No metrics data to plot.
The attempt to load metrics for this article has failed.
The attempt to plot a graph for these metrics has failed.

EcoSal Plus

Domain 4:

Synthesis and Processing of Macromolecules

Assembly of Outer Membrane β-Barrel Proteins: the Bam Complex

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.
  • Authors: Juliana C. Malinverni1, and Thomas J. Silhavy2
  • Editors: James M. Slauch3, Harris Bernstein4
    Affiliations: 1: Department of Molecular Biology, Princeton University, Princeton NJ 08544; 2: Department of Molecular Biology, Princeton University, Princeton NJ 08544; 3: The Schoold of Molecular and Cellular Biology, University of Illinois at Urbana-Champaign, Urbana, IL; 4: National Institutes of Health, Bethesda, MD
  • Received 06 January 2010 Accepted 22 March 2010 Published 26 March 2011
  • Address correspondence to Thomas J. Silhavy [email protected]
image of Assembly of Outer Membrane β-Barrel Proteins: the Bam Complex
    Preview this reference work article:
    Zoom in

    Assembly of Outer Membrane β-Barrel Proteins: the Bam Complex, Page 1 of 2

    | /docserver/preview/fulltext/ecosalplus/4/2/4_3_8_module-1.gif /docserver/preview/fulltext/ecosalplus/4/2/4_3_8_module-2.gif
  • Abstract:

    The major class of integral proteins found in the outer membrane (OM) of and adopt a β-barrel conformation (OMPs). OMPs are synthesized in the cytoplasm with a typical signal sequence at the amino terminus, which directs them to the secretion machinery (SecYEG) located in the inner membrane for translocation to the periplasm. Chaperones such as SurA, or DegP and Skp, escort these proteins across the aqueous periplasm protecting them from aggregation. The chaperones then deliver OMPs to a highly conserved outer membrane assembly site termed the Bam complex. In , the Bam complex is composed of an essential OMP, BamA, and four associated OM lipoproteins, BamBCDE, one of which, BamD, is also essential. Here we provide an overview of what we know about the process of OMP assembly and outline the various hypotheses that have been proposed to explain how proteins might be integrated into the asymmetric OM lipid bilayer in an environment that lacks obvious energy sources. In addition, we describe the envelope stress responses that ensure the fidelity of OM biogenesis and how factors, such as phage and certain toxins, have coopted this essential machine to gain entry into the cell.

  • Citation: Malinverni J, Silhavy T. 2011. Assembly of Outer Membrane β-Barrel Proteins: the Bam Complex, EcoSal Plus 2011; doi:10.1128/ecosalplus.4.3.8

Article Version

An updated version has been published for this content:
Outer Membrane Protein Insertion by the β-barrel Assembly Machine


