Dihydroartemisinin ameliorates inflammatory disease by its reciprocal effects on Th and regulatory T cell function via modulating the mammalian target of rapamycin pathway

Journal of Immunology

Volumn 189, Issue 9, 2012, Pages 4417-4425

  Zhao, Yan G ^a,b   Wang, Yunqi ^a   Guo, Zengli ^a   Gu, Ai Di ^a   Dan, Han C ^c   Baldwin, Albert S ^c   Hao, Weidong ^b   Wan, Yisong Y ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b PEKING UNIVERSITY HEALTH SCIENCE CENTER   (China)

^c UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DIHYDROARTEMISININ; MAMMALIAN TARGET OF RAPAMYCIN; PROTEIN KINASE B; SMAD PROTEIN; TRANSFORMING GROWTH FACTOR BETA RECEPTOR;

ALLERGIC ENCEPHALOMYELITIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIPROLIFERATIVE ACTIVITY; ARTICLE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; IMMUNOREGULATION; IN VITRO STUDY; INFLAMMATORY DISEASE; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTE PROLIFERATION; MAMMALIAN TARGET OF RAPAMYCIN PATHWAY; MOUSE; NONHUMAN; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; SIGNAL TRANSDUCTION; TH17 CELL;

AMINO ACID SEQUENCE; ANIMALS; ARTEMISININS; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; INFLAMMATION; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MOLECULAR SEQUENCE DATA; SIGNAL TRANSDUCTION; T-LYMPHOCYTES, HELPER-INDUCER; T-LYMPHOCYTES, REGULATORY; TOR SERINE-THREONINE KINASES;

EID: 84867902905     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1200919     Document Type: Article

References (43)

