This Article
Right arrow Full Text
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Boland, A.
Right arrow Articles by Cornelis, G. R.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Boland, A.
Right arrow Articles by Cornelis, G. R.

 Previous Article  |  Next Article 

Infect Immun, May 1998, p. 1878-1884, Vol. 66, No. 5
0019-9567/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.

Role of YopP in Suppression of Tumor Necrosis Factor Alpha Release by Macrophages during Yersinia Infection

Anne Boland and Guy R. Cornelis*

Microbial Pathogenesis Unit, Christian de Duve Institute of Cellular Pathology, and Faculté de Médecine, Université Catholique de Louvain, B-1200 Brussels, Belgium

Received 6 November 1997/Returned for modification 23 December 1997/Accepted 12 February 1998

The Yersinia plasmid-encoded Yop virulon enables extracellular adhering bacteria to deliver toxic effector proteins inside their target cells. It includes a type III secretion system (Ysc), at least two translocator proteins (YopB, YopD), and a set of intracellular Yop effectors (YopE, YopH, YopO, YopM, and YopP). Infection of macrophages with a wild-type strain leads to low levels of tumor necrosis factor alpha (TNF-alpha ) release compared to infection with plasmid-cured strains, suggesting that the virulence plasmid encodes a factor impairing the normal TNF-alpha response of infected macrophages. This effect is correlated with the inhibition of the macrophage mitogen-activated protein kinase (MAPK) activities. To identify the Yop protein responsible for the suppression of TNF-alpha release, we infected J774A.1 and PU5-1.8 macrophages with a battery of knockout Yersinia enterocolitica mutants and we quantified the TNF-alpha released. Mutants affected in secretion (yscN), in translocation (yopB and yopD), or in synthesis of all the known Yop effectors (yopH, yopO, yopP, yopE, and yopM polymutants) were unable to block the TNF-alpha response of the macrophages. In contrast, single yopE, yopH, yopO, and yopM mutants behaved like the wild-type strain. A yopP mutant elicited elevated TNF-alpha release, and complementation of the yopP mutant or the yop effector polymutant strain with yopP alone led to a drop in TNF-alpha release. In addition, YopP was also responsible for the inhibition of the extracellular signal-regulated kinase2 (ERK2) and p38 MAPK activities. These results show that YopP is the Yop effector responsible for the Yersinia-induced suppression of TNF-alpha release by infected macrophages.

* Corresponding author. Mailing address: Microbial Pathogenesis Unit, Avenue Hippocrate, 74, UCL Box 74-49, B-1200 Brussels, Belgium. Phone: 32 2 764 74 49. Fax: 32 2 764 74 98. E-mail: Cornelis{at}mipa.ucl.ac.be.

Infect Immun, May 1998, p. 1878-1884, Vol. 66, No. 5
0019-9567/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.


This article has been cited by other articles:

