Protein abundance profiling of the Escherichia coli cytosol

BMC Genomics

Volumn 9, Issue , 2008, Pages

  Ishihama, Yasushi ^a,b   Schmidt, Thorsten ^c   Rappsilber, Juri ^b,f   Mann, Matthias ^b,d   Harlt, F Ulrich ^d   Kerner, Michael J ^e   Frishman, Dmitrij ^c,g  

^a KEIO UNIVERSITY   (Japan)

^b UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^c TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^d MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^e TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

^f UNIVERSITY OF EDINBURGH   (United Kingdom)

^g INSTITUTE OF EPIDEMIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; ESCHERICHIA COLI PROTEIN; MESSENGER RNA; RIBOSOME PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; BACTERIAL CELL; BACTERIAL STRAIN; CELL COUNT; CONTROLLED STUDY; CORRELATION ANALYSIS; CYTOSOLIC FRACTION; ENERGY METABOLISM; ESCHERICHIA COLI; GENE EXPRESSION PROFILING; HYDROPHOBICITY; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; NONHUMAN; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN METABOLISM; PROTEIN SYNTHESIS; PROTEIN TRANSPORT; CYTOSOL; METABOLISM; METHODOLOGY; PROTEOMICS;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

CHROMATOGRAPHY, LIQUID; CYTOSOL; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MASS SPECTROMETRY; PROTEOMICS;

EID: 42049108914     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-9-102     Document Type: Article

References (71)

