Th17 Cells Are Long Lived and Retain a Stem Cell-like Molecular Signature

Immunity

Volumn 35, Issue 6, 2011, Pages 972-985

  Muranski, Pawel ^a   Borman, Zachary A ^a   Kerkar, Sid P ^a   Klebanoff, Christopher A ^a   Ji, Yun ^a   Sanchez Perez, Luis ^a   Sukumar, Madhusudhanan ^a   Reger, Robert N ^a   Yu, Zhiya ^a   Kern, Steven J ^b   Roychoudhuri, Rahul ^a   Ferreyra, Gabriela A ^b   Shen, Wei ^a   Durum, Scott K ^a   Feigenbaum, Lionel ^c   Palmer, Douglas C ^a   Antony, Paul A ^d   Chan, Chi Chao ^e   Laurence, Arian ^f   Danner, Robert L ^b   Gattinoni, Luca ^a   Restifo, Nicholas P ^a   more..

^a NATIONAL CANCER INSTITUTE   (United States)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

^c SAIC FREDERICK INC   (United States)

^d UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^e NATIONAL EYE INSTITUTE   (United States)

^f NATIONAL INSTITUTE OF ARTHRITIS AND MUSCULOSKELETAL AND SKIN DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; CD27 ANTIGEN; GAMMA INTERFERON; INTERLEUKIN 17; WNT PROTEIN;

ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ARTICLE; AUTOIMMUNITY; CD8+ T LYMPHOCYTE; CELL DIFFERENTIATION; CELL FUNCTION; CELL RENEWAL; CONTROLLED STUDY; IN VIVO STUDY; MEMORY CELL; MEMORY T LYMPHOCYTE; MOUSE; MULTIPOTENT STEM CELL; NONHUMAN; PRIORITY JOURNAL; STEM CELL; T LYMPHOCYTE SUBPOPULATION; TH17 CELL;

ANIMALS; ANTIGENS, CD27; CELL DIFFERENTIATION; CELL SURVIVAL; GENE EXPRESSION PROFILING; INTERLEUKIN-17; MICE; MICE, TRANSGENIC; NEOPLASMS; STEM CELLS; T-LYMPHOCYTE SUBSETS; TH1 CELLS; TH17 CELLS;

EID: 84255215452     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2011.09.019     Document Type: Article

References (82)

