of Multiple Viral Variants', Journal of Virology, 85: 8359.
24. Goonetilleke, N., et al. (2009) 'The first T cell response to transmitted/ founder virus contributes to the control of acute viremia in HIV-1 infection', Journal of Experimental Medicine, 206: 1253.
25. Haddox, H. K., Dingens, A. S., and Bloom, J. D. (2016) 'Experimental Estimation of the Effects of All Amino-Acid Mutations to HIVs Envelope Protein on Viral Replication in Cell Culture', PLoS Pathogens, 12: E1006114.
26. Haigh, J. (1978) 'The accumulation of deleterious genes in a population-Muller's Ratchet', Theoretical Population Biology, 14: 251.
27. Haldane, J. B. S. (1937) 'The Effect of Variation of Fitness', The American Naturalist, 71: 337.
28. Hartl, M., et al. (2016) 'Within-patient HIV mutation frequencies reveal fitness costs of CpG dinucleotides, drastic amino acid changes and GA mutations', bioRxiv, 057026.
29. Hedskog, C., et al. (2010) 'Dynamics of HIV-1 Quasispecies during Antiviral Treatment Dissected Using Ultra-Deep Pyrosequencing', PLoS One, 5: E11345.
30. Hinkley, T., et al. (2011) 'A systems analysis of mutational effects in HIV-1 protease and reverse transcriptase', Nature Genetics, 43: 487.
31. Holtz, C. M., and Mansky, L. M. (2013) 'Variation of HIV-1
32. Mutation Spectra among Cell', Journal of Virology, 87: 5296.
33. Johnson, J. A., et al. (2008) 'Minority HIV-1 Drug Resistance Mutations Are Present in Antiretroviral Treatment Naive Populations and Associate with Reduced Treatment Efficacy', PLoS Medicine, 5: E158.
34. Johnson, V., et al. (2011) '2011 update of the drug resistance mutations in HIV-1', Topics in Antiviral Medicine, 19: 156.
35. Joos, B., et al. (2008) 'HIV rebounds from latently infected cells, rather than from continuing low-level replication', PNAS, 105: 16725.
36. Kessinger, T. A., Perelson, A. S., and Neher, R. A. (2013) 'Inferring HIV escape rates from multi-locus genotype data', Frontiers in Immunology, 4: 252.
37. Kimura, M. (1964) 'Diffusion Models in Population Genetics', Journal of Applied Probability, 1: 177.
38. (1968) 'Evolutionary Rate at the Molecular Level', Nature, 2175129: 624.
39. LANL HIV sequence data base (2016) HXB2 Genome Annotation. http: //www. HIV. lanl. gov/content/sequence/HIV/MAP/ annotation. html
40. Leslie, A. J., et al. (2004) 'HIV evolution: CTL escape mutation and reversion after transmission', Nature Medicine, 10: 282.
41. Lewis, D. A., et al. (1999) 'Uniquely Altered DNA Replication Fidelity Conferred by an Amino Acid Change in the Nucleotide Binding Pocket of Human Immunodeficiency Virus Type 1
42. Reverse Transcriptase', Journal of Biological Chemistry, 274: 32924.
43. Li, B., et al. (2007) 'Rapid Reversion of Sequence Polymorphisms Dominates Early Human Immunodeficiency Virus Type 1 Evolution', Journal of Virology, 81: 193.
44. Li, G., et al. (2015) 'An integrated map of HIV genome-wide variation from a population perspective', Retrovirology, 12: 18.
45. Li, J. Z., et al. (2011) 'Low-frequency HIV-1 drug resistance mutations and risk of NNRTI-based antiretroviral treatment failure: A systematic review and pooled analysis', JAMA, 305: 1327.
46. Lu, K., et al. (2011) 'NMR detection of structures in the HIV-1 5-leader RNA that regulate genome packaging', Science, 334: 242.
47. Malim, M. H. (2009) 'APOBEC proteins and intrinsic resistance to HIV-1 infection', Philosophical Transactions of the Royal Society of London B: Biological Sciences, 364: 675.
48. Mansky, L. M., and Temin, H. M. (1995) 'Lower in vivo mutation rate of human immunodeficiency virus type 1 than that predicted from the fidelity of purified reverse transcriptase', Journal of Virology, 69: 5087.
49. Martinez-Picado, J., and Martinez, M. A. (2008) 'HIV-1 reverse transcriptase inhibitor resistance mutations and fitness: A view from the clinic and ex vivo', Virus Research Retroviral Reverse Transcription, 134: 104-12.
