HIV-1-associated uracil DNA glycosylase activity controls dUTP misincorporation in viral DNA and is essential to the HIV-1 life cycle

Molecular Cell

Volumn 17, Issue 4, 2005, Pages 479-490

  Priet, Stéphane ^a,c   Gros, Nathalie ^a,d   Navarro, Jean Marc ^a,e   Boretto, Joëlle ^b   Canard, Bruno ^b   Quérat, Gilles ^a,c   Sire, Joséphine ^a,c  

^a INSERM   (France)

^b Centre National de la Recherche Scientifique   (France)

^c AIX MARSEILLE UNIVERSITY   (France)

^d UNIVERSITÉ DE LYON   (France)

^e CENTRE D IMMUNOLOGIE DE MARSEILLE LUMINY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; DEOXYURIDINE TRIPHOSPHATE PYROPHOSPHATASE; INTEGRASE; RNA DIRECTED DNA POLYMERASE; URACIL; URACIL DNA GLYCOSYLTRANSFERASE; VIRUS DNA; VIRUS ENZYME;

ARTICLE; CATALYSIS; CONTROLLED STUDY; ENZYME ACTIVITY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; LIFE CYCLE; NONHUMAN; NORMAL HUMAN; NUCLEOTIDE SEQUENCE; POLYMERIZATION; PROTEIN DOMAIN; PROTEIN FUNCTION; VIRION; VIRUS GENOME; VIRUS PARTICLE;

DNA VIRUSES; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 13944277344     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2005.01.016     Document Type: Article

References (55)

