HUWE1 interacts with PCNA to alleviate replication stress

EMBO Reports

Volumn 17, Issue 6, 2016, Pages 874-886

  Choe, Katherine N ^a   Nicolae, Claudia M ^a   Constantin, Daniel ^a   Imamura Kawasawa, Yuka ^a   Delgado Diaz, Maria Rocio ^b   De, Subhajyoti ^c,d,e   Freire, Raimundo ^b   Smits, Veronique A ^b   Moldovan, George Lucian ^a  

^a PENN STATE COLLEGE OF MEDICINE   (United States)

^b HOSPITAL UNIVERSITARIO DE CANARIAS   (Spain)

^c UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^d Food Science and Human Nutrition   (United States)

^e UNIVERSITY OF COLORADO   (United States)

Author keywords

DNA replication; genomic instability; H2AX; HUWE1; PCNA

Indexed keywords

CYCLINE; DNA; HISTONE H2AX; HUWE1 PROTEIN; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; HISTONE; HUWE1 PROTEIN, HUMAN; PROTEIN BINDING; UBIQUITIN; UBIQUITIN PROTEIN LIGASE;

ARTICLE; CONTROLLED STUDY; DNA DAMAGE CHECKPOINT; DNA STRAND BREAKAGE; FEMALE; GENOMIC INSTABILITY; HELA CELL LINE; HUMAN; HUMAN CELL; IN VITRO STUDY; INTRACELLULAR SIGNALING; MOLECULAR INTERACTION; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; U2OS CELL LINE; UBIQUITINATION; CELL LINE; DNA DAMAGE; DNA REPAIR; DNA REPLICATION; GENE INACTIVATION; GENETICS; METABOLISM; PHENOTYPE; PHYSIOLOGICAL STRESS; PROTEIN PROCESSING; PROTEIN TRANSPORT;

CELL LINE; DNA DAMAGE; DNA REPAIR; DNA REPLICATION; GENE KNOCKOUT TECHNIQUES; GENOMIC INSTABILITY; HISTONES; HUMANS; PHENOTYPE; PROLIFERATING CELL NUCLEAR ANTIGEN; PROTEIN BINDING; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN TRANSPORT; STRESS, PHYSIOLOGICAL; UBIQUITIN; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

EID: 84971499032     PISSN: 1469221X     EISSN: 14693178     Source Type: Journal    
DOI: 10.15252/embr.201541685     Document Type: Article

References (64)

