Type I IFN does not promote susceptibility to foodborne Listeria monocytogenes

Journal of Immunology

Volumn 196, Issue 7, 2016, Pages 3109-3116

  Pitts, Michelle G ^a   Myers Morales, Tanya ^a   D'Orazio, Sarah E F ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; ALPHA INTERFERON RECEPTOR; BETA INTERFERON; INTERFERON; INTERFERON RECEPTOR; INTERLEUKIN 10;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL LOAD; BACTERIAL TRANSMISSION; CELL DEATH; CONTROLLED STUDY; CYTOKINE RELEASE; DENDRITIC CELL; DOWN REGULATION; FOOD POISONING; HOST PATHOGEN INTERACTION; IMMUNE DEFICIENCY; IN VIVO STUDY; INFECTION SENSITIVITY; INNATE IMMUNITY; INTERFERON PRODUCTION; LISTERIA MONOCYTOGENES; LISTERIOSIS; LIVER; MACROPHAGE; MOUSE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPLEEN; SPLEEN CELL; T LYMPHOCYTE; WILD TYPE MOUSE; ANIMAL; BIOSYNTHESIS; DEFICIENCY; DISEASE MODEL; DISEASE PREDISPOSITION; GENE EXPRESSION; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; LYMPHOCYTE DEPLETION; METABOLISM; NEUTROPHIL; SIGNAL TRANSDUCTION;

ANIMALS; DENDRITIC CELLS; DISEASE MODELS, ANIMAL; DISEASE SUSCEPTIBILITY; GENE EXPRESSION; INTERFERON TYPE I; INTERFERON-BETA; LISTERIA MONOCYTOGENES; LISTERIOSIS; LYMPHOCYTE DEPLETION; MACROPHAGES; MICE; MICE, KNOCKOUT; NEUTROPHIL INFILTRATION; NEUTROPHILS; RECEPTORS, INTERFERON; SIGNAL TRANSDUCTION; SPLEEN; T-LYMPHOCYTES;

EID: 84962577620     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1502192     Document Type: Article

References (53)

