The major phase-variable outer membrane protein of Escherichia coli structurally resembles the immunoglobulin A1 protease class of exported protein and is regulated by a novel mechanism involving dam and OxyR

Journal of Bacteriology

Volumn 181, Issue 7, 1999, Pages 2132-2141

  Henderson, Ian R ^a,b   Owen, Peter ^a  

^a TRINITY COLLEGE DUBLIN   (Ireland)

^b Center for Vaccine Development   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN 43; BACTERIAL ENZYME; DEOXYADENOSINE METHYLASE; IMMUNOGLOBULIN A1 PROTEASE; INTEGRIN; OUTER MEMBRANE PROTEIN; PROTEIN OXYR; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GENE; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME MECHANISM; ESCHERICHIA COLI; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE ISOLATION; HAEMOPHILUS; NEISSERIA; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN SECONDARY STRUCTURE; REGULATORY MECHANISM; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY; SPECIES DIFFERENCE;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; HAEMOPHILUS; NEGIBACTERIA; NEISSERIA; PROKARYOTA;

EID: 0032940207     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/jb.181.7.2132-2141.1999     Document Type: Article

References (78)

1. Adley, C. C., and A. I. Bukhari. 1984. Methylation dependent expression of the mom gene of bacteriophage Mu: deletions downstream from the methylation sites affect expression. Nucleic Acids Res. 12:3535-3550.
2. Altschul, S. F., W. Gish, W. Miller, E. W. Meyers, and D. Lipman. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403-410.
3. Ausubel, F. M., R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struhl (ed.). 1989. Current protocols in molecular biology. Greene Publishing Associates, New York, N.Y.
4. Bachmann, B. J. 1972. Pedigrees of some mutant strains of Escherichia coli K-12. Bacteriol. Rev. 36:525-557.
5. Bardwell, J. C., K. McGovern, and J. Beckwith. 1991. Identification of a protein required for disulphide bond formation in vivo. Cell 67:581-589.
6. Benz, I., and M. A. Schmidt. 1989. Cloning and expression of an adhesin (AIDA-I) involved in diffuse adherence of enteropathogenic Escherichia coli. Infect. Immun. 57:1506-1511.
7. Benz, I., and M. A. Schmidt. 1992. AIDA-I, the adhesin involved in diffuse adherence of the diarrhoeagenic Escherichia coli strain 2787 (O126:H27) is synthesized via a precursor molecule. Mol. Microbiol. 6:1539-1546.
8. Berger, B., D. B. Wilson, E. Wolf, T. Tonchev, M. Milla, and P. S. Kim. 1995. Predicting coiled coils by use of pairwise residue correlations. Proc. Natl. Acad. Sci. USA 92:8259-8263.
9. Blyn, L. B., B. A. Braaten, and D. A. Low. 1990. Regulation of pap pilin phase variation by a mechanism involving differential Dam methylation states. EMBO J. 9:4045-4054.
10. Blyn, L. B., B. A. Braaten, C. A. White-Ziegler, D. H. Rolfson, and D. A. Low. 1989. Phase-variation of pyelonephritis-associated pili in Escherichia coli: evidence for transcriptional regulation EMBO J. 8:613-620.
11. 70. J. Bacteriol. 173:4482-4492.
12. Bölker, M., and R. Kahmann. 1989. The Escherichia coli regulatory protein OxyR discriminates between methylated and unmethylated states of the phage Mu mom promoter. EMBO J. 8:2403-2410.
13. Bölker, M., F. G. Wulczyn, and R. Kahmann. 1989. Role of bacteriophage MuC protein in activation of the mom gene promoter. J. Bacteriol. 171: 2019-2027.
14. Bourdon, M. A., T. Krusius, S. Campbell, N. B. Schwartz, and E. Ruoslahti. 1987. Identification and synthesis of a recognition signal for the attachment of glycosaminoglycans to proteins. Proc. Natl. Acad. Sci. USA 84:3194-3198.
