1.92 Angstrom Zinc-Free APOBEC3F Catalytic Domain Crystal Structure

Journal of Molecular Biology

Volumn 428, Issue 11, 2016, Pages 2307-2316

  Shaban, Nadine M ^a   Shi, Ke ^a   Li, Ming ^a   Aihara, Hideki ^a   Harris, Reuben S ^a,b  

^a UNIVERSITY OF MINNESOTA   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

Author keywords

APOBEC3 regulation; cytosine deaminase; HIV 1 restriction factor; X ray crystallography; zinc free and zinc bound APOBEC3 structures

Indexed keywords

APOLIPOPROTEIN B MESSENGER RNA EDITING ENZYME CATALYTIC POLYPEPTIDE 3F; COBALT; CYSTEINE; ZINC; CYTOSINE DEAMINASE; PROTEIN BINDING; VIF PROTEIN;

ARTICLE; CRYSTAL STRUCTURE; CRYSTALLIZATION; DISULFIDE BOND; ENZYME ACTIVE SITE; ENZYME RECONSTITUTION; PH; PHYLOGENY; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN STRUCTURE; CHEMISTRY; HUMAN IMMUNODEFICIENCY VIRUS 1; METABOLISM; PHYSIOLOGY;

CATALYTIC DOMAIN; CYSTEINE; CYTOSINE DEAMINASE; HIV-1; PROTEIN BINDING; VIF GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; ZINC;

EID: 84969850614     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2016.04.026     Document Type: Article

References (61)

