APOBEC: From mutator to editor

Journal of Genetics and Genomics

Volumn 44, Issue 9, 2017, Pages 423-437

  Yang, Bei ^a   Li, Xiaosa ^a   Lei, Liqun ^a   Chen, Jia ^a  

^a SHANGHAITECH UNIVERSITY   (China)

Author keywords

APOBEC; Base editing; Base editor; CRISPR Cas9; Mutagenesis

Indexed keywords

APOLIPOPROTEIN B MRNA EDITING ENZYME CATALYTIC POLYPEPTIDE LIKE; SINGLE STRANDED DNA; CYTIDINE DEAMINASE;

CANCER PROGNOSIS; CARCINOGENESIS; CRISPR-CAS9 SYSTEM; CRYSTAL STRUCTURE; DNA REPLICATION; DNA TRANSCRIPTION; GENE EDITING; GENE MUTATION; GENETIC SCREENING; HUMAN; MUTAGENESIS; NONHUMAN; PROTEIN FAMILY; REVIEW; TELOMERE; ANIMAL; CHEMISTRY; GENETICS; GENOMICS; METABOLISM; MUTATION;

ANIMALS; CYTIDINE DEAMINASE; DNA, SINGLE-STRANDED; GENE EDITING; GENOMICS; HUMANS; MUTATION;

EID: 85030170755     PISSN: 16738527     EISSN: 18735533     Source Type: Journal    
DOI: 10.1016/j.jgg.2017.04.009     Document Type: Review

References (206)

1. Ahasan, M.M., Wakae, K., Wang, Z., Kitamura, K., Liu, G., Koura, M., Imayasu, M., Sakamoto, N., Hanaoka, K., Nakamura, M., Kyo, S., Kondo, S., Fujiwara, H., Yoshizaki, T., Mori, S., Kukimoto, I., Muramatsu, M., APOBEC3A and 3C decrease human papillomavirus 16 pseudovirion infectivity. Biochem. Biophys. Res. Commun. 457 (2015), 295–299.
2. Alexandrov, L.B., Ju, Y.S., Haase, K., Van Loo, P., Martincorena, I., Nik-Zainal, S., Totoki, Y., Fujimoto, A., Nakagawa, H., Shibata, T., Campbell, P.J., Vineis, P., Phillips, D.H., Stratton, M.R., Mutational signatures associated with tobacco smoking in human cancer. Science 354 (2016), 618–622.
3. Alexandrov, L.B., Nik-Zainal, S., Wedge, D.C., Aparicio, S.A., Behjati, S., Biankin, A.V., Bignell, G.R., Bolli, N., Borg, A., Borresen-Dale, A.L., Boyault, S., Burkhardt, B., Butler, A.P., Caldas, C., Davies, H.R., Desmedt, C., Eils, R., Eyfjord, J.E., Foekens, J.A., Greaves, M., Hosoda, F., Hutter, B., Ilicic, T., Imbeaud, S., Imielinski, M., Jager, N., Jones, D.T., Jones, D., Knappskog, S., Kool, M., Lakhani, S.R., Lopez-Otin, C., Martin, S., Munshi, N.C., Nakamura, H., Northcott, P.A., Pajic, M., Papaemmanuil, E., Paradiso, A., Pearson, J.V., Puente, X.S., Raine, K., Ramakrishna, M., Richardson, A.L., Richter, J., Rosenstiel, P., Schlesner, M., Schumacher, T.N., Span, P.N., Teague, J.W., Totoki, Y., Tutt, A.N., Valdes-Mas, R., van Buuren, M.M., van 't Veer, L., Vincent-Salomon, A., Waddell, N., Yates, L.R., Australian Pancreatic Cancer Genome, I., Consortium, I.B.C., Consortium, I.M.-S., PedBrain, I., Zucman-Rossi, J., Futreal, P.A., McDermott, U., Lichter, P., Meyerson, M., Grimmond, S.M., Siebert, R., Campo, E., Shibata, T., Pfister, S.M., Campbell, P.J., Stratton, M.R., Signatures of mutational processes in human cancer. Nature 500 (2013), 415–421.
4. Balakrishnan, L., Bambara, R.A., Okazaki fragment metabolism. Cold Spring Harb. Perspect. Biol., 5, 2013 pii: a010173.
5. Barnes, D.E., Lindahl, T., Repair and genetic consequences of endogenous DNA base damage in mammalian cells. Annu. Rev. Genet. 38 (2004), 445–476.
6. Benayoun, B.A., Pollina, E.A., Brunet, A., Epigenetic regulation of ageing: linking environmental inputs to genomic stability. Nat. Rev. Mol. Cell Biol. 16 (2015), 593–610.
7. Bishop, K.N., Holmes, R.K., Sheehy, A.M., Davidson, N.O., Cho, S.J., Malim, M.H., Cytidine deamination of retroviral DNA by diverse APOBEC proteins. Curr. Biol. 14 (2004), 1392–1396.
8. Blanc, V., Kennedy, S., Davidson, N.O., A novel nuclear localization signal in the auxiliary domain of apobec-1 complementation factor regulates nucleocytoplasmic import and shuttling. J. Biol. Chem. 278 (2003), 41198–41204.
9. 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. U. S. A. 101 (2004), 3770–3774.
10. Bohn, M.F., Shandilya, S.M., Albin, J.S., Kouno, T., Anderson, B.D., McDougle, R.M., Carpenter, M.A., Rathore, A., Evans, L., Davis, A.N., Zhang, J., Lu, Y., Somasundaran, M., Matsuo, H., Harris, R.S., Schiffer, C.A., Crystal structure of the DNA cytosine deaminase APOBEC3F: the catalytically active and HIV-1 Vif-binding domain. Structure 21 (2013), 1042–1050.
11. Bohn, M.F., Shandilya, S.M., Silvas, T.V., Nalivaika, E.A., Kouno, T., Kelch, B.A., Ryder, S.P., Kurt-Yilmaz, N., Somasundaran, M., Schiffer, C.A., The ssDNA mutator APOBEC3A is regulated by cooperative dimerization. Structure 23 (2015), 903–911.
12. Bransteitter, R., Pham, P., Scharff, M.D., Goodman, M.F., Activation-induced cytidine deaminase deaminates deoxycytidine on single-stranded DNA but requires the action of RNase. Proc. Natl. Acad. Sci. U. S. A. 100 (2003), 4102–4107.
13. Burns, M.B., Lackey, L., Carpenter, M.A., Rathore, A., Land, A.M., Leonard, B., Refsland, E.W., Kotandeniya, D., Tretyakova, N., Nikas, J.B., Yee, D., Temiz, N.A., Donohue, D.E., McDougle, R.M., Brown, W.L., Law, E.K., Harris, R.S., APOBEC3B is an enzymatic source of mutation in breast cancer. Nature 494 (2013), 366–370.
14. Burns, M.B., Temiz, N.A., Harris, R.S., Evidence for APOBEC3B mutagenesis in multiple human cancers. Nat. Genet. 45 (2013), 977–983.
15. Byeon, I.J., Ahn, J., Mitra, M., Byeon, C.H., Hercik, K., Hritz, J., Charlton, L.M., Levin, J.G., Gronenborn, A.M., NMR structure of human restriction factor APOBEC3A reveals substrate binding and enzyme specificity. Nat. Commun., 4, 2013, 1890.
16. Byeon, I.J., Byeon, C.H., Wu, T., Mitra, M., Singer, D., Levin, J.G., Gronenborn, A.M., Nuclear magnetic resonance structure of the APOBEC3B catalytic domain: structural basis for substrate binding and DNA deaminase activity. Biochemistry 55 (2016), 2944–2959.
17. Caglayan, M., Wilson, S.H., Oxidant and environmental toxicant-induced effects compromise DNA ligation during base excision DNA repair. DNA Repair 35 (2015), 85–89.
18. Caval, V., Suspene, R., Shapira, M., Vartanian, J.P., Wain-Hobson, S., A prevalent cancer susceptibility APOBEC3A hybrid allele bearing APOBEC3B 3′UTR enhances chromosomal DNA damage. Nat. Commun., 5, 2014, 5129.
19. Ceccaldi, R., Rondinelli, B., D'Andrea, A.D., Repair pathway choices and consequences at the double-strand break. Trends Cell Biol. 26 (2016), 52–64.
