Uracil DNA glycosylase 2 negatively regulates HIV-1 LTR transcription

Nucleic Acids Research

Volumn 37, Issue 18, 2009, Pages 6008-6018

  Fenard, David ^a,b   Houzet, Laurent ^a,c   Bernard, Eric ^a   Tupin, Audrey ^a   Brun, Sonia ^a   Mougel, Marylène ^a   Devaux, Christian ^a   Chazal, Nathalie ^a   Briant, Laurence ^a  

^a University of Montpellier I and II   (France)

^b GÉNÉTHON   (France)

^c NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PHORBOL ESTER; RNA; TRANSACTIVATOR PROTEIN; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; URACIL DNA GLYCOSIDASE; URACIL DNA GLYCOSIDASE 2;

ANTIVIRAL ACTIVITY; ARTICLE; CATALYSIS; CONTROLLED STUDY; ENZYME INHIBITION; GENE MUTATION; GENE OVEREXPRESSION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; MUTATIONAL ANALYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DEPLETION; RNA INTERFERENCE; RNA SYNTHESIS; TRANSCRIPTION INITIATION; VIRUS INHIBITION; VIRUS PARTICLE; VIRUS REPLICATION;

CATALYTIC DOMAIN; CELL LINE; HIV INTEGRASE; HIV LONG TERMINAL REPEAT; HIV-1; HIV-2; HUMANS; PROMOTER REGIONS, GENETIC; PROTEASOME ENDOPEPTIDASE COMPLEX; TAT GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; TETRADECANOYLPHORBOL ACETATE; TRANSCRIPTION, GENETIC; TRANSCRIPTIONAL ACTIVATION; TUMOR NECROSIS FACTOR-ALPHA; URACIL-DNA GLYCOSIDASE; VIRION; VPR GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 70350694412     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkp673     Document Type: Article

References (40)