1. Driessen AJ, Nouwen N. 2008. Protein translocation across the bacterial cytoplasmic membrane. Annu Rev Biochem 77:643–667. [PubMed][CrossRef]
2. Juncker AS, Willenbrock H, Von Heijne G, Brunak S, Nielsen H, Krogh A. 2003. Prediction of lipoprotein signal peptides in Gram-negative bacteria. Protein Sci 12:1652–1662. [PubMed][CrossRef]
3. Paetzel M, Karla A, Strynadka NC, Dalbey RE. 2002. Signal peptidases. Chem Rev 102:4549–4580. [PubMed][CrossRef]
4. Seydel A, Gounon P, Pugsley AP. 1999. Testing the ‘+2 rule’ for lipoprotein sorting in the Escherichia coli cell envelope with a new genetic selection. Mol Microbiol 34:810–821. [PubMed][CrossRef]
5. Wülfing C, Plückthun A. 1994. Protein folding in the periplasm of Escherichia coli. Mol Microbiol 12:685–692. [PubMed][CrossRef]
6. Kamio Y, Nikaido H. 1976. Outer membrane of Salmonella typhimurium: accessibility of phospholipid head groups to phospholipase c and cyanogen bromide activated dextran in the external medium. Biochemistry 15:2561–2570. [PubMed][CrossRef]
7. Nikaido H. 2003. Molecular basis of bacterial outer membrane permeability revisited. Microbiol Mol Biol Rev 67:593–656. [PubMed][CrossRef]
8. Nikaido H. 2005. Restoring permeability barrier function to outer membrane. Chem Biol 12:507–509. [PubMed][CrossRef]
9. Ishinaga M, Kanamoto R, Kito M. 1979. Distribution of phospholipid molecular species in outer and cytoplasmic membrane of Escherichia coli. J Biochem 86:161–165.[PubMed]
10. Osborn MJ, Gander JE, Parisi E, Carson J. 1972. Mechanism of assembly of the outer membrane of Salmonella typhimurium. Isolation and characterization of cytoplasmic and outer membrane. J Biol Chem 247:3962–3972.[PubMed]
11. Bocquet-Pagès C, Lazdunski C, Lazdunski A. 1981. Lipid-synthesis-dependent biosynthesis (or assembly) of major outer-membrane proteins of Escherichia coli. Eur J Biochem 118:105–111. [PubMed][CrossRef]
12. Bolla J-M, Lazdunski C, Pagès J-M. 1988. The assembly of the major outer membrane protein OmpF of Escherichia coli depends on lipid synthesis. EMBO J 7:3595–3599.[PubMed]
13. Bulieris PV, Behrens S, Holst O, Kleinschmidt JH. 2003. Folding and insertion of the outer membrane protein OmpA is assisted by the chaperone Skp and by lipopolysaccharide. J Biol Chem 278:9092–9099. [PubMed][CrossRef]
14. de Cock H, Pasveer M, Tommassen J, Bouveret E. 2001. Identification of phospholipids as new components that assist in the in vitro trimerization of a bacterial pore protein. Eur J Biochem 268:865–875. [PubMed][CrossRef]
15. de Cock H, van Blokland S, Tommassen J. 1996. In vitro insertion and assembly of outer membrane protein PhoE of Escherichia coli K-12 into the outer membrane. Role of Triton X-100. J Biol Chem 271:12885–12890. [PubMed][CrossRef]
16. Laird MW, Kloser AW, Misra R. 1994. Assembly of LamB and OmpF in deep rough lipopolysaccharide mutants of Escherichia coli K-12. J Bacteriol 176:2259–2264.[PubMed]
17. Ried G, Hindennach I, Henning U. 1990. Role of lipopolysaccharide in assembly of Escherichia coli outer membrane proteins OmpA, OmpC, and OmpF. J Bacteriol 172:6048–6053.[PubMed]
18. Sen K, Nikaido H. 1990. In vitro trimerization of OmpF porin secreted by spheroplasts of Escherichia coli. Proc Natl Acad Sci USA 87:743–747. [PubMed][CrossRef]
19. Sen K, Nikaido H. 1991. Lipopolysaccharide structure required for in vitro trimerization of Escherichia coli OmpF porin. J Bacteriol 173:926–928.[PubMed]
20. Doerrler WT, Gibbons HS, Raetz CRH. 2004. MsbA-dependent translocation of lipids across the inner membrane of Escherichia coli. J Biol Chem 279:45102–45109. [PubMed][CrossRef]
21. Polissi A, Georgopoulos C. 1996. Mutational analysis and properties of the msbA gene of Escherichia coli, coding for an essential ABC family transporter. Mol Microbiol 20:1221–1233. [PubMed][CrossRef]
22. Zhou Z, White KA, Polissi A, Georgopoulos C, Raetz CRH. 1998. Function of Escherichia coli MsbA, an essential ABC family transporter, in Lipid A and phospholipid biosynthesis. J Biol Chem 273:12466–12475. [PubMed][CrossRef]
23. Ruiz N, Kahne D, Silhavy TJ. 2009. Transport of lipopolysaccharide across the cell envelope: the long road of discovery. Nat Rev Microbiol 7:677–683. [PubMed][CrossRef]
24. Braun M, Silhavy TJ. 2002. Imp/OstA is required for cell envelope biogenesis in Escherichia coli. Mol Microbiol 45:1289–1302. [PubMed][CrossRef]
25. Ruiz N, Gronenberg LS, Kahne D, Silhavy TJ. 2008. Identification of two inner-membrane proteins required for the transport of lipopolysaccharide to the outer membrane of Escherichia coli. Proc Natl Acad Sci USA 105:5537–5542. [PubMed][CrossRef]
26. Sperandeo P, Cescutti R, Villa R, Di Benedetto C, Candia D, Deho G, Polissi A. 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. [PubMed][CrossRef]
27. Sperandeo P, Lau FK, Carpentieri A, De Castro C, Molinaro A, Deho G, Silhavy TJ, Polissi A. 2008. Functional analysis of the protein machinery required for transport of lipopolysaccharide to the outer membrane of Escherichia coli. J Bacteriol 190:4460–4469. [PubMed][CrossRef]
28. Wu T, McCandlish AC, Gronenberg LS, Chng S-S, Silhavy TJ, Kahne D. 2006. Identification of a protein complex that assembles lipopolysaccharide in the outer membrane of Escherichia coli. Proc Natl Acad Sci USA 103:11754–11759. [PubMed][CrossRef]
29. Xu Z, Knafels JD, Yoshino K. 2000. Crystal structure of the bacterial protein export chaperone secB. Nat Struct Biol 7:1172–1177. [PubMed][CrossRef]
30. Hayashi S, Wu HC. 1990. Lipoproteins in bacteria. J Bioenerg Biomembr 22:451–471. [PubMed][CrossRef]
31. Gan K, Gupta SD, Sankaran K, Schmid MB, Wu HC. 1993. Isolation and characterization of a temperature-sensitive mutant of Salmonella typhimurium defective in prolipoprotein modification. J Biol Chem 268:16544–16550.
32. Inouye S, Franceschini T, Sato M, Itakura K, Inouye M. 1983. Prolipoprotein signal peptidase of Escherichia coli requires a cysteine residue at the cleavage site. EMBO J 2:87–91.[PubMed]
33. Gupta SD, Gan K, Schmid MB, Wu HC. 1993. Characterization of a temperature-sensitive mutant of Salmonella typhimurium defective in apolipoprotein N-acyltransferase. J Biol Chem 268:16551–16556.[PubMed]
34. Jacob-Dubuisson F, Villeret V, Clantin B, Delattre AS, Saint N. 2009. First structural insights into the TpsB/Omp85 superfamily. Biol Chem 390:675–684. [PubMed][CrossRef]
35. Dong C, Beis K, Nesper J, Brunkan-LaMontagne AL, Clarke BR, Whitfield C, Naismith JH. 2006. Wza the translocon for E. coli capsular polysaccharides defines a new class of membrane protein. Nature 444:226–229. [PubMed][CrossRef]
36. Collin S, Guilvout I, Chami M, Pugsley AP. 2007. YaeT-independent multimerization and outer membrane association of secretin PulD. Mol Microbiol 64:1350–1357. [PubMed][CrossRef]
37. Guilvout I, Chami M, Engel A, Pugsley AP, Bayan N. 2006. Bacterial outer membrane secretin PulD assembles and inserts into the inner membrane in the absence of its pilotin. EMBO J 25:5241–5249. [PubMed][CrossRef]
38. Whitfield C, Naismith JH. 2008. Periplasmic export machines for outer membrane assembly. Curr Opin Struct Biol 18:466–474. [PubMed][CrossRef]
39. Drummelsmith J, Whitfield C. 2000. Translocation of group 1 capsular polysaccharide to the surface of Escherichia coli requires a multimeric complex in the outer membrane. EMBO J 19:57–66. [PubMed][CrossRef]
40. Cavalier-Smith T. 2006. Rooting the tree of life by transition analyses. Biol Direct 1:19. [PubMed][CrossRef]
