Chemical cross-linking and mass spectrometry to determine the subunit interaction network in a recombinant human SAGA HAT subcomplex

Protein Science

Volumn 24, Issue 8, 2015, Pages 1232-1246

  Nguyen Huynh, Nha Thi ^a   Sharov, Grigory ^b   Potel, Clément ^a,d,e   Fichter, Pélagie ^b   Trowitzsch, Simon ^c   Berger, Imre ^c   Lamour, Valérie ^b   Schultz, Patrick ^b   Potier, Noëlle ^a   Leize Wagner, Emmanuelle ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

^b INSTITUT DE GÉNÉTIQUE ET DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

^c EUROPEAN MOLECULAR BIOLOGY LABORATORY   (France)

^d UTRECHT UNIVERSITY   (Netherlands)

^e NETHERLANDS PROTEOMICS CENTRE   (Netherlands)

Author keywords

Cross linking mass spectrometry; Protein protein interaction; Proteomics; SAGA HAT subcomplex

Indexed keywords

ADA2B PROTEIN; ADA3 PROTEIN; HISTONE ACETYLTRANSFERASE; HISTONE ACETYLTRANSFERASE GCN5; PROTEIN; TRANSCRIPTION FACTOR SAGA; UNCLASSIFIED DRUG; ACYLTRANSFERASE; BIS(SULFOSUCCINIMIDYL)SUBERATE; CROSS LINKING REAGENT; HISTONE ACETYLTRANSFERASE PCAF; MULTIPROTEIN COMPLEX; P300-CBP-ASSOCIATED FACTOR; PROTEIN SUBUNIT; RECOMBINANT PROTEIN; SGF29 PROTEIN, HUMAN; SIGNAL TRANSDUCING ADAPTOR PROTEIN; SUCCINIMIDE DERIVATIVE; TADA2B PROTEIN, HUMAN; TADA3 PROTEIN, HUMAN; TRANSCRIPTION FACTOR;

AMINO ACID SEQUENCE; ARTICLE; CONTROLLED STUDY; CROSS LINKING; ENZYME ACTIVE SITE; GENE EXPRESSION; GENETIC LINKAGE; HUMAN; MASS SPECTROMETRY; MOLECULAR INTERACTION; MOLECULAR MODEL; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; PROTEIN SECONDARY STRUCTURE; SEQUENCE ANALYSIS; SIZE EXCLUSION CHROMATOGRAPHY; STOICHIOMETRY; TANDEM MASS SPECTROMETRY; X RAY CRYSTALLOGRAPHY; CHEMICAL STRUCTURE; CHEMISTRY; METABOLISM; MOLECULAR GENETICS; PROCEDURES; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; PROTEIN SUBUNIT;

ACETYLTRANSFERASES; ADAPTOR PROTEINS, SIGNAL TRANSDUCING; AMINO ACID SEQUENCE; CROSS-LINKING REAGENTS; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MULTIPROTEIN COMPLEXES; P300-CBP TRANSCRIPTION FACTORS; PROTEIN CONFORMATION; PROTEIN INTERACTION MAPPING; PROTEIN INTERACTION MAPS; PROTEIN MULTIMERIZATION; PROTEIN SUBUNITS; RECOMBINANT PROTEINS; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; SUCCINIMIDES; TRANSCRIPTION FACTORS;

EID: 84943389760     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1002/pro.2676     Document Type: Article

References (61)

