Methylcytosine and normal cytosine deamination by the foreign DNA restriction enzyme APOBEC3A

Journal of Biological Chemistry

Volumn 287, Issue 41, 2012, Pages 34801-34808

  Carpenter, Michael A ^a,b   Li, Ming ^a,b   Rathore, Anurag ^a,b   Lackey, Lela ^a,b   Law, Emily K ^a,b   Land, Allison M ^a,b   Leonard, Brandon ^a,b   Shandilya, Shivender M D ^c   Bohn, Markus Frederik ^c   Schiffer, Celia A ^c   Brown, William L ^a,b   Harris, Reuben S ^a,b  

^a UNIVERSITY OF MINNESOTA   (United States)

^b UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATION INDUCED CYTIDINE DEAMINASE; CELL TYPES; DNA CLEARANCE; EVOLUTIONARY ADAPTATION; EXCISION REPAIR; GENOMIC DNA; HUMAN CELLS; IMMUNE FUNCTION; METHYLCYTOSINE; NUCLEOBASES; PLASMID DNA; RESTRICTION ENZYMES; SINGLE-STRANDED DNA;

ENZYMES; SUBSTRATES;

DNA;

5 METHYLCYTOSINE; CELL DNA; CYTOSINE; INTERFERON; NUCLEIC ACID BASE; PROTEIN APOBEC3A; RESTRICTION ENDONUCLEASE; SINGLE STRANDED DNA; THYMINE; UNCLASSIFIED DRUG; URACIL;

ARTICLE; BONE MARROW CELL; CELL LINEAGE; CONTROLLED STUDY; DNA MODIFICATION; DNA TRANSFECTION; ENZYME ACTIVITY; ENZYME MODIFICATION; ENZYME SPECIFICITY; EVOLUTIONARY ADAPTATION; HUMAN; HUMAN CELL; INNATE IMMUNITY; INTERFERON INDUCTION; PRIORITY JOURNAL; PROTEIN FOLDING;

5-METHYLCYTOSINE; CYTIDINE DEAMINASE; DEAMINATION; DNA; ENZYME INDUCTION; HEK293 CELLS; HUMANS; IMMUNITY, INNATE; INTERFERONS; PLASMIDS; PROTEINS; THYMINE; URACIL;

EID: 84867266936     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.385161     Document Type: Article

References (49)

