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Research Article

The DNA Methylation Landscape of PD-1 (PDCD1) and Adjacent LncRNA AC131097.3 in Head and Neck Squamous Cell Carcinoma

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Pages 113-127 | Received 21 May 2020, Accepted 15 Nov 2020, Published online: 22 Dec 2020

References

  • Siegel RL , MillerKD , JemalA. Cancer statistics, 2020. CA Cancer J. Clin.70(1), 7–30 (2020).
  • Gillison ML , KochWM , CaponeRBet al. Evidence for a causal association between human papillomavirus and a subset of head and neck cancers. J. Natl Cancer Inst.92(9), 709–720 (2000).
  • Ang KK , HarrisJ , WheelerRet al. Human papillomavirus and survival of patients with oropharyngeal cancer. N. Engl. J. Med.363(1), 24–35 (2010).
  • Leemans CR , BraakhuisBJM , BrakenhoffRH. The molecular biology of head and neck cancer. Nat. Rev. Cancer11(1), 9–22 (2011).
  • zur Hausen H . The search for infectious causes of human cancers: where and why. Virology392(1), 1–10 (2009).
  • zur Hausen H . Papillomaviruses and cancer: from basic studies to clinical application. Nat. Rev. Cancer2(5), 342–350 (2002).
  • Slebos RJC , YiY , ElyKet al. Gene expression differences associated with human papillomavirus status in head and neck squamous cell carcinoma. Clin. Cancer Res.12(3 Pt 1), 701–709 (2006).
  • Schoppy DW , SunwooJB. Immunotherapy for head and neck squamous cell carcinoma. Hematol/Oncol Clin. North Am.29(6), 1033–1043 (2015).
  • Ang KK , ChenA , CurranWJet al. Head and neck carcinoma in the United States: first comprehensive report of the Longitudinal Oncology Registry of Head and Neck Carcinoma (LORHAN). Cancer118(23), 5783–5792 (2012).
  • Kleffel S , PoschC , BarthelSRet al. Melanoma cell-intrinsic PD-1 receptor functions promote tumor growth. Cell162(6), 1242–1256 (2015).
  • Okazaki T , HonjoT. PD-1 and PD-1 ligands: from discovery to clinical application. Int. Immunol.19(7), 813–824 (2007).
  • Zech HB , LabanS , SchafhausenP , BussmannL , BetzC , BuschC-J. Therapie der rezidivierten und fernmetastasierten Plattenepithelkarzinome des Kopf-Hals-Bereichs: highlights des ASCO-Meetings 2019. HNO67(12), 898–904 (2019).
  • Larkins E , BlumenthalGM , YuanWet al. FDA approval summary: pembrolizumab for the treatment of recurrent or metastatic head and neck squamous cell carcinoma with disease progression on or after platinum-containing chemotherapy. Oncologist22(7), 873–878 (2017).
  • Sen DR , KaminskiJ , BarnitzRAet al. The epigenetic landscape of T cell exhaustion. Science354(6316), 1165–1169 (2016).
  • Pauken KE , SammonsMA , OdorizziPMet al. Epigenetic stability of exhausted T cells limits durability of reinvigoration by PD-1 blockade. Science354(6316), 1160–1165 (2016).
  • Robertson KD . DNA methylation and human disease. Nat. Rev. Genet.6(8), 597–610 (2005).
  • Johnson AA , AkmanK , CalimportSRG , WuttkeD , StolzingA , de MagalhãesJP. The role of DNA methylation in aging, rejuvenation, and age-related disease. Rejuvenation Res.15(5), 483–494 (2012).
  • Taby R , IssaJ-PJ. Cancer epigenetics. CA Cancer J. Clin.60(6), 376–392 (2010).
  • Jones PA . Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nat. Rev. Genet.13(7), 484–492 (2012).
  • Schmidl C , DelacherM , HuehnJ , FeuererM. Epigenetic mechanisms regulating T-cell responses. J. Allergy Clin. Immunol.142(3), 728–743 (2018).
  • Ghoneim HE , ZamoraAE , ThomasPG , YoungbloodBA. Cell-intrinsic barriers of T cell-based immunotherapy. Trends Mol. Med.22(12), 1000–1011 (2016).
  • Yang X , HanH , de CarvalhoDD , LayFD , JonesPA , LiangG. Gene body methylation can alter gene expression and is a therapeutic target in cancer. Cancer Cell26(4), 577–590 (2014).
