Enzymatic activities and DNA substrate specificity of mycobacterium tuberculosis DNA helicase XPB

PLoS ONE

Volumn 7, Issue 5, 2012, Pages

  Balasingham, Seetha V ^a,b   Zegeye, Ephrem Debebe ^a   Homberset, Håvard ^a   Rossi, Marie L ^c,d   Laerdahl, Jon K ^a,b   Bohr, Vilhelm A ^c   Tønjum, Tone ^a,b  

^a UNIVERSITY OF OSLO   (Norway)

^b OSLO UNIVERSITY HOSPITAL   (Norway)

^c NATIONAL INSTITUTE ON AGING   (United States)

^d INTREXON CORPORATION   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; COMPLEMENTARY DNA; DEOXYADENOSINE TRIPHOSPHATE; DNA; DNA HELICASE XPB; HELICASE; MAGNESIUM ION; MANGANESE; RNA; UNCLASSIFIED DRUG;

ARTICLE; CATALYSIS; CONTROLLED STUDY; DNA DENATURATION; DNA STRAND; ENZYME ACTIVITY; ENZYME SPECIFICITY; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; NUCLEOTIDE SEQUENCE;

ADENOSINE TRIPHOSPHATASES; DNA DAMAGE; DNA HELICASES; DNA REPAIR; DNA REPLICATION; DNA, BACTERIAL; DNA-BINDING PROTEINS; MYCOBACTERIUM TUBERCULOSIS; PROTEIN STRUCTURE, TERTIARY; RNA POLYMERASE II; SUBSTRATE SPECIFICITY; TRANSCRIPTION FACTOR TFIIH; TRANSCRIPTION, GENETIC;

BACTERIA (MICROORGANISMS); CORYNEBACTERINEAE; EUKARYOTA; MYCOBACTERIUM TUBERCULOSIS;

EID: 84861313408     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0036960     Document Type: Article

References (57)

