Macrophage activation redirects Yersinia-infected host cell death from apoptosis to caspase-1-dependent pyroptosis

PLoS Pathogens

Volumn 3, Issue 11, 2007, Pages 1570-1582

  Bergsbaken, Tessa ^a   Cookson, Brad T ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; INTERLEUKIN 18; INTERLEUKIN 1BETA CONVERTING ENZYME; LIGAND; LIPOPOLYSACCHARIDE; TOLL LIKE RECEPTOR; TRANSLOCON; CASPASE 3; UNCLASSIFIED DRUG; YOPP PROTEIN, YERSINIA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CELL MEMBRANE PERMEABILITY; CELL VIABILITY; CONTROLLED STUDY; CYTOKINE RELEASE; DNA DAMAGE; ENZYME ACTIVATION; FEMALE; HOST CELL; IMMUNE RESPONSE; INFECTION SENSITIVITY; INFLAMMATION; MACROPHAGE ACTIVATION; MEMBRANE DAMAGE; MOUSE; NONHUMAN; PROTEIN DEGRADATION; PYROPTOSIS; WILD TYPE; YERSINIA PSEUDOTUBERCULOSIS; YERSINIOSIS; ANIMAL; C57BL MOUSE; CONFOCAL MICROSCOPY; HOST PATHOGEN INTERACTION; IMMUNOLOGY; MACROPHAGE; METABOLISM; MICROBIOLOGY; PATHOLOGY; PHYSIOLOGY;

BACTERIA (MICROORGANISMS); YERSINIA; YERSINIA PESTIS; YERSINIA PSEUDOTUBERCULOSIS;

ANIMALS; APOPTOSIS; BACTERIAL PROTEINS; CASPASE 1; CASPASE 3; CELL MEMBRANE PERMEABILITY; FEMALE; HOST-PATHOGEN INTERACTIONS; INFLAMMATION; MACROPHAGE ACTIVATION; MACROPHAGES; MICE; MICE, INBRED C57BL; MICROSCOPY, CONFOCAL; TOLL-LIKE RECEPTORS; YERSINIA INFECTIONS;

EID: 37349046671     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.0030161     Document Type: Article

References (82)

1. Cornelis GR, Boland A, Boyd AP, Geuijen C, Iriarte M, et al. (1998) The virulence plasmid of Yersinia, an antihost genome. Microbiol Mol Biol Rev 62: 1315-1352.
2. Cornelis GR (2002) Yersinia type III secretion: send in the effectors. J Cell Biol 158: 401-408.
3. Ruckdeschel K, Roggenkamp A, Lafont V, Mangeat P, Heesemann J, et al. (1997) Interaction of Yersinia enterocolitica with macrophages leads to macrophage cell death through apoptosis. Infect Immun 65: 4813-4821.
4. Monack DM, Mecsas J, Ghori N, Falkow S (1997) Yersinia signals macrophages to undergo apoptosis and YopJ is necessary for this cell death. Proc Natl Acad Sci U S A 94: 10385-10390.
5. Zhang Y, Bliska JB (2005) Immunol Role of macrophage apoptosis in the pathogenesis of Yersinia. Curr Top Microbiol 289: 151-173.
6. Zhang Y, Bliska JB (2003) Role of Toll-like receptor signaling in the apoptotic response of macrophages to Yersinia infection. Infect Immun 71: 1513-1519.
7. Haase R, Kirschning CJ, Sing A, Schrottner P, Fukase K, et al. (2003) A dominant role of Toll-like receptor 4 in the signaling of apoptosis in bacteria-faced macrophages. J Immunol 171: 4294-4303.
8. Hoebe K, Du X, Georgel P, Janssen E, Tabeta K, et al. (2003) Identification of Lps2 as a key transducer of MyD88-independent TIR signalling. Nature 424: 743-748.