15. Boyer, H. W., and D. Roulland-Dussoix. 1969. A complementation analysis of the restriction and modification of DNA in Escherichia coli. J. Mol. Biol. 41:459-472.
16. Braaten, B. A., L. B. Blyn, B. S. Skinner, and D. A. Low. 1991. Evidence for a methylation-blocking factor (mbf) locus involved in pap pilus expression and phase variation in Escherichia coli. J. Bacteriol. 173:1789-1800.
17. Busby, S., D. Kotlarz, and H. Buc. 1983. Deletion mutagenesis of the Escherichia coli galactose operon promoter region. J. Mol. Biol. 167:259-274.
18. Caffrey, P., and P. Owen. 1989. Purification and N-terminal sequence of the α subunit of antigen 43, a unique protein complex associated with the outer membrane of Escherichia coli. J. Bacteriol. 171:3634-3640.
19. Caffrey, P., T. McVeigh, and P. Owen. 1988. Western immunoblotting, p. 255-266. In P. Owen and T. J. Foster (ed.). Immunochemical and molecular genetic analysis of bacterial pathogens. Elsevier Science Publishing. Amsterdam, The Netherlands.
20. Casadaban, M. J. 1976. Transposition and fusion of the lac genes to selected promoters in Escherichia coli using bacteriophage lambda and Mu. J. Mol. Biol. 104:541-555.
21. Casadaban, M. J., and S. N. Cohen. 1980. Analysis of gene control signals by DNA fusion and cloning in Escherichia coli. J. Mol. Biol. 138:179-207.
22. Christman, M. F., R. W. Morgan, F. S. Jacobson, and B. N. Ames. 1985. Positive control of a regulon for defenses against oxidative stress and some heat-shock proteins in Salmonella typhimurium. Cell 41:753-762.
23. Connell, N., Z. Han, F. Moreno, and R. Kolter. 1987. An E. coli promoter induced by the cessation of growth. Mol. Microbiol. 1:195-201.
24. Dersch, P., K. Schmidt, and E. Bremer. 1993. Synthesis of the Escherichia coli K-12 nucleoid-associated DNA-binding protein H-NS is subjected to growth-phase control and autoregulation. Mol. Microbiol. 8:875-889.
25. Diderichsen, B. 1980. flu, a metastable gene controlling surface properties of Escherichia coli. J. Bacteriol. 141:858-867.
26. Dorman, C. J. 1994. Genetics of bacterial virulence. Blackwell Scientific Publications, Oxford, England.
27. Dybvig, K. 1993. DNA rearrangements and phenotypic switching in prokaryotes. Mol. Microbiol. 10:465-471.
28. Earhart, C. F., M. Lundigran, C. L. Pickett, and J. R. Pierce. 1979. Escherichia coli K-12 mutants that lack major outer membrane protein a. FEMS Microbiol. Lett. 6:277-280.
29. Emini, E. A., J. V. Hughes, D. S. Perlow, and J. Boger. 1985. Induction of hepatitis A virus-neutralizing antibody by a virus-specific synthetic peptide. J. Virol. 55:836-839.
30. Foltmann, B. 1981. Gastric proteinases - structure, function, evolution and mechanism of action. Essays Biochem. 17:52-84.
31. Hale, W. B., M. W. van der Woude, and D. A. Low. 1994. Analysis of nonmethylated GATC sites in the Escherichia coli chromosome and identification of sites that are differentially methylated in response to environmental stimuli. J. Bacteriol. 176:3438-3441.
32. Henderson, I. R., F. Navarro-Garcia, and J. P. Nataro. 1998. The great escape: structure and function of autotransporters. Trends Microbiol. 6:370-376.
33. Henderson, I. R., M. Meehan, and P. Owen. 1997. Antigen 43, a phase-variable bipartite outer membrane protein, determines colony morphology and autoaggregation in Escherichia coli K-12. FEMS Microbiol. Lett. 149: 115-120.
34. Huisman, O., M. Faelen, D. Girard, A. Jaffé, A. Toussaint, and J. Rouvière-Yaniv. 1989. Multiple defects in Escherichia coli mutants lacking HU protein. J. Bacteriol. 171:3704-3712.
35. Isberg, R. R., and G. Tran Van Nhieu. 1994. Binding and internalization of microorganisms by integrin receptors. Trends Microbiol. 2:10-14.
