Impaired NLRP3 inflammasome function in elderly mice during influenza infection is rescued by treatment with nigericin

Journal of Immunology

Volumn 188, Issue 6, 2012, Pages 2815-2824

  Stout Delgado, Heather W ^a   Vaughan, Sarah E ^a   Shirali, Anushree C ^b   Jaramillo, Richard J ^a   Harrod, Kevin S ^a  

^a LOVELACE RESPIRATORY RESEARCH INSTITUTE   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CRYOPYRIN; INFLAMMASOME; INTERLEUKIN 18; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; INTERLEUKIN 33; NIGERICIN;

ADOPTIVE TRANSFER; AGE DISTRIBUTION; AGING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL INFILTRATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DENDRITIC CELL; ENZYME ACTIVATION; ENZYME ACTIVITY; FEMALE; IN VITRO STUDY; IN VIVO STUDY; INFECTION SENSITIVITY; INFLUENZA; MALE; MORBIDITY; MORTALITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEFECT; PROTEIN EXPRESSION; PROTEIN FUNCTION; RISK REDUCTION; SIGNAL TRANSDUCTION; TREATMENT RESPONSE; VIRUS STRAIN;

ADOPTIVE TRANSFER; AGING; ANIMALS; ANTIVIRAL AGENTS; BLOTTING, WESTERN; CARRIER PROTEINS; CASPASE 1; DISEASE MODELS, ANIMAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; INFLAMMASOMES; MALE; MICE; MICE, INBRED BALB C; NIGERICIN; ORTHOMYXOVIRIDAE INFECTIONS; REAL-TIME POLYMERASE CHAIN REACTION;

EID: 84857866008     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1103051     Document Type: Article

References (48)

