CLC number:
On-line Access: 2021-08-20
Received: 2020-12-09
Revision Accepted: 2021-03-19
Crosschecked: 0000-00-00
Cited: 0
Clicked: 3776
Chunhui LI, Chunhong WANG. LG-ESSs and HG-ESSs: underlying molecular alterations and potential therapeutic strategies[J]. Journal of Zhejiang University Science B, 2021, 22(8): 633-646.
@article{title="LG-ESSs and HG-ESSs: underlying molecular alterations and potential therapeutic strategies",
author="Chunhui LI, Chunhong WANG",
journal="Journal of Zhejiang University Science B",
volume="22",
number="8",
pages="633-646",
year="2021",
publisher="Zhejiang University Press & Springer",
doi="10.1631/jzus.B2000797"
}
%0 Journal Article
%T LG-ESSs and HG-ESSs: underlying molecular alterations and potential therapeutic strategies
%A Chunhui LI
%A Chunhong WANG
%J Journal of Zhejiang University SCIENCE B
%V 22
%N 8
%P 633-646
%@ 1673-1581
%D 2021
%I Zhejiang University Press & Springer
%DOI 10.1631/jzus.B2000797
TY - JOUR
T1 - LG-ESSs and HG-ESSs: underlying molecular alterations and potential therapeutic strategies
A1 - Chunhui LI
A1 - Chunhong WANG
J0 - Journal of Zhejiang University Science B
VL - 22
IS - 8
SP - 633
EP - 646
%@ 1673-1581
Y1 - 2021
PB - Zhejiang University Press & Springer
ER -
DOI - 10.1631/jzus.B2000797
Abstract: Endometrial stromal tumors (ESTs) include endometrial stromal nodule (ESN), low-grade endometrial stromal sarcoma (LG-ESS), high-grade endometrial stromal sarcoma (HG-ESS), and undifferentiated uterine sarcoma (UUS). Since these are rare tumor types, there is an unmet clinical need for the systematic therapy of advanced LG-ESS or HG-ESS. Cytogenetic and molecular advances in ESTs have shown that multiple recurrent gene fusions are present in a large proportion of LG-ESSs, and HG-ESSs are identified by the tyrosine 3-monooxygenase/tryptophan 5-monooxygenase activation protein epsilon (YWHAE)-family with sequence similarity 22 (FAM22) fusion. Recently, a group of ESSs harboring both zinc finger CCCH domain-containing protein 7B (ZC3H7B)-B-cell lymphoma 6 corepressor (BCOR) fusion and internal tandem duplication (ITD) of the BCOR gene have been provisionally classified as HG-ESSs. In this review, we firstly describe current knowledge about the molecular characteristics of recurrent aberrant proteins and their roles in the tumorigenesis of LG-ESSs and HG-ESSs. Next, we summarize the possibly shared signal pathways in the tumorigenesis of LG-ESSs and HG-ESSs, and list potentially actionable targets. Finally, based on the above discussion, we propose a few promising therapeutic strategies for LG-ESSs and HG-ESSs with recurrent gene alterations.
[1]Abu-RustumNR, 2021. Uterine Neoplasms Version 1.2021. NCCN Clinical Practice Guidelines in Oncology.NCCN Guidelines®.https://www.nccn.org/guidelines/guidelines-detail?category=1&id=1473
[2]AllenAJ, AliSM, GowenK, et al., 2017. A recurrent endometrial stromal sarcoma harbors the novel fusion JAZF1-BCORL1. Gynecol Oncol Rep, 20:51-53.
[3]AstolfiA, FioreM, MelchiondaF, et al., 2019. BCOR involvement in cancer. Epigenomics, 11(7):835-855.
[4]AttarN, KurdistaniSK, 2017. Exploitation of EP300 and CREBBP lysine acetyltransferases by cancer. Cold Spring Harb Perspect Med, 7(3):a026534.
[5]AvvakumovN, CôtéJ, 2007. The MYST family of histone acetyltransferases and their intimate links to cancer. Oncogene, 26(37):5395-5407.
[6]BaekMH, ParkJY, RhimCC, et al., 2016. Immunohistochemical characterization of histone deacetylase as a potential prognostic marker and therapeutic target in endometrial stromal sarcoma. Anticancer Res, 36(5):2527-2534.
[7]BirveA, SenguptaAK, BeuchleD, et al., 2001. Su(z)12, a novel Drosophila Polycomb group gene that is conserved in vertebrates and plants. Development, 128(17):3371-3379.
