Tautomerism provides a molecular explanation for the mutagenic properties of the anti-HIV nucleoside 5-aza-5,6-dihydro-2′-deoxycytidine

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 32, 2014, Pages

  Li, Deyu ^a,b   Fedeles, Bogdan I ^a,b   Singh, Vipender ^a,b   Peng, Chunte Sam ^a,c   Silvestre, Katherine J ^a   Simi, Allison K ^a   Simpson, Jeffrey H ^a   Tokmakoff, Andrei ^a,c   Essigmann, John M ^a,b  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b Massachusetts Institute of Technology Cambridge   (United States)

^c UNIVERSITY OF CHICAGO   (United States)

Author keywords

KP1461; Site specific mutagenesis; Spectral deconvolution; Viral decay acceleration; Viral extinction

Indexed keywords

5 AZA 5,6 DIHYDRO 2' DEOXYCYTIDINE; ANTI HUMAN IMMUNODEFICIENCY VIRUS AGENT; ANTIVIRUS AGENT; KP 1212; NUCLEIC ACID BASE; NUCLEOSIDE; NUCLEOSIDE ANALOG; UNCLASSIFIED DRUG; VIRUS VECTOR;

ARTICLE; CELL CULTURE; ERROR; GENOME; IN VITRO STUDY; INFRARED RADIATION; MOLECULAR MECHANICS; MUTAGENIC ACTIVITY; MUTAGENICITY; MUTATION RATE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; SITE DIRECTED MUTAGENESIS; SPECTROSCOPY; TAUTOMER; TAUTOMERIZATION; TEMPERATURE MEASUREMENT; VIRUS REPLICATION;

KP1461; SITE-SPECIFIC MUTAGENESIS; SPECTRAL DECONVOLUTION; VIRAL DECAY ACCELERATION; VIRAL EXTINCTION;

ANTI-HIV AGENTS; AZACITIDINE; BACTERIOPHAGE M13; BASE PAIRING; DEOXYCYTIDINE; GENOME, VIRAL; HIV; HUMANS; ISOMERISM; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, CHEMICAL; MUTAGENS; SPECTROPHOTOMETRY, INFRARED; VIRUS REPLICATION;

EID: 84905986028     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1405635111     Document Type: Article

References (60)