1. Ballesteros-Tato A., Randall T.D. Memory: The incomplete unhappening of differentiation. Immunity 2011, 35:496-498.
2. Bending D., De la Peña H., Veldhoen M., Phillips J.M., Uyttenhove C., Stockinger B., Cooke A. Highly purified Th17 cells from BDC2.5NOD mice convert into Th1-like cells in NOD/SCID recipient mice. J. Clin. Invest. 2009, 119:565-572.
3. Benoist C., Germain R.N., Mathis D. A plaidoyer for 'systems immunology'. Immunol. Rev. 2006, 210:229-234.
4. Berger C., Jensen M.C., Lansdorp P.M., Gough M., Elliott C., Riddell S.R. Adoptive transfer of effector CD8+ T cells derived from central memory cells establishes persistent T cell memory in primates. J. Clin. Invest. 2008, 118:294-305.
5. Beyersdorf N., Ding X., Tietze J.K., Hanke T. Characterization of mouse CD4 T cell subsets defined by expression of KLRG1. Eur. J. Immunol. 2007, 37:3445-3454.
6. Brenchley J.M., Paiardini M., Knox K.S., Asher A.I., Cervasi B., Asher T.E., Scheinberg P., Price D.A., Hage C.A., Kholi L.M., et al. Differential Th17 CD4 T-cell depletion in pathogenic and nonpathogenic lentiviral infections. Blood 2008, 112:2826-2835.
7. Carlson M.J., West M.L., Coghill J.M., Panoskaltsis-Mortari A., Blazar B.R., Serody J.S. In vitro-differentiated TH17 cells mediate lethal acute graft-versus-host disease with severe cutaneous and pulmonary pathologic manifestations. Blood 2009, 113:1365-1374.
8. Dang E.V., Barbi J., Yang H.Y., Jinasena D., Yu H., Zheng Y., Bordman Z., Fu J., Kim Y., Yen H.R., et al. Control of T(H)17/T(reg) balance by hypoxia-inducible factor 1. Cell 2011, 146:772-784.
9. Ding Y., Shen S., Lino A.C., Curotto de Lafaille M.A., Lafaille J.J. Beta-catenin stabilization extends regulatory T cell survival and induces anergy in nonregulatory T cells. Nat. Med. 2008, 14:162-169.
10. Durant L., Watford W.T., Ramos H.L., Laurence A., Vahedi G., Wei L., Takahashi H., Sun H.W., Kanno Y., Powrie F., O'Shea J.J. Diverse targets of the transcription factor STAT3 contribute to T cell pathogenicity and homeostasis. Immunity 2010, 32:605-615.
11. Gattinoni L., Klebanoff C.A., Palmer D.C., Wrzesinski C., Kerstann K., Yu Z., Finkelstein S.E., Theoret M.R., Rosenberg S.A., Restifo N.P. Acquisition of full effector function in vitro paradoxically impairs the in vivo antitumor efficacy of adoptively transferred CD8+ T cells. J. Clin. Invest. 2005, 115:1616-1626.
12. Gattinoni L., Powell D.J., Rosenberg S.A., Restifo N.P. Adoptive immunotherapy for cancer: Building on success. Nat. Rev. Immunol. 2006, 6:383-393.
13. Gattinoni L., Zhong X.S., Palmer D.C., Ji Y., Hinrichs C.S., Yu Z., Wrzesinski C., Boni A., Cassard L., Garvin L.M., et al. Wnt signaling arrests effector T cell differentiation and generates CD8+ memory stem cells. Nat. Med. 2009, 15:808-813.
14. Gattinoni L., Ji Y., Restifo N.P. Wnt/beta-catenin signaling in T-cell immunity and cancer immunotherapy. Clin. Cancer Res. 2010, 16:4695-4701.
15. Gattinoni L., Lugli E., Ji Y., Pos Z., Paulos C.M., Quigley M.F., Almeida J.R., Gostick E., Yu Z.Y., Carpenito C., et al. A human memory T cell subset with stem cell-like properties. Nat. Med. 2011, 17:1290-1297.
16. Ghoreschi K., Laurence A., Yang X.P., Tato C.M., McGeachy M.J., Konkel J.E., Ramos H.L., Wei L., Davidson T.S., Bouladoux N., et al. Generation of pathogenic T(H)17 cells in the absence of TGF-β signalling. Nature 2010, 467:967-971.