1. Van Maele,B. and Debyser,Z. (2005) HIV-1 integration: An interplay between HIV-1 integrase, cellular and viral proteins. AIDS Rev., 7, 26-43.
2. Lloyd,A.G., Tateishi,S., Bieniasz,P.D., Muesing,M.A., Yamaizumi,M. and Mulder,L.C. (2006) Effect of DNA repair protein Rad18 on viral infection. PLoS Pathog., 2, e40.
3. Lau,A., Kanaar,R., Jackson,S.P. and O'Connor,M.J. (2004) Suppression of retroviral infection by the RAD52 DNA repair protein. EMBO J., 23, 3421-3429.
4. Yoder,K., Sarasin,A., Kraemer,K., McIlhatton,M., Bushman,F. and Fishel,R. (2006) The DNA repair genes XPB and XPD defend cells from retroviral infection. Proc. Natl Acad. Sci. USA, 103, 4622-4627.
5. Kavli,B., Sundheim,O., Akbari,M., Otterlei,M., Nilsen,H., Skorpen,F., Aas,P.A., Hagen,L., Krokan,H.E. and Slupphaug,G. (2002) 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, 39926-39936.
6. Nilsen,H., Rosewell,I., Robins,P., Skjelbred,C.F., Andersen,S., Slupphaug,G., Daly,G., Krokan,H.E., Lindahl,T. and Barnes,D.E. (2000) Uracil-DNA glycosylase (UNG)-deficient mice reveal a primary role of the enzyme during DNA replication. Mol. Cell, 5, 1059-1065.
7. Priet,S., Navarro,J.M., Gros,N., Querat,G. and Sire,J. (2003) 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 4566-4571.
8. Willetts,K.E., Rey,F., Agostini,I., Navarro,J.M., Baudat,Y., Vigne,R. and Sire,J. (1999) 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 1682-1688.
9. Mansky,L.M., Preveral,S., Selig,L., Benarous,R. and 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, 7039-7047.
10. Chen,R., Le Rouzic,E., Kearney,J.A., Mansky,L.M. and Benichou,S. (2004) 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, 28419-28425.
11. Priet,S., Gros,N., Navarro,J.M., Boretto,J., Canard,B., Querat,G. and Sire,J. (2005) HIV-1-associated uracil DNA glycosylase activity controls dUTP misincorporation in viral DNA and is essential to the HIV-1 life cycle. Mol. Cell, 17, 479-490.
12. Priet,S., Navarro,J.M., Gros,N., Querat,G. and Sire,J. (2003) Differential incorporation of uracil DNA glycosylase UNG2 into HIV-1, HIV-2, and SIV(MAC) viral particles. Virology, 307, 283-289.
13. Kaiser,S.M. and Emerman,M. (2006) Uracil DNA Glycosylase Is Dispensable for Human Immunodeficiency Virus Type 1 Replication and Does Not Contribute to the Antiviral Effects of the Cytidine Deaminase Apobec3G. J. Virol., 80, 875-882.
14. Bouhamdan,M., Benichou,S., Rey,F., Navarro,J.M., Agostini,I., Spire,B., Camonis,J., Slupphaug,G., Vigne,R., Benarous,R. et al. (1996) Human immunodeficiency virus type 1 Vpr protein binds to the uracil DNA glycosylase DNA repair enzyme. J. Virol., 70, 697-704.
15. Schrofelbauer,B., Hakata,Y. and Landau,N.R. (2007) HIV-1 Vpr function is mediated by interaction with the damage-specific DNA-binding protein DDB1. Proc. Natl Acad. Sci. USA, 104, 4130-4135.
16. Schrofelbauer,B., Yu,Q., Zeitlin,S.G. and Landau,N.R. (2005) Human immunodeficiency virus type 1 Vpr induces the degradation of the UNG and SMUG uracil-DNA glycosylases. J. Virol., 79, 10978-10987.
17. Slupphaug,G., Eftedal,I., Kavli,B., Bharati,S., Helle,N.M., Haug,T., Levine,D.W. and Krokan,H.E. (1995) Properties of a recombinant human uracil-DNA glycosylase from the UNG gene and evidence that UNG encodes the major uracil-DNA glycosylase. Biochemistry, 34, 128-138.
18. Brun,S., Solignat,M., Gay,B., Bernard,E., Chaloin,L., Fenard,D., Devaux,C., Chazal,N. and Briant,L. (2008) VSV-G pseudotyping rescues HIV-1 CA mutations that impair core assembly or stability. Retrovirology, 5, 57.
19. Cartier,C., Hemonnot,B., Gay,B., Bardy,M., Sanchiz,C., Devaux,C. and Briant,L. (2003) Active cAMP-dependent protein kinase incorporated within highly purified HIV-1 particles is required for viral infectivity and interacts with viral capsid protein. J. Biol. Chem., 278 35211-35219.
20. Houzet,L., Paillart,J.C., Smagulova,F., Maurel,S., Morichaud,Z., Marquet,R. and Mougel,M. (2007) HIV controls the selective packaging of genomic, spliced viral and cellular RNAs into virions through different mechanisms. Nucleic Acids Res., 35, 2695-2704.
