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Anti-Cancer Agents in Medicinal Chemistry

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ISSN (Print): 1871-5206
ISSN (Online): 1875-5992

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Research Article

Hyperoside Inhibits RNF8-mediated Nuclear Translocation of β-catenin to Repress PD-L1 Expression and Prostate Cancer

Author(s): Jie Chen, Yi Zhao, Xiaoli Wang, Long Zang, Dengke Yin* and Song Tan*

Volume 24, Issue 6, 2024

Published on: 16 January, 2024

Page: [464 - 476] Pages: 13

DOI: 10.2174/0118715206289246240110044931

Price: $65

Abstract

Background: Hyperoside is a flavonol glycoside isolated from Hypericum perforatum L. that has inhibitory effects on cancer cells; however, its effects on prostate cancer (PCa) remain unclear. Therefore, we studied the anti-PCa effects of hyperoside and its underlying mechanisms in vitro and in vivo.

Aim: This study aimed to explore the mechanism of hyperoside in anti-PCa.

Methods: 3-(4,5-Dimethyl-2-Thiazolyl)-2,5-Diphenyl Tetrazolium Bromide (MTT), transwell, and flow cytometry assays were used to detect PCa cell growth, invasion, and cell apoptosis. Immunoblot analysis, immunofluorescence, immunoprecipitation, and quantitative real-time PCR (qRT-PCR) were used to analyze the antitumor mechanism of hyperoside.

Results: Hyperoside inhibited PCa cell growth, invasion, and cell cycle and induced cell apoptosis. Furthermore, RING finger protein 8 (RNF8), an E3 ligase that assembles K63 polyubiquitination chains, was predicted to be a direct target of hyperoside and was downregulated by hyperoside. Downregulation of RNF8 by hyperoside impeded the nuclear translocation of β-catenin and disrupted the Wnt/β-catenin pathway, which reduced the expression of the target genes c-myc, cyclin D1, and programmed death ligand 1 (PD-L1). Decreased PD-L1 levels contributed to induced immunity in Jurkat cells in vitro. Finally, in vivo studies demonstrated that hyperoside significantly reduced tumor size, inhibited PD-L1 and RNF8 expression, and induced apoptosis in tumor tissues of a subcutaneous mouse model.

Conclusion: Hyperoside exerts its anti-PCa effect by reducing RNF8 protein, inhibiting nuclear translocation of β-catenin, and disrupting the Wnt/β-catenin pathway, in turn reducing the expression of PD-L1 and improving Jurkat cell immunity.

