Tazemetostat for Advanced Epithelioid Sarcoma: Current Status and Future Perspectives

References

• World Health Organization (WHO) Classification of Soft Tissue and Bone Tumours. International Agency for Reasearch on Cancer (IARC), Lyon, France,294–296 (2020).
   Google Scholar
• Frezza AM , BottaL, PasqualiSet al. An epidemiological insight into epithelioid sarcoma (ES): the open issue of distal-type (DES) versus proximal type (PES). Presented at: the European Society of Medical Oncology Annual MeetingMadrid, Spain8–12 September 2017.
   Google Scholar
• Chbani L , GuillouL, TerrierPet al. Epithelioid sarcoma: a clinicopathologic and immunohistochemical analysis of 106 cases from the French sarcoma group. Am. J. Clin. Pathol.131, 222–227 (2009).
   PubMed Web of Science ®Google Scholar
• Jones RL et al. Role of palliative chemotherapy in advanced epithelioid sarcoma. Am. J. Clin. Oncol.35, 351–357 (2012).
   PubMed Web of Science ®Google Scholar
• Rakheja D , WilsonKS, MeehanJ, SchultzRA, GomezAM. ‘Proximal-type’ and classic epithelioid sarcomas represent a clinicopathologic continuum: case report. Pediatr. Dev. Pathol.8, 105–114 (2005).
   PubMed Web of Science ®Google Scholar
• Armah HB , ParwaniAV. Epithelioid sarcoma. Arch. Pathol. Lab. Med.133, 814–819 (2009).
   PubMed Web of Science ®Google Scholar
• Modena P et al. SMARCB1/INI1 tumor suppressor gene is frequently inactivated in epithelioid sarcomas. Cancer Res.65, 4012–4019 (2005).
   PubMed Web of Science ®Google Scholar
• Hornick JL , DalCin P, FletcherCDM. Loss of INI1 expression is characteristic of both conventional and proximal-type epithelioid sarcoma. Am. J. Surg. Pathol.33, 542–550 (2009).
   PubMed Web of Science ®Google Scholar
• Brenca M et al. SMARCB1/INI1 genetic inactivation is responsible for tumorigenic properties of epithelioid sarcoma cell line VAESBJ. Mol. Cancer Ther.12, 1060–1072 (2013).
   PubMed Web of Science ®Google Scholar
• Sullivan LM , FolpeAL, PawelBR, JudkinsAR, BiegelJA. Epithelioid sarcoma is associated with a high percentage of SMARCB1 deletions. Mod. Pathol.26, 385–392 (2013).
   PubMed Web of Science ®Google Scholar
• Daigle S , StacchiottiS, SchöskiP, VillalobosV, CoteG, ChughT. Molecular characterization of epithelioid sarcoma (ES) tumors derived from patients enrolled in a Phase II study of tazemetostat (NCT02601950). Ann. Oncol. Off. J. Eur. Soc. Med. Oncol.29(Suppl. 8), 670–682 (2018).
   Google Scholar
• Le Loarer F et al. Consistent SMARCB1 homozygous deletions in epithelioid sarcoma and in a subset of myoepithelial carcinomas can be reliably detected by FISH in archival material. Genes Chromosomes Cancer53, 475–486 (2014).
   PubMed Web of Science ®Google Scholar
• Asano N et al. Prognostic value of relevant clinicopathologic variables in epithelioid sarcoma: a multi-institutional retrospective study of 44 patients. Ann. Surg. Oncol.22, 2624–2632 (2015).
   PubMed Web of Science ®Google Scholar
• Guillou L , WaddenC, CoindreJM, KrauszT, FletcherCD. ‘Proximal-type’ epithelioid sarcoma, a distinctive aggressive neoplasm showing rhabdoid features. Clinicopathologic, immunohistochemical, and ultrastructural study of a series. Am. J. Surg. Pathol.21, 130–146 (1997).
   PubMed Web of Science ®Google Scholar
• Hasegawa T et al. Proximal-type epithelioid sarcoma: a clinicopathologic study of 20 cases. Mod. Pathol.14, 655–663 (2001).
