Quantitative profiling of the membrane proteome in Halophilic archaeon

Molecular and Cellular Proteomics

Volumn 5, Issue 9, 2006, Pages 1543-1558

  Bisle, Birgit ^a   Schmidt, Alexander ^a   Scheibe, Burghardt ^b   Klein, Christian ^a   Tebbe, Andreas ^a   Kellermann, Joseph ^a   Siedler, Frank ^a   Pfeiffer, Friedhelm ^a   Lottspeich, Friedrich ^a   Oesterhelt, Dieter ^a  

^a MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^b BIACORE AB   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; BACTERIAL PROTEIN; BACTERIORHODOPSIN; CYSTEINE; ISOTOPE; LYSINE; MEMBRANE PROTEIN; PROTEOME;

AEROBIC METABOLISM; AMINO TERMINAL SEQUENCE; ANAEROBIC METABOLISM; ARTICLE; BACTERIAL GROWTH; CELL ENERGY; CONTROLLED STUDY; CORRELATION ANALYSIS; ENERGY METABOLISM; FUNCTIONAL PROTEOMICS; HALOBACTERIUM SALINARUM; ISOTOPE LABELING; MATHEMATICAL ANALYSIS; METABOLIC REGULATION; NONHUMAN; PHOTOTROPHIC BACTERIUM; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; QUANTITATIVE ANALYSIS; SEPARATION TECHNIQUE; TWO DIMENSIONAL ELECTROPHORESIS;

CELL MEMBRANE; CHROMATOGRAPHY, LIQUID; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; ELECTROPHORESIS, POLYACRYLAMIDE GEL; HALOBACTERIUM SALINARUM; ISOELECTRIC FOCUSING; MEMBRANE PROTEINS; PROTEOME; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

ARCHAEA; HALOBACTERIUM SALINARUM;

EID: 33749238059     PISSN: 15359476     EISSN: None     Source Type: Journal    
DOI: 10.1074/mcp.M600106-MCP200     Document Type: Article

References (74)

