Note to users. If you're seeing this message, it means that your browser cannot find this page's style/presentation instructions -- or possibly that you are using a browser that does not support current Web standards. Find out more about why this message is appearing, and what you can do to make your experience of our site the best it can be.
Disruption of Signaling by Yersinia Effector YopJ, a Ubiquitin-Like Protein Protease
Kim Orth,1Zhaohui Xu,1Mary
Beth Mudgett,2Zhao Qin Bao,1Lance E. Palmer,3James B. Bliska,3Walter F. Mangel,4Brian Staskawicz,2Jack E. Dixon1*
Homologs of the Yersinia virulence effector YopJ are
found in both plant and animal bacterial pathogens, as well as plantsymbionts. These YopJ family members were shown to act as cysteineproteases. The catalytic triad of the protease was required forinhibition of the mitogen-activated protein kinase (MAPK) andnuclear
factor B (NF-B) signaling in animal cells and for inductionof
localized cell death in plants. The substrates for YopJ wereshown to
be highly conserved ubiquitin-like molecules, which arecovalently
added to numerous regulatory proteins. YopJ familymembers exert their
pathogenic effect on cells by disrupting thisposttranslational
modification.
1 Department of Biological Chemistry,
University of Michigan, Ann Arbor, Michigan 48109-0606, USA.
2 Department of Plant and Microbial Biology,
University of California Berkeley, Berkeley, CA 94720-3102, USA.
3 Department of Molecular Genetics and Microbiology,
School of Medicine, State University of New York at Stony Brook, Stony
Brook, New York 11794-5222, USA.
4 Department of
Biology, Brookhaven National Laboratory, Upton, NY 11973-5000, USA.
*
To whom correspondence should be addressed. E-mail:
jedixon{at}umich.edu
The Activities of the Yersinia Protein Kinase A (YpkA) and Outer Protein J (YopJ) Virulence Factors Converge on an eIF2{alpha} Kinase.
D. J. Wiley, N. Shrestha, J. Yang, N. Atis, K. Dayton, and K. Schesser (2009)
J. Biol. Chem.
284, 24744-24753
|Abstract »|Full Text »|PDF »
Y4lO of Rhizobium sp. Strain NGR234 Is a Symbiotic Determinant Required for Symbiosome Differentiation.
F.-J. Yang, L.-L. Cheng, L. Zhang, W.-J. Dai, Z. Liu, N. Yao, Z.-P. Xie, and C. Staehelin (2009)
J. Bacteriol.
191, 735-746
|Abstract »|Full Text »|PDF »
The Yersinia pestis Ail Protein Mediates Binding and Yop Delivery to Host Cells Required for Plague Virulence.
Yersinia pestis Type III Secretion System-Dependent Inhibition of Human Polymorphonuclear Leukocyte Function.
J. L. Spinner, J. A. Cundiff, and S. D. Kobayashi (2008)
Infect. Immun.
76, 3754-3760
|Abstract »|Full Text »|PDF »
In Vitro Activation of the I{kappa}B Kinase Complex by Human T-cell Leukemia Virus Type-1 Tax.
S. Mukherjee, V. S. Negi, G. Keitany, Y. Tanaka, and K. Orth (2008)
J. Biol. Chem.
283, 15127-15133
|Abstract »|Full Text »|PDF »
Assessment of the Genetic Diversity of Xanthomonas axonopodis pv. phaseoli and Xanthomonas fuscans subsp. fuscans as a Basis To Identify Putative Pathogenicity Genes and a Type III Secretion System of the SPI-1 Family by Multiple Suppression Subtractive Hybridizations.
S. M. Alavi, S. Sanjari, F. Durand, C. Brin, C. Manceau, and S. Poussier (2008)
Appl. Envir. Microbiol.
74, 3295-3301
|Abstract »|Full Text »|PDF »
The HopZ Family of Pseudomonas syringae Type III Effectors Require Myristoylation for Virulence and Avirulence Functions in Arabidopsis thaliana.
