Hfq reduces envelope stress by controlling expression of envelope-localized proteins and protein complexes in enteropathogenic Escherichia coli

Molecular Microbiology

Volumn 92, Issue 4, 2014, Pages 681-697

  Vogt, Stefanie L ^a   Raivio, Tracy L ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ENVELOPE PROTEIN; ESCHERICHIA COLI PROTEIN; OUTER MEMBRANE PROTEIN; PROTEIN BFP; PROTEIN CPX; PROTEIN HFQ; REGULATOR PROTEIN; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; CPXA PROTEIN, E COLI; CPXR PROTEIN, BACTERIA; HFQ PROTEIN, E COLI; HOST FACTOR 1; PROTEIN KINASE; SIGMA FACTOR; SPORULATION-SPECIFIC SIGMA FACTORS;

'BUNDLE FORMING PILUS; ARTICLE; BACTERIAL GENE; BACTERIAL MEMBRANE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIUM PILUS; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; ENTEROPATHOGENIC ESCHERICHIA COLI; ESCHERICHIA COLI K 12; GENE ACTIVATION; GENE DELETION; GENE EXPRESSION REGULATION; GENE LOSS; HFQ GENE; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; GENETICS; METABOLISM; NUCLEOTIDE SEQUENCE; PHYSIOLOGICAL STRESS; PHYSIOLOGY;

ESCHERICHIA COLI; NEGIBACTERIA; PERA;

BACTERIAL PROTEINS; DNA MUTATIONAL ANALYSIS; ENTEROPATHOGENIC ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE DELETION; GENE EXPRESSION REGULATION, BACTERIAL; HOST FACTOR 1 PROTEIN; PROTEIN KINASES; SIGMA FACTOR; STRESS, PHYSIOLOGICAL;

EID: 84899932222     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12581     Document Type: Article

References (104)

1. E envelope stress response. Curr Opin Microbiol 11: 535-540.
2. E-dependent extracytoplasmic stress response is controlled by the regulated proteolysis of an anti-sigma factor. Genes Dev 13: 2449-2461.
3. Ali, S.S., Xia, B., Liu, J., and Navarre, W.W. (2012) Silencing of foreign DNA in bacteria. Curr Opin Microbiol 15: 175-181.
4. Baba, T., Ara, T., Hasegawa, M., Takai, Y., Okumura, Y., Baba, M., etal. (2006) Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol Syst Biol 2: 2006.0008.
5. Bojer, M.S., Jakobsen, H., Struve, C., Krogfelt, K.A., and Løbner-Olesen, A. (2012) Lack of the RNA chaperone hfq attenuates pathogenicity of several Escherichia coli pathotypes towards Caenorhabditis elegans. Microbes Infect 14: 1034-1039.
6. E response in Salmonella hfq mutants. Biochimie 90: 1539-1544.
7. Buelow, D.R., and Raivio, T.L. (2005) Cpx signal transduction is influenced by a conserved N-terminal domain in the novel inhibitor CpxP and the periplasmic protease DegP. J Bacteriol 187: 6622-6630.
8. Bury-Moné, S., Nomane, Y., Reymond, N., Barbet, R., Jacquet, E., Imbeaud, S., etal. (2009) Global analysis of extracytoplasmic stress signaling in Escherichia coli. PLoS Genet 5: e1000651.
9. Chen, S., Zhang, A., Blyn, L.B., and Storz, G. (2004) MicC, a second small-RNA regulator of Omp protein expression in Escherichia coli. J Bacteriol 186: 6689-6697.
10. E and the Cpx signal transduction systems control the synthesis of periplasmic protein-folding enzymes in Escherichia coli. Genes Dev 11: 1183-1193.
11. Danese, P.N., and Silhavy, T.J. (1998) CpxP, a stress-combative member of the Cpx regulon. J Bacteriol 180: 831-839.
12. Danese, P.N., Snyder, W.B., Cosma, C.L., Davis, L.J., and Silhavy, T.J. (1995) The Cpx two-component signal transduction pathway of Escherichia coli regulates transcription of the gene specifying the stress-inducible periplasmic protease, DegP. Genes Dev 9: 387-398.
