Epigenetic regulation of major histocompatibility complexes in gastrointestinal malignancies and the potential for clinical interception.
Cancer immune evasion
Epigenetic regulation
Gastrointestinal cancer
Immunotherapy
MHC
Journal
Clinical epigenetics
ISSN: 1868-7083
Titre abrégé: Clin Epigenetics
Pays: Germany
ID NLM: 101516977
Informations de publication
Date de publication:
24 Jun 2024
24 Jun 2024
Historique:
received:
10
11
2023
accepted:
18
06
2024
medline:
25
6
2024
pubmed:
25
6
2024
entrez:
24
6
2024
Statut:
epublish
Résumé
Gastrointestinal malignancies encompass a diverse group of cancers that pose significant challenges to global health. The major histocompatibility complex (MHC) plays a pivotal role in immune surveillance, orchestrating the recognition and elimination of tumor cells by the immune system. However, the intricate regulation of MHC gene expression is susceptible to dynamic epigenetic modification, which can influence functionality and pathological outcomes. By understanding the epigenetic alterations that drive MHC downregulation, insights are gained into the molecular mechanisms underlying immune escape, tumor progression, and immunotherapy resistance. This systematic review examines the current literature on epigenetic mechanisms that contribute to MHC deregulation in esophageal, gastric, pancreatic, hepatic and colorectal malignancies. Potential clinical implications are discussed of targeting aberrant epigenetic modifications to restore MHC expression and 0 the effectiveness of immunotherapeutic interventions. The integration of epigenetic-targeted therapies with immunotherapies holds great potential for improving clinical outcomes in patients with gastrointestinal malignancies and represents a compelling avenue for future research and therapeutic development.
Sections du résumé
BACKGROUND
BACKGROUND
Gastrointestinal malignancies encompass a diverse group of cancers that pose significant challenges to global health. The major histocompatibility complex (MHC) plays a pivotal role in immune surveillance, orchestrating the recognition and elimination of tumor cells by the immune system. However, the intricate regulation of MHC gene expression is susceptible to dynamic epigenetic modification, which can influence functionality and pathological outcomes.
MAIN BODY
METHODS
By understanding the epigenetic alterations that drive MHC downregulation, insights are gained into the molecular mechanisms underlying immune escape, tumor progression, and immunotherapy resistance. This systematic review examines the current literature on epigenetic mechanisms that contribute to MHC deregulation in esophageal, gastric, pancreatic, hepatic and colorectal malignancies. Potential clinical implications are discussed of targeting aberrant epigenetic modifications to restore MHC expression and 0 the effectiveness of immunotherapeutic interventions.
CONCLUSION
CONCLUSIONS
The integration of epigenetic-targeted therapies with immunotherapies holds great potential for improving clinical outcomes in patients with gastrointestinal malignancies and represents a compelling avenue for future research and therapeutic development.
Identifiants
pubmed: 38915093
doi: 10.1186/s13148-024-01698-8
pii: 10.1186/s13148-024-01698-8
doi:
Types de publication
Journal Article
Systematic Review
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
83Subventions
Organisme : NIH HHS
ID : CA122959
Pays : United States
Informations de copyright
© 2024. The Author(s).
Références
Zahnow CA, Topper M, Stone M, Murray-Stewart T, Li H, Baylin SB, et al. Inhibitors of DNA methylation, histone deacetylation, and histone demethylation: a perfect combination for cancer therapy. Adv Cancer Res. 2016;130:55–111.
pubmed: 27037751
doi: 10.1016/bs.acr.2016.01.007
Kobayashi KS, van den Elsen PJ. NLRC5: a key regulator of MHC class I-dependent immune responses. Nat Rev Immunol. 2012;12(12):813–20.
pubmed: 23175229
doi: 10.1038/nri3339
Wong CC, Li W, Chan B, Yu J. Epigenomic biomarkers for prognostication and diagnosis of gastrointestinal cancers. Semin Cancer Biol. 2019;55:90–105.
pubmed: 29665409
doi: 10.1016/j.semcancer.2018.04.002
Løvig T, Andersen SN, Thorstensen L, Diep CB, Meling GI, Lothe RA, et al. Strong HLA-DR expression in microsatellite stable carcinomas of the large bowel is associated with good prognosis. Br J Cancer. 2002;87(7):756–62.
pubmed: 12232760
pmcid: 2364272
doi: 10.1038/sj.bjc.6600507
Cabrera CM, Jiménez P, Cabrera T, Esparza C, Ruiz-Cabello F, Garrido F. Total loss of MHC class I in colorectal tumors can be explained by two molecular pathways: beta2-microglobulin inactivation in MSI-positive tumors and LMP7/TAP2 downregulation in MSI-negative tumors. Tissue Antigens. 2003;61(3):211–9.