   PubMed Web of Science ®Google Scholar
• Frezza AM et al. The natural history of epithelioid sarcoma. A retrospective multicentre case-series within the Italian Sarcoma Group. Eur. J. Surg. Oncol.46(7), 1320–1326 (2020).
   PubMed Web of Science ®Google Scholar
• Frezza AM et al. Anthracycline, gemcitabine, and pazopanib in epithelioid sarcoma: a multi-institutional case series. JAMA Oncol.4, e180219–e180219 (2018).
   PubMed Web of Science ®Google Scholar
• Chase DR , EnzingerFM. Epithelioid sarcoma. Diagnosis, prognostic indicators, and treatment. Am. J. Surg. Pathol.9, 241–263 (1985).
   PubMed Web of Science ®Google Scholar
• Fisher C . Epithelioid sarcoma of Enzinger. Adv. Anat. Pathol.13, 114–121 (2006).
   PubMed Web of Science ®Google Scholar
• Evans HL , BaerSC. Epithelioid sarcoma: a clinicopathologic and prognostic study of 26 cases. Semin. Diagn. Pathol.10, 286–291 (1993).
   PubMed Web of Science ®Google Scholar
• Baratti D et al. Epithelioid sarcoma: prognostic factors and survival in a series of patients treated at a single institution. Ann. Surg. Oncol.14, 3542–3551 (2007).
   PubMed Web of Science ®Google Scholar
• Jawad MU , ExteinJ, MinES, ScullySP. Prognostic factors for survival in patients with epithelioid sarcoma: 441 cases from the SEER database. Clin. Orthop. Relat. Res.467, 2939–2948 (2009).
   PubMed Web of Science ®Google Scholar
• Wolf PS , FlumDR, TanasMR, RubinBP, MannGN. Epithelioid sarcoma: the University of Washington experience. Am. J. Surg.196, 407–412 (2008).
   PubMed Web of Science ®Google Scholar
• Shimm DS , SuitHD. Radiation therapy of epithelioid sarcoma. Cancer52, 1022–1025 (1983).
   PubMed Web of Science ®Google Scholar
• Livi L et al. Treatment of epithelioid sarcoma at the royal marsden hospital. Sarcoma7, 149–152 (2003).
   PubMedGoogle Scholar
• Neuwirth MG et al. Isolated limb perfusion and infusion for extremity soft tissue sarcoma: a contemporary systematic review and meta-analysis. Ann. Surg. Oncol.24, 3803–3810 (2017).
   PubMed Web of Science ®Google Scholar
• Ross HM , LewisJJ, WoodruffJM, BrennanMF. Epithelioid sarcoma: clinical behavior and prognostic factors of survival. Ann. Surg. Oncol.4, 491–495 (1997).
   PubMed Web of Science ®Google Scholar
• Spillane AJ Thomas JM , FisherC. Epithelioid sarcoma: the clinicopathological complexities of this rare soft tissue sarcoma. Ann. Surg. Oncol.7, 218–225 (2000).
   PubMed Web of Science ®Google Scholar
• Schmitt T , KasperB. New medical treatment options and strategies to assess clinical outcome in soft-tissue sarcoma. Expert Rev. Anticancer Ther.9, 1159–1167 (2009).
   PubMed Web of Science ®Google Scholar
• Pink D et al. Gemcitabine and docetaxel for epithelioid sarcoma: results from a retrospective, multi-institutional analysis. Oncology87, 95–103 (2014).
   PubMed Web of Science ®Google Scholar
• Irimura S et al. Successful treatment with pazopanib for multiple lung metastases of inguinal epithelioid sarcoma: a case report. Case Rep. Oncol.8, 378–384 (2015).
   PubMedGoogle Scholar
• Touati N et al. European Organisation for research and treatment of cancer soft tissue and Bone Sarcoma Group experience with advanced/metastatic epithelioid sarcoma patients treated in prospective trials: clinical profile and response to systemic therapy. Clin. Oncol. (R. Coll. Radiol).30, 448–454 (2018).
