The role and regulation of human Th17 cells in tumor immunity

American Journal of Pathology

Volumn 182, Issue 1, 2013, Pages 10-20

  Ye, Jian ^a   Livergood, Rob S ^a   Peng, Guangyong ^a  

^a SAINT LOUIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CCR4; CHEMOKINE RECEPTOR CCR5; CHEMOKINE RECEPTOR CCR6; CHEMOKINE RECEPTOR CCR7; CHEMOKINE RECEPTOR CXCR3; CHEMOKINE RECEPTOR CXCR4; CHEMOKINE RECEPTOR CXCR5; CHEMOKINE RECEPTOR CXCR6; GAMMA INTERFERON; GRANZYME A; GRANZYME B; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 17; INTERLEUKIN 2; INTERLEUKIN 23; INTERLEUKIN 4; INTERLEUKIN 6; INTERLEUKIN 8; L SELECTIN; MACROPHAGE INFLAMMATORY PROTEIN 3ALPHA; MONOCYTE CHEMOTACTIC PROTEIN 1; RANTES; TOLL LIKE RECEPTOR; TRANSFORMING GROWTH FACTOR BETA1; TUMOR NECROSIS FACTOR ALPHA;

ACUTE GRANULOCYTIC LEUKEMIA; BLADDER CARCINOMA; CARCINOGENESIS; CELL DIFFERENTIATION; CELL EXPANSION; CELL FUNCTION; CELL MIGRATION; CELL SURVIVAL; COLORECTAL CANCER; CYTOKINE RELEASE; DISEASE MARKER; HUMAN; HUMAN CELL; IMMUNOREGULATION; LIVER CELL CARCINOMA; MELANOMA; MULTIPLE MYELOMA; OVARY CANCER; PLASTICITY; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; REVIEW; TH1 CELL; TH17 CELL; TH2 CELL; TUMOR IMMUNITY; TUMOR MICROENVIRONMENT;

HUMANS; IMMUNITY, CELLULAR; IMMUNOPHENOTYPING; LYMPHOCYTES, TUMOR-INFILTRATING; NEOPLASMS; T-LYMPHOCYTES, REGULATORY; TH17 CELLS; TUMOR MICROENVIRONMENT;

EID: 84871317687     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2012.08.041     Document Type: Review

References (83)

1. L.E. Harrington, R.D. Hatton, P.R. Mangan, H. Turner, T.L. Murphy, K.M. Murphy, and C.T. Weaver Interleukin 17-producing CD4+ effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages Nat Immunol 6 2005 1123 1132 (Pubitemid 41541790)
2. H. Park, Z. Li, X.O. Yang, S.H. Chang, R. Nurieva, Y.H. Wang, Y. Wang, L. Hood, Z. Zhu, Q. Tian, and C. Dong A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17 Nat Immunol 6 2005 1133 1141 (Pubitemid 41541791)
3. C. Dong TH17 cells in development: an updated view of their molecular identity and genetic programming Nat Rev Immunol 8 2008 337 348 (Pubitemid 351595217)
4. E. Bettelli, T. Korn, and V.K. Kuchroo Th17: The third member of the effector T cell trilogy Curr Opin Immunol 19 2007 652 657 (Pubitemid 350236805)
5. M. Veldhoen, R.J. Hocking, C.J. Atkins, R.M. Locksley, and B. Stockinger TGFbeta in the context of an inflammatory cytokine milieu supports de novo differentiation of IL-17-producing T cells Immunity 24 2006 179 189 (Pubitemid 43214587)
6. E. Bettelli, Y. Carrier, W. Gao, T. Korn, T.B. Strom, M. Oukka, H.L. Weiner, and V.K. Kuchroo Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells Nature 441 2006 235 238
7. P.R. Mangan, 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 Transforming growth factor-beta induces development of the T(H)17 lineage Nature 441 2006 231 234
8. T. Korn, E. Bettelli, W. Gao, A. Awasthi, A. Jäger, T.B. Strom, M. Oukka, and V.K. Kuchroo IL-21 initiates an alternative pathway to induce proinflammatory T(H)17 cells Nature 448 2007 484 487 (Pubitemid 47123515)