1. Wallin, E., and Von Heijne, G. (1998) Genome-wide analysis of integral membrane proteins from eubacterial, archaean, and eukaryotic organisms. Protein Sci. 7, 1029-1038
2. Stevens, T. J., and Arkin I. T. (2000) Do more complex organisms have a greater proportion of membrane proteins in their genomes? Proteins Struct. Funct. Genet. 39, 417-420
3. Klein, C., Garcia-Rizo, C., Bisle, B., Scheffer, B., Zischka, H., Pfeiffer, F., Siedler, F., and Oesterhelt, D. (2005) The membrane proteome of Halobacterium salinarum. Proteomics 5, 180-197
4. Santoni, V., Molloy, M., and Rabilloud, T. (2000) Membrane proteins and proteomics: un amour impossible? Electrophoresis 21, 1054-1070
5. Krogh, A., Larsson, B., Von Heijne, G., and Sonnhammer, E. L. L. (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J. Mol. Biol. 305, 567-580
6. Falb, M., Pfeiffer, F., Palm, P., Rodewald, K., Hickmann, V., Tittor, J., and Oesterhelt, D. (2005) Living with two extremes: conclusions from the genome sequence of Natronomonas pharaonis. Genome Res. 15, 1336-1343
7. Bunai, K., and Yamane, K. (2005) Effectiveness and limitation of two-dimensional gel electrophoresis in bacterial membrane protein proteomics and perspectives. J. Chromatogr. B Anal. Technol. Biomed. Life Sci. 815, 227-236
8. Twine, S. M., Mykytczuk, N. C. S., Petit, M., Tremblay, T. L., Conlan, J. W., and Kelly, J. F. (2005) Francisella tularensis proteome: low levels of ASB-14 facilitate the visualization of membrane proteins in total protein extracts. J. Proteome Res. 4, 1848-1854
9. Wehmhoner, D., Dieterich, G., Fischer, E., Baumgartner, M., Wehland, J., and Jansch, L. (2005) "LANESPECTOR", a tool for membrane proteome profiling based on sodium dodecyl sulfate-polyacrylamide gel electrophoresis/liquid chromatography-tandem mass spectrometry analysis: application to Listeria monocytogenes membrane proteins. Electrophoresis 26, 2450-2460
10. Schindler, J., Lewandrowski, U., Sickmann, A., Friauf, E., and Nothwang, H. G. (2006) Proteomic analysis of brain plasma membranes isolated by affinity two-phase partitioning. Mol. Cell. Proteomics 5, 390-400
11. Wu, C. C., MacCoss, M. J., Howell, K. E., and Yates, J. R. (2003) A method for the comprehensive proteomic analysis of membrane proteins. Nat. Biotechnol. 21, 532-538
12. Wu, C. C., and Yates, J. R. (2003) The application of mass spectrometry to membrane proteomics. Nat. Biotechnol. 21, 262-267
13. Nielsen, P. A., Olsen, J. V., Podtelejnikov, A. V., Andersen, J. R., Mann, M., and Wisniewski, J. R. (2005) Proteomic mapping of brain plasma membrane proteins. Mol. Cell. Proteomics 4, 402-408
14. Fischer, F., Wolters, D., Rogner, M., and Poetsch, A. (2006) Toward the complete membrane proteome: high coverage of integral membrane proteins through transmembrane peptide detection. Mol. Cell. Proteomics 5, 444-453
15. Unlu, M., Morgan, M. E., and Minden, J. S. (1997) Difference gel electrophoresis: a single gel method for detecting changes in protein extracts. Electrophoresis 18, 2071-2077
16. Tonge, R., Shaw, J., Middleton, B., Rowlinson, R., Rayner, S., Young, J., Pognan, F., Hawkins, E., Currie, I., and Davison, M. (2001) Validation and development of fluorescence two-dimensional differential gel electrophoresis proteomics technology. Proteomics 1, 377-396
17. Alban, A., David, S. O., Bjorkesten, L., Andersson, C., Sloge, E., Lewis, S., and Currie, I. (2003) A novel experimental design for comparative two-dimensional gel analysis: two-dimensional difference gel electrophoresis incorporating a pooled internal standard. Proteomics 3, 36-44
18. Marouga, R., David, S., and Hawkins, E. (2005) The development of the DIGE system: 2D fluorescence difference gel analysis technology. Anal. Bioanal. Chem. 382, 669-678
19. Perales, M., Eubel, H., Heinemeyer, J., Colaneri, A., Zabaleta, E., and Braun, H. P. (2005) Disruption of a nuclear gene encoding a mitochondrial γ carbonic anhydrase reduces complex I and supercomplex 1+1112 levels and alters mitochondrial physiology in Arabidopsis. J. Mol. Biol. 350, 263-277