9. Ruckdeschel K, Pfaffinger G, Haase R, Sing A, Weighardt H, et al. (2004) Signaling of apoptosis through TLRs critically involves toll/IL-1 receptor domain-containing adapter inducing IFN-beta, but not MyD88, in bacteriainfected murine macrophages. J Immunol 173: 3320-3328.
10. Karin M, Lin A (2002) NF-kappaB at the crossroads of life and death. Nat Immunol 3: 221-227.
11. Zhang Y, Ting AT, Marcu KB, Bliska JB (2005) Inhibition of MAPK and NFkappa B pathways is necessary for rapid apoptosis in macrophages infected with Yersinia. J Immunol 174: 7939-7949.
12. Park JM, Greten FR, Wong A, Westrick RJ, Arthur JS, et al. (2005) Signaling pathways and genes that inhibit pathogen-induced macrophage apoptosis - CREB and NF-kappaB as key regulators. Immunity 23: 319-329.
13. Boland A, Cornelis GR (1998) Role of YopP in suppression of tumor necrosis factor alpha release by macrophages during Yersinia infection. Infect Immun 66: 1878-1884.
14. Schesser K, Spiik AK, Dukuzumuremyi JM, Neurath MF, Pettersson S, et al. (1998) The yopJ locus is required for Yersinia-mediated inhibition of NF-kappaB activation and cytokine expression: YopJ contains a eukaryotic SH2-like domain that is essential for its repressive activity. Mol Microbiol 28: 1067-1079.
15. Palmer LE, Hobbie S, Galan JE, Bliska JB (1998) YopJ of Yersinia pseudotuberculosis is required for the inhibition of macrophage TNF-alpha production and downregulation of the MAP kinases p38 and JNK. Mol Microbiol 27: 953-965.
16. Denecker G, Declercq W, Geuijen CA, Boland A, Benabdillah R, et al. (2001) Yersinia enterocolitica YopP-induced apoptosis of macrophages involves the apoptotic signaling cascade upstream of bid. J Biol Chem 276: 19706-19714.
17. Autenrieth IB, Heesemann J (1992) In vivo neutralization of tumor necrosis factor-alpha and interferon-gamma abrogates resistance to Yersinia enterocolitica infection in mice. Med Microbiol Immunol (Berl) 181: 333-338.
18. Galyov EE, Hakansson S, Wolf-Watz H (1994) Characterization of the operon encoding the YpkA Ser/Thr protein kinase and the YopJ protein of Yersinia pseudotuberculosis. J Bacteriol 176: 4543-4548.
19. Lemaitre N, Sebbane F, Long D, Hinnebusch BJ (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.
20. Straley SC, Bowmer WS (1986) Virulence genes regulated at the transcriptional level by Ca2+ in Yersinia pestis include structural genes for outer membrane proteins. Infect Immun 51: 445-454.
21. Monack DM, Mecsas J, Bouley D, Falkow S (1998) Yersinia-induced apoptosis in vivo aids in the establishment of a systemic infection of mice. J Exp Med 188: 2127-2137.
22. Trulzsch K, Sporleder T, Igwe EI, 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.
23. Nakajima R, Brubaker RR (1993) Association between virulence of Yersinia pestis and suppression of gamma interferon and tumor necrosis factor alpha. Infect Immun 61: 23-31.
24. Lathem WW, Crosby SD, Miller VL, Goldman WE (2005) Progression of primary pneumonic plague: a mouse model of infection, pathology, and bacterial transcriptional activity. Proc Natl Acad Sci U S A 102: 17786-17791.
25. Dube PH, Revell PA, Chaplin DD, Lorenz RG, Miller VL (2001) A role for IL-1 alpha in inducing pathologic inflammation during bacterial infection. Proc Natl Acad Sci U S A 98: 10880-10885.
26. Handley SA, Dube PH, Revell PA, Miller VL (2004) Characterization of oral Yersinia enterocolitica infection in three different strains of inbred mice. Infect Immun 72: 1645-1656.
