Identification of a Specific Chaperone for SptP, a Substrate of the Centisome 63 Type III Secretion System of Salmonella typhimurium
10.1128/jb.180.13.3393-3399.1998
Crossref journal-article
American Society for Microbiology
Journal of Bacteriology (235)
Abstract

ABSTRACT Salmonella typhimurium uses of a type III protein secretion system encoded at centisome 63 of its chromosome to deliver effector molecules into the host cell. These proteins stimulate host cell responses such as reorganization of the actin cytoskeleton and activation of transcription factors. One of these effector proteins is SptP, a tyrosine phosphatase that causes disruption of the host cell actin cytoskeleton. A characteristic feature of many substrates of type III secretion systems is their association with specific cytoplasmic chaperones which appears to be required for secretion and/or translocation of these proteins into the host cell. We report here the identification of SicP, a 13-kDa acidic polypeptide that is encoded immediately upstream of sptP . A loss-of-function mutation in sicP resulted in drastically reduced levels of SptP but did not affect sptP expression, indicating that SicP exerts its effect posttranscriptionally. Pulse-chase experiments demonstrated that the loss of SicP leads to increased degradation of SptP. In addition, we show that SicP binds to SptP directly and that the binding site is located between residues 15 and 100 of the tyrosine phosphatase. Taken together, these results indicate that SicP acts as a specific chaperone for SptP.

Bibliography

Fu, Y., & Galán, J. E. (1998). Identification of a Specific Chaperone for SptP, a Substrate of the Centisome 63 Type III Secretion System of Salmonella typhimurium. Journal of Bacteriology, 180(13), 3393–3399.

