Structure of the translocator domain of a bacterial autotransporter

EMBO Journal

Volumn 23, Issue 6, 2004, Pages 1257-1266

  Oomen, Clasien J ^a,b   Van Ulsen, Peter ^b,c   Van Gelder, Patrick ^d   Feijen, Maya ^c   Tommassen, Jan ^c   Gros, Piet ^a  

^a UTRECHT UNIVERSITY   (Netherlands)

^b NETHERLANDS VACCINE INSTITUTE   (Netherlands)

^c UTRECHT UNIVERSITY   (Netherlands)

^d VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

Author keywords

Autotransporters; Crystal structure; Neisseria meningitidis; Outer membrane protein; Protein secretion

Indexed keywords

AUTOTRANSPORTER NAIP; PROTEIN; UNCLASSIFIED DRUG;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; ARTICLE; CONTROLLED STUDY; CRYSTAL STRUCTURE; MODEL; NEISSERIA MENINGITIDIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN STRUCTURE; PROTEIN TRANSPORT; STRUCTURE ANALYSIS;

AMINO ACID SEQUENCE; CEPHALOSPORINS; CRYSTALLOGRAPHY, X-RAY; ESCHERICHIA COLI; GENE EXPRESSION; MEMBRANE TRANSPORT PROTEINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NEISSERIA MENINGITIDIS; PROTEIN BINDING; PROTEIN FOLDING; PROTEIN RENATURATION; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; SERINE ENDOPEPTIDASES;

BACTERIA (MICROORGANISMS); INSERTION SEQUENCES; NEGIBACTERIA; NEISSERIA; NEISSERIA MENINGITIDIS;

EID: 1942471665     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.emboj.7600148     Document Type: Article

References (44)

