Epigenetic suppression of the antitumor cytotoxicity of NK cells by histone deacetylase inhibitor valproic acid

American Journal of Cancer Research

Volumn 6, Issue 3, 2016, Pages 600-614

  Shi, Xiumin ^a   Li, Min ^a   Cui, Meizi ^a   Niu, Chao ^a   Xu, Jianting ^a   Zhou, Lei ^a   Li, Wei ^a   Gao, Yushun ^c   Kong, Weisheng ^d   Cui, Jiuwei ^a   Hu, Jifan ^a,b   Jin, Haofan ^a  

^a JILIN UNIVERSITY   (China)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c CANCER HOSPITAL   (China)

^d BASO Cell Science and Technology Co Ltd   (China)

Author keywords

Apoptosis; DNA methylation; Epigenetics; Expression; Histone methylation; NK cell; Tumor killing; Valproic acid

Indexed keywords

GAMMA INTERFERON; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; NATURAL KILLER CELL RECEPTOR NKG2D; PROGRAMMED DEATH 1 LIGAND 1; PROGRAMMED DEATH 1 RECEPTOR; STAT5 PROTEIN; VALPROIC ACID;

ADULT; AGED; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CELL VIABILITY; CLINICAL ARTICLE; CONTROLLED STUDY; CPG ISLAND; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DEGRANULATION; DNA METHYLATION; DOWN REGULATION; FEMALE; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; IN VITRO STUDY; MALE; NATURAL KILLER CELL MEDIATED CYTOTOXICITY; NKG2D GENE; NUCLEAR REPROGRAMMING; UPREGULATION;

EID: 84992310439     PISSN: None     EISSN: 21566976     Source Type: Journal    
DOI: None     Document Type: Article

References (63)

