Skip to content
naulon

No retraction, correction or concern found when last checked on Oct 30, 2026.

Release of outer membrane vesicles by Gram‐negative bacteria is a novel envelope stress response

Amanda J. McBroom, Meta J. Kuehn

Molecular Microbiology · 2006

doi:10.1111/j.1365-2958.2006.05522.x

Abstract

Summary Conditions that impair protein folding in the Gram‐negative bacterial envelope cause stress. The destabilizing effects of stress in this compartment are recognized and countered by a number of signal transduction mechanisms. Data presented here reveal another facet of the complex bacterial stress response, release of outer membrane vesicles. Native vesicles are composed of outer membrane and periplasmic material, and they are released from the bacterial surface without loss of membrane integrity. Here we demonstrate that the quantity of vesicle release correlates directly with the level of protein accumulation in the cell envelope. Accumulation of material occurs under stress, and is exacerbated upon impairment of the normal housekeeping and stress‐responsive mechanisms of the cell. Mutations that cause increased vesiculation enhance bacterial survival upon challenge with stressing agents or accumulation of toxic misfolded proteins. Preferential packaging of a misfolded protein mimic into vesicles for removal indicates that the vesiculation process can act to selectively eliminate unwanted material. Our results demonstrate that production of bacterial outer membrane vesicles is a fully independent, general envelope stress response. In addition to identifying a novel mechanism for alleviating stress, this work provides physiological relevance for vesicle production as a protective mechanism.

Shown for reading. Its publisher allows quoting it, not republishing it.

References 49

  1. 1.

    Ades SE. Control of the alternative sigma factor sigmaE in Escherichia coli. Curr Opin Microbiol. 2004;7:157-162.

    Not in our library10.1016/j.mib.2004.02.010

  2. 2.

    Alba BM, Gross CA. Regulation of the Escherichia coli sigma-dependent envelope stress response. Mol Microbiol. 2004;52:613-619.

    Not in our library10.1111/j.1365-2958.2003.03982.x

  3. 3.

    Alba BM, Zhong HJ, Pelayo JC, Gross CA. degS (hhoB) is an essential Escherichia coli gene whose indispensable function is to provide sigmaE activity. Mol Microbiol. 2001;40:1323-1333.

    Not in our library10.1046/j.1365-2958.2001.02475.x

  4. 4.

    Bauman SJ, Kuehn MJ. Purification of outer membrane vesicles from Pseudomonas aeruginosa and their activation of an IL-8 response. Microbes Infect. 2006;8:2400-2408.

    Not in our library10.1016/j.micinf.2006.05.001

  5. 5.

    Beveridge TJ. Structures of gram-negative cell walls and their derived membrane vesicles. J Bacteriol. 1999;181:4725-4733.

    Not in our library10.1128/jb.181.16.4725-4733.1999

  6. 6.

    Bianchi AA, Baneyx F. Hyperosmotic shock induces the sigma32 and sigmaE stress regulons of Escherichia coli. Mol Microbiol. 1999;34:1029-1038.

    Not in our library10.1046/j.1365-2958.1999.01664.x

  7. 7.

    Casadaban MJ. Transposition and fusion of the lac genes to selected promoters in Escherichia coli using bacteriophage lambda and Mu. J Mol Biol. 1976;104:541-555.

    Not in our library10.1016/0022-2836(76)90119-4

  8. 8.

    Clausen T, Southan C, Ehrmann M. The HtrA family of proteases: implications for protein composition and cell fate. Mol Cell. 2002;10:443-455.

    Not in our library10.1016/s1097-2765(02)00658-5

  9. 9.

    Clayton A, Turkes A, Navabi H, Mason MD, Tabi Z. Induction of heat shock proteins in B-cell exosomes. J Cell Sci. 2005;118:3631-3638.

    Not in our library10.1242/jcs.02494

  10. 10.

    Danese PN, Snyder WB, Cosma CL, Davis LJ, Silhavy TJ. The Cpx two-component signal transduction pathway of Escherichia coli regulates transcription of the gene specifying the stress-inducible periplasmic protease, DegP. Genes Dev. 1995;9:387-398.