41. Wu T, Malinverni J, Ruiz N, Kim S, Silhavy TJ, Kahne D. 2005. Identification of a multicomponent complex required for outer membrane biogenesis in Escherichia coli. Cell 121:235–45. [PubMed][CrossRef]
42. Sklar JG, Wu T, Gronenberg LS, Malinverni JC, Kahne D, Silhavy TJ. 2007. Lipoprotein SmpA is a component of the YaeT complex that assembles outer membrane proteins in Escherichia coli. Proc Natl Acad Sci USA 104:6400–6405. [PubMed][CrossRef]
43. Stenberg F, Chovanec P, Maslen SL, Robinson CV, Ilag LL, von Heijne G, Daley DO. 2005. Protein complexes of the Escherichia coli cell envelope. J Biol Chem 280:34409–34419. [PubMed][CrossRef]
44. Eckart K, Eichacker L, Sohrt K, Schleiff E, Heins L, Soll J. 2002. A Toc75-like protein import channel is abundant in chloroplasts. EMBO Rep 3:557–562. [PubMed][CrossRef]
45. Hsu SC, Patel R, Bedard J, Jarvis P, Inoue K. 2008. Two distinct Omp85 paralogs in the chloroplast outer envelope membrane are essential for embryogenesis in Arabidopsis thaliana. Plant Signal Behav 3:1134–1135.[PubMed]
46. Inoue K, Potter D. 2004. The chloroplastic protein translocation channel Toc75 and its paralog OEP80 represent two distinct protein families and are targeted to the chloroplastic outer envelope by different mechanisms. Plant J 39:354–365. [PubMed][CrossRef]
47. Gentle I, Gabriel K, Beech P, Waller R, Lithgow T. 2004. The Omp85 family of proteins is essential for outer membrane biogenesis in mitochondria and bacteria. J Cell Biol 164:19–24. [PubMed][CrossRef]
48. Kozjak V, Wiedemann N, Milenkovic D, Lohaus C, Meyer HE, Guiard B, Meisinger C, Pfanner N. 2003. An essential role of Sam50 in the protein sorting and assembly machinery of the mitochondrial outer membrane. J Biol Chem 278:48520–48523. [PubMed][CrossRef]
49. Paschen SA, Waizenegger T, Stan T, Preuss M, Cyrklaff M, Hell K, Rapaport D, Neupert W. 2003. Evolutionary conservation of biogenesis of β-barrel membrane proteins. Nature 426:862–866. [PubMed][CrossRef]
50. Reumann S, Davila-Aponte J, Keegstra K. 1999. The evolutionary origin of the protein-translocating channel of chloroplastic envelope membranes: identification of a cyanobacterial homolog. Proc Natl Acad Sci USA 96:784–789. [PubMed][CrossRef]
51. 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. [PubMed][CrossRef]
52. Voulhoux R, Bos MP, Geurtsen J, Mols M, Tommassen J. 2003. Role of a highly conserved bacterial protein in outer membrane protein assembly. Science 299:262–265. [PubMed][CrossRef]
53. Werner J, Misra R. 2005. YaeT (Omp85) affects the assembly of lipid-dependent and lipid-independent outer membrane proteins of Escherichia coli. Mol Microbiol 57:1450–1459. [PubMed][CrossRef]
54. Mecsas J, Rouviere PE, Erickson JW, Donohue TJ, Gross CA. 1993. The activity of σ E, an Escherichia coli heat-inducible sigma-factor, is modulated by expression of outer membrane proteins. Genes Dev 7:2618–2628. [PubMed][CrossRef]
55. Walsh NP, Alba BM, Bose B, Gross CA, Sauer RT. 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. [PubMed][CrossRef]
56. Hunke S, Betton J-M. 2003. Temperature effect on inclusion body formation and stress response in the periplasm of Escherichia coli. Mol Microbiol 50:1579–1589. [PubMed][CrossRef]
57. Jones CH, Danese PN, Pinkner JS, Silhavy TJ, Hultgren SJ. 1997. The chaperone-assisted membrane release and folding pathway is sensed by two signal transduction systems. EMBO J 16:6394–6406. [PubMed][CrossRef]
58. Danese PN, Silhavy TJ. 1998. CpxP, a stress-combative member of the Cpx regulon. J Bacteriol 180:831–839.[PubMed]
59. Nakayama S, 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.[PubMed]
60. Miyadai H, Tanaka-Masuda K, Tokuda S-i, Matsuyama H. 2004. Effects of lipoprotein overproduction on the induction of DegP (HtrA) involved in quality control in the Escherichia coli periplasm. J Biol Chem 279:39807–39813. [PubMed][CrossRef]
61. Snyder WB, Davis LJ, Danese PN, Cosma CL, Silhavy TJ. 1995. Overproduction of NlpE, a new outer membrane lipoprotein, suppresses the toxicity of periplasmic LacZ by activation of the Cpx signal transduction pathway. J Bacteriol 177:4216–4223.[PubMed]
62. Danese PN, Oliver GR, Barr K, Bowman GD, Rick PD, Silhavy TJ. 1998. Accumulation of the enterobacterial common antigen lipid II biosynthetic intermediate stimulates degP transcription in Escherichia coli. J Bacteriol 180:5875–5884.[PubMed]
63. 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.[PubMed]
64. DiGiuseppe PA, Silhavy TJ. 2003. Signal detection and target gene induction by the CpxRA two-component system. J Bacteriol 185:2432–2440. [PubMed][CrossRef]
65. Klein G, Lindner B, Brabetz W, Brade H, Raina S. 2009. Escherichia coli K-12 suppressor-free mutants lacking early glycosyltransferases and late acyltransferases: minimal lipopolysaccharide structure and induction of envelope stress response. J Biol Chem 284:15369–15389. [PubMed][CrossRef]
66. Tam C, Missiakas D. 2005. Changes in lipopolysaccharide structure induce the σ E-dependent response of Escherichia coli. Mol Microbiol 55:1403–1412. [PubMed][CrossRef]
67. Bianchi AA, Baneyx F. 1999. Hyperosmotic shock induces the σ 32 and σ E stress regulons of Escherichia coli. Mol Microbiol 34:1029–1038. [PubMed][CrossRef]
68. Jubelin G, Vianney A, Beloin C, Ghigo JM, Lazzaroni JC, Lejeune P, Dorel C. 2005. CpxR/OmpR interplay regulates curli gene expression in response to osmolarity in Escherichia coli. J Bacteriol 187:2038–2049. [PubMed][CrossRef]
69. Prigent-Combaret C, Brombacher E, Vidal O, Ambert A, Lejeune P, Landini P, 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. [PubMed][CrossRef]
70. Gerken H, Leiser OP, Bennion D, 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. [PubMed][CrossRef]
71. Price NL, Raivio TL. 2009. Characterization of the Cpx regulon in Escherichia coli strain MC4100. J Bacteriol 191:1798–1815. [PubMed][CrossRef]
72. Ruiz N, Silhavy TJ. 2005. Sensing external stress: watchdogs of the Escherichia coli cell envelope. Curr Opin Microbiol 8:122–126. [PubMed][CrossRef]
73. Ades SE. 2008. Regulation by destruction: design of the σ E envelope stress response. Curr Opin Microbiol 11:535–540. [PubMed][CrossRef]
74. Ades SE, Connolly LE, Alba BM, Gross CA. 1999. The Escherichia coli σ E-dependent extracytoplasmic stress response is controlled by the regulated proteolysis of an anti-σ factor. Genes Dev 13:2449–2461. [PubMed][CrossRef]
75. Alba BM, Leeds JA, Onufryk C, Lu CZ, Gross CA. 2002. DegS and YaeL participate sequentially in the cleavage of RseA to activate the σ E-dependent extracytoplasmic stress response. Genes Dev 16:2156–2168. [PubMed][CrossRef]
76. De Las Peñas A, Connolly L, Gross CA. 1997. The σ E-mediated response to extracytoplasmic stress in Escherichia coli is transduced by RseA and RseB, two negative regulators of σ E. Mol Microbiol 24:373–385. [PubMed][CrossRef]
77. Missiakas D, Mayer MP, Lemaire M, Georgopoulos C, Raina S. 1997. Modulation of the Escherichia coli σ E (RpoE) heat-shock transcription-factor activity by the RseA, RseB and RseC proteins. Mol Microbiol 24:355–371. [PubMed][CrossRef]
78. Rhodius VA, Suh WC, Nonaka G, West J, Gross CA. 2006. Conserved and variable functions of the σ E stress response in related genomes. PLoS Biol 4:e2. [PubMed][CrossRef]
79. Danese PN, Silhavy TJ. 1997. The σ E and the Cpx signal transduction systems control the synthesis of periplasmic protein-folding enzymes in Escherichia coli. Genes Dev 11:1183–1193. [PubMed][CrossRef]
