Constitutive expression of the maltoporin LamB in the absence of OmpR damages the cell envelope

Journal of Bacteriology

Volumn 193, Issue 4, 2011, Pages 842-853

  Reimann, Sylvia A ^a   Wolfe, Alan J ^a  

^a LOYOLA UNIVERSITY CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MALTOSE; PHOSPHATE; PORIN;

ARTICLE; BACTERIAL GENE; BACTERIAL MEMBRANE; BIOCHEMISTRY; CELL DAMAGE; CELL DEATH; CELL SURVIVAL; CONTROLLED STUDY; CYTOLYSIS; GENETIC TRANSCRIPTION; LAMB GENE; MALT GENE; MICROSCOPY; MUTANT; NONHUMAN; OMPR GENE; OSMOREGULATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULON;

BACTERIAL OUTER MEMBRANE PROTEINS; BACTERIAL PROTEINS; CELL MEMBRANE; ESCHERICHIA COLI; GENE EXPRESSION REGULATION, BACTERIAL; PORINS; RECEPTORS, VIRUS; TRANS-ACTIVATORS;

EID: 79551477097     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.01004-10     Document Type: Article

References (89)

1. Alba, B. M., and C. A. Gross. 2004. Regulation of the Escherichia coli sigma-dependent envelope stress response. Mol. Microbiol. 52:613-619.
2. Alba, B. M., J. A. Leeds, C. Onufryk, C. Z. Lu, and C. A. Gross. 2002. DegS and YaeL participate sequentially in the cleavage of RseA to activate the sigma(E)-dependent extracytoplasmic stress response. Genes Dev. 16:2156-2168.
3. Amemura, M., K. Makino, H. Shinagawa, A. Kobayashi, and A. Nakata. 1985. Nucleotide sequence of the genes involved in phosphate transport and regulation of the phosphate regulon in Escherichia coli. J. Mol. Biol. 184:241-250.
4. Baba, T., et al. 2006. Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol. Syst. Biol. 2:2006.0008.
5. Beatty, C. M., D. F. Browning, S. J. Busby, and A. J. Wolfe. 2003. Cyclic AMP receptor protein-dependent activation of the Escherichia coli acsP2 promoter by a synergistic class III mechanism. J. Bacteriol. 185:5148-5157.
6. Boos, W., and A. Bohm. 2000. Learning new tricks from an old dog: MalT of the Escherichia coli maltose system is part of a complex regulatory network. Trends Genet. 16:404-409.
7. Boos, W., and H. Shuman. 1998. Maltose/maltodextrin system of Escherichia coli: transport, metabolism, and regulation. Microbiol. Mol. Biol. Rev. 62:204-229.
8. Bossi, L., and N. Figueroa-Bossi. 2007. A small RNA downregulates LamB maltoporin in Salmonella. Mol. Microbiol. 65:799-810. (Pubitemid 47077237)
9. Brzoska, P., and W. Boos. 1988. Characteristics of a ugp-encoded and phoBdependent glycerophosphoryl diester phosphodiesterase which is physically dependent on the Ugp transport system of Escherichia coli. J. Bacteriol. 170:4125-4135.
10. Case, C. C., B. Bukau, S. Granett, M. R. Villarejo, and W. Boos. 1986. Contrasting mechanisms of envZ control of mal and pho regulon genes in Escherichia coli. J. Bacteriol. 166:706-712.
11. Chapon, C. 1982. Role of the catabolite activator protein in the expression of the maltose regulon of Escherichia coli. Ann. Microbiol. (Paris) 133A:77-80. (Pubitemid 12189078)
12. Chapon, C., and A. Kolb. 1983. Action of CAP on the malT promoter in vitro. J. Bacteriol. 156:1135-1143.
13. Cox, G. B., H. Rosenberg, J. A. Downie, and S. Silver. 1981. Genetic analysis of mutants affected in the Pst inorganic phosphate transport system. J. Bacteriol. 148:1-9.