   PubMed Web of Science ®Google Scholar
• Nakamura T et al. The clinical outcome of pazopanib treatment in Japanese patients with relapsed soft tissue sarcoma: a Japanese Musculoskeletal Oncology Group (JMOG) study. Cancer122, 1408–1416 (2016).
   PubMed Web of Science ®Google Scholar
• Geoerger B et al. Pembrolizumab in paediatric patients with advanced melanoma or a PD-L1-positive, advanced, relapsed, or refractory solid tumour or lymphoma (KEYNOTE-051): interim analysis of an open-label, single-arm, Phase I–II trial. Lancet Oncol.21, 121–133 (2020).
   PubMed Web of Science ®Google Scholar
• Gounder M , SchöffskiP, JonesRLet al. Tazemetostat in advanced epithelioid sarcoma with INI1/SMARCB1 loss: results from an international, open-label, Phase II basket study. Lancet Oncol.21, 1423–1432 (2020).
   PubMed Web of Science ®Google Scholar
• Masliah-Planchon J , BiècheI, GuinebretièreJ-M, BourdeautF, DelattreO. SWI/SNF chromatin remodeling and human malignancies. Annu. Rev. Pathol.10, 145–171 (2015).
   PubMed Web of Science ®Google Scholar
• Huether R et al. The landscape of somatic mutations in epigenetic regulators across 1,000 paediatric cancer genomes. Nat. Commun.5, 3630 (2014).
   PubMed Web of Science ®Google Scholar
• Dalgliesh GL et al. Systematic sequencing of renal carcinoma reveals inactivation of histone modifying genes. Nature463, 360–363 (2010).
   PubMed Web of Science ®Google Scholar
• Simon JA , TamkunJW. Programming off and on states in chromatin: mechanisms of polycomb and trithorax group complexes. Curr. Opin. Genet. Dev.12, 210–218 (2002).
   PubMed Web of Science ®Google Scholar
• Mu W , StarmerJ, YeeD, MagnusonT. EZH2 variants differentially regulate polycomb repressive complex 2 in histone methylation and cell differentiation. Epigenetics Chromatin11, 71 (2018).
   PubMed Web of Science ®Google Scholar
• Cao R et al. Role of histone H3 lysine 27 methylation in polycomb-group silencing. Science298, 1039–1043 (2002).
   PubMed Web of Science ®Google Scholar
• Müller J et al. Histone methyltransferase activity of a Drosophila polycomb group repressor complex. Cell111, 197–208 (2002).
   PubMed Web of Science ®Google Scholar
• Czermin B et al. Drosophila enhancer of Zeste/ESC complexes have a histone H3 methyltransferase activity that marks chromosomal polycomb sites. Cell111, 185–196 (2002).
   PubMed Web of Science ®Google Scholar
• Viré E et al. The Polycomb group protein EZH2 directly controls DNA methylation. Nature439, 871–874 (2006).
   PubMed Web of Science ®Google Scholar
• Margueron R , ReinbergD. The polycomb complex PRC2 and its mark in life. Nature469, 343–349 (2011).
   PubMed Web of Science ®Google Scholar
• Di Croce L , HelinK. Transcriptional regulation by polycomb group proteins. Nat. Struct. Mol. Biol.20, 1147–1155 (2013).
   PubMed Web of Science ®Google Scholar
• Wilson BG et al. Epigenetic antagonism between polycomb and SWI/SNF complexes during oncogenic transformation. Cancer Cell18, 316–328 (2010).
   PubMed Web of Science ®Google Scholar
• Kadoch C , CopelandRA, KeilhackH. PRC2 and SWI/SNF chromatin remodeling complexes in health and disease. Biochemistry55, 1600–1614 (2016).
   PubMed Web of Science ®Google Scholar
• Kim KH , RobertsCWM. Targeting EZH2 in cancer. Nat. Med.22, 128–134 (2016).
   PubMed Web of Science ®Google Scholar
• Yamagishi M , UchimaruK. Targeting EZH2 in cancer therapy. Curr. Opin. Oncol.29, 375–381 (2017).
   PubMed Web of Science ®Google Scholar
• Karantanos T , ChistofidesA, BarhdanK, LiL, BoussiotisVA. Regulation of T cell differentiation and function by EZH2. Front. Immunol.7, 172 (2016).