  • Ehrlich M , LaceyM. DNA methylation and differentiation: silencing, upregulation and modulation of gene expression. Epigenomics5(5), 553–568 (2013).
  • Esteller M , Garcia-FoncillasJ , AndionEet al. Inactivation of the DNA-repair gene MGMT and the clinical response of gliomas to alkylating agents. N. Engl. J. Med.343(19), 1350–1354 (2000).
  • Church TR , WandellM , Lofton-DayCet al. Prospective evaluation of methylated SEPT9 in plasma for detection of asymptomatic colorectal cancer. Gut63(2), 317–325 (2014).
  • Partin AW , van NesteL , KleinEAet al. Clinical validation of an epigenetic assay to predict negative histopathological results in repeat prostate biopsies. J. Urol.192(4), 1081–1087 (2014).
  • van Kessel KEM , BeukersW , LurkinIet al. Validation of a DNA methylation-mutation urine assay to select patients with hematuria for cystoscopy. J. Urol.197(3 Pt 1), 590–595 (2017).
  • Imperiale TF , RansohoffDF , ItzkowitzSH. Multitarget stool DNA testing for colorectal-cancer screening. N. Engl. J. Med.371(2), 187–188 (2014).
  • Kataoka K , ShiraishiY , TakedaYet al. Aberrant PD-L1 expression through 3′-UTR disruption in multiple cancers. Nature534(7607), 402–406 (2016).
  • Ricci C , MorandiL , RighiAet al. PD-1 (PDCD1) promoter methylation in Merkel cell carcinoma: prognostic relevance and relationship with clinico-pathological parameters. Mod. Pathol.32(9), 1359–1372 (2019).
  • Goltz D , GevenslebenH , DietrichJet al. PDCD1 (PD-1) promoter methylation predicts outcome in head and neck squamous cell carcinoma patients. Oncotarget8(25), 41011–41020 (2017).
  • Goltz D , GevenslebenH , DietrichJet al. Promoter methylation of the immune checkpoint receptor PD-1 (PDCD1) is an independent prognostic biomarker for biochemical recurrence-free survival in prostate cancer patients following radical prostatectomy. Oncoimmunology5(10), e1221555 (2016).
  • Röver LK , GevenslebenH , DietrichJet al. PD-1 (PDCD1) promoter methylation is a prognostic factor in patients with diffuse lower-grade gliomas harboring isocitrate dehydrogenase (IDH) mutations. EBioMedicine28, 97–104 (2018).
  • Sannigrahi MK , SharmaR , SinghV , PandaNK , RattanV , KhullarM. Role of host miRNA Hsa-miR-139-3p in HPV-16-induced carcinomas. Clin. Cancer Res.23(14), 3884–3895 (2017).
  • Li H , ShengY , ZhangY , GaoN , DengX , ShengX. MicroRNA-138 is a potential biomarker and tumor suppressor in human cervical carcinoma by reversely correlated with TCF3 gene. Gynecol. Oncol.145(3), 569–576 (2017).
  • Huarte M , RinnJL. Large non-coding RNAs: missing links in cancer?Hum. Mol. Genet.19(R2), R152–R161 (2010).
  • Yu F , ChenB , DongP , ZhengJ. HOTAIR epigenetically modulates PTEN expression via MicroRNA-29b: a novel mechanism in regulation of liver fibrosis. Mol. Ther.25(1), 205–217 (2017).
  • Lewis BP , BurgeCB , BartelDP. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell120(1), 15–20 (2005).
  • Shao Y , ZhangD , LiXet al. MicroRNA-203 increases cell radiosensitivity via directly targeting Bmi-1 in hepatocellular carcinoma. Mol. Pharm.15(8), 3205–3215 (2018).
  • Marchese FP , RaimondiI , HuarteM. The multidimensional mechanisms of long noncoding RNA function. Genome Biol.18(1), 206 (2017).
  • Yang X , WangCC , LeeWYW , TrovikJ , ChungTKH , KwongJ. Long non-coding RNA HAND2-AS1 inhibits invasion and metastasis in endometrioid endometrial carcinoma through inactivating neuromedin U. Cancer Lett.413, 23–34 (2018).
  • Smit EF , BaasP. Lung cancer in 2015: bypassing checkpoints, overcoming resistance, and honing in on new targets. Nature reviews. Clin. Oncol.13(2), 75–76 (2016).
  • Li H , YuB , LiJet al. Overexpression of lncRNA H19 enhances carcinogenesis and metastasis of gastric cancer. Oncotarget5(8), 2318–2329 (2014).
