Probing the structural basis of RecQ helicase function

Biophysical Chemistry

Volumn 149, Issue 3, 2010, Pages 67-77

  Vindigni, Alessandro ^a   Marino, Francesca ^a   Gileadi, Opher ^b  

^a INTERNATIONAL CENTRE FOR GENETIC ENGINEERING AND BIOTECHNOLOGY   (Italy)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

DNA repair; DNA replication; DNA strand annealing; DNA unwinding; Genome stability; RecQ helicases

Indexed keywords

EXONUCLEASE; RECQ HELICASE;

ATOMIC FORCE MICROSCOPY; CANCER SURVIVAL; CARBOXY TERMINAL SEQUENCE; CATALYSIS; CRYSTAL STRUCTURE; DNA DAMAGE; DNA RECOMBINATION; DNA REPLICATION; ENZYME ACTIVITY; EXCISION REPAIR; GENE MUTATION; GENOMIC INSTABILITY; HOMOLOGOUS RECOMBINATION; HUMAN; HYDROLYSIS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN MOTIF; REVIEW; SEQUENCE ALIGNMENT; SINGLE NUCLEOTIDE POLYMORPHISM;

DNA REPAIR; DNA REPLICATION; DNA, CRUCIFORM; GENOMIC INSTABILITY; HUMANS; PROTEIN STRUCTURE, TERTIARY; RECQ HELICASES;

EID: 77953024275     PISSN: 03014622     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bpc.2010.03.012     Document Type: Review

References (93)

