Isolation and characterization of plant protein complexes by mass spectrometry

Proteomics

Volumn 11, Issue 9, 2011, Pages 1824-1833

  Pflieger, Delphine ^a   Bigeard, Jean ^a   Hirt, Heribert ^a  

^a UNIVERSITÉ D EVRY VAL D ESSONNE   (France)

Author keywords

MS; Plant proteomics; Protein complexes; Tandem affinity purification

Indexed keywords

COMPLEMENTARY DNA; COP9 SIGNALOSOME; HEAT SHOCK PROTEIN 70; HEAT SHOCK PROTEIN 90; PROTEIN KINASE; TATA BINDING PROTEIN; VEGETABLE PROTEIN;

AFFINITY CHROMATOGRAPHY; ARABIDOPSIS; BINDING AFFINITY; CELL CYCLE; DYNAMICS; GENE SEQUENCE; HUMAN; MASS SPECTROMETRY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN ISOLATION; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; REVIEW; STOICHIOMETRY;

MASS SPECTROMETRY; PLANT PROTEINS; PLANTS; PROTEOME; PROTEOMICS;

EID: 79955007479     PISSN: 16159853     EISSN: 16159861     Source Type: Journal    
DOI: 10.1002/pmic.201000635     Document Type: Review

References (85)

1. Green, D. E., Studies in organized enzyme systems. Harvey Lect. 1958, 177-227.
2. Srere, P. A., Macromolecular interactions: tracing the roots. Trends Biochem. Sci. 2000, 25, 150-153.
3. Yanofsky, C., Rachmeler, M., The exclusion of free indole as an intermediate in the biosynthesis of tryptophan in Neurospora crassa. Biochim. Biophys. Acta 1958, 28, 640-641.
4. Winkel, B. S., Metabolic channeling in plants. Annu. Rev. Plant Biol. 2004, 55, 85-107.
5. Graham, J. W., Williams, T. C., Morgan, M., Fernie, A. R. et al., Glycolytic enzymes associate dynamically with mitochondria in response to respiratory demand and support substrate channeling. Plant Cell 2007, 19, 3723-3738.
6. Droux, M., Ruffet, M. L., Douce, R., Job, D., Interactions between serine acetyltransferase and O-acetylserine (thiol) lyase in higher plants - structural and kinetic properties of the free and bound enzymes. Eur. J. Biochem. 1998, 255, 235-245.
7. Gontero, B., Cardenas, M. L., Ricard, J., A functional five-enzyme complex of chloroplasts involved in the Calvin cycle. Eur. J. Biochem. 1988, 173, 437-443.
8. Graciet, E., Gans, P., Wedel, N., Lebreton, S. et al., The small protein CP12: a protein linker for supramolecular complex assembly. Biochemistry 2003, 42, 8163-8170.
9. Suzuki, J. Y., Ytterberg, A. J., Beardslee, T. A., Allison, L. A. et al., Affinity purification of the tobacco plastid RNA polymerase and in vitro reconstitution of the holoenzyme. Plant J. 2004, 40, 164-172.
10. Asahara, H., Chong, S., In vitro genetic reconstruction of bacterial transcription initiation by coupled synthesis and detection of RNA polymerase holoenzyme. Nucleic Acids Res. 2010, 38, e141.
11. Sharon, M., Robinson, C. V., The role of mass spectrometry in structure elucidation of dynamic protein complexes. Annu. Rev. Biochem. 2007, 76, 167-193.
12. Ramani, A. K., Li, Z. H., Hart, G. T., Carlson, M. W. et al., A map of human protein interactions derived from co-expression of human mRNAs and their orthologs. Mol. Syst. Biol. 2008, 4.
13. Dong, M., Yang, L. L., Williams, K., Fisher, S. J. et al., A "tagless" strategy for identification of stable protein complexes genome-wide by multidimensional orthogonal chromatographic separation and iTRAQ reagent tracking. J. Proteome Res 2008, 7, 1836-1849.
14. Liu, X. P., Yang, W. C., Gao, Q., Regnier, F., Toward chromatographic analysis of interacting protein networks. J. Chromatogr. 2008, 1178, 24-32.
