Notch signaling in the pathogenesis, progression and identification of potential targets for cholangiocarcinoma (Review)
- Authors:
- Peeranate Vanaroj
- Wanna Chaijaroenkul
- Kesara Na‑Bangchang
-
Affiliations: Graduate Program in Bioclinical Sciences, Chulabhorn International College of Medicine, Thammasat University, Pathumthani, 12120 Thailand - Published online on: January 19, 2022 https://doi.org/10.3892/mco.2022.2499
- Article Number: 66
-
Copyright: © Vanaroj et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
This article is mentioned in:
Abstract
Khan SA, Tavolari S and Brandi G: Cholangiocarcinoma: Epidemiology and risk factors. Liver Int. 39 (Suppl 1):S19–S31. 2019.PubMed/NCBI View Article : Google Scholar | |
Mao Y, Huang X, Shuang Z, Lin G, Wang J, Duan F, Chen J and Li S: PARP inhibitor olaparib sensitizes cholangiocarcinoma cells to radiation. Cancer Med. 7:1285–1296. 2018.PubMed/NCBI View Article : Google Scholar | |
Papoutsoglou P, Louis C and Coulouarn C: Transforming growth factor-beta (TGFbeta) signaling pathway in cholangiocarcinoma. Cells. 8(960)2019.PubMed/NCBI View Article : Google Scholar | |
Pancewicz-Wojtkiewicz J: Epidermal growth factor receptor and notch signaling in non-small-cell lung cancer. Cancer Med. 5:3572–3578. 2016.PubMed/NCBI View Article : Google Scholar | |
Kandasamy K, Mohan SS, Raju R, Keerthikumar S, Kumar GS, Venugopal AK, Telikicherla D, Navarro JD, Mathivanan S, Pecquet C, et al: NetPath: A public resource of curated signal transduction pathways. Genome Biol. 11(R3)2010.PubMed/NCBI View Article : Google Scholar | |
Hopfer O, Zwahlen D, Fey MF and Aebi S: The Notch pathway in ovarian carcinomas and adenomas. Br J Cancer. 93:709–718. 2005.PubMed/NCBI View Article : Google Scholar | |
Stockhausen MT, Kristoffersen K and Poulsen HS: The functional role of Notch signaling in human gliomas. Neuro Oncol. 12:199–211. 2010.PubMed/NCBI View Article : Google Scholar | |
Kontomanolis EN, Kalagasidou S, Pouliliou S, Anthoulaki X, Georgiou N, Papamanolis V and Fasoulakis ZN: The notch pathway in breast cancer progression. ScientificWorldJournal. 2018(2415489)2018.PubMed/NCBI View Article : Google Scholar | |
Huang Q, Li J, Zheng J and Wei A: The carcinogenic role of the notch signaling pathway in the development of hepatocellular carcinoma. J Cancer. 10:1570–1579. 2019.PubMed/NCBI View Article : Google Scholar | |
Sriuranpong V, Borges MW, Ravi RK, Arnold DR, Nelkin BD, Baylin SB and Ball DW: Notch signaling induces cell cycle arrest in small cell lung cancer cells. Cancer Res. 61:3200–3205. 2001.PubMed/NCBI | |
Shao H, Cai L, Grichnik JM, Livingstone AS, Velazquez OC and Liu ZJ: Activation of Notch1 signaling in stromal fibroblasts inhibits melanoma growth by upregulating WISP-1. Oncogene. 30:4316–4326. 2011.PubMed/NCBI View Article : Google Scholar | |
Yamamoto M, Xin B, Watanabe K, Ooshio T, Fujii K, Chen X, Okada Y, Abe H, Taguchi Y, Miyokawa N, et al: Oncogenic determination of a broad spectrum of phenotypes of hepatocyte-derived mouse liver tumors. Am J Pathol. 187:2711–2725. 2017.PubMed/NCBI View Article : Google Scholar | |
