Proteomics of differential extraction fractions enriched for chromatin-binding proteins from colon adenoma and carcinoma tissues

Biochimica et Biophysica Acta - Proteins and Proteomics

Volumn 1844, Issue 5, 2014, Pages 1034-1043

  Knol, Jaco C ^a   De Wit, Meike ^a   Albrethsen, Jakob ^a,b   Piersma, Sander R ^a   Pham, Thang V ^a   Mongera, Sandra ^a   Carvalho, Beatriz ^a   Fijneman, Remond J A ^a   Meijer, Gerrit A ^a   Jiménez, Connie R ^a  

^a VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^b University of Copenhagen   (Denmark)

Author keywords

Adenoma; Cancer tissue; Carcinoma; Chromatin binding; Colorectal; Proteomics

Indexed keywords

CELL CYCLE PROTEIN; CHROMATIN BINDING PROTEIN; PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CANCER GROWTH; CANCER TISSUE; CELL STRESS; CHROMATIN; CHROMOSOMAL INSTABILITY; CHROMOSOME SEGREGATION; CLINICAL ARTICLE; COLON ADENOMA; COLON CARCINOMA; COLORECTAL CANCER; CONTROLLED STUDY; DIFFERENTIATION; DNA RECOMBINATION; DNA REPAIR; HUMAN; HUMAN TISSUE; MICROSATELLITE INSTABILITY; PRIORITY JOURNAL; PROTEOMICS;

ADENOMA; CANCER TISSUE; CARCINOMA; CHROMATIN-BINDING; COLORECTAL; PROTEOMICS;

ADENOMA; CHROMATIN; CHROMATOGRAPHY, LIQUID; COLORECTAL NEOPLASMS; GENE ONTOLOGY; HUMANS; MICROSATELLITE INSTABILITY; NEOPLASM PROTEINS; NUCLEAR PROTEINS; PROTEOMICS; SUBCELLULAR FRACTIONS; TANDEM MASS SPECTROMETRY; TUMOR MARKERS, BIOLOGICAL;

EID: 84898600802     PISSN: 15709639     EISSN: 18781454     Source Type: Journal    
DOI: 10.1016/j.bbapap.2013.12.006     Document Type: Article

References (85)

