HLTF's Ancient HIRAN Domain Binds 3' DNA Ends to Drive Replication Fork Reversal

Molecular Cell

Volumn 58, Issue 6, 2015, Pages 1090-1100

  Kile, Andrew C ^a   Chavez, Diana A ^b   Bacal, Julien ^a   Eldirany, Sherif ^c   Korzhnev, Dmitry M ^c   Bezsonova, Irina ^c   Eichman, Brandt F ^b   Cimprich, Karlene A ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARRIER PROTEIN; HLTF PROTEIN; OLIGONUCLEOTIDE; OLIGOSACCHARIDE; RAD18 PROTEIN; SINGLE STRANDED DNA; UNCLASSIFIED DRUG; DNA; DNA BINDING PROTEIN; HLTF PROTEIN, HUMAN; PROTEIN BINDING; TRANSCRIPTION FACTOR;

ARTICLE; DNA DAMAGE; DNA REPLICATION; DNA STRUCTURE; IN VITRO STUDY; PROTEIN DNA BINDING; PROTEIN STRUCTURE; AMINO ACID SEQUENCE; BINDING SITE; BIOLOGICAL MODEL; CHEMICAL STRUCTURE; CHEMISTRY; CONFORMATION; GENETICS; HUMAN; METABOLISM; MOLECULAR GENETICS; MUTATION; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; NUCLEOTIDE SEQUENCE; PROTEIN TERTIARY STRUCTURE; RNA INTERFERENCE; SEQUENCE HOMOLOGY; TUMOR CELL LINE; WESTERN BLOTTING; X RAY CRYSTALLOGRAPHY;

AMINO ACID SEQUENCE; BASE SEQUENCE; BINDING SITES; BLOTTING, WESTERN; CELL LINE, TUMOR; CRYSTALLOGRAPHY, X-RAY; DNA; DNA REPLICATION; DNA, SINGLE-STRANDED; DNA-BINDING PROTEINS; HUMANS; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, GENETIC; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; NUCLEIC ACID CONFORMATION; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RNA INTERFERENCE; SEQUENCE HOMOLOGY, AMINO ACID; SEQUENCE HOMOLOGY, NUCLEIC ACID; TRANSCRIPTION FACTORS;

EID: 84937627613     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2015.05.013     Document Type: Article

References (46)

