Advertisement

N-Methylmethionine at the Amino Terminus of a Protein Required for Bacterial Chemotaxis

  • Ann Stock
Part of the Advances in Experimental Medicine and Biology book series (NATO ASI F, volume 231)

Abstract

The methylation of glutamate residues during Chemotaxis has been extensively investigated in Escherichia coli and Salmonella typhimurium (see Stock and Simms, this volume). This reaction is thought to function to modulate the activities of receptor proteins located in the cytoplasmic membrane. Levels of glutamate methylation are controlled by the activities of specific enzymes: the CheR methyltransferase adds groups and the CheB methylesterase removes them. Although reversible methylation at glutamates provides an important adaptive function in chemosensing, it is not essential for Chemotaxis, and mutants completely deficient in both the CheR and CheB enzymes retain an ability to migrate towards favorable environmental conditions. Genetic studies indicate that four cytoplasmic proteins are essential for Chemotaxis, CheA, CheW, CheY, and CheZ (Table 1). These appear to provide a link between chemoreceptors in the membrane and the flagellar motor. One of these components, the CheZ protein, is methylated at its amino terminus (Stock et al., 1987c). Both in terms of its function and chemistry, CheZ methylation is quite different from the reversible methylation that occurs at glutamate residues in the receptors.

Keywords

Myosin Light Chain Methyl Transferase Bacterial Chemotaxis Flagellar Motor Flagellar Rotation 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Alix, J.-H., Hayes, D., Lontie, J.-F., Colson, C. , Glatigny, A., and Lederer, F., 1979a, Methylated amino acids in ribosomal proteins from Escherichia coli treated with ethionine and from a mutant lacking methylation of protein L11, Biochimie. 61:671.CrossRefGoogle Scholar
  2. Alix, J.-H., Hayes, D., and Nierhaus, K. H., 1979b, Properties of ribosomes and RNA synthesized by Escherichia coli grown in the presence of ethionine, J. Mol. Biol., 127:375.Google Scholar
  3. Berg, H. C. , and Brown, D. A., 1972, Chemotaxis in Escherichia coli analysed by three-dimensional tracking, Nature (London). 239:500.CrossRefGoogle Scholar
  4. Block, S. M., Segall, J. E., and Berg, H. C., 1983, Adaptation kinetics in bacterial Chemotaxis, J. Bacteriol., 154:312.PubMedGoogle Scholar
  5. Brauer, D. , and Wittmann-Liebold, B. , 1977, The primary structure of the initiation factor IF-3 from Escherichia coli, FEBS Lett. 79:269.PubMedCrossRefGoogle Scholar
  6. Brosius, J., and Chen, R., 1976, The primary structure of protein L16 located at the peptidyltransferase center of Escherichia coli ribosomes, FEBS Lett., 68:105.PubMedCrossRefGoogle Scholar
  7. Brown, D. A., and Berg, H. C., 1974, Temporal stimulation of Chemotaxis in Escherichia coli, Proc. Natl. Acad. Sci. U. S. A., 71:1388.PubMedCrossRefGoogle Scholar
  8. Chang, F. N. , and Budzilowicz, C. , 1977, Characterization of methylated neutral amino acids from Escherichia coli ribosomes, J. Bacteriol., 131:105.PubMedGoogle Scholar
  9. Chang, C. N. , Schwartz, M. , and Chang, F. N. , 1976, Identification and characterization of a new methylated amino acid in ribosomal protein L33 of Escherichia coli, Biochem. Biophys. Res. Commun., 73:233.PubMedCrossRefGoogle Scholar
