Variation of the chemical reactivity of Thermus thermophilus HB8 ribosomal proteins as a function of pH

Proteomics

Volumn 10, Issue 20, 2010, Pages 3669-3687

  Running, William E ^a   Reilly, James P ^a  

^a INDIANA UNIVERSITY   (United States)

Author keywords

Bacterial ribosomes; Chemical labeling; MS; pH dependence; Protein chemistry; Technology

Indexed keywords

ASPARTIC ACID; BACTERIAL PROTEIN; GLUTAMIC ACID; LYSINE; RIBOSOMAL PROTEIN L1; RIBOSOME PROTEIN; RIBOSOME PROTEIN L10; RIBOSOME PROTEIN L11; RIBOSOME PROTEIN L12; RIBOSOME PROTEIN L13; RIBOSOME PROTEIN L14; RIBOSOME PROTEIN L15; RIBOSOME PROTEIN L16; RIBOSOME PROTEIN L17; RIBOSOME PROTEIN L18; RIBOSOME PROTEIN L19; RIBOSOME PROTEIN L2; RIBOSOME PROTEIN L20; RIBOSOME PROTEIN L21; RIBOSOME PROTEIN L22; RIBOSOME PROTEIN L23; RIBOSOME PROTEIN L24; RIBOSOME PROTEIN L3; RIBOSOME PROTEIN L4; RIBOSOME PROTEIN L5; RIBOSOME PROTEIN L6; RIBOSOME PROTEIN L7; RIBOSOME PROTEIN L9; RIBOSOME RNA; UNCLASSIFIED DRUG; UNINDEXED DRUG;

ARTICLE; CONFORMATIONAL TRANSITION; HYDROGEN BOND; ION CYCLOTRON RESONANCE MASS SPECTROMETRY; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN MODIFICATION; PROTEIN STRUCTURE; RIBOSOME; THERMUS THERMOPHILUS;

BACTERIAL PROTEINS; CRYSTALLOGRAPHY, X-RAY; HYDROGEN-ION CONCENTRATION; LYSINE; MASS SPECTROMETRY; MODELS, MOLECULAR; MOLECULAR STRUCTURE; PEPTIDES; PROTEIN STRUCTURE, TERTIARY; PROTEIN SUBUNITS; RIBOSOMAL PROTEINS; THERMUS THERMOPHILUS;

BACTERIA (MICROORGANISMS); THERMUS THERMOPHILUS;

EID: 78649410257     PISSN: 16159853     EISSN: 16159861     Source Type: Journal    
DOI: 10.1002/pmic.201000342     Document Type: Article

References (67)

