Hrq1, a homolog of the human RecQ4 helicase, acts catalytically and structurally to promote genome integrity

Cell Reports

Volumn 6, Issue 2, 2014, Pages 346-356

  Bochman, Matthew L ^a,b   Paeschke, Katrin ^a,c   Chan, Angela ^a   Zakian, Virginia A ^a  

^a PRINCETON UNIVERSITY   (United States)

^b INDIANA UNIVERSITY   (United States)

^c UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

HELICASE; PROTEIN HRQ1; UNCLASSIFIED DRUG;

ARTICLE; CANCER INHIBITION; CATALYSIS; CONTROLLED STUDY; DNA CROSS LINKING; DNA STRAND BREAKAGE; ENZYME ACTIVITY; ENZYME STRUCTURE; GENOME; IN VIVO STUDY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; SEQUENCE HOMOLOGY; TELOMERE HOMEOSTASIS;

SACCHAROMYCETALES;

DNA BREAKS; GENOME, FUNGAL; GENOMIC INSTABILITY; PROTEIN BINDING; RECQ HELICASES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TELOMERE; TELOMERE HOMEOSTASIS;

EID: 84895900335     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2013.12.037     Document Type: Article

References (62)

1. Abdelhaleem M. Helicases: an overview. Methods Mol. Biol. 2010, 587:1-12.
2. Adelman C.A., Lolo R.L., Birkbak N.J., Murina O., Matsuzaki K., Horejsi Z., Parmar K., Borel V., Skehel J.M., Stamp G., et al. HELQ promotes RAD51 paralogue-dependent repair to avert germ cell loss and tumorigenesis. Nature 2013, 502:381-384.
3. Ashton T.M., Hickson I.D. Yeast as a model system to study RecQ helicase function. DNA Repair (Amst.) 2010, 9:303-314.
4. Averbeck D., Averbeck S. DNA photodamage, repair, gene induction and genotoxicity following exposures to 254nm UV and 8-methoxypsoralen plus UVA in a eukaryotic cell system. Photochem. Photobiol. 1998, 68:289-295.
5. Azvolinsky A., Giresi P.G., Lieb J.D., Zakian V.A. Highly transcribed RNA polymerase II genes are impediments to replication fork progression in Saccharomyces cerevisiae. Mol. Cell 2009, 34:722-734.
6. Barea F., Tessaro S., Bonatto D. In silico analyses of a new group of fungal and plant RecQ4-homologous proteins. Comput. Biol. Chem. 2008, 32:349-358.
7. Bernstein K.A., Gangloff S., Rothstein R. The RecQ DNA helicases in DNA repair. Annu. Rev. Genet. 2010, 44:393-417.
8. Bochman M.L., Schwacha A. Differences in the single-stranded DNA binding activities of MCM2-7 and MCM467: MCM2 and MCM5 define a slow ATP-dependent step. J.Biol. Chem. 2007, 282:33795-33804.
9. Boulé J.B., Vega L.R., Zakian V.A. The yeast Pif1p helicase removes telomerase from telomeric DNA. Nature 2005, 438:57-61.
10. Brabec V. DNA modifications by antitumor platinum and ruthenium compounds: their recognition and repair. Prog. Nucleic Acid Res. Mol. Biol. 2002, 71:1-68.
11. Brendel M., Bonatto D., Strauss M., Revers L.F., Pungartnik C., Saffi J., Henriques J.A. Role of PSO genes in repair of DNA damage of Saccharomyces cerevisiae. Mutat. Res. 2003, 544:179-193.
12. Capp C., Wu J., Hsieh T.S. RecQ4: the second replicative helicase?. Crit. Rev. Biochem. Mol. Biol. 2010, 45:233-242.
13. Cejka P., Kowalczykowski S.C. The full-length Saccharomyces cerevisiae Sgs1 protein is a vigorous DNA helicase that preferentially unwinds holliday junctions. J.Biol. Chem. 2010, 285:8290-8301.
14. Chisholm K.M., Aubert S.D., Freese K.P., Zakian V.A., King M.C., Welcsh P.L. A genomewide screen for suppressors of Alu-mediated rearrangements reveals a role for PIF1. PLoS ONE 2012, 7:e30748.
15. Choi D.H., Lee R., Kwon S.H., Bae S.H. Hrq1 functions independently of Sgs1 to preserve genome integrity in Saccharomyces cerevisiae. J.Microbiol. 2013, 51:105-112.
16. Clauson C., Scharer O.D., Niedernhofer L. Advances in understanding the complex mechanisms of DNA interstrand cross-link repair. Cold Spring Harbor perspectives in medicine 2013, 3:a012732.
17. Cromie G.A., Hyppa R.W., Smith G.R. The fission yeast BLM homolog Rqh1 promotes meiotic recombination. Genetics 2008, 179:1157-1167.