pubmed: 12694570
doi: 10.1034/j.1399-0039.2003.00020.x
Reith W, Satola S, Sanchez CH, Amaldi I, Lisowska-Grospierre B, Griscelli C, et al. Congenital immunodeficiency with a regulatory defect in MHC class II gene expression lacks a specific HLA-DR promoter binding protein. RF-X Cell. 1988;53(6):897–906.
pubmed: 3133120
Jongsma MLM, Guarda G, Spaapen RM. The regulatory network behind MHC class I expression. Mol Immunol. 2019;113:16–21.
pubmed: 29224918
doi: 10.1016/j.molimm.2017.12.005
Masternak K, Barras E, Zufferey M, Conrad B, Corthals G, Aebersold R, et al. A gene encoding a novel RFX-associated transactivator is mutated in the majority of MHC class II deficiency patients. Nat Genet. 1998;20(3):273–7.
pubmed: 9806546
doi: 10.1038/3081
Nagarajan UM, Louis-Plence P, DeSandro A, Nilsen R, Bushey A, Boss JM. RFX-B is the gene responsible for the most common cause of the bare lymphocyte syndrome, an MHC class II immunodeficiency. Immunity. 1999;10(2):153–62.
pubmed: 10072068
doi: 10.1016/S1074-7613(00)80016-3
Durand B, Sperisen P, Emery P, Barras E, Zufferey M, Mach B, et al. RFXAP, a novel subunit of the RFX DNA binding complex is mutated in MHC class II deficiency. EMBO J. 1997;16(5):1045–55.
pubmed: 9118943
pmcid: 1169704
doi: 10.1093/emboj/16.5.1045
Masternak K, Muhlethaler-Mottet A, Villard J, Zufferey M, Steimle V, Reith W. CIITA is a transcriptional coactivator that is recruited to MHC class II promoters by multiple synergistic interactions with an enhanceosome complex. Genes Dev. 2000;14(9):1156–66.
pubmed: 10809673
pmcid: 316580
doi: 10.1101/gad.14.9.1156
Moreno CS, Emery P, West JE, Durand B, Reith W, Mach B, et al. Purified X2 binding protein (X2BP) cooperatively binds the class II MHC X box region in the presence of purified RFX, the X box factor deficient in the bare lymphocyte syndrome. J Immunol. 1995;155(9):4313–21.
pubmed: 7594590
doi: 10.4049/jimmunol.155.9.4313
Jabrane-Ferrat N, Nekrep N, Tosi G, Esserman L, Peterlin BM. MHC class II enhanceosome: how is the class II transactivator recruited to DNA-bound activators? Int Immunol. 2003;15(4):467–75.
pubmed: 12663676
doi: 10.1093/intimm/dxg048
van den Elsen PJ. Expression regulation of major histocompatibility complex class I and class II encoding genes. Front Immunol. 2011;2:48.
pubmed: 22566838
pmcid: 3342053
Ludigs K, Seguín-Estévez Q, Lemeille S, Ferrero I, Rota G, Chelbi S, et al. NLRC5 exclusively transactivates MHC class I and related genes through a distinctive SXY module. PLoS Genet. 2015;11(3):e1005088.
pubmed: 25811463
pmcid: 4374748
doi: 10.1371/journal.pgen.1005088
Kuenzel S, Till A, Winkler M, Häsler R, Lipinski S, Jung S, et al. The nucleotide-binding oligomerization domain-like receptor NLRC5 is involved in IFN-dependent antiviral immune responses. J Immunol. 2010;184(4):1990–2000.
pubmed: 20061403
doi: 10.4049/jimmunol.0900557
Neerincx A, Lautz K, Menning M, Kremmer E, Zigrino P, Hösel M, et al. A role for the human nucleotide-binding domain, leucine-rich repeat-containing family member NLRC5 in antiviral responses. J Biol Chem. 2010;285(34):26223–32.
pubmed: 20538593
pmcid: 2924034
doi: 10.1074/jbc.M110.109736
Benko S, Magalhaes JG, Philpott DJ, Girardin SE. NLRC5 limits the activation of inflammatory pathways. J Immunol. 2010;185(3):1681–91.
pubmed: 20610642
doi: 10.4049/jimmunol.0903900
Staehli F, Ludigs K, Heinz LX, Seguín-Estévez Q, Ferrero I, Braun M, et al. NLRC5 deficiency selectively impairs MHC class I- dependent lymphocyte killing by cytotoxic T cells. J Immunol. 2012;188(8):3820–8.
pubmed: 22412192
doi: 10.4049/jimmunol.1102671
Tong Y, Cui J, Li Q, Zou J, Wang HY, Wang RF. Enhanced TLR-induced NF-κB signaling and type I interferon responses in NLRC5 deficient mice. Cell Res. 2012;22(5):822–35.
pubmed: 22473004
pmcid: 3343662
doi: 10.1038/cr.2012.53
Meissner TB, Li A, Liu YJ, Gagnon E, Kobayashi KS. The nucleotide-binding domain of NLRC5 is critical for nuclear import and transactivation activity. Biochem Biophys Res Commun. 2012;418(4):786–91.