1. Zeman MK, Cimprich KA, (2014) Causes and consequences of replication stress. Nat Cell Biol 16: 2-9
2. Papamichos-Chronakis M, Peterson CL, (2013) Chromatin and the genome integrity network. Nat Rev Genet 14: 62-75
3. Gaillard H, Garcia-Muse T, Aguilera A, (2015) Replication stress and cancer. Nat Rev Cancer 15: 276-289
4. Moldovan GL, Pfander B, Jentsch S, (2007) PCNA, the maestro of the replication fork. Cell 129: 665-679
5. Maga G, Hubscher U, (2003) Proliferating cell nuclear antigen (PCNA): a dancer with many partners. J Cell Sci 116: 3051-3060
6. Waters LS, Minesinger BK, Wiltrout ME, D'Souza S, Woodruff RV, Walker GC, (2009) Eukaryotic translesion polymerases and their roles and regulation in DNA damage tolerance. Microbiol Mol Biol Rev 73: 134-154
7. Hoege C, Pfander B, Moldovan GL, Pyrowolakis G, Jentsch S, (2002) RAD6-dependent DNA repair is linked to modification of PCNA by ubiquitin and SUMO. Nature 419: 135-141
8. Guo C, Kosarek-Stancel JN, Tang TS, Friedberg EC, (2009) Y-family DNA polymerases in mammalian cells. Cell Mol Life Sci 66: 2363-2381
9. Chang DJ, Cimprich KA, (2009) DNA damage tolerance: when it's OK to make mistakes. Nat Chem Biol 5: 82-90
10. Bienko M, Green CM, Crosetto N, Rudolf F, Zapart G, Coull B, Kannouche P, Wider G, Peter M, Lehmann AR, et al, (2005) Ubiquitin-binding domains in Y-family polymerases regulate translesion synthesis. Science 310: 1821-1824
11. Bernassola F, Karin M, Ciechanover A, Melino G, (2008) The HECT family of E3 ubiquitin ligases: multiple players in cancer development. Cancer Cell 14: 10-21
12. Chen D, Brooks CL, Gu W, (2006) ARF-BP1 as a potential therapeutic target. Br J Cancer 94: 1555-1558
13. Chen D, Kon N, Li M, Zhang W, Qin J, Gu W, (2005) ARF-BP1/Mule is a critical mediator of the ARF tumor suppressor. Cell 121: 1071-1083
14. Adhikary S, Marinoni F, Hock A, Hulleman E, Popov N, Beier R, Bernard S, Quarto M, Capra M, Goettig S, et al, (2005) The ubiquitin ligase HectH9 regulates transcriptional activation by Myc and is essential for tumor cell proliferation. Cell 123: 409-421
15. Yoon SY, Lee Y, Kim JH, Chung AS, Joo JH, Kim CN, Kim NS, Choe IS, Kim JW, (2005) Over-expression of human UREB1 in colorectal cancer: HECT domain of human UREB1 inhibits the activity of tumor suppressor p53 protein. Biochem Biophys Res Commun 326: 7-17
16. Confalonieri S, Quarto M, Goisis G, Nuciforo P, Donzelli M, Jodice G, Pelosi G, Viale G, Pece S, Di Fiore PP, (2009) Alterations of ubiquitin ligases in human cancer and their association with the natural history of the tumor. Oncogene 28: 2959-2968
17. Liu YX, Zhang SF, Ji YH, Guo SJ, Wang GF, Zhang GW, (2012) Whole-exome sequencing identifies mutated PCK2 and HUWE1 associated with carcinoma cell proliferation in a hepatocellular carcinoma patient. Oncol Lett 4: 847-851
18. Zhao X, Heng JI, Guardavaccaro D, Jiang R, Pagano M, Guillemot F, Iavarone A, Lasorella A, (2008) The HECT-domain ubiquitin ligase Huwe1 controls neural differentiation and proliferation by destabilizing the N-Myc oncoprotein. Nat Cell Biol 10: 643-653
19. Kurokawa M, Kim J, Geradts J, Matsuura K, Liu L, Ran X, Xia W, Ribar TJ, Henao R, Dewhirst MW, et al, (2013) A Network of Substrates of the E3 Ubiquitin Ligases MDM2 and HUWE1 Control Apoptosis Independently of p53. Sci Signal 6: ra32
20. Inoue S, Hao Z, Elia AJ, Cescon D, Zhou L, Silvester J, Snow B, Harris IS, Sasaki M, Li WY, et al, (2013) Mule/Huwe1/Arf-BP1 suppresses Ras-driven tumorigenesis by preventing c-Myc/Miz1-mediated down-regulation of p21 and p15. Genes Dev 27: 1101-1114
21. Pervin S, Tran A, Tran L, Urman R, Braga M, Chaudhuri G, Singh R, (2011) Reduced association of anti-apoptotic protein Mcl-1 with E3 ligase Mule increases the stability of Mcl-1 in breast cancer cells. Br J Cancer 105: 428-437
22. Qi CF, Zhang R, Sun J, Li Z, Shin DM, Wang H, Kovalchuk AL, Sakai T, Xiong H, Kon N, et al, (2013) Homeostatic defects in B cells deficient in the E3 ubiquitin ligase ARF-BP1 are restored by enhanced expression of MYC. Leuk Res 37: 1680-1689
