From Chaperones to the Membrane with a BAM!

Trends in Biochemical Sciences

Volumn 41, Issue 10, 2016, Pages 872-882

  Plummer, Ashlee M ^a   Fleming, Karen G ^a  

^a JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

BAM complex; chaperones; outer membrane proteins

Indexed keywords

BETA BARREL ASSEMBLY MACHINERY COMPLEX; CHAPERONE; MULTIPROTEIN COMPLEX; OUTER MEMBRANE PROTEIN; UNCLASSIFIED DRUG; ESCHERICHIA COLI PROTEIN; PROTEIN BINDING;

BACTERIAL OUTER MEMBRANE; BIOGENESIS; CATALYSIS; ENERGY RESOURCE; ESCHERICHIA COLI; IN VITRO STUDY; IN VIVO STUDY; MOLECULAR DYNAMICS; NEUTRON SCATTERING; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN ASSEMBLY; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MISFOLDING; PROTEIN MOTIF; REVIEW; BETA SHEET; BINDING SITE; CHEMISTRY; GENE EXPRESSION; GENETICS; METABOLISM; PERIPLASM; PROTEIN DOMAIN; PROTEIN TRANSPORT; PROTEIN UNFOLDING; THERMODYNAMICS; ULTRASTRUCTURE;

BACTERIAL OUTER MEMBRANE PROTEINS; BINDING SITES; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION; MOLECULAR CHAPERONES; MOLECULAR DYNAMICS SIMULATION; PERIPLASM; PROTEIN BINDING; PROTEIN CONFORMATION, BETA-STRAND; PROTEIN FOLDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN TRANSPORT; PROTEIN UNFOLDING; THERMODYNAMICS;

EID: 84978887291     PISSN: 09680004     EISSN: 13624326     Source Type: Journal    
DOI: 10.1016/j.tibs.2016.06.005     Document Type: Review

References (77)

