Different quaternary structures of human RECQ1 are associated with its dual enzymatic activity

PLoS Biology

Volumn 5, Issue 2, 2007, Pages 0157-0168

  Muzzolini, Laura ^a   Beuron, Fabienne ^b,c   Patwardhan, Ardan ^b   Popuri, Venkateswarlu ^a   Cui, Sheng ^a,d   Niccolini, Benedetta ^a   Rappas, Mathieu ^b   Freemont, Paul S ^b   Vindigni, Alessandro ^a  

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

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

^c INSTITUTE OF CANCER RESEARCH   (United Kingdom)

^d UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

OLIGOMER; RECOMBINANT PROTEIN; RECQ HELICASE; SINGLE STRANDED DNA; DNA;

ARTICLE; ENZYME ACTIVITY; GEL PERMEATION CHROMATOGRAPHY; PROTEIN FUNCTION; PROTEIN QUATERNARY STRUCTURE; PROTEIN STRUCTURE; TRANSMISSION ELECTRON MICROSCOPY; BINDING COMPETITION; ELECTRON MICROSCOPY; GEL CHROMATOGRAPHY; HUMAN; METABOLISM;

BINDING, COMPETITIVE; CHROMATOGRAPHY, GEL; DNA; HUMANS; MICROSCOPY, ELECTRON; PROTEIN STRUCTURE, QUATERNARY; RECQ HELICASES;

EID: 33846941210     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.0050020     Document Type: Article

References (56)

