Architecturally diverse proteins converge on an analogous mechanism to inactivate Uracil-DNA glycosylase

Nucleic Acids Research

Volumn 41, Issue 18, 2013, Pages 8760-8775

  Cole, Ambrose R ^a   Ofer, Sapir ^a,b   Ryzhenkova, Ksenia ^a   Baltulionis, Gediminas ^a   Hornyak, Peter ^a,c   Savva, Renos ^a  

^a UNIVERSITY OF LONDON   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY OF SUSSEX   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN P56; URACIL DNA GLYCOSIDASE; VIRUS PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME INHIBITION; EXCISION REPAIR; HYDROPHOBICITY; MOLECULAR RECOGNITION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN SUBUNIT; PROTEIN TARGETING; SITE DIRECTED MUTAGENESIS; STRUCTURE ACTIVITY RELATION;

AMINO ACID SEQUENCE; BACILLUS PHAGES; BINDING SITES; CATALYTIC DOMAIN; DNA; HERPESVIRUS 1, HUMAN; HUMANS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; LEUCINE; MODELS, MOLECULAR; MOLECULAR MIMICRY; MOLECULAR SEQUENCE DATA; MUTATION; PROTEIN STRUCTURE, SECONDARY; URACIL-DNA GLYCOSIDASE; VIRAL PROTEINS;

EID: 84885938840     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt633     Document Type: Article

References (46)

