The chaperone-assisted membrane release and folding pathway is sensed by two signal transduction systems

EMBO Journal

Volumn 16, Issue 21, 1997, Pages 6394-6406

  Jones, C Hal ^a   Danese, Paul N ^b   Pinkner, Jerome S ^a   Silhavy, Thomas J ^b   Hultgren, Scott J ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b PRINCETON UNIVERSITY   (United States)

Author keywords

Chaperone; Periplasmic stress; Periplasmic targeting; Protein folding; Signal transduction

Indexed keywords

BACTERIAL PROTEIN; CHAPERONE; PROTEIN SUBUNIT; SIGMA FACTOR;

ARTICLE; BACTERIUM PILUS; CARBOXY TERMINAL SEQUENCE; CELL GROWTH; CELL MEMBRANE; CONTROLLED STUDY; CYTOPLASM; ENTEROBACTERIACEAE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; SIGNAL TRANSDUCTION;

ADHESINS, ESCHERICHIA COLI; BACTERIAL OUTER MEMBRANE PROTEINS; BACTERIAL PROTEINS; BIOLOGICAL TRANSPORT; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; FIMBRIAE PROTEINS; FIMBRIAE, BACTERIAL; HEAT-SHOCK PROTEINS; MACROMOLECULAR SUBSTANCES; MEMBRANE PROTEINS; MODELS, BIOLOGICAL; MOLECULAR CHAPERONES; PERIPLASMIC PROTEINS; PROTEIN FOLDING; PROTEIN KINASES; RECOMBINANT FUSION PROTEINS; SERINE ENDOPEPTIDASES; SIGMA FACTOR; SIGNAL TRANSDUCTION; SPHEROPLASTS; TRANSCRIPTION FACTORS;

BACTERIA (MICROORGANISMS); ENTEROBACTERIACEAE;

EID: 0030775342     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/16.21.6394     Document Type: Article

References (46)

