Crystal structure of Escherichia coli BamB, a lipoprotein component of the β-barrel assembly machinery complex

Journal of Molecular Biology

Volumn 406, Issue 5, 2011, Pages 667-678

  Kim, Kelly H ^a   Paetzel, Mark ^a  

^a SIMON FRASER UNIVERSITY   (Canada)

Author keywords

lipoprotein; outer membrane biogenesis; outer membrane protein; protein folding; protein structure

Indexed keywords

LIPOPROTEIN; OUTER MEMBRANE PROTEIN; PROTEIN BAMA; PROTEIN BAMB; PROTEIN BAMC; PROTEIN BAMD; PROTEIN BAME; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; BETA SHEET; BIOINFORMATICS; CATALYSIS; CRYSTAL STRUCTURE; ESCHERICHIA COLI; LIGAND BINDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN PROTEIN INTERACTION;

ESCHERICHIA COLI; NEGIBACTERIA;

EID: 79951772443     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2010.12.020     Document Type: Article

References (49)

1. Costerton, J. W., Ingram, J. M. & Cheng, K. J. (1974). Structure and function of the cell envelope of gram-negative bacteria. Bacteriol. Rev. 38, 87-110.
2. Bos, M. P., Robert, V. & Tommassen, J. (2007). Biogenesis of the gram-negative bacterial outer membrane. Annu. Rev. Microbiol. 61, 191-214.
3. Delcour, A. H. (2009). Outer membrane permeability and antibiotic resistance. Biochem. Biophys. Acta, 1794, 808-816.
4. Walther, D. M., 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.
5. Gatsos, X., Perry, A. J., Anwari, K., Dolezal, P., Wolynec, P. P., Likic, V. A. et al. (2008). Protein secretion and outer membrane assembly in Alpha-proteobacteria. FEMS Microbiol. Rev. 32, 995-1009.
6. Gentle, I. E., Burri, L. & Lithgow, T. (2005). Molecular architecture and function of the Omp85 family of proteins. Mol. Microbiol. 58, 1216-1225.
7. Voulhoux, R. & Tommassen, J. (2004). Omp85, an evolutionarily conserved bacterial protein involved in outer-membrane-protein assembly. Res. Microbiol. 155, 129-135.
8. Wu, T., Malinverni, J., Ruiz, N., Kim, S., Silhavy, T. J. & Kahne, D. (2005). Identification of a multicomponent complex required for outer membrane biogenesis in Escherichia coli. Cell, 121, 235-245. (Pubitemid 40546391)
9. Knowles, T. J., Scott-Tucker, A., Overduin, M. & Henderson, I. R. (2009). Membrane protein architects: the role of the BAM complex in outer membrane protein assembly. Nat. Rev. Microbiol. 7, 206-214.
10. 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. (Pubitemid 38082453)
11. Voulhoux, R., Bos, M. P., Geurtsen, J., Mols, M. & Tommassen, J. (2003). Role of a highly conserved bacterial protein in outer membrane protein assembly. Science, 299, 262-265. (Pubitemid 36125214)
12. Sklar, J. G., Wu, T., Gronenberg, L. S., Malinverni, J. C., Kahne, D. & Silhavy, T. J. (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.
13. Malinverni, J. C., Werner, J., Kim, S., Sklar, J. G., Kahne, D., Misra, R. & Silhavy, T. J. (2006). YfiO stabilizes the YaeT complex and is essential for outer membrane protein assembly in Escherichia coli. Mol. Microbiol. 61, 151-164.
14. Anwari, K., Poggio, S., Perry, A., Gatsos, X., Ramarathinam, S. H., Williamson, N. A. et al. (2010). A modular BAM complex in the outer membrane of the α-proteobacterium Caulobacter crescentus. PLoS One, 5, e8619.
15. Doerrler, W. T. & Raetz, C. R. (2005). Loss of outer membrane proteins without inhibition of lipid export in an Escherichia coli YaeT mutant. J. Biol. Chem. 280, 27679-27687.
16. Fitzpatrick, D. A. & McInerney, J. O. (2005). Evidence of positive Darwinian selection in Omp85, a highly conserved bacterial outer membrane protein essential for cell viability. J. Mol. Evol. 60, 268-273.
17. Ryan, K. R., Taylor, J. A. & Bowers, L. M. (2010). The BAM complex subunit BamE (SmpA) is required for membrane integrity, stalk growth and normal levels of outer membrane β-barrel proteins in Caulobacter crescentus. Microbiology, 156, 742-756.
18. Charlson, E. S., Werner, J. N. & Misra, R. (2006). Differential effects of yfgL mutation on Escherichia coli outer membrane proteins and lipopolysaccharide. J. Bacteriol. 188, 7186-7194. (Pubitemid 44547623)
19. Knowles, T. J., Jeeves, M., Bobat, S., Dancea, F., McClelland, D., Palmer, T. et al. (2008). Fold and function of polypeptide transport-associated domains responsible for delivering unfolded proteins to membranes. Mol. Microbiol. 68, 1216-1227.
20. Gatzeva-Topalova, P. Z., Walton, T. A. & Sousa, M. C. (2008). Crystal structure of YaeT: conformational flexibility and substrate recognition. Structure, 16, 1873-1881.
21. Misra, R. (2007). First glimpse of the crystal structure of YaeT's POTRA domains. ACS Chem. Biol. 2, 649-651.