1. E.W. Refsland, and R.S. Harris The APOBEC3 family of retroelement restriction factors Curr. Top. Microbiol. Immunol. 371 2013 1 27
2. S.G. Conticello The AID/APOBEC family of nucleic acid mutators Genome Biol. 9 2008 229
3. R.A. Goodman, M.R. Macbeth, and P.A. Beal ADAR proteins: structure and catalytic mechanism Curr. Top. Microbiol. Immunol. 353 2012 1 33
4. J.S. Albin, W.L. Brown, and R.S. Harris Catalytic activity of APOBEC3F is required for efficient restriction of Vif-deficient human immunodeficiency virus Virology. 450-451 2014 49 54
5. R.K. Holmes, F.A. Koning, K.N. Bishop, and M.H. Malim APOBEC3F can inhibit the accumulation of HIV-1 reverse transcription products in the absence of hypermutation. Comparisons with APOBEC3G J. Biol. Chem. 282 2007 2587 2595
6. E. Miyagi, C.R. Brown, S. Opi, M. Khan, R. Goila-Gaur, and S. Kao Stably expressed APOBEC3F has negligible antiviral activity J. Virol. 84 2010 11,067 11,075
7. R.S. Harris, and J.P. Dudley APOBECs and virus restriction Virology 479-480 2015 131 145
8. S.M. Shandilya, M.F. Bohn, and C.A. Schiffer A computational analysis of the structural determinants of APOBEC3's catalytic activity and vulnerability to HIV-1 Vif Virology. 471-473 2014 105 116
9. M.F. Bohn, S.M. Shandilya, T.V. Silvas, E.A. Nalivaika, T. Kouno, and B.A. Kelch The ssDNA mutator APOBEC3A is regulated by cooperative dimerization Structure. 23 2015 903 911
10. M. Mitra, K. Hercik, I.J. Byeon, J. Ahn, S. Hill, and K. Hinchee-Rodriguez Structural determinants of human APOBEC3A enzymatic and nucleic acid binding properties Nucleic Acids Res. 42 2014 1095 1110
11. K. Shi, M.A. Carpenter, K. Kurahashi, R.S. Harris, and H. Aihara Crystal structure of the DNA deaminase APOBEC3B catalytic domain J. Biol. Chem. 290 2015 28,120 28,130
12. S. Kitamura, H. Ode, M. Nakashima, M. Imahashi, Y. Naganawa, and T. Kurosawa The APOBEC3C crystal structure and the interface for HIV-1 Vif binding Nat. Struct. Mol. Biol. 19 2012 1005 1010
13. M.F. Bohn, S.M. Shandilya, J.S. Albin, T. Kouno, B.D. Anderson, and R.M. McDougle Crystal structure of the DNA cytosine deaminase APOBEC3F: the catalytically active and HIV-1 Vif-binding domain Structure. 21 2013 1042 1050
14. K.K. Siu, A. Sultana, F.C. Azimi, and J.E. Lee Structural determinants of HIV-1 Vif susceptibility and DNA binding in APOBEC3F Nat. Commun. 4 2013 2593
15. M. Nakashima, H. Ode, T. Kawamura, S. Kitamura, Y. Naganawa, and H. Awazu Structural insights into HIV-1 Vif-APOBEC3F interaction J. Virol. 90 2015 1034 1047
16. T. Kouno, E.M. Luengas, M. Shigematsu, S.M. Shandilya, J. Zhang, and L. Chen Structure of the Vif-binding domain of the antiviral enzyme APOBEC3G Nat. Struct. Mol. Biol. 22 2015 485 491
17. K.M. Chen, E. Harjes, P.J. Gross, A. Fahmy, Y. Lu, and K. Shindo Structure of the DNA deaminase domain of the HIV-1 restriction factor APOBEC3G Nature. 452 2008 116 119
18. S.M. Shandilya, M.N. Nalam, E.A. Nalivaika, P.J. Gross, J.C. Valesano, and K. Shindo Crystal structure of the APOBEC3G catalytic domain reveals potential oligomerization interfaces Structure. 18 2010 28 38
19. L.G. Holden, C. Prochnow, Y.P. Chang, R. Bransteitter, L. Chelico, and U. Sen Crystal structure of the anti-viral APOBEC3G catalytic domain and functional implications Nature. 456 2008 121 124
20. A. Furukawa, T. Nagata, A. Matsugami, Y. Habu, R. Sugiyama, and F. Hayashi Structure, interaction and real-time monitoring of the enzymatic reaction of wild-type APOBEC3G EMBO J. 28 2009 440 451
21. M. Li, S.M. Shandilya, M.A. Carpenter, A. Rathore, W.L. Brown, and A.L. Perkins First-in-class small molecule inhibitors of the single-strand DNA cytosine deaminase APOBEC3G ACS Chem. Biol. 7 2012 506 517
22. X. Lu, T. Zhang, Z. Xu, S. Liu, B. Zhao, and W. Lan 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 2015 4010 4021
