A mathematical model for scanning and catalysis on single-stranded DNA, illustrated with activation-induced deoxycytidine deaminase

Journal of Biological Chemistry

Volumn 288, Issue 41, 2013, Pages 29786-29795

  Mak, Chi H ^a   Pham, Phuong ^a   Afif, Samir A ^a   Goodman, Myron F ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AVERAGE DISTANCE; CATALYTIC EFFICIENCIES; DEOXYCYTIDINE DEAMINASE; MATHEMATICAL ANALYSIS; SINGLE-STRANDED DNA; SOMATIC HYPERMUTATION; STATISTICAL PROPERTIES; TWO-POINT CORRELATION;

AMINES; CATALYSIS; DNA; EFFICIENCY; ENZYMES; MATHEMATICAL MODELS; TRANSCRIPTION;

SCANNING;

ACTIVATION INDUCED CYTIDINE DEAMINASE; SINGLE STRANDED DNA;

ARTICLE; CATALYSIS; CLONAL VARIATION; DEAMINATION; ENZYME ANALYSIS; ENZYME BINDING; GENE REARRANGEMENT; GENE SEQUENCE; GENETIC RECOMBINATION; GENETIC VARIABILITY; IMMUNOGLOBULIN GENE; MATHEMATICAL MODEL; POINT MUTATION; PRIORITY JOURNAL; PROCESS OPTIMIZATION; PROTEIN MOTIF; REPORTER GENE; SOMATIC MUTATION;

AID; DNA ENZYMES; ENZYME CATALYSIS; MATHEMATICAL MODELING; MUTAGENESIS; PROTEIN DNA-INTERACTION; SSDNA SCANNING; STOCHASTIC PROCESSES;

ALGORITHMS; BIOCATALYSIS; CYTIDINE DEAMINASE; DNA, SINGLE-STRANDED; KINETICS; MODELS, BIOLOGICAL; MUTATION; SUBSTRATE SPECIFICITY; TRANSCRIPTION, GENETIC;

EID: 84885595546     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.506550     Document Type: Article

References (47)

