Pre-steady-state kinetic analysis of the incorporation of anti-HIV nucleotide analogs catalyzed by human X- and Y-family DNA polymerases

Antimicrobial Agents and Chemotherapy

Volumn 55, Issue 1, 2011, Pages 276-283

  Brown, Jessica A ^a   Pack, Lindsey R ^a   Fowler, Jason D ^a   Suo, Zucai ^a  

^a OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA DIRECTED DNA POLYMERASE BETA; DNA DIRECTED DNA POLYMERASE ETA; DNA DIRECTED DNA POLYMERASE IOTA; DNA DIRECTED DNA POLYMERASE KAPPA; DNA DIRECTED DNA POLYMERASE LAMBDA; DNA POLYMERASE; DNA POLYMERASE REV1; EMTRICITABINE; LAMIVUDINE; TENOFOVIR; UNCLASSIFIED DRUG; ZIDOVUDINE;

ARTICLE; BINDING AFFINITY; CATALYSIS; DNA DAMAGE; DNA REPAIR; DRUG BINDING; ENZYME KINETICS; ENZYME SPECIFICITY; ENZYME SUBSTRATE; HUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION;

ADENINE; ANTI-HIV AGENTS; DNA-DIRECTED DNA POLYMERASE; HUMANS; LAMIVUDINE; MOLECULAR STRUCTURE; PHOSPHONIC ACIDS; REVERSE TRANSCRIPTASE INHIBITORS; STRUCTURE-ACTIVITY RELATIONSHIP; ZIDOVUDINE;

EID: 78650647927     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.01229-10     Document Type: Article

References (58)