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[1]
Sung, H.; Ferlay, J.; Siegel, R.L.; Laversanne, M.; Soerjomataram, I.; Jemal, A.; Bray, F. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J. Clin., 2021, 71(3), 209-249.
[http://dx.doi.org/10.3322/caac.21660] [PMID: 33538338]
[2]
Sandhu, S.; Moore, C.M.; Chiong, E.; Beltran, H.; Bristow, R.G.; Williams, S.G. Prostate cancer. Lancet, 2021, 398(10305), 1075-1090.
[http://dx.doi.org/10.1016/S0140-6736(21)00950-8] [PMID: 34370973]
[3]
Yu, J.; Gritsina, G.; Gao, W-Q. Transcriptional repression by androgen receptor: Roles in castration-resistant prostate cancer. Asian J. Androl., 2019, 21(3), 215-223.
[http://dx.doi.org/10.4103/aja.aja_19_19] [PMID: 30950412]
[4]
Powers, E.; Karachaliou, G.S.; Kao, C.; Harrison, M.R.; Hoimes, C.J.; George, D.J.; Armstrong, A.J.; Zhang, T. Novel therapies are changing treatment paradigms in metastatic prostate cancer. J. Hematol. Oncol., 2020, 13(1), 144.
[http://dx.doi.org/10.1186/s13045-020-00978-z] [PMID: 33115529]
[5]
Cha, H.R.; Lee, J.H.; Ponnazhagan, S. Revisiting immunotherapy: A focus on prostate cancer. Cancer Res., 2020, 80(8), 1615-1623.
[http://dx.doi.org/10.1158/0008-5472.CAN-19-2948] [PMID: 32066566]
[6]
Claps, M.; Mennitto, A.; Guadalupi, V.; Sepe, P.; Stellato, M.; Zattarin, E.; Gillessen, S.S.; Sternberg, C.N.; Berruti, A.; De Braud, F.G.M.; Verzoni, E.; Procopio, G. Immune-checkpoint inhibitors and metastatic prostate cancer therapy: Learning by making mistakes. Cancer Treat. Rev., 2020, 88, 102057.
[http://dx.doi.org/10.1016/j.ctrv.2020.102057] [PMID: 32574991]
[7]
Nitti, M.; Piras, S.; Lisa Furfaro, A.; Brondolo, L.; Maria Marinari, U.; Adelaide Pronzato, M. Neuroblastoma cell response to oxidative stress is impaired by retinoic acid-induced differentiation: Role of HO-1. Free Radic. Biol. Med., 2016, 100, S106-S107.
[http://dx.doi.org/10.1016/j.freeradbiomed.2016.10.272]
[8]
Hu, J.; Wu, X.; Yang, C.; Rashid, K.; Ma, C.; Hu, M.; Ding, Q.; Jiang, H. Anticancer effect of icaritin on prostate cancer via regulating miR‐381‐3p and its target gene UBE2C. Cancer Med., 2019, 8(18), 7833-7845.
[http://dx.doi.org/10.1002/cam4.2630] [PMID: 31646760]
[9]
Drake, C.G. Prostate cancer as a model for tumour immunotherapy. Nat. Rev. Immunol., 2010, 10(8), 580-593.
[http://dx.doi.org/10.1038/nri2817] [PMID: 20651745]
[10]
Topalian, S.L.; Drake, C.G.; Pardoll, D.M. Targeting the PD-1/B7-H1(PD-L1) pathway to activate anti-tumor immunity. Curr. Opin. Immunol., 2012, 24(2), 207-212.
[http://dx.doi.org/10.1016/j.coi.2011.12.009] [PMID: 22236695]
[11]
Kotanides, H.; Li, Y.; Malabunga, M.; Carpenito, C.; Eastman, S.W.; Shen, Y.; Wang, G.; Inigo, I.; Surguladze, D.; Pennello, A.L.; Persaud, K.; Hindi, S.; Topper, M.; Chen, X.; Zhang, Y.; Bulaon, D.K.; Bailey, T.; Lao, Y.; Han, B.; Torgerson, S.; Chin, D.; Sonyi, A.; Haidar, J.N.; Novosiadly, R.D.; Moxham, C.M.; Plowman, G.D.; Ludwig, D.L.; Kalos, M. Bispecific targeting of PD-1 and PD-L1 enhances T-cell activation and antitumor immunity. Cancer Immunol. Res., 2020, 8(10), 1300-1310.
