IL-27 and IL-21 are associated with T Cell IL-10 responses in human visceral leishmaniasis

Journal of Immunology

Volumn 186, Issue 7, 2011, Pages 3977-3985

  Ansari, Nasim Akhtar ^a,b   Kumar, Rajiv ^a,b   Gautam, Shalini ^b   Nylén, Susanne ^c   Singh, Om Prakash ^b   Sundar, Shyam ^b   Sacks, David ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b BANARAS HINDU UNIVERSITY   (India)

^c KAROLINSKA INSTITUTE   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

CD14 ANTIGEN; CD3 ANTIGEN; CYTOKINE; GAMMA INTERFERON; INTERFERON REGULATORY FACTOR 1; INTERLEUKIN 10; INTERLEUKIN 12P40; INTERLEUKIN 1BETA; INTERLEUKIN 21; INTERLEUKIN 23 RECEPTOR; INTERLEUKIN 23P19; INTERLEUKIN 27; INTERLEUKIN 27P28; MESSENGER RNA; PROTEIN EBI 3; RECOMBINANT CYTOKINE; RECOMBINANT INTERLEUKIN 21; RETINOID RELATED ORPHAN RECEPTOR GAMMA; RETINOID RELATED ORPHAN RECEPTOR GAMMA T; UNCLASSIFIED DRUG;

ADULT; ANTIGEN SPECIFICITY; ARTICLE; CD3+ T LYMPHOCYTE; CELL EXPANSION; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; FEEDBACK SYSTEM; FEMALE; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; MACROPHAGE; MAJOR CLINICAL STUDY; MALE; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BLOOD LEVEL; PROTEIN INDUCTION; SPLEEN CELL; T LYMPHOCYTE; TH17 CELL; UPREGULATION; VISCERAL LEISHMANIASIS;

ADULT; FEEDBACK, PHYSIOLOGICAL; FEMALE; HUMANS; INTERLEUKIN-10; INTERLEUKIN-17; INTERLEUKINS; LEISHMANIASIS, VISCERAL; MACROPHAGES; MALE; RNA, MESSENGER; SPLEEN; T-LYMPHOCYTES; T-LYMPHOCYTES, HELPER-INDUCER; UP-REGULATION; YOUNG ADULT;

EID: 79955000536     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1003588     Document Type: Article

References (48)

