Disulfide bond-mediated passenger domain stalling as a structural probe of autotransporter outer membrane secretion in vivo

Methods in Enzymology

Volumn 492, Issue , 2011, Pages 233-251

  Renn, Jonathan P ^a,b   Clark, Patricia L ^a  

^a UNIVERSITY OF NOTRE DAME   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYSTEINE; MERCAPTOETHANOL; PROTEIN AUTOTRANSPORTER; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

AMINO TERMINAL SEQUENCE; BACTERIAL VIRULENCE; CARBOXY TERMINAL SEQUENCE; CRYSTAL STRUCTURE; CYTOPLASM; DISULFIDE BOND; FLUORESCENCE MICROSCOPY; IN VIVO STUDY; NONHUMAN; OUTER MEMBRANE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN SECRETION; REVIEW; WILD TYPE;

NEGIBACTERIA;

EID: 79951991133     PISSN: 00766879     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-12-381268-1.00030-6     Document Type: Chapter

References (52)

1. Bardwell, J. C. (1994). Building bridges: Disulphide bond formation in the cell. Mol. Microbiol. 14, 199-205.
2. Barnard, T. J., et al. (2007). Autotransporter structure reveals intra-barrel cleavage followed by conformational changes. Nat. Struct. Mol. Biol. 14, 1214-1220.
3. Benz, I., and Schmidt, M. A. (1992). AIDA-I, the adhesin involved in diffuse adherence of the diarrhoeagenic Escherichia coli strain 2787 (O126:H27), is synthesized via a precursor molecule. Mol. Microbiol. 6, 1539-1546.
4. Bernstein, H. D. (2007). Are bacterial 'autotransporters' really transporters? Trends Microbiol. 15, 441-447.
5. Cover, T. L., and Blaser, M. J. (1992). Purification and characterization of the vacuolating toxin from Helicobacter pylori. J. Biol. Chem. 267, 10570-10575.
6. Dautin, N., and Bernstein, H. D. (2007). Protein secretion in Gram-negative bacteria via the autotransporter pathway. Annu. Rev. Microbiol. 61, 89-112.
7. Dautin, N., et al. (2007). Cleavage of a bacterial autotransporter by an evolutionarily convergent autocatalytic mechanism. EMBO J. 26, 1942-1952. (Pubitemid 46624049)
8. Dutta, P. R., et al. (2003). Structure-function analysis of the enteroaggregative Escherichia coli plasmid-encoded toxin autotransporter using scanning linker mutagenesis. J. Biol. Chem. 278, 39912-39920.
9. Emsley, P., et al. (1996). Structure of Bordetella pertussis virulence factor P.69 pertactin. Nature 381, 90-92. (Pubitemid 26130010)
10. Eslava, C., et al. (1998). Pet, an autotransporter enterotoxin from enteroaggregative Escherichia coli. Infect. Immun. 66, 3155-3163.
11. Galan, J. E., and Collmer, A. (1999). Type III secretion machines: Bacterial devices for protein delivery into host cells. Science 284, 1322-1328. (Pubitemid 29289652)
12. Gangwer, K. A., et al. (2007). Crystal structure of the Helicobacter pylori vacuolating toxin p55 domain. Proc. Natl. Acad. Sci. USA 104, 16293-16298.
13. Henderson, I. R., et al. (1998). The great escape: Structure and function of the autotransporter proteins. Trends Microbiol. 6, 370-378. (Pubitemid 28473198)
14. Henderson, I. R., et al. (2004). Type V protein secretion pathway: The autotransporter story. Microbiol. Mol. Biol. Rev. 68, 692-744.
15. Ieva, R., and Bernstein, H. D. (2009). Interaction of an autotransporter passenger domain with BamA during its translocation across the bacterial outer membrane. Proc. Natl. Acad. Sci. USA 106, 19120-19125.
16. Ieva, R., et al. (2008). Incorporation of a polypeptide segment into the beta-domain pore during the assembly of a bacterial autotransporter. Mol. Microbiol. 67, 188-201.
17. Jain, S., and Goldberg, M. B. (2007). Requirement for YaeT in the outer membrane assembly of autotransporter proteins. J. Bacteriol. 189, 5393-5398.
18. Johnson, T. A., et al. (2009). Active-site gating regulates substrate selectivity in a chymotrypsin-like serine protease: The structure of Haemophilus influenzae immunoglobulin A1 protease. J. Mol. Biol. 389, 559-574.
19. Jong, W. S., et al. (2007). Limited tolerance towards folded elements during secretion of the autotransporter Hbp. Mol. Microbiol. 63, 1524-1536.
20. Junker, M., et al. (2006). Pertactin beta-helix folding mechanism suggests common themes for the secretion and folding of autotransporter proteins. Proc. Natl. Acad. Sci. USA 103, 4918-4923.
21. Junker, M., et al. (2009). Vectorial transport and folding of an autotransporter virulence protein during outer membrane secretion. Mol. Microbiol. 71, 1323-1332.
22. Kenjale, R., et al. (2009). Structural determinants of autoproteolysis of the Haemophilus influenzae Hap autotransporter. Infect. Immun. 77, 4704-4713.
23. Klauser, T., et al. (1990). Extracellular transport of cholera toxin B subunit using Neisseria IgA protease beta-domain: Conformation-dependent outer membrane translocation. EMBO J. 9, 1991-1999.
