Histone deacetylase inhibitors enhance CD1d-dependent NKT cell responses to lymphoma

Cancer Immunology, Immunotherapy

Volumn 65, Issue 11, 2016, Pages 1411-1421

  Tiper, Irina V ^a   Webb, Tonya J ^a  

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

Author keywords

Cancer; CD1d; Epigenetics; HDAC inhibitors; Immunotherapy; NKT cells

Indexed keywords

CD1D ANTIGEN; HISTONE DEACETYLASE 2; INTERLEUKIN 10; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; STAT3 PROTEIN; TRICHOSTATIN A; ANTINEOPLASTIC AGENT; CD1D PROTEIN, HUMAN; GAMMA INTERFERON; HISTONE DEACETYLASE INHIBITOR; HLA ANTIGEN CLASS 2; HYDROXAMIC ACID; IL10 PROTEIN, HUMAN; STAT3 PROTEIN, HUMAN;

ANTIGEN PRESENTATION; ARTICLE; BINDING AFFINITY; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; CYTOKINE RELEASE; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; MANTLE CELL LYMPHOMA; NATURAL KILLER CELL; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; REGULATORY MECHANISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUMOR IMMUNITY; WESTERN BLOTTING; ACTIVE IMMUNOTHERAPY; DRUG EFFECTS; GENETIC EPIGENESIS; GENETICS; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; LYMPHOMA, MANTLE-CELL; METABOLISM; NATURAL KILLER T CELL; PROCEDURES; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

ANTIGEN PRESENTATION; ANTIGENS, CD1D; ANTINEOPLASTIC AGENTS; CELL LINE, TUMOR; EPIGENESIS, GENETIC; HISTOCOMPATIBILITY ANTIGENS CLASS II; HISTONE DEACETYLASE INHIBITORS; HUMANS; HYDROXAMIC ACIDS; IMMUNOTHERAPY, ACTIVE; INTERFERON-GAMMA; INTERLEUKIN-10; LYMPHOCYTE ACTIVATION; LYMPHOMA, MANTLE-CELL; NATURAL KILLER T-CELLS; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR;

EID: 84986309323     PISSN: 03407004     EISSN: 14320851     Source Type: Journal    
DOI: 10.1007/s00262-016-1900-z     Document Type: Article

References (51)

