Human HLTF mediates postreplication repair by its HIRAN domain-dependent replication fork remodelling

Nucleic Acids Research

Volumn 43, Issue 21, 2015, Pages 10277-10291

  Achar, Yathish Jagadheesh ^a   Balogh, David ^a   Neculai, Dante ^b   Juhasz, Szilvia ^a   Morocz, Monika ^a   Gali, Himabindu ^a   Dhe Paganon, Sirano ^c   Venclovas, Česlovas ^d   Haracska, Lajos ^a  

^a INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^b ZHEJIANG UNIVERSITY   (China)

^c DANA FARBER CANCER INSTITUTE   (United States)

^d VILNIUS UNIVERSITY   (Lithuania)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; CARRIER PROTEIN; DOUBLE STRANDED DNA TRANSLOCASE; HLTF PROTEIN; MOLECULAR MOTOR; NUCLEIC ACID BINDING PROTEIN; UBIQUITIN PROTEIN LIGASE; UNCLASSIFIED DRUG; CYCLINE; DNA; DNA BINDING PROTEIN; HLTF PROTEIN, HUMAN; TRANSCRIPTION FACTOR;

ARTICLE; CONTROLLED STUDY; DNA BINDING; DNA DAMAGE; DNA REPAIR; DNA REPLICATION; ENZYME ACTIVITY; HIRAN DOMAIN; HUMAN; HUMAN CELL; POSTREPLICATION REPAIR; PRIORITY JOURNAL; PROTEIN DOMAIN; REPLICATION FORK; UBIQUITINATION; CELL LINE; CHEMISTRY; METABOLISM; PROTEIN TERTIARY STRUCTURE;

ADENOSINE TRIPHOSPHATASES; CELL LINE; DNA; DNA REPAIR; DNA REPLICATION; DNA-BINDING PROTEINS; HUMANS; PROLIFERATING CELL NUCLEAR ANTIGEN; PROTEIN STRUCTURE, TERTIARY; TRANSCRIPTION FACTORS; UBIQUITIN-PROTEIN LIGASES;

EID: 84964667405     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkv896     Document Type: Article

References (47)