  10. Chen, R., Brosius, J., Wittmann-Liebold, B., and Schafer, W., 1977, Occurrence of methylated amino acids as N-termini of proteins from Escherichia coli ribosomes, J. Mol. Biol., 111:173.PubMedCrossRefGoogle Scholar
  11. Clegg, D. O., and Koshland, D. E. Jr., 1984, The role of a signaling protein in bacterial sensing: behavioral effects of increased gene expression, Proc. Natl. Acad. Sci. U. S. A., 81:5056.PubMedCrossRefGoogle Scholar
  12. Colson, C., Lhoest, J., and Urlings, C., 1979, Genetics of ribosomal protein methylation in Escherichia coli, Molec. Gen. Genet., 169:245.PubMedCrossRefGoogle Scholar
  13. Czernilofsky, A. P., Collatz, E. E., Stoffler, G., and Kuechler, E., 1974, Proteins at the tRNA binding sites of Escherichia coli ribosomes, Proc. Natl. Acad. Sci. U. S. A., 71:230.PubMedCrossRefGoogle Scholar
  14. Dayhoff, M. O., 1978, “Atlas of Protein Sequence and Structure,” (electronic data base released Mar. 1987), National Biomedical Research Foundation, Silver Spring, Maryland.Google Scholar
  15. Dietrich, S., Schrandt, I., and Nierhaus, K. H., 1974, Interdependence of E. coli ribosomal proteins at the peptidyltransferase centre, FEBS Lett., 47:136.PubMedCrossRefGoogle Scholar
  16. Dognin, M. J., and Wittmann-Liebold, B., 1977, The primary structure of L11, the most heavily methylated protein from Escherichia coli ribosomes, FEBS Lett., 84:342.PubMedCrossRefGoogle Scholar
  17. Dognin, M. J., and Wittmann-Liebold, B., 1980, Purification and primary structure determination of the N-terminal blocked protein, L11, from Escherichia coli ribosomes, Eur. J. Biochem., 112:131.PubMedCrossRefGoogle Scholar
  18. Elgin, S. C. R., Schilling, J., and Hood, L. E., 1970, Sequence of histone H2B of Drosophila melanogaster, Biochemistry. 18:5679.CrossRefGoogle Scholar
  19. Frank, G., and Weeds, G. A., 1974, The amino-acid sequence of the alkali light chains of rabbit skeletal-muscle myosin, Eur. J. Biochem., 44:317.PubMedCrossRefGoogle Scholar
  20. Froholm, L. O., and Sletten, K., 1977, Purification and N-terminal sequence of a fimbrial protein from Moraxella nonliquefaciens, FEBS Lett., 73:29.PubMedCrossRefGoogle Scholar
  21. Frost, L. S., Carpenter, M., and Paranchych, W., 1978, N-Methylphenylalanine at the N-terminus of pilin isolated from Pseudomonas aeruginosa K., Nature (London). 271:87.CrossRefGoogle Scholar
  22. Grand, R. J. A., 1982, The structure and function of myosin light chains, Life Chem. Rep., 1:105.Google Scholar
  23. Henry, G. D., Dalgarno, D. C., Marcus, G., Scott, M., Levine, B. A., and Trayer, I. P., 1982, The occurrence of α-N-trimethylalanine as the N-terminal amino acid of some myosin light chains, FEBS Lett., 144:11.PubMedCrossRefGoogle Scholar
  24. Henry, G. D., Trayer, I. P., Brewer, S., and Levine, B. A., 1985a, The widespread distribution of α-N-trimethylalanine as the N-terminal amino acid of light chains from vertebrate striated muscle myosins, Eur. J. Biochem., 148:75.CrossRefGoogle Scholar
  25. Henry, G. D. , Winstanley, M. A., Dalgarno, D. C., Marcus, G. , Scott, M. , Levine, B. A., and Trayer, I. P., 1985b, Characterization of the actin-binding site on the alkali light chain of myosin, Biochem. Biophvs. Acta. 830:233.CrossRefGoogle Scholar
