Zinc enhancement of cytidine deaminase activity highlights a potential allosteric role of loop-3 in regulating APOBEC3 enzymes

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Marx, Ailie ^a   Galilee, Meytal ^a   Alian, Akram ^a  

^a TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

CYTIDINE DEAMINASE; PROTEIN SUBUNIT; RECOMBINANT PROTEIN; ZINC;

ALLOSTERISM; AMINO ACID SEQUENCE; BINDING SITE; BIOSYNTHESIS; CHEMISTRY; GENETICS; HUMAN; ISOLATION AND PURIFICATION; METABOLISM; MOLECULAR DYNAMICS; MOLECULAR GENETICS; PROTEIN SECONDARY STRUCTURE; PROTEIN SUBUNIT; SEQUENCE ALIGNMENT; SITE DIRECTED MUTAGENESIS;

ALLOSTERIC REGULATION; AMINO ACID SEQUENCE; BINDING SITES; CYTIDINE DEAMINASE; HUMANS; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PROTEIN STRUCTURE, SECONDARY; PROTEIN SUBUNITS; RECOMBINANT PROTEINS; SEQUENCE ALIGNMENT; ZINC;

EID: 84950342088     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep18191     Document Type: Article

References (41)

1. Rebhandl, S., Huemer, M., Greil, R. & Geisberger, R. AID/APOBEC deaminases and cancer. Oncoscience 2, 320-333 (2015).
2. Swanton, C., McGranahan, N., Starrett, G. J. & Harris, R. S. APOBEC Enzymes: Mutagenic Fuel for Cancer Evolution and Heterogeneity. Cancer Discov. doi: 10.1158/2159-8290.CD-15-0344 (2015).
3. Conticello, S. G. The AID/APOBEC family of nucleic acid mutators. Genome Biol 9, 229, doi: 10.1186/gb-2008-9-6-229 (2008).
4. Vasudevan, A. A. et al. Structural features of antiviral DNA cytidine deaminases. Biol Chem 394, 1357-1370, doi: 10.1515/hsz-2013-0165 (2013).
5. Refsland, E. W. & Harris, R. S. The APOBEC3 Family of Retroelement Restriction Factors. Curr Top Microbiol Immunol 371, 1-27, doi: 10.1007/978-3-642-37765-5-1 (2013).
6. Gerber, A. P. & Keller, W. RNA editing by base deamination: More enzymes, more targets, new mysteries. Trends Biochem Sci 26, 376-384 (2001).
7. Rathore, A. et al. The Local Dinucleotide Preference of APOBEC3G Can Be Altered from 5?-CC to 5?-TC by a Single Amino Acid Substitution. J Mol Biol, doi: 10.1016/j.jmb.2013.07.040 (2013).
8. 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, doi: 10.1074/jbc.M114.624262 (2015).
9. Marx, A. & Alian, A. The first crystal structure of a dTTP-bound deoxycytidylate deaminase validates and details the allostericinhibitor binding site. J Biol Chem 290, 682-690, doi: 10.1074/jbc.M114.617720 (2015).
10. Losey, H. C., Ruthenburg, A. J. & Verdine, G. L. Crystal structure of Staphylococcus aureus tRNA adenosine deaminase TadA in complex with RNA. Nat Struct Mol Biol 13, 153-159, doi: 10.1038/nsmb1047 (2006).
11. Kohli, R. M. et al. A portable hot spot recognition loop transfers sequence preferences from APOBEC family members to activationinduced cytidine deaminase. J Biol Chem 284, 22898-22904, doi: 10.1074/jbc.M109.025536 (2009).
12. Holden, L. G. et al. Crystal structure of the anti-viral APOBEC3G catalytic domain and functional implications. Nature 456, 121-124, doi: 10.1038/nature07357 (2008).
13. King, J. J. et al. Catalytic pocket inaccessibility of activation-induced cytidine deaminase is a safeguard against excessive mutagenic activity. Structure 23, 615-627, doi: 10.1016/j.str.2015.01.016 (2015).
14. Byeon, I. J. et al. NMR structure of human restriction factor APOBEC3A reveals substrate binding and enzyme specificity. Nat Commun 4, 1890, doi: 10.1038/ncomms2883 (2013).
15. 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, doi: 10.1038/nature05492 (2007).
16. Shandilya, S. M. et al. Crystal structure of the APOBEC3G catalytic domain reveals potential oligomerization interfaces. Structure 18, 28-38, doi: 10.1016/j.str.2009.10.016 (2010).
17. Bohn, M. F. et al. The ssDNA Mutator APOBEC3A Is Regulated by Cooperative Dimerization. Structure 23, 903-911, doi: 10.1016/j. str.2015.03.016 (2015).
18. Kitamura, S. et al. The APOBEC3C crystal structure and the interface for HIV-1 Vif binding. Nat Struct Mol Biol 19, 1005-1010, doi: 10.1038/nsmb.2378 (2012).
19. Siu, K. K., Sultana, A., Azimi, F. C. & Lee, J. E. Structural determinants of HIV-Vif susceptibility and DNA binding in APOBEC3F. Nat Commun 4, 2593, doi: 10.1038/ncomms3593 (2013).
