A Conserved G4 DNA Binding Domain in RecQ Family Helicases

Journal of Molecular Biology

Volumn 358, Issue 4, 2006, Pages 1071-1080

  Huber, Michael D ^a   Duquette, Michelle L ^a   Shiels, Jerome C ^a   Maizels, Nancy ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Bloom syndrome; cancer; DNA binding domain; G quadruplex; genomic instability

Indexed keywords

DNA; HELICASE; RECQ HELICASE;

ARTICLE; BINDING AFFINITY; DNA BINDING; ENZYME ACTIVITY; GENE TARGETING; GENETIC DISORDER; GENOMIC INSTABILITY; HUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN FUNCTION;

EID: 33646100776     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2006.01.077     Document Type: Article

References (65)

1. Bachrati C.Z., and Hickson I.D. RecQ helicases: suppressors of tumorigenesis and premature aging. Biochem. J. 374 (2003) 577-606
2. Hickson I.D. RecQ helicases: caretakers of the genome. Nature Rev. Cancer 3 (2003) 169-178
3. Kaneko H., and Kondo N. Clinical features of Bloom syndrome and function of the causative gene, BLM helicase. Expert Rev. Mol. Diagn. 4 (2004) 393-401
4. Opresko P.L., Cheng W.H., and Bohr V.A. Junction of RecQ helicase biochemistry and human disease. J. Biol. Chem. 279 (2004) 18099-18102
5. Goss K.H., Risinger M.A., Kordich J.J., Sanz M.M., Straughen J.E., Slovek L.E., et al. Enhanced tumor formation in mice heterozygous for Blm mutation. Science 297 (2002) 2051-2053
6. Shimamoto A., Nishikawa K., Kitao S., and Furuichi Y. Human RecQ5beta, a large isomer of RecQ5 DNA helicase, localizes in the nucleoplasm and interacts with topoisomerases 3alpha and 3beta. Nucl. Acids Res. 28 (2000) 1647-1655
7. Jeong Y.S., Kang Y., Lim K.H., Lee M.H., Lee J., and Koo H.S. Deficiency of Caenorhabditis elegans RecQ5 homologue reduces life span and increases sensitivity to ionizing radiation. DNA Repair (Amst.) 2 (2003) 1309-1319
8. Wang W., Seki M., Narita Y., Nakagawa T., Yoshimura A., Otsuki M., et al. Functional relation among RecQ family helicases RecQL1, RecQL5, and BLM in cell growth and sister chromatid exchange formation. Mol. Cell. Biol. 23 (2003) 3527-3535
9. Garcia P.L., Liu Y., Jiricny J., West S.C., and Janscak P. Human RECQ5beta, a protein with DNA helicase and strand-annealing activities in a single polypeptide. EMBO J. 23 (2004) 2882-2891
10. Imamura O., Fujita K., Itoh C., Takeda S., Furuichi Y., and Matsumoto T. Werner and Bloom helicases are involved in DNA repair in a complementary fashion. Oncogene 21 (2002) 954-963
11. Du X., Shen J., Kugan N., Furth E.E., Lombard D.B., Cheung C., et al. Telomere shortening exposes functions for the mouse Werner and Bloom syndrome genes. Mol. Cell. Biol. 24 (2004) 8437-8446
12. Spillare, E. A., Wang, X. W., von Kobbe, C., Bohr, V. A., Hickson, I. D. & Harris, C. C. (2005). Redundancy of DNA helicases in p53-mediated apoptosis. Oncogene, E-pub ahead of print.
13. Cohen H., and Sinclair D.A. Recombination-mediated lengthening of terminal telomeric repeats requires the Sgs1 DNA helicase. Proc. Natl Acad. Sci. USA 98 (2001) 3174-3179
