High-resolution structure of the E.coli RecQ helicase catalytic core

EMBO Journal

Volumn 22, Issue 19, 2003, Pages 4910-4921

  Bernstein, Douglas A ^a   Zittel, Morgan C ^a   Keck, James L ^a  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

Helicase; RecQ; Structure; Winged helix; Zn2+ binding

Indexed keywords

ADENOSINE TRIPHOSPHATE DERIVATIVE; BACTERIAL DNA; DNA TOPOISOMERASE; DNA TOPOISOMERASE 3; HELICASE; RECQ HELICASE; UNCLASSIFIED DRUG; ZINC ION;

ARTICLE; BACTERIAL CELL; BACTERIAL GENE; BLOOM SYNDROME; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME BINDING; ENZYME MECHANISM; ENZYME STRUCTURE; ESCHERICHIA COLI; EUKARYOTIC CELL; GENE MUTATION; GENOME; METAL BINDING; MISSENSE MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN MOTIF; RECQ GENE;

ADENOSINE TRIPHOSPHATASES; AMINO ACID SEQUENCE; CATALYTIC DOMAIN; DNA HELICASES; ESCHERICHIA COLI; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; PROTEIN STRUCTURE, TERTIARY; RECQ HELICASES;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; EUKARYOTA;

EID: 0141865522     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/cdg500     Document Type: Article

References (74)

