Epistasis is an evolutionary process in which the effect of a nucleotide at one site in the genome is dependent on the presence or absence of particular nucleotides at other sites in the genome. One of the simplest types of epistasis occurs between Watson-Crick (WC) nucleotides in RNA secondary structures, which are under constraint to maintain base-pairing. In this study, I examine the effects of mutations at WC sites in the RNA secondary structure of HIV-1. I show that while epistasis plays a major role in the evolution of the HIV-1 secondary structure, different types of mutations have variable effects on fitness. Therefore, by favoring certain mutational trajectories, HIV-1 can evolve rapidly despite strong epistatic constraint on its RNA secondary structure.
Vyšlo v časopise: Strong Epistatic Selection on the RNA Secondary Structure of HIV. PLoS Pathog 10(9): e32767. doi:10.1371/journal.ppat.1004363 Kategorie: Research Article prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1004363
1. KimuraM (1985) The role of compensatory neutral mutations in molecular evolution. J Genet 64 : 7–19.
2. PhillipsPC (2008) Epistasis—the essential role of gene interactions in the structure and evolution of genetic systems. Nat Rev Genet 9 : 855–867.
3. KirbyDA, MuseSV, StephanW (1995) Maintenance of pre-mRNA secondary structure by epistatic selection. Proc Natl Acad Sci USA 92 : 9047–9051.
4. HuynenMA, HogewegP (1994) Pattern generation in molecular evolution: exploitation of the variation in RNA landscapes. J Mol Evol 39 : 71–79.
5. StephanW (1996) The rate of compensatory evolution. Genetics 144 : 419–426.
6. InnanH, StephanW (2001) Selection intensity against deleterious mutations in RNA secondary structures and the rate of compensatory nucleotide substitutions. Genetics 159 : 389–399.
7. GarcíaM, CrawfordJM, LatimerJW, Rivera-CruzE, PerdueML (1996) Heterogeneity in the haemagglutinin gene and emergence of the highly pathogenic phenotype among recent H5N2 avian influenza viruses from Mexico. J Gen Virol 77 : 1493–1504.
8. ContrerasAM, HiasaY, HeW, TerellaA, SchmidtEV, et al. (2002) Viral RNA mutations are region specific and increased by ribavirin in a full-length hepatitis C virus replication system. J Virol 76 : 8505–8517.
9. TuplinA, WoodJ, EvansDJ, PatelAH, SimmondsP (2002) Thermodynamic and phylogenetic prediction of RNA secondary structures in the coding region of hepatitis C virus. RNA 8 : 824–841.
10. LeSY, ChenJH, BraunMJ, GondaMA, MaizelJV (1988) Stability of RNA stem-loop structure and distribution of non-random structure in the human immunodeficiency virus (HIV-1). Nucleic Acids Res 16 : 5153–5168.
11. LeSY, ChenJH, ChatterjeeD, MaizelJV (1989) Sequence divergence and open regions of RNA secondary structures in the envelope regions of the 17 human immunodeficiency isolates. Nucleic acids Res 17 : 3275–3288.
12. YoshidaK, NakamuraM, OhnoT (1997) Mutations of the HIV type 1 V3 loop under selection pressure with neutralizing monoclonal antibody NM-01. AIDS Res Hum Retroviruses 13 : 1283–1290.
13. SanjuánR, BorderíaAV (2011) Interplay between RNA structure and protein evolution in HIV-1. Mol Biol Evol 28 : 1333–1338.
14. KniesJL, DangKK, VisionTJ, HoffmanNG, SwanstromR, et al. (2008) Compensatory evolution in RNA secondary structures increases substitution rate variation among sites. Mol Biol Evol 25 : 1778–1787.
15. MuseSV (1995) Evolutionary analyses of DNA sequences subject to constraints on secondary structure. Genetics 139 : 1429–1439.
16. PedersonJ, MeyerI, ForsbergR, SimmondsP, HeinJ (2004) A comparative method for finding and folding RNA secondary structures within protein-coding regions. Nucleic Acids Res 32 : 4925–4936.
17. ChenY, StephanW (2003) Compensatory evolution of a precursor messenger RNA secondary structure in the Drosophila melanogaster Adh gene. Proc Natl Acad Sci USA 100 : 11499–11504.
18. WoeseCR, GutellR, GuptaR, NollerHF (1983) Detailed analysis of the higher-order structure of 16S-like ribosomal ribonucleic acids. Microbiol Rev 47 : 621.
19. RoussetF, PelandakisM, SolignacM (1991) Evolution of compensatory substitutions through G.U intermediate states in Drosophila rRNA. Proc Natl Acad Sci USA 88 : 10032–10036.
20. DutheilJY, JossinetF, WestofE (2010) Base pairing constraints drive structural epistasis in ribosomal RNA sequences. Mol Biol Evol 27 : 1868–1876.
21. KernAD, KondrashovFA (2004) Mechanisms and convergence of compensatory evolution in mammalian mitochondrial tRNAs. Nature Genet 36 : 1207–1212.
22. MeerMV, KondrashovAS, Artzy-RandrupY, KondrashovFA (2010) Compensatory evolution in mitochondrial tRNAs navigates valleys of low fitness. Nature 464 : 279–282.
23. OlsthoornRCL, LicisN, van DuinJ (1994) Leeway and constraints in the forced evolution of a regulatory RNA helix. EMBO J 13 : 2660–2668.
24. BerkhoutB (1991) Structural features in TAR RNA of human and simian immunodeficiency viruses: a phylogenetic approach. Nucleic Acids Res 20 : 27–31.