[http://dx.doi.org/10.1158/2326-6066.CIR-20-0304] [PMID: 32873605]
[12]
Jiang, X.; Wang, J.; Deng, X.; Xiong, F.; Ge, J.; Xiang, B.; Wu, X.; Ma, J.; Zhou, M.; Li, X.; Li, Y.; Li, G.; Xiong, W.; Guo, C.; Zeng, Z. Role of the tumor microenvironment in PD-L1/PD-1-mediated tumor immune escape. Mol. Cancer, 2019, 18(1), 10.
[http://dx.doi.org/10.1186/s12943-018-0928-4] [PMID: 30646912]
[13]
Xu, Y.; Song, G.; Xie, S.; Jiang, W.; Chen, X.; Chu, M.; Hu, X.; Wang, Z. The roles of PD-1/PD-L1 in the prognosis and immunotherapy of prostate cancer. Mol. Ther., 2021, 29(6), 1958-1969.
[http://dx.doi.org/10.1016/j.ymthe.2021.04.029] [PMID: 33932597]
[14]
Kir, G.; Cecikoglu, G.E.; Olgun, Z.C.; Kazan, H.O.; Yildirim, A. PTEN loss and PD-L1 expression of different histological patterns of prostate cancer. Pathol. Res. Pract., 2022, 229, 153738.
[http://dx.doi.org/10.1016/j.prp.2021.153738] [PMID: 34922209]
[15]
Gevensleben, H.; Dietrich, D.; Golletz, C.; Steiner, S.; Jung, M.; Thiesler, T.; Majores, M.; Stein, J.; Uhl, B.; Müller, S.; Ellinger, J.; Stephan, C.; Jung, K.; Brossart, P.; Kristiansen, G. The immune checkpoint regulator PD-L1 is highly expressed in aggressive primary prostate cancer. Clin. Cancer Res., 2016, 22(8), 1969-1977.
[http://dx.doi.org/10.1158/1078-0432.CCR-15-2042] [PMID: 26573597]
[16]
Sommer, U.; Ebersbach, C.; Beier, A.M.K.; Baretton, G.B.; Thomas, C.; Borkowetz, A.; Erb, H.H.H. Influence of androgen deprivation therapy on the PD-L1 expression and immune activity in prostate cancer tissue. Front. Mol. Biosci., 2022, 9, 878353.
[http://dx.doi.org/10.3389/fmolb.2022.878353] [PMID: 35836932]
[17]
Zeng, L.; Li, L.; Zeng, Q.; Deng, Y.; Yin, L.; Liao, L. Mitogenic activity of Artocarpus lingnanensis lectin and its apoptosis induction in Jurkat T cells. J. Nat. Med., 2018, 72(3), 745-756.
[http://dx.doi.org/10.1007/s11418-018-1212-z] [PMID: 29651698]
[18]
Da Silva, T.; Oliveira-Brito, P.; Gonçalves, T.; Vendruscolo, P.; Roque-Barreira, M.; Artin, M. ArtinM mediates murine T cell activation and induces cell death in jurkat human leukemic T cells. Int. J. Mol. Sci., 2017, 18(7), 1400.
[http://dx.doi.org/10.3390/ijms18071400] [PMID: 28665310]
[19]
Chen, J.; Qin, P.; Tao, Z.; Ding, W.; Yao, Y.; Xu, W.; Yin, D.; Tan, S. Anticancer activity of methyl protodioscin against prostate cancer by modulation of cholesterol-associated MAPK signaling pathway via FOXO1 induction. Biol. Pharm. Bull., 2023, 46(4), 574-585.
[http://dx.doi.org/10.1248/bpb.b22-00682] [PMID: 37005301]
[20]
Zhou, T.; Yi, F.; Wang, Z.; Guo, Q.; Liu, J.; Bai, N.; Li, X.; Dong, X.; Ren, L.; Cao, L.; Song, X. The functions of DNA damage factor RNF8 in the pathogenesis and progression of cancer. Int. J. Biol. Sci., 2019, 15(5), 909-918.
[http://dx.doi.org/10.7150/ijbs.31972] [PMID: 31182912]
[21]
Yang, Y.; Zhang, W.; Lan, P. Immune checkpoint and other receptor-ligand pairs modulating macrophages in cancer: Present and prospects. Cancers, 2022, 14(23), 5963.
[http://dx.doi.org/10.3390/cancers14235963] [PMID: 36497444]
[22]
