Quantitative "Fragmentome" mapping reveals novel, domain-specific partners for the modular protein RepoMan (Recruits PP1 onto mitotic chromatin at anaphase)

Molecular and Cellular Proteomics

Volumn 12, Issue 5, 2013, Pages 1468-1486

  Prévost, Michèle ^a   Chamousset, Delphine ^a   Nasa, Isha ^b   Freele, Emily ^a   Morrice, Nick ^c   Moorhead, Greg ^b   Trinkle Mulcahy, Laura ^a  

^a UNIVERSITY OF OTTAWA   (Canada)

^b UNIVERSITY OF CALGARY   (Canada)

^c BEATSON INSTITUTE FOR CANCER RESEARCH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

PHOSPHOPROTEIN PHOSPHATASE 1; REPOMAN; RIBOSOME PROTEIN; UNCLASSIFIED DRUG;

ANAPHASE; ARTICLE; CHROMATIN; CONTROLLED STUDY; CYTOPLASM; DNA DAMAGE; FLUORESCENCE IMAGING; FOLLOW UP; FRAGMENTATION REACTION; GENE MAPPING; HUMAN; MITOSIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN METABOLISM; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; PROTEOMICS; SIGNAL NOISE RATIO; VALIDATION STUDY;

CARRIER PROTEINS; CELL CYCLE PROTEINS; HELA CELLS; HUMANS; MITOSIS; MULTIPROTEIN COMPLEXES; NUCLEAR PROTEINS; PEPTIDE FRAGMENTS; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN INTERACTION MAPPING; PROTEIN PHOSPHATASE 2; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN SUBUNITS; PROTEOME; RECEPTORS, NEUROPEPTIDE Y;

EID: 84877604649     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M112.023291     Document Type: Article

References (48)