    Not in our library10.1101/gad.9.4.387

  11. 11.

    Danese PN, Oliver GR, Barr K, Bowman GD, Rick PD, Silhavy TJ. Accumulation of the enterobacterial common antigen lipid II biosynthetic intermediate stimulates degP transcription in Escherichia coli. J Bacteriol. 1998;180:5875-5884.

    Not in our library10.1128/jb.180.22.5875-5884.1998

  12. 12.

    Darwin AJ. The phage-shock-protein response. Mol Microbiol. 2005;57:621-628.

    Not in our library10.1111/j.1365-2958.2005.04694.x

  13. 13.

    De Las Penas A, Connolly L, Gross C. SigmaE is an essential sigma factor in Escherichia coli. J Bacteriol. 1997a;179:6862-6864.

    Not in our library10.1128/jb.179.21.6862-6864.1997

  14. 14.

    De Las Penas A, Connolly L, Gross CA. The sigmaE-mediated response to extracytoplasmic stress in Escherichia coli is transduced by RseA and RseB, two negative regulators of sigmaE. Mol Microbiol. 1997b;24:373-385.

    Not in our library10.1046/j.1365-2958.1997.3611718.x

  15. 15.

    Dorel C, Lejeune P, Rodrigue A. The Cpx system of Escherichia coli, a strategic signaling pathway for confronting adverse conditions and for settling biofilm communities? Res Microbiol. 2006;157:306-314.

    Not in our library10.1016/j.resmic.2005.12.003

  16. 16.

    Duguay AR, Silhavy TJ. Quality control in the bacterial periplasm. Biochim Biophys Acta. 2004;1694:121-134.

    Not in our library10.1016/j.bbamcr.2004.04.012

  17. 17.

    Economou A, Christie PJ, Fernandez RC, Palmer T, Plano GV, Pugsley AP. Secretion by numbers: protein traffic in prokaryotes. Mol Microbiol. 2006;62:308-319.

    Not in our library10.1111/j.1365-2958.2006.05377.x

  18. 18.

    Jovanovic G, Weiner L, Model P. Identification, nucleotide sequence, and characterization of PspF, the transcriptional activator of the Escherichia coli stress-induced psp operon. J Bacteriol. 1996;178:1936-1945.

    Not in our library10.1128/jb.178.7.1936-1945.1996

  19. 19.

    Kesty NC, Kuehn MJ. Incorporation of heterologous outer membrane and periplasmic proteins into Escherichia coli outer membrane vesicles. J Biol Chem. 2004;279:2069-2076.

    Not in our library10.1074/jbc.m307628200

  20. 20.

    Kuehn MJ, Kesty NC. Bacterial outer membrane vesicles and the host–pathogen interaction. Genes Dev. 2005;19:2645-2655.

    Not in our library10.1101/gad.1299905

  21. 21.

    McBroom AJ, Kuehn MJ, Curtiss R. Outer membrane vesicles. EcoSal – Escherichia coli and Salmonella: Cellular and Molecular Biology. 2005.

    Not in our library

  22. 22.

    McBroom AJ, Johnson AP, Vemulapalli S, Kuehn MJ. Outer membrane vesicle production by Escherichia coli is independent of membrane instability. J Bacteriol. 2006;188:5385-5392.

    Not in our library10.1128/jb.00498-06

  23. 23.

    McCarty JS, Walker GC. DnaK mutants defective in ATPase activity are defective in negative regulation of the heat shock response: expression of mutant DnaK proteins results in filamentation. J Bacteriol. 1994;176:764-780.

    Not in our library10.1128/jb.176.3.764-780.1994

  24. 24.

    Martinez MC, Tesse A, Zobairi F, Andriantsitohaina R. Shed membrane microparticles from circulating and vascular cells in regulating vascular function. Am J Physiol Heart Circ Physiol. 2005;288:H1004-H1009.

    Not in our library10.1152/ajpheart.00842.2004

  25. 25.

    Mayrand D, Grenier D. Biological activities of outer membrane vesicles. Can J Microbiol. 1989;35:607-613.