1. 1 Masuda, T., et al. Unbiased quantitation of Escherichia coli membrane proteome using phase transfer surfactants. Mol. Cell. Proteomics 8 (2009), 2770–2777.
2. 2 Kumamoto, C., Escherichia coli SecB protein associates with exported protein precursors in vivo. Proc. Natl. Acad. Sci. U.S.A. 86 (1989), 5320–5324.
3. 3 Ruiz, N., et al. Advances in understanding bacterial outer-membrane biogenesis. Nat. Rev. Microbiol. 4 (2006), 57–66.
4. 4 Murakami, S., et al. Crystal structure of bacterial multidrug efflux transporter AcrB. Nature 419 (2002), 587–593.
5. 5 Ebie Tan, A., et al. Self-association of unfolded outer membrane proteins. Macromol. Biosci. 10 (2010), 763–767.
6. 6 Danoff, E.J., Fleming, K.G., Aqueous, unfolded OmpA forms amyloid-like fibrils upon self-association. PLoS ONE, 10, 2015, e0132301.
7. 7 Wülfing, C., Plückthun, A., Protein folding in the periplasm of Escherichia coli. Mol. Microbiol. 12 (1994), 685–692.
8. 8 Moon, C.P., et al. Membrane protein thermodynamic stability may serve as the energy sink for sorting in the periplasm. Proc. Natl. Acad. Sci. U.S.A. 110 (2013), 4285–4290.
9. 9 Wu, S., et al. Interaction between bacterial outer membrane proteins and periplasmic quality control factors: a kinetic partitioning mechanism. Biochem. J. 438 (2011), 505–511.
10. 10 Ge, X., et al. Identification of FkpA as a key quality control factor for the biogenesis of outer membrane proteins under heat shock conditions. J. Bacteriol. 196 (2014), 672–680.
11. 11 Fleming, K.G., A combined kinetic push and thermodynamic pull as driving forces for outer membrane protein sorting and folding in bacteria. Philos. Trans. R. Soc. B, 370, 2015, 20150026.
12. 12 Walton, T.A., Sousa, M.C., Crystal structure of Skp, a prefoldin-like chaperone that protects soluble and membrane proteins from aggregation. Mol. Cell 15 (2004), 367–374.
13. 13 Strauch, K.L., et al. 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 (1989), 2689–2696.
14. 14 Krojer, T., et al. Structural basis for the regulated protease and chaperone function of DegP. Nature 453 (2008), 885–890.
15. 15 Walton, T.A., et al. The cavity-chaperone Skp protects its substrate from aggregation but allows independent folding of substrate domains. Proc. Natl. Acad. Sci. U.S.A. 106 (2009), 1772–1777.
16. 16 Sandlin, C.W., et al. Skp trimer formation is insensitive to salts in the physiological range. Biochemistry 54 (2015), 7059–7062.
17. 17 Lyu, Z.X., et al. Direct observation of the uptake of outer membrane proteins by the periplasmic chaperone Skp. PLoS ONE, 7, 2012, e46068.
18. 18 Burmann, B.M., et al. Conformation and dynamics of the periplasmic membrane-protein–chaperone complexes OmpX–Skp and tOmpA–Skp. Nat. Struct. Mol. Biol. 20 (2013), 1265–1272.
19. 19 Zaccai, N.R., et al. Deuterium labeling together with contrast variation small-angle neutron scattering suggests how Skp Captures and releases unfolded outer membrane proteins. Method Enzymol. 566 (2015), 159–210.
20. 20 Rouviere, P.E., Gross, C.A., SurA, a periplasmic protein with peptidyl-prolyl isomerase activity, participates in the assembly of outer membrane porins. Genes Dev. 10 (1996), 3170–3182.
21. 21 Arié, J.P., et al. Chaperone function of FkpA, a heat shock prolyl isomerase, in the periplasm of Escherichia coli. Mol. Microbiol. 39 (2001), 199–210.
22. 22 Bitto, E., McKay, D.B., Crystallographic structure of SurA, a molecular chaperone that facilitates folding of outer membrane porins. Structure 10 (2002), 1489–1498.
23. 23 Saul, F.A., et al. Structural and functional studies of FkpA from Escherichia coli, a cis/trans peptidyl-prolyl isomerase with chaperone activity. J. Mol. Biol. 335 (2004), 595–608.
24. 24 Thoma, J., et al. Impact of holdase chaperones Skp and SurA on the folding of β-barrel outer-membrane proteins. Nat. Struct. Mol. Biol. 22 (2015), 795–802.
25. 25 Soltes, G.R., et al. The activity of Escherichia coli chaperone SurA is regulated by conformational changes involving a parvulin domain. J. Bacteriol. 198 (2016), 921–929.
