Impact of host membrane pore formation by the Yersinia pseudotuberculosis type III secretion system on the macrophage innate immune response

Infection and Immunity

Volumn 81, Issue 3, 2013, Pages 905-914

  Kwuan, Laura ^a   Adams, Walter ^a   Auerbuch, Victoria ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; INTERLEUKIN 1BETA; TOLL LIKE RECEPTOR; TRANSCRIPTION FACTOR EGR 1; TRANSLOCON; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; YOPB PROTEIN; YOPD PROTEIN;

ARTICLE; BACTERIAL STRAIN; CELL DEATH; CELL SURVIVAL; CYTOKINE PRODUCTION; CYTOKINE RELEASE; CYTOPLASM; HOST CELL; INFLAMMATION; INNATE IMMUNITY; MACROPHAGE; NONHUMAN; NUCLEAR PORE; PRIORITY JOURNAL; PROTEIN EXPRESSION; TYPE III SECRETION SYSTEM; YERSINIA PSEUDOTUBERCULOSIS;

ANIMALS; CELL DEATH; CELL LINE; EARLY GROWTH RESPONSE PROTEIN 1; GENE DELETION; GENE EXPRESSION REGULATION; INTERLEUKIN-1BETA; MACROPHAGES; MICE; MICE, INBRED C57BL; POLYMERASE CHAIN REACTION; TUMOR NECROSIS FACTOR-ALPHA; YERSINIA PSEUDOTUBERCULOSIS;

EID: 84874696620     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.01014-12     Document Type: Article

References (53)