21. Houzet,L., Morichaud,Z. and Mougel,M. (2007) Fully-spliced HIV-1 RNAs are reverse transcribed with similar efficiencies as the genomic RNA in virions and cells, but more efficiently in AZT-treated cells. Retrovirology, 4, 30.
22. Selig,L., Benichou,S., Rogel,M.E., Wu,L.I., Vodicka,M.A., Sire,J., Benarous,R. and Emerman,M. (1997) Uracil DNA glycosylase specifically interacts with Vpr of both human immunodeficiency virus type 1 and simian immunodeficiency virus of sooty mangabeys, but binding does not correlate with cell cycle arrest. J. Virol., 71, 4842-4846.
23. Priet,S., Navarro,J.M., Querat,G. and Sire,J. (2003) Reversion of the lethal phenotype of an HIV-1 integrase mutant virus by overexpression of the same integrase mutant protein. J. Biol. Chem., 278, 20724-20730.
24. Nilsen,H., Otterlei,M., Haug,T., Solum,K., Nagelhus,T.A., Skorpen,F. and Krokan,H.E. (1997) Nuclear and mitochondrial uracil-DNA glycosylases are generated by alternative splicing and transcription from different positions in the UNG gene. Nucleic Acids Res., 25, 750-755.
25. Sheehy,A.M., Gaddis,N.C., Choi,J.D. and Malim,M.H. (2002) Isolation of a human gene that inhibits HIV-1 infection and is suppressed by the viral Vif protein. Nature, 418, 646-650.
26. Harris,R.S. and Liddament,M.T. (2004) Retroviral restriction by APOBEC proteins. Nat. Rev. Immunol., 4, 868-877.
27. Branzei,D. and Foiani,M. (2008) Regulation of DNA repair throughout the cell cycle. Nat. Rev. Mol. Cell Biol., 9, 297-308.
28. Novina,C.D., Murray,M.F., Dykxhoorn,D.M., Beresford,P.J., Riess,J., Lee,S.K., Collman,R.G., Lieberman,J., Shankar,P. and Sharp,P.A. (2002) siRNA-directed inhibition of HIV-1 infection. Nat. Med., 8, 681-686.
29. Blot,G., Lopez-Verges,S., Treand,C., Kubat,N.J., Delcroix-Genete,D., Emiliani,S., Benarous,R. and Berlioz-Torrent,C. (2006) Luman, a new partner of HIV-1 TMgp41, interferes with Tat-mediated transcription of the HIV-1 LTR. J. Mol. Biol., 364, 1034-1047.
30. Goutsias,J. and Kim,S. (2004) A nonlinear discrete dynamical model for transcriptional regulation: Construction and properties. Biophys. J. 86, 1922-1945.
31. Mol,C.D., Arvai,A.S., Slupphaug,G., Kavli,B., Alseth,I., Krokan,H.E. and Tainer,J.A. (1995) Crystal structure and mutational analysis of human uracil-DNA glycosylase: Structural basis for specificity and catalysis. Cell, 80, 869-878.
32. Hagen,L., Kavli,B., Sousa,M.M., Torseth,K., Liabakk,N.B., Sundheim,O., Pena-Diaz,J., Otterlei,M., Horning,O., Jensen,O.N. et al. (2008) Cell cycle-specific UNG2 phosphorylations regulate protein turnover, activity and association with RPA. EMBO J., 27, 51-61.
33. Le Rouzic,E. and Benichou,S. (2005) The Vpr protein from HIV-1: Distinct roles along the viral life cycle. Retrovirology, 2, 11.
34. Cortazar,D., Kunz,C., Saito,Y., Steinacher,R. and Schar,P. (2007) The enigmatic thymine DNA glycosylase. DNA Repair (Amst), 6, 489-504.
35. Kondo,E., Gu,Z., Horii,A. and Fukushige,S. (2005) The thymine DNA glycosylase MBD4 represses transcription and is associated with methylated p16(INK4a) and hMLH1 genes. Mol. Cell Biol., 25, 4388-4396.
36. Kovtun,I.V. and McMurray,C.T. (2007) Crosstalk of DNA glycosylases with pathways other than base excision repair. DNA Repair (Amst), 6 517-529.
37. Missero,C., Pirro,M.T., Simeone,S., Pischetola,M. and Di Lauro,R. (2001) The DNA glycosylase T:G mismatch-specific thymine DNA glycosylase represses thyroid transcription factor-1-activated transcription. J. Biol. Chem., 276, 33569-33575.
38. Zhou,J., Blue,E.K., Hu,G. and Herring,B.P. (2008) Thymine DNA glycosylase represses myocardin-induced smooth muscle cell differentiation by competing with serum response factor for myocardin binding. J. Biol. Chem., 283, 35383-35392.
39. Verma,S.C., Bajaj,B.G., Cai,Q., Si.H., Seelhammer,T. and Robertson,E.S. (2006) Latency-associated nuclear antigen of Kaposi's sarcoma-associated herpesvirus recruits uracil DNA glycosylase 2 at the terminal repeats and is important for latent persistence of the virus. J. Virol., 80, 11178-11190.
40. Yu,X., Yu,Y., Liu,B., Luo,K., Kong,W., Mao,P. and Yu,X.F. (2003) Induction of APOBEC3G ubiquitination and degradation by an HIV-1 Vif-Cul5-SCF complex. Science, 302, 1056-1060.