Crystal structures of APOBEC3G N-domain alone and its complex with DNA

Nature Communications

Volumn 7, Issue , 2016, Pages

  Xiao, Xiao ^a,b   Li, Shu Xing ^b   Yang, Hanjing ^b   Chen, Xiaojiang S ^a,b,c  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APOLIPOPROTEIN B MESSENGER RNA EDITING ENZYME CATALYTIC POLYPEPTIDE 3G; SINGLE STRANDED DNA; VIRUS DNA; PROTEIN BINDING; RECOMBINANT PROTEIN; VIF PROTEIN;

CHEMICAL BINDING; CRYSTAL STRUCTURE; DEGRADATION; DNA; GENE EXPRESSION; HUMAN IMMUNODEFICIENCY VIRUS; INFECTIVITY; NUCLEIC ACID;

ARTICLE; CONTROLLED STUDY; CRYSTAL STRUCTURE; DIMERIZATION; DNA BINDING; GENETIC CONSERVATION; HUMAN IMMUNODEFICIENCY VIRUS 1; NONHUMAN; OLIGOMERIZATION; PROTEIN DEGRADATION; PROTEIN DOMAIN; SURFACE CHARGE; ANIMAL; CHEMISTRY; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; PRIMATE; PROTEIN MULTIMERIZATION; STRUCTURE ACTIVITY RELATION; X RAY CRYSTALLOGRAPHY;

HUMAN IMMUNODEFICIENCY VIRUS 1; PRIMATES;

ANIMALS; APOBEC-3G DEAMINASE; CRYSTALLOGRAPHY, X-RAY; DNA, SINGLE-STRANDED; HIV-1; PRIMATES; PROTEIN BINDING; PROTEIN DOMAINS; PROTEIN MULTIMERIZATION; RECOMBINANT PROTEINS; STRUCTURE-ACTIVITY RELATIONSHIP; VIF GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS;

EID: 84982703210     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms12193     Document Type: Article

References (64)