80. Dartigalongue C, Missiakas D, Raina S. 2001. Characterization of the Escherichia coli σ E regulon. J Biol Chem 276:20866–20875. [PubMed][CrossRef]
81. De Wulf P, McGuire AM, Liu X, Lin EC. 2002. Genome-wide profiling of promoter recognition by the two-component response regulator CpxR-P in Escherichia coli. J Biol Chem 277:26652–26661. [PubMed][CrossRef]
82. Kabir MS, Yamashita D, Koyama S, Oshima T, Kurokawa K, Maeda M, Tsunedomi R, Murata M, Wada C, Mori H, Yamada M. 2005. Cell lysis directed by σ E in early stationary phase and effect of induction of the rpoE gene on global gene expression in Escherichia coli. Microbiology 151:2721–2735. [PubMed][CrossRef]
83. Pogliano J, Lynch AS, Belin D, Lin EC, 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. [PubMed][CrossRef]
84. Skovierova H, Rowley G, Rezuchova B, Homerova D, Lewis C, Roberts M, Kormanec J. 2006. Identification of the σ E regulon of Salmonella enterica serovar Typhimurium. Microbiology 152:1347–1359. [PubMed][CrossRef]
85. Lazar SW, Kolter R. 1996. SurA assists the folding of Escherichia coli outer membrane proteins. J Bacteriol 178:1770–1773.[PubMed]
86. Spiess C, Beil A, Ehrmann M. 1999. A temperature-dependent switch from chaperone to protease in a widely conserved heat shock protein. Cell 97:339–347. [PubMed][CrossRef]
87. Strauch KL, Beckwith J. 1988. An Escherichia coli mutation preventing degradation of abnormal periplasmic proteins. Proc Natl Acad Sci USA 85:1576–1580. [PubMed][CrossRef]
88. Mutalik V, Nonaka G, Ades S, Rhodius VA, Gross CA. 2009. Promoter strength properties of the complete σ E regulon of E. coli and Salmonella. J Bacteriol 191:7279–7287. [PubMed][CrossRef]
89. Onufryk C, Crouch M-L, Fang FC, Gross CA. 2005. A characterization of six lipoproteins in the σ E regulon. J Bacteriol 187:4552–4561. [PubMed][CrossRef]
90. Rezuchova B, Miticka H, Homerova D, Roberts M, Kormanec J. 2003. New members of the Escherichia coli σ E regulon identified by a two-plasmid system. FEMS Microbiol Lett 225:1–7. [PubMed][CrossRef]
91. Johansen J, Eriksen M, Kallipolitis B, Valentin-Hansen P. 2008. Down-regulation of outer membrane proteins by noncoding RNAs: unraveling the cAMP-CRP- and σE-dependent CyaR-ompX regulatory case. J Mol Biol 383:1–9. [PubMed][CrossRef]
92. Johansen J, Rasmussen AA, Overgaard M, Valentin-Hansen P. 2006. Conserved small non-coding RNAs that belong to the σ E regulon: role in down-regulation of outer membrane proteins. J Mol Biol 364:1–8. [PubMed][CrossRef]
93. Udekwu KI, Wagner EG. 2007. σ E controls biogenesis of the antisense RNA MicA. Nucleic Acids Res 35:1279–1288. [PubMed][CrossRef]
94. Bossi L, Figueroa-Bossi N. 2007. A small RNA downregulates LamB maltoporin in Salmonella. Mol Microbiol 65:799–810. [PubMed][CrossRef]
95. Papenfort K, Pfeiffer V, Mika F, Lucchini S, Hinton JCD, Vogel J. 2006. σ E-dependent small RNAs of Salmonella respond to membrane stress by accelerating global omp mRNA decay. Mol Microbiol 62:1674–1688. [PubMed][CrossRef]
96. Button JE, Silhavy TJ, Ruiz N. 2007. A suppressor of cell death caused by the loss of σ E downregulates extracytoplasmic stress responses and outer membrane vesicle production in Escherichia coli. J Bacteriol 189:1523–1530. [PubMed][CrossRef]
97. De Las Peñas A, Connolly L, Gross CA. 1997. σ E is an essential sigma factor in Escherichia coli. J Bacteriol 179:6862–6864.[PubMed]
98. Humphreys S, Stevenson A, Bacon A, Weinhardt AB, Roberts M. 1999. The alternative sigma factor, σ E, is critically important for the virulence of Salmonella typhimurium. Infect Immun 67:1560–1568.[PubMed]
99. Johnson K, Charles I, Dougan G, Pickard D, O’Gaora P, Costa G, Ali T, Miller I, Hormaeche C. 1991. The role of a stress-response protein in Salmonella typhimurium virulence. Mol Microbiol 5:401–407. [PubMed][CrossRef]
100. 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. [PubMed][CrossRef]
101. Otto K, Silhavy TJ. 2002. Surface sensing and adhesion of Escherichia coli controlled by the Cpx-signaling pathway. Proc Natl Acad Sci USA 99:2287–2292. [PubMed][CrossRef]
102. Fleischer R, Heermann R, Jung K, Hunke S. 2007. Purification, reconstitution, and characterization of the CpxRAP envelope stress system of Escherichia coli. J Biol Chem 282:8583–8593. [PubMed][CrossRef]
103. Raivio TL, Laird MW, Joly JC, Silhavy TJ. 2000. Tethering of CpxP to the inner membrane prevents spheroplast induction of the Cpx envelope stress response. Mol Microbiol 37:1186–1197. [PubMed][CrossRef]
104. Sánchez-Pulido L, Devos D, Genevrois S, Vicente M, Valencia A. 2003. POTRA: a conserved domain in the FtsQ family and a class of β-barrel outer membrane proteins. Trends Biochem Sci 28:523–526. [PubMed][CrossRef]
105. Moslavac S, Mirus O, Bredemeier R, Soll J, von Haeseler A, Schleiff E. 2005. Conserved pore-forming regions in polypeptide-transporting proteins. FEBS J 272:1367–1378. [PubMed][CrossRef]
106. Schleiff E, Soll J, Küchler M, Kühlbrandt W, Harrer R. 2003. Characterization of the translocon of the outer envelope of chloroplasts. J Cell Biol 160:541–551. [PubMed][CrossRef]
107. Gatsos X, Perry AJ, Anwari K, Dolezal P, Wolynec PP, Likic VA, Purcell AW, Buchanan SK, Lithgow T. 2008. Protein secretion and outer membrane assembly in Alphaproteobacteria. FEMS Microbiol Rev 32:995–1009. [PubMed][CrossRef]
108. Kim S, Malinverni JC, Sliz P, Silhavy TJ, Harrison SC, Kahne D. 2007. Structure and function of an essential component of the outer membrane protein assembly machine. Science 317:961–964. [PubMed][CrossRef]
109. Stegmeier JF, Andersen C. 2006. Characterization of pores formed by YaeT (Omp85) from Escherichia coli. J Biochem 140:275–283. [PubMed][CrossRef]
110. Clantin B, Delattre A-S, Rucktooa P, Saint N, Meli AC, Locht C, Jacob-Dubuisson F, Villeret V. 2007. Structure of the membrane protein FhaC: a member of the Omp85-TpsB transporter superfamily. Science 317:957–961.[PubMed]
111. Gatzeva-Topalova PZ, Walton TA, Sousa MC. 2008. Crystal structure of YaeT: conformational flexibility and substrate recognition. Structure 16:1873–1881. [PubMed][CrossRef]
112. Knowles TJ, Jeeves M, Bobat S, Dancea F, McClelland D, Palmer T, Overduin M, Henderson IR. 2008. Fold and function of polypeptide transport-associated domains responsible for delivering unfolded proteins to membranes. Mol Microbiol 68:1216–1227. [PubMed][CrossRef]
113. Ward R, Zoltner M, Beer L, El Mkami H, Henderson IR, Palmer T, Norman DG. 2009. The orientation of a tandem POTRA domain pair, of the β-barrel assembly protein BamA, determined by PELDOR spectroscopy. Structure 17:1187–1194. [PubMed][CrossRef]
114. Guédin S, Willery E, Tommassen J, Fort E, Drobecq H, Locht C, Jacob-Dubuisson F. 2000. Novel topological features of FhaC, the outer membrane transporter involved in the secretion of the Bordetella pertussis filamentous hemagglutinin. J Biol Chem 275:30202–30210. [PubMed][CrossRef]
115. Harrison SC. 1996. Peptide-surface association: the case of PDZ and PTB domains. Cell 86:341–343. [PubMed][CrossRef]
116. Bos MP, Robert V, Tommassen J. 2007. Functioning of outer membrane protein assembly factor Omp85 requires a single POTRA domain. EMBO Rep 8:1149–1154. [PubMed][CrossRef]
117. Gentle IE, Burri L, Lithgow T. 2005. Molecular architecture and function of the Omp85 family of proteins. Mol Microbiol 58:1216–1225. [PubMed][CrossRef]