[8]BoudreaultAA, CronierD, SelleckW, et al., 2003. Yeast Enhancer of Polycomb defines global Esa1-dependent acetylation of chromatin. Genes Dev, 17(11):1415-1428.
[9]BrandtLP, AlbersJ, HejhalT, et al., 2017. Oncogenic HrasG12V expression plus knockdown of Cdkn2a using ecotropic lentiviral vectors induces high-grade endometrial stromal sarcoma. PLoS ONE, 12(10):e0186102.
[10]BrunetA, KanaiF, StehnJ, et al., 2002. 14-3-3 transits to the nucleus and participates in dynamic nucleocytoplasmic transport. J Cell Biol, 156(5):817-828.
[11]BrunettiM, GorunovaL, DavidsonB, et al., 2018. Identification of an EPC2-PHF1 fusion transcript in low-grade endometrial stromal sarcoma. Oncotarget, 9(27):19203-19208.
[12]CastañedaA, SerranoC, Hernández-TrejoJA, et al., 2017. pVHL suppresses Akt/β-catenin-mediated cell proliferation by inhibiting 14-3-3ζ expression. Biochem J, 474(16):2679-2689.
[13]ChamberlainPP, HamannLG, 2019. Development of targeted protein degradation therapeutics. Nat Chem Biol, 15(10):937-944.
[14]ChammasP, MocaviniI, di CroceL, 2020. Engaging chromatin: PRC2 structure meets function. Br J Cancer, 122(3):315-328.
[15]CheXH, ChenH, XuZM, et al., 2010. 14-3-3epsilon contributes to tumour suppression in laryngeal carcinoma by affecting apoptosis and invasion. BMC Cancer, 10:306.
[16]ChenSM, JiaoLY, ShubbarM, et al., 2018. Unique structural platforms of Suz12 dictate distinct classes of PRC2 for chromatin binding. Mol Cell, 69(5):840-852.e5.
[17]ChiangS, AliR, MelnykN, et al., 2011. Frequency of known gene rearrangements in endometrial stromal tumors. Am J Surg Pathol, 35(9):1364-1372.
[18]ChiangS, LeeCH, StewartCJR, et al., 2017. BCOR is a robust diagnostic immunohistochemical marker of genetically diverse high-grade endometrial stromal sarcoma, including tumors exhibiting variant morphology. Mod Pathol, 30(9):1251-1261.
[19]ChoiJ, BachmannAL, TauscherK, et al., 2017. DNA binding by PHF1 prolongs PRC2 residence time on chromatin and thereby promotes H3K27 methylation. Nat Struct Mol Biol, 24(12):1039-1047.
[20]ChoiYJ, JungSH, KimMS, et al., 2015. Genomic landscape of endometrial stromal sarcoma of uterus. Oncotarget, 6(32):33319-33328.
[21]ConklinCMJ, LongacreTA, 2014. Endometrial stromal tumors: the new WHO classification. Adv Anat Pathol, 21(6):383-393.
[22]ConwaySJ, 2020. Bifunctional molecules beyond PROTACs. J Med Chem, 63(6):2802-2806.
[23]Cossu-RoccaP, ContiniM, UrasMG, et al., 2012. Tyrosine kinase receptor status in endometrial stromal sarcoma: an immunohistochemical and genetic-molecular analysis. Int J Gynecol Pathol, 31(6):570-579.
[24]CotziaP, BenayedR, MullaneyK, et al., 2019. Undifferentiated uterine sarcomas represent under-recognized high-grade endometrial stromal sarcomas. Am J Surg Pathol, 43(5):662-669.
[25]DeshmukhU, BlackJ, Perez-IrizarryJ, et al., 2019. Adjuvant hormonal therapy for low-grade endometrial stromal sarcoma. Reprod Sci, 26(5):600-608.
[26]DewaeleB, PrzybylJ, QuattroneA, et al., 2014. Identification of a novel, recurrent MBTD1-CXorf67 fusion in low-grade endometrial stromal sarcoma. Int J Cancer, 134(5):1112-1122.
[27]DicksonBC, LumA, SwansonD, et al., 2018. Novel EPC1 gene fusions in endometrial stromal sarcoma. Genes Chromosomes Cancer, 57(11):598-603.
[28]EryilmazJ, PanP, AmayaMF, et al., 2009. Structural studies of a four-MBT repeat protein MBTD1. PLoS ONE, 4(10):e7274.