1. Matson SW, Bean DW, George JW (1994) DNA helicases: Enzymes with essential roles in all aspects of DNA metabolism. Bioessays 16: 13-22.
2. Singleton MR, Wigley DB (2002) Modularity and specialization in superfamily 1 and 2 helicases. J Bacteriol 184: 1819-1826.
3. von Hippel PH (2004) Helicases become mechanistically simpler and functionally more complex. Nat Struct Mol Biol 11: 494-496.
4. Lohman TM, Bjornson KP (1996) Mechanisms of helicase-catalyzed DNA unwinding. Annu Rev Biochem 65: 169-214.
5. Soultanas P, Wigley DB (2001) Unwinding the 'Gordian knot' of helicase action. Trends Biochem Sci 26: 47-54.
6. Soultanas P, Wigley DB (2000) DNA helicases: 'Inching forward'. Curr Opin Struct Biol 10: 124-128.
7. Velankar SS, Soultanas P, Dillingham MS, Subramanya HS, Wigley DB (1999) Crystal structures of complexes of PcrA DNA helicase with a DNA substrate indicate an inchworm mechanism. Cell 97: 75-84.
8. Ha T, Rasnik I, Cheng W, Babcock HP, Gauss GH, et al. (2002) Initiation and re-initiation of DNA unwinding by the Escherichia coli Rep helicase. Nature 419: 638-641.
9. Maluf NK, Fischer CJ, Lohman TM (2003) A dimer of Escherichia coli UvrD is the active form of the helicase in vitro. J Mol Biol 325: 913-935.
10. Gai D, Zhao R, Li D, Finkielstein CV, Chen XS (2004) Mechanisms of conformational change for a replicative hexameric helicase of SV40 large tumor antigen. Cell 119: 47-60.
11. Patel SS, Picha KM (2000) Structure and function of hexameric helicases. Annu Rev Biochem 69: 651-697.
12. Yu X, Hingorani MM, Patel SS, Egelman EH (1996) DNA is bound within the central hole to one or two of the six subunits of the T7 DNA helicase. Nat Struct Biol 3: 740-743.
13. Hickson ID (2003) RecQ helicases: Caretakers of the genome. Nat Rev Cancer 3: 169-178.
14. Opresko PL, Cheng WH, Bohr VA (2004) Junction of RecQ helicase biochemistry and human disease. J Biol Chem 279: 18099-18102.
15. Ellis NA, Groden J, Ye TZ, Straughen J, Lennon DJ, et al. (1995) The Bloom's syndrome gene product is homologous to RecQ helicases. Cell 83: 655-666.
16. Kitao S, Lindor NM, Shiratori M, Furuichi Y, Shimamoto A (1999) Rothmund-Thomson syndrome responsible gene, RECQL4: Genomic structure and products. Genomics 61: 268-276.
17. Yu CE, Oshima J, Fu YH, Wijsman EM, Hisama F, et al. (1996) Positional cloning of the Werner's syndrome gene. Science 272: 258-262.
18. Constantinou A, Tarsounas M, Karow JK, Brosh RM, Bohr VA, et al. (2000) Werner's syndrome protein (WRN) migrates Holliday junctions and colocalizes with RPA upon replication arrest. EMBO Rep 1: 80-84.
19. Fry M, Loeb LA (1999) Human Werner syndrome DNA helicase unwinds tetrahelical structures of the fragile X syndrome repeat sequence d(CGG)n. J Biol Chem 274: 12797-12802.
20. Karow JK, Constantinou A, Li JL, West SC, Hickson ID (2000) The Bloom's syndrome gene product promotes branch migration of holliday junctions. Proc Natl Acad Sci U S A 97: 6504-6508.
21. Mohaghegh P, Karow JK, Brosh RM Jr, Bohr VA, Hickson ID (2001) The Bloom's and Werner's syndrome proteins are DNA structure-specific helicases. Nucleic Acids Res 29: 2843-2849.
22. Sun H, Bennett RJ, Maizels N (1999) The Saccharomyces cerevisiae Sgs1 helicase efficiently unwinds G-G paired DNAs. Nucleic Acids Res 27: 1978-1984.
23. Cheok CF, Wu L, Garcia PL, Janscak P, Hickson ID (2005) The Bloom's syndrome helicase promotes the annealing of complementary single-stranded DNA. Nucleic Acids Res 33: 3932-3941.
24. Garcia PL, Liu Y, Jiricny J, West SC, Janscak P (2004) Human RECQ5beta, a protein with DNA helicase and strand-annealing activities in a single polypeptide. EMBO J 23: 2882-2891.
25. 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.
26. Macris MA, 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.
27. 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.
28. Karow JK, Newman RH, Freemont PS, Hickson ID (1999) Oligomeric ring structure of the Bloom's syndrome helicase. Curr Biol 9: 597-600.
29. Janscak P, Garcia PL, Hamburger F, Makuta Y, Shiraishi K, et al. (2003) Characterization and mutational analysis of the RecQ core of the bloom syndrome protein. J Mol Biol 330: 29-42.
30. Cui S, Arosio D, Doherty KM, Brosh RM Jr, Falaschi A, et al. (2004) Analysis of the unwinding activity of the dimeric RECQ1 helicase in the presence of human replication protein A. Nucleic Acids Res 32: 2158-2170.