26. 26 Hu, K., et al. Structural plasticity of peptidyl-prolyl isomerase sFkpA is a key to its chaperone function as revealed by solution NMR. Biochemistry 45 (2006), 11983–11991.
27. 27 Patel, G.J., Kleinschmidt, J.H., The lipid bilayer-inserted membrane protein BamA of Escherichia coli facilitates insertion and folding of outer membrane protein a from its complex with Skp. Biochemistry 52 (2013), 3974–3986.
28. 28 McMorran, L.M., et al. Dissecting the effects of periplasmic chaperones on the in vitro folding of the outer membrane protein PagP. J. Mol. Biol. 425 (2013), 3178–3191.
29. 29 Sklar, J.G., et al. Defining the roles of the periplasmic chaperones SurA, Skp, and DegP in Escherichia coli. Genes Dev. 21 (2007), 2473–2484.
30. 30 Bennion, D., et al. Dissection of β-barrel outer membrane protein assembly pathways through characterizing BamA POTRA 1 mutants of Escherichia coli. Mol. Microbiol. 77 (2010), 1153–1171.
31. 31 Rizzitello, A., et al. Genetic evidence for parallel pathways of chaperone activity in the periplasm of Escherichia coli. J. Bacteriol. 183 (2001), 6794–6800.
32. 32 Vertommen, D., et al. Characterization of the role of the Escherichia coli periplasmic chaperone SurA using differential proteomics. Proteomics 9 (2009), 2432–2443.
33. 33 Bitto, E., McKay, D.B., The periplasmic molecular chaperone protein SurA binds a peptide motif that is characteristic of integral outer membrane proteins. J. Biol. Chem. 278 (2003), 49316–49322.
34. 34 Hennecke, G., et al. The periplasmic chaperone SurA exploits two features characteristic of integral outer membrane proteins for selective substrate recognition. J. Biol. Chem. 280 (2005), 23540–23548.
35. 35 Jarchow, S., et al. Identification of potential substrate proteins for the periplasmic Escherichia coli chaperone Skp. Proteomics 8 (2008), 4987–4994.
36. 36 Voulhoux, R., et al. Role of a highly Conserved bacterial protein in outer membrane protein assembly. Science 299 (2003), 262–266.
37. 37 Wu, T., et al. Identification of a multicomponent complex required for outer membrane biogenesis in Escherichia coli. Cell 121 (2005), 235–245.
38. 38 Onufryk, C., et al. Characterization of six lipoproteins in the sigmaE regulon. J. Bacteriol. 187 (2005), 4552–4561.
39. 39 Malinverni, J.C., et al. YfiO stabilizes the YaeT complex and is essential for outer membrane protein assembly in Escherichia coli. Mol. Microbiol. 61 (2006), 151–164.
40. 40 Sklar, J.G., et al. Lipoprotein SmpA is a component of the YaeT complex that assembles outer membrane proteins in Escherichia coli. Proc. Natl. Acad. Sci. U.S.A. 104 (2007), 6400–6405.
41. 41 Werner, J., Misra, R., YaeT (Omp85) affects the assembly of lipid-dependent and lipid-independent outer membrane proteins of Escherichia coli. Mol. Microbiol. 57 (2005), 1450–1459.
42. 42 Osborn, M.J., et al. Macromolecules: mechanism of assembly of the outer membrane of Salmonella typhimurium: site of synthesis of lipopolysaccharide. J. Biol. Chem. 247 (1972), 3962–3972.
43. 43 Kamio, Y., Nikaido, H., Outer membrane of Salmonella typhimurium: accessibility of phospholipid head groups to phospholipase C and cyanogen bromide activated dextran in the external medium. Biochemistry 15 (1976), 2561–2570.
44. 44 Gessmann, D., et al. Outer membrane β-barrel protein folding is physically controlled by periplasmic lipid head groups and BamA. Proc. Natl. Acad. Sci. U.S.A. 111 (2014), 5878–5883.
45. 45 Hagan, C.L., et al. Reconstitution of outer membrane protein assembly from purified components. Science 328 (2010), 890–892.
46. 46 Danoff, E.J., Fleming, K.G., Membrane defects accelerate outer membrane β-barrel protein folding. Biochemistry 54 (2015), 97–99.
47. 47 Noinaj, N., et al. Structural insight into the biogenesis of β-barrel membrane proteins. Nature 501 (2013), 385–390.
48. 48 Hagan, C.L., Kahne, D., The reconstituted Escherichia coli bam complex catalyzes multiple rounds of β-barrel assembly. Biochemistry 50 (2011), 7444–7446.
49. 49 Plummer, A.M., Fleming, K.G., BamA alone accelerates outer membrane protein folding in vitro through a catalytic mechanism. Biochemistry 54 (2015), 6009–6011.
