DNA cytosine and methylcytosine deamination by APOBEC3B: Enhancing methylcytosine deamination by engineering APOBEC3B

Biochemical Journal

Volumn 471, Issue 1, 2015, Pages 25-35

  Fu, Yang ^a   Ito, Fumiaki ^a   Zhang, Gewen ^a,c   Fernandez, Braulio ^a   Yang, Hanjing ^a   Chen, Xiaojiang S ^a,b  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c CENTRAL SOUTH UNIVERSITY   (China)

Author keywords

Cytosine methylcytosine (C mC) selectivity; Enzyme engineering; Multiple determinants for mC specificity; Substrate specificity alteration; Zinc (Zn) deaminase

Indexed keywords

5 METHYLCYTOSINE; APOLIPOPROTEIN B MESSENGER RNA EDITING ENZYME CATALYTIC POLYPEPTIDE 3B; CYTOSINE; CYTOSINE DEAMINASE; GENOMIC DNA; HYDROLASE; UNCLASSIFIED DRUG; APOBEC3B PROTEIN, HUMAN; CYTIDINE DEAMINASE;

ARTICLE; DEAMINATION; DNA BINDING; ENZYME ENGINEERING; ENZYME SPECIFICITY; FUNCTIONAL ASSESSMENT; INNATE IMMUNITY; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN ENGINEERING; PROTEIN EXPRESSION; STEADY STATE; CHEMISTRY; GENETICS; HUMAN; PROTEIN TERTIARY STRUCTURE;

CYTIDINE DEAMINASE; CYTOSINE; HUMANS; PROTEIN ENGINEERING; PROTEIN STRUCTURE, TERTIARY;

EID: 84942327978     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20150382     Document Type: Article

References (68)