1. Bahr, A., De Graeve, F., Kedinger, C. and Chatton, B. (1998) Point mutations causing Bloom's syndrome abolish ATPase and DNA helicase activities of the BLM protein. Oncogene, 17, 2565-2571.
2. Barakat, A., Ababou, M., Onclercq, R., Dutertre, S., Chadli, E., Hda, N., Benslimane, A. and Amor-Gueret, M. (2000) Identification of a novel BLM missense mutation (2706T>C) in a Moroccan patient with Bloom's syndrome. Hum. Mutat., 15, 584-585.
3. Berg, J.M. and Shi, Y. (1996) The galvanization of biology: a growing appreciation for the roles of zinc. Science, 271, 1081-1085.
4. Bernstein, D.A. and Keck, J.L. (2003) Domain mapping of Escherichia coli RecQ defines the roles of conserved amino- and carboxyl-terminal regions in the RecQ family. Nucleic Acids Res., 31, 2778-2785.
5. Caruthers, J.M., Johnson, E.R. and McKay, D.B. (2000) Crystal structure of yeast initiation factor 4A, a DEAD-box RNA helicase. Proc. Natl Acad. Sci. USA, 97, 13080-13085.
6. Caruthers, J.M. and McKay, D.B. (2002) Helicase structure and mechanism. Curr. Opin. Struct. Biol., 12, 123-133.
7. Champoux, J.J. (2001) DNA topoisomerases: structure, function and mechanism. Annu. Rev. Biochem., 70, 369-413.
8. Cobb, J.A., Bjergbaek, L. and Gasser, S.M. (2002) RecQ helicases: at the heart of genetic stability. FEBS Lett., 529, 43-48.
9. Courcelle, J., Carswell-Crumpton, C. and Hanawalt, P.C. (1997) recF and recR are required for the resumption of replication at DNA replication forks in Escherichia coli. Proc. Natl Acad. Sci. USA, 94, 3714-3719.
10. Courcelle, J., Crowley, D.J. and Hanawalt, P.C. (1999) Recovery of DNA replication in UV-irradiated Escherichia coli requires both excision repair and recF protein function. J. Bacteriol., 181, 916-922.
11. Courcelle, J., Donaldson, J.R., Chow, K.H. and Courcelle, C.T. (2003) DNA damage-induced replication fork regression and processing in Escherichia coli. Science, 299, 1064-1067.
12. Courcelle, J. and Hanawalt, P.C. (1999) RecQ and RecJ process blocked replication forks prior to the resumption of replication in UV-irradiated Escherichia coli. Mol. Gen. Genet., 262, 543-551.
13. Cowtan, K. (1994) Joint CCP4 ESF-EACBM Newsletter. Protein Crystallogr., 31, 34.
14. DiGate, R.J. and Marians, K.J. (1988) Identification of a potent decatenating enzyme from Escherichia coli. J. Biol. Chem., 263, 13366-13373.
15. Ellis, N.A., Groden, J., Ye, T.Z., Straughen, J., Lennon, D.J., Ciocci, S., Proytcheva, M. and German, J. (1995) The Bloom's syndrome gene product is homologous to RecQ helicases. Cell, 83, 655-666.
16. Foucault, F., Vaury, C., Barakat, A., Thibout, D., Planchon, P., Jaulin, C., Praz, F. and Amor-Gueret, M. (1997) Characterization of a new BLM mutation associated with a topoisomerase II alpha defect in a patient with Bloom's syndrome. Hum. Mol. Genet., 6, 1427-1434.
17. Gajiwala, K.S. and Burley, S.K. (2000) Winged helix proteins. Curr. Opin. Struct. Biol., 10, 110-116.
18. Gangloff, S., McDonald, J.P., Bendixen, C., Arthur, L. and Rothstein, R. (1994) The yeast type I topoisomerase Top3 interacts with Sgs1, a DNA helicase homolog: a potential eukaryotic reverse gyrase. Mol. Cell Biol., 14, 8391-8398.
19. Gorbalenya, A.E. and Koonin, E.V. (1993) Helicases: amino acid sequence comparisons and structure-function relationships. Curr. Opin. Struct. Biol., 3, 419-429.
20. Hanada, K., Ukita, T., Kohno, Y., Saito, K., Kato, J. and Ikeda, H. (1997) RecQ DNA helicase is a suppressor of illegitimate recombination in Escherichia coli. Proc. Natl Acad. Sci. USA, 94, 3860-3865.
21. Harmon, F.G., DiGate, R.J. and Kowalczykowski, S.C. (1999) RecQ helicase and topoisomerase III comprise a novel DNA strand passage function: a conserved mechanism for control of DNA recombination. Mol. Cell, 3, 611-620.
22. Harmon, F.G. and Kowalczykowski, S.C. (1998) RecQ helicase, in concert with RecA and SSB proteins, initiates and disrupts DNA recombination. Genes Dev., 12, 1134-1144.
23. Harmon, F.G. and Kowalczykowski, S.C. (2001) Biochemical characterization of the DNA helicase activity of the Escherichia coli RecQ helicase. J. Biol. Chem., 276, 232-243.
24. Holm, L. and Sander, C. (1993) Protein structure comparison by alignment of distance matrices. J. Mol. Biol. 233, 123-138.
