APOBEC3G cytosine deamination hotspots are defined by both sequence context and single-stranded DNA secondary structure

Nucleic Acids Research

Volumn 41, Issue 12, 2013, Pages 6139-6148

  Holtz, Colleen M ^a   Sadler, Holly A ^a   Mansky, Louis M ^a,b,c  

^a School of Dentistry   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

^c UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APOLIPOPROTEIN B MESSENGER RNA EDITING ENZYME CATALYTIC POLYPEPTIDE 3G; CYTOSINE; CYTOSINE DEAMINASE; SINGLE STRANDED DNA;

ARTICLE; CONTROLLED STUDY; DEAMINATION; DNA CONFORMATION; DNA FLANKING REGION; DNA STRUCTURE; ENZYME ACTIVITY; ENZYME SPECIFICITY; FLUORESCENCE RESONANCE ENERGY TRANSFER; HYDROLYSIS; MOLECULAR RECOGNITION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RESTRICTION SITE; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION;

BASE SEQUENCE; CELL LINE; CYTIDINE DEAMINASE; CYTOSINE; DEAMINATION; DNA, SINGLE-STRANDED; HUMANS; NUCLEIC ACID CONFORMATION;

EID: 84880231858     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt246     Document Type: Article

References (44)

1. Malim, M.H. (2009) APOBEC proteins and intrinsic resistance to HIV-1 infection. Philos. Trans. R. Soc. Lond. B Biol. Sci., 364, 675-687.
2. Jern, P., Russell, R.A., Pathak, V.K. and Coffin, J.M. (2009) Likely role of APOBEC3G-mediated G-to-A mutations in HIV-1 evolution and drug resistance. PLoS Pathog., 5, e1000367.
3. Sadler, H.A., Stenglein, M.D., Harris, R.S. and Mansky, L.M. (2010) APOBEC3G contributes to HIV-1 variation through sublethal mutagenesis. J. Virol., 84, 7396-7404.
4. Hache, G., Mansky, L.M. and Harris, R.S. (2006) Human APOBEC3 proteins, retrovirus restriction, and HIV drug resistance. AIDS Rev., 8, 148-157.
5. Goila-Gaur, R. and Strebel, K. (2008) HIV-1 Vif, APOBEC, and intrinsic immunity. Retrovirology, 5, 51.
6. Harris, R.S. and Liddament, M.T. (2004) Retroviral restriction by APOBEC proteins. Nat. Rev. Immunol., 4, 868-877.
7. Zhang, H., Yang, B., Pomerantz, R.J., Zhang, C., Arunachalam, S.C. and Gao, L. (2003) The cytidine deaminase CEM15 induces hypermutation in newly synthesized HIV-1 DNA. Nature, 424, 94-98.
8. Mangeat, B., Turelli, P., Caron, G., Friedli, M., Perrin, L. and Trono, D. (2003) Broad antiretroviral defence by human APOBEC3G through lethal editing of nascent reverse transcripts. Nature, 424, 99-103.
9. Harris, R.S., Bishop, K.N., Sheehy, A.M., Craig, H.M., Petersen-Mahrt, S.K., Watt, I.N., Neuberger, M.S. and Malim, M.H. (2003) DNA deamination mediates innate immunity to retroviral infection. Cell, 113, 803-809.
10. Kohli, R.M., Maul, R.W., Guminski, A.F., McClure, R.L., Gajula, K.S., Saribasak, H., McMahon, M.A., Siliciano, R.F., Gearhart, P.J. and Stivers, J.T. (2010) Local sequence targeting in the AID/APOBEC family differentially impacts retroviral restriction and antibody diversification. J. Biol. Chem., 285, 40956-40964.
11. Rausch, J.W., Chelico, L., Goodman, M.F. and Le Grice, S.F. (2009) Dissecting APOBEC3G substrate specificity by nucleoside analog interference. J. Biol. Chem., 284, 7047-7058.
