Activation of the NLRP3 inflammasome in dendritic cells induces IL-1Β-dependent adaptive immunity against tumors

Nature Medicine

Volumn 15, Issue 10, 2009, Pages 1170-1178

  Ghiringhelli, François ^a,b   Apetoh, Lionel ^a,b,d,e   Tesniere, Antoine ^a,b,d   Aymeric, Laetitia ^a,b,d   Ma, Yuting ^a,b,d   Ortiz, Carla ^a,b,d,f   Vermaelen, Karim ^a,b,d,g   Panaretakis, Theocharis ^a,b,d   Mignot, Grégoire ^a,b,c   Ullrich, Evelyn ^a,b,d   Perfettini, Jean Luc ^a,b,d   Schlemmer, Frédéric ^a,b,d   Tasdemir, Ezgi ^a,b,d   Uhl, Martin ^h   Génin, Pierre ⁱ   Civas, Ahmet ⁱ   Ryffel, Bernhard ^j   Kanellopoulos, Jean ⁱ   Tschopp, Jürg ^k   André, Fabrice ^a,b,d   Lidereau, Rosette ^l   McLaughlin, Nicole M ^m   Haynes, Nicole M ^m   Smyth, Mark J ^m   Kroemer, Guido ^a,b,d   Zitvogel, Laurence ^a,b,n   more..

^a INSERM   (France)

^b INSTITUT GUSTAVE ROUSSY   (France)

^c CENTRE GEORGES FRANÇOIS LECLERC   (France)

^d UNIVERSITÉ PARIS SACLAY   (France)

^e BRIGHAM AND WOMEN S HOSPITAL   (United States)

^f UNIVERSITY OF CHILE   (Chile)

^g GHENT UNIVERSITY HOSPITAL   (Belgium)

^h INSTITUT PASTEUR   (France)

ⁱ CNRS   (France)

^j Laboratoire d'Immunologie et Embryologie Moleculaires Orleans   (France)

^k UNIVERSITY OF LAUSANNE   (Switzerland)

^l CENTRE RENÉ HUGUENIN   (France)

^m PETER MACCALLUM CANCER CENTRE   (Australia)

ⁿ CIC BT507   (France)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; ANTHRACYCLINE; CRYOPYRIN; DOXORUBICIN; GAMMA INTERFERON; INTERLEUKIN 1 RECEPTOR; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; NUCLEOTIDE BINDING OLIGOMERIZATION DOMAIN LIKE RECEPTOR; OXALIPLATIN; PURINERGIC P2X7 RECEPTOR;

ADAPTIVE IMMUNITY; ALLELE; ANIMAL CELL; ANIMAL EXPERIMENT; ANTIGEN RECOGNITION; ARTICLE; BREAST CANCER; BREAST METASTASIS; CANCER CHEMOTHERAPY; CD8+ T LYMPHOCYTE; CELL STIMULATION; COLON CANCER; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; DRUG EFFICACY; FIBROSARCOMA; HUMAN; INNATE IMMUNITY; LOSS OF FUNCTION MUTATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN INDUCTION; SINGLE NUCLEOTIDE POLYMORPHISM; T CELL LYMPHOMA; TUMOR CELL DESTRUCTION; TUMOR IMMUNITY;

MUS;

EID: 70350569295     PISSN: 10788956     EISSN: 1546170X     Source Type: Journal    
DOI: 10.1038/nm.2028     Document Type: Article

References (52)

