IL-24 protects against Salmonella typhimurium infection by stimulating early neutrophil Th1 cytokine production, which in turn activates CD8 + T cells

European Journal of Immunology

Volumn 39, Issue 12, 2009, Pages 3357-3368

  Ma, Yunfeng ^a   Chen, Haidan ^a   Wang, Qilong ^a   Luo, Fengling ^a   Yan, Jun ^b   Zhang, Xiao Lian ^a  

^a WUHAN UNIVERSITY   (China)

^b University of Louisville School of Medicine   (United States)

Author keywords

Cd8+ T cells; Interleukin 24; Neutrophils; Salmonella typhimurium C5; Th1 cytokines

Indexed keywords

CD8 ANTIGEN; GAMMA INTERFERON; INTERLEUKIN 12; INTERLEUKIN 24; NITRIC OXIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBACTERIAL ACTIVITY; ARTICLE; BACTERIAL IMMUNITY; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; HOST RESISTANCE; IMMUNOTHERAPY; IN VITRO STUDY; IN VIVO STUDY; KNOCKOUT MOUSE; MALE; MOUSE; NEUTROPHIL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTECTION; SALMONELLA TYPHIMURIUM; T LYMPHOCYTE ACTIVATION; TH1 CELL; TYPHOID FEVER;

ANIMALS; BLOTTING, WESTERN; CD8-POSITIVE T-LYMPHOCYTES; CELL LINE, TUMOR; CYTOKINES; ENZYME-LINKED IMMUNOSORBENT ASSAY; HUMANS; INTERFERON-GAMMA; INTERLEUKIN-12; INTERLEUKINS; LYMPHOCYTE ACTIVATION; MALE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; MUTATION; NEUTROPHILS; NITRIC OXIDE; RECOMBINANT FUSION PROTEINS; SALMONELLA INFECTIONS, ANIMAL; SALMONELLA TYPHIMURIUM; TH1 CELLS; TRANSFECTION; TYPHOID FEVER;

EID: 73249135127     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.200939678     Document Type: Article

References (39)