Zhou, L.; Wu, F.; Jin, W.; Yan, B.; Chen, X.; He, Y.; Yang, W.; Du, W.; Zhang, Q.; Guo, Y.; Yuan, Q.; Dong, X.; Yu, W.; Zhang, J.; Xiao, L.; Tong, P.; Shan, L.; Efferth, T. Theabrownin inhibits cell cycle progression and tumor growth of lung carcinoma through c-myc-related mechanism. Front. Pharmacol., 2017, 8, 75.
[http://dx.doi.org/10.3389/fphar.2017.00075] [PMID: 28289384]
[23]
Carrubba, A.; Lazzara, S.; Giovino, A.; Ruberto, G.; Napoli, E. Content variability of bioactive secondary metabolites in Hypericum perforatum L. Phytochem. Lett., 2021, 46, 71-78.
[http://dx.doi.org/10.1016/j.phytol.2021.09.011]
[24]
Xu, S.; Chen, S.; Xia, W.; Sui, H.; Fu, X. Hyperoside: A review of its structure, synthesis, pharmacology, pharmacokinetics and toxicity. Molecules, 2022, 27(9), 3009.
[http://dx.doi.org/10.3390/molecules27093009] [PMID: 35566359]
[25]
Zou, Y.; Lu, Y.; Wei, D. Antioxidant activity of a flavonoid-rich extract of Hypericum perforatum L. in vitro. J. Agric. Food Chem., 2004, 52(16), 5032-5039.
[http://dx.doi.org/10.1021/jf049571r] [PMID: 15291471]
[26]
Xie, Q.; Wen, H.; Zhang, Q.; Zhou, W.; Lin, X.; Xie, D.; Liu, Y. Inhibiting PI3K-AKt signaling pathway is involved in antitumor effects of ginsenoside Rg3 in lung cancer cell. Biomed. Pharmacother., 2017, 85, 16-21.
[http://dx.doi.org/10.1016/j.biopha.2016.11.096] [PMID: 27930981]
[27]
Wang, K.; Zhang, H.; Yuan, L.; Li, X.; Cai, Y. Potential implications of hyperoside on oxidative stress-induced human diseases: A comprehensive review. J. Inflamm. Res., 2023, 16, 4503-4526. [https://doi.org/]
[28]
Sun, J.; Zheng, Y.; Mamun, M.A.A.; Li, X.; Chen, X.; Gao, Y. Research progress of PD-1/PD-L1 immunotherapy in gastrointestinal tumors. Biomed. Pharmacother., 2020, 129, 110504.
[http://dx.doi.org/10.1016/j.biopha.2020.110504] [PMID: 32768978]
[29]
Zhao, L.; Chen, X.; Wu, H.; He, Q.; Ding, L.; Yang, B. Strategies to synergize PD-1/PD-L1 targeted cancer immunotherapies to enhance antitumor responses in ovarian cancer. Biochem. Pharmacol., 2023, 215, 115724.
[http://dx.doi.org/10.1016/j.bcp.2023.115724] [PMID: 37524205]
[30]
Sun, K.; Luo, J.; Jing, X.; Xiang, W.; Guo, J.; Yao, X.; Liang, S.; Guo, F.; Xu, T. Hyperoside ameliorates the progression of osteoarthritis: An in vitro and in vivo study. Phytomedicine, 2021, 80, 153387.
[http://dx.doi.org/10.1016/j.phymed.2020.153387] [PMID: 33130473]
[31]
Jang, S.A.; Park, D.W.; Sohn, E.H.; Lee, S.R.; Kang, S.C. Hyperoside suppresses tumor necrosis factor α-mediated vascular inflammatory responses by downregulating mitogen-activated protein kinases and nuclear actor-κB signaling. Chem. Biol. Interact., 2018, 294, 48-55.
[http://dx.doi.org/10.1016/j.cbi.2018.08.013] [PMID: 30125551]
[32]
Kwon, S.H.; Lee, S.R.; Park, Y.J.; Ra, M.; Lee, Y.; Pang, C.; Kim, K.H. Suppression of 6-hydroxydopamine-induced oxidative stress by hyperoside via activation of Nrf2/HO-1 signaling in dopaminergic neurons. Int. J. Mol. Sci., 2019, 20(23), 5832.
[http://dx.doi.org/10.3390/ijms20235832] [PMID: 31757050]
[33]
