Multiple envelope stress response pathways are activated in an Escherichia coli strain with mutations in two members of the deda membrane protein family

Journal of Bacteriology

Volumn 195, Issue 1, 2013, Pages 12-24

  Sikdar, Rakesh ^a   Simmons, Angelica R ^a   Doerrler, William T ^a  

^a LOUISIANA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DEDA PROTEIN; MEMBRANE PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL CELL; BACTERIAL GROWTH; BACTERIAL MEMBRANE; BACTERIAL MUTATION; CELL DIVISION; CELL GROWTH; CELL STRESS; CONTROLLED STUDY; ESCHERICHIA COLI; GENE DELETION; NONHUMAN; PH; PLASMID; PRIORITY JOURNAL; PROTEIN EXPRESSION; TEMPERATURE SENSITIVITY;

CARRIER PROTEINS; CELL MEMBRANE; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; MEMBRANE PROTEINS; MULTIGENE FAMILY; MUTATION; PLASMIDS; STRESS, PHYSIOLOGICAL;

ESCHERICHIA COLI;

EID: 84872012492     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00762-12     Document Type: Article

References (81)

1. Elofsson A, von Heijne G. 2007. Membrane protein structure: prediction vs reality. Annu. Rev. Biochem. 76:125-140.
2. Khafizov K, Staritzbichler R, Stamm M, Forrest LR. 2010. A study of the evolution of inverted-topology repeats from LeuT-fold transporters using AlignMe. Biochemistry 49:10702-10713.
3. Baba T, Ara T, Hasegawa M, Takai Y, Okumura Y, Baba M, Datsenko KA, Tomita M, Wanner BL, Mori H. 2006. Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection.Mol. Syst. Biol. 2:2006.0008. doi:10.1038/msb4100050.
4. Thompkins K, Chattopadhyay B, Xiao Y, Henk MC, Doerrler WT.2008. Temperature sensitivity and cell division defects in an Escherichia coli strain with mutations in yghB and yqjA, encoding related and conserved inner membrane proteins. J. Bacteriol. 190:4489-4500.
5. Sikdar R, Doerrler WT. 2010. Inefficient Tat-dependent export of periplasmic amidases in an Escherichia coli strain with mutations in two DedA family genes. J. Bacteriol. 192:807-818.
6. Lee PA, Tullman-Ercek D, Georgiou G. 2006. The bacterial twinarginine translocation pathway. Annu. Rev. Microbiol. 60:373-395.
7. Boughner LA, Doerrler WT. 2012. Multiple deletions reveal the essentiality of the DedA membrane protein family in Escherichia coli. Microbiology 158(Pt 5):1162-1171.
8. Fraser CM, Casjens S, Huang WM, Sutton GG, Clayton R, Lathigra R, White O, Ketchum KA, Dodson R, Hickey EK, Gwinn M, Dougherty B, Tomb JF, Fleischmann RD, Richardson D, Peterson J, Kerlavage AR, Quackenbush J, Salzberg S, Hanson M, van Vugt R, Palmer N, Adams MD, Gocayne J, Weidman J, Utterback T, Watthey L, McDonald L, Artiach P, Bowman C, Garland S, Fuji C, Cotton MD, Horst K, Roberts K, Hatch B, Smith HO, Venter JC. 1997. Genomic sequence of a Lyme disease spirochaete, Borrelia burgdorferi. Nature 390:580-586.
9. Liang FT, Xu Q, Sikdar R, Xiao Y, Cox JS, Doerrler WT. 2010. BB0250 of Borrelia burgdorferi is a conserved and essential inner membrane protein required for cell division. J. Bacteriol. 192:6105-6115.
10. Dilks K, Rose RW, Hartmann E, Pohlschroder M. 2003. Prokaryotic utilization of the twin-arginine translocation pathway: a genomic survey. J. Bacteriol. 185:1478-1483.
11. Ize B, Stanley NR, Buchanan G, Palmer T. 2003. Role of the Escherichia coli Tat pathway in outer membrane integrity. Mol. Microbiol. 48:1183-1193.
12. Sargent F, Bogsch EG, Stanley NR, Wexler M, Robinson C, Berks BC, Palmer T. 1998. Overlapping functions of components of a bacterial Secindependent protein export pathway. EMBO J. 17:3640-3650.
13. Stanley NR, Findlay K, Berks BC, Palmer T. 2001. Escherichia coli strains blocked in Tat-dependent protein export exhibit pleiotropic defects in the cell envelope. J. Bacteriol. 183:139-144.
14. Bury-Mone S, Nomane Y, Reymond N, Barbet R, Jacquet E, Imbeaud S, Jacq A, Bouloc P. 2009. Global analysis of extracytoplasmic stress signaling in Escherichia coli. PLoS Genet. 5:e1000651. doi:10.1371/journal.pgen.1000651.
