90
Views
0
CrossRef citations to date
0
Altmetric
Research Article

A Signature Based on Chromatin Regulation and Tumor Microenvironment Infiltration in Clear Cell Renal Cell Carcinoma

ORCID Icon, &
Pages 995-1013 | Received 02 Jun 2022, Accepted 26 Aug 2022, Published online: 26 Sep 2022

References

  • Bahadoram S , DavoodiM , HassanzadehS , BahadoramM , BarahmanM , MafakherL. Renal cell carcinoma: an overview of the epidemiology, diagnosis, and treatment. G. Ital. Nefrol.39(3), (2022).
  • Gopee-Ramanan P , ChinSS , LimC , ShanbhogueKP , SchiedaN , KrishnaS. Renal neoplasms in young adults. Radiographics42(2), 433–450 (2022).
  • Kitchlu A , ReidJ , JeyakumarNet al. Cancer risk and mortality in patients with kidney disease: a population-based cohort study. Am. J. Kidney Dis. doi:10.1053/j.ajkd.2022.02.020 (2022) ( Epub ahead of print).
  • Jonasch E , WalkerCL , RathmellWK. Clear cell renal cell carcinoma ontogeny and mechanisms of lethality. Nat. Rev. Nephrol.17(4), 245–261 (2021).
  • Siegel RL , MillerKD , JemalA. Cancer statistics, 2020. CA Cancer J. Clin.70(1), 7–30 (2020).
  • Wettersten HI , AboudOA , LaraPNJr , WeissRH. Metabolic reprogramming in clear cell renal cell carcinoma. Nat. Rev. Nephrol.13(7), 410–419 (2017).
  • Williamson SR . Clear cell papillary renal cell carcinoma: an update after 15 years. Pathology53(1), 109–119 (2021).
  • Ambrosetti D , CouttsM , PaoliCet al. Cancer-associated fibroblasts in renal cell carcinoma: implication in prognosis and resistance to anti-angiogenic therapy. BJU Int.129(1), 80–92 (2022).
  • Rini BI , PlimackER , StusVet al. Pembrolizumab plus axitinib versus sunitinib for advanced renal-cell carcinoma. N. Engl. J. Med.380(12), 1116–1127 (2019).
  • Rini BI , PowlesT , AtkinsMBet al. Atezolizumab plus bevacizumab versus sunitinib in patients with previously untreated metastatic renal cell carcinoma (IMmotion151): a multicentre, open-label, phase 3, randomised controlled trial. Lancet393(10189), 2404–2415 (2019).
  • Pryor D , BresselM , LawrentschukNet al. A phase I/II study of stereotactic radiotherapy and pembrolizumab for oligometastatic renal tumours (RAPPORT): clinical trial protocol. Contemp. Clin. Trials Commun.21, 100703 (2021).
  • Miao D , MargolisCA , GaoWet al. Genomic correlates of response to immune checkpoint therapies in clear cell renal cell carcinoma. Science359(6377), 801–806 (2018).
  • Jonasch E , GaoJ , RathmellWK. Renal cell carcinoma. BMJ349, g4797 (2014).
  • Chevrier S , LevineJH , ZanotelliVRTet al. An immune atlas of clear cell renal cell carcinoma. Cell169(4), 736–749.e718 (2017).
  • Ghatalia P , GordetskyJ , KuoFet al. Prognostic impact of immune gene expression signature and tumor infiltrating immune cells in localized clear cell renal cell carcinoma. J. Immunother. Cancer7(1), 139 (2019).
  • Şenbabaoğlu Y , GejmanRS , WinerAGet al. Tumor immune microenvironment characterization in clear cell renal cell carcinoma identifies prognostic and immunotherapeutically relevant messenger RNA signatures. Genome Biol.17(1), 231 (2016).
  • Lu J , XuJ , LiJet al. FACER: comprehensive molecular and functional characterization of epigenetic chromatin regulators. Nucleic Acids Res.46(19), 10019–10033 (2018).
  • Bannister AJ , KouzaridesT. Regulation of chromatin by histone modifications. Cell Res.21(3), 381–395 (2011).
  • Plass C , PfisterSM , LindrothAM , BogatyrovaO , ClausR , LichterP. Mutations in regulators of the epigenome and their connections to global chromatin patterns in cancer. Nat. Rev. Genet.14(11), 765–780 (2013).