9. L. Zhou, I.I. Ivanov, R. Spolski, R. Min, K. Shenderov, T. Egawa, D.E. Levy, W.J. Leonard, and D.R. Littman IL-6 programs T(H)-17 cell differentiation by promoting sequential engagement of the IL-21 and IL-23 pathways Nat Immunol 8 2007 967 974 (Pubitemid 47300011)
10. Y. Chung, S.H. Chang, G.J. Martinez, X.O. Yang, R. Nurieva, H.S. Kang, L. Ma, S.S. Watowich, A.M. Jetten, Q. Tian, and C. Dong Critical regulation of early Th17 cell differentiation by interleukin-1 signaling Immunity 30 2009 576 587
11. N.J. Wilson, K. Boniface, J.R. Chan, B.S. McKenzie, W.M. Blumenschein, J.D. Mattson, B. Basham, K. Smith, T. Chen, F. Morel, J.C. Lecron, R.A. Kastelein, D.J. Cua, T.K. McClanahan, E.P. Bowman, and R. de Waal Malefyt Development, cytokine profile and function of human interleukin 17-producing helper T cells Nat Immunol 8 2007 950 957 (Pubitemid 47300009)
12. I.I. Ivanov, B.S. McKenzie, L. Zhou, C.E. Tadokoro, A. Lepelley, J.J. Lafaille, D.J. Cua, and D.R. Littman The orphan nuclear receptor RORgammat directs the differentiation program of proinflammatory IL-17+ T helper cells Cell 126 2006 1121 1133 (Pubitemid 44380299)
13. Q. Chen, W. Yang, S. Gupta, P. Biswas, P. Smith, G. Bhagat, and A.B. Pernis IRF-4-binding protein inhibits interleukin-17 and interleukin-21 production by controlling the activity of IRF-4 transcription factor Immunity 29 2008 899 911
14. E.V. Dang, J. Barbi, H.Y. Yang, D. Jinasena, H. Yu, Y. Zheng, Z. Bordman, J. Fu, Y. Kim, H.R. Yen, W. Luo, K. Zeller, L. Shimoda, S.L. Topalian, G.L. Semenza, C.V. Dang, D.M. Pardoll, and F. Pan Control of T(H)17/T(reg) balance by hypoxia-inducible factor 1 Cell 146 2011 772 784
15. L.Z. Shi, R. Wang, G. Huang, P. Vogel, G. Neale, D.R. Green, and H. Chi HIF1alpha-dependent glycolytic pathway orchestrates a metabolic checkpoint for the differentiation of TH17 and Treg cells J Exp Med 208 2011 1367 1376
16. S. Dandekar, M.D. George, and A.J. Baumler Th17 cells, HIV and the gut mucosal barrier Curr Opin HIV AIDS 5 2010 173 178
17. L.A. Tesmer, S.K. Lundy, S. Sarkar, and D.A. Fox Th17 cells in human disease Immunol Rev 223 2008 87 113 (Pubitemid 351986173)
18. C.M. Koebel, W. Vermi, J.B. Swann, N. Zerafa, S.J. Rodig, L.J. Old, M.J. Smyth, and R.D. Schreiber Adaptive immunity maintains occult cancer in an equilibrium state Nature 450 2007 903 907 (Pubitemid 350231320)
19. G.P. Dunn, L.J. Old, and R.D. Schreiber The immunobiology of cancer immunosurveillance and immunoediting Immunity 21 2004 137 148 (Pubitemid 39094044)
20. C. Galand, S. Donnou, L. Crozet, S. Brunet, V. Touitou, H. Ouakrim, W.H. Fridman, C. Sautès-Fridman, and S. Fisson Th17 cells are involved in the local control of tumor progression in primary intraocular lymphoma PLoS One 6 2011 e24622
21. K.M. Dhodapkar, S. Barbuto, P. Matthews, A. Kukreja, A. Mazumder, D. Vesole, S. Jagannath, and M.V. Dhodapkar Dendritic cells mediate the induction of polyfunctional human IL17-producing cells (Th17-1 cells) enriched in the bone marrow of patients with myeloma Blood 112 2008 2878 2885
