Quantitative proteomics reveals dynamic interactions of the minichromosome maintenance complex (MCM) in the cellular response to etoposide induced DNA damage

Molecular and Cellular Proteomics

Volumn 14, Issue 7, 2015, Pages 2002-2013

  Drissi, Romain ^a   Dubois, Marie Line ^a   Douziech, Mélanie ^a   Boisvert, François Michel ^a  

^a UNIVERSITÉ DE SHERBROOKE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CHROMODOMAIN HELICASE DNA BINDING PROTEIN 3; ETOPOSIDE; GREEN FLUORESCENT PROTEIN; HISTONE CHAPERONE ASF1; HISTONE H2AX; HYBRID PROTEIN; IMPORTIN 7; MINICHROMOSOME MAINTENANCE PROTEIN; PROTEIN; UNCLASSIFIED DRUG; NONHISTONE PROTEIN; PROTEIN BINDING;

ARTICLE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CONTROLLED STUDY; DNA DAMAGE; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; ISOTOPE LABELING; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEOMICS; QUANTITATIVE ANALYSIS; QUANTITATIVE ASSAY; STABLE ISOTOPE LABELING WITH AMINO ACIDS IN CELL CULTURE; UBIQUITINATION; AMINO ACID SEQUENCE; CELL FRACTIONATION; CHEMISTRY; DRUG EFFECTS; METABOLISM; MOLECULAR GENETICS; PROCEDURES; PROTEIN TRANSPORT; TUMOR CELL LINE;

EUKARYOTA;

AMINO ACID SEQUENCE; CELL LINE, TUMOR; CHROMOSOMAL PROTEINS, NON-HISTONE; DNA DAMAGE; ETOPOSIDE; GREEN FLUORESCENT PROTEINS; HUMANS; MINICHROMOSOME MAINTENANCE PROTEINS; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN TRANSPORT; PROTEOMICS; SUBCELLULAR FRACTIONS;

EID: 84936764814     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M115.048991     Document Type: Article

References (44)