Authors 2
  1. Yixin Fu (first)
  2. Jorge E. Galán (additional)
References 39 Referenced 91
  1. Allaoui A. Mounier J. Prevost M. C. Sansonetti P. J. Parsot C. icsB: a Shigella flexneri virulence gene necessary for the lysis of protrusions during intercellular spread.Mol. Microbiol.6199216051616 (10.1111/j.1365-2958.1992.tb00885.x) / Mol. Microbiol. / icsB: a Shigella flexneri virulence gene necessary for the lysis of protrusions during intercellular spread by Allaoui A. (1992)
  2. Anderson D. M. Schneewind O. A mRNA signal for the type III secretion of Yop proteins by Yersinia enterocolitica.Science278199711401143 (10.1126/science.278.5340.1140) / Science / A mRNA signal for the type III secretion of Yop proteins by Yersinia enterocolitica by Anderson D. M. (1997)
  3. Burston S. G. Clarke A. R. Molecular chaperones: physical and mechanistic properties.Essays Biochem.291995125136 / Essays Biochem. / Molecular chaperones: physical and mechanistic properties by Burston S. G. (1995)
  4. 10.1128/JB.134.3.1141-1156.1978
  5. 10.1046/j.1365-2958.1997.3831750.x
  6. 10.1128/iai.64.9.3524-3531.1996
  7. Collazo C. Galán J. E. The invasion-associated type III system of Salmonella typhimurium directs the translocation of Sip proteins into the host cell.Mol. Microbiol.241997747756 (10.1046/j.1365-2958.1997.3781740.x) / Mol. Microbiol. / The invasion-associated type III system of Salmonella typhimurium directs the translocation of Sip proteins into the host cell by Collazo C. (1997)
  8. Collazo C. M. Zierler M. K. Galán J. E. Functional analysis of the Salmonella typhimurium invasion genes invI and invJ and identification of a target of the protein secretion apparatus encoded in the inv locus.Mol. Microbiol.1519952538 (10.1111/j.1365-2958.1995.tb02218.x) / Mol. Microbiol. / Functional analysis of the Salmonella typhimurium invasion genes invI and invJ and identification of a target of the protein secretion apparatus encoded in the inv locus by Collazo C. M. (1995)
  9. Eichelberg K. and J. E. Galán. Unpublished data.
  10. Frithz-Lindsten E. Rosqvist R. Johansson L. The chaperone-like protein YerA of Yersinia pseudotuberculosis stabilizes YopE in the cytoplasm but is dispensible for targeting to the secretion loci.Mol. Microbiol.161995635647 (10.1111/j.1365-2958.1995.tb02426.x) / Mol. Microbiol. / The chaperone-like protein YerA of Yersinia pseudotuberculosis stabilizes YopE in the cytoplasm but is dispensible for targeting to the secretion loci by Frithz-Lindsten E. (1995)
  11. Fu Y. Galán J. E. The Salmonella spp. protein tyrosine phosphatase SptP is translocated into host cells and disrupts the host-cell cytoskeleton.Mol. Microbiol.271998359368 (10.1046/j.1365-2958.1998.00684.x) / Mol. Microbiol. / The Salmonella spp. protein tyrosine phosphatase SptP is translocated into host cells and disrupts the host-cell cytoskeleton by Fu Y. (1998)
  12. Fu Y. and J. E. Galán. Unpublished data.
  13. Galán J. E. Molecular bases of Salmonella entry into host cells.Mol. Microbiol.201996263271 (10.1111/j.1365-2958.1996.tb02615.x) / Mol. Microbiol. / Molecular bases of Salmonella entry into host cells by Galán J. E. (1996)
  14. Galán J. E. Bliska J. B. Cross-talk between bacterial pathogens and their host cells.Annu. Rev. Cell Dev. Biol.121996219253 (10.1146/annurev.cellbio.12.1.221) / Annu. Rev. Cell Dev. Biol. / Cross-talk between bacterial pathogens and their host cells by Galán J. E. (1996)
  15. Galán J. E. Ginocchio C. Costeas P. Molecular and functional characterization of the Salmonella typhimurium invasion gene invA: homology of InvA to members of a new protein family.J. Bacteriol.17199243384349 (10.1128/jb.174.13.4338-4349.1992) / J. Bacteriol. / Molecular and functional characterization of the Salmonella typhimurium invasion gene invA: homology of InvA to members of a new protein family by Galán J. E. (1992)
  16. Ginocchio C. Olmsted S. B. Wells C. L. Galán J. E. Contact with epithelial cells induces the formation of surface appendages on Salmonella typhimurium.Cell761994717724 (10.1016/0092-8674(94)90510-X) / Cell / Contact with epithelial cells induces the formation of surface appendages on Salmonella typhimurium by Ginocchio C. (1994)
  17. Guan K.-L. Dixon J. E. Eukaryotic proteins expressed in Escherichia coli: an improved thrombin cleavage and purification procedure of fusion proteins with glutathione S-transferase.Ann. Biochem.1921991262267 (10.1016/0003-2697(91)90534-Z) / Ann. Biochem. / Eukaryotic proteins expressed in Escherichia coli: an improved thrombin cleavage and purification procedure of fusion proteins with glutathione S-transferase by Guan K.-L. (1991)
  18. 10.1128/jb.177.14.4121-4130.1995
  19. Hardt W.-D. Galán J. E. A secreted Salmonella protein with homology to an avirulence determinant of plant pathogenic bacteria.Proc. Natl. Acad. Sci. USA94199798879892 (10.1073/pnas.94.18.9887) / Proc. Natl. Acad. Sci. USA / A secreted Salmonella protein with homology to an avirulence determinant of plant pathogenic bacteria by Hardt W.-D. (1997)