15. Olinares, P. D., Ponnala, L., van Wijk, K. J., Megadalton complexes in the chloroplast stroma of Arabidopsis thaliana characterized by size exclusion chromatography, mass spectrometry, and hierarchical clustering. Mol. Cell. Proteomics 2010, 9, 1594-1615.
16. Remmerie, N., Roef, L., Van De Slijke, E., Van Leene, J. et al., A bioanalytical method for the proteome wide display and analysis of protein complexes from whole plant cell lysates. Proteomics 2009, 9, 598-609.
17. Kikuchi, S., Oishi, M., Hirabayashi, Y., Lee, D. W. et al., A 1-megadalton translocation complex containing Tic20 and Tic21 mediates chloroplast protein import at the inner envelope membrane. Plant Cell 2009, 21, 1781-1797.
18. Balabaskaran Nina, P., Dudkina, N. V., Kane, L. A., van Eyk, J. E. et al., Highly divergent mitochondrial ATP synthase complexes in Tetrahymena thermophila. PLoS Biol. 2010, 8, e1000418.
19. Wang, X., Chen, G., Liu, H., Zhao, Z., Li, Z., Four-dimensional orthogonal electrophoresis system for screening protein complexes and protein-protein interactions combined with mass spectrometry. J. Proteome Res.
20. Munro, S., Pelham, H. R. B., Use of peptide tagging to detect proteins expressed from cloned genes: deletion mapping functional domains of Drosophila hsp7O. EMBO J. 1984, 3, 3087-3093.
21. Rigaut, G., Shevchenko, A., Rutz, B., Wilm, M. et al., A generic protein purification method for protein complex characterization and proteome exploration. Nat. Biotechnol. 1999, 17, 1030-1032.
22. Kocher, T., Superti-Furga G: mass spectrometry-based functional proteomics: from molecular machines to protein networks. Nat. Methods 2007, 4, 807-815.
23. Terpe, K., Overview of tag protein fusions: from molecular and biochemical fundamentals to commercial systems. Appl. Microbiol. Biotechnol. 2003, 60, 523-533.
24. Hochuli, E., Bannwarth, W., Dobeli, H., Gentz, R., Stuber, D., Genetic approach to facilitate purification of recombinant proteins with a novel metal chelate adsorbent. Bio-Technology 1988, 6, 1321-1325.
25. Hochuli, E., Dobeli, H., Schacher, A., New metal chelate adsorbent selective for proteins and peptides containing neighboring histidine-residues. J. Chromatogr. 1987, 411, 177-184.
26. Smith, D. B., Johnson, K. S., Single-step purification of polypeptides expressed in Escherichia coli as fusions with glutathione S-transferase. Gene 1988, 67, 31-40.
27. Diguan, C., Li, P., Riggs, P. D., Inouye, H., Vectors that facilitate the expression and purification of foreign peptides in Escherichia coli by fusion to maltose-binding protein. Gene 1988, 67, 21-30.
28. StofkoHahn, R. E., Carr, D. W., Scott, J. D., A single step purification for recombinant proteins - characterization of a microtubule associated protein (map-2) fragment which associates with the type-II camp-dependent protein-kinase. FEBS Lett. 1992, 302, 274-278.
29. Voss, S., Skerra, A., Mutagenesis of a flexible loop in streptavidin leads to higher affinity for the strep-tag II peptide and improved performance in recombinant protein purification. Protein Eng. 1997, 10, 975-982.
30. Book, A. J., Gladman, N. P., Lee, S. S., Scalf, M. et al., Affinity purification of the Arabidopsis 26S proteasome reveals a diverse array of plant proteolytic complexes. J. Biol. Chem. 2010, 285, 25554-25569.
31. Goudreault, M., D'Ambrosio, L. M., Kean, M. J., Mullin, M. J. 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.
32. Gavin, A. C., Bosche, M., Krause, R., Grandi, P. et al., Functional organization of the yeast proteome by systematic analysis of protein complexes. Nature 2002, 415, 141-147.