1. Bullitt, E., Jones, C.H., Striker, R., Soto, G., Jacob-Dubuisson, F., Pinkner, J., Wick, M.-J., Makowski, L. and Hultgren, S.J. (1996) Development of pilus organelle subassemblies in vitro depends on chaperone uncapping of a beta zipper. Proc. Natl Acad. Sci. USA. 93, 12890-12895.
2. Cosma, C.L., Danese, P.N., Carlson, J.H., Silhavy, T.J. and Snyder, W.B. (1995) Mutational activation of the Cpx signal transduction pathway of Escherichia coli suppresses the toxicity conferred by certain envelope-associated stresses. Mol. Microbiol., 18, 491-505.
3. Danese, P.N. and Silhavy, T.J. (1997) The σE and the Cpx signal transduction systems control the synthesis of periplasmic protein-folding enzymes in Escherichia coli. Genes Dev. 11, 1183-1193.
4. Danese, P.N., Snyder, W.B., Cosma, C.L., Davis, L.J.B. and Silhavy, T.J. (1995) The Cpx two-component signal transduction pathway of Escherichia coli regulates degP transcription. Genes Dev., 9, 387-398.
5. De Las Penas, A., Connolly, L. and Gross, C.A. (1997) The σE-mediated response to extracytoplasmic stress in Escherichia coli is transduced by RseA and RseB, two negative regulators of σE. Mol. Microbiol., 24, 373-385.
6. Dodd, D.C., Bassford, P.J.J. and Eisenstein, B.I. (1984) Dependence of secretion and assembly of type 1 fimbrial subunits of Escherichia coli on normal protein transport. J. Bacteriol., 159, 1077-1079.
7. Dodson, K.W., Jacob-Dubuisson, F., Striker, R.T., and Hultgren, S.J. (1993) Outer membrane PapC usher discriminately recognizes periplasmic chaperone-pilus subunit complexes. Proc. Natl Acad. Sci. USA. 90, 3670-3674.
8. Furste, J.P., Pansegrau, W., Frank, R., Blocker, H., Scholz, P., Bagdasarian, M. and Lanka, E. (1986) Molecular cloning of the plasmid RP4 primase region in a multi-host-range tacP expression sector. Gene. 48, 119-131.
9. Hanahan, D. (1983) Studies in transformation of Escherichia coli with plasmids. J. Mol Biol., 166, 557-580.
10. Hultgren, S.J., Lindberg, F., Magnusson, G., Kihlberg, J., Tennent, J.M. and Normark, S. (1989) The PapG adhesin of uropathogenic Escherichia coli contains separate regions for receptor binding and for the incorporation into the pilus. Proc. Natl Acad. Sci. USA. 86, 4357-4361.
11. Hullgren, S.J., Normark, S. and Abraham, S.N. (1991) Chaperone-assisted assembly and molecular architecture of adhesive pili. Annu. Rev. Microbiol., 45, 383-415.
12. Hultgren, S.J., Abraham, S.N., Caparon, M.G., Falk, P., St Geme, J.W. and Normark, S. (1993) Pilus and non-pilus bacterial adhesins: assembly and function in cell recognition. Cell. 73, 887-901.
13. Hultgren, S.J., Jones, C.H. and Normark, S.N. (1996) Bacterial adhesins and their assembly. In Neidhardt, F.C. (ed.). Escherichia coli and Salmonella: Cellular and Molecular Biology. ASM Press, Washington, DC, pp. 2730-2756.
14. Hung, D.L., Knight, S.D., Woods, R.M., Pinkner, J.S. and Hultgren, S.J. (1996) Molecular basis of two subfamilies of immunoglobulin-like chaperones. EMBO J., 15, 3792-3805.
15. Jacob-Dubuisson, F., Heuser, J., Dodson, K., Normark, S. and Hultgren, S.J. (1993) Initiation of assembly and association of the structural elements of a bacterial pilus depend on two specialized tip proteins. EMBO J., 12, 837-847.
16. Jacob-Dubuisson, F., Pinkner, J., Xu, Z., Striker, R., Padmanhaban, A. and Hultgren, S.J. (1994) PapD chaperone function in pilus biogenesis depends on oxidant and chaperone-like activities of DsbA. Proc. Natl Acad. Sci. USA. 91, 11552-11556.
17. Jones, C.H., Pinkner, J.S., Nicholes, A.V., Slonim, L.N., Abraham, S.N. and Hultgren, S.J. (1993) FimC is a periplasmic PapD-like chaperone that directs assembly of type 1 pili in bacteria. Proc. Natl Acad. Sci. USA. 90, 8397-8401.
18. Kolmar, H., Waller, P.R.H. and Sauer, R.T. (1996) The DegP and DegQ periplasmic endoproteases of Escherichia coli: specificity for cleavage sites and substrate conformation. J. Bacteriol., 178, 5925-5929.
19. Kuehn, M.J., Normark, S. and Hultgren, S.J. (1991) Immunoglobulin-like PapD chaperone caps and uncaps interactive surfaces of nascently translocated pilus subunits. Proc. Natl Acad. Sci. USA. 88, 10586-10590.
20. Kuehn, M.J., Heuser, J., Normark, S. and Hultgren, S.J. (1992) P pili in uropathogenic E. coli are composite fibres with distinct fibrillar adhesive tips. Nature. 356, 252-255.
21. Kuehn, M.J., Ogg, D.J., Kihlberg, J., Slonim, L.N., Flemmer, K., Bergfors, T. and Hultgren, S.J. (1993) Structural basis of pilus subunit recognition by the PapD chaperone. Science. 262, 1234-1241.
22. Kuroiwa, T., Sakaguchi, M., Mihara, K. and Omura, T. (1991) Systematic analysis of stop transfer sequence for microsomal membrane. J. Biol. Chem., 266, 9251-9255.
