Identifying novel protein complexes in cancer cells using epitope-tagging of endogenous human genes and affinity-purification mass spectrometry

Journal of Proteome Research

Volumn 11, Issue 12, 2012, Pages 5630-5641

  Song, Jing ^a   Hao, Yujun ^a   Du, Zhanwen ^a   Wang, Zhenghe ^a   Ewing, Rob M ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Adenomatous Polyposis Coli; AP MS; colorectal cancer; epitope tagging; knock in; protein complexes; Protein protein interactions

Indexed keywords

APC PROTEIN; DNMT1 PROTEIN; EPIDERMAL GROWTH FACTOR RECEPTOR 2; EPITOPE; ERBB2 INTERACTING PROTEIN; FLIGHTLESS 1 HOMOLOGUE PROTEIN; MRE11A PROTEIN; PROTEIN; UNCLASSIFIED DRUG;

AFFINITY PURIFICATION MASS SPECTROMETRY; ARTICLE; CONTROLLED STUDY; HUMAN; HUMAN CELL; MASS SPECTROMETRY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN INTERACTION; PURIFICATION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; CELL NUCLEUS; CHROMATOGRAPHY, AFFINITY; COLONIC NEOPLASMS; CYTOPLASM; DEPENDOVIRUS; EPITOPE MAPPING; GENETIC VECTORS; GENOME, HUMAN; HCT116 CELLS; HEK293 CELLS; HUMANS; MASS SPECTROMETRY; MICROFILAMENT PROTEINS; MULTIPROTEIN COMPLEXES; NEOPLASM PROTEINS; PROTEIN INTERACTION MAPPING; PROTEOMICS; RECEPTORS, CYTOPLASMIC AND NUCLEAR; REPRODUCIBILITY OF RESULTS; SENSITIVITY AND SPECIFICITY; TRANSFECTION;

EUKARYOTA;

EID: 84870888665     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr300598t     Document Type: Article

References (57)