1. LaRue, R. S. et al. Guidelines for naming nonprimate APOBEC3 genes and proteins. J. Virol. 83, 494-497 (2009).
2. Feng, Y., Baig, T. T., Love, R. P. & Chelico, L. Suppression of APOBEC3-mediated restriction of HIV-1 by Vif. Front Microbiol. 5, 450 (2014).
3. Bransteitter, R., Prochnow, C. & Chen, X. S. The current structural and functional understanding of APOBEC deaminases. Cell. Mol. Life. Sci. 66, 3137-3147 (2009).
4. Fu, Y. et al. DNA cytosine and methylcytosine deamination by APOBEC3B: enhancing methylcytosine deamination by engineering APOBEC3B. Biochem. J. 471, 25-35 (2015).
5. 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, 646-650 (2002).
6. Mangeat, B. et al. Broad antiretroviral defence by human APOBEC3G through lethal editing of nascent reverse transcripts. Nature 424, 99-103 (2003).
7. Yu, Q. et al. Single-strand specificity of APOBEC3G accounts for minus-strand deamination of the HIV genome. Nat. Struct. Mol. Biol. 11, 435-442 (2004).
8. Harris, R. S. et al. DNA deamination mediates innate immunity to retroviral infection. Cell 113, 803-809 (2003).
9. Chelico, L., Pham, P., Calabrese, P. & Goodman, M. F. APOBEC3G DNA deaminase acts processively 30-4 50 on single-stranded DNA. Nat. Struct. Mol. Biol. 13, 392-399 (2006).
10. Iwatani, Y., Takeuchi, H., Strebel, K. & Levin, J. G. Biochemical activities of highly purified, catalytically active human APOBEC3G: correlation with antiviral effect. J. Virol. 80, 5992-6002 (2006).
11. Navarro, F. et al. Complementary function of the two catalytic domains of APOBEC3G. Virology 333, 374-386 (2005).
12. Svarovskaia, E. S. et al. Human apolipoprotein B mRNA-editing enzymecatalytic polypeptide-like 3G (APOBEC3G) is incorporated into HIV-1 virions through interactions with viral and nonviral RNAs. J. Biol. Chem. 279, 35822-35828 (2004).
13. Wang, T. et al. 7SL RNA mediates virion packaging of the antiviral cytidine deaminase APOBEC3G. J. Virol. 81, 13112-13124 (2007).
14. Chelico, L., Prochnow, C., Erie, D. A., Chen, X. S. & Goodman, M. F. Structural model for deoxycytidine deamination mechanisms of the HIV-1 inactivation enzyme APOBEC3G. J. Biol. Chem. 285, 16195-16205 (2010).
15. Holden, L. G. et al. Crystal structure of the anti-viral APOBEC3G catalytic domain and functional implications. Nature 456, 121-124 (2008).
16. Iwatani, Y. et al. Deaminase-independent inhibition of HIV-1 reverse transcription by APOBEC3G. Nucleic Acids Res. 35, 7096-7108 (2007).
17. Bishop, K. N., Verma, M., Kim, E. Y., Wolinsky, S. M. & Malim, M. H. APOBEC3G inhibits elongation of HIV-1 reverse transcripts. PLoS Pathog. 4, e1000231 (2008).
18. Adolph, M. B., Webb, J. & Chelico, L. Retroviral restriction factor APOBEC3G delays the initiation of DNA synthesis by HIV-1 reverse transcriptase. PLoS ONE 8, e64196 (2013).
19. 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, 1398-1403 (2003).
20. Stopak, K., de Noronha, C., Yonemoto, W. & Greene, W. C. HIV-1 Vif blocks the antiviral activity of APOBEC3G by impairing both its translation and intracellular stability. Mol. Cell 12, 591-601 (2003).
21. Yu, X. et al. Induction of APOBEC3G ubiquitination and degradation by an HIV-1 Vif-Cul5-SCF complex. Science 302, 1056-1060 (2003).
22. Mehle, A. et al. Vif overcomes the innate antiviral activity of APOBEC3G by promoting its degradation in the ubiquitin-proteasome pathway. J. Biol. Chem. 279, 7792-7798 (2004).
23. Jager, S. et al. Vif hijacks CBF-beta to degrade APOBEC3G and promote HIV-1 infection. Nature 481, 371-375 (2012).
24. Zhang, W., Du, J., Evans, S. L., Yu, Y. & Yu, X. F. T-cell differentiation factor CBF-beta regulates HIV-1 Vif-mediated evasion of host restriction. Nature 481, 376-379 (2012).
25. Huthoff, H. & Malim, M. H. Identification of amino acid residues in APOBEC3G required for regulation by human immunodeficiency virus type 1 Vif and Virion encapsidation. J. Virol. 81, 3807-3815 (2007).
26. Lavens, D. et al. Definition of the interacting interfaces of Apobec3G and HIV-1 Vif using MAPPIT mutagenesis analysis. Nucleic Acids Res. 38, 1902-1912 (2010).
27. Bogerd, H. P., Doehle, B. P., Wiegand, H. L. & Cullen, B. R. A single amino acid difference in the host APOBEC3G protein controls the primate species specificity of HIV type 1 virion infectivity factor. Proc. Natl Acad. Sci. USA 101, 3770-3774 (2004).
28. Mangeat, B., Turelli, P., Liao, S. & Trono, D. A single amino acid determinant governs the species-specific sensitivity of APOBEC3G to Vif action. J. Biol. Chem. 279, 14481-14483 (2004).
29. Schrofelbauer, B., Chen, D. & Landau, N. R. A single amino acid of APOBEC3G controls its species-specific interaction with virion infectivity factor (Vif). Proc. Natl Acad. Sci. USA 101, 3927-3932 (2004).
30. Xu, H. et al. A single amino acid substitution in human APOBEC3G antiretroviral enzyme confers resistance to HIV-1 virion infectivity factor-induced depletion. Proc. Natl Acad. Sci. USA 101, 5652-5657 (2004).
31. Letko, M., Booiman, T., Kootstra, N., Simon, V. & Ooms, M. Identification of the HIV-1 Vif and human APOBEC3G protein interface. Cell Rep. 13, 1789-1799 (2015).
32. Kouno, T. et al. Structure of the Vif-binding domain of the antiviral enzyme APOBEC3G. Nat. Struct. Mol. Biol. 22, 485-491 (2015).