1. Purdy MD, Bennett BC, McIntire WE, Khan AK, Kasson PM, Yeager M (2014) Function and dynamics of macromolecular complexes explored by integrative structural and computational biology. Curr Opin Struct Biol 27: 138-148.
2. Göbl C, Madl T, Simon B, Sattler M (2014) NMR approaches for structural analysis of multidomain proteins and complexes in solution. Prog Nucl Magn Reson Spectrosc 80: 26-63.
3. Rodrigues JPGLM, Bonvin AMJJ (2014) Integrative computational modeling of protein interactions. FEBS J 281: 1988-2003.
4. Heck AJR (2008) Native mass spectrometry: A bridge between interactomics and structural biology. Nat Methods 5: 927-933.
5. Lanucara F, Holman SW, Gray CJ, Eyers CE (2014) The power of ion mobility-mass spectrometry for structural characterization and the study of conformational dynamics. Nat Chem 6: 281-294.
6. Konermann L, Tong X, Pan Y (2008) Protein structure and dynamics studied by mass spectrometry: H/D exchange, hydroxyl radical labeling, and related approaches. J Mass Spectrom 43: 1021-1036.
7. Merkley ED, Cort JR, Adkins JN (2013) Cross-linking and mass spectrometry methodologies to facilitate structural biology: Finding a path through the maze. J Struct Funct Genomics 14: 77-90.
8. Stengel F, Aebersold R, Robinson CV (2012) Joining Forces: Integrating Proteomics and Cross-linking with the Mass Spectrometry of Intact Complexes. Mol Cell Proteomics 11: R111.014027.
9. Singh P, Panchaud A, Goodlett DR (2010) Chemical Cross-Linking and Mass Spectrometry As a Low-Resolution Protein Structure Determination Technique. Anal Chem 82: 2636-2642.
10. Leitner A, Walzthoeni T, Kahraman A, Herzog F, Rinner O, Beck M, Aebersold R (2010) Probing Native Protein Structures by Chemical Cross-linking, Mass Spectrometry, and Bioinformatics. Mol Cell Proteomics 9: 1634-1649.
11. Rappsilber J (2011) The beginning of a beautiful friendship: Cross-linking/mass spectrometry and modelling of proteins and multi-protein complexes. J Struct Biol 173: 530-540.
12. Murakami K, Elmlund H, Kalisman N, Bushnell DA, Adams CM, Azubel M, Elmlund D, Levi-Kalisman Y, Liu X, Gibbons BJ, Levitt M, Kornberg RD (2013) Architecture of an RNA polymerase II transcription pre-initiation complex. Science 342: 1238724.
13. Müller MQ, Sinz A (2012) Chemical cross-linking and high-resolution mass spectrometry to study protein-drug interactions. Methods Mol Biol 803: 205-218.
14. Kalisman N, Adams CM, Levitt M (2012) Subunit order of eukaryotic TRiC/CCT chaperonin by crosslinking, mass spectrometry, and combinatorial homology modeling. Proc Natl Acad Sci 109: 2884-2889.
15. Lössl P, Kölbel K, Tänzler D, Nannemann D, Ihling CH, Keller MV, Schneider M, Zaucke F, Meiler J, Sinz A (2014) Analysis of nidogen-1/laminin g1 interaction by cross-linking, mass spectrometry, and computational modeling reveals multiple binding modes. PLoS ONE 9: E112886.
16. Thierbach K, von Appen A, Thoms M, Beck M, Flemming D, Hurt E (2013) Protein Interfaces of the Conserved Nup84 Complex from Chaetomium thermophilum Shown by Crosslinking Mass Spectrometry and Electron Microscopy. Structure 21: 1672-1682.
17. Kim SJ, Fernandez-Martinez J, Sampathkumar P, Martel A, Matsui T, Tsuruta H, Weiss TM, Shi Y, Markina-Inarrairaegui A, Bonanno JB, Sauder JM, Burley SK, Chait BT, Almo SC, Rout MP, Sali A. (2014) Integrative Structure-Function Mapping of the Nucleoporin Nup133 Suggests a Conserved Mechanism for Membrane Anchoring of the Nuclear Pore Complex. Mol. Cell. Proteomics 13: 2911-2926.