17. Grosso J.F., Kelleher C.C., Harris T.J., Maris C.H., Hipkiss E.L., De Marzo A., Anders R., Netto G., Getnet D., Bruno T.C., et al. LAG-3 regulates CD8+ T cell accumulation and effector function in murine self- and tumor-tolerance systems. J. Clin. Invest. 2007, 117:3383-3392.
18. Haining W.N., Wherry E.J. Integrating genomic signatures for immunologic discovery. Immunity 2010, 32:152-161.
19. Haining W.N., Ebert B.L., Subrmanian A., Wherry E.J., Eichbaum Q., Evans J.W., Mak R., Rivoli S., Pretz J., Angelosanto J., et al. Identification of an evolutionarily conserved transcriptional signature of CD8 memory differentiation that is shared by T and B cells. J. Immunol. 2008, 181:1859-1868.
20. Hendriks J., Gravestein L.A., Tesselaar K., van Lier R.A.W., Schumacher T.N.M., Borst J. CD27 is required for generation and long-term maintenance of T cell immunity. Nat. Immunol. 2000, 1:433-440.
21. Hirano T., Ishihara K., Hibi M. Roles of STAT3 in mediating the cell growth, differentiation and survival signals relayed through the IL-6 family of cytokine receptors. Oncogene 2000, 19:2548-2556.
22. Hirota K., Duarte J.H., Veldhoen M., Hornsby E., Li Y., Cua D.J., Ahlfors H., Wilhelm C., Tolaini M., Menzel U., et al. Fate mapping of IL-17-producing T cells in inflammatory responses. Nat. Immunol. 2011, 12:255-263.
23. Homann D., Teyton L., Oldstone M.B.A. Differential regulation of antiviral T-cell immunity results in stable CD8+ but declining CD4+ T-cell memory. Nat. Med. 2001, 7:913-919.
24. Joshi N.S., Cui W., Chandele A., Lee H.K., Urso D.R., Hagman J., Gapin L., Kaech S.M. Inflammation directs memory precursor and short-lived effector CD8(+) T cell fates via the graded expression of T-bet transcription factor. Immunity 2007, 27:281-295.
25. Kaech S.M., Wherry E.J., Ahmed R. Effector and memory T-cell differentiation: Implications for vaccine development. Nat. Rev. Immunol. 2002, 2:251-262.
26. Kerkar S.P., Sanchez-Perez L., Yang S.C., Borman Z.A., Muranski P., Ji Y., Chinnasamy D., Kaiser A.D.M., Hinrichs C.S., Klebanoff C.A., et al. Genetic engineering of murine CD8+ and CD4+ T cells for preclinical adoptive immunotherapy studies. J. Immunother. 2011, 34:343-352.
27. Kim J.W., Lemke G. Hedgehog-regulated localization of Vax2 controls eye development. Genes Dev. 2006, 20:2833-2847.
28. Klebanoff C.A., Gattinoni L., Torabi-Parizi P., Kerstann K., Cardones A.R., Finkelstein S.E., Palmer D.C., Antony P.A., Hwang S.T., Rosenberg S.A., et al. Central memory self/tumor-reactive CD8+ T cells confer superior antitumor immunity compared with effector memory T cells. Proc. Natl. Acad. Sci. USA 2005, 102:9571-9576.
29. Klebanoff C.A., Gattinoni L., Restifo N.P. CD8+ T-cell memory in tumor immunology and immunotherapy. Immunol. Rev. 2006, 211:214-224.
30. Kryczek I., Zhao E.D., Liu Y., Wang Y., Vatan L., Szeliga W., Moyer J., Klimczak A., Lange A., Zou W.P. Human TH17 cells are long-lived effector memory cells. Sci. Transl. Med. 2011, 3:ra100.
31. Lee Y.K., Turner H., Maynard C.L., Oliver J.R., Chen D., Elson C.O., Weaver C.T. Late developmental plasticity in the T helper 17 lineage. Immunity 2009, 30:92-107.
32. Luckey C.J., Bhattacharya D., Goldrath A.W., Weissman I.L., Benoist C., Mathis D. Memory T and memory B cells share a transcriptional program of self-renewal with long-term hematopoietic stem cells. Proc. Natl. Acad. Sci. USA 2006, 103:3304-3309.