[29]FerreiraJ, FélixA, LennerzJK, et al., 2018. Recent advances in the histological and molecular classification of endometrial stromal neoplasms. Virchows Arch, 473(6):665-678.
[30]FröhlichLF, MrakovcicM, SmoleC, et al., 2014. Epigenetic silencing of apoptosis-inducing gene expression can be efficiently overcome by combined SAHA and TRAIL treatment in uterine sarcoma cells. PLoS ONE, 9(3):e91558.
[31]FroimchukE, JangY, GeK, 2017. Histone H3 lysine 4 methyltransferase KMT2D. Gene, 627:337-342.
[32]HanLS, LiuYJ, RicciottiRW, et al., 2020. A novel MBTD1-PHF1 gene fusion in endometrial stromal sarcoma: a case report and literature review. Genes Chromosomes Cancer, 59(7):428-432.
[33]HarbM, BeckerMM, VitourD, et al., 2008. Nuclear localization of cytoplasmic poly(A)-binding protein upon rotavirus infection involves the interaction of NSP3 with eIF4G and RoXaN. J Virol, 82(22):11283-11293.
[34]HashizumeR, AndorN, IharaY, et al., 2014. Pharmacologic inhibition of histone demethylation as a therapy for pediatric brainstem glioma. Nat Med, 20(12):1394-1396.
[35]HassanAH, ProchassonP, NeelyKE, et al., 2002. Function and selectivity of bromodomains in anchoring chromatin-modifying complexes to promoter nucleosomes. Cell, 111(3):369-379.
[36]HennigY, CaselitzJ, BartnitzkeS, et al., 1997. A third case of a low-grade endometrial stromal sarcoma with at(7;17)(p14~21;q11.2~21). Cancer Genet Cytogenet, 98(1):84-86.
[37]HoangLN, AnejaA, ConlonN, et al., 2017. Novel high-grade endometrial stromal sarcoma: a morphologic mimicker of myxoid leiomyosarcoma. Am J Surg Pathol, 41(1):12-24.
[38]HrzenjakA, 2016. JAZF1/SUZ12 gene fusion in endometrial stromal sarcomas. Orphanet J Rare Dis, 11:15.
[39]HrzenjakA, MoinfarF, KremserML, et al., 2006. Valproate inhibition of histone deacetylase 2 affects differentiation and decreases proliferation of endometrial stromal sarcoma cells. Mol Cancer Ther, 5(9):2203-2210.
[40]HsuJHR, RasmussonT, RobinsonJ, et al., 2020. EED-targeted PROTACs degrade EED, EZH2, and SUZ12 in the PRC2 complex. Cell Chem Biol, 27(1):41-46.e17.
[41]HübnerJM, MüllerT, PapageorgiouDN, et al., 2019. EZHIP/CXorf67 mimics K27M mutated oncohistones and functions as an intrinsic inhibitor of PRC2 function in aggressive posterior fossa ependymoma. Neuro-Oncol, 21(7):878-889.
[42]HungMC, LinkW, 2011. Protein localization in disease and therapy. J Cell Sci, 124(Pt 20):3381-3392.
[43]JacquetK, Fradet-TurcotteA, AvvakumovN, et al., 2016. The TIP60 complex regulates bivalent chromatin recognition by 53BP1 through direct H4K20me binding and H2AK15 acetylation. Mol Cell, 62(3):409-421.
[44]KalenderME, SevincA, YilmazM, et al., 2009. Detection of complete response to imatinib mesylate (Glivec®/Gleevec®) with 18F-FDG PET/CT for low-grade endometrial stromal sarcoma. Cancer Chemother Pharmacol, 63(3):555-559.
[45]KaoYC, SungYS, ArganiP, et al., 2020. NTRK3 overexpression in undifferentiated sarcomas with YWHAE and BCOR genetic alterations. Mod Pathol, 33(7):1341-1349.
[46]KennyC, McDonaghN, LazaroA, et al., 2018. Dysregulated mitogen-activated protein kinase signalling as an oncogenic basis for clear cell sarcoma of the kidney. J Pathol, 244(3):334-345.
[47]KhotskayaYB, HollaVR, FaragoAF, et al., 2017. Targeting TRK family proteins in cancer. Pharmacol Ther, 173:58-66.
[48]KimKO, HsuAC, LeeHG, et al., 2014. Proteomic identification of 14-3-3ϵas a linker protein between pERK1/2 inhibition and BIM upregulation in human osteosarcoma cells . J Orthop Res, 32(6):848-854.
