Activation of the NLRP3 inflammasome is not a feature of all particulate vaccine adjuvants

Immunology and Cell Biology

Volumn 92, Issue 6, 2014, Pages 535-542

  Neumann, Silke ^a,b   Burkert, Kristina ^b,c   Kemp, Roslyn ^a   Rades, Thomas ^d   Dunbar, P Rod ^b,c   Hook, Sarah ^a,b  

^a UNIVERSITY OF OTAGO   (New Zealand)

^b MAURICE WILKINS CENTRE FOR MOLECULAR BIODISCOVERY   (New Zealand)

^c UNIVERSITY OF AUCKLAND   (New Zealand)

^d UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

ALUMINUM POTASSIUM SULFATE; CATHEPSIN B; CHITOSAN DERIVATIVE; CHITOSAN NANOPARTICLE; CRYOPYRIN; CUBOSOME; FREUND ADJUVANT; INFLAMMASOME; INTERLEUKIN 1BETA; LIPID; N (3 PROPYLCARBAMOYLOXIRANE 2 CARBONYL)ISOLEUCYLPROLINE; NANOPARTICLE; POLYMER; TOLL LIKE RECEPTOR AGONIST; UNCLASSIFIED DRUG; VACCINE; WATER OIL CREAM; ALUMINUM SULFATE; CARRIER PROTEIN; CHITOSAN; CIAS1 PROTEIN, MOUSE; CTSB PROTEIN, HUMAN; CTSB PROTEIN, MOUSE; IL1B PROTEIN, HUMAN; IL1B PROTEIN, MOUSE; IMMUNOLOGICAL ADJUVANT; NLRP3 PROTEIN, HUMAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BONE MARROW; CELL STRUCTURE; CONTROLLED STUDY; CYTOKINE RELEASE; DENDRITIC CELL; DRUG DELIVERY SYSTEM; DRUG FORMULATION; DRUG MANUFACTURE; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IMMUNOGENICITY; IN VITRO STUDY; IN VIVO STUDY; LYSOSOME; MALE; MEDIATOR; MOUSE; NONHUMAN; PARTICLE SIZE; PERIPHERAL BLOOD MONONUCLEAR CELL; PERITONEUM MACROPHAGE; ZETA POTENTIAL; ANIMAL; CLINICAL TRIAL; FEMALE; IMMUNOLOGY;

MURINAE; MUS;

ADJUVANTS, IMMUNOLOGIC; ALUM COMPOUNDS; ANIMALS; CARRIER PROTEINS; CATHEPSIN B; CHITOSAN; FEMALE; FREUND'S ADJUVANT; HUMANS; INFLAMMASOMES; INTERLEUKIN-1BETA; MALE; MICE; NANOPARTICLES;

EID: 84904042707     PISSN: 08189641     EISSN: 14401711     Source Type: Journal    
DOI: 10.1038/icb.2014.21     Document Type: Article

References (39)

