IL-23 protection against Plasmodium berghei infection in mice is partially dependent on IL-17 from macrophages

European Journal of Immunology

Volumn 43, Issue 10, 2013, Pages 2696-2706

  Ishida, Hidekazu ^a,d   Imai, Takashi ^a   Suzue, Kazutomo ^a   Hirai, Makoto ^a   Taniguchi, Tomoyo ^a   Yoshimura, Akihiko ^b   Iwakura, Yoichiro ^c   Okada, Hiroko ^a   Suzuki, Tomohisa ^a   Shimokawa, Chikako ^a,e   Hisaeda, Hajime ^a  

^a GUNMA UNIVERSITY   (Japan)

^b KEIO UNIVERSITY   (Japan)

^c UNIVERSITY OF TOKYO   (Japan)

^d Otsuka Pharmacertical Co Ltd   (Japan)

^e Institute of Physical and Chemical Research   (Japan)

Author keywords

IL 17; IL 23; Macrophage; Malaria; Plasmodium berghei

Indexed keywords

INTERLEUKIN 17; INTERLEUKIN 23;

ADOPTIVE TRANSFER; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; IMMUNITY; MACROPHAGE; MOUSE; NONHUMAN; PARASITEMIA; PLASMODIUM BERGHEI; PLASMODIUM BERGHEI INFECTION; PRIORITY JOURNAL; SPLEEN CELL;

IL-17; IL-23; MACROPHAGE; MALARIA; PLASMODIUM BERGHEI;

ADOPTIVE TRANSFER; ANIMALS; CELL MOVEMENT; CELLS, CULTURED; CHEMOKINE CCL2; FEMALE; HUMANS; INTERLEUKIN-17; INTERLEUKIN-23 SUBUNIT P19; MACROPHAGES; MALARIA; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MODELS, ANIMAL; PARASITEMIA; PLASMODIUM BERGHEI; SPLEEN;

EID: 84885760629     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201343493     Document Type: Article

References (46)