27. Autenrieth IB, Hantschmann P, Heymer B, Heesemann J (1993) Immunohistological characterization of the cellular immune response against Yersinia enterocolitica in mice: evidence for the involvement of T lymphocytes. Immunobiology 187: 1-16.
28. 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
29. Gordon S (2003) Alternative activation of macrophages. Nat Rev Immunol 3: 23-35.
30. Montminy SW, Khan N, McGrath S, Walkowicz MJ, Sharp F, et al. (2006) Virulence factors of Yersinia pestis are overcome by a strong lipopolysaccharide response. Nat Immunol 7: 1066-1073.
31. Nonaka T, Kuwabara T, Mimuro H, Kuwae A, Imajoh-Ohmi S (2003) Shigella-induced necrosis and apoptosis of U937 cells and J774 macrophages. Microbiology 149: 2513-2527.
32. Le Feuvre RA, Brough D, Iwakura Y, Takeda K, Rothwell NJ (2002) Priming of macrophages with lipopolysaccharide potentiates P2X7-mediated cell death via a caspase-1-dependent mechanism, independently of cytokine production. J Biol Chem 277: 3210-3218.
33. Ruckdeschel K, Richter K (2002) Lipopolysaccharide desensitization of macrophages provides protection against Yersinia enterocolitica-induced apoptosis. Infect Immun 70: 5259-5264.
34. Cookson BT, Brennan MA (2001) Pro-inflammatory programmed cell death. Trends Microbiol 9: 113-114.
35. Mills SD, Boland A, Sory MP, van der Smissen P, Kerbourch C, et al. (1997) Yersinia enterocolitica induces apoptosis in macrophages by a process requiring functional type III secretion and translocation mechanisms and involving YopP, presumably acting as an effector protein. Proc Natl Acad Sci U S A 94: 12638-12643.
36. Sory MP, Cornelis GR (1994) Translocation of a hybrid YopE-adenylate cyclase from Yersinia enterocolitica into HeLa cells. Mol Microbiol 14: 583-594.
37. Fink SL, Cookson BT (2005) Apoptosis, pyroptosis, and necrosis: mechanistic description of dead and dying eukaryotic cells. Infect Immun 73: 1907-1916.
38. Brennan MA, Cookson BT (2000) Salmonella induces macrophage death by caspase-1-dependent necrosis. Mol Microbiol 38: 31-40.
39. Griffiths RJ, Stam EJ, Downs JT, Otterness IG (1995) ATP induces the release of IL-1 from LPS-primed cells in vivo. J Immunol 154: 2821-2828.
40. Mariathasan S, Weiss DS, Dixit VM, Monack DM (2005) Innate immunity against Francisella tularensis is dependent on the ASC/caspase-1 axis. J Exp Med 202: 1043-1049.
41. Fink SL, Cookson BT (2006) Caspase-1-dependent pore formation during pyroptosis leads to osmotic lysis of infected host macrophages. Cell Microbiol 8: 1812-1825.
42. Garcia-Calvo M, Peterson EP, Leiting B, Ruel R, Nicholson DW, et al. (1998) Inhibition of human caspases by peptide-based and macromolecular inhibitors. J Biol Chem 273: 32608-32613.
43. Fantuzzi G, Dinarello CA (1999) Interleukin-18 and interleukin-1 beta: two cytokine substrates for ICE (caspase-1). J Clin Immunol 19: 1-11.
44. Zychlinsky A, Prevost MC, Sansonetti PJ (1992) Shigella flexneri induces apoptosis in infected macrophages. Nature 358: 167-169.
45. Chen LM, Kaniga K, Galan JE (1996) Salmonella spp. are cytotoxic for cultured macrophages. Mol Microbiol 21: 1101-1115.
46. Stockbauer KE, Foreman-Wykert AK, Miller JF (2003) Bordetella type III secretion induces caspase 1-independent necrosis. Cell Microbiol 5: 123-132.