14. Cox, G. B., D. Webb, and H. Rosenberg. 1989. Specific amino acid residues in both the PstB and PstC proteins are required for phosphate transport by the Escherichia coli Pst system. J. Bacteriol. 171:1531-1534.
15. Dardonville, B., and O. Raibaud. 1990. Characterization of malT mutants that constitutively activate the maltose regulon of Escherichia coli. J. Bacteriol. 172:1846-1852.
16. Dartigalongue, C., D. Missiakas, and S. Raina. 2001. Characterization of the Escherichia coli sigma E regulon. J. Biol. Chem. 276:20866-20875.
17. Das, S., J. C. Noe, S. Paik, and T. Kitten. 2005. An improved arbitrary primed PCR method for rapid characterization of transposon insertion sites. J. Microbiol. Methods 63:89-94.
18. Datsenko, K. A., and B. L. Wanner. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. U. S. A. 97:6640-6645.
19. Debarbouille, M., H. A. Shuman, T. J. Silhavy, and M. Schwartz. 1978. Dominant constitutive mutations in malT, the positive regulator gene of the maltose regulon in Escherichia coli. J. Mol. Biol. 124:359-371.
20. de Boer, P. A., R. E. Crossley, and L. I. Rothfield. 1989. A division inhibitor and a topological specificity factor coded for by the minicell locus determine proper placement of the division septum in E. coli. Cell 56:641-649.
21. Duguay, A. R., and T. J. Silhavy. 2004. Quality control in the bacterial periplasm. Biochim. Biophys. Acta 1694:121-134.
22. Fredericks, C. E., S. Shibata, S. Aizawa, S. A. Reimann, and A. J. Wolfe. 2006. Acetyl phosphate-sensitive regulation of flagellar biogenesis and capsular biosynthesis depends on the Rcs phosphorelay. Mol. Microbiol. 61:734-747.
23. Greenspan, P., and S. D. Fowler. 1985. Spectrofluorometric studies of the lipid probe, Nile red. J. Lipid Res. 26:781-789.
24. Guven, K., M. Yolcu, R. Gul-Guven, S. Erdogan, and D. D. Pomerai. 2005. The effects of organic pesticides on inner membrane permeability in Escherichia coli ML35. Cell Biol. Toxicol. 21:73-81.
25. Hayden, J. D., and S. E. Ades. 2008. The extracytoplasmic stress factor, SigmaE, is required to maintain cell envelope integrity in Escherichia coli. PLoS One 3:e1573.
26. Herrera, G., A. Martinez, M. Blanco, and J. E. O'Connor. 2002. Assessment of Escherichia coli B with enhanced permeability to fluorochromes for flow cytometric assays of bacterial cell function. Cytometry 49:62-69.
27. Hsieh, Y. J., and B. L. Wanner. 2010. Global regulation by the seven-component Pi signaling system. Curr. Opin. Microbiol. 13:198-203.
28. Igo, M. M., J. M. Slauch, and T. J. Silhavy. 1990. Signal transduction in bacteria: kinases that control gene expression. New Biol. 2:5-9.
29. Johansen, J., A. A. Rasmussen, M. Overgaard, and P. Valentin-Hansen. 2006. Conserved small non-coding RNAs that belong to the SigmaE regulon: role in down-regulation of outer membrane proteins. J. Mol. Biol. 364:1-8.
30. Johansson, J., B. Dagberg, E. Richet, and B. E. Uhlin. 1998. H-NS and StpA proteins stimulate expression of the maltose regulon in Escherichia coli. J. Bacteriol. 180:6117-6125.
31. Kazakov, A. E., O. Vassieva, M. S. Gelfand, A. Osterman, and R. Overbeek. 2003. Bioinformatics classification and functional analysis of PhoH homologs. In Silico Biol. 3:3-15.
32. Kitagawa, M., et al. 2005. Complete set of ORF clones of Escherichia coli ASKA library (a complete set of E. coli K-12 ORF archive): unique resources for biological research. DNA Res. 12:291-299.