50. 50 Gu, Y., et al. Structural basis of outer membrane protein insertion by the BAM complex. Nature 531 (2016), 64–69.
51. 51 Noinaj, N., et al. Lateral opening and exit pore formation are required for BamA function. Structure 22 (2014), 1055–1062.
52. 52 Ahn, V.E., et al. A hydrocarbon ruler measures palmitate in the enzymatic acylation of endotoxin. EMBO J. 23 (2004), 2931–2941.
53. 53 Gruss, F., et al. The structural basis of autotransporter translocation by TamA. Nat. Struct. Mol. Biol. 20 (2013), 1318–1320.
54. 54 Dong, H., et al. Structural basis for outer membrane lipopolysaccharide insertion. Nature 511 (2014), 52–56.
55. 55 Hearn, E.M., et al. Transmembrane passage of hydrophobic compounds through a protein channel wall. Nature 458 (2009), 367–370.
56. 56 Hong, H., et al. The outer membrane protein OmpW forms an eight-stranded β-barrel with a hydrophobic channel. J. Biol. Chem. 281 (2006), 7568–7577.
57. 57 Rollauer, S.E., et al. Outer membrane protein biogenesis in Gram-negative bacteria. Philos. Trans. R. Soc. B, 370, 2015, 20150023.
58. 58 Knowles, T.J., et al. Fold and function of polypeptide transport-associated domains responsible for delivering unfolded proteins to membranes. Mol. Microbiol. 68 (2008), 1216–1227.
59. 59 Kim, S., et al. Structure and function of an essential component of the outer membrane protein assembly machine. Science 317 (2007), 961–964.
60. 60 Gatzeva-Topalova, P.Z., et al. Crystal structure of YaeT: conformational flexibility and substrate recognition. Structure 16 (2008), 1873–1881.
61. 61 Gatzeva-Topalova, P.Z., et al. Structure and flexibility of the complete periplasmic domain of BamA: the protein insertion machine of the outer membrane. Structure 18 (2010), 1492–1501.
62. 62 Fleming, P.J., et al. BamA POTRA domain interacts with a native lipid membrane surface. Biophys. J 110 (2016), 2698–2709.
63. 63 Jansen, K.B., et al. Crystal structure of BamB bound to a periplasmic domain fragment of BamA, the central component of the β-barrel assembly machine. J. Biol. Chem. 290 (2015), 2126–2136.
64. 64 Bergal, H.T., et al. The structure of a BamA–BamD fusion illuminates the architecture of the β-barrel assembly machine core. Structure 24 (2015), 243–251.
65. 65 Bakelar, J., et al. The structure of the β-barrel assembly machinery complex. Science 351 (2016), 180–186.
66. 66 Han, L., et al. Structure of the BAM complex and its implications for biogenesis of outer-membrane proteins. Nat. Struct. Mol. Biol. 23 (2016), 192–196.
67. 67 Hagan, C.L., et al. Inhibition of the β-barrel assembly machine by a peptide that binds BamD. Proc. Natl. Acad. Sci. U.S.A. 112 (2015), 2011–2016.
68. 68 Ursell, T.S., et al. Analysis of surface protein expression reveals the growth pattern of the Gram-negative outer membrane. PLoS Comput. Biol., 8, 2012, e1002680.
69. 69 Rassam, P., et al. Supramolecular assemblies underpin turnover of outer membrane proteins in bacteria. Nature 523 (2015), 333–336.
70. 70 Kleanthous, C., et al. Protein–protein interactions and the spatiotemporal dynamics of bacterial outer membrane proteins. Curr. Opin. Struct. Biol. 35 (2015), 109–115.
71. 71 Hagan, C.L., et al. Bam lipoproteins assemble BamA in vitro. Biochemistry 52 (2013), 6108–6113.
72. 72 Wu, E.L., et al. E. coli outer membrane and interactions with OmpLA. Biophys. J. 106 (2014), 2493–2502.
73. 73 PyMOL Molecular Graphics System, Version 1.3 Schrödinger, LLC.
74. 74 Humphrey, W., et al. VMD: visual molecular dynamics. J. Mol. Graph. 14 (1996), 33–38.
75. 75 Sapra, K.T., et al. One beta hairpin after the other: exploring mechanical unfolding pathways of the transmembrane beta-barrel protein OmpG. Angew. Chem. Int. Ed. Engl. 48 (2009), 8306–8308.
76. 76 Bosshart, P.D., et al. The transmembrane protein KpOmpA anchoring the outer membrane of Klebsiella pneumoniae unfolds and refolds in response to tensile load. Structure 20 (2012), 121–127.
77. 77 Thoma, J., et al. Out but not in: the large transmembrane β-barrel protein FhuA unfolds but cannot refold via β-hairpins. Structure 20 (2012), 2185–2190.