J. D. Lewis, W. Abada, W. Ma, D. S. Guttman, and D. Desveaux (2008)
J. Bacteriol.
190, 2880-2891
|Abstract »|Full Text »|PDF »
Salmonella Secreted Factor L Deubiquitinase of Salmonella typhimurium Inhibits NF-{kappa}B, Suppresses I{kappa}B{alpha} Ubiquitination and Modulates Innate Immune Responses.
G. Le Negrate, B. Faustin, K. Welsh, M. Loeffler, M. Krajewska, P. Hasegawa, S. Mukherjee, K. Orth, S. Krajewski, A. Godzik, et al. (2008)
J. Immunol.
180, 5045-5056
|Abstract »|Full Text »|PDF »
Modulation of Host Innate Immune Response in the Bladder by Uropathogenic Escherichia coli.
B. K. Billips, S. G. Forrestal, M. T. Rycyk, J. R. Johnson, D. J. Klumpp, and A. J. Schaeffer (2007)
Infect. Immun.
75, 5353-5360
|Abstract »|Full Text »|PDF »
A Functional Ubiquitin-Specific Protease Embedded in the Large Tegument Protein (ORF64) of Murine Gammaherpesvirus 68 Is Active during the Course of Infection.
S. Gredmark, C. Schlieker, V. Quesada, E. Spooner, and H. L. Ploegh (2007)
J. Virol.
81, 10300-10309
|Abstract »|Full Text »|PDF »
Salmonella Effector AvrA Regulation of Colonic Epithelial Cell Inflammation by Deubiquitination.
Z. Ye, E. O. Petrof, D. Boone, E. C. Claud, and J. Sun (2007)
Am. J. Pathol.
171, 882-892
|Abstract »|Full Text »|PDF »
Genetic Analysis of SUMOylation in Arabidopsis: Conjugation of SUMO1 and SUMO2 to Nuclear Proteins Is Essential.
S. A. Saracco, M. J. Miller, J. Kurepa, and R. D. Vierstra (2007)
Plant Physiology
145, 119-134
|Abstract »|Full Text »|PDF »
SseL, a Salmonella deubiquitinase required for macrophage killing and virulence.
A. Rytkonen, J. Poh, J. Garmendia, C. Boyle, A. Thompson, M. Liu, P. Freemont, J. C. D. Hinton, and D. W. Holden (2007)
PNAS
104, 3502-3507
|Abstract »|Full Text »|PDF »
A Conserved Carboxylesterase Is a SUPPRESSOR OF AVRBST-ELICITED RESISTANCE in Arabidopsis.
S. Cunnac, A. Wilson, J. Nuwer, A. Kirik, G. Baranage, and M. B. Mudgett (2007)
PLANT CELL
19, 688-705
|Abstract »|Full Text »|PDF »
Intranasal Inoculation of Mice with Yersinia pseudotuberculosis Causes a Lethal Lung Infection That Is Dependent on Yersinia Outer Proteins and PhoP.
M. L. Fisher, C. Castillo, and J. Mecsas (2007)
Infect. Immun.
75, 429-442
|Abstract »|Full Text »|PDF »
Acetylation of MEK2 and I{kappa}B kinase (IKK) activation loop residues by YopJ inhibits signaling.
R. Mittal, S.-Y. Peak-Chew, and H. T. McMahon (2006)
PNAS
103, 18574-18579
|Abstract »|Full Text »|PDF »
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.
N. Lemaitre, F. Sebbane, D. Long, and B. Joseph Hinnebusch (2006)
Infect. Immun.
74, 5126-5131
|Abstract »|Full Text »|PDF »
AopP, a type III effector protein of Aeromonas salmonicida, inhibits the NF-{kappa}B signalling pathway..
D. Fehr, C. Casanova, A. Liverman, H. Blazkova, K. Orth, D. Dobbelaere, J. Frey, and S. E. Burr (2006)
Microbiology
152, 2809-2818
|Abstract »|Full Text »|PDF »
SUMO-Conjugating and SUMO-Deconjugating Enzymes from Arabidopsis.
T. Colby, A. Matthai, A. Boeckelmann, and H.-P. Stuible (2006)
Plant Physiology
142, 318-332
|Abstract »|Full Text »|PDF »
Autophagy Contributes to Caspase-independent Macrophage Cell Death.