Wang J, Dong M, Xu Z, Song X, Zhang S, Qiao Y, Che L, Gordan J, Hu K, Liu Y, et al: Notch2 controls hepatocyte-derived cholangiocarcinoma formation in mice. Oncogene. 37:3229–3242. 2018.PubMed/NCBI View Article : Google Scholar | |
Li X, Tao J, Cigliano A, Sini M, Calderaro J, Azoulay D, Wang C, Liu Y, Jiang L, Evert K, et al: Co-activation of PIK3CA and Yap promotes development of hepatocellular and cholangiocellular tumors in mouse and human liver. Oncotarget. 6:10102–10115. 2015.PubMed/NCBI View Article : Google Scholar | |
Zender S, Nickeleit I, Wuestefeld T, Sörensen I, Dauch D, Bozko P, El-Khatib M, Geffers R, Bektas H, Manns MP, et al: A critical role for notch signaling in the formation of cholangiocellular carcinomas. Cancer Cell. 23:784–795. 2013.PubMed/NCBI View Article : Google Scholar | |
Ishii T, Yasuchika K, Suemori H, Nakatsuji N, Ikai I and Uemoto S: Alpha-fetoprotein producing cells act as cancer progenitor cells in human cholangiocarcinoma. Cancer Lett. 294:25–34. 2010.PubMed/NCBI View Article : Google Scholar | |
Zhou Q, Wang Y, Peng B, Liang L and Li J: The roles of Notch1 expression in the migration of intrahepatic cholangiocarcinoma. BMC Cancer. 13(244)2013.PubMed/NCBI View Article : Google Scholar | |
Wu WR, Zhang R, Shi XD, Zhu MS, Xu LB, Zeng H and Liu C: Notch1 is overexpressed in human intrahepatic cholangiocarcinoma and is associated with its proliferation, invasiveness and sensitivity to 5-fluorouracil in vitro. Oncol Rep. 31:2515–2524. 2014.PubMed/NCBI View Article : Google Scholar | |
Gu Y, Xiao L, Ming Y, Zheng Z and Li W: Corilagin suppresses cholangiocarcinoma progression through Notch signaling pathway in vitro and in vivo. Int J Oncol. 48:1868–1876. 2016.PubMed/NCBI View Article : Google Scholar | |
Li JH, Zhu XX, Li FX, Huang CS, Huang XT, Wang JQ, Gao ZX, Li SJ, Xu QC, Zhao W and Yin XY: MFAP5 facilitates the aggressiveness of intrahepatic Cholangiocarcinoma by activating the Notch1 signaling pathway. J Exp Clin Cancer Res. 38(476)2019.PubMed/NCBI View Article : Google Scholar | |
Ren J, Wang S, Jin L, Ma F, Zhou D and Cai Q: Cinobufagin inhibits tumor growth by inducing apoptosis through Notch signaling pathways in human cholangiocarcinoma. Transl Cancer Res. 8:2461–2469. 2019. | |
Sheng Y, Wei J, Zhang Y, Gao X, Wang Z, Yang J, Yan S, Zhu Y, Zhang Z, Xu D, et al: Mutated EPHA2 is a target for combating lymphatic metastasis in intrahepatic cholangiocarcinoma. Int J Cancer. 144:2440–2452. 2019.PubMed/NCBI View Article : Google Scholar | |
O'Rourke CJ, Matter MS, Nepal C, Caetano-Oliveira R, Ton PT, Factor VM and Andersen JB: Identification of a pan-gamma-secretase inhibitor response signature for notch-driven cholangiocarcinoma. Hepatology. 71:196–213. 2020.PubMed/NCBI View Article : Google Scholar | |
Wu WR, Shi XD, Zhang R, Zhu MS, Xu LB, Yu XH, Zeng H, Wang J and Liu C: Clinicopathological significance of aberrant Notch receptors in intrahepatic cholangiocarcinoma. Int J Clin Exp Pathol. 7:3272–3279. 2014.PubMed/NCBI | |
Ding N, Che L, Li XL, Liu Y, Jiang LJ, Fan B, Tao JY, Chen X and Ji JF: Oncogenic potential of IDH1R132C mutant in cholangiocarcinoma development in mice. World J Gastroenterol. 22:2071–2080. 2016.PubMed/NCBI View Article : Google Scholar | |