1. Ahn, J., V. S. Kraynov, X. Zhong, B. G. Werneburg, and M. D. Tsai. 1998. DNA polymerase beta: effects of gapped DNA substrates on dNTP specificity, fidelity, processivity and conformational changes. Biochem. J. 331: 79-87.
2. Benbrik, E., P. Chariot, S. Bonavaud, M. Ammi-Said, E. Frisdal, C. Rey, R.Gherardi, and G. Barlovatz-Meimon. 1997. Cellular and mitochondrial toxicity of zidovudine (AZT), didanosine (ddI) and zalcitabine (ddC) on cultured human muscle cells. J. Neurol Sci. 149:19-25.
3. Birkus, G., M. Hajek, P. Kramata, I. Votruba, A. Holy, and B. Otova. 2002. Tenofovir diphosphate is a poor substrate and a weak inhibitor of rat DNA polymerases alpha, delta, and epsilon*. Antimicrob. Agents Chemother. 46:1610-1613.
4. Birkus, G., M. J. Hitchcock, and T. Cihlar. 2002. Assessment of mitochondrial toxicity in human cells treated with tenofovir: comparison with other nucleoside reverse transcriptase inhibitors. Antimicrob. Agents Chemother. 46:716-723. (Pubitemid 34157656)
5. Brown, J. A., W. W. Duym, J. D. Fowler, and Z. Suo. 2007. Single-turnover kinetic analysis of the mutagenic potential of 8-oxo-7,8-dihydro-2′- deoxyguanosine during gap-filling synthesis catalyzed by human DNA polymerases lambda and beta. J. Mol. Biol. 367:1258-1269.
6. Brown, J. A., J. D. Fowler, and Z. Suo. 2010. Kinetic investigation of nucleotide selection employed by a protein template-dependent DNA polymerase. Biochemistry 49:5504-5510.
7. Brown, J. A., L. R. Pack, S. M. Sherrer, A. K. Kshetry, S. A. Newmister, J. D. Fowler, J. S. Taylor, and Z. Suo. 2010. Identification of critical residues for the tight binding of both correct and incorrect nucleotides to human DNA polymerase lambda. J. Mol. Biol. 403:505-515.
8. Darque, A., G. Valette, F. Rousseau, L. H. Wang, J. P. Sommadossi, and X. J. Zhou. 1999. Quantitation of intracellular triphosphate of emtricitabine in peripheral blood mononuclear cells from human immunodeficiency virusinfected patients. Antimicrob. Agents Chemother. 43:2245-2250.
9. Dereuddre-Bosquet, N., B. Roy, K. Routledge, P. Clayette, G. Foucault, and M. Lepoivre. 2004. Inhibitors of CTP biosynthesis potentiate the anti-human immunodeficiency virus type 1 activity of 3TC in activated peripheral blood mononuclear cells. Antiviral Res. 61:67-70.
10. Duym, W. W., K. A. Fiala, N. Bhatt, and Z. Suo. 2006. Kinetic effect of a downstream strand and its 5′-terminal moieties on single nucleotide gapfilling synthesis catalyzed by human DNA polymerase lambda. J. Biol. Chem. 281:35649-35655.
11. Feng, J. Y., and K. S. Anderson. 1999. Mechanistic studies comparing the incorporation of (+) and (-) isomers of 3TCTP by HIV-1 reverse transcriptase. Biochemistry 38:55-63.
12. Feng, J. Y., A. A. Johnson, K. A. Johnson, and K. S. Anderson. 2001. Insights into the molecular mechanism of mitochondrial toxicity by AIDS drugs. J. Biol. Chem. 276:23832-23837.
13. Feng, J. Y., E. Murakami, S. M. Zorca, A. A. Johnson, K. A. Johnson, R. F. Schinazi, P. A. Furman, and K. S. Anderson. 2004. Relationship between antiviral activity and host toxicity: comparison of the incorporation efficiencies of 2′,3′-dideoxy-5-fluoro-3′-thiacytidine- triphosphate analogs by human immunodeficiency virus type 1 reverse transcriptase and human mitochondrial DNA polymerase. Antimicrob. Agents Chemother. 48:1300-1306.
14. Fiala, K. A., W. Abdel-Gawad, and Z. Suo. 2004. Pre-steady-state kinetic studies of the fidelity and mechanism of polymerization catalyzed by truncated human DNA polymerase lambda. Biochemistry 43:6751-6762.
15. Fiala, K. A., W. W. Duym, J. Zhang, and Z. Suo. 2006. Up-regulation of the fidelity of human DNA polymerase lambda by its non-enzymatic proline-rich domain. J. Biol. Chem. 281:19038-19044.
16. Fiala, K. A., and Z. Suo. 2004. Pre-steady-state kinetic studies of the fidelity of Sulfolobus solfataricus P2 DNA polymerase IV. Biochemistry 43:2106-2115. (Pubitemid 38233272)
17. Gao, W. Y., T. Shirasaka, D. G. Johns, S. Broder, and H. Mitsuya. 1993.Differential phosphorylation of azidothymidine, dideoxycytidine, and dideoxyinosine in resting and activated peripheral blood mononuclear cells. J. Clin. Invest. 91:2326-2333.
18. Guo, C., J. N. Kosarek-Stancel, T. S. Tang, and E. C. Friedberg. 2009. Y-family DNA polymerases in mammalian cells. Cell. Mol. Life Sci. 66:2363-2381.