Y. Xu, S. O. Kim, Y. Li, and J. Han (2006)
J. Biol. Chem.
281, 19179-19187
|Abstract »|Full Text »|PDF »
The Type III Pseudomonal Exotoxin U Activates the c-Jun NH2-Terminal Kinase Pathway and Increases Human Epithelial Interleukin-8 Production.
A. Cuzick, F. R. Stirling, S. L. Lindsay, and T. J. Evans (2006)
Infect. Immun.
74, 4104-4113
|Abstract »|Full Text »|PDF »
Interaction of Yersinia pestis with Macrophages: Limitations in YopJ-Dependent Apoptosis..
A. Zauberman, S. Cohen, E. Mamroud, Y. Flashner, A. Tidhar, R. Ber, E. Elhanany, A. Shafferman, and B. Velan (2006)
Infect. Immun.
74, 3239-3250
|Abstract »|Full Text »|PDF »
Yersinia YopJ Acetylates and Inhibits Kinase Activation by Blocking Phosphorylation..
S. Mukherjee, G. Keitany, Y. Li, Y. Wang, H. L. Ball, E. J. Goldsmith, and K. Orth (2006)
Science
312, 1211-1214
|Abstract »|Full Text »|PDF »
Balance of bacterial pro- and anti-inflammatory mediators dictates net effect of enteropathogenic Escherichia coli on intestinal epithelial cells.
R. Sharma, S. Tesfay, F. L. Tomson, R. P. Kanteti, V. K. Viswanathan, and G. Hecht (2006)
Am J Physiol Gastrointest Liver Physiol
290, G685-G694
|Abstract »|Full Text »|PDF »
Identification and Characterization of a Novel Bacterial Virulence Factor That Shares Homology with Mammalian Toll/Interleukin-1 Receptor Family Proteins.
R. M. Newman, P. Salunkhe, A. Godzik, and J. C. Reed (2006)
Infect. Immun.
74, 594-601
|Abstract »|Full Text »|PDF »
Haustorially Expressed Secreted Proteins from Flax Rust Are Highly Enriched for Avirulence Elicitors.
A.-M. Catanzariti, P. N. Dodds, G. J. Lawrence, M. A. Ayliffe, and J. G. Ellis (2006)
PLANT CELL
18, 243-256
|Abstract »|Full Text »|PDF »
Yersinia Outer Protein P Suppresses TGF-{beta}-Activated Kinase-1 Activity to Impair Innate Immune Signaling in Yersinia enterocolitica-Infected Cells.
R. Haase, K. Richter, G. Pfaffinger, G. Courtois, and K. Ruckdeschel (2005)
J. Immunol.
175, 8209-8217
|Abstract »|Full Text »|PDF »
Yersinia virulence factor YopJ acts as a deubiquitinase to inhibit NF-{kappa}B activation.
H. Zhou, D. M. Monack, N. Kayagaki, I. Wertz, J. Yin, B. Wolf, and V. M. Dixit (2005)
J. Exp. Med.
202, 1327-1332
|Abstract »|Full Text »|PDF »
Epidermal Growth Factor Receptor Acts as a Negative Regulator for Bacterium Nontypeable Haemophilus influenzae-induced Toll-like Receptor 2 Expression via an Src-dependent p38 Mitogen-activated Protein Kinase Signaling Pathway.
F. Mikami, H. Gu, H. Jono, A. Andalibi, H. Kai, and J.-D. Li (2005)
J. Biol. Chem.
280, 36185-36194
|Abstract »|Full Text »|PDF »
Initiation and termination of NF-{kappa}B signaling by the intracellular protozoan parasite Toxoplasma gondii.
S. Shapira, O. S. Harb, J. Margarit, M. Matrajt, J. Han, A. Hoffmann, B. Freedman, M. J. May, D. S. Roos, and C. A. Hunter (2005)
J. Cell Sci.
118, 3501-3508
|Abstract »|Full Text »|PDF »
Suppression of Bladder Epithelial Cytokine Responses by Uropathogenic Escherichia coli.
D. A. Hunstad, S. S. Justice, C. S. Hung, S. R. Lauer, and S. J. Hultgren (2005)
Infect. Immun.