  26. Hermodson, M. A., Chen, K. C. S., and Buchanan, T. M. , 1978, Neisseria pili proteins: amino-terminal amino acid sequences and identification of an unusual amino acid, Biochemistry. 17:442.PubMedCrossRefGoogle Scholar
  27. Jenks, W. P., and Regenstein, J., 1976, in: “Handbook of Biochemistry and Molecular Biology, 3rd ed., Physical and Chemical Data. Volume I,” G. D. Fasman, ed., CRC Press, Cleveland, Ohio.Google Scholar
  28. Kuo, S. C., and Koshland, D. E., Jr., 1987, Roles of cheY and cheZ gene products in controlling flagellar rotation in bacterial Chemotaxis of Escherichia coli, J. Bacteriol., 169:1307.PubMedGoogle Scholar
  29. Kutsukake, K., and Lino, T., 1985, Refined genetic analysis of the region II che mutants in Salmonella typhimurium, Molec. Gen. Genet., 199:406.PubMedCrossRefGoogle Scholar
  30. Lederer, F., Alix, J.-H., and Hayes, D., 1977, N-Trimethylalanine, a novel blocking group, found in E. coli ribosomal protein L11, Biochem. Biophys. Res. Commun., 77:470.Google Scholar
  31. Marrs, C. F., Schoolnik, G. , Koomey, J. M. , Hardy, J., Rothbard, J., and Falkow, S., 1985, Cloning and sequencing of a Moraxella bovis pilin gene, J. Bacteriol., 163:132.PubMedGoogle Scholar
  32. Martinage, A., Briand, G., Van Dorsselaer, A., Turner, C. H., and Sautiere, P., 1985, Primary structure of histone H2B from gonads of the starfish Asterias rub ens, Eur. J. Biochem., 147:351.PubMedCrossRefGoogle Scholar
  33. Matsuda, G., Maita, T., and Umegane, T., 1981, The primary structure of L-1 light chain of chicken fast skeletal muscle myosin and its genetic implication, FEBS Lett., 126:111.PubMedCrossRefGoogle Scholar
  34. Matsumura, P., Rydel, J. J., Linzmeier, R., and Vacante, D. , 1984, Overexpression and sequence of the Escherichia coli cheY gene and biochemical activities of the CheY protein, J. Bacteriol., 160:36.PubMedGoogle Scholar
  35. McKern, N. M., O’Donnell, J., Inglis, A. S., Stewart, D. J., and Clark, B. L., 1983, Amino acid sequence of pilin from Bacteroides nodosus (strain 198), the causative organism of ovine footrot, FEBS Lett., 164:149.PubMedCrossRefGoogle Scholar
  36. Moore, V. G., Atchison, R. E., Thomas, G., Moran, M., and Noller, H. F., 1975, Identification of a ribosomal protein essential for peptidyl transferase activity, Proc. Natl. Acad. Sci. U. S. A., 72:844.PubMedCrossRefGoogle Scholar
  37. Mutoh, N., and Simon, M. I., 1986, Nucleotide sequence corresponding to five Chemotaxis genes in Escherichia coli, J. Bacteriol., 165:161.PubMedGoogle Scholar
  38. Nierhaus, K. H., and Montejo, V., 1973, A protein involved in the peptidyl transferase activity of Escherichia coli ribosomes, Proc. Natl. Acad. Sci. U. S. A., 70:1931.PubMedCrossRefGoogle Scholar
  39. Nierhaus, D., and Nierhaus, K. H., 1973, Identification of the chloramphenicol-binding protein in Escherichia coli ribosomes by partial reconstitution, Proc. Natl. Acad. Sci. U. S. A., 70:2224.PubMedCrossRefGoogle Scholar
  40. Nomoto, M., Hayashi, H., and Iwai, K., 1982a, Tetrahymena histone H2B. Complete amino acid sequence, J. Biochem., 91:897.Google Scholar
  41. Nomoto, M. , Kyogoku, Y. , and Iwai, K. , 1982b, tf-Trimethylalanine, a novel blocked N-terminal residue of Tetrahymena histone H2B, J. Biochem., 92:1675.PubMedGoogle Scholar