1. Campbell KS and Hasegawa J. Natural killer cell biology: an update and future directions. J Allergy Clin Immunol 2013; 132: 536-544.
2. Childs RW and Carlsten M. Therapeutic approaches to enhance natural killer cell cytotoxicity against cancer: the force awakens. Nat Rev Drug Discov 2015; 14: 487-498.
3. Klingemann H. Challenges of cancer therapy with natural killer cells. Cytotherapy 2015; 17: 245-249.
4. Tian Z, Gershwin ME and Zhang C. Regulatory NK cells in autoimmune disease. J Autoimmun 2012; 39: 206-215.
5. Hodny Z, Hubackova S and Bartek J. Cytokineinduced 'bystander' senescence in DDR and immuno-surveillance. Oncotarget 2013; 4: 1552-1553.
6. Locatelli F, Moretta F, Brescia L and Merli P. Natural killer cells in the treatment of high-risk acute leukaemia. Semin Immunol 2014; 26: 173-179.
7. Jewett A and Tseng HC. Tumor induced inactivation of natural killer cell cytotoxic function; implication in growth, expansion and differentiation of cancer stem cells. J Cancer 2011; 2: 443-457.
8. Lim O, Jung MY, Hwang YK and Shin EC. Present and Future of Allogeneic Natural Killer Cell Therapy. Front Immunol 2015; 6: 286.
9. Tasian SK and Gardner RA. CD19-redirected chimeric antigen receptor-modified T cells: a promising immunotherapy for children and adults with B-cell acute lymphoblastic leukemia (ALL). Ther Adv Hematol 2015; 6: 228- 241.
10. Grupp SA, Kalos M, Barrett D, Aplenc R, Porter DL, Rheingold SR, Teachey DT, Chew A, Hauck B, Wright JF, Milone MC, Levine BL and June CH. Chimeric antigen receptor- modified T cells for acute lymphoid leukemia. N Engl J Med 2013; 368: 1509-1518.
11. Kochenderfer JN, Dudley ME, Carpenter RO, Kassim SH, Rose JJ, Telford WG, Hakim FT, Halverson DC, Fowler DH, Hardy NM, Mato AR,Hickstein DD, Gea-Banacloche JC, Pavletic SZ, Sportes C, Maric I, Feldman SA, Hansen BG, Wilder JS, Blacklock-Schuver B, Jena B, Bishop MR, Gress RE and Rosenberg SA. Donor-derived CD19- targeted T cells cause regression of malignancy persisting after allogeneic hematopoietic stem cell transplantation. Blood 2013; 122: 4129-4139.
12. Magee MS and Snook AE. Challenges to chimeric antigen receptor (CAR)-T cell therapy for cancer. Discov Med 2014; 18: 265-271.
13. Yasmin R, Siraj S, Hassan A, Khan AR, Abbasi R and Ahmad N. Epigenetic regulation of inflammatory cytokines and associated genes in human malignancies. Mediators Inflamm 2015; 2015: 201703.
14. Hasim A, Abudula M, Aimiduo R, Ma JQ, Jiao Z, Akula G, Wang T and Abudula A. Post-transcriptional and epigenetic regulation of antigen processing machinery (APM) components and HLA-I in cervical cancers from Uighur women. PLoS One 2012; 7: e44952.
15. Tertipis N, Haeggblom L, Grun N, Nordfors C, Nasman A, Dalianis T and Ramqvist T. Reduced Expression of the Antigen Processing Machinery Components TAP2, LMP2, and LMP7 in Tonsillar and Base of Tongue Cancer and Implications for Clinical Outcome. Transl Oncol 2015; 8: 10-17.
16. Wang LX, Mei ZY, Zhou JH, Yao YS, Li YH, Xu YH, Li JX, Gao XN, Zhou MH, Jiang MM, Gao L, Ding Y, Lu XC, Shi JL, Luo XF, Wang J, Wang LL, Qu C, Bai XF and Yu L. Low dose decitabine treatment induces CD80 expression in cancer cells and stimulates tumor specific cytotoxic T lymphocyte responses. PLoS One 2013; 8: e62924.
17. Dubovsky JA, Powers JJ, Gao Y, Mariusso LF, Sotomayor EM and Pinilla-Ibarz JA. Epigenetic repolarization of T lymphocytes from chronic lymphocytic leukemia patients using 5-aza-2'- deoxycytidine. Leuk Res 2011; 35: 1193- 1199.
18. Wernig M, Lengner CJ, Hanna J, Lodato MA, Steine E, Foreman R, Staerk J, Markoulaki S and Jaenisch R. A drug-inducible transgenic system for direct reprogramming of multiple somatic cell types. Nat Biotechnol 2008; 26: 916-924.
19. Esteban MA, Wang T, Qin B, Yang J, Qin D, Cai J, Li W, Weng Z, Chen J, Ni S, Chen K, Li Y, Liu X, Xu J, Zhang S, Li F, He W, Labuda K, Song Y, Peterbauer A, Wolbank S, Redl H, Zhong M, Cai D, Zeng L and Pei D. Vitamin C enhances the generation of mouse and human induced pluripotent stem cells. Cell Stem Cell 2010; 6: 71- 79.
20. Huangfu D, Osafune K, Maehr R, Guo W, Eijkelenboom A, Chen S, Muhlestein W and Melton DA. Induction of pluripotent stem cells from primary human fibroblasts with only Oct4 and Sox2. Nat Biotechnol 2008; 26: 1269- 1275.
21. Chen M, Zhang H, Wu J, Xu L, Xu D, Sun J, He Y, Zhou X, Wang Z, Wu L, Xu S, Wang J, Jiang S, Hoffman AR, Hu X, Hu J and Li T. Promotion of the induction of cell pluripotency through metabolic remodeling by thyroid hormone triiodothyronine- activated PI3K/AKT signal pathway. Biomaterials 2012; 33: 5514-5523.