1. Guerin, P. J., P. Olliaro, S. Sundar, M. Boelaert, S. L. Croft, P. Desjeux, M. K. Wasunna, and A. D. Bryceson. 2002. Visceral leishmaniasis: Current status of control, diagnosis, and treatment, and a proposed research and development agenda. Lancet Infect. Dis. 2: 494-501. (Pubitemid 34826855)
2. Sundar, S., and M. Rai. 2002. Advances in the treatment of leishmaniasis. Curr. Opin. Infect. Dis. 15: 593-598. (Pubitemid 36026972)
3. Ansari, N. A., S. Saluja, and P. Salotra. 2006. Elevated levels of interferon-g, interleukin-10, and interleukin-6 during active disease in Indian kala azar. Clin. Immunol. 119: 339-345.
4. Caldas, A., C. Favali, D. Aquino, V. Vinhas, J. van Weyenbergh, C. Brodskyn, J. Costa, M. Barral-Netto, and A. Barral. 2005. Balance of IL-10 and interferong plasma levels in human visceral leishmaniasis: Implications in the pathogenesis. BMC Infect. Dis. 5: 113.
5. Ghalib, H. W., M. R. Piuvezam, Y. A. Skeiky, M. Siddig, F. A. Hashim, A. M. el- Hassan, D. M. Russo, and S. G. Reed. 1993. Interleukin 10 production correlates with pathology in human Leishmania donovani infections. J. Clin. Invest. 92: 324-329. (Pubitemid 23209013)
6. Karp, C. L., S. H. el-Safi, T. A. Wynn, M. M. Satti, A. M. Kordofani, F. A. Hashim, M. Hag-Ali, F. A. Neva, T. B. Nutman, and D. L. Sacks. 1993. In vivo cytokine profiles in patients with kala-azar. Marked elevation of both interleukin-10 and interferon-g. J. Clin. Invest. 91: 1644-1648. (Pubitemid 23127368)
7. + CD25+ (Foxp3) regulatory T cells in human visceral leishmaniasis. J. Exp. Med. 204: 805-817. (Pubitemid 46631610)
8. Nylén, S., and D. Sacks. 2007. Interleukin-10 and the pathogenesis of human visceral leishmaniasis. Trends Immunol. 28: 378-384. (Pubitemid 47385375)
9. Murphy, M. L., U. Wille, E. N. Villegas, C. A. Hunter, and J. P. Farrell. 2001. IL- 10 mediates susceptibility to Leishmania donovani infection. Eur. J. Immunol. 31: 2848-2856. (Pubitemid 32994535)
10. Murray, H. W., K. C. Flanders, D. D. Donaldson, J. P. Sypek, P. J. Gotwals, J. Liu, and X. Ma. 2005. Antagonizing deactivating cytokines to enhance host defense and chemotherapy in experimental visceral leishmaniasis. Infect. Immun. 73: 3903-3911. (Pubitemid 40923128)
11. Ghalib, H. W., J. A. Whittle, M. Kubin, F. A. Hashim, A. M. el-Hassan, K. H. Grabstein, G. Trinchieri, and S. G. Reed. 1995. IL-12 enhances Th1-type responses in human Leishmania donovani infections. J. Immunol. 154: 4623-4629.
12. Carvalho, E. M., O. Bacellar, C. Brownell, T. Regis, R. L. Coffman, and S. G. Reed. 1994. Restoration of IFN-g production and lymphocyte proliferation in visceral leishmaniasis. J. Immunol. 152: 5949-5956.
13. + T cells. Eur. J. Immunol. 36: 1764-1771. (Pubitemid 44089043)
14. Ranatunga, D., C. M. Hedrich, F. Wang, D. W. McVicar, N. Nowak, T. Joshi, L. Feigenbaum, L. R. Grant, S. Stäger, and J. H. Bream. 2009. A human IL10 BAC transgene reveals tissue-specific control of IL-10 expression and alters disease outcome. Proc. Natl. Acad. Sci. USA 106: 17123-17128.
15. +CD25- Foxp3- Th1 cells are the source of IL-10-mediated immune suppression in chronic cutaneous leishmaniasis. J. Exp. Med. 204: 285-297. (Pubitemid 46294545)
16. Stumhofer, J. S., and C. A. Hunter. 2008. Advances in understanding the antiinflammatory properties of IL-27. Immunol. Lett. 117: 123-130.
17. Yoshida, H., and Y. Miyazaki. 2008. Regulation of immune responses by interleukin-27. [Published erratum appears in 2009 Immunol. Rev. 227: 283.] Immunol. Rev. 226: 234-247.
18. Pot, C., H. Jin, A. Awasthi, S. M. Liu, C. Y. Lai, R. Madan, A. H. Sharpe, C. L. Karp, S. C. Miaw, I. C. Ho, and V. K. Kuchroo. 2009. Cutting edge: IL-27 induces the transcription factor c-Maf, cytokine IL-21, and the costimulatory receptor ICOS that coordinately act together to promote differentiation of IL-10- producing Tr1 cells. J. Immunol. 183: 797-801.