20. Cescon, D.W., Haibe-Kains, B., Mak, T.W., APOBEC3B expression in breast cancer reflects cellular proliferation, while a deletion polymorphism is associated with immune activation. Proc. Natl. Acad. Sci. U. S. A. 112 (2015), 2841–2846.
21. Chan, K., Roberts, S.A., Klimczak, L.J., Sterling, J.F., Saini, N., Malc, E.P., Kim, J., Kwiatkowski, D.J., Fargo, D.C., Mieczkowski, P.A., Getz, G., Gordenin, D.A., An APOBEC3A hypermutation signature is distinguishable from the signature of background mutagenesis by APOBEC3B in human cancers. Nat. Genet. 47 (2015), 1067–1072.
22. Chan, K., Sterling, J.F., Roberts, S.A., Bhagwat, A.S., Resnick, M.A., Gordenin, D.A., Base damage within single-strand DNA underlies in vivo hypermutability induced by a ubiquitous environmental agent. PLoS Genet., 8, 2012, e1003149.
23. Chan, L., Chang, B.H., Nakamuta, M., Li, W.H., Smith, L.C., Apobec-1 and apolipoprotein B mRNA editing. Biochim. Biophys. Acta 1345 (1997), 11–26.
24. Chelico, L., Pham, P., Calabrese, P., Goodman, M.F., APOBEC3G DNA deaminase acts processively 3′→5′ on single-stranded DNA. Nat. Struct. Mol. Biol. 13 (2006), 392–399.
25. Chen, B., Gilbert, L.A., Cimini, B.A., Schnitzbauer, J., Zhang, W., Li, G.W., Park, J., Blackburn, E.H., Weissman, J.S., Qi, L.S., Huang, B., Dynamic imaging of genomic loci in living human cells by an optimized CRISPR/Cas system. Cell 155 (2013), 1479–1491.
26. Chen, H., Lilley, C.E., Yu, Q., Lee, D.V., Chou, J., Narvaiza, I., Landau, N.R., Weitzman, M.D., APOBEC3A is a potent inhibitor of adeno-associated virus and retrotransposons. Curr. Biol. 16 (2006), 480–485.
27. Chen, J., Furano, A.V., Breaking bad: the mutagenic effect of DNA repair. DNA Repair 32 (2015), 43–51.
28. Chen, J., Miller, B.F., Furano, A.V., Repair of naturally occurring mismatches can induce mutations in flanking DNA. eLife, 3, 2014, e02001.
29. Chen, K.M., Harjes, E., Gross, P.J., Fahmy, A., Lu, Y., Shindo, K., Harris, R.S., Matsuo, H., Structure of the DNA deaminase domain of the HIV-1 restriction factor APOBEC3G. Nature 452 (2008), 116–119.
30. Chen, Q., Xiao, X., Wolfe, A., Chen, X.S., The in vitro biochemical characterization of an HIV-1 restriction factor APOBEC3F: importance of Loop 7 on both CD1 and CD2 for DNA binding and deamination. J. Mol. Biol. 428 (2016), 2661–2670.
31. Chu, V.T., Weber, T., Wefers, B., Wurst, W., Sander, S., Rajewsky, K., Kuhn, R., Increasing the efficiency of homology-directed repair for CRISPR-Cas9-induced precise gene editing in mammalian cells. Nat. Biotechnol. 33 (2015), 543–548.
32. Cong, L., Ran, F.A., Cox, D., Lin, S., Barretto, R., Habib, N., Hsu, P.D., Wu, X., Jiang, W., Marraffini, L.A., Zhang, F., Multiplex genome engineering using CRISPR/Cas systems. Science 339 (2013), 819–823.
33. Conticello, S.G., Harris, R.S., Neuberger, M.S., The Vif protein of HIV triggers degradation of the human antiretroviral DNA deaminase APOBEC3G. Curr. Biol. 13 (2003), 2009–2013.
34. 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 (2005), 367–377.
35. Cox, D.B., Platt, R.J., Zhang, F., Therapeutic genome editing: prospects and challenges. Nat. Med. 21 (2015), 121–131.
36. Cyranoski, D., Chinese scientists to pioneer first human CRISPR trial. Nature 535 (2016), 476–477.
37. Cyranoski, D., CRISPR gene-editing tested in a person for the first time. Nature, 539, 2016, 479.
38. Dang, Y., Wang, X., Esselman, W.J., Zheng, Y.H., Identification of APOBEC3DE as another antiretroviral factor from the human APOBEC family. J. Virol. 80 (2006), 10522–10533.
39. Davidson, N.O., Anant, S., MacGinnitie, A.J., Apolipoprotein B messenger RNA editing: insights into the molecular regulation of post-transcriptional cytidine deamination. Curr. Opin. Lipidol. 6 (1995), 70–74.
40. Doehle, B.P., Schafer, A., Cullen, B.R., Human APOBEC3B is a potent inhibitor of HIV-1 infectivity and is resistant to HIV-1 Vif. Virology 339 (2005), 281–288.
41. Dutko, J.A., Schafer, A., Kenny, A.E., Cullen, B.R., Curcio, M.J., Inhibition of a yeast LTR retrotransposon by human APOBEC3 cytidine deaminases. Curr. Biol. 15 (2005), 661–666.
42. Esnault, C., Heidmann, O., Delebecque, F., Dewannieux, M., Ribet, D., Hance, A.J., Heidmann, T., Schwartz, O., APOBEC3G cytidine deaminase inhibits retrotransposition of endogenous retroviruses. Nature 433 (2005), 430–433.
43. Etard, C., Roostalu, U., Strahle, U., Lack of Apobec2-related proteins causes a dystrophic muscle phenotype in zebrafish embryos. J. Cell Biol. 189 (2010), 527–539.
44. Faltas, B.M., Prandi, D., Tagawa, S.T., Molina, A.M., Nanus, D.M., Sternberg, C., Rosenberg, J., Mosquera, J.M., Robinson, B., Elemento, O., Sboner, A., Beltran, H., Demichelis, F., Rubin, M.A., Clonal evolution of chemotherapy-resistant urothelial carcinoma. Nat. Genet. 48 (2016), 1490–1499.
45. Furukawa, A., Nagata, T., Matsugami, A., Habu, Y., Sugiyama, R., Hayashi, F., Kobayashi, N., Yokoyama, S., Takaku, H., Katahira, M., Structure, interaction and real-time monitoring of the enzymatic reaction of wild-type APOBEC3G. EMBO J. 28 (2009), 440–451.
46. Gilbert, L.A., Horlbeck, M.A., Adamson, B., Villalta, J.E., Chen, Y., Whitehead, E.H., Guimaraes, C., Panning, B., Ploegh, H.L., Bassik, M.C., Qi, L.S., Kampmann, M., Weissman, J.S., Genome-scale CRISPR-mediated control of gene repression and activation. Cell 159 (2014), 647–661.
47. Gooch, B.D., Cullen, B.R., Functional domain organization of human APOBEC3G. Virology 379 (2008), 118–124.
48. Greenman, C., Stephens, P., Smith, R., Dalgliesh, G.L., Hunter, C., Bignell, G., Davies, H., Teague, J., Butler, A., Stevens, C., Edkins, S., O'Meara, S., Vastrik, I., Schmidt, E.E., Avis, T., Barthorpe, S., Bhamra, G., Buck, G., Choudhury, B., Clements, J., Cole, J., Dicks, E., Forbes, S., Gray, K., Halliday, K., Harrison, R., Hills, K., Hinton, J., Jenkinson, A., Jones, D., Menzies, A., Mironenko, T., Perry, J., Raine, K., Richardson, D., Shepherd, R., Small, A., Tofts, C., Varian, J., Webb, T., West, S., Widaa, S., Yates, A., Cahill, D.P., Louis, D.N., Goldstraw, P., Nicholson, A.G., Brasseur, F., Looijenga, L., Weber, B.L., Chiew, Y.E., DeFazio, A., Greaves, M.F., Green, A.R., Campbell, P., Birney, E., Easton, D.F., Chenevix-Trench, G., Tan, M.H., Khoo, S.K., Teh, B.T., Yuen, S.T., Leung, S.Y., Wooster, R., Futreal, P.A., Stratton, M.R., Patterns of somatic mutation in human cancer genomes. Nature 446 (2007), 153–158.
