A Scalable Genome-Editing-Based Approach for Mapping Multiprotein Complexes in Human Cells

Cell Reports

Volumn 13, Issue 3, 2015, Pages 621-633

  Dalvai, Mathieu ^a,b   Loehr, Jeremy ^a   Jacquet, Karine ^a,b   Huard, Caroline C ^a   Roques, Céline ^a,b   Herst, Pauline ^a,b   Côté, Jacques ^a,b   Doyon, Yannick ^a  

^a LAVAL UNIVERSITY   (Canada)

^b UNIVERSITÉ LAVAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

GENOMIC DNA; HOLOENZYME; MINICHROMOSOME MAINTENANCE PROTEIN 8; MINICHROMOSOME MAINTENANCE PROTEIN 9; MULTIPROTEIN COMPLEX; POLYCOMB REPRESSIVE COMPLEX 2; TRANSCRIPTION ACTIVATOR LIKE EFFECTOR NUCLEASE; MINICHROMOSOME MAINTENANCE PROTEIN; PROTEIN BINDING;

ARTICLE; BIOCHEMISTRY; CHROMATIN; CONTROLLED STUDY; CRISPR CAS SYSTEM; DNA REPAIR; GENOME ANALYSIS; HUMAN; HUMAN CELL; PEPTIDE MAPPING; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN ISOLATION; PROTEIN PURIFICATION; PROTEIN STRUCTURE; RNA EDITING; STRUCTURE ACTIVITY RELATION; CHEMISTRY; GENE TARGETING; HUMAN GENOME; PROCEDURES; PROTEOMICS; TUMOR CELL LINE;

CELL LINE, TUMOR; CRISPR-CAS SYSTEMS; GENE TARGETING; GENOME, HUMAN; HUMANS; MINICHROMOSOME MAINTENANCE PROTEINS; PROTEIN BINDING; PROTEOMICS;

EID: 84944676907     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2015.09.009     Document Type: Article

References (65)

