Parallel exploration of interaction space by BioID and affinity purification coupled to mass spectrometry

Methods in Molecular Biology

Volumn 1550, Issue , 2017, Pages 115-136

  Hesketh, Geoffrey G ^a   Youn, Ji Young ^a   Samavarchi Tehrani, Payman ^a   Raught, Brian ^b,c   Gingras, Anne Claude ^a,d  

^a MOUNT SINAI HOSPITAL   (Canada)

^b PRINCESS MARGARET HOSPITAL   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

^d UNIVERSITY OF TORONTO   (Canada)

Author keywords

Affinity purification; BioID; Biotin; FLAG tag; Mass spectrometry; Protein identification; Protein interactions; Protein network; Proteomics; Proximity labeling; Streptavidin

Indexed keywords

BIOTIN; PROTEIN; STREPTAVIDIN; HYBRID PROTEIN;

AFFINITY PURIFICATION; CONTROLLED STUDY; EMBRYO; HEK293 CELL LINE; HUMAN; HUMAN CELL; LIQUID CHROMATOGRAPHY-MASS SPECTROMETRY; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEOMICS; PURIFICATION; AFFINITY CHROMATOGRAPHY; BIOTINYLATION; CELL LINE; GENE EXPRESSION; GENE VECTOR; GENETICS; ISOLATION AND PURIFICATION; MASS SPECTROMETRY; METABOLISM; PROCEDURES; PROTEIN DEGRADATION; REPORTER GENE; STATISTICS; WORKFLOW;

BIOTINYLATION; CELL LINE; CHROMATOGRAPHY, AFFINITY; GENE EXPRESSION; GENES, REPORTER; GENETIC VECTORS; HUMANS; MASS SPECTROMETRY; PROTEIN INTERACTION MAPPING; PROTEINS; PROTEOLYSIS; PROTEOMICS; RECOMBINANT FUSION PROTEINS; STATISTICS AS TOPIC; WORKFLOW;

EID: 85012986102     PISSN: 10643745     EISSN: None     Source Type: Book Series    
DOI: 10.1007/978-1-4939-6747-6_10     Document Type: Chapter

References (41)