1. Macduff, D.A. and Harris, R.S. (2006) Directed DNA deamination by AID/APOBEC3 in immunity. Curr. Biol. 16, R186-R189
2. Conticello, S.G. (2008) The AID/APOBEC family of nucleic acid mutators. Genome Biol. 9, 229
3. Muramatsu, M., Kinoshita, K., Fagarasan, S., Yamada, S., Shinkai, Y. and Honjo, T. (2000) Class switch recombination and hypermutation require activation-induced cytidine deaminase (AID), a potential RNA editing enzyme. Cell 102, 553-563
4. Di Noia, J.M. and Neuberger, M.S. (2007) Molecular mechanisms of antibody somatic hypermutation. Annu. Rev. Biochem. 76, 1-22
5. Stenglein, M.D., Burns, M.B., Li, M., Lengyel, J. and Harris, R.S. (2010) APOBEC3 proteins mediate the clearance of foreign DNA from human cells. Nat. Struct. Mol. Biol. 17, 222-229
6. Chiu, Y.L. and Greene, W.C. (2008) The APOBEC3 cytidine deaminases: an innate defensive network opposing exogenous retroviruses and endogenous retroelements. Annu. Rev. Immunol. 26, 317-353
7. Sheehy, A.M., Gaddis, N.C., Choi, J.D. and Malim, M.H. (2002) Isolation of a human gene that inhibits HIV-1 infection and is suppressed by the viral Vif protein. Nature 418, 646-650
8. Mangeat, B., Turelli, P., Caron, G., Friedli, M., Perrin, L. and Trono, D. (2003) Broad antiretroviral defence by human APOBEC3G through lethal editing of nascent reverse transcripts. Nature 424, 99-103
9. Chen, H., Lilley, C.E., Yu, Q., Lee, D.V., Chou, J., Narvaiza, I., Landau, N.R. and Weitzman, M.D. (2006) APOBEC3A is a potent inhibitor of adeno-associated virus and retrotransposons. Curr. Biol. 16, 480-485
10. Love, R.P., Xu, H. and Chelico, L. (2012) Biochemical analysis of hypermutation by the deoxycytidine deaminase APOBEC3A. J. Biol. Chem. 287, 30812-30822
11. Gillick, K., Pollpeter, D., Phalora, P., Kim, E.Y., Wolinsky, S.M. and Malim, M.H. (2013) Suppression of HIV-1 infection by APOBEC3 proteins in primary human CD4(+) T cells is associated with inhibition of processive reverse transcription as well as excessive cytidine deamination. J. Virol. 87, 1508-1517
12. Chaipan, C., Smith, J.L., Hu, W.S. and Pathak, V.K. (2013) APOBEC3G restricts HIV-1 to a greater extent than APOBEC3F and APOBEC3DE in human primary CD4 + T cells and macrophages. J. Virol. 87, 444-453
13. Ooms, M., Krikoni, A., Kress, A.K., Simon, V. and Munk, C. (2012) APOBEC3A, APOBEC3B, and APOBEC3H haplotype 2 restrict human T-lymphotropic virus type 1. J. Virol. 86, 6097-6108
14. Romani, B., Engelbrecht, S. and Glashoff, R.H. (2009) Antiviral roles of APOBEC proteins against HIV-1 and suppression by Vif. Arch. Virol. 154, 1579-1588
15. Bonvin, M., Achermann, F., Greeve, I., Stroka, D., Keogh, A., Inderbitzin, D., Candinas, D., Sommer, P., Wain-Hobson, S., Vartanian, J.P. and Greeve, J. (2006) Interferon-inducible expression of APOBEC3 editing enzymes in human hepatocytes and inhibition of hepatitis B virus replication. Hepatology 43, 1364-1374
16. Bogerd, H.P., Wiegand, H.L., Hulme, A.E., Garcia-Perez, J.L., O'Shea, K.S., Moran, J.V. and Cullen, B.R. (2006) Cellular inhibitors of long interspersed element 1 and Alu retrotransposition. Proc. Natl. Acad. Sci. U.S.A. 103, 8780-8785
17. Doehle, B.P., Schafer, A. and Cullen, B.R. (2005) Human APOBEC3B is a potent inhibitor of HIV-1 infectivity and is resistant to HIV-1 Vif. Virology 339, 281-288
18. Doehle, B.P., Schafer, A., Wiegand, H.L., Bogerd, H.P. and Cullen, B.R. (2005) Differential sensitivity of murine leukemia virus to APOBEC3-mediated inhibition is governed by virion exclusion. J. Virol. 79, 8201-8207