13. Danese, P.N., Oliver, G.R., Barr, K., Bowman, G.D., Rick, P.D., and Silhavy, T.J. (1998) Accumulation of the enterobacterial common antigen lipid II biosynthetic intermediate stimulates degP transcription in Escherichia coli. J Bacteriol 180: 5875-5884.
14. E regulon. J Biol Chem 276: 20866-20875.
15. De Lay, N., and Gottesman, S. (2009) The Crp-activated small noncoding regulatory RNA CyaR (RyeE) links nutritional status to group behavior. J Bacteriol 191: 461-476.
16. De Lay, N., Schu, D.J., and Gottesman, S. (2013) Bacterial small RNA-based negative regulation: Hfq and its accomplices. J Biol Chem 288: 7996-8003.
17. De Wulf, P., Kwon, O., and Lin, E.C. (1999) The CpxRA signal transduction system of Escherichia coli: growth-related autoactivation and control of unanticipated target operons. J Bacteriol 181: 6772-6778.
18. E expression. Mol Microbiol 53: 345-354.
19. Donnenberg, M.S., and Kaper, J.B. (1991) Construction of an eae deletion mutant of enteropathogenic Escherichia coli by using a positive-selection suicide vector. Infect Immun 59: 4310-4317.
20. Dorel, C., Vidal, O., Prigent-Combaret, C., Vallet, I., and Lejeune, P. (1999) Involvement of the Cpx signal transduction pathway of E.coli in biofilm formation. FEMS Microbiol Lett 178: 169-175.
21. Dorman, C.J., and Kane, K.A. (2009) DNA bridging and antibridging: a role for bacterial nucleoid-associated proteins in regulating the expression of laterally acquired genes. FEMS Microbiol Rev 33: 587-592.
22. Douchin, V., Bohn, C., and Bouloc, P. (2006) Down-regulation of porins by a small RNA bypasses the essentiality of the regulated intramembrane proteolysis protease RseP in Escherichia coli. J Biol Chem 281: 12253-12259.
23. Edwards, R.A., Keller, L.H., and Schifferli, D.M. (1998) Improved allelic exchange vectors and their use to analyze 987P fimbria gene expression. Gene 207: 149-157.
24. E subunit of Escherichia coli RNA polymerase: a second alternate sigma factor involved in high-temperature gene expression. Genes Dev 3: 1462-1471.
25. Ferreira, G.M., and Spira, B. (2008) The pst operon of enteropathogenic Escherichia coli enhances bacterial adherence to epithelial cells. Microbiology 154: 2025-2036.
26. E-dependent envelope stress response in Salmonella enterica. Mol Microbiol 62: 838-852.
27. Fröhlich, K.S., and Vogel, J. (2009) Activation of gene expression by small RNA. Curr Opin Microbiol 12: 674-682.
28. Gerken, H., Leiser, O.P., Bennion, D., and Misra, R. (2010) Involvement and necessity of the Cpx regulon in the event of aberrant β-barrel outer membrane protein assembly. Mol Microbiol 75: 1033-1046.
29. Girón, J.A., Ho, A.S., and Schoolnik, G.K. (1991) An inducible bundle-forming pilus of enteropathogenic Escherichia coli. Science 254: 710-713.
30. Gogol, E.B., Rhodius, V.A., Papenfort, K., Vogel, J., and Gross, C.A. (2011) Small RNAs endow a transcriptional activator with essential repressor functions for single-tier control of a global stress regulon. Proc Natl Acad Sci USA 108: 12875-12880.
31. Gottesman, S. (2004) The small RNA regulators of Escherichia coli: roles and mechanisms. Annu Rev Microbiol 58: 303-328.
32. Guillier, M., and Gottesman, S. (2006) Remodelling of the Escherichia coli outer membrane by two small regulatory RNAs. Mol Microbiol 59: 231-247.