20. Julka, S., and Regnier, F. (2004) Quantitation in proteomics through stable isotope coding: a review. J. Proteome Res. 3, 350-363
21. Ong, S. E., and Mann, M. (2005) Mass spectrometry-based proteomics turns quantitative. Nat. Chem. Biol. 1, 252-262
22. Ong, S.E., Blagoev, B., Kratchmarova, I., Kristensen, D. B., Steen, H., Pandey, A., and Mann, M. (2002) Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Mol. Cell. Proteomics 1, 376-386
23. Gygi, S. P., Rist, B., Gerber, S. A., Turecek, F., Gelb, M. H., and Aebersold, R. (1999) Quantitative analysis of complex protein mixtures using isotope-coded affinity tags. Nat. Biotechnol. 17, 994-999
24. Ross, P. L., Huang, Y. L. N., Marchese, J. N., 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., and Pappin, D. J. (2004) Multiplexed protein quantitation in Saccharomyces cerevisiae using amine-reactive isobaric tagging reagents. Mol. Cell. Proteomics 3, 1154-1169
25. Munchbach, M., Quadroni, M., Miotto, G., and James, P. (2000) Quantitation and facilitated de novo sequencing of proteins by isotopic N-terminal labeling of peptides with a fragmentation directing moiety. Anal. Chem. 72, 4047-4057
26. Yao, X. D., Freas, A., Ramirez, J., Demirev, P. A., and Fenselau, C. (2001) Proteolytic O-18 labeling for comparative proteomics: model studies with two serotypes of adenovirus. Anal. Chem. 73, 2836-2842
27. Schmidt, A., Kellermann, J., and Lottspeich, F. (2005) A novel strategy for quantitative proteomics using isotope-coded protein labels. Proteomics 5, 4-15
28. Han, D. K., Eng, J., Zhou, H. L., and Aebersold, R. (2001) Quantitative profiling of differentiation-induced microsomal proteins using isotope-coded affinity tags and mass spectrometry. Nat. Biotechnol. 19, 946-951
29. Olsen, J. V., Andersen, J. R., Nielsen, P. A., Nielsen, M. L., Figeys, D., Mann, M., and Wisniewski, J. R. (2004) HysTag - a novel proteomic quantitation tool applied to differential display analysis of membrane proteins from distinct areas of mouse brain. Mol. Cell. Proteomics 3, 82-92
30. Foster, L. J., de Hoog, C. L., and Mann, M. (2003) Unbiased quantitative proteomics of lipid rafts reveals high specificity for signaling factors. Proc. Natl. Acad. Sci. U. S. A. 100, 5813-5818
31. Scheurer, S. B., Roesli, C., Neri, D., and Elia, G. (2005) A comparison of different biotinylation reagents, tryptic digestion procedures, and mass spectrometric techniques for 2-D peptide mapping of membrane proteins. Proteomics 5, 3035-3039
32. Scheurer, S. B., Rybak, J. N., Roesli, C., Brunisholz, R. A., Potthast, F., Schlapbach, R., Neri, D., and Elia, G. (2005) Identification and relative quantitation of membrane proteins by surface biotinylation and two-dimensional peptide mapping. Proteomics 5, 2718-2728
33. Ramus, C., de Peredo, A. G., Dahout, C., Gallagher, M., and Garin, J. (2006) An optimized strategy for ICAT quantitation of membrane proteins. Mol. Cell. Proteomics 5, 68-78
34. Blonder, J., Hale, M. L., Chan, K. C., Yu, L. R., Lucas, D. A., Conrads, T. P., Zhou, M., Popoff, M. R., Issaq, H. J., Stiles, B. G., and Veenstra, T. D. (2005) Quantitative profiling of the detergent-resistant membrane proteome of lota-b toxin induced Vero cells. J. Proteome Res. 4, 523-531
35. Blonder, J., Yu, L. R., Radeva, G., Chan, K. C., Lucas, D. A., Waybright, T. J., Issaq, H. J., Sharom, F. J., and Veenstra, T. D. (2006) Combined chemical and enzymatic stable isotope labeling for quantitative profiling of detergent-insoluble membrane proteins isolated using Triton X-100 and Brij-96. J. Proteome Res. 5, 349-360
36. Tebbe, A., Klein, C., Bisle, B., Siedler, F., Scheffer, B., Garcia-Rizo, C., Wolfertz, J., Hickmann, V., Pfeiffer, F., and Oesterhelt, D. (2005) Analysis of the cytosolic proteome of Halobacterium salinarum and its implication for genome annotation. Proteomics 5, 168-179
