Invariant natural killer T cells regulate anti-tumor immunity by controlling the population of dendritic cells in tumor and draining lymph nodes

Journal for ImmunoTherapy of Cancer

Volumn 2, Issue 1, 2014, Pages

  Pilones, Karsten A ^a   Aryankalayil, Joseph ^a   Babb, James S ^a   Demaria, Sandra ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Breast cancer; CD137; CD1d; CD8+ T cells; CTLA 4; Dendritic cells; Immunoregulation; Invariant NKT cells; Radiotherapy

Indexed keywords

B7 ANTIGEN; CD137 ANTIGEN; CD1D ANTIGEN; CD40 ANTIGEN; CD70 ANTIGEN; CD86 ANTIGEN; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4 ANTIBODY; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 4; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1;

ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST CARCINOMA; CANCER RADIOTHERAPY; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; DENDRITIC CELL; EPITOPE MAPPING; FLOW CYTOMETRY; GENE DELETION; IMMUNE DEFICIENCY; IMMUNOHISTOCHEMISTRY; LYMPH NODE; MOUSE; NATURAL KILLER T CELL; NONHUMAN; PRIORITY JOURNAL; TUMOR GROWTH;

EID: 84977177265     PISSN: None     EISSN: 20511426     Source Type: Journal    
DOI: 10.1186/s40425-014-0037-x     Document Type: Article

References (66)

1. Godfrey DI, Berzins SP. Control points in NKT-cell development. Nat Rev Immunol 2007, 7:505-518. 10.1038/nri2116, 17589542.
2. Taniguchi M, Seino K, Nakayama T. The NKT cell system: bridging innate and acquired immunity. Nat Immunol 2003, 4:1164-1165. 10.1038/ni1203-1164, 14639465.
3. Juno JA, Keynan Y, Fowke KR. Invariant NKT cells: regulation and function during viral infection. PLoS Pathog 2012, 8:e1002838. 10.1371/journal.ppat.1002838, 22916008.
4. Bendelac A. CD1: presenting unusual antigens to unusual T lymphocytes. Science 1995, 269:185-186. 10.1126/science.7542402, 7542402.
5. Lantz O, Bendelac A. An invariant T cell receptor alpha chain is used by a unique subset of major histocompatibility complex class I-specific CD4+ and CD4-8- T cells in mice and humans. J Exp Med 1994, 180:1097-1106. 10.1084/jem.180.3.1097, 7520467.
6. Porcelli S, Yockey CE, Brenner MB, Balk SP. Analysis of T cell antigen receptor (TCR) expression by human peripheral blood CD4-8- alpha/beta T cells demonstrates preferential use of several V beta genes and an invariant TCR alpha chain. J Exp Med 1993, 178:1-16. 10.1084/jem.178.1.1, 8391057.
7. Godfrey DI, MacDonald HR, Kronenberg M, Smyth MJ, Van Kaer L. NKT cells: what's in a name?. Nat Rev Immunol 2004, 4:231-237. 10.1038/nri1309, 15039760.
8. Kawano T, Cui J, Koezuka Y, Toura I, Kaneko Y, Motoki K, Ueno H, Nakagawa R, Sato H, Kondo E, Koseki H, Taniguchi M. CD1d-restricted and TCR-mediated activation of valpha14 NKT cells by glycosylceramides. Science 1997, 278:1626-1629. 10.1126/science.278.5343.1626, 9374463.
9. Matsuda JL, Naidenko OV, Gapin L, Nakayama T, Taniguchi M, Wang CR, Koezuka Y, Kronenberg M. Tracking the response of natural killer T cells to a glycolipid antigen using CD1d tetramers. J Exp Med 2000, 192:741-754. 10.1084/jem.192.5.741, 10974039.
