A novel role for the mono-ADP-ribosyltransferase PARP14/ARTD8 in promoting homologous recombination and protecting against replication stress

Nucleic Acids Research

Volumn 43, Issue 6, 2015, Pages 3143-3153

  Nicolae, Claudia M ^a   Aho, Erin R ^a,d   Choe, Katherine N ^a   Constantin, Daniel ^a   Hu, He Juan ^a,b   Lee, Deokjae ^c   Myung, Kyungjae ^c   Moldovan, George Lucian ^a  

^a PENN STATE COLLEGE OF MEDICINE   (United States)

^b Suzhou Health College   (China)

^c NATIONAL HUMAN GENOME RESEARCH INSTITUTE   (United States)

^d VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 14; PROTEIN ARTD8; RAD51 PROTEIN; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; CYCLINE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE INHIBITOR; PARP14 PROTEIN, HUMAN;

ADENOSINE DIPHOSPHATE RIBOSYLATION; ARTICLE; CELL CYCLE S PHASE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DNA REPLICATION; DOUBLE STRANDED DNA BREAK; GENOMIC INSTABILITY; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; PLASMID; PRIORITY JOURNAL; PROTEIN DEPLETION; RECOMBINATION REPAIR; REPLICATION STRESS; STRESS; CELL LINE; CHROMOSOME FRAGILE SITE; DNA DAMAGE; DNA REPAIR; DNA STRAND BREAKAGE; GENETICS; HEK293 CELL LINE; HELA CELL LINE; HOMOLOGOUS RECOMBINATION; METABOLISM;

CELL LINE; CHROMOSOME FRAGILE SITES; DNA BREAKS; DNA DAMAGE; DNA REPAIR; DNA REPLICATION; GENOMIC INSTABILITY; HEK293 CELLS; HELA CELLS; HOMOLOGOUS RECOMBINATION; HUMANS; POLY(ADP-RIBOSE) POLYMERASE INHIBITORS; POLY(ADP-RIBOSE) POLYMERASES; PROLIFERATING CELL NUCLEAR ANTIGEN; RNA, SMALL INTERFERING; S PHASE;

EID: 84942239332     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkv147     Document Type: Article

References (54)