  • Behjati S , TarpeyPS , PresneauNet al. Distinct H3F3A and H3F3B driver mutations define chondroblastoma and giant cell tumor of bone. Nat. Genet.45(12), 1479–1482 (2013).
  • Flores LF , TaderBR , TolosaEJ , SigafoosAN , MarksDL , Fernandez-ZapicoME. Nuclear dynamics and chromatin structure: implications for pancreatic cancer. Cells10(10), 2624 (2021).
  • Zhu K , LiuX , DengW , WangG , FuB. Identification of a chromatin regulator signature and potential candidate drugs for bladder cancer. Hereditas159(1), 13 (2022).
  • Hauer MH , GasserSM. Chromatin and nucleosome dynamics in DNA damage and repair. Genes Dev.31(22), 2204–2221 (2017).
  • Reyes AA , MarcumRD , HeY. Structure and function of chromatin remodelers. J. Mol. Biol.433(14), 166929 (2021).
  • Najem A , SoumoyL , SabbahMet al. Understanding molecular mechanisms of phenotype switching and crosstalk with TME to reveal new vulnerabilities of melanoma. Cells11(7), 1157 (2022).
  • Netea MG , SchlitzerA , PlacekK , JoostenLAB , SchultzeJL. Innate and adaptive immune memory: an evolutionary continuum in the host’s response to pathogens. Cell Host Microbe25(1), 13–26 (2019).
  • Sollberger G , TilleyDO , ZychlinskyA. Neutrophil extracellular traps: the biology of chromatin externalization. Dev. Cell44(5), 542–553 (2018).
  • Wang X , WangX , XuM , ShengW. Emerging roles of long noncoding RNAs in immuno-oncology. Front. Cell Dev. Biol.9, 722904 (2021).
  • Deng M , SunS , ZhaoRet al. The pyroptosis-related gene signature predicts prognosis and indicates immune activity in hepatocellular carcinoma. Mol. Med.28(1), 16 (2022).
  • Ma T , WangJ , LiuX , ZhangW , MengL , ZhangY. m6A methylation patterns and tumor microenvironment infiltration characterization in clear-cell renal cell carcinoma. Front. Genet.13, 864549 (2022).
  • Zhang B , WuQ , LiB , WangD , WangL , ZhouYL. m(6)A regulator-mediated methylation modification patterns and tumor microenvironment infiltration characterization in gastric cancer. Mol. Cancer19(1), 53 (2020).
  • Zhuo S , ChenZ , YangY , ZhangJ , TangJ , YangK. Clinical and biological significances of a ferroptosis-related gene signature in glioma. Front. Oncol.10, 590861 (2020).
  • Ritchie ME , PhipsonB , WuDet al. limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res.43(7), e47 (2015).
  • Edeline J , MottierS , VigneauCet al. Description of 2 angiogenic phenotypes in clear cell renal cell carcinoma. Hum. Pathol.43(11), 1982–1990 (2012).
  • Wilkerson MD , HayesDN. ConsensusClusterPlus: a class discovery tool with confidence assessments and item tracking. Bioinformatics26(12), 1572–1573 (2010).
  • Hänzelmann S , CasteloR , GuinneyJ. GSVA: gene set variation analysis for microarray and RNA-seq data. BMC Bioinformatics14, 7 (2013).
  • Charoentong P , FinotelloF , AngelovaMet al. Pan-cancer immunogenomic analyses reveal genotype-immunophenotype relationships and predictors of response to checkpoint blockade. Cell Rep.18(1), 248–262 (2017).
  • Hazra A , GogtayN. Biostatistics series module 3: comparing groups: numerical variables. Indian J. Dermatol.61(3), 251–260 (2016).
  • Correa AF , JegedeO , HaasNBet al. Predicting renal cancer recurrence: defining limitations of existing prognostic models with prospective trial-based validation. J. Clin. Oncol.37(23), 2062–2071 (2019).
  • Pierce SE , KimSH , GreenleafWJ. Finding needles in a haystack: dissecting tumor heterogeneity with single-cell transcriptomic and chromatin accessibility profiling. Curr. Opin. Genet. Dev.66, 36–40 (2021).
  • Zhang L , LiangY , LiSet al. The interplay of circulating tumor DNA and chromatin modification, therapeutic resistance, and metastasis. Mol. Cancer18(1), 36 (2019).
  • Zhao S , AllisCD , WangGG. The language of chromatin modification in human cancers. Nat. Rev. Cancer21(7), 413–430 (2021).
