Human-chromatin-related protein interactions identify a demethylase complex required for chromosome segregation

Cell Reports

Volumn 8, Issue 1, 2014, Pages 297-310

  Marcon, Edyta ^a   Ni, Zuyao ^a   Pu, Shuye ^b   Turinsky, Andrei L ^b   Trimble, SandraSmiley ^c   Olsen, Jonathan B ^c   Silverman Gavrila, Rosalind ^a   Silverman Gavrila, Lorelei ^c   Phanse, Sadhna ^a   Guo, Hongbo ^a   Zhong, Guoqing ^a   Guo, Xinghua ^a   Young, Peter ^a   Bailey, Swneke ^c,d   Roudeva, Denitza ^c   Zhao, Dorothy ^c   Hewel, Johannes ^a   Li, Joyce ^a   Gräslund, Susanne ^a   Paduch, Marcin ^e   Kossiakoff, Anthony A ^e   Lupien, Mathieu ^c,d,f   Emili, Andrew ^a,c   Wodak, Shoshana J ^b,c   Greenblatt, Jack ^a,c   more..

^a UNIVERSITY OF TORONTO   (Canada)

^b HOSPITAL FOR SICK CHILDREN RESEARCH INSTITUTE   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

^d PRINCESS MARGARET HOSPITAL   (Canada)

^e UNIVERSITY OF CHICAGO   (United States)

^f ONTARIO INSTITUTE FOR CANCER RESEARCH   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; CELL ENZYME; DEMETHYLASE; KDM8 PROTEIN; RCCD1 PROTEIN; UNCLASSIFIED DRUG; CARRIER PROTEIN; CHROMATIN; HISTONE DEMETHYLASE; KDM8 PROTEIN, HUMAN; MEMBRANE PROTEIN; PROTEIN BINDING; RCCD1 PROTEIN, HUMAN;

ARTICLE; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMOSOME SEGREGATION; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME ASSAY; HUMAN; HUMAN CELL; MASS SPECTROMETRY; MOLECULAR DYNAMICS; PREDICTION; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; GENETICS; HEK293 CELL LINE; METABOLISM;

CARRIER PROTEINS; CHROMATIN; CHROMOSOME SEGREGATION; HEK293 CELLS; HISTONE DEMETHYLASES; HUMANS; MEMBRANE PROTEINS; PROTEIN BINDING;

EID: 84904050623     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2014.05.050     Document Type: Article

References (44)