1. Platanias, L. C. 2005. Mechanisms of type-I- and type-II-interferon-mediated signalling. Nat. Rev. Immunol. 5:375-386.
2. Pestka, S., C. D. Krause, and M. R. Walter. 2004. Interferons, interferon-like cytokines, and their receptors. Immunol. Rev. 202:8-32.
3. Ishikawa, H., and G. N. Barber. 2008. STING is an endoplasmic reticulum adaptor that facilitates innate immune signalling. Nature 455:674-678.
4. Parvatiyar, K., Z. Zhang, R. M. Teles, S. Ouyang, Y. Jiang, S. S. Iyer, S. A. Zaver, M. Schenk, S. Zeng, W. Zhong, et al. 2012. The helicase DDX41 recognizes the bacterial secondary messengers cyclic di-GMP and cyclic di-AMP to activate a type I interferon immune response. Nat. Immunol. 13:1155-1161.
5. Müller, U., U. Steinhoff, L. F. Reis, S. Hemmi, J. Pavlovic, R. M. Zinkernagel, and M. Aguet. 1994. Functional role of type I and type II interferons in antiviral defense. Science 264:1918-1921.
6. Chawla-Sarkar, M., D. J. Lindner, Y. F. Liu, B. R. Williams, G. C. Sen, R. H. Silverman, and E. C. Borden. 2003. Apoptosis and interferons: role of interferon-stimulated genes as mediators of apoptosis. Apoptosis 8:237-249.
7. Stark, G. R., I. M. Kerr, B. R. Williams, R. H. Silverman, and R. D. Schreiber. 1998. How cells respond to interferons. Annu. Rev. Biochem. 67:227-264.
8. Hervas-Stubbs, S., J. L. Perez-Gracia, A. Rouzaut, M. F. Sanmamed, A. Le Bon, and I. Melero. 2011. Direct effects of type I interferons on cells of the immune system. Clin. Cancer Res. 17:2619-2627.
9. Fink, K., K. S. Lang, N. Manjarrez-Orduno, T. Junt, B. M. Senn, M. Holdener, S. Akira, R. M. Zinkernagel, and H. Hengartner. 2006. Early type I interferonmediated signals on B cells specifically enhance antiviral humoral responses. Eur. J. Immunol. 36:2094-2105.
10. Davidson, S., S. Crotta, T. M. McCabe, and A. Wack. 2014. Pathogenic potential of interferon ab in acute influenza infection. Nat. Commun. 5:3864.
11. Fujikura, D., S. Chiba, D. Muramatsu, M. Kazumata, Y. Nakayama, T. Kawai, S. Akira, H. Kida, and T. Miyazaki. 2013. Type-I interferon is critical for FasL expression on lung cells to determine the severity of influenza. PLoS One 8:e55321.
12. Mancuso, G., A. Midiri, C. Biondo, C. Beninati, S. Zummo, R. Galbo, F. Tomasello, M. Gambuzza, G. Macrì, A. Ruggeri, et al. 2007. Type I IFN signaling is crucial for host resistance against different species of pathogenic bacteria. J. Immunol. 178:3126-3133.
13. Manca, C., L. Tsenova, A. Bergtold, S. Freeman, M. Tovey, J. M. Musser, C. E. Barry, III, V. H. Freedman, and G. Kaplan. 2001. Virulence of a Mycobacterium tuberculosis clinical isolate in mice is determined by failure to induce Th1 type immunity and is associated with induction of IFN-a/b. Proc. Natl. Acad. Sci. USA 98:5752-5757.
14. Henry, T., G. S. Kirimanjeswara, T. Ruby, J. W. Jones, K. Peng, M. Perret, L. Ho, J. D. Sauer, Y. Iwakura, D. W. Metzger, and D. M. Monack. 2010. Type I IFN signaling constrains IL-17A/F secretion by gd T cells during bacterial infections. J. Immunol. 184:3755-3767.
15. Perkins, D. J., R. Rajaiah, S. M. Tennant, G. Ramachandran, E. E. Higginson, T. N. Dyson, and S. N. Vogel. 2015. Salmonella typhimurium co-opts the host type I IFN system to restrict macrophage innate immune transcriptional responses selectively. J. Immunol. 195:2461-2471.
16. Auerbuch, V., D. G. Brockstedt, N. Meyer-Morse, M. O'Riordan, and D. A. Portnoy. 2004. Mice lacking the type I interferon receptor are resistant to Listeria monocytogenes. J. Exp. Med. 200:527-533.
17. O'Connell, R. M., S. K. Saha, S. A. Vaidya, K. W. Bruhn, G. A. Miranda, B. Zarnegar, A. K. Perry, B. O. Nguyen, T. F. Lane, T. Taniguchi, et al. 2004. Type I interferon production enhances susceptibility to Listeria monocytogenes infection. J. Exp. Med. 200:437-445.