19. Kastelein, R. A., C. A. Hunter, and D. J. Cua. 2007. Discovery and biology of IL- 23 and IL-27: Related but functionally distinct regulators of inflammation. Annu. Rev. Immunol. 25: 221-242. (Pubitemid 46697908)
20. Collison, L. W., and D. A. Vignali. 2008. Interleukin-35: Odd one out or part of the family? Immunol. Rev. 226: 248-262.
21. Amadi-Obi, A., C. R. Yu, X. Liu, R. M. Mahdi, G. L. Clarke, R. B. Nussenblatt, I. Gery, Y. S. Lee, and C. E. Egwuagu. 2007. TH17 cells contribute to uveitis and scleritis and are expanded by IL-2 and inhibited by IL-27/STAT1. Nat. Med. 13: 711-718. (Pubitemid 46889754)
22. Molle, C., M. Goldman, and S. Goriely. 2010. Critical role of the IFN-stimulated gene factor 3 complex in TLR-mediated IL-27p28 gene expression revealing a two-step activation process. J. Immunol. 184: 1784-1792.
23. Zhang, J., X. Qian, H. Ning, J. Yang, H. Xiong, and J. Liu. 2010. Activation of IL-27 p28 gene transcription by interferon regulatory factor 8 in cooperation with interferon regulatory factor 1. J. Biol. Chem. 285: 21269-21281.
24. Wirtz, S., C. Becker, M. C. Fantini, E. E. Nieuwenhuis, I. Tubbe, P. R. Galle, H. J. Schild, M. Birkenbach, R. S. Blumberg, and M. F. Neurath. 2005. EBVinduced gene 3 transcription is induced by TLR signaling in primary dendritic cells via NF-kB activation. J. Immunol. 174: 2814-2824. (Pubitemid 40279698)
25. Stumhofer, J. S., J. S. Silver, A. Laurence, P. M. Porrett, T. H. Harris, L. A. Turka, M. Ernst, C. J. Saris, J. J. O'Shea, and C. A. Hunter. 2007. Interleukins 27 and 6 induce STAT3-mediated T cell production of interleukin 10. Nat. Immunol. 8: 1363-1371. (Pubitemid 350131173)
26. Rosas, L. E., A. A. Satoskar, K. M. Roth, T. L. Keiser, J. Barbi, C. Hunter, F. J. de Sauvage, and A. R. Satoskar. 2006. Interleukin-27R (WSX-1/T-cell cytokine receptor) gene-deficient mice display enhanced resistance to leishmania donovani infection but develop severe liver immunopathology. Am. J. Pathol. 168: 158-169. (Pubitemid 43062569)
27. + cells in nonhealing Leishmania major infection. J. Immunol. 183: 4619-4627.
28. Batten, M., J. Li, S. Yi, N. M. Kljavin, D. M. Danilenko, S. Lucas, J. Lee, F. J. de Sauvage, and N. Ghilardi. 2006. Interleukin 27 limits autoimmune encephalomyelitis by suppressing the development of interleukin 17-producing T cells. Nat. Immunol. 7: 929-936. (Pubitemid 44263906)
29. Stumhofer, J. S., A. Laurence, E. H. Wilson, E. Huang, C. M. Tato, L. M. Johnson, A. V. Villarino, Q. Huang, A. Yoshimura, D. Sehy, et al. 2006. Interleukin 27 negatively regulates the development of interleukin 17-producing T helper cells during chronic inflammation of the central nervous system. Nat. Immunol. 7: 937-945. (Pubitemid 44263907)
30. + T cells. J. Immunol. 183: 2435-2443.
31. Larousserie, F., E. Bardel, A. Coulomb L'Herminé, D. Canioni, N. Brousse, R. A. Kastelein, and O. Devergne. 2006. Variable expression of Epstein-Barr virus-induced gene 3 during normal B-cell differentiation and among B-cell lymphomas. J. Pathol. 209: 360-368. (Pubitemid 43997745)
32. Schmidt, C., T. Giese, B. Ludwig, I. Mueller-Molaian, T. Marth, S. Zeuzem, S. C. Meuer, and A. Stallmach. 2005. Expression of interleukin-12- related cytokine transcripts in inflammatory bowel disease: Elevated interleukin-23p19 and interleukin-27p28 in Crohn's disease but not in ulcerative colitis. Inflamm. Bowel Dis. 11: 16-23. (Pubitemid 40340252)
33. Guzzo, C., W. M. Hopman, N. F. Che Mat, W. Wobeser, and K. Gee. 2010. Impact of HIV infection, highly active antiretroviral therapy, and hepatitis C coinfection on serum interleukin-27. AIDS 24: 1371-1374.
