EspL is a bacterial cysteine protease effector that cleaves RHIM proteins to block necroptosis and inflammation

Nature Microbiology

Volumn 2, Issue , 2017, Pages

  Pearson, Jaclyn S ^a   Giogha, Cristina ^a   Mühlen, Sabrina ^a,f   Nachbur, Ueli ^a,b   Pham, Chi L L ^c   Zhang, Ying ^a   Hildebrand, Joanne M ^a,b   Oates, Clare V ^a   Lung, Tania Wong Fok ^a   Ingle, Danielle ^a,d   Dagley, Laura F ^a,b   Bankovacki, Aleksandra ^a,b   Petrie, Emma J ^a,b   Schroeder, Gunnar N ^e,g   Crepin, Valerie F ^e   Frankel, Gad ^e   Masters, Seth L ^a,b   Vince, James ^a,b   Murphy, James M ^a,b   Sunde, Margaret ^c   Webb, Andrew I ^a,b   Silke, John ^a,b   Hartland, Elizabeth L ^a   more..

^a UNIVERSITY OF MELBOURNE   (Australia)

^b WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^c UNIVERSITY OF SYDNEY   (Australia)

^d UNIVERSITY OF MELBOURNE   (Australia)

^e IMPERIAL COLLEGE LONDON   (United Kingdom)

^f HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

^g QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CYSTEINE PROTEINASE; DNA BINDING PROTEIN; ESCHERICHIA COLI PROTEIN; ESPL PROTEIN, E COLI; LIPOPOLYSACCHARIDE; RECEPTOR INTERACTING PROTEIN SERINE THREONINE KINASE; RIPK1 PROTEIN, HUMAN; RIPK1 PROTEIN, MOUSE; RIPK3 PROTEIN, HUMAN; RIPK3 PROTEIN, MOUSE; TUMOR NECROSIS FACTOR;

ANIMAL; APOPTOSIS; CELL DEATH; CITROBACTER RODENTIUM; DRUG EFFECT; ENTEROPATHOGENIC ESCHERICHIA COLI; ENZYMOLOGY; GENETICS; HEK293 CELL LINE; HUMAN; INFLAMMATION; METABOLISM; MOUSE; NECROSIS; PATHOGENICITY; PHOSPHORYLATION; SIGNAL TRANSDUCTION; TYPE III SECRETION SYSTEM;

ANIMALS; APOPTOSIS; CELL DEATH; CITROBACTER RODENTIUM; CYSTEINE PROTEASES; DNA-BINDING PROTEINS; ENTEROPATHOGENIC ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; HEK293 CELLS; HUMANS; INFLAMMATION; LIPOPOLYSACCHARIDES; MICE; NECROSIS; PHOSPHORYLATION; RECEPTOR-INTERACTING PROTEIN SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION; TUMOR NECROSIS FACTOR-ALPHA; TYPE III SECRETION SYSTEMS;

EID: 85009726401     PISSN: None     EISSN: 20585276     Source Type: Journal    
DOI: 10.1038/nmicrobiol.2016.258     Document Type: Article

References (43)