1. Bachmann MF, Jennings GT. Vaccine delivery: a matter of size, geometry, kinetics and molecular patterns. Nat Rev Immunol 2010; 10: 787-796.
2. Kufer TA, Sansonetti PJ. NLR functions beyond pathogen recognition. Nat Immunol 2011; 12: 121-128.
3. Gross O, Thomas CJ, Guarda G, Tschopp J. The inflammasome: an integrated view. Immunol Rev 2011; 243: 136-151.
4. Guo L, Wei G, Zhu J, Liao W, Leonard WJ, Zhao K et al. IL-1 family members and STAT activators induce cytokine production by Th2, Th17, and Th1 cells. Proc Natl Acad Sci USA 2009; 106: 13463-13468.
5. Tschopp J, Schroder K. NLRP3 inflammasome activation: The convergence of multiple signalling pathways on ROS production? Nat Rev Immunol 2010; 10: 210-215.
6. Ferrari D, Pizzirani C, Adinolfi E, Lemoli RM, Curti A, Idzko M et al. The P2-7 receptor: a key player in IL-1 processing and release. J Immunol 2006; 176: 3877-3883. (Pubitemid 44264361)
7. Perregaux D, Gabel CA. Interleukin-1 beta maturation and release in response to ATP and nigericin. Evidence that potassium depletion mediated by these agents is a necessary and common feature of their activity. J Biol Chem 1994; 269: 15195-15203.
8. Hornung V, Bauernfeind F, Halle A, Samstad EO, Kono H, Rock KL et al. Silica crystals and aluminum salts activate the NALP3 inflammasome through phagosomal destabilization. Nat Immunol 2008; 9: 847-856.
9. Sharp FA, Ruane D, Claass B, Creagh E, Harris J, Malyala P et al. Uptake of particulate vaccine adjuvants by dendritic cells activates the NALP3 inflammasome. Proc Natl Acad Sci USA 2009; 106: 870-875.
10. Wang Y, Rahman D, Lehner TA. Comparative study of stress-mediated immunological functions with the adjuvanticity of alum. J Biol Chem 2012; 287: 17152-17160.
11. Bueter CL, Lee CK, Rathinam VAK, Healy GJ, Taron CH, Specht CA et al. Chitosan but not chitin activates the inflammasome by a mechanism dependent upon phagocytosis. J Biol Chem 2011; 286: 35447-35455.
12. Morishige T, Yoshioka Y, Inakura H, Tanabe A, Yao X, Narimatsu S et al. The effect of surface modification of amorphous silica particles on NLRP3 inflammasome mediated IL-1[beta] production, ROS production and endosomal rupture. Biomaterials 2010; 31: 6833-6842.
13. Rizwan SB, Boyd BJ, Rades T, Hook S. Bicontinuous cubic liquid crystals as sustained delivery systems for peptides and proteins. Expert Opin Drug Deliv 2010; 7: 1133-1144.
14. Gordon S, Teichmann E, Young K, Finnie K, Rades T, Hook S. In vitro and in vivo investigation of thermosensitive chitosan hydrogels containing silica nanoparticles for vaccine delivery. Eur J Pharm Sci 2010; 41: 360-368.
15. Chua BY, Al Kobaisi M, Zeng W, Mainwaring D, Jackson DC. Chitosan microparticles and nanoparticles as biocompatible delivery vehicles for peptide and protein-based immunocontraceptive vaccines. Mol Pharm 2012; 9: 81-90.
16. Nagpal K, Singh SK, Mishra DN. Chitosan nanoparticles: a promising system in novel drug delivery. Chem Pharm Bull 2010; 58: 1423-1430.
17. Rizwan SB, Assmus D, Boehnke A, Hanley T, Boyd BJ, Rades T et al. Preparation of phytantriol cubosomes by solvent precursor dilution for the delivery of protein vaccines. Eur J Pharm Biopharm 2011; 79: 15-22.
18. Racovita S, Vasiliu S, Popa M, Luca C. Polysaccarides based on micro-and nanoparticles obtained by ionic gelation and their applications as drug delivery systems. Revue Romaine de Chimie 2008; 54: 709-718.
19. Kouiavskaia DV, Berard CA, Datena E, Hussain A, Dawson N, Klyushnenkova EN et al. Vaccination with agonist peptide PSA: 154-163 (155L) derived from prostate specific antigen induced CD8 T-cell response to the native peptide PSA: 154-163 but failed to induce the reactivity against tumor targets expressing PSA: a phase 2 study in patients with recurrent prostate cancer. J Immunother 2009; 32: 655-666.
20. Koide S, Steinman RM. Induction of murine interleukin 1: stimuli and responsive primary cells. Proc Natl Acad Sci USA 1987; 84: 3802-3806. (Pubitemid 17088367)