1. Achar Y.J., Balogh D., Haracska L. Coordinated protein and DNA remodeling by human HLTF on stalled replication fork. Proc. Natl. Acad. Sci. USA 2011, 108:14073-14078.
2. Alabert C., Bukowski-Wills J.-C., Lee S.-B., Kustatscher G., Nakamura K., de Lima Alves F., Menard P., Mejlvang J., Rappsilber J., Groth A. Nascent chromatin capture proteomics determines chromatin dynamics during DNA replication and identifies unknown fork components. Nat. Cell Biol. 2014, 16:281-293.
3. Bessho Y., Shibata R., Sekine S., Murayama K., Higashijima K., Hori-Takemoto C., Shirouzu M., Kuramitsu S., Yokoyama S. Structural basis for functional mimicry of long-variable-arm tRNA by transfer-messenger RNA. Proc. Natl. Acad. Sci. USA 2007, 104:8293-8298.
4. Bétous R., Mason A.C., Rambo R.P., Bansbach C.E., Badu-Nkansah A., Sirbu B.M., Eichman B.F., Cortez D. SMARCAL1 catalyzes fork regression and Holliday junction migration to maintain genome stability during DNA replication. Genes Dev. 2012, 26:151-162.
5. Bétous R., Couch F.B., Mason A.C., Eichman B.F., Manosas M., Cortez D. Substrate-selective repair and restart of replication forks by DNA translocases. Cell Rep. 2013, 3:1958-1969.
6. Bhattacharyya B., George N.P., Thurmes T.M., Zhou R., Jani N., Wessel S.R., Sandler S.J., Ha T., Keck J.L. Structural mechanisms of PriA-mediated DNA replication restart. Proc. Natl. Acad. Sci. USA 2014, 111:1373-1378.
7. Blastyák A., Pintér L., Unk I., Prakash L., Prakash S., Haracska L. Yeast Rad5 protein required for postreplication repair has a DNA helicase activity specific for replication fork regression. Mol. Cell 2007, 28:167-175.
8. Blastyák A., Hajdú I., Unk I., Haracska L. Role of double-stranded DNA translocase activity of human HLTF in replication of damaged DNA. Mol. Cell. Biol. 2010, 30:684-693.
9. Branzei D., Foiani M. Maintaining genome stability at the replication fork. Nat. Rev. Mol. Cell Biol. 2010, 11:208-219.
10. Choi K., Batke S., Szakal B., Lowther J., Hao F., Sarangi P., Branzei D., Ulrich H.D., Zhao X. Concerted and differential actions of two enzymatic domains underlie Rad5 contributions to DNA damage tolerance. Nucleic Acids Res. 2015, 43:2666-2677.
11. Ciccia A., Elledge S.J. The DNA damage response: making it safe to play with knives. Mol. Cell 2010, 40:179-204.
12. Ciccia A., Nimonkar A.V., Hu Y., Hajdu I., Achar Y.J., Izhar L., Petit S.A., Adamson B., Yoon J.C., Kowalczykowski S.C., et al. Polyubiquitinated PCNA recruits the ZRANB3 translocase to maintain genomic integrity after replication stress. Mol. Cell 2012, 47:396-409.
13. Ding L., Forsburg S.L. Essential domains of Schizosaccharomyces pombe Rad8 required for DNA damage response. G3 (Bethesda) 2014, 4:1373-1384.
14. Dong G., Nowakowski J., Hoffman D.W. Structure of small protein B: the protein component of the tmRNA-SmpB system for ribosome rescue. EMBO J. 2002, 21:1845-1854.
15. Dürr H., Körner C., Müller M., Hickmann V., Hopfner K.-P. X-ray structures of the Sulfolobus solfataricus SWI2/SNF2 ATPase core and its complex with DNA. Cell 2005, 121:363-373.
16. Follonier C., Oehler J., Herrador R., Lopes M. Friedreich's ataxia-associated GAA repeats induce replication-fork reversal and unusual molecular junctions. Nat. Struct. Mol. Biol. 2013, 20:486-494.
17. Gabbai C.B., Marians K.J. Recruitment to stalled replication forks of the PriA DNA helicase and replisome-loading activities is essential for survival. DNA Repair (Amst.) 2010, 9:202-209.
18. Gangavarapu V., Haracska L., Unk I., Johnson R.E., Prakash S., Prakash L. Mms2-Ubc13-dependent and -independent roles of Rad5 ubiquitin ligase in postreplication repair and translesion DNA synthesis in Saccharomyces cerevisiae. Mol. Cell. Biol. 2006, 26:7783-7790.
19. Hishiki A., Hara K., Ikegaya Y., Yokoyama H., Shimizu T., Sato M., Hashimoto H. Structure of a novel DNA-binding domain of helicase-like transcription factor (HLTF) and its functional implication in DNA damage tolerance. J. Biol. Chem. 2015, Published online April 9, 2015. 10.1074/jbc.M115.643643.
20. Hoege C., Pfander B., Moldovan G.L., Pyrowolakis G., Jentsch S. RAD6-dependent DNA repair is linked to modification of PCNA by ubiquitin and SUMO. Nature 2002, 419:135-141.
21. Iyer L.M., Babu M.M., Aravind L. The HIRAN domain and recruitment of chromatin remodeling and repair activities to damaged DNA. Cell Cycle 2006, 5:775-782.
22. Jackson D.A., Pombo A. Replicon clusters are stable units of chromosome structure: evidence that nuclear organization contributes to the efficient activation and propagation of S phase in human cells. J. Cell Biol. 1998, 140:1285-1295.
