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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

Molecular Mechanisms Underlying the Anti-Breast Cancer Stem Cell Activity of Pterocladia capillacea and Corallina officinalis Polysaccharides

Author(s): Hebatallah G. Hafez, Rafat M. Mohareb, Sohair M. Salem, Azza A. Matloub, Emad F. Eskander and Hanaa H. Ahmed*

Volume 22, Issue 6, 2022

Published on: 27 July, 2021

Page: [1213 - 1225] Pages: 13

DOI: 10.2174/1871520621666210727122756

Price: $65

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Abstract

Objective: This study aimed to appraise the activity of Pterocladia capillacea and Corallina officinalis polysaccharides against Breast Cancer Stem Cells (BCSCs). P. capillacea and C. officinalis polysaccharides were characterized to be sulfated polysaccharide-protein complexes.

Methods: Cytotoxicity of the polysaccharides against MDA-MB-231 and MCF-7 cell lines along with their impact on CD44+/CD24− and aldehyde dehydrogenase 1(ALDH1) positive BCSC population were determined. Their effect on gene expression of CSC markers, Wnt/β-catenin and Notch signaling pathways was evaluated.

Results: P. capillacea and C. officinalis polysaccharides inhibited the growth of breast cancer cells and reduced BCSC subpopulation. P. capillacea polysaccharides significantly down-regulated OCT4, SOX2, ALDH1A3 and vimentin in MDA-MB-231 as well as in MCF-7 cells except for vimentin that was up-regulated in MCF-7 cells. C. officinalis polysaccharides exhibited similar effects except for OCT4 that was up-regulated in MDA-MB-231 cells. Significant suppression of Cyclin D1 gene expression was noted in MDA-MB-231 and MCF-7 cells treated with P. capillacea or C. officinalis polysaccharides. β-catenin and c-Myc genes were significantly down-regulated in MDA-MB-231 cells treated with C. officinalis and P. capillacea polysaccharides, respectively, while being up-regulated in MCF-7 cells treated with either of them. Additionally, P. capillacea and C. officinalis polysaccharides significantly down-regulated Hes1 gene in MCF-7 cells despite increasing Notch1 gene expression level. However, significant down-regulation of Notch1 gene was observed in MDA-MB-231 cells treated with P. capillacea polysaccharides.

Conclusion: Collectively, this study provides evidence for the effectiveness of P. capillacea and C. officinalis polysaccharides in targeting BCSCs through interfering with substantial signaling pathways contributing to their functionality.

Keywords: Pterocladia capillacea, Corallina officinalis, polysaccharides, breast cancer stem cells, molecular signaling pathways, aldehyde dehydrogenase.