  • Rui X , XuY , HuangY , JiL , JiangX. lncRNA DLG1-AS1 promotes cell proliferation by competitively binding with miR-107 and up-regulating ZHX1 expression in cervical cancer. Cell. Physiol. Biochem.49(5), 1792–1803 (2018).
  • Wu F , ZhaoZ , ChaiRet al. Expression profile analysis of antisense long noncoding RNA identifies WDFY3-AS2 as a prognostic biomarker in diffuse glioma. Cancer Cell Int.18, 107 (2018).
  • Wang Q , ZhangJ , LiuYet al. A novel cell cycle-associated lncRNA, HOXA11-AS, is transcribed from the 5-prime end of the HOXA transcript and is a biomarker of progression in glioma. Cancer Lett.373(2), 251–259 (2016).
  • Mineo M , RicklefsF , RoojAKet al. The long non-coding RNA HIF1A-AS2 facilitates the maintenance of mesenchymal glioblastoma stem-like cells in hypoxic niches. Cell Rep.15(11), 2500–2509 (2016).
  • Sailer V , SailerU , BawdenEGet al. DNA methylation of indoleamine 2,3-dioxygenase 1 (IDO1) in head and neck squamous cell carcinomas correlates with IDO1 expression, HPV status, patients’ survival, immune cell infiltrates, mutational load, and interferon γ signature. EBioMedicine48, 341–352 (2019).
  • Holderried TAW , de VosL , BawdenEGet al. Molecular and immune correlates of TIM-3 (HAVCR2) and galectin 9 (LGALS9) mRNA expression and DNA methylation in melanoma. Clin. Epi.11(1), 161 (2019).
  • Klümper N , RalserDJ , BawdenEGet al. LAG3 (LAG-3, CD223) DNA methylation correlates with LAG3 expression by tumor and immune cells, immune cell infiltration, and overall survival in clear cell renal cell carcinoma. J. Immunother. Cancer8(1), e000552 (2020).
  • Fröhlich A , LoickS , BawdenEGet al. Comprehensive analysis of tumor necrosis factor receptor TNFRSF9 (4-1BB) DNA methylation with regard to molecular and clinicopathological features, immune infiltrates, and response prediction to immunotherapy in melanoma. EBioMedicine52, 102647 (2020).
  • Micevic G , ThakralD , McGearyM , BosenbergMW. PD-L1 methylation regulates PD-L1 expression and is associated with melanoma survival. Pigment Cell Melanoma Res.32(3), 435–440 (2019).
  • Franzen A , VogtTJ , MüllerTet al. PD-L1 (CD274) and PD-L2 (PDCD1LG2) promoter methylation is associated with HPV infection and transcriptional repression in head and neck squamous cell carcinomas. Oncotarget9(1), 641–650 (2018).
  • de Vos L , GrünwaldI , BawdenEGet al. The landscape of CD28, CD80, CD86, CTLA4, and ICOS DNA methylation in head and neck squamous cell carcinomas. Epigenetics15(11), 1195–1212 (2020).
  • The Cancer Genome Atlas Network . Comprehensive genomic characterization of head and neck squamous cell carcinomas. Nature517(7536), 576–582 (2015).
  • Chakravarthy A , HendersonS , ThirdboroughSMet al. Human papillomavirus drives tumor development throughout the head and neck: improved prognosis is associated with an immune response largely restricted to the oropharynx. J. Clin. Oncol.34(34), 4132–4141 (2016).
  • Kandoth C , McLellanMD , VandinFet al. Mutational landscape and significance across 12 major cancer types. Nature502(7471), 333–339 (2013).
  • Edgar R , DomrachevM , LashAE. Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. 30(1), 207–210 (2002).
  • Thorsson V , GibbsDL , BrownSDet al. The immune landscape of cancer. Immunity51(2), 411–412 (2019).
  • Saltz J , GuptaR , LeHet al. Spatial organization and molecular correlation of tumor-infiltrating lymphocytes using deep learning on pathology images. Cell Reports23(1), 181–193.e7 (2018).
  • Partlová S , BoučekJ , KloudováKet al. Distinct patterns of intratumoral immune cell infiltrates in patients with HPV-associated compared to nonvirally induced head and neck squamous cell carcinoma. Oncoimmunology4(1), e965570 (2015).
  • Gavrielatou N , DoumasS , EconomopoulouP , FoukasPG , PsyrriA. Biomarkers for immunotherapy response in head and neck cancer. Cancer Treatment Rev.84, 101977 (2020).