19. Yu, Q., Chen, D., Konig, R., Mariani, R., Unutmaz, D. and Landau, N.R. (2004) APOBEC3B and APOBEC3C are potent inhibitors of simian immunodeficiency virus replication. J. Biol. Chem. 279, 53379-53386
20. Vieira, V.C., Leonard, B., White, E.A., Starrett, G.J., Temiz, N.A., Lorenz, L.D., Lee, D., Soares, M.A., Lambert, P.F., Howley, P.M. and Harris, R.S. (2014) Human papillomavirus E6 triggers upregulation of the antiviral and cancer genomic DNA deaminase APOBEC3B. MBio 5, e02234-14
21. Xu, R., Zhang, X., Zhang, W., Fang, Y., Zheng, S. and Yu, X.F. (2007) Association of human APOBEC3 cytidine deaminases with the generation of hepatitis virus B × antigen mutants and hepatocellular carcinoma. Hepatology 46, 1810-1820
22. Bonvin, M. and Greeve, J. (2007) Effects of point mutations in the cytidine deaminase domains of APOBEC3B on replication and hypermutation of hepatitis B virus in vitro. J. Gen. Virol. 88, 3270-3274
23. Lucifora, J., Xia, Y., Reisinger, F., Zhang, K., Stadler, D., Cheng, X., Sprinzl, M.F., Koppensteiner, H., Makowska, Z., Volz, T. et al. (2014) Specific and nonhepatotoxic degradation of nuclear hepatitis B virus cccDNA. Science 343, 1221-1228
24. 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. et al. (2013) APOBEC3B is an enzymatic source of mutation in breast cancer. Nature 494, 366-370
25. Burns, M.B., Temiz, N.A. and Harris, R.S. (2013) Evidence for APOBEC3B mutagenesis in multiple human cancers. Nat. Genet. 45, 977-983
26. 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. et al. (2013) APOBEC3B upregulation and genomic mutation patterns in serous ovarian carcinoma. Cancer Res. 73, 7222-7231
27. Gwak, M., Choi, Y.J., Yoo, N.J. and Lee, S. (2014) Expression of DNA cytosine deaminase APOBEC3 proteins, a potential source for producing mutations, in gastric, colorectal and prostate cancers. Tumori 100, 112e-117e
28. Jin, Z., Han, Y.X. and Han, X.R. (2014) The role of APOBEC3B in chondrosarcoma. Oncol. Rep. 32, 1867-1872
29. Sieuwerts, A.M., Willis, S., Burns, M.B., Look, M.P., Meijer-Van Gelder, M.E., Schlicker, A., Heideman, M.R., Jacobs, H., Wessels, L., Leyland-Jones, B. et al. (2014) Elevated APOBEC3B correlates with poor outcomes for estrogen-receptor-positive breast cancers. Horm. Cancer 5, 405-413
30. Sasaki, H., Suzuki, A., Tatematsu, T., Shitara, M., Hikosaka, Y., Okuda, K., Moriyama, S., Yano, M. and Fujii, Y. (2014) gene overexpression in non-small-cell lung cancer. Biomed. Rep. 2, 392-395
31. Taylor, B.J., Nik-Zainal, S., Wu, Y.L., Stebbings, L.A., Raine, K., Campbell, P.J., Rada, C., Stratton, M.R. and Neuberger, M.S. (2013) DNA deaminases induce break-associated mutation showers with implication of APOBEC3B and 3A in breast cancer kataegis. eLife 2, e00534
32. Harris, R.S. (2015) Molecular mechanism and clinical impact of APOBEC3B-catalyzed mutagenesis in breast cancer. Breast Cancer Res. 17, 498
33. Burns, M.B., Leonard, B. and Harris, R.S. (2015) APOBEC3B: pathological consequences of an innate immune DNA mutator. Biomed. J. 35, 102-110
34. Cescon, D.W., Haibe-Kains, B. and Mak, T.W. (2015) 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, 2841-2846
35. Carpenter, M.A., Li, M., Rathore, A., Lackey, L., Law, E.K., Land, A.M., Leonard, B., Shandilya, S.M., Bohn, M.F., Schiffer, C.A. et al. (2012) Methylcytosine and normal cytosine deamination by the foreign DNA restriction enzyme APOBEC3A. J. Biol. Chem. 287, 34801-34808
36. Wijesinghe, P. and Bhagwat, A.S. (2012) Efficient deamination of 5-methylcytosines in DNA by human APOBEC3A, but not by AID or APOBEC3G. Nucleic Acids Res. 40, 9206-9217