18. Paramelle D, Miralles G, Subra G, Martinez J (2013) Chemical cross-linkers for protein structure studies by mass spectrometry. Proteomics 13: 438-456.
19. Sutherland BW, Toews J, Kast J (2008) Utility of formaldehyde cross-linking and mass spectrometry in the study of protein-protein interactions. J Mass Spectrom 43: 699-715.
20. Rhode BM, Hartmuth K, Urlaub H, Lührmann R (2003) Analysis of site-specific protein-RNA cross-links in isolated RNP complexes, combining affinity selection and mass spectrometry. RNA 9: 1542-1551.
21. Fritzsche R, Ihling CH, Götze M, Sinz A (2012) Optimizing the enrichment of cross-linked products for mass spectrometric protein analysis. Rapid Commun Mass Spectrom 26: 653-658.
22. Lascoux D, Paramelle D, Subra G, Heymann M, Geourjon C, Martinez J, Forest E (2007) Discrimination and selective enhancement of signals in the MALDI mass spectrum of a protein by combining a matrix-based label for lysine residues with a neutral matrix. Angew Chem Int Ed 46: 5594-5597.
23. Paramelle D, Cantel S, Enjalbal C, Amblard M, Forest E, Heymann M, Geourjon C, Martinez J, Subra G (2009) A new generation of cross-linkers for selective detection by MALDI MS. Proteomics 9: 5384-5388.
24. Götze M, Pettelkau J, Schaks S, Bosse K, Ihling CH, Krauth F, Fritzsche R, Kühn U, Sinz A (2011) StavroX-A Software for Analyzing Crosslinked Products in Protein Interaction Studies. J Am Soc Mass Spectrom 23: 76-87.
25. Rasmussen MI, Refsgaard JC, Peng L, Houen G, Højrup P (2011) CrossWork: Software-Assisted identification of cross-linked peptides. J Proteomics 74: 1871-1883.
26. Yang B, Wu YJ, Zhu M, Fan SB, Lin J, Zhang K, Li S, Chi H, Li YX, Chen HF, Luo SK, Ding YH, Wang LH, Hao Z, Xiu LY, Chen S, Ye K, He SM, Dong MQ (2012) Identification of cross-linked peptides from complex samples. Nat Methods 9: 904-906.
27. Rinner O, Seebacher J, Walzthoeni T, Mueller L, Beck M, Schmidt A, Mueller M, Aebersold R (2008) Identification of cross-linked peptides from large sequence databases. Nat Methods 5: 315-318.
28. Grant PA, Duggan L, Côte J, Roberts SM, Brownell JE, Candau R, Ohba R, Owen-Hughes T, Allis CD, Winston F, Berger SL, Workman JL (1997) Yeast Gcn5 functions in two multisubunit complexes to acetylate nucleosomal histones: Characterization of an Ada complex and the SAGA (Spt/Ada) complex. Genes Dev 11: 1640-1650.
29. Grünberg S, Hahn S (2013) Structural insights into transcription initiation by RNA polymerase II. Trends Biochem Sci 38: 603-611.
30. Hahn S, Young ET (2011) Transcriptional regulation in Saccharomyces cerevisiae: Transcription factor regulation and function, mechanisms of initiation, and roles of activators and coactivators. Genetics 189: 705-736.
31. Nagy Z, Tora L (2007) Distinct GCN5/PCAF-containing complexes function as co-Activators and are involved in transcription factor and global histone acetylation. Oncogene 26: 5341-5357.
32. Spedale G, Timmers HTM, Pijnappel WWMP (2012) ATAC-king the complexity of SAGA during evolution. Genes Dev 26: 527-541.
33. Eisenmann DM, Chapon C, Roberts SM, Dollard C, Winston F (1994) The Saccharomyces cerevisiae SPT8 gene encodes a very acidic protein that is functionally related to SPT3 and TATA-binding protein. Genetics 137: 647-657.