1. Feng, S., Jacobsen, S. E., and Reik, W. (2010) Epigenetic reprogramming in plant and animal development. Science 330, 622-627
2. Bhutani, N., Burns, D. M., and Blau, H. M. (2011) DNA demethylation dynamics. Cell 146, 866-872
3. Nabel, C. S., Manning, S. A., and Kohli, R. M. (2012) The curious chemical biology of cytosine. Deamination, methylation, and oxidation as modulators of genomic potential. ACS Chem. Biol. 7, 20-30
4. Gehring, M., Reik, W., and Henikoff, S. (2009) DNA demethylation by DNA repair. Trends Genet. 25, 82-90
5. Cortázar, D., Kunz, C., Selfridge, J., Lettieri, T., Saito, Y., MacDougall, E., Wirz, A., Schuermann, D., Jacobs, A. L., Siegrist, F., Steinacher, R., Jiricny, J., Bird, A., and Schär, P. (2011) Embryonic lethal phenotype reveals a function of TDG in maintaining epigenetic stability. Nature 470, 419-423
6. He, Y. F., Li, B. Z., Li, Z., Liu, P., Wang, Y., Tang, Q., Ding, J., Jia, Y., Chen, Z., Li, L., Sun, Y., Li, X., Dai, Q., Song, C. X., Zhang, K., He, C., and Xu, G. L. (2011) Tet-mediated formation of 5-carboxylcytosine and its excision by TDG in mammalian DNA. Science 333, 1303-1307
7. Ito, S., D'Alessio, A. C., Taranova, O. V., Hong, K., Sowers, L. C., and Zhang, Y. (2010) Role of Tet proteins in 5mC to 5hmC conversion, ES-cell self-renewal and inner cell mass specification. Nature 466, 1129-1133
8. Ito, S., Shen, L., Dai, Q., Wu, S. C., Collins, L. B., Swenberg, J. A., He, C., and Zhang, Y. (2011) Tet proteins can convert 5-methylcytosine to 5-formyl-cytosine and 5-carboxylcytosine. Science 333, 1300-1303
9. Wossidlo, M., Nakamura, T., Lepikhov, K., Marques, C. J., Zakhartchenko, V., Boiani, M., Arand, J., Nakano, T., Reik, W., and Walter, J. (2011) 5-Hydroxymethylcytosine in the mammalian zygote is linked with epigenetic reprogramming. Nat. Commun. 2, 241
10. Hajkova, P., Jeffries, S. J., Lee, C., Miller, N., Jackson, S. P., and Surani, M. A. (2010) Genome-wide reprogramming in the mouse germ line entails the base excision repair pathway. Science 329, 78-82
11. Fritz, E. L., and Papavasiliou, F. N. (2010) Cytidine deaminases. AIDing DNA demethylation? Genes Dev. 24, 2107-2114
12. 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 (Pubitemid 39656611)
13. 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 (Pubitemid 36418164)
14. 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 (Pubitemid 39655938)
15. 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
16. 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
17. Cortellino, S., Xu, J., Sannai, M., Moore, R., Caretti, E., Cigliano, A., Le Coz, M., Devarajan, K., Wessels, A., Soprano, D., Abramowitz, L. K., Bartolomei, M. S., Rambow, F., Bassi, M. R., Bruno, T., Fanciulli, M., Renner, C., Klein-Szanto, A. J., Matsumoto, Y., Kobi, D., Davidson, I., Alberti, C., Larue, L., and Bellacosa, A. (2011) Thymine DNA glycosylase is essential for active DNA demethylation by linked deamination-base excision repair. Cell 146, 67-79
18. 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
19. LaRue, R. S., Andrésdóttir, V., Blanchard, Y., Conticello, S. G., Derse, D., Emerman, M., Greene, W. C., Jónsson, S. R., Landau, N. R., Löchelt, M., Malik, H. S., Malim, M. H., Münk, C., O'Brien, S. J., Pathak, V. K., Strebel, K., Wain-Hobson, S., Yu, X. F., Yuhki, N., and Harris, R. S. (2009) Guidelines for naming nonprimate APOBEC3 genes and proteins. J. Virol. 83, 494-497
20. Conticello, S. G. (2008) The AID/APOBEC family of nucleic acid mutators. Genome Biol. 9, 229
21. Sato, Y., Probst, H. C., Tatsumi, R., Ikeuchi, Y., Neuberger, M. S., and Rada, C. (2010) Deficiency in APOBEC2 leads to a shift in muscle fiber type, diminished body mass, and myopathy. J. Biol. Chem. 285, 7111-7118
22. Vonica, A., Rosa, A., Arduini, B. L., and Brivanlou, A. H. (2011) APOBEC2, a selective inhibitor of TGFβ signaling, regulates left-right axis specification during early embryogenesis. Dev. Biol. 350, 13-23
23. Rogozin, I. B., Basu, M. K., Jordan, I. K., Pavlov, Y. I., and Koonin, E. V. (2005) APOBEC4, a new member of the AID/APOBEC family of polynucleotide (deoxy)cytidine deaminases predicted by computational analysis. Cell Cycle 4, 1281-1285 (Pubitemid 41365401)
24. Longerich, S., Basu, U., Alt, F., and Storb, U. (2006) AID in somatic hypermutation and class switch recombination. Curr. Opin Immunol. 18, 164-174 (Pubitemid 43327298)
25. Di Noia, J. M., and Neuberger, M. S. (2007) Molecular mechanisms of antibody somatic hypermutation. Annu. Rev. Biochem. 76, 1-22