49. Greider, C.W., Telomeres do D-loop-T-loop. Cell 97 (1999), 419–422.
50. Haradhvala, N.J., Polak, P., Stojanov, P., Covington, K.R., Shinbrot, E., Hess, J.M., Rheinbay, E., Kim, J., Maruvka, Y.E., Braunstein, L.Z., Kamburov, A., Hanawalt, P.C., Wheeler, D.A., Koren, A., Lawrence, M.S., Getz, G., Mutational strand asymmetries in cancer genomes reveal mechanisms of DNA damage and repair. Cell 164 (2016), 538–549.
51. Harjes, E., Gross, P.J., Chen, K.M., Lu, Y., Shindo, K., Nowarski, R., Gross, J.D., Kotler, M., Harris, R.S., Matsuo, H., An extended structure of the APOBEC3G catalytic domain suggests a unique holoenzyme model. J. Mol. Biol. 389 (2009), 819–832.
52. Harris, R.S., Bishop, K.N., Sheehy, A.M., Craig, H.M., Petersen-Mahrt, S.K., Watt, I.N., Neuberger, M.S., Malim, M.H., DNA deamination mediates innate immunity to retroviral infection. Cell 113 (2003), 803–809.
53. Harris, R.S., Dudley, J.P., APOBECs and virus restriction. Virology 479–480 (2015), 131–145.
54. Harris, R.S., Liddament, M.T., Retroviral restriction by APOBEC proteins. Nat. Rev. Immunol. 4 (2004), 868–877.
55. Harris, R.S., Petersen-Mahrt, S.K., Neuberger, M.S., RNA editing enzyme APOBEC1 and some of its homologs can act as DNA mutators. Mol. Cell 10 (2002), 1247–1253.
56. Hasler, J., Rada, C., Neuberger, M.S., Cytoplasmic activation-induced cytidine deaminase (AID) exists in stoichiometric complex with translation elongation factor 1alpha (eEF1A). Proc. Natl. Acad. Sci. U. S. A. 108 (2011), 18366–18371.
57. Henderson, S., Chakravarthy, A., Su, X., Boshoff, C., Fenton, T.R., APOBEC-mediated cytosine deamination links PIK3CA helical domain mutations to human papillomavirus-driven tumor development. Cell Rep. 7 (2014), 1833–1841.
58. Hess, G.T., Fresard, L., Han, K., Lee, C.H., Li, A., Cimprich, K.A., Montgomery, S.B., Bassik, M.C., Directed evolution using dCas9-targeted somatic hypermutation in mammalian cells. Nat. Methods 13 (2016), 1036–1042.
59. Holden, L.G., Prochnow, C., Chang, Y.P., Bransteitter, R., Chelico, L., Sen, U., Stevens, R.C., Goodman, M.F., Chen, X.S., Crystal structure of the anti-viral APOBEC3G catalytic domain and functional implications. Nature 456 (2008), 121–124.
60. Hoopes, J.I., Cortez, L.M., Mertz, T.M., Malc, E.P., Mieczkowski, P.A., Roberts, S.A., APOBEC3A and APOBEC3B preferentially deaminate the lagging strand template during DNA replication. Cell Rep. 14 (2016), 1273–1282.
61. Hulme, A.E., Bogerd, H.P., Cullen, B.R., Moran, J.V., Selective inhibition of Alu retrotransposition by APOBEC3G. Gene 390 (2007), 199–205.
62. Hultquist, J.F., Lengyel, J.A., Refsland, E.W., LaRue, R.S., Lackey, L., Brown, W.L., Harris, R.S., Human and rhesus APOBEC3D, APOBEC3F, APOBEC3G, and APOBEC3H demonstrate a conserved capacity to restrict Vif-deficient HIV-1. J. Virol. 85 (2011), 11220–11234.
63. 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, 2009, e1000330.
64. 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 (2007), 3807–3815.
65. Ito, S., Nagaoka, H., Shinkura, R., Begum, N., Muramatsu, M., Nakata, M., Honjo, T., Activation-induced cytidine deaminase shuttles between nucleus and cytoplasm like apolipoprotein B mRNA editing catalytic polypeptide 1. Proc. Natl. Acad. Sci. U. S. A. 101 (2004), 1975–1980.
66. Jarmuz, A., Chester, A., Bayliss, J., Gisbourne, J., Dunham, I., Scott, J., Navaratnam, N., An anthropoid-specific locus of orphan C to U RNA-editing enzymes on chromosome 22. Genomics 79 (2002), 285–296.
67. Jiang, F., Taylor, D.W., Chen, J.S., Kornfeld, J.E., Zhou, K., Thompson, A.J., Nogales, E., Doudna, J.A., Structures of a CRISPR-Cas9 R-loop complex primed for DNA cleavage. Science 351 (2016), 867–871.
68. Jinek, M., Chylinski, K., Fonfara, I., Hauer, M., Doudna, J.A., Charpentier, E., A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337 (2012), 816–821.
69. Kanu, N., Cerone, M.A., Goh, G., Zalmas, L.P., Bartkova, J., Dietzen, M., McGranahan, N., Rogers, R., Law, E.K., Gromova, I., Kschischo, M., Walton, M.I., Rossanese, O.W., Bartek, J., Harris, R.S., Venkatesan, S., Swanton, C., DNA replication stress mediates APOBEC3 family mutagenesis in breast cancer. Genome Biol., 17, 2016, 185.
70. Kazanov, M.D., Roberts, S.A., Polak, P., Stamatoyannopoulos, J., Klimczak, L.J., Gordenin, D.A., Sunyaev, S.R., APOBEC-induced cancer mutations are uniquely enriched in early-replicating, gene-dense, and active chromatin regions. Cell Rep. 13 (2015), 1103–1109.
71. Kim, D., Lim, K., Kim, S.T., Yoon, S.H., Kim, K., Ryu, S.M., Kim, J.S., Genome-wide target specificities of CRISPR RNA-guided programmable deaminases. Nat. Biotechnol. 35 (2017), 475–480.
72. Kim, K., Ryu, S.M., Kim, S.T., Baek, G., Kim, D., Lim, K., Chung, E., Kim, S., Kim, J.S., Highly efficient RNA-guided base editing in mouse embryos. Nat. Biotechnol. 35 (2017), 435–437.
73. Kim, Y.B., Komor, A.C., Levy, J.M., Packer, M.S., Zhao, K.T., Liu, D.R., Increasing the genome-targeting scope and precision of base editing with engineered Cas9-cytidine deaminase fusions. Nat. Biotechnol. 35 (2017), 371–376.
74. Kinomoto, M., Kanno, T., Shimura, M., Ishizaka, Y., Kojima, A., Kurata, T., Sata, T., Tokunaga, K., All APOBEC3 family proteins differentially inhibit LINE-1 retrotransposition. Nucleic Acids Res. 35 (2007), 2955–2964.
75. Kinoshita, K., Honjo, T., Linking class-switch recombination with somatic hypermutation. Nat. Rev. Mol. Cell Biol. 2 (2001), 493–503.
76. Kitamura, S., Ode, H., Nakashima, M., Imahashi, M., Naganawa, Y., Kurosawa, T., Yokomaku, Y., Yamane, T., Watanabe, N., Suzuki, A., Sugiura, W., Iwatani, Y., The APOBEC3C crystal structure and the interface for HIV-1 Vif binding. Nat. Struct. Mol. Biol. 19 (2012), 1005–1010.
77. Kock, J., Blum, H.E., Hypermutation of hepatitis B virus genomes by APOBEC3G, APOBEC3C and APOBEC3H. J. Gen. Virol. 89 (2008), 1184–1191.
78. Komor, A.C., Badran, A.H., Liu, D.R., CRISPR-based technologies for the manipulation of eukaryotic genomes. Cell 168 (2017), 20–36.
79. Komor, A.C., Kim, Y.B., Packer, M.S., Zuris, J.A., Liu, D.R., Programmable editing of a target base in genomic DNA without double-stranded DNA cleavage. Nature 533 (2016), 420–424.