73, 3999-4006
|Abstract »|Full Text »|PDF »
Inhibition of MAPK and NF-{kappa}B Pathways Is Necessary for Rapid Apoptosis in Macrophages Infected with Yersinia.
Y. Zhang, A. T. Ting, K. B. Marcu, and J. B. Bliska (2005)
J. Immunol.
174, 7939-7949
|Abstract »|Full Text »|PDF »
From The Cover: Insights into Lafora disease: Malin is an E3 ubiquitin ligase that ubiquitinates and promotes the degradation of laforin.
Inhibition of MAPK Signaling Pathways by VopA from Vibrio parahaemolyticus.
J. E. Trosky, S. Mukherjee, D. L. Burdette, M. Roberts, L. McCarter, R. M. Siegel, and K. Orth (2004)
J. Biol. Chem.
279, 51953-51957
|Abstract »|Full Text »|PDF »
Chlamydia Inhibit Host Cell Apoptosis by Degradation of Proapoptotic BH3-only Proteins.
S. F. Fischer, J. Vier, S. Kirschnek, A. Klos, S. Hess, S. Ying, and G. Hacker (2004)
J. Exp. Med.
200, 905-916
|Abstract »|Full Text »|PDF »
SUMO and ubiquitin in the nucleus: different functions, similar mechanisms?.
A Putative Polyketide Synthase/Peptide Synthetase from Magnaporthe grisea Signals Pathogen Attack to Resistant Rice.
H. U. Bohnert, I. Fudal, W. Dioh, D. Tharreau, J.-L. Notteghem, and M.-H. Lebrun (2004)
PLANT CELL
16, 2499-2513
|Abstract »|Full Text »|PDF »
The Plague Virulence Protein YopM Targets the Innate Immune Response by Causing a Global Depletion of NK Cells.
E. J. Kerschen, D. A. Cohen, A. M. Kaplan, and S. C. Straley (2004)
Infect. Immun.
72, 4589-4602
|Abstract »|Full Text »|PDF »
Modeling the Function of Bacterial Virulence Factors in Saccharomyces cerevisiae.
R. H. Valdivia (2004)
Eukaryot. Cell
3, 827-834
|Full Text »|PDF »
Broad Spectrum Identification of Cellular Small Ubiquitin-related Modifier (SUMO) Substrate Proteins.
Y. Zhao, S. W. Kwon, A. Anselmo, K. Kaur, and M. A. White (2004)
J. Biol. Chem.
279, 20999-21002
|Abstract »|Full Text »|PDF »
Leishmania major Amastigotes Induce p50/c-Rel NF-{kappa}B Transcription Factor in Human Macrophages: Involvement in Cytokine Synthesis.
L. Guizani-Tabbane, K. Ben-Aissa, M. Belghith, A. Sassi, and K. Dellagi (2004)
Infect. Immun.
72, 2582-2589
|Abstract »|Full Text »|PDF »
Interaction between a Geminivirus Replication Protein and the Plant Sumoylation System.
A. G. Castillo, L. J. Kong, L. Hanley-Bowdoin, and E. R. Bejarano (2004)
J. Virol.
78, 2758-2769
|Abstract »|Full Text »|PDF »
The Melampsora lini AvrL567 Avirulence Genes Are Expressed in Haustoria and Their Products Are Recognized inside Plant Cells.
P. N. Dodds, G. J. Lawrence, A.-M. Catanzariti, M. A. Ayliffe, and J. G. Ellis (2004)
PLANT CELL
16, 755-768
|Abstract »|Full Text »|PDF »
NopL, an Effector Protein of Rhizobium sp. NGR234, Thwarts Activation of Plant Defense Reactions.
A. V. Bartsev, W. J. Deakin, N. M. Boukli, C. B. McAlvin, G. Stacey, P. Malnoe, W. J. Broughton, and C. Staehelin (2004)
Plant Physiology
134, 871-879
|Abstract »|Full Text »|PDF »
XopC and XopJ, Two Novel Type III Effector Proteins from Xanthomonas campestris pv. vesicatoria.