1. Babu M., Vlasblom J., Pu S., Guo X., Graham C., Bean B.D., Burston H.E., Vizeacoumar F.J., Snider J., Phanse S., et al. Interaction landscape ofmembrane-protein complexes in Saccharomyces cerevisiae. Nature 2012, 489:585-589.
2. Bergmann J.H., Rodríguez M.G., Martins N.M., Kimura H., Kelly D.A., Masumoto H., Larionov V., Jansen L.E., Earnshaw W.C. Epigenetic engineering shows H3K4me2 is required for HJURP targeting and CENP-A assembly on a synthetic human kinetochore. EMBO J. 2011, 30:328-340.
3. Black J.C., Van Rechem C., Whetstine J.R. Histone lysine methylation dynamics: establishment, regulation, and biological impact. Mol. Cell 2012, 48:491-507.
4. Choi H., Larsen B., Lin Z.Y., Breitkreutz A., Mellacheruvu D., Fermin D., Qin Z.S., Tyers M., Gingras A.C., Nesvizhskii A.I. SAINT: probabilistic scoring of affinity purification-mass spectrometry data. Nat. Methods 2011, 8:70-73.
5. Clarke P.R., Zhang C. Spatial and temporal coordination of mitosis by Ran GTPase. Nat. Rev. Mol. Cell Biol. 2008, 9:464-477.
6. Collins S.R., Miller K.M., Maas N.L., Roguev A., Fillingham J., Chu C.S., Schuldiner M., Gebbia M., Recht J., Shales M., et al. Functional dissection of protein complexes involved in yeast chromosome biology using a genetic interaction map. Nature 2007, 446:806-810.
7. Dasso M., Nishitani H., Kornbluth S., Nishimoto T., Newport J.W. RCC1, a regulator of mitosis, is essential for DNA replication. Mol. Cell. Biol. 1992, 12:3337-3345.
8. Gavin A.C., Aloy P., Grandi P., Krause R., Boesche M., Marzioch M., Rau C., Jensen L.J., Bastuck S., Dümpelfeld B., et al. Proteome survey reveals modularity of the yeast cell machinery. Nature 2006, 440:631-636.
9. Goudreault M., D'Ambrosio L.M., Kean M.J., Mullin M.J., Larsen B.G., Sanchez A., Chaudhry S., Chen G.I., Sicheri F., Nesvizhskii A.I., et al. A PP2A phosphatase high density interaction network identifies a novel striatin-interacting phosphatase and kinase complex linked to the cerebral cavernous malformation 3 (CCM3) protein. Mol. Cell. Proteomics 2009, 8:157-171.
10. Guruharsha K.G., Rual J.F., Zhai B., Mintseris J., Vaidya P., Vaidya N., Beekman C., Wong C., Rhee D.Y., Cenaj O., et al. A protein complex network of Drosophila melanogaster. Cell 2011, 147:690-703.
11. Hart G.T., Lee I., Marcotte E.R. A high-accuracy consensus map of yeast protein complexes reveals modular nature of gene essentiality. BMC Bioinformatics 2007, 8:236.
12. Havugimana P.C., Hart G.T., Nepusz T., Yang H., Turinsky A.L., Li Z., Wang P.I., Boutz D.R., Fong V., Phanse S., et al. A census of human soluble protein complexes. Cell 2012, 150:1068-1081.
13. Hayakawa T., Ohtani Y., Hayakawa N., Shinmyozu K., Saito M., Ishikawa F., Nakayama J. RBP2 is an MRG15 complex component and down-regulates intragenic histone H3 lysine 4 methylation. Genes Cells 2007, 12:811-826.
14. Hegemann B., Hutchins J.R., Hudecz O., Novatchkova M., Rameseder J., Sykora M.M., Liu S., Mazanek M., Lénárt P., Hériché J.K., et al. Systematic phosphorylation analysis of human mitotic protein complexes. Sci. Signal. 2011, 4:rs12.
15. Hong S., Cho Y.W., Yu L.R., Yu H., Veenstra T.D., Ge K. Identification of JmjC domain-containing UTX and JMJD3 as histone H3 lysine 27 demethylases. Proc. Natl. Acad. Sci. USA 2007, 104:18439-18444.
16. Hou H., Yu H. Structural insights into histone lysine demethylation. Curr. Opin. Struct. Biol. 2010, 20:739-748.
17. Hsia D.A., Tepper C.G., Pochampalli M.R., Hsia E.Y., Izumiya C., Huerta S.B., Wright M.E., Chen H.W., Kung H.J., Izumiya Y. KDM8, a H3K36me2 histone demethylase that acts in the cyclin A1 coding region to regulate cancer cell proliferation. Proc. Natl. Acad. Sci. USA 2010, 107:9671-9676.
18. Ishimura A., Minehata K., Terashima M., Kondoh G., Hara T., Suzuki T. Jmjd5, an H3K36me2 histone demethylase, modulates embryonic cell proliferation through the regulation of Cdkn1a expression. Development 2012, 139:749-759.
19. Jelinic P., Pellegrino J., David G. A novel mammalian complex containing Sin3B mitigates histone acetylation and RNA polymerase II progression within transcribed loci. Mol. Cell. Biol. 2011, 31:54-62.
20. Joshi P., Greco T.M., Guise A.J., Luo Y., Yu F., Nesvizhskii A.I., Cristea I.M. The functional interactome landscape of the human histone deacetylase family. Mol. Syst. Biol. 2013, 9:672.
21. Kooistra S.M., Helin K. Molecular mechanisms and potential functions of histone demethylases. Nat. Rev. Mol. Cell Biol. 2012, 13:297-311.
22. Krogan N.J., Cagney G., Yu H., Zhong G., Guo X., Ignatchenko A., Li J., Pu S., Datta N., Tikuisis A.P., et al. Global landscape of protein complexes in the yeast Saccharomyces cerevisiae. Nature 2006, 440:637-643.