1. Abmayr S.M., Yao T., Parmely T., Workman J.L. Preparation of nuclear and cytoplasmic extracts from mammalian cells. Curr. Protoc. Mol. Biol. 2006, 12:11.
2. Alberts B. The cell as a collection of protein machines: preparing the next generation of molecular biologists. Cell 1998, 92:291-294.
3. Alekseyenko A.A., Gorchakov A.A., Kharchenko P.V., Kuroda M.I. Reciprocal interactions of human C10orf12 and C17orf96 with PRC2 revealed by BioTAP-XL cross-linking and affinity purification. Proc. Natl. Acad. Sci. USA 2014, 111:2488-2493.
4. Ali A.M., Pradhan A., Singh T.R., Du C., Li J., Wahengbam K., Grassman E., Auerbach A.D., Pang Q., Meetei A.R. FAAP20: a novel ubiquitin-binding FA nuclear core-complex protein required for functional integrity of the FA-BRCA DNA repair pathway. Blood 2012, 119:3285-3294.
5. Behrends C., Sowa M.E., Gygi S.P., Harper J.W. Network organization of the human autophagy system. Nature 2010, 466:68-76.
6. Bradbury A., Plückthun A. Reproducibility: Standardize antibodies used in research. Nature 2015, 518:27-29.
7. Cai Y., Jin J., Florens L., Swanson S.K., Kusch T., Li B., Workman J.L., Washburn M.P., Conaway R.C., Conaway J.W. The mammalian YL1 protein is a shared subunit of the TRRAP/TIP60 histone acetyltransferase and SRCAP complexes. J. Biol. Chem. 2005, 280:13665-13670.
8. An integrated encyclopedia of DNA elements in the human genome. Nature 2012, 489:57-74. ENCODE Project Consortium.
9. DeKelver R.C., Choi V.M., Moehle E.A., Paschon D.E., Hockemeyer D., Meijsing S.H., Sancak Y., Cui X., Steine E.J., Miller J.C., et al. Functional genomics, proteomics, and regulatory DNA analysis in isogenic settings using zinc finger nuclease-driven transgenesis into a safe harbor locus in the human genome. Genome Res. 2010, 20:1133-1142.
10. Doyon Y., Selleck W., Lane W.S., Tan S., Côté J. Structural and functional conservation of the NuA4 histone acetyltransferase complex from yeast to humans. Mol. Cell. Biol. 2004, 24:1884-1896.
11. Doyon Y., Cayrou C., Ullah M., Landry A.J., Côté V., Selleck W., Lane W.S., Tan S., Yang X.J., Côté J. ING tumor suppressor proteins are critical regulators of chromatin acetylation required for genome expression and perpetuation. Mol. Cell 2006, 21:51-64.
12. Doyon J.B., Zeitler B., Cheng J., Cheng A.T., Cherone J.M., Santiago Y., Lee A.H., Vo T.D., Doyon Y., Miller J.C., et al. Rapid and efficient clathrin-mediated endocytosis revealed in genome-edited mammalian cells. Nat. Cell Biol. 2011, 13:331-337.
13. Fuchs M., Gerber J., Drapkin R., Sif S., Ikura T., Ogryzko V., Lane W.S., Nakatani Y., Livingston D.M. The p400 complex is an essential E1A transformation target. Cell 2001, 106:297-307.
14. 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.
15. Gavin A.C., Maeda K., Kühner S. Recent advances in charting protein-protein interaction: mass spectrometry-based approaches. Curr. Opin. Biotechnol. 2011, 22:42-49.
16. 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.
17. 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.
18. 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.
19. Ho Y., Gruhler A., Heilbut A., Bader G.D., Moore L., Adams S.L., Millar A., Taylor P., Bennett K., Boutilier K., et al. Systematic identification of protein complexes in Saccharomyces cerevisiae by mass spectrometry. Nature 2002, 415:180-183.
20. Hockemeyer D., Soldner F., Beard C., Gao Q., Mitalipova M., DeKelver R.C., Katibah G.E., Amora R., Boydston E.A., Zeitler B., et al. Efficient targeting of expressed and silent genes in human ESCs and iPSCs using zinc-finger nucleases. Nat. Biotechnol. 2009, 27:851-857.
21. Hockemeyer D., Wang H., Kiani S., Lai C.S., Gao Q., Cassady J.P., Cost G.J., Zhang L., Santiago Y., Miller J.C., et al. Genetic engineering of human pluripotent cells using TALE nucleases. Nat. Biotechnol. 2011, 29:731-734.
22. Hsu P.D., Scott D.A., Weinstein J.A., Ran F.A., Konermann S., Agarwala V., Li Y., Fine E.J., Wu X., Shalem O., et al. DNA targeting specificity of RNA-guided Cas9 nucleases. Nat. Biotechnol. 2013, 31:827-832.
23. Hsu P.D., Lander E.S., Zhang F. Development and applications of CRISPR-Cas9 for genome engineering. Cell 2014, 157:1262-1278.