pubmed: 22310711
pmcid: 3289513
doi: 10.1016/j.bbrc.2012.01.104
Gobin SJ, van Zutphen M, Westerheide SD, Boss JM, van den Elsen PJ. The MHC-specific enhanceosome and its role in MHC class I and beta(2)-microglobulin gene transactivation. J Immunol. 2001;167(9):5175–84.
pubmed: 11673530
doi: 10.4049/jimmunol.167.9.5175
Robbins GR, Truax AD, Davis BK, Zhang L, Brickey WJ, Ting JP. Regulation of class I major histocompatibility complex (MHC) by nucleotide-binding domain, leucine-rich repeat-containing (NLR) proteins. J Biol Chem. 2012;287(29):24294–303.
pubmed: 22645137
pmcid: 3397855
doi: 10.1074/jbc.M112.364604
Meissner TB, Liu YJ, Lee KH, Li A, Biswas A, van Eggermond MC, et al. NLRC5 cooperates with the RFX transcription factor complex to induce MHC class I gene expression. J Immunol. 2012;188(10):4951–8.
pubmed: 22490869
doi: 10.4049/jimmunol.1103160
Bahram S, Bresnahan M, Geraghty DE, Spies T. A second lineage of mammalian major histocompatibility complex class I genes. Proc Natl Acad Sci USA. 1994;91(14):6259–63.
pubmed: 8022771
pmcid: 44180
doi: 10.1073/pnas.91.14.6259
Groh V, Rhinehart R, Secrist H, Bauer S, Grabstein KH, Spies T. Broad tumor-associated expression and recognition by tumor-derived gamma delta T cells of MICA and MICB. Proc Natl Acad Sci USA. 1999;96(12):6879–84.
pubmed: 10359807
pmcid: 22010
doi: 10.1073/pnas.96.12.6879
Groh V, Bahram S, Bauer S, Herman A, Beauchamp M, Spies T. Cell stress-regulated human major histocompatibility complex class I gene expressed in gastrointestinal epithelium. Proc Natl Acad Sci USA. 1996;93(22):12445–50.
pubmed: 8901601
pmcid: 38011
doi: 10.1073/pnas.93.22.12445
Bauer S, Groh V, Wu J, Steinle A, Phillips JH, Lanier LL, et al. Activation of NK cells and T cells by NKG2D, a receptor for stress-inducible MICA. Science. 1999;285(5428):727–9.
pubmed: 10426993
doi: 10.1126/science.285.5428.727
Cosman D, Müllberg J, Sutherland CL, Chin W, Armitage R, Fanslow W, et al. ULBPs, novel MHC class I-related molecules, bind to CMV glycoprotein UL16 and stimulate NK cytotoxicity through the NKG2D receptor. Immunity. 2001;14(2):123–33.
pubmed: 11239445
doi: 10.1016/S1074-7613(01)00095-4
Ritter C, Fan K, Paulson KG, Nghiem P, Schrama D, Becker JC. Reversal of epigenetic silencing of MHC class I chain-related protein A and B improves immune recognition of Merkel cell carcinoma. Sci Rep. 2016;6:21678.
pubmed: 26902929
pmcid: 4763224
doi: 10.1038/srep21678
Ting JP, Trowsdale J. Genetic control of MHC class II expression. Cell. 2002;109(Suppl):S21-33.
pubmed: 11983150
doi: 10.1016/S0092-8674(02)00696-7
Hake SB, Masternak K, Kammerbauer C, Janzen C, Reith W, Steimle V. CIITA leucine-rich repeats control nuclear localization, in vivo recruitment to the major histocompatibility complex (MHC) class II enhanceosome, and MHC class II gene transactivation. Mol Cell Biol. 2000;20(20):7716–25.
pubmed: 11003667
pmcid: 86349
doi: 10.1128/MCB.20.20.7716-7725.2000
Zika E, Ting JP. Epigenetic control of MHC-II: interplay between CIITA and histone-modifying enzymes. Curr Opin Immunol. 2005;17(1):58–64.
pubmed: 15653312
doi: 10.1016/j.coi.2004.11.008
Spilianakis C, Papamatheakis J, Kretsovali A. Acetylation by PCAF enhances CIITA nuclear accumulation and transactivation of major histocompatibility complex class II genes. Mol Cell Biol. 2000;20(22):8489–98.
pubmed: 11046145
pmcid: 102155
doi: 10.1128/MCB.20.22.8489-8498.2000
Tzortzakaki E, Spilianakis C, Zika E, Kretsovali A, Papamatheakis J. Steroid receptor coactivator 1 links the steroid and interferon gamma response pathways. Mol Endocrinol. 2003;17(12):2509–18.
pubmed: 12933903
doi: 10.1210/me.2002-0439
Devaiah BN, Singer DS. CIITA and its dual roles in MHC gene transcription. Front Immunol. 2013;4:476.