1. WHO. Malaria Fact sheet No. 94, 2013. [Online] Available from: http://www.who.int/mediacentre/factsheets/fs094/en/index.html. [Accessed Jun 19. 2013].
2. Salvador, A., Hernandez, R. M., Pedraz, J. L. and Igartua, M., Plasmodium falciparum malaria vaccines: current status, pitfalls and future directions. Expert Rev. Vaccines 2012. 11: 1071-1086.
3. Oppmann, B., Lesley, R., Blom, B., Timans, J. C., Xu, Y., Hunte, B., Vega, F. et al., Novel p19 protein engages IL-12p40 to form a cytokine, IL-23, with biological activities similar as well as distinct from IL-12. Immunity 2000. 13: 715-725.
4. Langrish, C. L., Chen, Y., Blumenschein, W. M., Mattson, J., Basham, B., Sedgwick, J. D., McClanahan, T. et al., IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. J. Exp. Med. 2005. 201: 233-240.
5. Kroenke, M. A., Carlson, T. J., Andjelkovic, A. V. and Segal, B. M., IL-12- and IL-23-modulated T cells induce distinct types of EAE based on histology, CNS chemokine profile, and response to cytokine inhibition. J. Exp. Med. 2008. 205: 1535-1541.
6. Kotloski, N. J., Nardelli, D. T., Peterson, S. H., Torrealba, J. R., Warner, T. F., Callister, S. M. and Schell, R. F., Interleukin-23 is required for development of arthritis in mice vaccinated and challenged with Borrelia species. Clin. Vaccine Immunol. 2008. 15: 1199-1207.
7. Munoz, M., Heimesaat, M. M., Danker, K., Struck, D., Lohmann, U., Plickert, R., Bereswill, S. et al., Interleukin (IL)-23 mediates Toxoplasma gondii-induced immunopathology in the gut via matrixmetalloproteinase-2 and IL-22 but independent of IL-17. J. Exp. Med. 2009. 206: 3047-3059.
8. Iwakura, Y. and Ishigame, H., The IL-23/IL-17 axis in inflammation. J. Clin. Invest. 2006. 116: 1218-1222.
9. Izcue, A., Hue, S., Buonocore, S., Arancibia-Carcamo, C. V., Ahern, P. P., Iwakura, Y., Maloy, K. J. et al., Interleukin-23 restrains regulatory T cell activity to drive T cell-dependent colitis. Immunity 2008. 28: 559-570.
10. Happel, K. I., Dubin, P. J., Zheng, M., Ghilardi, N., Lockhart, C., Quinton, L. J., Odden, A. et al., Divergent roles of IL-23 and IL-12 in host defense against Klebsiella pneumoniae. J. Exp. Med. 2005. 202: 761-769.
11. Kagami, S., Rizzo, H. L., Kurtz, S. E., Miller, L. S. and Blauvelt, A., IL-23 and IL-17A, but not IL-12 and IL-22, are required for optimal skin host defense against Candida albicans. J. Immunol. 2010. 185: 5453-5462.
12. Wu, Q., Martin, R. J., Rino, J. G., Breed, R., Torres, R. M. and Chu, H. W., IL-23-dependent IL-17 production is essential in neutrophil recruitment and activity in mouse lung defense against respiratory Mycoplasma pneumoniae infection. Microbes Infect. 2007. 9: 78-86.
13. Meeks, K. D., Sieve, A. N., Kolls, J. K., Ghilardi, N. and Berg, R. E., IL-23 is required for protection against systemic infection with Listeria monocytogenes. J. Immunol. 2009. 183: 8026-8034.
14. Khader, S. A., Pearl, J. E., Sakamoto, K., Gilmartin, L., Bell, G. K., Jelley-Gibbs, D. M., Ghilardi, N. et al., IL-23 compensates for the absence of IL-12p70 and is essential for the IL-17 response during tuberculosis but is dispensable for protection and antigen-specific IFN-gamma responses if IL-12p70 is available. J. Immunol. 2005. 175: 788-795.
15. Town, T., Bai, F., Wang, T., Kaplan, A. T., Qian, F., Montgomery, R. R., Anderson, J. F. et al., Toll-like receptor 7 mitigates lethal West Nile encephalitis via interleukin 23-dependent immune cell infiltration and homing. Immunity 2009. 30: 242-253.
16. Yoshimoto, T., Yoneto, T., Waki, S. and Nariuchi, H., Interleukin-12-dependent mechanisms in the clearance of blood-stage murine malaria parasite Plasmodium berghei XAT, an attenuated variant of P. berghei NK65. J. Infect. Dis. 1998. 177: 1674-1681.
17. Yoshimoto, T., Takahama, Y., Wang, C. R., Yoneto, T., Waki, S. and Nariuchi, H., A pathogenic role of IL-12 in blood-stage murine malaria lethal strain Plasmodium berghei NK65 infection. J. Immunol. 1998. 160: 5500-5505.
18. Adachi, K., Tsutsui, H., Kashiwamura, S., Seki, E., Nakano, H., Takeuchi, O., Takeda, K. et al., Plasmodium berghei infection in mice induces liver injury by an IL-12- and toll-like receptor/myeloid differentiation factor 88-dependent mechanism. J. Immunol. 2001. 167: 5928-5934.
19. + regulatory T cells. Nat. Med. 2004. 10: 29-30.
20. Hisaeda, H., Tetsutani, K., Imai, T., Moriya, C., Tu, L., Hamano, S., Duan, X. et al., Malaria parasites require TLR9 signaling for immune evasion by activating regulatory T cells. J. Immunol. 2008. 180: 2496-2503.
21. Pandya, A. D., Al-Jaderi, Z., Hoglund, R. A., Holmoy, T., Harbo, H. F., Norgauer, J. and Maghazachi, A. A., Identification of human NK17/NK1 cells. PLoS ONE 2011. 6: e26780.
22. Lapara, N. J., 3rd. and Kelly, B. L., Suppression of LPS-induced inflammatory responses in macrophages infected with Leishmania. J. Inflamm. 2010. 7: 8.