1. Sharp, P.M. (1986) Molecular evolution of bacteriophages: Evidence of selection against the restriction sites of host restriction enzymes. Mol. Biol. Evol., 3, 75-83.
2. Warren, R.A. (1980) Modified bases in bacteriophage DNAs. Annu. Rev. Microbiol., 34, 137-158.
3. Berkner, K.L. and Folk, W.R. (1979) The effects of substituted pyrimidines in DNAs on cleavage by sequence-specific endonucleases. J. Biol. Chem., 254, 2551-2560.
4. Huang, L.H., Farnet, C.M., Ehrlich, K.C. and Ehrlich, M. (1982) Digestion of highly modified bacteriophage DNA by restriction endonucleases. Nucleic Acids Res., 10, 1579-1591.
5. Takahashi, I. and Marmur, J. (1963) Replacement of thymidylic acid by deoxyuridylic acid in the deoxyribonucleic acid of a transducing phage for Bacillus subtilis. Nature, 197, 794-795.
6. Kiljunen, S., Hakala, K., Pinta, E., Huttunen, S., Pluta, P., Gador, A., Lo? nnberg, H. and Skurnik, M. (2005) Yersiniophage fR1-37 is a tailed bacteriophage having a 270 kb DNA genome with thymidine replaced by deoxyuridine. Microbiology, 151, 4093-4102.
7. Duncan, B.K. and Warner, H.R. (1977) Metabolism of uracilcontaining DNA: degradation of bacteriophage PBS2 DNA in Bacillus subtilis. J. Virol., 22, 835-838.
8. Tye, B.K., Nyman, P.O., Lehman, I.R., Hochhauser, S. and Weiss, B. (1977) Transient accumulation of Okazaki fragments as a result of uracil incorporation into nascent DNA. Proc. Natl Acad. Sci. USA, 74, 154-157.
9. Katz, G.E., Price, A.R. and Pomerantz, M.J. (1976) Bacteriophage PBS2-induced inhibition of uracil-containing DNA degradation. J. Virol., 20, 535-538.
10. Savva, R. and Pearl, L.H. (1995) Nucleotide mimicry in the crystal structure of the uracil-DNA glycosylase-uracil glycosylase inhibitor protein complex. Nat. Struct. Biol., 2, 752-757.
11. Putnam, C.D., Shroyer, M.J.N., Lundquist, A.J., Mol, C.D., Arvai, A.S., Mosbaugh, D.W. and Tainer, J.A. (1999) Protein mimicry of DNA from crystal structures of the uracil-DNA glycosylase inhibitor protein and its complex with Escherichia coli uracil-DNA glycosylase. J. Mol. Biol., 287, 331-346.
12. Pearl, L.H. (2000) Structure and function in the uracil-DNA glycosylase superfamily. Mutat. Res., 460, 165-81.
13. Lucas-Lledó , J.I., Maddamsetti, R. and Lynch, M. (2011) Phylogenomic Analysis of the Uracil-DNA Glycosylase Superfamily. Mol. Biol. Evol., 28, 1307-1317.
14. Lee, H.W., Dominy, B.N. and Cao, W. (2011) New family of deamination repair enzymes in uracil-DNA glycosylase superfamily. J. Biol. Chem., 286, 31282-31287.
15. Savva, R., McAuley-Hecht, K., Brown, T. and Pearl, L. (1995) The structural basis of specific base-excision repair by uracil-DNA glycosylase. Nature, 373, 487-493.
16. Parikh, S.S., Mol, C.D., Slupphaug, G., Bharati, S., Krokan, H.E. and Tainer, J.A. (1998) Base excision repair initiation revealed by crystal structures and binding kinetics of human uracil-DNA glycosylase with DNA. EMBO J., 17, 5214-5226.
17. Friedman, J.I., Majumdar, A. and Stivers, J.T. (2009) Nontarget DNA binding shapes the dynamic landscape for enzymatic recognition of DNA damage. Nucleic Acids Res., 37, 3493-3500.
18. Haushalter, K.A., Stukenberg, P.T., Kirschner, M.W. and Verdine, G.L. (1999) Identification of a new uracil-DNA glycosylase family by expression cloning using synthetic inhibitors. Curr. Biol., 9, 174-185.
19. Barrett, T.E., Savva, R., Panayotou, G., Barlow, T., Brown, T., Jiricny, J. and Pearl, L.H. (1998) Crystal Structure of a G:T/U Mismatch-Specific DNA Glycosylase: Mismatch Recognition by Complementary-Strand Interactions. Cell, 92, 117-129.
20. Koulis, A., Cowan, D.A., Pearl, L. and Savva, R. (1996) Uracil- DNA glycosylase activities in hyperthermophilic micro-organisms. FEMS Microbiol. Lett., 143, 267-271.
21. Schormann, N., Grigorian, A., Samal, A., Krishnan, R., DeLucas, L. and Chattopadhyay, D. (2007) Crystal structure of vaccinia virus uracil-DNA glycosylase reveals dimeric assembly. BMC Struct. Biol., 7, 45.
22. Serrano-Heras, G., Salas, M. and Bravo, A. (2006) A uracil-DNA glycosylase inhibitor encoded by a non-uracil containing viral DNA. J. Biol. Chem., 281, 7068-7074.
23. Warner, H.R., Johnson, L.K. and Snustad, D.P. (1980) Early events after infection of Escherichia coli by bacteriophage T5. III. Inhibition of uracil-DNA glycosylase activity. J. Virol., 33, 535-538.