22. Cui J, Li L, Wang C, Jin H, Yao C, Wang Y, Li D, Tian H, Niu C, Wang G, Han W, Xu J, Chen J and Li W. Combined cellular immunotherapy and chemotherapy improves clinical outcome in patients with gastric carcinoma. Cytotherapy 2015; 17: 979-988.
23. Kang L, Sun J, Wen X, Cui J, Wang G, Hoffman AR, Hu JF and Li W. Aberrant allele- switch imprinting of a novel IGF1R intragenic antisense non-coding RNA in breast cancers. Eur J Cancer 2015; 51: 260-270.
24. Goldstraw P, Crowley J, Chansky K, Giroux DJ, Groome PA, Rami-Porta R, Postmus PE, Rusch V, Sobin L; International Association for the Study of Lung Cancer International Staging Committee; Participating Institutions. The IASLC Lung Cancer Staging Project: proposals for the revision of the TNM stage groupings in the forthcoming (seventh) edition of the TNM Classification of malignant tumours. J Thorac Oncol 2007; 2: 706-714.
25. Pallis AG, Shepherd FA, Lacombe D and Gridelli C. Treatment of small-cell lung cancer in elderly patients. Cancer 2010; 116: 1192-1200.
26. Neri S, Mariani E, Meneghetti A, Cattini L and Facchini A. Calcein-acetyoxymethyl cytotoxicity assay: standardization of a method allowing additional analyses on recovered effector cells and supernatants. Clin Diagn Lab Immunol 2001; 8: 1131-1135.
27. Sun J, Li W, Sun Y, Yu D, Wen X, Wang H, Cui J, Wang G, Hoffman AR and Hu JF. A novel antisense long noncoding RNA within the IGF1R gene locus is imprinted in hematopoietic malignancies. Nucleic Acids Res 2014; 42: 9588- 9601.
28. Zhang H, Niu B, Hu JF, Wang H, Ling J, Qian G, Ge S and Hoffman AR. Interruption of intrachromosomal looping by CTCF decoy proteins abrogates genomic imprinting of human insulin- like growth factor II. J Cell Biol 2011; 193: 475-487.
29. Li T, Hu JF, Qiu X, Ling J, Chen H, Wang S, Hou A, Vu TH and Hoffman AR. CTCF regulates allelic expression of Igf2 by orchestrating a promoter- polycomb repressive complex-2 intrachromosomal loop. Mol Cell Biol 2008; 28: 6473-6482.
30. Zhang S, Zhong B, Chen M, Yang G, Li Y, Wang H, Wang G, Li W, Cui J, Hoffman AR and Hu J. Epigenetic reprogramming reverses the malignant epigenotype of the MMP/TIMP axis genes in tumor cells. Int J Cancer 2014; 134: 1583- 1594.
31. Li T, Chen H, Li W, Cui J, Wang G, Hu X, Hoffman AR and Hu J. Promoter histone H3K27 methylation in the control of IGF2 imprinting in human tumor cell lines. Hum Mol Genet 2014; 23: 117-128.
32. Zhang H, Jiao W, Sun L, Fan J, Chen M, Wang H, Xu X, Shen A, Li T, Niu B, Ge S, Li W, Cui J, Wang G, Sun J, Fan X, Hu X, Mrsny RJ, Hoffman AR and Hu JF. Intrachromosomal Looping Is Required for Activation of Endogenous Pluripotency Genes during Reprogramming. Cell Stem Cell 2013; 13: 30-35.
33. Serrano A, Castro-Vega I and Redondo M. Role of gene methylation in antitumor immune response: implication for tumor progression. Cancers (Basel) 2011; 3: 1672-1690.
34. Sola C, Andre P, Lemmers C, Fuseri N, Bonnafous C, Blery M, Wagtmann NR, Romagne F, Vivier E and Ugolini S. Genetic and antibodymediated reprogramming of natural killer cell missing-self recognition in vivo. Proc Natl Acad Sci U S A 2009; 106: 12879-12884.
35. Payne KK, Zoon CK, Wan W, Marlar K, Keim RC, Kenari MN, Kazim AL, Bear HD and Manjili MH. Peripheral blood mononuclear cells of patients with breast cancer can be reprogrammed to enhance anti-HER-2/neu reactivity and overcome myeloid-derived suppressor cells. Breast Cancer Res Treat 2013; 142: 45- 57.
36. Chen J, Guo L, Zhang L, Wu H, Yang J, Liu H, Wang X, Hu X, Gu T, Zhou Z, Liu J, Liu J, Wu H, Mao SQ, Mo K, Li Y, Lai K, Qi J, Yao H, Pan G, Xu GL and Pei D. Vitamin C modulates TET1 function during somatic cell reprogramming. Nat Genet 2013; 45: 1504-1509.
37. Betts MR, Brenchley JM, Price DA, De Rosa SC, Douek DC, Roederer M and Koup RA. Sensitive and viable identification of antigen-specific CD8+ T cells by a flow cytometric assay for degranulation. J Immunol Methods 2003; 281: 65-78.
38. Alter G, Malenfant JM and Altfeld M. CD107a as a functional marker for the identification of natural killer cell activity. J Immunol Methods 2004; 294: 15-22.
39. Pardoll DM. The blockade of immune checkpoints in cancer immunotherapy. Nat Rev Cancer 2012; 12: 252-264.
40. Muenst S, Soysal SD, Tzankov A and Hoeller S. The PD-1/PD-L1 pathway: biological background and clinical relevance of an emerging treatment target in immunotherapy. Expert Opin Ther Targets 2015; 19: 201-211.
41. Sakamoto N, Ishikawa T, Kokura S, Okayama T, Oka K, Ideno M, Sakai F, Kato A, Tanabe M, Enoki T, Mineno J, Naito Y, Itoh Y and Yoshikawa T. Phase I clinical trial of autologous NK cell therapy using novel expansion method in patients with advanced digestive cancer. J Transl Med 2015; 13: 277.
