The HRDC domain oppositely modulates the unwinding activity of E. coli RecQ helicase on duplex DNA and G-quadruplex

Abstract

RecQ family helicases are highly conserved from bacteria to humans and have essential roles in maintaining genome stability. Mutations in three human RecQ helicases cause severe diseases with the main features of premature aging and cancer predisposition. Most RecQ helicases shared a conserved domain arrangement which comprises a helicase core, an RecQ C-terminal domain, and an auxiliary element helicase and RNaseD C-terminal (HRDC) domain, the functions of which are poorly understood. In this study, we systematically characterized the roles of the HRDC domain in E. coli RecQ in various DNA transactions by single-molecule FRET. We found that RecQ repetitively unwinds the 3′-partial duplex and fork DNA with a moderate processivity and periodically patrols on the ssDNA in the 5′-partial duplex by translocation. The HRDC domain significantly suppresses RecQ activities in the above transactions. In sharp contrast, the HRDC domain is essential for the deep and long-time unfolding of the G4 DNA structure by RecQ. Based on the observations that the HRDC domain dynamically switches between RecA core- and ssDNA-binding modes after RecQ association with DNA, we proposed a model to explain the modulation mechanism of the HRDC domain. Our findings not only provide new insights into the activities of RecQ on different substrates but also highlight the novel functions of the HRDC domain in DNA metabolisms. RecQ family helicases are highly conserved from bacteria to humans and have essential roles in maintaining genome stability. Mutations in three human RecQ helicases cause severe diseases with the main features of premature aging and cancer predisposition. Most RecQ helicases shared a conserved domain arrangement which comprises a helicase core, an RecQ C-terminal domain, and an auxiliary element helicase and RNaseD C-terminal (HRDC) domain, the functions of which are poorly understood. In this study, we systematically characterized the roles of the HRDC domain in E. coli RecQ in various DNA transactions by single-molecule FRET. We found that RecQ repetitively unwinds the 3′-partial duplex and fork DNA with a moderate processivity and periodically patrols on the ssDNA in the 5′-partial duplex by translocation. The HRDC domain significantly suppresses RecQ activities in the above transactions. In sharp contrast, the HRDC domain is essential for the deep and long-time unfolding of the G4 DNA structure by RecQ. Based on the observations that the HRDC domain dynamically switches between RecA core- and ssDNA-binding modes after RecQ association with DNA, we proposed a model to explain the modulation mechanism of the HRDC domain. Our findings not only provide new insights into the activities of RecQ on different substrates but also highlight the novel functions of the HRDC domain in DNA metabolisms. RecQ family helicases play essential roles in genome integrity maintenance by processing a wide variety of DNA structures generated during DNA replication, repair, and recombination (1Brosh R.M. DNA helicases involved in DNA repair and their roles in cancer.Nat. Rev. Cancer. 2013; 13 (23842644): 542-55810.1038/nrc3560Crossref PubMed Scopus (196) Google Scholar, 2Vindigni A. Marino F. Gileadi O. Probing the structural basis of RecQ helicase function.Biophys. Chem. 2010; 149 (20392558): 67-7710.1016/j.bpc.2010.03.012Crossref PubMed Scopus (35) Google Scholar, 3Croteau D.L. Popuri V. Opresko P.L. Bohr V.A. Human RecQ helicases in DNA repair, recombination, and replication.Ann. Rev. Biochem. 