118. Hodak H, Clantin B, Willery E, Villeret V, Locht C, Jacob-Dubuisson F. 2006. Secretion signal of the filamentous haemagglutinin, a model two-partner secretion substrate. Mol Microbiol 61:368–382. [PubMed][CrossRef]
119. Anwari K, Poggio S, Perry A, Gatsos X, Ramarathinam SH, Williamson NA, Noinaj N, Buchanan S, Gabriel K, Purcell AW, Jacobs-Wagner C, Lithgow T. 2010. A modular BAM complex in the outer membrane of the α-proteobacterium Caulobacter crescentus. PLoS One 5:e8619. [PubMed][CrossRef]
120. Volokhina EB, Beckers F, Tommassen J, Bos MP. 2009. The β-barrel outer membrane protein assembly complex of Neisseria meningitidis. J Bacteriol 191:7074–7085. [PubMed][CrossRef]
121. Malinverni JC, Werner J, Kim S, Sklar JG, Kahne D, Misra R, Silhavy TJ. 2006. YfiO stabilizes the YaeT complex and is essential for outer membrane protein assembly in Escherichia coli. Mol Microbiol 61:151–164. [PubMed][CrossRef]
122. Vuong P, Bennion D, Mantei J, Frost D, Misra R. 2008. Analysis of YfgL and YaeT interactions through bioinformatics, mutagenesis, and biochemistry. J Bacteriol 190:1507–1517. [PubMed][CrossRef]
123. Charlson ES, Werner JN, Misra R. 2006. Differential effects of yfgL mutation on Escherichia coli outer membrane proteins and lipopolysaccharide. J Bacteriol 188:7186–7194. [PubMed][CrossRef]
124. Fardini Y, Chettab K, Grepinet O, Rochereau S, Trotereau J, Harvey P, Amy M, Bottreau E, Bumstead N, Barrow PA, Virlogeux-Payant I. 2007. The YfgL lipoprotein is essential for type III secretion system expression and virulence of Salmonella enterica serovar Enteritidis. Infect Immun 75:358–370. [PubMed][CrossRef]
125. Ruiz N, Falcone B, Kahne D, Silhavy TJ. 2005. Chemical conditionality: a genetic strategy to probe organelle assembly. Cell 121:307–317. [PubMed][CrossRef]
126. Inoue T, Shingaki R, Hirose S, Waki K, Mori H, Fukui K. 2007. Genome-wide screening of genes required for swarming motility in Escherichia coli K-12. J Bacteriol 189:950–957. [PubMed][CrossRef]
127. Khairnar NP, Kamble VA, Mangoli SH, Apte SK, Misra HS. 2007. Involvement of a periplasmic protein kinase in DNA strand break repair and homologous recombination in Escherichia coli. Mol Microbiol 65:294–304. [PubMed][CrossRef]
128. Rolhion N, Barnich N, Claret L, Darfeuille-Michaud A. 2005. Strong decrease in invasive ability and outer membrane vesicle release in Crohn's disease-associated adherent-invasive Escherichia coli strain LF82 with the yfgL gene deleted. J Bacteriol 187:2286–2296. [PubMed][CrossRef]
129. Amy M, Velge P, Senocq D, Bottreau E, Mompart F, Virlogeux-Payant I. 2004. Identification of a new Salmonella enterica serovar Enteritidis locus involved in cell invasion and in the colonisation of chicks. Res Microbiol 155:543–552. [PubMed][CrossRef]
130. Fülöp V, Jones DT. 1999. β-Propellers: structural rigidity and functional diversity. Curr Opin Struct Biol 9:715–721. [PubMed][CrossRef]
131. Matsushita K, Toyama H, Yamada M, Adachi O. 2002. Quinoproteins: structure, function, and biotechnological applications. Appl Microbiol Biotechnol 58:13–22. [PubMed][CrossRef]
132. Matsushita K, Arents JC, Bader R, Yamada M, Adachi O, Postma PW. 1997. Escherichia coli is unable to produce pyrroloquinoline quinone (PQQ). Microbiology 143:3149–3156. [PubMed][CrossRef]
133. Jawad Z, Paoli M. 2002. Novel sequences propel familiar folds. Structure 10:447–454. [PubMed][CrossRef]
134. Fardini Y, Trotereau J, Bottreau E, Souchard C, Velge P, Virlogeux-Payant I. 2009. Investigation of the role of the BAM complex and SurA chaperone in outer-membrane protein biogenesis and type III secretion system expression in Salmonella. Microbiology 155:1613–1622. [PubMed][CrossRef]
135. Fussenegger M, Facius D, Meier J, Meyer TF. 1996. A novel peptidoglycan-linked lipoprotein (ComL) that functions in natural transformation competence of Neisseria gonorrhoeae. Mol Microbiol 19:1095–1105. [PubMed][CrossRef]
136. Blatch GL, Lässle M. 1999. The tetratricopeptide repeat: a structural motif mediating protein-protein interactions. Bioessays 21:932–939. [PubMed][CrossRef]
137. Ochsner UA, Vasil AI, Johnson Z, Vasil ML. 1999. Pseudomonas aeruginosa fur overlaps with a gene encoding a novel outer membrane lipoprotein, OmlA. J Bacteriol 181:1099–1109.[PubMed]
138. Vanini MM, Spisni A, Sforça ML, Pertinhez TA, Benedetti CE. 2008. The solution structure of the outer membrane lipoprotein OmlA from Xanthomonas axonopodis pv. citri reveals a protein fold implicated in protein-protein interaction. Proteins 71:2051–2064. [PubMed][CrossRef]
139. Walther DM, Rapaport D, Tommassen J. 2009. Biogenesis of β-barrel membrane proteins in bacteria and eukaryotes: evolutionary conservation and divergence. Cell Mol Life Sci 66:2789–2804. [PubMed][CrossRef]
140. Hiratsu K, Amemura M, Nashimoto H, Shinagawa H, Makino K. 1995. The rpoE gene of Escherichia coli, which encodes σ E, is essential for bacterial growth at high temperature. J Bacteriol 177:2918–2922.[PubMed]
141. Lipinska B, Sharma S, Georgopoulos C. 1988. Sequence analysis and regulation of the htrA gene of Escherichia coli: a σ 32-independent mechanism of heat-inducible transcription. Nucleic Acids Res 16:10053–10067. [PubMed][CrossRef]
142. Behrens S, Maier R, de Cock H, Schmid FX, Gross CA. 2001. The SurA periplasmic PPIase lacking its parvulin domains functions in vivo and has chaperone activity. EMBO J 20:285–294. [PubMed][CrossRef]
143. Missiakas D, Betton J-M, Raina S. 1996. New components of protein folding in extracytoplasmic compartments of Escherichia coli SurA, FkpA and Skp/OmpH. Mol Microbiol 21:871–884. [PubMed][CrossRef]
144. Rizzitello AE, Harper JR, Silhavy TJ. 2001. Genetic evidence for parallel pathways of chaperone activity in the periplasm of Escherichia coli. J Bacteriol 183:6794–6800. [PubMed][CrossRef]
145. Rouvière PE, Gross CA. 1996. SurA, a periplasmic protein with peptidyl-prolyl isomerase activity, participates in the assembly of outer membrane porins. Genes Dev 10:3170–3182. [PubMed][CrossRef]
146. Ureta AR, Endres RG, Wingreen NS, Silhavy TJ. 2007. Kinetic analysis of the assembly of the outer membrane protein LamB in Escherichia coli mutants each lacking a secretion or targeting factor in a different cellular compartment. J Bacteriol 189:446–454. [PubMed][CrossRef]
147. Vertommen D, Ruiz N, Leverrier P, Silhavy TJ, Collet JF. 2009. Characterization of the role of the Escherichia coli periplasmic chaperone SurA using differential proteomics. Proteomics 9:2432–2443. [PubMed][CrossRef]
148. Tormo A, Almiron M, Kolter R. 1990. surA, an Escherichia coli gene essential for survival in stationary phase. J Bacteriol 172:4339–4347.[PubMed]
149. Rahfeld JU, Schierhorn A, Mann K, Fischer G. 1994. A novel peptidyl-prolyl cis/trans isomerase from Escherichia coli. FEBS Lett 343:65–69. [PubMed][CrossRef]
150. Rudd KE, Sofia HJ, Koonin EV, Plunkett G III, Lazar S, Rouviere PE. 1995. A new family of peptidyl-prolyl isomerases. Trends Biochem Sci 20:12–14. [PubMed][CrossRef]
151. Bitto E, McKay DB. 2002. Crystallographic structure of SurA, a molecular chaperone that facilitates folding of outer membrane porins. Structure 10:1489–1498. [PubMed][CrossRef]
152. Xu X, Wang S, Hu YX, McKay DB. 2007. The periplasmic bacterial molecular chaperone SurA adapts its structure to bind peptides in different conformations to assert a sequence preference for aromatic residues. J Mol Biol 373:367–381. [PubMed][CrossRef]
