HIV-1 and HIV-2 exhibit similar mutation frequencies and spectra in the absence of G-to-A hypermutation

Retrovirology

Volumn 12, Issue 1, 2015, Pages

  Rawson, Jonathan M O ^a,b   Landman, Sean R ^c   Reilly, Cavan S ^a,d   Mansky, Louis M ^a,b  

^a UNIVERSITY OF MINNESOTA   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

^c University of Minnesota   (United States)

^d UNIVERSITY OF MINNESOTA   (United States)

Author keywords

HIV 1; HIV 2; Hypermutation; Viral evolution; Viral mutagenesis

Indexed keywords

ADENINE; GUANINE; HYDROLASE; PROTEIN APOBEC3; RNA DIRECTED DNA POLYMERASE; UNCLASSIFIED DRUG; VIF PROTEIN; APOBEC3 PROTEIN, HUMAN; CYTOSINE DEAMINASE;

AMINO ACID SUBSTITUTION; AMPLICON; ANALYTICAL ERROR; ARTICLE; CONTROLLED STUDY; EMBRYO; HIGH THROUGHPUT SEQUENCING; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 2; MUTAGENESIS; MUTATION RATE; NONHUMAN; POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION; VIRUS REPLICATION; DNA SEQUENCE; GENETICS; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; POINT MUTATION; REGULATOR GENE; TUMOR CELL LINE; VIROLOGY;

HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 2;

CELL LINE, TUMOR; CYTOSINE DEAMINASE; GENES, VPR; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HIV INFECTIONS; HIV-1; HIV-2; HUMANS; MUTATION RATE; POINT MUTATION; SEQUENCE ANALYSIS, DNA; VIF GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; VIRUS REPLICATION;

EID: 84936776340     PISSN: None     EISSN: 17424690     Source Type: Journal    
DOI: 10.1186/s12977-015-0180-6     Document Type: Article

References (76)