1. Ciccia, A. and Elledge, S.J. (2010) The DNA damage response: making it safe to play with knives. Mol. Cell, 40, 179-204.
2. Izhar, L., Ziv, O., Cohen, I.S., Geacintov, N.E. and Livneh, Z. (2013) Genomic assay reveals tolerance of DNA damage by both translesion DNA synthesis and homology-dependent repair in mammalian cells. Proc. Natl. Acad. Sci. U.S.A., 110, E1462-E1469.
3. Zhang, H. and Lawrence, C.W. (2005) The error-free component of the RAD6/RAD18 DNA damage tolerance pathway of budding yeast employs sister-strand recombination. Proc. Natl. Acad. Sci. U.S.A., 102, 15954-15959.
4. Yoon, J.-H., Prakash, S. and Prakash, L. (2012) Requirement of Rad18 protein for replication through DNA lesions in mouse and human cells. Proc. Natl. Acad. Sci. U.S.A., 109, 7799-7804.
5. Prakash, S., Johnson, R.E. and Prakash, L. (2005) Eukaryotic translesion synthesis DNA polymerases: specificity of structure and function. Annu. Rev. Biochem., 74, 317-353.
6. Silverstein, T.D., Johnson, R.E., Jain, R., Prakash, L., Prakash, S. and Aggarwal, A.K. (2010) Structural basis for the suppression of skin cancers by DNA polymerase eta. Nature, 465, 1039-1043.
7. Adar, S., Izhar, L., Hendel, A., Geacintov, N. and Livneh, Z. (2009) Repair of gaps opposite lesions by homologous recombination in mammalian cells. Nucleic Acids Res., 37, 5737-5748.
8. Higgins, N.P., Kato, K. and Strauss, B. (1976) A model for replication repair in mammalian cells. J. Mol. Biol., 101, 417-425.
9. Klein, H.L. (2008) Molecular biology: DNA endgames. Nature, 455, 740-741.
10. Krejci, L., Van Komen, S., Li, Y., Villemain, J., Reddy, M.S., Klein, H., Ellenberger, T. and Sung, P. (2003) DNA helicase Srs2 disrupts the Rad51 presynaptic filament. Nature, 423, 305-309.
11. Neelsen, K.J. and Lopes, M. (2015) Replication fork reversal in eukaryotes: from dead end to dynamic response. Nat. Rev. Mol. Cell Biol., 16, 207-220.
12. Torres-Ramos, C.A., Prakash, S. and Prakash, L. (2002) Requirement of RAD5 and MMS2 for postreplication repair of UV-damaged DNA in Saccharomyces cerevisiae. Mol. Cell. Biol., 22, 2419-2426.
13. Gangavarapu, V., Haracska, L., Unk, I., Johnson, R.E., Prakash, S. and Prakash, L. (2006) Mms2-Ubc13-dependent and -independent roles of Rad5 ubiquitin ligase in postreplication repair and translesion DNA synthesis in Saccharomyces cerevisiae. Mol. Cell. Biol., 26, 7783-7790.
14. Gangavarapu, V., Prakash, S. and Prakash, L. (2007) Requirement of RAD52 group genes for postreplication repair of UV-damaged DNA in Saccharomyces cerevisiae. Mol. Cell. Biol., 27, 7758-7764.
15. Blastyák, A., Pintér, L., Unk, I., Prakash, L., Prakash, S. and Haracska, L. (2007) Yeast Rad5 protein required for postreplication repair has a DNA helicase activity specific for replication fork regression. Mol. Cell, 28, 167-175.
16. Xue, X., Choi, K., Bonner, J., Chiba, T., Kwon, Y., Xu, Y., Sanchez, H., Wyman, C., Niu, H., Zhao, X. et al. (2014) Restriction of replication fork regression activities by a conserved SMC complex. Mol. Cell, 56, 436-445.
17. Zheng, X.-F., Prakash, R., Saro, D., Longerich, S., Niu, H. and Sung, P. (2011) Processing of DNA structures via DNA unwinding and branch migration by the S. cerevisiae Mph1 protein. DNA Repair (Amst.), 10, 1034-1043.
18. Unk, I., Hajdú, I., Blastyák, A. and Haracska, L. (2010) Role of yeast Rad5 and its human orthologs, HLTF and SHPRH in DNA damage tolerance. DNA Repair (Amst.), 9, 257-267.
19. Moldovan, G.-L. and D'Andrea, A.D. (2011) DNA damage discrimination at stalled replication forks by the Rad5 homologs HLTF and SHPRH. Mol. Cell, 42, 141-143.
20. Unk, I., Hajdú, I., Fátyol, K., Hurwitz, J., Yoon, J.-H.J.-H., Prakash, L., Prakash, S., Haracska, L., Hajdu, I., Fatyol, K. et al. (2008) Human HLTF functions as a ubiquitin ligase for proliferating cell nuclear antigen polyubiquitination. Proc. Natl. Acad. Sci. U.S.A., 105, 3768-3773.
21. Lin, J.-R., Zeman, M.K., Chen, J.-Y., Yee, M.-C. and Cimprich, K.A. (2011) SHPRH and HLTF act in a damage-specific manner to coordinate different forms of postreplication repair and prevent mutagenesis. Mol. Cell, 42, 237-249.
22. Sandhu, S., Wu, X., Nabi, Z., Rastegar, M., Kung, S., Mai, S. and Ding, H. (2012) Loss of HLTF function promotes intestinal carcinogenesis. Mol. Cancer, 11, 18.
23. 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. et al. (2008) Polyubiquitination of proliferating cell nuclear antigen by HLTF and SHPRH prevents genomic instability from stalled replication forks. Proc. Natl. Acad. Sci. U.S.A., 105, 12411-12416.
24. Blastyák, A., Hajdú, I., Unk, I. and Haracska, L. (2010) Role of double-stranded DNA translocase activity of human HLTF in replication of damaged DNA. Mol. Cell. Biol., 30, 684-693.
25. Achar, Y.J., Balogh, D. and Haracska, L. (2011) Coordinated protein and DNA remodeling by human HLTF on stalled replication fork. Proc. Natl. Acad. Sci. U.S.A., 108, 14073-14078.
