Crossref journal-article
American Society for Microbiology
Journal of Bacteriology (235)
Abstract

ABSTRACT Pathogenic Yersinia species employ type III machines to target effector Yops into the cytosol of eukaryotic cells. Yersinia tyeA mutants are thought to be defective in the targeting of YopE and YopH without affecting the injection of YopM, YopN, YopO, YopP, and YopT into the cytosol of eukaryotic cells. One model suggests that TyeA may form a tether between YopN (LcrE) and YopD on the bacterial surface, a structure that may translocate YopE and YopH across the plasma membrane of eukaryotic cells (M. Iriarte, M. P. Sory, A. Boland, A. P. Boyd, S. D. Mills, I. Lambermont, and G. R. Cornelis, EMBO J. 17:1907–1918, 1998). We have examined the injection of Yop proteins by tyeA mutant yersiniae with the digitonin fractionation technique. We find that tyeA mutant yersiniae not only secreted YopE, YopH, YopM, and YopN into the extracellular medium but also targeted these polypeptides into the cytosol of HeLa cells. Protease protection, cell fractionation, and affinity purification experiments suggest that TyeA is located intracellularly and binds to YopN or YopD. We propose a model whereby TyeA functions as a negative regulator of the type III targeting pathway in the cytoplasm of yersiniae, presumably by preventing the export of YopN.

Bibliography

Cheng, L. W., & Schneewind, O. (2000). Yersinia enterocolitica TyeA, an Intracellular Regulator of the Type III Machinery, Is Required for Specific Targeting of YopE, YopH, YopM, and YopN into the Cytosol of Eukaryotic Cells. Journal of Bacteriology, 182(11), 3183–3190.