   PubMed Web of Science ®Google Scholar
• Völkel P , DupretB, LeBourhis X, AngrandP-O. Diverse involvement of EZH2 in cancer epigenetics. Am. J. Transl. Res.7, 175–193 (2015).
   PubMed Web of Science ®Google Scholar
• Workman JL , KingstonRE. Alteration of nucleosome structure as a mechanism of transcriptional regulation. Annu. Rev. Biochem.67, 545–579 (1998).
   PubMed Web of Science ®Google Scholar
• Kadoch C et al. Proteomic and bioinformatic analysis of mammalian SWI/SNF complexes identifies extensive roles in human malignancy. Nat. Genet.45, 592–601 (2013).
   PubMed Web of Science ®Google Scholar
• Versteege I et al. Truncating mutations of hSNF5/INI1 in aggressive paediatric cancer. Nature394, 203–206 (1998).
   PubMed Web of Science ®Google Scholar
• Knutson SK et al. Durable tumor regression in genetically altered malignant rhabdoid tumors by inhibition of methyltransferase EZH2. Proc. Natl Acad. Sci. USA110, 7922–7927 (2013).
   PubMed Web of Science ®Google Scholar
• Brach D et al. EZH2 inhibition by tazemetostat results in altered dependency on B-cell activation signaling in DLBCL. Mol. Cancer Ther.16, 2586–2597 (2017).
   PubMed Web of Science ®Google Scholar
• Tiffen JC et al. Targeting activating mutations of EZH2 leads to potent cell growth inhibition in human melanoma by derepression of tumor suppressor genes. Oncotarget6, 27023–27036 (2015).
   PubMedGoogle Scholar
• Ciarapica R et al. The Polycomb Group (PcG) protein EZH2 supports the survival of PAX3–FOXO1 alveolar rhabdomyosarcoma by repressing FBXO32 (Atrogin1/MAFbx). Oncogene33, 4173–4184 (2014).
   PubMed Web of Science ®Google Scholar
• Sun R et al. Overexpression of EZH2 is associated with the poor prognosis in osteosarcoma and function analysis indicates a therapeutic potential. Oncotarget7, 38333–38346 (2016).
   PubMedGoogle Scholar
• Honma D et al. Novel orally bioavailable EZH1/2 dual inhibitors with greater antitumor efficacy than an EZH2 selective inhibitor. Cancer Sci.108, 2069–2078 (2017).
   PubMed Web of Science ®Google Scholar
• Stacchiotti S et al. Comparative assessment of antitumor effects and autophagy induction as a resistance mechanism by cytotoxics and EZH2 inhibition in INI1-negative epithelioid sarcoma patient-derived xenograft. Cancers (Basel).11, 1015 (2019).
   PubMed Web of Science ®Google Scholar
• Italiano A et al. Tazemetostat, an EZH2 inhibitor, in relapsed or refractory B-cell non-Hodgkin lymphoma and advanced solid tumours: a first-in-human, open-label, Phase I study. Lancet Oncol.19, 649–659 (2018).
   PubMed Web of Science ®Google Scholar
• Hoy SM . Tazemetostat: first approval. Drugs80, 513–521 (2020).
   PubMed Web of Science ®Google Scholar
• Epizyme Inc . Tazverik (tazemetostat) tablets, for oral use: US prescribing information. (2020). https://www.accessdata.fda.gov/drugsatfda_docs/label/2020/211723s000lbl.pdf
   Google Scholar
• Agulnik M et al. A Phase II, multicenter study of the EZH2 inhibitor tazemetostat in adult subjects with INI1-negative tumors or relapsed/refractory synovial sarcoma. J. Clin. Oncol.34, TPS11071–TPS11071 (2016).
   Web of Science ®Google Scholar
• National Cancer Institute . Protocol development: Cancer Therapy Evaluation Program. (2013). http://ctep.cancer.gov/protocoldevelopment/electronic_applications/ctc.htm#ctc_40
   Google Scholar
• US FDA . Briefing document for the December 18, 2019 US FDA Oncologic Drugs Advisory Committee meeting: tazemetostat. (2019). https://www.fda.gov/media/133573/download
   Google Scholar
• Sanchez-Martin M , FerrandoA. The NOTCH1-MYC highway toward T-cell acute lymphoblastic leukemia. Blood129, 1124–1133 (2017).