pubmed: 24391648
pmcid: 3868913
doi: 10.3389/fimmu.2013.00476
Zika E, Greer SF, Zhu XS, Ting JP. Histone deacetylase 1/mSin3A disrupts gamma interferon-induced CIITA function and major histocompatibility complex class II enhanceosome formation. Mol Cell Biol. 2003;23(9):3091–102.
pubmed: 12697811
pmcid: 153210
doi: 10.1128/MCB.23.9.3091-3102.2003
Morgan JE, Shanderson RL, Boyd NH, Cacan E, Greer SF. The class II transactivator (CIITA) is regulated by post-translational modification cross-talk between ERK1/2 phosphorylation, mono-ubiquitination and Lys63 ubiquitination. 2015. Biosci Rep. https://doi.org/10.1042/BSR20150091 .
Zika E, Fauquier L, Vandel L, Ting JP. Interplay among coactivator-associated arginine methyltransferase 1, CBP, and CIITA in IFN-gamma-inducible MHC-II gene expression. Proc Natl Acad Sci USA. 2005;102(45):16321–6.
pubmed: 16254053
pmcid: 1283426
doi: 10.1073/pnas.0505045102
Spilianakis C, Kretsovali A, Agalioti T, Makatounakis T, Thanos D, Papamatheakis J. CIITA regulates transcription onset viaSer5-phosphorylation of RNA Pol II. EMBO J. 2003;22(19):5125–36.
pubmed: 14517250
pmcid: 204479
doi: 10.1093/emboj/cdg496
Nanda NK, Birch L, Greenberg NM, Prins GS. MHC class I and class II molecules are expressed in both human and mouse prostate tumor microenvironment. Prostate. 2006;66(12):1275–84.
pubmed: 16741922
pmcid: 2276872
doi: 10.1002/pros.20432
Wright KL, Ting JP. Epigenetic regulation of MHC-II and CIITA genes. Trends Immunol. 2006;27(9):405–12.
pubmed: 16870508
doi: 10.1016/j.it.2006.07.007
Holtz R, Choi JC, Petroff MG, Piskurich JF, Murphy SP. Class II transactivator (CIITA) promoter methylation does not correlate with silencing of CIITA transcription in trophoblasts. Biol Reprod. 2003;69(3):915–24.
pubmed: 12748124
doi: 10.1095/biolreprod.103.017103
Liu JH, Bian YM, Xie Y, Lu DP. Epigenetic modification and preliminary investigation of the mechanism of the immune evasion of HL-60 cells. Mol Med Rep. 2015;12(1):1059–65.
pubmed: 25815463
pmcid: 4438930
doi: 10.3892/mmr.2015.3526
Londhe P, Zhu B, Abraham J, Keller C, Davie J. CIITA is silenced by epigenetic mechanisms that prevent the recruitment of transactivating factors in rhabdomyosarcoma cells. Int J Cancer. 2012;131(4):E437–48.
pubmed: 21989738
pmcid: 3271171
doi: 10.1002/ijc.26478
Radosevich M, Jager M, Ono SJ. Inhibition of MHC class II gene expression in uveal melanoma cells is due to methylation of the CIITA gene or an upstream activator. Exp Mol Pathol. 2007;82(1):68–76.
pubmed: 16650406
doi: 10.1016/j.yexmp.2006.03.005
Cornett EM, Ferry L, Defossez PA, Rothbart SB. Lysine methylation regulators moonlighting outside the epigenome. Mol Cell. 2019;75(6):1092–101.
pubmed: 31539507
pmcid: 6756181
doi: 10.1016/j.molcel.2019.08.026
Sun Y. Tumor microenvironment and cancer therapy resistance. Cancer Lett. 2016;380(1):205–15.
pubmed: 26272180
doi: 10.1016/j.canlet.2015.07.044
Chang YC, Chen TC, Lee CT, Yang CY, Wang HW, Wang CC, et al. Epigenetic control of MHC class II expression in tumor-associated macrophages by decoy receptor 3. Blood. 2008;111(10):5054–63.
pubmed: 18349319
doi: 10.1182/blood-2007-12-130609
Hui L, Chen Y. Tumor microenvironment: sanctuary of the devil. Cancer Lett. 2015;368(1):7–13.
pubmed: 26276713
doi: 10.1016/j.canlet.2015.07.039
Senthebane DA, Rowe A, Thomford NE, Shipanga H, Munro D, Mazeedi M, et al. The role of tumor microenvironment in chemoresistance: to survive, keep your enemies closer. Int J Mol Sci. 2017;18(7):1586.
pubmed: 28754000
pmcid: 5536073
doi: 10.3390/ijms18071586
Soysal SD, Tzankov A, Muenst SE. Role of the tumor microenvironment in breast cancer. Pathobiol J Immunopathol Mol Cell Biol. 2015;82(3–4):142–52.