1. Mansky LM, Temin HM (1995) Lower in vivo mutation rate of human immunodeficiency virus type 1 than that predicted from the fidelity of purified reverse transcriptase. J Virol 69(8):5087-5094
2. Mansky LM (1996) Forward mutation rate of human immunodeficiency virus type 1 in a T lymphoid cell line. AIDS Res Hum Retroviruses 12(4):307-314
3. O'Neil PK, Sun G, Yu H, Ron Y, Dougherty JP, Preston BD (2002) Mutational analysis of HIV-1 long terminal repeats to explore the relative contribution of reverse transcriptase and RNA polymerase II to viral mutagenesis. J Biol Chem 277(41):38053-38061. doi: 10.1074/jbc.M204774200
4. Abram ME, Ferris AL, Shao W, Alvord WG, Hughes SH (2010) Nature, position, and frequency of mutations made in a single cycle of HIV-1 replication. J Virol 84(19):9864-9878. doi: 10.1128/JVI.00915-10
5. Schlub TE, Grimm AJ, Smyth RP, Cromer D, Chopra A, Mallal S et al (2014) 15-20% of HIV substitution mutations are associated with recombination. J Virol. doi: 10.1128/JVI.03136-13
6. McCulloch SD, Kunkel TA (2008) The fidelity of DNA synthesis by eukaryotic replicative and translesion synthesis polymerases. Cell Res 18(1):148-161. doi: 10.1038/cr.2008.4
7. Menendez-Arias L (2009) Mutation rates and intrinsic fidelity of retroviral reverse transcriptases. Viruses 1(3):1137-1165. doi: 10.3390/v1031137
8. Svarovskaia ES, Cheslock SR, Zhang WH, Hu WS, Pathak VK (2003) Retroviral mutation rates and reverse transcriptase fidelity. Front Biosci 8:d117-d134
9. Desimmie BA, Delviks-Frankenberrry KA, Burdick RC, Qi D, Izumi T, Pathak VK (2014) Multiple APOBEC3 restriction factors for HIV-1 and one Vif to rule them all. J Mol Biol 426(6):1220-1245. doi: 10.1016/j.jmb.2013.10.033
10. Refsland EW, Harris RS (2013) The APOBEC3 family of retroelement restriction factors. Curr Top Microbiol Immunol 371:1-27. doi: 10.1007/978-3-642-37765-5_1
11. Mulder LC, Harari A, Simon V (2008) Cytidine deamination induced HIV-1 drug resistance. Proc Natl Acad Sci USA 105(14):5501-5506. doi: 10.1073/pnas.0710190105
12. Kim EY, Bhattacharya T, Kunstman K, Swantek P, Koning FA, Malim MH et al (2010) Human APOBEC3G-mediated editing can promote HIV-1 sequence diversification and accelerate adaptation to selective pressure. J Virol 84(19):10402-10405. doi: 10.1128/JVI.01223-10
13. Sadler HA, Stenglein MD, Harris RS, Mansky LM (2010) APOBEC3G contributes to HIV-1 variation through sublethal mutagenesis. J Virol 84(14):7396-7404. doi: 10.1128/JVI.00056-10
14. Kim EY, Lorenzo-Redondo R, Little SJ, Chung YS, Phalora PK, Maljkovic Berry I et al (2014) Human APOBEC3 induced mutation of human immunodeficiency virus type-1 contributes to adaptation and evolution in natural infection. PLoS Pathog 10(7):e1004281. doi: 10.1371/journal.ppat.1004281
15. Sato K, Takeuchi JS, Misawa N, Izumi T, Kobayashi T, Kimura Y et al (2014) APOBEC3D and APOBEC3F potently promote HIV-1 diversification and evolution in humanized mouse model. PLoS Pathog 10(10):e1004453. doi: 10.1371/journal.ppat.1004453
16. Martinez MA, Vartanian JP, Wain-Hobson S (1994) Hypermutagenesis of RNA using human immunodeficiency virus type 1 reverse transcriptase and biased dNTP concentrations. Proc Natl Acad Sci USA 91(25):11787-11791
17. Mansky LM (1996) The mutation rate of human immunodeficiency virus type 1 is influenced by the vpr gene. Virology 222(2):391-400. doi: 10.1006/viro.1996.0436
18. Mansky LM, Le Rouzic E, Benichou S, Gajary LC (2003) Influence of reverse transcriptase variants, drugs, and Vpr on human immunodeficiency virus type 1 mutant frequencies. J Virol 77(3):2071-2080
19. Holtz CM, Mansky LM (2013) Variation of HIV-1 mutation spectra among cell types. J Virol 87(9):5296-5299. doi: 10.1128/JVI.03576-12
20. de Silva TI, Cotten M, Rowland-Jones SL (2008) HIV-2: the forgotten AIDS virus. Trends Microbiol 16(12):588-595. doi: 10.1016/j.tim.2008.09.003