   PubMed Web of Science ®Google Scholar
• Palmer S , AlberganteL, BlackburnCC, NewmanTJ. Thymic involution and rising disease incidence with age. Proc. Natl Acad. Sci. USA115, 1883–1888 (2018).
   PubMed Web of Science ®Google Scholar
• US FDA . FDA approves first treatment option specifically for patients with epithelioid sarcoma, a rare soft tissue cancer. (2020). http://www.fda.gov/
   Google Scholar
• US FDA . FDA approves tazemetostat for advanced epithelioid sarcoma. (2020). https://www.fda.gov/
   Google Scholar
• Bai J et al. Inhibition enhancer of zeste homologue 2 promotes senescence and apoptosis induced by doxorubicin in p53 mutant gastric cancer cells. Cell Prolif.47, 211–218 (2014).
   PubMed Web of Science ®Google Scholar
• Ennishi D et al. Molecular and genetic characterization of MHC deficiency identifies EZH2 as therapeutic target for enhancing immune recognition. Cancer Discov.9, 546–563 (2019).
   PubMed Web of Science ®Google Scholar
• Zingg D et al. The histone methyltransferase Ezh2 controls mechanisms of adaptive resistance to tumor immunotherapy. Cell Rep.20, 854–867 (2017).
   PubMed Web of Science ®Google Scholar
• Zhou L , MudiantoT, MaX, RileyR, UppaluriR. Targeting EZH2 enhances antigen presentation, antitumor immunity, and circumvents anti-PD-1 resistance in head and neck cancer. Clin. Cancer Res.26, 290–300 (2020).
   PubMed Web of Science ®Google Scholar
• Jamshidi F et al. The genomic landscape of epithelioid sarcoma cell lines and tumours. J. Pathol.238, 63–73 (2016).
   PubMed Web of Science ®Google Scholar
• Gounder MM et al. Immunologic correlates of the abscopal effect in a SMARCB1/INI1-negative poorly differentiated chordoma after EZH2 inhibition and radiotherapy. Clin. Cancer Res.25, 2064–2071 (2019).
   PubMed Web of Science ®Google Scholar
• Italiano A . Targeting epigenetics in sarcomas through EZH2 inhibition. J. Hematol. Oncol.13, 33 (2020).
   PubMed Web of Science ®Google Scholar
• DuPage M et al. The chromatin-modifying enzyme Ezh2 is critical for the maintenance of regulatory T cell identity after activation. Immunity42, 227–238 (2015).
   PubMed Web of Science ®Google Scholar
• Sápi Z et al. Epigenetic regulation of SMARCB1 By miR-206, -381 and -671-5p is evident in a variety of SMARCB1 immunonegative soft tissue sarcomas, while miR-765 appears specific for epithelioid sarcoma. A miRNA study of 223 soft tissue sarcomas. Genes Chromosomes Cancer55, 786–802 (2016).
   PubMed Web of Science ®Google Scholar
• Papp G , KrauszT, StrickerTP, SzendrőiM, SápiZ. SMARCB1 expression in epithelioid sarcoma is regulated by miR-206, miR-381, and miR-671-5p on Both mRNA and protein levels. Genes Chromosomes Cancer53, 168–176 (2014).
   PubMed Web of Science ®Google Scholar
• Kohashi K et al. Differential microRNA expression profiles between malignant rhabdoid tumor and epithelioid sarcoma: miR193a-5p is suggested to downregulate SMARCB1 mRNA expression. Mod. Pathol.27, 832–839 (2014).
   PubMed Web of Science ®Google Scholar
• Kohashi K et al. SWI/SNF chromatin-remodeling complex status in SMARCB1/INI1-preserved epithelioid sarcoma. Am. J. Surg. Pathol.42, 312–318 (2018).
   PubMed Web of Science ®Google Scholar