1. Klayman, D. L. 1985. Qinghaosu (artemisinin): an antimalarial drug from China. Science 228: 1049-1055. (Pubitemid 15227365)
2. Kremsner, P. G., and S. Krishna. 2004. Antimalarial combinations. Lancet 364: 285-294.
3. Eckstein-Ludwig, U., R. J. Webb, I. D. Van Goethem, J. M. East, A. G. Lee, M. Kimura, P. M. O'Neill, P. G. Bray, S. A. Ward, and S. Krishna. 2003. Artemisinins target the SERCA of Plasmodium falciparum. Nature 424: 957-961. (Pubitemid 37051688)
4. Singh, N. P., and H. Lai. 2001. Selective toxicity of dihydroartemisinin and holotransferrin toward human breast cancer cells. Life Sci. 70: 49-56. (Pubitemid 33130042)
5. Chen, H. H., H. J. Zhou, W. Q. Wang, and G. D. Wu. 2004. Antimalarial dihydroartemisinin also inhibits angiogenesis. Cancer Chemother. Pharmacol. 53: 423-432.
6. Wu, X., W. Zhang, X. Shi, P. An, W. Sun, and Z. Wang. 2010. Therapeutic effect of artemisinin on lupus nephritis mice and its mechanisms. Acta Biochim. Biophys. Sin. (Shanghai) 42: 916-923.
7. Zhou, W. L., J. M. Wu, Q. L. Wu, J. X. Wang, Y. Zhou, R. Zhou, P. L. He, X. Y. Li, Y. F. Yang, Y. Zhang, et al. 2005. A novel artemisinin derivative, 3-(12-beta-artemisininoxy) phenoxyl succinic acid (SM735), mediates immunosuppressive effects in vitro and in vivo. Acta Pharmacol. Sin. 26: 1352-1358. (Pubitemid 41607008)
8. Wang, J. X., W. Tang, R. Zhou, J. Wan, L. P. Shi, Y. Zhang, Y. F. Yang, Y. Li, and J. P. Zuo. 2008. The new water-soluble artemisinin derivative SM905 ameliorates collagen-induced arthritis by suppression of inflammatory and Th17 responses. Br. J. Pharmacol. 153: 1303-1310. (Pubitemid 351415509)
9. Wan, Y. Y., and R. A. Flavell. 2009. How diverse - CD4 effector T cells and their functions. J Mol Cell Biol 1: 20-36.
10. Coffman, R. L., and J. Carty. 1986. AT cell activity that enhances polyclonal IgE production and its inhibition by interferon-gamma. J. Immunol. 136: 949-954. (Pubitemid 16146381)
11. Mosmann, T. R., H. Cherwinski, M. W. Bond, M. A. Giedlin, and R. L. Coffman. 1986. Two types of murine helper T cell clone. I. Definition according to profiles of lymphokine activities and secreted proteins. J. Immunol. 136: 2348-2357. (Pubitemid 16136806)
12. Szabo, S. J., B. M. Sullivan, S. L. Peng, and L. H. Glimcher. 2003. Molecular mechanisms regulating Th1 immune responses. Annu. Rev. Immunol. 21: 713-758. (Pubitemid 37174546)
13. Park, H., Z. Li, X. O. Yang, S. H. Chang, R. Nurieva, Y. H. Wang, Y. Wang, L. Hood, Z. Zhu, Q. Tian, and C. Dong. 2005. A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nat. Immunol. 6: 1133-1141. (Pubitemid 41541791)
14. Harrington, L. E., R. D. Hatton, P. R. Mangan, H. Turner, T. L. Murphy, K. M. Murphy, and C. T. Weaver. 2005. Interleukin 17-producing CD4+ effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages. Nat. Immunol. 6: 1123-1132. (Pubitemid 41541790)
15. Mangan, P. R., L. E. Harrington, D. B. O'Quinn, W. S. Helms, D. C. Bullard, C. O. Elson, R. D. Hatton, S. M. Wahl, T. R. Schoeb, and C. T. Weaver. 2006. Transforming growth factor-beta induces development of the T(H)17 lineage. Nature 441: 231-234.
16. 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)
17. Langrish, C. L., Y. Chen, W. M. Blumenschein, J. Mattson, B. Basham, J. D. Sedgwick, T. McClanahan, R. A. Kastelein, and D. J. Cua. 2005. IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. J. Exp. Med. 201: 233-240. (Pubitemid 40189432)
18. Ivanov, I. I., B. S. McKenzie, L. Zhou, C. E. Tadokoro, A. Lepelley, J. J. Lafaille, D. J. Cua, and D. R. Littman. 2006. The orphan nuclear receptor RORgammat directs the differentiation program of proinflammatory IL-17+ T helper cells. Cell 126: 1121-1133. (Pubitemid 44380299)
19. Liang, S. C., X. Y. Tan, D. P. Luxenberg, R. Karim, K. Dunussi-Joannopoulos, M. Collins, and L. A. Fouser. 2006. Interleukin (IL)-22 and IL-17 are coexpressed by Th17 cells and cooperatively enhance expression of antimicrobial peptides. J. Exp. Med. 203: 2271-2279. (Pubitemid 44498362)
20. Veldhoen, M., K. Hirota, A. M. Westendorf, J. Buer, L. Dumoutier, J. C. Renauld, and B. Stockinger. 2008. The aryl hydrocarbon receptor links TH17-cell-mediated autoimmunity to environmental toxins. Nature 453: 106-109. (Pubitemid 351630329)
21. Yang, X. O., A. D. Panopoulos, R. Nurieva, S. H. Chang, D. Wang, S. S. Watowich, and C. Dong. 2007. STAT3 regulates cytokine-mediated generation of inflammatory helper T cells. J. Biol. Chem. 282: 9358-9363. (Pubitemid 47104613)
22. Sakaguchi, S. 2000. Regulatory T cells: key controllers of immunologic self-tolerance. Cell 101: 455-458.