10. Fujii S, Shimizu K, Smith C, Bonifaz L, Steinman RM. Activation of natural killer T cells by alpha-galactosylceramide rapidly induces the full maturation of dendritic cells in vivo and thereby acts as an adjuvant for combined CD4 and CD8 T cell immunity to a coadministered protein. J Exp Med 2003, 198:267-279. 10.1084/jem.20030324, 12874260.
11. Nicol A, Nieda M, Koezuka Y, Porcelli S, Suzuki K, Tadokoro K, Durrant S, Juji T. Human invariant valpha24+ natural killer T cells activated by alpha-galactosylceramide (KRN7000) have cytotoxic anti-tumour activity through mechanisms distinct from T cells and natural killer cells. Immunology 2000, 99:229-234. 10.1046/j.1365-2567.2000.00952.x, 10692041.
12. Kitamura H, Iwakabe K, Yahata T, Nishimura S, Ohta A, Ohmi Y, Sato M, Takeda K, Okumura K, Van Kaer L, Kawano T, Taniguchi M, Nishimura T. The natural killer T (NKT) cell ligand alpha-galactosylceramide demonstrates its immunopotentiating effect by inducing interleukin (IL)-12 production by dendritic cells and IL-12 receptor expression on NKT cells. J Exp Med 1999, 189:1121-1128. 10.1084/jem.189.7.1121, 10190903.
13. Smyth MJ, Crowe NY, Pellicci DG, Kyparissoudis K, Kelly JM, Takeda K, Yagita H, Godfrey DI. Sequential production of interferon-gamma by NK1.1(+) T cells and natural killer cells is essential for the antimetastatic effect of alpha-galactosylceramide. Blood 2002, 99:1259-1266. 10.1182/blood.V99.4.1259, 11830474.
14. Liu D, Song L, Brawley VS, Robison N, Wei J, Gao X, Tian G, Margol A, Ahmed N, Asgharzadeh S, Metelitsa LS. Medulloblastoma expresses CD1d and can be targeted for immunotherapy with NKT cells. Clin Immunol 2013, 149:55-64. 10.1016/j.clim.2013.06.005, 23891738.
15. Song L, Asgharzadeh S, Salo J, Engell K, Wu HW, Sposto R, Ara T, Silverman AM, DeClerck YA, Seeger RC, Metelitsa LS. Valpha24-invariant NKT cells mediate antitumor activity via killing of tumor-associated macrophages. J Clin Invest 2009, 119:1524-1536. 10.1172/JCI37869, 19411762.
16. Uemura Y, Liu TY, Narita Y, Suzuki M, Nakatsuka R, Araki T, Matsumoto M, Iwai LK, Hirosawa N, Matsuoka Y, Murakami M, Kimura T, Hase M, Kohno H, Sasaki Y, Ichihara Y, Ishihara O, Kikuchi H, Sakamoto Y, Jiao SC, Senju S, Sonoda Y. Cytokine-dependent modification of IL-12p70 and IL-23 balance in dendritic cells by ligand activation of Valpha24 invariant NKT cells. J Immunol 2009, 183:201-208. 10.4049/jimmunol.0900873, 19542431.
17. Yang YF, Tomura M, Ono S, Hamaoka T, Fujiwara H. Requirement for IFN-gamma in IL-12 production induced by collaboration between v(alpha)14(+) NKT cells and antigen-presenting cells. Int Immunol 2000, 12:1669-1675. 10.1093/intimm/12.12.1669, 11099306.
18. Crowe NY, Smyth MJ, Godfrey DI. A critical role for natural killer T cells in immunosurveillance of methylcholanthrene-induced sarcomas. J Exp Med 2002, 196:119-127. 10.1084/jem.20020092, 12093876.
19. Godfrey DI, Kronenberg M. Going both ways: immune regulation via CD1d-dependent NKT cells. J Clin Invest 2004, 114:1379-1388. 10.1172/JCI200423594, 15545985.
20. Kaieda S, Tomi C, Oki S, Yamamura T, Miyake S. Activation of invariant natural killer T cells by synthetic glycolipid ligands suppresses autoantibody-induced arthritis. Arthritis Rheum 2007, 56:1836-1845. 10.1002/art.22714, 17530712.