1. Ghaemmaghami S Huh WK Bower K Howson RW Belle A Dephoure N O'Shea EK Weissman JS Global analysis of protein expression in yeast Nature 2003, 425(6959):737-741. 10.1038/nature02046 14562106
2. Newman JR Ghaemmaghami S Ihmels J Breslow DK Noble M DeRisi JL Weissman JS Single-cell proteomic analysis of S. cerevisiae reveals the architecture of biological noise Nature 2006, 441(7095):840-846. 10.1038/ nature04785 16699522
3. Link AJ Eng J Schieltz DM Carmack E Mize GJ Morris DR Garvik BM Yates JR 3rd Direct analysis of protein complexes using mass spectrometry Nature Biotechnology 1999, 17(7):676-682. 10.1038/10890 10404161
4. Peng J Elias JE Thoreen CC Licklider LJ Gygi SP Evaluation of multidimensional chromatography coupled with tandem mass spectrometry (LC/LC-MS/MS) for large-scale protein analysis: The yeast proteome Journal of Proteome Research 2003, 2(1):43-50. 10.1021/pr025556v 12643542
5. Gygi SP Rist B Gerber SA Turecek F Gelb MH Aebersold R Quantitative analysis of complex protein mixtures using isotope-coded affinity tags Nat Biotechnol 1999, 17(10):994-999. 10.1038/13690 10504701
6. Oda Y Huang K Cross FR Cowburn D Chait BT Accurate quantitation of protein expression and site-specific phosphorylation Proc Natl Acad Sci USA 1999, 96(12):6591-6596. 21959 10359756 10.1073/pnas.96.12.6591
7. Mirgorodskaya OA Kozmin YP Titov MI Korner R Sonksen CP Roepstorff P Quantitation of peptides and proteins by matrix-assisted laser desorption/ionization mass spectrometry using (18)O-labeled internal standards Rapid Commun Mass Spectrom 2000, 14(14):1226-1232. 10.1002/ 1097-0231(20000730)14:14<1226::AID-RCM14>3.0.CO;2-V 10918372
8. Hansen KC Schmitt-Ulms G Chalkley RJ Hirsch J Baldwin MA Burlingame AL Mass spectrometric analysis of protein mixtures at low levels using cleavable 13C-isotope-coded affinity tag and multidimensional chromatography Mol Cell Proteomics 2003, 2(5):299-314. 12766231
9. Ross PL Huang YN Marchese JN Williamson B Parker K Hattan S Khainovski N Pillai S Dey S Daniels S Purkayastha S Juhasz P Martin S Bartlet-Jones M He F Jacobson A Pappin DJ Multiplexed protein quantitation in Saccharomyces cerevisiae using amine-reactive isobaric tagging reagents Molecular & Cellular Proteomics 2004, 3(12):1154-1169. 10.1074/ mcp.M400129-MCP200
10. Ong SE Blagoev B Kratchmarova I Kristensen DB Steen H Pandey A Mann M Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics Mol Cell Proteomics 2002, 1(5):376-386. 10.1074/mcp.M200025-MCP200 12118079
11. Barr JR Maggio VL Patterson DG Jr Cooper GR Henderson LO Turner WE Smith SJ Hannon WH Needham LL Sampson EJ Isotope dilution - mass spectrometric quantification of specific proteins: Model application with apolipoprotein A-I Clinical chemistry 1996, 42(10):1676-1682. 8855153
12. Gerber SA Rush J Stemman O Kirschner MW Gygi SP Absolute quantification of proteins and phosphoproteins from cell lysates by tandem MS Proc Natl Acad Sci U S A 2003, 100(12):6940-6945. 165809 12771378 10.1073/ pnas.0832254100
13. Rappsilber J Ishihama Y Foster LJ Mittler G Mann M Approximate relative abundance of proteins within a mixture determined from LC-MS data Abstracts of the 51st American Society for Mass Spectrometry Conference in Mass Spectrometry and Allied Topics,: June 8-12 2003; Santa Fe, NM, Montreal, Canada American Society for Mass Spectrometry 2003.
14. Forner F Foster LJ Campanaro S Valle G Mann M Quantitative proteomic comparison of rat mitochondria from muscle, heart, and liver Mol Cell Proteomics 2006, 5(4):608-619. 16415296
15. Silva JC Gorenstein MV Li GZ Vissers JP Geromanos SJ Absolute quantification of proteins by LCMSE: A virtue of parallel MS acquisition Mol Cell Proteomics 2006, 5(1):144-156. 16219938
16. Rappsilber J Ryder U Lamond AI Mann M Large-scale proteomic analysis of the human spliceosome Genome Res 2002, 12(8):1231-1245. 186633 12176931 10.1101/gr.473902
17. Sanders SL Jennings J Canutescu A Link AJ Weil PA Proteomics of the eukaryotic transcription machinery: Identification of proteins associated with components of yeast TFIID by multidimensional mass spectrometry Mol Cell Biol 2002, 22(13):4723-4738. 133885 12052880 10.1128/MCB.22.13.4723-4738.2002