23. A.M. Land, N.M. Shaban, L. Evans, J.F. Hultquist, J.S. Albin, and R.S. Harris APOBEC3F determinants of HIV-1 Vif sensitivity J. Virol. 88 2014 12,923 12,927
24. J.S. Albin, R.S. LaRue, J.A. Weaver, W.L. Brown, K. Shindo, and E. Harjes A single amino acid in human APOBEC3F alters susceptibility to HIV-1 Vif J. Biol. Chem. 285 2010 40,785 40,792
25. A. Rathore, M.A. Carpenter, O. Demir, T. Ikeda, M. Li, and N.M. Shaban The local dinucleotide preference of APOBEC3G can be altered from 5′-CC to 5′-TC by a single amino acid substitution J. Mol. Biol. 425 2013 4442 4454
26. M.A. Carpenter, E. Rajagurubandara, P. Wijesinghe, and A.S. Bhagwat Determinants of sequence-specificity within human AID and APOBEC3G DNA Repair. 9 2010 579 587
27. R.M. Kohli, S.R. Abrams, K.S. Gajula, R.W. Maul, P.J. Gearhart, and J.T. Stivers A portable hot spot recognition loop transfers sequence preferences from APOBEC family members to activation-induced cytidine deaminase J. Biol. Chem. 284 2009 22,898 22,904
28. V. Caval, M.S. Bouzidi, R. Suspene, H. Laude, M.C. Dumargne, and A. Bashamboo Molecular basis of the attenuated phenotype of human APOBEC3B DNA mutator enzyme Nucleic Acids Res. 43 2015 9340 9349
29. Y. Bulliard, I. Narvaiza, A. Bertero, S. Peddi, U.F. Rohrig, and M. Ortiz Structure-function analyses point to a polynucleotide-accommodating groove essential for APOBEC3A restriction activities J. Virol. 85 2011 1765 1776
30. S. Harjes, W.C. Solomon, M. Li, K.M. Chen, E. Harjes, and R.S. Harris Impact of H216 on the DNA binding and catalytic activities of the HIV restriction factor APOBEC3G J. Virol. 87 2013 7008 7014
31. Y. Fu, F. Ito, G. Zhang, B. Fernandez, H. Yang, and X.S. Chen DNA cytosine and methylcytosine deamination by APOBEC3B: enhancing methylcytosine deamination by engineering APOBEC3B Biochem. J. 471 2015 25 35
32. T.H. Yang, J.L. Cleland, X. Lam, J.D. Meyer, L.S. Jones, and T.W. Randolph Effect of zinc binding and precipitation on structures of recombinant human growth hormone and nerve growth factor J. Pharm. Sci. 89 2000 1480 1485
33. D. Matulis Selective precipitation of proteins. Curr. Protoc. Protein Sci. 83 2016 4.5.1 4.5.37 10.1002/0471140864.ps0405s83
34. I.J. Byeon, J. Ahn, M. Mitra, C.H. Byeon, K. Hercik, and J. Hritz NMR structure of human restriction factor APOBEC3A reveals substrate binding and enzyme specificity Nat. Commun. 4 2013 1890
35. C. Prochnow, R. Bransteitter, M.G. Klein, M.F. Goodman, and X.S. Chen The APOBEC-2 crystal structure and functional implications for the deaminase AID Nature. 445 2007 447 451
36. L. Betts, S. Xiang, S.A. Short, R. Wolfenden, and C.W. Carter Jr. Cytidine deaminase. The 2.3 Å crystal structure of an enzyme: transition-state analog complex J. Mol. Biol. 235 1994 635 656
37. S.J. Chung, J.C. Fromme, and G.L. Verdine. Structure of human cytidine deaminase bound to a potent inhibitor J. Med. Chem 48 2005 658 660
38. Y. Elias, and R.H. Huang Biochemical and structural studies of A-to-I editing by tRNA:A34 deaminases at the wobble position of transfer RNA Biochemistry. 44 2005 12,057 12,065
39. A.H. Teh, M. Kimura, M. Yamamoto, N. Tanaka, I. Yamaguchi, and T. Kumasaka The 1.48 Å resolution crystal structure of the homotetrameric cytidine deaminase from mouse Biochemistry. 45 2006 7825 7833
40. K. Xie, M.P. Sowden, G.S. Dance, A.T. Torelli, H.C. Smith, and J.E. Wedekind The structure of a yeast RNA-editing deaminase provides insight into the fold and function of activation-induced deaminase and APOBEC-1 Proc. Natl. Acad. Sci. U. S. A. 101 2004 8114 8119
41. E. Johansson, N. Mejlhede, J. Neuhard, and S. Larsen Crystal structure of the tetrameric cytidine deaminase from Bacillus subtilis at 2.0 Å resolution Biochemistry. 41 2002 2563 2570