21. Miellot-Gafsou A, Biton J, Bourgeois E, Herbelin A, Boissier MC, Bessis N. Early activation of invariant natural killer T cells in a rheumatoid arthritis model and application to disease treatment. Immunology 2010, 130:296-306. 10.1111/j.1365-2567.2009.03235.x, 20113367.
22. Miyamoto K, Miyake S, Yamamura T. A synthetic glycolipid prevents autoimmune encephalomyelitis by inducing TH2 bias of natural killer T cells. Nature 2001, 413:531-534. 10.1038/35097097, 11586362.
23. Hegde S, Fox L, Wang X, Gumperz JE. Autoreactive natural killer T cells: promoting immune protection and immune tolerance through varied interactions with myeloid antigen-presenting cells. Immunology 2010, 130:471-483. 10.1111/j.1365-2567.2010.03293.x, 20465577.
24. Hegde S, Lockridge JL, Becker YA, Ma S, Kenney SC, Gumperz JE. Human NKT cells direct the differentiation of myeloid APCs that regulate T cell responses via expression of programmed cell death ligands. J Autoimmun 2011, 37:28-38. 10.1016/j.jaut.2011.03.001, 21486688.
25. Pilones KA, Kawashima N, Yang AM, Babb JS, Formenti SC, Demaria S. Invariant natural killer T cells regulate breast cancer response to radiation and CTLA-4 blockade. Clin Cancer Res 2009, 15:597-606. 10.1158/1078-0432.CCR-08-1277, 19147765.
26. Boissonnas A, Scholer-Dahirel A, Simon-Blancal V, Pace L, Valet F, Kissenpfennig A, Sparwasser T, Malissen B, Fetler L, Amigorena S. Foxp3+ T cells induce perforin-dependent dendritic cell death in tumor-draining lymph nodes. Immunity 2010, 32:266-278. 10.1016/j.immuni.2009.11.015, 20137985.
27. Cui J, Shin T, Kawano T, Sato H, Kondo E, Toura I, Kaneko Y, Koseki H, Kanno M, Taniguchi M. Requirement for Valpha14 NKT cells in IL-12-mediated rejection of tumors. Science 1997, 278:1623-1626. 10.1126/science.278.5343.1623, 9374462.
28. Roark JH, Park SH, Jayawardena J, Kavita U, Shannon M, Bendelac A. CD1.1 expression by mouse antigen-presenting cells and marginal zone B cells. J Immunol 1998, 160:3121-3127. 9531266.
29. Demaria S, Kawashima N, Yang AM, Devitt ML, Babb JS, Allison JP, Formenti SC. Immune-mediated inhibition of metastases after treatment with local radiation and CTLA-4 blockade in a mouse model of breast cancer. Clin Cancer Res 2005, 11:728-734. 15701862.
30. Demaria S, Ng B, Devitt ML, Babb JS, Kawashima N, Liebes L, Formenti SC. Ionizing radiation inhibition of distant untreated tumors (abscopal effect) is immune mediated. Int J Radiat Oncol Biol Phys 2004, 58:862-870. 10.1016/j.ijrobp.2003.09.012, 14967443.
31. Yang D, Ud Din N, Browning DD, Abrams SI, Liu K. Targeting lymphotoxin beta receptor with tumor-specific T lymphocytes for tumor regression. Clin Cancer Res 2007, 13:5202-5210. 10.1158/1078-0432.CCR-07-1161, 17785576.
32. Ruocco MG, Pilones KA, Kawashima N, Cammer M, Huang J, Babb JS, Liu M, Formenti SC, Dustin ML, Demaria S. Suppressing T cell motility induced by anti-CTLA-4 monotherapy improves antitumor effects. J Clin Invest 2012, 122:3718-3730. 10.1172/JCI61931, 22945631.
