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

ABSTRACT The Yersinia pestis low-Ca 2+ response stimulon is responsible for the temperature- and Ca 2+ -regulated expression and secretion of plasmid pCD1-encoded antihost proteins (V antigen and Yops). We have previously shown that lcrD , yscC , yscD , yscG , and yscR encode proteins that are essential for high-level expression and secretion of V antigen and Yops at 37°C in the absence of Ca 2+ . In this study, we characterized yscO of the Yop secretion ( ysc ) operon that contains yscN through yscU by determining the localization of its gene product and the phenotype of an in-frame deletion. The yscO mutant grew and expressed the same levels of Yops as the parent at 37°C in the presence of Ca 2+ . In the absence of Ca 2+ , the mutant grew independently of Ca 2+ , expressed only basal levels of V antigen and Yops, and failed to secrete these. These defects could be partially complemented by providing yscO in trans in the yscO mutant. Overexpression of YopM and V antigen in the mutant failed to restore the export of either protein, showing that the mutation had a direct effect on secretion. These results indicated that the yscO gene product is required for high-level expression and secretion of V antigen and Yops. YscO was found by immunoblot analysis in the soluble and membrane fractions of bacteria growing at 37°C irrespective of the presence of Ca 2+ and in the culture medium in the absence of Ca 2+ . YscO is the only mobile protein identified so far in the Yersinia species that is required for secretion of V antigen and Yops.

Bibliography

Payne, P. L., & Straley, S. C. (1998). YscO of Yersinia pestis Is a Mobile Core Component of the Yop Secretion System. Journal of Bacteriology, 180(15), 3882–3890.

Authors 2
  1. Patricia L. Payne (first)
  2. Susan C. Straley (additional)
References 82 Referenced 47
  1. 10.1128/jb.177.15.4230-4237.1995
  2. Allaoui A. Schulte R. Cornelis G. R. Mutational analysis of the Yersinia enterocolitica virC operon: characterization of yscE, F, G, I, J, K required for Yop secretion and yscH encoding YopR.Mol. Microbiol.181995343355 (10.1111/j.1365-2958.1995.mmi_18020343.x) / Mol. Microbiol. / Mutational analysis of the Yersinia enterocolitica virC operon: characterization of yscE, F, G, I, J, K required for Yop secretion and yscH encoding YopR by Allaoui A. (1995)
  3. Allaoui A. Woestyn S. Sluiters C. Cornelis G. R. YscU, a Yersinia enterocolitica inner membrane protein involved in Yop secretion.J. Bacteriol.176199545344542 (10.1128/jb.176.15.4534-4542.1994) / J. Bacteriol. / YscU, a Yersinia enterocolitica inner membrane protein involved in Yop secretion by Allaoui A. (1995)
  4. 10.1016/S0022-2836(05)80360-2
  5. 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)
  6. Ben-Gurion R. Shafferman A. Essential virulence determinants of different Yersinia species are carried on a common plasmid.Plasmid51981183187 (10.1016/0147-619X(81)90019-6) / Plasmid / Essential virulence determinants of different Yersinia species are carried on a common plasmid by Ben-Gurion R. (1981)
  7. 10.1128/jb.176.9.2619-2626.1994
  8. 10.1093/nar/7.6.1513
  9. Boland A. Sory M.-P. Iriarte M. Kerbourch C. Wattiau P. Cornelis G. R. Status of YopM and YopN in the Yersinia Yop virulon: YopM of Y. enterocolitica is internalized inside the cytosol of PU5-1.8 macrophages by the YopB, D, N delivery apparatus.EMBO J.15199615915201 (10.1002/j.1460-2075.1996.tb00904.x) / EMBO J. / Status of YopM and YopN in the Yersinia Yop virulon: YopM of Y. enterocolitica is internalized inside the cytosol of PU5-1.8 macrophages by the YopB, D, N delivery apparatus by Boland A. (1996)