33. MacLeod M.K.L., Clambey E.T., Kappler J.W., Marrack P. CD4 memory T cells: What are they and what can they do?. Semin. Immunol. 2009, 21:53-61.
34. Marshall H.D., Chandele A., Jung Y.W., Meng H.L., Poholek A.C., Parish I.A., Rutishauser R., Cui W.G., Kleinstein S.H., Craft J., Kaech S.M. Differential Expression of Ly6C and T-bet Distinguish Effector and Memory Th1 CD4(+) Cell Properties during Viral Infection. Immunity 2011, 35:633-646.
35. Martin-Orozco N., Chung Y., Chang S.H., Wang Y.H., Dong C. Th17 cells promote pancreatic inflammation but only induce diabetes efficiently in lymphopenic hosts after conversion into Th1 cells. Eur. J. Immunol. 2009, 39:216-224.
36. Martin-Orozco N., Muranski P., Chung Y., Yang X.O., Yamazaki T., Lu S., Hwu P., Restifo N.P., Overwijk W.W., Dong C. T helper 17 cells promote cytotoxic T cell activation in tumor immunity. Immunity 2009, 31:787-798.
37. Maynard C.L., Weaver C.T. Intestinal effector T cells in health and disease. Immunity 2009, 31:389-400.
38. McKinstry K.K., Strutt T.M., Swain S.L. Regulation of CD4+ T-cell contraction during pathogen challenge. Immunol. Rev. 2010, 236:110-124.
39. Muranski P., Restifo N.P. Adoptive immunotherapy of cancer using CD4(+) T cells. Curr. Opin. Immunol. 2009, 21:200-208.
40. Muranski P., Boni A., Wrzesinski C., Citrin D.E., Rosenberg S.A., Childs R., Restifo N.P. Increased intensity lymphodepletion and adoptive immunotherapy-how far can we go?. Nat. Clin. Pract. Oncol. 2006, 3:668-681.
41. Muranski P., Boni A., Antony P.A., Cassard L., Irvine K.R., Kaiser A., Paulos C.M., Palmer D.C., Touloukian C.E., Ptak K., et al. Tumor-specific Th17-polarized cells eradicate large established melanoma. Blood 2008, 112:362-373.
42. Murphy K.M., Stockinger B. Effector T cell plasticity: Flexibility in the face of changing circumstances. Nat. Immunol. 2010, 11:674-680.
43. Murugaiyan G., Saha B. Protumor vs antitumor functions of IL-17. J. Immunol. 2009, 183:4169-4175.
44. Notani D., Gottimukkala K.P., Jayani R.S., Limaye A.S., Damle M.V., Mehta S., Purbey P.K., Joseph J., Galande S. Global regulator SATB1 recruits β-catenin and regulates T(H)2 differentiation in Wnt-dependent manner. PLoS Biol. 2010, 8:e1000296.
45. Oestreich K.J., Huang A.C., Weinmann A.S. The lineage-defining factors T-bet and Bcl-6 collaborate to regulate Th1 gene expression patterns. J. Exp. Med. 2011, 208:1001-1013.
46. Overwijk W.W., Theoret M.R., Finkelstein S.E., Surman D.R., de Jong L.A., Vyth-Dreese F.A., Dellemijn T.A., Antony P.A., Spiess P.J., Palmer D.C., et al. Tumor regression and autoimmunity after reversal of a functionally tolerant state of self-reactive CD8+ T cells. J. Exp. Med. 2003, 198:569-580.
47. Palmer M.T., Weaver C.T. Autoimmunity: Increasing suspects in the CD4+ T cell lineup. Nat. Immunol. 2010, 11:36-40.
48. Palmer D.C., Chan C.C., Gattinoni L., Wrzesinski C., Paulos C.M., Hinrichs C.S., Powell D.J., Klebanoff C.A., Finkelstein S.E., Fariss R.N., et al. Effective tumor treatment targeting a melanoma/melanocyte-associated antigen triggers severe ocular autoimmunity. Proc. Natl. Acad. Sci. USA 2008, 105:8061-8066.
49. Pepper M., Linehan J.L., Pagán A.J., Zell T., Dileepan T., Cleary P.P., Jenkins M.K. Different routes of bacterial infection induce long-lived TH1 memory cells and short-lived TH17 cells. Nat. Immunol. 2010, 11:83-89.
50. Pepper M., Pagán A.J., Igyártó B.Z., Taylor J.J., Jenkins M.K. Opposing signals from the bcl6 transcription factor and the interleukin-2 receptor generate T helper 1 central and effector memory cells. Immunity 2011, 35:583-595.