Huntzicker EG, Hötzel K, Choy L, Che L, Ross J, Pau G, Pau G, Sharma N, Siebel CW, Chen X and French DM: Differential effects of targeting Notch receptors in a mouse model of liver cancer. Hepatology. 61:942–952. 2015.PubMed/NCBI View Article : Google Scholar | |
Che L, Fan B, Pilo MG, Xu Z, Liu Y, Cigliano A, Cossu A, Palmieri G, Pascale RM, Porcu A, et al: Jagged 1 is a major Notch ligand along cholangiocarcinoma development in mice and humans. Oncogenesis. 5(e274)2016.PubMed/NCBI View Article : Google Scholar | |
Zhang S, Wang J, Wang H, Fan L, Fan B, Zeng B, Tao J, Li X, Che L, Cigliano A, et al: Hippo cascade controls lineage commitment of liver tumors in mice and humans. Am J Pathol. 188:995–1006. 2018.PubMed/NCBI View Article : Google Scholar | |
Xu M, Wang J, Xu Z, Li R, Wang P, Shang R, Cigliano A, Ribback S, Solinas A, Pes GM, et al: SNAIL promotes the cholangiocellular phenotype, but not epithelial-mesenchymal transition, in a murine hepatocellular carcinoma model. Cancer Res. 79:5563–5574. 2019.PubMed/NCBI View Article : Google Scholar | |
Cerec V, Andreola F and Pereira S: Effect of verteporfin-PDT on the Notch signaling pathway in cholangiocarcinoma (CCA) cell lines: SPIE; 7380, Photodynamic Therapy: Back to the Future, 73806J 2009. | |
Kwon H, Song K, Han C, Zhang J, Lu L, Chen W and Wu T: Epigenetic Silencing of miRNA-34a in human cholangiocarcinoma via EZH2 and DNA methylation: Impact on regulation of notch pathway. Am J Pathol. 187:2288–2299. 2017.PubMed/NCBI View Article : Google Scholar | |
Guest RV, Boulter L, Dwyer BJ, Kendall TJ, Man TY, Minnis-Lyons SE, Lu WY, Robson AJ, Gonzalez SF, Raven A, et al: Notch3 drives development and progression of cholangiocarcinoma. Proc Natl Acad Sci USA. 113:12250–12255. 2016.PubMed/NCBI View Article : Google Scholar | |
Scarzello AJ, Jiang Q, Back T, Dang H, Hodge D, Hanson C, Subleski J, Weiss JM, Stauffer JK, Chaisaingmongkol J, et al: LTβR signalling preferentially accelerates oncogenic AKT-initiated liver tumours. Gut. 65:1765–1775. 2016.PubMed/NCBI View Article : Google Scholar | |
Tschaharganeh DF, Xue W, Calvisi DF, Evert M, Michurina TV, Dow LE, Banito A, Katz SF, Kastenhuber ER, Weissmueller S, et al: p53-dependent Nestin regulation links tumor suppression to cellular plasticity in liver cancer. Cell. 158:579–592. 2014.PubMed/NCBI View Article : Google Scholar | |
El Khatib M, Bozko P, Palagani V, Malek NP, Wilkens L and Plentz RR: Activation of Notch signaling is required for cholangiocarcinoma progression and is enhanced by inactivation of p53 in vivo. PLoS One. 8(e77433)2013.PubMed/NCBI View Article : Google Scholar | |
Frampton G, Coufal M, Li H, Ramirez J and DeMorrow S: Opposing actions of endocannabinoids on cholangiocarcinoma growth is via the differential activation of Notch signaling. Exp Cell Res. 316:1465–1478. 2010.PubMed/NCBI View Article : Google Scholar | |
Fox V, Gokhale PJ, Walsh JR, Matin M, Jones M and Andrews PW: Cell-cell signaling through NOTCH regulates human embryonic stem cell proliferation. Stem Cells. 26:715–723. 2008.PubMed/NCBI View Article : Google Scholar | |