80. Konermann, S., Brigham, M.D., Trevino, A.E., Joung, J., Abudayyeh, O.O., Barcena, C., Hsu, P.D., Habib, N., Gootenberg, J.S., Nishimasu, H., Nureki, O., Zhang, F., Genome-scale transcriptional activation by an engineered CRISPR-Cas9 complex. Nature 517 (2015), 583–588.
81. Kuscu, C., Parlak, M., Tufan, T., Yang, J., Szlachta, K., Wei, X., Mammadov, R., Adli, M., CRISPR-STOP: gene silencing through base-editing-induced nonsense mutations. Nat. Methods 14 (2017), 710–712.
82. Landrum, M.J., Lee, J.M., Riley, G.R., Jang, W., Rubinstein, W.S., Church, D.M., Maglott, D.R., ClinVar: public archive of relationships among sequence variation and human phenotype. Nucleic Acids Res. 42 (2014), D980–D985.
83. Lecossier, D., Bouchonnet, F., Clavel, F., Hance, A.J., Hypermutation of HIV-1 DNA in the absence of the Vif protein. Science, 300, 2003, 1112.
84. Leonard, B., Hart, S.N., Burns, M.B., Carpenter, M.A., Temiz, N.A., Rathore, A., Vogel, R.I., Nikas, J.B., Law, E.K., Brown, W.L., Li, Y., Zhang, Y., Maurer, M.J., Oberg, A.L., Cunningham, J.M., Shridhar, V., Bell, D.A., April, C., Bentley, D., Bibikova, M., Cheetham, R.K., Fan, J.B., Grocock, R., Humphray, S., Kingsbury, Z., Peden, J., Chien, J., Swisher, E.M., Hartmann, L.C., Kalli, K.R., Goode, E.L., Sicotte, H., Kaufmann, S.H., Harris, R.S., APOBEC3B upregulation and genomic mutation patterns in serous ovarian carcinoma. Cancer Res. 73 (2013), 7222–7231.
85. Li, M., Shandilya, S.M., Carpenter, M.A., Rathore, A., Brown, W.L., Perkins, A.L., Harki, D.A., Solberg, J., Hook, D.J., Pandey, K.K., Parniak, M.A., Johnson, J.R., Krogan, N.J., Somasundaran, M., Ali, A., Schiffer, C.A., Harris, R.S., First-in-class small molecule inhibitors of the single-strand DNA cytosine deaminase APOBEC3G. ACS Chem. Biol. 7 (2012), 506–517.
86. Liang, P., Sun, H., Sun, Y., Zhang, X., Xie, X., Zhang, J., Zhang, Z., Chen, Y., Ding, C., Xiong, Y., Ma, W., Liu, D., Huang, J., Songyang, Z., Effective gene editing by high-fidelity base editor 2 in mouse zygotes. Protein Cell 8 (2017), 601–611.
87. Liao, W., Hong, S.H., Chan, B.H., Rudolph, F.B., Clark, S.C., Chan, L., APOBEC-2, a cardiac- and skeletal muscle-specific member of the cytidine deaminase supergene family. Biochem. Biophys. Res. Commun. 260 (1999), 398–404.
88. Liddament, M.T., Brown, W.L., Schumacher, A.J., Harris, R.S., APOBEC3F properties and hypermutation preferences indicate activity against HIV-1 in vivo. Curr. Biol. 14 (2004), 1385–1391.
89. Liu, X.S., Wu, H., Ji, X., Stelzer, Y., Wu, X., Czauderna, S., Shu, J., Dadon, D., Young, R.A., Jaenisch, R., Editing DNA methylation in the mammalian genome. Cell 167 (2016), 233–247 e217.
90. Long, J., Delahanty, R.J., Li, G., Gao, Y.T., Lu, W., Cai, Q., Xiang, Y.B., Li, C., Ji, B.T., Zheng, Y., Ali, S., Shu, X.O., Zheng, W., A common deletion in the APOBEC3 genes and breast cancer risk. J. Natl. Cancer Inst. 105 (2013), 573–579.
91. Lu, X., Zhang, T., Xu, Z., Liu, S., Zhao, B., Lan, W., Wang, C., Ding, J., Cao, C., 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.
92. Lu, Y., Zhu, J.K., Precise editing of a target base in the rice genome using a modified CRISPR/Cas9 system. Mol. Plant 10 (2017), 523–525.
93. Luo, K., Wang, T., Liu, B., Tian, C., Xiao, Z., Kappes, J., Yu, X.F., Cytidine deaminases APOBEC3G and APOBEC3F interact with human immunodeficiency virus type 1 integrase and inhibit proviral DNA formation. J. Virol. 81 (2007), 7238–7248.
94. Ma, H., Tu, L.C., Naseri, A., Huisman, M., Zhang, S., Grunwald, D., Pederson, T., Multiplexed labeling of genomic loci with dCas9 and engineered sgRNAs using CRISPRainbow. Nat. Biotechnol. 34 (2016), 528–530.
95. Ma, Y., Zhang, J., Yin, W., Zhang, Z., Song, Y., Chang, X., Targeted AID-mediated mutagenesis (TAM) enables efficient genomic diversification in mammalian cells. Nat. Methods 13 (2016), 1029–1035.
96. Maciejowski, J., Li, Y., Bosco, N., Campbell, P.J., de Lange, T., Chromothripsis and kataegis induced by telomere crisis. Cell 163 (2015), 1641–1654.
97. Mali, P., Aach, J., Stranges, P.B., Esvelt, K.M., Moosburner, M., Kosuri, S., Yang, L., Church, G.M., CAS9 transcriptional activators for target specificity screening and paired nickases for cooperative genome engineering. Nat. Biotechnol. 31 (2013), 833–838.
98. Mali, P., Yang, L., Esvelt, K.M., Aach, J., Guell, M., DiCarlo, J.E., Norville, J.E., Church, G.M., RNA-guided human genome engineering via Cas9. Science 339 (2013), 823–826.
99. Mangeat, B., Turelli, P., Caron, G., Friedli, M., Perrin, L., Trono, D., Broad antiretroviral defence by human APOBEC3G through lethal editing of nascent reverse transcripts. Nature 424 (2003), 99–103.
100. Mariani, R., Chen, D., Schrofelbauer, B., Navarro, F., Konig, R., Bollman, B., Munk, C., Nymark-McMahon, H., Landau, N.R., Species-specific exclusion of APOBEC3G from HIV-1 virions by Vif. Cell 114 (2003), 21–31.
101. Marin, M., Golem, S., Rose, K.M., Kozak, S.L., Kabat, D., Human immunodeficiency virus type 1 Vif functionally interacts with diverse APOBEC3 cytidine deaminases and moves with them between cytoplasmic sites of mRNA metabolism. J. Virol. 82 (2008), 987–998.
102. Marino, D., Perkovic, M., Hain, A., Jaguva Vasudevan, A.A., Hofmann, H., Hanschmann, K.M., Muhlebach, M.D., Schumann, G.G., Konig, R., Cichutek, K., Haussinger, D., Munk, C., APOBEC4 enhances the replication of HIV-1. PLoS One, 11, 2016, e0155422.
103. Maruyama, T., Dougan, S.K., Truttmann, M.C., Bilate, A.M., Ingram, J.R., Ploegh, H.L., Increasing the efficiency of precise genome editing with CRISPR-Cas9 by inhibition of nonhomologous end joining. Nat. Biotechnol. 33 (2015), 538–542.
104. Mbisa, J.L., Barr, R., Thomas, J.A., Vandegraaff, N., Dorweiler, I.J., Svarovskaia, E.S., Brown, W.L., Mansky, L.M., Gorelick, R.J., Harris, R.S., Engelman, A., Pathak, V.K., Human immunodeficiency virus type 1 cDNAs produced in the presence of APOBEC3G exhibit defects in plus-strand DNA transfer and integration. J. Virol. 81 (2007), 7099–7110.
105. Mehta, A., Kinter, M.T., Sherman, N.E., Driscoll, D.M., Molecular cloning of apobec-1 complementation factor, a novel RNA-binding protein involved in the editing of apolipoprotein B mRNA. Mol. Cell Biol. 20 (2000), 1846–1854.
