Epigenetic Regulation of Immune Checkpoints and T Cell Exhaustion Markers in Tumor-Infiltrating T Cells of Colorectal Cancer Patients

References

• Bray F , FerlayJ , SoerjomataramI , SiegelRL , TorreLA , JemalA. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J. Clin.68(6), 394–424 (2018).
   PubMed Web of Science ®Google Scholar
• Jung G , Hernandez-IllanE , MoreiraL , BalaguerF , GoelA. Epigenetics of colorectal cancer: biomarker and therapeutic potential. Nat. Rev. Gastroenterol. Hepatol.17(2), 111–130 (2020).
   PubMed Web of Science ®Google Scholar
• Sasidharan Nair V , ToorSM , TahaRZ , ShaathH , ElkordE. DNA methylation and repressive histones in the promoters of PD-1, CTLA-4, TIM-3, LAG-3, TIGIT, PD-L1, and galectin-9 genes in human colorectal cancer. Clin. Epigenetics10(1), 104 (2018).
   PubMedGoogle Scholar
• Ryser MD , YuM , GradyW , SiegmundK , ShibataD. Epigenetic heterogeneity in human colorectal tumors reveals preferential conservation and evidence of immune surveillance. Sci. Rep.8(1), 17292 (2018).
   PubMedGoogle Scholar
• Wang T , MadenSK , LuebeckGEet al. Dysfunctional epigenetic aging of the normal colon and colorectal cancer risk. Clin. Epigenetics12(1), 5 (2020).
   PubMed Web of Science ®Google Scholar
• Saleh R , ElkordE. Treg-mediated acquired resistance to immune checkpoint inhibitors. Cancer Lett.457, 168–179 (2019).
   PubMed Web of Science ®Google Scholar
• Saleh R , ElkordE. Acquired resistance to cancer immunotherapy: role of tumor-mediated immunosuppression. Semin. Cancer Biol.65, 13–27 (2020).
   PubMed Web of Science ®Google Scholar
• Pardoll DM . The blockade of immune checkpoints in cancer immunotherapy. Nat. Rev. Cancer12(4), 252–264 (2012).
   PubMed Web of Science ®Google Scholar
• Darvin P , ToorSM , SasidharanNair V , ElkordE. Immune checkpoint inhibitors: recent progress and potential biomarkers. Exp. Mol. Med.50(12), 1–11 (2018).
   PubMed Web of Science ®Google Scholar
• Toor SM , SasidharanNair V , DecockJ , ElkordE. Immune checkpoints in the tumor microenvironment. Semin. Cancer Biol.65, 1–12 (2020).
   PubMed Web of Science ®Google Scholar
• Seo H , ChenJ , Gonzalez-AvalosEet al. TOX and TOX2 transcription factors cooperate with NR4A transcription factors to impose CD8(+) T-cell exhaustion. Proc. Natl Acad. Sci. USA116(25), 12410–12415 (2019).
   PubMed Web of Science ®Google Scholar
• Kim K , ParkS , ParkSYet al. Single-cell transcriptome analysis reveals TOX as a promoting factor for T-cell exhaustion and a predictor for anti-PD-1 responses in human cancer. Genome Med.12(1), 22 (2020).
   PubMed Web of Science ®Google Scholar
• Wang X , HeQ , ShenHet al. TOX promotes the exhaustion of antitumor CD8(+) T cells by preventing PD1 degradation in hepatocellular carcinoma. J. Hepatol.71(4), 731–741 (2019).
   PubMed Web of Science ®Google Scholar
• Khan O , GilesJR , McdonaldSet al. TOX transcriptionally and epigenetically programs CD8(+) T-cell exhaustion. Nature571(7764), 211–218 (2019).
   PubMed Web of Science ®Google Scholar
• Elashi AA , SasidharanNair V , TahaRZ , ShaathH , ElkordE. DNA methylation of immune checkpoints in the peripheral blood of breast and colorectal cancer patients. Oncoimmunology8(2), e1542918 (2019).
   PubMed Web of Science ®Google Scholar
• Sasidharan Nair V , ElSalhat H , TahaRZ , JohnA , AliBR , ElkordE. DNA methylation and repressive H3K9 and H3K27 trimethylation in the promoter regions of PD-1, CTLA-4, TIM-3, LAG-3, TIGIT, and PD-L1 genes in human primary breast cancer. Clin. Epigenetics10, 78 (2018).
   PubMed Web of Science ®Google Scholar
• Saleh R , TahaRZ , ToorSMet al. Expression of immune checkpoints and T-cell exhaustion markers in early and advanced stages of colorectal cancer. Cancer Immunol. Immunother.69(10), 1989–1999 (2020).
   PubMed Web of Science ®Google Scholar
• D’acquisto F , CromptonT. CD3+CD4−CD8− (double negative) T cells: saviours or villains of the immune response?Biochem. Pharmacol.82(4), 333–340 (2011).
   PubMed Web of Science ®Google Scholar
• Lu X , SuB , XiaHet al. Low double-negative CD3(+)CD4(−)CD8(−) T cells are associated with incomplete restoration of CD4(+) T cells and higher immune activation in HIV-1 immunological nonresponders. Front. Immunol.7, 579 (2016).
   PubMed Web of Science ®Google Scholar
• Bernardo I , ManceboE , AguiloIet al. Phenotypic and functional evaluation of CD3+CD4-CD8-T cells in human CD8 immunodeficiency. Haematologica96(8), 1195–1203 (2011).
   PubMed Web of Science ®Google Scholar
• Ngollo M , LebertA , DauresMet al. Global analysis of H3K27me3 as an epigenetic marker in prostate cancer progression. BMC Cancer17(1), 261 (2017).