1. Bosch D, Leunissen J, Verbakel J, de Jong M, van Erp H, Tommassen J (1986) Periplasmic accumulation of truncated forms of outer-membrane PhoE protein of Escherichia coli K-12. J Mol Biol 189: 449-455
2. Bradley P, Cowen L, Menke M, King J, Berger B (2001) BETAWRAP: successful prediction of parallel β-helices from primary sequence reveals an association with many microbial pathogens. Proc Natl Acad Sci USA 98: 14819-14824
3. Brandon LB, Goldberg MB (2001) Periplasmic transit and disulfide-bond formation of the autotransported Shigella protein IcsA. J Bacteriol 183: 951-958
4. Brunger AT, Adams PD, Clore GM, DeLano WL, Gros P, Grosse-Kunstleve RW, Jiang JS, Kuszewski J, Nilges M, Pannu NS, Read RJ, Rice LM, Simonson T, Warren GL (1998) Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr D 54: 905-921
5. CCP4 (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr D 50: 760-763
6. Dekker N, Merck K, Tommassen J, Verheij HM (1995) In vitro folding of Escherichia coli outer-membrane phospholipase A. Eur J Biochem 232: 214-219
7. Driessen AJ, Fekkes P, van der Wolk JP (1998) The Sec system. Curr Opin Microbiol 1: 216-222
8. Emsley P, Charles IG, Fairweather NF, Isaacs NW (1996) Structure of Bordetella pertussis virulence factor P.69 pertactin. Nature 381: 90-92.
9. Filloux A, Michel G, Bally M (1998) GSP-dependent protein secretion in Gram-negative bacteria: the Xcp system of Pseudomonas aeruginosa. FEMS Microbiol Rev 22: 177-198
10. Fink DL, Cope LD, Hansen EJ, StGeme III JW (2001) The Hemophilus influenzae Hap autotransporter is a chymotrypsin clan serine protease and undergoes autoproteolysis via an intermolecular mechanism. J Biol Chem 276: 39492-39500
11. Henderson IR, Nataro JP (2001) Virulence functions of autotransporter proteins. Infect Immun 69: 1231-1243
12. Henderson IR, Navarro-Garcia F, Nataro JP (1998) The great escape: structure and function of the autotransporter proteins. Trends Microbiol 6: 370-378
13. Hendrixson DR, de la Morena ML, Stathopoulos C, StGeme III JW (1997) Structural determinants of processing and secretion of the Haemophilus influenzae hap protein. Mol Microbiol 26: 505-518
14. Jacob-Dubuisson F, Locht C, Antoine R (2001) Two-partner secretion in Gram-negative bacteria: a thrifty, specific pathway for large virulence proteins. Mol Microbiol 40: 306-313
15. Jose J, Jähnig F, Meyer TF (1995) Common structural features of IgA1 protease-like outer membrane protein autotransporters. Mol Microbiol 18: 378-380
16. Jose J, Kramer J, Klauser T, Pohlner J, Meyer TF (1996) Absence of periplasmic DsbA oxidoreductase facilitates export of cysteine-containing passenger proteins to the Escherichia coli cell surface via the Iga beta autotransporter pathway. Gene 178: 107-110
17. Kajava AV, Chen N, Cleaver R, Kessel M, Simon MN, Willery E, Jacob-Dubuisson F, Locht C, Steven AC (2001) Beta-helix model for the filamentous haemagglutinin adhesin of Bordetella pertussis and related bacterial secretory proteins. Mol Microbiol 42: 279-292
18. β-core. The essential unit for outer membrane targeting and extracellular protein secretion. J Mol Biol 234: 579-593
19. β-mediated outer membrane transport. EMBO J 11: 2327-2335
20. Koebnik R, Locher KP, Van Gelder P (2000) Structure and function of bacterial outer membrane proteins: barrels in a nutshell. Mol Microbiol 37: 239-253
21. Konieczny MPJ, Benz I, Hollinderbäumer B, Beinke C, Niederweis M, Schmidt MA (2001) Modular organization of the AIDA autotransporter translocator: the N-terminal β1-domain is surface-exposed and stabilizes the transmembrane β2-domain. Antonie van Leeuwenhoek 80: 19-34
22. Koronakis V, Sharff A, Koronakis E, Luisi B, Hughes C (2000) Crystal structure of the bacterial membrane protein TolC central to multidrug efflux and protein export. Nature 405: 914-919
23. 158 residue of the outer membrane PhoE pore protein of Escherichia coli K12 in bacteriophage TC45 recognition and in channel characteristics. Eur J Biochem 152: 691-697
24. Lee VT, Schneewind O (2001) Protein secretion and the pathogenesis of bacterial infections. Genes Dev 15: 1725-1752
25. Loveless BJ, Saier Jr MH (1997) A novel family of channelforming, autotransporting, bacterial virulence factors. Mol Membr Biol 14: 113-123
26. Maurer J, Jose J, Meyer TF (1997) Autodisplay: one-component system for efficient surface display and release of soluble recombinant proteins from Escherichia coli. J Bacteriol 179: 794-804
27. Ohnishi Y, Nishiyama M, Horinouchi S, Beppu T (1994) Involvement of the COOH-terminal pro-sequence of Serratia marcescens serine protease in the folding of the mature enzyme. J Biol Chem 269: 32800-32806
28. Oliver DC, Huang G, Nodel E, Pleasance S, Fernandez RC (2003) A conserved region within the Bordetella pertussis autotransporter BrkA is necessary for folding of its passenger domain. Mol Microbiol 47: 1367-1383
29. Otwinowski Z, Minor W (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol 276: 307-326
30. Pohlner J, Halter R, Beyreuther K, Meyer TF (1987) Gene structure and extracellular secretion of Neisseria gonorrhoeae IgA protease. Nature 325: 458-462
31. Purdy GE, Hong M, Payne SM (2002) Shigella flexneri DegP facilitates IcsA surface expression and is required for efficient intercellular spread. Infect Immun 70: 6355-6364
32. Schulz GE (2002) The structure of bacterial outer membrane proteins. Biochim Biophys Acta 1565: 308-317
33. Shannon JL, Fernandez RC (1999) The C-terminal domain of the Bordetella pertussis autotransporter BrkA forms a pore in lipid bilayer membranes. J Bacteriol 181: 5838-5842
34. Sijbrandi R, Urbanus ML, ten Hagen-Jongman CM, Bernstein HD, Oudega B, Otto BR, Luirink J (2003) SRP-mediated targeting and Sec-dependent translocation of an extracellular Escherichia coli protein. J Biol Chem 278: 4654-4659
35. Suhr M, Benz I, Schmidt MA (1996) Processing of the AIDA-I precursor: removal of AIDAc and evidence for the outer membrane anchoring as a beta-barrel structure. Mol Microbiol 22: 31-42
36. Terwilliger TC (2002) Automated structure solution, density modification and model building. Acta Crystallogr D 58: 1937-1940
37. Van Gelder P, Dumas F, Winterhalter M (2000) Understanding the function of bacterial outer membrane channels by reconstitution into black lipid membranes. Biophys Chem 85: 153-167
38. Van Gelder P, Saint N, van Boxtel R, Rosenbusch JP, Tommassen J (1997) Pore functioning of the outer membrane protein PhoE of Escherichia coli: mutagenesis of the constriction loop L3. Protein Eng 10: 699-706
39. van Ulsen P, van Alphen L, Hopman CT, van der Ende A, Tommassen J (2001) In vivo expression of Neisseria meningitidis proteins homologous to the Haemophilus influenzae Hap and Hia autotransporters. FEMS Immunol Med Microbiol 32: 53-64
40. van Ulsen P, van Alphen L, ten Hove J, Fransen F, van der Ley P, Tommassen J (2003) A Neisserial autotransporter NalP modulating the processing of other autotransporters. Mol Microbiol 50: 1017-1030
41. Veiga E, de Lorenzo V, Fernandez LA (1999) Probing secretion and translocation of a β-autotransporter using a reporter single-chain Fv as a cognate passenger domain. Mol Microbiol 33: 1232-1243
42. Veiga E, Sugawara E, Nikaido H, de Lorenzo V, Fernandez LA (2002) Export of autotransported proteins proceeds through an oligomeric ring shaped by C-terminal domains. EMBO J 21: 2122-2131
43. 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
44. Yen MR, Peabody CR, Partovi SM, Zhai Y, Tseng YH, Saier Jr MH (2002) Protein-translocating outer membrane porins of Gram-negative bacteria. Biochim Biophys Acta 1562: 6-31