23. Shevach, E. M. 2000. Regulatory T cells in autoimmmunity*. Annu. Rev. Immunol. 18: 423-449.
24. Bettelli, E., Y. Carrier, W. Gao, T. Korn, T. B. Strom, M. Oukka, H. L. Weiner, and V. K. Kuchroo. 2006. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 441: 235-238.
25. Zhou, L., J. E. Lopes, M. M. Chong, I. I. Ivanov, R. Min, G. D. Victora, Y. Shen, J. Du, Y. P. Rubtsov, A. Y. Rudensky, et al. 2008. TGF-beta-induced Foxp3 inhibits T(H)17 cell differentiation by antagonizing RORgammat function. Nature 453: 236-240. (Pubitemid 351667978)
26. Chen, W., W. Jin, N. Hardegen, K. J. Lei, L. Li, N. Marinos, G. McGrady, and S. M. Wahl. 2003. Conversion of peripheral CD4+CD25- naive T cells to CD4+CD25+ regulatory T cells by TGF-beta induction of transcription factor Foxp3. J. Exp. Med. 198: 1875-1886. (Pubitemid 38032120)
27. Wan, Y. Y., and R. A. Flavell. 2005. Identifying Foxp3-expressing suppressor T cells with a bicistronic reporter. Proc. Natl. Acad. Sci. USA 102: 5126-5131.
28. Pasare, C., and R. Medzhitov. 2003. Toll pathway-dependent blockade of CD4+CD25+ T cell-mediated suppression by dendritic cells. Science 299: 1033-1036. (Pubitemid 36222922)
29. Li, M. O., S. Sanjabi, and R. A. Flavell. 2006. Transforming growth factor-beta controls development, homeostasis, and tolerance of T cells by regulatory T cell-dependent and -independent mechanisms. Immunity 25: 455-471. (Pubitemid 44354214)
30. Liu, Y., P. Zhang, J. Li, A. B. Kulkarni, S. Perruche, and W. Chen. 2008. A critical function for TGF-beta signaling in the development of natural CD4 +CD25+Foxp3+ regulatory T cells. Nat. Immunol. 9: 632-640. (Pubitemid 351712634)
31. Massagué, J., and D. Wotton. 2000. Transcriptional control by the TGF-beta/Smad signaling system. EMBO J. 19: 1745-1754. (Pubitemid 30204386)
32. Grygielko, E. T., W. M. Martin, C. Tweed, P. Thornton, J. Harling, D. P. Brooks, and N. J. Laping. 2005. Inhibition of gene markers of fibrosis with a novel inhibitor of transforming growth factor-beta type I receptor kinase in puromycin-induced nephritis. J. Pharmacol. Exp. Ther. 313: 943-951. (Pubitemid 40726998)
33. Dunn, N. R., C. H. Koonce, D. C. Anderson, A. Islam, E. K. Bikoff, and E. J. Robertson. 2005. Mice exclusively expressing the short isoform of Smad2 develop normally and are viable and fertile. Genes Dev. 19: 152-163. (Pubitemid 40095824)
34. Lee, P. P., D. R. Fitzpatrick, C. Beard, H. K. Jessup, S. Lehar, K. W. Makar, M. Pérez-Melgosa, M. T. Sweetser, M. S. Schlissel, S. Nguyen, et al. 2001. A critical role for Dnmt1 and DNA methylation in T cell development, function, and survival. Immunity 15: 763-774. (Pubitemid 34008504)
35. Jäger, A., V. Dardalhon, R. A. Sobel, E. Bettelli, and V. K. Kuchroo. 2009. Th1, Th17, and Th9 effector cells induce experimental autoimmune encephalomyelitis with different pathological phenotypes. J. Immunol. 183: 7169-7177.
36. Komiyama, Y., S. Nakae, T. Matsuki, A. Nambu, H. Ishigame, S. Kakuta, K. Sudo, and Y. Iwakura. 2006. IL-17 plays an important role in the development of experimental autoimmune encephalomyelitis. J. Immunol. 177: 566-573. (Pubitemid 43939170)
37. McGeachy, M. J., L. A. Stephens, and S. M. Anderton. 2005. Natural recovery and protection from autoimmune encephalomyelitis: contribution of CD4+ CD25+ regulatory cells within the central nervous system. J. Immunol. 175: 3025-3032. (Pubitemid 41170521)
38. Delgoffe, G. M., T. P. Kole, Y. Zheng, P. E. Zarek, K. L. Matthews, B. Xiao, P. F. Worley, S. C. Kozma, and J. D. Powell. 2009. The mTOR kinase differentially regulates effector and regulatory T cell lineage commitment. Immunity 30: 832-844.
39. Haxhinasto, S., D. Mathis, and C. Benoist. 2008. The AKT-mTOR axis regulates de novo differentiation of CD4+Foxp3+ cells. J. Exp. Med. 205: 565-574. (Pubitemid 351439304)
40. Hay, N., and N. Sonenberg. 2004. Upstream and downstream of mTOR. Genes Dev. 18: 1926-1945. (Pubitemid 39071573)
41. Liu, G., S. Burns, G. Huang, K. Boyd, R. L. Proia, R. A. Flavell, and H. Chi. 2009. The receptor S1P1 overrides regulatory T cell-mediated immune suppression through Akt-mTOR. Nat. Immunol. 10: 769-777.
42. Brown, E. J., M. W. Albers, T. B. Shin, K. Ichikawa, C. T. Keith, W. S. Lane, and S. L. Schreiber. 1994. A mammalian protein targeted by G1-arresting rapamycin-receptor complex. Nature 369: 756-758.
43. Haque, A., S. E. Best, F. H. Amante, S. Mustafah, L. Desbarrieres, F. de Labastida, T. Sparwasser, G. R. Hill, and C. R. Engwerda. 2010. CD4+ natural regulatory T cells prevent experimental cerebral malaria via CTLA-4 when expanded in vivo. PLoS Pathog. 6: e1001221.