1. Aquaro S., Calio R., Balzarini J., Bellocchi M.C., Garaci E., Perno C.F. Macrophages and HIV infection. therapeutical approaches toward this strategic virus reservoir Antiviral Res. 55:2002;209-225
2. Boretto J., Longhi S., Navarro J.M., Selmi B., Sire J., Canard B. An integrated system to study multiply substituted human immunodeficiency virus type 1 reverse transcriptase. Anal. Biochem. 292:2001;139-147
3. BouHamdan M., Xue Y., Baudat Y., Hu B., Sire J., Pomerantz R.J., Duan L.X. Diversity of HIV-1 Vpr interactions involves usage of the WXXF motif of host cell proteins. J. Biol. Chem. 273:1998;8009-8016
4. Butler S.L., Hansen M.S., Bushman F.D. A quantitative assay for HIV DNA integration in vivo. Nat. Med. 7:2001;631-634
5. Cai H., Bloom L.B., Eritja R., Goodman M.F. Kinetics of deoxyribonucleotide insertion and extension at abasic template lesions in different sequence contexts using HIV-1 reverse transcriptase. J. Biol. Chem. 268:1993;23567-23572
6. Chen R., Le Rouzic E., Kearney J.A., Mansky L.M., Benichou S. Vpr-mediated incorporation of UNG2 into HIV-1 particles is required to modulate the virus mutation rate and for replication in macrophages. J. Biol. Chem. 279:2004;28419-28425
7. Cross D.R., Miller B.J., James S.J. A simplified HPLC method for simultaneously quantifying ribonucleotides and deoxyribonucleotides in cell extracts or frozen tissues. Cell Prolif. 26:1993;327-336
8. Cullen B.R. HIV-1 Vif. counteracting innate antiretroviral defenses Mol. Ther. 8:2003;525-527
9. Di Noia J., Neuberger M.S. Altering the pathway of immunoglobulin hypermutation by inhibiting uracil-DNA glycosylase. Nature. 419:2002;43-48
10. Elbashir S.M., Harborth J., Lendeckel W., Yalcin A., Weber K., Tuschl T. Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature. 411:2001;494-498
11. Gu Y., Sundquist W.I. Good to CU. Nature. 424:2003;21-22
12. Harris R.S., Bishop K.N., Sheehy A.M., Craig H.M., Petersen-Mahrt S.K., Watt I.N., Neuberger M.S., Malim M.H. DNA deamination mediates innate immunity to retroviral infection. Cell. 113:2003;803-809
13. Hoeijmakers J.H. Genome maintenance mechanisms for preventing cancer. Nature. 411:2001;366-374
14. Horowitz R.W., Zhang H., Schwartz E.L., Ladner R.D., Wadler S. Measurement of deoxyuridine triphosphate and thymidine triphosphate in the extracts of thymidylate synthase-inhibited cells using a modified DNA polymerase assay. Biochem. Pharmacol. 54:1997;635-638
15. Hottiger M., Podust V.N., Thimmig R.L., McHenry C., Hubscher U. Strand displacement activity of the human immunodeficiency virus type 1 reverse transcriptase heterodimer and its individual subunits. J. Biol. Chem. 269:1994;986-991
16. Julias J.G., Ferris A.L., Boyer P.L., Hughes S.H. Replication of phenotypically mixed human immunodeficiency virus type 1 virions containing catalytically active and catalytically inactive reverse transcriptase. J. Virol. 75:2001;6537-6546
17. Kavli B., Sundheim O., Akbari M., Otterlei M., Nilsen H., Skorpen F., Aas P.A., Hagen L., Krokan H.E., Slupphaug G. hUNG2 is the major repair enzyme for removal of uracil from U:A matches, U:G mismatches, and U in single-stranded DNA, with hSMUG1 as a broad specificity backup. J. Biol. Chem. 277:2002;39926-39936
18. Klarmann G.J., Chen X., North T.W., Preston B.D. Incorporation of uracil into minus strand DNA affects the specificity of plus strand synthesis initiation during lentiviral reverse transcription. J. Biol. Chem. 278:2003;7902-7909
19. Krokan H.E., Drablos F., Slupphaug G. Uracil in DNA-occurrence, consequences and repair. Oncogene. 21:2002;8935-8948
20. Lecossier D., Bouchonnet F., Clavel F., Hance A.J. Hypermutation of HIV-1 DNA in the absence of the Vif protein. Science. 300:2003;1112
21. Lerner D.L., Wagaman P.C., Phillips T.R., Prospero-Garcia O., Henriksen S.J., Fox H.S., Bloom F.E., Elder J.H. Increased mutation frequency of feline immunodeficiency virus lacking functional deoxyuridine-triphosphatase. Proc. Natl. Acad. Sci. USA. 92:1995;7480-7484
22. Lindahl T., Wood R.D. Quality control by DNA repair. Science. 286:1999;1897-1905
23. Mangeat B., Turelli P., Caron G., Friedli M., Perrin L., Trono D. Broad antiretroviral defence by human APOBEC3G through lethal editing of nascent reverse transcripts. Nature. 424:2003;99-103
24. Mansky L.M., Preveral S., Selig L., Benarous R., Benichou S. The interaction of vpr with uracil DNA glycosylase modulates the human immunodeficiency virus type 1 in vivo mutation rate. J. Virol. 74:2000;7039-7047
25. Mariani R., Chen D., Schrofelbauer B., Navarro F., Konig R., Bollman B., Munk C., Nymark-McMahon H., Landau N.R. Species-specific exclusion of APOBEC3G from HIV-1 virions by Vif. Cell. 114:2003;21-31
26. Marin M., Rose K.M., Kozak S.L., Kabat D. HIV-1 Vif protein binds the editing enzyme APOBEC3G and induces its degradation. Nat. Med. 9:2003;1398-1403
27. Martinez M.A., Sala M., Vartanian J.P., Wain-Hobson S. Reverse transcriptase and substrate dependence of the RNA hypermutagenesis reaction. Nucleic Acids Res. 23:1995;2573-2578
28. Masuda Y., Bennett R.A., Demple B. Rapid dissociation of human apurinic endonuclease (Ape1) from incised DNA induced by magnesium. J. Biol. Chem. 273:1998;30360-30365
29. McGeoch D.J. Protein sequence comparisons show that the 'pseudoproteases' encoded by poxviruses and certain retroviruses belong to the deoxyuridine triphosphatase family. Nucleic Acids Res. 18:1990;4105-4110