33. Krogan, N. J., Cagney, G., Yu, H., Zhong, G. et al., Global landscape of protein complexes in the yeast Saccharomyces cerevisiae. Nature 2006, 440, 637-643.
34. Gully, D., Moinier, D., Loiseau, L., Bouveret, E., New partners of acyl carrier protein detected in Escherichia coli by tandem affinity purification. FEBS Lett. 2003, 548, 90-96.
35. Knuesel, M., Wan, Y., Xiao, Z., Holinger, E. et al., Identification of novel protein-protein interactions using a versatile mammalian tandem affinity purification expression system. Mol. Cell. Proteomics 2003, 2, 1225-1233.
36. Forler, D., Kocher, T., Rode, M., Gentzel, M. et al., An efficient protein complex purification method for functional proteomics in higher eukaryotes. Nat. Biotechnol. 2003, 21, 89-92.
37. Rohila, J. S., Chen, M., Cerny, R., Fromm, M. E., Improved tandem affinity purification tag and methods for isolation of protein heterocomplexes from plants. Plant J. 2004, 38, 172-181.
38. Rivas, S., Romeis, T., Jones, J. D., The Cf-9 disease resistance protein is present in an approximately 420-kilodalton heteromultimeric membrane-associated complex at one molecule per complex. Plant Cell 2002, 14, 689-702.
39. Zhong, J., Haynes, P. A., Zhang, S., Yang, X. et al., Development of a system for the study of protein-protein interactions in planta: characterization of a TATA-box binding protein complex in Oryza sativa. J. Proteome Res. 2003, 2, 514-522.
40. Li, Y., Commonly used tag combinations for tandem affinity purification. Biotechnol. Appl. Biochem. 2010, 55, 73-83.
41. Rubio, V., Shen, Y., Saijo, Y., Liu, Y. et al., An alternative tandem affinity purification strategy applied to Arabidopsis protein complex isolation. Plant J. 2005, 41, 767-778.
42. Rohila, J. S., Chen, M., Chen, S., Chen, J. et al., Protein-protein interactions of tandem affinity purification-tagged protein kinases in rice. Plant J. 2006, 46, 1-13.
43. Rohila, J. S., Chen, M., Chen, S., Chen, J. et al., Protein-protein interactions of tandem affinity purified protein kinases from rice. PLoS One 2009, 4, e6685.
44. Van Leene, J., Stals, H., Eeckhout, D., Persiau, G. et al., A tandem affinity purification-based technology platform to study the cell cycle interactome in Arabidopsis thaliana. Mol. Cell. Proteomics 2007, 6, 1226-1238.
45. Van Leene, J., Witters, E., Inze, D., De Jaeger, G., Boosting tandem affinity purification of plant protein complexes. Trends Plant Sci. 2008, 13, 517-520.
46. Van Leene, J., Hollunder, J., Eeckhout, D., Persiau, G. et al., Targeted interactomics reveals a complex core cell cycle machinery in Arabidopsis thaliana. Mol. Syst. Biol. 2010, 6, 397.
47. Stingl, K., Schauer, K., Ecobichon, C., Labigne, A. et al., In vivo interactome of helicobacter pylori urease revealed by tandem affinity purification. Mol. Cell. Proteomics 2008, 7, 2429-2441.
48. Nittis, T., Guittat, L., LeDuc, R. D., Dao, B. et al., Revealing novel telomere proteins using in vivo cross-linking, tandem affinity purification, and label-free quantitative LC-FTICR-MS. Mol. Cell. Proteomics 2010, 9, 1144-1156.
49. Butland, G., Peregrin-Alvarez, J. M., Li, J., Yang, W. et al., Interaction network containing conserved and essential protein complexes in Escherichia coli. Nature 2005, 433, 531-537.
50. Gavin, A. C., Aloy, P., Grandi, P., Krause, R. et al., Proteome survey reveals modularity of the yeast cell machinery. Nature 2006, 440, 631-636.