26. Rada, C., Di Noia, J. M., and Neuberger, M. S. (2004) Mismatch recognition and uracil excision provide complementary paths to both Ig switching and the A/T-focused phase of somatic mutation. Mol Cell 16, 163-171 (Pubitemid 39388832)
27. Blanc, V., and Davidson, N. O. (2003) C-to-U RNA editing. Mechanisms leading to genetic diversity. J. Biol. Chem. 278, 1395-1398 (Pubitemid 36801361)
28. Malim, M. H. (2009) APOBEC proteins and intrinsic resistance to HIV-1 infection. Philos Trans. R. Soc. Lond. B Biol. Sci. 364, 675-687
29. Albin, J. S., and Harris, R. S. (2010) Interactions of host APOBEC3 restriction factors with HIV-1 in vivo. Implications for therapeutics. Expert Rev. Mol. Med. 12, e4
30. 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
31. Bulliard, Y., Narvaiza, I., Bertero, A., Peddi, S., Röhrig, U. F., Ortiz, M., Zoete, V., Castro-Díaz, N., Turelli, P., Telenti, A., Michielin, O., Weitzman, M. D., and Trono, D. (2011) Structure-function analyses point to a polynucleotide-accommodating groove essential for APOBEC3A restriction activities. J. Virol. 85, 1765-1776
32. Landry, S., Narvaiza, I., Linfesty, D. C., and Weitzman, M. D. (2011) APOBEC3A can activate the DNA damage response and cause cell-cycle arrest. EMBO Rep. 12, 444-450
33. 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 (Pubitemid 43343708)
34. Thielen, B. K., McNevin, J. P., McElrath, M. J., Hunt, B. V., Klein, K. C., and Lingappa, J. R. (2010) 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, 27753-27766
35. Koning, F. A., Newman, E. N., Kim, E. Y., Kunstman, K. J., Wolinsky, S. M., and Malim, M. H. (2009) Defining APOBEC3 expression patterns in human tissues and hematopoietic cell subsets. J. Virol. 83, 9474-9485
36. 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., and Harris, R. S. (2012) First-in-class small molecule inhibitors of the single-strand DNA cytosine deaminase APOBEC3G. ACS Chem. Biol. 7, 506-517
37. Refsland, E. W., Stenglein, M. D., Shindo, K., Albin, J. S., Brown, W. L., and Harris, R. S. (2010) Quantitative profiling of the full APOBEC3 mRNA repertoire in lymphocytes and tissues. Implications for HIV-1 restriction. Nucleic Acids Res. 38, 4274-4284
38. 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
39. Peng, G., Lei, K. J., Jin, W., Greenwell-Wild, T., and Wahl, S. M. (2006) Induction of APOBEC3 family proteins, a defensive maneuver underlying interferon-induced anti-HIV-1 activity. J. Exp. Med. 203, 41-46
40. Lindahl, T., Ljungquist, S., Siegert, W., Nyberg, B., and Sperens, B. (1977) DNA N-glycosidases. Properties of uracil-DNA glycosidase from Escherichia coli. J. Biol. Chem. 252, 3286-3294 (Pubitemid 8111183)
41. Stivers, J. T., Pankiewicz, K. W., and Watanabe, K. A. (1999) Kinetic mechanism of damage site recognition and uracil flipping by Escherichia coli uracil DNA glycosylase. Biochemistry 38, 952-963
42. Harris, R. S., Bishop, K. N., Sheehy, A. M., Craig, H. M., Petersen-Mahrt, S. K., Watt, I. N., Neuberger, M. S., and Malim, M. H. (2003) DNA deamination mediates innate immunity to retroviral infection. Cell 113, 803-809 (Pubitemid 36724943)
43. Nowarski, R., Britan-Rosich, E., Shiloach, T., and Kotler, M. (2008) Hypermutation by intersegmental transfer of APOBEC3G cytidine deaminase. Nat. Struct. Mol. Biol. 15, 1059-1066
44. Chelico, L., Pham, P., Calabrese, P., and Goodman, M. F. (2006) APOBEC3GDNAdeaminase acts processively 3′ → 5′ on single-stranded DNA. Nat. Struct. Mol. Biol. 13, 392-399 (Pubitemid 43881578)
45. Iwatani, Y., Chan, D. S., Wang, F., Maynard, K. S., Sugiura, W., Gronenborn, A. M., Rouzina, I., Williams, M. C., Musier-Forsyth, K., and Levin, J. G. (2007) Deaminase-independent inhibition of HIV-1 reverse transcription by APOBEC3G. Nucleic Acids Res. 35, 7096-7108
46. Harjes, E., Gross, P. J., Chen, K. M., Lu, Y., Shindo, K., Nowarski, R., Gross, J. D., Kotler, M., Harris, R. S., and Matsuo, H. (2009) An extended structure of the APOBEC3G catalytic domain suggests a unique holoenzyme model. J. Mol. Biol. 389, 819-832
47. 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 (Pubitemid 43878096)
48. 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., in press
49. 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., and Schiffer, C. A. (2010) Crystal structure of the APOBEC3G catalytic domain reveals potential oligomerization interfaces. Structure 18, 28-38