23. Maltseva DV, Khaustova NA, Fedotov NN, Matveeva EO, Lebedev AE, Shkurnikov MU, Galatenko VV, Schumacher U, Tonevitsky AG, (2013) High-throughput identification of reference genes for research and clinical RT-qPCR analysis of breast cancer samples. J Clin Bioinforma 3: 13
24. de Groot RE, Ganji RS, Bernatik O, Lloyd-Lewis B, Seipel K, Šedová K, Zdráhal Z, Dhople VM, Dale TC, Korswagen HC, et al, (2014) Huwe1-mediated ubiquitylation of dishevelled defines a negative feedback loop in the Wnt signaling pathway. Sci Signal 7: ra26
25. Jang ER, Shi P, Bryant J, Chen J, Dukhande V, Gentry MS, Jang H, Jeoung M, Galperin E, (2014) HUWE1 is a molecular link controlling RAF-1 activity supported by the Shoc2 scaffold. Mol Cell Biol 34: 3579-3593
26. Peter S, Bultinck J, Myant K, Jaenicke LA, Walz S, Müller J, Gmachl M, Treu M, Boehmelt G, Ade CP, et al, (2014) Tumor cell-specific inhibition of MYC function using small molecule inhibitors of the HUWE1 ubiquitin ligase. EMBO Mol Med 6: 1525-1541
27. Schaub FX, Cleveland JL, (2014) Tipping the MYC-MIZ1 balance: targeting the HUWE1 ubiquitin ligase selectively blocks MYC-activated genes. EMBO Mol Med 6: 1509-1511
28. Hao Z, Duncan GS, Su YW, Li WY, Silvester J, Hong C, You H, Brenner D, Gorrini C, Haight J, et al, (2012) The E3 ubiquitin ligase Mule acts through the ATM-p53 axis to maintain B lymphocyte homeostasis. J Exp Med 209: 173-186
29. Vaughan L, Tan CT, Chapman A, Nonaka D, Mack NA, Smith D, Booton R, Hurlstone AF, Malliri A, (2015) HUWE1 ubiquitylates and degrades the RAC activator TIAM1 promoting cell-cell adhesion disassembly, migration, and invasion. Cell Rep 10: 88-102
30. Brooks CL, Gu W, (2006) p53 ubiquitination: Mdm2 and beyond. Mol Cell 21: 307-315
31. Hall JR, Kow E, Nevis KR, Lu CK, Luce KS, Zhong Q, Cook JG, (2007) Cdc6 stability is regulated by the Huwe1 ubiquitin ligase after DNA damage. Mol Biol Cell 18: 3340-3350
32. Herold S, Hock A, Herkert B, Berns K, Mullenders J, Beijersbergen R, Bernards R, Eilers M, (2008) Miz1 and HectH9 regulate the stability of the checkpoint protein, TopBP1. EMBO J 27: 2851-2861
33. Parsons JL, Tait PS, Finch D, Dianova II, Edelmann MJ, Khoronenkova SV, Kessler BM, Sharma RA, McKenna WG, Dianov GL, (2009) Ubiquitin ligase ARF-BP1/Mule modulates base excision repair. EMBO J 28: 3207-3215
34. Khoronenkova SV, Dianov GL, (2011) The emerging role of Mule and ARF in the regulation of base excision repair. FEBS Lett 585: 2831-2835
35. Markkanen E, van Loon B, Ferrari E, Parsons JL, Dianov GL, Hübscher U, (2012) Regulation of oxidative DNA damage repair by DNA polymerase λ and MutYH by cross-talk of phosphorylation and ubiquitination. Proc Natl Acad Sci USA 109: 437-442
36. Wang X, Lu G, Li L, Yi J, Yan K, Wang Y, Zhu B, Kuang J, Lin M, Zhang S, et al, (2014) HUWE1 interacts with BRCA1 and promotes its degradation in the ubiquitin-proteasome pathway. Biochem Biophys Res Commun 444: 549-554
37. Dungrawala H, Cortez D, (2015) Purification of proteins on newly synthesized DNA using iPOND. Methods Mol Biol 1228: 123-131
38. Sirbu BM, Couch FB, Feigerle JT, Bhaskara S, Hiebert SW, Cortez D, (2011) Analysis of protein dynamics at active, stalled, and collapsed replication forks. Genes Dev 25: 1320-1327
39. Wu CY, Kang HY, Yang WL, Wu J, Jeong YS, Wang J, Chan CH, Lee SW, Zhang X, Lamothe B, et al, (2011) Critical role of monoubiquitination of histone H2AX protein in histone H2AX phosphorylation and DNA damage response. J Biol Chem 286: 30806-30815
40. Pan MR, Peng G, Hung WC, Lin SY, (2011) Monoubiquitination of H2AX protein regulates DNA damage response signaling. J Biol Chem 286: 28599-28607
41. Ozeri-Galai E, Bester AC, Kerem B, (2012) The complex basis underlying common fragile site instability in cancer. Trends Genet 28: 295-302