33. Guillier, M., Gottesman, S., and Storz, G. (2006) Modulating the outer membrane with small RNAs. Genes Dev 20: 2338-2348.
34. 32-mediated cytoplasmic stress response in Escherichia coli. J Bacteriol 189: 1963-1973.
35. Hansen, A.-M., and Kaper, J.B. (2009) Hfq affects the expression of the LEE pathogenicity island in enterohaemorrhagic Escherichia coli. Mol Microbiol 73: 446-465.
36. E stress response by DegS: how the PDZ domain keeps the protease inactive in the resting state and allows integration of different OMP-derived stress signals upon folding stress. Genes Dev 21: 2659-2670.
37. Hayashi, K., Morooka, N., Yamamoto, Y., Fujita, K., Isono, K., Choi, S., etal. (2006) Highly accurate genome sequences of Escherichia coli K-12 strains MG1655 and W3110. Mol Syst Biol 2: 2006-2007.
38. Hernday, A.D., Braaten, B.A., Broitman-Maduro, G., Engelberts, P., and Low, D.A. (2004) Regulation of the Pap epigenetic switch by CpxAR: phosphorylated CpxR inhibits transition to the phase ON state by competition with Lrp. Mol Cell 16: 537-547.
39. Ho, S.N., Hunt, H.D., Horton, R.M., Pullen, J.K., and Pease, L.R. (1989) Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77: 51-59.
40. Hoang, T.T., Karkhoff-Schweizer, R.R., Kutchma, A.J., and Schweizer, H.P. (1998) A broad-host-range Flp-FRT recombination system for site-specific excision of chromosomally-located DNA sequences: application for isolation of unmarked Pseudomonas aeruginosa mutants. Gene 212: 77-86.
41. Holmqvist, E., Reimegård, J., Sterk, M., Grantcharova, N., Römling, U., and Wagner, E.G.H. (2010) Two antisense RNAs target the transcriptional regulator CsgD to inhibit curli synthesis. EMBO J 29: 1840-1850.
42. Holmqvist, E., Unoson, C., Reimegård, J., and Wagner, E.G.H. (2012) A mixed double negative feedback loop between the sRNA MicF and the global regulator Lrp. Mol Microbiol 84: 414-427.
43. Hussein, R., and Lim, H.N. (2011) Disruption of small RNA signaling caused by competition for Hfq. Proc Natl Acad Sci USA 108: 1110-1115.
44. Iguchi, A., Thomson, N.R., Ogura, Y., Saunders, D., Ooka, T., Henderson, I.R., etal. (2009) Complete genome sequence and comparative genome analysis of enteropathogenic Escherichia coli O127:H6 strain E2348/69. J Bacteriol 191: 347-354.
45. E regulon: role in down-regulation of outer membrane proteins. J Mol Biol 364: 1-8.
46. Jones, C.H., Danese, P.N., Pinkner, J.S., Silhavy, T.J., and Hultgren, S.J. (1997) The chaperone-assisted membrane release and folding pathway is sensed by two signal transduction systems. EMBO J 16: 6394-6406.
47. Jørgensen, M.G., Nielsen, J.S., Boysen, A., Franch, T., Møller-Jensen, J., and Valentin-Hansen, P. (2012) Small regulatory RNAs control the multi-cellular adhesive lifestyle of Escherichia coli. Mol Microbiol 84: 36-50.
48. Kendall, M.M., Gruber, C.C., Rasko, D.A., Hughes, D.T., and Sperandio, V. (2011) Hfq virulence regulation in enterohemorrhagic Escherichia coli O157:H7 strain 86-24. J Bacteriol 193: 6843-6851.
49. Kulesus, R.R., Diaz-Perez, K., Slechta, E.S., Eto, D.S., and Mulvey, M.A. (2008) Impact of the RNA chaperone Hfq on the fitness and virulence potential of uropathogenic Escherichia coli. Infect Immun 76: 3019-3026.
50. Leuko, S., and Raivio, T.L. (2012) Mutations that impact the enteropathogenic Escherichia coli (EPEC) Cpx envelope stress response attenuate virulence in Galleria mellonella. Infect Immun 80: 3077-3085.