25. 2+ release from Escherichia coli aspartate transcarbamoylase. J. Biol. Chem., 259, 14793-14803.
26. Janscak, P., Garcia, P.L., Hamburger, F., Makuta, Y., Shiraishi, K., Imai, Y., Ikeda, H. and Bickle, T.A. (2003) Characterization and mutational analysis of the RecQ core of the Bloom syndrome protein. J. Mol. Biol., 330, 29-42.
27. Jones, T.A., Zou, J.Y., Cowan, S.W. and Kjeldgaard, M. (1991) Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr. D, 47, 110-119.
28. Kabsch, W. (1988) Evaluation of single-crystal X-ray diffraction from a position sensitive detector. J. Appl. Crystallogr., 21, 916-924.
29. Karow, J.K., Newman, R.H., Freemont, P.S. and Hickson, I.D. (1999) Oligomeric ring structure of the Bloom's syndrome helicase. Curr. Biol., 9, 597-600.
30. Karow, J.K., Wu, L. and Hickson, I.D. (2000) RecQ family helicases: roles in cancer and aging. Curr. Opin. Genet. Dev., 10, 32-38.
31. Kawasaki, K., Maruyama, S., Nakayama, M., Matsumoto, K. and Shibata, T. (2002) Drosophila melanogaster RECQ5/QE DNA helicase: stimulation by GTP binding. Nucleic Acids Res., 30, 3682-3691.
32. Kim, J.L., Morgenstern, K.A., Griffith, J.P., Dwyer, M.D., Thomson, J.A., Murcko, M.A., Lin, C. and Caron, P.R. (1998) Hepatitis C virus NS3 RNA helicase domain with a bound oligonucleotide: the crystal structure provides insights into the mode of unwinding. Structure, 6, 89-100.
33. Kitao, S., Shimamoto, A., Goto, M., Miller, R.W., Smithson, W.A., Lindor, N.M. and Furuichi, Y. (1999) Mutations in RECQL4 cause a subset of cases of Rothmund-Thomson syndrome. Nat. Genet., 22, 82-84.
34. Korolev, S., Hsieh, J., Gauss, G.H., Lohman, T.M. and Waksman, G. (1997) Major domain swivelling revealed by the crystal structures of complexes of E. coli Rep helicase bound to single-stranded DNA and ADP. Cell, 90, 635-647.
35. Kowalczykowski, S.C., Dixon, D.A., Eggleston, A.K., Lauder, S.D. and Rehrauer, W.M. (1994) Biochemistry of homologous recombination in Escherichia coli. Microbiol. Rev., 58, 401-465.
36. Krishna, S.S., Majumdar, I. and Grishin, N.V. (2003) Structural classification of zinc fingers. Nucleic Acids Res., 31, 532-550.
37. Lamzin, V.S. and Wilson, K.S. (1993) Automated refinement of protein models. Acta Cryst. D, 49, 129-147.
38. Leslie, A.G.W. (1992) Newsletter on Protein Crystallography No. 26, Daresbury Laboratory.
39. Lima, C.D., Wang, J.C. and Mondragon, A. (1994) Three-dimensional structure of the 67K N-terminal fragment of E. coli DNA topoisomerase I. Nature, 367, 138-146.
40. Liu, L.F. and Wang, J.C. (1987) Supercoiling of the DNA template during transcription. Proc. Natl Acad. Sci. USA, 84, 7024-7027.
41. Liu, Z., Macias, M.J., Bottomley, M.J., Stier, G., Linge, J.P., Nilges, M., Bork, P. and Sattler, M. (1999) The three-dimensional structure of the HRDC domain and implications for the Werner and Bloom syndrome proteins Structure, 7, 1557-1566.
42. Matsumoto, T., Imamura, O., Goto, M. and Furuichi, Y. (1998) Charaterization of the nuclear localization sequence in the DNA helicase involved in Werner's syndrome. Int. J. Mol. Med., 1, 71-76.
43. Matsumoto, T., Shimamoto, A., Goto, M. and Furuichi, Y. (1997) Impaired nuclear localization of defective DNA helicases in Werner's syndrome. Nat. Genet., 16, 335-336.
44. Mondragon, A. and DiGate, R. (1999) The structure of Escherichia coli DNA topoisomerase III. Struc. Fold Des., 7, 1373-1383.
45. Morozov, V., Mushegian, A.R., Koonin, E.V. and Bork, P. (1997) A putative nucleic acid-binding domain in Bloom's and Werner's syndrome helicases. Trends Biochem. Sci., 22, 417-418.
46. Mullen, J.R., Kaliraman, V. and Brill, S.J. (2000) Bipartite structure of the SGS1 DNA helicase in Saccharomyces cerevisiae. Genetics, 154, 1101-1114.
47. Mullen, J.R., Kaliraman, V., Ibrahim, S.S. and Brill, S.J. (2001) Requirement for three novel protein complexes in the absence of the Sgs1 DNA helicase in Saccharomyces cerevisiae. Genetics, 157, 103-118.
48. Murshudov, G.N., Vagin, A.A. and Dodson, E.J. (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D, 53, 240-255.