33. Hurtado JC, Kim SH, Pollok KE, Lee ZH, Kwon BS. Potential role of 4-1BB in T cell activation. Comparison with the costimulatory molecule CD28. J Immunol 1995, 155:3360-3367. 7561030.
34. Shuford WW, Klussman K, Tritchler DD, Loo DT, Chalupny J, Siadak AW, Brown TJ, Emswiler J, Raecho H, Larsen CP, Pearson TC, Ledbetter JA, Aruffo A, Mittler RS. 4-1BB costimulatory signals preferentially induce CD8+ T cell proliferation and lead to the amplification in vivo of cytotoxic T cell responses. J Exp Med 1997, 186:47-55. 10.1084/jem.186.1.47, 9206996.
35. Chacon JA, Pilon-Thomas S, Sarnaik AA, Radvanyi LG. Continuous 4-1BB co-stimulatory signals for the optimal expansion of tumor-infiltrating lymphocytes for adoptive T-cell therapy. Oncoimmunology 2013, 2:e25581. 10.4161/onci.25581, 24319633.
36. Chacon JA, Wu RC, Sukhumalchandra P, Molldrem JJ, Sarnaik A, Pilon-Thomas S, Weber J, Hwu P, Radvanyi L. Co-stimulation through 4-1BB/CD137 improves the expansion and function of CD8(+) melanoma tumor-infiltrating lymphocytes for adoptive T-cell therapy. PLoS ONE 2013, 8:e60031. 10.1371/journal.pone.0060031, 23560068.
37. Daniel-Meshulam I, Horovitz-Fried M, Cohen CJ. Enhanced antitumor activity mediated by human 4-1BB-engineered T cells. Int J Cancer 2013, 133:2903-2913. 23754772.
38. Newcomb EW, Lukyanov Y, Kawashima N, Alonso-Basanta M, Wang SC, Liu M, Jure-Kunkel M, Zagzag D, Demaria S, Formenti SC. Radiotherapy enhances antitumor effect of anti-CD137 therapy in a mouse Glioma model. Radiat Res 2010, 173:426-432. 10.1667/RR1904.1, 20334514.
39. Kaur P, Nagaraja GM, Zheng H, Gizachew D, Galukande M, Krishnan S, Asea A. A mouse model for triple-negative breast cancer tumor-initiating cells (TNBC-TICs) exhibits similar aggressive phenotype to the human disease. BMC Cancer 2012, 12:120. 10.1186/1471-2407-12-120, 22452810.
40. Matsumura S, Wang B, Kawashima N, Braunstein S, Badura M, Cameron TO, Babb JS, Schneider RJ, Formenti SC, Dustin ML, Demaria S. Radiation-induced CXCL16 release by breast cancer cells attracts effector T cells. J Immunol 2008, 181:3099-3107. 10.4049/jimmunol.181.5.3099, 18713980.
41. Hayakawa Y, Rovero S, Forni G, Smyth MJ. Alpha-galactosylceramide (KRN7000) suppression of chemical- and oncogene-dependent carcinogenesis. Proc Natl Acad Sci U S A 2003, 100:9464-9469. 10.1073/pnas.1630663100, 12867593.
42. Kawano T, Cui J, Koezuka Y, Toura I, Kaneko Y, Sato H, Kondo E, Harada M, Koseki H, Nakayama T, Tanaka Y, Taniguchi M. Natural killer-like nonspecific tumor cell lysis mediated by specific ligand-activated Valpha14 NKT cells. Proc Natl Acad Sci U S A 1998, 95:5690-5693. 10.1073/pnas.95.10.5690, 9576945.
43. Metelitsa LS, Naidenko OV, Kant A, Wu HW, Loza MJ, Perussia B, Kronenberg M, Seeger RC. Human NKT cells mediate antitumor cytotoxicity directly by recognizing target cell CD1d with bound ligand or indirectly by producing IL-2 to activate NK cells. J Immunol 2001, 167:3114-3122. 10.4049/jimmunol.167.6.3114, 11544296.