51. Lobos, S.R., and Mora, G.C. (1991) Alteration in the electrophoretic mobility of OmpC due to variations in the ammonium persulfate concentration in sodium dodecyl sulfate-polyacrylamide gel electrophoresis. Electrophoresis 12: 448-450.
52. Ma, Q., and Wood, T.K. (2009) OmpA influences Escherichia coli biofilm formation by repressing cellulose production through the CpxRA two-component system. Environ Microbiol 11: 2735-2746.
53. McEwen, J., and Silverman, P. (1980) Chromosomal mutations of Escherichia coli that alter expression of conjugative plasmid functions. Proc Natl Acad Sci USA 77: 513-517.
54. MacRitchie, D.M., Ward, J.D., Nevesinjac, A.Z., and Raivio, T.L. (2008) Activation of the Cpx envelope stress response down-regulates expression of several locus of enterocyte effacement-encoded genes in enteropathogenic Escherichia coli. Infect Immun 76: 1465-1475.
55. Mandin, P., and Gottesman, S. (2010) Integrating anaerobic/aerobic sensing and the general stress response through the ArcZ small RNA. EMBO J 29: 3094-3107.
56. Martínez-Laguna, Y., Calva, E., and Puente, J.L. (1999) Autoactivation and environmental regulation of bfpT expression, the gene coding for the transcriptional activator of bfpA in enteropathogenic Escherichia coli. Mol Microbiol 33: 153-166.
57. E, an Escherichia coli heat-inducible σ-factor, is modulated by expression of outer membrane proteins. Genes Dev 7: 2618-2628.
58. Mellies, J.L., Barron, A.M.S., and Carmona, A.M. (2007) Enteropathogenic and enterohemorrhagic Escherichia coli virulence gene regulation. Infect Immun 75: 4199-4210.
59. Mika, F., Busse, S., Possling, A., Berkholz, J., Tschowri, N., Sommerfeldt, N., etal. (2012) Targeting of csgD by the small regulatory RNA RprA links stationary phase, biofilm formation and cell envelope stress in Escherichia coli. Mol Microbiol 84: 51-65.
60. Mileykovskaya, E., and Dowhan, W. (1997) The Cpx two-component signal transduction pathway is activated in Escherichia coli mutant strains lacking phosphatidylethanolamine. J Bacteriol 179: 1029-1034.
61. E (RpoE) heat-shock transcription-factor activity by the RseA, RseB and RseC proteins. Mol Microbiol 24: 355-371.
62. Moon, K., and Gottesman, S. (2011) Competition among Hfq-binding small RNAs in Escherichia coli. Mol Microbiol 82: 1545-1562.
63. Muffler, A., Fischer, D., and Hengge-Aronis, R. (1996) The RNA-binding protein HF-I, known as a host factor for phage Qbeta RNA replication, is essential for rpoS translation in Escherichia coli. Genes Dev 10: 1143-1151.
64. Nakayama, S., and Watanabe, H. (1995) Involvement of cpxA, a sensor of a two-component regulatory system, in the pH-dependent regulation of expression of Shigella sonnei virF gene. J Bacteriol 177: 5062-5069.
65. Nevesinjac, A.Z., and Raivio, T.L. (2005) The Cpx envelope stress response affects expression of the type IV bundle-forming pili of enteropathogenic Escherichia coli. J Bacteriol 187: 672-686.
66. Opdyke, J.A., Kang, J.-G., and Storz, G. (2004) GadY, a small-RNA regulator of acid response genes in Escherichia coli. J Bacteriol 186: 6698-6705.
67. E-dependent small RNAs of Salmonella respond to membrane stress by accelerating global omp mRNA decay. Mol Microbiol 62: 1674.
68. Papenfort, K., Said, N., Welsink, T., Lucchini, S., Hinton, J.C., and Vogel, J. (2009) Specific and pleiotropic patterns of mRNA regulation by ArcZ, a conserved, Hfq-dependent small RNA. Mol Microbiol 74: 139-158.
