High throughput protein-protein interaction data: clues for the architecture of protein complexes
Tóm tắt
High-throughput techniques are becoming widely used to study protein-protein interactions and protein complexes on a proteome-wide scale. Here we have explored the potential of these techniques to accurately determine the constituent proteins of complexes and their architecture within the complex. Two-dimensional representations of the 19S and 20S proteasome, mediator, and SAGA complexes were generated and overlaid with high quality pairwise interaction data, core-module-attachment classifications from affinity purifications of complexes and predicted domain-domain interactions. Pairwise interaction data could accurately determine the members of each complex, but was unexpectedly poor at deciphering the topology of proteins in complexes. Core and module data from affinity purification studies were less useful for accurately defining the member proteins of these complexes. However, these data gave strong information on the spatial proximity of many proteins. Predicted domain-domain interactions provided some insight into the topology of proteins within complexes, but was affected by a lack of available structural data for the co-activator complexes and the presence of shared domains in paralogous proteins. The constituent proteins of complexes are likely to be determined with accuracy by combining data from high-throughput techniques. The topology of some proteins in the complexes will be able to be clearly inferred. We finally suggest strategies that can be employed to use high throughput interaction data to define the membership and understand the architecture of proteins in novel complexes.
Tài liệu tham khảo
Alberts B: The cell as a collection of protein machines: preparing the next generation of molecular biologists. Cell 1998,92(3):291–4. 10.1016/S0092-8674(00)80922-8
Aloy P, Russell RB: The third dimension for protein interactions and complexes. Trends Biochem Sci 2002,27(12):633–8. 10.1016/S0968-0004(02)02204-1
Gavin AC, Bosche M, Krause R, Grandi P, Marzioch M, Bauer A, Schultz J, Rick JM, Michon AM, Cruciat CM, others: Functional organization of the yeast proteome by systematic analysis of protein complexes. Nature 2002,415(6868):141–7. 10.1038/415141a
Tucker CL, Gera JF, Uetz P: Towards an understanding of complex protein networks. Trends Cell Biol 2001,11(3):102–6. 10.1016/S0962-8924(00)01902-4
Goll J, Uetz P: The elusive yeast interactome. Genome Biol 2006,7(6):223.
Fields S, Song O: A novel genetic system to detect protein-protein interactions. Nature 1989,340(6230):245–6. 10.1038/340245a0
Rain JC, Selig L, De Reuse H, Battaglia V, Reverdy C, Simon S, Lenzen G, Petel F, Wojcik J, Schachter V, others: The protein-protein interaction map of Helicobacter pylori. Nature 2001,409(6817):211–5. 10.1038/35051615
Ito T, Chiba T, Ozawa R, Yoshida M, Hattori M, Sakaki Y: A comprehensive two-hybrid analysis to explore the yeast protein interactome. Proc Natl Acad Sci USA 2001,98(8):4569–74. 10.1073/pnas.061034498
Giot L, Bader JS, Brouwer C, Chaudhuri A, Kuang B, Li Y, Hao YL, Ooi CE, Godwin B, Vitols E, others: A protein interaction map of Drosophila melanogaster. Science 2003,302(5651):1727–36. 10.1126/science.1090289
Rual JF, Venkatesan K, Hao T, Hirozane-Kishikawa T, Dricot A, Li N, Berriz GF, Gibbons FD, Dreze M, Ayivi-Guedehoussou N, others: Towards a proteome-scale map of the human protein-protein interaction network. Nature 2005,437(7062):1173–8. 10.1038/nature04209
Han JD, Bertin N, Hao T, Goldberg DS, Berriz GF, Zhang LV, Dupuy D, Walhout AJ, Cusick ME, Roth FP, others: Evidence for dynamically organized modularity in the yeast protein-protein interaction network. Nature 2004,430(6995):88–93. 10.1038/nature02555
Gavin AC, Aloy P, Grandi P, Krause R, Boesche M, Marzioch M, Rau C, Jensen LJ, Bastuck S, Dumpelfeld B, others: Proteome survey reveals modularity of the yeast cell machinery. Nature 2006,440(7084):631–6. 10.1038/nature04532
Rigaut G, Shevchenko A, Rutz B, Wilm M, Mann M, Seraphin B: A generic protein purification method for protein complex characterization and proteome exploration. Nat Biotechnol 1999,17(10):1030–2. 10.1038/13732
Pang CN, Krycer JR, Lek A, Wilkins MR: Are protein complexes made of cores, modules and attachments? Proteomics 2008,8(3):425–34. 10.1002/pmic.200700801
Flores A, Briand JF, Gadal O, Andrau JC, Rubbi L, Van Mullem V, Boschiero C, Goussot M, Marck C, Carles C, others: A protein-protein interaction map of yeast RNA polymerase III. Proc Natl Acad Sci USA 1999,96(14):7815–20. 10.1073/pnas.96.14.7815
Houser-Scott F, Xiao S, Millikin CE, Zengel JM, Lindahl L, Engelke DR: Interactions among the protein and RNA subunits of Saccharomyces cerevisiae nuclear RNase P. Proc Natl Acad Sci USA 2002,99(5):2684–9. 10.1073/pnas.052586299