1. Porecha, R. H., and Stivers, J. T. (2008) Uracil DNA glycosylase uses DNA hopping and short-range sliding to trap extrahelical uracils. Proc. Natl. Acad. Sci. U.S.A. 105, 10791-10796
2. Schonhoft, J. D., and Stivers, J. T. (2012) Timing facilitated site transfer of an enzyme on DNA. Nat. Chem. Biol. 8, 205-210
3. Blainey, P. C., Luo, G., Kou, S. C., Mangel, W. F., Verdine, G. L., Bagchi, B., and Xie, X. S. (2009) Nonspecifically bound proteins spin while diffusing along DNA. Nat. Struct. Mol. Biol. 16, 1224-1229
4. Blainey, P. C., van Oijen, A. M., Banerjee, A., Verdine, G. L., and Xie, X. S. (2006) A base-excision DNA-repair protein finds intrahelical lesion bases by fast sliding in contact with DNA. Proc. Natl. Acad. Sci. U.S.A. 103, 5752-5757
5. Gowers, D. M., Wilson, G. G., and Halford, S. E. (2005) Measurement of the contributions of 1D and 3D pathways to the translocation of a protein along DNA. Proc. Natl. Acad. Sci. U.S.A. 102, 15883-15888
6. Gorman, J., Chowdhury, A., Surtees, J. A., Shimada, J., Reichman, D. R., Alani, E., and Greene, E. C. (2007) Dynamic basis for one-dimensional DNA scanning by the mismatch repair complex Msh2-Msh6. Mol. Cell 28, 359-370
7. Gorman, J., and Greene, E. C. (2008) Visualizing one-dimensional diffusion of proteins along DNA. Nat. Struct. Mol. Biol. 15, 768-774
8. Berg, O. G., Winter, R. B., and von Hippel, P. H. (1981) Diffusion-driven mechanisms of protein translocation on nucleic acids. 1. Models and theory. Biochemistry 20, 6929-6948
9. von Hippel, P. H., and Berg, O. G. (1989) Facilitated target location in biological systems. J. Biol. Chem. 264, 675-678
10. Coppey, M., Bénichou, O., Voituriez, R., and Moreau, M. (2004) Kinetics of target site localization of a protein on DNA: a stochastic approach. Biophys. J. 87, 1640-1649
11. Bénichou, O., Coppey, M., Moreau, M., Suet, P.-H., and Voituriez, R. (2005) Optimal search strategies for hidden targets. Phys. Rev. Lett 94, 198101
12. Halford, S. E. (2001) Hopping, jumping and looping by restriction enzymes. Biochem. Soc. Trans 29, 363-374
13. Conticello, S. G., Langlois, M. A., Yang, Z., and Neuberger, M. S. (2007) DNA deamination in immunity: AID in the context of its APOBEC relatives. Adv. Immunol 94, 37-73
14. Jaszczur, M., Bertram, J. G., Pham, P., Scharff, M. D., and Goodman, M. F. (2013) AID and Apobec3G haphazard deamination and mutational diversity. Cell Mol. Life Sci. 70, 3089-3108
15. Di Noia, J. M., and Neuberger, M. S. (2007) Molecular mechanisms of antibody somatic hypermutation. Annu. Rev. Biochem. 76, 1-22
16. Peled, J. U., Kuang, F. L., Iglesias-Ussel, M. D., Roa, S., Kalis, S. L., Goodman, M. F., and Scharff, M. D. (2008) The biochemistry of somatic hypermutation. Annu. Rev. Immunol 26, 481-511
17. 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
18. Pham, P., Bransteitter, R., Petruska, J., and Goodman, M. F. (2003) Processive AID-catalysed cytosine deamination on single-stranded DNA simulates somatic hypermutation. Nature 424, 103-107
19. Chaudhuri, J., Tian, M., Khuong, C., Chua, K., Pinaud, E., and Alt, F. W. (2003) Transcription-targeted DNA deamination by the AID antibody diversification enzyme. Nature 422, 726-730
20. Flory, P. J. (1953) Principles of Polymer Chemistry, Cornell University Press, Ithaca, NY
21. de Gennes, P.-G. (1979) Scaling Concepts in Polymer Physics, Cornell University Press, Ithaca, NY
22. Doi, M., and Edwards, S. F. (1986) The Theory of Polymer Dynamics, Oxford University Press, Oxford
23. Fisher, M. E. (1984) Walks, walls, wetting, and melting. J. Stat Phys. 34, 667-729
24. Loring, R. F., and Fayer, M. D. (1982) Electronic excited state transport and trapping in one and two dimensional disordered systems. Chem. Phys. 70, 139-147
25. Pham, P., Calabrese, P., Park, S. J., and Goodman, M. F. (2011) Analysis of a single-stranded DNA-scanning process in which activation-induced deoxycytidine deaminase (AID) deaminates C to U haphazardly and inefficiently to ensure mutational diversity. J. Biol. Chem. 286, 24931-24942
26. Bransteitter, R., Pham, P., Calabrese, P., and Goodman, M. F. (2004) Biochemical analysis of hypermutational targeting by wild type and mutant activation-induced cytidine deaminase. J. Biol. Chem. 279, 51612-51621
27. Hu, T., Grosberg, A. Y., and Shklovskii, B. I. (2006) How proteins search for their specific sites on DNA: the role of DNA conformation. Biophys. J. 90, 2731-2744
28. Gardiner, C. W. (1994) Handbook of Stochastic Methods: for Physics, Chemistry and the Natural Sciences (Lecture Notes in Mathematics), 2nd ed., pp. 236-299, Springer-Verlag New York Inc., New York
29. Meester, R. (2008) A Natural Introduction to Probability Theory, 2nd Ed., pp. 137-151, Birkhauser, Basel, Switzerland
30. Press, W., Teukolsky, S., Vetterling, W., and Flannery, B. (2007) Numerical Recipes 3rd Edition: The Art of Scientific Computing, 3rd ed., pp. 82-89, Cambridge University Press, New York
31. Halford, S. E., and Marko, J. F. (2004) How do site-specific DNA-binding proteins find their targets? Nucleic Acids Res. 32, 3040-3052
32. Condamin, S., Bénichou, O., Tejedor, V., Voituriez, R., and Klafter, J. (2007) First-passage times in complex scale-invariant media. Nature 450, 77-80
33. Lomholt, M. A., van den Broek, B., Kalisch, S.-M. J., Wuite, G. J. L., and Metzler, R. (2009) Facilitated diffusion with DNA coiling. Proc. Natl. Acad. Sci. U.S.A. 106, 8204-8208
34. Marcovitz, A., and Levy, Y. (2011) Frustration in protein-DNA binding influences conformational switching and target search kinetics. Proc. Natl. Acad. Sci. U.S.A. 108, 17957-17962
35. 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
36. Senavirathne, G., Jaszczur, M., Auerbach, P. A., Upton, T. G., Chelico, L., Goodman, M. F., and Rueda, D. (2012) Single-stranded DNA scanning and deamination by APOBEC3G cytidine deaminase at single molecule resolution. J. Biol. Chem. 287, 15826-15835
37. Shen, H. M., Ratnam, S., and Storb, U. (2005) Targeting of the activationinduced cytosine deaminase is strongly influenced by the sequence and structure of the targeted DNA. Mol. Cell Biol. 25, 10815-10821
38. Canugovi, C., Samaranayake, M., and Bhagwat, A. S. (2009) Transcriptional pausing and stalling causes multiple clustered mutations by human activation-induced deaminase. FASEB J. 23, 34-44
39. Yu, K., Chedin, F., Hsieh, C. L., Wilson, T. E., and Lieber, M. R. (2003) R-loops at immunoglobulin class switch regions in the chromosomes of stimulated B cells. Nat. Immunol. 4, 442-451
40. Darzacq, X., Shav-Tal, Y., de Turris, V., Brody, Y., Shenoy, S. M., Phair, R. D., and Singer, R. H. (2007) In vivo dynamics of RNA polymerase II transcription. Nat. Struct. Mol. Biol. 14, 796-806
41. Singh, J., and Padgett, R. A. (2009) Rates of in situ transcription and splicing in large human genes. Nat. Struct. Mol. Biol. 16, 1128-1133
42. 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
43. Storb, U., Shen, H. M., and Nicolae, D. (2009) Somatic hypermutation: processivity of the cytosine deaminase AID and error-free repair of the resulting uracils. Cell Cycle 8, 3097-3101
44. 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., and Harris, R. S. (2013) APOBEC3B is an enzymatic source of mutation in breast cancer. Nature 494, 366-370
45. Lada, A. G., Dhar, A., Boissy, R. J., Hirano, M., Rubel, A. A., Rogozin, I. B., and Pavlov, Y. I. (2012) AID/APOBEC cytosine deaminase induces genome- wide kataegis. Biol. Direct 7, 47; discussion 47
46. 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., and Gordenin, D. A. (2012) Clustered mutations in yeast and in human cancers can arise from damaged long single-strand DNA regions. Mol. Cell 46, 424-435
47. 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