The RBBP6/ZBTB38/MCM10 Axis Regulates DNA Replication and Common Fragile Site Stability

Cell Reports

Volumn 7, Issue 2, 2014, Pages 575-587

  Miotto, Benoit ^a   Chibi, Moredreck ^a,b   Xie, Ping ^c,d   Koundrioukoff, Stéphane ^f   Moolman Smook, Hanlie ^e   Pugh, David ^b   Debatisse, Michelle ^f   He, Fuchu ^c   Zhang, Lingqiang ^c,d   Defossez, Pierre Antoine ^a  

^a Université Sorbonne Paris Cité   (France)

^b UNIVERSITY OF THE WESTERN CAPE   (South Africa)

^c BEIJING INSTITUTE OF RADIATION MEDICINE   (China)

^d DALIAN MEDICAL UNIVERSITY   (China)

^e STELLENBOSCH UNIVERSITY   (South Africa)

^f CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

MCM10 PROTEIN; RBBP6 PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR ZBTB38; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; CARRIER PROTEIN; DNA BINDING PROTEIN; MCM10 PROTEIN, HUMAN; MINICHROMOSOME MAINTENANCE PROTEIN; RBBP6 PROTEIN, HUMAN; REPRESSOR PROTEIN; ZBTB38 PROTEIN, HUMAN;

ARTICLE; CHROMATIN; CHROMOSOMAL INSTABILITY; COMMON FRAGILE SITE; CONTROLLED STUDY; DNA DAMAGE; DNA REPLICATION; DOWN REGULATION; GENE OVEREXPRESSION; GENETIC REGULATION; HUMAN; HUMAN CELL; HUMAN GENOME; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DEPLETION; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; UBIQUITINATION; CHROMOSOME FRAGILE SITE; CHROMOSOME FRAGILITY; GENETICS; HELA CELL LINE; METABOLISM;

CARRIER PROTEINS; CHROMOSOME FRAGILE SITES; CHROMOSOME FRAGILITY; DNA REPLICATION; DNA-BINDING PROTEINS; HELA CELLS; HUMANS; MINICHROMOSOME MAINTENANCE PROTEINS; REPRESSOR PROTEINS;

EID: 84899648617     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2014.03.030     Document Type: Article

References (55)