1. Collins, M. O.; Choudhary, J. S. Mapping multiprotein complexes by affinity purification and mass spectrometry Curr. Opin. Biotechnol. 2008, 19 (4) 324-330
2. Gavin, A. C.; Bosche, M.; Krause, R.; Grandi, P.; Marzioch, M.; Bauer, A.; Schultz, J.; Rick, J. M.; Michon, A. M.; Cruciat, C. M.; Remor, M.; Hofert, C.; Schelder, M.; Brajenovic, M.; Ruffner, H.; Merino, A.; Klein, K.; Hudak, M.; Dickson, D.; Rudi, T.; Gnau, V.; Bauch, A.; Bastuck, S.; Huhse, B.; Leutwein, C.; Heurtier, M. A.; Copley, R. R.; Edelmann, A.; Querfurth, E.; Rybin, V.; Drewes, G.; Raida, M.; Bouwmeester, T.; Bork, P.; Seraphin, B.; Kuster, B.; Neubauer, G.; Superti-Furga, G. Functional organization of the yeast proteome by systematic analysis of protein complexes Nature 2002, 415 (6868) 141-147
3. Ho, Y.; Gruhler, A.; Heilbut, A.; Bader, G. D.; Moore, L.; Adams, S. L.; Millar, A.; Taylor, P.; Bennett, K.; Boutilier, K.; Yang, L. Y.; Wolting, C.; Donaldson, I.; Schandorff, S.; Shewnarane, J.; Vo, M.; Taggart, J.; Goudreault, M.; Muskat, B.; Alfarano, C.; Dewar, D.; Lin, Z.; Michalickova, K.; Willems, A. R.; Sassi, H.; Nielsen, P. A.; Rasmussen, K. J.; Andersen, J. R.; Johansen, L. E.; Hansen, L. H.; Jespersen, H.; Podtelejnikov, A.; Nielsen, E.; Crawford, J.; Poulsen, V.; Sorensen, B. D.; Matthiesen, J.; Hendrickson, R. C.; Gleeson, F.; Pawson, T.; Moran, M. F.; Durocher, D.; Mann, M.; Hogue, C. W. V.; Figeys, D.; Tyers, M. Systematic identification of protein complexes in Saccharomyces cerevisiae by mass spectrometry Nature 2002, 415 (6868) 180-183
4. Krogan, N. J.; Cagney, G.; Yu, H. Y.; Zhong, G. Q.; Guo, X. H.; Ignatchenko, A.; Li, J.; Pu, S. Y.; Datta, N.; Tikuisis, A. P.; Punna, T.; Peregrin-Alvarez, J. M.; Shales, M.; Zhang, X.; Davey, M.; Robinson, M. D.; Paccanaro, A.; Bray, J. E.; Sheung, A.; Beattie, B.; Richards, D. P.; Canadien, V.; Lalev, A.; Mena, F.; Wong, P.; Starostine, A.; Canete, M. M.; Vlasblom, J.; Wu, S.; Orsi, C.; Collins, S. R.; Chandran, S.; Haw, R.; Rilstone, J. J.; Gandi, K.; Thompson, N. J.; Musso, G.; St Onge, P.; Ghanny, S.; Lam, M. H. Y.; Butland, G.; Altaf-Ui, A. M.; Kanaya, S.; Shilatifard, A.; O'Shea, E.; Weissman, J. S.; Ingles, C. J.; Hughes, T. R.; Parkinson, J.; Gerstein, M.; Wodak, S. J.; Emili, A.; Greenblatt, J. F. Global landscape of protein complexes in the yeast Saccharomyces cerevisiae Nature 2006, 440 (7084) 637-643
5. Ewing, R. M.; Chu, P.; Elisma, F.; Li, H.; Taylor, P.; Climie, S.; McBroom-Cerajewski, L.; Robinson, M. D.; O'Connor, L.; Li, M.; Taylor, R.; Dharsee, M.; Ho, Y.; Heilbut, A.; Moore, L.; Zhang, S.; Ornatsky, O.; Bukhman, Y. V.; Ethier, M.; Sheng, Y.; Vasilescu, J.; Abu-Farha, M.; Lambert, J. P.; Duewel, H. S.; Stewart, I. I.; Kuehl, B.; Hogue, K.; Colwill, K.; Gladwish, K.; Muskat, B.; Kinach, R.; Adams, S. L.; Moran, M. F.; Morin, G. B.; Topaloglou, T.; Figeys, D. Large-scale mapping of human protein-protein interactions by mass spectrometry Mol. Syst. Biol. 2007, 3, 89
6. Glatter, T.; Wepf, A.; Aebersold, R.; Gstaiger, M. An integrated workflow for charting the human interaction proteome: insights into the PP2A system Mol. Syst. Biol. 2009, 5, 237
7. Clark, D. P.; Pazdemik, N. J. Biotechnology: Applying the Genetic Revolution; Academic Press: Burlington, MA, 2009; ISBN 978-0-12-17552-2.
8. Major, M. B.; Camp, N. D.; Berndt, J. D.; Yi, X. H.; Goldenberg, S. J.; Hubbert, C.; Biechele, T. L.; Gingras, A. C.; Zheng, N.; MacCoss, M. J.; Angers, S.; Moon, R. T. Wilms tumor suppressor WTX negatively regulates WNT/beta-catenin signaling Science 2007, 316 (5827) 1043-1046