18. Daee D.L., Ferrari E., Longerich S., Zheng X.F., Xue X., Branzei D., Sung P., Myung K. Rad5-dependent DNA repair functions of the Saccharomyces cerevisiae FANCM protein homolog Mph1. J.Biol. Chem. 2012, 287:26563-26575.
19. Daee D.L., Myung K. Fanconi-like crosslink repair in yeast. Genome integrity 2012, 3:7.
20. Dittmar J.C., Pierce S., Rothstein R., Reid R.J. Physical and genetic-interaction density reveals functional organization and informs significance cutoffs in genome-wide screens. Proc. Natl. Acad. Sci. USA 2013, 110:7389-7394.
21. Frei C., Gasser S.M. The yeast Sgs1p helicase acts upstream of Rad53p in the DNA replication checkpoint and colocalizes with Rad53p in S-phase-specific foci. Genes Dev. 2000, 14:81-96.
22. Groocock L.M., Prudden J., Perry J.J., Boddy M.N. The RecQ4 orthologue Hrq1 is critical for DNA interstrand cross-link repair and genome stability in fission yeast. Mol. Cell. Biol. 2012, 32:276-287.
23. Hall B.M., Ma C.X., Liang P., Singh K.K. Fluctuation analysis CalculatOR: a web tool for the determination of mutation rate using Luria-Delbruck fluctuation analysis. Bioinformatics 2009, 25:1564-1565.
24. Henriques J.A., Moustacchi E. Interactions between mutations for sensitivity to psoralen photoaddition (pso) and to radiation (rad) in Saccharomyces cerevisiae. J.Bacteriol. 1981, 148:248-256.
25. Hiom K. Dna repair: Rad52 - the means to an end. Curr. Biol. 1999, 9:R446-R448.
26. Huang P., Pryde F.E., Lester D., Maddison R.L., Borts R.H., Hickson I.D., Louis E.J. SGS1 is required for telomere elongation in the absence of telomerase. Curr. Biol. 2001, 11:125-129.
27. Jin W., Liu H., Zhang Y., Otta S.K., Plon S.E., Wang L.L. Sensitivity of RECQL4-deficient fibroblasts from Rothmund-Thomson syndrome patients to genotoxic agents. Hum. Genet. 2008, 123:643-653.
28. Johnson F.B., Marciniak R.A., McVey M., Stewart S.A., Hahn W.C., Guarente L. The Saccharomyces cerevisiae WRN homolog Sgs1p participates in telomere maintenance in cells lacking telomerase. EMBO J. 2001, 20:905-913.
29. Kolodner R.D., Putnam C.D., Myung K. Maintenance of genome stability in Saccharomyces cerevisiae. Science 2002, 297:552-557.
30. Kwon S.H., Choi D.H., Lee R., Bae S.H. Saccharomyces cerevisiae Hrq1 requires a long 3'-tailed DNA substrate for helicase activity. Biochem. Biophys. Res. Commun. 2012, 427:623-628.
31. Larizza L., Roversi G., Volpi L. Rothmund-Thomson syndrome. Orphanet J. Rare Dis. 2010, 5:2.
32. Lee W., St Onge R.P., Proctor M., Flaherty P., Jordan M.I., Arkin A.P., Davis R.W., Nislow C., Giaever G. Genome-wide requirements for resistance to functionally distinct DNA-damaging agents. PLoS Genet. 2005, 1:e24.
33. Liao C., Hu B., Arno M.J., Panaretou B. Genomic screening invivo reveals the role played by vacuolar H+ ATPase and cytosolic acidification in sensitivity to DNA-damaging agents such as cisplatin. Mol. Pharmacol. 2007, 71:416-425.
34. Liu Y. Rothmund-Thomson syndrome helicase, RECQ4: on the crossroad between DNA replication and repair. DNA Repair (Amst.) 2010, 9:325-330.
35. Lydeard J.R., Lipkin-Moore Z., Jain S., Eapen V.V., Haber J.E. Sgs1 and exo1 redundantly inhibit break-induced replication and de novo telomere addition at broken chromosome ends. PLoS Genet. 2010, 6:e1000973.
36. 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.
37. Mao F.J., Sidorova J.M., Lauper J.M., Emond M.J., Monnat R.J. The human WRN and BLM RecQ helicases differentially regulate cell proliferation and survival after chemotherapeutic DNA damage. Cancer Res. 2010, 70:6548-6555.
38. Marrero V.A., Symington L.S. Extensive DNA end processing by exo1 and sgs1 inhibits break-induced replication. PLoS Genet. 2010, 6:e1001007.
39. Mirzaei H., Syed S., Kennedy J., Schmidt K.H. Sgs1 truncations induce genome rearrangements but suppress detrimental effects of BLM overexpression in Saccharomyces cerevisiae. J.Mol. Biol. 2011, 405:877-891.