1. Branzei,D. and Foiani,M. (2010) Maintaining genome stability at the replication fork. Nat. Rev. Mol. Cell Biol., 11, 208-219.
2. Ciccia,A. and Elledge,S.J. (2010) The DNA damage response: making it safe to play with knives. Mol. Cell, 40, 179-204.
3. Jackson,S.P. (2009) The DNA-damage response: new molecular insights and new approaches to cancer therapy. Biochem. Soc. Trans., 37, 483-494.
4. Moynahan,M.E. and Jasin,M. (2010) Mitotic homologous recombination maintains genomic stability and suppresses tumorigenesis. Nat. Rev. Mol. Cell Biol., 11, 196-207.
5. San Filippo,J., Sung,P. and Klein,H. (2008) Mechanism of eukaryotic homologous recombination. Annu. Rev. Biochem., 77, 229-257.
6. Schild,D. and Wiese,C. (2010) Overexpression of RAD51 suppresses recombination defects: a possible mechanism to reverse genomic instability. Nucleic Acids Res., 38, 1061-1070.
7. Vollebergh,M.A., Jonkers,J. and Linn,S.C. (2012) Genomic instability in breast and ovarian cancers: translation into clinical predictive biomarkers. Cell. Mol. Life Sci., 69, 223-245.
8. Budke,B., Kalin,J.H., Pawlowski,M., Zelivianskaia,A.S., Wu,M., Kozikowski,A.P. and Connell,P.P. (2013) An optimized RAD51 inhibitor that disrupts homologous recombination without requiring Michael acceptor reactivity. J. Med. Chem., 56, 254-263.
9. Budke,B., Logan,H.L., Kalin,J.H., Zelivianskaia,A.S., Cameron McGuire,W., Miller,L.L., Stark,J.M., Kozikowski,A.P., Bishop,D.K. and Connell,P.P. (2012) RI-1: a chemical inhibitor of RAD51 that disrupts homologous recombination in human cells. Nucleic Acids Res., 40, 7347-7357.
10. Bryant,H.E., Schultz,N., Thomas,H.D., Parker,K.M., Flower,D., Lopez,E., Kyle,S., Meuth,M., Curtin,N.J. and Helleday,T. (2005) Specific killing of BRCA2-deficient tumours with inhibitors of poly(ADP-ribose) polymerase. Nature, 434, 913-917.
11. Farmer,H., McCabe,N., Lord,C.J., Tutt,A.N., Johnson,D.A., Richardson,T.B., Santarosa,M., Dillon,K.J., Hickson,I., Knights,C. et al. (2005) Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy. Nature, 434, 917-921.
12. Budzowska,M. and Kanaar,R. (2009) Mechanisms of dealing with DNA damage-induced replication problems. Cell Biochem. Biophys., 53, 17-31.
13. Chang,D.J. and Cimprich,K.A. (2009) DNA damage tolerance: when it's OK to make mistakes. Nat. Chem. Biol., 5, 82-90.
14. Franchitto,A. and Pichierri,P. (2011) Understanding the molecular basis of common fragile sites instability: role of the proteins involved in the recovery of stalled replication forks. Cell Cycle, 10, 4039-4046.
15. Ozeri-Galai,E., Bester,A.C. and Kerem,B. (2012) The complex basis underlying common fragile site instability in cancer. Trends Genet., 28, 295-302.
16. Bartkova,J., Horejsi,Z., Koed,K., Kramer,A., Tort,F., Zieger,K., Guldberg,P., Sehested,M., Nesland,J.M., Lukas,C. et al. (2005) DNA damage response as a candidate anti-cancer barrier in early human tumorigenesis. Nature, 434, 864-870.
17. Gorgoulis,V.G., Vassiliou,L.V., Karakaidos,P., Zacharatos,P., Kotsinas,A., Liloglou,T., Venere,M., Ditullio,R.A. Jr, Kastrinakis,N.G., Levy,B. et al. (2005) Activation of the DNA damage checkpoint and genomic instability in human precancerous lesions. Nature, 434, 907-913.
18. Halazonetis,T.D., Gorgoulis,V.G. and Bartek,J. (2008) An oncogene-induced DNA damage model for cancer development. Science, 319, 1352-1355.
19. Lundin,C., Erixon,K., Arnaudeau,C., Schultz,N., Jenssen,D., Meuth,M. and Helleday,T. (2002) Different roles for nonhomologous end joining and homologous recombination following replication arrest in mammalian cells. Mol. Cell. Biol., 22, 5869-5878.