1. Aguilera A., Gómez-González B. Genome instability: a mechanistic view of its causes and consequences. Nat. Rev. Genet. 2008, 9:204-217.
2. Arlt M.F., Ozdemir A.C., Birkeland S.R., Wilson T.E., Glover T.W. Hydroxyurea induces de novo copy number variants in human cells. Proc. Natl. Acad. Sci. USA 2011, 108:17360-17365.
3. Balestrini A., Cosentino C., Errico A., Garner E., Costanzo V. GEMC1 is a TopBP1-interacting protein required for chromosomal DNA replication. Nat. Cell Biol. 2010, 12:484-491.
4. Bergoglio V., Boyer A.S., Walsh E., Naim V., Legube G., Lee M.Y., Rey L., Rosselli F., Cazaux C., Eckert K.A., Hoffmann J.S. DNA synthesis by Pol η promotes fragile site stability by preventing under-replicated DNA in mitosis. J.Cell Biol. 2013, 201:395-408.
5. Buchwald G., van der Stoop P., Weichenrieder O., Perrakis A., van Lohuizen M., Sixma T.K. Structure and E3-ligase activity of the Ring-Ring complex of polycomb proteins Bmi1 and Ring1b. EMBO J. 2006, 25:2465-2474.
6. Burrell R.A., McGranahan N., Bartek J., Swanton C. The causes and consequences of genetic heterogeneity in cancer evolution. Nature 2013, 501:338-345.
7. Chan K.L., Hickson I.D. On the origins of ultra-fine anaphase bridges. Cell Cycle 2009, 8:3065-3066.
8. Chen J., Tang H., Wu Z., Zhou C., Jiang T., Xue Y., Huang G., Yan D., Peng Z. Overexpression of RBBP6, alone or combined with mutant TP53, is predictive of poor prognosis in colon cancer. PLoS ONE 2013, 8:e66524.
9. Chibi M., Meyer M., Skepu A., G Rees D.J., Moolman-Smook J.C., Pugh D.J. RBBP6 interacts with multifunctional protein YB-1 through its RING finger domain, leading to ubiquitination and proteosomal degradation of YB-1. J.Mol. Biol. 2008, 384:908-916.
10. Debatisse M., Le Tallec B., Letessier A., Dutrillaux B., Brison O. Common fragile sites: mechanisms of instability revisited. Trends Genet. 2012, 28:22-32.
11. Domínguez-Kelly R., Martín Y., Koundrioukoff S., Tanenbaum M.E., Smits V.A., Medema R.H., Debatisse M., Freire R. Wee1 controls genomic stability during replication by regulating the Mus81-Eme1 endonuclease. J.Cell Biol. 2011, 194:567-579.
12. Filion G.J., Zhenilo S., Salozhin S., Yamada D., Prokhortchouk E., Defossez P.A. A family of human zinc finger proteins that bind methylated DNA and repress transcription. Mol. Cell. Biol. 2006, 26:169-181.
13. Fungtammasan A., Walsh E., Chiaromonte F., Eckert K.A., Makova K.D. A genome-wide analysis of common fragile sites: what features determine chromosomal instability in the human genome?. Genome Res. 2012, 22:993-1005.
14. Germann S.M., Oestergaard V.H., Haas C., Salis P., Motegi A., Lisby M. Dpb11/TopBP1 plays distinct roles in DNA replication, checkpoint response and homologous recombination. DNA Repair (Amst.) 2011, 10:210-224.
15. Harrigan J.A., Belotserkovskaya R., Coates J., Dimitrova D.S., Polo S.E., Bradshaw C.R., Fraser P., Jackson S.P. Replication stress induces 53BP1-containing OPT domains in G1 cells. J.Cell Biol. 2011, 193:97-108.
16. Helmrich A., Ballarino M., Tora L. Collisions between replication and transcription complexes cause common fragile site instability at the longest human genes. Mol. Cell 2011, 44:966-977.
17. Im J.S., Ki S.H., Farina A., Jung D.S., Hurwitz J., Lee J.K. Assembly of the Cdc45-Mcm2-7-GINS complex in human cells requires the Ctf4/And-1, RecQL4, and Mcm10 proteins. Proc. Natl. Acad. Sci. USA 2009, 106:15628-15632.
18. Jacome A., Fernandez-Capetillo O. Lac operator repeats generate a traceable fragile site in mammalian cells. EMBO Rep. 2011, 12:1032-1038.
19. Kanke M., Kodama Y., Takahashi T.S., Nakagawa T., Masukata H. Mcm10 plays an essential role in origin DNA unwinding after loading of the CMG components. EMBO J. 2012, 31:2182-2194.