44. Nakagawa R, Motoki K, Nakamura H, Ueno H, Iijima R, Yamauchi A, Tsuyuki S, Inamoto T, Koezuka Y. Antitumor activity of alpha-galactosylceramide, KRN7000, in mice with EL-4 hepatic metastasis and its cytokine production. Oncol Res 1998, 10:561-568. 10367937.
45. Fujii S, Shimizu K, Hemmi H, Steinman RM. Innate Valpha14(+) natural killer T cells mature dendritic cells, leading to strong adaptive immunity. Immunol Rev 2007, 220:183-198. 10.1111/j.1600-065X.2007.00561.x, 17979847.
46. Melief CJ. Mini-review: regulation of cytotoxic T lymphocyte responses by dendritic cells: peaceful coexistence of cross-priming and direct priming?. Eur J Immunol 2003, 33:2645-2654. 10.1002/eji.200324341, 14515248.
47. Singh-Jasuja H, Thiolat A, Ribon M, Boissier MC, Bessis N, Rammensee HG, Decker P. The mouse dendritic cell marker CD11c is down-regulated upon cell activation through Toll-like receptor triggering. Immunobiology 2013, 218:28-39. 10.1016/j.imbio.2012.01.021, 22445076.
48. Stranges PB, Watson J, Cooper CJ, Choisy-Rossi CM, Stonebraker AC, Beighton RA, Hartig H, Sundberg JP, Servick S, Kaufmann G, Fink PJ, Chervonsky AV. Elimination of antigen-presenting cells and autoreactive T cells by Fas contributes to prevention of autoimmunity. Immunity 2007, 26:629-641. 10.1016/j.immuni.2007.03.016, 17509906.
49. Hermans IF, Ritchie DS, Yang J, Roberts JM, Ronchese F. CD8+ T cell-dependent elimination of dendritic cells in vivo limits the induction of antitumor immunity. J Immunol 2000, 164:3095-3101. 10.4049/jimmunol.164.6.3095, 10706699.
50. Castriconi R, Cantoni C, Della Chiesa M, Vitale M, Marcenaro E, Conte R, Biassoni R, Bottino C, Moretta L, Moretta A. Transforming growth factor beta 1 inhibits expression of NKp30 and NKG2D receptors: consequences for the NK-mediated killing of dendritic cells. Proc Natl Acad Sci U S A 2003, 100:4120-4125. 10.1073/pnas.0730640100, 12646700.
51. Yang J, Huck SP, McHugh RS, Hermans IF, Ronchese F. Perforin-dependent elimination of dendritic cells regulates the expansion of antigen-specific CD8+ T cells in vivo. Proc Natl Acad Sci U S A 2006, 103:147-152. 10.1073/pnas.0509054103, 16373503.
52. Nicol A, Nieda M, Koezuka Y, Porcelli S, Suzuki K, Tadokoro K, Durrant S, Juji T. Dendritic cells are targets for human invariant Valpha24+ natural killer T-cell cytotoxic activity: an important immune regulatory function. Exp Hematol 2000, 28:276-282. 10.1016/S0301-472X(99)00149-6, 10720692.
53. Lee YJ, Holzapfel KL, Zhu J, Jameson SC, Hogquist KA. Steady-state production of IL-4 modulates immunity in mouse strains and is determined by lineage diversity of iNKT cells. Nat Immunol 2013, 14:1146-1154. 10.1038/ni.2731, 24097110.
54. Hegde S, Chen X, Keaton JM, Reddington F, Besra GS, Gumperz JE. NKT cells direct monocytes into a DC differentiation pathway. J Leukoc Biol 2007, 81:1224-1235. 10.1189/jlb.1206718, 17311932.
55. Hegde S, Jankowska-Gan E, Roenneburg DA, Torrealba J, Burlingham WJ, Gumperz JE. Human NKT cells promote monocyte differentiation into suppressive myeloid antigen-presenting cells. J Leukoc Biol 2009, 86:757-768. 10.1189/jlb.0209059, 19465641.