36. Izard, J. W., and D. A. Kendall. 1994. Signal peptides: exquisitely designed transport promoters. Mol. Microbiol. 13:765-773.
37. Jähnig, F. 1990. Structure predictions of membrane proteins are not that bad. Trends Biochem Sci. 15:93-95.
38. Jeanteur, D., J. H. Lakey, and F. Pattus. 1991. The bacterial porin superfamily: sequence alignment and structure prediction. Mol. Microbiol. 5:2153-2164.
39. Kahmann, R. 1983. Methylation regulates the expression of a DNA modification function encoded by bacteriophage Mu. Cold Spring Harbor Symp. Quant. Biol. 47:639-646.
40. Kaufmann, A., Y.-D. Stierhof, and U. Henning. 1994. New outer membrane-associated protease of Escherichia coli K-12. J. Bacteriol. 176:359-367.
41. Koch, C., J. Vandekerckhove, and R. Kahmann. 1988. Escherichia coli host factor for site-specific DNA inversion: cloning and characterization of the fis gene. Proc. Natl. Acad. Sci. USA 85:4237-4241.
42. Kohara, Y., K. Akiyama, and K. Isono. 1987. The physical map of the whole L. coli chromosome: application of a new strategy for rapid analysis and sorting of a large genomic library. Cell 50:495-508.
43. Kullik, I., J. Stevens, M. B. Toledano, and G. Storz. 1995. Mutational analysis of the redox-sensitive transcriptional regulator OxyR: regions important for DNA binding and multimerization. J. Bacteriol. 177:1285-1291.
44. Kullik, I., M. B. Toledano, L. A. Tartaglia, and G. Storz. 1995. Mutational analysis of the redox-sensitive transcriptional regulator OxyR: regions important for oxidation and transcriptional activation. J. Bacteriol. 177:1275-1284.
45. Kyte, J., and R. F. Doolittle. 1982. A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 157:105-132.
46. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature (London) 227:680-685.
47. Loveless, B. J., and M. H. Saier, Jr. 1997. A novel family of channel-forming, autotransporting, bacterial virulence factors. Mol. Membr. Biol. 14:113-123.
48. Lupas, A. 1996. Prediction and analysis of coiled coil structures. Methods Enzymol. 266:513-525.
49. Lupas, A., M. van Dyke, and J. Stock. 1991. Predicting coiled coils from protein sequences. Science 252:1162-1164.
50. McNairn, E., N. NiBhriain, and C. J. Dorman. 1995. Overexpression of the Shigella flexneri genes coding for DNA topoisomerase IV compensates for loss of DNA topoisomerase I: effect on virulence gene expression. Mol. Microbiol. 15:507-517.
51. Menzel, R., and M. Gellert. 1987. Fusions of the Escherichia coli gyrA and gyrB control regions to the galactokinase gene are inducible by coumermycin treatment. J. Bacteriol. 169:1272-1278.
52. Miller, J. H. 1992. A short course in bacterial genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
53. Noda, A., J. B. Courtwright, P. F. Denor, G. Webb, Y. Kohara, and A. Ishihama. 1991. Rapid identification of specific genes in Esherichia coli by hybridization to membranes containing the ordered set of phage clones. BioTechniques 10:474-477.
54. Nowicki, B., M. Rhen, V. Väisänen-Rhen, A. Pere, and T. K. Korhonen. 1984. Immunofluorescence study of fimbrial phase variation on Escherichia coli KS71. J. Bacteriol. 160:691-695.
55. Owen, P. 1992. The gram-negative outer membrane: structure, biochemistry and vaccine potential. Biochem. Soc. Trans. 20:1-6.
56. Owen, P., M. Meehan, H. de Loughrey-Doherty, and I. Henderson. 1996. Phase-variable outer membrane proteins in Escherichia coli. FEMS Immunol. Med. Microbiol. 16:63-76.
57. Owen, P., P. Caffrey, and L.-G. Josefsson. 1987. Identification and partial characterization of a novel bipartite protein antigen associated with the outer membrane of Escherichia coli. J. Bacteriol. 169:3770-3777.