1. E.G. Fey, K.M. Wan, and S. Penman Epithelial cytoskeletal framework and nuclear matrix-intermediate filament scaffold: three-dimensional organization and protein composition J. Cell Biol. 98 1984 1973 1984 (Pubitemid 14121828)
2. E.G. Fey, and S. Penman Nuclear matrix proteins reflect cell type of origin in cultured human cells Proc. Natl. Acad. Sci. U. S. A. 85 1988
3. J. Albrethsen, J.C. Knol, S.R. Piersma, T.V. Pham, M. de wit, S. Mongera, B. Carvalho, H.M.W. Verheul, R.J.A. Fijneman, G.A. Meijer, and C.R. Jimenez Subnuclear proteomics in colorectal cancer: identification of proteins enriched in the nuclear matrix fraction and regulation in adenoma to carcinoma progression Mol. Cell. Proteomics 9 2010 988 1005
4. P. Dey Cancer nucleus: morphology and beyond Diagn. Cytopathol. 38 2010 382 390
5. M.S. Pino, and D.C. Chung The chromosomal instability pathway in colon cancer Gastroenterology 38 2010 2059 2072
6. M. Hermsen, C. Postma, J. Baak, M. Weiss, A. Rapallo, A. Sciutto, G. Roemen, J.-W. Arends, R. Williams, W. Giaretti, A. De Goeij, and G. Meijer Colorectal adenoma to carcinoma progression follows multiple pathways of chromosomal instability Gastroenterology 123 2002 1109 1119
7. C.B. Diep, K. Kleivi, F.R. Ribeiro, M.R. Teixeira, O.C. Lindgjaerde, and R.A. Lothe The order of genetic events associated with colorectal cancer progression inferred from meta-analysis of copy number changes Genes Chromosom. Cancer 45 2006 31 41 (Pubitemid 46930859)
8. R.P.M. Brosens, E.J.T.H. Belt, J.C. Haan, T.E. Buffart, B. Carvalho, H. Grabsch, P. Quirke, M.A. Cuesta, A.F. Engel, B. Ylstra, and G.A. Meijer Deletion of chromosome 4q predicts outcome in Stage II colon cancer patients Cell. Oncol. 34 2011 215 223
9. Z. Wang, J.M. Cummins, D. Shen, D.P. Cahill, P.V. Jallepalli, T.-L. Wang, D.W. Parsons, G. Traverso, M. Awad, N. Silliman, J. Ptak, S. Szabo, J.K.V. Willson, S.D. Markowitz, M.L. Goldberg, R. Karess, K.W. Kinzler, B. Vogelstein, V.E. Velculescu, and C. Lengauer Three classes of genes mutated in colorectal cancers with chromosomal instability Cancer Res. 64 2004 2998 3001 (Pubitemid 38581395)
10. H. Liu, R.G. Sadygov, and J.R. Yates A model for random sampling and estimation of relative protein abundance in shotgun proteomics Anal. Chem. 76 2004 4193 4201 (Pubitemid 38943698)
11. S.R. Piersma, U. Fiedler, S. Span, A. Lingnau, T.V. Pham, S. Hoffmann, M.H.G. Kubbutat, and C.R. Jimenez Workflow comparison for label-free, quantitative secretome proteomics for cancer biomarker discovery: method evaluation, differential analysis, and verification in serum J. Proteome Res. 9 2010 1913 1922
12. T.V. Pham, S.R. Piersma, M. Warmoes, and C.R. Jimenez On the beta-binomial model for analysis of spectral count data in label-free tandem mass spectrometry-based proteomics Bioinformatics 26 2010 363 369
13. S. Rastogi, and B. Rost LocDB: experimental annotations of localization for Homo sapiens and Arabidopsis thaliana Nucleic Acids Res. 39 2010 D230 D234
14. J.L. Fink, S. Karunaratne, A. Mittal, D.M. Gardiner, N. Hamilton, D. Mahony, C. Kai, H. Suzuki, Y. Hayashizaki, and R.D. Teasdale Towards defining the nuclear proteome Genome Biol. 9 2008 R15
15. N. Mohamad, and M. Boden The proteins of intra-nuclear bodies: a data-driven analysis of sequence, interaction and expression BMC Syst. Biol. 4 2010 44
16. D.C. Bauer, K. Willadsen, F.A. Buske, K.-A.L. Cao, T.L. Bailey, G. Dellaire, and M. Boden Sorting the nuclear proteome Bioinformatics 27 2011 7 14