21. Campbell-Yesufu OT, Gandhi RT (2011) Update on human immunodeficiency virus (HIV)-2 infection. Clin Infect Dis 52(6):780-787. doi: 10.1093/cid/ciq248
22. Coffey LL, Beeharry Y, Borderia AV, Blanc H, Vignuzzi M (2011) Arbovirus high fidelity variant loses fitness in mosquitoes and mice. Proc Natl Acad Sci USA 108(38):16038-16043. doi: 10.1073/pnas.1111650108
23. Meng T, Kwang J (2014) Attenuation of human enterovirus 71 high-replication-fidelity variants in AG129 mice. J Virol 88(10):5803-5815. doi: 10.1128/JVI.00289-14
24. Vignuzzi M, Stone JK, Arnold JJ, Cameron CE, Andino R (2006) Quasispecies diversity determines pathogenesis through cooperative interactions in a viral population. Nature 439(7074):344-348. doi: 10.1038/nature04388
25. Vignuzzi M, Wendt E, Andino R (2008) Engineering attenuated virus vaccines by controlling replication fidelity. Nat Med 14(2):154-161. doi: 10.1038/nm1726
26. Zeng J, Wang H, Xie X, Li C, Zhou G, Yang D et al (2014) Ribavirin-resistant variants of foot-and-mouth disease virus: the effect of restricted quasispecies diversity on viral virulence. J Virol 88(8):4008-4020. doi: 10.1128/JVI.03594-13
27. Lemey P, Kosakovsky Pond SL, Drummond AJ, Pybus OG, Shapiro B, Barroso H et al (2007) Synonymous substitution rates predict HIV disease progression as a result of underlying replication dynamics. PLoS Comput Biol 3(2):e29. doi: 10.1371/journal.pcbi.0030029
28. MacNeil A, Sankale JL, Meloni ST, Sarr AD, Mboup S, Kanki P (2007) Long-term intrapatient viral evolution during HIV-2 infection. J Infect Dis 195(5):726-733. doi: 10.1086/511308
29. Skar H, Borrego P, Wallstrom TC, Mild M, Marcelino JM, Barroso H et al (2010) HIV-2 genetic evolution in patients with advanced disease is faster than that in matched HIV-1 patients. J Virol 84(14):7412-7415. doi: 10.1128/JVI.02548-09
30. Matamoros T, Kim B, Menendez-Arias L (2008) Mechanistic insights into the role of Val75 of HIV-1 reverse transcriptase in misinsertion and mispair extension fidelity of DNA synthesis. J Mol Biol 375(5):1234-1248. doi: 10.1016/j.jmb.2007.11.021
31. Alvarez M, Matamoros T, Menendez-Arias L (2009) Increased thermostability and fidelity of DNA synthesis of wild-type and mutant HIV-1 group O reverse transcriptases. J Mol Biol 392(4):872-884. doi: 10.1016/j.jmb.2009.07.081
32. Ribeiro AC, Maia e Silva A, Santa-Marta M, Pombo A, Moniz-Pereira J, Goncalves J et al (2005) Functional analysis of Vif protein shows less restriction of human immunodeficiency virus type 2 by APOBEC3G. J Virol 79(2):823-833. doi: 10.1128/JVI.79.2.823-833.2005
33. Schirmer M, Ijaz UZ, D'Amore R, Hall N, Sloan WT, Quince C (2015) Insight into biases and sequencing errors for amplicon sequencing with the Illumina MiSeq platform. Nucleic Acids Res 43(6):e37. doi: 10.1093/nar/gku1341
34. Dohm JC, Lottaz C, Borodina T, Himmelbauer H (2008) Substantial biases in ultra-short read data sets from high-throughput DNA sequencing. Nucleic Acids Res 36(16):e105. doi: 10.1093/nar/gkn425
35. Minoche AE, Dohm JC, Himmelbauer H (2011) Evaluation of genomic high-throughput sequencing data generated on Illumina HiSeq and genome analyzer systems. Genome Biol 12(11):R112. doi: 10.1186/gb-2011-12-11-r112
36. Abnizova I, Leonard S, Skelly T, Brown A, Jackson D, Gourtovaia M et al (2012) Analysis of context-dependent errors for illumina sequencing. J Bioinform Comput Biol. 10(2):1241005. doi: 10.1142/S0219720012410053
37. Judo MS, Wedel AB, Wilson C (1998) Stimulation and suppression of PCR-mediated recombination. Nucleic Acids Res 26(7):1819-1825
38. Smyth RP, Schlub TE, Grimm A, Venturi V, Chopra A, Mallal S et al (2010) Reducing chimera formation during PCR amplification to ensure accurate genotyping. Gene 469(1-2):45-51. doi: 10.1016/j.gene.2010.08.009
39. Thompson JR, Marcelino LA, Polz MF (2002) Heteroduplexes in mixed-template amplifications: formation, consequence and elimination by 'reconditioning PCR'. Nucleic Acids Res 30(9):2083-2088
