The ssDNA mutator APOBEC3A is regulated by cooperative dimerization

Structure

Volumn 23, Issue 5, 2015, Pages 903-911

  Bohn, Markus Frederik ^a   Shandilya, Shivender M D ^a   Silvas, Tania V ^a   Nalivaika, Ellen A ^a   Kouno, Takahide ^a,b   Kelch, Brian A ^a   Ryder, Sean P ^a   Kurt Yilmaz, Nese ^a   Somasundaran, Mohan ^a   Schiffer, Celia A ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APOBEC3A PROTEIN, HUMAN; CYTIDINE DEAMINASE; PROTEIN; PROTEIN BINDING; SINGLE STRANDED DNA; ZINC;

BINDING SITE; CHEMISTRY; DIMERIZATION; ENZYME SPECIFICITY; GENETICS; HUMAN; METABOLISM; MOLECULAR MODEL; MUTATION; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; X RAY CRYSTALLOGRAPHY;

BINDING SITES; CRYSTALLOGRAPHY, X-RAY; CYTIDINE DEAMINASE; DIMERIZATION; DNA, SINGLE-STRANDED; HUMANS; MODELS, MOLECULAR; MUTATION; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; PROTEINS; SUBSTRATE SPECIFICITY; ZINC;

EID: 84930189135     PISSN: 09692126     EISSN: 18784186     Source Type: Journal    
DOI: 10.1016/j.str.2015.03.016     Document Type: Article

References (76)

1. A. Ara, R.P. Love, and L. Chelico Different mutagenic potential of HIV-1 restriction factors APOBEC3G and APOBEC3F is determined by distinct single-stranded DNA scanning mechanisms PLoS Pathog. 10 2014 e1004024
2. D.S. Auld Zinc coordination sphere in biochemical zinc sites Biometals 14 2001 271 313
3. L. Betts, S. Xiang, S.A. Short, R. Wolfenden, and C.W. Carter Cytidine deaminase. The 2.3 A crystal structure of an enzyme: transition-state analog complex J. Mol. Biol. 235 1994 635 656
4. K.N. Bishop, R.K. Holmes, A.M. Sheehy, N.O. Davidson, S.-J. Cho, and M.H. Malim Cytidine deamination of retroviral DNA by diverse APOBEC proteins Curr. Biol. 14 2004 1392 1396
5. M.-F. Bohn, and C.A. Schiffer REdiii: a pipeline for automated structure solution Acta Crystallogr. D Biol. Crystallogr. 71 2015 10.1107/S139900471500303X
6. M.-F. Bohn, S.M.D. Shandilya, J.S. Albin, T. Kouno, B.D. Anderson, R.M. McDougle, M.A. Carpenter, A. Rathore, L. Evans, and A.N. Davis Crystal structure of the DNA cytosine deaminase APOBEC3F: the catalytically active and HIV-1 Vif-binding domain Structure 21 2013 1042 1050
7. Y. Bulliard, I. Narvaiza, A. Bertero, S. Peddi, U.F. Röhrig, M. Ortiz, V. Zoete, N. Castro-Díaz, P. Turelli, and A. Telenti Structure-function analyses point to a polynucleotide-accommodating groove essential for APOBEC3A restriction activities J. Virol. 85 2011 1765 1776
8. M.B. Burns, L. Lackey, M.A. Carpenter, A. Rathore, A.M. Land, B. Leonard, E.W. Refsland, D. Kotandeniya, N. Tretyakova, and J.B. Nikas APOBEC3B is an enzymatic source of mutation in breast cancer Nature 494 2013 366 370
9. M.B. Burns, N.A. Temiz, and R.S. Harris Evidence for APOBEC3B mutagenesis in multiple human cancers Nat. Genet. 45 2013 977 983
10. I.-J.L. Byeon, J. Ahn, M. Mitra, C.-H. Byeon, K. Hercík, J. Hritz, L.M. Charlton, J.G. Levin, and A.M. Gronenborn NMR structure of human restriction factor APOBEC3A reveals substrate binding and enzyme specificity Nat. Commun. 4 2013 1890
11. Cancer Genome Atlas Research Network Comprehensive molecular characterization of urothelial bladder carcinoma Nature 507 2014 315 322