40. Moldovan G.L., Madhavan M.V., Mirchandani K.D., McCaffrey R.M., Vinciguerra P., D'Andrea A.D. DNA polymerase POLN participates incross-link repair and homologous recombination. Mol. Cell. Biol. 2010, 30:1088-1096.
41. Myung K., Chen C., Kolodner R.D. Multiple pathways cooperate in the suppression of genome instability in Saccharomyces cerevisiae. Nature 2001, 411:1073-1076.
42. Myung K., Datta A., Chen C., Kolodner R.D. SGS1, the Saccharomyces cerevisiae homologue of BLM and WRN, suppresses genome instability and homeologous recombination. Nat. Genet. 2001, 27:113-116.
43. Paeschke K., Bochman M.L., Garcia P.D., Cejka P., Friedman K.L., Kowalczykowski S.C., Zakian V.A. Pif1 family helicases suppress genome instability at G-quadruplex motifs. Nature 2013, 497:458-462.
44. Putnam C.D., Kolodner R.D. Determination of gross chromosomal rearrangement rates. Cold Spring Harb. Protoc. 2010, Published online September 1, 2010. 10.1101/pdb.prot5492.
45. Runge K.W., Zakian V.A. Introduction of extra telomeric DNA sequences into Saccharomyces cerevisiae results in telomere elongation. Mol. Cell. Biol. 1989, 9:1488-1497.
46. Schärer O.D. DNA interstrand crosslinks: natural and drug-induced DNA adducts that induce unique cellular responses. ChemBioChem 2005, 6:27-32.
47. Schulz V.P., Zakian V.A. The saccharomyces PIF1 DNA helicase inhibits telomere elongation and de novo telomere formation. Cell 1994, 76:145-155.
48. Shin J.H., Kelman Z. DNA unwinding assay using streptavidin-bound oligonucleotides. BMC Mol. Biol. 2006, 7:43.
49. Sikorski R.S., Hieter P. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 1989, 122:19-27.
50. Singh D.K., Popuri V., Kulikowicz T., Shevelev I., Ghosh A.K., Ramamoorthy M., Rossi M.L., Janscak P., Croteau D.L., Bohr V.A. The human RecQ helicases BLM and RECQL4 cooperate to preserve genome stability. Nucleic Acids Res. 2012, 40:6632-6648.
51. Stavropoulos D.J., Bradshaw P.S., Li X., Pasic I., Truong K., Ikura M., Ungrin M., Meyn M.S. The Bloom syndrome helicase BLM interacts with TRF2 in ALT cells and promotes telomeric DNA synthesis. Hum. Mol. Genet. 2002, 11:3135-3144.
52. Studier F.W. Protein production by auto-induction in high density shaking cultures. Protein Expr. Purif. 2005, 41:207-234.
53. Suzuki T., Kohno T., Ishimi Y. DNA helicase activity in purified human RECQL4 protein. J.Biochem. 2009, 146:327-335.
54. Tang G., Peng L., Baldwin P.R., Mann D.S., Jiang W., Rees I., Ludtke S.J. EMAN2: an extensible image processing suite for electron microscopy. J.Struct. Biol. 2007, 157:38-46.
55. Teng S.-C., Zakian V.A. Telomere-telomere recombination is anefficient bypass pathway for telomere maintenance in Saccharomyces cerevisiae. Mol. Cell. Biol. 1999, 19:8083-8093.
56. Teng S.-C., Chang J., McCowan B., Zakian V.A. Telomerase-independent lengthening of yeast telomeres occurs by an abrupt Rad50p-dependent, Rif-inhibited recombinational process. Mol. Cell 2000, 6:947-952.
57. Tomasz M. Mitomycin C: small, fast and deadly (but very selective). Chem. Biol. 1995, 2:575-579.
58. Ward T.A., Dudášová Z., Sarkar S., Bhide M.R., Vlasáková D., Chovanec M., McHugh P.J. Components of a Fanconi-like pathway control Pso2-independent DNA interstrand crosslink repair in yeast. PLoS Genet. 2012, 8:e1002884.
59. Wellinger R.J., Zakian V.A. Everything you ever wanted to knowabout Saccharomyces cerevisiae telomeres: beginning to end. Genetics 2012, 191:1073-1105.
60. Wu Y., Brosh R.M. Helicase-inactivating mutations as a basis for dominant negative phenotypes. Cell Cycle 2010, 9:4080-4090.
61. Zhou J.-Q., Monson E.M., Teng S.-C., Schulz V.P., Zakian V.A. The Pif1p helicase, a catalytic inhibitor of telomerase lengthening of yeast telomeres. Science 2000, 289:771-774.
62. Zhu Z., Chung W.H., Shim E.Y., Lee S.E., Ira G. Sgs1 helicase and two nucleases Dna2 and Exo1 resect DNA double-strand break ends. Cell 2008, 134:981-994.