  • Larkin J , GohXY , VetterM , PickeringL , SwantonC. Epigenetic regulation in RCC: opportunities for therapeutic intervention?Nat. Rev. Urol.9(3), 147–155 (2012).
  • Sanchez DJ , SimonMC. Genetic and metabolic hallmarks of clear cell renal cell carcinoma. Biochim. Biophys. Acta Rev. Cancer1870(1), 23–31 (2018).
  • Kwok CT , MarshallAD , RaskoJE , WongJJ. Genetic alterations of m(6)A regulators predict poorer survival in acute myeloid leukemia. J. Hematol. Oncol.10(1), 39 (2017).
  • Chen S , HeZ , PengTet al. PRR11 promotes ccRCC tumorigenesis by regulating E2F1 stability. JCI Insight6(19), e145172 (2021).
  • Du W , ZhangL , Brett-MorrisAet al. HIF drives lipid deposition and cancer in ccRCC via repression of fatty acid metabolism. Nat. Commun.8(1), 1769 (2017).
  • Ciechomska IA , JayaprakashC , MaleszewskaM , KaminskaB. Histone modifying enzymes and chromatin modifiers in glioma pathobiology and therapy responses. Adv. Exp. Med. Biol.1202, 259–279 (2020).
  • Hong SH , SonKH , HaSYet al. Nucleoporin 210 serves a key scaffold for SMARCB1 in liver cancer. Cancer Res.81(2), 356–370 (2021).
  • Okabe A , HuangKK , MatsusakaKet al. Cross-species chromatin interactions drive transcriptional rewiring in Epstein–Barr virus-positive gastric adenocarcinoma. Nat. Genet.52(9), 919–930 (2020).
  • Brownlee PM , ChambersAL , CloneyR , BianchiA , DownsJA. BAF180 promotes cohesion and prevents genome instability and aneuploidy. Cell Rep.6(6), 973–981 (2014).
  • Gerlinger M , RowanAJ , HorswellSet al. Intratumor heterogeneity and branched evolution revealed by multiregion sequencing. N. Engl. J. Med.366(10), 883–892 (2012).
  • Gu YF , CohnS , ChristieAet al. Modeling renal cell carcinoma in mice: Bap1 and Pbrm1 inactivation drive tumor grade. Cancer Discov.7(8), 900–917 (2017).
  • Turajlic S , XuH , LitchfieldKet al. Tracking cancer evolution reveals constrained routes to metastases: TRACERx Renal. Cell173(3), 581–594.e512 (2018).
  • Kim JY , LeeSH , MoonKCet al. The impact of PBRM1 expression as a prognostic and predictive marker in metastatic renal cell carcinoma. J. Urol.194(4), 1112–1119 (2015).
  • Da Costa WH , RezendeM , CarneiroFCet al. Polybromo-1 (PBRM1), a SWI/SNF complex subunit is a prognostic marker in clear cell renal cell carcinoma. BJU Int.113(5b), e157–e163 (2014).
  • Jiang W , DulaimiE , DevarajanKet al. Intratumoral heterogeneity analysis reveals hidden associations between protein expression losses and patient survival in clear cell renal cell carcinoma. Oncotarget8(23), 37423–37434 (2017).
  • Tennenbaum DM , ManleyBJ , ZaborEet al. Genomic alterations as predictors of survival among patients within a combined cohort with clear cell renal cell carcinoma undergoing cytoreductive nephrectomy. Urol. Oncol.35(8), 532.e537–532.e513 (2017).
  • Bihr S , OhashiR , MooreALet al. Expression and mutation patterns of PBRM1, BAP1 and SETD2 mirror specific evolutionary subtypes in clear cell renal cell carcinoma. Neoplasia21(2), 247–256 (2019).
  • Piva F , GiuliettiM , OcchipintiGet al. Computational analysis of the mutations in BAP1, PBRM1 and SETD2 genes reveals the impaired molecular processes in renal cell carcinoma. Oncotarget6(31), 32161–32168 (2015).
  • Qi Y , XiaY , LinZet al. Tumor-infiltrating CD39(+)CD8(+) T cells determine poor prognosis and immune evasion in clear cell renal cell carcinoma patients. Cancer Immunol. Immunother.69(8), 1565–1576 (2020).
  • Schleypen JS , Von GeldernM , WeissEHet al. Renal cell carcinoma-infiltrating natural killer cells express differential repertoires of activating and inhibitory receptors and are inhibited by specific HLA class I allotypes. Int. J. Cancer106(6), 905–912 (2003).