17. S. Maere, K. Heymans, and M. Kuiper BiNGO: a Cytoscape plugin to assess overrepresentation of gene ontology categories in biological networks Bioinformatics 21 2005 3448 3449 (Pubitemid 41222459)
18. D.W. Huang, B.T. Sherman, and R.A. Lempicki Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources Nat. Protoc. 2008 44 57
19. B. Carvalho, A.H. Sillars-Hardebol, C. Postma, S. Mongera, J.T.S. Droste, A. Obulkasim, M. van de Wiel, W. van Criekinge, B. Ylstra, R.J.A. Fijneman, and G.A. Meijer Colorectal adenoma to carcinoma progression is accompanied by changes in gene expression associated with ageing, chromosomal instability, and fatty acid metabolism Cell. Oncol. 35 2012 53 63
20. B. Carvalho, C. Postma, S. Mongera, E. Hopmans, S. Diskin, M.A. van de Wiel, W. van Criekinge, O. Thas, A. Matthai, M.A. Cuesta, J.S. Terhaar sive Droste, M. Craanen, E. Schrock, B. Ylstra, and G.A. Meijer Multiple putative oncogenes at the chromosome 20q amplicon contribute to colorectal adenoma to carcinoma progression Gut 58 2009 79 89
21. D. Szklarczyk, A. Franceschini, M. Kuhn, M. Simonovic, A. Roth, P. Minguez, T. Doerks, M. Stark, J. Muller, P. Bork, L.J. Jensen, and C. von Mering The STRING database in 2011: functional interaction networks of proteins, globally integrated and scored Nucleic Acids Res. 39 2011 D561 D568
22. D. Ruggero, and P.P. Pandolfi Does the ribosome translate cancer? Nat. Rev. Cancer 3 2003 179 192 (Pubitemid 37328870)
23. L. Montanaro, D. Treré, and M. Derenzini Nucleolus, ribosomes, and cancer Am. J. Pathol. 173 2008 301 310
24. D. Silvera, S.C. Formenti, and R.J. Schneider Translational control in cancer Nat. Rev. Cancer 10 2010 254 266
25. R.P. Stevenson, D. Veltman, and L.M. Machesky Actin-bundling proteins in cancer progression at a glance J. Cell Sci. 125 2012 1073 1079
26. R.A. Cairns, I.S. Harris, and T.W. Mak Regulation of cancer cell metabolism Nat. Rev. Cancer 11 2011 85 95
27. J.R. Warner, and K.B. McIntosh How common are extraribosomal functions of ribosomal proteins? Mol. Cell 34 2009 3 11
28. W. Yang, Y. Xia, H. Ji, Y. Zheng, J. Liang, W. Huang, X. Gao, K. Aldape, and Z. Lu Nuclear PKM2 regulates β-catenin transactivation upon EGFR activation Nature 478 2011 118 122
29. D. Chowdhury, M.-C. Keogh, H. Ishii, C.L. Peterson, S. Buratowski, and J. Lieberman γ-H2AX dephosphorylation by protein phosphatase 2A facilitates DNA double-strand break repair Mol. Cell 20 2005 801 809 (Pubitemid 41740701)
30. M. Bollen, D.W. Gerlich, and B. Lesage Mitotic phosphatases: from entry guards to exit guides Trends Cell Biol. 19 2009 531 541
31. C. Wurzenberger, and D.W. Gerlich Phosphatases: providing safe passage through mitotic exit Nat. Rev. Mol. Cell Biol. 12 2011 469 482
32. D. Santamaría, C. Barrière, A. Cerqueira, S. Hunt, C. Tardy, K. Newton, J.F. Cáceres, P. Dubus, M. Malumbres, and M. Barbacid Cdk1 is sufficient to drive the mammalian cell cycle Nature 448 2007 811 815 (Pubitemid 47266342)
33. M.L. Coleman, C.J. Marshall, and M.F. Olson RAS and RHO GTPases in G1-phase cell-cycle regulation Nat. Rev. Mol. Cell Biol. 5 2004 355 366 (Pubitemid 38579473)
34. T. Gorsler, U. Murzik, T. Ulbricht, J. Hentschel, P. Hemmerich, and C. Melle DNA damage-induced translocation of S100A11 into the nucleus regulates cell proliferation BMC Cell Biol. 11 2010 100
35. K.B. Shannon IQGAP family members in yeast, Dictyostelium, and mammalian cells Int. J. Cell Biol. 2012 2012 1 14
36. A. Margalit, A. Brachner, J. Gotzmann, R. Foisner, and Y. Gruenbaum Barrier-to-autointegration factor - a BAFfling little protein Trends Cell Biol. 17 2007 202 208 (Pubitemid 46507807)