1. Blow, J. J., and Gillespie, P. J. (2008) Replication licensing and cancer-a fatal entanglement? Nat. Rev. Cancer 8, 799-806.
2. Blow, J. J., and Dutta, A. (2005) Preventing re-replication of chromosomal DNA. Nature Rev. 6, 476-486.
3. Allen, C., Ashley, A. K., Hromas, R., and Nickoloff, J. A. (2011) More forks on the road to replication stress recovery. J. Mol. Cell. Biol. 3, 4-12.
4. Nam, E. A., and Cortez, D. (2011) ATR signalling: More than meeting at the fork. Biochem. J. 436, 527-536.
5. Bell, S. D., and Botchan, M. R. (2013) The minichromosome maintenance replicative helicase. Perspectives Biol. 5, a012807.
6. Sclafani, R. A., Fletcher, R. J., and Chen, X. S. (2004) Two heads are better than one: Regulation of DNA replication by hexameric helicases. Genes Development 18, 2039-2045.
7. Maiorano, D., Lutzmann, M., and Mechali, M. (2006) MCM proteins and DNA replication. Current Opinion Cell Biol. 18, 130-136.
8. Bochman, M. L., and Schwacha, A. (2009) The Mcm complex: unwinding the mechanism of a replicative helicase. Microbiol. Mol. Biol. Rev. 73, 652-683.
9. Arias, E. E., and Walter, J. C. (2007) Strength in numbers: preventing rereplication via multiple mechanisms in eukaryotic cells. Genes Develop. 21, 497-518.
10. Bailis, J. M., and Forsburg, S. L. (2004) MCM proteins: DNA damage, mutagenesis and repair. Curr. Opin. Genet. Dev. 14, 17-21.
11. Forsburg, S. L. (2004) Eukaryotic MCM proteins: Beyond replication initiation. Microbiol. Mol. Biol. Rev. 68, 109-131.
12. Bailis, J. M., and Forsburg, S. L. (2004) MCM proteins: DNA damage, mutagenesis and repair. Curr. Opin. Genet. Dev. 14, 17-21.
13. Das, M., Singh, S., Pradhan, S., and Narayan, G. (2014) MCM Paradox: Abundance of eukaryotic replicative helicases and genomic integrity. Mol. Biol. Int. 2014:574850.
14. Crevel, I., Crevel, G., Gostan, T., de Renty, C., Coulon, V., and Cotterill, S. (2011) Decreased MCM2-6 in Drosophila S2 cells does not generate significant DNA damage or cause a marked increase in sensitivity to replication interference. PLoS One 6, e27101.
15. Crevel, G., Hashimoto, R., Vass, S., Sherkow, J., Yamaguchi, M., Heck, M. M., and Cotterill, S. (2007) Differential requirements for MCM proteins in DNA replication in Drosophila S2 cells. PLoS One 2, e833.
16. Lei, M., Kawasaki, Y., and Tye, B. K. (1996) Physical interactions among Mcm proteins and effects of Mcm dosage on DNA replication in Saccharomyces cerevisiae. Mol. Cell. Biol. 16, 5081-5090.
17. Oehlmann, M., Score, A. J., and Blow, J. J. (2004) The role of Cdc6 in ensuring complete genome licensing and S phase checkpoint activation. J. Cell Biol. 165, 181-190.
18. Ibarra, A., Schwob, E., and Mendez, J. (2008) Excess MCM proteins protect human cells from replicative stress by licensing backup origins of replication. Proc. Natl. Acad. Sci. U.S.A. 105, 8956-8961.
19. Ong, S. E., Blagoev, B., Kratchmarova, I., Kristensen, D. B., Steen, H., Pandey, A., and Mann, M. (2002) Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Mol. Cell. Proteomics 1, 376-386.
20. Trinkle-Mulcahy, L., Boulon, S., Lam, Y. W., Urcia, R., Boisvert, F. M., Vandermoere, F., Morrice, N. A., Swift, S., Rothbauer, U., Leonhardt, H., and Lamond, A. (2008) Identifying specific protein interaction partners using quantitative mass spectrometry and bead proteomes. J. Cell Biol. 183, 223-239.
21. Montecucco, A., and Biamonti, G. (2007) Cellular response to etoposide treatment. Cancer Lett. 252, 9-18.
22. Torres, J. Z., Miller, J. J., and Jackson, P. K. (2009) High-throughput generation of tagged stable cell lines for proteomic analysis. Proteomics 9, 2888-2891.
23. Shevchenko, A., Wilm, M., Vorm, O., and Mann, M. (1996) Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal. Chem. 68, 850-858.
24. Cox, J., and Mann, M. (2008) MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol. 26, 1367-1372.
25. Cox, J., Matic, I., Hilger, M., Nagaraj, N., Selbach, M., Olsen, J. V., and Mann, M. (2009) A practical guide to the MaxQuant computational platform for SILAC-based quantitative proteomics. Nat. Protocols 4, 698-705.