153. Göthel SF, Marahiel MA. 1999. Peptidyl-prolyl cis-trans isomerases, a superfamily of ubiquitous folding catalysts. Cell Mol Life Sci 55:423–436. [PubMed][CrossRef]
154. Hennecke G, Nolte J, Volkmer-Engert R, Schneider-Mergener J, Behrens S. 2005. The periplasmic chaperone SurA exploits two features characteristic of integral outer membrane proteins for selective substrate recognition. J Biol Chem 280:23540–23548. [PubMed][CrossRef]
155. Webb HM, Ruddock LW, Marchant RJ, Jonas K, Klappa P. 2001. Interaction of the periplasmic peptidylprolyl cis-trans isomerase SurA with model peptides. The N-terminal region of SurA is essential and sufficient for peptide binding. J Biol Chem 276:45622–45627. [PubMed][CrossRef]
156. Bitto E, McKay DB. 2003. The periplasmic molecular chaperone protein SurA binds a peptide motif that is characteristic of integral outer membrane proteins. J Biol Chem 278:49316–49322. [PubMed][CrossRef]
157. Bitto E, McKay DB. 2004. Binding of phage-display-selected peptides to the periplasmic chaperone protein SurA mimics binding of unfolded outer membrane proteins. FEBS Lett 568:94–98. [PubMed][CrossRef]
158. Sklar JG, Wu T, Kahne D, Silhavy TJ. 2007. Defining the roles of the periplasmic chaperones SurA, Skp, and DegP in Escherichia coli. Genes Dev 21:2473–2484. [PubMed][CrossRef]
159. Typas A, Nichols RJ, Siegele DA, Shales M, Collins SR, Lim B, Braberg H, Yamamoto N, Takeuchi R, Wanner BL, Mori H, Weissman JS, Krogan NJ, Gross CA. 2008. High-throughput, quantitative analyses of genetic interactions in E. coli. Nat Methods 5:781–787. [PubMed][CrossRef]
160. Schäfer U, Beck K, Müller M. 1999. Skp, a molecular chaperone of Gram-negative bacteria, is required for the formation of soluble periplasmic intermediates of outer membrane proteins. J Biol Chem 274:24567–24574. [PubMed][CrossRef]
161. Chen R, Henning U. 1996. A periplasmic protein (Skp) of Escherichia coli selectively binds a class of outer membrane proteins. Mol Microbiol 19:1287–1294. [PubMed][CrossRef]
162. Holck A, Kleppe K. 1988. Cloning and sequencing of the gene for the DNA-binding 17K protein of Escherichia coli. Gene 67:117–124. [PubMed][CrossRef]
163. Harms N, Koningstein G, Dontje W, Muller M, Oudega B, Luirink J, de Cock H. 2001. The early interaction of the outer membrane protein PhoE with the periplasmic chaperone Skp occurs at the cytoplasmic membrane. J Biol Chem 276:18804–18811. [PubMed][CrossRef]
164. de Cock H, Schafer U, Potgeter M, Demel R, Muller M, Tommassen J. 1999. Affinity of the periplasmic chaperone Skp of Escherichia coli for phospholipids, lipopolysaccharides and non native outer membrane proteins. Role of Skp in the biogenesis of outer membrane protein. Eur J Biochem 259:96–103. [PubMed][CrossRef]
165. Jarchow S, Luck C, Gorg A, Skerra A. 2008. Identification of potential substrate proteins for the periplasmic Escherichia coli chaperone Skp. Proteomics 8:4987–4994. [PubMed][CrossRef]
166. Qu J, Mayer C, Behrens S, Holst O, Kleinschmidt JH. 2007. The trimeric periplasmic chaperone Skp of Escherichia coli forms 1:1 complexes with outer membrane proteins via hydrophobic and electrostatic interactions. J Mol Biol 374:91–105. [PubMed][CrossRef]
167. Wagner JK, Heindl JE, Gray AN, Jain S, Goldberg MB. 2009. Contribution of the periplasmic chaperone Skp to efficient presentation of the autotransporter IcsA on the surface of Shigella flexneri. J Bacteriol 191:815–821. [PubMed][CrossRef]
168. Geyer R, Galanos C, Westphal O, Golecki JR. 1979. A lipopolysaccharide-binding cell-surface protein from Salmonella minnesota. Isolation, partial characterization and occurrence in different Enterobacteriaceae. Eur J Biochem 98:27–38. [PubMed][CrossRef]
169. Schlapschy M, Dommel MK, Hadian K, Fogarasi M, Korndörfer IP, Skerra A. 2004. The periplasmic E. coli chaperone Skp is a trimer in solution: biophysical and preliminary crystallographic characterization. Biol Chem 385:137–143. [PubMed][CrossRef]
170. Korndörfer IP, Dommel MK, Skerra A. 2004. Structure of the periplasmic chaperone Skp suggests functional similarity with cytosolic chaperones despite differing architecture. Nat Struct Mol Biol 11:1015–1020. [PubMed][CrossRef]
171. Walton TA, Sousa MC. 2004. Crystal structure of Skp, a prefoldin-like chaperone that protects soluble and membrane proteins from aggregation. Mol Cell 15:367–374. [PubMed][CrossRef]
172. Walton TA, Sandoval CM, Fowler CA, Pardi A, Sousa MC. 2009. The cavity-chaperone Skp protects its substrate from aggregation but allows independent folding of substrate domains. Proc Natl Acad Sci USA 106:1772–1777. [PubMed][CrossRef]
173. Lipinska B, Zylicz M, Georgopoulos C. 1990. The HtrA (DegP) protein, essential for Escherichia coli survival at high temperatures, is an endopeptidase. J Bacteriol 172:1791–1797.[PubMed]
174. 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.[PubMed]
175. Swamy KH, Chung CH, Goldberg AL. 1983. Isolation and characterization of protease Do from Escherichia coli, a large serine protease containing multiple subunits. Arch Biochem Biophys 224:543–554. [PubMed][CrossRef]
176. Kolmar H, Waller PR, Sauer RT. 1996. The DegP and DegQ periplasmic endoproteases of Escherichia coli: specificity for cleavage sites and substrate conformation. J Bacteriol 178:5925–5929.[PubMed]
177. 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.[PubMed]
178. Skórko-Glonek J, Wawrzynow A, Krzewski K, Kurpierz K, Lipinska B. 1995. Site-directed mutagenesis of the HtrA (DegP) serine protease, whose proteolytic activity is indispensable for Escherichia coli survival at elevated temperatures. Gene 163:47–52. [PubMed][CrossRef]
179. Castillo Keller M, Misra R. 2003. Protease-deficient DegP suppresses lethal effects of a mutant OmpC protein by its capture. J Bacteriol 185:148–154. [PubMed][CrossRef]
180. Misra R, Castillo Keller M, Deng M. 2000. Overexpression of protease-deficient DegP(S210A) rescues the lethal phenotype of Escherichia coli OmpF assembly mutants in a degP background. J Bacteriol 182:4882–4888. [PubMed][CrossRef]
181. Skórko-Glonek J, Laskowska E, Sobiecka-Szkatula A, Lipinska B. 2007. Characterization of the chaperone-like activity of HtrA (DegP) protein from Escherichia coli under the conditions of heat shock. Arch Biochem Biophys 464:80–89. [PubMed][CrossRef]
182. Iwanczyk J, Damjanovic D, Kooistra J, Leong V, Jomaa A, Ghirlando R, Ortega J. 2007. Role of the PDZ domains in Escherichia coli DegP protein. J Bacteriol 189:3176–3186. [PubMed][CrossRef]
183. Spiers A, Lamb HK, Cocklin S, Wheeler KA, Budworth J, Dodds AL, Pallen MJ, Maskell DJ, Charles IG, Hawkins AR. 2002. PDZ domains facilitate binding of high temperature requirement protease A (HtrA) and tail-specific protease (Tsp) to heterologous substrates through recognition of the small stable RNA A ( ssrA)-encoded peptide. J Biol Chem 277:39443–39449. [PubMed][CrossRef]
184. Jiang J, Zhang X, Chen Y, Wu Y, Zhou ZH, Chang Z, Sui SF. 2008. Activation of DegP chaperone-protease via formation of large cage-like oligomers upon binding to substrate proteins. Proc Natl Acad Sci USA 105:11939–11944. [PubMed][CrossRef]
185. Jomaa A, Damjanovic D, Leong V, Ghirlando R, Iwanczyk J, Ortega J. 2007. The inner cavity of Escherichia coli DegP protein is not essential for molecular chaperone and proteolytic activity. J Bacteriol 189:706–716. [PubMed][CrossRef]