[49]KommossFKF, StichelD, SchrimpfD, et al., 2020a. DNA methylation-based profiling of uterine neoplasms: a novel tool to improve gynecologic cancer diagnostics. J Cancer Res Clin Oncol, 146(1):97-104.
[50]KommossFKF, ChangKTE, StichelD, et al., 2020b. Endometrial stromal sarcomas with BCOR-rearrangement harbor MDM2 amplifications. J Pathol Clin Res, 6(3):178-184.
[51]LaiAC, ToureM, HellerschmiedD, et al., 2016. Modular PROTAC design for the degradation of oncogenic BCR-ABL. Angew Chem Int Ed Engl, 55(2):807-810.
[52]LealMF, RibeiroHF, ReyJA, et al., 2016. YWHAE silencing induces cell proliferation, invasion and migration through the up-regulation of CDC25B and MYC in gastric cancer cells: new insights about YWHAE role in the tumor development and metastasis process. Oncotarget, 7(51):85393-85410.
[53]LeeCH, OuWB, Mariño-EnriquezA, et al., 2012. 14-3-3 fusion oncogenes in high-grade endometrial stromal sarcoma. Proc Natl Acad Sci USA, 109(3):929-934.
[54]LeeCH, HoangLN, YipS, et al., 2014. Frequent expression of KIT in endometrial stromal sarcoma with YWHAE genetic rearrangement. Mod Pathol, 27(5):751-757.
[55]LeeW, TeckieS, WiesnerT, et al., 2014. PRC2 is recurrently inactivated through EED or SUZ12 loss in malignant peripheral nerve sheath tumors. Nat Genet, 46(11):1227-1232.
[56]LewisN, SoslowRA, DelairDF, et al., 2018. ZC3H7B-BCOR high-grade endometrial stromal sarcomas: a report of 17 cases of a newly defined entity. Mod Pathol, 31(4):674-684.
[57]LiH, MaXY, WangJL, et al., 2007. Effects of rearrangement and allelic exclusion of JJAZ1/SUZ12 on cell proliferation and survival. Proc Natl Acad Sci USA, 104(50):20001-20006.
[58]LiangSF, XuYH, ShenGB, et al., 2009. Quantitative protein expression profiling of 14-3-3 isoforms in human renal carcinoma shows 14-3-3 epsilon is involved in limitedly increasing renal cell proliferation.Electrophoresis, 30(23):4152-4162.
[59]LinDI, HemmerichA, EdgerlyC, et al., 2020. Genomic profiling of BCOR-rearranged uterine sarcomas reveals novel gene fusion partners, frequent CDK4 amplification and CDKN2A loss. Gynecol Oncol, 157(2):357-366.
[60]LiuRQ, GaoJ, YangY, et al., 2018. PHD finger protein 1 (PHF1) is a novel reader for histone H4R3 symmetric dimethylation and coordinates with PRMT5-WDR77/CRL4B complex to promote tumorigenesis. Nucleic Acids Res, 46(13):6608-6626.
[61]LiuTA, JanYJ, KoBS, et al., 2013. 14-3-3ε overexpression contributes to epithelial-mesenchymal transition of hepatocellular carcinoma. PLoS ONE, 8(3):e57968.
[62]MaXY, WangJL, WangJH, et al., 2017. The JAZF1-SUZ12 fusion protein disrupts PRC2 complexes and impairs chromatin repression during human endometrial stromal tumorogenesis. Oncotarget, 8(3):4062-4078.
[63]MakiseN, SekimizuM, KobayashiE, et al., 2019. Low-grade endometrial stromal sarcoma with a novel MEAF6-SUZ12 fusion. Virchows Arch, 475(4):527-531.
[64]Mariño-EnriquezA, LauriaA, PrzybylJ, et al., 2018. BCOR internal tandem duplication in high-grade uterine sarcomas. Am J Surg Pathol, 42(3):335-341.
[65]MauriD, PavlidisN, PolyzosNP, et al., 2006. Survival with aromatase inhibitors and inactivators versus standard hormonal therapy in advanced breast cancer: meta-analysis. J Natl Cancer Inst, 98(18):1285-1291.
[66]MeiJW, YangZY, XiangHG, et al., 2019. MicroRNA-1275 inhibits cell migration and invasion in gastric cancer by regulating vimentin and E-cadherin via JAZF1. BMC Cancer, 19:740.
[67]MicciF, PanagopoulosI, BjerkehagenB, et al., 2006. Consistent rearrangement of chromosomal band 6p21 with generation of fusion genes JAZF1/PHF1 and EPC1/PHF1 in endometrial stromal sarcoma. Cancer Res, 66(1):107-112.