12. M.A. Carpenter, M. Li, A. Rathore, L. Lackey, E.K. Law, A.M. Land, B. Leonard, S.M.D. Shandilya, M.-F. Bohn, and C.A. Schiffer Methylcytosine and normal cytosine deamination by the foreign DNA restriction enzyme APOBEC3A J. Biol. Chem. 287 2012 34801 34808
13. V. Caval, R. Suspène, M. Shapira, J.-P. Vartanian, and S. Wain-Hobson A prevalent cancer susceptibility APOBEC3A hybrid allele bearing APOBEC3B 3'UTR enhances chromosomal DNA damage Nat. Commun. 5 2014 5129
14. L. Chelico, P. Pham, P. Calabrese, and M.F. Goodman APOBEC3G DNA deaminase acts processively 3' - > 5' on single-stranded DNA Nat. Struct. Mol. Biol. 13 2006 392 399
15. L. Chelico, E.J. Sacho, D.A. Erie, and M.F. Goodman A model for oligomeric regulation of APOBEC3G cytosine deaminase-dependent restriction of HIV J. Biol. Chem. 283 2008 13780 13791
16. L. Chelico, C. Prochnow, D.A. Erie, X.S. Chen, and M.F. Goodman Structural model for deoxycytidine deamination mechanisms of the HIV-1 inactivation enzyme APOBEC3G J. Biol. Chem. 285 2010 16195 16205
17. K.-M.M. Chen, E. Harjes, P.J. Gross, A. Fahmy, Y. Lu, K. Shindo, R.S. Harris, and H. Matsuo Structure of the DNA deaminase domain of the HIV-1 restriction factor APOBEC3G Nature 452 2008 116 119
18. Y. Dang, X. Wang, W.J. Esselman, and Y.-H. Zheng Identification of APOBEC3DE as another antiretroviral factor from the human APOBEC family J. Virol. 80 2006 10522 10533
19. E.C. de Bruin, N. McGranahan, R. Mitter, M. Salm, D.C. Wedge, L. Yates, M. Jamal-Hanjani, S. Shafi, N. Murugaesu, and A.J. Rowan Spatial and temporal diversity in genomic instability processes defines lung cancer evolution Science 346 2014 251 256
20. W.L. DeLano The PyMOL User's Manual 2002 DeLano Scientific LLC
21. P. Emsley, and K. Cowtan Coot: model-building tools for molecular graphics Acta Crystallogr. D Biol. Crystallogr. 60 2004 2126 2132
22. D.-M. Franchini, K.-M. Schmitz, and S.K. Petersen-Mahrt 5-Methylcytosine DNA demethylation: more than losing a methyl group Annu. Rev. Genet. 46 2012 419 441
23. J.U. Guo, Y. Su, C. Zhong, G.-L. Ming, and H. Song Hydroxylation of 5-methylcytosine by TET1 promotes active DNA demethylation in the adult brain Cell 145 2011 423 434
24. G. Hache, M.T. Liddament, and R.S. Harris The retroviral hypermutation specificity of APOBEC3F and APOBEC3G is governed by the C-terminal DNA cytosine deaminase domain J. Biol. Chem. 280 2005 10920 10924
25. T.A. Halgren Identifying and characterizing binding sites and assessing druggability J. Chem. Inf. Model. 49 2009 377 389
26. A. Harari, M. Ooms, L.C.F. Mulder, and V. Simon Polymorphisms and splice variants influence the antiretroviral activity of human APOBEC3H J. Virol. 83 2009 295 303
27. E. Harjes, P.J. Gross, K.-M.M. Chen, Y. Lu, K. Shindo, R. Nowarski, J.D. Gross, M. Kotler, R.S. Harris, and H. Matsuo An extended structure of the APOBEC3G catalytic domain suggests a unique holoenzyme model J. Mol. Biol. 389 2009 819 832
28. R.S. Harris, K.N. Bishop, A.M. Sheehy, H.M. Craig, S.K. Petersen-Mahrt, I.N. Watt, M.S. Neuberger, and M.H. Malim DNA deamination mediates innate immunity to retroviral infection Cell 113 2003 803 809
29. L.G. Holden, C. Prochnow, Y.P. Chang, R. Bransteitter, L. Chelico, U. Sen, R.C. Stevens, M.F. Goodman, and X.S. Chen Crystal structure of the anti-viral APOBEC3G catalytic domain and functional implications Nature 456 2008 121 124
