Fork sensing and strand switching control antagonistic activities of RecQ helicases

Nature Communications

Volumn 4, Issue , 2013, Pages

  Klaue, Daniel ^a   Kobbe, Daniela ^b   Kemmerich, Felix ^a   Kozikowska, Alicja ^a   Puchta, Holger ^b   Seidel, Ralf ^a,c  

^a DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^b KARLSRUHE INSTITUTE OF TECHNOLOGY   (Germany)

^c UNIVERSITY OF MÜNSTER   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; RECQ HELICASE; SINGLE STRANDED DNA;

BIOACTIVITY; DICOTYLEDON; ENZYME ACTIVITY; FUNCTIONAL ROLE; GENE EXPRESSION; GENOMICS; MAGNETIC METHOD; SUBSTRATE;

ARABIDOPSIS THALIANA; ARTICLE; CELL ACTIVITY; CONTROLLED STUDY; DNA HAIRPIN; ENZYME ACTIVITY; GENE SWITCHING; NONHUMAN; OPTICAL TWEEZERS;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; DNA REPLICATION; DNA, PLANT; DNA, SINGLE-STRANDED; MODELS, BIOLOGICAL; NUCLEIC ACID CONFORMATION; RECQ HELICASES;

ARABIDOPSIS THALIANA; EUKARYOTA;

EID: 84879664794     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms3024     Document Type: Article

References (50)