1. Matzinger, P. The danger model: a renewed sense of self. Science 296, 301-305 (2002).
2. Savill, J., Dransfeld, I., Gregory, C. & Haslett, C. A blast from the past: clearance of apoptotic cells regulates immune responses. Nat. Rev. Immunol. 2, 965-975 (2002).
3. Leadbetter, E.A. et al. Chromatin-IgG complexes activate B cells by dual engagement of IgM and Toll-like receptors. Nature 416, 603-607 (2002).
4. Lau, C.M. et al. RNA-associated autoantigens activate B cells by combined B cell antigen receptor/Toll-like receptor 7 engagement. J. Exp. Med. 202, 1171-1177 (2005).
5. Chen, C.J. et al. Identifcation of a key pathway required for the sterile infammatory response triggered by dying cells. Nat. Med. 13, 851-856 (2007).
6. Akira, S., Uematsu, S. & Takeuchi, O. Pathogen recognition and innate immunity. Cell 124, 783-801 (2006).
7. Fritz, J.H., Ferrero, R.L., Philpott, D.J. & Girardin, S.E. Nod-like proteins in immunity, infammation and disease. Nat. Immunol. 7, 1250-1257 (2006).
8. Medzhitov, R. Toll-like receptors and innate immunity. Nat. Rev. Immunol. 1, 135-145 (2001).
9. Beutler, B. et al. Genetic analysis of host resistance: Toll-like receptor signaling and immunity at large. Annu. Rev. Immunol. 24, 353-389 (2006).
10. Zitvogel, L., Apetoh, L., Ghiringhelli, F. & Kroemer, G. Immunological aspects of cancer chemotherapy. Nat. Rev. Immunol. 8, 59-73 (2008).
11. Obeid, M. et al. Calreticulin exposure is required for the immunogenicity of gamma-irradiation and UVC light-induced apoptosis. Cell Death Differ. 14, 1848-1850 (2007).
12. Banchereau, J. & Steinman, R.M. Dendritic cells and the control of immunity. Nature 392, 245-252 (1998).
13. Obeid, M. et al. Calreticulin exposure dictates the immunogenicity of cancer cell death. Nat. Med. 13, 54-61 (2007).
14. Lotze, M.T. et al. The grateful dead: damage-associated molecular pattern molecules and reduction/oxidation regulate immunity. Immunol. Rev. 220, 60-81 (2007).
15. Apetoh, L. et al. Toll-like receptor 4-dependent contribution of the immune system to anticancer chemotherapy and radiotherapy. Nat. Med. 13, 1050-1059 (2007).
16. Sancho, D. et al. Identifcation of a dendritic cell receptor that couples sensing of necrosis to immunity. Nature 458, 899-903 (2009).
17. Martinon, F. & Tschopp, J. Infammatory caspases and infammasomes: master switches of infammation. Cell Death Differ. 14, 10-22 (2007).
18. Di Virgilio, F. Liaisons dangereuses: P2X7 and the infammasome. Trends Pharmacol. Sci. 28, 465-472 (2007).
19. Eisenbarth, S.C., Colegio, O.R., O'Connor, W., Sutterwala, F.S. & Flavell, R.A. Crucial role for the Nalp3 infammasome in the immunostimulatory properties of aluminium adjuvants. Nature 453, 1122-1126 (2008).
20. Agostini, L. et al. NALP3 forms an IL-1β-processing infammasome with increased activity in Muckle-Wells autoinfammatory disorder. Immunity 20, 319-325 (2004).
21. Poyet, J.L. et al. Identifcation of Ipaf, a human caspase-1-activating protein related to Apaf-1. J. Biol. Chem. 276, 28309-28313 (2001).
22. Martinon, F. , Burns, K. & Tschopp, J. The infammasome: a molecular platform triggering activation of infammatory caspases and processing of proIL-β. Mol. Cell 10, 417-426 (2002).
23. Sutterwala, F.S. et al. Critical role for NALP3/CIAS1/Cryopyrin in innate and adaptive immunity through its regulation of caspase-1. Immunity 24, 317-327 (2006).
24. Martinon, F., Petrilli, V., Mayor, A., Tardivel, A. & Tschopp, J. Gout-associated uric acid crystals activate the NALP3 infammasome. Nature 440, 237-241 (2006).
25. Mariathasan, S. et al. Cryopyrin activates the infammasome in response to toxins and ATP. Nature 440, 228-232 (2006).
26. Ferrari, D. et al. The P2X7 receptor: a key player in IL-1 processing and release. J. Immunol. 176, 3877-3883 (2006).
27. Kanneganti, T.D. et al. Critical role for Cryopyrin/Nalp3 in activation of caspase-1 in response to viral infection and double-stranded RNA. J. Biol. Chem. 281, 36560-36568 (2006).