30. J.F. Hultquist, J.A. Lengyel, E.W. Refsland, R.S. Larue, L. Lackey, W.L. Brown, and R.S. Harris Human and rhesus APOBEC3D, APOBEC3F, APOBEC3G, and APOBEC3H demonstrate a conserved capacity to restrict Vif-deficient HIV-1 J. Virol. 85 2011 1765 1776
31. Y. Iwatani, H. Takeuchi, K. Strebel, and J.G. Levin Biochemical activities of highly purified, catalytically active human APOBEC3G: correlation with antiviral effect J. Virol. 80 2006 5992 6002
32. A. Jarmuz, A. Chester, J. Bayliss, J. Gisbourne, I. Dunham, J. Scott, and N. Navaratnam An anthropoid-specific locus of orphan C to U RNA-editing enzymes on chromosome 22 Genomics 79 2002 285 296
33. E.-Y. Kim, T. Bhattacharya, K. Kunstman, P. Swantek, F.A. Koning, M.H. Malim, and S.M. Wolinsky Human APOBEC3G-mediated editing can promote HIV-1 sequence diversification and accelerate adaptation to selective pressure J. Virol. 84 2010 10402 10405
34. S. Kitamura, H. Ode, and Y. Iwatani Structural features of antiviral APOBEC3 proteins are linked to their functional activities Front. Microbiol. 2 2011 258
35. S. Landry, I. Narvaiza, D.C. Linfesty, and M.D. Weitzman APOBEC3A can activate the DNA damage response and cause cell-cycle arrest EMBO Rep. 12 2011 444 450
36. R.S. LaRue, S.R. Jónsson, K.A.T. Silverstein, M. Lajoie, D. Bertrand, N. El-Mabrouk, I. Hötzel, V. Andrésdóttir, T.P.L. Smith, and R.S. Harris The artiodactyl APOBEC3 innate immune repertoire shows evidence for a multi-functional domain organization that existed in the ancestor of placental mammals BMC Mol. Biol. 9 2008 104
37. R.S. LaRue, V. Andresdottir, Y. Blanchard, S.G. Conticello, D. Derse, M. Emerman, W.C. Greene, S.R. Jonsson, N.R. Landau, and M. Lochelt Guidelines for naming nonprimate APOBEC3 genes and proteins J. Virol. 83 2009 494 497
38. D. Lecossier, F. Bouchonnet, F. Clavel, and A.J. Hance Hypermutation of HIV-1 DNA in the absence of the Vif protein Science 300 2003 1112
39. M. Li, S.M.D. Shandilya, M.A. Carpenter, A. Rathore, W.L. Brown, A.L. Perkins, D.A. Harki, J. Solberg, D.J. Hook, and K.K. Pandey First-in-class small molecule inhibitors of the single-strand DNA cytosine deaminase APOBEC3G ACS Chem. Biol. 7 2012 506 517
40. J. Li, Y. Chen, M. Li, M.A. Carpenter, R.M. McDougle, E.M. Luengas, P.J. Macdonald, R.S. Harris, and J.D. Mueller APOBEC3 multimerization correlates with HIV-1 packaging and restriction activity in living cells J. Mol. Biol. 426 2014 1296 1307
41. M.T. Liddament, W.L. Brown, A.J. Schumacher, and R.S. Harris APOBEC3F properties and hypermutation preferences indicate activity against HIV-1 in vivo Curr. Biol. 14 2004 1385 1391
42. L.A. Loeb, J.M. Essigmann, F. Kazazi, J. Zhang, K.D. Rose, and J.I. Mullins Lethal mutagenesis of HIV with mutagenic nucleoside analogs Proc. Natl. Acad. Sci. USA 96 1999 1492 1497
43. E.C. Logue, N. Bloch, E. Dhuey, R. Zhang, P. Cao, C. Herate, L. Chauveau, S.R. Hubbard, and N.R. Landau A DNA sequence recognition loop on APOBEC3A controls substrate specificity PLoS One 9 2014 e97062
44. R.P. Love, H. Xu, and L. Chelico Biochemical analysis of hypermutation by the deoxycytidine deaminase APOBEC3A J. Biol. Chem. 287 2012 30812 30822