42. T.P. Ko, J.J. Lin, C.Y. Hu, Y.H. Hsu, A.H. Wang, and S.H. Liaw Crystal structure of yeast cytosine deaminase. Insights into enzyme mechanism and evolution J. Biol. Chem. 278 2003 19,111 19,117
43. H.C. Losey, A.J. Ruthenburg, and G.L. Verdine Crystal structure of Staphylococcus aureus tRNA adenosine deaminase TadA in complex with RNA Nat. Struct. Mol. Biol. 13 2006 153 159
44. M.R. Macbeth, H.L. Schubert, A.P. Vandemark, A.T. Lingam, C.P. Hill, and B.L. Bass Inositol hexakisphosphate is bound in the ADAR2 core and required for RNA editing Science. 309 2005 1534 1539
45. D.K. Wilson, F.B. Rudolph, and F.A. Quiocho Atomic structure of adenosine deaminase complexed with a transition-state analog: understanding catalysis and immunodeficiency mutations Science. 252 1991 1278 1284
46. S. Xiang, S.A. Short, R. Wolfenden, and C.W. Carter Jr. The structure of the cytidine deaminase-product complex provides evidence for efficient proton transfer and ground-state destabilization Biochemistry. 36 1997 4768 4774
47. M. Kuratani, R. Ishii, Y. Bessho, R. Fukunaga, T. Sengoku, and M. Shirouzu Crystal structure of tRNA adenosine deaminase (TadA) from Aquifex aeolicus J. Biol. Chem. 280 2005 16,002 16,008
48. S. Xiang, S.A. Short, R. Wolfenden, and C.W. Carter Jr. Transition-state selectivity for a single hydroxyl group during catalysis by cytidine deaminase Biochemistry. 34 1995 4516 4523
49. E. Johansson, J. Neuhard, M. Willemoes, and S. Larsen Structural, kinetic, and mutational studies of the zinc ion environment in tetrameric cytidine deaminase Biochemistry. 43 2004 6020 6029
50. G.C. Ireton, G. McDermott, M.E. Black, and B.L. Stoddard The structure of Escherichia coli cytosine deaminase J. Mol. Biol. 315 2002 687 697
51. J. Kim, V. Malashkevich, S. Roday, M. Lisbin, V.L. Schramm, and S.C. Almo Structural and kinetic characterization of Escherichia coli TadA, the wobble-specific tRNA deaminase Biochemistry. 45 2006 6407 6416
52. T. Kumasaka, M. Yamamoto, M. Furuichi, M. Nakasako, A.H. Teh, and M. Kimura Crystal structures of blasticidin S deaminase (BSD): implications for dynamic properties of catalytic zinc J. Biol. Chem. 282 2007 37,103 37,111
53. T. Helleday, S. Eshtad, and S. Nik-Zainal Mechanisms underlying mutational signatures in human cancers Nat. Rev. Genet. 15 2014 585 598
54. C. Swanton, N. McGranahan, G.J. Starrett, and R.S. Harris APOBEC enzymes: mutagenic fuel for cancer evolution and heterogeneity Cancer Discovery 5 2015 704 712
55. S.A. Roberts, and D.A. Gordenin Hypermutation in human cancer genomes: footprints and mechanisms Nat. Rev. Cancer. 14 2014 786 800
56. N.M. Giles, A.B. Watts, G.I. Giles, F.H. Fry, J.A. Littlechild, and C. Jacob Metal and redox modulation of cysteine protein function Chem. Biol. 10 2003 677 693
57. Z. Otwinowski, and W. Minor Processing of x-ray diffraction data collected in oscillation mode C.W. Carter Jr R.M. Sweets, Methods in Enzymology Macromolecular Crystallography, Part A 276 1997 Academic Press New York 307 326
58. A.J. McCoy, R.W. Grosse-Kunstleve, P.D. Adams, M.D. Winn, L.C. Storoni, and R.J. Read Phaser crystallographic software J. Appl. Crystallogr. 40 2007 658 674
59. P. Emsley, B. Lohkamp, W.G. Scott, and K. Cowtan Features and development of Coot Acta crystallographica. Section D, Biol. Crystallogr. 66 2010 486 501
60. P.D. Adams, P.V. Afonine, G. Bunkoczi, V.B. Chen, I.W. Davis, and N. Echols PHENIX: a comprehensive Python-based system for macromolecular structure solution Acta Crystallogr. Sect. D: Biol. Crystallogr. 66 2010 213 221
61. M.A. Carpenter, M. Li, A. Rathore, L. Lackey, E.K. Law, and A.M. Land Methylcytosine and normal cytosine deamination by the foreign DNA restriction enzyme APOBEC3A J. Biol. Chem. 287 2012 34,801 34,808