1. Nathan C, Shiloh MU, (2000) Reactive oxygen and nitrogen intermediates in the relationship between mammalian hosts and microbial pathogens. Proc Natl Acad Sci U S A 97: 8841-8848.
2. Manganelli R, Provvedi R, Rodrigue S, Beaucher J, Gaudreau L, et al. (2004) Sigma factors and global gene regulation in Mycobacterium tuberculosis. J Bacteriol 186: 895-902.
3. Olsen I, Balasingham SV, Davidsen T, Debebe E, Rodland EA, et al. (2009) Characterization of the major formamidopyrimidine-DNA glycosylase homolog in Mycobacterium tuberculosis and its linkage to variable tandem repeats. FEMS Immunol Med Microbiol 56: 151-161.
4. Ambur OH, Davidsen T, Frye SA, Balasingham SV, Lagesen K, et al. (2009) Genome dynamics in major bacterial pathogens. FEMS Microbiol Rev 33: 453-470.
5. Mizrahi V, Andersen SJ, (1998) DNA repair in Mycobacterium tuberculosis. What have we learnt from the genome sequence? Mol Microbiol 29: 1331-1339.
6. Matson SW, Bean DW, George JW, (1994) DNA helicases: enzymes with essential roles in all aspects of DNA metabolism. Bioessays 16: 13-22.
7. Schmid SR, Linder P, (1992) D-E-A-D protein family of putative RNA helicases. Mol Microbiol 6: 283-291.
8. Weeda G, van Ham RC, Vermeulen W, Bootsma D, van der Eb AJ, et al. (1990) A presumed DNA helicase encoded by ERCC-3 is involved in the human repair disorders xeroderma pigmentosum and Cockayne's syndrome. Cell 62: 777-791.
9. Schaeffer L, Roy R, Humbert S, Moncollin V, Vermeulen W, et al. (1993) DNA repair helicase: a component of BTF2 (TFIIH) basic transcription factor. Science 260: 58-63.
10. Biswas T, Pero JM, Joseph CG, Tsodikov OV, (2009) DNA-dependent ATPase activity of bacterial XPB helicases. Biochemistry 48: 2839-2848.
11. Poterszman A, Lamour V, Egly JM, Moras D, Thierry JC, et al. (1997) A eukaryotic XPB/ERCC3-like helicase in Mycobacterium leprae? Trends Biochem Sci 22: 418-419.
12. Voloshin ON, Vanevski F, Khil PP, Camerini-Otero RD, (2003) Characterization of the DNA damage-inducible helicase DinG from Escherichia coli. J Biol Chem 278: 28284-28293.
13. Coin F, Oksenych V, Egly JM, (2007) Distinct roles for the XPB/p52 and XPD/p44 subcomplexes of TFIIH in damaged DNA opening during nucleotide excision repair. Mol Cell 26: 245-256.
14. Lehmann AR, (2003) DNA repair-deficient diseases, xeroderma pigmentosum, Cockayne syndrome and trichothiodystrophy. Biochimie 85: 1101-1111.
15. Giglia-Mari G, Coin F, Ranish JA, Hoogstraten D, Theil A, et al. (2004) A new, tenth subunit of TFIIH is responsible for the DNA repair syndrome trichothiodystrophy group A. Nat Genet 36: 714-719.
16. Oh KS, Khan SG, Jaspers NG, Raams A, Ueda T, et al. (2006) Phenotypic heterogeneity in the XPB DNA helicase gene (ERCC3): xeroderma pigmentosum without and with Cockayne syndrome. Hum Mutat 27: 1092-1103.
17. Yang W, (2008) Structure and mechanism for DNA lesion recognition. Cell Res 18: 184-197.
18. Sancar A, (1996) DNA excision repair. Annu Rev Biochem 65: 43-81.
19. Mazloum N, Stegman MA, Croteau DL, Van Houten B, Kwon NS, et al. (2011) Identification of a chemical that inhibits the mycobacterial UvrABC complex in nucleotide excision repair. Biochemistry 50: 1329-1335.
20. Truglio JJ, Croteau DL, Van Houten B, Kisker C, (2006) Prokaryotic nucleotide excision repair: the UvrABC system. Chem Rev 106: 233-252.
21. Hanawalt PC, Ford JM, Lloyd DR, (2003) Functional characterization of global genomic DNA repair and its implications for cancer. Mutat Res 544: 107-114.
22. Jeppesen DK, Bohr VA, Stevnsner T, (2011) DNA repair deficiency in neurodegeneration. Prog Neurobiol 94: 166-200.
23. Curti E, Smerdon SJ, Davis EO, (2007) Characterization of the helicase activity and substrate specificity of Mycobacterium tuberculosis UvrD. J Bacteriol 189: 1542-1555.
24. Sinha KM, Stephanou NC, Gao F, Glickman MS, Shuman S, (2007) Mycobacterial UvrD1 is a Ku-dependent DNA helicase that plays a role in multiple DNA repair events, including double-strand break repair. J Biol Chem 282: 15114-15125.
25. Sinha KM, Stephanou NC, Unciuleac MC, Glickman MS, Shuman S, (2008) Domain requirements for DNA unwinding by mycobacterial UvrD2, an essential DNA helicase. Biochemistry 47: 9355-9364.
26. Fan L, Arvai AS, Cooper PK, Iwai S, Hanaoka F, et al. (2006) Conserved XPB core structure and motifs for DNA unwinding: implications for pathway selection of transcription or excision repair. Mol Cell 22: 27-37.
27. Gorbalenya AE, Koonin EV, (1993) Helicases: amino acid sequence comparisons and structure-function relationships. Current Opinion in Structural Biology 3: 419-429.
28. Coin F, Marinoni JC, Rodolfo C, Fribourg S, Pedrini AM, et al. (1998) Mutations in the XPD helicase gene result in XP and TTD phenotypes, preventing interaction between XPD and the p44 subunit of TFIIH. Nat Genet 20: 184-188.