1. Frenkel LM, et al. (2003) Multiple viral genetic analyses detect low-level human immunodeficiency virus type 1 replication during effective highly active antiretroviral therapy. J Virol 77(10):5721-5730
2. Mullins JI, Jensen MA (2006) Evolutionary dynamics of HIV-1 and the control of AIDS. Curr Top Microbiol Immunol 299:171-192
3. Johnston R (2010) HIV cure: Controversy, consensus, and a consortium. AIDS Res Hum Retroviruses 26(9):943-946
4. Esté JA, Cihlar T (2010) Current status and challenges of antiretroviral research and therapy. Antiviral Res 85(1):25-33
5. Broder S (2010) The development of antiretroviral therapy and its impact on the HIV-1/AIDS pandemic. Antiviral Res 85(1):1-18
6. EigenM(2002) Error catastrophe and antiviral strategy. Proc Natl Acad Sci USA 99(21): 13374-13376
7. Loeb LA, et al. (1999) Lethal mutagenesis of HIV with mutagenic nucleoside analogs. Proc Natl Acad Sci USA 96(4):1492-1497
8. Smith RA, Loeb LA, Preston BD (2005) Lethal mutagenesis of HIV. Virus Res 107(2): 215-228
9. Clouser CL, Patterson SE, Mansky LM (2010) Exploiting drug repositioning for discovery of a novel HIV combination therapy. J Virol 84(18):9301-9309
10. Graci JD, Cameron CE (2008) Therapeutically targeting RNA viruses via lethal mutagenesis. Future Virol 3(6):553-566
11. Perales C, Martín V, Domingo E (2011) Lethal mutagenesis of viruses. Curr Opin Virol 1(5):419-422
12. Elena SF (2012) RNA virus genetic robustness: Possible causes and some consequences. Curr Opin Virol 2(5):525-530
13. de la Torre JC (2005) Arenavirus extinction through lethal mutagenesis. Virus Res 107(2):207-214
14. Bonnac LF, Mansky LM, Patterson SE (2013) Structure-activity relationships and design of viral mutagens and application to lethal mutagenesis. J Med Chem 56(23):9403-9414
15. Koito A, Ikeda T (2013) Intrinsic immunity against retrotransposons by APOBEC cytidine deaminases. Front Microbiol 4:28
16. Jaszczur M, Bertram JG, Pham P, Scharff MD, Goodman MF (2013) AID and Apobec3G haphazard deamination and mutational diversity. Cell Mol Life Sci 70(17):3089-3108
17. Smyth RP, Davenport MP, Mak J (2012) The origin of genetic diversity in HIV-1. Virus Res 169(2):415-429
18. Ortega-Prieto AM, et al. (2013) Extinction of hepatitis C virus by ribavirin in hepatoma cells involves lethal mutagenesis. PLoS ONE 8(8):e71039
19. Dietz J, et al. (2013) Deep sequencing reveals mutagenic effects of ribavirin during monotherapy of hepatitis C virus genotype 1-infected patients. J Virol 87(11): 6172-6181
20. Moreno H, Grande-Pérez A, Domingo E, Martín V (2012) Arenaviruses and lethal mutagenesis. Prospects for new ribavirin-based interventions. Viruses 4(11): 2786-2805
21. Graci JD, Cameron CE (2002) Quasispecies, error catastrophe, and the antiviral activity of ribavirin. Virology 298(2):175-180
22. Crotty S, et al. (2000) The broad-spectrum antiviral ribonucleoside ribavirin is an RNA virus mutagen. Nat Med 6(12):1375-1379
23. Baranovich T, et al. (2013) T-705 (favipiravir) induces lethal mutagenesis in influenza A H1N1 viruses in vitro. J Virol 87(7):3741-3751
24. Manrubia SC, Domingo E, Lázaro E (2010) Pathways to extinction: Beyond the error threshold. Philos Trans R Soc Lond B Biol Sci 365(1548):1943-1952
25. Domingo E, Sheldon J, Perales C (2012) Viral quasispecies evolution. Microbiol Mol Biol Rev 76(2):159-216
26. Domingo E, Grande-Pérez A, Martín V (2008) Future prospects for the treatment of rapidly evolving viral pathogens: Insights from evolutionary biology. Expert Opin Biol Ther 8(10):1455-1460
27. Domingo E, et al. (2006) Viruses as quasispecies: Biological implications. Curr Top Microbiol Immunol 299:51-82
28. Mullins JI, et al. (2011) Mutation of HIV-1 genomes in a clinical population treated with the mutagenic nucleoside KP1461. PLoS ONE 6(1):e15135
29. Harris KS, Brabant W, Styrchak S, Gall A, Daifuku R (2005) KP-1212/1461, a nucleoside designed for the treatment of HIV by viral mutagenesis. Antiviral Res 67(1):1-9
30. Murakami E, Basavapathruni A, Bradley WD, Anderson KS (2005) Mechanism of action of a novel viral mutagenic covert nucleotide: Molecular interactions with HIV-1 reverse transcriptase and host cell DNA polymerases. Antiviral Res 67(1):10-17
31. Watson JD, Crick FH (1953) Genetical implications of the structure of deoxyribonucleic acid. Nature 171(4361):964-967
32. Lowdin P-O (1963) Proton tunneling in DNA and its biological implications. Rev Mod Phys 35:724-732
33. Topal MD, Fresco JR (1976) Complementary base pairing and the origin of substitution mutations. Nature 263(5575):285-289
34. Goodman MF (1995) DNA models. Mutations caught in the act. Nature 378(6554): 237-238