1. Nelson, D. L., Cox, M. M., Lehninger Principles of Biochemistry, 3rd. ed., Worth Publishers, New York 2000.
2. Walsh, C. T., Antibiotics: Actions, Origins, Resistance, ASM Press, Washington, DC 2003.
3. Livermore, D. M., Bacterial resistance: origins, epidemiology, and impact. Clin. Infect. Dis. 2003, 36, S11-S23.
4. Ehrenberg, M., Structure and function of the ribosome. Scientific background on the Nobel prize in chemistry 2009. Accessed February 15, 2009 at http://nobelprize.org/nobel_prizes/chemistry/laureates/2009/sci.html.
5. Drenth, J., Principles of Protein X-ray Crystallography, Springer-Verlag, New York 1994.
6. Reed, D. G., Protein NMR Techniques, Methods in Molecular Biology v. 60, Humana Press, Totowa, NJ 1997.
7. Akashi, S., Sirouzu, M., Terada, T., Ito, Y., Yokoyama, S., Takio, K., Characterization of the structural difference between active and inactive forms of the Ras protein by chemical modification followed by mass spectrometric peptide mapping. Anal. Biochem. 1997, 248, 15-25.
8. Benjamin, D. R., Robinson, C. V., Hendrick, J. P., Hartl, F. U., Dobson, C. M., Mass spectrometry of ribosomes and ribosomal subunits. Proc. Natl. Acad. Sci. USA 1998, 95, 7391-7395.
9. Ilag, L. L., Videler, H., McKay, A. R., Sobott, F. et al., Heptameric (L12)6/L10 rather than canonical pentameric complexes are found by tandem MS of intact ribosomes from thermophilic bacteria. Proc. Natl. Acad. Sci. USA 2005, 102, 8192-8197.
10. Englander, S. W., Mayne, L., Sosnick, T. R., Hydrogen exchange: the modern legacy of Linderstrøm-Lang. Protein Sci. 1997, 6, 1101-1109.
11. Ehring, H., Hydrogen exchange/electrospray ionization mass spectrometry studies of structural features of proteins and protein/protein interactions. Anal. Biochem. 1999, 267, 252-259.
12. Smith, D. L., Deng, Y., Zhang, Z., Probing the non-covalent structure of proteins by amide hydrogen exchange and mass spectrometry. J. Mass Spectrom. 1997, 32, 135-146.
13. Neurath, H., in Jaenicke, R. (Ed.), Protein Folding, Elsevier, New York 1980, pp. 501-523.
14. Hubbard, S. J., The structural aspects of limited proteolysis of native proteins. Biochim. Biophys. Acta 1998, 1382, 191-206.
15. Suh, M.-J., Pourshahian, S., Limbach, P. A., Developing limited proteolysis and mass spectrometry for the characterization of ribosome topology. J. Am. Soc. Mass Spectrom. 2007, 18, 1304-1317.
16. Hamburg, D.-M., Suh, M.-J., Limbach, P. A., Limited proteolysis analysis of the ribosome is affected by subunit association. Biopolymers 2009, 91, 410-422.
17. Glocker, M. O., Borchers, C., Fiedler, W., Suckau, D., Przybylski, M., Molecular characterization of surface topology in protein tertiary structures by amino-acylation and mass spectrometric peptides mapping. Bioconjugate Chem. 1994, 5, 583-590.
18. Glocker, M. O., Nock, S., Sprinzl, M., Przybylski, M., Characterization of surface topology and binding area in complexes of the elongation factor proteins EF-Ts and EFTu-GDP from Thermus thermophilus: a study by protein chemical modification and mass spectrometry. Chem. Eur. J. 1998, 4, 707-715.
19. Fiedler, W., Borchers, C., Macht, M., Deininger, S.-O., Przybylski, M., Molecular characterization of a conformational epitope of hen egg white lysozyme by differential chemical modification of immune complexes and mass spectrometric peptide mapping. Bioconjugate Chem. 1998, 9, 236-241.
20. Mendoza, V. L., Vachet, R. M., Protein surface mapping using diethylpyrocarbonate with mass spectrometric detection. Anal. Chem. 2008, 80, 2895-2904.
21. Guan, J.-Q., Chance, M. R., Structural proteomics of macromolecular assemblies using oxidative footprinting and mass spectromtery. Trends Biochem. Sci. 2005, 30, 583-592.
22. Sharp, J. S., Becker, J. M., Hettich, R. L., Analysis of protein solvent accessible surfaces by photochemical oxidation and mass spectromtery. Anal. Chem. 2004, 76, 672-683.