23. Sutton, C. E., Lalor, S. J., Sweeney, C. M., Brereton, C. F., Lavelle, E. C. and Mills, K. H., Interleukin-1 and IL-23 induce innate IL-17 production from gammadelta T cells, amplifying Th17 responses and autoimmunity. Immunity 2009. 31: 331-341.
24. Doisne, J. M., Soulard, V., Becourt, C., Amniai, L., Henrot, P., Havenar-Daughton, C., Blanchet, C. et al., Cutting edge: crucial role of IL-1 and IL-23 in the innate IL-17 response of peripheral lymph node NK1.1- invariant NKT cells to bacteria. J. Immunol. 2011. 186: 662-666.
25. Song, C., Luo, L., Lei, Z., Li, B., Liang, Z., Liu, G., Li, D. et al., IL-17-producing alveolar macrophages mediate allergic lung inflammation related to asthma. J. Immunol. 2008. 181: 6117-6124.
26. Andreasen, C., Powell, D. A. and Carbonetti, N. H., Pertussis toxin stimulates IL-17 production in response to Bordetella pertussis infection in mice. PLoS ONE 2009. 4: e7079.
27. + T cells are required for HSP65 expression in host macrophages and for protection of mice infected with Plasmodium yoelii. Parasitol. Int. 2001. 50: 201-209.
28. + T cells in protective immunity against murine blood-stage infection with Plasmodium yoelii 17XL strain. Eur. J. Immunol. 2010. 40: 1053-1061.
29. van Rooijen, N. and Sanders, A., Liposome mediated depletion of macrophages: mechanism of action, preparation of liposomes and applications. J. Immunol. Methods 1994. 174: 83-93.
30. Qiu, Z., Dillen, C., Hu, J., Verbeke, H., Struyf, S., van Damme, J. and Opdenakker, G., Interleukin-17 regulates chemokine and gelatinase B expression in fibroblasts to recruit both neutrophils and monocytes. Immunobiology 2009. 214: 835-842.
31. Shahrara, S., Pickens, S. R., Mandelin, A. M. 2nd, Karpus, W. J., Huang, Q., Kolls, J. K., and Pope, R. M., IL-17-mediated monocyte migration occurs partially through CC chemokine ligand 2/monocyte chemoattractant protein-1 induction. J. Immunol. 2010. 184: 4479-4487.
32. Onishi, R. M. and Gaffen, S. L., Interleukin-17 and its target genes: mechanisms of interleukin-17 function in disease. Immunology 2010. 129: 311-321.
33. Mirzadegan, T., Diehl, F., Ebi, B., Bhakta, S., Polsky, I., McCarley, D., Mulkins, M. et al., Identification of the binding site for a novel class of CCR2b chemokine receptor antagonists: binding to a common chemokine receptor motif within the helical bundle. J. Biol. Chem. 2000. 275: 25562-25571.
34. Ishida, H., Matsuzaki-Moriya, C., Imai, T., Yanagisawa, K., Nojima, Y., Suzue, K., Hirai, M. et al., Development of experimental cerebral malaria is independent of IL-23 and IL-17. Biochem. Biophys. Res. Commun. 2010. 402: 790-795.
35. Teixeira-Coelho, M., Cruz, A., Carmona, J., Sousa, C., Ramos-Pereira, D., Saraiva, A. L., Veldhoen, M. et al., TLR2 deficiency by compromising p19 (IL-23) expression limits Th 17 cell responses to Mycobacterium tuberculosis. Int. Immunol. 2011. 23: 89-96.
36. Bhan, U., Ballinger, M. N., Zeng, X., Newstead, M. J., Cornicelli, M. D. and Standiford, T. J., Cooperative interactions between TLR4 and TLR9 regulate interleukin 23 and 17 production in a murine model of gram negative bacterial pneumonia. PLoS ONE 2010. 5: e9896.
37. Husted, T. L., Blanchard, J., Schuster, R., Shen, H. and Lentsch, A. B., Potential role for IL-23 in hepatic ischemia/reperfusion injury. Inflamm. Res. 2006. 55: 177-178.
38. Huang, Z., van Velkinburgh, J. C., Ni, B. and Wu, Y., Pivotal roles of the interleukin-23/T helper 17 cell axis in hepatitis B. Liver Int. 2012. 32: 894-901.
39. Mastelic, B., do Rosario, A. P., Veldhoen, M., Renauld, J. C., Jarra, W., Sponaas, A. M., Roetynke, S. et al., IL-22 protects against liver pathology and lethality of an experimental blood-stage malaria infection. Front. Immunol. 2012. 3: 85.
40. +. T cell-mediated immune pathology. Infect. Immun. 2011. 79: 1882-1888.
41. Chen, L., Zhang, Z. and Sendo, F., Neutrophils play a critical role in the pathogenesis of experimental cerebral malaria. Clin. Exp. Immunol. 2000. 120: 125-133.
42. + T lymphocyte-mediated loss of marginal metallophilic macrophages following infection with Plasmodium chabaudi chabaudi AS. J. Immunol. 2006. 177: 2518-2526.
43. Sponaas, A-M., do Rosario, A. P. F., Voisine, C., Mastelic, B., Tohompson, J., Koering, S., Jarra, W. et al., Migrating monocytes recureted to the spleen play an imporant role in control of blood stage malaria. Blood 2009. 114: 5522-5531.
44. Webb, A., Johnson, A., Fortunato, M., Platt, A., Crabbe, T., Christie, M. I., Watt, G. F. et al., Evidence for IP-3K-dependent migration of Th17-polarized cells in response to CCR2 and CCR6 agonists. J. Leukoc. Biol. 2008. 84: 1202-1212.
45. Ong'echa, J. M., Remo, A. M., Kristoff, J., Hittner, J. B., Were, T., Ouma, C., Otieno, R. O. et al., Increased circulating interleukin (IL)-23 in children with malarial anemia: in vivo and in vitro relationship with co-regulatory cytokines IL-12 and IL-10. Clin. Immunol. 2008. 126: 211-221.
46. + cells impairs the recovery process in ischaemia/reperfusion-induced acute kidney injury. Nephrol. Dial. Transplant. 2010. 25: 2908-2921.