33. Chen, K. M. et al. Structure of the DNA deaminase domain of the HIV-1 restriction factor APOBEC3G. Nature 452, 116-119 (2008).
34. Shandilya, S. M. et al. Crystal structure of the APOBEC3G catalytic domain reveals potential oligomerization interfaces. Structure 18, 28-38 (2010).
35. Kitamura, S. et al. The APOBEC3C crystal structure and the interface for HIV-1 Vif binding. Nat. Struct. Mol. Biol. 19, 1005-1010 (2012).
36. Siu, K. K., Sultana, A., Azimi, F. C. & Lee, J. E. Structural determinants of HIV-1 Vif susceptibility and DNA binding in APOBEC3F. Nat. Commun. 4, 2593 (2013).
37. Bohn, M. F. et al. Crystal structure of the DNA cytosine deaminase APOBEC3F: The catalytically active and HIV-1 Vif-binding domain. Structure 21, 1042-1050 (2013).
38. Byeon, I. J. et al. NMR structure of human restriction factor APOBEC3A reveals substrate binding and enzyme specificity. Nat. Commun. 4, 1890 (2013).
39. Bohn, M. F. et al. The ssDNA mutator APOBEC3A is regulated by cooperative dimerization. Structure 23, 903-911 (2015).
40. Harjes, E. et al. An extended structure of the APOBEC3G catalytic domain suggests a unique holoenzyme model. J. Mol. Biol. 389, 819-832 (2009).
41. Shi, K., Carpenter, M. A., Kurahashi, K., Harris, R. S. & Aihara, H. Crystal structure of the DNA deaminase APOBEC3B catalytic domain. J. Biol. Chem. 290, 28120-28130 (2015).
42. Burgess, R. R. Use of polyethyleneimine in purification of DNA-binding proteins. Methods Enzymol. 208, 3-10 (1991).
43. Nakashima, M. et al. Structural insights into HIV-1 Vif-APOBEC3F interaction. J. Virol. 90, 1034-1047 (2015).
44. Shlyakhtenko, L. S. et al. Nanoscale structure and dynamics of ABOBEC3G complexes with single-stranded DNA. Biochemistry 51, 6432-6440 (2012).
45. Pham, P., Bransteitter, R., Petruska, J. & Goodman, M. F. Processive AID-catalysed cytosine deamination on single-stranded DNA simulates somatic hypermutation. Nature 424, 103-107 (2003).
46. Shandilya, S. M., Bohn, M. F. & Schiffer, C. A. A computational analysis of the structural determinants of APOBEC3's catalytic activity and vulnerability to HIV-1 Vif. Virology 471-473C, 105-116 (2014).
47. Teh, A. H. et al. The 1. 48 A resolution crystal structure of the homotetrameric cytidine deaminase from mouse. Biochemistry 45, 7825-7833 (2006).
48. Mitra, M. et al. Structural determinants of human APOBEC3A enzymatic and nucleic acid binding properties. Nucleic Acids Res. 42, 1095-1110 (2014).
49. Lu, X. et al. Crystal structure of DNA cytidine deaminase ABOBEC3G catalytic deamination domain suggests a binding mode of full-length enzyme to single-stranded DNA. J. Biol. Chem. 290, 4010-4021 (2014).
50. Logue, E. C. et al. A DNA sequence recognition loop on APOBEC3A controls substrate specificity. PLoS ONE 9, e97062 (2014).
51. Bulliard, Y. et al. Structure-function analyses point to a polynucleotideaccommodating groove essential for APOBEC3A restriction activities. J. Virol. 85, 1765-1776 (2011).
52. Conticello, S. G., Thomas, C. J., Petersen-Mahrt, S. K. & Neuberger, M. S. Evolution of the AID/APOBEC family of polynucleotide (deoxy)cytidine deaminases. Mol. Biol. Evol. 22, 367-377 (2005).
53. Chiu, Y. L. et al. Cellular APOBEC3G restricts HIV-1 infection in resting CD4 T cells. Nature 435, 108-114 (2005).
54. Wedekind, J. E. et al. Nanostructures of APOBEC3G support a hierarchical assembly model of high molecular mass ribonucleoprotein particles from dimeric subunits. J. Biol. Chem. 281, 38122-38126 (2006).
55. Huthoff, H., Autore, F., Gallois-Montbrun, S., Fraternali, F. & Malim, M. H. RNA-dependent oligomerization of APOBEC3G is required for restriction of HIV-1. PLoS Pathog. 5, e1000330 (2009).
56. Bulliard, Y. et al. Functional analysis and structural modeling of human APOBEC3G reveal the role of evolutionarily conserved elements in the inhibition of human immunodeficiency virus type 1 infection and Alu transposition. J. Virol. 83, 12611-12621 (2009).
57. Polevoda, B. et al. RNA binding to APOBEC3G induces the disassembly of functional deaminase complexes by displacing single-stranded DNA substrates. Nucleic Acids Res. 43, 9434-9445 (2015).
58. Kelley, L. A., Mezulis, S., Yates, C. M., Wass, M. N. & Sternberg, M. J. The Phyre2 web portal for protein modeling, prediction and analysis. Nature Protocols 10, 845-858 (2015).
59. Baker, N. A., Sept, D., Joseph, S., Holst, M. J. & McCammon, J. A. Electrostatics of nanosystems: Application to microtubules and the ribosome. Proc. Natl Acad. Sci. USA 98, 10037-10041 (2001).
60. Krissinel, E. & Henrick, K. Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions. Acta Crystallogr. Sect. D 60, 2256-2268 (2004).
61. Krissinel, E. & Henrick, K. Inference of macromolecular assemblies from crystalline state. J. Mol. Biol. 372, 774-797 (2007).
62. Ho, B. K. & Gruswitz, F. HOLLOW: generating accurate representations of channel and interior surfaces in molecular structures. BMC Struct. Biol. 8, 49 (2008).
63. Nguyen, K. L. et al. Codon optimization of the HIV-1 vpu and vif genes stabilizes their mRNA and allows for highly efficient Rev-independent expression. Virology 319, 163-175 (2004).
64. Prochnow, C., Bransteitter, R., Klein, M. G., Goodman, M. F. & Chen, X. S. The APOBEC-2 crystal structure and functional implications for the deaminase AID. Nature 445, 447-451 (2007).