Structure, interaction and real-time monitoring of the enzymatic reaction of wild-type APOBEC3G

EMBO Journal

Volumn 28, Issue 4, 2009, Pages 440-451

  Furukawa, Ayako ^a   Nagata, Takashi ^a   Matsugami, Akimasa ^a   Habu, Yuichirou ^b   Sugiyama, Ryuichi ^b   Hayashi, Fumiaki ^c   Kobayashi, Naohiro ^c   Yokoyama, Shigeyuki ^c,d   Takaku, Hiroshi ^b   Katahira, Masato ^a,e  

^a YOKOHAMA CITY UNIVERSITY   (Japan)

^b CHIBA INSTITUTE OF TECHNOLOGY   (Japan)

^c RIKEN   (Japan)

^d UNIVERSITY OF TOKYO   (Japan)

^e JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

APOBEC3G; Cytidine deaminase; HIV; Structure; Vif

Indexed keywords

APOLIPOPROTEIN B MESSENGER RNA EDITING ENZYME CATALYTIC POLYPEPTIDE 3G; MUTANT PROTEIN;

ARTICLE; ENZYME MECHANISM; HUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DNA INTERACTION; PROTEIN DOMAIN; PROTEIN STRUCTURE; WILD TYPE;

ANIMALS; CODON; CYTIDINE; CYTIDINE DEAMINASE; DNA, SINGLE-STRANDED; HIV-1; HUMANS; HYDROGEN-ION CONCENTRATION; KINETICS; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, MOLECULAR; MOLECULAR CONFORMATION; MUTATION; PROTEIN STRUCTURE, TERTIARY; VIF GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 60549109045     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2008.290     Document Type: Article

References (43)