15. Connolly L, De Las Penas A, Alba BM, Gross CA. 1997. The response to extracytoplasmic stress in Escherichia coli is controlled by partially overlapping pathways. Genes Dev. 11:2012-2021.
16. Raivio TL, Silhavy TJ. 1999. The sigmaE and Cpx regulatory pathways:overlapping but distinct envelope stress responses. Curr. Opin. Microbiol.2:159-165.
17. Vogt SL, Raivio TL. 2012. Just scratching the surface: an expanding view of the Cpx envelope stress response. FEMS Microbiol. Lett. 326:2-11.
18. Dartigalongue C, Missiakas D, Raina S. 2001. Characterization of the Escherichia coli sigma E regulon. J. Biol. Chem. 276:20866-20875.
19. Price NL, Raivio TL. 2009. Characterization of the Cpx regulon in Escherichia coli strain MC4100. J. Bacteriol. 191:1798-1815.
20. Otto K, Silhavy TJ. 2002. Surface sensing and adhesion of Escherichia coli controlled by the Cpx-signaling pathway. Proc. Natl. Acad. Sci. U. S. A.99:2287-2292.
21. De Wulf P, Kwon O, Lin EC. 1999. The CpxRA signal transduction system of Escherichia coli: growth-related autoactivation and control of unanticipated target operons. J. Bacteriol. 181:6772-6778.
22. Wolfe AJ, Parikh N, Lima BP, Zemaitaitis B. 2008. Signal integration by the two-component signal transduction response regulator CpxR. J. Bacteriol.190:2314-2322.
23. Engl C, Beek AT, Bekker M, de Mattos JT, Jovanovic G, Buck M. 2011.Dissipation of proton motive force is not sufficient to induce the phage shock protein response in Escherichia coli. Curr. Microbiol. 62:1374-1385.
24. Joly N, Engl C, Jovanovic G, Huvet M, Toni T, Sheng X, Stumpf MP, Buck M. 2010. Managing membrane stress: the phage shock protein (Psp)response, from molecular mechanisms to physiology. FEMS Microbiol.Rev. 34:797-827.
25. Jovanovic G, Lloyd LJ, Stumpf MP, Mayhew AJ, Buck M. 2006. Induction and function of the phage shock protein extracytoplasmic stress response in Escherichia coli. J. Biol. Chem. 281:21147-21161.
26. Jovanovic G, Engl C, Mayhew AJ, Burrows PC, Buck M. 2010. Properties of the phage-shock-protein (Psp) regulatory complex that govern signal transduction and induction of the Psp response in Escherichia coli. Microbiology 156:2920-2932.
27. Rowley G, Spector M, Kormanec J, Roberts M. 2006. Pushing the envelope: extracytoplasmic stress responses in bacterial pathogens. Nat.Rev. Microbiol. 4:383-394.
28. Kobayashi R, Suzuki T, Yoshida M. 2007. Escherichia coli phage-shock protein A (PspA) binds to membrane phospholipids and repairs proton leakage of the damaged membranes. Mol. Microbiol. 66:100-109.
29. Ebel W, Vaughn GJ, Peters HK, 3rd, Trempy JE. 1997. Inactivation of mdoH leads to increased expression of colanic acid capsular polysaccharide in Escherichia coli. J. Bacteriol. 179:6858-6861.
30. Majdalani N, Gottesman S. 2005. The Rcs phosphorelay: a complex signal transduction system. Annu. Rev. Microbiol. 59:379-405.
31. Parker CT, Kloser AW, Schnaitman CA, Stein MA, Gottesman S, Gibson BW. 1992. Role of the rfaG and rfaP genes in determining the lipopolysaccharide core structure and cell surface properties of Escherichia coli K-12. J. Bacteriol. 174:2525-2538.
32. Shiba Y, Yokoyama Y, Aono Y, Kiuchi T, Kusaka J, Matsumoto K, Hara H. 2004. Activation of the Rcs signal transduction system is responsible for the thermosensitive growth defect of an Escherichia coli mutant lacking phosphatidylglycerol and cardiolipin. J. Bacteriol. 186:6526-6535.
33. Laubacher ME, Ades SE. 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.
34. Majdalani N, Hernandez D, Gottesman S. 2002. Regulation and mode of action of the second small RNA activator of RpoS translation, RprA. Mol.Microbiol. 46:813-826.
35. Huang YH, Ferrieres L, Clarke DJ. 2006. The role of the Rcs phosphorelay in Enterobacteriaceae. Res. Microbiol. 157:206-212.
36. Castanie-Cornet MP, Cam K, Jacq A. 2006. RcsF is an outer membrane lipoprotein involved in the RcsCDB phosphorelay signaling pathway in Escherichia coli. J. Bacteriol. 188:4264-4270.