18. Carrero, J. A., B. Calderon, and E. R. Unanue. 2004. Type I interferon sensitizes lymphocytes to apoptosis and reduces resistance to Listeria infection. J. Exp. Med. 200:535-540.
19. Rayamajhi, M., J. Humann, K. Penheiter, K. Andreasen, and L. L. Lenz. 2010. Induction of IFN-ab enables Listeria monocytogenes to suppress macrophage activation by IFN-g. J. Exp. Med. 207:327-337.
20. D'Orazio, S. E. 2014. Animal models for oral transmission of Listeria monocytogenes. Front. Cell. Infect. Microbiol. 4:15.
21. Jones, G. S., K. M. Bussell, T. Myers-Morales, A. M. Fieldhouse, E. N. Bou Ghanem, and S. E. F. D'Orazio. 2015. Intracellular Listeria monocytogenes comprise a minimal but vital fraction of the intestinal burden following foodborne infection. Infect. Immun. 83:3146-3156.
22. Wollert, T., B. Pasche, M. Rochon, S. Deppenmeier, J. Van Den Heuvel, A. D. Gruber, D. W. Heinz, A. Lengeling, and W. D. Schubert. 2007. Extending the host range of Listeria monocytogenes by rational protein design. Cell 129:891-902.
23. Jones, G. S., and S. E. D'Orazio. 2013. Listeria monocytogenes: cultivation and laboratory maintenance. Curr. Protoc. Microbiol. 31:1-7.
24. Cao, Y.-A., A. J. Wagers, A. Beilhack, J. Dusich, M. H. Bachmann, R. S. Negrin, I. L. Weissman, and C. H. Contag. 2004. Shifting foci of hematopoiesis during reconstitution from single stem cells. Proc. Natl. Acad. Sci. USA 101:221-226.
25. Bou Ghanem, E. N., T. Myers-Morales, and S. E. D'Orazio. 2013. A mouse model of foodborne Listeria monocytogenes infection. Curr. Protoc. Microbiol. 31:9B.3.1-9B.3.16.
26. Bou Ghanem, E. N., T. Myers-Morales, G. S. Jones, and S. E. D'Orazio. 2013. Oral transmission of Listeria monocytogenes in mice via ingestion of contaminated food. J. Vis. Exp. (75):e50381.
27. Conlan, J. W. 1999. Early host-pathogen interactions in the liver and spleen during systemic murine listeriosis: an overview. Immunobiology 201:178-187.
28. Kernbauer, E., V. Maier, I. Rauch, M. Muller, and T. Decker. 2013. Route of infection determines the impact of type I interferons on innate immunity to Listeria monocytogenes. PLoS One 8:e65007.
29. Bou Ghanem, E. N., G. S. Jones, T. Myers-Morales, P. D. Patil, A. N. Hidayatullah, and S. E. D'Orazio. 2012. InlA promotes dissemination of Listeria monocytogenes to the mesenteric lymph nodes during food borne infection of mice. PLoS Pathog. 8:e1003015.
30. Jiang, J., L. L. Lau, and H. Shen. 2003. Selective depletion of nonspecific T cells during the early stage of immune responses to infection. J. Immunol. 171:4352-4358.
31. high regulatory phenotype in macrophages. J. Immunol. 185:2044-2050.
32. Voll, R. E., M. Herrmann, E. A. Roth, C. Stach, J. R. Kalden, and I. Girkontaite. 1997. Immunosuppressive effects of apoptotic cells. Nature 390:350-351.
33. Kearney, S. J., C. Delgado, E. M. Eshleman, K. K. Hill, B. P. O'Connor, and L. L. Lenz. 2013. Type I IFNs downregulate myeloid cell IFN-γ receptor by inducing recruitment of an early growth response 3/NGFI-A binding protein 1 complex that silences ifngr1 transcription. J. Immunol. 191:3384-3392.
34. + T cells to innate immunity: IFN-γ secretion induced by IL-12 and IL-18. Eur. J. Immunol. 32:2807-2816.
35. Thäle, C., and A. F. Kiderlen. 2005. Sources of interferon-γ (IFN-g) in early immune response to Listeria monocytogenes. Immunobiology 210:673-683.
36. Yin, J., and T. A. Ferguson. 2009. Identification of an IFN-g-producing neutrophil early in the response to Listeria monocytogenes. J. Immunol. 182:7069-7073.