26. Boisvert, F. M., Lam, Y. W., Lamont, D., and Lamond, A. I. (2010) A quantitative proteomics analysis of subcellular proteome localization and changes induced by DNA damage. Mol. Cell. Proteomics 9, 457-470.
27. Spiess, C., Meyer, A. S., Reissmann, S., and Frydman, J. (2004) Mechanism of the eukaryotic chaperonin: protein folding in the chamber of secrets. Trends Cell Biol. 14, 598-604.
28. Maiorano, D., Lemaitre, J. M., and Mechali, M. (2000) Stepwise regulated chromatin assembly of MCM2-7 proteins. J. Biol. Chem. 275, 8426-8431.
29. Sheu, Y. J., and Stillman, B. (2006) Cdc7-Dbf4 phosphorylates MCM proteins via a docking site-mediated mechanism to promote S phase progression. Mol. Cell 24, 101-113.
30. Kulartz, M., Hiller, E., Kappes, F., Pinna, L. A., and Knippers, R. (2004) Protein kinase CK2 phosphorylates the cell cycle regulatory protein Geminin. Biochem.Biophys. Res. Commun. 315, 1011-1017.
31. Kim, S. T., Lim, D. S., Canman, C. E., and Kastan, M. B. (1999) Substrate specificities and identification of putative substrates of ATM kinase family members. J. Biol. Chem. 274, 37538-37543.
32. O'Neill, T., Dwyer, A. J., Ziv, Y., Chan, D. W., Lees-Miller, S. P., Abraham, R. H., Lai, J. H., Hill, D., Shiloh, Y., Cantley, L. C., and Rathbun, G. A. (2000) Utilization of oriented peptide libraries to identify substrate motifs selected by ATM. J. Biol. Chem. 275, 22719-22727.
33. Hershko, A., Heller, H., Elias, S., and Ciechanover, A. (1983) Components of ubiquitin-protein ligase system. Resolution, affinity purification, and role in protein breakdown. J. Biol. Chem. 258, 8206-8214.
34. Marotti, L. A. Jr., Newitt, R., Wang, Y., Aebersold, R., and Dohlman, H. G. (2002) Direct identification of a G protein ubiquitination site by mass spectrometry. Biochemistry 41, 5067-5074.
35. Peng, J., and Gygi, S. P. (2001) Proteomics: The move to mixtures. J. Mass Spectrom. 36, 1083-1091.
36. Sakwe, A. M., Nguyen, T., Athanasopoulos, V., Shire, K., and Frappier, L. (2007) Identification and characterization of a novel component of the human minichromosome maintenance complex. Mol. Cell. Biol. 27, 3044-3055.
37. Goodarzi, A. A., Kurka, T., and Jeggo, P. A. (2011) KAP-1 phosphorylation regulates CHD3 nucleosome remodeling during the DNA double-strand break response. Nat. Structural Mol. Biol. 18, 831-839.
38. Brunton, H., Goodarzi, A. A., Noon, A. T., Shrikhande, A., Hansen, R. S., Jeggo, P. A., and Shibata, A. (2011) Analysis of human syndromes with disordered chromatin reveals the impact of heterochromatin on the efficacy of ATM-dependent G2/M checkpoint arrest. Mol. Cell. Biol. 31, 4022-4035.
39. Larsen, D. H., Poinsignon, C., Gudjonsson, T., Dinant, C., Payne, M. R., Hari, F. J., Rendtlew Danielsen, J. M., Menard, P., Sand, J. C., Stucki, M., Lukas, C., Bartek, J., Andersen, J. S., and Lukas, J. (2010) The chromatin- remodeling factor CHD4 coordinates signaling and repair after DNA damage. J. Cell Biol. 190, 731-740.
40. Campos, E. I., Fillingham, J., Li, G., Zheng, H., Voigt, P., Kuo, W. H., Seepany, H., Gao, Z., Day, L. A., Greenblatt, J. F., and Reinberg, D. (2010) The program for processing newly synthesized histones H3.1 and H4. Nat. Structural Mol. Biol. 17, 1343-1351.
41. Xu, M., Long, C., Chen, X., Huang, C., Chen, S., and Zhu, B. (2010) Partitioning of histone H3-H4 tetramers during DNA replication-dependent chromatin assembly. Science 328, 94-98.
42. Groth, A., Corpet, A., Cook, A. J., Roche, D., Bartek, J., Lukas, J., and Almouzni, G. (2007) Regulation of replication fork progression through histone supply and demand. Science 318, 1928-1931.
43. Demartino, G. N., and Gillette, T. G. (2007) Proteasomes: Machines for all reasons. Cell 129, 659-662.
44. Motegi, A., Murakawa, Y., and Takeda, S. (2009) The vital link between the ubiquitin-proteasome pathway and DNA repair: Impact on cancer therapy. Cancer Lett. 283, 1-9.