40. Mansky LM, Preveral S, Selig L, Benarous R, Benichou S (2000) The interaction of vpr with uracil DNA glycosylase modulates the human immunodeficiency virus type 1 In vivo mutation rate. J Virol 74(15):7039-7047
41. Abram ME, Ferris AL, Das K, Quinones O, Shao W, Tuske S et al (2014) Mutations in HIV-1 reverse transcriptase affect the errors made in a single cycle of viral replication. J Virol 88(13):7589-7601. doi: 10.1128/JVI.00302-14
42. Bishop KN, Holmes RK, Sheehy AM, Davidson NO, Cho SJ, Malim MH (2004) Cytidine deamination of retroviral DNA by diverse APOBEC proteins. Curr Biol 14(15):1392-1396. doi: 10.1016/j.cub.2004.06.057
43. Harris RS, Bishop KN, Sheehy AM, Craig HM, Petersen-Mahrt SK, Watt IN et al (2003) DNA deamination mediates innate immunity to retroviral infection. Cell 113(6):803-809
44. Liddament MT, Brown WL, Schumacher AJ, Harris RS (2004) APOBEC3F properties and hypermutation preferences indicate activity against HIV-1 in vivo. Curr Biol 14(15):1385-1391. doi: 10.1016/j.cub.2004.06.050
45. Harari A, Ooms M, Mulder LC, Simon V (2009) Polymorphisms and splice variants influence the antiretroviral activity of human APOBEC3H. J Virol 83(1):295-303. doi: 10.1128/JVI.01665-08
46. Nakamura K, Oshima T, Morimoto T, Ikeda S, Yoshikawa H, Shiwa Y et al (2011) Sequence-specific error profile of Illumina sequencers. Nucleic Acids Res 39(13):e90. doi: 10.1093/nar/gkr344
47. Quail MA, Smith M, Coupland P, Otto TD, Harris SR, Connor TR et al (2012) A tale of three next generation sequencing platforms: comparison of Ion Torrent, Pacific Biosciences and Illumina MiSeq sequencers. BMC Genom 13:341. doi: 10.1186/1471-2164-13-341
48. Ross MG, Russ C, Costello M, Hollinger A, Lennon NJ, Hegarty R et al (2013) Characterizing and measuring bias in sequence data. Genome Biol 14(5):R51. doi: 10.1186/gb-2013-14-5-r51
49. Van den Hoecke S, Verhelst J, Vuylsteke M, Saelens X (2015) Analysis of the genetic diversity of influenza A viruses using next-generation DNA sequencing. BMC Genom 16:79. doi: 10.1186/s12864-015-1284-z
50. Schmitt MW, Kennedy SR, Salk JJ, Fox EJ, Hiatt JB, Loeb LA (2012) Detection of ultra-rare mutations by next-generation sequencing. Proc Natl Acad Sci USA 109(36):14508-14513. doi: 10.1073/pnas.1208715109
51. Huang KJ, Wooley DP (2005) A new cell-based assay for measuring the forward mutation rate of HIV-1. J Virol Methods 124(1-2):95-104. doi: 10.1016/j.jviromet.2004.11.010
52. Langlois MA, Beale RC, Conticello SG, Neuberger MS (2005) Mutational comparison of the single-domained APOBEC3C and double-domained APOBEC3F/G anti-retroviral cytidine deaminases provides insight into their DNA target site specificities. Nucleic Acids Res 33(6):1913-1923. doi: 10.1093/nar/gki343
53. Piroozmand A, Yamamoto Y, Khamsri B, Fujita M, Uchiyama T, Adachi A (2007) Generation and characterization of APOBEC3G-positive 293T cells for HIV-1 Vif study. J Med Invest 54(1-2):154-158
54. Doehle BP, Schafer A, Cullen BR (2005) Human APOBEC3B is a potent inhibitor of HIV-1 infectivity and is resistant to HIV-1 Vif. Virology 339(2):281-288. doi: 10.1016/j.virol.2005.06.005
55. Simon V, Zennou V, Murray D, Huang Y, Ho DD, Bieniasz PD (2005) Natural variation in Vif: differential impact on APOBEC3G/3F and a potential role in HIV-1 diversification. PLoS Pathog 1(1):e6. doi: 10.1371/journal.ppat.0010006
56. Binka M, Ooms M, Steward M, Simon V (2012) The activity spectrum of Vif from multiple HIV-1 subtypes against APOBEC3G, APOBEC3F, and APOBEC3H. J Virol 86(1):49-59. doi: 10.1128/JVI.06082-11
57. Iwabu Y, Kinomoto M, Tatsumi M, Fujita H, Shimura M, Tanaka Y et al (2010) Differential anti-APOBEC3G activity of HIV-1 Vif proteins derived from different subtypes. J Biol Chem 285(46):35350-35358. doi: 10.1074/jbc.M110.173286