22. K. Noonan, L. Marchionni, J. Anderson, D. Pardoll, G.D. Roodman, and I. Borrello A novel role of IL-17-producing lymphocytes in mediating lytic bone disease in multiple myeloma Blood 116 2010 3554 3563
23. X. Zhu, L.A. Mulcahy, R.A. Mohammed, A.H. Lee, H.A. Franks, L. Kilpatrick, A. Yilmazer, E.C. Paish, I.O. Ellis, P.M. Patel, and A.M. Jackson IL-17 expression by breast-cancer-associated macrophages: IL-17 promotes invasiveness of breast cancer cell lines Breast Cancer Res 10 2008 R95
24. X. Su, J. Ye, E.C. Hsueh, Y. Zhang, D.F. Hoft, and G. Peng Tumor microenvironments direct the recruitment and expansion of human Th17 cells J Immunol 184 2010 1630 1641
25. I. Kryczek, M. Banerjee, P. Cheng, L. Vatan, W. Szeliga, S. Wei, E. Huang, E. Finlayson, D. Simeone, T.H. Welling, A. Chang, G. Coukos, R. Liu, and W. Zou Phenotype, distribution, generation, and functional and clinical relevance of Th17 cells in the human tumor environments Blood 114 2009 1141 1149
26. M. Tosolini, A. Kirilovsky, B. Mlecnik, T. Fredriksen, S. Mauger, G. Bindea, A. Berger, P. Bruneval, W.H. Fridman, F. Pagès, and J. Galon Clinical impact of different classes of infiltrating T cytotoxic and helper cells (Th1, th2, treg, th17) in patients with colorectal cancer [Erratum appeared in Cancer Res 2011, 71:4732] Cancer Res 71 2011 1263 1271
27. J.N. Hahn, V.G. Falck, and F.R. Jirik Smad4 deficiency in T cells leads to the Th17-associated development of premalignant gastroduodenal lesions in mice J Clin Invest 121 2011 4030 4042
28. T. Maruyama, K. Kono, Y. Mizukami, Y. Kawaguchi, K. Mimura, M. Watanabe, S. Izawa, and H. Fujii Distribution of Th17 cells and FoxP3(+) regulatory T cells in tumor-infiltrating lymphocytes, tumor-draining lymph nodes and peripheral blood lymphocytes in patients with gastric cancer Cancer Sci 101 2010 1947 1954
29. J.P. Zhang, J. Yan, J. Xu, X.H. Pang, M.S. Chen, L. Li, C. Wu, S.P. Li, and L. Zheng Increased intratumoral IL-17-producing cells correlate with poor survival in hepatocellular carcinoma patients J Hepatol 50 2009 980 989
30. P. Muranski, A. Boni, P.A. Antony, L. Cassard, K.R. Irvine, A. Kaiser, C.M. Paulos, D.C. Palmer, C.E. Touloukian, K. Ptak, L. Gattinoni, C. Wrzesinski, C.S. Hinrichs, K.W. Kerstann, L. Feigenbaum, C.C. Chan, and N.P. Restifo Tumor-specific Th17-polarized cells eradicate large established melanoma Blood 112 2008 362 373
31. I. Kryczek, S. Wei, L. Zou, S. Altuwaijri, W. Szeliga, J. Kolls, A. Chang, and W. Zou Cutting edge: th17 and regulatory T cell dynamics and the regulation by IL-2 in the tumor microenvironment J Immunol 178 2007 6730 6733 (Pubitemid 46847396)
32. Y. Miyahara, K. Odunsi, W. Chen, G. Peng, J. Matsuzaki, and R.F. Wang Generation and regulation of human CD4+ IL-17-producing T cells in ovarian cancer Proc Natl Acad Sci USA 105 2008 15505 15510