1. Hanahan D, Weinberg RA (2011) Hallmarks of cancer: the next generation. Cell 144:646–674. doi:10.1016/j.cell.2011.02.013
2. Kim R, Emi M, Tanabe K, Arihiro K (2006) Tumor-driven evolution of immunosuppressive networks during malignant progression. Cancer Res 66:5527–5536. doi:10.1158/0008-5472.can-05-4128
3. Gajewski TF, Schreiber H, Fu Y-X (2013) Innate and adaptive immune cells in the tumor microenvironment. Nat Immunol 14:1014–1022. doi:10.1038/ni.2703
4. Terabe M, Berzofsky JA (2014) The immunoregulatory role of type I and type II NKT cells in cancer and other diseases. Cancer Immunol Immunother 63:199–213. doi:10.1007/s00262-013-1509-4
5. Li J, Sun W, Subrahmanyam PB, Page C, Younger KM, Tiper IV, Frieman M, Kimball AS, Webb TJ (2014) NKT cell responses to B cell lymphoma. Med Sci 2:82–97. doi:10.3390/medsci2020082
6. Brossay L, Kronenberg M (1999) Highly conserved antigen-presenting function of CD1d molecules. Immunogenetics 50:146–151
7. Terabe M, Berzofsky JA (2014) The immunoregulatory role of type I and type II NKT cells in cancer and other diseases. Cancer Immunol Immunother 63(3):199–213. doi:10.1007/s00262-013-1509-4
8. Robertson FC, Berzofsky JA, Terabe M (2014) NKT cell networks in the regulation of tumor immunity. Front Immunol 5:543. doi:10.3389/fimmu.2014.00543
9. Vivier E, Ugolini S, Blaise D, Chabannon C, Brossay L (2012) Targeting natural killer cells and natural killer T cells in cancer. Nat Rev Immunol 12:239–252
10. Sun W, Subrahmanyam PB, East JE, Webb TJ (2012) Connecting the dots: artificial antigen presenting cell-mediated modulation of natural killer T cells. J Interferon Cytokine Res 32:505–516. doi:10.1089/jir.2012.0045
11. Tahir SM, Cheng O, Shaulov A, Koezuka Y, Bubley GJ, Wilson SB, Balk SP, Exley MA (2001) Loss of IFN-gamma production by invariant NK T cells in advanced cancer. J Immunol. 167:4046–4050
12. Molling JW, Kolgen W, van der Vliet HJ et al (2005) Peripheral blood IFN-gamma-secreting Valpha24 + Vbeta11 + NKT cell numbers are decreased in cancer patients independent of tumor type or tumor load. Int J Cancer 116:87–93. doi:10.1002/ijc.20998
13. Shimizu K, Hidaka M, Kadowaki N et al (2006) Evaluation of the function of human invariant NKT cells from cancer patients using alpha-galactosylceramide-loaded murine dendritic cells. J Immunol. 177:3484–3492
14. Igney FH, Krammer PH (2002) Immune escape of tumors: apoptosis resistance and tumor counterattack. J Leukoc Biol 71:907–920
15. Romero JM, Jimenez P, Cabrera T, Cozar JM, Pedrinaci S, Tallada M, Garrido F, Ruiz-Cabello F (2005) Coordinated downregulation of the antigen presentation machinery and HLA class I/beta2-microglobulin complex is responsible for HLA-ABC loss in bladder cancer. Int J Cancer 113:605–610. doi:10.1002/ijc.20499
16. Bubenik J (2004) MHC class I down-regulation: tumour escape from immune surveillance? (review). Int J Oncol 25:487–491
17. Khanna R (1998) Tumour surveillance: missing peptides and MHC molecules. Immunol Cell Biol 76:20–26. doi:10.1046/j.1440-1711.1998.00717.x
18. Gunnellini M, Falchi L (2012) Therapeutic activity of Lenalidomide in mantle cell lymphoma and indolent non-Hodgkin’s lymphomas. Adv Hematol. 2012:523842. doi:10.1155/2012/523842
19. Dreyling M, Ferrero S, Hermine O (2014) How to manage mantle cell lymphoma. Leukemia 28:2117–2130. doi:10.1038/leu.2014.171
20. Pérez-Galán P, Dreyling M, Wiestner A (2011) Mantle cell lymphoma: biology, pathogenesis, and the molecular basis of treatment in the genomic era. Blood 117:26–38. doi:10.1182/blood-2010-04-189977
21. Cheng F, Wang H, Horna P et al (2012) Stat3 inhibition augments the immunogenicity of B-cell lymphoma cells, leading to effective antitumor immunity. Cancer Res 72:4440–4448. doi:10.1158/0008-5472.can-11-3619
22. Lu K, Chen N, Zhou XX, Ge XL, Feng LL, Li PP, Li XY, Geng LY, Wang X (2015) The STAT3 inhibitor WP1066 synergizes with vorinostat to induce apoptosis of mantle cell lymphoma cells. Biochem Biophys Res Commun 464:292–298. doi:10.1016/j.bbrc.2015.06.145
23. Aggarwal BB, Kunnumakkara AB, Harikumar KB, Gupta SR, Tharakan ST, Koca C, Dey S, Sung B (2009) Signal transducer and activator of transcription-3, inflammation, and cancer: how intimate is the relationship? Ann N Y Acad Sci 1171:59–76. doi:10.1111/j.1749-6632.2009.04911.x
24. Chang Q, Bournazou E, Sansone P et al (2013) The IL-6/JAK/Stat3 feed-forward loop drives tumorigenesis and metastasis. Neoplasia 15:848–862
25. Carpenter RL, Lo HW (2014) STAT3 Target genes relevant to human cancers. Cancers (Basel). 6:897–925. doi:10.3390/cancers6020897
26. West AC, Johnstone RW (2014) New and emerging HDAC inhibitors for cancer treatment. J Clin Invest 124:30–39. doi:10.1172/jci69738
27. Marks PA (2010) Histone deacetylase inhibitors: a chemical genetics approach to understanding cellular functions. Biochim Biophys Acta 1799:717–725. doi:10.1016/j.bbagrm.2010.05.008
28. Woan KV, Sahakian E, Sotomayor EM, Seto E, Villagra A (2012) Modulation of antigen-presenting cells by HDAC inhibitors: implications in autoimmunity and cancer. Immunol Cell Biol 90:55–65. doi:10.1038/icb.2011.96