37. C. Asencio, I.F. Davidson, R. Santarella-Mellwig, T.B.N. Ly-Hartig, M. Mall, M.R. Wallenfang, I.W. Mattaj, and M. Gorjánácz Coordination of kinase and phosphatase activities by Lem4 enables nuclear envelope reassembly during mitosis Cell 150 2012 122 135
38. B. Zhu, S.S. Mandal, A.-D. Pham, Y. Zheng, H. Erdjument-Bromage, S.K. Batra, P. Tempst, and D. Reinberg The human PAF complex coordinates transcription with events downstream of RNA synthesis Gene Dev. 2005 1668 1673 (Pubitemid 41058361)
39. L. Ding, M. Paszkowski-Rogacz, A. Nitzsche, M.M. Slabicki, A.-K. Heninger, I. de Vries, R. Kittler, M. Junqueira, A. Shevchenko, H. Schulz, N. Hubner, M.X. Doss, A. Sachinidis, J. Hescheler, R. Iacone, K. Anastassiadis, A.F. Stewart, M.T. Pisabarro, A. Caldarelli, and I. Poser et al. A genome-scale RNAi screen for Oct4 modulators defines a role of the Paf1 complex for embryonic stem cell identity Stem Cells 4 2009 403 415
40. C. Mosimann, G. Hausmann, and K. Basler Parafibromin/hyrax activates Wnt/Wg target gene transcription by direct association with β-catenin/ Armadillo Cell 125 2006 327 341 (Pubitemid 44313810)
41. L. Vermeulen, F. De Sousa, E. Melo, M. van der Heijden, K. Cameron, J.H. de Jong, T. Borovski, J.B. Tuynman, M. Todaro, C. Merz, H. Rodermond, M.R. Sprick, K. Kemper, D.J. Richel, G. Stassi, and J.P. Medema Wnt activity defines colon cancer stem cells and is regulated by the microenvironment Nat. Cell Biol. 12 2010 468 476
42. X. Zhang, M.J. Gamble, S. Stadler, B.D. Cherrington, C.P. Causey, P.R. Thompson, M.S. Roberson, W.L. Kraus, and S.A. Coonrod Genome-wide analysis reveals PADI4 cooperates with Elk-1 to activate c-Fos expression in breast cancer cells PLoS Genet. 7 2011 e1002112
43. S. Iyengar KAP1 protein: an enigmatic master regulator of the genome J. Biol. Chem. 30 2011 26267 26276
44. C.D. Venkov, A.J. Link, J.L. Jennings, D. Plieth, T. Inoue, K. Nagai, C. Xu, Y.N. Dimitrova, F.J. Rauscher III, and E.G. Neilson A proximal activator of transcription in epithelial-mesenchymal transition J. Clin. Invest. 117 2007 482 491 (Pubitemid 46203977)
45. B.C. Yasuhiro Sekia, D. Akira Kurisakia, K. Watanabe-Susakia, Y. Nakajimaa, M. Nakanishib, Y. Araie, K. Shiotae, H. Suginoa, and B. Makoto Asashimaa TIF1β regulates the pluripotency of embryonic stem cells in a phosphorylation-dependent manner Proc. Natl. Acad. Sci. U. S. A. 107 2010 10926 10931
46. X.-F. Zhoua, J. Yua, M. Changa, M. Zhangb, C. Dapeng Zhoub, F. Cammasd, and S.-C. Suna TRIM28 mediates chromatin modifications at the TCRα enhancer and regulates the development of T and natural killer T cells Proc. Natl. Acad. Sci. U. S. A. 109 2012 20083 20088
47. D.-H. Lee, A.A. Goodarzi, G.O. Adelmant, Y. Pan, P.A. Jeggo, J.A. Marto, and D. Chowdhury Phosphoproteomic analysis reveals that PP4 dephosphorylates KAP-1 impacting the DNA damage response EMBO J. 31 2012 2403 2415
48. M. Okuwaki, K. Kato, and K. Nagata Functional characterization of human nucleosome assembly protein 1-like proteins as histone chaperones Genes Cells 15 2010 13 27
49. F. Mongelard, and P. Bouvet Nucleolin: a multiFACeTed protein Trends Cell Biol. 17 2007 80 86 (Pubitemid 46199181)
50. U. Murzik, P. Hemmerich, S. Weidtkamp-Peters, T. Ulbricht, W. Bussen, J. Hentschel, F. von Eggeling, and C. Melle Rad54B targeting to DNA double-strand break repair sites requires complex formation with S100A11 Mol. Biol. Cell 19 2008 2926 2935
51. Y. Pommier Topoisomerase I inhibitors: camptothecins and beyond Nat. Rev. Cancer 6 2006 789 802 (Pubitemid 44450467)