51. Giot, L., Bader, J. S., Brouwer, C., Chaudhuri, A. et al., A protein interaction map of Drosophila melanogaster. Science 2003, 302, 1727-1736.
52. Arifuzzaman, M., Maeda, M., Itoh, A., Nishikata, K. et al., Large-scale identification of protein-protein interaction of Escherichia coli K-12. Genome Res. 2006, 16, 686-691.
53. Ho, Y., Gruhler, A., Heilbut, A., Bader, G. D. et al., Systematic identification of protein complexes in Saccharomyces cerevisiae by mass spectrometry. Nature 2002, 415, 180-183.
54. Ewing, R. M., Chu, P., Elisma, F., Li, H. et al., Large-scale mapping of human protein-protein interactions by mass spectrometry. Mol. Syst. Biol. 2007, 3, 89.
55. Breitkreutz, A., Choi, H., Sharom, J. R., Boucher, L. et al., A global protein kinase and phosphatase interaction network in yeast. Science 2010, 328, 1043-1046.
56. Hutchins, J. R., Toyoda, Y., Hegemann, B., Poser, I. et al., Systematic analysis of human protein complexes identifies chromosome segregation proteins. Science 2010, 328, 593-599.
57. Bouwmeester, T., Bauch, A., Ruffner, H., Angrand, P. O. et al., A physical and functional map of the human TNF-alpha/NF-kappa B signal transduction pathway. Nat. Cell Biol. 2004, 6, 97-105.
58. Ranish, J. A., Yi, E. C., Leslie, D. M., Purvine, S. O. et al., The study of macromolecular complexes by quantitative proteomics. Nat. Genet. 2003, 33, 349-355.
59. Blagoev, B., Kratchmarova, I., Ong, S. E., Nielsen, M. et al., A proteomics strategy to elucidate functional protein-protein interactions applied to EGF signaling. Nat. Biotechnol. 2003, 21, 315-318.
60. Brand, M., Ranish, J. A., Kummer, N. T., Hamilton, J. et al., Dynamic changes in transcription factor complexes during erythroid differentiation revealed by quantitative proteomics. Nat. Struc. Mol. Biol. 2004, 11, 73-80.
61. Corvey, C., Koetter, P., Beckhaus, T., Hack, J. et al., Carbon source-dependent assembly of the Snf1p kinase complex in Candida albicans. J. Biol. Chem. 2005, 280, 25323-25330.
62. Kaake, R. M., Milenkovic, T., Przulj, N., Kaiser, P., Huang, L., Characterization of cell cycle specific protein interaction networks of the yeast 26S proteasome complex by the QTAX strategy. J. Proteome Res. 2010, 9, 2016-2029.
63. Selbach, M., Mann, M., Protein interaction screening by quantitative immunoprecipitation combined with knockdown (QUICK). Nat. Methods 2006, 3, 981-983.
64. Sardiu, M. E., Cai, Y., Jin, J., Swanson, S. K. et al., Probabilistic assembly of human protein interaction networks from label-free quantitative proteomics. Proc. Natl. Acad. Sci. USA 2008, 105, 1454-1459.
65. Rinner, O., Mueller, L. N., Hubalek, M., Muller, M. et al., An integrated mass spectrometric and computational framework for the analysis of protein interaction networks. Nat. Biotechnol. 2007, 25, 345-352.
66. Kito, K., Kawaguchi, N., Okada, S., Ito, T., Discrimination between stable and dynamic components of protein complexes by means of quantitative proteomics. Proteomics 2008, 8, 2366-2370.
67. Wang, X. R., Huang, L., Identifying dynamic interactors of protein complexes by quantitative mass spectrometry. Mol. Cell. Proteomics 2008, 7, 46-57.
68. Mousson, F., Kolkman, A., Pijnappel, W., Timmers, H. T. M., Heck, A. J. R., Quantitative proteomics reveals regulation of dynamic components within TATA-binding protein (TBP) transcription complexes. Mol. Cell. Proteomics 2008, 7, 845-852.