24. Hutchins J.R., Toyoda Y., Hegemann B., Poser I., Hériché J.K., Sykora M.M., Augsburg M., Hudecz O., Buschhorn B.A., Bulkescher J., et al. Systematic analysis of human protein complexes identifies chromosome segregation proteins. Science 2010, 328:593-599.
25. Huttlin E.L., Ting L., Bruckner R.J., Gebreab F., Gygi M.P., Szpyt J., Tam S., Zarraga G., Colby G., Baltier K., et al. The BioPlex Network: A Systematic Exploration of the Human Interactome. Cell 2015, 162:425-440.
26. Ikura T., Ogryzko V.V., Grigoriev M., Groisman R., Wang J., Horikoshi M., Scully R., Qin J., Nakatani Y. Involvement of the TIP60 histone acetylase complex in DNA repair and apoptosis. Cell 2000, 102:463-473.
27. Joung J.K., Sander J.D. TALENs: a widely applicable technology for targeted genome editing. Nat. Rev. Mol. Cell Biol. 2013, 14:49-55.
28. 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.
29. Krogan N.J., Lippman S., Agard D.A., Ashworth A., Ideker T. The cancer cell map initiative: defining the hallmark networks of cancer. Mol. Cell 2015, 58:690-698.
30. Lalonde M.E., Cheng X., Côté J. Histone target selection within chromatin: an exemplary case of teamwork. Genes Dev. 2014, 28:1029-1041.
31. Lawrence M.S., Stojanov P., Mermel C.H., Robinson J.T., Garraway L.A., Golub T.R., Meyerson M., Gabriel S.B., Lander E.S., Getz G. Discovery and saturation analysis of cancer genes across 21 tumour types. Nature 2014, 505:495-501.
32. Leiserson M.D., Vandin F., Wu H.T., Dobson J.R., Eldridge J.V., Thomas J.L., Papoutsaki A., Kim Y., Niu B., McLellan M., et al. Pan-cancer network analysis identifies combinations of rare somatic mutations across pathways and protein complexes. Nat. Genet. 2015, 47:106-114.
33. Lombardo A., Cesana D., Genovese P., Di Stefano B., Provasi E., Colombo D.F., Neri M., Magnani Z., Cantore A., Lo Riso P., et al. Site-specific integration and tailoring of cassette design for sustainable gene transfer. Nat. Methods 2011, 8:861-869.
34. Lutzmann M., Grey C., Traver S., Ganier O., Maya-Mendoza A., Ranisavljevic N., Bernex F., Nishiyama A., Montel N., Gavois E., et al. MCM8- and MCM9-deficient mice reveal gametogenesis defects and genome instability due to impaired homologous recombination. Mol. Cell 2012, 47:523-534.
35. Maiorano D., Lutzmann M., Méchali M. MCM proteins and DNA replication. Curr. Opin. Cell Biol. 2006, 18:130-136.
36. Mali P., Yang L., Esvelt K.M., Aach J., Guell M., DiCarlo J.E., Norville J.E., Church G.M. RNA-guided human genome engineering via Cas9. Science 2013, 339:823-826.
37. Marcon E., Ni Z., Pu S., Turinsky A.L., Trimble S.S., Olsen J.B., Silverman-Gavrila R., Silverman-Gavrila L., Phanse S., Guo H., et al. Human-chromatin-related protein interactions identify a demethylase complex required for chromosome segregation. Cell Rep. 2014, 8:297-310.
38. Margueron R., Reinberg D. The Polycomb complex PRC2 and its mark in life. Nature 2011, 469:343-349.
39. Mozzetta C., Pontis J., Fritsch L., Robin P., Portoso M., Proux C., Margueron R., Ait-Si-Ali S. The histone H3 lysine 9 methyltransferases G9a and GLP regulate polycomb repressive complex 2-mediated gene silencing. Mol. Cell 2014, 53:277-289.
40. Musselman C.A., Avvakumov N., Watanabe R., Abraham C.G., Lalonde M.E., Hong Z., Allen C., Roy S., Nuñez J.K., Nickoloff J., et al. Molecular basis for H3K36me3 recognition by the Tudor domain of PHF1. Nat. Struct. Mol. Biol. 2012, 19:1266-1272.
41. Nishimura K., Ishiai M., Horikawa K., Fukagawa T., Takata M., Takisawa H., Kanemaki M.T. Mcm8 and Mcm9 form a complex that functions in homologous recombination repair induced by DNA interstrand crosslinks. Mol. Cell 2012, 47:511-522.
42. Park J.H., Sun X.J., Roeder R.G. The SANT domain of p400 ATPase represses acetyltransferase activity and coactivator function of TIP60 in basal p21 gene expression. Mol. Cell. Biol. 2010, 30:2750-2761.
43. Park J., Long D.T., Lee K.Y., Abbas T., Shibata E., Negishi M., Luo Y., Schimenti J.C., Gambus A., Walter J.C., Dutta A. The MCM8-MCM9 complex promotes RAD51 recruitment at DNA damage sites to facilitate homologous recombination. Mol. Cell. Biol. 2013, 33:1632-1644.