18. Ishihama Y Oda Y Tabata T Sato T Nagasu T Rappsilber J Mann M Exponentially modified protein abundance index (emPAI) for estimation of absolute protein amount in proteomics by the number of sequenced peptides per protein Mol Cell Proteomics 2005, 4(9):1265-1272. 10.1074/ mcp.M500061-MCP200 15958392
19. Zybailov B Mosley AL Sardiu ME Coleman MK Florens L Washburn MP Statistical analysis of membrane proteome expression changes in Saccharomyces cerevisiae J Proteome Res 2006, 5(9):2339-2347. 10.1021/ pr060161n 16944946
20. de Godoy LM Olsen JV de Souza GA Li G Mortensen P Mann M Status of complete proteome analysis by mass spectrometry: SILAC labeled yeast as a model system Genome Biol 2006, 7(6):R50. 1779535 16784548 10.1186/ gb-2006-7-6-r50
21. Lipton MS Pasa-Tolic L Anderson GA Anderson DJ Auberry DL Battista JR Daly MJ Fredrickson J Hixson KK Kostandarithes H Masselon C Markillie LM Moore RJ Romine MF Shen Y Stritmatter E Tolic N Udseth HR Venkateswaran A Wong KK Zhao R Smith RD Global analysis of the Deinococcus radiodurans proteome by using accurate mass tags Proceedings of the National Academy of Sciences of the United States of America 2002, 99(17):11049-11054. 129300 12177431 10.1073/pnas.172170199
22. Blattner FR Plunkett G 3rd Bloch CA Perna NT Burland V Riley M Collado-Vides J Glasner JD Rode CK Mayhew GF Gregor J Davis NW Kirkpatrick HA Goeden MA Rose DJ Mau B Shao Y The complete genome sequence of Escherichia coli K-12 Science 1997, 277(5331):1453-1474. 10.1126/science.277.5331.1453 9278503
23. Keseler IM Collado-Vides J Gama-Castro S Ingraham J Paley S Paulsen IT Peralta-Gil M Karp PD EcoCyc: A comprehensive database resource for Escherichia coli Nucleic Acids Res 2005, 33 Database:D334-337. 540062 15608210
24. Misra RV Horler RS Reindl W Goryanin II Thomas GH EchoBASE: An integrated post-genomic database for Escherichia coli Nucleic Acids Res 2005, 33 Database:D329-333. 539982 15608209
25. VanBogelen RA Abshire KZ Moldover B Olson ER Neidhardt FC Escherichia coli proteome analysis using the gene-protein database Electrophoresis 1997, 18(8):1243-1251. 10.1002/elps.1150180805 9298644
26. Link AJ Robison K Church GM Comparing the predicted and observed properties of proteins encoded in the genome of Escherichia coli K-12 Electrophoresis 1997, 18(8):1259-1313. 10.1002/elps.1150180807 9298646
27. Gevaert K Van Damme J Goethals M Thomas GR Hoorelbeke B Demol H Martens L Puype M Staes A Vandekerckhove J Chromatographic isolation of methionine-containing peptides for gel-free proteome analysis: identification of more than 800 Escherichia coli proteins Molecular & Cellular Proteomics 2002, 1(11):896-903. 10.1074/mcp.M200061-MCP200
28. Corbin RW Paliy O Yang F Shabanowitz J Platt M Lyons CE Jr Root K McAuliffe J Jordan MI Kustu S Soupene E Hunt DF Toward a protein profile of Escherichia coli: Comparison to its transcription profile Proceedings of the National Academy of Sciences of the United States of America 2003, 100(16):9232-9237. 170901 12878731 10.1073/pnas.1533294100
29. Taoka M Yamauchi Y Shinkawa T Kaji H Motohashi W Nakayama H Takahashi N Isobe T Only a small subset of the horizontally transferred chromosomal genes in Escherichia coli are translated into proteins Mol Cell Proteomics 2004, 3(8):780-787. 10.1074/mcp.M400030-MCP200 15115803
30. Wu CC Yates JR 3rd The application of mass spectrometry to membrane proteomics Nat Biotechnol 2003, 21(3):262-267. 10.1038/nbt0303-262 12610573
31. Pedersen S Bloch PL Reeh S Neidhardt FC Patterns of protein synthesis in E. coli: A catalog of the amount of 140 individual proteins at different growth rates Cell 1978, 14(1):179-190. 10.1016/0092-8674(78)90312-4 352533
32. Howe JG Hershey JW Initiation factor and ribosome levels are coordinately controlled in Escherichia coli growing at different rates J Biol Chem 1983, 258(3):1954-1959. 6337147
33. Ishii N Nakahigashi K Baba T Robert M Soga T Kanai A Hirasawa T Naba M Hirai K Hoque A Ho PY Kakazu Y Sugawara K Igarashi S Harada S Masuda T Sugiyama N Togashi T Hasegawa M Takai Y Yugi K Arakawa K Iwata N Toya Y Nakayama Y Nishioka T Shimizu K Mori H Tomita M Multiple high-throughput analyses monitor the response of E. coli to perturbations Science 2007, 316(5824):593-597. 10.1126/science.1132067 17379776