1. Graham, S. M., Salmonellosis in children in developing and developed countries and populations. Curr. Opin. Infect. Dis. 2002. 15: 507-512.
2. Maskey, A. P., Basnyat, B., Thwaites, G. E., Campbell, J. I., Farrar, J. J. and Zimmerman, M. D., Emerging trends in enteric fever in Nepal: 9124 cases confirmed by blood culture 1993-2003. Trans. R. Soc. Trop. Med. Hyg. 2008. 102: 91-95.
3. Parry, C. M., Hien, T. T., Dougan, G., White, N. J. and Farrar, J. J., Typhoid fever. N. Engl. J. Med. 2002. 347: 1770-1782.
4. Swanson, S. J., Snider, C., Braden, C. R., Boxrud, D., Wunschmann, A., Rudroff, J. A., Lockett, J. et al., Multidrug-resistant Salmonella enterica serotype typhimurium associated with pet rodents. N. Engl. J. Med. 2007. 356: 21-28.
5. Woods, C. W., Murdoch, D. R., Zimmerman, M. D., Glover, W. A., Basnyat, B., Wolf, L., Belbase, R. H. et al., Emergence of Salmonella enterica serotype paratyphi A as a major cause of enteric fever in Kathmandu, Nepal. Trans. R. Soc. Trop. Med. Hyg. 2006. 100: 1063-1067.
6. Gordon, M. A., Salmonella infections in immunocompromised adults. J. Infect. 2008. 56: 413-422.
7. Raffatellu, M., Santos, R. L., Verhoeven, D. E., George, M. D., Wilson, R. P., Winter, S. E., Godinez, I. et al., Simian immunodeficiency virus-induced mucosal interleukin-17 deficiency promotes Salmonella dissemination from the gut. Nat. Med. 2008. 14: 421-428.
8. Pan, Q., Zhang, X. L., Wu, H. Y., He, P. W., Wang, F., Zhang, M. S., Hu, J. M. et al., Aptamers that preferentially bind type IVB pili and inhibit human monocytic-cell invasion by Salmonella enterica serovar typhi. Antimicrob. Agents Chemother. 2005. 49: 4052-4060.
9. Oral, H. B., Kotenko, S. V., Yilmaz, M., Mani, O., Zumkehr, J., Blaser, K., Akdis, C. A. et al., Regulation of T cells and cytokines by the interleukin-10 (IL-10)-family cytokines IL-19, IL-20, IL-22, IL-24 and IL-26. Eur. J. Immunol. 2006. 36: 380-388.
10. Garn, H., Schmidt, A., Grau, V., Stumpf, S., Kaufmann, A., Becker, M., Gemsa, D. et al., IL-24 is expressed by rat and human macrophages. Immunobiology 2002. 205: 321-334.
11. Jiang, H., Lin, J. J., Su, Z. Z., Goldstein, N. I. and Fisher, P. B., Subtraction hybridization identifies a novel melanoma differentiation associated gene, mda-7, modulated during human melanoma differentiation, growth and progression. Oncogen 1995. 11: 2477-2486.
12. Huang, E. Y., Madireddi, M. T., Gopalkrishnan, R. V., Leszczyniecka, M., Su, Z., Lebedeva, I. V., Kang, D. et al., Genomic structure, chromosomal localization and expression profile of a novel melanoma differentiation associated (mda-7) gene with cancer specific growth suppressing and apoptosis inducing properties. Oncogen 2001. 20: 7051-7063.
13. Mhashilkar, A. M., Schrock, R. D., Hindi, M., Liao, J., Sieger, K., Kourouma, F., Zou-Yang, X. H. et al., Melanoma differentiation associated gene-7 (mda-7): a novel anti-tumor gene for cancer gene therapy. Mol. Med. 2001. 7: 271-282.
14. Sauane, M., Su, Z. Z., Gupta, P., Lebedeva, I. V., Dent, P., Sarkar, D. and Fisher, P. B., Autocrine regulation of mda-7/IL-24 mediates cancer-specific apoptosis. Proc. Natl. Acad. Sci. USA 2008. 105: 9763-9768.
15. Caudell, E. G., Mumm, J. B., Poindexter, N., Ekmekcioglu, S., Mhashilkar, A. M., Yang, X. H., Retter, M. W. et al., The protein product of the tumor suppressor gene, melanoma differentiation-associated gene 7, exhibits immunostimulatory activity and is designated IL-24. J. Immunol. 2002. 168: 6041-6046.
16. Nairz, M., Fritsche, G., Brunner, P., Talasz, H., Hantke, K. and Weiss, G., Interferon-gamma limits the availability of iron for intramacrophage Salmonella typhimurium. Eur. J. Immunol. 2008. 38: 1923-1936.
17. Monack, D. M., Mueller, A. and Falkow, S., Persistent bacterial infections: the interface of the pathogen and the host immune system. Nat. Rev. Microbiol. 2004. 2: 747-765.
18. Peng, Y., Lin, F. C., Verardi, P. H., Jones, L. A., McChesney, M. B. and Yilma, T. D., Pseudotyped single-cycle simian immunodeficiency viruses expressing gamma interferon augment T-cell priming responses in vitro. J. Virol. 2007. 81: 2187-2195.
19. Lehmann, J., Bellmann, S., Werner, C., Schroder, R., Schutze, N. and Alber, G., IL-12p40-dependent agonistic effects on the development of protective innate and adaptive immunity against Salmonella enteritidis. J. Immunol. 2001. 167: 5304-5315.