23. Lan F., Bayliss P.E., Rinn J.L., Whetstine J.R., Wang J.K., Chen S., Iwase S., Alpatov R., Issaeva I., Canaani E., et al. A histone H3 lysine 27 demethylase regulates animal posterior development. Nature 2007, 449:689-694.
24. Lee N., Erdjument-Bromage H., Tempst P., Jones R.S., Zhang Y. The H3K4 demethylase lid associates with and inhibits histone deacetylase Rpd3. Mol. Cell. Biol. 2009, 29:1401-1410.
25. Lin S., Shen H., Li J.L., Tang S., Gu Y., Chen Z., Hu C., Rice J.C., Lu J., Wu L. Proteomic and functional analyses reveal the role of chromatin reader SFMBT1 in regulating epigenetic silencing and the myogenic gene program. J.Biol. Chem. 2013, 288:6238-6247.
26. Mak A.B., Ni Z., Hewel J.A., Chen G.I., Zhong G., Karamboulas K., Blakely K., Smiley S., Marcon E., Roudeva D., et al. A lentiviral functional proteomics approach identifies chromatin remodeling complexes important for the induction of pluripotency. Mol. Cell. Proteomics 2010, 9:811-823.
27. Malovannaya A., Li Y., Bulynko Y., Jung S.Y., Wang Y., Lanz R.B., O'Malley B.W., Qin J. Streamlined analysis schema for high-throughput identification of endogenous protein complexes. Proc. Natl. Acad. Sci. USA 2010, 107:2431-2436.
28. Malovannaya A., Lanz R.B., Jung S.Y., Bulynko Y., Le N.T., Chan D.W., Ding C., Shi Y., Yucer N., Krenciute G., et al. Analysis of the human endogenous coregulator complexome. Cell 2011, 145:787-799.
29. Midic U., Oldfield C.J., Dunker A.K., Obradovic Z., Uversky V.N. Protein disorder in the human diseasome: unfoldomics of human genetic diseases. BMC Genomics 2009, 10(Suppl 1):S12.
30. Moshkin Y.M., Kan T.W., Goodfellow H., Bezstarosti K., Maeda R.K., Pilyugin M., Karch F., Bray S.J., Demmers J.A.A., Verrijzer C.P. Histone chaperones ASF1 and NAP1 differentially modulate removal of active histone marks by LID-RPD3 complexes during NOTCH silencing. Mol. Cell 2009, 35:782-793.
31. Ni Z., Olsen J.B., Guo X., Zhong G., Ruan E.D., Marcon E., Young P., Guo H., Li J., Moffat J., et al. Control of the RNA polymerase II phosphorylation state in promoter regions by CTD interaction domain-containing proteins RPRD1A and RPRD1B. Transcription 2011, 2:237-242.
32. On T., Xiong X., Pu S., Turinsky A., Gong Y., Emili A., Zhang Z., Greenblatt J., Wodak S.J., Parkinson J. The evolutionary landscape of the chromatin modification machinery reveals lineage specific gains, expansions, and losses. Proteins 2010, 78:2075-2089.
33. Pu S., Vlasblom J., Emili A., Greenblatt J., Wodak S.J. Identifying functional modules in the physical interactome of Saccharomyces cerevisiae. Proteomics 2007, 7:944-960.
34. Pu S., Turinsky A.L., Vlasblom J., On T., Xiong X., Emili A., Zhang Z., Greenblatt J., Parkinson J., Wodak S.J. Expanding the landscape of chromatin modification (CM)-related functional domains and genes in human. PLoS ONE 2010, 5:e14122.
35. Rieder C.L., Schultz A., Cole R., Sluder G. Anaphase onset in vertebrate somatic cells is controlled by a checkpoint that monitors sister kinetochore attachment to the spindle. J.Cell Biol. 1994, 127:1301-1310.
36. Schlicker A., Domingues F.S., Rahnenführer J., Lengauer T. A new measure for functional similarity of gene products based on Gene Ontology. BMC Bioinformatics 2006, 7:302.
37. Seiler D.M., Rouquette J., Schmid V.J., Strickfaden H., Ottmann C., Drexler G.A., Mazurek B., Greubel C., Hable V., Dollinger G., et al. Double-strand break-induced transcriptional silencing is associated with loss of tri-methylation at H3K4. Chromosome Res. 2011, 19:883-899.
38. Silkworth W.T., Nardi I.K., Scholl L.M., Cimini D. Multipolar spindle pole coalescence is a major source of kinetochore mis-attachment and chromosome mis-segregation in cancer cells. PLoS ONE 2009, 4:e6564.
39. Sowa M.E., Bennett E.J., Gygi S.P., Harper J.W. Defining the human deubiquitinating enzyme interaction landscape. Cell 2009, 138:389-403.
40. van Dongen S., Abreu-Goodger C. Using MCL to extract clusters from networks. Methods Mol. Biol. 2012, 804:281-295.
41. Vlasblom J., Wu S., Pu S., Superina M., Liu G., Orsi C., Wodak S.J. GenePro: a Cytoscape plug-in for advanced visualization and analysis of interaction networks. Bioinformatics 2006, 22:2178-2179.
42. Zhang B., Park B.H., Karpinets T., Samatova N.F. From pull-down data to protein interaction networks and complexes with biological relevance. Bioinformatics 2008, 24:979-986.
43. Zhang J., Bonasio R., Strino F., Kluger Y., Holloway J.K., Modzelewski A.J., Cohen P.E., Reinberg D. SFMBT1 functions with LSD1 to regulate expression of canonical histone genes and chromatin-related factors. Genes Dev. 2013, 27:749-766.
44. Zhu Q., Pao G.M., Huynh A.M., Suh H., Tonnu N., Nederlof P.M., Gage F.H., Verma I.M. BRCA1 tumour suppression occurs via heterochromatin-mediated silencing. Nature 2011, 477:179-184.