1. Trinkle-Mulcahy, L., Andersen, J., Lam, Y. W., Moorhead, G., Mann, M., and Lamond, A. I. (2006) Repo-Man recruits PP1 gamma to chromatin and is essential for cell viability. J. Cell Biol. 172, 679-692
2. Vagnarelli, P., Hudson, D. F., Ribeiro, S. A., Trinkle-Mulcahy, L., Spence, J. M., Lai, F., Farr, C. J., Lamond, A. I., and Earnshaw, W. C. (2006) Condensin and Repo-Man-PP1 co-operate in the regulation of chromosome architecture during mitosis. Nat. Cell Biol. 8, 1133-1142 (Pubitemid 44473609)
3. Wurzenberger, C., Held, M., Lampson, M. A., Poser, I., Hyman, A. A., and Gerlich, D. W. (2012) Sds22 and Repo-Man stabilize chromosome segregation by counteracting Aurora B on anaphase kinetochores. J. Cell Biol. 198, 173-183
4. Qian J, Lesage B, Beullens M, Van Eynde A, Bollen M. (2011) PP1/Repoman dephosphorylates mitotic histone H3 at T3 and regulates chromosomal aurora B targeting. Current Biol. 21, 766-773
5. Vagnarelli, P., Ribeiro, S., Sennels, L., Sanchez-Pulido, L., de Lima Alves, F., Verheyen, T., Kelly, D. A., Ponting, C. P., Rappsilber, J., and Earnshaw, W. C. (2011) Repo-man coordinates chromosomal reorganization with nuclear envelope reassembly during mitotic exit. Cell 21, 328-342
6. Moorhead, G. B., Trinkle-Mulcahy, L., and Ulke-Lemée, A. (2007) Emerging roles of nuclear protein phosphatases. Nat. Rev. Mol. Cell Biol. 8, 234-244
7. Ceulemans, H., and Bollen, M. (2004) Functional diversity of protein phosphatase-1, a cellular economizer and reset button. Physiol. Rev. 84, 1-39 (Pubitemid 38049874)
8. Peng, A., Lewellyn, A. L., Schiemann, W. P., and Maller, J. L. (2010) Repo-man controls a protein phosphatase 1-dependent threshold for DNA damage checkpoint activation. Current Biol. 20, 387-396
9. 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
10. Trinkle-Mulcahy, L. (2012) Resolving protein interactions and complexes by affinity purification followed by label-based quantitative mass spectrometry. Proteomics 12, 1623-1638
11. Selbach, M., and Mann, M. (2006) Protein interaction screening by quantitative immunoprecipitation combined with knockdown (QUICK). Nat Meth 3, 981-983 (Pubitemid 44782696)
12. Lam, Y. W., Lamond, A. I., Mann, M., and Andersen, J. S. (2007) Analysis of nucleolar protein dynamics reveals the nuclear degradation of ribosomal proteins. Current Biol. 17, 749-760 (Pubitemid 46635118)
13. Chamousset, D., De Wever, V., Moorhead, G. B., Chen, Y., Boisvert, F. M., Lamond, A. I., and Trinkle-Mulcahy, L. (2010) RRP1B targets PP1 to mammalian cell nucleoli and is associated with Pre-60S ribosomal subunits. Mol. Biol. Cell 21, 4212-4226
14. Trinkle-Mulcahy, L., Sleeman, J. E., and Lamond, A. I. (2001) Dynamic targeting of protein phosphatase 1 within the nuclei of living mammalian cells. J. Cell Sci. 114, 4219-4228 (Pubitemid 33138659)
15. Chamousset, D., Mamane, S., Boisvert, F. M., and Trinkle-Mulcahy, L. (2010) Efficient extraction of nucleolar proteins for interactome analyses. Proteomics 10, 3045-3050
16. 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
17. Cox, J., Neuhauser, N., Michalski, A., Scheltema, R. A., Olsen, J. V., and Mann, M. (2011) Andromeda: A peptide search engine integrated into the MaxQuant environment. J. Proteome Res. 10, 1794-1805
18. Linding, R. (2003) GlobPlot: exploring protein sequences for globularity and disorder. Nucleic Acids Res. 31, 3701-3708
19. Scott, M. S., Boisvert, F. M., McDowall, M. D., Lamond, A. I., and Barton, G. J. (2010) Characterization and prediction of protein nucleolar localization sequences. Nucleic Acids Res. 38, 7388-7399
20. McCright, B., Rivers, A. M., Audlin, S., and Virshup, D. M. (1996) The B56 family of protein phosphatase 2A (PP2A) regulatory subunits encodes differentiation-induced phosphoproteins that target PP2A to both nucleus and cytoplasm*. J. Biol. Chem. 271, 22081-22089 (Pubitemid 26303837)
21. Lee, T. Y., Lai, T. Y., Lin, S. C., Wu, C. W., Ni, I. F., Yang, Y. S., Hung, L. Y., Law, B. K., and Chiang, C. W. (2010) The B56γ3 regulatory subunit of protein phosphatase 2A (PP2A) regulates S phase-specific nuclear accumulation of PP2A and the G1 to S transition. J. Biol. Chem. 285, 21567-21580
22. Kinoshita, E. (2005) Phosphate-binding Tag, a new tool to visualize phosphorylated proteins. Mol. Cell. Proteomics 5, 749-757
23. Kettenbach, A. N., Schweppe, D. K., Faherty, B. K., Pechenick, D., Pletnev, A. A., and Gerber, S. A. (2011) Quantitative phosphoproteomics identifies substrates and functional modules of aurora and polo-like kinase activities in mitotic cells. Sci. Signal. 4, 1-15
24. Dephoure, N., Zhou, C., Villen, J., Beausoleil, S. A., Bakalarski, C. E., Elledge, S. J., and Gygi, S. P. (2008) A quantitative atlas of mitotic phosphorylation. Proc. Natl. Acad. Sci. U. S. A. 105, 10762-10767
25. Stoldt, S., Wenzel, D., Schulze, E., Doenecke, D., and Happel, N. (2007) G1 phase-dependent nucleolar accumulation of human histone H1x. Biol. Cell 99, 541-552 (Pubitemid 47543312)