  • Wiley, D. J., Shrestha, N., Yang, J., Atis, N., Dayton, K., Schesser, K. (2009). The Activities of the Yersinia Protein Kinase A (YpkA) and Outer Protein J (YopJ) Virulence Factors Converge on an eIF2{alpha} Kinase. J. Biol. Chem. 284: 24744-24753 [Abstract] [Full Text]  
  • Lawrenz, M. B., Lenz, J. D., Miller, V. L. (2009). A Novel Autotransporter Adhesin Is Required for Efficient Colonization during Bubonic Plague. Infect. Immun. 77: 317-326 [Abstract] [Full Text]  
  • Zhang, Y., Murtha, J., Roberts, M. A., Siegel, R. M., Bliska, J. B. (2008). Type III Secretion Decreases Bacterial and Host Survival following Phagocytosis of Yersinia pseudotuberculosis by Macrophages. Infect. Immun. 76: 4299-4310 [Abstract] [Full Text]  
  • Li, B., Yang, R. (2008). Interaction between Yersinia pestis and the Host Immune System. Infect. Immun. 76: 1804-1811 [Full Text]  
  • Auerbuch, V., Isberg, R. R. (2007). Growth of Yersinia pseudotuberculosis in Mice Occurs Independently of Toll-Like Receptor 2 Expression and Induction of Interleukin-10. Infect. Immun. 75: 3561-3570 [Abstract] [Full Text]  
  • McNally, A., La Ragione, R. M., Best, A., Manning, G., Newell, D. G. (2007). An aflagellate mutant Yersinia enterocolitica biotype 1A strain displays altered invasion of epithelial cells, persistence in macrophages, and cytokine secretion profiles in vitro. Microbiology 153: 1339-1349 [Abstract] [Full Text]  
  • Rytkonen, A., Poh, J., Garmendia, J., Boyle, C., Thompson, A., Liu, M., Freemont, P., Hinton, J. C. D., Holden, D. W. (2007). SseL, a Salmonella deubiquitinase required for macrophage killing and virulence. Proc. Natl. Acad. Sci. USA 104: 3502-3507 [Abstract] [Full Text]  
  • McNally, A., Dalton, T., Ragione, R. M. L., Stapleton, K., Manning, G., Newell, D. G. (2006). Yersinia enterocolitica isolates of differing biotypes from humans and animals are adherent, invasive and persist in macrophages, but differ in cytokine secretion profiles in vitro.. J Med Microbiol 55: 1725-1734 [Abstract] [Full Text]  
  • Velan, B., Bar-Haim, E., Zauberman, A., Mamroud, E., Shafferman, A., Cohen, S. (2006). Discordance in the Effects of Yersinia pestis on the Dendritic Cell Functions Manifested by Induction of Maturation and Paralysis of Migration. Infect. Immun. 74: 6365-6376 [Abstract] [Full Text]  
  • Lemaitre, N., Sebbane, F., Long, D., Joseph Hinnebusch, B. (2006). Yersinia pestis YopJ Suppresses Tumor Necrosis Factor Alpha Induction and Contributes to Apoptosis of Immune Cells in the Lymph Node but Is Not Required for Virulence in a Rat Model of Bubonic Plague. Infect. Immun. 74: 5126-5131 [Abstract] [Full Text]  
  • Zauberman, A., Cohen, S., Mamroud, E., Flashner, Y., Tidhar, A., Ber, R., Elhanany, E., Shafferman, A., Velan, B. (2006). Interaction of Yersinia pestis with Macrophages: Limitations in YopJ-Dependent Apoptosis.. Infect. Immun. 74: 3239-3250 [Abstract] [Full Text]  
  • Sharma, R., Tesfay, S., Tomson, F. L., Kanteti, R. P., Viswanathan, V. K., Hecht, G. (2006). Balance of bacterial pro- and anti-inflammatory mediators dictates net effect of enteropathogenic Escherichia coli on intestinal epithelial cells. Am. J. Physiol. Gastrointest. Liver Physiol. 290: G685-G694 [Abstract] [Full Text]  
  • Lukaszewski, R. A., Kenny, D. J., Taylor, R., Rees, D. G. C., Hartley, M. G., Oyston, P. C. F. (2005). Pathogenesis of Yersinia pestis Infection in BALB/c Mice: Effects on Host Macrophages and Neutrophils. Infect. Immun. 73: 7142-7150 [Abstract] [Full Text]  