24. Asensio, J.L., Pérez-Lago, L., Lá zaro, J.M., Gonzá lez, C., Serrano- Heras, G. and Salas, M. (2011) Novel dimeric structure of phage f29-encoded protein p56: insights into uracil-DNA glycosylase inhibition. Nucleic Acids Res., 39, 9779-9788.
25. Acharya, N., Kumar, P. and Varshney, U. (2003) Complexes of the uracil-DNA glycosylase inhibitor protein, Ugi, with Mycobacterium smegmatis and Mycobacterium tuberculosis uracil-DNA glycosylases. Microbiol., 149, 1647-1658.
26. Putnam, C.D. and Tainer, J.A. (2005) Protein mimicry of DNA and pathway regulation. DNA Repair, 4, 1410-1420.
27. Pérez-Lago, L., Serrano-Heras, G., Ban? os, B., Lá zaro, J.M., Alcorlo, M., Villar, L. and Salas, M. (2011) Characterization of Bacillus subtilis uracil-DNA glycosylase and its inhibition by phage f29 protein p56. Mol. Microbiol., 80, 1657-1666.
28. Serrano-Heras, G., Ruiz-Maso, J.A., del Solar, G., Espinosa, M., Bravo, A. and Salas, M. (2007) Protein p56 from the Bacillus subtilis phage f29 inhibits DNA-binding ability of uracil-DNA glycosylase. Nucleic Acids Res., 35, 5393-5401.
29. dos Reis, M., Wernisch, L. and Savva, R. (2003) Unexpected correlations between gene expression and codon usage Bias from microarray data for the whole Escherichia coli K-12 genome. Nucleic Acids Res., 31, 6976-6985.
30. Cabrita, L.D., Gilis, D., Robertson, A.L., Dehouck, Y., Rooman, M. and Bottomley, S.P. (2007) Enhancing the stability and solubility of TEV protease using in silico design. Protein Sci., 16, 2360-2367.
31. Savva, R. and Pearl, L.H. (1995) Cloning and expression of the Uracil-DNA Glycosylase Inhibitor (UGI) from Bacteriophage PBS-1, and crystallization of a uracil-DNA glycosylase-UGI complex. Proteins Struct. Funct. Genet., 22, 287-289.
32. Hennessy, D.N., Narayanan, B. and Rosenberg, J.M. (2009) Automatic implementation of precise grid screens: The fourcorners method. Acta Crystallogr. D Biol. Crystallogr., 65, 1001-1003.
33. Newman, J., Egan, D., Walter, T.S., Meged, R., Berry, I., Ben Jelloul, M., Sussman, J.L., Stuart, D.I. and Perrakis, A. (2005) Towards rationalization of crystallization screening for small- to medium-sized academic laboratories: The PACT/JCSG+strategy. Acta Crystallogr. D Biol. Crystallogr., 61, 1426-1431.
34. Broennimann, Ch., Eikenberry, E.F., Henrich, B., Horisberger, R., Huelsen, G., Pohl, E., Schmitt, B., Schulze-Briese, C., Suzuki, M. and Tomizaki, T. (2006) The PILATUS 1M detector. J. Synchrotron Radiat., 13, 120-130.
35. Winn, M.D., Ballard, C.C., Cowtan, K.D., Dodson, E.J., Emsley, P., Evans, P.R., Keegan, R.M., Krissinel, E.B., Leslie, A.G. and McCoy, A. (2011) Overview of the CCP4 suite and current developments. Acta Crystallogr. D Biol. Crystallogr., 67, 235-142.
36. Winter, G. (2010) xia2: An expert system for macromolecular crystallography data reduction. J. Appl. Cryst., 43, 186-190.
37. McCoy, A.J., Grosse-Kunstleve, R.W., Adams, P.D., Winn, M.D., Storoni, L.C. and Read, R.J. (2007) Phaser crystallographic software. J. Appl. Cryst., 40, 658-674.
38. Bricogne, G., Blanc, E., Brandl, M., Flensburg, C., Keller, P., Paciorek, W., Roversi, P., Sharff, A., Smart, O.S. and Vonrhein, C. (2011) BUSTER version 2.10.0. Global Phasing Ltd, Cambridge, UK.
39. Emsley, P., Lohkamp, B., Scott, W.G. and Cowtan, K. (2010) Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr., 66, 486-501.
40. Kleywegt, G.J. and Jones, T.A. (1994) Detection, delineation, measurement and display of cavities in macromolecular structures. Acta Crystallogr. D Biol. Crystallogr., 50, 178-185.
41. Williams, M.A. (2013) Protein-ligand interactions: fundamentals. Methods Mol. Biol., 1008, 3-34.
42. Henschel, A., Kim, W.K. and Schroeder, M. (2006) Equivalent binding sites reveal convergently evolved interaction motifs. Bioinformatics, 22, 550-555.
43. Mulder, L.C., Harari, A. and Simon, V. (2008) Cytidine deamination induced HIV-1 drug resistance. Proc. Natl Acad. Sci. USA, 105, 5501-5506.
44. Martomo, S.A. and Gearhart, P.J. (2006) Somatic hypermutation: subverted DNA repair. Curr. Opin. Immunol., 18, 243-248.
45. Limor-Waisberg, K., Carmi, A., Scherz, A., Pilpel, Y. and Furman, I. (2011) Specialization versus adaptation: Two strategies employed by cyanophages to enhance their translation efficiencies. Nucleic Acids Res., 39, 6016-6028.
46. Jern, P., Russell, R.A., Pathak, V.K. and Coffin, J.M. (2009) Likely role of APOBEC3G-mediated G-to-A mutations in HIV-1 evolution and drug resistance. PLoS Pathog., 5, e1000367.