   PubMedGoogle Scholar
• Qin J , WenB , LiangY , YuW , LiH. Histone modifications and their role in colorectal cancer (review). Pathol. Oncol. Res.26(4), 2023–2033 (2020).
   PubMed Web of Science ®Google Scholar
• Aliahmad P , SeksenyanA , KayeJ. The many roles of TOX in the immune system. Curr. Opin. Immunol.24(2), 173–177 (2012).
   PubMed Web of Science ®Google Scholar
• Chaudhary B , ElkordE. Regulatory T cells in the tumor microenvironment and cancer progression: role and therapeutic targeting. Vaccines (Basel)4(3), doi:10.3390/vaccines4030028 (2016).
   PubMed Web of Science ®Google Scholar
• Yasinska IM , SakhnevychSS , PavlovaLet al. The Tim-3-Galectin-9 pathway and its regulatory mechanisms in human breast cancer. Front. Immunol.10, 1594 (2019).
   PubMed Web of Science ®Google Scholar
• Sasidharan Nair V , ElkordE. Immune checkpoint inhibitors in cancer therapy: a focus on T-regulatory cells. Immunol. Cell Biol.96(1), 21–33 (2018).
   PubMed Web of Science ®Google Scholar
• Galon J , CostesA , Sanchez-CaboFet al. Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science313(5795), 1960–1964 (2006).
   PubMed Web of Science ®Google Scholar
• Crespo J , SunH , WellingTH , TianZ , ZouW. T-cell anergy, exhaustion, senescence, and stemness in the tumor microenvironment. Curr. Opin. Immunol.25(2), 214–221 (2013).
   PubMed Web of Science ®Google Scholar
• Pauken KE , WherryEJ. Overcoming T-cell exhaustion in infection and cancer. Trends Immunol.36(4), 265–276 (2015).
   PubMed Web of Science ®Google Scholar
• Blackburn SD , ShinH , HainingWNet al. Coregulation of CD8+ T-cell exhaustion by multiple inhibitory receptors during chronic viral infection. Nat. Immunol.10(1), 29–37 (2009).
   PubMed Web of Science ®Google Scholar
• Scott AC , DundarF , ZumboPet al. TOX is a critical regulator of tumour-specific T-cell differentiation. Nature571(7764), 270–274 (2019).
   PubMed Web of Science ®Google Scholar
• Toor SM , MurshedK , Al-DhaheriM , KhawarM , AbuNada M , ElkordE. Immune checkpoints in circulating and tumor-infiltrating CD4(+) T-cell subsets in colorectal cancer patients. Front. Immunol.10, 2936 (2019).
   PubMed Web of Science ®Google Scholar
• Tseng YH , HoHL , LaiCRet al. PD-L1 expression of tumor cells, macrophages, and immune cells in non-small-cell lung cancer patients with malignant pleural effusion. J. Thorac. Oncol.13(3), 447–453 (2018).
   PubMed Web of Science ®Google Scholar
• Brochez L , MeiresonA , ChevoletI , SundahlN , OstP , KruseV. Challenging PD-L1 expressing cytotoxic T cells as a predictor for response to immunotherapy in melanoma. Nat. Commun.9(1), 2921 (2018).
   PubMedGoogle Scholar
• Xu B , YuanL , GaoQet al. Circulating and tumor-infiltrating Tim-3 in patients with colorectal cancer. Oncotarget6(24), 20592–20603 (2015).
   PubMed Web of Science ®Google Scholar
• Bestor TH , EdwardsJR , BoulardM. Notes on the role of dynamic DNA methylation in mammalian development. Proc. Natl Acad. Sci. USA112(22), 6796–6799 (2015).
   PubMed Web of Science ®Google Scholar
• Lichtenstein AV , KisseljovaNP. DNA methylation and carcinogenesis. Biochemistry Mosc.66(3), 235–255 (2001).
   PubMed Web of Science ®Google Scholar
• Wu J , ShiH. Unlocking the epigenetic code of T-cell exhaustion. Transl. Cancer Res.6(Suppl. 2), S384–S387 (2017).
   PubMedGoogle Scholar
• Yang R , ChengS , LuoNet al. Distinct epigenetic features of tumor-reactive CD8+ T cells in colorectal cancer patients revealed by genome-wide DNA methylation analysis. Genome Biol.21(1), 2 (2019).
   PubMed Web of Science ®Google Scholar
• Coit P , DozmorovMG , MerrillJTet al. Epigenetic reprogramming in naive CD4+ T cells favoring T-cell activation and nonTh1 effector T-cell immune response as an early event in lupus flares. Arthritis Rheumatol.68(9), 2200–2209 (2016).
   PubMed Web of Science ®Google Scholar
• Xia A , ZhangY , XuJ , YinT , LuXJ. T-cell dysfunction in cancer immunity and immunotherapy. Front. Immunol10, 1719 (2019).
   PubMed Web of Science ®Google Scholar
• Derks S , BoschLJ , NiessenHEet al. Promoter CpG island hypermethylation- and H3K9me3 and H3K27me3-mediated epigenetic silencing targets the deleted in colon cancer (DCC) gene in colorectal carcinogenesis without affecting neighboring genes on chromosomal region 18q21. Carcinogenesis30(6), 1041–1048 (2009).
   PubMed Web of Science ®Google Scholar
• Fahrner JA , EguchiS , HermanJG , BaylinSB. Dependence of histone modifications and gene expression on DNA hypermethylation in cancer. Cancer Res.62(24), 7213–7218 (2002).
   PubMed Web of Science ®Google Scholar
• Healey MA , HuR , BeckAHet al. Association of H3K9me3 and H3K27me3 repressive histone marks with breast cancer subtypes in the Nurses’ Health study. Breast Cancer Res. Treat.147(3), 639–651 (2014).
   PubMed Web of Science ®Google Scholar