Chen J, Kesari S, Rooney C, Strack PR, Chen J, Shen H, Wu L and Griffin JD: Inhibition of notch signaling blocks growth of glioblastoma cell lines and tumor neurospheres. Genes Cancer. 1:822–835. 2010.PubMed/NCBI View Article : Google Scholar | |
Balint K, Xiao M, Pinnix CC, Soma A, Veres I, Juhasz I, Brown EJ, Capobianco AJ, Herlyn M and Liu ZJ: Activation of Notch1 signaling is required for beta-catenin-mediated human primary melanoma progression. J Clin Invest. 115:3166–3176. 2005.PubMed/NCBI View Article : Google Scholar | |
Puget S, Grill J, Valent A, Bieche I, Dantas-Barbosa C, Kauffmann A, Dessen P, Lacroix L, Geoerger B, Job B, et al: Candidate genes on chromosome 9q33-34 involved in the progression of childhood ependymomas. J Clin Oncol. 27:1884–1892. 2009.PubMed/NCBI View Article : Google Scholar | |
Chen J, Chang H, Peng X, Gu Y, Yi L, Zhang Q, Zhu J and Mi M: 3,6-dihydroxyflavone suppresses the epithelial-mesenchymal transition in breast cancer cells by inhibiting the Notch signaling pathway. Sci Rep. 6(28858)2016.PubMed/NCBI View Article : Google Scholar | |
Wang X, Wu B and Zhong Z: Downregulation of YAP inhibits proliferation, invasion and increases cisplatin sensitivity in human hepatocellular carcinoma cells. Oncol Lett. 16:585–593. 2018.PubMed/NCBI View Article : Google Scholar | |
Wei X, Jia Y, Lou H, Ma J, Huang Q, Meng Y, Sun C, Yang Z, Li X, Xu S, et al: Targeting YAP suppresses ovarian cancer progression through regulation of the PI3K/Akt/mTOR pathway. Oncol Rep. 42:2768–2776. 2019.PubMed/NCBI View Article : Google Scholar | |
Götte M, Greve B, Kelsch R, Müller-Uthoff H, Weiss K, Kharabi Masouleh B, Sibrowski W, Kiesel L and Buchweitz O: The adult stem cell marker Musashi-1 modulates endometrial carcinoma cell cycle progression and apoptosis via Notch-1 and p21WAF1/CIP1. Int J Cancer. 129:2042–2049. 2011.PubMed/NCBI View Article : Google Scholar | |
Cheng C, Cui H, Zhang L, Jia Z, Song B, Wang F, Li Y, Liu J, Kong P, Shi R, et al: Genomic analyses reveal FAM84B and the NOTCH pathway are associated with the progression of esophageal squamous cell carcinoma. Gigascience. 5(1)2016.PubMed/NCBI View Article : Google Scholar | |
De Salvo M, Raimondi L, Vella S, Adesso L, Ciarapica R, Verginelli F, Pannuti A, Citti A, Boldrini R, Milano GM, et al: Hyper-activation of Notch3 amplifies the proliferative potential of rhabdomyosarcoma cells. PLoS One. 9(e96238)2014.PubMed/NCBI View Article : Google Scholar | |
Singh S, Arcaroli J, Chen Y, Thompson DC, Messersmith W, Jimeno A and Vasiliou V: ALDH1B1 is crucial for colon tumorigenesis by modulating Wnt/β-catenin, notch and PI3K/Akt signaling pathways. PLoS One. 10(e0121648)2015.PubMed/NCBI View Article : Google Scholar | |
Zhang XS, Hu YH, Gao HY, Lan XW and Xue YW: Downregulation of Notch1 inhibits the invasion and metastasis of human gastric cancer cells SGC7901 and MKN74 in vitro through PTEN activation and dephosphorylation of Akt and FAK. Mol Med Rep. 16:2318–2324. 2017.PubMed/NCBI View Article : Google Scholar | |
Dumont AG, Yang Y, Reynoso D, Katz D, Trent JC and Hughes DP: Anti-tumor effects of the Notch pathway in gastrointestinal stromal tumors. Carcinogenesis. 33:1674–1683. 2012.PubMed/NCBI View Article : Google Scholar | |