1. Singh, D. K., Ghosh, A. K., Croteau, D. L. & Bohr, V. A. RecQ helicases in DNA double strand break repair and telomere maintenance. Mutat. Res. 736, 15-24 (2011).
2. Bernstein, K. A., Gangloff, S. & Rothstein, R. The RecQ DNA helicases in DNA repair. Annu. Rev. Genet. 44, 393-417 (2010).
3. Chu, W. K. & Hickson, I. D. RecQ helicases: multifunctional genome caretakers. Nat. Rev. Cancer. 9, 644-654 (2009).
4. Hartung, F. & Puchta, H. The RecQ gene family in plants. J. Plant. Physiol. 163, 287-296 (2006). (Pubitemid 43112083)
5. Hartung, F., Suer, S. & Puchta, H. Two closely related RecQ helicases have antagonistic roles in homologous recombination and DNA repair in Arabidopsis thaliana. Proc. Natl Acad. Sci. USA 104, 18836-18841 (2007). (Pubitemid 350210783)
6. Hartung, F., Suer, S., Knoll, A., Wurz-Wildersinn, R. & Puchta, H. Topoisomerase 3alpha and RMI1 suppress somatic crossovers and are essential for resolution of meiotic recombination intermediates in Arabidopsis thaliana. PLoS Genet. 4, e1000285 (2008).
7. Kobbe, D., Blanck, S., Demand, K., Focke, M. & Puchta, H. AtRECQ2, a RecQ helicase homologue from Arabidopsis thaliana, is able to disrupt various recombinogenic DNA structures in vitro. Plant J. 55, 397-405 (2008). (Pubitemid 352033350)
8. Kobbe, D., Blanck, S., Focke, M. & Puchta, H. Biochemical characterization of AtRECQ3 reveals significant differences relative to other RecQ helicases. Plant Physiol. 151, 1658-1666 (2009).
9. Dessinges, M. N., Lionnet, T., Xi, X. G., Bensimon, D. & Croquette, V. Singlemolecule assay reveals strand switching and enhanced processivity of UvrD. Proc. Natl Acad. Sci. USA 101, 6439-6444 (2004). (Pubitemid 38585992)
10. Johnson, D. S., Bai, L., Smith, B. Y., Patel, S. S. & Wang, M. D. Single-molecule studies reveal dynamics of DNA unwinding by the ring-shaped T7 helicase. Cell 129, 1299-1309 (2007). (Pubitemid 46962089)
11. Lionnet, T., Spiering, M. M., Benkovic, S. J., Bensimon, D. & Croquette, V. Real-time observation of bacteriophage T4 gp41 helicase reveals an unwinding mechanism. Proc. Natl Acad. Sci. USA 104, 19790-19795 (2007).
12. Seidel, R., Bloom, J. G. P., Dekker, C. & Szczelkun, M. D. Motor step size and ATP coupling efficiency of the dsDNA translocase EcoR124I. EMBO J. 27, 1388-1398 (2008). (Pubitemid 351655181)
13. Serebrov, V. & Pyle, A. M. Periodic cycles of RNA unwinding and pausing by hepatitis C virus NS3 helicase. Nature 430, 476-480 (2004). (Pubitemid 38987912)
14. Myong, S., Rasnik, I., Joo, C., Lohman, T. M. & Ha, T. Repetitive shuttling of a motor protein on DNA. Nature 437, 1321-1325 (2005). (Pubitemid 41568672)
15. Seidel, R. et al. Dynamics of initiation, termination and reinitiation of DNA translocation by the motor protein EcoR124I. EMBO J. 24, 4188-4197 (2005). (Pubitemid 41752887)
16. Yodh, J. G., Stevens, B. C., Kanagaraj, R., Janscak, P. & Ha, T. BLM helicase measures DNA unwound before switching strands and hRPA promotes unwinding reinitiation. EMBO J. 28, 405-416 (2009).
17. Park, J. et al. PcrA helicase dismantles RecA filaments by reeling in DNA in uniform steps. Cell 142, 544-555 (2010).
18. Tomko, E. J. et al. 50-Single-stranded/duplex DNA junctions are loading sites for E. coli UvrD translocase. EMBO J. 29, 3826-3839 (2010).
19. Klaue, D. & Seidel, R. Torsional stiffness of single superparamagnetic microspheres in an external magnetic field. Phys. Rev. Lett. 102, 028302 (2009).
20. Myong, S., Bruno, M. M., Pyle, A. M. & Ha, T. Spring-loaded mechanism of DNA unwinding by hepatitis C virus NS3 helicase. Science 317, 513-516 (2007). (Pubitemid 47196115)
21. Manosas, M., Xi, X. G., Bensimon, D. & Croquette, V. Active and passive mechanisms of helicases. Nucleic Acids Res. 38, 5518-5526 (2010).
22. Roy, R., Kozlov, A. G., Lohman, T. M. & Ha, T. SSB protein diffusion on singlestranded DNA stimulates RecA filament formation. Nature 461, 1092-1097 (2009).
23. Senavirathne, G. et al. Single-stranded DNA scanning and deamination by APOBEC3G cytidine deaminase at single molecule resolution. J. Biol. Chem. 287, 15826-15835 (2012).
24. 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 97, 75-84 (1999). (Pubitemid 29165891)
25. Kim, J. L. et al. 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 (1998). (Pubitemid 28084402)