20. Kappo M.A., Ab E., Hassem F., Atkinson R.A., Faro A., Muleya V., Mulaudzi T., Poole J.O., McKenzie J.M., Chibi M., et al. Solution structure of RING finger-like domain of retinoblastoma-binding protein-6 (RBBP6) suggests it functions as a U-box. J.Biol. Chem. 2012, 287:7146-7158.
21. Kim W., Bennett E.J., Huttlin E.L., Guo A., Li J., Possemato A., Sowa M.E., Rad R., Rush J., Comb M.J., et al. Systematic and quantitative assessment of the ubiquitin-modified proteome. Mol. Cell 2011, 44:325-340.
22. Kote-Jarai Z., Olama A.A., Giles G.G., Severi G., Schleutker J., Weischer M., Campa D., Riboli E., Key T., Gronberg H., et al. Seven prostate cancer susceptibility loci identified by a multi-stage genome-wide association study. Nat. Genet. 2011, 43:785-791. UK Genetic Prostate Cancer Study Collaborators/British Association of Urological Surgeons' Section of Oncology, UK ProtecT Study Collaborators, The Australian Prostate Cancer BioResourceUK ProtecT Study Collaborators, The Australian Prostate Cancer BioResource, PRACTICAL ConsortiumPRACTICAL Consortium.
23. Koundrioukoff S., Carignon S., Técher H., Letessier A., Brison O., Debatisse M. Stepwise activation of the ATR signaling pathway upon increasing replication stress impacts fragile site integrity. PLoS Genet. 2013, 9:e1003643.
24. Kumagai A., Shevchenko A., Shevchenko A., Dunphy W.G. Treslin collaborates with TopBP1 in triggering the initiation of DNA replication. Cell 2010, 140:349-359.
25. Le Tallec B., Millot G.A., Blin M.E., Brison O., Dutrillaux B., Debatisse M. Common fragile site profiling in epithelial and erythroid cells reveals that most recurrent cancer deletions lie in fragile sites hosting large genes. Cell Rep. 2013, 4:420-428.
26. Letessier A., Millot G.A., Koundrioukoff S., Lachagès A.M., Vogt N., Hansen R.S., Malfoy B., Brison O., Debatisse M. Cell-type-specific replication initiation programs set fragility of the FRA3B fragile site. Nature 2011, 470:120-123.
27. Li L., Deng B., Xing G., Teng Y., Tian C., Cheng X., Yin X., Yang J., Gao X., Zhu Y., et al. PACT is a negative regulator of p53 and essential for cell growth and embryonic development. Proc. Natl. Acad. Sci. USA 2007, 104:7951-7956.
28. Lukas C., Savic V., Bekker-Jensen S., Doil C., Neumann B., Pedersen R.S., Grøfte M., Chan K.L., Hickson I.D., Bartek J., Lukas J. 53BP1 nuclear bodies form around DNA lesions generated by mitotic transmission of chromosomes under replication stress. Nat. Cell Biol. 2011, 13:243-253.
29. Mbita Z., Meyer M., Skepu A., Hosie M., Rees J., Dlamini Z. De-regulation of the RBBP6 isoform 3/DWNN in human cancers. Mol. Cell. Biochem. 2012, 362:249-262.
30. Miotto B., Struhl K. HBO1 histone acetylase is a coactivator of the replication licensing factor Cdt1. Genes Dev. 2008, 22:2633-2638.
31. Motadi L.R., Bhoola K.D., Dlamini Z. Expression and function of retinoblastoma binding protein 6 (RBBP6) in human lung cancer. Immunobiology 2011, 216:1065-1073.
32. Naim V., Wilhelm T., Debatisse M., Rosselli F. ERCC1 and MUS81-EME1 promote sister chromatid separation by processing late replication intermediates at common fragile sites during mitosis. Nat. Cell Biol. 2013, 15:1008-1015.
33. Ozeri-Galai E., Bester A.C., Kerem B. The complex basis underlying common fragile site instability in cancer. Trends Genet. 2012, 28:295-302.
34. Rouzeau S., Cordelières F.P., Buhagiar-Labarchède G., Hurbain I., Onclercq-Delic R., Gemble S., Magnaghi-Jaulin L., Jaulin C., Amor-Guéret M. Bloom's syndrome and PICH helicases cooperate with topoisomerase IIα in centromere disjunction before anaphase. PLoS ONE 2012, 7:e33905.
35. Sakai Y., Saijo M., Coelho K., Kishino T., Niikawa N., Taya Y. cDNA sequence and chromosomal localization of a novel human protein, RBQ-1 (RBBP6), that binds to the retinoblastoma gene product. Genomics 1995, 30:98-101.
36. Sasai N., Matsuda E., Sarashina E., Ishida Y., Kawaichi M. Identification of a novel BTB-zinc finger transcriptional repressor, CIBZ, that interacts with CtBP corepressor. Genes Cells 2005, 10:871-885.