106. Middlebrooks, C.D., Banday, A.R., Matsuda, K., Udquim, K.I., Onabajo, O.O., Paquin, A., Figueroa, J.D., Zhu, B., Koutros, S., Kubo, M., Shuin, T., Freedman, N.D., Kogevinas, M., Malats, N., Chanock, S.J., Garcia-Closas, M., Silverman, D.T., Rothman, N., Prokunina-Olsson, L., Association of germline variants in the APOBEC3 region with cancer risk and enrichment with APOBEC-signature mutations in tumors. Nat. Genet. 48 (2016), 1330–1338.
107. Mikl, M.C., Watt, I.N., Lu, M., Reik, W., Davies, S.L., Neuberger, M.S., Rada, C., Mice deficient in APOBEC2 and APOBEC3. Mol. Cell Biol. 25 (2005), 7270–7277.
108. Minegishi, Y., Lavoie, A., Cunningham-Rundles, C., Bedard, P.M., Hebert, J., Cote, L., Dan, K., Sedlak, D., Buckley, R.H., Fischer, A., Durandy, A., Conley, M.E., Mutations in activation-induced cytidine deaminase in patients with hyper IgM syndrome. Clin. Immunol. 97 (2000), 203–210.
109. Morganella, S., Alexandrov, L.B., Glodzik, D., Zou, X., Davies, H., Staaf, J., Sieuwerts, A.M., Brinkman, A.B., Martin, S., Ramakrishna, M., Butler, A., Kim, H.Y., Borg, A., Sotiriou, C., Futreal, P.A., Campbell, P.J., Span, P.N., Van Laere, S., Lakhani, S.R., Eyfjord, J.E., Thompson, A.M., Stunnenberg, H.G., van de Vijver, M.J., Martens, J.W., Borresen-Dale, A.L., Richardson, A.L., Kong, G., Thomas, G., Sale, J., Rada, C., Stratton, M.R., Birney, E., Nik-Zainal, S., The topography of mutational processes in breast cancer genomes. Nat. Commun., 7, 2016, 11383.
110. Morita, S., Noguchi, H., Horii, T., Nakabayashi, K., Kimura, M., Okamura, K., Sakai, A., Nakashima, H., Hata, K., Nakashima, K., Hatada, I., Targeted DNA demethylation in vivo using dCas9-peptide repeat and scFv-TET1 catalytic domain fusions. Nat. Biotechnol. 34 (2016), 1060–1065.
111. Mukhopadhyay, D., Anant, S., Lee, R.M., Kennedy, S., Viskochil, D., Davidson, N.O., C→U editing of neurofibromatosis 1 mRNA occurs in tumors that express both the type II transcript and apobec-1, the catalytic subunit of the apolipoprotein B mRNA-editing enzyme. Am. J. Hum. Genet. 70 (2002), 38–50.
112. Muramatsu, M., Kinoshita, K., Fagarasan, S., Yamada, S., Shinkai, Y., Honjo, T., Class switch recombination and hypermutation require activation-induced cytidine deaminase (AID), a potential RNA editing enzyme. Cell 102 (2000), 553–563.
113. Muramatsu, M., Sankaranand, V.S., Anant, S., Sugai, M., Kinoshita, K., Davidson, N.O., Honjo, T., 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 (1999), 18470–18476.
114. Nakamura, H., Arai, Y., Totoki, Y., Shirota, T., Elzawahry, A., Kato, M., Hama, N., Hosoda, F., Urushidate, T., Ohashi, S., Hiraoka, N., Ojima, H., Shimada, K., Okusaka, T., Kosuge, T., Miyagawa, S., Shibata, T., Genomic spectra of biliary tract cancer. Nat. Genet. 47 (2015), 1003–1010.
115. Nakashima, M., Ode, H., Kawamura, T., Kitamura, S., Naganawa, Y., Awazu, H., Tsuzuki, S., Matsuoka, K., Nemoto, M., Hachiya, A., Sugiura, W., Yokomaku, Y., Watanabe, N., Iwatani, Y., Structural insights into HIV-1 Vif-APOBEC3F interaction. J. Virol. 90 (2015), 1034–1047.
116. Narvaiza, I., Linfesty, D.C., Greener, B.N., Hakata, Y., Pintel, D.J., Logue, E., Landau, N.R., Weitzman, M.D., Deaminase-independent inhibition of parvoviruses by the APOBEC3A cytidine deaminase. PLoS Pathog., 5, 2009, e1000439.
117. Navarro, F., Bollman, B., Chen, H., Konig, R., Yu, Q., Chiles, K., Landau, N.R., Complementary function of the two catalytic domains of APOBEC3G. Virology 333 (2005), 374–386.
118. Newman, E.N., Holmes, R.K., Craig, H.M., Klein, K.C., Lingappa, J.R., Malim, M.H., Sheehy, A.M., Antiviral function of APOBEC3G can be dissociated from cytidine deaminase activity. Curr. Biol. 15 (2005), 166–170.
119. Nik-Zainal, S., Alexandrov, L.B., Wedge, D.C., Van Loo, P., Greenman, C.D., Raine, K., Jones, D., Hinton, J., Marshall, J., Stebbings, L.A., Menzies, A., Martin, S., Leung, K., Chen, L., Leroy, C., Ramakrishna, M., Rance, R., Lau, K.W., Mudie, L.J., Varela, I., McBride, D.J., Bignell, G.R., Cooke, S.L., Shlien, A., Gamble, J., Whitmore, I., Maddison, M., Tarpey, P.S., Davies, H.R., Papaemmanuil, E., Stephens, P.J., McLaren, S., Butler, A.P., Teague, J.W., Jonsson, G., Garber, J.E., Silver, D., Miron, P., Fatima, A., Boyault, S., Langerod, A., Tutt, A., Martens, J.W., Aparicio, S.A., Borg, A., Salomon, A.V., Thomas, G., Borresen-Dale, A.L., Richardson, A.L., Neuberger, M.S., Futreal, P.A., Campbell, P.J., Stratton, M.R., Breast cancer working group of the international cancer genome, C. Mutational processes molding the genomes of 21 breast cancers. Cell 149 (2012), 979–993.
120. Nik-Zainal, S., Davies, H., Staaf, J., Ramakrishna, M., Glodzik, D., Zou, X., Martincorena, I., Alexandrov, L.B., Martin, S., Wedge, D.C., Van Loo, P., Ju, Y.S., Smid, M., Brinkman, A.B., Morganella, S., Aure, M.R., Lingjaerde, O.C., Langerod, A., Ringner, M., Ahn, S.M., Boyault, S., Brock, J.E., Broeks, A., Butler, A., Desmedt, C., Dirix, L., Dronov, S., Fatima, A., Foekens, J.A., Gerstung, M., Hooijer, G.K., Jang, S.J., Jones, D.R., Kim, H.Y., King, T.A., Krishnamurthy, S., Lee, H.J., Lee, J.Y., Li, Y., McLaren, S., Menzies, A., Mustonen, V., O'Meara, S., Pauporte, I., Pivot, X., Purdie, C.A., Raine, K., Ramakrishnan, K., Rodriguez-Gonzalez, F.G., Romieu, G., Sieuwerts, A.M., Simpson, P.T., Shepherd, R., Stebbings, L., Stefansson, O.A., Teague, J., Tommasi, S., Treilleux, I., Van den Eynden, G.G., Vermeulen, P., Vincent-Salomon, A., Yates, L., Caldas, C., van't Veer, L., Tutt, A., Knappskog, S., Tan, B.K., Jonkers, J., Borg, A., Ueno, N.T., Sotiriou, C., Viari, A., Futreal, P.A., Campbell, P.J., Span, P.N., Van Laere, S., Lakhani, S.R., Eyfjord, J.E., Thompson, A.M., Birney, E., Stunnenberg, H.G., van de Vijver, M.J., Martens, J.W., Borresen-Dale, A.L., Richardson, A.L., Kong, G., Thomas, G., Stratton, M.R., Landscape of somatic mutations in 560 breast cancer whole-genome sequences. Nature 534 (2016), 47–54.
121. Nik-Zainal, S., Wedge, D.C., Alexandrov, L.B., Petljak, M., Butler, A.P., Bolli, N., Davies, H.R., Knappskog, S., Martin, S., Papaemmanuil, E., Ramakrishna, M., Shlien, A., Simonic, I., Xue, Y., Tyler-Smith, C., Campbell, P.J., Stratton, M.R., 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.
