Unraveling tobacco BY-2 protein complexes with BN PAGE/LC-MS/MS and clustering methods

Journal of Proteomics

Volumn 74, Issue 8, 2011, Pages 1201-1217

  Remmerie, Noor ^a,b   De Vijlder, Thomas ^a,b   Valkenborg, Dirk ^a,c,d   Laukens, Kris ^b,e   Smets, Koen ^b   Vreeken, Jilles ^b   Mertens, Inge ^a,c   Carpentier, Sebastien C ^f   Panis, Bart ^f   De Jaeger, Geert ^g,h   Blust, Ronny ^b   Prinsen, Els ^b   Witters, Erwin ^a,b,c  

^a Center for Proteomics (CFP)   (Belgium)

^b UNIVERSITY OF ANTWERP   (Belgium)

^c FLEMISH INSTITUTE FOR TECHNOLOGICAL RESEARCH VITO   (Belgium)

^d HASSELT UNIVERSITY   (Belgium)

^e Biomedical Informatics Research Center Antwerp (Biomina)   (Belgium)

^f UNIVERSITY OF LEUVEN   (Belgium)

^g DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^h GHENT UNIVERSITY   (Belgium)

Author keywords

Blue native gel electrophoresis; Clustering; Data mining; Liquid chromatography; Nicotiana tabacum cv. Bright Yellow 2; Protein complexes

Indexed keywords

BRIGHT YELLOW 2 PROTEIN; PROTEASOME; UNCLASSIFIED DRUG; VEGETABLE PROTEIN;

ARTICLE; BLUE NATIVE GEL ELECTROPHORESIS; CELL LYSATE; CLUSTER ANALYSIS; GEL ELECTROPHORESIS; GENETIC ANALYSIS; LIQUID CHROMATOGRAPHY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN ISOLATION; PROTEIN MODIFICATION; PROTEIN PURIFICATION; TANDEM MASS SPECTROMETRY; TOBACCO;

CHROMATOGRAPHY, LIQUID; CLUSTER ANALYSIS; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; ELECTROPHORESIS, POLYACRYLAMIDE GEL; MULTIPROTEIN COMPLEXES; PLANT PROTEINS; TANDEM MASS SPECTROMETRY; TOBACCO;

NICOTIANA TABACUM;

EID: 79961012403     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2011.03.023     Document Type: Article

References (76)