34. Zhu, C., R. Zhang, L. Liu, S. T. Rasool, Y. Mu, W. Sun, Q. Hao, F. Liu, Y. Zhu, and J. Wu. 2009. Hepatitis B virus enhances interleukin-27 expression both in vivo and in vitro. Clin. Immunol. 131: 92-97.
35. Kenney, R. T., D. L. Sacks, A. A. Gam, H. W. Murray, and S. Sundar. 1998. Splenic cytokine responses in Indian kala-azar before and after treatment. J. Infect. Dis. 177: 815-818.
36. Pitta, M. G., A. Romano, S. Cabantous, S. Henri, A. Hammad, B. Kouriba, L. Argiro, M. el Kheir, B. Bucheton, C. Mary, et al. 2009. IL-17 and IL-22 are associated with protection against human kala azar caused by Leishmania donovani. J. Clin. Invest. 119: 2379-2387.
37. Korn, T., E. Bettelli, W. Gao, A. Awasthi, A. Jäger, T. B. Strom, M. Oukka, and V. K. Kuchroo. 2007. IL-21 initiates an alternative pathway to induce proinflammatory T(H)17 cells. Nature 448: 484-487. (Pubitemid 47123515)
38. Nurieva, R., X. O. Yang, G. Martinez, Y. Zhang, A. D. Panopoulos, L. Ma, K. Schluns, Q. Tian, S. S. Watowich, A. M. Jetten, and C. Dong. 2007. Essential autocrine regulation by IL-21 in the generation of inflammatory T cells. Nature 448: 480-483. (Pubitemid 47123514)
39. Saraiva, M., J. R. Christensen, M. Veldhoen, T. L. Murphy, K. M. Murphy, and A. O'Garra. 2009. Interleukin-10 production by Th1 cells requires interleukin- 12-induced STAT4 transcription factor and ERK MAP kinase activation by high antigen dose. Immunity 31: 209-219.
40. Batten, M., N. M. Kljavin, J. Li, M. J. Walter, F. J. de Sauvage, and N. Ghilardi. 2008. Cutting edge: IL-27 is a potent inducer of IL-10 but not FoxP3 in murine T cells. J. Immunol. 180: 2752-2756.
41. Fitzgerald, D. C., G. X. Zhang, M. El-Behi, Z. Fonseca-Kelly, H. Li, S. Yu, C. J. Saris, B. Gran, B. Ciric, and A. Rostami. 2007. Suppression of autoimmune inflammation of the central nervous system by interleukin 10 secreted by interleukin 27-stimulated T cells. Nat. Immunol. 8: 1372-1379. (Pubitemid 350131174)
42. Awasthi, A., Y. Carrier, J. P. Peron, E. Bettelli, M. Kamanaka, R. A. Flavell, V. K. Kuchroo, M. Oukka, and H. L. Weiner. 2007. A dominant function for interleukin 27 in generating interleukin 10-producing anti-inflammatory T cells. Nat. Immunol. 8: 1380-1389. (Pubitemid 350131175)
43. Spolski, R., H. P. Kim, W. Zhu, D. E. Levy, and W. J. Leonard. 2009. IL-21 mediates suppressive effects via its induction of IL-10. J. Immunol. 182: 2859-2867.
44. Ozaki, K., R. Spolski, C. G. Feng, C. F. Qi, J. Cheng, A. Sher, H. C. Morse, III, C. Liu, P. L. Schwartzberg, and W. J. Leonard. 2002. A critical role for IL-21 in regulating immunoglobulin production. Science 298: 1630-1634. (Pubitemid 35387203)
45. Kumar, R., Y. Goto, K. Gidwani, K. D. Cowgill, S. Sundar, and S. G. Reed. 2010. Evaluation of ex vivo human immune response against candidate antigens for a visceral leishmaniasis vaccine. Am. J. Trop. Med. Hyg. 82: 808-813.
46. Mahmoodi, M., S. Rajabalian, A. Fekri, and I. Esfandiarpour. 2005. Evaluation of in vitro production of IFN-g, IL-10, IL-12 and IL-13 by blood cells in patients with cutaneous leishmaniasis lesions. Iran. J. Allergy Asthma Immunol. 4: 15-21.
47. Liu, J., X. Guan, and X. Ma. 2007. Regulation of IL-27 p28 gene expression in macrophages through MyD88- and interferon-g-mediated pathways. J. Exp. Med. 204: 141-152. (Pubitemid 46148764)
48. Poleganov, M. A., M. Bachmann, J. Pfeilschifter, and H. Mühl. 2008. Genomewide analysis displays marked induction of EBI3/IL-27B in IL-18-activated AML-derived KG1 cells: Critical role of two kB binding sites in the human EBI3 promotor. Mol. Immunol. 45: 2869-2880.