12. Bishop, K.N., Holmes, R.K., Sheehy, A.M., Davidson, N.O., Cho, S.J. and Malim, M.H. (2004) Cytidine deamination of retroviral DNA by diverse APOBEC proteins. Curr. Biol., 14, 1392-1396.
13. Yu, Q., Konig, R., Pillai, S., Chiles, K., Kearney, M., Palmer, S., Richman, D., Coffin, J.M. and Landau, N.R. (2004) Single-strand specificity of APOBEC3G accounts for minus-strand deamination of the HIV genome. Nat. Struct. Mol. Biol., 11, 435-442.
14. Kijak, G.H., Janini, M., Tovanabutra, S., Sanders-Buell, E.E., Birx, D.L., Robb, M.L., Michael, N.L. and McCutchan, F.E. (2007) HyperPack: a software package for the study of levels, contexts, and patterns of APOBEC-mediated hypermutation in HIV. AIDS Res. Hum. Retrov., 23, 554-557.
15. Thielen, B.K., Klein, K.C., Walker, L.W., Rieck, M., Buckner, J.H., Tomblingson, G.W. and Lingappa, J.R. (2007) T cells contain an RNase-insensitive inhibitor of APOBEC3G deaminase activity. PLoS Pathog., 3, 1320-1334.
16. Iwatani, Y., Takeuchi, H., Strebel, K. and Levin, J.G. (2006) Biochemical activities of highly purified, catalytically active human APOBEC3G: correlation with antiviral effect. J. Virol., 80, 5992-6002.
17. Darlix, J.L., Godet, J., Ivanyi-Nagy, R., Fosse, P., Mauffret, O. and Mely, Y. (2011) Flexible nature and specific functions of the HIV-1 nucleocapsid protein. J. Mol. Biol., 410, 565-581.
18. Levin, J.G., Mitra, M., Mascarenhas, A. and Musier-Forsyth, K. (2010) Role of HIV-1 nucleocapsid protein in HIV-1 reverse transcription. RNA Biol., 7, 754-774.
19. Muriaux, D. and Darlix, J.L. (2010) Properties and functions of the nucleocapsid protein in virus assembly. RNA Biol., 7, 744-753.
20. Mirambeau, G., Lyonnais, S. and Gorelick, R.J. (2010) Features, processing states, and heterologous protein interactions in the modulation of the retroviral nucleocapsid protein function. RNA Biol., 7, 724-734.
21. Godet, J. and Mely, Y. (2010) Biophysical studies of the nucleic acid chaperone properties of the HIV-1 nucleocapsid protein. RNA Biol., 7, 687-699.
22. Thomas, J.A. and Gorelick, R.J. (2008) Nucleocapsid protein function in early infection processes. Virus Res., 134, 39-63.
23. Watts, J.M., Dang, K.K., Gorelick, R.J., Leonard, C.W., Bess, J.W. Jr, Swanstrom, R., Burch, C.L. and Weeks, K.M. (2009) Architecture and secondary structure of an entire HIV-1 RNA genome. Nature, 460, 711-716.
24. Zuker, M. (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res., 31, 3406-3415.
25. Stenglein, M.D., Burns, M.B., Li, M., Lengyel, J. and Harris, R.S. (2010) APOBEC3 proteins mediate the clearance of foreign DNA from human cells. Nat. Struct. Mol. Biol., 17, 222-229.
26. Wu, W., Henderson, L.E., Copeland, T.D., Gorelick, R.J., Bosche, W.J., Rein, A. and Levin, J.G. (1996) Human immunodeficiency virus type 1 nucleocapsid protein reduces reverse transcriptase pausing at a secondary structure near the murine leukemia virus polypurine tract. J. Virol., 70, 7132-7142.
27. Henderson, L.E., Bowers, M.A., Sowder, R.C. II, Serabyn, S.A., Johnson, D.G., Bess, J.W. Jr, Arthur, L.O., Bryant, D.K. and Fenselau, C. (1992) Gag proteins of the highly replicative MN strain of human immunodeficiency virus type 1: posttranslational modifications, proteolytic processings, and complete amino acid sequences. J. Virol., 66, 1856-1865.