122. Nishida, K., Arazoe, T., Yachie, N., Banno, S., Kakimoto, M., Tabata, M., Mochizuki, M., Miyabe, A., Araki, M., Hara, K.Y., Shimatani, Z., Kondo, A., Targeted nucleotide editing using hybrid prokaryotic and vertebrate adaptive immune systems. Science, 353, 2016.
123. Noguchi, C., Ishino, H., Tsuge, M., Fujimoto, Y., Imamura, M., Takahashi, S., Chayama, K., G to A hypermutation of hepatitis B virus. Hepatology 41 (2005), 626–633.
124. Nordentoft, I., Lamy, P., Birkenkamp-Demtroder, K., Shumansky, K., Vang, S., Hornshoj, H., Juul, M., Villesen, P., Hedegaard, J., Roth, A., Thorsen, K., Hoyer, S., Borre, M., Reinert, T., Fristrup, N., Dyrskjot, L., Shah, S., Pedersen, J.S., Orntoft, T.F., Mutational context and diverse clonal development in early and late bladder cancer. Cell Rep. 7 (2014), 1649–1663.
125. O'Hare, T., Eide, C.A., Deininger, M.W., Bcr-Abl kinase domain mutations, drug resistance, and the road to a cure for chronic myeloid leukemia. Blood 110 (2007), 2242–2249.
126. Okuyama, S., Marusawa, H., Matsumoto, T., Ueda, Y., Matsumoto, Y., Endo, Y., Takai, A., Chiba, T., Excessive activity of apolipoprotein B mRNA editing enzyme catalytic polypeptide 2 (APOBEC2) contributes to liver and lung tumorigenesis. Int. J. Cancer 130 (2012), 1294–1301.
127. Orthwein, A., Patenaude, A.M., Affar el, B., Lamarre, A., Young, J.C., Di Noia, J.M., Regulation of activation-induced deaminase stability and antibody gene diversification by Hsp90. J. Exp. Med. 207 (2010), 2751–2765.
128. Paquet, D., Kwart, D., Chen, A., Sproul, A., Jacob, S., Teo, S., Olsen, K.M., Gregg, A., Noggle, S., Tessier-Lavigne, M., Efficient introduction of specific homozygous and heterozygous mutations using CRISPR/Cas9. Nature 533 (2016), 125–129.
129. Periyasamy, M., Patel, H., Lai, C.F., Nguyen, V.T., Nevedomskaya, E., Harrod, A., Russell, R., Remenyi, J., Ochocka, A.M., Thomas, R.S., Fuller-Pace, F., Gyorffy, B., Caldas, C., Navaratnam, N., Carroll, J.S., Zwart, W., Coombes, R.C., Magnani, L., Buluwela, L., Ali, S., APOBEC3B-mediated cytidine deamination is required for estrogen receptor action in breast cancer. Cell Rep. 13 (2015), 108–121.
130. Pham, P., Bransteitter, R., Petruska, J., Goodman, M.F., Processive AID-catalysed cytosine deamination on single-stranded DNA simulates somatic hypermutation. Nature 424 (2003), 103–107.
131. Pinder, J., Salsman, J., Dellaire, G., Nuclear domain ‘knock-in’ screen for the evaluation and identification of small molecule enhancers of CRISPR-based genome editing. Nucleic Acids Res. 43 (2015), 9379–9392.
132. Pinto, Y., Gabay, O., Arbiza, L., Sams, A.J., Keinan, A., Levanon, E.Y., Clustered mutations in hominid genome evolution are consistent with APOBEC3G enzymatic activity. Genome Res. 26 (2016), 579–587.
133. 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 (2007), 447–451.
134. Qi, L.S., Larson, M.H., Gilbert, L.A., Doudna, J.A., Weissman, J.S., Arkin, A.P., Lim, W.A., Repurposing CRISPR as an RNA-guided platform for sequence-specific control of gene expression. Cell 152 (2013), 1173–1183.
135. Ran, F.A., Hsu, P.D., Lin, C.Y., Gootenberg, J.S., Konermann, S., Trevino, A.E., Scott, D.A., Inoue, A., Matoba, S., Zhang, Y., Zhang, F., Double nicking by RNA-guided CRISPR Cas9 for enhanced genome editing specificity. Cell 154 (2013), 1380–1389.
136. Rathore, A., Carpenter, M.A., Demir, O., Ikeda, T., Li, M., Shaban, N.M., Law, E.K., Anokhin, D., Brown, W.L., Amaro, R.E., Harris, R.S., 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.
137. Rees, H.A., Komor, A.C., Yeh, W.H., Caetano-Lopes, J., Warman, M., Edge, A.S.B., Liu, D.R., Improving the DNA specificity and applicability of base editing through protein engineering and protein delivery. Nat. Commun., 8, 2017, 15790.
138. Ren, X., Yang, Z., Xu, J., Sun, J., Mao, D., Hu, Y., Yang, S.J., Qiao, H.H., Wang, X., Hu, Q., Deng, P., Liu, L.P., Ji, J.Y., Li, J.B., Ni, J.Q., Enhanced specificity and efficiency of the CRISPR/Cas9 system with optimized sgRNA parameters in Drosophila. Cell Rep. 9 (2014), 1151–1162.
139. Revy, P., Muto, T., Levy, Y., Geissmann, F., Plebani, A., Sanal, O., Catalan, N., Forveille, M., Dufourcq-Labelouse, R., Gennery, A., Tezcan, I., Ersoy, F., Kayserili, H., Ugazio, A.G., Brousse, N., Muramatsu, M., Notarangelo, L.D., Kinoshita, K., Honjo, T., Fischer, A., Durandy, A., Activation-induced cytidine deaminase (AID) deficiency causes the autosomal recessive form of the Hyper-IgM syndrome (HIGM2). Cell 102 (2000), 565–575.
140. Richardson, C.D., Ray, G.J., DeWitt, M.A., Curie, G.L., Corn, J.E., Enhancing homology-directed genome editing by catalytically active and inactive CRISPR-Cas9 using asymmetric donor DNA. Nat. Biotechnol. 34 (2016), 339–344.
141. Richardson, S.R., Narvaiza, I., Planegger, R.A., Weitzman, M.D., Moran, J.V., APOBEC3A deaminates transiently exposed single-strand DNA during LINE-1 retrotransposition. eLife, 3, 2014, e02008.
142. Robert, F., Barbeau, M., Ethier, S., Dostie, J., Pelletier, J., Pharmacological inhibition of DNA-PK stimulates Cas9-mediated genome editing. Genome Med., 7, 2015, 93.
143. Roberts, S.A., Gordenin, D.A., Hypermutation in human cancer genomes: footprints and mechanisms. Nat. Rev. Cancer 14 (2014), 786–800.
144. Roberts, S.A., Lawrence, M.S., Klimczak, L.J., Grimm, S.A., Fargo, D., Stojanov, P., Kiezun, A., Kryukov, G.V., Carter, S.L., Saksena, G., Harris, S., Shah, R.R., Resnick, M.A., Getz, G., Gordenin, D.A., An APOBEC cytidine deaminase mutagenesis pattern is widespread in human cancers. Nat. Genet. 45 (2013), 970–976.
145. Roberts, S.A., Sterling, J., Thompson, C., Harris, S., Mav, D., Shah, R., Klimczak, L.J., Kryukov, G.V., Malc, E., Mieczkowski, P.A., Resnick, M.A., Gordenin, D.A., Clustered mutations in yeast and in human cancers can arise from damaged long single-strand DNA regions. Mol. Cell 46 (2012), 424–435.
146. Rogozin, I.B., Basu, M.K., Jordan, I.K., Pavlov, Y.I., Koonin, E.V., APOBEC4, a new member of the AID/APOBEC family of polynucleotide (deoxy)cytidine deaminases predicted by computational analysis. Cell Cycle 4 (2005), 1281–1285.
147. Rosenberg, B.R., Hamilton, C.E., Mwangi, M.M., Dewell, S., Papavasiliou, F.N., Transcriptome-wide sequencing reveals numerous APOBEC1 mRNA-editing targets in transcript 3′ UTRs. Nat. Struct. Mol. Biol. 18 (2011), 230–236.
148. Rosler, C., Kock, J., Kann, M., Malim, M.H., Blum, H.E., Baumert, T.F., von Weizsacker, F., APOBEC-mediated interference with hepadnavirus production. Hepatology 42 (2005), 301–309.