1. Ting JP, Duncan JA, Lei Y. 2010. How the noninflammasome NLRs function in the innate immune system. Science 327:286-290.
2. Kawai T, Akira S. 2011. Toll-like receptors and their crosstalk with other innate receptors in infection and immunity. Immunity 34:637-650.
3. Schroder K, Tschopp J. 2010. The inflammasomes. Cell 140:821-832.
4. Vance RE, Isberg RR, Portnoy DA. 2009. Patterns of pathogenesis: discrimination of pathogenic and nonpathogenic microbes by the innate immune system. Cell Host Microbe 6:10-21.
5. Troisfontaines P, Cornelis GR. 2005. Type III secretion: more systems than you think. Physiology (Bethesda) 20:326-339.
6. Auerbuch V, Golenbock DT, Isberg RR. 2009. Innate immune recognition of Yersinia pseudotuberculosis type III secretion. PLoS Pathog. 5:e1000686. doi:10.1371/journal.ppat.1000686.
7. Bergsbaken T, Cookson BT. 2007. Macrophage activation redirects yersinia-infected host cell death from apoptosis to caspase-1-dependent pyroptosis. PLoS Pathog. 3:e161. doi:10.1371/journal.ppat.0030161.
8. Shin H, Cornelis GR. 2007. Type III secretion translocation pores of Yersinia enterocolitica trigger maturation and release of pro-inflammatory IL-1beta. Cell. Microbiol. 9:2893-2902.
9. Miao EA, Ernst RK, Dors M, Mao DP, Aderem A. 2008. Pseudomonas aeruginosa activates caspase 1 through Ipaf. Proc. Natl. Acad. Sci. U. S. A. 105:2562-2567.
10. de Grado M, Rosenberger CM, Gauthier A, Vallance BA, Finlay BB. 2001. Enteropathogenic Escherichia coli infection induces expression of the early growth response factor by activating mitogen-activated protein kinase cascades in epithelial cells. Infect. Immun. 69:6217-6224.
11. Lavoie EG, Wangdi T, Kazmierczak BI. 2011. Innate immune responses to Pseudomonas aeruginosa infection. Microbes Infect. 13:1133-1145.
12. Cornelis GR. 2006. The type III secretion injectisome. Nat. Rev. Microbiol. 4:811-825.
13. Durand EA, Maldonado-Arocho FJ, Castillo C, Walsh RL, Mecsas J. 2010. The presence of professional phagocytes dictates the number of host cells targeted for Yop translocation during infection. Cell. Microbiol. 12: 1064-1082.
14. Marketon MM, Depaolo RW, Debord KL, Jabri B, Schneewind O. 2005. Plague bacteria target immune cells during infection. Science 309:1739-1741.
15. Koberle M, Klein-Gunther A, Schutz M, Fritz M, Berchtold S, Tolosa E, Autenrieth IB, Bohn E. 2009. Yersinia enterocolitica targets cells of the innate and adaptive immune system by injection of Yops in a mouse infection model. PLoS Pathog. 5:e1000551. doi:10.1371/journal.ppat.1000551.
16. Viboud GI, Bliska JB. 2005. Yersinia outer proteins: role in modulation of host cell signaling responses and pathogenesis. Annu. Rev. Microbiol. 59: 69-89.
17. Hamad MA, Nilles ML. 2007. Roles of YopN, LcrG and LcrV in controlling Yops secretion by Yersinia pestis. Adv. Exp. Med. Biol. 603:225-234.
18. Williams AW, Straley SC. 1998. YopD of Yersinia pestis plays a role in negative regulation of the low-calcium response in addition to its role in translocation of Yops. J. Bacteriol. 180:350-358.
19. Cambronne ED, Schneewind O. 2002. Yersinia enterocolitica type III secretion: yscM1 and yscM2 regulate yop gene expression by a posttranscriptional mechanism that targets the 5= untranslated region of yop mRNA. J. Bacteriol. 184:5880-5893.
20. Anderson DM, Ramamurthi KS, Tam C, Schneewind O. 2002. YopD and LcrH regulate expression of Yersinia enterocolitica YopQ by a posttranscriptional mechanism and bind to yopQ RNA. J. Bacteriol. 184:1287-1295.
21. Sun YH, Rolan HG, Tsolis RM. 2007. Injection of flagellin into the host cell cytosol by Salmonella enterica serotype Typhimurium. J. Biol. Chem. 282:33897-33901.
22. Miao EA, Mao DP, Yudkovsky N, Bonneau R, Lorang CG, Warren SE, Leaf IA, Aderem A. 2010. Innate immune detection of the type III secretion apparatus through the NLRC4 inflammasome. Proc. Natl. Acad. Sci. U. S. A. 107:3076-3080.
23. Kofoed EM, Vance RE. 2011. Innate immune recognition of bacterial ligands by NAIPs determines inflammasome specificity. Nature 477:592-595.
24. Zhao Y, Yang J, Shi J, Gong YN, Lu Q, Xu H, Liu L, Shao F. 2011. The NLRC4 inflammasome receptors for bacterial flagellin and type III secretion apparatus. Nature 477:596-600.
25. Brodsky IE, Monack D. 2009. NLR-mediated control of inflammasome assembly in the host response against bacterial pathogens. Semin. Immunol. 21:199-207.
26. Brodsky IE, Palm NW, Sadanand S, Ryndak MB, Sutterwala FS, Flavell RA, Bliska JB, Medzhitov R. 2010. A Yersinia effector protein promotes virulence by preventing inflammasome recognition of the type III secretion system. Cell Host Microbe 7:376-387.
27. Viboud GI, So SS, Ryndak MB, Bliska JB. 2003. Proinflammatory signalling stimulated by the type III translocation factor YopB is counteracted by multiple effectors in epithelial cells infected with Yersinia pseudotuberculosis. Mol. Microbiol. 47:1305-1315.