19. Hanes, J. W., and K. A. Johnson. 2007. A novel mechanism of selectivity against AZT by the human mitochondrial DNA polymerase. Nucleic Acids Res. 35:6973-6983.
20. Hawkins, T., W. Veikley, R. L. St. Claire III, B. Guyer, N. Clark, and B. P. Kearney. 2005. Intracellular pharmacokinetics of tenofovir diphosphate, carbovir triphosphate, and lamivudine triphosphate in patients receiving triplenucleoside regimens. J. Acquir. Immune Defic. Syndr. 39:406-411.
21. Igoudjil, A., K. Begriche, D. Pessayre, and B. Fromenty. 2006. Mitochondrial, metabolic and genotoxic effects of antiretroviral nucleoside reversetranscriptase inhibitors. Anti Infect. Agents Med. Chem. 5:273-292.
22. Johnson, A. A., and K. A. Johnson. 2001. Fidelity of nucleotide incorporation by human mitochondrial DNA polymerase. J. Biol. Chem. 276:38090-38096.
23. Johnson, A. A., A. S. Ray, J. Hanes, Z. Suo, J. M. Colacino, K. S. Anderson, and K. A. Johnson. 2001. Toxicity of antiviral nucleoside analogs and the human mitochondrial DNA polymerase. J. Biol. Chem. 276:40847-40857. (Pubitemid 37373231)
24. Johnson, K. A. 1992. Transient-state kinetic analysis of enzyme reaction pathways. Enzymes 20:1-61.
25. Kerr, S. G., and K. S. Anderson. 1997. Pre-steady-state kinetic characterization of wild type and 3′-azido-3′-deoxythymidine (AZT) resistant human immunodeficiency virus type 1 reverse transcriptase: implication of RNA directed DNA polymerization in the mechanism of AZT resistance. Biochemistry 36:14064-14070.
26. Lee, H., J. Hanes, and K. A. Johnson. 2003. Toxicity of nucleoside analogues used to treat AIDS and the selectivity of the mitochondrial DNA polymerase. Biochemistry 42:14711-14719.
27. Lee, H. R., S. A. Helquist, E. T. Kool, and K. A. Johnson. 2008. Importance of hydrogen bonding for efficiency and specificity of the human mitochondrial DNA polymerase. J. Biol. Chem. 283:14402-14410.
28. Lee, H. R., and K. A. Johnson. 2006. Fidelity of the human mitochondrial DNA polymerase. J. Biol. Chem. 281:36236-36240.
29. Lehmann, A. R. 2006. New functions for Y family polymerases. Mol. Cell 24:493-495.
30. Margot, N. A., E. Isaacson, I. McGowan, A. K. Cheng, R. T. Schooley, and M. D. Miller. 2002. Genotypic and phenotypic analyses of HIV-1 in antiretroviral- experienced patients treated with tenofovir DF. AIDS 16:1227-1235.
31. Martin, J. L., C. E. Brown, N. Matthews-Davis, and J. E. Reardon. 1994. Effects of antiviral nucleoside analogs on human DNA polymerases and mitochondrial DNA synthesis. Antimicrob. Agents Chemother. 38:2743-2749.
32. Masuda, Y., and K. Kamiya. 2006. Role of single-stranded DNA in targeting REV1 to primer termini. J. Biol. Chem. 281:24314-24321.
33. Masuda, Y., M. Takahashi, N. Tsunekuni, T. Minami, M. Sumii, K. Miyagawa, and K. Kamiya. 2001. Deoxycytidyl transferase activity of the human REV1 protein is closely associated with the conserved polymerase domain. J. Biol. Chem. 276:15051-15058.
34. McColl, D. J., N. A. Margot, M. Wulfsohn, D. F. Coakley, A. K. Cheng, and M. D. Miller. 2004. Patterns of resistance emerging in HIV-1 from antiretroviral-experienced patients undergoing intensification therapy with tenofovir disoproxil fumarate. J. Acquir. Immune Defic. Syndr. 37:1340-1350.
35. McCulloch, S. D., and T. A. Kunkel. 2008. The fidelity of DNA synthesis by eukaryotic replicative and translesion synthesis polymerases. Cell Res. 18: 148-161.
36. Moyle, G. 2000. Toxicity of antiretroviral nucleoside and nucleotide analogues: is mitochondrial toxicity the only mechanism? Drug Saf. 23:467-481.
37. Olivero, O. A. 2007. Mechanisms of genotoxicity of nucleoside reverse transcriptase inhibitors. Environ. Mol. Mutagen. 48:215-223.
38. Olivero, O. A., G. M. Shearer, C. A. Chougnet, A. A. Kovacs, A. L. Landay, R. Baker, A. M. Stek, M. M. Khoury, L. A. Proia, H. A. Kessler, B. E. Sha, R. E. Tarone, and M. C. Poirier. 1999. Incorporation of zidovudine into leukocyte DNA from HIV-1-positive adults and pregnant women, and cord blood from infants exposed in utero. AIDS 13:919-925.
39. Patterson, T. A., W. Little, X. Cheng, S. G. Widen, A. Kumar, W. A. Beard, and S. H. Wilson. 2000. Molecular cloning and high-level expression of human polymerase beta cDNA and comparison of the purified recombinant human and rat enzymes. Protein Expr. Purif. 18:100-110.