9. Matsuyama, A.; Arai, R.; Yashiroda, Y.; Shirai, A.; Kamata, A.; Sekido, S.; Kobayashi, Y.; Hashimoto, A.; Hamamoto, M.; Hiraoka, Y.; Horinouchi, S.; Yoshida, M. ORFeome cloning and global analysis of protein localization in the fission yeast Schizosaccharomyces pombe Nat. Biotechnol. 2006, 24 (7) 841-847
10. Poser, I.; Sarov, M.; Hutchins, J. R. A.; Heriche, J. K.; Toyoda, Y.; Pozniakovsky, A.; Weigl, D.; Nitzsche, A.; Hegemann, B.; Bird, A. W.; Pelletier, L.; Kittler, R.; Hua, S.; Naumann, R.; Augsburg, M.; Sykora, M. M.; Hofemeister, H.; Zhang, Y. M.; Nasmyth, K.; White, K. P.; Dietzel, S.; Mechtler, K.; Durbin, R.; Stewart, A. F.; Peters, J. M.; Buchholz, F.; Hyman, A. A. BAC TransgeneOmics: a high-throughput method for exploration of protein function in mammals Nat. Methods 2008, 5 (5) 409-415
11. Lee, A. Y. L.; Liu, E.; Wu, X. The Mre11/Rad50/Nbs1 complex plays an important role in the prevention of DNA rereplication in mammalian cells J. Biol. Chem. 2007, 282 (44) 32243
12. Olson, E.; Nievera, C. J.; Lee, A. Y. L.; Chen, L.; Wu, X. The Mre11-Rad50-Nbs1 complex acts both upstream and downstream of ataxia telangiectasia mutated and Rad3-related protein (ATR) to regulate the S-phase checkpoint following UV treatment J. Biol. Chem. 2007, 282 (31) 22939
13. Damelin, M.; Bestor, T. H. Biological functions of DNA methyltransferase 1 require its methyltransferase activity Mol. Cell. Biol. 2007, 27 (11) 3891-3899
14. Ceol, C. J.; Pellman, D.; Zon, L. I. APC and colon cancer: two hits for one Nat. Med. 2007, 13 (11) 1286-1287
15. Fodde, R.; Smits, R.; Clevers, H. APC, signal transduction and genetic instability in colorectal cancer Nat. Rev. Cancer 2001, 1 (1) 55-67
16. Brocardo, M.; Nathke, I. S.; Henderson, B. R. Redefining the subcellular location and transport of APC: new insights using a panel of antibodies EMBO Rep. 2005, 6 (2) 184-190
17. Zhang, X. D.; Guo, C. G.; Chen, Y. T.; Shulha, H. P.; Schnetz, M. P.; LaFramboise, T.; Bartels, C. F.; Markowitz, S.; Weng, Z. P.; Scacheri, P. C.; Wang, Z. H. Epitope tagging of endogenous proteins for genome-wide ChIP-chip studies Nat. Methods 2008, 5 (2) 163-165
18. Jimenez, C. R.; Huang, L.; Qiu, Y.; Burlingame, A. L. Current Protocols in Protein Science; John Wiley and Sons Inc.: New York, 1998.
19. Searle, B. C. Scaffold: A bioinformatic tool for validating MS/MS-based proteomic studies Proteomics 2010, 10, 1265-1269
20. Keller, A.; Nesvizhskii, A. I.; Kolker, E.; Aebersold, R. Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search Anal. Chem. 2002, 74 (20) 5383-5392
21. Nesvizhskii, A. I.; Keller, A.; Kolker, E.; Aebersold, R. A statistical model for identifying proteins by tandem mass spectrometry Anal. Chem. 2003, 75 (17) 4646-4658
22. Carney, J. P.; Maser, R. S.; Olivares, H.; Davis, E. M.; Le Beau, M.; Yates, J. R.; Hays, L.; Morgan, W. F.; Petrini, J. H. J. The hMre11/hRad50 protein complex and Nijmegen breakage syndrome: Linkage of double-strand break repair to the cellular DNA damage response Cell 1998, 93 (3) 477-486
23. De Marzo, A. M.; Marchi, V. L.; Yang, E. S.; Veeraswamy, R.; Lin, X.; Nelson, W. G. Abnormal regulation of DNA methyltransferase expression during colorectal carcinogenesis Cancer Res. 1999, 59, 3855-3860
24. Morin, P. J.; Sparks, A. B.; Korinek, V.; Barker, N.; Clevers, H.; Vogelstein, B.; Kinzler, K. W. Activation of beta-catenin-Tcf signaling in colon cancer by mutations in beta-catenin or APC Science 1997, 275 (5307) 1787-1790
25. Aoki, K.; Taketo, M. M. Adenomatous polyposis coli (APC): a multi-functional tumor suppressor gene J. Cell Sci. 2007, 120 (19) 3327-3335
