Home LiteratureArticle Details
PMID: 21270336 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Inflammasome-independent role of the apoptosis-associated speck-like protein containing CARD (ASC) in the adjuvant effect of MF59.

Ellebedy AH, Lupfer C, Ghoneim HE, DeBeauchamp J, Kanneganti TD, Webby RJ

Abstract

Clinical studies have indicated that subvirion inactivated vaccines against avian influenza viruses, particularly H5N1, are poorly immunogenic in humans. As a consequence, the use of adjuvants has been championed for the efficient vaccination of a naïve population against avian influenza. Aluminum salts (alum) and the oil-in-water emulsion MF59 are safe and effective adjuvants that are being used with influenza vaccines, but the mechanism underlying their stimulation of the immune system remains poorly understood. It was shown recently that activation of a cytosolic innate immune-sensing complex known as "NLR-Pyrin domain containing 3" (NLRP3) inflammasome, also known as "cryopyrin," "cold-induced autoinflammatory syndrome 1" (CIAS1), or nacht domain-, leucine-rich repeat-, and PYD-containing protein 3 (Nalp3), is essential for the adjuvant effect of alum. Here we show that the inflammasome component apoptosis-associated speck-like protein containing a caspase recruitment domain (ASC), an adapter protein within the NLRP3 inflammasome, is a crucial element in the adjuvant effect of MF59 when combined with H5N1 subunit vaccines. In the absence of ASC, H5-specific IgG antibody responses are significantly reduced, whereas the responses are intact in NLRP3(-/-) and caspase-1(-/-) mice. This defect is caused mainly by the failure of antigen-specific B cells to switch from IgM to IgG production. We conclude that ASC plays an inflammasome-independent role in the induction of antigen-specific humoral immunity after vaccination with MF59-adjuvanted influenza vaccines. These findings have important implications for the rational design of next-generation adjuvants.