23. Jones J.M., Nakai H. Duplex opening by primosome protein PriA for replisome assembly on a recombination intermediate. J. Mol. Biol. 1999, 289:503-516.
24. Krijger P.H.L., Lee K.-Y., Wit N., van den Berk P.C.M., Wu X., Roest H.P., Maas A., Ding H., Hoeijmakers J.H.J., Myung K., Jacobs H. HLTF and SHPRH are not essential for PCNA polyubiquitination, survival and somatic hypermutation: existence of an alternative E3 ligase. DNA Repair (Amst.) 2011, 10:438-444.
25. Lin J.-R., Zeman M.K., Chen J.-Y., Yee M.-C., Cimprich K.A. SHPRH and HLTF act in a damage-specific manner to coordinate different forms of postreplication repair and prevent mutagenesis. Mol. Cell 2011, 42:237-249.
26. Ma J.-B., Ye K., Patel D.J. Structural basis for overhang-specific small interfering RNA recognition by the PAZ domain. Nature 2004, 429:318-322.
27. Mason A.C., Rambo R.P., Greer B., Pritchett M., Tainer J.A., Cortez D., Eichman B.F. A structure-specific nucleic acid-binding domain conserved among DNA repair proteins. Proc. Natl. Acad. Sci. USA 2014, 111:7618-7623.
28. Minca E.C., Kowalski D. Multiple Rad5 activities mediate sister chromatid recombination to bypass DNA damage at stalled replication forks. Mol. Cell 2010, 38:649-661.
29. Mizukoshi T., Tanaka T., Arai K., Kohda D., Masai H. A critical role of the 3' terminus of nascent DNA chains in recognition of stalled replication forks. J. Biol. Chem. 2003, 278:42234-42239.
30. Motegi A., Sood R., Moinova H., Markowitz S.D., Liu P.P., Myung K. Human SHPRH suppresses genomic instability through proliferating cell nuclear antigen polyubiquitination. J. Cell Biol. 2006, 175:703-708.
31. Motegi A., Liaw H.-J., Lee K.-Y., Roest H.P., Maas A., Wu X., Moinova H., Markowitz S.D., Ding H., Hoeijmakers J.H.J., Myung K. Polyubiquitination of proliferating cell nuclear antigen by HLTF and SHPRH prevents genomic instability from stalled replication forks. Proc. Natl. Acad. Sci. USA 2008, 105:12411-12416.
32. Neelsen K.J., Lopes M. Replication fork reversal in eukaryotes: from dead end to dynamic response. Nat. Rev. Mol. Cell Biol. 2015, 16:207-220.
33. Neelsen K.J., Zanini I.M.Y., Herrador R., Lopes M. Oncogenes induce genotoxic stress by mitotic processing of unusual replication intermediates. J. Cell Biol. 2013, 200:699-708.
34. Ortiz-Bazán M.Á., Gallo-Fernández M., Saugar I., Jiménez-Martín A., Vázquez M.V., Tercero J.A. Rad5 plays a major role in the cellular response to DNA damage during chromosome replication. Cell Rep. 2014, 9:460-468.
35. Sandhu S., Wu X., Nabi Z., Rastegar M., Kung S., Mai S., Ding H. Loss of HLTF function promotes intestinal carcinogenesis. Mol. Cancer 2012, 11:18.
36. Sasaki K., Ose T., Okamoto N., Maenaka K., Tanaka T., Masai H., Saito M., Shirai T., Kohda D. Structural basis of the 3'-end recognition of a leading strand in stalled replication forks by PriA. EMBO J. 2007, 26:2584-2593.
37. Saugar I., Ortiz-Bazán M.Á., Tercero J.A. Tolerating DNA damage during eukaryotic chromosome replication. Exp. Cell Res. 2014, 329:170-177.
38. 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.
39. Sirbu B.M., Couch F.B., Feigerle J.T., Bhaskara S., Hiebert S.W., Cortez D. Analysis of protein dynamics at active, stalled, and collapsed replication forks. Genes Dev. 2011, 25:1320-1327.
40. Theobald D.L., Mitton-Fry R.M., Wuttke D.S. Nucleic acid recognition by OB-fold proteins. Annu. Rev. Biophys. Biomol. Struct. 2003, 32:115-133.
41. Tsutakawa S.E., Classen S., Chapados B.R., Arvai A.S., Finger L.D., Guenther G., Tomlinson C.G., Thompson P., Sarker A.H., Shen B., et al. Human flap endonuclease structures, DNA double-base flipping, and a unified understanding of the FEN1 superfamily. Cell 2011, 145:198-211.
42. Unk I., Hajdú I., Fátyol K., Szakál B., Blastyák A., Bermudez V., Hurwitz J., Prakash L., Prakash S., Haracska L. Human SHPRH is a ubiquitin ligase for Mms2-Ubc13-dependent polyubiquitylation of proliferating cell nuclear antigen. Proc. Natl. Acad. Sci. USA 2006, 103:18107-18112.
43. Unk I., Hajdú I., Fátyol K., Hurwitz J., Yoon J.-H., Prakash L., Prakash S., Haracska L. Human HLTF functions as a ubiquitin ligase for proliferating cell nuclear antigen polyubiquitination. Proc. Natl. Acad. Sci. USA 2008, 105:3768-3773.
44. Unk I., Hajdú I., Blastyák A., Haracska L. Role of yeast Rad5 and its human orthologs, HLTF and SHPRH in DNA damage tolerance. DNA Repair (Amst.) 2010, 9:257-267.
45. Zellweger R., Dalcher D., Mutreja K., Berti M., Schmid J.A., Herrador R., Vindigni A., Lopes M. Rad51-mediated replication fork reversal is a global response to genotoxic treatments in human cells. J. Cell Biol. 2015, 208:563-579.
46. Zeman M.K., Cimprich K.A. Causes and consequences of replication stress. Nat. Cell Biol. 2014, 16:2-9.