58. Bourara K, Liegler TJ, Grant RM (2007) Target cell APOBEC3C can induce limited G-to-A mutation in HIV-1. PLoS Pathog 3(10):1477-1485. doi: 10.1371/journal.ppat.0030153
59. Rawson JM, Heineman RH, Beach LB, Martin JL, Schnettler EK, Dapp MJ et al (2013) 5,6-Dihydro-5-aza-2'-deoxycytidine potentiates the anti-HIV-1 activity of ribonucleotide reductase inhibitors. Bioorg Med Chem 21(22):7222-7228. doi: 10.1016/j.bmc.2013.08.023
60. Smith JL, Izumi T, Borbet TC, Hagedorn AN, Pathak VK (2014) HIV-1 and HIV-2 Vif interact with human APOBEC3 proteins using completely different determinants. J Virol 88(17):9893-9908. doi: 10.1128/JVI.01318-14
61. Beale RC, Petersen-Mahrt SK, Watt IN, Harris RS, Rada C, Neuberger MS (2004) Comparison of the differential context-dependence of DNA deamination by APOBEC enzymes: correlation with mutation spectra in vivo. J Mol Biol 337(3):585-596. doi: 10.1016/j.jmb.2004.01.046
62. Holtz CM, Sadler HA, Mansky LM (2013) APOBEC3G cytosine deamination hotspots are defined by both sequence context and single-stranded DNA secondary structure. Nucleic Acids Res 41(12):6139-6148. doi: 10.1093/nar/gkt246
63. Wiegand HL, Doehle BP, Bogerd HP, Cullen BR (2004) A second human antiretroviral factor, APOBEC3F, is suppressed by the HIV-1 and HIV-2 Vif proteins. EMBO J 23(12):2451-2458. doi: 10.1038/sj.emboj.7600246
64. Yu Q, Konig R, Pillai S, Chiles K, Kearney M, Palmer S et al (2004) Single-strand specificity of APOBEC3G accounts for minus-strand deamination of the HIV genome. Nat Struct Mol Biol 11(5):435-442. doi: 10.1038/nsmb758
65. Suspene R, Rusniok C, Vartanian JP, Wain-Hobson S (2006) Twin gradients in APOBEC3 edited HIV-1 DNA reflect the dynamics of lentiviral replication. Nucleic Acids Res 34(17):4677-4684. doi: 10.1093/nar/gkl555
66. Kong R, Li H, Bibollet-Ruche F, Decker JM, Zheng NN, Gottlieb GS et al (2012) Broad and potent neutralizing antibody responses elicited in natural HIV-2 infection. J Virol 86(2):947-960. doi: 10.1128/JVI.06155-11
67. Dapp MJ, Clouser CL, Patterson S, Mansky LM (2009) 5-Azacytidine can induce lethal mutagenesis in human immunodeficiency virus type 1. J Virol 83(22):11950-11958. doi: 10.1128/JVI.01406-09
68. Chen J, Powell D, Hu WS (2006) High frequency of genetic recombination is a common feature of primate lentivirus replication. J Virol 80(19):9651-9658. doi: 10.1128/JVI.00936-06
69. Abada P, Noble B, Cannon PM (2005) Functional domains within the human immunodeficiency virus type 2 envelope protein required to enhance virus production. J Virol 79(6):3627-3638. doi: 10.1128/JVI.79.6.3627-3638.2005
70. Vodicka MA, Goh WC, Wu LI, Rogel ME, Bartz SR, Schweickart VL et al (1997) Indicator cell lines for detection of primary strains of human and simian immunodeficiency viruses. Virology 233(1):193-198. doi: 10.1006/viro.1997.8606
71. Boussif O, Lezoualc'h F, Zanta MA, Mergny MD, Scherman D, Demeneix B et al (1995) A versatile vector for gene and oligonucleotide transfer into cells in culture and in vivo: polyethylenimine. Proc Natl Acad Sci USA. 92(16):7297-7301
72. Kutner RH, Zhang XY, Reiser J (2009) Production, concentration and titration of pseudotyped HIV-1-based lentiviral vectors. Nat Protoc 4(4):495-505. doi: 10.1038/nprot.2009.22
73. Tsai H, Missirian V, Ngo KJ, Tran RK, Chan SR, Sundaresan V et al (2013) Production of a high-efficiency TILLING population through polyploidization. Plant Physiol 161(4):1604-1614. doi: 10.1104/pp.112.213256
74. Wu TD, Nacu S (2010) Fast and SNP-tolerant detection of complex variants and splicing in short reads. Bioinformatics 26(7):873-881. doi: 10.1093/bioinformatics/btq057
75. McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A et al (2010) The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 20(9):1297-1303. doi: 10.1101/gr.107524.110
76. Wolfinger R, O'Connell M (1993) Generalized linear mixed models: a pseudo-likelihood approach. J Stat Comput Simul 48:233-243