1. Snider J, Kotlyar M, Saraon P, Yao Z, Jurisica I, Stagljar I (2015) Fundamentals of protein interaction network mapping. Mol Syst Biol 11(12):848. doi:10.15252/msb.20156351
2. Gingras AC, Gstaiger M, Raught B, Aebersold R (2007) Analysis of protein complexes using mass spectrometry. Nat Rev Mol Cell Biol 8(8):645–654. doi:10.1038/nrm2208
3. Gavin AC, Bosche M, Krause R, Grandi P, Marzioch M, Bauer A, Schultz J, Rick JM, Michon AM, Cruciat CM, 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 MA, Copley RR, Edelmann A, Querfurth E, Rybin V, Drewes G, Raida M, Bouwmeester T, Bork P, Seraphin B, Kuster B, Neubauer G, Superti-Furga G (2002) Functional organization of the yeast proteome by systematic analysis of protein complexes. Nature 415(6868):141–147. doi:10.1038/415141a
4. Ho Y, Gruhler A, Heilbut A, Bader GD, Moore L, Adams SL, Millar A, Taylor P, Bennett K, Boutilier K, Yang L, 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 AR, Sassi H, Nielsen PA, Rasmussen KJ, Andersen JR, Johansen LE, Hansen LH, Jespersen H, Podtelejnikov A, Nielsen E, Crawford J, Poulsen V, Sorensen BD, Matthiesen J, Hendrickson RC, Gleeson F, Pawson T, Moran MF, Durocher D, Mann M, Hogue CW, Figeys D, Tyers M (2002) Systematic identification of protein complexes in Saccharomyces cerevisiae by mass spectrometry. Nature 415(6868):180– 183. doi:10.1038/415180a
5. Hein MY, Hubner NC, Poser I, Cox J, Nagaraj N, Toyoda Y, Gak IA, Weisswange I, Mansfeld J, Buchholz F, Hyman AA, Mann M (2015) A human interactome in three quantitative dimensions organized by stoichiometries and abundances. Cell 163(3):712–723. doi:10.1016/j.cell.2015.09.053
6. Huttlin EL, Ting L, Bruckner RJ, Gebreab F, Gygi MP, Szpyt J, Tam S, Zarraga G, Colby G, Baltier K, Dong R, Guarani V, Vaites LP, Ordureau A, Rad R, Erickson BK, Wuhr M, Chick J, Zhai B, Kolippakkam D, Mintseris J, Obar RA, Harris T, Artavanis-Tsakonas S, Sowa ME, De Camilli P, Paulo JA, Harper JW, Gygi SP (2015) The bioplex network: a systematic exploration of the human interactome. Cell 162(2):425–440. doi:10.1016/j. cell.2015.06.043
7. Breitkreutz A, Choi H, Sharom JR, Boucher L, Neduva V, Larsen B, Lin ZY, Breitkreutz BJ, Stark C, Liu G, Ahn J, Dewar-Darch D, Reguly T, Tang X, Almeida R, Qin ZS, Pawson T, Gingras AC, Nesvizhskii AI, Tyers M (2010) A global protein kinase and phosphatase interaction network in yeast. Science 328(5981):1043– 1046. doi:10.1126/science.1176495
8. Sowa ME, Bennett EJ, Gygi SP, Harper JW (2009) Defining the human deubiquitinating enzyme interaction landscape. Cell 138(2):389– 403. doi:10.1016/j.cell.2009.04.042
9. Choi H, Larsen B, Lin ZY, Breitkreutz A, Mellacheruvu D, Fermin D, Qin ZS, Tyers M, Gingras AC, Nesvizhskii AI (2011) SAINT: probabilistic scoring of affinity purification-mass spectrometry data. Nat Methods 8(1):70–73. doi:10.1038/nmeth.1541
10. Dunham WH, Mullin M, Gingras AC (2012) Affinity-purification coupled to mass spectrometry: basic principles and strategies. Proteomics 12(10):1576–1590. doi:10.1002/pmic. 201100523
11. Bisson N, James DA, Ivosev G, Tate SA, Bonner R, Taylor L, Pawson T (2011) Selected reaction monitoring mass spectrometry reveals the dynamics of signaling through the GRB2 adaptor. Nat Biotechnol 29(7):653–658. doi:10.1038/nbt.1905
12. Zheng Y, Zhang C, Croucher DR, Soliman MA, St-Denis N, Pasculescu A, Taylor L, Tate SA, Hardy WR, Colwill K, Dai AY, Bagshaw R, Dennis JW, Gingras AC, Daly RJ, Pawson T (2013) Temporal regulation of EGF signalling networks by the scaffold protein Shc1. Nature 499(7457):166–171. doi:10.1038/ nature12308
13. Lambert JP, Ivosev G, Couzens AL, Larsen B, Taipale M, Lin ZY, Zhong Q, Lindquist S, Vidal M, Aebersold R, Pawson T, Bonner R, Tate S, Gingras AC (2013) Mapping differential interactomes by affinity purification coupled with data-independent mass spectrometry acquisition. Nat Methods 10(12):1239–1245. doi:10.1038/nmeth.2702