26. Mayya, V., Lundgren, D. H., Hwang, S. I., Rezaul, K., Wu, L., Eng, J. K., Rodionov, V., and Han, D. K. (2009) Quantitative phosphoproteomic analysis of T cell receptor signaling reveals system-wide modulation of protein-protein interactions. Science Signaling 2:ra46
27. Wang, B., Malik, R., Nigg, E. A., and Körner, R. (2008) Evaluation of the low-specificity protease elastase for large-scale phosphoproteome analysis. Anal. Chem. 80, 9526-9533
28. Yu, L. R., Zhu, Z., Chan, K. C., Issaq, H. J., Dimitrov, D. S., and Veenstra, T. D. (2007) Improved titanium dioxide enrichment of phosphopeptides from HeLa cells and high confident phosphopeptide identification by cross-validation of MS/MS and MS/MS/MS spectra. J. Proteome Res. 6, 4150-4162 (Pubitemid 350158493)
29. Olsen, J. V., Blagoev, B., Gnad, F., Macek, B., Kumar, C., Mortensen, P., and Mann, M. (2006) Global, in vivo, and site-specific phosphorylation dynamics in signaling networks. Cell 127, 635-648 (Pubitemid 44647421)
30. Malik, R., Lenobel, R., Santamaria, A., Ries, A., Nigg, E. A., Körner R. (2009) Quantitative analysis of the human spindle phosphoproteome at distinct mitotic stages. J. Proteome Res. 8, 4553-4563
31. Hubner, N. C., Bird, A. W., Cox, J., Splettstoesser, B., Bandilla, P., Poser, I., Hyman, A., and Mann, M. (2010) Quantitative proteomics combined with BAC TransgeneOmics reveals in vivo protein interactions. J. Cell Biol.189, 739-754
32. Kitajima, T. S., Sakuno, T., Ishiguro, K. I., Iemura, S. I., Natsume, T., Kawashima, S. A., and Watanabe, Y. (2006) Shugoshin collaborates with protein phosphatase 2A to protect cohesin. EMBO J. 441, 46-52
33. Foley, E. A., Maldonado, M., and Kapoor, T. M. (2011) Formation of stable attachments between kinetochores and microtubules depends on the B56-PP2A phosphatase. EMBO J. 13, 1265-1271
34. Herzog, F., Kahraman, A., Boehringer, D., Mak, R., Bracher, A., Walzthoeni, T., Leitner, A., Beck, M., Hartl, F. U., Ban, N., Malmstrom, L., and Aebersold, R. (2012) Structural probing of a protein phosphatase 2A network by chemical cross-linking and mass spectrometry. Science 337, 1348-1352
35. Nardozzi JD, Lott K, Cingolani G. (2010) Phosphorylation meets nuclear import: a review. Cell Commun. Signal. 8, 32
36. Kitamura, R., Sekimoto, T., Ito, S., Harada, S., Yamagata, H., Masai, H., Yoneda, Y., and Yanagi, K. (2006) Nuclear import of Epstein-Barr virus nuclear antigen 1 mediated by NPI-1 (Importin α5) is up- and down-regulated by phosphorylation of the nuclear localization signal for which Lys379 and Arg380 are essential. J. Virol. 80, 1979-1991 (Pubitemid 43228738)
37. Xiao, C. Y. (1997) SV40 large tumor antigen nuclear import is regulated by the double-stranded DNA-dependent protein kinase site (serine 120) flanking the nuclear localization sequence. J. Biol. Chem. 272, 22191-22198
38. Kondoh, K., Terasawa, K., Morimoto, H., and Nishida, E. (2006) Regulation of nuclear translocation of extracellular signal-regulated kinase 5 by active nuclear import and export mechanisms. Mol. Cell. Biol. 26, 1679-1690
39. Morimoto, H., Kondoh, K., Nishimoto, S., Terasawa, K., and Nishida, E. (2007) Activation of a C-terminal transcriptional activation domain of ERK5 by autophosphorylation. J. Biol. Chem. 282, 35449-35456 (Pubitemid 350277147)
40. Kehlenbach, R. H. (2000) Phosphorylation of the nuclear transport machinery down-regulates nuclear protein import in vitro. J. Biol. Chem. 275, 17848-17856
41. De Wever, V., Reiter, W., Ballarini, A., Ammerer, G., and Brocard, C. (2005) A dual role for PP1 in shaping the Msn2-dependent transcriptional response to glucose starvation. EMBO J. 24, 4115-4123 (Pubitemid 41752880)
42. Jäkel, S., Albig, W., Kutay, U., Bischoff, F. R., Schwamborn, K., Doenecke, D., and Görlich, D. (1999) The importin β/importin 7 heterodimer is a functional nuclear import receptor for histone H1. EMBO J. 18, 2411-2423
43. Plafker, S. M., and Macara, I. G. (2002) Ribosomal protein L12 uses a distinct nuclear import pathway mediated by importin 11. Mol. Cell. Biol. 22, 1266-1275 (Pubitemid 34094861)
44. Bridges, D., and Moorhead, G. B. G. (2004) 14-3-3 Proteins: a number of functions for a numbered protein. Sci. Signal. 242:re10
45. Hill, R., and Lee, P. W. (2010) The DNA-dependent protein kinase (DNAPK): More than just a case of making ends meet? Cell Cycle 9, 3460-3469
46. Kunkel, T. A., and Erie, D. A. (2005) DNA Mismatch Repair*. Annu. Rev. Biochem. 74, 681-710
47. Li, X., andSchimenti, J. C. (2007) Mouse pachytene checkpoint 2 (Trip13) is required for completing meiotic recombination but not synapsis. PLoS Genet. 3, e130
48. Douglas, P., Zhong, J., Ye, R., Moorhead, G. B., Xu, X., and Lees-Miller, S. P. (2010) Protein phosphatase 6 interacts with the DNA-dependent protein kinase catalytic subunit and dephosphorylates γ-H2AX. Mol. Cell. Biol. 30, 1368-1381