Pneumolysin activates the NLRP3 inflammasome and promotes proinflammatory cytokines independently of TLR4

PLoS Pathogens

Volumn 6, Issue 11, 2010, Pages

  McNeela, Edel A ^a   Burke, Áine ^a   Neill, Daniel R ^b   Baxter, Cathy ^a   Fernandes, Vitor E ^b   Ferreira, Daniela ^b   Smeaton, Sarah ^b   El Rachkidy, Rana ^b   McLoughlin, Rachel M ^a   Mori, Andres ^a   Moran, Barry ^a   Fitzgerald, Katherine A ^c   Tschopp, Jurg ^d   Pétrilli, Virginie ^d   Andrew, Peter W ^b   Kadioglu, Aras ^b   Lavelle, Ed C ^a  

^a TRINITY COLLEGE DUBLIN   (Ireland)

^b UNIVERSITY OF LEICESTER   (United Kingdom)

^c UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^d UNIVERSITY OF LAUSANNE   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CRYOPYRIN; CYTOKINE; ENDOTOXIN; GAMMA INTERFERON; INFLAMMASOME; INTERLEUKIN 12; INTERLEUKIN 17; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 23; INTERLEUKIN 6; PNEUMOCOCCUS VACCINE; PNEUMOLYSIN; SUBUNIT VACCINE; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR AGONIST; TUMOR NECROSIS FACTOR ALPHA ANTIBODY; AUTACOID; BACTERIAL PROTEIN; CARRIER PROTEIN; CIAS1 PROTEIN, MOUSE; PLY PROTEIN, STREPTOCOCCUS PNEUMONIAE; STREPTOLYSIN; TLR4 PROTEIN, MOUSE;

ADAPTIVE IMMUNITY; ADOPTIVE TRANSFER; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN SPECIFICITY; ARTICLE; CELL MATURATION; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DENDRITIC CELL; FEMALE; INFECTION PREVENTION; INFLAMMATION; LYMPHOCYTE PROLIFERATION; MOUSE; NONHUMAN; NOSE INFECTION; PNEUMOCOCCAL INFECTION; RESPIRATORY TRACT INFECTION; SPLEEN CELL; STREPTOCOCCUS PNEUMONIAE; T LYMPHOCYTE; ANIMAL; BAGG ALBINO MOUSE; BONE MARROW; C3H MOUSE; C57BL MOUSE; CELL CULTURE; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; IMMUNOLOGY; LUNG; LYMPHOCYTE ACTIVATION; METABOLISM; MICROBIOLOGY; NATURAL KILLER CELL; PATHOGENICITY; SECRETION; SPLEEN;

MUS; STREPTOCOCCUS PNEUMONIAE;

ANIMALS; BACTERIAL PROTEINS; BONE MARROW; CARRIER PROTEINS; CELLS, CULTURED; CYTOKINES; DENDRITIC CELLS; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; INFLAMMATION MEDIATORS; KILLER CELLS, NATURAL; LUNG; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED BALB C; MICE, INBRED C3H; MICE, INBRED C57BL; PNEUMOCOCCAL INFECTIONS; SPLEEN; STREPTOCOCCUS PNEUMONIAE; STREPTOLYSINS; TOLL-LIKE RECEPTOR 4;

EID: 79251515144     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1001191     Document Type: Article

References (49)