30. Mehle A., Strack B., Ancuta P., Zhang C., McPike M., Gabuzda D. Vif overcomes the innate antiviral activity of APOBEC3G by promoting its degradation in the ubiquitin-proteasome pathway. J. Biol. Chem. 279:2004;7792-7798
31. Mol C.D., Arvai A.S., Slupphaug G., Kavli B., Alseth I., Krokan H.E., Tainer J.A. Crystal structure and mutational analysis of human uracil-DNA glycosylase. structural basis for specificity and catalysis Cell. 80:1995;869-878
32. Nagahara H., Vocero-Akbani A.M., Snyder E.L., Ho A., Latham D.G., Lissy N.A., Becker-Hapak M., Ezhevsky S.A., Dowdy S.F. Transduction of full-length TAT fusion proteins into mammalian cells. TAT-p27Kip1 induces cell migration Nat. Med. 4:1998;1449-1452
33. Nilsen H., Otterlei M., Haug T., Solum K., Nagelhus T.A., Skorpen F., Krokan H.E. Nuclear and mitochondrial uracil-DNA glycosylases are generated by alternative splicing and transcription from different positions in the UNG gene. Nucleic Acids Res. 25:1997;750-755
34. O'Doherty U., Swiggard W.J., Malim M.H. Human immunodeficiency virus type 1 spinoculation enhances infection through virus binding. J. Virol. 74:2000;10074-10080
35. Prasad R., Beard W.A., Strauss P.R., Wilson S.H. Human DNA polymerase beta deoxyribose phosphate lyase. Substrate specificity and catalytic mechanism. J. Biol. Chem. 273:1998;15263-15270
36. Priet S., Navarro J.M., Gros N., Querat G., Sire J. Differential incorporation of uracil DNA glycosylase UNG2 into HIV-1, HIV-2, and SIV(MAC) viral particles. Virology. 307:2003;283-289. a
37. Priet S., Navarro J.M., Gros N., Querat G., Sire J. Functional Role of HIV-1 Virion-associated Uracil DNA Glycosylase 2 in the Correction of G:U Mispairs to G:C Pairs. J. Biol. Chem. 278:2003;4566-4571. b
38. Roizman, B., and Sears, A.E. (1990). Herpes simplex viruses and their replication. In Virology, B.N.F. e. al., ed. (New York, Raven Press), pp. 1795-1841.
39. Sheehy A.M., Gaddis N.C., Choi J.D., Malim M.H. Isolation of a human gene that inhibits HIV-1 infection and is suppressed by the viral Vif protein. Nature. 418:2002;646-650
40. Slupphaug G., Eftedal I., Kavli B., Bharati S., Helle N.M., Haug T., Levine D.W., Krokan H.E. Properties of a recombinant human uracil-DNA glycosylase from the UNG gene and evidence that UNG encodes the major uracil-DNA glycosylase. Biochemistry. 34:1995;128-138
41. Song E., Lee S.K., Dykxhoorn D.M., Novina C., Zhang D., Crawford K., Cerny J., Sharp P.A., Lieberman J., Manjunath N., Shankar P. Sustained small interfering RNA-mediated human immunodeficiency virus type 1 inhibition in primary macrophages. J. Virol. 77:2003;7174-7181
42. Steagall W.K., Robek M.D., Perry S.T., Fuller F.J., Payne S.L. Incorporation of uracil into viral DNA correlates with reduced replication of EIAV in macrophages. Virology. 210:1995;302-313
43. Strauss P.R., Beard W.A., Patterson T.A., Wilson S.H. Substrate binding by human apurinic/apyrimidinic endonuclease indicates a Briggs-Haldane mechanism. J. Biol. Chem. 272:1997;1302-1307
44. Studebaker A.W., Ariza M.E., Balendiran G.K., Williams M.V. Novel approaches for modulating dUTPase and uracil-DNA glycosylase. potential uses for cancer and viral chemotherapy Drug Design Reviews-Online. 1:2004;1-13
45. Suspene R., Sommer P., Henry M., Ferris S., Guetard D., Pochet S., Chester A., Navaratnam N., Wain-Hobson S., Vartanian J.P. APOBEC3G is a single-stranded DNA cytidine deaminase and functions independently of HIV reverse transcriptase. Nucleic Acids Res. 32:2004;2421-2429
46. Takeshita M., Chang C.N., Johnson F., Will S., Grollman A.P. Oligodeoxynucleotides containing synthetic abasic sites. Model substrates for DNA polymerases and apurinic/apyrimidinic endonucleases. J. Biol. Chem. 262:1987;10171-10179
47. Telenitsky, A., and Goff, S.P. (1997). Reverse transcriptase and the generation of retroviral DNA. In Retroviruses, J.M. Coffin, S.H. Hughes, and H.E. Varmus, eds. (Cold Spring Harbor Laboratory Press), pp. 121-160.
48. Turelli P., Guiguen F., Mornex J.F., Vigne R., Querat G. dUTPase-minus caprine arthritis-encephalitis virus is attenuated for pathogenesis and accumulates G-to-A substitutions. J. Virol. 71:1997;4522-4530
49. Wang Z., Mosbaugh D.W. Uracil-DNA glycosylase inhibitor gene of bacteriophage PBS2 encodes a binding protein specific for uracil-DNA glycosylase. J. Biol. Chem. 264:1989;1163-1171
50. Wiebauer K., Jiricny J. In vitro correction of G.T mispairs to G.C pairs in nuclear extracts from human cells. Nature. 339:1989;234-236
51. Willetts K.E., Rey F., Agostini I., Navarro J.M., Baudat Y., Vigne R., Sire J. DNA repair enzyme uracil DNA glycosylase is specifically incorporated into human immunodeficiency virus type 1 viral particles through a Vpr-independent mechanism. J. Virol. 73:1999;1682-1688
52. Wu X., Liu H., Xiao H., Kim J., Seshaiah P., Natsoulis G., Boeke J.D., Hahn B.H., Kappes J.C. Targeting foreign proteins to human immunodeficiency virus particles via fusion with Vpr and Vpx. J. Virol. 69:1995;3389-3398
53. Yu Q., Konig R., Pillai S., Chiles K., Kearney M., Palmer S., Richman D., Coffin J.M., Landau N.R. Single-strand specificity of APOBEC3G accounts for minus-strand deamination of the HIV genome. Nat. Struct. Mol. Biol. 11:2004;435-442
54. Yu X., Yu Y., Liu B., Luo K., Kong W., Mao P., Yu X.F. Induction of APOBEC3G ubiquitination and degradation by an HIV-1 Vif-Cul5-SCF complex. Science. 302:2003;1056-1060
55. Zhang H., Yang B., Pomerantz R.J., Zhang C., Arunachalam S.C., Gao L. The cytidine deaminase CEM15 induces hypermutation in newly synthesized HIV-1 DNA. Nature. 424:2003;94-98