L. Noel, F. Thieme, J. Gabler, D. Buttner, and U. Bonas (2003)
J. Bacteriol.
185, 7092-7102
|Abstract »|Full Text »|PDF »
A Salmonella protein causes macrophage cell death by inducing autophagy.
L. D. Hernandez, M. Pypaert, R. A. Flavell, and J. E. Galan (2003)
J. Cell Biol.
163, 1123-1131
|Abstract »|Full Text »|PDF »
Signal-induced Ubiquitination of I{kappa}B Kinase-{beta}.
R. S. Carter, K. N. Pennington, B. J. Ungurait, P. Arrate, and D. W. Ballard (2003)
J. Biol. Chem.
278, 48903-48906
|Abstract »|Full Text »|PDF »
A Nuclear Protease Required for Flowering-Time Regulation in Arabidopsis Reduces the Abundance of SMALL UBIQUITIN-RELATED MODIFIER Conjugates.
G. Murtas, P. H. Reeves, Y.-F. Fu, I. Bancroft, C. Dean, and G. Coupland (2003)
PLANT CELL
15, 2308-2319
|Abstract »|Full Text »|PDF »
Cleavage of Arabidopsis PBS1 by a Bacterial Type III Effector.
F. Shao, C. Golstein, J. Ade, M. Stoutemyer, J. E. Dixon, and R. W. Innes (2003)
Science
301, 1230-1233
|Abstract »|Full Text »|PDF »
Interleukin-10 and Inhibition of Innate Immunity to Yersiniae: Roles of Yops and LcrV (V Antigen).
R. R. Brubaker (2003)
Infect. Immun.
71, 3673-3681
|Full Text »|PDF »
Modification of GATA-2 Transcriptional Activity in Endothelial Cells by the SUMO E3 Ligase PIASy.
T.-H. Chun, H. Itoh, L. Subramanian, J. A. Iniguez-Lluhi, and K. Nakao (2003)
Circ. Res.
92, 1201-1208
|Abstract »|Full Text »|PDF »
Small Ubiquitin-Like Modifier Modulates Abscisic Acid Signaling in Arabidopsis.
L. M. Lois, C. D. Lima, and N.-H. Chua (2003)
PLANT CELL
15, 1347-1359
|Abstract »|Full Text »
Pseudomonas syringae Exchangeable Effector Loci: Sequence Diversity in Representative Pathovars and Virulence Function in P. syringae pv. syringae B728a.
W.-L. Deng, A. H. Rehm, A. O. Charkowski, C. M. Rojas, and A. Collmer (2003)
J. Bacteriol.
185, 2592-2602
|Abstract »|Full Text »|PDF »
The Small Ubiquitin-like Modifier (SUMO) Protein Modification System in Arabidopsis. ACCUMULATION OF SUMO1 AND -2 CONJUGATES IS INCREASED BY STRESS.
J. Kurepa, J. M. Walker, J. Smalle, M. M. Gosink, S. J. Davis, T. L. Durham, D.-Y. Sung, and R. D. Vierstra (2003)
J. Biol. Chem.
278, 6862-6872
|Abstract »|Full Text »|PDF »
Biochemical characterization of the Yersinia YopT protease: Cleavage site and recognition elements in Rho GTPases.
F. Shao, P. O. Vacratsis, Z. Bao, K. E. Bowers, C. A. Fierke, and J. E. Dixon (2003)
PNAS
100, 904-909
|Abstract »|Full Text »|PDF »
Small ubiquitin-related modifier-1 modification mediates resolution of CREB-dependent responses to hypoxia.
K. M. Comerford, M. O. Leonard, J. Karhausen, R. Carey, S. P. Colgan, and C. T. Taylor (2003)
PNAS
100, 986-991
|Abstract »|Full Text »|PDF »
Yersinia Effector YopJ Inhibits Yeast MAPK Signaling Pathways by an Evolutionarily Conserved Mechanism.
S. Yoon, Z. Liu, Y. Eyobo, and K. Orth (2003)
J. Biol. Chem.
278, 2131-2135
|Abstract »|Full Text »|PDF »
Evidence for Targeting of Yop Effectors by the Chromosomally Encoded Ysa Type III Secretion System of Yersinia enterocolitica.