14. Huang P., Pryde F.E., Lester D., Maddison R.L., Borts R.H., Hickson I.D., and Louis E.J. SGS1 is required for telomere elongation in the absence of telomerase. Curr. Biol. 11 (2001) 125-129
15. Johnson F.B., Marciniak R.A., McVey M., Stewart S.A., Hahn W.C., and Guarente L. The Saccharomyces cerevisiae WRN homolog Sgs1p participates in telomere maintenance in cells lacking telomerase. EMBO J. 20 (2001) 905-913
16. Chang S., Multani A.S., Cabrera N.G., Naylor M.L., Laud P., Lombard D., et al. Essential role of limiting telomeres in the pathogenesis of Werner syndrome. Nature Genet. 36 (2004) 877-882
17. Crabbe L., Verdun R.E., Haggblom C.I., and Karlseder J. Defective telomere lagging strand synthesis in cells lacking WRN helicase activity. Science 306 (2004) 1951-1953
18. Opresko P.L., Otterlei M., Graakjaer J., Bruheim P., Dawut L., Kolvraa S., et al. The Werner syndrome helicase and exonuclease cooperate to resolve telomeric D loops in a manner regulated by TRF1 and TRF2. Mol. Cell. 14 (2004) 763-774
19. Laud P.R., Multani A.S., Bailey S.M., Wu L., Ma J., Kingsley C., et al. Elevated telomere-telomere recombination in WRN-deficient, telomere dysfunctional cells promotes escape from senescence and engagement of the ALT pathway. Genes Dev. 19 (2005) 2560-2570
20. Mandell J.G., Goodrich K.J., Bahler J., and Cech T.R. Expression of a RecQ helicase homolog affects progression through crisis in fission yeast lacking telomerase. J. Biol. Chem. 280 (2005) 5249-5257
21. Sinclair D.A., Mills K., and Guarente L. Accelerated aging and nucleolar fragmentation in yeast sgs1 mutants. Science 277 (1997) 1313-1316
22. Sinclair D.A., and Guarente L. Extrachromosomal rDNA circles-a cause of aging in yeast. Cell 91 (1997) 1033-1042
23. Marciniak R.A., Lombard D.B., Johnson F.B., and Guarente L. Nucleolar localization of the Werner syndrome protein in human cells. Proc. Natl Acad. Sci. USA 95 (1998) 6887-6892
24. Cobb J.A., Bjergbaek L., Shimada K., Frei C., and Gasser S.M. DNA polymerase stabilization at stalled replication forks requires Mec1 and the RecQ helicase Sgs1. EMBO J. 22 (2003) 4325-4336
25. Schawalder J., Paric E., and Neff N.F. Telomere and ribosomal DNA repeats are chromosomal targets of the bloom syndrome DNA helicase. BMC Cell Biol. 4 (2003) 15
26. Versini G., Comet I., Wu M., Hoopes L., Schwob E., and Pasero P. The yeast Sgs1 helicase is differentially required for genomic and ribosomal DNA replication. EMBO J. 22 (2003) 1939-1949
27. Weitao T., Budd M., and Campbell J.L. Evidence that yeast SGS1, DNA2, SRS2, and FOB1 interact to maintain rDNA stability. Mutat. Res. 532 (2003) 157-172
28. Kondo N., Motoyoshi F., Mori S., Kuwabara N., Orii T., and German J. Long-term study of the immunodeficiency of Bloom's syndrome. Acta Paediatr. 81 (1992) 86-90
29. Sun H., Karow J.K., Hickson I.D., and Maizels N. The Bloom's syndrome helicase unwinds G4 DNA. J. Biol. Chem. 273 (1998) 27587-27592
30. Sun H., Bennett R.J., and Maizels N. The Saccharomyces cerevisiae Sgs1 helicase efficiently unwinds G-G paired DNAs. Nucl. Acids Res. 27 (1999) 1978-1984
31. Wu X., and Maizels N. Substrate-specific inhibition of RecQ helicase. Nucl. Acids Res. 29 (2001) 1765-1771