  10. 10.1128/iai.48.1.234-240.1985
  11. Burrows T. W. Bacon G. A. The basis of virulence in Pasteurella pestis: comparative behaviour of virulent and avirulent strains in vivo.Br. J. Exp. Pathol.351954134143 / Br. J. Exp. Pathol. / The basis of virulence in Pasteurella pestis: comparative behaviour of virulent and avirulent strains in vivo by Burrows T. W. (1954)
  12. Clontech Laboratories Transformer site-directed mutagenesis kit. 1994 Clontech Laboratories Palo Alto Calif
  13. Collazo C. M. Zierler M. K. Galan 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)
  14. Cornelis G. R. Yersinia pathogenicity factors Bacterial pathogenesis of plants and animals. Molecular and cellular mechanisms. Dangl J. Y. 1994 243 263 Springer-Verlag New York N.Y (10.1007/978-3-642-78624-2_11)
  15. 10.1046/j.1365-2958.1997.2731623.x
  16. Davis R. H. Botstein D. Roth J. R. Advanced bacterial genetics. 1980 Cold Spring Harbor Laboratory Cold Spring Harbor N.Y
  17. 10.1128/IAI.59.12.4310-4317.1991
  18. Economou A. Wickner W. SecA promotes preprotein translocation by undergoing ATP-driven cycles of membrane insertion and deinsertion.Cell781994835843 (10.1016/S0092-8674(94)90582-7) / Cell / SecA promotes preprotein translocation by undergoing ATP-driven cycles of membrane insertion and deinsertion by Economou A. (1994)
  19. 10.1046/j.1365-2958.1998.00783.x
  20. Ferber D. M. Brubaker R. Plasmids in Yersinia pestis.Infect. Immun.271981839841 (10.1128/iai.31.2.839-841.1981) / Infect. Immun. / Plasmids in Yersinia pestis by Ferber D. M. (1981)
  21. 10.1128/jb.176.3.569-579.1994
  22. Fields K. A. and S. C. Straley. Unpublished data.
  23. Forsberg A. Viitanen A.-M. Skurnik 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)
  24. 10.1128/iai.62.12.5234-5241.1994
  25. 10.1128/jb.174.13.4338-4349.1992
  26. 10.1128/jb.160.3.842-848.1984
  27. 10.1002/j.1460-2075.1993.tb06056.x
  28. 10.1128/jb.174.14.4820-4828.1992
  29. Hakansson S. Galyov E. 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 Hakansson S. (1996)
  30. Hakansson S. Schesser K. Persson C. Galyov E. E. Rosqvist R. Homble F. Wolf-Watz H. The YopB protein of Yersinia pseudotuberculosis is essential for the translocation of Yop effector proteins across the target cell plasma membrane disrupting activity.EMBO J.15199658125823 (10.1002/j.1460-2075.1996.tb00968.x) / EMBO J. / The YopB protein of Yersinia pseudotuberculosis is essential for the translocation of Yop effector proteins across the target cell plasma membrane disrupting activity by Hakansson S. (1996)
  31. Hensel M. Shea J. E. Raupach B. Monack D. Falkow S. Gleeson C. Kubo T. Holden D. W. Functional analysis of ssaJ and ssaK/U operon, 13 genes encoding components of the type III secretion apparatus of Salmonella pathogenicity island 2.Mol. Microbiol.241997155167 (10.1046/j.1365-2958.1997.3271699.x) / Mol. Microbiol. / Functional analysis of ssaJ and ssaK/U operon, 13 genes encoding components of the type III secretion apparatus of Salmonella pathogenicity island 2 by Hensel M. (1997)
  32. Holmstroem A. Pettersson J. Rosqvist R. Hakansson S. Tafazoli F. Faellman M. Magnusson K. E. Wolf-Watz H. Forsberg A. YopK of Yersinia pseudotuberculosis controls translocation of Yop effectors across the eukaryotic cell membrane.Mol. Microbiol.2419977391 (10.1046/j.1365-2958.1997.3211681.x) / Mol. Microbiol. / YopK of Yersinia pseudotuberculosis controls translocation of Yop effectors across the eukaryotic cell membrane by Holmstroem A. (1997)