20. 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, doi: 10.1016/j.str.2013.04.010 (2013).
21. Kouno, T. et al. Structure of the Vif-binding domain of the antiviral enzyme APOBEC3G. Nat Struct Mol Biol 22, 485-491, doi: 10.1038/nsmb.3033 (2015).
22. Li, M. et al. First-in-class small molecule inhibitors of the single-strand DNA cytosine deaminase APOBEC3G. ACS Chem Biol 7, 506-517, doi: 10.1021/cb200440y (2012).
23. Laitaoja, M., Valjakka, J. & Janis, J. Zinc coordination spheres in protein structures. Inorg Chem 52, 10983-10991, doi: 10.1021/ic401072d (2013).
24. Zhang, Y. et al. Chloroviruses encode a bifunctional dCMP-dCTP deaminase that produces two key intermediates in dTTP formation. J Virol 81, 7662-7671, doi: 10.1128/JVI.00186-07 (2007).
25. Conticello, S. G., Langlois, M. A., Yang, Z. & Neuberger, M. S. DNA deamination in immunity: AID in the context of its APOBEC relatives. Adv Immunol 94, 37-73, doi: 10.1016/S0065-2776(06)94002-4 (2007).
26. Nowarski, R., Britan-Rosich, E., Shiloach, T. & Kotler, M. Hypermutation by intersegmental transfer of APOBEC3G cytidine deaminase. Nat Struct Mol Biol 15, 1059-1066, doi: 10.1038/nsmb.1495 (2008).
27. Shlyakhtenko, L. S. et al. Atomic force microscopy studies provide direct evidence for dimerization of the HIV restriction factor APOBEC3G. J Biol Chem 286, 3387-3395, doi: 10.1074/jbc.M110.195685 (2011).
28. Bulliard, Y. et al. Structure-function analyses point to a polynucleotide-accommodating groove essential for APOBEC3A restriction activities. J Virol 85, 1765-1776, doi: 10.1128/JVI.01651-10 (2011).
29. Shivarov, V., Shinkura, R. & Honjo, T. Dissociation of in vitro DNA deamination activity and physiological functions of AID mutants. Proc Natl Acad Sci USA 105, 15866-15871, doi: 10.1073/pnas.0806641105 (2008).
30. Ikeda, T. et al. Intrinsic restriction activity by apolipoprotein B mRNA editing enzyme APOBEC1 against the mobility of autonomous retrotransposons. Nucleic Acids Res 39, 5538-5554, doi: 10.1093/nar/gkr124 (2011).
31. Macbeth, M. R.et al. Inositol hexakisphosphate is bound in the ADAR2 core and required for RNA editing. Science 309, 1534-1539, doi: 10.1126/science.1113150 (2005).
32. Chen, K. M. et al. Extensive mutagenesis experiments corroborate a structural model for the DNA deaminase domain of APOBEC3G. FEBS Lett 581, 4761-4766, doi: 10.1016/j.febslet.2007.08.076 (2007).
33. Demorest, Z. L., Li, M. & Harris, R. S. Phosphorylation directly regulates the intrinsic DNA cytidine deaminase activity of activationinduced deaminase and APOBEC3G protein. J Biol Chem 286, 26568-26575, doi: 10.1074/jbc.M111.235721 (2011).
34. Logue, E. C. et al. A DNA sequence recognition loop on APOBEC3A controls substrate specificity. PLoS One 9, e97062, doi: 10.1371/journal.pone.0097062 (2014).
35. Dang, Y. et al. Identification of a single amino acid required for APOBEC3 antiretroviral cytidine deaminase activity. J Virol 85, 5691-5695, doi: 10.1128/JVI.00243-11 (2011).
36. 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 471-473, 105-116, doi: 10.1016/j.virol.2014.09.023 (2014).
37. Nair, S., Sanchez-Martinez, S., Ji, X. & Rein, A. Biochemical and biological studies of mouse APOBEC3. J Virol 88, 3850-3860, doi: 10.1128/JVI.03456-13 (2014).
38. Santa-Marta, M., da Silva, F. A., Fonseca, A. M. & Goncalves, J. HIV-1 Vif can directly inhibit apolipoprotein B mRNA-editing enzyme catalytic polypeptide-like 3 G-mediated cytidine deamination by using a single amino acid interaction and without protein degradation. J Biol Chem 280, 8765-8775, doi: 10.1074/jbc.M409309200 (2005).
39. Britan-Rosich, E., Nowarski, R. & Kotler, M. Multifaceted counter-APOBEC3G mechanisms employed by HIV-1 Vif. J Mol Biol 410, 1065-1076, doi: 10.1016/j.jmb.2011.03.058 (2011).
40. Notredame, C., Higgins, D. G. & Heringa, J. T-Coffee: A novel method for fast and accurate multiple sequence alignment. J Mol Biol 302, 205-217, doi: 10.1006/jmbi.2000.4042 (2000).
41. Lee, V. E., Schulman, J. M., Stiefel, E. I. & Lee, C. C. Reversible precipitation of bovine serum albumin by metal ions and synthesis, structure and reactivity of new tetrathiometallate chelating agents. J Inorg Biochem 101, 1707-1718, doi: 10.1016/j. jinorgbio.2007.07.015 (2007).