37. Hirakawa H, Inazumi Y, Masaki T, Hirata T, Yamaguchi A. 2005.Indole induces the expression of multidrug exporter genes in Escherichia coli. Mol. Microbiol. 55:1113-1126.
38. Nishino K, Honda T, Yamaguchi A. 2005. Genome-wide analyses of Escherichia coli gene expression responsive to the BaeSR two-component regulatory system. J. Bacteriol. 187:1763-1772.
39. Krulwich TA, Sachs G, Padan E. 2011. Molecular aspects of bacterial pH sensing and homeostasis. Nat. Rev. Microbiol. 9:330-343.
40. Edgar R, Bibi E. 1997. MdfA, an Escherichia coli multidrug resistance protein with an extraordinarily broad spectrum of drug recognition. J.Bacteriol. 179:2274-2280.
41. Lewinson O, Adler J, Poelarends GJ, Mazurkiewicz P, Driessen AJ, Bibi E. 2003. The Escherichia coli multidrug transporter MdfA catalyzes both electrogenic and electroneutral transport reactions. Proc. Natl. Acad. Sci.U. S. A. 100:1667-1672.
42. Lewinson O, Padan E, Bibi E. 2004. Alkalitolerance: a biological function for a multidrug transporter in pH homeostasis. Proc. Natl. Acad. Sci.U. S. A. 101:14073-14078.
43. Paulsen IT, Brown MH, Skurray RA. 1996. Proton-dependent multidrug efflux systems. Microbiol. Rev. 60:575-608.
44. Lipinska B, King J, Ang D, Georgopoulos C. 1988. Sequence analysis and transcriptional regulation of the Escherichia coli grpE gene, encoding a heat shock protein. Nucleic Acids Res. 16:7545-7562.
45. Bernhardt TG, de Boer PA. 2003. The Escherichia coli amidase AmiC is a periplasmic septal ring component exported via the twin-arginine transport pathway. Mol. Microbiol. 48:1171-1182.
46. Engl C, Jovanovic G, Lloyd LJ, Murray H, Spitaler M, Ying L, Errington J, Buck M. 2009. In vivo localizations of membrane stress controllers PspA and PspG in Escherichia coli. Mol. Microbiol. 73:382-396.
47. Shimohata N, Chiba S, Saikawa N, Ito K, Akiyama Y. 2002. The Cpx stress response system of Escherichia coli senses plasma membrane proteins and controls HtpX, a membrane protease with a cytosolic active site. Genes Cells 7:653-662.
48. Cherepanov PP, Wackernagel W. 1995. Gene disruption in Escherichia coli: TcR and KmR cassettes with the option of Flp-catalyzed excision of the antibiotic-resistance determinant. Gene 158:9-14.
49. Datsenko KA, Wanner BL. 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.
50. Miller JH. 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
51. Doerrler WT, Raetz CRH. 2002. ATPase activity of the MsbA lipid flippase of Escherichia coli. J. Biol. Chem. 277:36697-36705.
52. Hiratsu K, Amemura M, Nashimoto H, Shinagawa H, Makino K. 1995. The rpoE gene of Escherichia coli, which encodes sigma E, is essential for bacterial growth at high temperature. J. Bacteriol. 177:2918-2922.
53. Pogliano J, Dong JM, De Wulf P, Furlong D, Boyd D, Losick R, Pogliano K, Lin EC. 1998. Aberrant cell division and random FtsZ ring positioning in Escherichia coli cpxA, mutants. J. Bacteriol. 180:3486-3490.
54. Tsuchido T, VanBogelen RA, Neidhardt FC. 1986. Heat shock response in Escherichia coli influences cell division. Proc. Natl. Acad. Sci. U. S. A.83:6959-6963.
55. Guisbert E, Yura T, Rhodius VA, Gross CA. 2008. Convergence of molecular, modeling, and systems approaches for an understanding of the Escherichia coli heat shock response. Microbiol. Mol. Biol. Rev. 72:545-554.
56. Duguay AR, Silhavy TJ. 2004. Quality control in the bacterial periplasm.Biochim. Biophys. Acta 1694:121-134.
57. Rouviere PE, De Las Penas A, Mecsas J, Lu CZ, Rudd KE, Gross CA.1995. rpoE, the gene encoding the second heat-shock sigma factor, sigma E, in Escherichia coli. EMBO J. 14:1032-1042.
58. Danese PN, Silhavy TJ. 1997. The sigma(E) and the Cpx signal transduction systems control the synthesis of periplasmic protein-folding enzymes in Escherichia coli. Genes Dev. 11:1183-1193.