34. Lopez-Campistrous A Semchuk P Burke L Palmer-Stone T Brokx SJ Broderick G Bottorff D Bolch S Weiner JH Ellison MJ Localization, annotation, and comparison of the Escherichia coli K-12 proteome under two states of growth Mol Cell Proteomics 2005, 4(8):1205-1209. 10.1074/ mcp.D500006-MCP200 15911532
35. Rey S Acab M Gardy JL Laird MR deFays K Lambert C Brinkman FS PSORTdb: A protein subcellular localization database for bacteria Nucleic Acids Res 2005, 33 Database:D164-168. 539981 15608169
36. Gardy JL Laird MR Chen F Rey S Walsh CJ Ester M Brinkman FS PSORTb v.2.0: Expanded prediction of bacterial protein subcellular localization and insights gained from comparative proteome analysis Bioinformatics 2005, 21(5):617-623. 10.1093/bioinformatics/bti057 15501914
37. Errington J Daniel RA Scheffers DJ Cytokinesis in bacteria Microbiol Mol Biol Rev 2003, 67(1):52-65. 150516 12626683 10.1128/MMBR.67.1.52-65.2003
38. van Heeswijk WC Rabenberg M Westerhoff HV Kahn D The genes of the glutamine synthetase adenylylation cascade are not regulated by nitrogen in Escherichia coli Mol Microbiol 1993, 9(3):443-457. 10.1111/ j.1365-2958.1993.tb01706.x 8412694
39. Greenbaum D Jansen R Gerstein M Analysis of mRNA expression and protein abundance data: An approach for the comparison of the enrichment of features in the cellular population of proteins and transcripts Bioinformatics 2002, 18(4):585-596. 10.1093/bioinformatics/18.4.585 12016056
40. Karlin S Mrazek J Campbell A Kaiser D Characterizations of highly expressed genes of four fast-growing bacteria J Bacteriol 2001, 183(17):5025-5040. 95378 11489855 10.1128/JB.183.17.5025-5040.2001
41. Andreeva A Howorth D Brenner SE Hubbard TJ Chothia C Murzin AG SCOP database in 2004: Refinements integrate structure and sequence family data Nucleic Acids Res 2004, 32 Database:D226-229. 308773 14681400 10.1093/nar/gkh039
42. Gerstein M Levitt M A structural census of the current population of protein sequences PNAS 1997, 94(22):11911-11916. 23653 9342336 10.1073/ pnas.94.22.11911
43. Chiti F Stefani M Taddei N Ramponi G Dobson CM Rationalization of the effects of mutations on peptide and protein aggregation rates Nature 2003, 424(6950):805-808. 10.1038/nature01891 12917692
44. DuBay KF Pawar AP Chiti F Zurdo J Dobson CM Vendruscolo M Prediction of the absolute aggregation rates of amyloidogenic polypeptide chains J Mol Biol 2004, 341(5):1317-1326. 10.1016/j.jmb.2004.06.043 15302561
45. Calamai M Taddei N Stefani M Ramponi G Chiti F Relative influence of hydrophobicity and net charge in the aggregation of two homologous proteins Biochemistry 2003, 42(51):15078-15083. 10.1021/bi030135s 14690417
46. Cai CZ Han LY Ji ZL Chen X Chen YZ SVM-Prot: Web-based support vector machine software for functional classification of a protein from its primary sequence Nucleic Acids Res 2003, 31(13):3692-3697. 169006 12824396 10.1093/nar/gkg600
47. Gerdes SY Scholle MD Campbell JW Balazsi G Ravasz E Daugherty MD Somera AL Kyrpides NC Anderson I Gelfand MS Bhattacharya A Kapatral V D'Souza M Baev MV Grechkin Y Mseeh F Fonstein MY Overbeek R Barabasi AL Oltvai ZN Osterman AL Experimental determination and system level analysis of essential genes in Escherichia coli MG1655 Journal of Bacteriology 2003, 185(19):5673-5684. 193955 13129938 10.1128/JB.185.19.5673-5684.2003
48. Coghlan A Wolfe KH Relationship of codon bias to mRNA concentration and protein length in Saccharomyces cerevisiae Yeast 2000, 16(12):1131-1145. 10.1002/1097-0061(20000915)16:12<1131::AID-YEA609>3.0.CO;2-F 10953085
49. Jansen R Gerstein M Analysis of the yeast transcriptome with structural and functional categories: Characterizing highly expressed proteins Nucleic Acids Res 2000, 28(6):1481-1488. 111042 10684945 10.1093/nar/ 28.6.1481
50. Gygi SP Rochon Y Franza BR Aebersold R Correlation between protein and mRNA abundance in yeast Mol Cell Biol 1999, 19(3):1720-1730. 83965 10022859