Authors 2
  1. Luisa W. Cheng (first)
  2. Olaf Schneewind (additional)
References 42 Referenced 69
  1. 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)
  2. Anderson D. M. Schneewind O. Type III machines of Gram-negative pathogens: injecting virulence factors into host cells and more.Curr. Opin. Microbiol.219991824 (10.1016/S1369-5274(99)80003-4) / Curr. Opin. Microbiol. / Type III machines of Gram-negative pathogens: injecting virulence factors into host cells and more by Anderson D. M. (1999)
  3. Anderson D. M. Schneewind O. Yersinia enterocolitica type III secretion: an mRNA signal that couples translation and secretion of YopQ.Mol. Microbiol.31199911391148 (10.1046/j.1365-2958.1999.01254.x) / Mol. Microbiol. / Yersinia enterocolitica type III secretion: an mRNA signal that couples translation and secretion of YopQ by Anderson D. M. (1999)
  4. 10.1128/jb.173.5.1607-1616.1991
  5. 10.1002/j.1460-2075.1996.tb00904.x
  6. Butler T. Yersinia species Infectious diseases 5th ed. Mandell G. L. Douglas R. G. Bennett J. E. 1995 1748 1756 Churchill Livingstone New York N.Y
  7. 10.1046/j.1365-2958.1997.3831750.x
  8. Cheng L. W. Schneewind O. Yersinia enterocolitica type III secretion: on the role of SycE in targeting YopE into HeLa cells.J. Biol. Chem.27419992210222108 (10.1074/jbc.274.31.22102) / J. Biol. Chem. / Yersinia enterocolitica type III secretion: on the role of SycE in targeting YopE into HeLa cells by Cheng L. W. (1999)
  9. 10.1128/JB.180.21.5495-5504.1998
  10. 10.1128/MMBR.62.4.1315-1352.1998
  11. 10.1046/j.1365-2958.1997.2731623.x
  12. Day J. B. Plano G. V. A complex composed of SycN and YscB functions as a specific chaperone for YopN in Yersinia pestis.Mol. Microbiol.301998777789 (10.1046/j.1365-2958.1998.01110.x) / Mol. Microbiol. / A complex composed of SycN and YscB functions as a specific chaperone for YopN in Yersinia pestis by Day J. B. (1998)
  13. 10.1128/IAI.67.10.5395-5408.1999
  14. Forsberg A. Viitanen A.-M. Skunik M. Wolf-Watz H. The surface-located YopN protein is involved in calcium signal transduction in Yersinia pseudotuberculosis.Mol. Microbiol.51991977986 (10.1111/j.1365-2958.1991.tb00773.x) / Mol. Microbiol. / The surface-located YopN protein is involved in calcium signal transduction in Yersinia pseudotuberculosis by Forsberg A. (1991)
  15. 10.1128/jb.160.3.842-848.1984
  16. Hakånsson S. Gaylov E. Rosqvist R. Wolf-Watz H. The Yersinia YpkA Ser/Thr kinase is translocated and subsequently targeted to the inner surface of the HeLa cell plasma membrane.Mol. Microbiol.201996593603 (10.1046/j.1365-2958.1996.5251051.x) / Mol. Microbiol. / The Yersinia YpkA Ser/Thr kinase is translocated and subsequently targeted to the inner surface of the HeLa cell plasma membrane by Hakånsson S. (1996)
  17. 10.1046/j.1365-2958.1997.3211681.x
  18. 10.1128/JB.181.2.675-680.1999
  19. Iriarte M. Cornelis G. R. YopT, a new Yersinia effector protein, affects the cytoskeleton of host cells.Mol. Microbiol.291998915929 (10.1046/j.1365-2958.1998.00992.x) / Mol. Microbiol. / YopT, a new Yersinia effector protein, affects the cytoskeleton of host cells by Iriarte M. (1998)
  20. Iriarte M. Sory M.-P. Boland A. Boyd A. P. Mills S. D. Lambermont I. Cornelis G. R. TyeA, a protein involved in control of Yop release and in translocation of Yersinia Yop effectors.EMBO J.17199819071918 (10.1093/emboj/17.7.1907) / EMBO J. / TyeA, a protein involved in control of Yop release and in translocation of Yersinia Yop effectors by Iriarte M. (1998)
  21. 10.1128/JB.180.18.4912-4921.1998
  22. Koster M. Bitter W. de Cock H. Allaoui A. Cornelis G. R. Tommassen J. The outer membrane component, YscC, of the Yop secretion machinery of Yersinia enterocolitica forms a ring-shaped multimeric complex.Mol. Microbiol.261997789797 (10.1046/j.1365-2958.1997.6141981.x) / Mol. Microbiol. / The outer membrane component, YscC, of the Yop secretion machinery of Yersinia enterocolitica forms a ring-shaped multimeric complex by Koster M. (1997)
  23. 10.1046/j.1365-2958.1998.00822.x
  24. Lee V. T. Schneewind O. Type III secretion machines and the pathogenesis of enteric infections caused by Yersinia and Salmonella spp.Immunol. Rev.1681999241255 (10.1111/j.1600-065X.1999.tb01296.x) / Immunol. Rev. / Type III secretion machines and the pathogenesis of enteric infections caused by Yersinia and Salmonella spp by Lee V. T. (1999)