33. K.A. Charles, H. Kulbe, R. Soper, M. Escorcio-Correia, T. Lawrence, A. Schultheis, P. Chakravarty, R.G. Thompson, G. Kollias, J.F. Smyth, F.R. Balkwill, and T. Hagemann The tumor-promoting actions of TNF-alpha involve TNFR1 and IL-17 in ovarian cancer in mice and humans J Clin Invest 119 2009 3011 3023
34. L. Leveque, F. Deknuydt, G. Bioley, L.J. Old, J. Matsuzaki, K. Odunsi, M. Ayyoub, and D. Valmori Interleukin 2-mediated conversion of ovarian cancer-associated CD4+ regulatory T cells into proinflammatory interleukin 17-producing helper T cells J Immunother 32 2009 101 108
35. K.S. Sfanos, T.C. Bruno, C.H. Maris, L. Xu, C.J. Thoburn, A.M. DeMarzo, A.K. Meeker, W.B. Isaacs, and C.G. Drake Phenotypic analysis of prostate-infiltrating lymphocytes reveals TH17 and Treg skewing Clin Cancer Res 14 2008 3254 3261
36. E. Derhovanessian, V. Adams, K. Hähnel, A. Groeger, H. Pandha, S. Ward, and G. Pawelec Pretreatment frequency of circulating IL-17+ CD4+ T-cells, but not Tregs, correlates with clinical response to whole-cell vaccination in prostate cancer patients Int J Cancer 125 2009 1372 1379
37. F. Annunziato, L. Cosmi, V. Santarlasci, L. Maggi, F. Liotta, B. Mazzinghi, E. Parente, L. Fili, S. Ferri, F. Frosali, F. Giudici, P. Romagnani, P. Parronchi, F. Tonelli, E. Maggi, and S. Romagnani Phenotypic and functional features of human Th17 cells J Exp Med 204 2007 1849 1861 (Pubitemid 47240944)
38. M.J. McGeachy, K.S. Bak-Jensen, Y. Chen, C.M. Tato, W. Blumenschein, T. McClanahan, and D.J. Cua TGF-beta and IL-6 drive the production of IL-17 and IL-10 by T cells and restrain T(H)-17 cell-mediated pathology Nat Immunol 8 2007 1390 1397 (Pubitemid 350138974)
39. M.J. McGeachy, and D.J. Cua Th17 cell differentiation: The long and winding road Immunity 28 2008 445 453 (Pubitemid 351467042)
40. A. Peters, Y. Lee, and V.K. Kuchroo The many faces of Th17 cells Curr Opin Immunol 23 2011 702 706
41. K. Ghoreschi, A. Laurence, X.P. Yang, K. Hirahara, and J.J. O'Shea T helper 17 cell heterogeneity and pathogenicity in autoimmune disease Trends Immunol 32 2011 395 401
42. H.W. Lim, J. Lee, P. Hillsamer, and C.H. Kim Human Th17 cells share major trafficking receptors with both polarized effector T cells and FOXP3+ regulatory T cells J Immunol 180 2008 122 129
43. K. Hirota, H. Yoshitomi, M. Hashimoto, S. Maeda, S. Teradaira, N. Sugimoto, T. Yamaguchi, T. Nomura, H. Ito, T. Nakamura, N. Sakaguchi, and S. Sakaguchi Preferential recruitment of CCR6-expressing Th17 cells to inflamed joints via CCL20 in rheumatoid arthritis and its animal model J Exp Med 204 2007 2803 2812 (Pubitemid 350179551)
44. I. Kryczek, K. Wu, E. Zhao, S. Wei, L. Vatan, W. Szeliga, E. Huang, J. Greenson, A. Chang, J. Rolinski, P. Radwan, J. Fang, G. Wang, and W. Zou IL-17+ regulatory T cells in the microenvironments of chronic inflammation and cancer J Immunol 186 2011 4388 4395
45. C. Huang, and Z.X. Fu Localization of IL-17+Foxp3+ T cells in esophageal cancer Immunol Invest 40 2011 400 412
46. J. Ye, X. Su, E.C. Hsueh, Y. Zhang, J.M. Koenig, D.F. Hoft, and G. Peng Human tumor-infiltrating Th17 cells have the capacity to differentiate into IFN-gamma(+) and FOXP3(+) T cells with potent suppressive function Eur J Immunol 41 2011 936 951