20. Sauane, M., Gupta, P., Lebedeva, I. V., Su, Z. Z., Sarkar, D., Randolph, A., Valerie, K. et al., N-glycosylation of MDA-7/IL-24 is dispensable for tumor cell-specific apoptosis and "bystander" antitumor activity. Cancer Res. 2006. 66: 11869-11877.
21. Rudd, P. M., Elliott, T., Cresswell, P., Wilson, I. A. and Dwek, R. A., Glycosylation and the immune system. Science 2001. 291: 2370-2376.
22. Lau, K. S., Partridge, E. A., Grigorian, A., Silvescu, C. I., Reinhold, V. N., Demetriou, M. and Dennis, J. W., Complex N-glycan number and degree of branching cooperate to regulate cell proliferation and differentiation. Cell. 2007. 129: 123-134.
23. Matsuzaki, J., Tsuji, T., Chamoto, K., Takeshima, T., Sendo, F. and Nishimura, T., Successful elimination of memory-type CD8+T cell subsets by the administration of anti-Gr-1 monoclonal antibody in vivo. Cell Immunol. 2003. 224: 98-105.
24. Watanabe, K., Noda, K., Hamano, S., Koga, M., Kishihara, K., Nomoto, K. and Tada, I., The crucial role of granulocytes in the early host defense against Strongyloides ratti infection in mice. Parasitl. Res. 2000. 86: 188-193.
25. Verfaillie, T., Cox, E. and Goddeeris, B. M., Immunostimulatory capacity of DNA vaccine vectors in porcine PBMC: a specific role for CpG-motifs. Vet. Immunol. Immunopathol. 2005. 103: 141-151.
26. Fierer, J., Polymorphonuclear leukocytes and innate immunity to Salmonella infections in mice. Microbes Infect. 2001. 3: 1233-1237.
27. Rutkowski, M. R., McNamee, L. A. and Harmsen, A. G., Neutrophils and inducible nitric-oxide synthase are critical for early resistance to the establishment of Tritrichomonas foetus infection. J. Parasitol. 2007. 93: 562-574.
28. Roger, T. and Calandra, T., TLR2-mediated neutrophil depletion exacerbates bacterial sepsis. Proc. Natl. Acad. Sci. USA 2009. 106: 6889-6890.
29. Kirby, A. C., Yrlid, U. and Wick, M. J., The innate immune response differs in primary and secondary Salmonella infection. J. Immunol. 2002. 169: 4450-4459.
30. Eriksson, S., Chambers, B. J. and Rhen, M., Nitric oxide produced by murine dendritic cells is cytotoxic for intracellular Salmonella enterica sv. typhimurium. Scand. J. Immunol. 2003. 58: 493-502.
31. McCartney-Francis, N. L., Song, X., Mizel, D. E. and Wahl, S. M., Selective inhibition of inducible nitric oxide synthase exacerbates erosive joint disease. J. Immunol. 2001. 166: 2734-2740.
32. Schaefer, G., Venkataraman, C. and Schindler, U., Cutting edge: FISP (IL-4-induced secreted protein), a novel cytokine-like molecule secreted by Th2 cells. J Immunol. 2001. 166: 5859-5863.
33. Wegenka, U. M., Dikopoulos, N., Reimann, J., Adler, G. and Wahl, C., The murine liver is a potential target organ for IL-19, IL-20 and IL-24: Type I Interferons and LPS regulate the expression of IL-20R2. J. Hepatol. 2007. 46: 257-265.
34. Ethuin, F., Gerard, B., Benna, J. E., Boutten, A., Gougereot-Pocidalo, M. A., Jacob, L. and Chollet-Martin, S., Human neutrophils produce interferon gamma upon stimulation by interleukin-12. Lab. Invest. 2004. 84: 1363-1371.
35. Yeaman, G. R., Collins, J. E., Currie, J. K., Guyre, P. M., Wira, C. R. and Fanger, M. W., IFN-gamma is produced by polymorphonuclear neutrophils in human uterine endometrium and by cultured peripheral blood polymorphonuclear neutrophils. J. Immunol. 1998. 160: 5145-5153.
36. Keel, M., Ungethum, U., Steckholzer, U., Niederer, E., Hartung, T., Trentz, O. and Ertel, W., Interleukin-10 counterregulates proinflammatory cytokine-induced inhibition of neutrophil apoptosis during severe sepsis. Blood 1997. 90: 3356-3363.
37. Wang, M., Tan, Z., Zhang, R., Kotenko, S. V. and Liang, P., Interleukin 24 (MDA-7/MOB-5) signals through two heterodimeric receptors, IL-22R1/IL-20R2 and IL-20R1/IL-20R2. J. Biol. Chem. 2002. 277: 7341-7347.
38. Mastroeni, P., Clare, S., Khan, S., Harrison, J. A., Hormaeche, C. E., Okamura, H., Kurimoto, M. et al., Interleukin 18 contributes to host resistance and gamma interferon production in mice infected with virulent Salmonella typhimurium. Infect. Immun. 1999. 67: 478-483.
39. Silva, E., Arcaroli, J., He, Q., Svetkauskaite, D., Coldren, C., Nick, J. A., Poch, K. et al., HMGB1 and LPS induce distinct patterns of gene expression and activation in neutrophils from patients with sepsis-induced acute lung injury. Intensive Care Med. 2007. 33: 1829-1839.