  25. Lee V. T. Schneewind O. Type III machines of pathogenic yersiniae secrete virulence factors into the extracellular milieu.Mol. Microbiol.31199916191629 (10.1046/j.1365-2958.1999.01270.x) / Mol. Microbiol. / Type III machines of pathogenic yersiniae secrete virulence factors into the extracellular milieu by Lee V. T. (1999)
  26. 10.1128/jb.173.5.1677-1685.1991
  27. 10.1128/iai.58.9.2840-2849.1990
  28. Nouwen N. Ranson N. Saibil H. Wolpensinger B. Engel A. Ghazi A. Pugsley A. P. Secretin PulD: association with pilot PulS, structure, and ion-conducting channel formation.Proc. Natl. Acad. Sci. USA96199981738177 (10.1073/pnas.96.14.8173) / Proc. Natl. Acad. Sci. USA / Secretin PulD: association with pilot PulS, structure, and ion-conducting channel formation by Nouwen N. (1999)
  29. Persson C. Nordfelth R. Holmström A. Hakånsson S. Rosqvist R. Wolf-Watz H. Cell-surface-bound Yersinia translocate the protein tyrosine phosphatase YopH by a polarized mechanism into the target cell.Mol. Microbiol.181995135150 (10.1111/j.1365-2958.1995.mmi_18010135.x) / Mol. Microbiol. / Cell-surface-bound Yersinia translocate the protein tyrosine phosphatase YopH by a polarized mechanism into the target cell by Persson C. (1995)
  30. 10.1046/j.1365-2958.1999.01408.x
  31. 10.1128/iai.59.12.4562-4569.1991
  32. 10.1002/j.1460-2075.1994.tb06341.x
  33. Russel M. Phage assembly: a paradigm for bacterial virulence factor export? Science 265 1994 612 614 (10.1126/science.8036510) / Science / Phage assembly: a paradigm for bacterial virulence factor export? by Russel M. (1994)
  34. 10.1128/jb.178.24.7227-7233.1996
  35. Skrzypek E. Straley S. C. LcrG, a secreted protein involved in negative regulation of the low-calcium response in Yersinia pestis.J. Bacteriol.175199335203528 (10.1128/jb.175.11.3520-3528.1993) / J. Bacteriol. / LcrG, a secreted protein involved in negative regulation of the low-calcium response in Yersinia pestis by Skrzypek E. (1993)
  36. Sory M.-P. Boland A. Lambermont I. Cornelis G. R. Identification of the YopE and YopH domains required for secretion and internalization into the cytosol of macrophages, using the cyaA gene fusion approach.Proc. Natl. Acad. Sci. USA9219951199812002 (10.1073/pnas.92.26.11998) / Proc. Natl. Acad. Sci. USA / Identification of the YopE and YopH domains required for secretion and internalization into the cytosol of macrophages, using the cyaA gene fusion approach by Sory M.-P. (1995)
  37. Stainier I. Iriarte M. Cornelis G. R. YscM1 and YscM2, two Yersinia enterocolitica proteins causing downregulation of yop transcription.Mol. Microbiol.261997833843 (10.1046/j.1365-2958.1997.6281995.x) / Mol. Microbiol. / YscM1 and YscM2, two Yersinia enterocolitica proteins causing downregulation of yop transcription by Stainier I. (1997)
  38. Straley S. C. Plano G. V. Skrzypek E. Haddix P. L. Fields K. A. Regulation by Ca2+ in the Yersinia low-Ca2+ response.Mol. Microbiol.8199310051010 (10.1111/j.1365-2958.1993.tb01644.x) / Mol. Microbiol. / Regulation by Ca2+ in the Yersinia low-Ca2+ response by Straley S. C. (1993)
  39. 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)
  40. 10.1128/JB.180.2.350-358.1998
  41. 10.1128/jb.165.2.443-447.1986
  42. 10.1128/jb.164.2.704-711.1985
Dates
Type When
Created 23 years, 1 month ago (July 27, 2002, 6:03 a.m.)
Deposited 4 years, 1 month ago (July 29, 2021, 1:52 p.m.)
Indexed 2 months, 3 weeks ago (June 4, 2025, 6:29 a.m.)
Issued 25 years, 2 months ago (June 1, 2000)
Published 25 years, 2 months ago (June 1, 2000)
Published Print 25 years, 2 months ago (June 1, 2000)
Funders 0

None

@article{Cheng_2000, title={Yersinia enterocolitica TyeA, an Intracellular Regulator of the Type III Machinery, Is Required for Specific Targeting of YopE, YopH, YopM, and YopN into the Cytosol of Eukaryotic Cells}, volume={182}, ISSN={1098-5530}, url={http://dx.doi.org/10.1128/jb.182.11.3183-3190.2000}, DOI={10.1128/jb.182.11.3183-3190.2000}, number={11}, journal={Journal of Bacteriology}, publisher={American Society for Microbiology}, author={Cheng, Luisa W. and Schneewind, Olaf}, year={2000}, month=jun, pages={3183–3190} }