51. Beyer A Hollunder J Nasheuer HP Wilhelm T Post-transcriptional expression regulation in the yeast Saccharomyces cerevisiae on a genomic scale Mol Cell Proteomics 2004, 3(11):1083-1092. 10.1074/ mcp.M400099-MCP200 15326222
52. Sharp PM Li WH The Codon Adaptation Index - a measure of directional synonymous codon usage bias, and its potential applications Nucleic Acids Res 1987, 15(3):1281-1295. 340524 3547335 10.1093/nar/15.3.1281
53. Jansen R Bussemaker HJ Gerstein M Revisiting the codon adaptation index from a whole-genome perspective: Analyzing the relationship between gene expression and codon occurrence in yeast using a variety of models Nucleic Acids Res 2003, 31(8):2242-2251. 153734 12682375 10.1093/nar/ gkg306
54. Futcher B Latter GI Monardo P McLaughlin CS Garrels JI A sampling of the yeast proteome Mol Cell Biol 1999, 19(11):7357-7368. 84729 10523624
55. Kerner MJ Naylor DJ Ishihama Y Maier T Chang HC Stines AP Georgopoulos C Frishman D Hayer-Hartl M Mann M Hartl FU Proteome-wide analysis of chaperonin-dependent protein folding in Escherichia coli Cell 2005, 122(2):209-220. 10.1016/j.cell.2005.05.028 16051146
56. Meek JL Prediction of peptide retention times in high-pressure liquid chromatography on the basis of amino acid composition Proc Natl Acad Sci USA 1980, 77(3):1632-1636. 348551 6929513 10.1073/pnas.77.3.1632
57. Sakamoto Y Kawakami N Sasagawa T Prediction of peptide retention times J Chromatogr 1988, 442:69-79. 10.1016/S0021-9673(00)94457-1 3417835
58. Boeckmann B Bairoch A Apweiler R Blatter MC Estreicher A Gasteiger E Martin MJ Michoud K O'Donovan C Phan I Pilbout S Schneider M The SWISS-PROT protein knowledgebase and its supplement TrEMBL in 2003 Nucleic Acids Research 2003, 31(1):365-370. 165542 12520024 10.1093/nar/ gkg095
59. Altschul SF Madden TL Schaffer AA Zhang J Zhang Z Miller W Lipman DJ Gapped BLAST and PSI-BLAST: A new generation of protein database search programs Nucleic Acids Res 1997, 25(17):3389-3402. 146917 9254694 10.1093/nar/25.17.3389
60. Ruepp A Zollner A Maier D Albermann K Hani J Mokrejs M Tetko I Guldener U Mannhaupt G Munsterkotter M Mewes HW The FunCat, a functional annotation scheme for systematic classification of proteins from whole genomes Nucleic Acids Research 2004, 32(18):5539-5545. 524302 15486203 10.1093/nar/gkh894
61. Krogh A Larsson B von Heijne G Sonnhammer EL Predicting transmembrane protein topology with a hidden Markov model: Application to complete genomes J Mol Biol 2001, 305(3):567-580. 10.1006/jmbi.2000.4315 11152613
62. Hartigan JA Clustering Algorithms New York: Wiley 1975
63. Witten IH Frank E Data Mining: Practical machine learning tools and techniques San Fransisco: Morgan Kaufmann 2 2005.
64. Schmidt T Frishman D PROMPT: A protein mapping and comparison tool BMC Bioinformatics 2006, 7:331. 1569443 16817977 10.1186/1471-2105-7-331
65. Huerta AM Salgado H Thieffry D Collado-Vides J RegulonDB: A database on transcriptional regulation in Escherichia coli Nucleic Acids Res 1998, 26(1):55-59. 147189 9399800 10.1093/nar/26.1.55
66. Linding R Russell RB Neduva V Gibson TJ GlobPlot: Exploring protein sequences for globularity and disorder Nucleic Acids Res 2003, 31(13):3701-3708. 169197 12824398 10.1093/nar/gkg519
67. Wright PE Dyson HJ Intrinsically unstructured proteins: Re-assessing the protein structure-function paradigm J Mol Biol 1999, 293(2):321-331. 10.1006/jmbi.1999.3110 10550212
68. Tompa P Intrinsically unstructured proteins Trends Biochem Sci 2002, 27(10):527-533. 10.1016/S0968-0004(02)02169-2 12368089
69. Wong P Fritz A Frishman D Designability, aggregation propensity and duplication of disease-associated proteins Protein Eng Des Sel 2005, 18(10):503-508. 10.1093/protein/gzi056 16155116
70. Kyte J Doolittle RF A simple method for displaying the hydropathic character of a protein J Mol Biol 1982, 157(1):105-132. 10.1016/ 0022-2836(82)90515-0 7108955
71. Lopez-Campistrous A Semchuk P Burke L Palmer-Stone T Brokx SJ Broderick G Bottorff D Bolch S Weiner JH Ellison MJ Localization, annotation, and comparison of the Escherichia coli K-12 proteome under two states of growth Molecular & Cellular Proteomics 2005, 4(8):1205-1209. 10.1074/ mcp.D500006-MCP200