2014; 83 83 (24606147): 519-55210.1146/annurev-biochem-060713-035428Crossref PubMed Scopus (302) Google Scholar). These proteins are conserved in both prokaryotes and eukaryotes (4Larsen N.B. Hickson I.D. RecQ helicases: Conserved guardians of genomic integrity.Adv. Exp. Med. Biol. 2013; 973 (23161011): 161-18410.1007/978-1-4614-5037-5_8Crossref Scopus (109) Google Scholar). In humans, there are five RecQ helicases: RecQ1, BLM, WRN, RecQ4, and RecQ5. Importantly, mutations in BLM, WRN, and RecQ4 genes cause Bloom, Werner, and Rothmund-Thompson syndromes, which are linked to profound developmental abnormalities and increased cancer risk (5Mohaghegh 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 (11433031): 2843-284910.1093/nar/29.13.2843Crossref PubMed Scopus (456) Google Scholar). Meanwhile, the latter two syndromes are also characterized by premature aging. In Escherichia coli, RecQ functions in the RecF recombination pathway to repair the ssDNA gaps and dsDNA breaks (6Handa 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 (19451222): 1234-124510.1101/gad.1780709Crossref PubMed Scopus (103) Google Scholar). E. coli RecQ is also involved in suppressing illegitimate recombination (7Hanada K. Ukita T. Kohno Y. Saito K. Kato J. Ikeda H. RecQ DNA helicase is a suppressor of illegitimate recombination in Escherichia coli.Proc. Natl. Acad. Sci. U. S. A. 1997; 94 (9108069): 3860-386510.1073/pnas.94.8.3860Crossref PubMed Scopus (236) Google Scholar), repairing stalled replication forks, and promoting the induction of SOS response (8Hishida T. Han Y.W. Shibata T. Kubota Y. Ishino Y. Iwasaki H. Shinagawa H. Role of the Escherichia coli RecQ DNA helicase in SOS signaling and genome stabilization at stalled replication forks.Genes Dev. 2004; 18 (15289460): 1886-189710.1101/gad.1223804Crossref PubMed Scopus (103) Google Scholar). The ability of RecQ family helicases to resolve complex DNA structures is associated with their architecture consisting of evolutionarily conserved domains (9Vindigni A. Hickson I.D. RecQ helicases: multiple structures for multiple functions?.HFSP J. 2009; 3 (19949442): 153-16410.2976/1.3079540Crossref PubMed Scopus (48) Google Scholar). First, a conserved helicase core is formed by two RecA domains that harbor the ATPase cleft and drive the 3′-5′ directed translocation on ssDNA. Second, the helicase core is followed by a RecQ C-terminal (RQC) domain, which contains a Zn2+ binding domain and a β-hairpin winged-helix domain. RQC is primarily responsible for substrate recognition and DNA unwinding. In addition, an auxiliary element, the helicase, and the RNaseD C-terminal (HRDC) domain, which is connected to RQC by a flexible linker, exist in some RecQ helicases, including E. coli RecQ, human BLM, and WRN. The primary and of the HRDC domain different and HRDC is in two human RecQ helicases substrate to DNA helicases: of the RecQ HRDC 13 PubMed Scopus Google Scholar, and of the HRDC domain from human syndrome Acids Res. 2010; PubMed Scopus Google Scholar, P. O. K. Y. E. J. Hickson I.D. Gileadi O. structure of the Bloom's syndrome helicase a for the HRDC domain in PubMed Scopus Google Scholar, A. A. Y. T. K. structure of the HRDC domain of human syndrome Biochem. 2010; PubMed Scopus Google Scholar, K. N. T. structure of the HRDC domain of human syndrome Biol. Chem. PubMed Scopus Google Scholar, P. The structure of the HRDC domain and for the and syndrome PubMed Scopus Google Scholar). These the functions of HRDC in the various DNA transactions of RecQ family helicases, on and In the duplex DNA activities of RecQ family helicases have that human unwinds duplex DNA in a highly by between and modes P. T. helicase DNA and J. 2009; PubMed Scopus Google Scholar, S. Y. and an of the Acids Res. PubMed Scopus Google Scholar). have also in RecQ helicases, human P. O. of helicase core ssDNA during DNA PubMed Scopus Google Scholar, S. H. H. J. K. T. J. Bohr V.A. S. syndrome a Acids Res. PubMed Scopus Google Scholar), F. A. H. and activities of RecQ 2013; PubMed Scopus Google Scholar), and S. H. of DNA by the RecQ Acids Res. PubMed Scopus Google Scholar), that helicases a complex mechanism to duplex DNA the a complex dsDNA with Y. In J. V. K. Y. T. DNA and directed processing of by RecQ helicase of Natl. Acad. Sci. U. S. A. PubMed Scopus Google Scholar), and of two modes S. V. roles for E. coli RecQ DNA helicase domains and with Acids Res. PubMed Scopus Google for E. coli RecQ In addition, HRDC to the of ATPase in E. coli RecQ The HRDC domain of RecQ helicase DNA translocation and DNA PubMed Scopus Google Scholar). E. coli