33. Koch, A. L. 1998. The biophysics of the gram-negative periplasmic space. Crit. Rev. Microbiol. 24:23-59.
34. Koebnik, R., K. P. Locher, and P. Van Gelder. 2000. Structure and function of bacterial outer membrane proteins: barrels in a nutshell. Mol. Microbiol. 37:239-253.
35. Korteland, J., J. Tommassen, and B. Lugtenberg. 1982. PhoE protein pore of the outer membrane of Escherichia coli K12 is a particularly efficient channel for organic and inorganic phosphate. Biochim. Biophys. Acta 690:282-289.
36. Kullman, L., M. Winterhalter, and S. M. Bezrukov. 2002. Transport of maltodextrins through maltoporin: a single-channel study. Biophys. J. 82:803-812.
37. Kumari, S., et al. 2000. Regulation of acetyl coenzyme A synthetase in Escherichia coli. J. Bacteriol. 182:4173-4179.
38. Larsen, R. A., M. M. Wilson, A. M. Guss, and W. W. Metcalf. 2002. Genetic analysis of pigment biosynthesis in Xanthobacter autotrophicus Py2 using a new, highly efficient transposon mutagenesis system that is functional in a wide variety of bacteria. Arch. Microbiol. 178:193-201.
39. Laubacher, M. E., and S. E. Ades. 2008. The Rcs phosphorelay is a cell envelope stress response activated by peptidoglycan stress and contributes to intrinsic antibiotic resistance. J. Bacteriol. 190:2065-2074.
40. Lauro, F. M., et al. 2008. Large-scale transposon mutagenesis of Photobacterium profundum SS9 reveals new genetic loci important for growth at low temperature and high pressure. J. Bacteriol. 190:1699-1709.
41. Mecsas, J., P. E. Rouviere, J. W. Erickson, T. J. Donohue, and C. A. Gross. 1993. The activity of sigma E, an Escherichia coli heat-inducible sigma-factor, is modulated by expression of outer membrane proteins. Genes Dev. 7:2618-2628.
42. Metcalf, W. W., P. M. Steed, and B. L. Wanner. 1990. Identification of phosphate starvation-inducible genes in Escherichia coli K-12 by DNA sequence analysis of psi::lacZ(Mu d1) transcriptional fusions. J. Bacteriol. 172:3191-3200.
43. Mizuno, T., and S. Mizushima. 1990. Signal transduction and gene regulation through the phosphorylation of two regulatory components: the molecular basis for the osmotic regulation of the porin genes. Mol. Microbiol. 4:1077-1082.
44. Morona, R., and P. Reeves. 1982. The tolC locus of Escherichia coli affects the expression of three major outer membrane proteins. J. Bacteriol. 150:1016-1023.
45. Muda, M., N. N. Rao, and A. Torriani. 1992. Role of PhoU in phosphate transport and alkaline phosphatase regulation. J. Bacteriol. 174:8057-8064.
46. Mulder, E., and C. L. Woldringh. 1993. Plasmolysis bays in Escherichia coli: are they related to development and positioning of division sites? J. Bacteriol. 175:2241-2247.
47. Mutalik, V. K., G. Nonaka, S. E. Ades, V. A. Rhodius, and C. A. Gross. 2009. Promoter strength properties of the complete sigma E regulon of Escherichia coli and Salmonella enterica. J. Bacteriol. 191:7279-7287.
48. Nikaido, H., and E. Y. Rosenberg. 1983. Porin channels in Escherichia coli: studies with liposomes reconstituted from purified proteins. J. Bacteriol. 153:241-252.
49. Oshima, T., et al. 2002. Transcriptome analysis of all two-component regulatory system mutants of Escherichia coli K-12. Mol. Microbiol. 46:281-291.