29. Lesnik EA, Guinosso CJ, Kawasaki AM, Sasmor H, Zounes M, et al. (1993) Oligodeoxynucleotides containing 2′-O-modified adenosine: synthesis and effects on stability of DNA:RNA duplexes. Biochemistry 32: 7832-7838.
30. Sproat BS, Lamond AI, Beijer B, Neuner P, Ryder U, (1989) Highly efficient chemical synthesis of 2′-O-methyloligoribonucleotides and tetrabiotinylated derivatives; novel probes that are resistant to degradation by RNA or DNA specific nucleases. Nucleic Acids Res 17: 3373-3386.
31. Cordin O, Tanner NK, Doere M, Linder P, Banroques J, (2004) The newly discovered Q motif of DEAD-box RNA helicases regulates RNA-binding and helicase activity. Embo J 23: 2478-2487.
32. Oksenych V, de Jesus BB, Zhovmer A, Egly JM, Coin F, (2009) Molecular insights into the recruitment of TFIIH to sites of DNA damage. Embo J 28: 2971-2980.
33. Dvir A, Conaway RC, Conaway JW, (1997) A role for TFIIH in controlling the activity of early RNA polymerase II elongation complexes. Proc Natl Acad Sci U S A 94: 9006-9010.
34. Hellman LM, Fried MG, (2007) Electrophoretic mobility shift assay (EMSA) for detecting protein-nucleic acid interactions. Nat Protoc 2: 1849-1861.
35. Rouillon C, White MF, (2010) The XBP-Bax1 helicase-nuclease complex unwinds and cleaves DNA: implications for eukaryal and archaeal nucleotide excision repair. J Biol Chem 285: 11013-11022.
36. Cole ST, Brosch R, Parkhill J, Garnier T, Churcher C, et al. (1998) Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393: 537-544.
37. Berquist BR, Wilson DM 3rd, (2009) Nucleic acid binding activity of human Cockayne syndrome B protein and identification of Ca(2+) as a novel metal cofactor. J Mol Biol 391: 820-832.
38. Matson SW, George JW, (1987) DNA helicase II of Escherichia coli. Characterization of the single-stranded DNA-dependent NTPase and helicase activities. J Biol Chem 262: 2066-2076.
39. Eoff RL, Raney KD, (2010) Kinetic mechanism for DNA unwinding by multiple molecules of Dda helicase aligned on DNA. Biochemistry 49: 4543-4553.
40. Voloshin ON, Camerini-Otero RD, (2007) The DinG protein from Escherichia coli is a structure-specific helicase. J Biol Chem 282: 18437-18447.
41. Machwe A, Xiao L, Groden J, Matson SW, Orren DK, (2005) RecQ family members combine strand pairing and unwinding activities to catalyze strand exchange. J Biol Chem 280: 23397-23407.
42. Sharma S, Sommers JA, Choudhary S, Faulkner JK, Cui S, et al. (2005) Biochemical analysis of the DNA unwinding and strand annealing activities catalyzed by human RECQ1. J Biol Chem 280: 28072-28084.
43. Weinert BT, Rio DC, (2007) DNA strand displacement, strand annealing and strand swapping by the Drosophila Bloom's syndrome helicase. Nucleic Acids Res 35: 1367-1376.
44. Paques F, Haber JE, (1999) Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae. Microbiol Mol Biol Rev 63: 349-404.
45. Gupta R, Barkan D, Redelman-Sidi G, Shuman S, Glickman MS, (2011) Mycobacteria exploit three genetically distinct DNA double-strand break repair pathways. Mol Microbiol 79: 316-330.
46. Fishman-Lobell J, Rudin N, Haber JE, (1992) Two alternative pathways of double-strand break repair that are kinetically separable and independently modulated. Mol Cell Biol 12: 1292-1303.
47. Sayers EW, Barrett T, Benson DA, Bolton E, Bryant SH, et al. (2011) Database resources of the National Center for Biotechnology Information. Nucleic Acids Res 39: D38-51.
48. Ward JJ, Sodhi JS, McGuffin LJ, Buxton BF, Jones DT, (2004) Prediction and functional analysis of native disorder in proteins from the three kingdoms of life. J Mol Biol 337: 635-645.
49. Obradovic Z, Peng K, Vucetic S, Radivojac P, Dunker AK, (2005) Exploiting heterogeneous sequence properties improves prediction of protein disorder. Proteins 61 (Suppl 7): 176-182.
50. Jones DT, (1999) Protein secondary structure prediction based on position-specific scoring matrices. J Mol Biol 292: 195-202.
51. Arnold K, Bordoli L, Kopp J, Schwede T, (2006) The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22: 195-201.
52. Singleton MR, Scaife S, Wigley DB, (2001) Structural analysis of DNA replication fork reversal by RecG. Cell 107: 79-89.
53. Katoh K, Toh H, (2008) Recent developments in the MAFFT multiple sequence alignment program. Brief Bioinform 9: 286-298.
54. Waterhouse AM, Procter JB, Martin DM, Clamp M, Barton GJ, (2009) Jalview Version 2-a multiple sequence alignment editor and analysis workbench. Bioinformatics 25: 1189-1191.
55. DeLano WL, (2010) The PyMOL Molecular Graphics System, version 1.3. Schrödinger, LLC, New York.
56. Blattner FR, Plunkett G 3rd, Bloch CA, Perna NT, Burland V, et al. (1997) The complete genome sequence of Escherichia coli K-12. Science 277: 1453-1462.
57. Weel-Sneve R, Bjoras M, Kristiansen KI, (2008) Overexpression of the LexA-regulated tisAB RNA in E. coli inhibits SOS functions; implications for regulation of the SOS response. Nucleic Acids Res 36: 6249-6259.