Salmonella downregulates nod-like receptor family card domain containing protein 4 expression to promote its survival in b cells by preventing inflammasome activation and cell death

Journal of Immunology

Volumn 190, Issue 3, 2013, Pages 1201-1209

  Perez Lopez, Araceli ^a   Rosales Reyes, Roberto ^a   Alpuche Aranda, Celia Mercedes ^b   Ortiz Navarrete, Vianney ^a,b,c  

^a INSTITUTO POLITÉCNICO NACIONAL   (Mexico)

^b UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

^c SECRETARÍA DE SALUD   (Mexico)

Author keywords

[No Author keywords available]

Indexed keywords

HEMATOPOIETIC CELL KINASE; INFLAMMASOME; INTERLEUKIN 1BETA; NOD LIKE RECEPTOR FAMILY CARD DOMAIN CONTAINING PROTEIN 4; NUCLEOTIDE BINDING OLIGOMERIZATION DOMAIN LIKE RECEPTOR; PROTEIN YAP; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; B LYMPHOCYTE; BACTERIAL SURVIVAL; BACTERIAL VIRULENCE; CELL DEATH; CONTROLLED STUDY; CYTOKINE RELEASE; DOWN REGULATION; FEMALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SALMONELLA; SALMONELLOSIS; TRANSCRIPTION INITIATION; TYPE III SECRETION SYSTEM;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; B-LYMPHOCYTES; BACTERIAL PROTEINS; CALCIUM-BINDING PROTEINS; CYTOKINES; CYTOTOXICITY, IMMUNOLOGIC; DOWN-REGULATION; FEMALE; FLAGELLIN; GENE EXPRESSION REGULATION; IMMUNE EVASION; INFLAMMASOMES; INTERLEUKIN-1BETA; MACROPHAGES; MICE; MICE, INBRED BALB C; PHOSPHOPROTEINS; PROTO-ONCOGENE PROTEINS C-HCK; SALMONELLA INFECTIONS, ANIMAL; SALMONELLA TYPHIMURIUM; TRANSCRIPTION, GENETIC; VIRULENCE;

EID: 84872705482     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1200415     Document Type: Article

References (45)