24. Klauser, T., et al. (1992). Selective extracellular release of cholera toxin B subunit by Escherichia coli: Dissection of Neisseria Iga beta-mediated outer membrane transport. EMBO J. 11, 2327-2335.
25. Kostakioti, M., and Stathopoulos, C. (2004). Functional analysis of the Tsh autotransporter from an avian pathogenic Escherichia coli strain. Infect. Immun. 72, 5548-5554.
26. Kostakioti, M., and Stathopoulos, C. (2006). Role of the alpha-helical linker of the C-terminal translocator in the biogenesis of the serine protease subfamily of autotransporters. Infect. Immun. 74, 4961-4969.
27. Leininger, E., et al. (1991). Pertactin, an Arg-Gly-Asp-containing Bordetella pertussis surface protein that promotes adherence of mammalian cells. Proc. Natl. Acad. Sci. USA 88, 345-349.
28. Letley, D. P., et al. (2006). Paired cysteine residues are required for high levels of the Helicobacter pylori autotransporter VacA. Microbiology 152, 1319-1325.
29. Loveless, B. J., and Saier, M. H., Jr. (1997). A novel family of channel-forming, autotransporting, bacterial virulence factors. Mol. Membr. Biol. 14, 113-123.
30. Mansell, T. J., et al. (2008). Engineering the protein folding landscape in gram-negative bacteria. Curr. Protein Pept. Sci. 9, 138-149.
31. Nishimura, K., et al. (2010). Autotransporter passenger proteins: Virulence factors with common structural themes. J. Mol. Med. 88, 451-458.
32. Oliver, D. C., et al. (2003). A conserved region within the Bordetella pertussis autotransporter BrkA is necessary for folding of its passenger domain. Mol. Microbiol. 47, 1367-1383.
33. Oomen, C. J., et al. (2004). Structure of the translocator domain of a bacterial autotransporter. EMBO J. 23, 1257-1266. (Pubitemid 38524998)
34. Otto, B. R., et al. (1998). Characterization of a hemoglobin protease secreted by the pathogenic Escherichia coli strain EB1. J. Exp. Med. 188, 1091-1103.
35. Otto, B. R., et al. (2005). Crystal structure of hemoglobin protease, a heme binding autotransporter protein from pathogenic Escherichia coli. J. Biol. Chem. 280, 17339-17345.
36. Pohlner, J., et al. (1987). Gene structure and extracellular secretion of Neisseria gonorrhoeae IgA protease. Nature 325, 458-462. (Pubitemid 17056417)
37. Rego, A. T., et al. (2010). Two-step and one-step secretion mechanisms in gram-negative bacteria: Contrasting the type IV secretion system and the chaperone-usher pathway of pilus biogenesis. Biochem. J. 425, 475-488.
38. Remaut, H., et al. (2008). Fiber formation across the bacterial outer membrane by the chaperone/usher pathway. Cell 133, 640-652. (Pubitemid 351636304)
39. Renn, J. P., and Clark, P. L. (2008). A conserved stable core structure in the passenger domain beta-helix of autotransporter virulence proteins. Biopolymers 89, 420-427.
40. Rietsch, A., et al. (1996). An in vivo pathway for disulfide bond isomerization in Escherichia coli. Proc. Natl. Acad. Sci. USA 93, 13048-13053.
41. Saier, M. H., Jr. (2006). Protein secretion and membrane insertion systems in gram-negative bacteria. J. Membr. Biol. 214, 75-90.
42. Sauri, A., et al. (2009). The Bam (Omp85) complex is involved in secretion of the autotransporter haemoglobin protease. Microbiology 155, 3982-3991.
43. Savage, D. C. (1977). Microbial ecology of the gastrointestinal tract. Annu. Rev. Microbiol. 31, 107-133.
44. Sijbrandi, R., et al. (2003). Signal recognition particle (SRP)-mediated targeting and Sec-dependent translocation of an extracellular Escherichia coli protein. J. Biol. Chem. 278, 4654-4659.
45. Skillman, K. M., et al. (2005). Efficient secretion of a folded protein domain by a monomeric bacterial autotransporter. Mol. Microbiol. 58, 945-958.
46. St Geme, J. W., 3rd, and Cutter, D. (2000). The Haemophilus influenzae Hia adhesin is an autotransporter protein that remains uncleaved at the C terminus and fully cell associated. J. Bacteriol. 182, 6005-6013.
47. Steinhauer, J., et al. (1999). The unipolar Shigella surface protein IcsA is targeted directly to the bacterial old pole: IcsP cleavage of IcsA occurs over the entire bacterial surface. Mol. Microbiol. 32, 367-377.
48. Tan, J. T., and Bardwell, J. C. (2004). Key players involved in bacterial disulfide-bond formation. Chembiochem 5, 1479-1487.
49. Thanassi, D. G., et al. (2005). Protein secretion in the absence of ATP: The autotransporter, two-partner secretion and chaperone/usher pathways of Gram-negative bacteria (review). Mol. Membr. Biol. 22, 63-72.
50. van den Berg, B. (2010). Crystal structure of a full-length autotransporter. J. Mol. Biol. 396, 627-633.
51. van Ulsen, P., et al. (2003). A Neisserial autotransporter NalP modulating the processing of other autotransporters. Mol. Microbiol. 50, 1017-1030.
52. Voulhoux, R., et al. (2003). Role of a highly conserved bacterial protein in outer membrane protein assembly. Science 299, 262-265. (Pubitemid 36125214)