40. Perry, C. M., and D. Faulds. 1997. Lamivudine. A review of its antiviral activity, pharmacokinetic properties and therapeutic efficacy in the management of HIV infection. Drugs 53:657-680. (Pubitemid 27145958)
41. Peyriere, H., J. Reynes, I. Rouanet, N. Daniel, C. M. de Boever, J. M. Mauboussin, H. Leray, L. Moachon, D. Vincent, and D. Salmon-Ceron. 2004. Renal tubular dysfunction associated with tenofovir therapy: report of 7 cases. J. Acquir. Immune Defic. Syndr. 35:269-273.
42. Pruvost, A., E. Negredo, H. Benech, F. Theodoro, J. Puig, E. Grau, E. Garcia, J. Molto, J. Grassi, and B. Clotet. 2005. Measurement of intracellular didanosine and tenofovir phosphorylated metabolites and possible interaction of the two drugs in human immunodeficiency virus-infected patients. Antimicrob. Agents Chemother. 49:1907-1914.
43. Ramadan, K., I. Shevelev, and U. Hubscher. 2004. The DNA polymerase X family: controllers of DNA quality? Nat. Rev. Mol. Cell Biol. 5:1038-1043.
44. Ray, A. S., E. Murakami, C. N. Peterson, J. Shi, R. F. Schinazi, and K. S. Anderson. 2002. Interactions of enantiomers of 2′,3′-didehydro- 2′,3′- dideoxy-fluorocytidine with wild type and M184V mutant HIV-1 reverse transcriptase. Antiviral Res. 56:189-205.
45. Reardon, J. E., R. C. Crouch, and L. St. John-Williams. 1994. Reduction of 3′-azido-3′-deoxythymidine (AZT) and AZT nucleotides by thiols. Kinetics and product identification. J. Biol. Chem. 269:15999-16008.
46. Rousseau, F. S., C. Wakeford, H. Mommeja-Marin, I. Sanne, C. Moxham, J. Harris, L. Hulett, L. H. Wang, J. B. Quinn, and D. W. Barry. 2003. Prospective randomized trial of emtricitabine versus lamivudine short-term monotherapy in human immunodeficiency virus-infected patients. J. Infect. Dis. 188:1652-1658.
47. Schaaf, B., S. P. Aries, E. Kramme, J. Steinhoff, and K. Dalhoff. 2003. Acute renal failure associated with tenofovir treatment in a patient with acquired immunodeficiency syndrome. Clin. Infect. Dis. 37:e41-e43.
48. Sherrer, S. M., K. A. Fiala, J. M. Pryor, S. A. Newmister, J. D. Fowler, and Z. Suo. 2010. Quantitative analysis of the efficiency and mutagenic spectra of abasic lesion bypass catalyzed by human Y-family DNA polymerases. Nucleic Acids Res. [Epub ahead of print.] doi:10.1093/nar/gkq719.
49. Sommadossi, J. P., R. Carlisle, and Z. Zhou. 1989. Cellular pharmacology of 3′-azido-3′-deoxythymidine with evidence of incorporation into DNA of human bone marrow cells. Mol. Pharmacol. 36:9-14.
50. Suo, Z., and K. A. Johnson. 1998. Selective inhibition of HIV-1 reverse transcriptase by an antiviral inhibitor, (R)-9-(2-phosphonylmethoxypropyl) adenine. J. Biol. Chem. 273:27250-27258.
51. Tuske, S., S. G. Sarafianos, A. D. Clark, Jr., J. Ding, L. K. Naeger, K. L. White, M. D. Miller, C. S. Gibbs, P. L. Boyer, P. Clark, G. Wang, B. L. Gaffney, R. A. Jones, D. M. Jerina, S. H. Hughes, and E. Arnold. 2004. Structures of HIV-1 RT-DNA complexes before and after incorporation of the anti-AIDS drug tenofovir. Nat. Struct. Mol. Biol. 11:469-474.
52. Uwai, Y., H. Ida, Y. Tsuji, T. Katsura, and K. Inui. 2007. Renal transport of adefovir, cidofovir, and tenofovir by SLC22A family members (hOAT1, hOAT3, and hOCT2). Pharm. Res. 24:811-815.
53. Wang, L. H., J. Begley, R. L. St. Claire III, J. Harris, C. Wakeford, and F. S. Rousseau. 2004. Pharmacokinetic and pharmacodynamic characteristics of emtricitabine support its once daily dosing for the treatment of HIV infection. AIDS Res. Hum. Retroviruses 20:1173-1182.
54. Washington, M. T., S. A. Helquist, E. T. Kool, L. Prakash, and S. Prakash. 2003. Requirement of Watson-Crick hydrogen bonding for DNA synthesis by yeast DNA polymerase eta. Mol. Cell. Biol. 23:5107-5112.
55. Waters, L. S., B. K. Minesinger, M. E. Wiltrout, S. D'Souza, R. V. Woodruff, and G. C. Walker. 2009. Eukaryotic translesion polymerases and their roles and regulation in DNA damage tolerance. Microbiol. Mol. Biol. Rev. 73:134-154.
56. Wolfle, W. T., M. T. Washington, E. T. Kool, T. E. Spratt, S. A. Helquist, L. Prakash, and S. Prakash. 2005. Evidence for a Watson-Crick hydrogen bonding requirement in DNA synthesis by human DNA polymerase kappa. Mol. Cell. Biol. 25:7137-7143.
57. Wutzler, P., and R. Thust. 2001. Genetic risks of antiviral nucleoside analogues: a survey. Antiviral Res. 49:55-74.
58. Yamtich, J., and J. B. Sweasy. 2010. DNA polymerase family X: function, structure, and cellular roles. Biochim. Biophys. Acta 1804:1136-1150.