69. Papenfort, K., Podkaminski, D., Hinton, J.C.D., and Vogel, J. (2012) The ancestral SgrS RNA discriminates horizontally acquired Salmonella mRNAs through a single G-U wobble pair. Proc Natl Acad Sci USA 109: E757-E764.
70. Peters, J.E., Thate, T.E., and Craig, N.L. (2003) Definition of the Escherichia coli MC4100 genome by use of a DNA array. J Bacteriol 185: 2017-2021.
71. Pogliano, J., Lynch, A.S., Belin, D., Lin, E.C., and Beckwith, J. (1997) Regulation of Escherichia coli cell envelope proteins involved in protein folding and degradation by the Cpx two-component system. Genes Dev 11: 1169-1182.
72. Price, N.L., and Raivio, T.L. (2009) Characterization of the Cpx regulon in Escherichia coli strain MC4100. J Bacteriol 191: 1798-1815.
73. Prigent-Combaret, C., Brombacher, E., Vidal, O., Ambert, A., Lejeune, P., Landini, P., and Dorel, C. (2001) Complex regulatory network controls initial adhesion and biofilm formation in Escherichia coli via regulation of the csgD gene. J Bacteriol 183: 7213-7223.
74. Puente, J.L., Bieber, D., Ramer, S.W., Murray, W., and Schoolnik, G.K. (1996) The bundle-forming pili of enteropathogenic Escherichia coli: transcriptional regulation by environmental signals. Mol Microbiol 20: 87-100.
75. Quan, S., Koldewey, P., Tapley, T., Kirsch, N., Ruane, K.M., Pfizenmaier, J., etal. (2011) Genetic selection designed to stabilize proteins uncovers a chaperone called Spy. Nat Struct Mol Biol 18: 262-269.
76. 24) heat shock sigma factor of Escherichia coli. EMBO J 14: 1043-1055.
77. Raivio, T.L., Popkin, D.L., and Silhavy, T.J. (1999) The Cpx envelope stress response is controlled by amplification and feedback inhibition. J Bacteriol 181: 5263-5272.
78. Raivio, T.L., Leblanc, S.K.D., and Price, N.L. (2013) The Escherichia coli Cpx envelope stress response regulates genes of diverse function that impact antibiotic resistance and membrane integrity. J Bacteriol 195: 2755-2767.
79. Rasmussen, A.A., Eriksen, M., Gilany, K., Udesen, C., Franch, T., Petersen, C., and Valentin-Hansen, P. (2005) Regulation of ompA mRNA stability: the role of a small regulatory RNA in growth phase-dependent control. Mol Microbiol 58: 1421-1429.
80. E regulon identified by a two-plasmid system. FEMS Microbiol Lett 225: 1-7.
81. E stress response in related genomes. PLoS Biol 4: e2.
82. E, in Escherichia coli. EMBO J 14: 1032-1042.
83. Shakhnovich, E.A., Davis, B.M., and Waldor, M.K. (2009) Hfq negatively regulates type III secretion in EHEC and several other pathogens. Mol Microbiol 74: 347-363.
84. Shin, S., Castanie-Cornet, M.P., Foster, J.W., Crawford, J.A., Brinkley, C., and Kaper, J.B. (2001) An activator of glutamate decarboxylase genes regulates the expression of enteropathogenic Escherichia coli virulence genes through control of the plasmid-encoded regulator, Per. Mol Microbiol 41: 1133-1150.
85. Silhavy, T.J., and Berman, M.L. (1984) Experiments with Gene Fusions. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
86. Simonsen, K.T., Nielsen, G., Bjerrum, J.V., Kruse, T., Kallipolitis, B.H., and Møller-Jensen, J. (2011) A role for the RNA chaperone Hfq in controlling adherent-invasive Escherichia coli colonization and virulence. PLoS ONE 6: e16387.
87. Sittka, A., Lucchini, S., Papenfort, K., Sharma, C.M., Rolle, K., Binnewies, T.T., etal. (2008) Deep sequencing analysis of small noncoding RNA and mRNA targets of the global post-transcriptional regulator, Hfq. PLoS Genet 4: e1000163.