32. Gellert M., Lipsett M.N., and Davies D.R. Helix formation by guanylic acid. Proc. Natl Acad. Sci. USA 48 (1962) 2013-2018
33. Sen D., and Gilbert W. Formation of parallel four-stranded complexes by guanine-rich motifs in DNA and its implications for meiosis. Nature 334 (1988) 364-366
34. Duquette M.L., Handa P., Vincent J.A., Taylor A.F., and Maizels N. Intracellular transcription of G-rich DNAs induces formation of G-loops, novel structures containing G4 DNA. Genes Dev. 18 (2004) 1618-1629
35. Duquette M.L., Pham P., Goodman M.F., and Maizels N. AID binds to transcription-induced structures in c-MYC that map to regions associated with translocation and hypermutation. Oncogene 24 (2005) 5791-5798
36. Schaffitzel C., Berger I., Postberg J., Hanes J., Lipps H.J., and Pluckthun A. In vitro generated antibodies specific for telomeric guanine-quadruplex DNA react with Stylonychia lemnae macronuclei. Proc. Natl Acad. Sci. USA 98 (2001) 8572-8577
37. Paeschke, K., Simonsson, T., Postberg, J., Rhodes, D. & Lipps, H. J. (2005). Telomere end-binding proteins control the formation of G-quadruplex DNA structures in vivo. Nature Struct. Mol. Biol. 12, 847-854.
38. Zaug A.J., Podell E.R., and Cech T.R. Human POT1 disrupts telomeric G-quadruplexes allowing telomerase extension in vitro. Proc. Natl Acad. Sci. USA 102 (2005) 10864-10869
39. Singleton M.R., and Wigley D.B. Modularity and specialization in superfamily 1 and 2 helicases. J. Bacteriol. 184 (2002) 1819-1826
40. Gorbalenya A.E., and Koonin E.V. Helicases: amino acid sequence comparisons and structure-function relationships. Curr. Opin. Struct. Biol. 3 (1993) 419-429
41. Bernstein D.A., and Keck J.L. Domain mapping of Escherichia coli RecQ defines the roles of conserved N- and C-terminal regions in the RecQ family. Nucl. Acids Res. 31 (2003) 2778-2785
42. Tanner N.K., Cordin O., Banroques J., Doere M., and Linder P. The Q motif: a newly identified motif in DEAD box helicases may regulate ATP binding and hydrolysis. Mol. Cell. 11 (2003) 127-138
43. Cordin O., Tanner N.K., Doere M., Linder P., and Banroques J. The newly discovered Q motif of DEAD-box RNA helicases regulates RNA-binding and helicase activity. EMBO J. 23 (2004) 2478-2487
44. von Kobbe C., Thoma N.H., Czyzewski B.K., Pavletich N.P., and Bohr V.A. Werner syndrome protein contains three structure-specific DNA binding domains. J. Biol. Chem. 278 (2003) 52997-53006
45. Lee J.W., Kusumoto R., Doherty K.M., Lin G.X., Zeng W., Cheng W.H., et al. Modulation of Werner syndrome protein function by a single mutation in the conserved RQC domain. J. Biol. Chem. 280 (2005) 39627-39636
46. Liu Z., Macias M.J., Bottomley M.J., Stier G., Linge J.P., Nilges M., et al. The three-dimensional structure of the HRDC domain and implications for the Werner and Bloom syndrome proteins. Struct. Fold. Des. 7 (1999) 1557-1566
47. Bernstein D.A., and Keck J.L. Conferring substrate specificity to DNA helicases: role of the RecQ HRDC domain. Structure (Camb) 13 (2005) 1173-1182
48. Huber M.D., Lee D.C., and Maizels N. GH DNA unwinding by BLM and Sgs1p: substrate specificity and substrate-specific inhibition. Nucl. Acids Res. 30 (2002) 3954-3961