47. W. Zou, and N.P. Restifo T(H)17 cells in tumour immunity and immunotherapy [Erratum appeared in Nat Rev Immunol 2011, 11:565] Nat Rev Immunol 10 2010 248 256
48. D. Mucida, Y. Park, G. Kim, O. Turovskaya, I. Scott, M. Kronenberg, and H. Cheroutre Reciprocal TH17 and regulatory T cell differentiation mediated by retinoic acid Science 317 2007 256 260 (Pubitemid 47076203)
49. A. Kimura, T. Naka, K. Nohara, Y. Fujii-Kuriyama, and T. Kishimoto Aryl hydrocarbon receptor regulates Stat1 activation and participates in the development of Th17 cells Proc Natl Acad Sci USA 105 2008 9721 9726 (Pubitemid 352031367)
50. M. Veldhoen, K. Hirota, A.M. Westendorf, J. Buer, L. Dumoutier, J.C. Renauld, and B. Stockinger The aryl hydrocarbon receptor links TH17-cell-mediated autoimmunity to environmental toxins Nature 453 2008 106 109 (Pubitemid 351630329)
51. A. Ohta, E. Gorelik, S.J. Prasad, F. Ronchese, D. Lukashev, M.K. Wong, X. Huang, S. Caldwell, K. Liu, P. Smith, J.F. Chen, E.K. Jackson, S. Apasov, S. Abrams, and M. Sitkovsky A2A adenosine receptor protects tumors from antitumor T cells Proc Natl Acad Sci USA 103 2006 13132 13137 (Pubitemid 44338928)
52. J.M. Wilson, C.C. Kurtz, S.G. Black, W.G. Ross, M.S. Alam, J. Linden, and P.B. Ernst The A2B adenosine receptor promotes Th17 differentiation via stimulation of dendritic cell IL-6 J Immunol 186 2011 6746 6752
53. R. Medzhitov Toll-like receptors and innate immunity Nat Rev Immunol 1 2001 135 145 (Pubitemid 33741967)
54. A.J. van Beelen, Z. Zelinkova, E.W. Taanman-Kueter, F.J. Muller, D.W. Hommes, S.A. Zaat, M.L. Kapsenberg, and E.C. de Jong Stimulation of the intracellular bacterial sensor NOD2 programs dendritic cells to promote interleukin-17 production in human memory T cells Immunity 27 2007 660 669 (Pubitemid 47615504)
55. H.G. Evans, T. Suddason, I. Jackson, L.S. Taams, and G.M. Lord Optimal induction of T helper 17 cells in humans requires T cell receptor ligation in the context of Toll-like receptor-activated monocytes Proc Natl Acad Sci USA 104 2007 17034 17039 (Pubitemid 350210986)
56. J.M. Reynolds, B.P. Pappu, J. Peng, G.J. Martinez, Y. Zhang, Y. Chung, L. Ma, X.O. Yang, R.I. Nurieva, Q. Tian, and C. Dong Toll-like receptor 2 signaling in CD4(+) T lymphocytes promotes T helper 17 responses and regulates the pathogenesis of autoimmune disease Immunity 32 2010 692 702
57. M.H. Nyirenda, L. Sanvito, P.J. Darlington, K. O'Brien, G.X. Zhang, C.S. Constantinescu, A. Bar-Or, and B. Gran TLR2 stimulation drives human naive and effector regulatory T cells into a Th17-like phenotype with reduced suppressive function J Immunol 187 2011 2278 2290
58. E. Tartour, F. Fossiez, I. Joyeux, A. Galinha, A. Gey, E. Claret, X. Sastre-Garau, J. Couturier, V. Mosseri, V. Vives, J. Banchereau, W.H. Fridman, J. Wijdenes, S. Lebecque, and C. Sautès-Fridman Interleukin 17, a T-cell-derived cytokine, promotes tumorigenicity of human cervical tumors in nude mice Cancer Res 59 1999 3698 3704 (Pubitemid 29381875)