1. Tweten RK (2005) Cholesterol-dependent cytolysins, a family of versatile poreforming toxins. Infect Immun 73: 6199-6209.
2. Berry AM, Yother J, Briles DE, Hansman D, Paton JC (1989) Reduced virulence of a defined pneumolysin-negative mutant of Streptococcus pneumoniae. Infect Immun 57: 2037-2042.
3. Canvin JR, Marvin AP, Sivakumaran M, Paton JC, Boulnois GJ, et al. (1995) The role of pneumolysin and autolysin in the pathology of pneumonia and septicemia in mice infected with a type 2 pneumococcus. J Infect Dis 172: 119-123.
4. Kadioglu A, Gingles NA, Grattan K, Kerr A, Mitchell TJ, et al. (2000) Host cellular immune response to pneumococcal lung infection in mice. Infect Immun 68: 492-501.
5. Kadioglu A, Taylor S, Iannelli F, Pozzi G, Mitchell TJ, et al. (2002) Upper and lower respiratory tract infection by Streptococcus pneumoniae is affected by pneumolysin deficiency and differences in capsule type. Infect Immun 70: 2886-2890.
6. Feldman C, Munro NC, Jeffery PK, Mitchell TJ, Andrew PW, et al. (1991) Pneumolysin induces the salient histologic features of pneumococcal infection in the rat lung in vivo. Am J Respir Cell Mol Biol 5: 416-423.
7. Mitchell TJ, Andrew PW, Saunders FK, Smith AN, Boulnois GJ (1991) Complement activation and antibody binding by pneumolysin via a region of the toxin homologous to a human acute-phase protein. Mol Microbiol 5: 1883-1888.
8. Cockeran R, Steel HC, Mitchell TJ, Feldman C, Anderson R (2001) Pneumolysin potentiates production of prostaglandin E(2) and leukotriene B(4) by human neutrophils. Infect Immun 69: 3494-3496.
9. Cockeran R, Theron AJ, Steel HC, Matlola NM, Mitchell TJ, et al. (2001) Proinflammatory interactions of pneumolysin with human neutrophils. J Infect Dis 183: 604-611.
10. Kadioglu A, Coward W, Colston MJ, Hewitt CR, Andrew PW (2004) CD4-Tlymphocyte interactions with pneumolysin and pneumococci suggest a crucial protective role in the host response to pneumococcal infection. Infect Immun 72: 2689-2697.
11. Braun JS, Hoffmann O, Schickhaus M, Freyer D, Dagand E, et al. (2007) Pneumolysin causes neuronal cell death through mitochondrial damage. Infect Immun 75: 4245-4254.
12. Houldsworth S, Andrew PW, Mitchell TJ (1994) Pneumolysin stimulates production of tumor necrosis factor alpha and interleukin-1 beta by human mononuclear phagocytes. Infect Immun 62: 1501-1503.
13. Malley R, Henneke P, Morse SC, Cieslewicz MJ, Lipsitch M, et al. (2003) Recognition of pneumolysin by Toll-like receptor 4 confers resistance to pneumococcal infection. Proc Natl Acad Sci U S A 100: 1966-1971.
14. Srivastava A, Henneke P, Visintin A, Morse SC, Martin V, et al. (2005) The apoptotic response to pneumolysin is Toll-like receptor 4 dependent and protects against pneumococcal disease. Infect Immun 73: 6479-6487.
15. Ratner AJ, Hippe KR, Aguilar JL, Bender MH, Nelson AL, et al. (2006) Epithelial cells are sensitive detectors of bacterial pore-forming toxins. J Biol Chem 281: 12994-12998.
16. Koga T, Lim JH, Jono H, Ha UH, Xu H, et al. (2008) Tumor suppressor cylindromatosis acts as a negative regulator for Streptococcus pneumoniaeinduced NFAT signaling. J Biol Chem 283: 12546-12554.
17. Benton KA, Paton JC, Briles DE (1997) The hemolytic and complementactivating properties of pneumolysin do not contribute individually to virulence in a pneumococcal bacteremia model. Microb Pathog 23: 201-209.
18. Branger J, Knapp S, Weijer S, Leemans JC, Pater JM, et al. (2004) Role of Tolllike receptor 4 in gram-positive and gram-negative pneumonia in mice. Infect Immun 72: 788-794.
19. Rubins JB, Pomeroy C (1997) Role of gamma interferon in the pathogenesis of bacteremic pneumococcal pneumonia. Infect Immun 65: 2975-2977.
20. Nakamatsu M, Yamamoto N, Hatta M, Nakasone C, Kinjo T, et al. (2007) Role of interferon-gamma in Valpha14+ natural killer T cell-mediated host defense against Streptococcus pneumoniae infection in murine lungs. Microbes Infect 9: 364-374.
21. Lu YJ, Gross J, Bogaert D, Finn A, Bagrade L, et al. (2008) Interleukin-17A mediates acquired immunity to pneumococcal colonization. PLoS Pathog 4: e1000159.
22. Steinman RM, Hemmi H (2006) Dendritic cells: translating innate to adaptive immunity. Curr Top Microbiol Immunol 311: 17-58.
23. Martin-Fontecha A, Thomsen LL, Brett S, Gerard C, Lipp M, et al. (2004) Induced recruitment of NK cells to lymph nodes provides IFN-gamma for T(H)1 priming. Nat Immunol 5: 1260-1265.
24. Sutton CE, Lalor SJ, Sweeney CM, Brereton CF, Lavelle EC, et al. (2009) Interleukin-1 and IL-23 induce innate IL-17 production from gammadelta T cells, amplifying Th17 responses and autoimmunity. Immunity 31: 331-341.