34. Brand M, Leurent C, Mallouh V, Tora L, Schultz P (1999) Three-dimensional structures of the TAFIIcontaining complexes TFIID and TFTC. Science 286: 2151-2153.
35. Wu P-YJ, Ruhlmann C, Winston F, Schultz P (2004) Molecular Architecture of the S. cerevisiae SAGA Complex. Mol Cell 15: 199-208.
36. Lee KK, Sardiu ME, Swanson SK, Gilmore JM, Torok M, Grant PA, Florens L, Workman JL, Washburn MP (2011) Combinatorial depletion analysis to assemble the network architecture of the SAGA and ADA chromatin remodeling complexes. Mol Syst Biol 7: 503.
37. Bian C, Xu C, Ruan J, Lee KK, Burke TL, Tempel W, Barsyte D, Li J, Wu M, Zhou BO, Fleharty BE, Paulson A, Allali-Hassani A, Zhou JQ, Mer G, Grant PA, Workman JL, Zang J, Min J (2011) Sgf29 binds histone H3K4me2/3 and is required for SAGA complex recruitment and histone H3 acetylation. EMBO J 30: 2829-2842.
38. Durant M, Pugh BF (2006) Genome-wide relationships between TAF1 and histone acetyltransferases in Saccharomyces cerevisiae. Mol Cell Biol 26: 2791-2802.
39. Hassan AH, Prochasson P, Neely KE, Galasinski SC, Chandy M, Carrozza MJ, Workman JL (2002) Function and selectivity of bromodomains in anchoring chromatin-modifying complexes to promoter nucleosomes. Cell 111: 369-379.
40. Vermeulen M, Eberl HC, Matarese F, Marks H, Denissov S, Butter F, Lee KK, Olsen JV, Hyman AA, Stunnenberg HG, Mann M (2010) Quantitative interaction proteomics and genome-wide profiling of epigenetic histone marks and their readers. Cell 142: 967-980.
41. Trowitzsch S, Bieniossek C, Nie Y, Garzoni F, Berger I (2010) New baculovirus expression tools for recombinant protein complex production. J Struct Biol 172: 45-54.
42. Lee YJ, Lackner LL, Nunnari JM, Phinney BS (2007) Shotgun Cross-Linking Analysis for Studying Quaternary and Tertiary Protein Structures. J Proteome Res 6: 3908-3917.
43. Wenzel R, Röhling U, Nazabal A, Hillenkamp F (2009) A detector device for high mass ion detection, a method for analyzing ions of high mass and a device for selection between ion detectors. Available from: Patent WO/2009/086642.
44. Müller DR, Schindler P, Towbin H, Wirth U, Voshol H, Hoving S, Steinmetz MO (2001) Isotope-Tagged crosslinking reagents. A new tool in mass spectrometric protein interaction analysis. Anal Chem 73: 1927-1934.
45. Gaucher SP, Hadi MZ, Young MM (2006) Influence of crosslinker identity and position on gas-phase dissociation of Lys-Lys crosslinked peptides. J Am Soc Mass Spectrom 17: 395-405.
46. Hilton GR, Benesch JLP (2012) Two decades of studying non-covalent biomolecular assemblies by means of electrospray ionization mass spectrometry. J R Soc Interface 9: 801-816.
47. Mann M, Hendrickson RC, Pandey A (2001) Analysis of proteins and proteomes by mass spectrometry. Annu Rev Biochem 70: 437-473.
48. Schubert P, Hoffman MD, Sniatynski MJ, Kast J (2006) Advances in the analysis of dynamic protein complexes by proteomics and data processing. Anal Bioanal Chem 386: 482-493.
49. Candau R, Berger SL (1996) Structural and functional analysis of yeast putative adaptors. Evidence for an adaptor complex in vivo. J Biol Chem 271: 5237-5245.
50. Kurabe N, Katagiri K, Komiya Y, Ito R, Sugiyama A, Kawasaki Y, Tashiro F (2007) Deregulated expression of a novel component of TFTC/STAGA histone acetyltransferase complexes, rat SGF29, in hepatocellular carcinoma: Possible implication for the oncogenic potential of c-Myc. Oncogene 26: 5626-5634.