1. Matson S.W., Bean D.W., George J.W. DNA helicases: enzymes with essential roles in all aspects of DNA metabolism. Bioessays 1994, 16:13-22.
2. Singleton M.R., Wigley D.B. Modularity and specialization in superfamily 1 and 2 helicases. J. Bacteriol. 2002, 184:1819-1826.
3. von Hippel P.H. Helicases become mechanistically simpler and functionally more complex. Nat. Struct. Mol. Biol. 2004, 11:494-496.
4. Lohman T.M., Tomko E.J., Wu C.G. Non-hexameric DNA helicases and translocases: mechanisms and regulation. Nat. Rev. Mol. Cell Biol. 2008, 9:391-401.
5. Singleton M.R., Dillingham M.S., Wigley D.B. Structure and mechanism of helicases and nucleic acid translocases. Annu. Rev. Biochem. 2007, 76:23-50.
6. Bachrati C.Z., Hickson I.D. RecQ helicases: guardian angels of the DNA replication fork. Chromosoma 2008, 117:219-233.
7. Bohr V.A. Rising from the RecQ-age: the role of human RecQ helicases in genome maintenance. Trends Biochem. Sci. 2008, 33:609-620.
8. Chu W.K., Hickson I.D. RecQ helicases: multifunctional genome caretakers. Nat. Rev. Cancer 2009, 9:644-654.
9. Hickson I.D. RecQ helicases: caretakers of the genome. Nat. Rev. Cancer 2003, 3:169-178.
10. Nakayama H., Nakayama K., Nakayama R., Irino N., Nakayama Y., Hanawalt P.C. 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. 1984, 195:474-480.
11. Ellis N.A., Groden J., Ye T.Z., Straughen J., Lennon D.J., Ciocci S., Proytcheva M., German J. The Bloom's syndrome gene product is homologous to RecQ helicases. Cell 1995, 83:655-666.
12. Kitao S., Lindor N.M., Shiratori M., Furuichi Y., Shimamoto A. Rothmund-thomson syndrome responsible gene, RECQL4: genomic structure and products. Genomics 1999, 61:268-276.
13. Siitonen H.A., Kopra O., Kaariainen H., Haravuori H., Winter R.M., Saamanen A.M., Peltonen L., Kestila M. Molecular defect of RAPADILINO syndrome expands the phenotype spectrum of RECQL diseases. Hum. Mol. Genet. 2003, 12:2837-2844.
14. Van Maldergem L., Siitonen H.A., Jalkh N., Chouery E., De Roy M., Delague V., Muenke M., Jabs E.W., Cai J., Wang L.L., Plon S.E., Fourneau C., Kestila M., Gillerot Y., Megarbane A., Verloes A. Revisiting the craniosynostosis-radial ray hypoplasia association: Baller-Gerold syndrome caused by mutations in the RECQL4 gene. J. Med. Genet. 2006, 43:148-152.
15. Yu C.E., Oshima J., Fu Y.H., Wijsman E.M., Hisama F., Alisch R., Matthews S., Nakura J., Miki T., Ouais S., Martin G.M., Mulligan J., Schellenberg G.D. Positional cloning of the Werner's syndrome gene. Science 1996, 272:258-262.
16. Li D., Frazier M., Evans D.B., Hess K.R., Crane C.H., Jiao L., Abbruzzese J.L. Single nucleotide polymorphisms of RecQ1, RAD54L, and ATM genes are associated with reduced survival of pancreatic cancer. J. Clin. Oncol. 2006, 24:1720-1728.
17. Fry M., Loeb L.A. Human werner syndrome DNA helicase unwinds tetrahelical structures of the fragile X syndrome repeat sequence d(CGG)n. J. Biol. Chem. 1999, 274:12797-12802.
18. Mohaghegh P., Karow J.K., Brosh R.M., Bohr V.A., Hickson I.D. The Bloom's and Werner's syndrome proteins are DNA structure-specific helicases. Nucleic Acids Res. 2001, 29:2843-2849.
19. Popuri V., Bachrati C.Z., Muzzolini L., Mosedale G., Costantini S., Giacomini E., Hickson I.D., Vindigni A. The Human RecQ helicases, BLM and RECQ1, display distinct DNA substrate specificities. J. Biol. Chem. 2008, 283:17766-17776.
20. Sun H., Bennett R.J., Maizels N. The Saccharomyces cerevisiae Sgs1 helicase efficiently unwinds G-G paired DNAs. Nucleic Acids Res. 1999, 27:1978-1984.
21. Sun H., Karow J.K., Hickson I.D., Maizels N. The Bloom's syndrome helicase unwinds G4 DNA. J. Biol. Chem. 1998, 273:27587-27592.
22. Constantinou A., Tarsounas M., Karow J.K., Brosh R.M., Bohr V.A., Hickson I.D., West S.C. Werner's syndrome protein (WRN) migrates Holliday junctions and co-localizes with RPA upon replication arrest. EMBO Rep. 2000, 1:80-84.
23. Karow J.K., Constantinou A., Li J.L., West S.C., Hickson I.D. The Bloom's syndrome gene product promotes branch migration of holliday junctions. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:6504-6508.
24. Cheok C.F., Wu L., Garcia P.L., Janscak P., Hickson I.D. The Bloom's syndrome helicase promotes the annealing of complementary single-stranded DNA. Nucleic Acids Res. 2005, 33:3932-3941.