  • Zhang, Y., Ting, A. T., Marcu, K. B., Bliska, J. B. (2005). Inhibition of MAPK and NF-{kappa}B Pathways Is Necessary for Rapid Apoptosis in Macrophages Infected with Yersinia. J. Immunol. 174: 7939-7949 [Abstract] [Full Text]  
  • Sebbane, F., Gardner, D., Long, D., Gowen, B. B., Hinnebusch, B. J. (2005). Kinetics of Disease Progression and Host Response in a Rat Model of Bubonic Plague. Am. J. Pathol. 166: 1427-1439 [Abstract] [Full Text]  
  • Trulzsch, K., Geginat, G., Sporleder, T., Ruckdeschel, K., Hoffmann, R., Heesemann, J., Russmann, H. (2005). Yersinia Outer Protein P Inhibits CD8 T Cell Priming in the Mouse Infection Model. J. Immunol. 174: 4244-4251 [Abstract] [Full Text]  
  • Erfurth, S. E., Grobner, S., Kramer, U., Gunst, D. S. J., Soldanova, I., Schaller, M., Autenrieth, I. B., Borgmann, S. (2004). Yersinia enterocolitica Induces Apoptosis and Inhibits Surface Molecule Expression and Cytokine Production in Murine Dendritic Cells. Infect. Immun. 72: 7045-7054 [Abstract] [Full Text]  
  • Huang, X.-Z., Lindler, L. E. (2004). The pH 6 Antigen Is an Antiphagocytic Factor Produced by Yersinia pestis Independent of Yersinia Outer Proteins and Capsule Antigen. Infect. Immun. 72: 7212-7219 [Abstract] [Full Text]  
  • Trulzsch, K., Sporleder, T., Igwe, E. I., Russmann, H., Heesemann, J. (2004). Contribution of the Major Secreted Yops of Yersinia enterocolitica O:8 to Pathogenicity in the Mouse Infection Model. Infect. Immun. 72: 5227-5234 [Abstract] [Full Text]  
  • Schotte, P., Denecker, G., Van Den Broeke, A., Vandenabeele, P., Cornelis, G. R., Beyaert, R. (2004). Targeting Rac1 by the Yersinia Effector Protein YopE Inhibits Caspase-1-mediated Maturation and Release of Interleukin-1{beta}. J. Biol. Chem. 279: 25134-25142 [Abstract] [Full Text]  
  • Marceau, M., Dubuquoy, L., Caucheteux-Rousseaux, C., Foligne, B., Desreumaux, P., Simonet, M. (2004). Yersinia pseudotuberculosis Anti-Inflammatory Components Reduce Trinitrobenzene Sulfonic Acid-Induced Colitis in the Mouse. Infect. Immun. 72: 2438-2441 [Abstract] [Full Text]  
  • Brubaker, R. R. (2003). Interleukin-10 and Inhibition of Innate Immunity to Yersiniae: Roles of Yops and LcrV (V Antigen). Infect. Immun. 71: 3673-3681 [Full Text]  
  • Foultier, B., Troisfontaines, P., Vertommen, D., Marenne, M.-N., Rider, M., Parsot, C., Cornelis, G. R. (2003). Identification of Substrates and Chaperone from the Yersinia enterocolitica 1B Ysa Type III Secretion System. Infect. Immun. 71: 242-253 [Abstract] [Full Text]  
  • Young, B. M., Young, G. M. (2002). Evidence for Targeting of Yop Effectors by the Chromosomally Encoded Ysa Type III Secretion System of Yersinia enterocolitica. J. Bacteriol. 184: 5563-5571 [Abstract] [Full Text]  
  • Cornelis, G. R. (2002). Yersinia type III secretion: send in the effectors. JCB 158: 401-408 [Abstract] [Full Text]  
  • Grosdent, N., Maridonneau-Parini, I., Sory, M.-P., Cornelis, G. R. (2002). Role of Yops and Adhesins in Resistance of Yersinia enterocolitica to Phagocytosis. Infect. Immun. 70: 4165-4176 [Abstract] [Full Text]  
  • Sauvonnet, N., Pradet-Balade, B., Garcia-Sanz, J. A., Cornelis, G. R. (2002). Regulation of mRNA Expression in Macrophages after Yersinia enterocolitica Infection. ROLE OF DIFFERENT Yop EFFECTORS. J. Biol. Chem. 277: 25133-25142 [Abstract] [Full Text]  
  • Denecker, G., Totemeyer, S., Mota, L. J., Troisfontaines, P., Lambermont, I., Youta, C., Stainier, I., Ackermann, M., Cornelis, G. R. (2002). Effect of Low- and High-Virulence Yersinia enterocolitica Strains on the Inflammatory Response of Human Umbilical Vein Endothelial Cells. Infect. Immun. 70: 3510-3520 [Abstract] [Full Text]  