26. Du, Z.; Song, J.; Wang, Y.; Zhao, Y.; Guda, K.; Yang, S.; Kao, H.-Y.; Xu, Y.; Willis, J.; Markowitz, S. D.; Sedwick, D.; Ewing, R. M.; Wang, Z. DNMT1 stability is regulated by proteins coordinating deubiquitination and acetylation-driven ubiquitination Sci. Signaling 2010, 3 (146) ra80
27. Kouzmenko, A. P.; Takeyama, K.; Kawasaki, Y.; Akiyama, T.; Kato, S. Truncation mutations abolish chromatin-associated activities of adenomatous polyposis coli Oncogene 2008, 27 (36) 4888-4899
28. Patel, B. B.; Li, X.-M.; Dixon, M. P.; Blagoi, E. L.; Nicolas, E.; Seeholzer, S. H.; Cheng, D.; He, Y. A.; Coudry, R. A.; Howard, S. D.; Riddle, D. M.; Cooper, H. C.; Boman, B. M.; Conrad, P.; Crowell, J. A.; Bellacosa, A.; Knudson, A.; Yeung, A. T.; Kopelovich, L. APC ± alters colonic fibroblast proteome in FAP Oncotarget 2011, 2 (3) 197-208
29. Brocardo, M.; Hendersonj, B. R. Detection of cytoplasmic and nuclear localization of adenomatous polyposis coli (APC) protein in cells Methods Mol. Biol. 2008, 468, 77-89
30. Neufeld, K. Nuclear APC Adv. Exp. Med. Biol. 2009, 656, 13-29
31. Lee, Y.-H.; Stallcup, M. R. Interplay of bac-I and FLAP1 for regulation of beta-catenin dependent transcription Nucleic Acids Res. 2006, 34 (18) 5052-5059
32. Liu, J.; Bang, A. G.; Kintner, C.; Orth, A. P.; Chanda, S. K.; Ding, S.; Schultz, P. G. Identification of the Wnt signaling activator leucine-rich repeat in Flightless interaction protein 2 by a genome-wide functional analysis Proc. Natl. Acad. Sci. U.S.A. 2005, 102 (6) 1927-1932
33. Stark, C.; Breitkreutz, B.-J.; Chatr-aryamontri, A.; Boucher, L.; Oughtred, R.; Livstone, M. S.; Nixon, J.; Van Auken, K.; Wang, X.; Shi, X.; Reguly, T.; Rust, J. M.; Winter, A.; Dolinski, K.; Tyers, M. The BioGRID Interaction Database: 2011 update Nucleic Acids Res. 2011, 39 (Suppl. 1) D698-D704
34. Bandyopadhyay, S.; Chiang, C.-y.; Srivastava, J.; Gersten, M.; White, S.; Bell, R.; Kurschner, C.; Martin, C. H.; Smoot, M.; Sahasrabudhe, S.; Barber, D. L.; Chanda, S. K.; Ideker, T. A human MAP kinase interactome Nat. Methods 2010, 7 (10) 801-805
35. Jensen, L. J.; Bork, P. Not Comparable, But Complementary Science 2008, 322 (5898) 56-57
36. Ress, A.; Moelling, K. Interaction partners of the PDZ domain of erbin Protein Pept. Lett. 2006, 13 (9) 877-881
37. Ress, A.; Moelling, K. The PDZ protein erbin modulates beta-catenin-dependent transcription Eur. Surg. Res. 2008, 41 (3) 284-289
38. Takizawa, S.; Nagasaka, K.; Nakagawa, S.; Yano, T.; Nakagawa, K.; Yasugi, T.; Takeuchi, T.; Kanda, T.; Huibregtse, J. M.; Akiyama, T.; Taketani, Y. Human scribble, a novel tumor suppressor identified as a target of high-risk HPV E6 for ubiquitin-mediated degradation, interacts with adenomatous polyposis coli Genes Cells 2006, 11 (4) 453-464
39. Hilger, M.; Mann, M. Triple SILAC to determine stimulus specific interactions in the Wnt pathway J. Proteome Res. 2012, 11 (2) 982-994
40. Rohila, J. S.; Chen, M.; Chen, S.; Chen, J.; Cerny, R.; Dardick, C.; Canlas, P.; Xu, X.; Gribskov, M.; Kanrar, S.; Zhu, J.-K.; Ronald, P.; Fromm, M. E. Protein-protein interactions of tandem affinity purification-tagged protein kinases in rice Plant J. 2006, 46 (1) 1-13
41. Li, S.; Armstrong, C. M.; Bertin, N.; Ge, H.; Milstein, S.; Boxem, M.; Vidalain, P.-O.; Han, J.-D. J.; Chesneau, A.; Hao, T.; Goldberg, D. S.; Li, N.; Martinez, M.; Rual, J.-F.; Lamesch, P.; Xu, L.; Tewari, M.; Wong, S. L.; Zhang, L. V.; Berriz, G. F.; Jacotot, L.; Vaglio, P.; Reboul, J.; Hirozane-Kishikawa, T.; Li, Q.; Gabel, H. W.; Elewa, A.; Baumgartner, B.; Rose, D. J.; Yu, H.; Bosak, S.; Sequerra, R.; Fraser, A.; Mango, S. E.; Saxton, W. M.; Strome, S.; van den Heuvel, S.; Piano, F.; Vandenhaute, J.; Sardet, C.; Gerstein, M.; Doucette-Stamm, L.; Gunsalus, K. C.; Harper, J. W.; Cusick, M. E.; Roth, F. P.; Hill, D. E.; Vidal, M. A Map of the Interactome Network of the Metazoan C. elegans Science 2004, 303 (5657) 540-543