doi: 10.1159/000430499
Frankel T, Lanfranca MP, Zou W. The Role of Tumor Microenvironment in Cancer Immunotherapy. Adv Exp Med Biol. 2017;1036:51–64.
pubmed: 29275464
doi: 10.1007/978-3-319-67577-0_4
Kim M, Park C, Jung J, Yeo SG. The histone deacetylase class I, II inhibitor trichostatin A delays peripheral neurodegeneration. J Mol Histol. 2019;50(2):167–78.
pubmed: 30671879
doi: 10.1007/s10735-019-09815-1
Papa S, Choy PM, Bubici C. The ERK and JNK pathways in the regulation of metabolic reprogramming. Oncogene. 2019;38(13):2223–40.
pubmed: 30487597
doi: 10.1038/s41388-018-0582-8
Tai SK, Chang HC, Lan KL, Lee CT, Yang CY, Chen NJ, et al. Decoy receptor 3 enhances tumor progression via induction of tumor-associated macrophages. J Immunol. 2012;188(5):2464–71.
pubmed: 22287720
doi: 10.4049/jimmunol.1101101
Göttlicher M, Minucci S, Zhu P, Krämer OH, Schimpf A, Giavara S, et al. Valproic acid defines a novel class of HDAC inhibitors inducing differentiation of transformed cells. EMBO J. 2001;20(24):6969–78.
pubmed: 11742974
pmcid: 125788
doi: 10.1093/emboj/20.24.6969
Sun Y, Sun Y, Yue S, Wang Y, Lu F. Histone deacetylase inhibitors in cancer therapy. Curr Top Med Chem. 2018;18(28):2420–8.
pubmed: 30526462
doi: 10.2174/1568026619666181210152115
Satoh A, Toyota M, Ikeda H, Morimoto Y, Akino K, Mita H, et al. Epigenetic inactivation of class II transactivator (CIITA) is associated with the absence of interferon-gamma-induced HLA-DR expression in colorectal and gastric cancer cells. Oncogene. 2004;23(55):8876–86.
pubmed: 15467734
doi: 10.1038/sj.onc.1208144
Meazza R, Comes A, Orengo AM, Ferrini S, Accolla RS. Tumor rejection by gene transfer of the MHC class II transactivator in murine mammary adenocarcinoma cells. Eur J Immunol. 2003;33(5):1183–92.
pubmed: 12731043
doi: 10.1002/eji.200323712
Serrano A, Tanzarella S, Lionello I, Mendez R, Traversari C, Ruiz-Cabello F, et al. Rexpression of HLA class I antigens and restoration of antigen-specific CTL response in melanoma cells following 5-aza-2’-deoxycytidine treatment. Int J Cancer. 2001;94(2):243–51.
pubmed: 11668505
doi: 10.1002/ijc.1452
Natale F, Vivo M, Falco G, Angrisano T. Deciphering DNA methylation signatures of pancreatic cancer and pancreatitis. Clin Epigenetics. 2019;11(1):132.
pubmed: 31492175
pmcid: 6729090
doi: 10.1186/s13148-019-0728-8
Mishra NK, Guda C. Genome-wide DNA methylation analysis reveals molecular subtypes of pancreatic cancer. Oncotarget. 2017;8(17):28990–9012.
pubmed: 28423671
pmcid: 5438707
doi: 10.18632/oncotarget.15993
Liu B, Pilarsky C. Analysis of DNA hypermethylation in pancreatic cancer using methylation-specific PCR and bisulfite sequencing. Methods Mol Biol. 2018;1856:269–82.
pubmed: 30178258
doi: 10.1007/978-1-4939-8751-1_16
Bailey P, Chang DK, Nones K, Johns AL, Patch AM, Gingras MC, et al. Genomic analyses identify molecular subtypes of pancreatic cancer. Nature. 2016;531(7592):47–52.
pubmed: 26909576
doi: 10.1038/nature16965
Cao W, Zhou G, Qiu J, Xu L, Ding X, Zhang H, et al. Research on the epigenetic modification of pancreatic cancer vaccine. Hepatogastroenterology. 2014;61(130):272–7.
pubmed: 24901123
Tao Y, Lin F, Li T, Xie J, Shen C, Zhu Z. Epigenetically modified pancreatic carcinoma PANC-1 cells can act as cancer vaccine to enhance antitumor immune response in mice. Oncol Res. 2013;21(6):307–16.
pubmed: 25198660
doi: 10.3727/096504014X13983417587320
Maslov AY, Lee M, Gundry M, Gravina S, Strogonova N, Tazearslan C, et al. 5-aza-2’-deoxycytidine-induced genome rearrangements are mediated by DNMT1. Oncogene. 2012;31(50):5172–9.
pubmed: 22349820
pmcid: 3381073
doi: 10.1038/onc.2012.9
Bubna AK. Vorinostat-an overview. Indian J Dermatol. 2015;60(4):419.