52. G.B. Celli, E.L. Denchi, and T. de Lange Ku70 stimulates fusion of dysfunctional telomeres yet protects chromosome ends from homologous recombination Nat. Publ. Group 8 2006 855 890
53. S.E. Holt, D.L. Aisner, J. Baur, V.M. Tesmer, M. Dy, M. Ouellette, J.B. Trager, G.B. Morin, D.O. Toft, J.W. Shay, W.E. Wright, and M.A. White Functional requirement of p23 and Hsp90 in telomerase complexes Gene Dev. 1999 817 826 (Pubitemid 29169841)
54. D.C. DeZwaan, and B.C. Freeman HSP90 manages the ends Trends Biochem. Sci. 35 2010 384 391
55. E. Zelin, Y. Zhang, O.A. Toogun, S. Zhong, and B.C. Freeman The p23 molecular chaperone and GCN5 acetylase jointly modulate protein-DNA dynamics and open chromatin status Mol. Cell 48 2012 459 470
56. M.A. D'Angelo, J.S. Gomez-Cavazos, A. Mei, D.H. Lackner, and M.W. Hetzer A change in nuclear pore complex composition regulates cell differentiation Dev. Cell 22 2012 446 458
57. J. Hansson, M.R. Rafiee, S. Reiland, J.M. Polo, J. Gehring, S. Okawa, W. Huber, K. Hochedlinger, and J. Krijgsveld Highly coordinated proteome dynamics during reprogramming of somatic cells to pluripotency Cell Rep. 2 2012 1579 1592
58. A. O'Loghlen, A.M. Muñoz-Cabello, A. Gaspar-Maia, H.-A. Wu, A. Banito, N. Kunowska, T. Racek, H.N. Pemberton, P. Beolchi, F. Lavial, O. Masui, M. Vermeulen, T. Carroll, J. Graumann, E. Heard, N. Dillon, V. Azuara, A.P. Snijders, G. Peters, and E. Bernstein et al. MicroRNA regulation of Cbx7 mediates a switch of Polycomb orthologs during ESC differentiation Stem Cells 10 2012 33 46
59. L. Morey, G. Pascual, L. Cozzuto, G. Roma, A. Wutz, S.A. Benitah, and L. Di Croce Nonoverlapping functions of the polycomb group Cbx family of proteins in embryonic stem cells Stem Cells 10 2012 47 62
60. X. Chen, K. Skutt-Kakaria, J. Davison, Y.L. Ou, E. Choi, P. Malik, K. Loeb, B. Wood, G. Georges, B. Torok-Storb, and P.J. Paddison G9a/GLP-dependent histone H3K9me2 patterning during human hematopoietic stem cell lineage commitment Gene Dev. 26 2012 2499 2511
61. Y. Chang, L. Sun, K. Kokura, J.R. Horton, M. Fukuda, A. Espejo, V. Izumi, J.M. Koomen, M.T. Bedford, X. Zhang, Y. Shinkai, J. Fang, and X. Cheng MPP8 mediates the interactions between DNA methyltransferase Dnmt3a and H3K9 methyltransferase GLP/G9a Nat. Commun. 2 2011 533
62. K. Yamane, K. Tateishi, R.J. Klose, J. Fang, L.A. Fabrizio, H. Erdjument-Bromage, J. Taylor-Papadimitriou, P. Tempst, and Y. Zhang PLU-1 is an H3K4 demethylase involved in transcriptional repression and breast cancer cell proliferation Mol. Cell 25 2007 801 812 (Pubitemid 46436533)
63. A.P. Bracken, and K. Helin Epigenetics and Genetics: Polycomb Group Proteins: Navigators of Lineage Pathways Led Astray in Cancer 2009 1 12
64. J. Ueda, M. Tachibana, T. Ikura, and Y. Shinkai Zinc finger protein Wiz links G9a/GLP histone methyltransferases to the co-repressor molecule CtBP J. Biol. Chem. 281 2006 20120 20128 (Pubitemid 44065786)
65. A. Loyola, J.-Y. Huang, G. LeRoy, S. Hu, Y.-H. Wang, R.J. Donnelly, W.S. Lane, S.-C. Lee, and D. Reinberg Functional analysis of the subunits of the chromatin assembly factor RSF Mol. Cell. Biol. 23 2003 6759 6768 (Pubitemid 37214647)
66. G. Dobreva, M. Chahrour, M. Dautzenberg, L. Chirivella, B. Kanzler, I. Fariñas, G. Karsenty, and R. Grosschedl SATB2 is a multifunctional determinant of craniofacial patterning and osteoblast differentiation Cell 125 2006 971 986 (Pubitemid 43810153)