42. Lu X, Parvathaneni S, Hara T, Lal A, Sharma S, (2013) Replication stress induces specific enrichment of RECQ1 at common fragile sites FRA3B and FRA16D. Mol Cancer 12: 29
43. Mattiroli F, Vissers JH, van Dijk WJ, Ikpa P, Citterio E, Vermeulen W, Marteijn JA, Sixma TK, (2012) RNF168 ubiquitinates K13-15 on H2A/H2AX to drive DNA damage signaling. Cell 150: 1182-1195
44. Hoeller D, Dikic I, (2009) Targeting the ubiquitin system in cancer therapy. Nature 458: 438-444
45. Peterson CL, Cote J, (2004) Cellular machineries for chromosomal DNA repair. Genes Dev 18: 602-616
46. Pathania S, Bade S, Le Guillou M, Burke K, Reed R, Bowman-Colin C, Su Y, Ting DT, Polyak K, Richardson AL, et al, (2014) BRCA1 haploinsufficiency for replication stress suppression in primary cells. Nat Commun 5: 5496
47. Schlacher K, Christ N, Siaud N, Egashira A, Wu H, Jasin M, (2011) Double-strand break repair-independent role for BRCA2 in blocking stalled replication fork degradation by MRE11. Cell 145: 529-542
48. Hall JR, Lee HO, Bunker BD, Dorn ES, Rogers GC, Duronio RJ, Cook JG, (2008) Cdt1 and Cdc6 are destabilized by rereplication-induced DNA damage. J Biol Chem 283: 25356-25363
49. Ciccia A, Elledge SJ, (2010) The DNA damage response: making it safe to play with knives. Mol Cell 40: 179-204
50. Ward IM, Chen J, (2001) Histone H2AX is phosphorylated in an ATR-dependent manner in response to replicational stress. J Biol Chem 276: 47759-47762
51. Ewald B, Sampath D, Plunkett W, (2007) H2AX phosphorylation marks gemcitabine-induced stalled replication forks and their collapse upon S-phase checkpoint abrogation. Mol Cancer Ther 6: 1239-1248
52. Gagou ME, Zuazua-Villar P, Meuth M, (2010) Enhanced H2AX phosphorylation, DNA replication fork arrest, and cell death in the absence of Chk1. Mol Biol Cell 21: 739-752
53. Wang J, Gong Z, Chen J, (2011) MDC1 collaborates with TopBP1 in DNA replication checkpoint control. J Cell Biol 193: 267-273
54. Liu Z, Oughtred R, Wing SS, (2005) Characterization of E3Histone, a novel testis ubiquitin protein ligase which ubiquitinates histones. Mol Cell Biol 25: 2819-2831
55. Liu Z, Miao D, Xia Q, Hermo L, Wing SS, (2007) Regulated expression of the ubiquitin protein ligase, E3(Histone)/LASU1/Mule/ARF-BP1/HUWE1, during spermatogenesis. Dev Dyn 236: 2889-2898
56. Atsumi Y, Minakawa Y, Ono M, Dobashi S, Shinohe K, Shinohara A, Takeda S, Takagi M, Takamatsu N, Nakagama H, et al, (2015) ATM and SIRT6/SNF2H mediate transient H2AX stabilization when DSBs form by blocking HUWE1 to allow efficient gammaH2AX foci formation. Cell Rep 13: 2728-2740
57. McGlynn P, Lloyd RG, (2002) Recombinational repair and restart of damaged replication forks. Nat Rev Mol Cell Biol 3: 859-870
58. Petermann E, Orta ML, Issaeva N, Schultz N, Helleday T, (2010) Hydroxyurea-stalled replication forks become progressively inactivated and require two different RAD51-mediated pathways for restart and repair. Mol Cell 37: 492-502
59. Yeeles JT, Poli J, Marians KJ, Pasero P, (2013) Rescuing stalled or damaged replication forks. Cold Spring Harb Perspect Biol 5: a012815
60. O'Connor KW, Dejsuphong D, Park E, Nicolae CM, Kimmelman AC, D'Andrea AD, Moldovan GL, (2013) PARI overexpression promotes genomic instability and pancreatic tumorigenesis. Cancer Res 73: 2529-2539
61. Nicolae CM, Aho ER, Vlahos AH, Choe KN, De S, Karras GI, Moldovan GL, (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
62. Nicolae CM, Aho ER, Choe KN, Constantin D, Hu HJ, Lee D, Myung K, Moldovan GL, (2015) A novel role for the mono-ADP-ribosyltransferase PARP14/ARTD8 in promoting homologous recombination and protecting against replication stress. Nucleic Acids Res 43: 3143-3153
63. Moldovan GL, Dejsuphong D, Petalcorin MI, Hofmann K, Takeda S, Boulton SJ, D'Andrea AD, (2012) Inhibition of homologous recombination by the PCNA-interacting protein PARI. Mol Cell 45: 75-86
64. Fu H, Maunakea AK, Martin MM, Huang L, Zhang Y, Ryan M, Kim R, Lin CM, Zhao K, Aladjem MI, (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