88. Smith, S.G.J., Mahon, V., Lambert, M.A., and Fagan, R.P. (2007) A molecular Swiss army knife: OmpA structure, function and expression. FEMS Microbiol Lett 273: 1-11.
89. Storz, G., Vogel, J., and Wassarman, K.M. (2011) Regulation by small RNAs in bacteria: expanding frontiers. Mol Cell 43: 880-891.
90. Thomason, M.K., Fontaine, F., De Lay, N., and Storz, G. (2012) A small RNA that regulates motility and biofilm formation in response to changes in nutrient availability in Escherichia coli. Mol Microbiol 84: 17-35.
91. E regulates and is regulated by a small RNA in Escherichia coli. J Bacteriol 189: 4243-4256.
92. Tobe, T., Schoolnik, G.K., Sohel, I., Bustamante, V.H., and Puente, J.L. (1996) Cloning and characterization of bfpTVW, genes required for the transcriptional activation of bfpA in enteropathogenic Escherichia coli. Mol Microbiol 21: 963-975.
93. Tsui, H.C., Leung, H.C., and Winkler, M.E. (1994) Characterization of broadly pleiotropic phenotypes caused by an hfq insertion mutation in Escherichia coli K-12. Mol Microbiol 13: 35-49.
94. Udekwu, K.I., Darfeuille, F., Vogel, J., Reimegård, J., Holmqvist, E., and Wagner, E.G.H. (2005) Hfq-dependent regulation of OmpA synthesis is mediated by an antisense RNA. Genes Dev 19: 2355-2366.
95. Vanmaele, R.P., and Armstrong, G.D. (1997) Effect of carbon source on localized adherence of enteropathogenic Escherichia coli. Infect Immun 65: 1408-1413.
96. Vogel, J., and Luisi, B.F. (2011) Hfq and its constellation of RNA. Nat Rev Microbiol 9: 578-589.
97. Vogel, J., and Papenfort, K. (2006) Small non-coding RNAs and the bacterial outer membrane. Curr Opin Microbiol 9: 605-611.
98. Vogt, S.L., and Raivio, T.L. (2012) Just scratching the surface: an expanding view of the Cpx envelope stress response. FEMS Microbiol Lett 326: 2-11.
99. Vogt, S.L., Nevesinjac, A.Z., Humphries, R., Donnenberg, M.S., Armstrong, G.D., and Raivio, T.L. (2010) The Cpx envelope stress response both facilitates and inhibits elaboration of the enteropathogenic Escherichia coli bundle-forming pilus. Mol Microbiol 76: 1095-1110.
100. Vogt, S.L., Acosta, N., Wong, J.L., Wang, J., and Raivio, T.L. (2012) The CpxAR two-component system regulates a complex envelope stress response in Gram negative bacteria. In Two Component Systems in Bacteria. Gross, R., and Beier, D. (eds). Wymondham, UK: Horizon Scientific Press, pp. 231-267.
101. Vytvytska, O., Moll, I., Kaberdin, V.R., von Gabain, A., and Bläsi, U. (2000) Hfq (HF1) stimulates ompA mRNA decay by interfering with ribosome binding. Genes Dev 14: 1109-1118.
102. Walsh, N.P., Alba, B.M., Bose, B., Gross, C.A., and Sauer, R.T. (2003) OMP peptide signals initiate the envelope-stress response by activating DegS protease via relief of inhibition mediated by its PDZ domain. Cell 113: 61-71.
103. Zhang, A., Altuvia, S., Tiwari, A., Argaman, L., Hengge-Aronis, R., and Storz, G. (1998) The OxyS regulatory RNA represses rpoS translation and binds the Hfq (HF-I) protein. EMBO J 17: 6061-6068.
104. Zhou, X., Keller, R., Volkmer, R., Krauss, N., Scheerer, P., and Hunke, S. (2011) Structural basis for two-component system inhibition and pilus sensing by the auxiliary CpxP protein. J Biol Chem 286: 9805-9814.