1. Sun, X., Yin, J., Starovasnik, M. A., Fairbrother, W. J. & Dixit, V. M. Identification of a novel homotypic interaction motif required for the phosphorylation of receptor-interacting protein (RIP) by RIP3. J. Biol. Chem. 277, 9505-9511 (2002).
2. Kaiser, W. J. & Offermann, M. K. Apoptosis induced by the toll-like receptor adaptor TRIF is dependent on its receptor interacting protein homotypic interaction motif. J. Immunol. 174, 4942-4952 (2005).
3. Rebsamen, M. et al. DAI/ZBP1 recruits RIP1 and RIP3 through RIP homotypic interaction motifs to activate NF-κB. EMBO Rep. 10, 916-922 (2009).
4. Li, J. et al. The RIP1/RIP3 necrosome forms a functional amyloid signaling complex required for programmed necrosis. Cell 150, 339-350 (2012).
5. Pasparakis, M. & Vandenabeele, P. Necroptosis and its role in inflammation. Nature 517, 311-320 (2015).
6. Micheau, O. & Tschopp, J. Induction of TNF receptor I-mediated apoptosis via two sequential signaling complexes. Cell 114, 181-190 (2003).
7. Holler, N. et al. Fas triggers an alternative, caspase-8-independent cell death pathway using the kinase RIP as effector molecule. Nat. Immunol. 1, 489-495 (2000).
8. Cho, Y. S. et al. Phosphorylation-driven assembly of the RIP1-RIP3 complex regulates programmed necrosis and virus-induced inflammation. Cell 137, 1112-1123 (2009).
9. He, S. et al. Receptor interacting protein kinase-3 determines cellular necrotic response to TNF-α. Cell 137, 1100-1111 (2009).
10. Murphy, J. M. et al. The pseudokinase MLKL mediates necroptosis via a molecular switch mechanism. Immunity 39, 443-453 (2013).
11. Sun, L. et al. Mixed lineage kinase domain-like protein mediates necrosis signaling downstream of RIP3 kinase. Cell 148, 213-227 (2012).
12. Cai, Z. et al. Plasma membrane translocation of trimerized MLKL protein is required for TNF-induced necroptosis. Nat. Cell Biol. 16, 55-65 (2014).
13. Hildebrand, J. M. et al. Activation of the pseudokinase MLKL unleashes the four-helix bundle domain to induce membrane localization and necroptotic cell death. Proc. Natl Acad. Sci. USA 111, 15072-15077 (2014).
14. Kaiser, W. J. et al. Toll-like receptor 3-mediated necrosis via TRIF, RIP3, and MLKL. J. Biol. Chem. 288, 31268-31279 (2013).
15. Upton, J. W., Kaiser, W. J. & Mocarski, E. S. DAI/ZBP1/DLM-1 complexes with RIP3 to mediate virus-induced programmed necrosis that is targeted by murine cytomegalovirus vIRA. Cell Host Microbe 11, 290-297 (2012).
16. Lawlor, K. E. et al. RIPK3 promotes cell death and NLRP3 inflammasome activation in the absence of MLKL. Nat. Commun. 6, 6282 (2015).
17. Giogha, C., Lung, T. W., Pearson, J. S. & Hartland, E. L. Inhibition of death receptor signaling by bacterial gut pathogens. Cytokine Growth Factor Rev. 25, 235-243 (2014).
18. Pearson, J. S. et al. A type III effector antagonizes death receptor signalling during bacterial gut infection. Nature 501, 247-251 (2013).
19. Li, S. et al. Pathogen blocks host death receptor signalling by arginine GlcNAcylation of death domains. Nature 501, 242-246 (2013).
20. Zhang, L. et al. Cysteine methylation disrupts ubiquitin-chain sensing in NF-κB activation. Nature 481, 204-208 (2012).
21. Charpentier, X. & Oswald, E. Identification of the secretion and translocation domain of the enteropathogenic and enterohemorrhagic Escherichia coli effector Cif, using TEM-1 β-lactamase as a new fluorescence-based reporter. J. Bacteriol. 186, 5486-5495 (2004).
22. Wertz, I. E. et al. De-ubiquitination and ubiquitin ligase domains of A20 downregulate NF-κB signalling. Nature 430, 694-699 (2004).
23. Newton, K. et al. Ubiquitin chain editing revealed by polyubiquitin linkagespecific antibodies. Cell 134, 668-678 (2008).
24. Lin, Y., Devin, A., Rodriguez, Y. & Liu, Z. G. Cleavage of the death domain kinase RIP by caspase-8 prompts TNF-induced apoptosis. Genes Dev. 13, 2514-2526 (1999).
25. Altschul, S. F., Gish, W., Miller, W., Myers, E. W. & Lipman, D. J. Basic local alignment search tool. J. Mol. Biol. 215, 403-410 (1990).
26. Kelley, L. A. & Sternberg, M. J. Protein structure prediction on the Web: a case study using the Phyre server. Nat. Protoc. 4, 363-371 (2009).
27. Shao, F., Merritt, P. M., Bao, Z., Innes, R. W. & Dixon, J. E. A Yersinia effector and a Pseudomonas avirulence protein define a family of cysteine proteases functioning in bacterial pathogenesis. Cell 109, 575-588 (2002).
28. Humphries, F., Yang, S., Wang, B. & Moynagh, P. N. RIP kinases: key decision makers in cell death and innate immunity. Cell Death Differ. 22, 225-236 (2015).
29. Vince, J. E. et al. IAP antagonists target cIAP1 to induce TNFα-dependent apoptosis. Cell 131, 682-693 (2007).
30. Wickham, M. E. et al. Bacterial genetic determinants of non-O157 STEC outbreaks and hemolytic-uremic syndrome after infection. J. Infect. Dis. 194, 819-827 (2006).
31. Conzen, S. D. & Cole, C. N. The three transforming regions of SV40T antigen are required for immortalization of primary mouse embryo fibroblasts. Oncogene 11, 2295-2302 (1995).
32. Hornung, V. et al. Silica crystals and aluminum salts activate the NALP3 inflammasome through phagosomal destabilization. Nat. Immunol. 9, 847-856 (2008).
33. Tanzer, M. C. et al. Evolutionary divergence of the necroptosis effector MLKL. Cell Death Differ. 23, 1185-1197 (2016).
34. Catanzariti, A. M., Soboleva, T. A., Jans, D. A., Board, P. G. & Baker, R. T. An efficient system for high-level expression and easy purification of authentic recombinant proteins. Protein Sci. 13, 1331-1339 (2004).
35. Galan, J. E., Ginocchio, C. & Costeas, P. Molecular and functional characterization of the Salmonella invasion gene invA: homology of invA to members of a new protein family. J. Bacteriol. 174, 4338-4349 (1992).
36. Datsenko, K. A. & Wanner, B. L. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl Acad. Sci. USA 97, 6640-6645 (2000).
37. McKenzie, G. J. & Craig, N. L. Fast, easy and efficient: site-specific insertion of transgenes into enterobacterial chromosomes using Tn7 without need for selection of the insertion event. BMC Microbiol. 6, 39 (2006).
38. Huang, K. F., Chiou, S. H., Ko, T. P., Yuann, J. M. & Wang, A. H. The 1.35 Å structure of cadmium-substituted TM-3, a snake-venom metalloproteinase from Taiwan habu: elucidation of a TNFα-converting enzyme-like active-site structure with a distorted octahedral geometry of cadmium. Acta Crystallogr. D 58, 1118-1128 (2002).
39. Gouet, P., Courcelle, E., Stuart, D. I. & Metoz, F. ESPript: analysis of multiple sequence alignments in PostScript. Bioinformatics 15, 305-308 (1999).
40. Coppolino, M. G. et al. Requirement for N-ethylmaleimide-sensitive factor activity at different stages of bacterial invasion and phagocytosis. J. Biol. Chem. 276, 4772-4780 (2001).
41. Edgar, R. C. MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5, 113 (2004).
42. Stamatakis, A. RAxML version 8: a tool for phylogenetic analysis and postanalysis of large phylogenies. Bioinformatics 30, 1312-1313 (2014).
43. Huson, D. H. & Scornavacca, C. Dendroscope 3: an interactive tool for rooted phylogenetic trees and networks. Syst. Biol. 61, 1061-1067 (2012).