Yu XM, Phan T, Patel PN, Jaskula-Sztul R and Chen H: Chrysin activates Notch1 signaling and suppresses tumor growth of anaplastic thyroid carcinoma in vitro and in vivo. Cancer. 119:774–781. 2013.PubMed/NCBI View Article : Google Scholar | |
Jaskula-Sztul R, Pisarnturakit P, Landowski M, Chen H and Kunnimalaiyaan M: Expression of the active Notch1 decreases MTC tumor growth in vivo. J Surg Res. 171:23–27. 2011.PubMed/NCBI View Article : Google Scholar | |
Dong X, Lin Q, Aihara A, Li Y, Huang CK, Chung W, Tang Q, Chen X, Carlson R, Nadolny C, et al: Aspartate β-Hydroxylase expression promotes a malignant pancreatic cellular phenotype. Oncotarget. 6:1231–1248. 2015.PubMed/NCBI View Article : Google Scholar | |
Sturla LM, Tong M, Hebda N, Gao J, Thomas JM, Olsen M and de la Monte SM: Aspartate-β-hydroxylase (ASPH): A potential therapeutic target in human malignant gliomas. Heliyon. 2(e00203)2016.PubMed/NCBI View Article : Google Scholar | |
Adler JT, Hottinger DG, Kunnimalaiyaan M and Chen H: Histone deacetylase inhibitors upregulate Notch-1 and inhibit growth in pheochromocytoma cells. Surgery. 144:956–961; discussion 961-2. 2008.PubMed/NCBI View Article : Google Scholar | |
Walden D, Kunnimalaiyaan S, Sokolowski K, Clark TG and Kunnimalaiyaan M: Antiproliferative and apoptotic effects of xanthohumol in cholangiocarcinoma. Oncotarget. 8:88069–88078. 2017.PubMed/NCBI View Article : Google Scholar | |
Huang CK, Iwagami Y, Aihara A, Chung W, de la Monte S, Thomas JM, Olsen M, Carlson R, Yu T, Dong X and Wands J: Anti-Tumor effects of second generation β-Hydroxylase inhibitors on cholangiocarcinoma development and progression. PLoS One. 11(e0150336)2016.PubMed/NCBI View Article : Google Scholar | |
Cao Y, Yu L, Dai G, Zhang S, Zhang Z, Gao T and Guo W: Cinobufagin induces apoptosis of osteosarcoma cells through inactivation of Notch signaling. Eur J Pharmacol. 794:77–84. 2017.PubMed/NCBI View Article : Google Scholar | |
Sun Z, Zhou C, Liu F, Zhang W, Chen J, Pan Y, Ma L, Liu Q, Du Y, Yang J and Wang Q: Inhibition of breast cancer cell survival by Xanthohumol via modulation of the Notch signaling pathway in vivo and in vitro. Oncol Lett. 15:908–916. 2018.PubMed/NCBI View Article : Google Scholar | |
Gan RH, Lin LS, Xie J, Huang L, Ding LC, Su BH, Peng XE, Zheng DL and Lu YG: FLI-06 intercepts notch signaling and suppresses the proliferation and self-renewal of tongue cancer cells. Onco Targets Ther. 12:7663–7674. 2019.PubMed/NCBI View Article : Google Scholar | |
Dai L, He J, Liu Y, Byun J, Vivekanandan A, Pennathur S, Fan X and Lubman DM: Dose-dependent proteomic analysis of glioblastoma cancer stem cells upon treatment with γ-secretase inhibitor. Proteomics. 11:4529–4540. 2011.PubMed/NCBI View Article : Google Scholar | |
Tammam J, Ware C, Efferson C, O'Neil J, Rao S, Qu X, Gorenstein J, Angagaw M, Kim H, Kenific C, et al: Down-regulation of the Notch pathway mediated by a gamma-secretase inhibitor induces anti-tumour effects in mouse models of T-cell leukaemia. Br J Pharmacol. 158:1183–1195. 2009.PubMed/NCBI View Article : Google Scholar | |