  20. Hardt W.-D. Urlaub H. Galán J. E. A target of the centisome 63 type III protein secretion system of Salmonella typhimurium is encoded by a cryptic bacteriophage.Proc. Natl. Acad. Sci. USA95199825742579 (10.1073/pnas.95.5.2574) / Proc. Natl. Acad. Sci. USA / A target of the centisome 63 type III protein secretion system of Salmonella typhimurium is encoded by a cryptic bacteriophage by Hardt W.-D. (1998)
  21. Hartl F. U. Molecular chaperones in cellular protein folding.Nature3811996571579 (10.1038/381571a0) / Nature / Molecular chaperones in cellular protein folding by Hartl F. U. (1996)
  22. 10.1128/jb.177.24.7078-7085.1995
  23. 10.1128/jb.177.14.3965-3971.1995
  24. Kaniga K. Uralil J. Bliska J. B. Galán J. E. A secreted tyrosine phosphatase with modular effector domains encoded by the bacterial pathogen Salmonella typhimurium.Mol. Microbiol.211996633641 (10.1111/j.1365-2958.1996.tb02571.x) / Mol. Microbiol. / A secreted tyrosine phosphatase with modular effector domains encoded by the bacterial pathogen Salmonella typhimurium by Kaniga K. (1996)
  25. 10.1128/iai.61.4.1544-1546.1993
  26. Ménard R. Sansonetti P. J. Parsot C. The secretion of the Shigella flexneri Ipa invasins is induced by the epithelial cell and controlled by IpaB and IpaD.EMBO J.13199452935302 (10.1002/j.1460-2075.1994.tb06863.x) / EMBO J. / The secretion of the Shigella flexneri Ipa invasins is induced by the epithelial cell and controlled by IpaB and IpaD by Ménard R. (1994)
  27. Ménard R. Sansonetti P. J. Parsot C. Vasselon T. The IpaB and IpaC invasins of Shigella flexneri associate in the extracellular medium and are partitioned in the cytoplasm by a specific chaperon.Cell791994515529 (10.1016/0092-8674(94)90260-7) / Cell / The IpaB and IpaC invasins of Shigella flexneri associate in the extracellular medium and are partitioned in the cytoplasm by a specific chaperon by Ménard R. (1994)
  28. 10.1128/JB.170.6.2575-2583.1988
  29. 10.1128/mcb.14.2.1333-1346.1994
  30. 10.1111/j.1365-2958.1995.mmi_17010169.x
  31. 10.1002/j.1460-2075.1994.tb06341.x
  32. 10.1128/jb.178.24.7227-7233.1996
  33. Wattiau P. Bernier B. Deslée P. Michiels T. Cornelis G. R. Individual chaperones required for Yop secretion by Yersinia.Proc. Natl. Acad. Sci. USA9119941049310497 (10.1073/pnas.91.22.10493) / Proc. Natl. Acad. Sci. USA / Individual chaperones required for Yop secretion by Yersinia by Wattiau P. (1994)
  34. Wattiau P. Cornelis G. R. SycE, a chaperone-like protein of Yersinia enterocolitica involved in the secretion of YopE.Mol. Microbiol.81993123131 (10.1111/j.1365-2958.1993.tb01209.x) / Mol. Microbiol. / SycE, a chaperone-like protein of Yersinia enterocolitica involved in the secretion of YopE by Wattiau P. (1993)
  35. Wattiau P. Woestyn S. Cornelis G. R. Customized secretion chaperones in pathogenic bacteria.Mol. Microbiol.201996255262 (10.1111/j.1365-2958.1996.tb02614.x) / Mol. Microbiol. / Customized secretion chaperones in pathogenic bacteria by Wattiau P. (1996)
  36. Woestyn S. Sory M. P. Boland A. Lequenne O. Cornelis G. R. The cytosolic SycE and SycH chaperones of Yersinia protect the region of YopE and YopH involved in translocation across eukaryotic cell membranes.Mol. Microbiol.20199612611271 (10.1111/j.1365-2958.1996.tb02645.x) / Mol. Microbiol. / The cytosolic SycE and SycH chaperones of Yersinia protect the region of YopE and YopH involved in translocation across eukaryotic cell membranes by Woestyn S. (1996)
  37. 10.1046/j.1365-2958.1996.00116.x
  38. 10.1128/iai.63.10.4024-4028.1995
  39. Zukowski M. M. Gaffney D. F. Speck D. Kauffman M. Findell A. Wisecup A. Lecocq J.-P. Chromogenic identification of genetic regulatory signals in Bacillus subtilis based on expression of a cloned Pseudomonas gene.Proc. Natl. Acad. Sci. USA80198311011105 (10.1073/pnas.80.4.1101) / Proc. Natl. Acad. Sci. USA / Chromogenic identification of genetic regulatory signals in Bacillus subtilis based on expression of a cloned Pseudomonas gene by Zukowski M. M. (1983)
Dates
Type When
Created 5 years, 8 months ago (Dec. 31, 2019, 11:24 a.m.)
Deposited 4 years, 1 month ago (July 29, 2021, 2:22 p.m.)
Indexed 2 months, 2 weeks ago (June 16, 2025, 10:11 a.m.)
Issued 27 years, 2 months ago (July 1, 1998)
Published 27 years, 2 months ago (July 1, 1998)
Published Print 27 years, 2 months ago (July 1, 1998)
Funders 0

None

@article{Fu_1998, title={Identification of a Specific Chaperone for SptP, a Substrate of the Centisome 63 Type III Secretion System of Salmonella typhimurium}, volume={180}, ISSN={1098-5530}, url={http://dx.doi.org/10.1128/jb.180.13.3393-3399.1998}, DOI={10.1128/jb.180.13.3393-3399.1998}, number={13}, journal={Journal of Bacteriology}, publisher={American Society for Microbiology}, author={Fu, Yixin and Galán, Jorge E.}, year={1998}, month=jul, pages={3393–3399} }