22. Kim, S., Malinverni, J. C., Sliz, P., Silhavy, T. J., Harrison, S. C. & Kahne, D. (2007). Structure and function of an essential component of the outer membrane protein assembly machine. Science, 317, 961-964. (Pubitemid 47301326)
23. Clantin, B., Delattre, A. S., Rucktooa, P., Saint, N., Meli, A. C., Locht, C. et al. (2007). Structure of the membrane protein FhaC: a member of the Omp85-TpsB transporter superfamily. Science, 317, 957-961; 24.
24. Bos, M. P., Robert, V. & Tommassen, J. (2007). Functioning of outer membrane protein assembly factor Omp85 requires a single POTRA domain. EMBO Rep. 8, 1149-1154. (Pubitemid 350201733)
25. Meli, A. C., Hodak, H., Clantin, B., Locht, C., Molle, G., Jacob-Dubuisson, F. & Saint, N. (2006). Channel properties of TpsB transporter FhaC point to two functional domains with a C-terminal protein-conducting pore. J. Biol. Chem. 281, 158-166.
26. Robert, V., Volokhina, E. B., Senf, F., Bos, M. P., Van Gelder, P. & Tommassen, J. (2006). Assembly factor Omp85 recognizes its outer membrane protein substrates by a species-specific C-terminal motif. PLoS Biol. 4, e377.
27. Ureta, A., Endres, R., Wingree, N. & Silhavy, T. (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. (Pubitemid 46106377)
28. Onufryk, C., Crouch, M. L., Fang, F. C. & Gross, C. A. (2005). Characterization of six lipoproteins in the regulon. J. Bacteriol. 187, 4552-4561.
29. 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. (Pubitemid 351304004)
30. Fülöp, V. & Jones, D. (1999). Beta propellers: structural rigidity and functional diversity. Curr. Opin. Struct. Biol. 9, 715-721.
31. Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H. et al. (2007). ClustalWand Clustal X version 2.0. Bioinformatics, 23, 2947-2948.
32. Holm, L., Kaariainen, S., Rosenstrom, P. & Schenkel, A. (2008). Searching protein structure databases with DaliLite v.3. Bioinformatics, 24, 2780-2781.
33. Chen, Z., Matsushita, K., Yamashita, T., Fujii, T., Toyama, H., Adachi, O. et al. (2002). Structure at 1.9 Å resolutin of a quinohemoprotein alcohol dehydrogenase from Pseudomonas putida HK5. Structure, 10, 837-849. (Pubitemid 34628712)
34. Hao, B., Oehlmann, S., Sowa, M., Harper, J. & Pavletich, N. (2007). Structure of a Fbw7-Skp1-cyclin E complex: multisite-phosphorylated substrate recognition by SCF ubiquitin ligases. Mol. Cell, 26, 131-143.
35. Sjogren, T. & Hajdu, J. (2001). Structure of the bound dioxygen species in the cytochrome oxidase reaction of cytochrome cd1 nitrite reductase. J. Biol. Chem. 276, 13072-13076.
36. Cerna, D. & Wilson, D. (2005). The structure of Sif2p, a WD repeat protein functioning in the SET3 corepressor complex. J. Mol. Biol. 351, 923-935.
37. Fardini, Y., Chettab, K., Grepinet, O., Rocherau, S., Troterau, J., Harvey, P. et al. (2007). The YfgL lipoprotein is essential for type III secretion system expression and virulence of Salmonella enterica serovar Enteritidis. Infect. Immun. 75, 358-370.
38. 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 colonization of chicks. Res. Microbiol. 155, 543-552.
39. Powell, H. (1999). The Rossmann Fourier autoindexing algorithm in MOSFLM. Acta Crystallogr., Sect. D: Biol. Crystallogr. 55, 1690-1695.
40. Adams, P., Afonine, P., Bunkoczi, G., Chen, B., Davis, I., Echools, N. et al. (2010). PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr., Sect. D: Biol. Crystallogr. 66, 213-221.
41. Emsley, P. & Cowtan, K. (2004). Coot: model-building tools for molecular graphics. Acta Crystallogr., Sect. D: Biol. Crystallogr. 60, 2126-2132. (Pubitemid 41742764)
42. Murshudov, G., Vagin, A. & Dodson, E. (1997). Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. 30, 1022-1025.
43. Kabsch, W. & Sander, C. (1983). Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers, 22, 2577-2637.
44. Hutchinson, E. G. & Thornton, J. M. (1996). PROMOTIF - a program to identify and analyze structural motifs in proteins. Protein Sci. 5, 212-220. (Pubitemid 26054277)
45. Laskowski, R., Macarther, M., Moss, D. & Thornton, J. (1993). PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26, 283-291.
46. Liang, J., Edelsbrunner, H. & Woodward, C. (1998). Anatomy of protein pocket and cavities: measurement of binding site geometry an implications for ligand design. Protein Sci. 7, 1884-1897. (Pubitemid 28432430)
47. Tsodikov, O., Record, M. & Sergeev, Y. (2002). Novel computer program for fast exact calculation of accessible and molecular surface areas and average surface curvature. J. Comput. Chem. 23, 600-609.
48. DeLano, W. L. (2002). The PyMOL Molecular Graphics System.
49. Gouet, P., Courcelle, E., Stuart, D. I. & Metoz, F. (1999). ESPript: analysis of multiple sequence alignments in PostScript. Bioinformatics, 15, 305-308. (Pubitemid 29213756)