56. Giaccone G, Punt CJ, Ando Y, Ruijter R, Nishi N, Peters M, von Blomberg BM, Scheper RJ, van der Vliet HJ, van den Eertwegh AJ, Roelvink M, Beijnen J, Zwierzina H, Pinedo HM. A phase I study of the natural killer T-cell ligand alpha-galactosylceramide (KRN7000) in patients with solid tumors. Clin Cancer Res 2002, 8:3702-3709. 12473579.
57. Imataki O, Heike Y, Makiyama H, Iizuka A, Ikarashi Y, Ishida T, Wakasugi H, Takaue Y. Insufficient ex vivo expansion of Valpha24(+) natural killer T cells in malignant lymphoma patients related to the suppressed expression of CD1d molecules on CD14(+) cells. Cytotherapy 2008, 10:497-506. 10.1080/14653240802072747, 18608348.
58. Pilones KA, Aryankalayil J, Demaria S. Invariant NKT cells as novel targets for immunotherapy in solid tumors. Clin Dev Immunol 2012, 2012:720803. 10.1155/2012/720803, 23118781.
59. Terabe M, Swann J, Ambrosino E, Sinha P, Takaku S, Hayakawa Y, Godfrey DI, Ostrand-Rosenberg S, Smyth MJ, Berzofsky JA. A nonclassical non-Valpha14Jalpha18 CD1d-restricted (type II) NKT cell is sufficient for down-regulation of tumor immunosurveillance. J Exp Med 2005, 202:1627-1633. 10.1084/jem.20051381, 16365146.
60. Scheuplein F, Thariath A, Macdonald S, Truneh A, Mashal R, Schaub R. A humanized monoclonal antibody specific for invariant natural killer T (iNKT) cells for in vivo depletion. PLoS ONE 2013, 8:e76692. 10.1371/journal.pone.0076692, 24086759.
61. Aslakson CJ, Miller FR. Selective events in the metastatic process defined by analysis of the sequential dissemination of subpopulations of a mouse mammary tumor. Cancer Res 1992, 52:1399-1405. 1540948.
62. Bendelac A, Lantz O, Quimby ME, Yewdell JW, Bennink JR, Brutkiewicz RR. CD1 recognition by mouse NK1+ T lymphocytes. Science 1995, 268:863-865. 10.1126/science.7538697, 7538697.
63. Wong J, Armour E, Kazanzides P, Iordachita I, Tryggestad E, Deng H, Matinfar M, Kennedy C, Liu Z, Chan T, Gray O, Verhaegen F, McNutt T, Ford E, DeWeese TL. High-resolution, small animal radiation research platform with x-ray tomographic guidance capabilities. Int J Radiat Oncol Biol Phys 2008, 71:1591-1599. 10.1016/j.ijrobp.2008.04.025, 18640502.
64. Quezada SA, Peggs KS, Simpson TR, Shen Y, Littman DR, Allison JP. Limited tumor infiltration by activated T effector cells restricts the therapeutic activity of regulatory T cell depletion against established melanoma. J Exp Med 2008, 205:2125-2138. 10.1084/jem.20080099, 18725522.
65. Liu Y, Goff RD, Zhou D, Mattner J, Sullivan BA, Khurana A, Cantu C, Ravkov EV, Ibegbu CC, Altman JD, Teyton L, Bendelac A, Savage PB. A modified alpha-galactosyl ceramide for staining and stimulating natural killer T cells. J Immunol Methods 2006, 312:34-39. 10.1016/j.jim.2006.02.009, 16647712.
66. Slansky JE, Rattis FM, Boyd LF, Fahmy T, Jaffee EM, Schneck JP, Margulies DH, Pardoll DM. Enhanced antigen-specific antitumor immunity with altered peptide ligands that stabilize the MHC-peptide-TCR complex. Immunity 2000, 13:529-538. 10.1016/S1074-7613(00)00052-2, 11070171.