50. Mayrose, I., et al. (2013) 'Synonymous site conservation in the HIV-1 genome', BMC Evolutionary Biology, 13: 164.
51. Meyer, A. G., and Wilke, C. O. (2015) 'The utility of protein structure as a predictor of site-wise dN/dS varies widely among HIV-1 proteins', Journal of the Royal Society Interface, 12: 20150579.
52. Neher, R. A., and Leitner, T. (2010) 'Recombination rate and selection strength in HIV intra-patient evolution', PLoS Computational Biology, 6: E1000660.
53. Ngandu, N. K., et al. (2008) 'Extensive purifying selection acting on synonymous sites in HIV-1 Group M sequences', Virology Journal, 5: 160.
54. O'Neil, P. K., et al. (2002) 'Mutational analysis of HIV-1 long terminal repeats to explore the relative contribution of reverse transcriptase and RNA polymerase II to viral mutagenesis', Journal of Biological Chemistry, 277: 38053-61.
55. Parera, M., Fernndez, G., Clotet, B., and Martinez, M. A. (2007) 'HIV-1 Protease Catalytic Efficiency Effects Caused by Random Single Amino Acid Substitutions', Molecular Biology and Evolution, 24: 382.
56. Pereyra, F., et al. (2014) 'HIV Control Is Mediated in Part by CD8+ T-Cell Targeting of Specific Epitopes', Journal of Virology, 88: 12937.
57. Petropoulos, C. J., et al. (2000) 'A Novel Phenotypic Drug Susceptibility Assay for Human Immunodeficiency Virus Type 1', Antimicrobial Agents and Chemotherapy, 44: 920.
58. Pollom, E., et al. (2013) 'Comparison of SIV and HIV-1 Genomic RNA Structures Reveals Impact of Sequence Evolution on Conserved and Non-Conserved Structural Motifs', PLoS Pathogens, 9: E1003294.
59. Rihn, S. J., Hughes, J., Wilson, S. J., and Bieniasz, P. D. (2015) 'Uneven Genetic Robustness of HIV-1 Integrase', Journal of Virology, 89: 552.
60. Sanjuan, R. (2010) 'Mutational fitness effects in RNA and single-stranded DNA viruses: common patterns revealed by site-directed mutagenesis studies', Philosophical Transactions of the Royal Society of London B: Biological Sciences, 365: 1975.
61. Schneidewind, A., et al. (2009) 'Transmission and Long-Term Stability of Compensated CD8 Escape Mutations', Journal of Virology, 83: 3993.
62. Seifert, D., et al. (2015) 'A framework for inferring fitness landscapes of patient-derived viruses using quasispecies theory', Genetics, 199: 191.
63. Shekhar, K., et al. (2013) 'Spin models inferred from patientderived viral sequence data faithfully describe HIV fitness landscapes', Physics Review E, 88: 062705.
64. Siegfried, N. A., et al. (2014) 'RNA motif discovery by SHAPE and mutational profiling (SHAPE-MaP)', Nature Methods, 11: 959.
65. Smyth, R. P., Davenport, M. P., and Mak, J. (2012) 'The origin of genetic diversity in HIV-1', Virus Research, 169: 10.
66. Sükösd, Z., et al. (2015) 'Full-length RNA structure prediction of the HIV-1 genome reveals a conserved core domain', Nucleic Acids Research, 43: 10168-79.
67. Thyagarajan, B., and Bloom, J. D. (2014) 'The inherent mutational tolerance and antigenic evolvability of influenza hemagglutinin', eLife Sciences, 3: E03300.
68. Vabret, N., et al. (2014) 'Large-scale nucleotide optimization of simian immunodeficiency virus reduces its capacity to stimulate type I interferon in vitro', Journal of Virology, 88: 4161.
69. Walker, B., and McMichael, A. (2012) 'The T-cell response to HIV', Cold Spring Harbor Perspectives in Medicine, 2/11: A007054.
70. Wei, X., et al. (1995) 'Viral dynamics in human immunodeficiency virus type 1 infection', Nature, 373: 117.
71. Zanini, F., et al. (2015) 'Quantifying Selection against Synonymous Mutations in HIV-1 env Evolution', eLife Sciences, 4: E11282.
72. Zanini, F., and Neher, R. A. (2013) 'Population genomics of intrapatient HIV-1 evolution', Journal of Virology, 87: 11843.