25. Gingles NA, Alexander JE, Kadioglu A, Andrew PW, Kerr A, et al. (2001) Role of genetic resistance in invasive pneumococcal infection: identification and study of susceptibility and resistance in inbred mouse strains. Infect Immun 69: 426-434.
26. Kadioglu A, Andrew PW (2005) Susceptibility and resistance to pneumococcal disease in mice. Brief Funct Genomic Proteomic 4: 241-247.
27. Kafka D, Ling E, Feldman G, Benharroch D, Voronov E, et al. (2008) Contribution of IL-1 to resistance to Streptococcus pneumoniae infection. Int Immunol 20: 1139-1146.
28. Martinon F, Mayor A, Tschopp J (2009) The inflammasomes: guardians of the body. Annu Rev Immunol 27: 229-265.
29. Walev I, Reske K, Palmer M, Valeva A, Bhakdi S (1995) Potassium-inhibited processing of IL-1 beta in human monocytes. EMBO J 14: 1607-1614.
30. Gurcel L, Abrami L, Girardin S, Tschopp J, van der Goot FG (2006) Caspase-1 activation of lipid metabolic pathways in response to bacterial pore-forming toxins promotes cell survival. Cell 126: 1135-1145.
31. Hornung V, Bauernfeind F, Halle A, Samstad EO, Kono H, et al. (2008) Silica crystals and aluminum salts activate the NALP3 inflammasome through phagosomal destabilization. Nat Immunol 9: 847-856.
32. Yoshimori T, Yamamoto A, Moriyama Y, Futai M, Tashiro Y (1991) Bafilomycin A1, a specific inhibitor of vacuolar-type H(+)-ATPase, inhibits acidification and protein degradation in lysosomes of cultured cells. J Biol Chem 266: 17707-17712.
33. Martin B, Hirota K, Cua DJ, Stockinger B, Veldhoen M (2009) Interleukin-17-producing gammadelta T cells selectively expand in response to pathogen products and environmental signals. Immunity 31: 321-330.
34. Iwakura Y, Nakae S, Saijo S, Ishigame H (2008) The roles of IL-17A in inflammatory immune responses and host defense against pathogens. Immunol Rev 226: 57-79.
35. Stockinger B, Veldhoen M (2007) Differentiation and function of Th17 T cells. Curr Opin Immunol 19: 281-286.
36. Sutton C, Brereton C, Keogh B, Mills KH, Lavelle EC (2006) A crucial role for interleukin (IL)-1 in the induction of IL-17-producing T cells that mediate autoimmune encephalomyelitis. J Exp Med 203: 1685-1691.
37. Zhu J, Paul WE (2008) CD4 T cells: fates, functions, and faults. Blood 112: 1557-1569.
38. Shoma S, Tsuchiya K, Kawamura I, Nomura T, Hara H, et al. (2008) Critical involvement of pneumolysin in production of interleukin-1alpha and caspase-1-dependent cytokines in infection with Streptococcus pneumoniae in vitro: a novel function of pneumolysin in caspase-1 activation. Infect Immun 76: 1547-1557.
39. Riol-Blanco L, Lazarevic V, Awasthi A, Mitsdoerffer M, Wilson BS, et al. (2010) IL-23 receptor regulates unconventional IL-17-producing T cells that control bacterial infections. J Immunol 184: 1710-1720.
40. Benton KA, Everson MP, Briles DE (1995) A pneumolysin-negative mutant of Streptococcus pneumoniae causes chronic bacteremia rather than acute sepsis in mice. Infect Immun 63: 448-455.
41. Bergeron Y, Ouellet N, Deslauriers AM, Simard M, Olivier M, et al. (1998) Cytokine kinetics and other host factors in response to pneumococcal pulmonary infection in mice. Infect Immun 66: 912-922.
42. Zwijnenburg PJ, van der Poll T, Florquin S, Roord JJ, Van Furth AM (2003) IL- 1 receptor type 1 gene-deficient mice demonstrate an impaired host defense against pneumococcal meningitis. J Immunol 170: 4724-4730.
43. Broz P, Newton K, Lamkanfi M, Mariathasan S, Dixit VM, et al. (2010) Redundant roles for inflammasome receptors NLRP3 and NLRC4 in host defense against Salmonella. J Exp Med 207: 1745-1755.
44. Sharp FA, Ruane D, Claass B, Creagh E, Harris J, et al. (2009) Uptake of particulate vaccine adjuvants by dendritic cells activates the NALP3 inflammasome. Proc Natl Acad Sci U S A 106: 870-875.
45. Chu J, Thomas LM, Watkins SC, Franchi L, Nunez G, et al. (2009) Cholesteroldependent cytolysins induce rapid release of mature IL-1{beta} from murine macrophages in a NLRP3 inflammasome and cathepsin B-dependent manner. J Leukoc Biol.
46. Jones MR, Simms BT, Lupa MM, Kogan MS, Mizgerd JP (2005) Lung NFkappaB activation and neutrophil recruitment require IL-1 and TNF receptor signaling during pneumococcal pneumonia. J Immunol 175: 7530-7535.
47. Gilbert RJ, Rossjohn J, Parker MW, Tweten RK, Morgan PJ, et al. (1998) Selfinteraction of pneumolysin, the pore-forming protein toxin of Streptococcus pneumoniae. J Mol Biol 284: 1223-1237.
48. Lutz MB, Kukutsch N, Ogilvie AL, Rossner S, Koch F, et al. (1999) An advanced culture method for generating large quantities of highly pure dendritic cells from mouse bone marrow. J Immunol Methods 223: 77-92.
49. Davies JQ, Gordon S (2005) Isolation and culture of murine macrophages. Methods Mol Biol 290: 91-103.