49. Larson E.D., Duquette M.L., Cummings W.J., Streiff R.J., and Maizels N. MutSalpha binds to and promotes synapsis of transcriptionally activated immunoglobulin switch regions. Curr. Biol. 15 (2005) 470-474
50. Neff N.F., Ellis N.A., Ye T.Z., Noonan J., Huang K., Sanz M., and Proytcheva M. The DNA helicase activity of BLM is necessary for the correction of the genomic instability of bloom syndrome cells. Mol. Biol. Cell 10 (1999) 665-676
51. Bernstein D.A., Zittel M.C., and Keck J.L. High-resolution structure of the E. coli RecQ helicase catalytic core. EMBO J. 22 (2003) 4910-4921
52. Hanakahi L.A., Sun H., and Maizels N. High affinity interactions of nucleolin with G-G-paired rDNA. J. Biol. Chem. 274 (1999) 15908-15912
53. Dempsey L.A., Sun H., Hanakahi L.A., and Maizels N. G4 DNA binding by LR1 and its subunits, nucleolin and hnRNP D, A role for G-G pairing in immunoglobulin switch recombination. J. Biol. Chem. 274 (1999) 1066-1071
54. Cocco M.J., Hanakahi L.A., Huber M.D., and Maizels N. Specific interactions of distamycin with G-quadruplex DNA. Nucl. Acids Res. 31 (2003) 2944-2951
55. Anuradha S., and Muniyappa K. Saccharomyces cerevisiae Hop1 zinc finger motif is the minimal region required for its function in vitro. J. Biol. Chem. 279 (2004) 28961-28969
56. Lei M., Zaug A.J., Podell E.R., and Cech T.R. Switching human telomerase on and off with hPOT1 protein in vitro. J. Biol. Chem. 280 (2005) 20449-20456
57. Aravind L., Anantharaman V., Balaji S., Babu M.M., and Iyer L.M. The many faces of the helix-turn-helix domain: transcription regulation and beyond. FEMS Microbiol. Rev. 29 (2005) 231-262
58. Daniels D.S., Woo T.T., Luu K.X., Noll D.M., Clarke N.D., Pegg A.E., and Tainer J.A. DNA binding and nucleotide flipping by the human DNA repair protein AGT. Nature Struct. Mol. Biol. 11 (2004) 714-720
59. Wu L., Lung Chan K., Ralf C., Bernstein D.A., Garcia P.L., Bohr V.A., et al. The HRDC domain of BLM is required for the dissolution of double Holliday junctions. EMBO J. 24 (2005) 2679-2687
60. Bennett R.J., Keck J.L., and Wang J.C. Binding specificity determines polarity of DNA unwinding by the Sgs1 protein of S. cerevisiae. J. Mol. Biol. 289 (1999) 235-248
61. Janscak P., Garcia P.L., Hamburger F., Makuta Y., Shiraishi K., Imai Y., et al. Characterization and mutational analysis of the RecQ core of the bloom syndrome protein. J. Mol. Biol. 330 (2003) 29-42
62. Appella E., and Anderson C.W. Post-translational modifications and activation of p53 by genotoxic stresses. Eur. J. Biochem. 268 (2001) 2764-2772
63. Macris, M. A., Krejci, L., Bussen, W., Shimamoto, A. & Sung, P. (2005). Biochemical characterization of the RECQ4 protein, mutated in Rothmund-Thomson syndrome. DNA Repair (Amst.), 5, 172-180.
64. Kitao S., Ohsugi I., Ichikawa K., Goto M., Furuichi Y., and Shimamoto A. Cloning of two new human helicase genes of the RecQ family: biological significance of multiple species in higher eukaryotes. Genomics 54 (1998) 443-452
65. Karow J.K., Chakraverty R.K., and Hickson I.D. The Bloom's syndrome gene product is a 3′-5′ DNA helicase. J. Biol. Chem. 272 (1997) 30611-30614