1. La Gruta, N. L., K. Kedzierska, J. Stambas, and P. C. Doherty. 2007. A question of self-preservation: immunopathology in influenza virus infection. Immunol. Cell Biol. 85: 85-92. (Pubitemid 46398724)
2. Toapanta, F. R., and T. M. Ross. 2009. Impaired immune responses in the lungs of aged mice following influenza infection. Respir. Res. 10: 112.
3. Gruver, A. L., L. L. Hudson, and G. D. Sempowski. 2007. Immunosenescence of ageing. J. Pathol. 211: 144-156. (Pubitemid 46195513)
4. Jiang, J., E. M. Fisher, and D. M. Murasko. 2011. CD8 T cell responses to influenza virus infection in aged mice. Ageing Res. Rev. 10: 422-427.
5. Gardner, E. M., E. W. Gonzalez, S. Nogusa, and D. M. Murasko. 2006. Agerelated changes in the immune response to influenza vaccination in a racially diverse, healthy elderly population. Vaccine 24: 1609-1614. (Pubitemid 43238237)
6. Po, J. L., E. M. Gardner, F. Anaraki, P. D. Katsikis, and D. M. Murasko. 2002. Age-associated decrease in virus-specific CD8+ T lymphocytes during primary influenza infection. Mech. Ageing Dev. 123: 1167-1181. (Pubitemid 34603100)
7. Effros, R. B., and R. L. Walford. 1983. The immune response of aged mice to influenza: diminished T-cell proliferation, interleukin 2 production and cytotoxicity. Cell. Immunol. 81: 298-305. (Pubitemid 13017143)
8. Effros, R. B., and R. L. Walford. 1983. Diminished T-cell response to influenza virus in aged mice. Immunology 49: 387-392. (Pubitemid 13096788)
9. Iwasaki, A., and R. Medzhitov. 2004. Toll-like receptor control of the adaptive immune responses. Nat. Immunol. 5: 987-995. (Pubitemid 41057715)
10. Diebold, S. S., T. Kaisho, H. Hemmi, S. Akira, and C. Reis e Sousa. 2004. Innate antiviral responses by means of TLR7-mediated recognition of single-stranded RNA. Science 303: 1529-1531.
11. Ichinohe, T., H. K. Lee, Y. Ogura, R. Flavell, and A. Iwasaki. 2009. Inflammasome recognition of influenza virus is essential for adaptive immune responses. J. Exp. Med. 206: 79-87.
12. Rehwinkel, J. 2010. Exposing viruses: RNA patterns sensed by RIG-I-like receptors. J. Clin. Immunol. 30: 491-495.
13. Rehwinkel, J., C. P. Tan, D. Goubau, O. Schulz, A. Pichlmair, K. Bier, N. Robb, F. Vreede, W. Barclay, E. Fodor, and C. Reis e Sousa. 2010. RIG-I detects viral genomic RNA during negative-strand RNA virus infection. Cell 140: 397-408.
14. Panda, A., F. Qian, S. Mohanty, D. van Duin, F. K. Newman, L. Zhang, S. Chen, V. Towle, R. B. Belshe, E. Fikrig, et al. 2010. Age-associated decrease in TLR function in primary human dendritic cells predicts influenza vaccine response. J. Immunol. 184: 2518-2527.
15. Shaw, A. C., S. Joshi, H. Greenwood, A. Panda, and J. M. Lord. 2010. Aging of the innate immune system. Curr. Opin. Immunol. 22: 507-513.
16. Wong, C. P., K. R. Magnusson, and E. Ho. 2010. Aging is associated with altered dendritic cells subset distribution and impaired proinflammatory cytokine production. Exp. Gerontol. 45: 163-169.
17. Agrawal, A., S. Agrawal, J. Tay, and S. Gupta. 2008. Biology of dendritic cells in aging. J. Clin. Immunol. 28: 14-20.
18. Qian, F., X. Wang, L. Zhang, A. Lin, H. Zhao, E. Fikrig, and R. R. Montgomery. 2011. Impaired interferon signaling in dendritic cells from older donors infected in vitro with West Nile virus. J. Infect. Dis. 203: 1415-1424.
19. Ichinohe, T., I. K. Pang, and A. Iwasaki. 2010. Influenza virus activates inflammasomes via its intracellular M2 ion channel. Nat. Immunol. 11: 404-410.
20. Nakahira, K., J. A. Haspel, V. A. Rathinam, S. J. Lee, T. Dolinay, H. C. Lam, J. A. Englert, M. Rabinovitch, M. Cernadas, H. P. Kim, et al. 2011. Autophagy proteins regulate innate immune responses by inhibiting the release of mitochondrial DNA mediated by the NALP3 inflammasome. Nat. Immunol. 12: 222-230.
21. Elinav, E., T. Strowig, J. Henao-Mejia, and R. A. Flavell. 2011. Regulation of the antimicrobial response by NLR proteins. Immunity 34: 665-679.
22. Mutini, C., S. Falzoni, D. Ferrari, P. Chiozzi, A. Morelli, O. R. Baricordi, G. Collo, P. Ricciardi-Castagnoli, and F. Di Virgilio. 1999. Mouse dendritic cells express the P2X7 purinergic receptor: characterization and possible participation in antigen presentation. J. Immunol. 163: 1958-1965. (Pubitemid 29382198)
23. Thomas, P. G., P. Dash, J. R. Aldridge, Jr., A. H. Ellebedy, C. Reynolds, A. J. Funk, W. J. Martin, M. Lamkanfi, R. J. Webby, K. L. Boyd, et al. 2009. The intracellular sensor NLRP3 mediates key innate and healing responses to influenza A virus via the regulation of caspase-1. Immunity 30: 566-575.
24. Allen, I. C., M. A. Scull, C. B. Moore, E. K. Holl, E. McElvania-TeKippe, D. J. Taxman, E. H. Guthrie, R. J. Pickles, and J. P. Ting. 2009. The NLRP3 inflammasome mediates in vivo innate immunity to influenza A virus through recognition of viral RNA. Immunity 30: 556-565.
25. Szretter, K. J., A. L. Balish, and J. M. Katz. 2006. Influenza: propagation, quantification, and storage. Curr. Protoc. Microbiol. Chapter 15: Unit 15G.1