69. Pflieger, D., Junger, M. A., Muller, M., Rinner, O. et al., Quantitative proteomic analysis of protein complexes: concurrent identification of interactors and their state of phosphorylation. Mol. Cell. Proteomics 2008, 7, 326-346.
70. Przybylski, C., Junger, M. A., Aubertin, J., Radvanyi, F. et al., Quantitative analysis of protein complex constituents and their phosphorylation states on a LTQ-Orbitrap Instrument. J. Proteome Res. 2010.
71. Smolka, M. B., Albuquerque, C. P., Chen, S. H., Schmidt, K. H. et al., Dynamic changes in protein-protein interaction and protein phosphorylation probed with amine-reactive isotope tag. Mol. Cell. Proteomics 2005, 4, 1358-1369.
72. Pijnappel, W. P., Kolkman, A., Baltissen, M. P., Heck, A. J., Timmers, H. M., Quantitative mass spectrometry of TATA binding protein-containing complexes and subunit phosphorylations during the cell cycle. Proteome Sci. 2009, 7, 46.
73. Vermeulen, M., Eberl, H. C., Matarese, F., Marks, H. et al., Quantitative interaction proteomics and genome-wide profiling of epigenetic histone marks and their readers. Cell 2010, 142, 967-980.
74. Petrotchenko, E. V., Borchers, C. H., Crosslinking combined with mass spectrometry for structural proteomics. Mass. Spectrom. Rev. 2010.
75. Rinner, O., Seebacher, J., Walzthoeni, T., Mueller, L. N. et al., Identification of cross-linked peptides from large sequence databases. Nat. Methods 2008, 5, 315-318.
76. Zhang, H., Tang, X., Munske, G. R., Tolic, N. et al., Identification of protein-protein interactions and topologies in living cells with chemical cross-linking and mass spectrometry. Mol. Cell. Proteomics 2009, 8, 409-420.
77. Gerber, S. A., Rush, J., Stemman, O., Kirschner, M. W., Gygi, S. P., Absolute quantification of proteins and phosphoproteins from cell lysates by tandem MS. Proc. Natl. Acad. Sci. USA 2003, 100, 6940-6945.
78. Schmidt, C., Lenz, C., Grote, M., Luhrmann, R., Urlaub, H., Determination of protein stoichiometry within protein complexes using absolute quantification and multiple reaction monitoring. Anal. Chem. 2010, 82, 2784-2796.
79. Kito, K., Ota, K., Fujita, T., Ito, T., A synthetic protein approach toward accurate mass spectrometric quantification of component stoichiometry of multiprotein complexes. J. Proteome Res. 2007, 6, 792-800.
80. Pratt, J. M., Simpson, D. M., Doherty, M. K., Rivers, J. et al., Multiplexed absolute quantification for proteomics using concatenated signature peptides encoded by QconCAT genes. Nat. Protoc. 2006, 1, 1029-1043.
81. Brun, V., Dupuis, A., Adrait, A., Marcellin, M. et al., Isotope-labeled protein standards: toward absolute quantitative proteomics. Mol. Cell. Proteomics 2007, 6, 2139-2149.
82. Hanke, S., Besir, H., Oesterhelt, D., Mann, M., Absolute SILAC for accurate quantitation of proteins in complex mixtures down to the attomole level. J. Proteome Res. 2008, 7, 1118-1130.
83. Wepf, A., Glatter, T., Schmidt, A., Aebersold, R., Gstaiger, M., Quantitative interaction proteomics using mass spectrometry. Nat. Methods 2009, 6, 203-205.
84. Holzmann, J., Pichler, P., Madalinski, M., Kurzbauer, R., Mechtler, K., Stoichiometry determination of the MP1-p14 complex using a novel and cost-efficient method to produce an equimolar mixture of standard peptides. Anal. Chem. 2009, 81, 10254-10261.
85. Hernandez, H., Dziembowski, A., Taverner, T., Seraphin, B., Robinson, C. V., Subunit architecture of multimeric complexes isolated directly from cells. EMBO Rep. 2006, 7, 605-610.