47. Sun GW, Lu J, Pervaiz S, Cao WP, Gan YH (2005) Caspase-1 dependent macrophage death induced by Burkholderia pseudomallei. Cell Microbiol 7: 1447-1458.
48. Neyt C, Cornelis GR (1999) Insertion of a Yop translocation pore into the macrophage plasma membrane by Yersinia enterocolitica: requirement for translocators YopB and YopD, but not LcrG. Mol Microbiol 33: 971-981.
49. Viboud GI, Bliska JB (2001) A bacterial type III secretion system inhibits actin polymerization to prevent pore formation in host cell membranes. EMBO J 20: 5373-5382.
50. Medvedev AE, Lentschat A, Wahl LM, Golenbock DT, Vogel SN (2002) Dysregulation of LPS-induced Toll-like receptor 4-MyD88 complex formation and IL-1 receptor-associated kinase 1 activation in endotoxin-tolerant cells. J Immunol 169: 5209-5216.
51. Brint EK, Xu D, Liu H, Dunne A, McKenzie AN, et al. (2004) ST2 is an inhibitor of interleukin 1 receptor and Toll-like receptor 4 signaling and maintains endotoxin tolerance. Nat Immunol 5: 373-379.
52. Sakahira H, Enari M, Nagata S (1998) Cleavage of CAD inhibitor in CAD activation and DNA degradation during apoptosis. Nature 391: 96-99.
53. Smolewski P, Bedner E, Du L, Hsieh TC, Wu JM, et al. (2001) Detection of caspases activation by fluorochrome-labeled inhibitors: multiparameter analysis by laser scanning cytometry. Cytometry 44: 73-82.
54. Fukushima H, Sato T, Nagasako R, Takeda I (1991) Acute mesenteric lymphadenitis due to Yersinia pseudotuberculosis lacking a virulence plasmid. J Clin Microbiol 29: 1271-1275.
55. Bartra SS, Jackson MW, Ross JA, Plano GV (2006) Calcium-regulated type III secretion of Yop proteins by an Escherichia coli hha mutant carrying a Yersinia pestis pCD1 virulence plasmid. Infect Immun 74: 1381-1386.
56. Schotte P, Denecker G, Van Den Broeke A, Vandenabeele P, Cornelis GR, et al. (2004) Targeting Rac1 by the Yersinia effector protein YopE inhibits caspase-1-mediated maturation and release of interleukin-1beta. J Biol Chem 279: 25134-25142.
57. Savill J, Dransfield I, Gregory C, Haslett C (2002) A blast from the past: clearance of apoptotic cells regulates immune responses. Nat Rev Immunol 2: 965-975.
58. Voll RE, Herrmann M, Roth EA, Stach C, Kalden JR, et al. (1997) Immunosuppressive effects of apoptotic cells. Nature 390: 350-351.
59. Fadok VA, Bratton DL, Konowal A, Freed PW, Westcott JY, et al. (1998) Macrophages that have ingested apoptotic cells in vitro inhibit proinflammatory cytokine production through autocrine/paracrine mechanisms involving TGF-beta, PGE2, and PAF. J Clin Invest 101: 890-898.
60. Stuart LM, Lucas M, Simpson C, Lamb J, Savill J, et al. (2002) Inhibitory effects of apoptotic cell ingestion upon endotoxin-driven myeloid dendritic cell maturation. J Immunol 168: 1627-1635.
61. Albert ML (2004) Death-defying immunity: do apoptotic cells influence antigen processing and presentation? Nat Rev Immunol 4: 223-231.
62. Trulzsch K, Geginat G, Sporleder T, Ruckdeschel K, Hoffmann R, et al. (2005) Yersinia outer protein P inhibits CD8 T cell priming in the mouse infection model. J Immunol 174: 4244-4251.
63. Matzinger P (2002) The danger model: a renewed sense of self. Science 296: 301-305.
64. Dinarello CA, Fantuzzi G (2003) Interleukin-18 and host defense against infection. J Infect Dis 187 (Suppl 2): S370-384.