26. Inaba, K., M. Inaba, N. Romani, H. Aya, M. Deguchi, S. Ikehara, S. Muramatsu, and R. M. Steinman. 1992. Generation of large numbers of dendritic cells from mouse bone marrow cultures supplemented with granulocyte/macrophage colony-stimulating factor. J. Exp. Med. 176: 1693-1702.
27. Sauer, K. A., P. Scholtes, R. Karwot, and S. Finotto. 2006. Isolation of CD4+ T cells from murine lungs: a method to analyze ongoing immune responses in the lung. Nat. Protoc. 1: 2870-2875.
28. Dimmock, N. J., and A. C. Marriott. 2006. In vivo antiviral activity: defective interfering virus protects better against virulent Influenza A virus than avirulent virus. J. Gen. Virol. 87: 1259-1265.
29. Bender, B. S., S. F. Taylor, D. S. Zander, and R. Cottey. 1995. Pulmonary immune response of young and aged mice after influenza challenge. J. Lab. Clin. Med. 126: 169-177.
30. Murasko, D. M., and J. Jiang. 2005. Response of aged mice to primary virus infections. Immunol. Rev. 205: 285-296. (Pubitemid 40780192)
31. Kanneganti, T. D., N. Ozören, M. Body-Malapel, A. Amer, J. H. Park, L. Franchi, J. Whitfield, W. Barchet, M. Colonna, P. Vandenabeele, et al. 2006. Bacterial RNA and small antiviral compounds activate caspase-1 through cryopyrin/ Nalp3. Nature 440: 233-236. (Pubitemid 43372103)
32. Sutterwala, F. S., Y. Ogura, M. Szczepanik, M. Lara-Tejero, G. S. Lichtenberger, E. P. Grant, J. Bertin, A. J. Coyle, J. E. Galán, P. W. Askenase, and R. A. Flavell. 2006. Critical role for NALP3/CIAS1/Cryopyrin in innate and adaptive immunity through its regulation of caspase-1. Immunity 24: 317-327.
33. Aimanianda, V., J. Haensler, S. Lacroix-Desmazes, S. V. Kaveri, and J. Bayry. 2009. Novel cellular and molecular mechanisms of induction of immune responses by aluminum adjuvants. Trends Pharmacol. Sci. 30: 287-295.
34. Sharp, F. A., D. Ruane, B. Claass, E. Creagh, J. Harris, P. Malyala, M. Singh, D. T. O'Hagan, V. Pétrilli, J. Tschopp, et al. 2009. Uptake of particulate vaccine adjuvants by dendritic cells activates the NALP3 inflammasome. Proc. Natl. Acad. Sci. USA 106: 870-875.
35. Cassel, S. L., S. C. Eisenbarth, S. S. Iyer, J. J. Sadler, O. R. Colegio, L. A. Tephly, A. B. Carter, P. B. Rothman, R. A. Flavell, and F. S. Sutterwala. 2008. The Nalp3 inflammasome is essential for the development of silicosis. Proc. Natl. Acad. Sci. USA 105: 9035-9040.
36. Hornung, V., F. Bauernfeind, A. Halle, E. O. Samstad, H. Kono, K. L. Rock, K. A. Fitzgerald, and E. Latz. 2008. Silica crystals and aluminum salts activate the NALP3 inflammasome through phagosomal destabilization. Nat. Immunol. 9: 847-856.
37. Li, H., S. B. Willingham, J. P. Ting, and F. Re. 2008. Cutting edge: inflammasome activation by alum and alum's adjuvant effect are mediated by NLRP3. J. Immunol. 181: 17-21.
38. Guachalla, L. M., and K. L. Rudolph. 2010. ROS induced DNA damage and checkpoint responses: influences on aging? Cell Cycle 9: 4058-4060.
39. Solle, M., J. Labasi, D. G. Perregaux, E. Stam, N. Petrushova, B. H. Koller, R. J. Griffiths, and C. A. Gabel. 2001. Altered cytokine production in mice lacking P2X(7) receptors. J. Biol. Chem. 276: 125-132. (Pubitemid 32050297)
40. Kahlenberg, J. M., and G. R. Dubyak. 2004. Mechanisms of caspase-1 activation by P2X7 receptor-mediated K+ release. Am. J. Physiol. Cell Physiol. 286: C1100-C1108. (Pubitemid 38506925)
41. Kanneganti, T. D., M. Lamkanfi, Y. G. Kim, G. Chen, J. H. Park, L. Franchi, P. Vandenabeele, and G. Núñez. 2007. Pannexin-1-mediated recognition of bacterial molecules activates the cryopyrin inflammasome independent of Tolllike receptor signaling. Immunity 26: 433-443. (Pubitemid 46603000)
42. Ichinohe, T., I. K. Pang, Y. Kumamoto, D. R. Peaper, J. H. Ho, T. S. Murray, and A. Iwasaki. 2011. Microbiota regulates immune defense against respiratory tract influenza A virus infection. Proc. Natl. Acad. Sci. USA 108: 5354-5359.
43. Bokov, A., A. Chaudhuri, and A. Richardson. 2004. The role of oxidative damage and stress in aging. Mech. Ageing Dev. 125: 811-826. (Pubitemid 39482409)
44. Thiem, U., H. J. Heppner, and L. Pientka. 2011. Elderly patients with community-acquired pneumonia: optimal treatment strategies. Drugs Aging 28: 519-537.
45. Rozzini, R., and M. Trabucchi. 2011. Pneumonia and mortality beyond hospital discharge in elderly patients. Chest 139: 473-474, author reply 474-475.
46. Pérez-Trallero, E., J. M. Marimón, J. Larruskain, M. Alonso, and M. Ercibengoa. 2011. Antimicrobial susceptibilities and serotypes of Streptococcus pneumoniae isolates from elderly patients with pneumonia and acute exacerbation of chronic obstructive pulmonary disease. Antimicrob. Agents Chemother. 55: 2729-2734.
47. Mouton, C. P., O. V. Bazaldua, B. Pierce, and D. V. Espino. 2001. Common infections in older adults. Am. Fam. Physician 63: 257-268. (Pubitemid 32147023)
48. McNeela, E. A., A. Burke, D. R. Neill, C. Baxter, V. E. Fernandes, D. Ferreira, S. Smeaton, R. El-Rachkidy, R. M. McLoughlin, A. Mori, et al. 2010. Pneumolysin activates the NLRP3 inflammasome and promotes proinflammatory cytokines independently of TLR4. PLoS Pathog. 6: e1001191.