29. Prince HM, Bishton MJ, Harrison SJ (2009) Clinical studies of histone deacetylase inhibitors. Clin Cancer Res 15:3958–3969. doi:10.1158/1078-0432.ccr-08-2785
30. Ray S, Lee C, Hou T, Boldogh I, Brasier AR (2008) Requirement of histone deacetylase1 (HDAC1) in signal transducer and activator of transcription 3 (STAT3) nucleocytoplasmic distribution. Nucleic Acids Res 36:4510–4520. doi:10.1093/nar/gkn419
31. Yu H, Pardoll D, Jove R (2009) STATs in cancer inflammation and immunity: a leading role for STAT3. Nat Rev Cancer 9:798–809
32. Ostrand-Rosenberg S (2008) Immune surveillance: a balance between protumor and antitumor immunity. Curr Opin Genet Dev 18:11–18. doi:10.1016/j.gde.2007.12.007
33. Brutkiewicz RR, Bennink JR, Yewdell JW, Bendelac A (1995) TAP-independent, beta 2-microglobulin-dependent surface expression of functional mouse CD1.1. J Exp Med 182:1913–1919
34. Roberts TJ, Sriram V, Spence PM, Gui M, Hayakawa K, Bacik I, Bennink JR, Yewdell JW, Brutkiewicz RR (2002) Recycling CD1d1 molecules present endogenous antigens processed in an endocytic compartment to NKT cells. J Immunol. 168:5409–5414
35. Amin HM, McDonnell TJ, Medeiros LJ, Rassidakis GZ, Leventaki V, O’Connor SL, Keating MJ, Lai R (2003) Characterization of 4 mantle cell lymphoma cell lines. Arch Pathol Lab Med 127:424–431. doi:10.1043/0003-9985(2003)127<0424:comclc>2.0.co;2
36. East JE, Sun W, Webb TJ (2012) Artificial antigen presenting cell (aAPC) mediated activation and expansion of natural killer T cells. J Vis Exp. 70 doi:10.3791/4333
37. Chen QY, Jackson N (2004) Human CD1D gene has TATA boxless dual promoters: an SP1-binding element determines the function of the proximal promoter. J Immunol. 172:5512–5521
38. Yang PM, Lin PJ, Chen CC (2012) CD1d induction in solid tumor cells by histone deacetylase inhibitors through inhibition of HDAC1/2 and activation of Sp1. Epigenetics 7:390–399. doi:10.4161/epi.19373
39. Batalo M, Bose P, Holkova B, Grant S (2014) Targeting mantle cell lymphoma with a strategy of combined proteasome and histone deacetylase inhibition. In: Dou PQ (ed) Resistance to proteasome inhibitors in cancer: molecular mechanisms and strategies to overcome resistance. Springer International Publishing, Cham, pp 149–179
40. Mittal SK, Roche PA (2015) Suppression of antigen presentation by IL-10. Curr Opin Immunol 34:22–27. doi:10.1016/j.coi.2014.12.009
41. Alvarez-Breckenridge CA, Yu J, Price R et al (2012) The histone deacetylase inhibitor valproic acid lessens NK cell action against oncolytic virus-infected glioblastoma cells by inhibition of STAT5/T-BET signaling and generation of gamma interferon. J Virol 86:4566–4577. doi:10.1128/jvi.05545-11
42. Chen QY, Zhang T, Pincus SH, Wu S, Ricks D, Liu D, Sun Z, Maclaren N, Lan MS (2010) Human CD1D gene expression is regulated by LEF-1 through distal promoter regulatory elements. J Immunol 184:5047–5054. doi:10.4049/jimmunol.0901912
43. Magner WJ, Kazim AL, Stewart C, Romano MA, Catalano G, Grande C, Keiser N, Santaniello F, Tomasi TB (2000) Activation of MHC class I, II, and CD40 gene expression by histone deacetylase inhibitors. J Immunol 165:7017–7024
44. Khan AN, Gregorie CJ, Tomasi TB (2008) Histone deacetylase inhibitors induce TAP, LMP, Tapasin genes and MHC class I antigen presentation by melanoma cells. Cancer Immunol Immunother 57:647–654. doi:10.1007/s00262-007-0402-4
45. Manning J, Indrova M, Lubyova B et al (2008) Induction of MHC class I molecule cell surface expression and epigenetic activation of antigen-processing machinery components in a murine model for human papilloma virus 16-associated tumours. Immunology 123:218–227. doi:10.1111/j.1365-2567.2007.02689.x
46. Song W, Tai YT, Tian Z, Hideshima T, Chauhan D, Nanjappa P, Exley MA, Anderson KC, Munshi NC (2011) HDAC inhibition by LBH589 affects the phenotype and function of human myeloid dendritic cells. Leukemia 25:161–168. doi:10.1038/leu.2010.244
47. Frikeche J, Simon T, Brissot E, Gregoire M, Gaugler B, Mohty M (2012) Impact of valproic acid on dendritic cells function. Immunobiology 217:704–710. doi:10.1016/j.imbio.2011.11.010
48. Frikeche J, Peric Z, Brissot E, Gregoire M, Gaugler B, Mohty M (2012) Impact of HDAC inhibitors on dendritic cell functions. Exp Hematol 40:783–791. doi:10.1016/j.exphem.2012.06.008
49. Scuto A, Kirschbaum M, Buettner R, Kujawski M, Cermak JM, Atadja P, Jove R (2013) SIRT1 activation enhances HDAC inhibition-mediated upregulation of GADD45G by repressing the binding of NF-kappaB/STAT3 complex to its promoter in malignant lymphoid cells. Cell Death Dis 4:e635. doi:10.1038/cddis.2013.159
50. Iyer AK, Liu J, Gallo RM, Kaplan MH, Brutkiewicz RR (2015) STAT3 promotes CD1d-mediated lipid antigen presentation by regulating a critical gene in glycosphingolipid biosynthesis. Immunology 146:444–455. doi:10.1111/imm.12521
51. Ribas A, Wolchok JD (2013) Combining cancer immunotherapy and targeted therapy. Curr Opin Immunol 25:291–296. doi:10.1016/j.coi.2013.02.011