MeSH Terms
Adjuvants, Immunologic/therapeutic use Animals CARD Signaling Adaptor Proteins Carrier Proteins/genetics,immunology,metabolism Caspase 1/genetics,immunology Cytokines/immunology Cytoskeletal Proteins/genetics,immunology,metabolism Enzyme-Linked Immunosorbent Assay Enzyme-Linked Immunospot Assay Flow Cytometry Hemagglutination Tests Humans Influenza A Virus, H5N1 Subtype/immunology Influenza Vaccines/therapeutic use Influenza, Human/prevention & control Mice Mice, Knockout NLR Family, Pyrin Domain-Containing 3 Protein Polysorbates/therapeutic use Squalene/therapeutic use Statistics, Nonparametric
Chemicals
Adjuvants, Immunologic CARD Signaling Adaptor Proteins Carrier Proteins Cytokines Cytoskeletal Proteins Influenza Vaccines MF59 oil emulsion NLR Family, Pyrin Domain-Containing 3 Protein NLRP3 protein, human PYCARD protein, human Polysorbates Squalene Caspase 1
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Ellebedy Ali H
Department of Infectious Diseases, St. Jude Children's Research Hospital, Memphis, TN 38105, USA.
Lupfer Christopher
Ghoneim Hazem E
DeBeauchamp Jennifer
Kanneganti Thirumala-Devi
Webby Richard J
References (28)
28 references, click to expand
  1. Combination adjuvants for the induction of potent, long-lasting antibody and T-cell responses to influenza vaccine in mice.
    Vaccine. 2008 Jan 24;26(4):552-61 PMID: 18162266
  2. Comparison of three different influenza vaccines in institutionalised elderly.
    Vaccine. 2001 May 14;19(25-26):3472-5 PMID: 11348713
  3. Cutting edge: alum adjuvant stimulates inflammatory dendritic cells through activation of the NALP3 inflammasome.
    J Immunol. 2008 Sep 15;181(6):3755-9 PMID: 18768827
  4. NALP3: a key player in caspase-1 activation.
    J Endotoxin Res. 2006;12(4):251-6 PMID: 16953978
  5. Dendritic cells internalize vaccine adjuvant after intramuscular injection.
    Cell Immunol. 1998 May 25;186(1):18-27 PMID: 9637761
  6. Detection of anti-H5 responses in human sera by HI using horse erythrocytes following MF59-adjuvanted influenza A/Duck/Singapore/97 vaccine.
    Virus Res. 2004 Jul;103(1-2):91-5 PMID: 15163495
  7. Germinal center reaction.
    Curr Opin Hematol. 2001 Jan;8(1):52-9 PMID: 11138628
  8. Adjuvant-enhanced antibody responses in the absence of toll-like receptor signaling.
    Science. 2006 Dec 22;314(5807):1936-8 PMID: 17185603
  9. Inflammasomes: guardians of cytosolic sanctity.
    Immunol Rev. 2009 Jan;227(1):95-105 PMID: 19120479
  10. Safety and immunogenicity of an inactivated split-virion influenza A/Vietnam/1194/2004 (H5N1) vaccine: phase I randomised trial.
    Lancet. 2006 May 20;367(9523):1657-64 PMID: 16714186
  11. Safety and immunogenicity of nonadjuvanted and MF59-adjuvanted influenza A/H9N2 vaccine preparations.
    Clin Infect Dis. 2006 Nov 1;43(9):1135-42 PMID: 17029131
  12. Effects of adjuvants on the safety and immunogenicity of an avian influenza H5N1 vaccine in adults.
    J Infect Dis. 2008 Mar 1;197(5):667-75 PMID: 18260764
  13. Fast rise of broadly cross-reactive antibodies after boosting long-lived human memory B cells primed by an MF59 adjuvanted prepandemic vaccine.
    Proc Natl Acad Sci U S A. 2009 May 12;106(19):7962-7 PMID: 19416838
  14. Cutting edge: critical role for PYCARD/ASC in the development of experimental autoimmune encephalomyelitis.
    J Immunol. 2010 May 1;184(9):4610-4 PMID: 20368281
  15. Cutting edge: inflammasome activation by alum and alum's adjuvant effect are mediated by NLRP3.
    J Immunol. 2008 Jul 1;181(1):17-21 PMID: 18566365
  16. Intracellular NOD-like receptors in host defense and disease.
    Immunity. 2007 Oct;27(4):549-59 PMID: 17967410
  17. Safety and antigenicity of non-adjuvanted and MF59-adjuvanted influenza A/Duck/Singapore/97 (H5N3) vaccine: a randomised trial of two potential vaccines against H5N1 influenza.
    Lancet. 2001 Jun 16;357(9272):1937-43 PMID: 11425416
  18. The adjuvants aluminum hydroxide and MF59 induce monocyte and granulocyte chemoattractants and enhance monocyte differentiation toward dendritic cells.
    J Immunol. 2008 Apr 15;180(8):5402-12 PMID: 18390722
  19. Cross-reactivity to highly pathogenic avian influenza H5N1 viruses after vaccination with nonadjuvanted and MF59-adjuvanted influenza A/Duck/Singapore/97 (H5N3) vaccine: a potential priming strategy.
    J Infect Dis. 2005 Apr 15;191(8):1210-5 PMID: 15776364
  20. Crucial role for the Nalp3 inflammasome in the immunostimulatory properties of aluminium adjuvants.
    Nature. 2008 Jun 19;453(7198):1122-6 PMID: 18496530
  21. Adjuvanted H5N1 vaccine induces early CD4+ T cell response that predicts long-term persistence of protective antibody levels.
    Proc Natl Acad Sci U S A. 2009 Mar 10;106(10):3877-82 PMID: 19237568
  22. Adjuvants for pandemic influenza vaccines.
    Curr Top Microbiol Immunol. 2009;333:323-44 PMID: 19768413
  23. Inflammasome-independent role of apoptosis-associated speck-like protein containing a CARD (ASC) in T cell priming is critical for collagen-induced arthritis.
    J Biol Chem. 2010 Apr 16;285(16):12454-62 PMID: 20177071
  24. The Nlrp3 inflammasome is critical for aluminium hydroxide-mediated IL-1beta secretion but dispensable for adjuvant activity.
    Eur J Immunol. 2008 Aug;38(8):2085-9 PMID: 18624356
  25. Broad Clade 2 cross-reactive immunity induced by an adjuvanted clade 1 rH5N1 pandemic influenza vaccine.
    PLoS One. 2008 Feb 27;3(2):e1665 PMID: 18301743
  26. Alum induces innate immune responses through macrophage and mast cell sensors, but these sensors are not required for alum to act as an adjuvant for specific immunity.
    J Immunol. 2009 Oct 1;183(7):4403-14 PMID: 19734227
  27. Safety and immunogenicity of an inactivated subvirion influenza A (H5N1) vaccine.
    N Engl J Med. 2006 Mar 30;354(13):1343-51 PMID: 16571878
  28. The NLR gene family: a standard nomenclature.
    Immunity. 2008 Mar;28(3):285-7 PMID: 18341998
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
1091-6490
Published
2011-02-15
Epub
2011-00-26
Pages
2927-32
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC3041074
Subset
IM
Grants
NIAID NIH HHS · HHSN266200700005C · United States
NIAMS NIH HHS · R01 AR056296 · United States
NIAMS NIH HHS · AR056296 · United States
Corrections
ErratumIn
-
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com