25. Garcia P.L., Liu Y., Jiricny J., West S.C., Janscak P. Human RECQ5beta, a protein with DNA helicase and strand-annealing activities in a single polypeptide. Embo J. 2004, 23:2882-2891.
26. Machwe A., Xiao L., Groden J., Matson S.W., Orren D.K. RecQ family members combine strand pairing and unwinding activities to catalyze strand exchange. J. Biol. Chem. 2005, 280:23397-23407.
27. Macris M.A., Krejci L., Bussen W., Shimamoto A., Sung P. Biochemical characterization of the RECQ4 protein, mutated in Rothmund-Thomson syndrome. DNA Repair (Amst) 2006, 5:172-180.
28. Sharma S., Sommers J.A., Choudhary S., Faulkner J.K., Cui S., Andreoli L., Muzzolini L., Vindigni A., Brosh R.M. Biochemical analysis of the DNA unwinding and strand annealing activities catalyzed by human RECQ1. J. Biol. Chem. 2005, 280:28072-28084.
29. Huang S., Li B., Gray M.D., Oshima J., Mian I.S., Campisi J. The premature ageing syndrome protein, WRN, is a 3′->5′ exonuclease. Nat. Genet. 1998, 20:114-116.
30. Shen J.C., Gray M.D., Oshima J., Kamath-Loeb A.S., Fry M., Loeb L.A. Werner syndrome protein. I. DNA helicase and dna exonuclease reside on the same polypeptide. J. Biol. Chem. 1998, 273:34139-34144.
31. Ouyang K.J., Woo L.L., Ellis N.A. Homologous recombination and maintenance of genome integrity: cancer and aging through the prism of human RecQ helicases. Mech. Ageing Dev. 2008, 129:425-440.
32. Sharma S., Doherty K.M., Brosh R.M. Mechanisms of RecQ helicases in pathways of DNA metabolism and maintenance of genomic stability. Biochem. J. 2006, 398:319-337.
33. S. Thangavel, R. Mendoza-Maldonado, E. Tissino, J.M. Sidorova, J. Yin, W. Wang, R.J. Monnat, Jr., A. Falaschi, A. Vindigni, The human RECQ1 and RECQ4 helicases play distinct roles in DNA replication initiation, Mol. Cell. Biol. 30 (2010) 1382-1396.
34. Compton S.A., Tolun G., Kamath-Loeb A.S., Loeb L.A., Griffith J.D. The Werner syndrome protein binds replication fork and holliday junction DNAs as an oligomer. J. Biol. Chem. 2008, 283:24478-24483.
35. Karow J.K., Newman R.H., Freemont P.S., Hickson I.D. Oligomeric ring structure of the Bloom's syndrome helicase. Curr. Biol. 1999, 9:597-600.
36. Muftuoglu M., Kulikowicz T., Beck G., Lee J.W., Piotrowski J., Bohr V.A. Intrinsic ssDNA annealing activity in the C-terminal region of WRN. Biochemistry 2008, 47:10247-10254.
37. Muzzolini L., Beuron F., Patwardhan A., Popuri V., Cui S., Niccolini B., Rappas M., Freemont P.S., Vindigni A. Different quaternary structures of human RECQ1 are associated with its dual enzymatic activity. PLoS Biol. 2007, 5:e20.
38. Vindigni A., Hickson I.D. RecQ helicases: multiple structures for multiple functions?. Hfsp J. 2009, 3:153-164.
39. Gorbalenya A.E., Koonin E.V., Donchenko A.P., Blinov V.M. Two related superfamilies of putative helicases involved in replication, recombination, repair and expression of DNA and RNA genomes. Nucleic Acids Res. 1989, 17:4713-4730.
40. Zittel M.C., Keck J.L. Coupling DNA-binding and ATP hydrolysis in Escherichia coli RecQ: role of a highly conserved aromatic-rich sequence. Nucleic Acids Res. 2005, 33:6982-6991.
41. Buttner K., Nehring S., Hopfner K.P. Structural basis for DNA duplex separation by a superfamily-2 helicase. Nat. Struct. Mol. Biol. 2007, 14:647-652.
42. Bernstein D.A., Zittel M.C., Keck J.L. High-resolution structure of the E. coli RecQ helicase catalytic core. Embo J. 2003, 22:4910-4921.
43. Pike A.C., Shrestha B., Popuri V., Burgess-Brown N., Muzzolini L., Costantini S., Vindigni A., Gileadi O. Structure of the human RECQ1 helicase reveals a putative strand-separation pin. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:1039-1044.
44. Lee J.Y., Yang W. UvrD helicase unwinds DNA one base pair at a time by a two-part power stroke. Cell 2006, 127:1349-1360.
45. Velankar S.S., Soultanas P., Dillingham M.S., Subramanya H.S., Wigley D.B. Crystal structures of complexes of PcrA DNA helicase with a DNA substrate indicate an inchworm mechanism. Cell 1999, 97:75-84.
46. Saikrishnan K., Powell B., Cook N.J., Webb M.R., Wigley D.B. Mechanistic basis of 5′-3′ translocation in SF1B helicases. Cell 2009, 137:849-859.
47. Hopfner K.P., Michaelis J. Mechanisms of nucleic acid translocases: lessons from structural biology and single-molecule biophysics. Curr. Opin. Struct. Biol. 2007, 17:87-95.
48. Pyle A.M. Translocation and unwinding mechanisms of RNA and DNA helicases. Annu. Rev. Biophys. 2008, 37:317-336.