65. Xu D, Trajkovic V, Hunter D, Leung BP, Schulz K, et al. (2000) IL-18 induces the differentiation of Th1 or Th2 cells depending upon cytokine milieu and genetic background. Eur J Immunol 30: 3147-3156.
66. Hein J, Sing A, Di Genaro MS, Autenrieth IB (2001) Interleukin-12 and interleukin-18 are indispensable for protective immunity against enteropathogenic Yersinia. Microb Pathog 31: 195-199.
67. Autenrieth IB, Vogel U, Preger S, Heymer B, Heesemann J (1993) Experimental Yersinia enterocolitica infection in euthymic and T-celldeficient athymic nude C57BL/6 mice: comparison of time course, histomorphology, and immune response. Infect Immun 61: 2585-2595.
68. Autenrieth IB, Tingle A, Reske-Kunz A, Heesemann J (1992) T lymphocytes mediate protection against Yersinia enterocolitica in mice: characterization of murine T-cell clones specific for Y. enterocolitica. Infect Immun 60: 1140-1149.
69. Martinon F, Tschopp J (2004) Inflammatory caspases: linking an intracellular innate immune system to autoinflammatory diseases. Cell 117: 561-574.
70. Ren T, Zamboni DS, Roy CR, Dietrich WF, Vance RE (2006) Flagellindeficient Legionella mutants evade caspase-1- and Naip5-mediated macrophage immunity. PLoS Pathog 2: e18. doi:10.1371/journal.ppat.0020018
71. Molofsky AB, Byrne BG, Whitfield NN, Madigan CA, Fuse ET, et al. (2006) Cytosolic recognition of flagellin by mouse macrophages restricts Legionella pneumophila infection. J Exp Med 203: 1093-1104.
72. Miao EA, Alpuche-Aranda CM, Dors M, Clark AE, Bader MW, et al. (2006) Cytoplasmic flagellin activates caspase-1 and secretion of interleukin 1beta via Ipaf. Nat Immunol 7: 569-575.
73. Franchi L, Amer A, Body-Malapel M, Kanneganti TD, Ozoren N, et al. (2006) Cytosolic flagellin requires Ipaf for activation of caspase-1 and interleukin 1beta in salmonella-infected macrophages. Nat Immunol 7: 576-582.
74. Deng W, Burland V, Plunkett G 3rd, Boutin A, Mayhew GF, et al. (2002) Genome sequence of Yersinia pestis KIM. J Bacteriol 184: 4601-4611.
75. Chen TH, Elberg SS (1977) Scanning electron microscopic study of virulent Yersinia pestis and Yersinia pseudotuberculosis type 1. Infect Immun 15: 972-977.
76. Byrne GI, Ojcius DM (2004) Chlamydia and apoptosis: life and death decisions of an intracellular pathogen. Nat Rev Microbiol 2: 802-808.
77. Laguna RK, Creasey EA, Li Z, Valtz N, Isberg RR (2006) A Legionella pneumophila-translocated substrate that is required for growth within macrophages and protection from host cell death. Proc Natl Acad Sci U S A 103: 18745-18750.
78. Boquet P, Ricci V, Galmiche A, Gauthier NC (2003) Gastric cell apoptosis and H. pylori: has the main function of VacA finally been identified? Trends Microbiol 11: 410-413.
79. 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.
80. Cummings LA, Wilkerson WD, Bergsbaken T, Cookson BT (2006) In vivo, fliC expression by Salmonella enterica serovar Typhimurium is heterogeneous, regulated by ClpX, and anatomically restricted. Mol Microbiol 61: 795-809.
81. Higuchi K, Smith JL (1961) Studies on the nutrition and physiology of Pasteurella pestis. VI. A differential plating medium for the estimation of the mutation rate to avirulence. J Bacteriol 81: 605-608.
82. Swanson MS, Isberg RR (1995) Association of Legionella pneumophila with the macrophage endoplasmic reticulum. Infect Immun 63: 3609-3620.