Cleavage of a bacterial autotransporter by an evolutionarily convergent autocatalytic mechanism

EMBO Journal

Volumn 26, Issue 7, 2007, Pages 1942-1952

  Dautin, Nathalie ^a   Barnard, Travis J ^a   Anderson, D Eric ^b   Bernstein, Harris D ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

Author keywords

Autotransporters; E. coli; Enzyme mechanism; Protease; Secretion

Indexed keywords

ASPARAGINE; ASPARTIC ACID; BACTERIAL PROTEIN; ESCHERICHIA COLI SECRETED PROTEIN B; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CATALYSIS; CONTROLLED STUDY; CYCLIZATION; IN VITRO STUDY; MUTATIONAL ANALYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN PURIFICATION;

AMINO ACID SEQUENCE; ASPARAGINE; ASPARTIC ACID; CATALYSIS; CONSERVED SEQUENCE; DETERGENTS; DNA MUTATIONAL ANALYSIS; ESCHERICHIA COLI; ESCHERICHIA COLI O157; EVOLUTION, MOLECULAR; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; PROTEIN PRECURSORS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STRUCTURE, TERTIARY; SOLUTIONS; SUCCINIMIDES;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; EUKARYOTA; MIRIDAE;

EID: 34247238897     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/sj.emboj.7601638     Document Type: Article

References (35)