  • Ulett, G. C., Ketheesan, N., Clair, T. W., McElnea, C. L., Barnes, J. L., Hirst, R. G. (2002). Analogous Cytokine Responses to Burkholderia pseudomallei Strains Contrasting in Virulence Correlate with Partial Cross-Protection in Immunized Mice. Infect. Immun. 70: 3953-3958 [Abstract] [Full Text]  
  • Ruckdeschel, K., Mannel, O., Schrottner, P. (2002). Divergence of Apoptosis-Inducing and Preventing Signals in Bacteria-Faced Macrophages Through Myeloid Differentiation Factor 88 and IL-1 Receptor-Associated Kinase Members. J. Immunol. 168: 4601-4611 [Abstract] [Full Text]  
  • Sing, A., Roggenkamp, A., Geiger, A. M., Heesemann, J. (2002). Yersiniaenterocolitica Evasion of the Host Innate Immune Response by V Antigen-Induced IL-10 Production of Macrophages Is Abrogated in IL-10-Deficient Mice. J. Immunol. 168: 1315-1321 [Abstract] [Full Text]  
  • Ruckdeschel, K., Richter, K., Mannel, O., Heesemann, J. (2001). Arginine-143 of Yersinia enterocolitica YopP Crucially Determines Isotype-Related NF-kappa B Suppression and Apoptosis Induction in Macrophages. Infect. Immun. 69: 7652-7662 [Abstract] [Full Text]  
  • Jubier-Maurin, V., Boigegrain, R.-A., Cloeckaert, A., Gross, A., Alvarez-Martinez, M.-T., Terraza, A., Liautard, J., Kohler, S., Rouot, B., Dornand, J., Liautard, J. P. (2001). Major Outer Membrane Protein Omp25 of Brucella suis Is Involved in Inhibition of Tumor Necrosis Factor Alpha Production during Infection of Human Macrophages. Infect. Immun. 69: 4823-4830 [Abstract] [Full Text]  
  • Ruckdeschel, K., Mannel, O., Richter, K., Jacobi, C. A., Trulzsch, K., Rouot, B., Heesemann, J. (2001). Yersinia Outer Protein P of Yersinia enterocolitica Simultaneously Blocks the Nuclear Factor-{{kappa}}B Pathway and Exploits Lipopolysaccharide Signaling to Trigger Apoptosis in Macrophages. J. Immunol. 166: 1823-1831 [Abstract] [Full Text]  
  • Lee, J., Klüsener, B., Tsiamis, G., Stevens, C., Neyt, C., Tampakaki, A. P., Panopoulos, N. J., Nöller, J., Weiler, E. W., Cornelis, G. R., Mansfield, J. W., Nürnberger, T. (2000). HrpZPsph from the plant pathogen Pseudomonas syringae pv. phaseolicola binds to lipid bilayers and forms an ion-conducting pore invitro. Proc. Natl. Acad. Sci. USA 10.1073/pnas.011265298v1 [Abstract] [Full Text]  
  • Orth, K., Xu, Z., Mudgett, M. B., Bao, Z. Q., Palmer, L. E., Bliska, J. B., Mangel, W. F., Staskawicz, B., Dixon, J. E. (2000). Disruption of Signaling by Yersinia Effector YopJ, a Ubiquitin-Like Protein Protease. Science 290: 1594-1597 [Abstract] [Full Text]  
  • Tafazoli, F., Holmstrom, A., Forsberg, A., Magnusson, K.-E. (2000). Apically Exposed, Tight Junction-Associated beta 1-Integrins Allow Binding and YopE-Mediated Perturbation of Epithelial Barriers by Wild-Type Yersinia Bacteria. Infect. Immun. 68: 5335-5343 [Abstract] [Full Text]  
  • Boyd, A. P., Lambermont, I., Cornelis, G. R. (2000). Competition between the Yops of Yersinia enterocolitica for Delivery into Eukaryotic Cells: Role of the SycE Chaperone Binding Domain of YopE. J. Bacteriol. 182: 4811-4821 [Abstract] [Full Text]  
  • FRENCH, N, PETTERSSON, S (2000). Microbe-host interactions in the alimentary tract: the gateway to understanding inflammatory bowel disease. Gut 47: 162-163 [Full Text]  
  • Cornelis, G. R. (2000). Molecular and cell biology aspects of plague. Proc. Natl. Acad. Sci. USA 97: 8778-8783 [Abstract] [Full Text]  