  • Bauml JM , AggarwalC , CohenRB. Immunotherapy for head and neck cancer: where are we now and where are we going?Ann. Transl. Med.7(Suppl. 3), S75 (2019).
  • Denaro N , MerlanoMC. Immunotherapy in head and neck squamous cell cancer. Clin. Exp. Otorhinolaryngol.11(4), 217–223 (2018).
  • Saleh K , EidR , HaddadFG , Khalife-SalehN , KourieHR. New developments in the management of head and neck cancer – impact of pembrolizumab. Ther. Clin. Risk Manag.14, 295–303 (2018).
  • Lechner M , FentonTR. The genomics, epigenomics, and transcriptomics of HPV-associated oropharyngeal cancer-understanding the basis of a rapidly evolving disease. Adv. Genet.93, 1–56 (2016).
  • Lyford-Pike S , PengS , YoungGDet al. Evidence for a role of the PD-1:PD-L1 pathway in immune resistance of HPV-associated head and neck squamous cell carcinoma. Cancer Res.73(6), 1733–1741 (2013).
  • Youngblood B , OestreichKJ , HaS-Jet al. Chronic virus infection enforces demethylation of the locus that encodes PD-1 in antigen-specific CD8(+) T cells. Immunity35(3), 400–412 (2011).
  • McPherson RC , KonkelJE , PrendergastCTet al. Epigenetic modification of the PD-1 (Pdcd1) promoter in effector CD4(+) T cells tolerized by peptide immunotherapy. eLife3, e03416 (2014).
  • Ikawa T , MasudaK , EndoTAet al. Conversion of T cells to B cells by inactivation of polycomb-mediated epigenetic suppression of the B-lineage program. Genes Deve.30(22), 2475–2485 (2016).
  • Fröhlich A , SirokayJ , FietzSet al. Molecular, clinicopathological, and immune correlates of LAG3 promoter DNA methylation in melanoma. EBioMedicine59, 102962 (2020).
  • Gameiro SF , GhasemiF , BarrettJWet al. Treatment-naïve HPV+ head and neck cancers display a T-cell-inflamed phenotype distinct from their HPV- counterparts that has implications for immunotherapy. Oncoimmunology7(10), e1498439 (2018).
  • Cabili MN , TrapnellC , GoffLet al. Integrative annotation of human large intergenic noncoding RNAs reveals global properties and specific subclasses. Genes Dev.25(18), 1915–1927 (2011).
  • Guglas K , BogaczyńskaM , KolendaTet al. lncRNA in HNSCC: challenges and potential. Contemp. Oncol. (Pozn).21(4), 259–266 (2017).
  • Shi T , GaoG , CaoY. Long noncoding RNAs as novel biomarkers have a promising future in cancer diagnostics. Dis. Markers2016, 9085195 (2016).
  • Gibb EA , EnfieldKSS , StewartGLet al. Long noncoding RNAs are expressed in oral mucosa and altered in oral premalignant lesions. Oral Oncology47(11), 1055–1061 (2011).
  • Wu J , XieH. Expression of long noncoding RNA-HOX transcript antisense intergenic RNA in oral squamous cell carcinoma and effect on cell growth. Tumour Biol.36(11), 8573–8578 (2015).
  • Wu Y , ZhangL , ZhangLet al. Long non-coding RNA HOTAIR promotes tumor cell invasion and metastasis by recruiting EZH2 and repressing E-cadherin in oral squamous cell carcinoma. Int. J. Oncol.46(6), 2586–2594 (2015).
  • Dietrich D , LescheR , TetznerRet al. Analysis of DNA methylation of multiple genes in microdissected cells from formalin-fixed and paraffin-embedded tissues. J. Histochem. Cytochem.57(5), 477–489 (2009).
  • Uhl B , GevenslebenH , TolkachYet al. PITX2 DNA methylation as biomarker for individualized risk assessment of prostate cancer in core biopsies. J. Mol. Diagn.19(1), 107–114 (2017).
  • Goltz D , GevenslebenH , VogtTJet al. CTLA4 methylation predicts response to anti-PD-1 and anti-CTLA-4 immunotherapy in melanoma patients. JCI Insight3(13), e96793 (2018).
  • Li J , HanL , RoebuckPet al. TANRIC: An Interactive Open Platform to Explore the Function of lncRNAs in Cancer. Cancer Res. 75(18), 3728–3737 (2016).

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