1. Brown, A., and C. E. Hormaeche. 1989. The antibody response to salmonellae in mice and humans studied by immunoblots and ELISA. Microb. Pathog. 6: 445-454. (Pubitemid 19223599)
2. Dougan, G., V. John, S. Palmer, and P. Mastroeni. 2011. Immunity to salmonellosis. Immunol. Rev. 240: 196-210.
3. Ugrinovic, S., N. Ménager, N. Goh, and P. Mastroeni. 2003. Characterization and development of T-cell immune responses in B-cell-deficient (Igh-6(-/-)) mice with Salmonella enterica serovar Typhimurium infection. Infect. Immun. 71: 6808-6819. (Pubitemid 37475309)
4. Souwer, Y., A. Griekspoor, T. Jorritsma, J. de Wit, H. Janssen, J. Neefjes, and S. M. van Ham. 2009. B cell receptor-mediated internalization of salmonella: A novel pathway for autonomous B cell activation and antibody production. J. Immunol. 182: 7473-7481.
5. Sztein, M. B., M. K. Tanner, Y. Polotsky, J. M. Orenstein, and M. M. Levine. 1995. Cytotoxic T lymphocytes after oral immunization with attenuated vaccine strains of Salmonella typhi in humans. J. Immunol. 155: 3987-3993.
6. Verjans, G. M., J. H. Ringrose, L. van Alphen, T. E. Feltkamp, and J. G. Kusters. 1994. Entrance and survival of Salmonella typhimurium and Yersinia enterocolitica within human B-and T-cell lines. Infect. Immun. 62: 2229-2235. (Pubitemid 24157047)
7. Yrlid, U., M. Svensson, A. Hakansson, B. J. Chambers, H. G. Ljunggren, and M. J. Wick. 2001. In vivo activation of dendritic cells and T cells during Salmonella enterica serovar Typhimurium infection. Infect. Immun. 69: 5726-5735. (Pubitemid 32786511)
8. Rosales-Reyes, R., C. Alpuche-Aranda, Mde. L. Ramírez-Aguilar, A. D. Castro-Eguiluz, and V. Ortiz-Navarrete. 2005. Survival of Salmonella enterica serovar Typhimurium within late endosomal-lysosomal compartments of B lymphocytes is associated with the inability to use the vacuolar alternative major histocompatibility complex class I antigen-processing pathway. Infect. Immun. 73: 3937-3944. (Pubitemid 40923132)
9. Geddes, K., F. Cruz, and F. Heffron. 2007. Analysis of cells targeted by Salmonella type III secretion in vivo. PLoS Pathog. 3: E196.
10. Castro-Eguiluz, D., R. Pelayo, V. Rosales-Garcia, R. Rosales-Reyes, C. Alpuche-Aranda, and V. Ortiz-Navarrete. 2009. B cell precursors are targets for Salmonella infection. Microb. Pathog. 47: 52-56.
11. Kumar, H., T. Kawai, and S. Akira. 2011. Pathogen recognition by the innate immune system. Int. Rev. Immunol. 30: 16-34.
12. Takeda, K., T. Kaisho, and S. Akira. 2003. Toll-like receptors. Annu. Rev. Immunol. 21: 335-376. (Pubitemid 37174535)
13. Miao, E. A., C. M. Alpuche-Aranda, M. Dors, A. E. Clark, M. W. Bader, S. I. Miller, and A. Aderem. 2006. Cytoplasmic flagellin activates caspase-1 and secretion of interleukin 1beta via Ipaf. Nat. Immunol. 7: 569-575. (Pubitemid 43797337)
14. Franchi, L., A. Amer, M. Body-Malapel, T. D. Kanneganti, N. Ozoren, R. Jagirdar, N. Inohara, P. Vandenabeele, J. Bertin, A. Coyle, et al. 2006. Cytosolic flagellin requires Ipaf for activation of caspase-1 and interleukin 1beta in salmonella-infected macrophages. Nat. Immunol. 7: 576-582. (Pubitemid 43797338)
15. Monack, D. M., B. Raupach, A. E. Hromockyj, and S. Falkow. 1996. Salmonella typhimurium invasion induces apoptosis in infected macrophages. Proc. Natl. Acad. Sci. USA 93: 9833-9838. (Pubitemid 26296695)
16. Poyet, J. L., S. M. Srinivasula, M. Tnani, M. Razmara, T. Fernandes-Alnemri, and E. S. Alnemri. 2001. Identification of Ipaf, a human caspase-1-activating protein related to Apaf-1. J. Biol. Chem. 276: 28309-28313.
17. Sadasivam, S., S. Gupta, V. Radha, K. Batta, T. K. Kundu, and G. Swarup. 2005. Caspase-1 activator Ipaf is a p53-inducible gene involved in apoptosis. Oncogene 24: 627-636. (Pubitemid 40188567)
18. Paliwal, P., V. Radha, and G. Swarup. 2007. Regulation of p73 by Hck through kinase-dependent and independent mechanisms. BMC Mol. Biol. 8: 45.
19. Strano, S., O. Monti, N. Pediconi, A. Baccarini, G. Fontemaggi, E. Lapi, F. Mantovani, A. Damalas, G. Citro, A. Sacchi, et al. 2005. The transcriptional coactivator Yes-associated protein drives p73 gene-target specificity in response to DNA damage. Mol. Cell 18: 447-459. (Pubitemid 40704759)
20. Tomlinson, V., K. Gudmundsdottir, P. Luong, K. Y. Leung, A. Knebel, and S. Basu. 2010. JNK phosphorylates Yes-associated protein (YAP) to regulate apoptosis. Cell Death Dis. 1: E29.
21. Racoosin, E. L., and J. A. Swanson. 1989. Macrophage colony-stimulating factor (rM-CSF) stimulates pinocytosis in bone marrow-derived macrophages. J. Exp. Med. 170: 1635-1648. (Pubitemid 19284563)
22. Miao, E. A., M. Brittnacher, A. Haraga, R. L. Jeng, M. D. Welch, and S. I. Miller. 2003. Salmonella effectors translocated across the vacuolar membrane interact with the actin cytoskeleton. Mol. Microbiol. 48: 401-415. (Pubitemid 36819077)