pubmed: 26288427
pmcid: 4533557
doi: 10.4103/0019-5154.160511
Chou SD, Khan AN, Magner WJ, Tomasi TB. Histone acetylation regulates the cell type specific CIITA promoters, MHC class II expression and antigen presentation in tumor cells. Int Immunol. 2005;17(11):1483–94.
pubmed: 16210330
doi: 10.1093/intimm/dxh326
Zenke K, Muroi M, Tanamoto KI. IRF1 supports DNA binding of STAT1 by promoting its phosphorylation. Immunol Cell Biol. 2018;96(10):1095–103.
pubmed: 29893425
doi: 10.1111/imcb.12185
Abou El Hassan M, Huang K, Eswara MB, Xu Z, Yu T, Aubry A, et al. Properties of STAT1 and IRF1 enhancers and the influence of SNPs. BMC Mol Biol. 2017;18(1):6.
pubmed: 28274199
pmcid: 5343312
doi: 10.1186/s12867-017-0084-1
Beresford GW, Boss JM. CIITA coordinates multiple histone acetylation modifications at the HLA-DRA promoter. Nat Immunol. 2001;2(7):652–7.
pubmed: 11429551
doi: 10.1038/89810
Grewal SI, Moazed D. Heterochromatin and epigenetic control of gene expression. Science. 2003;301(5634):798–802.
pubmed: 12907790
doi: 10.1126/science.1086887
Richards EJ, Elgin SC. Epigenetic codes for heterochromatin formation and silencing: rounding up the usual suspects. Cell. 2002;108(4):489–500.
pubmed: 11909520
doi: 10.1016/S0092-8674(02)00644-X
Greer SF, Zika E, Conti B, Zhu XS, Ting JP. Enhancement of CIITA transcriptional function by ubiquitin. Nat Immunol. 2003;4(11):1074–82.
pubmed: 14528304
doi: 10.1038/ni985
Eckschlager T, Plch J, Stiborova M, Hrabeta J. Histone deacetylase inhibitors as anticancer drugs. Int J Mol Sci. 2017;18(7):1414.
pubmed: 28671573
pmcid: 5535906
doi: 10.3390/ijms18071414
Okada K, Hakata S, Terashima J, Gamou T, Habano W, Ozawa S. Combination of the histone deacetylase inhibitor depsipeptide and 5-fluorouracil upregulates major histocompatibility complex class II and p21 genes and activates caspase-3/7 in human colon cancer HCT-116 cells. Oncol Rep. 2016;36(4):1875–85.
pubmed: 27509880
pmcid: 5022900
doi: 10.3892/or.2016.5008
Moreno CS, Beresford GW, Louis-Plence P, Morris AC, Boss JM. CREB regulates MHC class II expression in a CIITA-dependent manner. Immunity. 1999;10(2):143–51.
pubmed: 10072067
doi: 10.1016/S1074-7613(00)80015-1
Rhee I, Bachman KE, Park BH, Jair KW, Yen RW, Schuebel KE, et al. DNMT1 and DNMT3b cooperate to silence genes in human cancer cells. Nature. 2002;416(6880):552–6.
pubmed: 11932749
doi: 10.1038/416552a
Chávez-Blanco A, De la Cruz-Hernández E, Domínguez GI, Rodríguez-Cortez O, Alatorre B, Pérez-Cárdenas E, et al. Upregulation of NKG2D ligands and enhanced natural killer cell cytotoxicity by hydralazine and valproate. Int J Oncol. 2011;39(6):1491–9.
pubmed: 21805029
Chen YS, Li J, Neja S, Kapoor S, Tovar Perez JE, Tripathi C, et al. Metabolomics of acute vs. chronic spinach intake in an apc-mutant genetic background: linoleate and butanoate metabolites targeting HDAC activity and IFN-γ signaling. Cells. 2022;11(3):573.
pubmed: 35159382
pmcid: 8834217
doi: 10.3390/cells11030573
Kailasam A, Mittal SK, Agrawal DK. Epigenetics in the pathogenesis of esophageal adenocarcinoma. Clin Transl Sci. 2015;8(4):394–402.
pubmed: 25388215
doi: 10.1111/cts.12242
Hu JM, Li L, Chen YZ, Liu C, Cui X, Yin L, et al. HLA-DRB1 and HLA-DQB1 methylation changes promote the occurrence and progression of Kazakh ESCC. Epigenetics. 2014;9(10):1366–73.
pubmed: 25437052
pmcid: 4623353
doi: 10.4161/15592294.2014.969625
Dhatchinamoorthy K, Colbert JD, Rock KL. Cancer immune evasion through loss of MHC class I antigen presentation. Front Immunol. 2021;12:636568.
pubmed: 33767702
pmcid: 7986854
doi: 10.3389/fimmu.2021.636568
Sheyhidin I, Hasim A, Zheng F, Ma H. Epigenetic changes within the promoter regions of antigen processing machinery family genes in Kazakh primary esophageal squamous cell carcinoma. Asian Pacific J Cancer Prevent APJCP. 2014;15(23):10299–306.