58. Owen, P., P. Caffrey, L.-G. Josefsson, and M. Meehan. 1991. Outer membrane proteins: old and new. p. 127-139. In E. Z. Ron and S. Rottem (ed.), Microbial surface components and toxins in relation to pathogenesis. Plenum Press, New York, N.Y.
59. Palmer, B. R., and M. G. Marinus. 1994. The dam and dcm strains of Escherichia coli - a review. Gene 143:1-12.
60. Parker, B., and M. G. Marinus. 1988. A simple and rapid method to obtain substitution mutations in Escherichia coli: isolation of a dam deletion/insertion mutation. Gene 73:531-535.
61. Parker, J. M. R., D. Gou, and R. S. Hodges. 1986. New hydrophilicity scale derived from high-performance liquid chromatography peptide retention data: correlation of predicted surface residues with antigenicity and X-ray derived accessible sites. Biochemistry 25:5425-5432.
62. Pearson, W. R., and D. J. Lipman. 1988. Improved tools for biological sequence comparison. Proc. Natl. Acad. Sci. USA 85:2444-2448.
63. Plasterk, R., H. A. Vrieling, and P. Van de Putte. 1983. Transcription initiation of Mu mom depends on methylation of the promoter region and a phage-coded transactivator. Nature (London) 301:344-347.
64. Rao, J. K. M., J. W. Erickson, and A. Wlodawer. 1991. Structural and evolutionary relationships between retroviral and eucaryotic aspartic proteinases. Biochemistry 30:4663-4671.
65. Roberts, M., N. F. Fairweather, E. Leininger, D. Pickard, E. L. Hewlett, A. Robinson, C. Hayward, G. Dougan, and I. G. Charles. 1991. Construction and characterization of Bordetella pertussis mutants lacking the vir-regulated P.69 outer membrane protein. Mol. Microbiol. 5:1393-1404.
66. Saraste, M., P. R. Sibbald, and A. Wittinghofer. 1990. The P-loop: a common motif in ATP- and GTP-binding proteins. Trends Biochem. Sci. 15:430-434.
67. Schägger, H., and G. von Jagow. 1987. Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100-kDa. Anal. Biochem. 166:368-379.
68. Schnaitman, C. A., and G. A. McDonald. 1984. Regulation of outer membrane protein synthesis in Escherichia coli K-12: deletion of ompC affects expression of the OmpF protein. J. Bacteriol. 159:555-563.
69. Smith, S. G. J. 1995. Regulation of CS1 fimbrial expression. Ph.D. thesis. Trinity College. Dublin, Ireland.
70. Southern, E. M. 1975. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J. Mol. Biol. 98:503-517.
71. Storz, G., L. A. Tartaglia, and B. N. Ames. 1990. Transcriptional regulator of oxidative stress-inducible genes: direct activation by oxidation. Science 248: 189-194.
72. Strauch, K. L., K. Johnson, and J. Beckwith. 1989. Characterization of degP, a gene required for protcolysis in the cell envelope and essential for growth of Escherichia coli at high temperature. J. Bacteriol. 171:2689-2696.
73. Tao, K., C. Zou, N. Fujita, and A. Ishihama. 1995. Mapping of the OxyR protein contact site in the C-terminal region of RNA polymerase alpha subunit. J. Bacteriol. 177:6740-6744.
74. Van der Woude, M., B. Braaten, and D. Low. 1996. Epigenetic phase variation of the pap operon in Escherichia coli. Trends Microbiol. 4:5-9.
75. Warne, S. R., J. M. Varley, G. J. Boulnois, and M. G. Norton. 1990. Identification and characterization of a gene that controls colony morphology and auto-aggregation in Escherichia coli K-12. J. Gen. Microbiol. 136:455-462.
76. Wolf, E., P. S. Kim, and B. Berger. 1997. Multicoil: a program for predicting two- and three-stranded coiled coils. Protein Sci. 6:1179-1189.
77. Yu, X.-M., and W. S. Reznikoff. 1984. Deletion analysis of the CAP-CAMP binding site of the Escherichia coli lactose promoter. Nucleic Acids Res. 12:5449-5464.
78. Zheng, M., F. Aslund, and G. Storz. 1998. Activation of the OxyR transcription factor by reversible disulfide bond formation. Science 279:1718-1721.