67. K. Magnusson, M. de wit, D.J. Brennan, L.B. Johnson, S.F. McGee, E. Lundberg, K. Naicker, R. Klinger, C. Kampf, A. Asplund, K. Wester, M. Gry, A. Bjartell, W.M. Gallagher, E. Rexhepaj, S. Kilpinen, O.-P. Kallioniemi, E. Belt, J. Goos, and G. Meijer et al. SATB2 in combination with cytokeratin 20 identifies over 95% of all colorectal carcinomas Am. J. Surg. Pathol. 35 2011 937 948
68. T.L. Ripmaster, G.P. Vaughn, and J.L. Woolford A putative ATP-dependent RNA helicase involved in Saccharomyces cerevisiae ribosome assembly Proc. Natl. Acad. Sci. U. S. A. 89 1992 11131 11135
69. C.-T. Chang, G.M. Hautbergue, M.J. Walsh, N. Viphakone, T.B. van Dijk, S. Philipsen, and S.A. Wilson Chtop is a component of the dynamic TREX mRNA export complex EMBO J. 32 2013 473 486
70. H. Xu, J.M. Tomaszewski, and M.J. McKay Can corruption of chromosome cohesion create a conduit to cancer? Nat. Rev. Cancer 11 2011 199 210
71. I. Onn, J.M. Heidinger-Pauli, V. Guacci, E. Ünal, and D.E. Koshland Sister chromatid cohesion: a simple concept with a complex reality Annu. Rev. Cell Dev. Biol. 24 2008 105 129
72. K. Nasmyth, and C.H. Haering Cohesin: its roles and mechanisms Annu. Rev. Genet. 43 2009 525 558
73. D. Dorsett Cohesin: genomic insights into controlling gene transcription and development Curr. Opin. Genet. Dev. 21 2011 199 206
74. S.L. Kline The human Mis12 complex is required for kinetochore assembly and proper chromosome segregation J. Cell Biol. 173 2006 9 17
75. R.-S. Nozawa, K. Nagao, H.-T. Masuda, O. Iwasaki, T. Hirota, N. Nozaki, H. Kimura, and C. Obuse Human POGZ modulates dissociation of HP1α from mitotic chromosome arms through Aurora B activation Nat. Cell Biol. 12 2010 719 727
76. S.F. Bakhoum, and D.A. Compton Chromosomal instability and cancer: a complex relationship with therapeutic potential J. Clin. Invest. 122 2012 1138 1143
77. H. Xu, K. Balakrishnan, J. Malaterre, M. Beasley, Y. Yan, J. Essers, E. Appeldoorn, J.M. Thomaszewski, M. Vazquez, S. Verschoor, M.F. Lavin, I. Bertonchello, R.G. Ramsay, and M.J. McKay Rad21-cohesin haploinsufficiency impedes DNA repair and enhances gastrointestinal radiosensitivity in mice PLoS ONE 5 2010 e12112
78. N. Wu, and H. Yu The Smc complexes in DNA damage response Cell Biosci. 2 2012 5
79. T. Iwasaki Identification and characterization of RRM-containing coactivator activator (CoAA) as TRBP-interacting protein, and its splice variant as a coactivator modulator (CoAM) J. Biol. Chem. 276 2001 33375 33383
80. D. Auboeuf, D.H. Dowhan, X. Li, K. Larkin, L. Ko, S.M. Berget, and B.W. OMalley CoAA, a nuclear receptor coactivator protein at the interface of transcriptional coactivation and RNA splicing Mol. Cell. Biol. 24 2004 442 453 (Pubitemid 38010068)
81. O. Fernandez-Capetillo, A. Lee, M. Nussenzweig, and A. Nussenzweig H2AX: the histone guardian of the genome DNA Repair 3 2004 959 967 (Pubitemid 38997938)
82. J. Lukas, C. Lukas, and J. Bartek More than just a focus: the chromatin response to DNA damage and its role in genome integrity maintenance Nat. Cell Biol. 13 2011 1161 1169
83. S. Hübner, D.A. Jans, and D. Drenckhahn Roles of cytoskeletal and junctional plaque proteins in nuclear signaling Int. Rev. Cytol. 2001 207 265 (Pubitemid 32738367)
84. P.D. McCrea, D. Gu, and M.S. Balda Junctional music that the nucleus hears: cell-cell contact signaling and the modulation of gene activity Cold Spring Harb. Perspect. Biol. 1 2009 a002923
85. J. Eberhard, A. Gaber, S. Wangefjord, B. Nodin, M. Uhlén, K. Ericson Lindquist, and K. Jirström A cohort study of the prognostic and treatment predictive value of SATB2 expression in colorectal cancer Br. J. Cancer 106 5 Feb 28 2012 931 938