Lee, S.H.; Lee, J.Y.; Kwon, Y.I.; Jang, H.D. Anti-osteoclastic activity of artemisia capillaris thunb. Extract depends upon attenuation of osteoclast differentiation and bone resorption-associated acidification due to chlorogenic acid, hyperoside, and scoparone. Int. J. Mol. Sci., 2017, 18(2), 322.
[http://dx.doi.org/10.3390/ijms18020322] [PMID: 28165389]
[34]
Wang, Q.; Wei, H.C.; Zhou, S.J.; Li, Y.; Zheng, T.T.; Zhou, C.Z.; Wan, X.H. Hyperoside: A review on its sources, biological activities, and molecular mechanisms. Phytother. Res., 2022, 36(7), 2779-2802.
[http://dx.doi.org/10.1002/ptr.7478] [PMID: 35561084]
[35]
Guo, W.; Yu, H.; Zhang, L.; Chen, X.; Liu, Y.; Wang, Y.; Zhang, Y. Effect of hyperoside on cervical cancer cells and transcriptome analysis of differentially expressed genes. Cancer Cell Int., 2019, 19(1), 235.
[http://dx.doi.org/10.1186/s12935-019-0953-4] [PMID: 31516392]
[36]
Qiu, J.; Zhang, T.; Zhu, X.; Yang, C.; Wang, Y.; Zhou, N.; Ju, B.; Zhou, T.; Deng, G.; Qiu, C. Hyperoside induces breast cancer cells apoptosis via ROS-mediated NF-kappaB signaling pathway. Int. J. Mol. Sci., 2019, 21(1), 131.
[http://dx.doi.org/10.3390/ijms21010131] [PMID: 31878204]
[37]
Chen, D.; Wu, Y.X.; Qiu, Y.; Wan, B.; Liu, G.; Chen, J.; Lu, M.; Pang, Q. Hyperoside suppresses hypoxia-induced A549 survival and proliferation through ferrous accumulation via AMPK/HO-1 axis. Phytomedicine, 2020, 67, 153138.
[http://dx.doi.org/10.1016/j.phymed.2019.153138] [PMID: 31881478]
[38]
Ping, M.H. Hyperin controls the development and therapy of gastric cancer via regulating Wnt/beta-catenin signaling. Cancer Manag. Res., 2020, 12, 11773-11782.
[http://dx.doi.org/10.2147/CMAR.S270544] [PMID: 33235505]
[39]
Zhang, Y.; Dong, H.; Zhang, J.; Zhang, L. Inhibitory effect of hyperoside isolated from Zanthoxylum bungeanum leaves on SW620 human colorectal cancer cells via induction of the p53 signaling pathway and apoptosis. Mol. Med. Rep., 2017, 16(2), 1125-1132.
[http://dx.doi.org/10.3892/mmr.2017.6710] [PMID: 29067453]
[40]
Boukes, G.J.; van de Venter, M. The apoptotic and autophagic properties of two natural occurring prodrugs, hyperoside and hypoxoside, against pancreatic cancer cell lines. Biomed. Pharmacother., 2016, 83, 617-626.
[http://dx.doi.org/10.1016/j.biopha.2016.07.029] [PMID: 27459118]
[41]
Zhu, X.; Ji, M.; Han, Y.; Guo, Y.; Zhu, W.; Gao, F.; Yang, X.; Zhang, C. PGRMC1-dependent autophagy by hyperoside induces apoptosis and sensitizes ovarian cancer cells to cisplatin treatment. Int. J. Oncol., 2017, 50(3), 835-846.
[http://dx.doi.org/10.3892/ijo.2017.3873] [PMID: 28197632]
[42]
Liu, C.; Kuang, J.; Wang, Y.; Duan, T.; Min, L.; Lu, C.; Zhang, T.; Chen, R.; Wu, Y.; Zhu, L. A functional reference map of the RNF8 interactome in cancer. Biol. Direct, 2022, 17(1), 17.
[http://dx.doi.org/10.1186/s13062-022-00331-z] [PMID: 35831895]
[43]
Ding, P.; Xu, Y.; Li, L.; Lv, X.; Li, L.; Chen, J.; Zhou, D.; Wang, X.; Wang, Q.; Zhang, W.; Liao, T.; Ji, Q.H.; Lei, Q.Y.; Hu, W. Intracellular complement C5a/C5aR1 stabilizes β-catenin to promote colorectal tumorigenesis. Cell Rep., 2022, 39(9), 110851.