1. Beale RC, Petersen-Mahrt SK, Watt IN, Harris RS, Rada C, Neuberger MS (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
2. Cen S, Guo F, Niu M, Saadatmand J, Deflassieux J, Kleiman L (2004) The interaction between HIV-1 Gag and APOBEC3G. J Biol Chem 279: 33177-33184
3. Chelico L, Pham P, Calabrese P, Goodman MF (2006) APOBEC3G DNA deaminase acts processively 3′→5′ on single-stranded DNA. Nat Struct Mol Biol 13: 392-399
4. Chen KM, Harjes E, Gross PJ, Fahmy A, Lu Y, Shindo K, Harris RS, Matsuo H (2008) Structure of the DNA deaminase domain of the HIV-1 restriction factor APOBEC3G. Nature 452: 116-119
5. Clore GM, Gronenborn AM (1994) Multidimensional heteronuclear nuclear magnetic resonance of proteins. Methods Enzymol 239: 349-363
6. Conticello SG, Harris RS, Neuberger MS (2003) The Vif protein of HIV triggers degradation of the human antiretroviral DNA deaminase APOBEC3G. Curr Biol 13: 2009-2013
7. Cornilescu G, Delaglio F, Bax A (1999) Protein backbone angle restraints from searching a database for chemical shift and sequence homology. J Biomol NMR 13: 289-302
8. Delaglio F, Grzesiek S, Vuister GW, Zhu G, Pfeifer J, Bax A (1995) NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J Biomol NMR 6: 277-293
9. Enokizono Y, Konishi Y, Nagata K, Ouhashi K, Uesugi S, Ishikawa F, Katahira M (2005) Structure of hnRNP D complexed with single-stranded telomere DNA and unfolding of the quadruplex by heterogeneous nuclear ribonucleoprotein D. J Biol Chem 280: 18862-18870
10. Esnault C, Heidmann O, Delebecque F, Dewannieux M, Ribet D, Hance AJ, Heidmann T, Schwartz O (2005) APOBEC3G cytidine deaminase inhibits retrotransposition of endogenous retroviruses. Nature 433: 430-433
11. Greene WC (2004) The brightening future of HIV therapeutics. Nat Immunol 5: 867-871
12. Goddard TD, Kneller DG (2006) SPARKY 3. San Francisco: University of California
13. Harris RS, Bishop KN, Sheehy AM, Craig HM, Petersen-Mahrt SK, Watt IN, Neuberger MS, Malim MH (2003) DNA deamination mediates innate immunity to retroviral infection. Cell 113: 803-809
14. Harris RS, Liddament MT (2004) Retroviral restriction by APOBEC proteins. Nat Rev Immunol 4: 868-877
15. Holden LG, Prochnow C, Chang YP, Bransteitter R, Chelico L, Sen U, Stevens RC, Goodman MF, Chen XS (2008) Crystal structure of the anti-viral APOBEC3G catalytic domain and functional implications. Nature 456: 121-124
16. Kobayashi M, Takaori-Kondo A, Miyauchi Y, Iwai K, Uchiyama T (2005) Ubiquitination of APOBEC3G by an HIV-1 Vif-Cullin5-Elongin B-Elongin C complex is essential for Vif function. J Biol Chem 280: 18573-18578
17. Kobayashi N, Iwahara J, Koshiba S, Tomizawa T, Tochio N, Guntert P, Kigawa T, Yokoyama S (2007) KUJIRA, a package of integrated modules for systematic and interactive analysis of NMR data directed to high-throughput NMR structure studies. J Biomol NMR 39: 31-52
18. Laskowski RA, Rullmannn JA, MacArthur MW, Kaptein R, Thornton JM (1996) AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR. J Biomol NMR 8: 477-486
19. Lecossier D, Bouchonnet F, Clavel F, Hance AJ (2003) Hypermutation of HIV-1 DNA in the absence of the Vif protein. Science 300: 1112
20. Losey HC, Ruthenburg AJ, Verdine GL (2006) Crystal structure of Staphylococcus aureus tRNA adenosine deaminase TadA in complex with RNA. Nat Struct Mol Biol 13: 153-159
21. Mangeat B, Turelli P, Caron G, Friedli M, Perrin L, Trono D (2003) Broad antiretroviral defence by human APOBEC3G through lethal editing of nascent reverse transcripts. Nature 424: 99-103
22. Mangeat B, Turelli P, Liao S, Trono D (2004) A single amino acid determinant governs the species-specific sensitivity of APOBEC3G to Vif action. J Biol Chem 279: 14481-14483
23. Mariani R, Chen D, Schrofelbauer B, Navarro F, Konig R, Bollman B, Munk C, Nymark-McMahon H, Landau NR (2003) Species-specific exclusion of APOBEC3G from HIV-1 virions by Vif. Cell 114: 21-31
24. Marin M, Rose KM, Kozak SL, Kabat D (2003) HIV-1 Vif protein binds the editing enzyme APOBEC3G and induces its degradation. Nat Med 9: 1398-1403
25. Marti-Renom MA, Stuar AC, Fiser A, Sanchez R, Melo F, Sali A (2000) Comparative protein structure modeling of genes and genomes. Annu Rev Biophys Biomol Struct 29: 291-325
26. Mehle A, Strack B, Ancuta P, Zhang C, McPike M, Gabuzda D (2004) Vif overcomes the innate antiviral activity of APOBEC3G by promoting its degradation in the ubiquitin-proteasome pathway. J Biol Chem 279: 7792-7798
27. Miyanoiri Y, Kobayashi H, Imai T, Watanabe M, Nagata T, Uesugi S, Okano H, Katahira M (2003) Origin of higher affinity to RNA of the N-terminal RNA-binding domain than that of the C-terminal one of a mouse neural protein, musashi1, as revealed by comparison of their structures, modes of interaction, surface electrostatic potentials, and backbone dynamics. J Biol Chem 278: 41309-41315
28. Muramatsu M, Sankaranand VS, Anant S, Sugai M, Kinoshita K, Davidson NO, Honjo T (1999) Specific expression of activation-induced cytidine deaminase (AID), a novel member of the RNA-editing deaminase family in germinal center B cells. J Biol Chem 274: 18470-18476
29. Navaratnam N, Morrison JR, Bhattacharya S, Patel D, Funahashi T, Giannoni F, Teng BB, Davidson NO, Scott J (1993) The p27 catalytic subunit of the apolipoprotein B mRNA editing enzyme is a cytidine deaminase. J Biol Chem 268: 20709-20712
30. Navarro F, Bollman B, Chen H, Konig R, Yu Q, Chiles K, Landau NR (2005) Complementary function of the two catalytic domains of APOBEC3G. Virology 333: 374-386
31. Prochnow C, Bransteitter R, Klein MG, Goodman MF, Chen XS (2007) The APOBEC-2 crystal structure and functional implications for the deaminase AID. Nature 445: 447-451
32. Rogozin IB, Iyer LM, Liang L, Glazko GV, Liston VG, Pavlov YI, Aravind L, Pancer Z (2007) Evolution and diversification of lamprey antigen receptors: evidence for involvement of an AID-APOBEC family cytosine deaminase. Nat Immunol 8: 647-656
33. Schwieters CD, Kuszewski JJ, Tjandra N, Clore GM (2003) The Xplor-NIH NMR molecular structure determination package. J Magn Reson 160: 65-73
34. Sheehy AM, Gaddis NC, Choi JD, Malim MH (2002) Isolation of a human gene that inhibits HIV-1 infection and is suppressed by the viral Vif protein. Nature 418: 646-650
35. Shindo K, Takaori-Kondo A, Kobayashi M, Abudu A, Fukunaga K, Uchiyama T (2003) The enzymatic activity of CEM15/Apobec-3G is essential for the regulation of the infectivity of HIV-1 virion but not a sole determinant of its antiviral activity. J Biol Chem 278: 44412-44416
36. Suspene R, Sommer P, Henry M, Ferris S, Guetard D, Pochet S, Chester A, Navaratnam N, Wain-Hobson S, Vartanian JP (2004) APOBEC3G is a single-stranded DNA cytidine deaminase and functions independently of HIV reverse transcriptase. Nucleic Acids Res 32: 2421-2429
37. Teh AH, Kimura M, Yamamoto M, Tanaka N, Yamaguchi I, Kumasaka T (2006) The 1.48 A resolution crystal structure of the homotetrameric cytidine deaminase from mouse. Biochemistry 45: 7825-7833
38. Teng B, Burant CF, Davidson NO (1993) Molecular cloning of an apolipoprotein B messenger RNA editing protein. Science 260: 1816-1819
39. Wishart DS, Sykes BD (1994) The 13C chemical-shift index: a simple method for the identification of protein secondary structure using 13C chemical-shift data. J Biomol NMR 4: 171-180
40. Xiang S, Short SA, Wolfenden R, Carter Jr CW (1997) The structure of the cytidine deaminase-product complex provides evidence for efficient proton transfer and ground-state destabilization. Biochemistry 36: 4768-4774
41. Yu Q, Konig R, Pillai S, Chiles K, Kearney M, Palmer S, Richman D, Coffin JM, Landau NR (2004) Single-strand specificity of APOBEC3G accounts for minus-strand deamination of the HIV genome. Nat Struct Mol Biol 11: 435-442
42. Yu X, Yu Y, Liu B, Luo K, Kong W, Mao P, Yu XF (2003) Induction of APOBEC3G ubiquitination and degradation by an HIV-1 Vif-Cul5-SCF complex. Science 302: 1056-1060
43. Zhang H, Yang B, Pomerantz RJ, Zhang C, Arunachalam SC, Gao L (2003) The cytidine deaminase CEM15 induces hypermutation in newly synthesized HIV-1 DNA. Nature 424: 94-98