51. Ito T, Chiba T, Ozawa R, Yoshida M, Hattori M, Sakaki Y (2001) A comprehensive two-hybrid analysis to explore the yeast protein interactome. Proc Natl Acad Sci U S A 98: 4569-4574.
52. Rolland T, Taşan M, Charloteaux B, Pevzner SJ, Zhong Q, Sahni N, Yi S, Lemmens I, Fontanillo C, Mosca R, Kamburov A, Ghiassian SD, Yang X, Ghamsari L, Balcha D, Begg BE, Braun P, Brehme M, Broly MP, Carvunis AR, Convery-Zupan D, Corominas R, Coulombe-Huntington J, Dann E, Dreze M, Dricot A, Fan C, Franzosa E, Gebreab F, Gutierrez BJ, Hardy MF, Jin M, Kang S, Kiros R, Lin GN, Luck K, MacWilliams A, Menche J, Murray RR, Palagi A, Poulin MM, Rambout X, Rasla J, Reichert P, Romero V, Ruyssinck E, Sahalie JM, Scholz A, Shah AA, Sharma A, Shen Y, Spirohn K, Tam S, Tejeda AO, Trigg SA, Twizere JC, Vega K, Walsh J, Cusick ME, Xia Y, Barabasi AL, Iakoucheva LM, Aloy P, De Las Rivas J, Tavernier J, Calderwood MA, Hill DE, Hao T, Roth FP, Vidal M (2014) A proteome-scale map of the human interactome network. Cell 159: 1212-1226.
53. Rual J-F, Venkatesan K, Hao T, Hirozane-Kishikawa T, Dricot A, Li N, Berriz GF, Gibbons FD, Dreze M, Ayivi-Guedehoussou N, Klitgord N, Simon C, Boxem M, Milstein S, Rosenberg J, Goldberg DS, Zhang LV, Wong SL, Franklin G, Li S, Albala JS, Lim J, Fraughton C, Llamosas E, Cevik S, Bex C, Lamesch P, Sikorski RS, Vandenhaute J, Zoghbi HY, Smolyar A, Bosak S, Sequerra R, Doucette-Stamm L, Cusick ME, Hill DE, Roth FP, Vidal M (2005) Towards a proteome-scale map of the human protein-protein interaction network. Nature 437: 1173-1178.
54. Fischer L, Chen ZA, Rappsilber J (2013) Quantitative cross-linking/mass spectrometry using isotope-labelled cross-linkers. J Proteomics 88: 120-128.
55. Merkley ED, Rysavy S, Kahraman A, Hafen RP, Daggett V, Adkins JN (2014) Distance restraints from crosslinking mass spectrometry: Mining a molecular dynamics simulation database to evaluate lysine-lysine distances. Protein Sci 23: 747-759.
56. Gamper AM, Kim J, Roeder RG (2009) The STAGA subunit ADA2b is an important regulator of human GCN5 catalysis. Mol Cell Biol 29: 266-280.
57. Han Y, Luo J, Ranish J, Hahn S (2014) Architecture of the Saccharomyces cerevisiae SAGA transcription coactivator complex. EMBO J 33: 2534-2546.
58. Costanzo M, Baryshnikova A, Bellay J, Kim Y, Spear ED, Sevier CS, Ding H, Koh JL, Toufighi K, Mostafavi S, Prinz J, St Onge RP, VanderSluis B, Makhnevych T, Vizeacoumar FJ, Alizadeh S, Bahr S, Brost RL, Chen Y, Cokol M, Deshpande R, Li Z, Lin ZY, Liang W, Marback M, Paw J, San Luis BJ, Shuteriqi E, Tong AH, van Dyk N, Wallace IM, Whitney JA, Weirauch MT, Zhong G, Zhu H, Houry WA, Brudno M, Ragibizadeh S, Papp B, Pal C, Roth FP, Giaever G, Nislow C, Troyanskaya OG, Bussey H, Bader GD, Gingras AC, Morris QD, Kim PM, Kaiser CA, Myers CL, Andrews BJ, Boone C (2010) The genetic landscape of a cell. Science 327: 425-431.
59. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254.
60. Laemmli UK (1970) Cleavage of Structural Proteins during the Assembly of the Head of Bacteriophage T4. Nature 227: 680-685.
61. Burnette WN (1981) "Western Blotting": Electrophoretic transfer of proteins from sodium dodecyl sulfatepolyacrylamide gels to unmodified nitrocellulose and radiographic detection with antibody and radioiodinated protein A. Anal Biochem 112: 195-203.