RecQ unwinds duplex DNA there is and the modulation mechanism of In to processing duplex DNA, DNA, and helicases in the RecQ E. coli RecQ, RecQ, human BLM, and WRN, also in G4 DNA structure Y. S. and mechanism for by RecQ PubMed Scopus Google Scholar). formed in DNA and are in including genomic DNA recombination, replication, and maintenance K. V.A. DNA and of Rev. 13 PubMed Scopus Google Scholar). and helicases on a wide of G4 structures with of unfolding and P. O. of helicase core ssDNA during DNA PubMed Scopus Google Scholar, H. Opresko P.L. Bohr V.A. S. a mechanism shared by Natl. Acad. Sci. U. S. A. PubMed Scopus Google Scholar, S. J. P. A. P. Hickson I.D. Gileadi O. E. into the of helicase with 2014; PubMed Scopus Google Scholar, in different structural different Acids Res. PubMed Scopus Google Scholar). the and roles of have in the E. coli genome N. O. in E. coli genome a conserved Acids Res. Google Scholar). the mechanism of E. coli RecQ on G4 and HRDC the G4 of RecQ, to In this study, we characterized the of E. coli RecQ on different DNA including 5′-partial fork DNA, and G4 DNA, and the roles of HRDC by single-molecule Our that RecQ repetitively unwinds the 3′-partial duplex and fork DNA with moderate RecQ is also to periodically on the ssDNA in 5′-partial DNA In addition, RecQ G4 structure in a and and G4 DNA in an for a we that HRDC the of RecQ on duplex DNA and G4 structure Based on we proposed to explain the different modulation mechanism of HRDC in different DNA transactions. The structures of the E. coli RecQ core structure of the E. coli RecQ helicase J. PubMed Scopus Google Scholar), RecQ core to DNA of DNA binding and in RecQ Natl. Acad. Sci. U. S. A. PubMed Scopus Google Scholar), and human to DNA with HRDC P. O. K. Y. E. J. Hickson I.D. Gileadi O. structure of the Bloom's syndrome helicase a for the HRDC domain in PubMed Scopus Google Scholar, V. A. S. of human Bloom's syndrome helicase in complex with and duplex Biol. 2014; PubMed Scopus Google The HRDC domain is in both RecQ in BLM, the core and with both RecA domains P. O. K. Y. E. J. Hickson I.D. Gileadi O. structure of the Bloom's syndrome helicase a for the HRDC domain in PubMed Scopus Google Scholar, V. A. S. of human Bloom's syndrome helicase in complex with and duplex Biol. 2014; PubMed Scopus Google Scholar), that E. coli and RecQ the of HRDC in the of RecQ, in this study, we and the activities of E. coli RecQ to RecQ and which the HRDC domain on a of DNA substrates including 5′-partial fork DNA, and G4 which the ssDNA-binding ability of HRDC with a also to the of the between HRDC and ssDNA substrate to DNA helicases: of the RecQ HRDC 13 PubMed Scopus Google Scholar). into the mechanism of RecQ, we and the of HRDC at the single-molecule The substrate to a ssDNA at the of a duplex and by the and at the of the and the the at and the of RecQ, the between and in steps and the association and of RecQ. HRDC is connected to the of RecQ a and flexible the of with the RecA core the ssDNA of the DNA In we the HRDC domain in RecQ by a to and with different DNA substrates by F. Y. for of RecQ helicase with a in the single-molecule PubMed Scopus Google Scholar). We found that the HRDC domain with the helicase core and the in fork DNA and the the helicase core F. Y. for of RecQ helicase with a in the single-molecule PubMed Scopus Google Scholar). We the of HRDC on the of RecQ. The DNA binding in HRDC with the the of HRDC significantly in the binding of RecQ, with the from to an of we to the that the of in that in RecQ. In addition, the association to an at which an binding on DNA We also the helicase to DNA and the between two binding of RecQ, and the of and and followed the with the and is the three of RecQ is that RecQ to the DNA substrate The also on and new insights into by DNA Acids Res. 