59. Lipinska B, Fayet O, Baird L, Georgopoulos C. 1989. Identification,characterization, and mapping of the Escherichia coli htrA gene, whose product is essential for bacterial growth only at elevated temperatures. J.Bacteriol. 171:1574-1584.
60. Strauch KL, Johnson K, Beckwith J. 1989. Characterization of degP, a gene required for proteolysis in the cell envelope and essential for growth of Escherichia coli at high temperature. J. Bacteriol. 171:2689-2696.
61. Danese PN, Silhavy TJ. 1998. CpxP, a stress-combative member of the Cpx regulon. J. Bacteriol. 180:831-839.
62. Mileykovskaya E, Dowhan W. 1997. The Cpx two-component signal transduction pathway is activated in Escherichia coli mutant strains lacking phosphatidylethanolamine. J. Bacteriol. 179:1029-1034.
63. DeLisa MP, Lee P, Palmer T, Georgiou G. 2004. Phage shock protein PspA of Escherichia coli relieves saturation of protein export via the Tat pathway. J. Bacteriol. 186:366-373.
64. Kleerebezem M, Crielaard W, Tommassen J. 1996. Involvement of stress protein PspA (phage shock protein A) of Escherichia coli in maintenance of the protonmotive force under stress conditions. EMBO J. 15:162-171.
65. Kleerebezem M, Tommassen J. 1993. Expression of the pspA gene stimulates efficient protein export in Escherichia coli. Mol. Microbiol. 7:947-956.
66. Alder NN, Theg SM. 2003. Energetics of protein transport across biological membranes. A study of the thylakoid DeltapH-dependent/cpTat pathway. Cell 112:231-242.
67. Bageshwar UK, Musser SM. 2007. Two electrical potential-dependent steps are required for transport by the Escherichia coli Tat machinery. J. Cell Biol. 179:87-99.
68. Palmer T, Berks BC. 2012. The twin-arginine translocation (Tat) protein export pathway. Nat. Rev. Microbiol. 10:483-496.
69. Doerrler WT, Raetz CRH. 2005. Loss of outer membrane proteins without inhibition of lipid export in an Escherichia coli YaeT mutant. J. Biol.Chem. 280:27679-27687.
70. Sledjeski D, Gottesman S. 1995. A small RNA acts as an antisilencer of the H-NS-silenced rcsA gene of Escherichia coli. Proc. Natl. Acad. Sci. U. S. A.92:2003-2007.
71. Chen MH, Takeda S, Yamada H, Ishii Y, Yamashino T, Mizuno T. 2001.Characterization of the RcsC-YojN-RcsB phosphorelay signaling pathway involved in capsular synthesis in Escherichia coli. Biosci. Biotechnol.Biochem. 65:2364-2367.
72. Nagahama H, Oshima T, Mori H, Matsumoto K, Hara H. 2007. Hyperexpression of the osmB gene in an acidic phospholipid-deficient Escherichia coli mutant. J. Gen. Appl. Microbiol. 53:143-151.
73. Small P, Blankenhorn D, Welty D, Zinser E, Slonczewski JL. 1994. Acid and base resistance in Escherichia coli and Shigella flexneri: role of rpoS and growth pH. J. Bacteriol. 176:1729-1737.
74. Bulygin VV, Vinogradov AD. 1991. Interaction of Mg2 with F0.F1 mitochondrial ATPase as related to its slow active/inactive transition.Biochem. J. 276(Pt 1):149-156.
75. Ye JJ, Du J, Lin ZH. 1989. The effect of Mg2 on mitochondrial F0.F1 ATPase and characteristics of the nucleotide binding sites. Biochem. Int.19:1317-1321.
76. Mager T, Rimon A, Padan E, Fendler K. 2011. Transport mechanism and pH regulation of the Na/H antiporter NhaA from Escherichia coli: an electrophysiological study. J. Biol. Chem. 286:23570-23581.
77. Padan E, Bibi E, Ito M, Krulwich TA. 2005. Alkaline pH homeostasis in bacteria: new insights. Biochim. Biophys. Acta 1717:67-88.
78. Ledgham F, Quest B, Vallaeys T, Mergeay M, Coves J. 2005. A probable link between the DedA protein and resistance to selenite. Res. Microbiol.156:367-374.
79. Arai M, Liu L, Fujimoto T, Setiawan A, Kobayashi M.2011. DedA protein relates to action-mechanism of halicyclamine A, a marine spongean macrocyclic alkaloid, as an anti-dormant mycobacterial substance.Mar. Drugs 9:984-993.
80. Zechini B, Versace I. 2009. Inhibitors of multidrug resistant efflux systems in bacteria. Recent Pat. Antiinfect. Drug Discov. 4:37-50.
81. Doerrler WT, Sikdar R, Kumar S, Boughner LA. 2013. New functions for the ancient DedA membrane protein family. J. Bacteriol. 195:3-11.