45. B. Mangeat, P. Turelli, G. Caron, M. Friedli, L. Perrin, and D. Trono Broad antiretroviral defence by human APOBEC3G through lethal editing of nascent reverse transcripts Nature 424 2003 99 103
46. A.J. McCoy Solving structures of protein complexes by molecular replacement with Phaser Acta Crystallogr. D Biol. Crystallogr. 63 2007 32 41
47. M. Mitra, K. Hercík, I.-J.L. Byeon, J. Ahn, S. Hill, K. Hinchee-Rodriguez, D. Singer, C.-H. Byeon, L.M. Charlton, and G. Nam Structural determinants of human APOBEC3A enzymatic and nucleic acid binding properties Nucleic Acids Res. 42 2014 1095 1110
48. S. Nik-Zainal, L.B. Alexandrov, D.C. Wedge, P. Van Loo, C.D. Greenman, K. Raine, D. Jones, J. Hinton, J. Marshall, and L.A. Stebbings Mutational processes molding the genomes of 21 breast cancers Cell 149 2012 979 993
49. S. Nik-Zainal, D.C. Wedge, L.B. Alexandrov, M. Petljak, A.P. Butler, N. Bolli, H.R. Davies, S. Knappskog, S. Martin, and E. Papaemmanuil Association of a germline copy number polymorphism of APOBEC3A and APOBEC3B with burden of putative APOBEC-dependent mutations in breast cancer Nat. Genet. 46 2014 487 491
50. M. OhAinle, J.A. Kerns, M.M. Li, H.S. Malik, and M. Emerman Antiretroelement activity of APOBEC3H was lost twice in recent human evolution Cell Host Microbe 4 2008 249 259
51. Z. Otwinowski, and W. Minor Processing of X-ray diffraction data collected in oscillation mode Methods Enzymol. 276 1997 307 326
52. P. Pham, A. Landolph, C. Mendez, N. Li, and M.F. Goodman A biochemical analysis linking APOBEC3A to disparate HIV-1 restriction and skin cancer J. Biol. Chem. 288 2013 29294 29304
53. S.A. Roberts, J. Sterling, C. Thompson, S. Harris, D. Mav, R. Shah, L.J. Klimczak, G.V. Kryukov, E. Malc, and P.A. Mieczkowski Clustered mutations in yeast and in human cancers can arise from damaged long single-strand DNA regions Mol. Cell 46 2012 424 435
54. S.A. Roberts, M.S. Lawrence, L.J. Klimczak, S.A. Grimm, D. Fargo, P. Stojanov, A. Kiezun, G.V. Kryukov, S.L. Carter, and G. Saksena An APOBEC cytidine deaminase mutagenesis pattern is widespread in human cancers Nat. Genet. 45 2013 970 976
55. H.A. Sadler, M.D. Stenglein, R.S. Harris, and L.M. Mansky APOBEC3G contributes to HIV-1 variation through sublethal mutagenesis J. Virol. 84 2010 7396 7404
56. C.J. Sakofsky, S.A. Roberts, E. Malc, P.A. Mieczkowski, M.A. Resnick, D.A. Gordenin, and A. Malkova Break-induced replication is a source of mutation clusters underlying kataegis Cell Rep. 7 2014 1640 1648
57. S.M.D. Shandilya, M.N.L. Nalam, E.A. Nalivaika, P.J. Gross, J.C. Valesano, K. Shindo, M. Li, M. Munson, W.E. Royer, and E. Harjes Crystal structure of the APOBEC3G catalytic domain reveals potential oligomerization interfaces Structure 18 2010 28 38
58. S.M.D. 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
59. A.M. Sheehy, N.C. Gaddis, J.D. Choi, and M.H. Malim Isolation of a human gene that inhibits HIV-1 infection and is suppressed by the viral Vif protein Nature 418 2002 646 650
60. L.S. Shlyakhtenko, A.Y. Lushnikov, M. Li, L. Lackey, R.S. Harris, and Y.L. Lyubchenko Atomic force microscopy studies provide direct evidence for dimerization of the HIV restriction factor APOBEC3G J. Biol. Chem. 286 2011 3387 3395