1. Alberts B. The cell as a collection of protein machines: preparing the next generation of molecular biologists. Cell 1998, 92:291-294.
2. Nelson N., Ben-Shem A. The complex architecture of oxygenic photosynthesis. Nat. Rev. Mol. Cell. Biol. 2005, 6:818.
3. Desprez T., Juraniec M., Crowell E.F., Jouy H., Pochylova Z., Parcy F., et al. Organization of cellulose synthase complexes involved in primary cell wall synthesis in Arabidopsis thaliana. Proc Natl Acad Sci U S A 2007, 104:15572-15577.
4. Pauwels L., Barbero G.F., Geerinck J., Tilleman S., Grunewald W., Pérez A.C., et al. NINJA connects the co-repressor TOPLESS to jasmonate signalling. Nature 2010, 464:788-791.
5. Gavin A.C., Bösche M., Krause R., Grandi P., Marzioch M., Bauer A., et al. Functional organization of the yeast proteome by systematic analysis of protein complexes. Nature 2002, 415:141-147.
6. Van Leene J., Hollunder J., Eeckhout D., Persiau G., Van De Slijke E., Stals H., et al. Targeted interactomics reveals a complex core cell cycle machinery in Arabidopsis thaliana. Mol Syst Biol 2010, 6:397.
7. Fields S., Song O. A novel genetic system to detect protein protein interactions. Nature 1989, 340:245-246.
8. Williams N.E. Immunoprecipitation procedures. Methods Cell Biol 2000, 62:449-453.
9. Kerppola T.K. Bimolecular fluorescence complementation: visualization of molecular interactions in living cells. Methods Cell Biol 2008, 85:431-470.
10. Shoemaker B.A., Panchenko A.R. Deciphering protein-protein interactions. Part II. Computational methods to predict protein and domain interaction partners. Plos Comput Biol 2007, 3:e43.
11. Hartman N.T., Sicilia F., Lilley K.S., Dupree P. Proteomic complex detection using sedimentation. Anal Chem 2007, 79:2078-2083.
12. Kumaran S., Yi H., Krishnan H.B., Jez J.M. Assembly of the cysteine synthase complex and the regulatory role of protein-protein interactions. J Biol Chem 2009, 284:10268-10275.
13. Remmerie N., Roef L., Van De Slijke E., Van Leene J., Persiau G., Eeckhout D., 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.
14. Schägger H., Vonjagow G. Blue native electrophoresis for isolation of membrane-protein complexes in enzymatically active form. Anal Biochem 1991, 199:223-231.
15. Wittig I., Braun H.P., Schägger H. Blue native PAGE. Nat Protoc 2006, 1:418-428.
16. Reisinger V., Eichacker L.A. Solubilization of membrane protein complexes for blue native PAGE. J Proteomics 2008, 71:277-283.
17. Eubel H., Braun H., Millar A.H. Blue-native PAGE in plants: a tool in analysis of protein-protein interactions. Plant Methods 2005, 1:11.
18. Wittig I., Schägger H. Native electrophoretic techniques to identify protein-protein interactions. Proteomics 2009, 9:5214-5223.
19. Fandiño A.S., Rais I., Vollmer M., Elgass H., Schägger H., Karas M. LC-nanospray-MS/MS analysis of hydrophobic proteins from membrane protein complexes isolated by blue-native electrophoresis. J Mass Spectrom 2005, 40:1223-1231.
20. Wessels H.J., Vogel R.O., van den Heuvel L., Smeitink J.A., Rodenburg R.J., Nijtmans L.G., et al. LC-MS/MS as an alternative for SDS-PAGE in blue native analysis of protein complexes. Proteomics 2009, 9:4221-4228.
21. Helbig A.O., de Groot M.J., van Gestel R.A., Mohammed S., de Hulster E.A., Luttik M.A., et al. A three-way proteomics strategy allows differential analysis of yeast mitochondrial membrane protein complexes under anaerobic and aerobic conditions. Proteomics 2009, 9:4787-4798.
22. Andersen J.S., Wilkinson C.J., Mayor T., Mortensen P., Nigg E.A., Mann M. Proteomic characterization of the human centrosome by protein correlation profiling. Nature 2003, 426:570-574.
23. Freyhult E., Landfors M., Önskog J., Hvidsten T.R., Rydén P. Challenges in microarray class discovery: a comprehensive examination of normalization, gene selection and clustering. BMC Bioinformatics 2010, 11:503.
24. Datta S., Datta S. Methods for evaluating clustering algorithms for gene expression data using a reference set of functional classes. BMC Bioinformatics 2006, 7:397.
25. Yona G., Dirks W., Rahman S. Comparing algorithms for clustering of expression data: how to assess gene clusters. Methods Mol Biol 2009, 541:479-509.