[http://dx.doi.org/10.1016/j.celrep.2022.110851] [PMID: 35649359]
[44]
Mailand, N.; Bekker-Jensen, S.; Faustrup, H.; Melander, F.; Bartek, J.; Lukas, C.; Lukas, J. RNF8 ubiquitylates histones at DNA double-strand breaks and promotes assembly of repair proteins. Cell, 2007, 131(5), 887-900.
[http://dx.doi.org/10.1016/j.cell.2007.09.040] [PMID: 18001824]
[45]
Ren, L.; Zhou, T.; Wang, Y.; Wu, Y.; Xu, H.; Liu, J.; Dong, X.; Yi, F.; Guo, Q.; Wang, Z.; Li, X.; Bai, N.; Guo, W.; Guo, M.; Jiang, B.; Wu, X.; Feng, Y.; Song, X.; Zhang, S.; Zhao, Y.; Cao, L.; Han, S.; Xing, C. RNF8 induces β-catenin-mediated c-Myc expression and promotes colon cancer proliferation. Int. J. Biol. Sci., 2020, 16(12), 2051-2062.
[http://dx.doi.org/10.7150/ijbs.44119] [PMID: 32549753]
[46]
Kuang, J.; Min, L.; Liu, C.; Chen, S.; Gao, C.; Ma, J.; Wu, X.; Li, W.; Wu, L.; Zhu, L. RNF8 promotes epithelial-mesenchymal transition in lung cancer cells via stabilization of slug. Mol. Cancer Res., 2020, 18(11), 1638-1649.
[http://dx.doi.org/10.1158/1541-7786.MCR-19-1211] [PMID: 32753472]
[47]
Xu, Y.; Hu, Y.; Xu, T.; Yan, K.; Zhang, T.; Li, Q.; Chang, F.; Guo, X.; Peng, J.; Li, M.; Zhao, M.; Zhen, H.; Xu, L.; Zheng, D.; Li, L.; Shao, G. RNF8-mediated regulation of Akt promotes lung cancer cell survival and resistance to DNA damage. Cell Rep., 2021, 37(3), 109854.
[http://dx.doi.org/10.1016/j.celrep.2021.109854] [PMID: 34686341]
[48]
Kamali, A.N.; Bautista, J.M.; Eisenhut, M.; Hamedifar, H. Immune checkpoints and cancer immunotherapies: Insights into newly potential receptors and ligands. Ther. Adv. Vaccines Immunother., 2023, 11, 25151355231192043.
[http://dx.doi.org/10.1177/25151355231192043] [PMID: 37662491]
[49]
Zhou, T.; Wang, S.; Song, X.; Liu, W.; Dong, F.; Huo, Y.; Zou, R.; Wang, C.; Zhang, S.; Liu, W.; Sun, G.; Lin, L.; Zeng, K.; Dong, X.; Guo, Q.; Yi, F.; Wang, Z.; Li, X.; Jiang, B.; Cao, L.; Zhao, Y. RNF8 up-regulates AR/ARV7 action to contribute to advanced prostate cancer progression. Cell Death Dis., 2022, 13(4), 352.
[http://dx.doi.org/10.1038/s41419-022-04787-9] [PMID: 35428760]
[50]
Sun, B.; Liu, Y.; He, D.; Li, J.; Wang, J.; Wen, W.; Hong, M. Traditional Chinese medicines and their active ingredients sensitize cancer cells to TRAIL-induced apoptosis. J. Zhejiang Univ. Sci. B, 2021, 22(3), 190-203.
[http://dx.doi.org/10.1631/jzus.B2000497] [PMID: 33719224]
[51]
Valnegri, P.; Huang, J.; Yamada, T.; Yang, Y.; Mejia, L.A.; Cho, H.Y.; Oldenborg, A.; Bonni, A. RNF8/UBC13 ubiquitin signaling suppresses synapse formation in the mammalian brain. Nat. Commun., 2017, 8(1), 1271.
[http://dx.doi.org/10.1038/s41467-017-01333-6] [PMID: 29097665]
[52]
Murillo-Garzón, V.; Kypta, R. WNT signalling in prostate cancer. Nat. Rev. Urol., 2017, 14(11), 683-696.
[http://dx.doi.org/10.1038/nrurol.2017.144] [PMID: 28895566]
[53]
Schneider, J.A.; Logan, S.K. Revisiting the role of Wnt/β-catenin signaling in prostate cancer. Mol. Cell. Endocrinol, 2018, (462(PtA), 3-8.
[http://dx.doi.org/10.1016/j.mce.2017.02.008] [PMID: 28189566]