37. Aoshi, T., J. A. Carrero, V. Konjufca, Y. Koide, E. R. Unanue, and M. J. Miller. 2009. The cellular niche of Listeria monocytogenes infection changes rapidly in the spleen. Eur. J. Immunol. 39:417-425.
38. MacDonald, T. T., and P. B. Carter. 1980. Cell-mediated immunity to intestinal infection. Infect. Immun. 28:516-523.
39. Monk, I. R., P. G. Casey, C. Hill, and C. G. Gahan. 2010. Directed evolution and targeted mutagenesis to murinize Listeria monocytogenes internalin A for enhanced infectivity in the murine oral infection model. BMC Microbiol. 10:318.
40. Reutterer, B., S. Stockinger, A. Pilz, D. Soulat, R. Kastner, S. Westermayer, T. Rülicke, M. Müller, and T. Decker. 2008. Type I IFN are host modulators of strain-specific Listeria monocytogenes virulence. Cell. Microbiol. 10:1116-1129.
41. Schwartz, K. T., J. D. Carleton, S. J. Quillin, S. D. Rollins, D. A. Portnoy, and J. H. Leber. 2012. Hyperinduction of host b interferon by a Listeria monocytogenes strain naturally overexpressing the multidrug efflux pump MdrT. Infect. Immun. 80:1537-1545.
42. Yamamoto, T., H. Hara, K. Tsuchiya, S. Sakai, R. Fang, M. Matsuura, T. Nomura, F. Sato, M. Mitsuyama, and I. Kawamura. 2012. Listeria monocytogenes strain-specific impairment of the TetR regulator underlies the drastic increase in cyclic di-AMP secretion and b interferon-inducing ability. Infect. Immun. 80:2323-2332.
43. Pontiroli, F., O. Dussurget, I. Zanoni, M. Urbano, O. Beretta, F. Granucci, P. Ricciardi-Castagnoli, P. Cossart, and M. Foti. 2012. The timing of IFNb production affects early innate responses to Listeria monocytogenes and determines the overall outcome of lethal infection. PLoS One 7:e43455.
44. Feng, H., D. Zhang, D. Palliser, P. Zhu, S. Cai, A. Schlesinger, L. Maliszewski, and J. Lieberman. 2005. Listeria-infected myeloid dendritic cells produce IFN-β, priming T cell activation. J. Immunol. 175:421-432.
45. Dejager, L., S. Vandevyver, M. Ballegeer, E. Van Wonterghem, L. L. An, J. Riggs, R. Kolbeck, and C. Libert. 2014. Pharmacological inhibition of type I interferon signaling protects mice against lethal sepsis. J. Infect. Dis. 209:960-970.
46. Barker, J. R., B. J. Koestler, V. K. Carpenter, D. L. Burdette, C. M. Waters, R. E. Vance, and R. H. Valdivia. 2013. STING-dependent recognition of cyclic di-AMP mediates type I interferon responses during Chlamydia trachomatis infection. MBio 4:e00018-13.
47. Calame, D. G., S. L. Mueller-Ortiz, J. E. Morales, and R. A. Wetsel. 2014. The C5a anaphylatoxin receptor (C5aR1) protects against Listeria monocytogenes infection by inhibiting type 1 IFN expression. J. Immunol. 193:5099-5107.
48. Serbina, N. V., T. P. Salazar-Mather, C. A. Biron, W. A. Kuziel, and E. G. Pamer. 2003. TNF/iNOS-producing dendritic cells mediate innate immune defense against bacterial infection. Immunity 19:59-70.
49. Skrenta, H., Y. Yang, S. Pestka, and C. G. Fathman. 2000. Ligand-independent down-regulation of IFN-γ receptor 1 following TCR engagement. J. Immunol. 164:3506-3511.
50. Ling, P. D., M. K. Warren, and S. N. Vogel. 1985. Antagonistic effect of interferonb on the interferon-g-induced expression of Ia antigen in murine macrophages. J. Immunol. 135:1857-1863.
51. Kasper, L. H., and A. T. Reder. 2014. Immunomodulatory activity of interferonb. Ann. Clin. Transl. Neurol. 1:622-631.
52. Carrero, J. A. 2013. Confounding roles for type I interferons during bacterial and viral pathogenesis. Int. Immunol. 25:663-669.
53. Gough, D. J., N. L. Messina, C. J. Clarke, R. W. Johnstone, and D. E. Levy. 2012. Constitutive type I interferon modulates homeostatic balance through tonic signaling. Immunity 36:166-174.