50. Oshima, T., S. Ishikawa, K. Kurokawa, H. Aiba, and N. Ogasawara. 2006. Escherichia coli histone-like protein H-NS preferentially binds to horizontally acquired DNA in association with RNA polymerase. DNA Res. 13:141-153.
51. O'Toole, G. A., and R. Kolter. 1998. Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signalling pathways: a genetic analysis. Mol. Microbiol. 28:449-461.
52. Powell, B. S., M. P. Rivas, D. L. Court, Y. Nakamura, and C. L. Turnbough, Jr. 1994. Rapid confirmation of single copy lambda prophage integration by PCR. Nucleic Acids Res. 22:5765-5766.
53. Pruss, B. M., C. Besemann, A. Denton, and A. J. Wolfe. 2006. A complex transcription network controls the early stages of biofilm development by Escherichia coli. J. Bacteriol. 188:3731-3739.
54. Raivio, T. L. 2005. Envelope stress responses and Gram-negative bacterial pathogenesis. Mol. Microbiol. 56:1119-1128.
55. Raivio, T. L., and T. J. Silhavy. 2001. Periplasmic stress and ECF sigma factors. Annu. Rev. Microbiol. 55:591-624.
56. Raivio, T. L., and T. J. Silhavy. 1997. Transduction of envelope stress in Escherichia coli by the Cpx two-component system. J. Bacteriol. 179:7724-7733.
57. Rao, N. N., and A. Torriani. 1990. Molecular aspects of phosphate transport in Escherichia coli. Mol. Microbiol. 4:1083-1090.
58. Reimann, S. A., and A. J. Wolfe. 2009. A critical process controlled by MalT and OmpR is revealed through synthetic lethality. J. Bacteriol. 191:5320-5324.
59. Reyes, M., and H. A. Shuman. 1988. Overproduction of MalK protein prevents expression of the Escherichia coli mal regulon. J. Bacteriol. 170:4598-4602.
60. Rhodius, V. A., W. C. Suh, G. Nonaka, J. West, and C. A. Gross. 2006. Conserved and variable functions of the SigmaE stress response in related genomes. PLoS Biol. 4:e2.
61. Rice, C. D., J. E. Pollard, Z. T. Lewis, and W. R. McCleary. 2009. Employment of a promoter-swapping technique shows that PhoU modulates the activity of the PstSCAB2 ABC transporter in Escherichia coli. Appl. Environ. Microbiol. 75:573-582.
62. Richet, E. 1996. On the role of the multiple regulatory elements involved in the activation of the Escherichia coli malEp promoter. J. Mol. Biol. 264:852-862.
63. Rizzitello, A. E., J. R. Harper, and T. J. Silhavy. 2001. Genetic evidence for parallel pathways of chaperone activity in the periplasm of Escherichia coli. J. Bacteriol. 183:6794-6800.
64. Rotman, B. 1977. On the rate limiting step in downhill transport via the LacY permease of Escherichia coli. J. Supramol. Struct. 7:29-35. (Pubitemid 8289220)
65. Rouviere, P. E., and C. A. Gross. 1996. SurA, a periplasmic protein with peptidyl-prolyl isomerase activity, participates in the assembly of outer membrane porins. Genes Dev. 10:3170-3182.
66. Ruiz, N., B. Falcone, D. Kahne, and T. J. Silhavy. 2005. Chemical conditionality: a genetic strategy to probe organelle assembly. Cell 121:307-317.
67. Ruiz, N., D. Kahne, and T. J. Silhavy. 2006. Advances in understanding bacterial outer-membrane biogenesis. Nat. Rev. Microbiol. 4:57-66.
68. Ruiz, N., D. Kahne, and T. J. Silhavy. 2009. Transport of lipopolysaccharide across the cell envelope: the long road of discovery. Nat. Rev. Microbiol. 7:677-683.
69. Ruiz, N., T. Wu, D. Kahne, and T. J. Silhavy. 2006. Probing the barrier function of the outer membrane with chemical conditionality. ACS Chem. Biol. 1:385-395.
70. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratroy manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
71. Schlegel, A., O. Danot, E. Richet, T. Ferenci, and W. Boos. 2002. The N terminus of the Escherichia coli transcription activator MalT is the domain of interaction with MalY. J. Bacteriol. 184:3069-3077.
72. Schweizer, H., M. Argast, and W. Boos. 1982. Characteristics of a binding protein-dependent transport system for sn-glycerol-3-phosphate in Escherichia coli that is part of the pho regulon. J. Bacteriol. 150:1154-1163.
73. Silhavy, T. J., M. L. Berman, and L. W. Enquist. 1984. Experiments with gene fusions. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
74. Simons, R. W., F. Houman, and N. Kleckner. 1987. Improved single and multicopy lac-based cloning vectors for protein and operon fusions. Gene 53:85-96.
75. Sklar, J. G., T. Wu, D. Kahne, and T. J. Silhavy. 2007. Defining the roles of the periplasmic chaperones SurA, Skp, and DegP in Escherichia coli. Genes Dev. 21:2473-2484.
76. Sperandeo, P., et al. 2007. Characterization of lptA and lptB, two essential genes implicated in lipopolysaccharide transport to the outer membrane of Escherichia coli. J. Bacteriol. 189:244-253.
77. Steed, P. M., and B. L. Wanner. 1993. Use of the rep technique for allele replacement to construct mutants with deletions of the pstSCAB-phoU operon: evidence of a new role for the PhoU protein in the phosphate regulon. J. Bacteriol. 175:6797-6809.
78. Stenberg, F., et al. 2005. Protein complexes of the Escherichia coli cell envelope. J. Biol. Chem. 280:34409-34419.
79. Torriani, A. 1990. From cell membrane to nucleotides: the phosphate regulon in Escherichia coli. Bioessays 12:371-376.
80. Udekwu, K. I., and E. G. Wagner. 2007. Sigma E controls biogenesis of the antisense RNA MicA. Nucleic Acids Res. 35:1279-1288.
81. van Stelten, J., F. Silva, D. Belin, and T. J. Silhavy. 2009. Effects of antibiotics and a proto-oncogene homolog on destruction of protein translocator SecY. Science 325:753-756.
82. Vogel, J., and K. Papenfort. 2006. Small non-coding RNAs and the bacterial outer membrane. Curr. Opin. Microbiol. 9:605-611.
83. Wanner, B. L., and J. A. Boline. 1990. Mapping and molecular cloning of the phn (psiD) locus for phosphonate utilization in Escherichia coli. J. Bacteriol. 172:1186-1196.
84. Wanner, B. L., and B. D. Chang. 1987. The phoBR operon in Escherichia coli K-12. J. Bacteriol. 169:5569-5574.
85. Wanner, B. L., and P. Latterell. 1980. Mutants affected in alkaline phosphatase, expression: evidence for multiple positive regulators of the phosphate regulon in Escherichia coli. Genetics 96:353-366.
86. Wanner, B. L., and M. R. Wilmes-Riesenberg. 1992. Involvement of phosphotransacetylase, acetate kinase, and acetyl phosphate synthesis in control of the phosphate regulon in Escherichia coli. J. Bacteriol. 174:2124-2130.
87. Wu, T., et al. 2005. Identification of a multicomponent complex required for outer membrane biogenesis in Escherichia coli. Cell 121:235-245.
88. Zhang, L., R. Benz, and R. E. Hancock. 1999. Influence of proline residues on the antibacterial and synergistic activities of alpha-helical peptides. Biochemistry 38:8102-8111.
89. Zundel, C. J., D. C. Capener, and W. R. McCleary. 1998. Analysis of the conserved acidic residues in the regulatory domain of PhoB. FEBS Lett. 441:242-246.