37. Morgan, H.D., Dean, W., Coker, H.A., Reik, W. and Petersen-Mahrt, S.K. (2004) Activation-induced cytidine deaminase deaminates 5-methylcytosine in DNA and is expressed in pluripotent tissues: implications for epigenetic reprogramming. J. Biol. Chem. 279, 52353-52360
38. Bransteitter, R., Pham, P., Scharff, M.D. and Goodman, M.F. (2003) Activation-induced cytidine deaminase deaminates deoxycytidine on single-stranded DNA but requires the action of RNase. Proc. Natl. Acad. Sci. U.S.A. 100, 4102-4107
39. Larijani, M., Frieder, D., Sonbuchner, T.M., Bransteitter, R., Goodman, M.F., Bouhassira, E.E., Scharff, M.D. and Martin, A. (2005) Methylation protects cytidines from AID-mediated deamination. Mol. Immunol. 42, 599-604
40. Nabel, C.S., Jia, H., Ye, Y., Shen, L., Goldschmidt, H.L., Stivers, J.T., Zhang, Y. and Kohli, R.M. (2012) AID/APOBEC deaminases disfavor modified cytosines implicated in DNA demethylation. Nat. Chem. Biol. 8, 751-758
41. Tahiliani, M., Koh, K.P., Shen, Y., Pastor, W.A., Bandukwala, H., Brudno, Y., Agarwal, S., Iyer, L.M., Liu, D.R., Aravind, L. and Rao, A. (2009) Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science 324, 930-935
42. Popp, C., Dean, W., Feng, S., Cokus, S.J., Andrews, S., Pellegrini, M., Jacobsen, S.E. and Reik, W. (2010) Genome-wide erasure of DNA methylation in mouse primordial germ cells is affected by AID deficiency. Nature 463, 1101-1105
43. Bhutani, N., Brady, J.J., Damian, M., Sacco, A., Corbel, S.Y. and Blau, H.M. (2010) Reprogramming towards pluripotency requires AID-dependent DNA demethylation. Nature 463, 1042-1047
44. 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. et al. (2013) Crystal structure of the DNA cytosine deaminase APOBEC3F: the catalytically active and HIV-1 Vif-binding domain. Structure 21, 1042-1050
45. Siu, K.K., Sultana, A., Azimi, F.C. and Lee, J.E. (2013) Structural determinants of HIV-1 Vif susceptibility and DNA binding in APOBEC3F. Nat. Commun. 4, 2593
46. Kitamura, S., Ode, H., Nakashima, M., Imahashi, M., Naganawa, Y., Kurosawa, T., Yokomaku, Y., Yamane, T., Watanabe, N., Suzuki, A. et al. (2012) The APOBEC3C crystal structure and the interface for HIV-1 Vif binding. Nat. Struct. Mol. Biol. 19, 1005-1010
47. Byeon, I.J., Ahn, J., Mitra, M., Byeon, C.H., Hercik, K., Hritz, J., Charlton, L.M., Levin, J.G. and Gronenborn, A.M. (2013) NMR structure of human restriction factor APOBEC3A reveals substrate binding and enzyme specificity. Nat. Commun. 4, 1890
48. Holden, L.G., Prochnow, C., Chang, Y.P., Bransteitter, R., Chelico, L., Sen, U., Stevens, R.C., Goodman, M.F. and Chen, X.S. (2008) Crystal structure of the anti-viral APOBEC3G catalytic domain and functional implications. Nature 456, 121-124
49. Prochnow, C., Bransteitter, R., Klein, M.G., Goodman, M.F. and Chen, X.S. (2007) The APOBEC-2 crystal structure and functional implications for the deaminase AID. Nature 445, 447-451
50. Pak, V, Heidecker, G., Pathak, V.K. and Derse, D. (2011) The role of amino-terminal sequences in cellular localization and antiviral activity of APOBEC3B. J. Virol. 85, 8538-8547
51. Lackey, L, Demorest, Z.L., Land, A.M., Hultquist, J.F., Brown, W.L. and Harris, R.S. (2012) APOBEC3B and AID have similar nuclear import mechanisms. J. Mol. Biol. 419, 301-314
52. Shinohara, M., Io, K., Shindo, K., Matsui, M., Sakamoto, T., Tada, K., Kobayashi, M., Kadowaki, N. and Takaori-Kondo, A. (2012) APOBEC3B can impair genomic stability by inducing base substitutions in genomic DNA in human cells. Sci. Rep. 2, 806