20. Jensen,R.B., Carreira,A. and Kowalczykowski,S.C. (2010) Purified human BRCA2 stimulates RAD51-mediated recombination. Nature, 467, 678-683.
21. Chan,K.L., Palmai-Pallag,T., Ying,S. and Hickson,I.D. (2009) Replication stress induces sister-chromatid bridging at fragile site loci in mitosis. Nat. Cell Biol., 11, 753-760.
22. Guo,C., Kosarek-Stancel,J.N., Tang,T.S. and Friedberg,E.C. (2009) Y-family DNA polymerases in mammalian cells. Cell. Mol. Life Sci., 66, 2363-2381.
23. Guo,C., Tang,T.S., Bienko,M., Parker,J.L., Bielen,A.B., Sonoda,E., Takeda,S., Ulrich,H.D., Dikic,I. and Friedberg,E.C. (2006) Ubiquitin-binding motifs in REV1 protein are required for its role in the tolerance of DNA damage. Mol. Cell. Biol., 26, 8892-8900.
24. Hoege,C., Pfander,B., Moldovan,G.-L., Pyrowolakis,G. and Jentsch,S. (2002) RAD6-dependent DNA repair is linked to modification of PCNA by ubiquitin and SUMO. Nature, 419, 135-141.
25. Kannouche,P.L., Wing,J. and Lehmann,A.R. (2004) Interaction of human DNA polymerase eta with monoubiquitinated PCNA: a possible mechanism for the polymerase switch in response to DNA damage. Mol. Cell, 14, 491-500.
26. Moldovan,G.-L., Pfander,B. and Jentsch,S. (2007) PCNA, the maestro of the replication fork. Cell, 129, 665-679.
27. Moldovan,G.L., Dejsuphong,D., Petalcorin,M.I., Hofmann,K., Takeda,S., Boulton,S.J. and D'Andrea,A.D. (2012) Inhibition of homologous recombination by the PCNA-interacting protein PARI. Mol. Cell, 45, 75-86.
28. Papouli,E., Chen,S., Davies,A.A., Huttner,D., Krejci,L., Sung,P. and Ulrich,H.D. (2005) Crosstalk between SUMO and ubiquitin on PCNA is mediated by recruitment of the helicase Srs2p. Mol. Cell, 19, 123-133.
29. Pfander,B., Moldovan,G.-L., Sacher,M., Hoege,C. and Jentsch,S. (2005) SUMO-modified PCNA recruits Srs2 to prevent recombination during S phase. Nature, 436, 428-433.
30. Feijs,K.L., Forst,A.H., Verheugd,P. and Luscher,B. (2013) Macrodomain-containing proteins: regulating new intracellular functions of mono(ADP-ribosyl)ation. Nat. Rev. Mol. Cell Biol., 14, 443-451.
31. Feijs,K.L., Verheugd,P. and Luscher,B. (2013) Expanding functions of intracellular resident mono-ADP-ribosylation in cell physiology. FEBS J., 280, 3519-3529.
32. Gibson,B.A. and Kraus,W.L. (2012) New insights into the molecular and cellular functions of poly(ADP-ribose) and PARPs. Nat. Rev. Mol. Cell Biol., 13, 411-424.
33. Hottiger,M.O. (2011) ADP-ribosylation of histones by ARTD1: an additional module of the histone code? FEBS Lett., 585, 1595-1599.
34. Kalisch,T., Ame,J.C., Dantzer,F. and Schreiber,V. (2012) New readers and interpretations of poly(ADP-ribosyl)ation. Trends Biochem. Sci., 37, 381-390.
35. Nicolae,C.M., Aho,E.R., Vlahos,A.H., Choe,K.N., De,S., Karras,G.I. and Moldovan,G.L. (2014) The ADP-ribosyltransferase PARP10/ARTD10 interacts with proliferating cell nuclear antigen (PCNA) and is required for DNA damage tolerance. J. Biol. Chem., 289, 13627-13637.
36. Feijs,K.L., Kleine,H., Braczynski,A., Forst,A.H., Herzog,N., Verheugd,P., Linzen,U., Kremmer,E. and Luscher,B. (2013) ARTD10 substrate identification on protein microarrays: regulation of GSK3beta by mono-ADP-ribosylation. Cell Commun. Signal., 11, 5-15.
37. Verheugd,P., Forst,A.H., Milke,L., Herzog,N., Feijs,K.L., Kremmer,E., Kleine,H. and Luscher,B. (2013) Regulation of NF-kappaB signalling by the mono-ADP-ribosyltransferase ARTD10. Nat. Commun., 4, 1683-1694.
38. Goenka,S. and Boothby,M. (2006) Selective potentiation of Stat-dependent gene expression by collaborator of Stat6 (CoaSt6), a transcriptional cofactor. Proc. Natl. Acad. Sci. U.S.A., 103, 4210-4215.