Tanaka M, Setoguchi T, Hirotsu M, Gao H, Sasaki H, Matsunoshita Y and Komiya S: Inhibition of Notch pathway prevents osteosarcoma growth by cell cycle regulation. Br J Cancer. 100:1957–1965. 2009.PubMed/NCBI View Article : Google Scholar | |
Li ZL, Chen C, Yang Y, Wang C, Yang T, Yang X and Liu SC: Gamma secretase inhibitor enhances sensitivity to doxorubicin in MDA-MB-231 cells. Int J Clin Exp Pathol. 8:4378–4387. 2015.PubMed/NCBI | |
Liu X, Xu QR, Xie WF and Wang MD: DAPT suppresses the proliferation of human glioma cell line SHG-44. Asian Pac J Trop Med. 7:552–556. 2014.PubMed/NCBI View Article : Google Scholar | |
Li H, Li D and Meng N: Effects of RUNX3 mediated Notch signaling pathway on biological characteristics of colorectal cancer cells. Int J Oncol. 50:2059–2068. 2017.PubMed/NCBI View Article : Google Scholar | |
He G, Mu T, Yuan Y, Yang W, Zhang Y, Chen Q, Bian M, Pan Y, Xiang Q, Chen Z and Sun A: Effects of notch signaling pathway in cervical cancer by curcumin mediated photodynamic therapy and its possible mechanisms in vitro and in vivo. J Cancer. 10:4114–4122. 2019.PubMed/NCBI View Article : Google Scholar | |
Peng X, Zhou J, Li B, Zhang T, Zuo Y and Gu X: Notch1 and PI3K/Akt signaling blockers DAPT and LY294002 coordinately inhibit metastasis of gastric cancer through mutual enhancement. Cancer Chemother Pharmacol. 85:309–320. 2020.PubMed/NCBI View Article : Google Scholar | |
Zhao ZL, Zhang L, Huang CF, Ma SR, Bu LL, Liu JF, Yu GT, Liu B, Gutkind JS, Kulkarni AB, et al: NOTCH1 inhibition enhances the efficacy of conventional chemotherapeutic agents by targeting head neck cancer stem cell. Sci Rep. 6(24704)2016.PubMed/NCBI View Article : Google Scholar | |
Qin J, Wang R, Zhao C, Wen J, Dong H, Wang S, Li Y, Zhao Y, Li J, Yang Y, et al: Notch signaling regulates osteosarcoma proliferation and migration through Erk phosphorylation. Tissue Cell. 59:51–61. 2019.PubMed/NCBI View Article : Google Scholar | |
Tian Q, Xue Y, Zheng W, Sun R, Ji W, Wang X and An R: Overexpression of hypoxia-inducible factor 1α induces migration and invasion through Notch signaling. Int J Oncol. 47:728–738. 2015.PubMed/NCBI View Article : Google Scholar | |
Jiang LY, Zhang XL, Du P and Zheng JH: γ-Secretase Inhibitor, DAPT inhibits self-renewal and stemness maintenance of ovarian cancer stem-like cells in vitro. Chin J Cancer Res. 23:140–146. 2011.PubMed/NCBI View Article : Google Scholar | |
Ji Q, Hao X, Zhang M, Tang W, Yang M, Li L, Xiang D, Desano JT, Bommer GT, Fan D, et al: MicroRNA miR-34 inhibits human pancreatic cancer tumor-initiating cells. PLoS One. 4(e6816)2009.PubMed/NCBI View Article : Google Scholar | |
de Antonellis P, Medaglia C, Cusanelli E, Andolfo I, Liguori L, De Vita G, Carotenuto M, Bello A, Formiggini F, Galeone A, et al: MiR-34a targeting of Notch ligand delta-like 1 impairs CD15+/CD133+ tumor-propagating cells and supports neural differentiation in medulloblastoma. PLoS One. 6(e24584)2011.PubMed/NCBI View Article : Google Scholar | |
Wang J, Wang C, Meng Q, Li S, Sun X, Bo Y and Yao W: siRNA targeting Notch-1 decreases glioma stem cell proliferation and tumor growth. Mol Biol Rep. 39:2497–2503. 2012.PubMed/NCBI View Article : Google Scholar |