31. Huang S, Beresten S, Li B, Oshima J, Ellis NA, et al. (2000) Characterization of the human and mouse WRN 3′→5′ exonuclease. Nucleic Acids Res 28: 2396-2405.
32. Xue Y, Ratcliff GC, Wang H, Davis-Searles PR, Gray MD, et al. (2002) A minimal exonuclease domain of WRN forms a hexamer on DNA and possesses both 3′- 5′ exonuclease and 5′-protruding strand endonuclease activities. Biochemistry 41: 2901-2912.
33. Levin MK, Patel SS (1999) The helicase from hepatitis C virus is active as an oligomer. J Biol Chem 274: 31839-31846.
34. Eoff RL, Raney KD (2006) Intermediates revealed in the kinetic mechanism for DNA unwinding by a monomeric helicase. Nat Struct Mol Biol 13: 242-249.
35. Caruthers JM, McKay DB (2002) Helicase structure and mechanism. Curr Opin Struct Biol 12: 123-133.
36. Korolev S, Hsieh J, Gauss GH, Lohman TM, Waksman G (1997) Major domain swiveling revealed by the crystal structures of complexes of E. coli Rep helicase bound to single-stranded DNA and ADP. Cell 90: 635-647.
37. Sengoku T, Nureki O, Nakamura A, Kobayashi S, Yokoyama S (2006) Structural basis for RNA unwinding by the DEAD-box protein Drosophila Vasa. Cell 125: 287-300.
38. Brosh RM Jr, Matson SW (1995) Mutations in motif II of Escherichia coli DNA helicase II render the enzyme nonfunctional in both mismatch repair and excision repair with differential effects on the unwinding reaction. J Bacteriol 177: 5612-5621.
39. Hall MC, Matson SW (1999) Helicase motifs: The engine that powers DNA unwinding. Mol Microbiol 34: 867-877.
40. Lammens A, Schele A, Hopfner KP (2004) Structural biochemistry of ATP-driven dimerization and DNA-stimulated activation of SMC ATPases. Curr Biol 14: 1778-1782.
41. Bennett RJ, Keck JL (2004) Structure and function of RecQ DNA helicases. Crit Rev Biochem Mol Biol 39: 79-97.
42. Bernstein DA, Zittel MC, Keck JL (2003) High-resolution structure of the E. coli RecQ helicase catalytic core. EMBO J 22: 4910-4921.
43. Harmon FG, Kowalczykowski SC (2001) Biochemical characterization of the DNA helicase activity of the Escherichia coli RecQ helicase. J Biol Chem 276: 232-243.
44. Xu HQ, Deprez E, Zhang AH, Tauc P, Ladjimi MM, et al. (2003) The Escherichia coli RecQ helicase functions as a monomer. J Biol Chem 278: 34925-34933.
45. Choudhary S, Sommers JA, Brosh RM Jr (2004) Biochemical and kinetic characterization of the DNA helicase and exonuclease activities of werner syndrome protein. J Biol Chem 279: 34603-34613.
46. Zhang XD, Dou SX, Xie P, Hu JS, Wang PY, et al. (2006) Escherichia coli RecQ is a rapid, efficient, and monomeric helicase. J Biol Chem 281: 12655-12663.
47. Singleton MR, Wentzell LM, Liu Y, West SC, Wigley DB (2002) Structure of the single-strand annealing domain of human RAD52 protein. Proc Natl Acad Sci U S A 99: 13492-13497.
48. Wu L, Hickson ID (2003) The Bloom's syndrome helicase suppresses crossing over during homologous recombination. Nature 426: 870-874.
49. Wu L, Lung Chan K, Ralf C, Bernstein DA, Garcia PL, et al. (2005) The HRDC domain of BLM is required for the dissolution of double Holliday junctions. EMBO J 24: 2679-2687.
50. Wang W, Seki M, Narita Y, Nakagawa T, Yoshimura A, et al. (2003) Functional relation among RecQ family helicases RecQL1, RecQL5, and BLM in cell growth and sister chromatid exchange formation. Mol Cell Biol 23: 3527-3535.
51. Doherty KM, Sharma S, Uzdilla LA, Wilson TM, Cui S, et al. (2005) RECQ1 helicase interacts with human mismatch repair factors that regulate genetic recombination. J Biol Chem 280: 28085-28094.
52. Bjornson KP, Modrich P (2003) Differential and simultaneous adenosine diand triphosphate binding by MutS. J Biol Chem 278: 18557-18562.
53. van Heel M, Harauz G, Orlova EV, Schmidt R, Schatz M (1996) A new generation of the IMAGIC image processing system. J Struct Biol 116: 17-24.
54. van Heel M, Frank J (1981) Use of multivariate statistics in analysing the images of biological macromolecules. Ultramicroscopy 6: 187-194.
55. Van Heel M (1987) Angular reconstitution: A posteriori assignment of projection directions for 3D reconstruction. Ultramicroscopy 21: 111-123.
56. van Heel M, Schatz M (2005) Fourier shell correlation threshold criteria. J Struct Biol 151: 250-262.