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RecQ helicase HRDC domains are essential for binding and of the structure for 2013; PubMed Scopus Google Scholar), E. coli RecQ to G4 poorly with to and a is for the RecA domains to the helicase the N. RecQ to of the G4 a G4 unfolding E. RecQ helicase HRDC domains are essential for binding and of the structure for 2013; PubMed Scopus Google Scholar). there are essential between two helicases, and we that E. coli RecQ is an helicase to the mechanism of HRDC RecQ family only have RecQ family different in for E. coli RecQ, E. P. The Escherichia coli RecQ helicase functions a Biol. Chem. PubMed Scopus Google Scholar, P. Escherichia coli RecQ is a and Biol. Chem. PubMed Scopus Google found that is in to a of this is not by the of RecQ unwinds DNA a N. E. E. P. E. Escherichia coli RecQ helicase to DNA a Biol. Chem. 2010; PubMed Scopus Google and Kowalczykowski Y. In J. V. K. Y. T. DNA and directed processing of by RecQ helicase of Natl. Acad. Sci. U. S. A. PubMed Scopus Google both found that multiple E. coli RecQ to DNA on the In this study, we to the binding dsDNA and G4 we RecQ a to the single-molecule Y. In J. V. K. Y. T. DNA and directed processing of by RecQ helicase of Natl. Acad. Sci. U. S. A. PubMed Scopus Google Scholar, S. V. roles for E. coli RecQ DNA helicase domains and with Acids Res. PubMed Scopus Google Scholar). We have that the HRDC domain not only significantly the binding between RecQ and DNA substrate by with the RecA core and ssDNA but also the between different RecQ in DNA in the is the for the three helicases and Meanwhile, HRDC to on the we of the flexible linker, HRDC also to dynamically with the RecA core of RecQ to the of RecQ in DNA is also that multiple RecQ the duplex DNA and G4 DNA with the translocation at Our that HRDC suppresses the dsDNA of RecQ RecQ binding to In addition, HRDC significantly the of the duplex by RecQ with a moderate E. coli RecQ is a DNA recombination and repair helicase, the above observations that HRDC play a in the and RecQ the duplex in formed in the illegitimate recombination (7Hanada K. Ukita T. Kohno Y. Saito K. Kato J. Ikeda H. RecQ DNA helicase is a suppressor of illegitimate recombination in Escherichia coli.Proc. Natl. Acad. Sci. U. S. A. 1997; 94 (9108069): 3860-386510.1073/pnas.94.8.3860Crossref PubMed Scopus (236) Google Scholar). HRDC significantly RecQ binding to the G4 substrate and and long-time unfolding of G4 we that HRDC for some by RecQ repairing stalled replication by G4 N. O. in E. coli genome a conserved Acids Res. Google Scholar, S. Escherichia coli DNA structures during DNA J. PubMed Scopus Google Scholar). In that the auxiliary structural HRDC the activities of E. coli RecQ in processing different DNA structures by dynamically with the RecA core and ssDNA and new insights into the of RecQ during DNA replication, recombination, and The RecQ and in single-molecule and to the to DNA substrates from The and of the are in DNA in single-molecule DNA with a of and ssDNA G4 by the at for to in The in to the of to the The of the and in the and The duplex DNA in the DNA binding with a of the two The and of E. coli RecQ, and K. and HRDC structural in RecQ Biol. Chem. 2014; PubMed Scopus Google Scholar). we to E. coli RecQ RecQ In RecQ into the and in by at 18 for the by after by at RecQ by to and The by K. and HRDC structural in RecQ Biol. Chem. 2014; PubMed Scopus Google Scholar). The by the the of RecQ, and HRDC and RecQ contains is to the HRDC domain with a we on the flexible between the RQC and HRDC domains to a on H. A. a new for Chem. 2004; PubMed Scopus Google Scholar), in F. Y. for of RecQ helicase with a in the single-molecule PubMed Scopus Google Scholar). In with a and and by in and at for The and at The a to in PubMed Scopus Google Scholar). in RecQ and into the We an of for at a of the of DNA with a of at different and the to the of DNA The and the of the and including by in with to association with and from duplex and the in G4 The of and from with and of RecQ to DNA by at a of The DNA binding of the Escherichia coli RecQ Biol. Chem. 2004; PubMed Scopus (48) Google Scholar). DNA with in this of to a of binding to for and the The binding by the is the binding is the and is the are this and in the We at for with RecQ C-terminal helicase and RNaseD C-terminal single-molecule

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