53. Chelico, L, Pham, P., Calabrese, P. and Goodman, M.F. (2006) APOBEC3G DNA deaminase acts processively 3' → 5'on single-stranded DNA. Nat. Struct. Mol. Biol. 13, 392-399
54. Yoo, J. and Medina-Franco, J.L. (2011) Homology modeling, docking and structure-based pharmacophore of inhibitors of DNA methyltransferase. J. Comput. Aided Mol. Des. 25, 555-567
55. Bogerd, H.P., Wiegand, H.L., Doehle, B.P. and Cullen, B.R. (2007) The intrinsic antiretroviral factor APOBEC3B contains two enzymatically active cytidine deaminase domains. Virology 364, 486-493
56. Abdouni, H., King, J.J., Suliman, M., Quinlan, M., Fifield, H. and Larijani, M. (2013) Zebrafish AID is capable of deaminating methylated deoxycytidines. Nucleic Acids Res. 41, 5457-5468
57. Hakata, Y. and Landau, N.R. (2006) Reversed functional organization of mouse and human APOBEC3 cytidine deaminase domains. J. Biol. Chem. 281, 36624-36631
58. Langlois, M.A., Beale, R.C., Conticello, S.G. and Neuberger, M.S. (2005) Mutational comparison of the single-domained APOBEC3C and double-domained APOBEC3F/G anti-retroviral cytidine deaminases provides insight into their DNA target site specificities. Nucleic Acids Res. 33, 1913-1923
59. Narvaiza, I., Linfesty, D.C., Greener, B.N., Hakata, Y, Pintel, D.J., Logue, E., Landau, N.R. and Weitzman, M.D. (2009) Deaminase-independent inhibition of parvoviruses by the APOBEC3A cytidine deaminase. PLoS Pathog. 5, e1000439
60. Kohli, R.M., Abrams, S.R., Gajula, K.S., Maul, R.W., Gearhart, P.J. and Stivers, J.T. (2009) A portable hot spot recognition loop transfers sequence preferences from APOBEC family members to activation-induced cytidine deaminase. J. Biol. Chem. 284, 22898-22904
61. Kohli, R.M., Maul, R.W., Guminski, A.F, McClure, R.L., Gajula, K.S., Saribasak, H., McMahon, M.A., Siliciano, R.F, Gearhart, P.J. and Stivers, J.T. (2010) Local sequence targeting in the AID/APOBEC family differentially impacts retroviral restriction and antibody diversification. J. Biol. Chem. 285, 40956-40964
62. Carpenter, M.A., Rajagurubandara, E., Wijesinghe, P. and Bhagwat, A.S. (2010) Determinants of sequence-specificity within human AID and APOBEC3G. DNA Repair (Amst.) 9, 579-587
63. Wang, M., Rada, C. and Neuberger, M.S. (2010) Altering the spectrum of immunoglobulin V gene somatic hypermutation by modifying the active site of AID. J. Exp. Med. 207, 141-153
64. Mitra, M., Hercik, K., Byeon, I.J., Ahn, J., Hill, S., Hinchee-Rodriguez, K., Singer, D., Byeon, C.H., Charlton, L.M., Nam, G. et al. (2014) Structural determinants of human APOBEC3A enzymatic and nucleic acid binding properties. Nucleic Acids Res. 42, 1095-1110
65. 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. and Harris, R.S. (2013) 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, 4442-4454
66. Logue, E.C., Bloch, N., Dhuey, E., Zhang, R., Cao, P., Herate, C, Chauveau, L, Hubbard, S.R. and Landau, N.R. (2014) A DNA sequence recognition loop on APOBEC3A controls substrate specificity. PLoS One 9, e97062
67. Gajula, K.S., Huwe, P.J., Mo, C.Y, Crawford, D.J., Stivers, J.T, Radhakrishnan, R. and Kohli, R.M. (2014) High-throughput mutagenesis reveals functional determinants for DNA targeting by activation-induced deaminase. Nucleic Acids Res. 42, 9964-9975
68. Bulliard, Y, Narvaiza, I., Bertero, A., Peddi, S., Rohrig, U.F, Ortiz, M., Zoete, V, Castro-Diaz, N., Turelli, P., Telenti, A. et al. (2011) Structure-function analyses point to a polynucleotide-accommodating groove essential for APOBEC3A restriction activities. J. Virol. 85, 1765-1776