35. Kunkel TA (2004) DNA replication fidelity. J Biol Chem 279(17):16895-16898
36. Rüterjans H, Kaun E, Hull WE, Limbach HH (1982) Evidence for tautomerism in nucleic acid base pairs. 1H NMR study of 15N labeled tRNA. Nucleic Acids Res 10(21):7027-7039
37. Purrello R, et al. (1993) Keto-iminol tautomerism of protonated cytidine monophosphate characterized by ultraviolet resonance Raman spectroscopy: implications of C+ iminol tautomer for base mispairing. J Am Chem Soc 115:760-767
38. Wang W, Hellinga HW, Beese LS (2011) Structural evidence for the rare tautomer hypothesis of spontaneous mutagenesis. Proc Natl Acad Sci USA 108(43): 17644-17648
39. Suen W, Spiro TG, Sowers LC, Fresco JR (1999) Identification by UV resonance Raman spectroscopy of an imino tautomer of 5-hydroxy-2-deoxycytidine, a powerful base analog transition mutagen with a much higher unfavored tautomer frequency than that of the natural residue 2-deoxycytidine. Proc Natl Acad Sci USA 96(8):4500-4505
40. Sečkářová P, et al. (2004) Direct determination of tautomerism in purine derivatives by low-temperature NMR spectroscopy. Tetrahedron Lett 45:6259-6263
41. Singh V, et al. (2014) Direct observation of multiple tautomers of oxythiamine and their recognition by the thiamine pyrophosphate riboswitch. ACS Chem Biol 9(1):227-236
42. Delaney JC, Essigmann JM (2006) Assays for determining lesion bypass efficiency and mutagenicity of site-specific DNA lesions in vivo. Methods Enzymol 408:1-15
43. Delaney JC, Essigmann JM (2004) Mutagenesis, genotoxicity, and repair of 1-methyladenine, 3-alkylcytosines, 1-methylguanine, and 3-methylthymine in alkB Escherichia coli. Proc Natl Acad Sci USA 101(39):14051-14056
44. Friedberg EC (2006) DNA Repair And Mutagenesis (ASM Press, Washington, DC), 2nd Ed
45. Nir E, Kleinermanns K, de Vries MS (2000) Pairing of isolated nucleic-acid bases in the absence of the DNA backbone. Nature 408(6815):949-951
46. Armentano D, et al. (2004) Self-assembling of cytosine nucleoside into triply-bound dimers in acid media. A comprehensive evaluation of proton-bound pyrimidine nucleosides by electrospray tandem mass spectrometry, X-rays diffractometry, and theoretical calculations. J Am Soc Mass Spectrom 15(2):268-279
47. Giorgi T, et al. (2002) Gel-like lyomesophases formed in organic solvents by self-assembled guanine ribbons. Chemistry 8(9):2143-2152
48. Davis JT (2004) G-quartets 40 years later: From 5'-GMP to molecular biology and supramolecular chemistry. Angew Chem Int Ed Engl 43(6):668-698
49. Sivakova S, Rowan SJ (2005) Nucleobases as supramolecular motifs. Chem Soc Rev 34(1):9-21
50. Miles HT (1961) Tautomeric forms in a polynucleotide helix and their bearing on the structure of DNA. Proc Natl Acad Sci USA 47:791-802
51. Peng CS, Jones KC, Tokmakoff A (2011) Anharmonic vibrational modes of nucleic acid bases revealed by 2D IR spectroscopy. J Am Chem Soc 133(39):15650-15660
52. Peng CS, Tokmakoff A (2012) Identification of lactam-lactim tautomers of aromatic heterocycles in aqueous solution using 2D IR spectroscopy. J Phys Chem Lett 3(22): 3302-3306
53. Peng CS, Baiz CR, Tokmakoff A (2013) Direct observation of ground-state lactamlactim tautomerization using temperature-jump transient 2D IR spectroscopy. Proc Natl Acad Sci USA 110(23):9243-9248
54. Matou-sová M, et al. (2011) 2́-deoxy-5,6-dihydro-5- azacytidine-A less toxic alternative of 2́-deoxy-5-azacytidine: A comparative study of hypomethylating potential. Epigenetics 6(6):769-776
55. Tripathi K, Balagam R, Vishnoi NK, Dixit NM(2012) Stochastic simulations suggest that HIV-1 survives close to its error threshold. PLOS Comput Biol 8(9):e1002684
56. van der Kuyl AC, Berkhout B (2012) The biased nucleotide composition of the HIV genome: A constant factor in a highly variable virus. Retrovirology 9:92
57. Gandhi VV, Samuels DC (2011) A review comparing deoxyribonucleoside triphosphate (dNTP) concentrations in the mitochondrial and cytoplasmic compartments of normal and transformed cells. Nucleosides Nucleotides Nucleic Acids 30(5):317-339
58. Rodman JH, et al. (1999) Systemic pharmacokinetics and cellular pharmacology of zidovudine in human immunodeficiency virus type 1-infected women and newborn infants. J Infect Dis 180(6):1844-1850
59. Chung HS, Khalil M, Smith AW, Tokmakoff A (2007) Transient two-dimensional IR spectrometer for probing nanosecond temperature-jump kinetics. Rev Sci Instrum 78(6):063101
60. Jones KC, Ganim Z, Peng CS, Tokmakoff A (2012) Transient two-dimensional spectroscopy with linear absorption corrections applied to temperature-jump two-dimensional infrared. J Opt Soc Am B 29:118-129.