Lehner B, Sanderson CM: A protein interaction framework for human mRNA degradation. Genome Res 2004,14(7):1315–23. 10.1101/gr.2122004
von Mering C, Krause R, Snel B, Cornell M, Oliver SG, Fields S, Bork P: Comparative assessment of large-scale data sets of protein-protein interactions. Nature 2002,417(6887):399–403. 10.1038/nature750
Edwards AM, Kus B, Jansen R, Greenbaum D, Greenblatt J, Gerstein M: Bridging structural biology and genomics: assessing protein interaction data with known complexes. Trends Genet 2002,18(10):529–36. 10.1016/S0168-9525(02)02763-4
Groll M, Ditzel L, Lowe J, Stock D, Bochtler M, Bartunik HD, Huber R: Structure of 20S proteasome from yeast at 2.4 A resolution. Nature 1997,386(6624):463–71. 10.1038/386463a0
Ferrell K, Wilkinson CR, Dubiel W, Gordon C: Regulatory subunit interactions of the 26S proteasome, a complex problem. Trends Biochem Sci 2000,25(2):83–8. 10.1016/S0968-0004(99)01529-7
Sharon M, Taverner T, Ambroggio XI, Deshaies RJ, Robinson CV: Structural organization of the 19S proteasome lid: insights from MS of intact complexes. PLoS Biol 2006,4(8):e267. 10.1371/journal.pbio.0040267
Chadick JZ, Asturias FJ: Structure of eukaryotic Mediator complexes. Trends Biochem Sci 2005,30(5):264–71. 10.1016/j.tibs.2005.03.001
Guglielmi B, van Berkum NL, Klapholz B, Bijma T, Boube M, Boschiero C, Bourbon HM, Holstege FC, Werner M: A high resolution protein interaction map of the yeast Mediator complex. Nucleic Acids Res 2004,32(18):5379–91. 10.1093/nar/gkh878
Baidoobonso SM, Guidi BW, Myers LC: Med19(Rox3) regulates Intermodule interactions in the Saccharomyces cerevisiae mediator complex. J Biol Chem 2007,282(8):5551–9. 10.1074/jbc.M609484200
Wu PY, Ruhlmann C, Winston F, Schultz P: Molecular architecture of the S. cerevisiae SAGA complex. Mol Cell 2004,15(2):199–208. 10.1016/j.molcel.2004.06.005
Timmers HT, Tora L: SAGA unveiled. Trends Biochem Sci 2005,30(1):7–10. 10.1016/j.tibs.2004.11.007
Daniel JA, Grant PA: Multi-tasking on chromatin with the SAGA coactivator complexes. Mutat Res 2007,618(1–2):135–48.
Finn RD, Marshall M, Bateman A: iPfam: visualization of protein-protein interactions in PDB at domain and amino acid resolutions. Bioinformatics 2005,21(3):410–2. 10.1093/bioinformatics/bti011
Walz J, Erdmann A, Kania M, Typke D, Koster AJ, Baumeister W: 26S proteasome structure revealed by three-dimensional electron microscopy. J Struct Biol 1998,121(1):19–29. 10.1006/jsbi.1998.3958
Woychik NA, Hampsey M: The RNA polymerase II machinery: structure illuminates function. Cell 2002,108(4):453–63. 10.1016/S0092-8674(02)00646-3
Bjorklund S, Gustafsson CM: The yeast Mediator complex and its regulation. Trends Biochem Sci 2005,30(5):240–4. 10.1016/j.tibs.2005.03.008
Collins SR, Miller KM, Maas NL, Roguev A, Fillingham J, Chu CS, Schuldiner M, Gebbia M, Recht J, Shales M, others: Functional dissection of protein complexes involved in yeast chromosome biology using a genetic interaction map. Nature 2007,446(7137):806–10. 10.1038/nature05649
Huisinga KL, Pugh BF: A genome-wide housekeeping role for TFIID and a highly regulated stress-related role for SAGA in Saccharomyces cerevisiae. Mol Cell 2004,13(4):573–85. 10.1016/S1097-2765(04)00087-5
Sterner DE, Grant PA, Roberts SM, Duggan LJ, Belotserkovskaya R, Pacella LA, Winston F, Workman JL, Berger SL: Functional organization of the yeast SAGA complex: distinct components involved in structural integrity, nucleosome acetylation, and TATA-binding protein interaction. Mol Cell Biol 1999,19(1):86–98.
Zapater M, Sohrmann M, Peter M, Posas F, de Nadal E: Selective requirement for SAGA in Hog1-mediated gene expression depending on the severity of the external osmostress conditions. Mol Cell Biol 2007,27(11):3900–10. 10.1128/MCB.00089-07
Baumeister W, Walz J, Zuhl F, Seemuller E: The proteasome: paradigm of a self-compartmentalizing protease. Cell 1998,92(3):367–80. 10.1016/S0092-8674(00)80929-0
Wu PY, Winston F: Analysis of Spt7 function in the Saccharomyces cerevisiae SAGA coactivator complex. Mol Cell Biol 2002,22(15):5367–79. 10.1128/MCB.22.15.5367-5379.2002
Schmidt M, Hanna J, Elsasser S, Finley D: Proteasome-associated proteins: regulation of a proteolytic machine. Biol Chem 2005,386(8):725–37. 10.1515/BC.2005.085
Aloy P, Bottcher B, Ceulemans H, Leutwein C, Mellwig C, Fischer S, Gavin AC, Bork P, Superti-Furga G, Serrano L, others: Structure-based assembly of protein complexes in yeast. Science 2004,303(5666):2026–9. 10.1126/science.1092645
Bertin N, Simonis N, Dupuy D, Cusick ME, Han JD, Fraser HB, Roth FP, Vidal M: Confirmation of organized modularity in the yeast interactome. PLoS Biol 2007,5(6):e153. 10.1371/journal.pbio.0050153
Ho E, Webber R, Wilkins MR: Interactive three-dimensional visualization and contextual analysis of protein interaction networks. J Proteome Res 2008,7(1):104–12. 10.1021/pr070274m