28. Ryndak MB, Chung H, London E, Bliska JB. 2005. Role of predicted transmembrane domains for type III translocation, pore formation, and signaling by the Yersinia pseudotuberculosis YopB protein. Infect. Immun. 73:2433-2443.
29. Vladimer GI, Weng D, Paquette SW, Vanaja SK, Rathinam VA, Aune MH, Conlon JE, Burbage JJ, Proulx MK, Liu Q, Reed G, Mecsas JC, Iwakura Y, Bertin J, Goguen JD, Fitzgerald KA, Lien E. 2012. The NLRP12 inflammasome recognizes Yersinia pestis. Immunity 37:96-107.
30. Bliska JB, Guan KL, Dixon JE, Falkow S. 1991. Tyrosine phosphate hydrolysis of host proteins by an essential Yersinia virulence determinant. Proc. Natl. Acad. Sci. U. S. A. 88:1187-1191.
31. Balada-Llasat JM, Mecsas J. 2006. Yersinia has a tropism for B and T cell zones of lymph nodes that is independent of the type III secretion system. PLoS Pathog. 2:e86. doi:10.1371/journal.ppat.0020086.
32. Andrews HL, Vogel JP, Isberg RR. 1998. Identification of linked Legionella pneumophila genes essential for intracellular growth and evasion of the endocytic pathway. Infect. Immun. 66:950-958.
33. Merriam JJ, Mathur R, Maxfield-Boumil R, Isberg RR. 1997. Analysis of the Legionella pneumophila fliI gene: intracellular growth of a defined mutant defective for flagellum biosynthesis. Infect. Immun. 65:2497-2501.
34. Olsson J, Edqvist PJ, Broms JE, Forsberg A, Wolf-Watz H, Francis MS. 2004. The YopD translocator of Yersinia pseudotuberculosis is a multifunctional protein comprised of discrete domains. J. Bacteriol. 186:4110-4123.
35. Francis MS, Wolf-Watz H. 1998. YopD of Yersinia pseudotuberculosis is translocated into the cytosol of HeLa epithelial cells: evidence of a structural domain necessary for translocation. Mol. Microbiol. 29:799-813.
36. Dewoody R, Merritt PM, Houppert AS, Marketon MM. 2011. YopK regulates the Yersinia pestis type III secretion system from within host cells. Mol. Microbiol. 79:1445-1461.
37. National Research Council. 1996. Guide for the care and use of laboratory animals. National Academies Press, Washington, DC.
38. Davis AJ, Mecsas J. 2007. Mutations in the Yersinia pseudotuberculosis type III secretion system needle protein, YscF, that specifically abrogate effector translocation into host cells. J. Bacteriol. 189:83-97.
39. Marenne MN, Journet L, Mota LJ, Cornelis GR. 2003. Genetic analysis of the formation of the Ysc-Yop translocation pore in macrophages by Yersinia enterocolitica: role of LcrV, YscF and YopN. Microb. Pathog. 35: 243-258.
40. Dacheux D, Goure J, Chabert J, Usson Y, Attree I. 2001. Pore-forming activity of type III system-secreted proteins leads to oncosis of Pseudomonas aeruginosa-infected macrophages. Mol. Microbiol. 40:76-85.
41. Kirby JE, Vogel JP, Andrews HL, Isberg RR. 1998. Evidence for poreforming ability by Legionella pneumophila. Mol. Microbiol. 27:323-336.
42. Mattei PJ, Faudry E, Job V, Izore T, Attree I, Dessen A. 2011. Membrane targeting and pore formation by the type III secretion system translocon. FEBS J. 278:414-426.
43. Faudry E, Vernier G, Neumann E, Forge V, Attree I. 2006. Synergistic pore formation by type III toxin translocators of Pseudomonas aeruginosa. Biochemistry 45:8117-8123.
44. Viboud GI, Bliska JB. 2002. Measurement of pore formation by contactdependent type III protein secretion systems. Methods Enzymol. 358:345-350.
45. Sorg I, Goehring UM, Aktories K, Schmidt G. 2001. Recombinant Yersinia YopT leads to uncoupling of RhoA-effector interaction. Infect. Immun. 69:7535-7543.
46. Tardy F, Homble F, Neyt C, Wattiez R, Cornelis GR, Ruysschaert JM, Cabiaux V. 1999. Yersinia enterocolitica type III secretion-translocation system: channel formation by secreted Yops. EMBO J. 18:6793-6799.
47. Bergsbaken T, Fink SL, Cookson BT. 2009. Pyroptosis: host cell death and inflammation. Nat. Rev. Microbiol. 7:99-109.
48. Walev I, Reske K, Palmer M, Valeva A, Bhakdi S. 1995. Potassiuminhibited processing of IL-1 beta in human monocytes.EMBOJ. 14:1607-1614.
49. Saleh M, Green DR. 2007. Caspase-1 inflammasomes: choosing between death and taxis. Cell Death Differ. 14:1559-1560.
50. Petrilli V, Papin S, Dostert C, Mayor A, Martinon F, Tschopp J. 2007. Activation of the NALP3 inflammasome is triggered by low intracellular potassium concentration. Cell Death Differ. 14:1583-1589.
51. Zheng Y, Lilo S, Brodsky IE, Zhang Y, Medzhitov R, Marcu KB, Bliska JB. 2011. A Yersinia effector with enhanced inhibitory activity on the NF-kappaB pathway activates the NLRP3/ASC/caspase-1 inflammasome in macrophages. PLoS Pathog. 7:e1002026. doi:10.1371/journal.ppat.1002026.
52. Rolli M, Kotlyarov A, Sakamoto KM, Gaestel M, Neininger A. 1999. Stress-induced stimulation of early growth response gene-1 by p38/stressactivated protein kinase 2 is mediated by a cAMP-responsive promoter element in a MAPKAP kinase 2-independent manner. J. Biol. Chem. 274: 19559-19564.
53. Lim CP, Jain N, Cao X. 1998. Stress-induced immediate-early gene, egr-1, involves activation of p38/JNK1. Oncogene 16:2915-2926.