23. Brennan, M. A., and B. T. Cookson. 2000. Salmonella induces macrophage death by caspase-1-dependent necrosis. Mol. Microbiol. 38: 31-40.
24. MacBeth, K. J., and C. A. Lee. 1993. Prolonged inhibition of bacterial protein synthesis abolishes Salmonella invasion. Infect. Immun. 61: 1544-1546. (Pubitemid 23099234)
25. Buchmeier, N. A., and F. Heffron. 1989. Intracellular survival of wild-type Salmonella typhimurium and macrophage-sensitive mutants in diverse populations of macrophages. Infect. Immun. 57: 1-7. (Pubitemid 19023171)
26. Dryer, R. L., and L. R. Covey. 2006. Use of chromatin immunoprecipitation (ChIP) to detect transcription factor binding to highly homologous promoters in chromatin isolated from unstimulated and activated primary human B cells. Biol. Proced. Online 8: 44-54.
27. Weiss, D. S., B. Raupach, K. Takeda, S. Akira, and A. Zychlinsky. 2004. Tolllike receptors are temporally involved in host defense. J. Immunol. 172: 4463-4469. (Pubitemid 38375262)
28. Morrissey, P. J., K. Charrier, and S. N. Vogel. 1995. Exogenous tumor necrosis factor alpha and interleukin-1 alpha increase resistance to Salmonella typhimurium: Efficacy is influenced by the Ity and Lps loci. Infect. Immun. 63: 3196-3198.
29. Martinon, F., K. Burns, and J. Tschopp. 2002. The inflammasome: A molecular platform triggering activation of inflammatory caspases and processing of proILbeta. Mol. Cell 10: 417-426. (Pubitemid 35007355)
30. Amer, A., L. Franchi, T. D. Kanneganti, M. Body-Malapel, N. Ozoren, G. Brady, S. Meshinchi, R. Jagirdar, A. Gewirtz, S. Akira, and G. Núnez. 2006. Regulation of Legionella phagosome maturation and infection through flagellin and host Ipaf. J. Biol. Chem. 281: 35217-35223. (Pubitemid 46043249)
31. Rosales-Reyes, R., A. Pérez-López, C. Sánchez- Gómez, R. R. Hernández-Mote, D. Castro-Eguiluz, V. Ortiz-Navarrete, and C. M. Alpuche-Aranda. 2012. Salmonella infects B cells by macropinocytosis and formation of spacious phagosomes but does not induce pyroptosis in favor of its survival. Microb. Pathog. 52: 367-374.
32. Kumar, Y., V. Radha, and G. Swarup. 2010. Interaction with Sug1 enables Ipaf ubiquitination leading to caspase 8 activation and cell death. Biochem. J. 427: 91-104.
33. Eckmann, L., and M. F. Kagnoff. 2001. Cytokines in host defense against Salmonella. Microbes Infect. 3: 1191-1200. (Pubitemid 34033754)
34. Elinav, E., T. Strowig, J. Henao-Mejia, and R. A. Flavell. 2011. Regulation of the antimicrobial response by NLR proteins. Immunity 34: 665-679.
35. Kawai, T., and S. Akira. 2011. Toll-like receptors and their crosstalk with other innate receptors in infection and immunity. Immunity 34: 637-650.
36. Lamkanfi, M., and V. M. Dixit. 2011. Modulation of inflammasome pathways by bacterial and viral pathogens. J. Immunol. 187: 597-602.
37. Taxman, D. J., M. T. Huang, and J. P. Ting. 2010. Inflammasome inhibition as a pathogenic stealth mechanism. Cell Host Microbe. 8: 7-11.
38. Ginocchio, C. C., S. B. Olmsted, C. L.Wells, and J. E. Galán. 1994. Contact with epithelial cells induces the formation of surface appendages on Salmonella typhimurium. Cell 76: 717-724. (Pubitemid 24070655)
39. Kaniga, K., S. Tucker, D. Trollinger, and J. E. Galán. 1995. Homologs of the Shigella IpaB and IpaC invasins are required for Salmonella typhimurium entry into cultured epithelial cells. J. Bacteriol. 177: 3965-3971.
40. Alpuche-Aranda, C. M., E. P. Berthiaume, B. Mock, J. A. Swanson, and S. I. Miller. 1995. Spacious phagosome formation within mouse macrophages correlates with Salmonella serotype pathogenicity and host susceptibility. Infect. Immun. 63: 4456-4462.
41. Wu, S., Z. Ye, X. Liu, Y. Zhao, Y. Xia, A. Steiner, E. O. Petrof, E. C. Claud, and J. Sun. 2010. Salmonella typhimurium infection increases p53 acetylation in intestinal epithelial cells. Am. J. Physiol. Gastrointest. Liver Physiol. 298: G784-G794.
42. Tarunina, M., and J. R. Jenkins. 1993. Human p53 binds DNA as a protein homodimer but monomeric variants retain full transcription transactivation activity. Oncogene 8: 3165-3173. (Pubitemid 23312925)
43. Fortier, A., K. Doiron, M. Saleh, S. Grinstein, and P. Gros. 2009. Restriction of Legionella pneumophila replication in macrophages requires concerted action of the transcriptional regulators Irf1 and Irf8 and nod-like receptors Naip5 and Nlrc4. Infect. Immun. 77: 4794-4805.
44. Vinzing, M., J. Eitel, J. Lippmann, A. C. Hocke, J. Zahlten, H. Slevogt, P. D. Nguessan, S. Gunther, B. Schmeck, S. Hippenstiel, et al. 2008. NAIP and Ipaf control Legionella pneumophila replication in human cells. J. Immunol. 180: 6808-6815.
45. Coers, J., R. E. Vance, M. F. Fontana, and W. F. Dietrich. 2007. Restriction of Legionella pneumophila growth in macrophages requires the concerted action of cytokine and Naip5/Ipaf signalling pathways. Cell. Microbiol. 9: 2344-2357. (Pubitemid 47365641)