L. S. Collier-Hyams, H. Zeng, J. Sun, A. D. Tomlinson, Z. Q. Bao, H. Chen, J. L. Madara, K. Orth, and A. S. Neish (2002)
J. Immunol.
169, 2846-2850
|Abstract »|Full Text »|PDF »
Yersinia type III secretion: send in the effectors.
Host-Pathogen Interactions: Subversion and Utilization of the NF-{kappa}B Pathway during Infection.
C. M. Tato and C. A. Hunter (2002)
Infect. Immun.
70, 3311-3317
|Full Text »|PDF »
Effect of Low- and High-Virulence Yersinia enterocolitica Strains on the Inflammatory Response of Human Umbilical Vein Endothelial Cells.
G. Denecker, S. Totemeyer, L. J. Mota, P. Troisfontaines, I. Lambermont, C. Youta, I. Stainier, M. Ackermann, and G. R. Cornelis (2002)
Infect. Immun.
70, 3510-3520
|Abstract »|Full Text »|PDF »
Deubiquitinating Function of Adenovirus Proteinase.
M. Y. Balakirev, M. Jaquinod, A. L. Haas, and J. Chroboczek (2002)
J. Virol.
76, 6323-6331
|Abstract »|Full Text »|PDF »
Divergence of Apoptosis-Inducing and Preventing Signals in Bacteria-Faced Macrophages Through Myeloid Differentiation Factor 88 and IL-1 Receptor-Associated Kinase Members.
K. Ruckdeschel, O. Mannel, and P. Schrottner (2002)
J. Immunol.
168, 4601-4611
|Abstract »|Full Text »|PDF »
A Functional Screen for the Type III (Hrp) Secretome of the Plant Pathogen Pseudomonas syringae.
D. S. Guttman, B. A. Vinatzer, S. F. Sarkar, M. V. Ranall, G. Kettler, and J. T. Greenberg (2002)
Science
295, 1722-1726
|Abstract »|Full Text »|PDF »
Arginine-143 of Yersinia enterocolitica YopP Crucially Determines Isotype-Related NF-kappa B Suppression and Apoptosis Induction in Macrophages.
K. Ruckdeschel, K. Richter, O. Mannel, and J. Heesemann (2001)
Infect. Immun.
69, 7652-7662
|Abstract »|Full Text »|PDF »
Uropathogenic Escherichia coli Potentiates Type 1 Pilus-Induced Apoptosis by Suppressing NF-kappa B.
D. J. Klumpp, A. C. Weiser, S. Sengupta, S. G. Forrestal, R. A. Batler, and A. J. Schaeffer (2001)
Infect. Immun.
69, 6689-6695
|Abstract »|Full Text »|PDF »
Association of Mitogen-Activated Protein Kinase Pathways with Gingival Epithelial Cell Responses to Porphyromonas gingivalis Infection.
K. Watanabe, O. Yilmaz, S. F. Nakhjiri, C. M. Belton, and R. J. Lamont (2001)
Infect. Immun.
69, 6731-6737
|Abstract »|Full Text »|PDF »
Apoptosis by pan-caspase inhibitors in lipopolysaccharide-activated macrophages.
S. O. Kim, K. Ono, and J. Han (2001)
Am J Physiol Lung Cell Mol Physiol
281, L1095-L1105
|Abstract »|Full Text »|PDF »
Expression of 35S::Pto Globally Activates Defense-Related Genes in Tomato Plants.
Arabidopsis NHO1 Is Required for General Resistance against Pseudomonas Bacteria.
M. Lu, X. Tang, and J.-M. Zhou (2001)
PLANT CELL
13, 437-447
|Abstract »|Full Text »
Yersinia enterocolitica YopP-induced Apoptosis of Macrophages Involves the Apoptotic Signaling Cascade Upstream of Bid.
G. Denecker, W. Declercq, C. A. W. Geuijen, A. Boland, R. Benabdillah, M. van Gurp, M.-P. Sory, P. Vandenabeele, and G. R. Cornelis (2001)
J. Biol. Chem.
276, 19706-19714
|Abstract »|Full Text »|PDF »