26. Lee, J. Y. & Yang, W. UvrD helicase unwinds DNA one base pair at a time by a two-part power stroke. Cell 127, 1349-1360 (2006). (Pubitemid 44960421)
27. Singleton, M. R., Dillingham, M. S. & Wigley, D. B. Structure and mechanism of helicases and nucleic acid translocases. Annu. Rev. Biochem. 76, 23-50 (2007).
28. Saikrishnan, K., Powell, B., Cook, N. J., Webb, M. R. & Wigley, D. B. Mechanistic basis of 50-30 translocation in SF1B helicases. Cell 137, 849-859 (2009).
29. Pugh, R. A., Wu, C. G. & Spies, M. Regulation of translocation polarity by helicase domain 1 in SF2B helicases. EMBO J. 31, 503-514 (2012).
30. Brosh, R. M., Waheed, J. & Sommers, J. A. Biochemical characterization of the DNA substrate specificity of Werner syndrome helicase. J. Biol. Chem. 277, 23236-23245 (2002). (Pubitemid 34952151)
31. Cheng, W., Dumont, S., Tinoco, I. & Bustamante, C. NS3 helicase actively separates RNA strands and senses sequence barriers ahead of the opening fork. Proc. Natl Acad. Sci. USA 104, 13954-13959 (2007). (Pubitemid 350003319)
32. Ribeck, N., Kaplan, D. L., Bruck, I. & Saleh, O. A. DnaB helicase activity is modulated by DNA geometry and force. Biophys. J. 99, 2170-2179 (2010).
33. Manosas, M., Perumal, S. K., Croquette, V. & Benkovic, S. J. Direct observation of stalled fork restart via fork regression in the T4 replication system. Science 338, 1217-1220 (2012).
34. Kim, Y. M. & Choi, B. S. Structure and function of the regulatory HRDC domain from human Bloom syndrome protein. Nucleic Acids Res. 38, 7764-7777 (2010).
35. Kitano, K., Kim, S. Y. & Hakoshima, T. Structural basis for DNA strand separation by the unconventional winged-helix domain of RecQ helicase WRN. Structure 18, 177-187 (2010).
36. Vindigni, A., Marino, F. & Gileadi, O. Probing the structural basis of RecQ helicase function. Biophys. Chem. 149, 67-77 (2010).
37. Gyimesi, M. et al. Complex activities of the human Bloom's syndrome helicase are encoded in a core region comprising the RecA and Zn-binding domains. Nucleic Acids Res. 40, 3952-3963 (2012).
38. Vindigni, A. & Hickson, I. D. RecQ helicases: multiple structures for multiple functions? HFSP J 3, 153-164 (2009).
39. Lucic, B. et al. A prominent beta-hairpin structure in the winged-helix domain of RECQ1 is required for DNA unwinding and oligomer formation. Nucleic Acids Res. 39, 1703-1717 (2011).
40. Bugreev, D. V., Yu, X., Egelman, E. H. & Mazin, A. V. Novel pro-and antirecombination activities of the Bloom's syndrome helicase. Genes Dev. 21, 3085-3094 (2007). (Pubitemid 350223526)
41. Hu, Y. et al. RECQL5/Recql5 helicase regulates homologous recombination and suppresses tumor formation via disruption of Rad51 presynaptic filaments. Genes Dev. 21, 3073-3084 (2007). (Pubitemid 350223525)
42. Kanagaraj, R., Saydam, N., Garcia, P. L., Zheng, L. & Janscak, P. Human RECQ5beta helicase promotes strand exchange on synthetic DNA structures resembling a stalled replication fork. Nucleic Acids Res. 34, 5217-5231 (2006). (Pubitemid 44742486)
43. Islam, M. N. et al. A variant of the breast cancer type 2 susceptibility protein (BRC) repeat is essential for the RECQL5 helicase to interact with RAD51 recombinase for genome stabilization. J. Biol. Chem. 287, 23808-23818 (2012).
44. Dray, E., Siaud, N., Dubois, E. & Doutriaux, M. P. Interaction between Arabidopsis Brca2 and its partners Rad51, Dmc1, and Dss1. Plant Physiol. 140, 1059-1069 (2006). (Pubitemid 43956257)
45. Kobbe, D., Focke, M. & Puchta, H. Purification and characterization of RecQ helicases of plants. Methods Mol. Biol. 587, 195-209 (2010).
46. Luzzietti, N., Knappe, S., Richter, I. & Seidel, R. Nicking enzyme-based internal labeling of DNA at multiple loci. Nat. Protoc. 7, 643-653 (2012).
47. Brutzer, H., Schwarz, F. W. & Seidel, R. Scanning evanescent fields using a pointlike light source and a nanomechanical DNA gear. Nano. Lett. 12, 473-478 (2012).
48. Luzzietti, N. et al. Efficient preparation of internally modified single-molecule constructs using nicking enzymes. Nucleic Acids Res. 39, e15 (2011).
49. Brutzer, H., Luzzietti, N., Klaue, D. & Seidel, R. Energetics at the DNA supercoiling transition. Biophys. J. 98, 1267-1276 (2010).
50. Otto, O. et al. Real-time particle tracking at 10, 000 fps using optical fiber illumination. Opt. Exp. 18, 22722-22733 (2010).