26. Sardiu M.E., Florens L., Washburn M.P. Evaluation of clustering algorithms for protein complex and protein interaction network assembly. J Proteome Res 2009, 8:2944-2952.
27. Sardiu M.E., Gilmore J.M., Carrozza M.J., Li B., Workman J.L., Florens L., et al. Determining protein complex connectivity using a probabilistic deletion network derived from quantitative proteomics. PLoS One 2009, 4:e7310.
28. Choi H., Kim S., Gingras A.C., Nesvizhskii A.I. Analysis of protein complexes through model-based biclustering of label-free quantitative AP-MS data. Mol Syst Biol 2010, 6:385.
29. Dittrich M.T., Klau G.W., Rosenwald A., Dandekar T., Müller T. Identifying functional modules in protein-protein interaction networks: an integrated exact approach. Bioinformatics 2008, 24:i223-i231.
30. 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.
31. Ashburner M., Ball C.A., Blake J.A., Botstein D., Butler H., Cherry J.M., et al. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet 2005, 25:25-29.
32. Nagata T., Nemoto Y., Hasezawa S. Tobacco BY-2 cell line as the 'HeLa' cell in the cell biology of higher plants. Int Rev Cytol 1992, 132:1-30.
33. Carpentier S.C., Panis B., Vertommen A., Swennen R., Sergeant K., Renaut J., et al. Proteome analysis of non-model plants: a challenging but powerful approach. Mass Spectrom Rev 2008, 27:354-377.
34. Searle B.C., Turner M., Nesvizhskii A.I. Improving sensitivity by probabilistically combining results from multiple MS/MS search methodologies. J Proteome Res 2008, 7:245-253.
35. Neuhoff V., Arold N., Taube D., Ehrhardt W. Improved staining of proteins in polyacrylamide gels including isoelectric focusing gels with clear background at nanogram sensitivity using Coomassie Brilliant Blue G-250 and R-250. Electrophoresis 1988, 9:255-262.
36. Shevchenko A., Tomas H., Havlis J., Olsen J.V., Mann M. In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat Protoc 2006, 1:2856-2860.
37. Lauber W.M., Carroll J.A., Dufield D.R., Kiesel J.R., Radabaugh M.R., Malone J.P. Mass spectrometry compatibility of two-dimensional gel protein stains. Electrophoresis 2001, 22:906-918.
38. Keller A., Nesvizhskii A.I., Kolker E., Aebersold R. Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal Chem 2002, 74:5383-5392.
39. Nesvizhskii A.I., Keller A., Kolker E., Aebersold R. A statistical model for identifying proteins by tandem mass spectrometry. Anal Chem 2003, 75:4646-4658.
40. Altschul S.F., Gish W., Miller W., Myers E.W., Lipman D.J. Basic local alignment search tool. J Mol Biol 1990, 215:403-410.
41. Spath H. Cluster dissection and analysis: theory, FORTRAN programs, examples 1985, Halsted Press, New York.
42. Geerts F., Goethals B., Mielikäinen T. Tiling databases. Lecture notes in computer science 2004, vol. 3245:278-289. Springer.
43. Maere S., Heymans K., Kuiper M. BiNGO: a Cytoscape plugin to assess overrepresentation of gene ontology categories in biological networks. Bioinformatics 2005, 21:3448-3449.
44. Cline M.S., Smoot M., Cerami E., Kuchinsky A., Landys N., Workman C., et al. Integration of biological networks and gene expression data using Cytoscape. Nat Protoc 2007, 2:2366-2382.
45. Jensen L.J., Kuhn M., Stark M., Chaffron S., Creevey C., Muller J., et al. STRING 8-a global view on proteins and their functional interactions in 630 organisms. Nucleic Acids Res 2009, 37:D412-D416.
46. Brandão M.M., Dantas L.L., Silva-Filho M.C. AtPIN: Arabidopsis thaliana protein interaction network. BMC Bioinformatics 2009, 10:454.
47. Aranda B., Achuthan P., Alam-Faruque Y., Armean I., Bridge A., Derow C., et al. The IntAct molecular interaction database in 2010. Nucleic Acids Res 2010, 38:D525-D531.
48. Wiles A.M., Doderer M., Ruan J., Gu T.T., Ravi D., Blackman B., et al. Building and analyzing protein interactome networks by cross-species comparisons. BMC Syst Biol 2010, 4:36.
49. Agrawal R., Srikant R. Fast algorithms for mining association rules. Proceedings of the Intl. Conf. on Very Large Data Bases (VLDB) 1994, 487-499.
50. Gavin A.C., Aloy P., Grandi P., Krause R., Boesche M., Marzioch M., et al. Proteome survey reveals modularity of the yeast cell machinery. Nature 2006, 440:631-636.
51. Pang C.N., Krycer J.R., Lek A., Wilkins M.R. Are protein complexes made of cores, modules and attachments?. Proteomics 2008, 8:425-434.