49. Bernstein D.A., Keck J.L. Domain mapping of Escherichia coli RecQ defines the roles of conserved N- and C-terminal regions in the RecQ family. Nucleic Acids Res. 2003, 31:2778-2785.
50. Tanner N.K., Cordin O., Banroques J., Doere M., Linder P. The Q motif: a newly identified motif in DEAD box helicases may regulate ATP binding and hydrolysis. Mol. Cell. 2003, 11:127-138.
51. Bahr A., De Graeve F., Kedinger C., Chatton B. Point mutations causing Bloom's syndrome abolish ATPase and DNA helicase activities of the BLM protein. Oncogene 1998, 17:2565-2571.
52. Onoda F., Seki M., Miyajima A., Enomoto T. 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. 2000, 459:203-209.
53. Hu J.S., Feng H., Zeng W., Lin G.X., Xi X.G. Solution structure of a multifunctional DNA- and protein-binding motif of human Werner syndrome protein. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:18379-18384.
54. K. Kitano, S.Y. Kim, T. Hakoshima, Structural basis for DNA strand separation by the unconventional winged-helix domain of RecQ helicase WRN, Structure 18 (2010) 177-187.
55. Guo R.B., Rigolet P., Zargarian L., Fermandjian S., Xi X.G. Structural and functional characterizations reveal the importance of a zinc binding domain in Bloom's syndrome helicase. Nucleic Acids Res. 2005, 33:3109-3124.
56. Janscak P., Garcia P.L., Hamburger F., Makuta Y., Shiraishi K., Imai Y., Ikeda H., Bickle T.A. Characterization and mutational analysis of the RecQ core of the bloom syndrome protein. J. Mol. Biol. 2003, 330:29-42.
57. Liu J.L., Rigolet P., Dou S.X., Wang P.Y., Xi X.G. The zinc finger motif of Escherichia coli RecQ is implicated in both DNA binding and protein folding. J. Biol. Chem. 2004, 279:42794-42802.
58. Berg J.M., Shi Y. The galvanization of biology: a growing appreciation for the roles of zinc. Science 1996, 271:1081-1085.
59. Daniels D.S., Woo T.T., Luu K.X., Noll D.M., Clarke N.D., Pegg A.E., Tainer J.A. DNA binding and nucleotide flipping by the human DNA repair protein AGT. Nat. Struct. Mol. Biol. 2004, 11:714-720.
60. Gajiwala K.S., Burley S.K. Winged helix proteins. Curr. Opin. Struct. Biol. 2000, 10:110-116.
61. Gajiwala K.S., Chen H., Cornille F., Roques B.P., Reith W., Mach B., Burley S.K. Structure of the winged-helix protein hRFX1 reveals a new mode of DNA binding. Nature 2000, 403:916-921.
62. Schultz S.C., Shields G.C., Steitz T.A. Crystal structure of a CAP-DNA complex: the DNA is bent by 90 degrees. Science 1991, 253:1001-1007.
63. Kim J.L., Morgenstern K.A., Griffith J.P., Dwyer M.D., Thomson J.A., Murcko M.A., Lin C., Caron P.R. Hepatitis C virus NS3 RNA helicase domain with a bound oligonucleotide: the crystal structure provides insights into the mode of unwinding. Structure 1998, 6:89-100.
64. Killoran M.P., Keck J.L. Three HRDC domains differentially modulate Deinococcus radiodurans RecQ DNA helicase biochemical activity. J. Biol. Chem. 2006, 281:12849-12857.
65. Bernstein D.A., Keck J.L. Conferring substrate specificity to DNA helicases: role of the RecQ HRDC domain. Structure 2005, 13:1173-1182.
66. Killoran M.P., Keck J.L. Structure and function of the regulatory C-terminal HRDC domain from Deinococcus radiodurans RecQ. Nucleic Acids Res. 2008, 36:3139-3149.
67. Kitano K., Yoshihara N., Hakoshima T. Crystal structure of the HRDC domain of human Werner syndrome protein, WRN. J. Biol. Chem. 2007, 282:2717-2728.
68. Liu Z., Macias M.J., Bottomley M.J., Stier G., Linge J.P., Nilges M., Bork P., Sattler M. The three-dimensional structure of the HRDC domain and implications for the Werner and Bloom syndrome proteins. Structure 1999, 7:1557-1566.
69. von Kobbe C., Thoma N.H., Czyzewski B.K., Pavletich N.P., Bohr V.A. Werner syndrome protein contains three structure-specific DNA binding domains. J. Biol. Chem. 2003, 278:52997-53006.
70. Wu L., Chan K.L., Ralf C., Bernstein D.A., Garcia P.L., Bohr V.A., Vindigni A., Janscak P., Keck J.L., Hickson I.D. The HRDC domain of BLM is required for the dissolution of double Holliday junctions. Embo J. 2005, 24:2679-2687.
71. Wu L., Hickson I.D. The Bloom's syndrome helicase suppresses crossing over during homologous recombination. Nature 2003, 426:870-874.
72. Mushegian A.R., Bassett D.E., Boguski M.S., Bork P., Koonin E.V. Positionally cloned human disease genes: patterns of evolutionary conservation and functional motifs. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:5831-5836.