61. L.S. Shlyakhtenko, A.Y. Lushnikov, A. Miyagi, M. Li, R.S. Harris, and Y.L. Lyubchenko Atomic force microscopy studies of APOBEC3G oligomerization and dynamics J. Struct. Biol. 184 2013 217 225
62. L.S. Shlyakhtenko, A.J. Lushnikov, M. Li, R.S. Harris, and Y.L. Lyubchenko Interaction of APOBEC3A with DNA assessed by atomic force microscopy PLoS One 9 2014 e99354
63. M.D. Stenglein, M.B. Burns, M. Li, J. Lengyel, and R.S. Harris APOBEC3 proteins mediate the clearance of foreign DNA from human cells Nat. Struct. Mol. Biol. 17 2010 222 229
64. R. Suspène, M.-M. Aynaud, J.-P. Vartanian, and S. Wain-Hobson Efficient deamination of 5-methylcytidine and 5-substituted cytidine residues in DNA by human APOBEC3A cytidine deaminase PLoS One 8 2013 e63461
65. B.K. Thielen, J.P. McNevin, M.J. McElrath, B.V.S. Hunt, K.C. Klein, and J.R. Lingappa Innate immune signaling induces high levels of TC-specific deaminase activity in primary monocyte-derived cells through expression of APOBEC3A isoforms J. Biol. Chem. 285 2010 27753 27766
66. T. Wang, C. Tian, W. Zhang, K. Luo, P.T.N. Sarkis, L. Yu, B. Liu, Y. Yu, and X.-F. Yu 7SL RNA mediates virion packaging of the antiviral cytidine deaminase APOBEC3G J. Virol. 81 2007 13112 13124
67. J.E. Wedekind, G.S.C. Dance, M.P. Sowden, and H.C. Smith Messenger RNA editing in mammals: new members of the APOBEC family seeking roles in the family business Trends Genet. 19 2003 207 216
68. J.E. Wedekind, R. Gillilan, A. Janda, J. Krucinska, J.D. Salter, R.P. Bennett, J. Raina, and H.C. Smith Nanostructures of APOBEC3G support a hierarchical assembly model of high molecular mass ribonucleoprotein particles from dimeric subunits J. Biol. Chem. 281 2006 38122 38126
69. A.F. Weil, D. Ghosh, Y. Zhou, L. Seiple, M.A. McMahon, A.M. Spivak, R.F. Siliciano, and J.T. Stivers Uracil DNA glycosylase initiates degradation of HIV-1 cDNA containing misincorporated dUTP and prevents viral integration Proc. Natl. Acad. Sci. USA 110 2013 E448 E457
70. H.L. Wiegand, B.P. Doehle, H.P. Bogerd, and B.R. Cullen A second human antiretroviral factor, APOBEC3F, is suppressed by the HIV-1 and HIV-2 Vif proteins EMBO J. 23 2004 2451 2458
71. P. Wijesinghe, and A.S. Bhagwat Efficient deamination of 5-methylcytosines in DNA by human APOBEC3A, but not by AID or APOBEC3G Nucleic Acids Res. 40 2012 9206 9217
72. 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
73. Q. Yu, R. Konig, S. Pillai, K. Chiles, M. Kearney, S. Palmer, D. Richman, J.M. Coffin, and N.R. Landau Single-strand specificity of APOBEC3G accounts for minus-strand deamination of the HIV genome Nat. Struct. Mol. Biol. 11 2004 435 442
74. H. Zhang, R.J. Pomerantz, C. Zhang, S.C. Arunachalam, B. Yang, and L. Gao The cytidine deaminase CEM15 induces hypermutation in newly synthesized HIV-1 DNA Nature 424 2003 94 98
75. Y.-H. Zheng, D. Irwin, T. Kurosu, K. Tokunaga, T. Sata, and B.M. Peterlin Human APOBEC3F is another host factor that blocks human immunodeficiency virus type 1 replication J. Virol. 78 2004 6073 6076
76. P.H. Zwart, P.V. Afonine, R.W. Grosse-Kunstleve, L.W. Hung, T.R. Ioerger, A.J. McCoy, E. McKee, N.W. Moriarty, R.J. Read, and J.C. Sacchettini Automated structure solution with the PHENIX suite Methods Mol. Biol. 426 2008 419 435