149. Russell, R.A., Smith, J., Barr, R., Bhattacharyya, D., Pathak, V.K., Distinct domains within APOBEC3G and APOBEC3F interact with separate regions of human immunodeficiency virus type 1 Vif. J. Virol. 83 (2009), 1992–2003.
150. Russell, R.A., Wiegand, H.L., Moore, M.D., Schafer, A., McClure, M.O., Cullen, B.R., Foamy virus Bet proteins function as novel inhibitors of the APOBEC3 family of innate antiretroviral defense factors. J. Virol. 79 (2005), 8724–8731.
151. Salter, J.D., Bennett, R.P., Smith, H.C., The APOBEC protein family: united by structure, divergent in function. Trends Biochem. Sci. 41 (2016), 578–594.
152. Salter, J.D., Morales, G.A., Smith, H.C., Structural insights for HIV-1 therapeutic strategies targeting Vif. Trends Biochem. Sci. 39 (2014), 373–380.
153. Sasada, A., Takaori-Kondo, A., Shirakawa, K., Kobayashi, M., Abudu, A., Hishizawa, M., Imada, K., Tanaka, Y., Uchiyama, T., APOBEC3G targets human T-cell leukemia virus type 1. Retrovirology, 2, 2005, 32.
154. Sato, Y., Probst, H.C., Tatsumi, R., Ikeuchi, Y., Neuberger, M.S., Rada, C., Deficiency in APOBEC2 leads to a shift in muscle fiber type, diminished body mass, and myopathy. J. Biol. Chem. 285 (2010), 7111–7118.
155. Schafer, A., Bogerd, H.P., Cullen, B.R., Specific packaging of APOBEC3G into HIV-1 virions is mediated by the nucleocapsid domain of the gag polyprotein precursor. Virology 328 (2004), 163–168.
156. Schrader, C.E., Guikema, J.E., Wu, X., Stavnezer, J., The roles of APE1, APE2, DNA polymerase beta and mismatch repair in creating S region DNA breaks during antibody class switch. Philos. Trans. R. Soc. Lond B Biol. Sci. 364 (2009), 645–652.
157. 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. U. S. A. 101 (2004), 3927–3932.
158. Schumacher, A.J., Nissley, D.V., Harris, R.S., APOBEC3G hypermutates genomic DNA and inhibits Ty1 retrotransposition in yeast. Proc. Natl. Acad. Sci. U. S. A. 102 (2005), 9854–9859.
159. Schumann, K., Lin, S., Boyer, E., Simeonov, D.R., Subramaniam, M., Gate, R.E., Haliburton, G.E., Ye, C.J., Bluestone, J.A., Doudna, J.A., Marson, A., Generation of knock-in primary human T cells using Cas9 ribonucleoproteins. Proc. Natl. Acad. Sci. U. S. A. 112 (2015), 10437–10442.
160. Seplyarskiy, V.B., Soldatov, R.A., Popadin, K.Y., Antonarakis, S.E., Bazykin, G.A., Nikolaev, S.I., APOBEC-induced mutations in human cancers are strongly enriched on the lagging DNA strand during replication. Genome Res. 26 (2016), 174–182.
161. Shaban, N.M., Shi, K., Li, M., Aihara, H., Harris, R.S., 1.92 angstrom zinc-free APOBEC3F catalytic domain crystal structure. J. Mol. Biol. 428 (2016), 2307–2316.
162. Shandilya, S.M., Nalam, M.N., Nalivaika, E.A., Gross, P.J., Valesano, J.C., Shindo, K., Li, M., Munson, M., Royer, W.E., Harjes, E., Kono, T., Matsuo, H., Harris, R.S., Somasundaran, M., Schiffer, C.A., Crystal structure of the APOBEC3G catalytic domain reveals potential oligomerization interfaces. Structure 18 (2010), 28–38.
163. 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 (2002), 646–650.
164. Sheehy, A.M., Gaddis, N.C., Malim, M.H., The antiretroviral enzyme APOBEC3G is degraded by the proteasome in response to HIV-1 Vif. Nat. Med. 9 (2003), 1404–1407.
165. Shen, B., Zhang, W., Zhang, J., Zhou, J., Wang, J., Chen, L., Wang, L., Hodgkins, A., Iyer, V., Huang, X., Skarnes, W.C., Efficient genome modification by CRISPR-Cas9 nickase with minimal off-target effects. Nat. Methods 11 (2014), 399–402.
166. Shi, K., Carpenter, M.A., Banerjee, S., Shaban, N.M., Kurahashi, K., Salamango, D.J., McCann, J.L., Starrett, G.J., Duffy, J.V., Demir, O., Amaro, R.E., Harki, D.A., Harris, R.S., Aihara, H., Structural basis for targeted DNA cytosine deamination and mutagenesis by APOBEC3A and APOBEC3B. Nat. Struct. Mol. Biol. 24 (2017), 131–139.
167. 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 (2015), 28120–28130.
168. Shimatani, Z., Kashojiya, S., Takayama, M., Terada, R., Arazoe, T., Ishii, H., Teramura, H., Yamamoto, T., Komatsu, H., Miura, K., Ezura, H., Nishida, K., Ariizumi, T., Kondo, A., Targeted base editing in rice and tomato using a CRISPR-Cas9 cytidine deaminase fusion. Nat. Biotechnol. 35 (2017), 441–443.
169. Shindo, K., Takaori-Kondo, A., Kobayashi, M., Abudu, A., Fukunaga, K., Uchiyama, T., 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 (2003), 44412–44416.
170. 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, 2013, 2593.
171. Skourti-Stathaki, K., Proudfoot, N.J., A double-edged sword: R loops as threats to genome integrity and powerful regulators of gene expression. Genes Dev. 28 (2014), 1384–1396.
172. Smith, J.L., Pathak, V.K., Identification of specific determinants of human APOBEC3F, APOBEC3C, and APOBEC3DE and African green monkey APOBEC3F that interact with HIV-1 Vif. J. Virol. 84 (2010), 12599–12608.
173. Song, J., Yang, D., Xu, J., Zhu, T., Chen, Y.E., Zhang, J., RS-1 enhances CRISPR/Cas9- and TALEN-mediated knock-in efficiency. Nat. Commun., 7, 2016, 10548.
174. Starrett, G.J., Luengas, E.M., McCann, J.L., Ebrahimi, D., Temiz, N.A., Love, R.P., Feng, Y., Adolph, M.B., Chelico, L., Law, E.K., Carpenter, M.A., Harris, R.S., The DNA cytosine deaminase APOBEC3H haplotype I likely contributes to breast and lung cancer mutagenesis. Nat. Commun., 7, 2016, 12918.
175. Stenglein, M.D., Harris, R.S., APOBEC3B and APOBEC3F inhibit L1 retrotransposition by a DNA deamination-independent mechanism. J. Biol. Chem. 281 (2006), 16837–16841.
176. Stephens, P., Edkins, S., Davies, H., Greenman, C., Cox, C., Hunter, C., Bignell, G., Teague, J., Smith, R., Stevens, C., O'Meara, S., Parker, A., Tarpey, P., Avis, T., Barthorpe, A., Brackenbury, L., Buck, G., Butler, A., Clements, J., Cole, J., Dicks, E., Edwards, K., Forbes, S., Gorton, M., Gray, K., Halliday, K., Harrison, R., Hills, K., Hinton, J., Jones, D., Kosmidou, V., Laman, R., Lugg, R., Menzies, A., Perry, J., Petty, R., Raine, K., Shepherd, R., Small, A., Solomon, H., Stephens, Y., Tofts, C., Varian, J., Webb, A., West, S., Widaa, S., Yates, A., Brasseur, F., Cooper, C.S., Flanagan, A.M., Green, A., Knowles, M., Leung, S.Y., Looijenga, L.H., Malkowicz, B., Pierotti, M.A., Teh, B., Yuen, S.T., Nicholson, A.G., Lakhani, S., Easton, D.F., Weber, B.L., Stratton, M.R., Futreal, P.A., Wooster, R., A screen of the complete protein kinase gene family identifies diverse patterns of somatic mutations in human breast cancer. Nat. Genet. 37 (2005), 590–592.