39. Vyas,S., Chesarone-Cataldo,M., Todorova,T., Huang,Y.H. and Chang,P. (2013) A systematic analysis of the PARP protein family identifies new functions critical for cell physiology. Nat. Commun., 4, 2240-2252.
40. Forst,A.H., Karlberg,T., Herzog,N., Thorsell,A.G., Gross,A., Feijs,K.L., Verheugd,P., Kursula,P., Nijmeijer,B., Kremmer,E. et al. (2013) Recognition of mono-ADP-ribosylated ARTD10 substrates by ARTD8 macrodomains. Structure, 21, 462-475.
41. Moldovan,G.-L., Madhavan,M.V., Mirchandani,K.D., McCaffrey,R.M., Vinciguerra,P. and D'Andrea,A.D. (2010) DNA polymerase POLN participates in cross-link repair and homologous recombination. Mol. Cell. Biol., 30, 1088-1096.
42. Wysocka,J., Reilly,P.T. and Herr,W. (2001) Loss of HCF-1-chromatin association precedes temperature-induced growth arrest of tsBN67 cells. Mol. Cell. Biol., 21, 3820-3829.
43. O'Connor,K.W., Dejsuphong,D., Park,E., Nicolae,C.M., Kimmelman,A.C., D'Andrea,A.D. and Moldovan,G.-L. (2013) PARI overexpression promotes genomic instability and pancreatic tumorigenesis. Cancer Res., 73, 2529-2539.
44. Canella,K.A. and Seidman,M.M. (2000) Mutation spectra in supF: approaches to elucidating sequence context effects. Mutat. Res., 450, 61-73.
45. Nakanishi,K., Yang,Y.G., Pierce,A.J., Taniguchi,T., Digweed,M., D'Andrea,A.D., Wang,Z.Q. and Jasin,M. (2005) Human Fanconi anemia monoubiquitination pathway promotes homologous DNA repair. Proc. Natl. Acad. Sci. U.S.A., 102, 1110-1115.
46. Fu,H., Maunakea,A.K., Martin,M.M., Huang,L., Zhang,Y., Ryan,M., Kim,R., Lin,C.M., Zhao,K. and Aladjem,M.I. (2013) Methylation of histone H3 on lysine 79 associates with a group of replication origins and helps limit DNA replication once per cell cycle. PLoS Genet., 9, e1003542.
47. Lu,X., Parvathaneni,S., Hara,T., Lal,A. and Sharma,S. (2013) Replication stress induces specific enrichment of RECQ1 at common fragile sites FRA3B and FRA16D. Mol. Cancer, 12, 29-40.
48. Wan,C., Kulkarni,A. and Wang,Y.H. (2010) ATR preferentially interacts with common fragile site FRA3B and the binding requires its kinase activity in response to aphidicolin treatment. Mutat. Res., 686, 39-46.
49. Bergoglio,V., Boyer,A.S., Walsh,E., Naim,V., Legube,G., Lee,M.Y., Rey,L., Rosselli,F., Cazaux,C., Eckert,K.A. et al. (2013) DNA synthesis by Pol eta promotes fragile site stability by preventing under-replicated DNA in mitosis. J. Cell Biol., 201, 395-408.
50. Yu,P., Huang,B., Shen,M., Lau,C., Chan,E., Michel,J., Xiong,Y., Payan,D.G. and Luo,Y. (2001) p15(PAF), a novel PCNA associated factor with increased expression in tumor tissues. Oncogene, 20, 484-489.
51. Lukas,C., Savic,V., Bekker-Jensen,S., Doil,C., Neumann,B., Pedersen,R.S., Grofte,M., Chan,K.L., Hickson,I.D., Bartek,J. et al. (2011) 53BP1 nuclear bodies form around DNA lesions generated by mitotic transmission of chromosomes under replication stress. Nat. Cell Biol., 13, 243-253.
52. Schwartz,M., Zlotorynski,E., Goldberg,M., Ozeri,E., Rahat,A., le Sage,C., Chen,B.P., Chen,D.J., Agami,R. and Kerem,B. (2005) Homologous recombination and nonhomologous end-joining repair pathways regulate fragile site stability. Genes Dev., 19, 2715-2726.
53. Jackson,S.P. and Durocher,D. (2013) Regulation of DNA damage responses by ubiquitin and SUMO. Mol. Cell, 49, 795-807.
54. Huang,T.T., Wuerzberger-Davis,S.M., Wu,Z.H. and Miyamoto,S. (2003) Sequential modification of NEMO/IKKgamma by SUMO-1 and ubiquitin mediates NF-kappaB activation by genotoxic stress. Cell, 115, 565-576.