42. Suter, B.; Fetchko, M. J.; Imhof, R.; Graham, C. I.; Stoffel-Studer, I.; Zbinden, C.; Raghavan, M.; Lopez, L.; Beneti, L.; Hort, J.; Fillingham, J.; Greenblatt, J. F.; Giaever, G.; Nislow, C.; Stagljar, I. Examining protein-protein interactions using endogenously tagged yeast arrays: The Cross-and-Capture system Genome Res. 2007, 17 (12) 1774-1782
43. Sopko, R.; Huang, D.; Preston, N.; Chua, G.; Papp, B.; Kafadar, K.; Snyder, M.; Oliver, S. G.; Cyert, M.; Hughes, T. R.; Boone, C.; Andrews, B. Mapping Pathways and Phenotypes by Systematic Gene Overexpression Mol. Cell 2006, 21 (3) 319-330
44. Hubner, N. C.; Ren, S.; Mann, M. Peptide separation with immobilized pI strips is an attractive alternative to in-gel protein digestion for proteome analysis Proteomics 2008, 8 (23-24) 4862-4872
45. Forler, D.; Kocher, T.; Rode, M.; Gentzel, M.; Izaurralde, E.; Wilm, M. An efficient protein complex purification method for functional proteomics in higher eukaryotes Nat. Biotechnol. 2003, 21 (1) 89-92
46. Huh, W. K.; Falvo, J. V.; Gerke, L. C.; Carroll, A. S.; Howson, R. W.; Weissman, J. S.; O'Shea, E. K. Global analysis of protein localization in budding yeast Nature 2003, 425 (6959) 686-691
47. Zhang, X. D.; Guo, A. L.; Yu, J. S.; Possemato, A.; Chen, Y. T.; Zheng, W. P.; Polakiewicz, R. D.; Kinzler, K. W.; Vogelstein, B.; Velculescu, V. E.; Wang, Z. H. J. Identification of STAT3 as a substrate of receptor protein tyrosine phosphatase T Proc. Natl. Acad. Sci. U.S.A. 2007, 104 (10) 4060-4064
48. Segditsas, S.; Sieber, O.; Deheragoda, M.; East, P.; Rowan, A.; Jeffery, R.; Nye, E.; Clark, S.; Spencer-Dene, B.; Stamp, G.; Poulsom, R.; Suraweera, N.; Silver, A.; Ilyas, M.; Tomlinson, I. Putative direct and indirect Wnt targets identified through consistent gene expression changes in APC-mutant intestinal adenomas from humans and mice. Hum. Mol. Genet. 2008, 17, (24), 3864-3875.
49. 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. U.S.A. 2010, 107 (6) 2431-2436
50. Griep, A. E.; John, M. C.; Ikeda, S; Ikeda, A. Gene targeting in the mouse Methods Mol. Biol. 2011, 770, 293-312
51. Bonfils, C.; Beaulieu, N.; Chan, E.; Cotton-Montpetit, J.; MacLeod, A. R. Characterization of the human DNA methyltransferase splice variant Dnmt1b J. Biol. Chem. 2000, 275, 10754-10760
52. Kawasaki, Y.; Senda, T.; Ishidate, T.; Koyama, R.; Morishita, T.; Iwayama, Y.; Higuchi, O.; Akiyama, T. Asef, a link between the tumor suppressor APC and G-protein signaling Science 2000, 289, 1194-1197
53. Rago, C.; Vogelstein, B.; Bunz, F. Genetic knockouts and knockins in human somatic cells Nat. Protoc. 2007, 2, 2734-2746
54. Kinzler, K. W; Vogelstein, B. Lessons from Hereditary Colorectal Cancer Cell 1996, 87 (2) 159-170
55. Henderson, B. R. Nuclear-cytoplasmic shuttling of APC regulates beta-catenin subcellular localization and turnover Nat. Cell Biol. 2000, 2 (9) 653-660
56. Kohli, M.; Rago, C.; Lengauer, C.; Kinzler, K. W.; Vogelstein, B. Facile methods for generating human somatic cell gene knockouts using recombinant adeno-associated viruses Nucleic Acids Res. 2004, 32 (1 PMC373311
57. Kim, J.-S.; Bonifant, C.; Bunz, F.; Lane, W. S.; Waldman, T. Epitope tagging of endogenous genes in diverse human cell lines Nucleic Acids Res. 2008, 36 (19 e127