59. M. Numasaki, M. Watanabe, T. Suzuki, H. Takahashi, A. Nakamura, F. McAllister, T. Hishinuma, J. Goto, M.T. Lotze, J.K. Kolls, and H. Sasaki IL-17 enhances the net angiogenic activity and in vivo growth of human non-small cell lung cancer in SCID mice through promoting CXCR-2-dependent angiogenesis J Immunol 175 2005 6177 6189 (Pubitemid 41508106)
60. L. Wang, T. Yi, M. Kortylewski, D.M. Pardoll, D. Zeng, and H. Yu IL-17 can promote tumor growth through an IL-6-Stat3 signaling pathway J Exp Med 206 2009 1457 1464
61. C. Wu, S. Wang, F. Wang, Q. Chen, S. Peng, Y. Zhang, J. Qian, J. Jin, and H. Xu Increased frequencies of T helper type 17 cells in the peripheral blood of patients with acute myeloid leukaemia Clin Exp Immunol 158 2009 199 204
62. R.H. Prabhala, D. Pelluru, M. Fulciniti, H.K. Prabhala, P. Nanjappa, W. Song, C. Pai, S. Amin, Y.T. Tai, P.G. Richardson, I.M. Ghobrial, S.P. Treon, J.F. Daley, K.C. Anderson, J.L. Kutok, and N.C. Munshi Elevated IL-17 produced by TH17 cells promotes myeloma cell growth and inhibits immune function in multiple myeloma Blood 115 2010 5385 5392
63. C.S. Hinrichs, A. Kaiser, C.M. Paulos, L. Cassard, L. Sanchez-Perez, B. Heemskerk, C. Wrzesinski, Z.A. Borman, P. Muranski, and N.P. Restifo Type 17 CD8+ T cells display enhanced antitumor immunity Blood 114 2009 596 599
64. F. Benchetrit, A. Ciree, V. Vives, G. Warnier, A. Gey, C. Sautès-Fridman, F. Fossiez, N. Haicheur, W.H. Fridman, and E. Tartour Interleukin-17 inhibits tumor cell growth by means of a T-cell-dependent mechanism Blood 99 2002 2114 2121 (Pubitemid 34525496)
65. N. Martin-Orozco, P. Muranski, Y. Chung, X.O. Yang, T. Yamazaki, S. Lu, P. Hwu, N.P. Restifo, W.W. Overwijk, and C. Dong T helper 17 cells promote cytotoxic T cell activation in tumor immunity Immunity 31 2009 787 798
66. I. Kryczek, S. Wei, W. Szeliga, L. Vatan, and W. Zou Endogenous IL-17 contributes to reduced tumor growth and metastasis Blood 114 2009 357 359
67. Z.J. Ye, Q. Zhou, Y.Y. Gu, S.M. Qin, W.L. Ma, J.B. Xin, X.N. Tao, and H.Z. Shi Generation and differentiation of IL-17-producing CD4+ T cells in malignant pleural effusion J Immunol 185 2010 6348 6354
68. A. Hamaï, P. Pignon, I. Raimbaud, K. Duperrier-Amouriaux, H. Senellart, S. Hiret, J.Y. Douillard, J. Bennouna, M. Ayyoub, and D. Valmori Human T(H)17 immune cells specific for the tumor antigen MAGE-A3 convert to IFN-gamma-secreting cells as they differentiate into effector T cells in vivo Cancer Res 72 2012 1059 1063
69. J.L. Gnerlich, J.B. Mitchem, J.S. Weir, N.V. Sankpal, H. Kashiwagi, B.A. Belt, M.R. Porembka, J.M. Herndon, T.J. Eberlein, P. Goedegebuure, and D.C. Linehan Induction of Th17 cells in the tumor microenvironment improves survival in a murine model of pancreatic cancer J Immunol 185 2010 4063 4071
70. M. Numasaki, J. Fukushi, M. Ono, S.K. Narula, P.J. Zavodny, T. Kudo, P.D. Robbins, H. Tahara, and M.T. Lotze Interleukin-17 promotes angiogenesis and tumor growth Blood 101 2003 2620 2627 (Pubitemid 36857622)