  • Schleypen JS , BaurN , KammererRet al. Cytotoxic markers and frequency predict functional capacity of natural killer cells infiltrating renal cell carcinoma. Clin. Cancer Res.12(3 Pt 1), 718–725 (2006).
  • Prinz PU , MendlerAN , BrechD , MasourisI , ObernederR , NoessnerE. NK-cell dysfunction in human renal carcinoma reveals diacylglycerol kinase as key regulator and target for therapeutic intervention. Int. J. Cancer135(8), 1832–1841 (2014).
  • Murphy KA , JamesBR , GuanY , TorryDS , WilberA , GriffithTS. Exploiting natural anti-tumor immunity for metastatic renal cell carcinoma. Hum. Vaccin. Immunother.11(7), 1612–1620 (2015).
  • Cózar JM , CantonJ , TalladaMet al. Analysis of NK cells and chemokine receptors in tumor infiltrating CD4 T lymphocytes in human renal carcinomas. Cancer Immunol. Immunother.54(9), 858–866 (2005).
  • Donskov F , VonDer Maase H. Impact of immune parameters on long-term survival in metastatic renal cell carcinoma. J. Clin. Oncol.24(13), 1997–2005 (2006).
  • Eckl J , BuchnerA , PrinzPUet al. Transcript signature predicts tissue NK cell content and defines renal cell carcinoma subgroups independent of TNM staging. J. Mol. Med. (Berl.)90(1), 55–66 (2012).
  • Borcherding N , VishwakarmaA , VoigtAPet al. Mapping the immune environment in clear cell renal carcinoma by single-cell genomics. Commun. Biol.4(1), 122 (2021).
  • Zhang C , HeH , HuXet al. Development and validation of a metastasis-associated prognostic signature based on single-cell RNA-seq in clear cell renal cell carcinoma. Aging (Albany NY)11(22), 10183–10202 (2019).
  • Zhang C , LiZ , QiF , HuX , LuoJ. Exploration of the relationships between tumor mutation burden with immune infiltrates in clear cell renal cell carcinoma. Ann.Transl. Med.7(22), 648 (2019).
  • Zhang L , ZhangM , WangLet al. Identification of CCL4 as an immune-related prognostic biomarker associated with tumor proliferation and the tumor microenvironment in clear cell renal cell carcinoma. Front. Oncol.11, 694664 (2021).
  • Ai L , XuA , XuJ. Roles of PD-1/PD-L1 pathway: signaling, cancer, and beyond. Adv. Exp. Med. Biol.1248, 33–59 (2020).
  • Chan TA , YarchoanM , JaffeeEet al. Development of tumor mutation burden as an immunotherapy biomarker: utility for the oncology clinic. Ann. Oncol.30(1), 44–56 (2019).
  • Huang RSP , HaberbergerJ , SeversonEet al. A pan-cancer analysis of PD-L1 immunohistochemistry and gene amplification, tumor mutation burden and microsatellite instability in 48,782 cases. Mod. Pathol.34(2), 252–263 (2021).
  • Picard E , VerschoorCP , MaGW , PawelecG. Relationships between immune landscapes, genetic subtypes and responses to immunotherapy in colorectal cancer. Front. Immunol.11, 369 (2020).
  • Samstein RM , LeeCH , ShoushtariANet al. Tumor mutational load predicts survival after immunotherapy across multiple cancer types. Nat. Genet.51(2), 202–206 (2019).
  • Kong SK , KimBS , LimH , KimHJ , KimYS. Dissection of PD-L1 promoter reveals differential transcriptional regulation of PD-L1 in VHL mutant clear cell renal cell carcinoma. Lab. Invest.102(4), 352–362 (2022).
  • Larrinaga G , Solano-IturriJD , ErrartePet al. Soluble PD-L1 is an independent prognostic factor in clear cell renal cell carcinoma. Cancers (Basel)13(4), 667 (2021).
  • Liu S , WangF , TanWet al. CTLA4 has a profound impact on the landscape of tumor-infiltrating lymphocytes with a high prognosis value in clear cell renal cell carcinoma (ccRCC). Cancer Cell Int.20, 519 (2020).
  • Möller K , FrauneC , BlessinNCet al. Tumor cell PD-L1 expression is a strong predictor of unfavorable prognosis in immune checkpoint therapy-naive clear cell renal cell cancer. Int. Urol. Nephrol.53(12), 2493–2503 (2021).

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.