  33. 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)
  34. 10.1128/jb.145.3.1365-1373.1981
  35. 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)
  36. 10.1126/science.280.5363.602
  37. 10.1038/227680a0
  38. Lee C. A. Type III secretion systems: machines to deliver bacterial proteins into eukaryotic cells? Trends Microbiol. 5 1997 148 156 (10.1016/S0966-842X(97)01029-9) / Trends Microbiol. / Type III secretion systems: machines to deliver bacterial proteins into eukaryotic cells? by Lee C. A. (1997)
  39. 10.1128/iai.58.8.2569-2577.1990
  40. Lupas A. Prediction and analysis of coiled-coil structures.Methods Enzymol.2261996513525 (10.1016/S0076-6879(96)66032-7) / Methods Enzymol. / Prediction and analysis of coiled-coil structures by Lupas A. (1996)
  41. 10.1126/science.252.5009.1162
  42. Maniatis T. E. Fritsch E. F. Sambrook J. Molecular cloning: a laboratory manual. 1982 Cold Spring Harbor Laboratory Cold Spring Harbor N.Y
  43. Masamune Y. Richardson C. C. Strand displacement during deoxyribonucleic acid synthesis at single strand breaks.J. Biol. Chem.246197126922701 (10.1016/S0021-9258(18)62341-5) / J. Biol. Chem. / Strand displacement during deoxyribonucleic acid synthesis at single strand breaks by Masamune Y. (1971)
  44. 10.1128/jb.173.16.4994-5009.1991
  45. Mullis K. B. Faloona F. A. Specific synthesis of DNA in vitro via a polymerase catalyzed chain reaction.Methods Enzymol.1551978335350 (10.1016/0076-6879(87)55023-6) / Methods Enzymol. / Specific synthesis of DNA in vitro via a polymerase catalyzed chain reaction by Mullis K. B. (1978)
  46. 10.1128/IAI.65.3.924-930.1997
  47. 10.1128/jb.179.4.1307-1316.1997
  48. Nishiyama K. Suzuki T. Tokuda H. Inversion of the membrane topology of SecG, coupled with SecA-dependent preprotein translocation.Cell8519967181 (10.1016/S0092-8674(00)81083-1) / Cell / Inversion of the membrane topology of SecG, coupled with SecA-dependent preprotein translocation by Nishiyama K. (1996)
  49. Nossal N. G. DNA synthesis on a double-stranded DNA template by the T4 bacteriophage DNA polymerase and the T4 gene 32 DNA unwinding protein.J. Biol. Chem.249197456685676 (10.1016/S0021-9258(20)79779-6) / J. Biol. Chem. / DNA synthesis on a double-stranded DNA template by the T4 bacteriophage DNA polymerase and the T4 gene 32 DNA unwinding protein by Nossal N. G. (1974)
  50. Payne P. L. and S. C. Straley. YscP of Yersinia pestis is a secreted component of the Yop secretion system. Submitted for publication.
  51. 10.1128/CMR.10.1.35
  52. 10.1128/jb.172.10.5929-5937.1990
  53. Persson C. Nordfelth R. Holmström N. Hakansson 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)
  54. Pettersson J. R. Nordfelth E. Dubinina T. Bergman T. Gustavsson M. Magnusson K.-E. Wolf-Watz H. Modulation of virulence factor expression by pathogen target cell contact.Science273199612311233 (10.1126/science.273.5279.1231) / Science / Modulation of virulence factor expression by pathogen target cell contact by Pettersson J. R. (1996)
  55. 10.1128/jb.173.22.7293-7303.1991
  56. 10.1128/jb.175.11.3536-3545.1993
  57. 10.1128/jb.177.13.3843-3854.1995
  58. Promega Corp Promega protocol and application guide 2nd ed. 1991 Promega Corp. Madison Wis
  59. Protsenko O. A. Anisimov P. I. Mosharov O. T. Konnov N. P. Popov Y. A. Kokushkin A. M. Detection and characterization of Yersinia pestis plasmids determining pesticin I, fraction I antigen, and “mouse” toxin synthesis.Sov. Genet.191983838846 / Sov. Genet. / Detection and characterization of Yersinia pestis plasmids determining pesticin I, fraction I antigen, and “mouse” toxin synthesis by Protsenko O. A. (1983)