23. Hambly, D. M., Gross, M. L., Laser flash photolysis of hydrogen peroxide to oxidize protein solvent-accessible residues on the microsecond timescale. J. Am. Soc. Mass Spectrom. 2005, 16, 2057-2063.
24. Tong, X., Wren, J. C., Konermann, L., Effects of protein concentration on the extent of γ-ray-mediated oxidative labeling studied by electrospray mass spectrometry. Anal. Chem. 2007, 79, 6376-6382.
25. Lundblad, R. L., Chemical Reagents for Protein Modification, 3rd Edn, CRC Press, Boca Raton, FL 2005.
26. Janecki, D. J., Beardsley, R. L., Reilly, J. P., Probing protein tertiary structure with amidination. Anal. Chem. 2005, 77, 7274-7281.
27. Liu, X., Broshears, W. C., Reilly, J. P., Probing the structure and activity of trypsin with amidination. Anal. Biochem. 2007, 367, 13-19.
28. Beardsley, R. L., Running, W. E., Reilly, J. P., Probing the structure of the Caulobacter crescentus ribosome with chemical labeling and mass spectrometry. J. Proteome Res. 2006, 5, 2935-2946.
29. Liu, X., Reilly, J. P., Correlating the chemical modification of Escherichia coli ribosomal proteins with crystal structure data. J. Proteome Res. 2009, 8, 4466-4478.
30. Running, W. E., Reilly, J. P., Ribosomal proteins of Deinococcus radiodurans: their solvent acessibility and reactivity. J. Proteome Res. 2009, 8, 1228-1246.
31. Lauber, M. A., Running, W. E., Reilly, J. P., B. subtilis ribosomal proteins: structural homology and post-translational modifications. J. Proteome Res. 2009, 8, 4193-4206.
32. Selmer, M., Dunham, C. M., Murphy IV, F. V., Weixlbaumer, A. et al., Structure of the 70S ribosome complexed with mRNA and tRNA. Science 2006, 313, 1935-1942.
33. Wimberly, B. T., Brodersen, D. E., Clemons, W. M. Jr., Morgan-Warren, R. J. et al., Structure of the 30S ribosomal subunit. Nature 2000, 407, 327-339.
34. Ogle, J. M., Brodersen, D. E., Clemons, W. M. Jr., Tarry, M. J. et al., Recognition of cognate Transfer RNA by the 30S ribosomal subunit. Science 2001, 292, 897-902.
35. Ogle, J. M., Murphy IV, F. V., Tarry, M. J., Ramakrishnan, V., Selection of tRNA by the ribosome requires a transition from an open to a closed form. Cell 2002, 111, 721-732.
36. Blaha, G., Stanley, R. E., Steitz, T. A., Formation of the first peptide bond: the structure of EF-P bound to the 70S ribosome. Science 2009, 325, 966-970.
37. Thumm, M., Hoenes, J., Pfleiderer, G., S-Methylthioacetimidate is a new reagent for the amidination of proteins at low pH. Biochim. Biophys. Acta 1987, 923, 263-267.
38. Beardsley, R. L., Reilly, J. P., Quantitation using enhanced signal tags: a technique for comparative proteomics. J. Proteome Res. 2003, 2, 15-21.
39. Reynolds, J. H., Acetimidation of bovine pancreatic ribonuclease A. Biochemistry 1968, 7, 3131-3135.
40. Fazili, K. M., Mir, M. M., Qasim, M. A., Changes in chemical stability upon chemical modification of lysine residues in bovine serum albumin by different reagents. Biochem. Mol. Biol. Int. 1993, 31, 807-816.
41. Spedding, G., in Rickwood, D., Hames, B. D. (Eds.). Ribosomes and Protein Synthesis: A Practical Approach, Oxford Press, New York 1990, pp. 1-29.
42. Read, S. M., Northcote, D. H., Minimization of variation in response to different proteins of the coomassie blue G dye-binding assay for proteins. Anal. Biochem. 1981, 116, 53-64.
43. Hardy, S. J. S., Kurland, C. G., Voynow, P., More, G., Ribosomal proteins of E. coli. I purification of the 30S ribosomal proteins. Biochemistry 1969, 8, 2897-2905.
44. Barritault, D., Expert-Bezancon, A., Guerin, M. F., Hayes, D., The use of acetone precipitation in the isolation of ribosomal proteins. Eur. J. Biochem. 1976, 63, 131-135.
45. Karty, J. A., Running, W. E., Reilly, J. P., Two-dimensional liquid phase separations of proteins using online fractionation and concentration between chromatographic dimensions. J. Chromatogr. B 2007, 847, 103-113.
46. Wang, L.-C., Okitsu, C. Y., Kochounian, H., Rodriguez, A. et al., A simple and inexpensive on-column frit fabrication method for fused silica capillaries for increased capacity and versatility in LC-MS/MS applications. Proteomics 2008, 8, 1758-1761.