  • Hein, J., Kempf, V. A. J., Diebold, J., Bucheler, N., Preger, S., Horak, I., Sing, A., Kramer, U., Autenrieth, I. B. (2000). Interferon Consensus Sequence Binding Protein Confers Resistance against Yersinia enterocolitica. Infect. Immun. 68: 1408-1417 [Abstract] [Full Text]  
  • Yao, T., Mecsas, J., Healy, J. I., Falkow, S., Chien, Y.-h. (1999). Suppression of T and B Lymphocyte Activation by a Yersinia pseudotuberculosis Virulence Factor, Yoph. JEM 190: 1343-1350 [Abstract] [Full Text]  
  • Chaux, P., Luiten, R., Demotte, N., Vantomme, V., Stroobant, V., Traversari, C., Russo, V., Schultz, E., Cornelis, G. R., Boon, T., van der Bruggen, P. (1999). Identification of Five MAGE-A1 Epitopes Recognized by Cytolytic T Lymphocytes Obtained by In Vitro Stimulation with Dendritic Cells Transduced with MAGE-A1. J. Immunol. 163: 2928-2936 [Abstract] [Full Text]  
  • Visser, L. G., Seijmonsbergen, E., Nibbering, P. H., van den Broek, P. J., van Furth, R. (1999). Yops of Yersinia enterocolitica Inhibit Receptor-Dependent Superoxide Anion Production by Human Granulocytes. Infect. Immun. 67: 1245-1250 [Abstract] [Full Text]  
  • Palmer, L. E., Pancetti, A. R., Greenberg, S., Bliska, J. B. (1999). YopJ of Yersinia spp. Is Sufficient To Cause Downregulation of Multiple Mitogen-Activated Protein Kinases in Eukaryotic Cells. Infect. Immun. 67: 708-716 [Abstract] [Full Text]  
  • Iriarte, M., Cornelis, G. R. (1999). Identification of SycN, YscX, and YscY, Three New Elements of the Yersinia Yop Virulon. J. Bacteriol. 181: 675-680 [Abstract] [Full Text]  
  • Monack, D. M., Mecsas, J., Bouley, D., Falkow, S. (1998). Yersinia-induced Apoptosis In Vivo Aids in the Establishment of a Systemic Infection of Mice. JEM 188: 2127-2137 [Abstract] [Full Text]  
  • Cornelis, G. R., Boland, A., Boyd, A. P., Geuijen, C., Iriarte, M., Neyt, C., Sory, M.-P., Stainier, I. (1998). The Virulence Plasmid of Yersinia, an Antihost Genome. Microbiol. Mol. Biol. Rev. 62: 1315-1352 [Abstract] [Full Text]  
  • Cornelis, G. R. (1998). The Yersinia Deadly Kiss. J. Bacteriol. 180: 5495-5504 [Full Text]  
  • Sarker, M. R., Sory, M.-P., Boyd, A. P., Iriarte, M., Cornelis, G. R. (1998). LcrG is Required for Efficient Translocation of Yersinia Yop Effector Proteins into Eukaryotic Cells. Infect. Immun. 66: 2976-2979 [Abstract] [Full Text]  
  • Dukuzumuremyi, J.-M., Rosqvist, R., Hallberg, B., Akerstrom, B., Wolf-Watz, H., Schesser, K. (2000). The Yersinia Protein Kinase A Is a Host Factor Inducible RhoA/Rac-binding Virulence Factor. J. Biol. Chem. 275: 35281-35290 [Abstract] [Full Text]  
  • Denecker, G., Declercq, W., Geuijen, C. A. W., Boland, A., Benabdillah, R., van Gurp, M., Sory, M.-P., Vandenabeele, P., Cornelis, G. R. (2001). Yersinia enterocolitica YopP-induced Apoptosis of Macrophages Involves the Apoptotic Signaling Cascade Upstream of Bid. J. Biol. Chem. 276: 19706-19714 [Abstract] [Full Text]  
  • Lee, J., Klusener, B., Tsiamis, G., Stevens, C., Neyt, C., Tampakaki, A. P., Panopoulos, N. J., Noller, J., Weiler, E. W., Cornelis, G. R., Mansfield, J. W., Nurnberger, T. (2001). HrpZPsph from the plant pathogen Pseudomonas syringae pv. phaseolicola binds to lipid bilayers and forms an ion-conducting pore invitro. Proc. Natl. Acad. Sci. USA 98: 289-294 [Abstract] [Full Text]  


Copyright © 2009 by the American Society for Microbiology.   For an alternate route to Journals.ASM.org, visit: http://intl-journals.asm.org | More Info»