28. Kumar, N.V. and Varshney, U. (1994) Inefficient excision of uracil from loop regions of DNA oligomers by E. coli uracil DNA glycosylase. Nucleic Acids Res., 22, 3737-3741.
29. Peyret, N., Seneviratne, P.A., Allawi, H.T. and SantaLucia, J. Jr (1999) Nearest-neighbor thermodynamics and NMR of DNA sequences with internal A.A, C.C, G.G, and T.T mismatches. Biochemistry, 38, 3468-3477.
30. SantaLucia, J. Jr (1998) A unified view of polymer, dumbbell, and oligonucleotide DNA nearest-neighbor thermodynamics. Proc. Natl Acad. Sci. USA, 95, 1460-1465.
31. Allawi, H.T. and SantaLucia, J. Jr (1997) Thermodynamics and NMR of internal G.T mismatches in DNA. Biochemistry, 36, 10581-10594.
32. Allawi, H.T. and SantaLucia, J. Jr (1998) Nearest neighbor thermodynamic parameters for internal G.A mismatches in DNA. Biochemistry, 37, 2170-2179.
33. Allawi, H.T. and SantaLucia, J. Jr (1998) Thermodynamics of internal C.T mismatches in DNA. Nucleic Acids Res., 26, 2694-2701.
34. Allawi, H.T. and SantaLucia, J. Jr (1998) Nearest-neighbor thermodynamics of internal A.C mismatches in DNA: sequence dependence and pH effects. Biochemistry, 37, 9435-9444.
35. Beale, R.C., Petersen-Mahrt, S.K., Watt, I.N., Harris, R.S., Rada, C. and Neuberger, M.S. (2004) Comparison of the differential context-dependence of DNA deamination by APOBEC enzymes: correlation with mutation spectra in vivo. J. Mol. Biol., 337, 585-596.
36. Dapp, M.J., Holtz, C.M. and Mansky, L.M. (2012) Concomitant lethal mutagenesis of human immunodeficiency virus type 1. J. Mol. Biol., 419, 158-170.
37. Senavirathne, G., Jaszczur, M., Auerbach, P.A., Upton, T.G., Chelico, L., Goodman, M.F. and Rueda, D. (2012) Single-stranded DNA scanning and deamination by APOBEC3G at single molecule resolution. J. Biol. Chem., 287, 15826-15835.
38. Larijani, M. and Martin, A. (2007) Single-stranded DNA structure and positional context of the target cytidine determine the enzymatic efficiency of AID. Mol. Cell Biol., 27, 8038-8048.
39. Chelico, L., Pham, P., Calabrese, P. and Goodman, M.F. (2006) APOBEC3G DNA deaminase acts processively 3'→ 5' on single-stranded DNA. Nat. Struct. Mol. Biol., 13, 392-399.
40. Chelico, L., Sacho, E.J., Erie, D.A. and Goodman, M.F. (2008) A model for oligomeric regulation of APOBEC3G cytosine deaminase-dependent restriction of HIV. J. Biol. Chem., 283, 13780-13791.
41. Mansky, L.M. and Temin, H.M. (1995) Lower in vivo mutation rate of human immunodeficiency virus type 1 than predicted from the fidelity of purified reverse transcriptase. J. Virol., 69, 5087-5094.
42. van der Kuyl, A.C. and Berkhout, B. (2012) The biased nucleotide composition of the HIV genome: a constant factor in a highly variable virus. Retrovirology, 9, 92.
43. Clouser, C.L., Patterson, S.E. and Mansky, L.M. (2010) Exploiting drug repositioning for discovery of a novel HIV combination therapy. J. Virol., 84, 9301-9309.
44. Dapp, M.J., Patterson, S.E. and Mansky, L.M. (2013) Back to the future: revisiting HIV-1 lethal mutagenesis. Trends Microbiol., 21, 56-62.