14. Collins BC, Gillet LC, Rosenberger G, Rost HL, Vichalkovski A, Gstaiger M, Aebersold R (2013) Quantifying protein interaction dynamics by SWATH mass spectrometry: application to the 14-3-3 system. Nat Methods 10(12): 1246–1253. doi:10.1038/nmeth.2703
15. Hubner NC, Bird AW, Cox J, Splettstoesser B, Bandilla P, Poser I, Hyman A, Mann M (2010) Quantitative proteomics combined with BAC TransgeneOmics reveals in vivo protein interactions. J Cell Biol 189(4):739–754. doi:10.1083/jcb.200911091
16. Roncagalli R, Hauri S, Fiore F, Liang Y, Chen Z, Sansoni A, Kanduri K, Joly R, Malzac A, Lahdesmaki H, Lahesmaa R, Yamasaki S, Saito T, Malissen M, Aebersold R, Gstaiger M, Malissen B (2014) Quantitative proteomics analysis of signalosome dynamics in primary T cells identifies the surface receptor CD6 as a lat adaptor-independent TCR signaling hub. Nat Immunol 15(4):384–392. doi:10.1038/ ni.2843
17. Blagoev B, Kratchmarova I, Ong SE, Nielsen M, Foster LJ, Mann M (2003) A proteomics strategy to elucidate functional protein-protein interactions applied to EGF signaling. Nat Biotechnol 21(3):315–318. doi:10.1038/ nbt790
18. Hilger M, Mann M (2012) Triple SILAC to determine stimulus specific interactions in the Wnt pathway. J Proteome Res 11(2):982–994. doi:10.1021/pr200740a
19. Pagliuca FW, Collins MO, Lichawska A, Zegerman P, Choudhary JS, Pines J (2011) Quantitative proteomics reveals the basis for the biochemical specificity of the cell-cycle machinery. Mol Cell 43(3):406–417. doi:10.1016/j.molcel.2011.05.031
20. Lavallee-Adam M, Rousseau J, Domecq C, Bouchard A, Forget D, Faubert D, Blanchette M, Coulombe B (2013) Discovery of cell compartment specific protein-protein interactions using affinity purification combined with tandem mass spectrometry. J Proteome Res 12(1):272–281. doi:10.1021/pr300778b
21. Kaake RM, Wang X, Burke A, Yu C, Kandur W, Yang Y, Novtisky EJ, Second T, Duan J, Kao A, Guan S, Vellucci D, Rychnovsky SD, Huang L (2014) A new in vivo cross-linking mass spectrometry platform to define protein-protein interactions in living cells. Mol Cell Proteomics 13(12):3533–3543. doi:10.1074/mcp. M114.042630
22. Babu M, Vlasblom J, Pu S, Guo X, Graham C, Bean BD, Burston HE, Vizeacoumar FJ, Snider J, Phanse S, Fong V, Tam YY, Davey M, Hnatshak O, Bajaj N, Chandran S, Punna T, Christopolous C, Wong V, Yu A, Zhong G, Li J, Stagljar I, Conibear E, Wodak SJ, Emili A, Greenblatt JF (2012) Interaction landscape of membrane-protein complexes in Saccharomyces cerevisiae. Nature 489(7417):585–589. doi:10.1038/nature11354
23. Hakhverdyan Z, Domanski M, Hough LE, Oroskar AA, Oroskar AR, Keegan S, Dilworth DJ, Molloy KR, Sherman V, Aitchison JD, Fenyo D, Chait BT, Jensen TH, Rout MP, LaCava J (2015) Rapid, optimized interactomic screening. Nat Methods 12(6):553–560. doi:10.1038/nmeth.3395
24. Roux KJ, Kim DI, Raida M, Burke B (2012) A promiscuous biotin ligase fusion protein identifies proximal and interacting proteins in mammalian cells. J Cell Biol 196(6):801–810. doi:10.1083/jcb.201112098
25. Rhee HW, Zou P, Udeshi ND, Martell JD, Mootha VK, Carr SA, Ting AY (2013) Proteomic mapping of mitochondria in living cells via spatially restricted enzymatic tagging. Science 339(6125):1328–1331. doi:10.1126/ science.1230593
26. KimDI, Birendra KC, Zhu W, Motamedchaboki K, Doye V, Roux KJ (2014) Probing nuclear pore complex architecture with proximity-dependent biotinylation. Proc Natl Acad Sci U S A 111(24):E2453–E2461. doi:10.1073/ pnas.1406459111
27. Lambert JP, Tucholska M, Go C, Knight JD, Gingras AC (2015) Proximity biotinylation and affinity purification are complementary approaches for the interactome mapping of chromatin-associated protein complexes. J Proteomics 118:81–94. doi:10.1016/j. jprot.2014.09.011