23. Lindberg, K. Tennent, J.M., Hultgren, S.J., Lund, B. and Normark, S. (1989) PapD, a periplasmic transport protein in P-pilus biogenesis. J. Bacteriol., 171, 6052-6058.
24. Lipinska, B., Zylicz, M. and Georgopoulos, C. (1990) The HtrA (DegP) protein, essential for Escherichia coli survival at high temperatures. is an endopeptidase. J. Bacteriol., 172, 1791-1797.
25. Matsuyama, S.-I., Tajima, T. and Tokuda, H. (1995) A novel periplasmic carrier protein involved in the sorting and transport of Escherichia coli lipoproteins destined for the outer membrane. EMBO J., 14, 3365-3372.
26. E. an Escherichia coli heat-inducible sigma factor, is modulated by outer membrane proteins. Genes Dev., 7, 2618-2628.
27. Missiakis, D. and Raina, S. (1997) Signal transduction pathways in response to protein misfolding in the extracytoplasmic compartments of E.coli: role of two new phophoprotein phophatases PrpA and PrpB. EMBO J., 16, 1670-1685.
28. Missiakis, D., Betton, J.-M. and Raina, S. (1996) New components of protein folding in extracytoplasmic compartments of Escherichia coli SurA, FkpA and Skp/OmpH. Mol. Microbiol. 21, 871-884.
29. Missiakis, D., Mayer, M.P., Lemaire, M., Georgopoulos, C. and Raina, S. (1997) Modulation of the Escherichia coli σE (RpoE) heat-shock transcription-factor activity by the RseA, RseB and RseC proteins. Mol. Microbiol., 24, 355-371.
30. Pogliano, J., Lynch, A.S., Belin, D., Lin, E.C.C. and Beckwith, J. (1997) Regulation of Escherichia coli cell envelope proteins involved in protein folding and degradation by the Cpx two-component system. Genes Dev. 11, 1169-1182.
31. Pugsley, A. and Possot, G. (1994) The general secretory pathway of Klebsiella oxytaca: no evidence for relocalization or assembly of pilin-like PuIG protein into a multiprotein complex. Mol. Microbiol., 10, 665-674.
32. Raina, S., Missiakas, D., Baird, L., Kumar, S. and Georgopoulos, C. (1993) Identification and transcriptional analysis of the Escherichia coli htrE operon which is homologous to pap and related pilin operons. J. Bacteriol., 175, 5009-5021.
33. Raina, S., Missiakis, D. and Georgopoulos, C. (1995) The rpoE gene encoding the sigma E (sigma 24) heat shock sigma factor of Escherichia coli. EMBO J., 14, 1043-1055.
34. Roberts, J.A. et al. (1994) The Gal α(1-4) Gal-specific tip adhesin of Escherichia coli P-fimbriae is needed for pyelonephritis to occur in the normal urinary tract. Proc. Natl Acad. Sci. USA. 91, 11889-11893.
35. Rouviere, P.E., de las Penas, A., Mecsas, J., Lu, C.Z., Rudd, K.E. and Gross, C.A. (1995) rpoE. the gene encoding the second heat-shock sigma factor, sigma E. in Escherichia coli. EMBO J., 14, 1032-1042.
36. Slauch, J.M. and Silhavy, T.J. (1991) cis-acting ompF mutations that result in OmpR-dependent constitutive expression. J. Bacteriol., 173, 4039-4048.
37. Slonim, L.N., Pinkner, J.S., Branden, C.I. and Hultgren, S.J. (1992) Interactive surface in the PapD chaperone cleft is conserved in pilus chaperone superfamily and essential in subunit recognition and assembly. EMBO J., 11, 4747-4756.
38. Snyder, W.B. and Silhavy, T.J. (1992) Enhanced export of β-galactosidase fusion proteins on prlF mutants is Ion dependent. J. Bacteriol., 174, 5661-5668.
39. Snyder, W.B., Davis, L.J., Danese, P.N., Cosma, C.L. and Silhavy, T.J. (1995) Overproduction of NlpE, a new outer membrane lipoprotein. suppresses the toxicity of periplasmic LacZ by activation of the Cpx signal transduction pathway. J. Bacteriol., 177, 4216-4223.
40. Stader, J., Benson, S.A. and Silhavy, T.J. (1986) Kinetic analysis of lamB mutant suggests the signal sequence plays multiple roles in protein export. J. Biol Chem., 261, 15075-15080.
41. Strauch, K.L. and Beckwith, J. (1988) An Escherichia coli mutation preventing degradation of abnormal periplasmic proteins. Proc. Natl Acad. Sci. USA. 85, 1576-1580.
42. Strauch, K.L., Johnson, K. and Beckwith, J. (1989) Characterization of degP, a gene required for proteolysis in the cell envelope of Escherichia coli at high temperature. J. Bacteriol., 171, 2689-2696.
43. Weis, W., Brown, J.H., Cusack, S., Paulson, J.C., Skehel, J.J. and Wiley, D.C. (1988) Structure of the influenza virus haemagglutinin complexed with its receptor, sialic acid. Nature. 333, 426-431.
44. Witholt, B., Boekhout, M., Brock, M., Kingman, J., van Heerikhuizen, H. and de Leig, L (1976) An efficient and reproducible procedure for the formation of spheroplasts from variously grown Escherichia coli. Anal. Biochem., 74, 160-170.
45. Xu, Z., Jones, C.H., Haslam, D., Dodson, K., Kihlberg, J. and Hultgren, S.J. (1995) Molecular dissection of PapD interaction with PapG reveals two chaperone binding sites. Mal. Microbiol., 16, 1011-1020.
46. Zoller, M.J. and Smith, M. (1983) Oligonucleotide-directed mutagenesis of DNA fragments cloned into M13 vectors. Methods Enzymol., 100, 468-500.