A Novel Intein-Like Autoproteolytic Mechanism in Autotransporter Proteins

Journal of Molecular Biology

Volumn 402, Issue 4, 2010, Pages 645-656

  Tajima, Nami ^a   Kawai, Fumihiro ^a   Park, Sam Yong ^a   Tame, Jeremy R H ^a  

^a YOKOHAMA CITY UNIVERSITY   (Japan)

Author keywords

b barrel; Pathogen; Proteolytic mechanism; Secretion; Virulence factor

Indexed keywords

ASPARAGINE; ASPARTIC ACID; CARRIER PROTEIN; INTEIN; MEMBRANE PROTEIN; MUTANT PROTEIN; POLYPEPTIDE; VIRULENCE FACTOR; BACTERIAL PROTEIN; HEMOGLOBIN-BINDING PROTEIN, BACTERIA; PROTEINASE; SIGNAL PEPTIDE;

AMINO TERMINAL SEQUENCE; ARTICLE; BETA SHEET; CARBOXY TERMINAL SEQUENCE; CRYSTAL STRUCTURE; CYTOPLASM; GRAM NEGATIVE BACTERIUM; MUTATION; NONHUMAN; OUTER MEMBRANE; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN SECRETION; CHEMISTRY; MOLECULAR CLONING; PROTEIN CONFORMATION; SITE DIRECTED MUTAGENESIS; X RAY CRYSTALLOGRAPHY;

NEGIBACTERIA;

BACTERIAL PROTEINS; CARRIER PROTEINS; CLONING, MOLECULAR; CRYSTALLOGRAPHY, X-RAY; ENDOPEPTIDASES; INTEINS; MUTAGENESIS, SITE-DIRECTED; PROTEIN CONFORMATION; PROTEIN SORTING SIGNALS;

EID: 77956916073     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2010.06.068     Document Type: Article

References (37)