doi: 10.7314/APJCP.2014.15.23.10299
Dawson MA, Kouzarides T. Cancer epigenetics: from mechanism to therapy. Cell. 2012;150(1):12–27.
pubmed: 22770212
doi: 10.1016/j.cell.2012.06.013
Duvic M, Talpur R, Ni X, Zhang C, Hazarika P, Kelly C, et al. Phase 2 trial of oral vorinostat (suberoylanilide hydroxamic acid, SAHA) for refractory cutaneous T-cell lymphoma (CTCL). Blood. 2007;109(1):31–9.
pubmed: 16960145
pmcid: 1785068
doi: 10.1182/blood-2006-06-025999
Sun T, Li Y, Yang W, Wu H, Li X, Huang Y, et al. Histone deacetylase inhibition up-regulates MHC class I to facilitate cytotoxic T lymphocyte-mediated tumor cell killing in glioma cells. J Cancer. 2019;10(23):5638–45.
pubmed: 31737100
pmcid: 6843866
doi: 10.7150/jca.34471
Yang H, Lan P, Hou Z, Guan Y, Zhang J, Xu W, et al. Histone deacetylase inhibitor SAHA epigenetically regulates miR-17-92 cluster and MCM7 to upregulate MICA expression in hepatoma. Br J Cancer. 2015;112(1):112–21.
pubmed: 25393367
doi: 10.1038/bjc.2014.547
Xiao W, Dong W, Zhang C, Saren G, Geng P, Zhao H, et al. Effects of the epigenetic drug MS-275 on the release and function of exosome-related immune molecules in hepatocellular carcinoma cells. Eur J Med Res. 2013;18(1):61.
pubmed: 24359553
pmcid: 3881022
doi: 10.1186/2047-783X-18-61
Zhang Y, Wu Q, Xu L, Wang H, Liu X, Li S, et al. Sensitive detection of colorectal cancer in peripheral blood by a novel methylation assay. Clin Epigenetics. 2021;13(1):90.
pubmed: 33892797
pmcid: 8066866
doi: 10.1186/s13148-021-01076-8
Han YD, Oh TJ, Chung TH, Jang HW, Kim YN, An S, et al. Early detection of colorectal cancer based on presence of methylated syndecan-2 (SDC2) in stool DNA. Clin Epigenetics. 2019;11(1):51.
pubmed: 30876480
pmcid: 6419806
doi: 10.1186/s13148-019-0642-0
Araghi M, Soerjomataram I, Jenkins M, Brierley J, Morris E, Bray F, et al. Global trends in colorectal cancer mortality: projections to the year 2035. Int J Cancer. 2019;144(12):2992–3000.
pubmed: 30536395
doi: 10.1002/ijc.32055
Morgan E, Arnold M, Camargo MC, Gini A, Kunzmann AT, Matsuda T, et al. The current and future incidence and mortality of gastric cancer in 185 countries, 2020–40: a population-based modelling study. EClinicalMedicine. 2022;47:101404.
pubmed: 35497064
pmcid: 9046108
doi: 10.1016/j.eclinm.2022.101404
Morgan E, Soerjomataram I, Rumgay H, Coleman HG, Thrift AP, Vignat J, et al. The global landscape of esophageal squamous cell carcinoma and esophageal adenocarcinoma incidence and mortality in 2020 and projections to 2040: new estimates from GLOBOCAN 2020. Gastroenterology. 2022;163(3):649-58.e2.
pubmed: 35671803
doi: 10.1053/j.gastro.2022.05.054
Ge T, Gu X, Jia R, Ge S, Chai P, Zhuang A, et al. Crosstalk between metabolic reprogramming and epigenetics in cancer: updates on mechanisms and therapeutic opportunities. Cancer Commun. 2022;42(11):1049–82.
doi: 10.1002/cac2.12374
Kapoor S, Gustafson T, Zhang M, Chen YS, Li J, Nguyen N, et al. Deacetylase plus bromodomain inhibition downregulates ERCC2 and suppresses the growth of metastatic colon cancer cells. Cancers. 2021;13(6):1438.
pubmed: 33809839
pmcid: 8004213
doi: 10.3390/cancers13061438
Rajendran P, Johnson G, Li L, Chen YS, Dashwood M, Nguyen N, et al. Acetylation of CCAR2 Establishes a BET/BRD9 acetyl switch in response to combined deacetylase and bromodomain inhibition. Cancer Res. 2019;79(5):918–27.
pubmed: 30643017
pmcid: 6397680
doi: 10.1158/0008-5472.CAN-18-2003
Mazur PK, Herner A, Mello SS, Wirth M, Hausmann S, Sánchez-Rivera FJ, et al. Combined inhibition of BET family proteins and histone deacetylases as a potential epigenetics-based therapy for pancreatic ductal adenocarcinoma. Nat Med. 2015;21(10):1163–71.