37. Muller, J. A., and DasSarma, S. (2005) Genomic analysis of anaerobic respiration in the archaeon Halobacterium sp strain NRC-1: dimethyl sulfoxide and trimethylamine N-oxide as terminal electron acceptors, J. Bacteriol. 187, 1659-1667
38. Oren, A., and Truper, H. G. (1990) Anaerobic growth of halophilic Archae-bacteria by reduction of dimethylsulfoxide and trimethylamine N-oxide. FEMS Microbiol. Lett. 70, 33-36
39. Ruepp, A., Muller, H. N., Lottspeich, F., and Soppa, J. (1995) Catabolic ornithine transcarbamylase of Halobacterium halobium (salinarium): purification, characterization, sequence determination, and evolution. J. Bacteriol. 177, 1129-1136
40. Ruepp, A., and Soppa, J. (1996) Fermentative arginine degradation in Halobacterium salinarium (formerly Halobacterium halobium): genes, gene products, and transcripts of the arcRACB gene cluster. J. Bacteriol. 178, 4942-4947
41. Oesterhelt, D., and Krippahl, G. (1983) Phototropic growth of halobacteria and its use for isolation of photosynthetically-deficient mutants. Ann. Microbiol. B134, 137-150
42. Oesterhelt, D., and Stoeckenius, W. (1974) Isolation of the cell membrane of Halobacterium halobium and its fractionation into red and purple membrane. Methods Enzymol. 31, 667-678
43. Wessel, D., and Flugge, U. I. (1984) A method for the quantitative recovery of protein in dilute solution in the presence of detergents and lipids. Anal. Biochem. 138, 141-143
44. Macfarlane, D. E. (1983) Use of benzyldimethyl-n-hexadecylammonium chloride ("16-BAC"), a cationic detergent, in an acidic polyacrylamide-gel electrophoresis system to detect base labile protein methylation in intact cells. Anal. Biochem. 132, 231-235
45. Hartinger, J., Stenius, K., Hogemann, D., and Jahn, R. (1996) 16-BAC/ SDS-PAGE: a two-dimensional get electrophoresis system suitable for the separation of integral membrane proteins. Anal. Biochem. 240, 126-133
46. Perkins, D. N., Pappin, D.J.C., Creasy, D. M., and Cottrell, J. S. (1999) Probability-based protein identification by searching sequence data-bases using mass spectrometry data. Electrophoresis 20, 3551-3567
47. Koch, M. K., and Oesterhelt, D. (2005) MpcT is the transducer for membrane potential changes in Halobacterium salinarum. Mol. Microbiol. 55, 1681-1694
48. Moore, R. E., Young, M. K., and Lee, T. D. (2002) Qscore: an algorithm for evaluating SEQUEST database search results. J. Am. Soc. Mass Spectrom. 13, 378-386
49. Peng, J. M., Elias, J. E., Thoreen, C. C., Licklider, L. J., and Gygi, S. P. (2003) Evaluation of multidimensional chromatography coupled with tandem mass spectrometry (LC/LC-MS/MS) for large-scale protein analysis: the yeast proteome. J. Proteome Res. 2, 43-50
50. Baliga, N. S., Pan, M., Goo, Y. A., Yi, E. C., Goodlett, D. R., Dimitrov, K., Shannon, P., Aebersold, R., Ng, W. V., and Hood, L. (2002) Coordinate regulation of energy transduction modules in Halobacterium sp. analyzed by a global systems approach. Proc. Natl. Acad. Sci. U. S. A. 99, 14913-14918
51. Gropp, R., Gropp, F., and Betlach, M. C. (1992) Association of the halobacterial 7S RNA to the polysome correlates with expression of the membrane protein bacterioopsin. Proc. Natl. Acad. Sci. U. S. A. 89, 1204-1208
52. Zhang, R. J., and Regnier, F. E. (2002) Minimizing resolution of isotopically coded peptides in comparative proteomics. J. Proteome Res. 1, 139-147
53. Hixson, K. K., Rodriguez, N., Camp, D. G., Strittmatter, E. F., Lipton, M. S., and Smith, R. D. (2002) Evaluation of enzymatic digestion and liquid chromatography-mass spectrometry peptide mapping of the integral membrane protein bacteriorhodopsin. Electrophoresis 23, 3224-3232
54. Blonder, J., Conrads, T. P., Yu, L. R., Terunuma, A., Janini, G. M., Issaq, H. J., Vogel, J. C., and Veenstra, T. D. (2004) A detergent- and cyanogen bromide-free method for integral membrane proteomics: application to Halobacterium purple membranes and the human epidermal membrane proteome. Proteomics 4, 31-45