186. Sassoon N, Arie JP, Betton JM. 1999. PDZ domains determine the native oligomeric structure of the DegP (HtrA) protease. Mol Microbiol 33:583–589. [PubMed][CrossRef]
187. Ortega J, Iwanczyk J, Jomaa A. 2009. Escherichia coli DegP: a structure-driven functional model. J Bacteriol 191:4705–4713. [PubMed][CrossRef]
188. Kim KI, Park SC, Kang SH, Cheong GW, Chung CH. 1999. Selective degradation of unfolded proteins by the self-compartmentalizing HtrA protease, a periplasmic heat shock protein in Escherichia coli. J Mol Biol 294:1363–1374. [PubMed][CrossRef]
189. Krojer T, Garrido-Franco M, Huber R, Ehrmann M, Clausen T. 2002. Crystal structure of DegP (HtrA) reveals a new protease-chaperone machine. Nature 416:455–459. [PubMed][CrossRef]
190. Krojer T, Sawa J, Schafer E, Saibil HR, Ehrmann M, Clausen T. 2008. Structural basis for the regulated protease and chaperone function of DegP. Nature 453:885–890. [PubMed][CrossRef]
191. Shen QT, Bai XC, Chang LF, Wu Y, Wang HW, Sui SF. 2009. Bowl-shaped oligomeric structures on membranes as DegP's new functional forms in protein quality control. Proc Natl Acad Sci USA 106:4858–4863. [PubMed][CrossRef]
192. Nikaido H. 1996. Outer membrane, p 29–47. In Neidhardt FC, Curtiss R III, Ingraham JL, Lin ECC, Low KB, Magasanik B, Reznikoff WS, Riley M, Schaechter M, and Umbarger HE (ed), Escherichia coli and Salmonella: Cellular and Molecular Biology, 2nd ed., vol. 1. ASM Press, Washington, DC.
193. Misra R, Peterson A, Ferenci T, Silhavy TJ. 1991. A genetic approach for analyzing the pathway of LamB assembly into the outer membrane of Escherichia coli. J Biol Chem 266:13592–13597.[PubMed]
194. Bayer ME. 1991. Zones of membrane adhesion in the cryofixed envelope of Escherichia coli. J Struct Biol 107:268–280. [PubMed][CrossRef]
195. Ishidate K, Creeger ES, Zrike J, Deb S, Glauner B, MacAlister TJ, Rothfield LI. 1986. Isolation of differentiated membrane domains from Escherichia coli and Salmonella typhimurium, including a fraction containing attachment sites between the inner and outer membranes and the murein skeleton of the cell envelope. J Biol Chem 261:428–443.[PubMed]
196. Smit J, Nikaido H. 1978. Outer membrane of gram-negative bacteria. XVIII. Electron microscopic studies on porin insertion sites and growth of cell surface of Salmonella typhimurium. J Bacteriol 135:687–702.[PubMed]
197. Bayer ME. 1968. Areas of adhesion between wall and membrane of Escherichia coli. J Gen Microbiol 53:395–404.[PubMed]
198. Kellenberger E. 1990. The ‘Bayer bridges’ confronted with results from improved electron microscopy methods. Mol Microbiol 4:697–705. [PubMed][CrossRef]
199. Freudl R, Schwarz H, Stierhof Y-D, Gamon K, Hindennach I, Henning U. 1986. An outer membrane protein (OmpA) of Escherichia coli K-12 undergoes a conformational change during export. J Biol Chem 261:11355–11361.[PubMed]
200. Eppens EF, Nouwen N, Tommassen J. 1997. Folding of a bacterial outer membrane protein during passage through the periplasm. EMBO J 16:4295–4301. [PubMed][CrossRef]
201. Tefsen B, Geurtsen J, Beckers F, Tommassen J, de Cock H. 2005. Lipopolysaccharide transport to the bacterial outer membrane in spheroplasts. J Biol Chem 280:4504–4509. [PubMed][CrossRef]
202. de Cock H, Struyve M, Kleerebezem M, van der Krift T, Tommassen J. 1997. Role of the carboxy-terminal phenylalanine in the biogenesis of outer membrane protein PhoE of Escherichia coli K-12. J Mol Biol 269:473–478. [PubMed][CrossRef]
203. Jackson ME, Pratt JM, Holland IB. 1986. Intermediates in the assembly of the TonA polypeptide into the outer membrane of Escherichia coli K12. J Mol Biol 189:477–486. [PubMed][CrossRef]
204. Robert V, Volokhina EB, Senf F, Bos MP, Gelder PV, Tommassen J. 2006. Assembly factor Omp85 recognizes its outer membrane protein substrates by a species-specific C-terminal motif. PLoS Biol 4:e377. [PubMed][CrossRef]
205. Struyvé, M, Moons M, Tommassen J. 1991. Carboxy-terminal phenylalanine is essential for the correct assembly of a bacterial outer membrane protein. J Mol Biol 218:141–148. [PubMed][CrossRef]
206. Kleinschmidt JH. 2006. Folding kinetics of the outer membrane proteins OmpA and FomA into phospholipid bilayers. Chem Phys Lipids 141:30–47. [PubMed][CrossRef]
207. Tamm LK, Hong H, Liang B. 2004. Folding and assembly of β-barrel membrane proteins. Biochim Biophys Acta 1666:250–263. [PubMed][CrossRef]
208. Tommassen J. 2007. Biochemistry. Getting into and through the outer membrane. Science 317:903–904. [PubMed][CrossRef]
209. Surana NK, Grass S, Hardy GG, Li H, Thanassi DG, Geme JWS III. 2004. Evidence for conservation of architecture and physical properties of Omp85-like proteins throughout evolution. Proc Natl Acad Sci USA 101:14497–14502. [PubMed][CrossRef]
210. Kleinschmidt JH, Tamm LK. 1996. Folding intermediates of a β-barrel membrane protein. Kinetic evidence for a multi-step membrane insertion mechanism. Biochemistry 35:12993–13000. [PubMed][CrossRef]
211. Kleinschmidt JH, Tamm LK. 2002. Secondary and tertiary structure formation of the b-barrel membrane protein OmpA is synchronized and depends on membrane thickness. J Mol Biol 324:319–330. [PubMed][CrossRef]
212. Pocanschi CL, Apell H-J, Puntervoll P, Hogh B, Jensen HB, Welte W, Kleinschmidt JH. 2006. The major outer membrane protein of Fusobacterium nucleatum (FomA) folds and inserts into lipid bilayers via parallel folding pathways. J Mol Biol 355:548–561. [PubMed][CrossRef]
213. Surrey T, Jähnig F. 1992. Refolding and oriented insertion of a membrane protein into a lipid bilayer. Proc Natl Acad Sci USA 89:7457–7461. [PubMed][CrossRef]
214. Kleinschmidt JH, den Blaauwen T, Driessen AJ, Tamm LK. 1999. Outer membrane protein A of Escherichia coli inserts and folds into lipid bilayers by a concerted mechanism. Biochemistry 38:5006–5016. [PubMed][CrossRef]
215. Kleinschmidt JH. 2003. Membrane protein folding on the example of outer membrane protein A of Escherichia coli. Cell Mol Life Sci 60:1547–1558. [PubMed][CrossRef]
216. Aoki SK, Malinverni JC, Jacoby K, Thomas B, Pamma R, Trinh BN, Remers S, Webb J, Braaten BA, Silhavy TJ, Low DA. 2008. Contact-dependent growth inhibition requires the essential outer membrane protein BamA (YaeT) as the receptor and the inner membrane transport protein AcrB. Mol Microbiol 70:323–340. [PubMed][CrossRef]
217. Smith DL, James CE, Sergeant MJ, Yaxian Y, Saunders JR, McCarthy AJ, Allison HE. 2007. Short-tailed Stx phages exploit the conserved YaeT protein to disseminate Shiga toxin genes among Enterobacteria. J Bacteriol 189:7223–7233. [PubMed][CrossRef]
218. Aoki SK, Pamma R, Hernday AD, Bickham JE, Braaten BA, Low DA. 2005. Contact-dependent inhibition of growth in Escherichia coli. Science 309:1245–1248. [PubMed][CrossRef]
219. Schmidt H, Bielaszewska M, Karch H. 1999. Transduction of enteric Escherichia coli isolates with a derivative of Shiga toxin 2-encoding bacteriophage φ3538 isolated from Escherichia coli O157:H7. Appl Environ Microbiol 65:3855–3861.[PubMed]
220. Aoki SK, Webb JS, Braaten BA, Low DA. 2009. Contact-dependent growth inhibition causes reversible metabolic downregulation in Escherichia coli. J Bacteriol 191:1777–1786. [PubMed][CrossRef]
221. Housden NG, Loftus SR, Moore GR, James R, Kleanthous C. 2005. Cell entry mechanism of enzymatic bacterial colicins: porin recruitment and the thermodynamics of receptor binding. Proc Natl Acad Sci USA 102:13849–13854. [PubMed][CrossRef]