49. Nakayama, H., Nakayama, K., Nakayama, R., Irino, N., Nakayama, Y. and Hanawalt, P.C. (1984) Isolation and genetic characterization of a thymineless death-resistant mutant of Escherichia coli K12: identification of a new mutation (recQ1) that blocks the RecF recombination pathway. Mol. Gen. Genet., 195, 474-480.
50. Navaza, J. (2001) Implementation of molecular replacement in AMoRe. Acta Crystallogr. D, 57, 1367-1372.
51. Nicholls, A., Sharp, K.A. and Honig, B. (1991) Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins, 11, 281-296.
52. Oakley, T.J. and Hickson, I.D. (2002) Defending genome integrity during S-phase: putative roles for RecQ helicases and topoisomerase III. DNA Repair (Amst.), 1, 175-207.
53. Onoda, F., Seki, M., Miyajima, A. and Enomoto, T. (2000) Elevation of sister chromatid exchange in Saccharomyces cerevisiae sgs1 disruptants and the relevance of the disruptants as a system to evaluate mutations in Bloom's syndrome gene. Mutat. Res., 459, 203-209.
54. Otwinowski, Z. (1991) Isomorphous Refinement and Anomalous Scattering. Proceedings of the CCP4 Study Weekend, 80-86.
55. Peter, B.J., Ullsperger, C., Hiasa, H., Marians, K.J. and Cozzarelli, N.R. (1998) The structure of supercoiled intermediates in DNA replication. Cell, 94, 819-827.
56. Riddles, P.W., Blakeley, R.L. and Zemer, B. (1983) Reassessment of Ellman's reagent. Methods Enzymol., 91, 49-60.
57. Rodriguez, A.C. and Stock, D. (2002) Crystal structure of reverse gyrase: insights into the positive supercoiling of DNA. EMBO J., 21, 418-426.
58. Rong, S.B., Valiaho, J. and Vihinen, M. (2000) Structural basis of Bloom syndrome (BS) causing mutations in the BLM helicase domain. Mol. Med., 6, 155-164.
59. Schneider, T.R. and Sheldrick, G.M. (2002) Substructure solution with SHELXD. Acta Crystallogr. D, 58, 1772-1779.
60. Schultz, S.C., Shields, G.C. and Steitz, T.A. (1991) Crystal structure of a CAP-DNA complex: the DNA is bent by 90 degrees. Science, 253, 1001-1007.
61. Singleton, M.R., Scaife, S. and Wigley, D.B. (2001) Structural analysis of DNA replication fork reversal by RecG. Cell, 107, 79-89.
62. Story, R.M., Li, H. and Abelson, J.N. (2001) Crystal structure of a DEAD box protein from the hyperthermophile Methanococcus jannaschii. Proc. Natl Acad. Sci. USA, 98, 1465-1470.
63. Subramanya, H.S., Bird, L.E., Brannigan, J.A. and Wigley, D.B. (1996) Crystal structure of a DExx box DNA helicase. Nature, 384, 379-383.
64. Ui, A., Satoh, Y., Onoda, F., Miyajima, A., Seki, M. and Enomoto, T. (2001) The N-terminal region of Sgs1, which interacts with Top3, is required for complementation of MMS sensitivity and suppression of hyper-recombination in sgs1 disruptants. Mol. Genet. Genomics, 265, 837-850.
65. Umezu, K., Nakayama, K. and Nakayama, H. (1990) Escherichia coli RecQ protein is a DNA helicase. Proc. Natl Acad. Sci. USA, 87, 5363-5367.
66. Van Duyne, G.D., Standaert, R.F., Karplus, P.A., Schreiber, S.L. and Clardy, J. (1993) Atomic structures of the human immunophilin FKBP-12 complexes with FK506 and rapamycin. J. Mol. Biol., 229, 105-124.
67. Velankar, S.S., Soultanas, P., Dillingham, M.S., Subramanya, H.S. and Wigley, D.B. (1999) Crystal structures of complexes of PcrA DNA helicase with a DNA substrate indicate an inchworm mechanism. Cell, 97, 75-84.
68. Wang, J.C. (2002) Cellular roles of DNA topoisomerases: a molecular perspective. Nat. Rev. Mol. Cell Biol., 3, 430-440.
69. Whitby, M.C. and Lloyd, R.G. (1998) Targeting Holliday junctions by the RecG branch migration protein of Escherichia coli. J. Biol. Chem., 273, 19729-19739.
70. Wu, L. and Hickson, I.D. (2001) RecQ helicases and topoisomerases: components of a conserved complex for the regulation of genetic recombination. Cell. Mol. Life Sci., 58, 894-901.
71. Wu, L. and Hickson, I.D. (2002) RecQ helicases and cellular responses to DNA damage. Mutat. Res., 509, 35-47.
72. Xu, H.Q., Deprez, E., Zhang, A.H., Tauc, P., Ladjimi, M.M., Brochon, J.-C., Auclair, C. and Xi, X.G. (2003) The Escherichia coli RecQ helicase functions as a monomer. J. Biol. Chem., (published on line, June 12, 2003).
73. Yao, N., Hesson, T., Cable, M., Hong, Z., Kwong, A.D., Le, H.V. and Weber, P.C. (1997) Structure of the hepatitis C virus RNA helicase domain. Nat. Struct. Biol., 4, 463-467.
74. Yu, C.E. et al. (1996) Positional cloning of the Werner's syndrome gene. Science, 272, 258-262.