26. Burkovics, P., Sebesta, M., Balogh, D., Haracska, L. and Krejci, L. (2014) Strand invasion by HLTF as a mechanism for template switch in fork rescue. Nucleic Acids Res., 42, 1711-1720.
27. Iyer, L.M., Babu, M.M. and Aravind, L. (2006) The HIRAN domain and recruitment of chromatin remodeling and repair activities to damaged DNA. Cell Cycle, 5, 775-782.
28. Hishiki, A., Hara, K., Ikegaya, Y., Yokoyama, H., Shimizu, T., Sato, M. and Hashimoto, H. (2015) Structure of a Novel DNA-binding Domain of Helicase-like Transcription Factor (HLTF) and Its Functional Implication in DNA Damage Tolerance. J. Biol. Chem., doi:10.1074/jbc.M115.643643.
29. Kile, A.C., Chavez, D.A., Bacal, J., Eldirany, S., Korzhnev, D.M., Bezsonova, I., Eichman, B.F. and Cimprich, K.A. (2015) HLTF's ancient HIRAN domain binds 30 DNA ends to drive replication fork reversal. Mol. Cell, 58, 1090-1100.
30. Karras, G.I. and Jentsch, S. (2010) The RAD6 DNA damage tolerance pathway operates uncoupled from the replication fork and is functional beyond S phase. Cell, 141, 255-267.
31. 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. (2012) Polyubiquitinated PCNA recruits the ZRANB3 translocase to maintain genomic integrity after replication stress. Mol. Cell, 47, 396-409.
32. Bétous, R., Mason, A.C., Rambo, R.P., Bansbach, C.E., Badu-Nkansah, A., Sirbu, B.M., Eichman, B.F. and Cortez, D. (2012) SMARCAL1 catalyzes fork regression and Holliday junction migration to maintain genome stability during DNA replication. Genes Dev., 26, 151-162.
33. Shah, P.P., Zheng, X., Epshtein, A., Carey, J.N., Bishop, D.K. and Klein, H.L. (2010) Swi2/Snf2-related translocases prevent accumulation of toxic Rad51 complexes during mitotic growth. Mol. Cell, 39, 862-872.
34. Hu, L., Kim, T.M., Son, M.Y., Kim, S.-A., Holland, C.L., Tateishi, S., Kim, D.H., Yew, P.R., Montagna, C., Dumitrache, L.C. et al. (2013) Two replication fork maintenance pathways fuse inverted repeats to rearrange chromosomes. Nature, 501, 569-572.
35. Juhasz, S., Balogh, D., Hajdu, I., Burkovics, P., Villamil, M.A., Zhuang, Z. and Haracska, L. (2012) Characterization of human Spartan/C1orf124, an ubiquitin-PCNA interacting regulator of DNA damage tolerance. Nucleic Acids Res., 40, 10795-10808.
36. Kabsch, W. (2010) XDS. Acta Crystallogr. D. Biol. Crystallogr., 66, 125-132.
37. Emsley, P. and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr. D. Biol. Crystallogr., 60, 2126-2132.
38. Smogorzewska, A., Matsuoka, S., Vinciguerra, P., McDonald, E.R., Hurov, K.E., Luo, J., Ballif, B.A., Gygi, S.P., Hofmann, K., D'Andrea, A.D. et al. (2007) Identification of the FANCI protein, a monoubiquitinated FANCD2 paralog required for DNA repair. Cell, 129, 289-301.
39. Mórocz, M., Gali, H., Raskó, I., Downes, C.S. and Haracska, L. (2013) Single cell analysis of human RAD18-dependent DNA post-replication repair by alkaline bromodeoxyuridine comet assay. PLoS One, 8, e70391.
40. Moinova, H.R., Chen, W.-D., Shen, L., Smiraglia, D., Olechnowicz, J., Ravi, L., Kasturi, L., Myeroff, L., Plass, C., Parsons, R. et al. (2002) HLTF gene silencing in human colon cancer. Proc. Natl. Acad. Sci. U.S.A., 99, 4562-4567.
41. Schlacher, K., Christ, N., Siaud, N., Egashira, A., Wu, H. and Jasin, M. (2011) Double-strand break repair-independent role for BRCA2 in blocking stalled replication fork degradation by MRE11. Cell, 145, 529-542.
42. Ray Chaudhuri, A., Hashimoto, Y., Herrador, R., Neelsen, K.J., Fachinetti, D., Bermejo, R., Cocito, A., Costanzo, V. and Lopes, M. (2012) Topoisomerase I poisoning results in PARP-mediated replication fork reversal. Nat. Struct. Mol. Biol., 19, 417-423.
43. Singleton, M.R., Scaife, S. and Wigley, D.B. (2001) Structural analysis of DNA replication fork reversal by RecG. Cell, 107, 79-89.
44. Mason, A.C., Rambo, R.P., Greer, B., Pritchett, M., Tainer, J.A., Cortez, D. and Eichman, B.F. (2014) A structure-specific nucleic acid-binding domain conserved among DNA repair proteins. Proc. Natl. Acad. Sci. U.S.A., 111, 7618-7623.
45. Nishino, T., Komori, K., Tsuchiya, D., Ishino, Y. and Morikawa, K. (2005) Crystal structure and functional implications of Pyrococcus furiosus hef helicase domain involved in branched DNA processing. Structure, 13, 143-153.
46. Newman, J.A., Savitsky, P., Allerston, C.K., Bizard, A.H., Özer, Ö ., Sarlós, K., Liu, Y., Pardon, E., Steyaert, J., Hickson, I.D. et al. (2015) Crystal structure of the Bloom's syndrome helicase indicates a role for the HRDC domain in conformational changes. Nucleic Acids Res., 43, 5221-5235.
47. Swan, M.K., Legris, V., Tanner, A., Reaper, P.M., Vial, S., Bordas, R., Pollard, J.R., Charlton, P.A., Golec, J.M.C. and Bertrand, J.A. (2014) Structure of human Bloom's syndrome helicase in complex with ADP and duplex DNA. Acta Crystallogr. D. Biol. Crystallogr., 70, 1465-1475