71. L. Zhou, M.M. Chong, and D.R. Littman Plasticity of CD4+ T cell lineage differentiation Immunity 30 2009 646 655
72. Y.K. Lee, R. Mukasa, R.D. Hatton, and C.T. Weaver Developmental plasticity of Th17 and Treg cells Curr Opin Immunol 21 2009 274 280
73. H.J. Koenen, R.L. Smeets, P.M. Vink, E. van Rijssen, A.M. Boots, and I. Joosten Human CD25highFoxp3pos regulatory T cells differentiate into IL-17-producing cells Blood 112 2008 2340 2352
74. K.S. Voo, Y.H. Wang, F.R. Santori, C. Boggiano, K. Arima, L. Bover, S. Hanabuchi, J. Khalili, E. Marinova, B. Zheng, D.R. Littman, and Y.J. Liu Identification of IL-17-producing FOXP3+ regulatory T cells in humans Proc Natl Acad Sci USA 106 2009 4793 4798
75. D. Valmori, C. Raffin, I. Raimbaud, and M. Ayyoub Human RORgammat+ TH17 cells preferentially differentiate from naive FOXP3+Treg in the presence of lineage-specific polarizing factors Proc Natl Acad Sci USA 107 2010 19402 19407
76. M. Ayyoub, F. Deknuydt, I. Raimbaud, C. Dousset, L. Leveque, G. Bioley, and D. Valmori Human memory FOXP3+ Tregs secrete IL-17 ex vivo and constitutively express the T(H)17 lineage-specific transcription factor RORgamma t Proc Natl Acad Sci USA 106 2009 8635 8640
77. R. Mukasa, A. Balasubramani, Y.K. Lee, S.K. Whitley, B.T. Weaver, Y. Shibata, G.E. Crawford, R.D. Hatton, and C.T. Weaver Epigenetic instability of cytokine and transcription factor gene loci underlies plasticity of the T helper 17 cell lineage Immunity 32 2010 616 627
78. A. Chaudhry, D. Rudra, P. Treuting, R.M. Samstein, Y. Liang, A. Kas, and A.Y. Rudensky CD4+ regulatory T cells control TH17 responses in a Stat3-dependent manner Science 326 2009 986 991
79. B. Hoechst, J. Gamrekelashvili, M.P. Manns, T.F. Greten, and F. Korangy Plasticity of human Th17 cells and iTregs is orchestrated by different subsets of myeloid cells Blood 117 2011 6532 6541
80. Y. Chen, C.J. Haines, I. Gutcher, K. Hochweller, W.M. Blumenschein, T. McClanahan, G. Hämmerling, M.O. Li, D.J. Cua, and M.J. McGeachy Foxp3(+) regulatory T cells promote T helper 17 cell development in vivo through regulation of interleukin-2 Immunity 34 2011 409 421
81. S. Huber, N. Gagliani, E. Esplugues, W. O'Connor Jr., F.J. Huber, A. Chaudhry, M. Kamanaka, Y. Kobayashi, C.J. Booth, A.Y. Rudensky, M.G. Roncarolo, M. Battaglia, and R.A. Flavell Th17 cells express interleukin-10 receptor and are controlled by Foxp3- and Foxp3+ regulatory CD4+ T cells in an interleukin-10-dependent manner Immunity 34 2011 554 565
82. A. Chaudhry, R.M. Samstein, P. Treuting, Y. Liang, M.C. Pils, J.M. Heinrich, R.S. Jack, F.T. Wunderlich, J.C. Brüning, W. Müller, and A.Y. Rudensky Interleukin-10 signaling in regulatory T cells is required for suppression of Th17 cell-mediated inflammation Immunity 34 2011 566 578
83. M.D. Sharma, D.Y. Hou, Y. Liu, P.A. Koni, R. Metz, P. Chandler, A.L. Mellor, Y. He, and D.H. Munn Indoleamine 2,3-dioxygenase controls conversion of Foxp3+ Tregs to TH17-like cells in tumor-draining lymph nodes Blood 113 2009 6102 6111