[68]MicciF, GorunovaL, GatiusS, et al., 2014. MEAF6/PHF1 is a recurrent gene fusion in endometrial stromal sarcoma. Cancer Lett, 347(1):75-78.
[69]MicciF, BrunettiM, dal CinP, et al., 2017. Fusion of the genes BRD8 and PHF1 in endometrial stromal sarcoma. Genes Chromosomes Cancer, 56(12):841-845.
[70]MondenT, WondisfordFE, HollenbergAN, 1997. Isolation and characterization of a novel ligand-dependent thyroid hormone receptor-coactivating protein. J Biol Chem, 272(47):29834-29841.
[71]OppelF, KiDH, ZimmermanMW, et al., 2020. suz12 inactivation in p53- and nf1-deficient zebrafish accelerates the onset of malignant peripheral nerve sheath tumors and expands the spectrum of tumor types. Dis Model Mech, 13(8):dmm042341.
[72]PanagopoulosI, MertensF, GriffinCA, 2008. An endometrial stromal sarcoma cell line with the JAZF1/PHF1 chimera. Cancer Genet Cytogenet, 185(2):74-77.
[73]PanagopoulosI, MicciF, ThorsenJ, et al., 2012. Novel fusion of MYST/Esa1-associated factor 6 and PHF1 in endometrial stromal sarcoma. PLoS ONE, 7(6):e39354.
[74]PanagopoulosI, ThorsenJ, GorunovaL, et al., 2013. Fusion of the ZC3H7B and BCOR genes in endometrial stromal sarcomas carrying an X;22-translocation. Genes Chromosomes Cancer, 52(7):610-618.
[75]PatelRB, LiT, LiaoZ, et al., 2017. Recent translational research into targeted therapy for liposarcoma. Stem Cell Investig, 4:21.
[76]PatelSB, McCormackC, HodgeJC, 2020. Non-fusion mutations in endometrial stromal sarcomas: what is the potential impact on tumourigenesis through cell cycle dysregulation? J Clin Pathol, 73(12):830-835.
[77]PiuntiA, SmithER, MorganMAJ, et al., 2019. CATACOMB: an endogenous inducible gene that antagonizes H3K27 methylation activity of Polycomb repressive complex 2 via an H3K27M-like mechanism. Sci Adv, 5(7):eaax2887.
[78]PotjewydF, TurnerAMW, BeriJ, et al., 2020. Degradation of polycomb repressive complex 2 with an EED-targeted bivalent chemical degrader. Cell Chem Biol, 27(1):47-56.e15.
[79]Prieto-GranadaCN, WiesnerT, MessinaJL, et al., 2016. Loss of H3K27me3 expression is a highly sensitive marker for sporadic and radiation-induced MPNST. Am J Surg Pathol, 40(4):479-489.
[80]PrzybylJ, KidzinskiL, HastieT, et al., 2018. Gene expression profiling of low-grade endometrial stromal sarcoma indicates fusion protein-mediated activation of the Wnt signaling pathway. Gynecol Oncol, 149(2):388-393.
[81]QinJZ, WhyteWA, AnderssenE, et al., 2012. The polycomb group protein L3mbtl2 assembles an atypical PRC1-family complex that is essential in pluripotent stem cells and early development. Cell Stem Cell, 11(3):319-332.
[82]QuanP, MoinfarF, KufferathI, et al., 2014. Effects of targeting endometrial stromal sarcoma cells via histone deacetylase and PI3K/AKT/mTOR signaling. Anticancer Res, 34(6):2883-2897.
[83]RubinJB, SegalRA, 2003. Growth, survival and migration: the Trk to cancer. Cancer Treat Res, 115:1-18.
[84]SalvatierraA, TarratsA, GomezC, et al., 2006. A case of c-kit positive high-grade stromal endometrial sarcoma responding to Imatinib Mesylate. Gynecol Oncol, 101(3):545-547.
[85]SarmaK, MargueronR, IvanovA, et al., 2008. Ezh2 requires PHF1 to efficiently catalyze H3 lysine 27 trimethylation in vivo. Mol Cell Biol, 28(8):2718-2731.
[86]SchoolmeesterJK, SciallisAP, GreippPT, et al., 2015. Analysis of MDM2 amplification in 43 endometrial stromal tumors: a potential diagnostic pitfall. Int J Gynecol Pathol, 34(6):576-583.