52. 6 biosynthesis proteins. Mol Plant 2010, 3:890-903.
53. Tanase K., Yamaki S. Purification and characterization of two sucrose synthase isoforms from Japanese pear fruit. Plant Cell Physiol 2000, 41:408-414.
54. Matic S., Akerlund H.E., Everitt E., Widell S. Sucrose synthase isoforms in cultured tobacco cells. Plant Physiol Biochem 2004, 42:299-306.
55. Reiter W.D., Vanzin G.F. Molecular genetics of nucleotide sugar interconversion pathways in plants. Plant Mol Biol 2001, 47:95-113.
56. Bush M.S., Hutchins A.P., Jones A.M., Naldrett M.J., Jarmolowski A., Lloyd C.W., et al. Selective recruitment of proteins to 5? cap complexes during the growth cycle in Arabidopsis. Plant J 2009, 59:400-412.
57. Yang P., Fu H., Walker J., Papa C.M., Smalle J., Ju Y.M., et al. Purification of the Arabidopsis 26S proteasome: biochemical and molecular analyses revealed the presence of multiple isoforms. J Biol Chem 2004, 279:6401-6413.
58. Peltier J.B., Cai Y., Sun Q., Zabrouskov V., Giacomelli L., Rudella A., et al. The oligomeric stromal proteome of Arabidopsis thaliana chloroplasts. Mol Cell Proteomics 2006, 5:114-133.
59. Jordan D.B., Bacot K.O., Carlson T.J., Kessel M., Viitanen P.V. Plant riboflavin biosynthesis. Cloning, chloroplast localization, expression, purification, and partial characterization of spinach lumazine synthase. J Biol Chem 1999, 274:22114-22121.
60. Xiao S., Dai L., Liu F., Wang Z., Peng W., Xie D. COS1: an Arabidopsis coronatine insensitive1 suppressor essential for regulation of jasmonate-mediated plant defense and senescence. Plant Cell 2004, 16:1132-1142.
61. Book A.J., Yang P., Scalf M., Smith L.M., Vierstra R.D. Tripeptidyl peptidase II. An oligomeric protease complex from Arabidopsis. Plant Physiol 2005, 138:1046-1057.
62. Nikolau B.J., Ohlrogge J.B., Wurtele E.S. Plant biotin-containing carboxylases. Arch Biochem Biophys 2003, 414:211-222.
63. Bates P.W., Vierstra R.D. UPL1 and 2, two 405kDa ubiquitin-protein ligases from Arabidopsis thaliana related to the HECT-domain protein family. Plant J 1999, 20:183-195.
64. Kim D.Y., Kim K.K. Structure and function of HtrA family proteins, the key players in protein quality control. J Biochem Mol Biol 2005, 38:266-274.
65. Sze H., Ward J.M., Lai S. Vacuolar H(+)-translocating ATPases from plants: structure, function, and isoforms. J Bioenerg Biomembr 1992, 24:371-381.
66. Drobny M., Schnölzer M., Fiedler S., Lüttge U., Fischer-Schliebs E., Christian A.L., et al. Phenotypic subunit composition of the tobacco (Nicotiana tabacum L.) vacuolar-type H(+)-translocating ATPase. Biochim Biophys Acta 2002, 1564:243-255.
67. Domgall I., Venzke D., Lüttge U., Ratajczak R., Böttcher B. Three-dimensional map of a plant V-ATPase based on electron microscopy. J Biol Chem 2002, 277:13115-13121.
68. Williams R.C., Shah C., Sackett D. Separation of tubulin isoforms by isoelectric focusing in immobilized pH gradient gels. Anal Biochem 1999, 275:265-267.
69. Gardiner J., Marc J. Putative microtubule-associated proteins from the Arabidopsis genome. Protoplasma 2003, 222:61-74.
70. Chuong S.D., Good A.G., Taylor G.J., Freeman M.C., Moorhead G.B., Muench D.G. Large-scale identification of tubulin-binding proteins provides insight on subcellular trafficking, metabolic channeling, and signaling in plant cells. Mol Cell Proteomics 2004, 3:970-983.
71. Young J.C., Barral J.M., Ulrich Hartl F. More than folding: localized functions of cytosolic chaperones. Trends Biochem Sci 2003, 28:541-547.
72. Srere P.A. Complexes of sequential metabolic enzymes. Annu Rev Biochem 1987, 56:89-124.
73. Mooney B.P., Miernyk J.A., Randall D.D. The complex fate of alpha-ketoacids. Annu Rev Plant Biol 2002, 53:357-375.
74. Douce R., Bourguignon J., Neuburger M., Rébeillé F. The glycine decarboxylase system: a fascinating complex. Trends Plant Sci 2001, 6:167-176.
75. Wheeler M.C., Tronconi M.A., Drincovich M.F., Andreo C.S., Flügge U.I., Maurino V.G. A comprehensive analysis of the NADP-malic enzyme gene family of Arabidopsis. Plant Physiol 2005, 139:39-51.
76. Bykova N.V., Egsgaard H., Møller I.M. Identification of 14 new phosphoproteins involved in important plant mitochondrial processes. FEBS Lett 2003, 540:141-146.