47. Mann, B., Madera, M., Sheng, Q., Tang, H. et al., Protein-Quant Suite: a bundle of automated software tools for label-free quantitative proteomics. Rapid Commun. Mass Spectrom. 2008, 22, 3823-3834.
48. Suh, M.-J., Hamburg, D.-M., Gregory, S. T., Dahlberg, A. E., Limbach, P. A., Extending ribosomal protein identifications to unsequenced bacterial strains using matrix assisted laser desorption/ionization mass spectrometry. Proteomics 2005, 5, 4818-4831.
49. Subramanian, A.-R., Structure and functions of ribosomal protein S1. Prog. Nucl. Acids Res. Mol. Biol. 1983, 28, 101-142.
50. Ramakrishnan, V., White, S. W., Ribosomal protein structures: insights into the architecture, machinery and evolution of the ribosome. Trends Biochem. Sci. 1998, 23, 208-212.
51. McLafferty, F. W., High-resolution tandem FT mass spectrometry above 10 kDa. Acc. Chem. Res. 1994, 27, 379-386.
52. Horn, D. M., Zubarev, R. A., McLafferty, F. W., Automated reduction and interpretation of high resolution electrospray mass spectra of large molecules. J. Am. Soc. Mass Spectrom. 2000, 11, 320-332.
53. Zabrouskov, V., Senko, M. W., Du, Y., Leduc, R. D., Kelleher, N. L., New and automated MSn approaches for top-down identification of modified proteins. J. Am. Soc. Mass Spectrom. 2005, 16, 2027-2038.
54. Diaconu, M., Kothe, U., Schl. unzen, F. et al., Structural basis for the function of the ribosomal L7/L12 stalk in factor binding and GTPase activation. Cell 2005, 121, 991-1004.
55. Creighton, T. E., Proteins: Structures and Molecular Properties, 2nd Edn, W. H. Freeman, New York 1993.
56. Kowalak, J. A., Walsh, K. A., β-Methylthioaspartic acid: identification of a novel posttranslational modification in ribosomal protein S12 from Escherichia coli. Protein Sci. 1996, 5, 1625-1632.
57. Miller, J. H., GUG and UUG are initiation codons in vivo, Cell 1974, 1, 73-76.
58. Frottin, F., Martinez, A., Peynott, P., Mitra, S. et al., The proteomics of N-terminal methionine cleavage. Mol. Cell. Proteomics 2006, 5, 2336-2349.
59. Muranova, T. A., Muranov, A. V., Markova, L. F., Ovchinnikov, Y. A., The primary structure of ribosomal protein L3 from Escherichia coli 70S ribosomes. FEBS Lett. 1978, 96, 301-305.
60. Diedrich, G., Burkhardt, N., Nierhaus, K. H., Large scale isolation of proteins of the large subunit from Escherichia coli ribosomes. Protein Exp. Purif. 1997, 10, 42-50.
61. Strader, M. B., VerBerkmoes, N. C., Tabb, D. L., Connelly, H. M. et al., Characterization of the 70S ribosome from Rhodopseudomonas palustris using an integrated "Top Down" and "Bottom Up" mass spectrometric approach. J. Proteome Res. 2004, 3, 965-978.
62. Vanet, A., Plumbridge, J. A., Guerin, M.-F., Alix, J.-H., Ribosomal protein methylation in Escherichia coli: the gene prmA, encoding the ribosomal protein L11 methylase, is dispensable. Mol. Microbiol. 1994, 14, 947-958.
63. Cameron, D. M., Gregory, S. T., Thompson, J., Suh, M.-J. et al., Thermus thermophilus L11 methyltransferase, prmA, is dispensable for growth and preferentially modifies free ribosomal protein L11 prior to ribosome assembly. J. Bacteriol. 2004, 186, 5819-5825.
64. Forsyth, W. R., Antosiewicz, J. M., Robertson, A. D., Empirical relationships between protein structure and carboxyl pKa values in proteins. Proteins 2002, 48, 388-403.
65. Grimsley, G. R., Scholtz, J. M., Pace, C. N., A summary of the measured pK values of the ionizable groups in folded proteins. Protein Sci. 2009, 18, 247-251.
66. Qin, B. Y., Bewley, M. C., Creamer, L. K., Baker, H. M. et al., Structural basis of the tanford transition of bovine β-lactoglobulin. Biochemistry 1998, 37, 14014-14023.
67. Pankavic, S., Miao, Y., Ortoleva, J., Shreif, Z., Ortoleva, P., Stochastic dynamics of bionanosystems: multiscale analysis and specialized ensembles. J. Chem. Phys. 2008, 128, 234908-1-234908-13.