[54]
Zhu, P.L.; Li, J.K.; Jiang, X.L.; Zhang, S.Q.; Zhang, Z.; Wang, Y.; Zhang, Z.; Chen, W.Q.; Yung, K.K.L. A traditional prescription comprising Astragali radix and Schisandra chinensis Fructus induces apoptosis and protective autophagy in hepatocellular carcinoma cells. J. Ethnopharmacol., 2023, 312, 116548.
[http://dx.doi.org/10.1016/j.jep.2023.116548] [PMID: 37100264]
[55]
He, T.C.; Sparks, A.B.; Rago, C.; Hermeking, H.; Zawel, L.; da Costa, L.T.; Morin, P.J.; Vogelstein, B.; Kinzler, K.W. Identification of c-MYC as a target of the APC pathway. Science, 1998, 281(5382), 1509-1512.
[http://dx.doi.org/10.1126/science.281.5382.1509] [PMID: 9727977]
[56]
Tetsu, O. McCormick, F. β-Catenin regulates expression of cyclin D1 in colon carcinoma cells. Nature, 1999, 398(6726), 422-426.
[http://dx.doi.org/10.1038/18884] [PMID: 10201372]
[57]
Gan, S.; Ye, J.; Li, J.; Hu, C.; Wang, J.; Xu, D.; Pan, X.; Chu, C.; Chu, J.; Zhang, J.; Zheng, J.; Zhang, X.; Xu, J.; Zhang, H.; Qu, F.; Cui, X. LRP11 activates β-catenin to induce PD-L1 expression in prostate cancer. J. Drug Target., 2020, 28(5), 508-515.
[http://dx.doi.org/10.1080/1061186X.2019.1687710] [PMID: 31865764]
[58]
Pawelec, G.; Borowitz, A.; Krammer, P.H.; Wernet, P. Constitutive interleukin 2 production by the JURKAT human leukemic T cell line. Eur. J. Immunol., 1982, 12(5), 387-392.
[http://dx.doi.org/10.1002/eji.1830120506] [PMID: 6980126]
[59]
Gholijani, N.; Gharagozloo, M.; Kalantar, F.; Ramezani, A.; Amirghofran, Z. Modulation of cytokine production and transcription factors activities in human jurkat T cells by thymol and carvacrol. Adv. Pharm. Bull., 2015, 5(Suppl. 1), 653-660.
[http://dx.doi.org/10.15171/apb.2015.089] [PMID: 26793612]
[60]
Wang, B.; Tian, T.; Kalland, K.H.; Ke, X.; Qu, Y. Targeting Wnt/β-catenin signaling for cancer immunotherapy. Trends Pharmacol. Sci., 2018, 39(7), 648-658.
[http://dx.doi.org/10.1016/j.tips.2018.03.008] [PMID: 29678298]
[61]
Yu, F.; Yu, C.; Li, F.; Zuo, Y.; Wang, Y.; Yao, L.; Wu, C.; Wang, C.; Ye, L. Wnt/β-catenin signaling in cancers and targeted therapies. Signal Transduct. Target. Ther., 2021, 6(1), 307.
[http://dx.doi.org/10.1038/s41392-021-00701-5] [PMID: 34456337]
[62]
Zhao, J.; Blayney, A.; Liu, X.; Gandy, L.; Jin, W.; Yan, L.; Ha, J.H.; Canning, A.J.; Connelly, M.; Yang, C.; Liu, X.; Xiao, Y.; Cosgrove, M.S.; Solmaz, S.R.; Zhang, Y.; Ban, D.; Chen, J.; Loh, S.N.; Wang, C. EGCG binds intrinsically disordered N-terminal domain of p53 and disrupts p53-MDM2 interaction. Nat. Commun., 2021, 12(1), 986.
[http://dx.doi.org/10.1038/s41467-021-21258-5] [PMID: 33579943]
[63]
Yao, F.; Zhou, Z.; Kim, J.; Hang, Q.; Xiao, Z.; Ton, B.N.; Chang, L.; Liu, N.; Zeng, L.; Wang, W.; Wang, Y.; Zhang, P.; Hu, X.; Su, X.; Liang, H.; Sun, Y.; Ma, L. SKP2- and OTUD1-regulated non-proteolytic ubiquitination of YAP promotes YAP nuclear localization and activity. Nat. Commun., 2018, 9(1), 2269.
[http://dx.doi.org/10.1038/s41467-018-04620-y] [PMID: 29891922]
[64]