pubmed: 26390243
pmcid: 4959788
doi: 10.1038/nm.3952
Burr ML, Sparbier CE, Chan KL, Chan YC, Kersbergen A, Lam EYN, et al. An evolutionarily conserved function of polycomb silences the MHC Class I antigen presentation pathway and enables immune evasion in cancer. Cancer Cell. 2019;36(4):385-401.e8.
pubmed: 31564637
pmcid: 6876280
doi: 10.1016/j.ccell.2019.08.008
Monterroza L, Parrilla MM, Samaranayake SG, Rivera-Rodriguez DE, Yoon SB, Bommireddy R, et al. Tumor-intrinsic enhancer of zeste homolog 2 controls immune cell infiltration, tumor growth, and lung metastasis in a triple-negative breast cancer model. Int J Mol Sci. 2024;25(10):5392.
pubmed: 38791429
pmcid: 11121204
doi: 10.3390/ijms25105392
Straining R, Eighmy W. Tazemetostat: EZH2 Inhibitor. J Adv Pract Oncol. 2022;13(2):158–63.
pubmed: 35369397
pmcid: 8955562
doi: 10.6004/jadpro.2022.13.2.7
Chu L, Qu Y, An Y, Hou L, Li J, Li W, et al. Induction of senescence-associated secretory phenotype underlies the therapeutic efficacy of PRC2 inhibition in cancer. Cell Death Dis. 2022;13(2):155.
pubmed: 35169119
pmcid: 8847585
doi: 10.1038/s41419-022-04601-6
Barghout SH, Machado RAC, Barsyte-Lovejoy D. Chemical biology and pharmacology of histone lysine methylation inhibitors. Biochim Biophys Acta Gene Regul Mech. 2022;1865(6):194840.
pubmed: 35753676
doi: 10.1016/j.bbagrm.2022.194840
Zha L, Cao Q, Cui X, Li F, Liang H, Xue B, et al. Epigenetic regulation of E-cadherin expression by the histone demethylase UTX in colon cancer cells. Med Oncol. 2016;33(3):21.
pubmed: 26819089
doi: 10.1007/s12032-016-0734-z
Gu SS, Zhang W, Wang X, Jiang P, Traugh N, Li Z, et al. Therapeutically Increasing MHC-I expression potentiates immune checkpoint blockade. Cancer Discov. 2021;11(6):1524–41.
pubmed: 33589424
pmcid: 8543117
doi: 10.1158/2159-8290.CD-20-0812
Xiong W, Gao X, Zhang T, Jiang B, Hu MM, Bu X, et al. USP8 inhibition reshapes an inflamed tumor microenvironment that potentiates the immunotherapy. Nat Commun. 2022;13(1):1700.
pubmed: 35361799
pmcid: 8971425
doi: 10.1038/s41467-022-29401-6
Shukla A, Cloutier M, Appiya Santharam M, Ramanathan S, Ilangumaran S. The MHC Class-I transactivator NLRC5: implications to cancer immunology and potential applications to cancer immunotherapy. Int J Mol Sci. 2021;22(4):1964.
pubmed: 33671123
pmcid: 7922096
doi: 10.3390/ijms22041964
Li L, Song Q, Zhou J, Ji Q. Controllers of histone methylation-modifying enzymes in gastrointestinal cancers. Biomed Pharmacother. 2024;174:116488.
pubmed: 38520871
doi: 10.1016/j.biopha.2024.116488
Dashwood RH, Ho E. Dietary histone deacetylase inhibitors: from cells to mice to man. Semin Cancer Biol. 2007;17(5):363–9.
pubmed: 17555985
pmcid: 2737738
doi: 10.1016/j.semcancer.2007.04.001
Kawazu M, Ueno T, Saeki K, Sax N, Togashi Y, Kanaseki T, et al. HLA Class I analysis provides insight into the genetic and epigenetic background of immune evasion in colorectal cancer with high microsatellite instability. Gastroenterology. 2022;162(3):799–812.
pubmed: 34687740
doi: 10.1053/j.gastro.2021.10.010
Anderson P, Aptsiauri N, Ruiz-Cabello F, Garrido F. HLA class I loss in colorectal cancer: implications for immune escape and immunotherapy. Cell Mol Immunol. 2021;18(3):556–65.
pubmed: 33473191
pmcid: 8027055
doi: 10.1038/s41423-021-00634-7
West AC, Smyth MJ, Johnstone RW. The anticancer effects of HDAC inhibitors require the immune system. Oncoimmunology. 2014;3(1):e27414.
pubmed: 24701376
pmcid: 3962507
doi: 10.4161/onci.27414
The Human Protein Atlas. https://www.proteinatlas.org/ . Accessed 10 October 2023.
UCSC Genome Browser. https://genome.ucsc.edu/ . Accessed 10 October 2023.
ENCODE. https://www.encodeproject.org/ . Accessed 10 October 2023.