1. Akiyama Y, Ito K (1990) SecY protein, a membrane-embedded secretion factor of E. coli, is cleaved by the OmpT protease in vitro. Biochem Biophys Res Commun 167: 711-715
2. Amitai G, Dassa B, Pietrokovski S (2004) Protein splicing of inteins with atypical glutamine and aspartate C-terminal residues. J Biol Chem 279: 3121-3131
3. Ansaldi M, Lepelletier M, Mejean V (1996) Site-specific mutagenesis by using an accurate recombinant polymerase chain reaction method. Anal Biochem 234: 110-111
4. Bagos PG, Liakopoulos TD, Spyropoulos IC, Hamodrakas SJ (2004) PRED-TMBB: a web server for predicting the topology of β-barrel outer membrane proteins. Nucleic Acids Res 32: W400-W404
5. Barrett AJ, Rawlings ND, Woessner JF (2003) The Handbook of Proteolytic Enzymes, 2nd edn. Elsevier (Amsterdam): Academic Press
6. Charles I, Fairweather N, Pickard D, Beesley J, Anderson R, Dougan G, Roberts M (1994) Expression of the Bordetella pertussis P.69 pertactin adhesin in Escherichia coli: fate of the carboxy-terminal domain. Microbiology 140: 3301-3308
7. Chen P, Tsuge H, Almassy RJ, Gribdskov CL, Katoh S, Vanderpool DL, Margosiak SA, Pinko C, Matthews DA, Kan CC (1996) Structure of the human cytomegalovirus protease catalytic domain reveals a novel serine protease fold and catalytic triad. Cell 86: 835-843
8. Dutta PR, Cappello R, Navarro-Garcia F, Nataro JP (2002) Functional comparison of serine protease autotransporters of Enterobacteriaceae. Infect Immun 70: 7105-7113
9. Egile C, d'Hauteville H, Parsot C, Sansonetti PJ (1997) SopA, the outer membrane protease responsible for polar localization of IcsA in Shigella flexneri. Mol Microbiol 23: 1063-1073
10. Eslava C, Navarro-Garcia F, Czeczulin JR, Henderson IR, Cravioto A, Nataro JP (1998) Pet, an autotransporter protein enterotoxin from enteroaggregative Escherichia coli. Infect Immun 66: 3155-3163
11. Ferris HU, Furukawa Y, Minamino T, Kroetz MB, Kihara M, Namba K, Macnab RM (2005) FlhB regulates ordered export of flagellar components via autocleavage mechanism. J Biol Chem 280: 41236-41242
12. Finn TM, Amsbaugh DF (1998) Vag8, a Bordetella pertussis bvg-regulated protein. Infect Immun 66: 3985-3989
13. Henderson IR, Czeczulin J, Eslava C, Noriega F, Nataro JP (1999) Characterization of Pic, a secreted protease of Shigella flexneri and enteroaggregative Escherichia coli. Infect Immun 67: 5587-5596
14. Henderson IR, Navarro-Garcia F, Desvaux M, Fernandez RC, Ala'Aldeen D (2004) Type V protein secretion pathway: the autotransporter story. Microbiol Mol Biol Rev 68: 692-744
15. Hendrixson DR, de la Morena ML, Stathopoulos C, St Geme III JW (1997) Structural determinants of processing and secretion of the Haemophilus influenzae Hap protein. Mol Microbiol 26: 505-518
16. Keiler KC, Sauer RT (1995) Identification of active site residues of the Tsp protease. J Biol Chem 270: 28864-28868
17. Middendorf B, Stübs D, Guiso N, Deppisch H, Gross R, Fuchs TM (2005) Phg, a novel member of the autotransporter family present in Bordetella species. Microbiol Res 160: 329-336
18. Oomen CJ, van Ulsen P, van Gelder P, Feijen M, Tommassen J, Gros P (2004) Structure of the translocator domain of a bacterial autotransporter. EMBO J 23: 1257-1266
19. Patel SK, Dotson J, Allen KP, Fleckenstein JM (2004) Identification and molecular characterization of EatA, an autotransporter protein of enterotoxigenic Escherichia coli. Infect Immun 72: 1786-1794
20. Pohlner J, Halter R, Beyreuther K, Meyer TF (1987) Gene structure and extracellular secretion of Neisseria gonorrhoeae IgA protease. Nature 325: 458-462
21. Schneemann A, Zhong W, Gallagher TM, Rueckert RR (1992) Maturation cleavage required for infectivity of a nodavirus. J Virol 66: 6728-6734
22. Serruto D, Adu-Bobie J, Scarselli M, Veggi D, Pizza M, Rappuoli R, Arico B (2003) Neisseria meningitidis App: a new adhesin with autocatalytic serine protease activity. Mol Microbiol 48: 323-334
23. Shere KD, Sallustio S, Manessis A, D'Aversa TG, Goldberg MB (1997) Disruption of IcsP, the major Shigella protease that cleaves IcsA, accelerates actin-based motility. Mol Microbiol 25: 451-462
24. Skillman KM, Barnard TJ, Peterson JH, Ghirlando R, Bernstein HD (2005) Efficient secretion of a folded protein domain by a monomeric bacterial autotransporter. Mol Microbiol 58: 945-958
25. Stein M, Kenny B, Stein MA, Finlay BB (1996) Characterization of EspC, a 110-kilodalton protein secreted by enteropathogenic Escherichia coli which is homologous to members of the immunoglobulin A protease-like family of secreted proteins. Infect Immun 178: 6546-6554
26. Szabady RL, Peterson JH, Skillman KM, Bernstein HD (2005) An unusual signal peptide facilitates the late steps in the biogenesis of a bacterial autotransporter. Proc Natl Acad Sci USA 102: 221-226
27. Taylor DJ, Johnson JE (2005) Folding and particle assembly are disrupted by single-point mutations near the autocatalytic cleavage site of Nudaurelia capensis ω virus capsid protein. Protein Sci 14: 401-408
28. Taylor DJ, Krishna NK, Canady MA, Schneemann A, Johnson JE (2002) Large-scale, pH-dependent, quaternary structure changes in an RNA virus capsid are reversible in the absence of subunit autoproteolysis. J Virol 76: 9972-9980
29. Turner DP, Wooldridge KG, Ala'Aldeen DA (2002) Autotransporter serine protease A of Neisseria meningitidis: an immunogenic, surface-exposed outer membrane, and secreted protein. Infect Immun 70: 4447-4461
30. Ulbrandt ND, Newitt JA, Bernstein HD (1997) The E. coli signal recognition particle is required for the insertion of a subset of inner membrane proteins. Cell 88: 187-196
31. 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
32. Vandeputte-Rutten L, Kramer RA, Kroon J, Dekker N, Egmond MR, Gros P (2001) Crystal structure of the outer membrane protease OmpT from Escherichia coli suggests a novel catalytic site. EMBO J 20: 5033-5039
33. Velarde JJ, Nataro JP (2004) Hydrophobic residues of the autotransporter EspP linker domain are important for outer membrane translocation of its passenger. J Biol Chem 279: 31495-31504
34. Wolfe MS, Xia W, Ostaszewski BL, Diehl TS, Kimberly WT, Selkoe DJ (1999) Two transmembrane aspartates in presenilin-1 required for presinilin endoproteolysis and gamma-secretase activity. Nature 398: 513-517
35. Zlotnick A, Reddy VS, Dasgupta R, Schneemann A, Ray Jr WJ, Rueckert RR, Johnson JE (1994) Capsid assembly in a family of animal viruses primes an autoproteolytic maturation that depends on a single aspartic residue. J Biol Chem 269: 13680-13684