  60. 10.1128/jb.174.10.3355-3363.1992
  61. 10.1002/j.1460-2075.1994.tb06341.x
  62. Sample A. K. Brubaker R. R. Post-translational regulation of Lcr plasmid-mediated peptides in pesticinogenic Yersinia pestis.Microb. Pathog.31987239248 (10.1016/0882-4010(87)90057-X) / Microb. Pathog. / Post-translational regulation of Lcr plasmid-mediated peptides in pesticinogenic Yersinia pestis by Sample A. K. (1987)
  63. Sample A. K. Fowler J. M. Brubaker R. R. Modulation of the low-calcium response in Yersinia pestis via plasmid-plasmid interaction.Microb. Pathog.21987443453 (10.1016/0882-4010(87)90051-9) / Microb. Pathog. / Modulation of the low-calcium response in Yersinia pestis via plasmid-plasmid interaction by Sample A. K. (1987)
  64. Sanger F. Nicklen S. Coulson A. R. DNA sequencing with chain-terminating inhibitors.Proc. Natl. Acad. Sci. USA74197754635467 (10.1073/pnas.74.12.5463) / Proc. Natl. Acad. Sci. USA / DNA sequencing with chain-terminating inhibitors by Sanger F. (1977)
  65. 10.1128/jb.175.8.2334-2346.1993
  66. 10.1128/jb.178.24.7227-7233.1996
  67. Skrzypek E. Haddix P. L. Plano G. V. Straley S. C. New suicide vector for gene replacement in yersiniae and other gram-negative bacteria.Plasmid.291993160163 (10.1006/plas.1993.1019) / Plasmid. / New suicide vector for gene replacement in yersiniae and other gram-negative bacteria by Skrzypek E. (1993)
  68. 10.1128/jb.177.9.2530-2542.1995
  69. 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)
  70. Skrzypek E. and S. C. Straley. Unpublished data.
  71. 10.1128/iai.56.10.2749-2752.1988
  72. Sodeinde O. A. Subrahmanyam Y. V. B. K. Stark K. Quan T. Bao Y. Goguen J. D. A surface protease and the invasive character of plague.Science258199210041007 (10.1126/science.1439793) / Science / A surface protease and the invasive character of plague by Sodeinde O. A. (1992)
  73. Sory M.-P. Cornelis G. Translocation of a hybrid YopE-adenylate cyclase from Yersinia enterocolitica into HeLa cells.Mol. Microbiol.141994583594 (10.1111/j.1365-2958.1994.tb02191.x) / Mol. Microbiol. / Translocation of a hybrid YopE-adenylate cyclase from Yersinia enterocolitica into HeLa cells by Sory M.-P. (1994)
  74. 10.1128/iai.51.2.445-454.1986
  75. 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)
  76. 10.1128/iai.61.8.3105-3110.1993
  77. Towbin H. Staehelin T. Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedures and some applications.Proc. Natl. Acad. Sci. USA76197943504354 (10.1073/pnas.76.9.4350) / Proc. Natl. Acad. Sci. USA / Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedures and some applications by Towbin H. (1979)
  78. 10.1128/iai.43.3.895-900.1984
  79. 10.1128/JB.180.2.350-358.1998
  80. 10.1128/jb.176.6.1561-1569.1994
  81. 10.1128/jb.164.2.704-711.1985
  82. 10.1128/jb.139.3.792-799.1979
Dates
Type When
Created 5 years, 7 months ago (Dec. 31, 2019, 11:25 a.m.)
Deposited 4 years ago (July 29, 2021, 2:23 p.m.)
Indexed 2 months, 2 weeks ago (June 4, 2025, 6:32 a.m.)
Issued 27 years ago (Aug. 1, 1998)
Published 27 years ago (Aug. 1, 1998)
Published Print 27 years ago (Aug. 1, 1998)
Funders 0

None

@article{Payne_1998, title={YscO of Yersinia pestis Is a Mobile Core Component of the Yop Secretion System}, volume={180}, ISSN={1098-5530}, url={http://dx.doi.org/10.1128/jb.180.15.3882-3890.1998}, DOI={10.1128/jb.180.15.3882-3890.1998}, number={15}, journal={Journal of Bacteriology}, publisher={American Society for Microbiology}, author={Payne, Patricia L. and Straley, Susan C.}, year={1998}, month=aug, pages={3882–3890} }