[87]SeagleBLL, ShilpiA, BuchananS, et al., 2017. Low-grade and high-grade endometrial stromal sarcoma: a National Cancer Database study. Gynecol Oncol, 146(2):254-262.
[88]SerkiesK, Abacjew-ChmyłkoA, Wieczorek-RutkowskaM, et al., 2018. Aromatase inhibitor therapy for endometrial stromal sarcoma—two-centre experience. Ginekol Pol, 89(11):607-610.
[89]SpringLM, WanderSA, AndreF, et al., 2020. Cyclin-dependent kinase 4 and 6 inhibitors for hormone receptor-positive breast cancer: past, present, and future. Lancet, 395(10226):817-827.
[90]SreekantaiahC, LiFP, WeidnerN, et al., 1991. An endometrial stromal sarcoma with clonal cytogenetic abnormalities. Cancer Genet Cytogenet, 55(2):163-166.
[91]StankunasK, BergerJ, RuseC, et al., 1998. The Enhancer of Polycomb gene of Drosophila encodes a chromatin protein conserved in yeast and mammals. Development, 125(20):4055-4066.
[92]StudachLL, MenneS, CairoS, et al., 2012. Subset of Suz12/PRC2 target genes is activated during hepatitis B virus replication and liver carcinogenesis associated with HBV X protein. Hepatology, 56(4):1240-1251.
[93]SungY, ParkS, ParkSJ, et al., 2018. Jazf1 promotes prostate cancer progression by activating JNK/Slug. Oncotarget, 9(1):755-765.
[94]ThielFC, HalmenS, 2018. Low-grade endometrial stromal sarcoma—a review. Oncol Res Treat, 41(11):687-692.
[95]UchidaC, MiwaS, KitagawaK, et al., 2005. Enhanced Mdm2 activity inhibits pRB function via ubiquitin‐dependent degradation. EMBO J, 24(1):160-169.
[96]UeyamaM, NishidaN, KorenagaM, et al., 2016. The impact of PNPLA3 and JAZF1 on hepatocellular carcinoma in non-viral hepatitis patients with type 2 diabetes mellitus. J Gastroenterol, 51(4):370-379.
[97]VerschoorAJ, FARMWarmerdam, BosseT, et al., 2018. A remarkable response to pazopanib, despite recurrent liver toxicity, in a patient with a high grade endometrial stromal sarcoma, a case report. BMC Cancer, 18:92.
[98]VilgelmAE, SalehN, Shattuck-BrandtR, et al., 2019. MDM2 antagonists overcome intrinsic resistance to CDK4/6 inhibition by inducing p21. Sci Transl Med, 11(505):eaav7171.
[99]WadeM, LiYC, MataniAS, et al., 2012. Functional analysis and consequences of Mdm2 E3 ligase inhibition in human tumor cells. Oncogene, 31(45):4789-4797.
[100]WienkenM, DickmannsA, NemajerovaA, et al., 2016. MDM2 associates with polycomb repressor complex 2 and enhances stemness-promoting chromatin modifications independent of p53. Mol Cell, 61(1):68-83.
[101]WongSJ, SenkovichO, ArtigasJA, et al., 2020. Structure and role of BCOR PUFD in noncanonical PRC1 assembly and disease. Biochemistry, 59(29):2718-2728.
[102]XuY, FulcinitiM, SamurMK, et al., 2020. YWHAE/14-3-3ε expression impacts the protein load, contributing to proteasome inhibitor sensitivity in multiple myeloma. Blood, 136(4):468-479.
[103]YangYF, LeeYC, WangYY, et al., 2019. YWHAE promotes proliferation, metastasis, and chemoresistance in breast cancer cells. Kaohsiung J Med Sci, 35(7):408-416.
[104]YaoWJ, TongS, TanJ, et al., 2019. NF45 promotes esophageal squamous carcinoma cell invasion by increasing Rac1 activity through 14-3-3ε protein. Arch Biochem Biophys, 663:101-108.
[105]ZhangCW, HanXR, YangXB, et al., 2018. Proteolysis targeting chimeras (PROTACs) of anaplastic lymphoma kinase (ALK). Eur J Med Chem, 151:304-314.
[106]ZhangH, DevoucouxM, SongXS, et al., 2020. Structural basis for EPC1-mediated recruitment of MBTD1 into the NuA4/TIP60 acetyltransferase complex. Cell Rep, 30(12):3996-4002.e4.
Open peer comments: Debate/Discuss/Question/Opinion
<1>