1. Jacob-Dubuisson F., Fernandez R., Coutte L. Protein secretion through autotransporter and two-partner pathways. Biochim. Biophys. Acta 2004, 1694:235-257.
2. Henderson I.R., Navarro-Garcia F., Nataro J.P. The great escape: structure and function of the autotransporter proteins. Trends Microbiol. 1998, 6:370-378.
3. Henderson I.R., Navarro-Garcia F., Desvaux M., Fernandez R.C., Ala'Aldeen D. Type V protein secretion pathway: the autotransporter story. Microbiol. Mol. Biol. Rev. 2004, 68:692-744.
4. Desvaux M., Parham N.J., Henderson I.R. Type V protein secretion: simplicity gone awry?. Curr. Issues Mol. Biol. 2004, 6:111-124.
5. Dautin N., Bernstein H.D. Protein secretion in Gram-negative bacteria via the autotransporter pathway. Annu. Rev. Microbiol. 2007, 61:89-112.
6. Pohlner J., Halter R., Beyreuther K., Meyer T.F. Gene structure and extracellular secretion of Neisseria gonorrhoeae IgA protease. Nature 1987, 325:458-462.
7. Voulhoux R., Bos M.P., Geurtsen J., Mols M., Tommassen J. Role of a highly conserved bacterial protein in outer membrane protein assembly. Science 2003, 299:262-265.
8. Wu T., Malinverni J., Ruiz N., Kim S., Silhavy T.J., Kahne D. Identification of a multicomponent complex required for outer membrane biogenesis in Escherichia coli. Cell 2005, 121:235-245.
9. Oliver D.C., Huang G., Nodel E., Pleasance S., Fernandez R.C. A conserved region within the Bordetella pertussis autotransporter BrkA is necessary for folding of its passenger domain. Mol. Microbiol. 2003, 47:1367-1383.
10. Ohnishi Y., Nishiyama M., Horinouchi S., Beppu T. Involvement of the COOH-terminal pro-sequence of Serratia marcescens serine protease in the folding of the mature enzyme. J. Biol. Chem. 1994, 269:32800-32806.
11. Berthiaume F., Rutherford N., Mourez M. Mutations affecting the biogenesis of the AIDA-I autotransporter. Res. Microbiol. 2007, 158:348-354.
12. Jose J., Meyer T.F. The autodisplay story, from discovery to biotechnical and biomedical applications. Microbiol. Mol. Biol. Rev. 2007, 71:600-619.
13. Meng G., Surana N.K., St Geme J.W., Waksman G. Structure of the outer membrane translocator domain of the Haemophilus influenzae Hia trimeric autotransporter. EMBO J. 2006, 25:2297-2304.
14. Oomen C.J., Van Ulsen P., Van Gelder P., Feijen M., Tommassen J., Gros P. Structure of the translocator domain of a bacterial autotransporter. EMBO J. 2004, 23:1257-1266.
15. Otto B.R., Sijbrandi R., Luirink J., Oudega B., Heddle J.G., Mizutani K., et al. Crystal structure of hemoglobin protease, a heme binding autotransporter protein from pathogenic Escherichia coli. J. Biol. Chem. 2005, 280:17339-17345.
16. Jong W.S., ten Hagen-Jongman C.M., den Blaauwen T., Slotboom D.J., Tame J.R.H., Wickstrom D., et al. Limited tolerance towards folded elements during secretion of the autotransporter Hbp. Mol. Microbiol. 2007, 63:1524-1536.
17. Barnard T.J., Dautin N., Lukacik P., Bernstein H.D., Buchanan S.K. Autotransporter structure reveals intra-barrel cleavage followed by conformational changes. Nat. Struct. Mol. Biol. 2007, 14:1214-1220.
18. van den Berg B. Crystal structure of a full-length autotransporter. J. Mol. Biol. 2010, 396:627-633.
19. Dautin N., Barnard T.J., Anderson D.E., Bernstein H.D. Cleavage of a bacterial autotransporter by an evolutionarily convergent autocatalytic mechanism. EMBO J. 2007, 26:1942-1952.
20. Kostakioti M., Stathopoulos C. Role of the alpha-helical linker of the C-terminal translocator in the biogenesis of the serine protease subfamily of autotransporters. Infect. Immun. 2006, 74:4961-4969.
21. Schulz G.E. Beta-barrel membrane proteins. Curr. Opin. Struct. Biol. 2000, 10:443-447.
22. Provence D.L., Curtiss R. Isolation and characterization of a gene involved in hemagglutination by an avian pathogenic Escherichia coli strain. Infect. Immun. 1994, 62:1369-1380.
23. Heaton A.L., Armentrout P.B. Thermodynamics and mechanism of protonated asparagine decomposition. J. Am. Soc. Mass Spectrom. 2009, 20:852-866.
24. Yen Y.T., Tsang C., Cameron T.A., Ankrah D.O., Rodou A., Stathopoulos C. Importance of conserved residues of the serine protease autotransporter bβ-domain in passenger domain processing and bβ-barrel assembly. Infect. Immun. 2010, 78:3516-3528.
25. Paulus H. Protein splicing and related forms of protein autoprocessing. Annu. Rev. Biochem. 2000, 69:447-496.
26. Sun P., Ye S., Ferrandon S., Evans T.C., Xu M.Q., Rao Z. Crystal structures of an intein from the split dnaE gene of Synechocystis sp. PCC6803 reveal the catalytic model without the penultimate histidine and the mechanism of zinc ion inhibition of protein splicing. J. Mol. Biol. 2005, 353:1093-1105.
27. a shift mechanism. J. Am. Chem. Soc. 2009, 131:11581-11589.
28. Ding Y., Xu M.Q., Ghosh I., Chen X., Ferrandon S., Lesage G., Rao Z. Crystal structure of a mini-intein reveals a conserved catalytic module involved in side chain cyclization of asparagine during protein splicing. J. Biol. Chem. 2003, 278:39133-39142.
29. Taylor D.J., Johnson J.E. Folding and particle assembly are disrupted by single-point mutations near the autocatalytic cleavage site of Nudaurelia capensis omega virus capsid protein. Protein Sci. 2005, 14:401-408.
30. Taylor D.J., Krishna N.K., Canady M.A., Schneemann A., Johnson J.E. Large-scale, pH-dependent, quaternary structure changes in an RNA virus capsid are reversible in the absence of subunit autoproteolysis. J. Virol. 2002, 76:9972-9980.
31. Velarde J.J., Nataro J.P. Hydrophobic residues of the autotransporter EspP linker domain are important for outer membrane translocation of its passenger. J. Biol. Chem. 2004, 279:31495-31504.
32. Skillman K.M., Barnard T.J., Peterson J.H., Ghirlando R., Bernstein H.D. Efficient secretion of a folded protein domain by a monomeric bacterial autotransporter. Mol. Microbiol. 2005, 58:945-958.
33. Khalid S., Sansom M.S. Molecular dynamics simulations of a bacterial autotransporter: NalP from Neisseria meningitidis. Mol. Membr. Biol. 2006, 23:499-508.
34. Vagin A., Teplyakov A. An approach to multi-copy search in molecular replacement. Acta Crystallogr. Sect. D 2000, 56:1622-1624.
35. Emsley P., Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr. Sect. D 2004, 60:2126-2132.
36. Murshudov G.N., Vagin A.A., Lebedev A., Wilson K.S., Dodson E.J. Efficient anisotropic refinement of macromolecular structures using FFT. Acta Crystallogr. Sect. D 1999, 55:247-255.
37. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. Sect. D 1994, 50:760-763. CCP4.