Lee, H.J.; Li, C.F.; Ruan, D.; Powers, S.; Thompson, P.A.; Frohman, M.A.; Chan, C.H.; Chan, C-H. The DNA damage transducer RNF8 facilitates cancer chemoresistance and progression through twist activation. Mol. Cell, 2016, 63(6), 1021-1033.
[http://dx.doi.org/10.1016/j.molcel.2016.08.009] [PMID: 27618486]
[65]
Zhang, Y.; Wang, X. Targeting the Wnt/β-catenin signaling pathway in cancer. J. Hematol. Oncol., 2020, 13(1), 165.
[http://dx.doi.org/10.1186/s13045-020-00990-3] [PMID: 33276800]
[66]
Cui, Y.; Zhao, M.; Yang, Y.; Xu, R.; Tong, L.; Liang, J.; Zhang, X.; Sun, Y.; Fan, Y. Reversal of epithelial-mesenchymal transition and inhibition of tumor stemness of breast cancer cells through advanced combined chemotherapy. Acta Biomater., 2022, 152, 380-392.
[http://dx.doi.org/10.1016/j.actbio.2022.08.024] [PMID: 36028199]
[67]
Rizzo, A.; Mollica, V.; Cimadamore, A.; Santoni, M.; Scarpelli, M.; Giunchi, F.; Cheng, L.; Lopez-Beltran, A.; Fiorentino, M.; Montironi, R.; Massari, F. Is there a role for immunotherapy in prostate cancer? Cells, 2020, 9(9), 2051.
[http://dx.doi.org/10.3390/cells9092051] [PMID: 32911806]
[68]
Liu, B.; Zhang, M.; Chu, H.; Zhang, H.; Wu, H.; Song, G.; Wang, P.; Zhao, K.; Hou, J.; Wang, X.; Zhang, L.; Gao, C. The ubiquitin E3 ligase TRIM31 promotes aggregation and activation of the signaling adaptor MAVS through Lys63-linked polyubiquitination. Nat. Immunol., 2017, 18(2), 214-224.
[http://dx.doi.org/10.1038/ni.3641] [PMID: 27992402]
[69]
Stultz, J.; Fong, L. How to turn up the heat on the cold immune microenvironment of metastatic prostate cancer. Prostate Cancer Prostatic Dis., 2021, 24(3), 697-717.
[http://dx.doi.org/10.1038/s41391-021-00340-5] [PMID: 33820953]
[70]
Bou-Dargham, M.J.; Sha, L.; Sang, Q.X.A.; Zhang, J. Immune landscape of human prostate cancer: Immune evasion mechanisms and biomarkers for personalized immunotherapy. BMC Cancer, 2020, 20(1), 572.
[http://dx.doi.org/10.1186/s12885-020-07058-y] [PMID: 32552802]
[71]
Li, H.; Zhao, Z.; Ling, J.; Pan, L.; Zhao, X.; Zhu, H.; Yu, J.; Xie, B.; Shen, J.; Chen, W. USP14 promotes K63-linked RIG-I deubiquitination and suppresses antiviral immune responses. Eur. J. Immunol., 2019, 49(1), 42-53.
[http://dx.doi.org/10.1002/eji.201847603] [PMID: 30466171]
[72]
Cao, L.; Liu, X.; Zheng, B.; Xing, C.; Liu, J. Role of K63-linked ubiquitination in cancer. Cell Death Discov., 2022, 8(1), 410.
[http://dx.doi.org/10.1038/s41420-022-01204-0] [PMID: 36202787]
[73]
Liu, S.; Qin, T.; Liu, Z.; Wang, J.; Jia, Y.; Feng, Y.; Gao, Y.; Li, K. anlotinib alters tumor immune microenvironment by downregulating PD-L1 expression on vascular endothelial cells. Cell Death Dis., 2020, 11(5), 309.
[http://dx.doi.org/10.1038/s41419-020-2511-3] [PMID: 32366856]
[74]
Han, L.; Yao, S.; Cao, S.; Mo, G.; Li, J.; Cao, Y.; Huang, F. Triterpenoid saponins from anemone flaccida suppress tumor cell proliferation by regulating MAPK, PD1/PDL1, and STAT3 signaling pathways and altering cancer metabolism. OncoTargets Ther., 2019, 12, 10917-10930.
[http://dx.doi.org/10.2147/OTT.S212666] [PMID: 31849495]

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