  42. Okamoto, Y., and Yount, R. G., 1985, Identification of an active site peptide of skeletal myosin after photoaffinity labeling with N-(4-azido-2-nitrophenyl)-2-aminoethyl diphosphate, Proc. Natl. Acad. Sci. U. S. A., 82:1575.PubMedCrossRefGoogle Scholar
  43. Paik, W.K., and Kim, S., 1980, “Protein Methylation,” John Wiley and Sons, New York.Google Scholar
  44. Paranchych, W., Frost, L. S., and Carpenter, M., 1978, N-Terminal amino acid sequence of pilin isolated from Pseudomonas aeruginosa, J. Bacteriol., 134:1179.PubMedGoogle Scholar
  45. Parkinson, J. S., 1978, Complementation analysis and deletion mapping of Escherichia coli mutants defective in Chemotaxis, J. Bacteriol., 135:45.PubMedGoogle Scholar
  46. Parkinson, J. S., and Parker, S. R., 1979, Interaction of the cheC and cheZ gene products is required for chemotactic behavior in Escherichia coli, Proc. Natl. Acad. Sci. U. S. A., 76:2390.PubMedCrossRefGoogle Scholar
  47. Parkinson, J. S., Parker, S. R., Talbert, P. B., and Houts, S. E., 1983, Interactions between Chemotaxis genes and flagellar genes in Escherichia coli, J. Bacteriol., 155:265.PubMedGoogle Scholar
  48. Pettigrew, G. W., Leaver, J. L., Meyer, T. E., Ryle, A. P., 1975, Purification, properties and amino acid sequence of atypical cytochrome c from two protozoa, Euglena gracilis and Crithidia oncopelti, Biochem. J., 147:291.PubMedGoogle Scholar
  49. Pettigrew, G. W. , and Smith, G. M. , 1977, Novel N-terminal protein blocking group identified as dimethylproline, Nature (London). 265:661.CrossRefGoogle Scholar
  50. Pongs, O., Bald, R. , and Erdmann, V. A., 1973, Identification of chloramphenicol-binding protein in Escherichia coli ribosomes by affinity labeling, Proc. Natl. Acad. Sci. U. S. A., 70:2229.PubMedCrossRefGoogle Scholar
  51. Ravid, S., Matsumura, P., and Eisenbach, M., 1986, Restoration of flagellar clockwise rotation in bacterial envelopes by insertion of the Chemotaxis protein CheY, Proc. Natl. Acad. Sci. U. S. A., 83:7157.PubMedCrossRefGoogle Scholar
  52. Ridgway, H. F., Silverman, M. , and Simon, M. I., 1977, Localization of proteins controlling motility and Chemotaxis in Escherichia coli, J. Bacteriol., 132:657.PubMedGoogle Scholar
  53. Schiltz, E. , Palm, D. , and Klein, H. W. , 1980, N-Terminal sequences of Escherichia coli and potato Phosphorylase, FEBS Lett., 109:59.PubMedCrossRefGoogle Scholar
  54. Segall, J. E., Ishihara, A., and Berg, H. C., 1985, Chemotactic signaling in filamentous cells of Escherichia coli, J. Bacteriol., 161:51.PubMedGoogle Scholar
  55. Segall, J. E., Manson, M. D. , and Berg, H. C. , 1982, Signal processing times in bacterial Chemotaxis, Nature (London). 296:855.CrossRefGoogle Scholar
  56. Silverman, M. , and Simon, M. , 1977a, Chemotaxis in Escherichia coli: methylation of che gene products, Proc. Natl. Acad. Sci. U. S. A., 74:3317.CrossRefGoogle Scholar
  57. Silverman, M., and Simon, M., 1977b, Identification of polypeptides necessary for Chemotaxis in Escherichia coli, J. Bacteriol., 130:1317.Google Scholar
  58. Smith, G. M., and Pettigrew, G. W., 1980, Identification of N,N-dimethylproline as the N-terminal blocking group of Crithidia oncopelti cytochrome C557, Eur. J. Biochem., 110:123.PubMedCrossRefGoogle Scholar