Article metrics loading...



The major class of integral proteins found in the outer membrane (OM) of and adopt a β-barrel conformation (OMPs). OMPs are synthesized in the cytoplasm with a typical signal sequence at the amino terminus, which directs them to the secretion machinery (SecYEG) located in the inner membrane for translocation to the periplasm. Chaperones such as SurA, or DegP and Skp, escort these proteins across the aqueous periplasm protecting them from aggregation. The chaperones then deliver OMPs to a highly conserved outer membrane assembly site termed the Bam complex. In , the Bam complex is composed of an essential OMP, BamA, and four associated OM lipoproteins, BamBCDE, one of which, BamD, is also essential. Here we provide an overview of what we know about the process of OMP assembly and outline the various hypotheses that have been proposed to explain how proteins might be integrated into the asymmetric OM lipid bilayer in an environment that lacks obvious energy sources. In addition, we describe the envelope stress responses that ensure the fidelity of OM biogenesis and how factors, such as phage and certain toxins, have coopted this essential machine to gain entry into the cell.

Highlighted Text: Show | Hide
Loading full text...

Full text loading...

Comment has been disabled for this content
Submit comment
Comment moderation successfully completed


Image of Figure 1
Figure 1

In , most OM lipoproteins and OMPs are synthesized and transported to the IM secretion machinery posttranslationally. SecB chaperone molecules bind to hydrophobic segments of OM proteins to prevent their aggregation in the cytoplasm. OM proteins are delivered to the SecA ATPase complexed with the IM translocation machinery, SecYEG, as well as other associated proteins of unknown function that are not depicted here (see reference  1 ). OM lipoproteins and OMPs are distinguished by the composition of their signal sequences and sorted for processing by separate pathways ( 2 , 3 ). OM lipoprotein biogenesis pathway (depicted to the left of the IM secretion machinery): the asterisk indicates a lipoprotein without an Asp amino acid at the +2 position, the main signal for sorting by the LolABCDE pathway to the OM in ( 4 ). OMP biogenesis pathway (depicted to the right of the IM secretion machinery): after signal sequence processing, the SurA chaperone is thought to complex with the bulk of OMPs in the periplasmic space and deliver them to the OM assembly site, the Bam complex. In the absence of SurA, the Skp/DegP pathway becomes an indispensable substitute. Details concerning the mechanisms behind Bam-mediated OMP assembly into the OM are unknown. See the text for references and further details.

Citation: Malinverni J, Silhavy T. 2011. Assembly of Outer Membrane β-Barrel Proteins: the Bam Complex, EcoSal Plus 2011; doi:10.1128/ecosalplus.4.3.8
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 2
Figure 2

The Bam complex is composed of the integral OMP, BamA, and four OM lipoproteins, BamB, -C, -D, and -E ( 41 , 42 ). BamA consists of an essential N-terminal periplasmic region with five POTRA domains and a C-terminal β-barrel domain ( 104 , 108 , 109 ). The arrangement of the periplasmic domain may be dynamic, with a putative hinge region between P2 and P3 that ranges from a comparatively straight (130°) ( 111 ) to a bent (100°) ( 108 ) conformation. The relative orientation of P5 (shaded in white) with respect to P1 through P4 is not represented in the existing crystal structures but is portrayed in a sharply kinked conformation in agreement with SAX data (see the text for details) ( 112 ). The C-terminal portion of BamA is predicted to be a β-barrel with several extracellular loops. Extracellular loop 6 (L6) is particularly interesting in that portions of L6 are highly conserved and are predicted to interact with other conserved features of the barrel ( 34 , 105 ). Biochemical and structural data from a BamA homolog, FhaC, imply that L6 may be a dynamic loop capable of extending into the barrel and reaching the periplasmic space ( 34 , 110 , 114 ).

Citation: Malinverni J, Silhavy T. 2011. Assembly of Outer Membrane β-Barrel Proteins: the Bam Complex, EcoSal Plus 2011; doi:10.1128/ecosalplus.4.3.8
Permissions and Reprints Request Permissions
Download as Powerpoint


Generic image for table
Table 1

Gram-negative phyla containing Bam complex and periplasmic chaperone proteins

Citation: Malinverni J, Silhavy T. 2011. Assembly of Outer Membrane β-Barrel Proteins: the Bam Complex, EcoSal Plus 2011; doi:10.1128/ecosalplus.4.3.8

Supplemental Material

No supplementary material available for this content.

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error