51. Railo A., Pajunen A., Itäranta P., Naillat F., Vuoristo J., Kilpeläinen P., Vainio S. Genomic response to Wnt signalling is highly context-dependent-evidence from DNA microarray and chromatin immunoprecipitation screens of Wnt/TCF targets. Exp. Cell Res. 2009, 315:2690-2704.
52. Reiley W.W., Shafiani S., Wittmer S.T., Tucker-Heard G., Moon J.J., Jenkins M.K., Urdahl K.B., Winslow G.M., Woodland D.L. Distinct functions of antigen-specific CD4 T cells during murine Mycobacterium tuberculosis infection. Proc. Natl. Acad. Sci. USA 2010, 107:19408-19413.
53. Roose J., Huls G., van Beest M., Moerer P., van der Horn K., Goldschmeding R., Logtenberg T., Clevers H. Synergy between tumor suppressor APC and the beta-catenin-Tcf4 target Tcf1. Science 1999, 285:1923-1926.
54. Rutishauser R.L., Martins G.A., Kalachikov S., Chandele A., Parish I.A., Meffre E., Jacob J., Calame K., Kaech S.M. Transcriptional repressor Blimp-1 promotes CD8(+) T cell terminal differentiation and represses the acquisition of central memory T cell properties. Immunity 2009, 31:296-308.
55. Sallusto F., Lanzavecchia A. Human Th17 cells in infection and autoimmunity. Microbes Infect. 2009, 11:620-624.
56. Shen X.L., Zhou J.H., Hathcock K.S., Robbins P., Powell D.J., Rosenberg S.A., Hodes R.J. Persistence of tumor infiltrating lymphocytes in adoptive immunotherapy correlates with telomere length. J. Immunother. 2007, 30:123-129.
57. Shi G., Ramaswamy M., Vistica B.P., Cox C.A., Tan C., Wawrousek E.F., Siegel R.M., Gery I. Unlike Th1, Th17 cells mediate sustained autoimmune inflammation and are highly resistant to restimulation-induced cell death. J. Immunol. 2009, 183:7547-7556.
58. Shi L.Z., Wang R., Huang G., Vogel P., Neale G., Green D.R., Chi H. HIF1α-dependent glycolytic pathway orchestrates a metabolic checkpoint for the differentiation of TH17 and Treg cells. J. Exp. Med. 2011, 208:1367-1376.
59. Staal F.J., Sen J.M. The canonical Wnt signaling pathway plays an important role in lymphopoiesis and hematopoiesis. Eur. J. Immunol. 2008, 38:1788-1794.
60. Staal F.J., Luis T.C., Tiemessen M.M. WNT signalling in the immune system: WNT is spreading its wings. Nat. Rev. Immunol. 2008, 8:581-593.
61. Stemberger C., Neuenhahn M., Gebhardt F.E., Schiemann M., Buchholz V.R., Busch D.H. Stem cell-like plasticity of naïve and distinct memory CD8+ T cell subsets. Semin. Immunol. 2009, 21:62-68.
62. Stockinger B., Hirota K., Duarte J., Veldhoen M. External influences on the immune system via activation of the aryl hydrocarbon receptor. Semin. Immunol. 2011, 23:99-105.
63. Subramanian A., Tamayo P., Mootha V.K., Mukherjee S., Ebert B.L., Gillette M.A., Paulovich A., Pomeroy S.L., Golub T.R., Lander E.S., Mesirov J.P. Gene set enrichment analysis: A knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl. Acad. Sci. USA 2005, 102:15545-15550.
64. Sun L., Ryan D.G., Zhou M.Y., Sun T.T., Lavker R.M. EEDA: A protein associated with an early stage of stratified epithelial differentiation. J. Cell. Physiol. 2006, 206:103-111.
65. Surh C.D., Sprent J. Glimpsing the real CD4+ T cell response. Nat. Immunol. 2010, 11:47-49.
66. Taylor J.J., Jenkins M.K. CD4+ memory T cell survival. Curr. Opin. Immunol. 2011, 23:319-323.
67. Waddington C.H. The Strategy of the Genes 1957, George Allen & Unwin, London.