55. Yu, Y. Q., Gilar, M., and Gebler, J. C. (2004) A complete peptide mapping of membrane proteins: a novel surfactant aiding the enzymatic digestion of bacteriorhodopsin. Rapid Commun. Mass Spectrom. 18, 711-715
56. Hufnagel, P., Schweiger, U., Eckerskorn, C., and Oesterhelt, D. (1996) Electrospray ionization mass spectrometry of genetically and chemically modified bacteriorhodopsins. Anal. Biochem. 243, 46-54
57. Zhong, H. Y., Marcus, S. L., and Li, L. (2005) Microwave-assisted acid hydrolysis of proteins combined with liquid chromatography MALDI MS/MS for protein identification. J. Am. Soc. Mass Spectrom. 16, 471-481
58. Wolfer, U., Dencher, N. A., Buldt, G., and Wrede, P. (1988) Bacteriorhodopsin precursor is processed in two steps. Eur. J. Biochem. 174, 51-57
59. Kolkman, A., Dirksen, E. H. C., Slijper, M., and Heck, A. J. R. (2005) Double standards in quantitative proteomics: direct comparative assessment of difference in get electrophoresis and metabolic stable isotope labeling. Mol. Cell. Proteomics 4, 255-266
60. Tian, Q., Stepaniants, S. B., Mao, M., Weng, L., Feetham, M. C., Doyle, M. J., Yi, E. C., Dai, H. Y., Thorsson, V., Eng, J., Goodlett, D., Berger, J. P., Gunter, B., Linseley, P. S., Stoughton, R. B., Aebersold, R., Collins, S. J., Hanlon, W. A., and Hood, L. E. (2004) Integrated genomic and proteomic analyses of gene expression in mammalian cells. Mol. Cell. Proteomics 3, 960-969
61. Berendt, F. J., Frohlich, T., Schmidt, S. E. M., Reichenbach, H. D., Wolf, E., and Arnold, G. J. (2005) Holistic differential analysis of embryo-induced alterations in the proteome of bovine endometrium in the preattachment period. Proteomics 5, 2551-2560
62. Patton, W. F., Schulenberg, B., and Steinberg, T. H. (2002) Two-dimensional gel electrophoresis; better than a poke in the ICAT? Curr. Opin. Biotechnol. 13, 321-328
63. Shand, R. F., and Betlach, M. C. (1991) Expression of the Bop gene cluster of Halobacterium halobium is induced by low oxygen tension and by light. J. Bacteriol. 173, 4692-4699
64. Sumper, M., Reitmeier, W., and Oesterhelt, D. (1976) Biosynthesis of the purple membrane of halobacteria. Angew Chem. Int. Ed. Engl. 15, 187-194
65. Schryvers, A., and Weiner, J. H. (1981) The anaerobic sn-glycerol-3-phosphate dehydrogenase of Escherichia coli. Purification and characterization. J. Biol. Chem. 256, 9959-9965
66. Schryvers, A., Lohmeier, E., and Weiner, J. H. (1978) Chemical and functional properties of native and reconstituted forms of membrane-bound, aerobic glycerol-3-phosphate dehydrogenase of Escherichia coli. J. Biol. Chem. 253, 783-788
67. Cole, S.T., Eiglmeier, K., Ahmed, S., Honore, N., Elmes, L., Anderson, W. F., and Weiner, J. H. (1988) Nucleotide sequence and gene-polypeptide relationships of the glpABC operon encoding the anaerobic sn-glycerol-3-phosphate dehydrogenase of Escherichia cofi K-12. J. Bacteriol. 170, 2448-2456
68. Kaplan, S. (1978) Control and kinetics of photosynthetic membrane development, in The Photosynthetic Bacteria (Clayton, R. K., and Sistrom, W. R., eds) pp. 809-840, Plenum Press, New York
69. Subramaniam, S., and Henderson, R. (2000) Molecular mechanism of vectorial proton translocation by bacteriorhodopsin. Mature 406, 653-657
70. Kühlbrandt, W. (2000) Bacteriorhodopsin - the movie. Nature 406, 569-570
71. Hartmann, R., Sickinger, H. D., and Oesterhelt, D. (1980) Anaerobic growth of halobacteria. Proc. Natl. Acad. Sci. U. S. A. 77, 3821-3825
72. Oesterhelt, D., and Krippahl, G. (1973), Light inhibition of respiration in Halobacterium halobium. FEBS Lett. 36, 72-76
73. Oren, A. (1983) Bacteriorhodopsin-mediated CO2 photoassimilation in the Dead Sea. Limnol. Oceanogr. 28, 33-41
74. Ring, G., and Eichler, J. (2004) In the Archaea Haloferax volcanii, membrane protein biogenesis and protein synthesis rates are affected by decreased ribosomal binding to the translocon. J. Biol. Chem. 279, 53160-53166