28. Kanneganti, T.D. et al. Bacterial RNA and small antiviral compounds activate caspase-1 through cryopyrin/Nalp3. Nature 440, 233-236 (2006).
29. Ogura, Y., Sutterwala, F.S. & Flavell, R.A. The infammasome: frst line of the immune response to cell stress. Cell 126, 659-662 (2006).
30. Dinarello, C.A. Interleukin-1β, interleukin-18, and the interleukin-1β converting enzyme. Ann. NY Acad. Sci. 856, 1-11 (1998).
31. Brydges, S. & Kastner, D.L. The systemic autoinfammatory diseases: inborn errors of the innate immune system. Curr. Top. Microbiol. Immunol. 305, 127-160 (2006).
32. Reginato, A.M. & Olsen, B.R. Genetics and experimental models of crystal-induced arthritis. Lessons learned from mice and men: is it crystal clear? Curr. Opin. Rheumatol. 19, 134-145 (2007).
33. McIntyre, K.W. et al. Inhibition of interleukin 1 (IL-1) binding and bioactivity in vitro and modulation of acute infammation in vivo by IL-1 receptor antagonist and anti-IL-1 receptor monoclonal antibody. J. Exp. Med. 173, 931-939 (1991).
34. Selzner, N. et al. Water induces autocrine stimulation of tumor cell killing through ATP release and P2 receptor binding. Cell Death Differ. 11(Suppl 2), S172-S180 (2004).
35. Solle, M. et al. Altered cytokine production in mice lacking P2X7 receptors. J. Biol. Chem. 276, 125-132 (2001).
36. Srinivasula, S.M. et al. The PYRIN-CARD protein ASC is an activating adaptor for caspase-1. J. Biol. Chem. 277, 21119-21122 (2002).
37. Koebel, CM. et al. Adaptive immunity maintains occult cancer in an equilibrium state. Nature 450, 903-907 (2007).
38. Gu, B.J. et al. A Glu-496 to Ala polymorphism leads to loss of function of the human P2X7 receptor. J. Biol. Chem. 276, 11135-11142 (2001).
39. Sluyter, R., Shemon, A.N. & Wiley, J.S. Glu496 to Ala polymorphism in the P2X7 receptor impairs ATP-induced IL-1p1 release from human monocytes. J. Immunol. 172, 3399-3405 (2004).
40. Bours, M.J., Swennen, E.L., Di Virgilio, F., Cronstein, B.N. & Dagnelie, P.C. Adenosine 5'-triphosphate and adenosine as endogenous signaling molecules in immunity and infammation. Pharmacol. Ther. 112, 358-404 (2006).
41. Blankenstein, T. The role of tumor stroma in the interaction between tumor and immune system. Curr. Opin. Immunol. 17, 180-186 (2005).
42. Hinrichs, C.S., Gattinoni, L. & Restifo, N.P. Programming CD8+ T cells for effective immunotherapy. Curr. Opin. Immunol. 18, 363-370 (2006).
43. Ferrari, D., Chiozzi, P., Falzoni, S., Hanau, S. & Di Virgilio, F. Purinergic modulation of interleukin-1p release from microglial cells stimulated with bacterial endotoxin. J. Exp. Med. 185, 579-582 (1997).
44. Adachi, O. et al. Targeted disruption of the Myd88 gene results in loss of IL-1-and IL-18-mediated function. Immunity 9, 143-150 (1998).
45. Franchi, L, Kanneganti, T.D., Dubyak, G.R. & Nunez, G. Differential requirement of P2X7 receptor and intracellular K+ for caspase-1 activation induced by intracellular and extracellular bacteria. J. Biol. Chem. 282, 18810-18818 (2007).
46. Muruve, D.A. et al. The infammasome recognizes cytosolic microbial and host DNA and triggers an innate immune response. Nature 452, 103-107 (2008).
47. Pétrilli, V., Dostert, C, Muruve, D.A. & Tschopp, J. The infammasome: a danger sensing complex triggering innate immunity. Curr. Opin. Immunol. 19, 615-622 (2007).
48. Krelin, Y. et al. Interleukin-1p-driven infammation promotes the development and invasiveness of chemical carcinogen-induced tumors. Cancer Res. 67, 1062-1071 (2007).
49. Hagemann, T., Balkwill, F. & Lawrence, T. Infammation and cancer: a double-edged sword. Cancer Cell 12, 300-301 (2007).
50. Greten, F.R. et al. IKKp links infammation and tumorigenesis in a mouse model of colitis-associated cancer. Cell 118, 285-296 (2004).
51. Naugler, W.E. et al. Gender disparity in liver cancer due to sex differences in MyD88-dependent IL-6 production. Science 317, 121-124 (2007).
52. Balkwill, F., Charles, K.A. & Mantovani, A. Smoldering and polarized infammation in the initiation and promotion of malignant disease. Cancer Cell 7, 211-217 (2005).