68. Wahren-Herlenius M., Kuchroo V.K. Gene-environment interaction in induction of autoimmunity. Semin. Immunol. 2011, 23:65-66.
69. Wei G., Wei L., Zhu J., Zang C., Hu-Li J., Yao Z., Cui K., Kanno Y., Roh T.Y., Watford W.T., et al. Global mapping of H3K4me3 and H3K27me3 reveals specificity and plasticity in lineage fate determination of differentiating CD4+ T cells. Immunity 2009, 30:155-167.
70. Williams M.A., Ravkov E.V., Bevan M.J. Rapid culling of the CD4+ T cell repertoire in the transition from effector to memory. Immunity 2008, 28:533-545.
71. Willinger T., Freeman T., Herbert M., Hasegawa H., McMichael A.J., Callan M.F. Human naive CD8 T cells down-regulate expression of the WNT pathway transcription factors lymphoid enhancer binding factor 1 and transcription factor 7 (T cell factor-1) following antigen encounter in vitro and in vivo. J. Immunol. 2006, 176:1439-1446.
72. Wirth T.C., Xue H.H., Rai D., Sabel J.T., Bair T., Harty J.T., Badovinac V.P. Repetitive antigen stimulation induces stepwise transcriptome diversification but preserves a core signature of memory CD8(+) T cell differentiation. Immunity 2010, 33:128-140.
73. Wu C.Y., Kirman J.R., Rotte M.J., Davey D.F., Perfetto S.P., Rhee E.G., Freidag B.L., Hill B.J., Douek D.C., Seder R.A. Distinct lineages of T(H)1 cells have differential capacities for memory cell generation in vivo. Nat. Immunol. 2002, 3:852-858.
74. Xie Y., Akpinarli A., Maris C., Hipkiss E.L., Lane M., Kwon E.K., Muranski P., Restifo N.P., Antony P.A. Naive tumor-specific CD4(+) T cells differentiated in vivo eradicate established melanoma. J. Exp. Med. 2010, 207:651-667.
75. Yang Y., Weiner J., Liu Y., Smith A.J., Huss D.J., Winger R., Peng H., Cravens P.D., Racke M.K., Lovett-Racke A.E. T-bet is essential for encephalitogenicity of both Th1 and Th17 cells. J. Exp. Med. 2009, 206:1549-1564.
76. Yang X.P., Ghoreschi K., Steward-Tharp S.M., Rodriguez-Canales J., Zhu J., Grainger J.R., Hirahara K., Sun H.W., Wei L., Vahedi G., et al. Opposing regulation of the locus encoding IL-17 through direct, reciprocal actions of STAT3 and STAT5. Nat. Immunol. 2011, 12:247-254.
77. Yu Q., Sharma A., Oh S.Y., Moon H.G., Hossain M.Z., Salay T.M., Leeds K.E., Du H., Wu B., Waterman M.L., et al. T cell factor 1 initiates the T helper type 2 fate by inducing the transcription factor GATA-3 and repressing interferon-gamma. Nat. Immunol. 2009, 10:992-999.
78. Yu Q., Sharma A., Ghosh A., Sen J.M. T cell factor-1 negatively regulates expression of IL-17 family of cytokines and protects mice from experimental autoimmune encephalomyelitis. J. Immunol. 2011, 186:3946-3952.
79. Zhou J., Shen X., Huang J., Hodes R.J., Rosenberg S.A., Robbins P.F. Telomere length of transferred lymphocytes correlates with in vivo persistence and tumor regression in melanoma patients receiving cell transfer therapy. J. Immunol. 2005, 175:7046-7052.
80. Zhou Q., Munger M.E., Highfill S.L., Tolar J., Weigel B.J., Riddle M., Sharpe A.H., Vallera D.A., Azuma M., Levine B.L., et al. Program death-1 signaling and regulatory T cells collaborate to resist the function of adoptively transferred cytotoxic T lymphocytes in advanced acute myeloid leukemia. Blood 2010, 116:2484-2493.
81. Zou W., Restifo N.P. T(H)17 cells in tumour immunity and immunotherapy. Nat. Rev. Immunol. 2010, 10:248-256.
82. Zygmunt B., Veldhoen M. T helper cell differentiation more than just cytokines. Adv. Immunol. 2011, 109:159-196.