28. Dingar D, Kalkat M, Chan PK, Srikumar T, Bailey SD, Tu WB, Coyaud E, Ponzielli R, Kolyar M, Jurisica I, Huang A, Lupien M, Penn LZ, Raught B (2015) BioID identifies novel c-MYC interacting partners in cultured cells and xenograft tumors. J Proteomics 118:95–111. doi:10.1016/j.jprot.2014.09.029
29. Couzens AL, Knight JD, Kean MJ, Teo G, Weiss A, Dunham WH, Lin ZY, Bagshaw RD, Sicheri F, Pawson T, Wrana JL, Choi H, Gingras AC (2013) Protein interaction network of the mammalian Hippo pathway reveals mechanisms of kinase-phosphatase interactions. Sci Signal 6(302):rs15. doi:10.1126/ scisignal.2004712
30. Firat-Karalar EN, Rauniyar N, Yates JR 3rd, Stearns T (2014) Proximity interactions among centrosome components identify regulators of centriole duplication. Curr Biol 24(6):664–670. doi:10.1016/j.cub.2014.01.067
31. Gupta GD, Coyaud E, Goncalves J, Mojarad BA, Liu Y, Wu Q, Gheiratmand L, Comartin D, Tkach JM, Cheung SW, Bashkurov M, Hasegan M, Knight JD, Lin ZY, Schueler M, Hildebrandt F, Moffat J, Gingras AC, Raught B, Pelletier L (2015) A dynamic protein interaction landscape of the human centrosome-cilium interface. Cell 163(6):1484–1499. doi:10.1016/j.cell.2015.10.065
32. Coyaud E, Mis M, Laurent EM, Dunham WH, Couzens AL, Robitaille M, Gingras AC, Angers S, Raught B (2015) BioID-based identification of Skp cullin F-box (SCF)beta-TrCP1/2 E3 ligase substrates. Mol Cell Proteomics 14(7):1781–1795. doi:10.1074/ mcp.M114.045658
33. Cheng YS, Seibert O, Kloting N, Dietrich A, Strassburger K, Fernandez-Veledo S, Vendrell JJ, Zorzano A, Bluher M, Herzig S, Berriel Diaz M, Teleman AA (2015) PPP2R5C couples hepatic glucose and lipid homeostasis. PLoS Genet 11(10):e1005561. doi:10.1371/ journal.pgen.1005561
34. Kean MJ, Couzens AL, Gingras AC (2012) Mass spectrometry approaches to study mammalian kinase and phosphatase associated proteins. Methods 57(4):400–408. doi:10.1016/j. ymeth.2012.06.002
35. Banks CA, Boanca G, Lee ZT, Florens L, Washburn MP (2015) Proteins interacting with cloning scars: a source of false positive protein-protein interactions. Sci Rep 5:8530. doi:10.1038/srep08530
36. Olhovsky M, Williton K, Dai AY, Pasculescu A, Lee JP, Goudreault M, Wells CD, Park JG, Gingras AC, Linding R, Pawson T, Colwill K (2011) OpenFreezer: a reagent information management software system. Nat Methods 8(8):612–613. doi:10.1038/nmeth.1658
37. Liu G, Zhang J, Larsen B, Stark C, Breitkreutz A, Lin ZY, Breitkreutz BJ, Ding Y, Colwill K, Pasculescu A, Pawson T, Wrana JL, Nesvizhskii AI, Raught B, Tyers M, Gingras AC (2010) ProHits: integrated software for mass spectrometry-based interaction proteomics. Nat Biotechnol 28(10):1015–1017. doi:10.1038/nbt1010-1015
38. Liu G, Zhang J, Choi H, Lambert JP, Srikumar T, Larsen B, Nesvizhskii AI, Raught B, Tyers M, Gingras AC (2012) Using ProHits to store, annotate, and analyze affinity purification-mass spectrometry (AP-MS) data. Curr Protoc Bioinformatics Chapter 8:Unit8.16. doi:10.1002/0471250953.bi0816s39
39. Teo G, Liu G, Zhang J, Nesvizhskii AI, Gingras AC, Choi H (2014) SAINTexpress: improvements and additional features in significance analysis of INTeractome software. J Proteomics 100:37–43. doi:10.1016/j.jprot.2013.10.023
40. Mellacheruvu D, Wright Z, Couzens AL, Lambert JP, St-Denis NA, Li T, Miteva YV, Hauri S, Sardiu ME, Low TY, Halim VA, Bagshaw RD, Hubner NC, Al-Hakim A, Bouchard A, Faubert D, Fermin D, Dunham WH, Goudreault M, Lin ZY, Badillo BG, Pawson T, Durocher D, Coulombe B, Aebersold R, Superti-Furga G, Colinge J, Heck AJ, Choi H, Gstaiger M, Mohammed S, Cristea IM, Bennett KL, Washburn MP, Raught B, Ewing RM, Gingras AC, Nesvizhskii AI (2013) The CRAPome: a contaminant repository for affinity purification-mass spectrometry data. Nat Methods 10(8):730–736. doi:10.1038/ nmeth.2557
41. Knight JD, Liu G, Zhang JP, Pasculescu A, Choi H, Gingras AC (2015) A web-tool for visualizing quantitative protein-protein interaction data. Proteomics 15(8):1432–1436. doi:10.1002/pmic.201400429