177. 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 (2003), 591–601.
178. Suspene, R., Aynaud, M.M., Guetard, D., Henry, M., Eckhoff, G., Marchio, A., Pineau, P., Dejean, A., Vartanian, J.P., Wain-Hobson, S., Somatic hypermutation of human mitochondrial and nuclear DNA by APOBEC3 cytidine deaminases, a pathway for DNA catabolism. Proc. Natl. Acad. Sci. U. S. A. 108 (2011), 4858–4863.
179. Suspene, R., Guetard, D., Henry, M., Sommer, P., Wain-Hobson, S., Vartanian, J.P., Extensive editing of both hepatitis B virus DNA strands by APOBEC3 cytidine deaminases in vitro and in vivo. Proc. Natl. Acad. Sci. U. S. A. 102 (2005), 8321–8326.
180. Taylor, B.J., Nik-Zainal, S., Wu, Y.L., Stebbings, L.A., Raine, K., Campbell, P.J., Rada, C., Stratton, M.R., Neuberger, M.S., DNA deaminases induce break-associated mutation showers with implication of APOBEC3B and 3A in breast cancer kataegis. eLife, 2, 2013, e00534.
181. Taylor, B.J., Wu, Y.L., Rada, C., Active RNAP pre-initiation sites are highly mutated by cytidine deaminases in yeast, with AID targeting small RNA genes. eLife, 3, 2014, e03553.
182. Teng, B., Burant, C.F., Davidson, N.O., Molecular cloning of an apolipoprotein B messenger RNA editing protein. Science 260 (1993), 1816–1819.
183. Tsai, S.Q., Wyvekens, N., Khayter, C., Foden, J.A., Thapar, V., Reyon, D., Goodwin, M.J., Aryee, M.J., Joung, J.K., Dimeric CRISPR RNA-guided FokI nucleases for highly specific genome editing. Nat. Biotechnol. 32 (2014), 569–576.
184. Turelli, P., Mangeat, B., Jost, S., Vianin, S., Trono, D., Inhibition of hepatitis B virus replication by APOBEC3G. Science, 303, 2004, 1829.
185. Vartanian, J.P., Guetard, D., Henry, M., Wain-Hobson, S., Evidence for editing of human papillomavirus DNA by APOBEC3 in benign and precancerous lesions. Science 320 (2008), 230–233.
186. Verhalen, B., Starrett, G.J., Harris, R.S., Jiang, M., Functional upregulation of the DNA cytosine deaminase APOBEC3B by polyomaviruses. J. Virol. 90 (2016), 6379–6386.
187. Vojta, A., Dobrinic, P., Tadic, V., Bockor, L., Korac, P., Julg, B., Klasic, M., Zoldos, V., Repurposing the CRISPR-Cas9 system for targeted DNA methylation. Nucleic Acids Res. 44 (2016), 5615–5628.
188. Walker, B.A., Wardell, C.P., Murison, A., Boyle, E.M., Begum, D.B., Dahir, N.M., Proszek, P.Z., Melchor, L., Pawlyn, C., Kaiser, M.F., Johnson, D.C., Qiang, Y.W., Jones, J.R., Cairns, D.A., Gregory, W.M., Owen, R.G., Cook, G., Drayson, M.T., Jackson, G.H., Davies, F.E., Morgan, G.J., APOBEC family mutational signatures are associated with poor prognosis translocations in multiple myeloma. Nat. Commun., 6, 2015, 6997.
189. Walser, J.C., Furano, A.V., The mutational spectrum of non-CpG DNA varies with CpG content. Genome Res. 20 (2010), 875–882.
190. Walser, J.C., Ponger, L., Furano, A.V., CpG dinucleotides and the mutation rate of non-CpG DNA. Genome Res. 18 (2008), 1403–1414.
191. Wiegand, H.L., Cullen, B.R., Inhibition of alpharetrovirus replication by a range of human APOBEC3 proteins. J. Virol. 81 (2007), 13694–13699.
192. Wiegand, H.L., Doehle, B.P., Bogerd, H.P., Cullen, B.R., A second human antiretroviral factor, APOBEC3F, is suppressed by the HIV-1 and HIV-2 Vif proteins. EMBO J. 23 (2004), 2451–2458.
193. Wilson, S.H., The dark side of DNA repair. eLife, 3, 2014, e03068.
194. Xiao, X., Li, S.X., Yang, H., Chen, X.S., Crystal structures of APOBEC3G N-domain alone and its complex with DNA. Nat. Commun., 7, 2016, 12193.
195. Xu, X., Tao, Y., Gao, X., Zhang, L., Li, X., Zou, W., Ruan, K., Wang, F., Xu, G.L., Hu, R., A CRISPR-based approach for targeted DNA demethylation. Cell Discov., 2, 2016, 16009.
196. Yang, Y., Yang, Y., Smith, H.C., Multiple protein domains determine the cell type-specific nuclear distribution of the catalytic subunit required for apolipoprotein B mRNA editing. Proc. Natl. Acad. Sci. U. S. A. 94 (1997), 13075–13080.
197. Yu, C., Liu, Y., Ma, T., Liu, K., Xu, S., Zhang, Y., Liu, H., La Russa, M., Xie, M., Ding, S., Qi, L.S., Small molecules enhance CRISPR genome editing in pluripotent stem cells. Cell Stem Cell 16 (2015), 142–147.
198. Yu, Q., Chen, D., Konig, R., Mariani, R., Unutmaz, D., Landau, N.R., APOBEC3B and APOBEC3C are potent inhibitors of simian immunodeficiency virus replication. J. Biol. Chem. 279 (2004), 53379–53386.
199. Yu, Q., Konig, R., Pillai, S., Chiles, K., Kearney, M., Palmer, S., Richman, D., Coffin, J.M., Landau, N.R., Single-strand specificity of APOBEC3G accounts for minus-strand deamination of the HIV genome. Nat. Struct. Mol. Biol. 11 (2004), 435–442.
200. Yu, X., Yu, Y., Liu, B., Luo, K., Kong, W., Mao, P., Yu, X.F., Induction of APOBEC3G ubiquitination and degradation by an HIV-1 Vif-Cul5-SCF complex. Science 302 (2003), 1056–1060.
201. Zalatan, J.G., Lee, M.E., Almeida, R., Gilbert, L.A., Whitehead, E.H., La Russa, M., Tsai, J.C., Weissman, J.S., Dueber, J.E., Qi, L.S., Lim, W.A., Engineering complex synthetic transcriptional programs with CRISPR RNA scaffolds. Cell 160 (2015), 339–350.
202. Zhang, H., Yang, B., Pomerantz, R.J., Zhang, C., Arunachalam, S.C., Gao, L., The cytidine deaminase CEM15 induces hypermutation in newly synthesized HIV-1 DNA. Nature 424 (2003), 94–98.
203. Zhang, Y., Qin, W., Lu, X., Xu, J., Huang, H., Bai, H., Li, S., Lin, S., Programmable base editing of zebrafish genome using a modified CRISPR-Cas9 system. Nat. Commun., 8, 2017, 118.
204. Zheng, H., Dai, W., Cheung, A.K., Ko, J.M., Kan, R., Wong, B.W., Leong, M.M., Deng, M., Kwok, T.C., Chan, J.Y., Kwong, D.L., Lee, A.W., Ng, W.T., Ngan, R.K., Yau, C.C., Tung, S., Lee, V.H., Lam, K.O., Kwan, C.K., Li, W.S., Yau, S., Chan, K.W., Lung, M.L., Whole-exome sequencing identifies multiple loss-of-function mutations of NF-kappaB pathway regulators in nasopharyngeal carcinoma. Proc. Natl. Acad. Sci. U. S. A. 113 (2016), 11283–11288.
205. Zhou, Y., Zhu, S., Cai, C., Yuan, P., Li, C., Huang, Y., Wei, W., High-throughput screening of a CRISPR/Cas9 library for functional genomics in human cells. Nature 509 (2014), 487–491.
206. Zong, Y., Wang, Y., Li, C., Zhang, R., Chen, K., Ran, Y., Qiu, J.L., Wang, D., Gao, C., Precise base editing in rice, wheat and maize with a Cas9-cytidine deaminase fusion. Nat. Biotechnol. 35 (2017), 438–440.