    Not in our library10.1139/m89-097

  26. 26.

    Mecsas J, Rouviere PE, Erickson JW, Donohue TJ, Gross CA. The activity of sigma E, an Escherichia coli heat-inducible sigma-factor, is modulated by expression of outer membrane proteins. Genes Dev. 1993;7:2618-2628.

    Not in our library10.1101/gad.7.12b.2618

  27. 27.

    Miller JH. Short Course in Bacterial Genetics: A Laboratory Manual and Handbook for Escherichia coli and Related Bacteria. 1992.

    Not in our library

  28. 28.

    Missiakas D, Betton JM, Raina S. New components of protein folding in extracytoplasmic compartments of Escherichia coli SurA, FkpA and Skp/OmpH. Mol Microbiol. 1996;21:871-884.

    Not in our library10.1046/j.1365-2958.1996.561412.x

  29. 29.

    Missiakas D, Mayer MP, Lemaire M, Georgopoulos C, Raina S. Modulation of the Escherichia coli sigmaE (RpoE) heat-shock transcription-factor activity by the RseA, RseB and RseC proteins. Mol Microbiol. 1997;24:355-371.

    Not in our library10.1046/j.1365-2958.1997.3601713.x

  30. 30.

    Mogensen JE, Otzen DE. Interactions between folding factors and bacterial outer membrane proteins. Mol Microbiol. 2005;57:326-346.

    Not in our library10.1111/j.1365-2958.2005.04674.x

  31. 31.

    Nishino K, Honda T, Yamaguchi A. Genome-wide analyses of Escherichia coli gene expression responsive to the BaeSR two-component regulatory system. J Bacteriol. 2005;187:1763-1772.

    Not in our library10.1128/jb.187.5.1763-1772.2005

  32. 32.

    Pilzer D, Gasser O, Moskovich O, Schifferli JA, Fishelson Z. Emission of membrane vesicles: roles in complement resistance, immunity and cancer. Springer Semin Immunopathol. 2005;27:375-387.

    Not in our library10.1007/s00281-005-0004-1

  33. 33.

    Raffa RG, Raivio TL. A third envelope stress signal transduction pathway in Escherichia coli. Mol Microbiol. 2002;45:1599-1611.

    Not in our library10.1046/j.1365-2958.2002.03112.x

  34. 34.

    Raivio TL. Envelope stress responses and Gram-negative bacterial pathogenesis. Mol Microbiol. 2005;56:1119-1128.

    Not in our library10.1111/j.1365-2958.2005.04625.x

  35. 35.

    Raivio TL, Popkin DL, Silhavy TJ. The Cpx envelope stress response is controlled by amplification and feedback inhibition. J Bacteriol. 1999;181:5263-5272.

    Not in our library10.1128/jb.181.17.5263-5272.1999

  36. 36.

    Raivio TL, Laird MW, Joly JC, Silhavy TJ. Tethering of CpxP to the inner membrane prevents spheroplast induction of the cpx envelope stress response. Mol Microbiol. 2000;37:1186-1197.

    Not in our library10.1046/j.1365-2958.2000.02074.x

  37. 37.
  38. 38.

    Rouviere PE, Gross CA. SurA, a periplasmic protein with peptidyl-prolyl isomerase activity, participates in the assembly of outer membrane porins. Genes Dev. 1996;10:3170-3182.

    Not in our library10.1101/gad.10.24.3170

  39. 39.

    Ruiz N, Silhavy TJ. Sensing external stress: watchdogs of the Escherichia coli cell envelope. Curr Opin Microbiol. 2005;8:122-126.

    Not in our library10.1016/j.mib.2005.02.013

  40. 40.

    Silhavy TJ, Berman ML, Enquist LW. Experiments with Gene Fusions. 1984.

    Not in our library

All 49 references

Cited by papers we hold 33

and 13 more

Reads

Read by people on this page

None yet.

Checked or read by AI through naulon

None yet.

A person counts once a day per paper. We keep no cookie and no address: a reader is a hash that changes every day. Any month under five reads shows no number.

Are you an author?

Is this your paper?

Claim it to add your note and be paid when agents cite it. Free.