21. Newman ZL, Leppla SH, Moayeri M. CA-074Me protection against anthrax lethal toxin. Infect Immun 2009; 77: 4327-4336.
22. Wilmar A, Lonez C, Vermeersch M, Andrianne M, Pérez-Morga D, Ruysschaert J-M et al. The cationic lipid, diC14 amidine, extends the adjuvant properties of aluminum salts through a TLR-4- and caspase-1-independent mechanism. Vaccine 2012; 30: 414-424.
23. St Pierre CA, Chan M, Iwakura Y, Ayers DC, Kurt-Jones EA, Finberg RW. Periprosthetic osteolysis: characterizing the innate immune response to titanium wear-particles. J Orthop Res 2010; 28: 1418-1424.
24. Martin WJ, Walton M, Harper J. Resident macrophages initiating and driving inflammation in a monosodium urate monohydrate crystal-induced murine peritoneal model of acute gout. Arthritis Rheum 2009; 60: 281-289.
25. Amidi M, Mastrobattista E, Jiskoot W, Hennink WE. Chitosan-based delivery systems for protein therapeutics and antigens. Adv Drug Deliv Rev 2010; 62: 59-82.
26. Rice-Ficht AC, Arenas-Gamboa AM, Kahl-McDonagh MM, Ficht TA. Polymeric particles in vaccine delivery. Curr Opin Microbiol 2010; 13: 106-112.
27. von Moltke J, Trinidad NJ, Moayeri M, Kintzer AF, Wang SB, van Rooijen N et al. Rapid induction of inflammatory lipid mediators by the inflammasome in vivo. Nature 2012; 490: 107-111.
28. Spreafico R, Ricciardi-Castagnoli P, Mortellaro A. The controversial relationship between NLRP3, alum, danger signals and the next-generation adjuvants. Eur J Immunol 2010; 40: 638-642.
29. Hossain A, Zheng CL, Kukita A, Kohashi O. Balance of Th1/Th2 cytokines associated with the preventive effect of incomplete freund's adjuvant on the development of adjuvant arthritis in LEW Rats. J Autoimmunity 2001; 17: 289-295. (Pubitemid 34098412)
30. de Souza JB. Immunization of Experimental Animals. eLS: John Wiley & Sons, Ltd, 2001.
31. Pazar B, Ea HK, Narayan S, Kolly L, Bagnoud N, Chobaz V et al. Basic calcium phosphate crystals induce monocyte/macrophage IL-1beta secretion through the NLRP3 inflammasome in vitro. J Immunol 2011; 186: 2495-2502.
32. Demento SL, Eisenbarth SC, Foellmer HG, Platt C, Caplan MJ, Mark Saltzman W et al. Inflammasome-activating nanoparticles as modular systems for optimizing vaccine efficacy. Vaccine 2009; 27: 3013-3021.
33. Vaine CA, Patel MK, Zhu J, Lee E, Finberg RW, Hayward RC et al. Tuning innate immune activation by surface texturing of polymer microparticles: the role of shape in inflammasome activation. J Immunol 2013; 190: 3525-3532.
34. Li R, Wang X, Ji Z, Sun B, Zhang H, Chang CH et al. Surface charge and cellular processing of covalently functionalized multiwall carbon nanotubes determine pulmonary toxicity. ACS Nano 2013; 7: 2352-2368.
35. Underhill DM, Goodridge HS. Information processing during phagocytosis. Nat Rev Immunol 2012; 12: 492-502.
36. Foti M, Granucci F, Aggujaro D, Liboi E, Luini W, Minardi S et al. Upon dendritic cell (DC) activation chemokines and chemokine receptor expression are rapidly regulated for recruitment and maintenance of DC at the inflammatory site. Int Immunol 1999; 11: 979-986. (Pubitemid 29276610)
37. Tsai ML, Bai SW, Chen RH. Cavitation effects versus stretch effects resulted in different size and polydispersity of ionotropic gelation chitosan-sodium tripolyphosphate nanoparticle. Carbohydr Polym 2008; 71: 448-457. (Pubitemid 350181062)
38. Rosenberg SA, Yang JC, Kammula US, Hughes MS, Restifo NP, Schwarz SL et al. Different adjuvanticity of incomplete Freund's adjuvant derived from beef or vegetable components in melanoma patients immunized with a peptide vaccine. J Immunother 2010; 33: 626-629.
39. Scheicher C, Mehlig M, Zecher R, Reske K. Dendritic cells from mouse bone marrow: In vitro differentiation using low doses of recombinant granulocyte-macrophage colonystimulating factor. J Immunol Methods 1992; 154: 253-264.