44. Plass C., Pfister S.M., Lindroth A.M., Bogatyrova O., Claus R., Lichter P. Mutations in regulators of the epigenome and their connections to global chromatin patterns in cancer. Nat. Rev. Genet. 2013, 14:765-780.
45. Rajendra E., Oestergaard V.H., Langevin F., Wang M., Dornan G.L., Patel K.J., Passmore L.A. The genetic and biochemical basis of FANCD2 monoubiquitination. Mol. Cell 2014, 54:858-869.
46. Ran F.A., Hsu P.D., Lin C.Y., Gootenberg J.S., Konermann S., Trevino A.E., Scott D.A., Inoue A., Matoba S., Zhang Y., Zhang F. Double nicking by RNA-guided CRISPR Cas9 for enhanced genome editing specificity. Cell 2013, 154:1380-1389.
47. Reyon D., Tsai S.Q., Khayter C., Foden J.A., Sander J.D., Joung J.K. FLASH assembly of TALENs for high-throughput genome editing. Nat. Biotechnol. 2012, 30:460-465.
48. Rigaut G., Shevchenko A., Rutz B., Wilm M., Mann M., Séraphin B. A generic protein purification method for protein complex characterization and proteome exploration. Nat. Biotechnol. 1999, 17:1030-1032.
49. Rolland T., Taşan M., Charloteaux B., Pevzner S.J., Zhong Q., Sahni N., Yi S., Lemmens I., Fontanillo C., Mosca R., et al. A proteome-scale map of the human interactome network. Cell 2014, 159:1212-1226.
50. Saksouk N., Avvakumov N., Champagne K.S., Hung T., Doyon Y., Cayrou C., Paquet E., Ullah M., Landry A.J., Côté V., et al. HBO1 HAT complexes target chromatin throughout gene coding regions via multiple PHD finger interactions with histone H3 tail. Mol. Cell 2009, 33:257-265.
51. Sardiu M.E., Cai Y., Jin J., Swanson S.K., Conaway R.C., Conaway J.W., Florens L., Washburn M.P. Probabilistic assembly of human protein interaction networks from label-free quantitative proteomics. Proc. Natl. Acad. Sci. USA 2008, 105:1454-1459.
52. Shalem O., Sanjana N.E., Hartenian E., Shi X., Scott D.A., Mikkelsen T.S., Heckl D., Ebert B.L., Root D.E., Doench J.G., Zhang F. Genome-scale CRISPR-Cas9 knockout screening in human cells. Science 2014, 343:84-87.
53. Shiloh Y., Ziv Y. The ATM protein kinase: regulating the cellular response to genotoxic stress, and more. Nat. Rev. Mol. Cell Biol. 2013, 14:197-210.
54. Sowa M.E., Bennett E.J., Gygi S.P., Harper J.W. Defining the human deubiquitinating enzyme interaction landscape. Cell 2009, 138:389-403.
55. Sternberg S.H., Doudna J.A. Expanding the Biologist's Toolkit with CRISPR-Cas9. Mol. Cell 2015, 58:568-574.
56. Steunou A.L., Rossetto D., Côté J. Regulating chromatin by histone acetylation. Fundamentals of Chromatin 2014, 147-212. Springer-Verlag. J.L. Workman, S.M. Abmayr (Eds.).
57. Tsai S.Q., Wyvekens N., Khayter C., Foden J.A., Thapar V., Reyon D., Goodwin M.J., Aryee M.J., Joung J.K. Dimeric CRISPR RNA-guided FokI nucleases for highly specific genome editing. Nat. Biotechnol. 2014, 32:569-576.
58. Tyteca S., Vandromme M., Legube G., Chevillard-Briet M., Trouche D. Tip60 and p400 are both required for UV-induced apoptosis but play antagonistic roles in cell cycle progression. EMBO J. 2006, 25:1680-1689.
59. Urnov F.D., Rebar E.J., Holmes M.C., Zhang H.S., Gregory P.D. Genome editing with engineered zinc finger nucleases. Nat. Rev. Genet. 2010, 11:636-646.
60. Van Leene J., Hollunder J., Eeckhout D., Persiau G., Van De Slijke E., Stals H., Van Isterdael G., Verkest A., Neirynck S., Buffel Y., et al. Targeted interactomics reveals a complex core cell cycle machinery in Arabidopsis thaliana. Mol. Syst. Biol. 2010, 6:397.
61. Venters B.J., Wachi S., Mavrich T.N., Andersen B.E., Jena P., Sinnamon A.J., Jain P., Rolleri N.S., Jiang C., Hemeryck-Walsh C., Pugh B.F. A comprehensive genomic binding map of gene and chromatin regulatory proteins in Saccharomyces. Mol. Cell 2011, 41:480-492.
62. Vogelstein B., Papadopoulos N., Velculescu V.E., Zhou S., Diaz L.A., Kinzler K.W. Cancer genome landscapes. Science 2013, 339:1546-1558.
63. Walden H., Deans A.J. The Fanconi anemia DNA repair pathway: structural and functional insights into a complex disorder. Annu. Rev. Biophys. 2014, 43:257-278.
64. Wang T., Wei J.J., Sabatini D.M., Lander E.S. Genetic screens in human cells using the CRISPR-Cas9 system. Science 2014, 343:80-84.
65. Weber C.M., Henikoff S. Histone variants: dynamic punctuation in transcription. Genes Dev. 2014, 28:672-682.