25. BerkhoutB, JeangKT (1991) Detailed mutational analysis of TAR RNA: critical spacing between the bulge and loop recognition domains. Nucleic Acids Res 19 : 6169–6176.
26. HarrisonGP, LeverAM (1992) The human immunodeficiency virus type 1 packaging signal and major splice donor region have a conserved stable secondary structure. J Virol 66 : 4144–4153.
27. KlaverB, BerkhoutB (1994) Evolution of a disrupted TAR RNA hairpin structure in the HIV-1 virus. EMBO J 13 : 2650–2659.
28. EmilianiS, Van LintC, FischleW, ParasPJr, OttM, et al. (1996) A point mutation in the HIV-1 Tat responsive element is associated with postintegration latency. Proc Natl Acad Sci USA 93 : 6377–6381.
29. McBrideMS, PanganibanAT (1996) The human immunodeficiency virus type 1 encapsidation site is a multipartite RNA element composed of functional hairpin structures. J Virol 70 : 2963–2973.
30. BerkhoutB, KlaverB, DasAT (1997) Forced evolution of a regulatory RNA helix in the HIV-1 genome. Nucleic Acids Res 25 : 94–947.
31. CleverJL, ParslowTG (1997) Mutant human immunodeficiency virus type 1 genomes with defects in RNA dimerization or encapsidation. J Virol 71 : 3407–3414.
32. DasAT, KlaverB, BerkhoutB (1999) A hairpin structure in the R region of the human immunodeficiency virus type 1 RNA genome is instrumental in polyadenylation site selection. J Virol 73 : 81–91.
33. HarrichD, HookerCW, ParryE (2000) The human immunodeficiency virus type 1 TAR RNA upper stem-loop plays distinct roles in reverse transcription and RNA packaging. J Virol 74 : 5639–5646.
34. KulinskiT, OlejniczakM, HuthoffH, BieleckiL, Pachulska-WieczorekK, et al. (2003) The apical loop of the HIV-1 TAR RNA hairpin is stabilized by a cross-loop base pair. J Biol Chem 278 : 38892–38901.
35. CobrinikD, SoskeyL, LeisJA (1988) Retroviral RNA secondary structure required for efficient initiation of reverse transcription. J Virol 62 : 3622–3630.
36. WilsonW, BraddockM, AdamsSE, RathjenPD, KingsmanSM, et al. (1988) HIV expression strategies: ribosomal frameshifting is directed by a short sequence in both mammalian and yeast systems. Cell 55 : 1159–1169.
37. CassanM, BerteauxV, AngrandPO, RoussetJP (1990) Expression vectors for quantifying in vivo translational ambiguity: their potential use to analyze frameshifting at the HIV gag-pol junction. Res Virol 141 : 597–610.
38. ParkinNT, ChamorroM, VarmusHE (1992) Human immunodeficiency virus type 1 gag-pol frameshifting is dependent on downstream mRNA secondary structure: demonstration by expression in vivo. J Virol 66 : 5147–5151.
39. JacquenetS, RopersD, BilodeauPS, DamierL, MouginA, et al. (2001) Conserved stem-loop structures in the HIV-1 RNA region containing the A3 3′ splic site and its cis-regulatory element: possible involvement in RNA splicing. Nucleic Acids Res 29 : 464–478.
40. GarciaJA, HarrichD, SoultanakisE, WuF, MitsuyasuR, et al. (1989) Human immunodeficiency virus type 1 LTR TATA and TAR region sequences required for transcriptional regulation. EMBO J 8 : 765–778.
41. AbbinkTEM, BerkhoutB (2008) RNA structure modulates splicing efficiency at the human immunodeficiency virus type I major splice donor. J Virol 82 : 3090–3098.
42. SchragSJ, PerrotV, LevinBR (1997) Adaptation to the fitness costs of antibiotic resistance in Escherichia coli. Proc R Soc Lond B Biol Sci 264 : 1287–1291.
43. Maisnier-PatinS, BergOG, LiljasL, AndersonDI (2002) Compensatory adaptation to the deleterious effect of antibiotic resistance in Salmonella typhimurium. Mol Microbiol 46 : 355–366.
44. HoffmanNG, SchifferCA, SwanstromR (2005) Covariation of amino acid positions in HIV-1 protease. Virology 331 : 206–207.
45. VaraniG, McClainWH (2000) The GU wobble base pair. EMBO Rep 1 : 18–23.
46. WattsJM, DangKK, GorelickRJ, LeonardCW, BessCWJr, et al. (2009) Architecture and secondary structure of an entire HIV-1 RNA genome. Nature 460 : 711–719.
47. PerelsonAS, RibeiroRM (2008) Estimating drug efficacy and viral dynamic parameters: HIV and HCV. Statist Med 27 : 4647–4657.
48. SunyaevS, RamenskyV, KochI, LatheW3rd, KondrashovAS, et al. (2001) Prediction of deleterious human alleles. Hum Mol Genet 10 : 591–597.
49. EddySR (1995) Multiple alignment using hidden Markov models. ISMB 3 : 114–120.
50. GaschenB, KuikenC, KorberB, FoleyB (2001) Retrieval and on-the-fly alignment of sequence fragments from the HIV database. Bioinformatics 17 : 415–418.
51. ManskyLM, TeminHM (2005) Lower in vivo mutation rate of human immunodeficiency virus type 1 than predicted from the fidelity of purified reverse transcriptase. J Virol 69 : 5087.
52. R Development Core Team (2009) R: A language and environment for statistical computing. R Foundation for Statistical Computing. Vienna, Austria.
Zvýšte si kvalifikáciu online z pohodlia domova
Nemáte účet? Registrujte sa
Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.