  59. Stock, A., Clarke, S., Clarke, C., and Stock, J., 1987a, N-Terminal methylation of proteins — structure, function, and specificity, FEBS. Lett., in press.Google Scholar
  60. Stock, A. M., Koshland, D. E. Jr., and Stock, J. B., 1985, Homologies between the Salmonella typhimurium CheY protein and proteins involved in the regulation of Chemotaxis, membrane protein synthesis, and sporulation, Proc. Natl. Acad. Sci. U. S. A., 82:7989.PubMedCrossRefGoogle Scholar
  61. Stock, A., Mottonen, J., Chen, T., and Stock, J., 1987b, Identification of a possible nucleotide binding site in CheW, a protein required for sensory transduction in bacterial Chemotaxis, J. Biol. Chem., 262:535.Google Scholar
  62. Stock, A., Schaeffer, E. , Koshland, D. E. Jr., and Stock, J., 1987c, A second type of protein methylation reaction in bacterial Chemotaxis, J. Biol. Chem., 262:8011.Google Scholar
  63. Stock, A. M., and Stock, J. B., 1987, Purification and characterization of the CheZ protein of bacterial Chemotaxis, J. Bacteriol., 169(7): in press.Google Scholar
  64. Stock, J., and Simms, S., 1987, Methylation, demethylation, and deamidation at glutamate residues in membrane chemoreceptor proteins, in: “Post-Translational Modifications of Proteins and Ageing,” V. Zappia, ed., Plenum Press, New York.Google Scholar
  65. Stoffler, G., Daya, L. , Rak, K. H. , and Garrett, R. A., 1971, Specific protein binding sites on 23 S RNA of Escherichia coli, Molec. Gen. Genet., 114:125.Google Scholar
  66. Tokunaga, M. , Suzuki, M. , Saeki, K., and Wakabayashi, T. , 1987, Position of the amino terminus of myosin light chain 1 and light chain 2 determined by electron microscopy with monoclonal antibody, J. Mol. Biol., 194:245.PubMedCrossRefGoogle Scholar
  67. Tsunasawa, S., Stewart, J. W. , and Sherman, F., 1985, Amino-terminal processing of mutant forms of yeast iso-1-cytochrome c, J. Biol. Chem., 260:5382.PubMedGoogle Scholar
  68. Valentine, J., and Pettigrew, G. W., 1982, A cytochrome c methyltransferase from Crithidia oncopelti, Biochem. J., 201:329.PubMedGoogle Scholar
  69. Van Helden P. D. , Strickland, W. N. , Brandt, W. F., and Von Holt, C., 1979, The complete amino-acid sequence of histone H2B from the mollusc Patella granatina, Eur. J. Biochem., 93:71.PubMedCrossRefGoogle Scholar
  70. Wittmann-Liebold, B., 1973, Studies on the primary structure of 20 proteins from Escherichia coli ribosomes by means of an improved protein sequenator, FEBS Lett., 36:247.PubMedCrossRefGoogle Scholar
  71. Wittmann-Liebold, B., and Pannenbecker, R., 1976, Primary structure of protein L33 from the large subunit of the Escherichia coli ribosome, FEBS Lett., 68, 115.PubMedCrossRefGoogle Scholar
  72. Wolfe, A. J., Conley, M. P., Kramer, T. J., and Berg, H. C., 1987, Reconstitution of signaling in bacterial Chemotaxis, J. Bacteriol., 169:1878.PubMedGoogle Scholar
  73. Yamaguchi, S., Aizawa, S.-I., Kihara, M., Isomura, M., Jones, C. J., and Macnab, R. M., 1986, Genetic evidence for a switching and energy-transducing complex in the flagellar motor of Salmonella typhimuriwn, J. Bacteriol., 168:1172.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1988

Authors and Affiliations

  • Ann Stock
    • 1
  1. 1.Department of Molecular BiologyPrinceton UniversityPrincetonUSA

Personalised recommendations