42. Parkhurst MR, Riley JP, Dudley ME and Rosenberg SA. Adoptive transfer of autologous natural killer cells leads to high levels of circulating natural killer cells but does not mediate tumor regression. Clin Cancer Res 2011; 17: 6287- 6297.
43. Slingerland M, Guchelaar HJ and Gelderblom H. Histone deacetylase inhibitors: an overview of the clinical studies in solid tumors. Anticancer Drugs 2014; 25: 140-149.
44. Juo YY, Gong XJ, Mishra A, Cui X, Baylin SB, Azad NS and Ahuja N. Epigenetic therapy for solid tumors: from bench science to clinical trials. Epigenomics 2015; 7: 215-235.
45. Grant S and Dai Y. Histone deacetylase inhibitors and rational combination therapies. Adv Cancer Res 2012; 116: 199-237.
46. Alvarez-Breckenridge CA, Yu J, Price R, Wei M, Wang Y, Nowicki MO, Ha YP, Bergin S, Hwang C, Fernandez SA, Kaur B, Caligiuri MA and Chiocca EA. 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 2012; 86: 4566-4577.
47. Ogbomo H, Michaelis M, Kreuter J, Doerr HW and Cinatl J Jr. Histone deacetylase inhibitors suppress natural killer cell cytolytic activity. FEBS Lett 2007; 581: 1317-1322.
48. Rossi LE, Avila DE, Spallanzani RG, Ziblat A, Fuertes MB, Lapyckyj L, Croci DO, Rabinovich GA, Domaica CI and Zwirner NW. Histone deacetylase inhibitors impair NK cell viability and effector functions through inhibition of activation and receptor expression. J Leukoc Biol 2012; 91: 321-331.
49. Kelly-Sell MJ, Kim YH, Straus S, Benoit B, Harrison C, Sutherland K, Armstrong R, Weng WK, Showe LC, Wysocka M and Rook AH. The histone deacetylase inhibitor, romidepsin, suppresses cellular immune functions of cutaneous T-cell lymphoma patients. Am J Hematol 2012; 87: 354-360.
50. Ning ZQ, Li ZB, Newman MJ, Shan S, Wang XH, Pan DS, Zhang J, Dong M, Du X and Lu XP. Chidamide (CS055/HBI-8000): a new histone deacetylase inhibitor of the benzamide class with antitumor activity and the ability to enhance immune cell-mediated tumor cell cytotoxicity. Cancer Chemother Pharmacol 2012; 69: 901-909.
51. Zhu S, Denman CJ, Cobanoglu ZS, Kiany S, Lau CC, Gottschalk SM, Hughes DP, Kleinerman ES and Lee DA. The narrow-spectrum HDAC inhibitor entinostat enhances NKG2D expression without NK cell toxicity, leading to enhanced recognition of cancer cells. Pharm Res 2015; 32: 779-792.
52. Ray A, Das DS, Song Y, Richardson P, Munshi NC, Chauhan D and Anderson KC. Targeting PD1-PDL1 immune checkpoint in plasmacytoid dendritic cell interactions withT cells, natural killer cells and multiple myeloma cells. Leukemia 2015; 29: 1441-1444.
53. Yokosuka T, Takamatsu M, Kobayashi-Imanishi W, Hashimoto-Tane A, Azuma M and Saito T. Programmed cell death 1 forms negative costimulatory microclusters that directly inhibit T cell receptor signaling by recruiting phosphatase SHP2. J Exp Med 2012; 209: 1201-1217.
54. Barber DL, Wherry EJ, Masopust D, Zhu B, Allison JP, Sharpe AH, Freeman GJ and Ahmed R. Restoring function in exhausted CD8 T cells during chronic viral infection. Nature 2006; 439: 682-687.
55. Golden-Mason L, Palmer B, Klarquist J, Mengshol JA, Castelblanco N and Rosen HR. Upregulation of PD-1 expression on circulating and intrahepatic hepatitis C virus-specific CD8+ T cells associated with reversible immune dysfunction. J Virol 2007; 81: 9249- 9258.
56. Niezgoda A, Niezgoda P and Czajkowski R. Novel Approaches to Treatment of Advanced Melanoma: A Review on Targeted Therapy and Immunotherapy. Biomed Res Int 2015; 2015: 851387.
57. Merelli B, Massi D, Cattaneo L and Mandala M. Targeting the PD1/PD-L1 axis in melanoma: biological rationale, clinical challenges and opportunities. Crit Rev Oncol Hematol 2014; 89: 140-165.
58. Carapito R and Bahram S. Genetics, genomics, and evolutionary biology of NKG2D ligands. Immunol Rev 2015; 267: 88-116.
59. Fujisaki H, Kakuda H, Shimasaki N, Imai C, Ma J, Lockey T, Eldridge P, Leung WH and Campana D. Expansion of highly cytotoxic human natural killer cells for cancer cell therapy. Cancer Res 2009; 69: 4010-4017.
60. Lanier LL. NKG2D Receptor and Its Ligands in Host Defense. Cancer Immunol Res 2015; 3: 575-582.
61. Hublitz P, Albert M and Peters AH. Mechanisms of transcriptional repression by histone lysine methylation. Int J Dev Biol 2009; 53: 335-354.
62. Kimura H. Histone modifications for human epigenome analysis. J Hum Genet 2013; 58: 439-445.
63. Nakayama J, Rice JC, Strahl BD, Allis CD and Grewal SI. Role of histone H3 lysine 9 methylation in epigenetic control of heterochromatin assembly. Science 2001; 292: 110-113.