73. Perry J.J., Yannone S.M., Holden L.G., Hitomi C., Asaithamby A., Han S., Cooper P.K., Chen D.J., Tainer J.A. WRN exonuclease structure and molecular mechanism imply an editing role in DNA end processing. Nat. Struct. Mol. Biol. 2006, 13:414-422.
74. Huang S., Beresten S., Li B., Oshima J., Ellis N.A., Campisi J. Characterization of the human and mouse WRN 3′->5′ exonuclease. Nucleic Acids Res. 2000, 28:2396-2405.
75. Xue Y., Ratcliff G.C., Wang H., Davis-Searles P.R., Gray M.D., Erie D.A., Redinbo M.R. A minimal exonuclease domain of WRN forms a hexamer on DNA and possesses both 3′-5′ exonuclease and 5′-protruding strand endonuclease activities. Biochemistry 2002, 41:2901-2912.
76. Cooper M.P., Machwe A., Orren D.K., Brosh R.M., Ramsden D., Bohr V.A. Ku complex interacts with and stimulates the Werner protein. Genes Dev. 2000, 14:907-912.
77. Li B., Comai L. Functional interaction between Ku and the werner syndrome protein in DNA end processing. J. Biol. Chem. 2000, 275:28349-28352.
78. Kagawa W., Kurumizaka H., Ishitani R., Fukai S., Nureki O., Shibata T., Yokoyama S. Crystal structure of the homologous-pairing domain from the human Rad52 recombinase in the undecameric form. Mol. Cell. 2002, 10:359-371.
79. Singleton M.R., Wentzell L.M., Liu Y., West S.C., Wigley D.B. Structure of the single-strand annealing domain of human RAD52 protein. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:13492-13497.
80. Kantake N., Madiraju M.V., Sugiyama T., Kowalczykowski S.C. Escherichia coli RecO protein anneals ssDNA complexed with its cognate ssDNA-binding protein: a common step in genetic recombination. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:15327-15332.
81. Leiros I., Timmins J., Hall D.R., McSweeney S. Crystal structure and DNA-binding analysis of RecO from Deinococcus radiodurans. Embo J. 2005, 24:906-918.
82. Makharashvili N., Koroleva O., Bera S., Grandgenett D.P., Korolev S. A novel structure of DNA repair protein RecO from Deinococcus radiodurans. Structure 2004, 12:1881-1889.
83. Handa N., Morimatsu K., Lovett S.T., Kowalczykowski S.C. Reconstitution of initial steps of dsDNA break repair by the RecF pathway of E. coli. Genes Dev. 2009, 23:1234-1245.
84. Sakai A., Cox M.M. RecFOR and RecOR as distinct RecA loading pathways. J. Biol. Chem. 2009, 284:3264-3272.
85. Lo Y.C., Paffett K.S., Amit O., Clikeman J.A., Sterk R., Brenneman M.A., Nickoloff J.A. Sgs1 regulates gene conversion tract lengths and crossovers independently of its helicase activity. Mol. Cell. Biol. 2006, 26:4086-4094.
86. Ariyoshi M., Nishino T., Iwasaki H., Shinagawa H., Morikawa K. Crystal structure of the holliday junction DNA in complex with a single RuvA tetramer. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:8257-8262.
87. Hargreaves D., Rice D.W., Sedelnikova S.E., Artymiuk P.J., Lloyd R.G., Rafferty J.B. Crystal structure of E. coli RuvA with bound DNA Holliday junction at 6 A resolution. Nat. Struct. Biol. 1998, 5:441-446.
88. Parsons C.A., Stasiak A., Bennett R.J., West S.C. Structure of a multisubunit complex that promotes DNA branch migration. Nature 1995, 374:375-378.
89. Rafferty J.B., Sedelnikova S.E., Hargreaves D., Artymiuk P.J., Baker P.J., Sharples G.J., Mahdi A.A., Lloyd R.G., Rice D.W. Crystal structure of DNA recombination protein RuvA and a model for its binding to the Holliday junction. Science 1996, 274:415-421.
90. Roe S.M., Barlow T., Brown T., Oram M., Keeley A., Tsaneva I.R., Pearl L.H. Crystal structure of an octameric RuvA-Holliday junction complex. Mol. Cell. 1998, 2:361-372.
91. Yamada K., Kunishima N., Mayanagi K., Ohnishi T., Nishino T., Iwasaki H., Shinagawa H., Morikawa K. Crystal structure of the Holliday junction migration motor protein RuvB from Thermus thermophilus HB8. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:1442-1447.
92. Yamada K., Miyata T., Tsuchiya D., Oyama T., Fujiwara Y., Ohnishi T., Iwasaki H., Shinagawa H., Ariyoshi M., Mayanagi K., Morikawa K. Crystal structure of the RuvA-RuvB complex: a structural basis for the Holliday junction migrating motor machinery. Mol. Cell. 2002, 10:671-681.
93. Holm L., Kaariainen S., Rosenstrom P., Schenkel A. Searching protein structure databases with DaliLite v.3. Bioinformatics 2008, 24:2780-2781.