37. Sasai N., Nakao M., Defossez P.A. Sequence-specific recognition of methylated DNA by human zinc-finger proteins. Nucleic Acids Res. 2010, 38:5015-5022.
38. Shi Y., Di Giammartino D.C., Taylor D., Sarkeshik A., Rice W.J., Yates J.R., Frank J., Manley J.L. Molecular architecture of the human pre-mRNA 3' processing complex. Mol. Cell 2009, 33:365-376.
39. Simons A., Melamed-Bessudo C., Wolkowicz R., Sperling J., Sperling R., Eisenbach L., Rotter V. PACT: cloning and characterization of a cellular p53 binding protein that interacts with Rb. Oncogene 1997, 14:145-155.
40. 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.
41. Sognier M.A., Hittelman W.N. Mitomycin-induced chromatid breaks in HeLa cells: a consequence of incomplete DNA replication. Cancer Res. 1986, 46:4032-4040.
42. Soutoglou E., Misteli T. Activation of the cellular DNA damage response in the absence of DNA lesions. Science 2008, 320:1507-1510.
43. Spandidos A., Wang X., Wang H., Seed B. PrimerBank: a resource of human and mouse PCR primer pairs for gene expression detection and quantification. Nucleic Acids Res. 2010, 38(Database issue):D792-D799.
44. Tanaka S., Komeda Y., Umemori T., Kubota Y., Takisawa H., Araki H. Efficient initiation of DNA replication in eukaryotes requires Dpb11/TopBP1-GINS interaction. Mol. Cell. Biol. 2013, 33:2614-2622.
45. Taylor M., Moore K., Murray J., Aves S.J., Price C. Mcm10 interacts with Rad4/Cut5(TopBP1) and its association with origins of DNA replication is dependent on Rad4/Cut5(TopBP1). DNA Repair (Amst.) 2011, 10:1154-1163.
46. Técher H., Koundrioukoff S., Azar D., Wilhelm T., Carignon S., Brison O., Debatisse M., Le Tallec B. Replication dynamics: biases and robustness of DNA fiber analysis. J.Mol. Biol. 2013, 425:4845-4855.
47. Thu Y.M., Bielinsky A.K. Enigmatic roles of Mcm10 in DNA replication. Trends Biochem. Sci. 2013, 38:184-194.
48. van Deursen F., Sengupta S., De Piccoli G., Sanchez-Diaz A., Labib K. Mcm10 associates with the loaded DNA helicase at replication origins and defines a novel step in its activation. EMBO J. 2012, 31:2195-2206.
49. Watase G., Takisawa H., Kanemaki M.T. Mcm10 plays a role in functioning of the eukaryotic replicative DNA helicase, Cdc45-Mcm-GINS. Curr. Biol. 2012, 22:343-349.
50. Wawrousek K.E., Fortini B.K., Polaczek P., Chen L., Liu Q., Dunphy W.G., Campbell J.L. Xenopus DNA2 is a helicase/nuclease that is found in complexes with replication proteins And-1/Ctf4 and Mcm10 and DSB response proteins Nbs1 and ATM. Cell Cycle 2010, 9:1156-1166.
51. Yamada D., Pérez-Torrado R., Filion G., Caly M., Jammart B., Devignot V., Sasai N., Ravassard P., Mallet J., Sastre-Garau X., et al. The human protein kinase HIPK2 phosphorylates and downregulates the methyl-binding transcription factor ZBTB4. Oncogene 2009, 28:2535-2544.
52. Ying S., Minocherhomji S., Chan K.L., Palmai-Pallag T., Chu W.K., Wass T., Mankouri H.W., Liu Y., Hickson I.D. MUS81 promotes common fragile site expression. Nat. Cell Biol. 2013, 15:1001-1007.
53. Yoshida K., Inoue I. Expression of MCM10 and TopBP1 is regulated by cell proliferation and UV irradiation via the E2F transcription factor. Oncogene 2004, 23:6250-6260.
54. Yoshitake Y., Nakatsura T., Monji M., Senju S., Matsuyoshi H., Tsukamoto H., Hosaka S., Komori H., Fukuma D., Ikuta Y., et al. Proliferation potential-related protein, an ideal esophageal cancer antigen for immunotherapy, identified using complementary DNA microarray analysis. Clin. Cancer Res. 2004, 10:6437-6448.
55. Zhu W., Ukomadu C., Jha S., Senga T., Dhar S.K., Wohlschlegel J.A., Nutt L.K., Kornbluth S., Dutta A. Mcm10 and And-1/CTF4 recruit DNA polymerase alpha to chromatin for initiation of DNA replication. Genes Dev. 2007, 21:2288-2299.