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[1]
Bray, F.; Ferlay, J.; Soerjomataram, I.; Siegel, R.L.; Torre, L.A.; Jemal, A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J. Clin., 2018, 68(6), 394-424.
[http://dx.doi.org/10.3322/caac.21492] [PMID: 30207593]
[2]
Gluz, O.; Liedtke, C.; Gottschalk, N.; Pusztai, L.; Nitz, U.; Harbeck, N. Triple-negative breast cancer--current status and future directions. Ann. Oncol., 2009, 20(12), 1913-1927.
[http://dx.doi.org/10.1093/annonc/mdp492] [PMID: 19901010]
[3]
Finn, R.S.; Press, M.F.; Dering, J.; Arbushites, M.; Koehler, M.; Oliva, C.; Williams, L.S.; Di Leo, A. Estrogen receptor, progesterone receptor, human epidermal growth factor receptor 2 (HER2), and epidermal growth factor receptor expression and benefit from lapatinib in a randomized trial of paclitaxel with lapatinib or placebo as first-line treatment in HER2-negative or unknown metastatic breast cancer. J. Clin. Oncol., 2009, 27(24), 3908-3915.
[http://dx.doi.org/10.1200/JCO.2008.18.1925] [PMID: 19620495]
[4]
Foulkes, W.D.; Smith, I.E.; Reis-Filho, J.S. Triple-negative breast cancer. N. Engl. J. Med., 2010, 363(20), 1938-1948.
[http://dx.doi.org/10.1056/NEJMra1001389] [PMID: 21067385]
[5]
Bianchini, G.; Balko, J.M.; Mayer, I.A.; Sanders, M.E.; Gianni, L. Triple-negative breast cancer: challenges and opportunities of a heterogeneous disease. Nat. Rev. Clin. Oncol., 2016, 13(11), 674-690.
[http://dx.doi.org/10.1038/nrclinonc.2016.66] [PMID: 27184417]
[6]
Wang, X.; Zhang, N.; Huo, Q.; Sun, M.; Dong, L.; Zhang, Y.; Xu, G.; Yang, Q. Huaier aqueous extract inhibits stem-like characteristics of MCF7 breast cancer cells via inactivation of hedgehog pathway. Tumour Biol., 2014, 35(11), 10805-10813.
[http://dx.doi.org/10.1007/s13277-014-2390-2] [PMID: 25077927]
[7]
Hosseini, B.A.; Pasdaran, A.; Kazemi, T.; Shanehbandi, D.; Karami, H.; Orangi, M.; Baradaran, B. Dichloromethane fractions of Scrophularia oxysepala extract induce apoptosis in MCF-7 human breast cancer cells. Bosn. J. Basic Med. Sci., 2015, 15(1), 26-32.
[http://dx.doi.org/10.17305/bjbms.2015.1.226] [PMID: 25725141]
[8]
Gerber, B.; Freund, M.; Reimer, T. Recurrent breast cancer: treatment strategies for maintaining and prolonging good quality of life. Dtsch. Arztebl. Int., 2010, 107(6), 85-91.
[PMID: 20204119]
[9]
Hu, G.; Chong, R.A.; Yang, Q.; Wei, Y.; Blanco, M.A.; Li, F.; Reiss, M.; Au, J.L.; Haffty, B.G.; Kang, Y. MTDH activation by 8q22 genomic gain promotes chemoresistance and metastasis of poor-prognosis breast cancer. Cancer Cell, 2009, 15(1), 9-20.
[http://dx.doi.org/10.1016/j.ccr.2008.11.013] [PMID: 19111877]
[10]
Balic, M.; Lin, H.; Young, L.; Hawes, D.; Giuliano, A.; McNamara, G.; Datar, R.H.; Cote, R.J. Most early disseminated cancer cells detected in bone marrow of breast cancer patients have a putative breast cancer stem cell phenotype. Clin. Cancer Res., 2006, 12(19), 5615-5621.
[http://dx.doi.org/10.1158/1078-0432.CCR-06-0169] [PMID: 17020963]
[11]
Dean, M.; Fojo, T.; Bates, S. Tumour stem cells and drug resistance. Nat. Rev. Cancer, 2005, 5(4), 275-284.
[http://dx.doi.org/10.1038/nrc1590] [PMID: 15803154]
[12]
Kong, D.; Li, Y.; Wang, Z.; Sarkar, F.H. Cancer Stem Cells and Epithelial-to-Mesenchymal Transition (EMT)-Phenotypic Cells: Are They Cousins or Twins? Cancers (Basel), 2011, 3(1), 716-729.
[http://dx.doi.org/10.3390/cancers30100716] [PMID: 21643534]
[13]
Huber, M.A.; Kraut, N.; Beug, H. Molecular requirements for epithelial-mesenchymal transition during tumor progression. Curr. Opin. Cell Biol., 2005, 17(5), 548-558.
[http://dx.doi.org/10.1016/j.ceb.2005.08.001] [PMID: 16098727]
[14]
Al-Hajj, M.; Wicha, M.S.; Benito-Hernandez, A.; Morrison, S.J.; Clarke, M.F. Prospective identification of tumorigenic breast cancer cells. Proc. Natl. Acad. Sci. USA, 2003, 100(7), 3983-3988.
[http://dx.doi.org/10.1073/pnas.0530291100] [PMID: 12629218]
[15]
Ginestier, C.; Hur, M.H.; Charafe-Jauffret, E.; Monville, F.; Dutcher, J.; Brown, M.; Jacquemier, J.; Viens, P.; Kleer, C.G.; Liu, S.; Schott, A.; Hayes, D.; Birnbaum, D.; Wicha, M.S.; Dontu, G. ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome. Cell Stem Cell, 2007, 1(5), 555-567.
[http://dx.doi.org/10.1016/j.stem.2007.08.014] [PMID: 18371393]
[16]
Zhou, S.; Morris, J.J.; Barnes, Y.; Lan, L.; Schuetz, J.D.; Sorrentino, B.P. Bcrp1 gene expression is required for normal numbers of side population stem cells in mice, and confers relative protection to mitoxantrone in hematopoietic cells in vivo. Proc. Natl. Acad. Sci. USA, 2002, 99(19), 12339-12344.
[http://dx.doi.org/10.1073/pnas.192276999] [PMID: 12218177]
[17]
Luo, M.; Clouthier, S.G.; Deol, Y.; Liu, S.; Nagrath, S.; Azizi, E.; Wicha, M.S. Breast cancer stem cells: current advances and clinical implications. Methods Mol. Biol., 2015, 1293, 1-49.
[http://dx.doi.org/10.1007/978-1-4939-2519-3_1] [PMID: 26040679]
[18]
Wen, Y.; Hou, Y.; Huang, Z.; Cai, J.; Wang, Z. SOX2 is required to maintain cancer stem cells in ovarian cancer. Cancer Sci., 2017, 108(4), 719-731.
[http://dx.doi.org/10.1111/cas.13186] [PMID: 28165651]
[19]
Wang, N.; Wang, Z.; Peng, C.; You, J.; Shen, J.; Han, S.; Chen, J. Dietary compound isoliquiritigenin targets GRP78 to chemosensitize breast cancer stem cells via β-catenin/ABCG2 signaling. Carcinogenesis, 2014, 35(11), 2544-2554.
[http://dx.doi.org/10.1093/carcin/bgu187] [PMID: 25194164]
[20]
Zhang, H.; Zhang, X.; Wu, X.; Li, W.; Su, P.; Cheng, H.; Xiang, L.; Gao, P.; Zhou, G. Interference of Frizzled 1 (FZD1) reverses multidrug resistance in breast cancer cells through the Wnt/β-catenin pathway. Cancer Lett., 2012, 323(1), 106-113.
[http://dx.doi.org/10.1016/j.canlet.2012.03.039] [PMID: 22484497]
[21]
Oliveira, L.R.; Jeffrey, S.S.; Ribeiro-Silva, A. Stem cells in human breast cancer. Histol. Histopathol., 2010, 25(3), 371-385.
[PMID: 20054808]
[22]
Phillips, T.M.; McBride, W.H.; Pajonk, F. The response of CD24(-/low)/CD44+ breast cancer-initiating cells to radiation. J. Natl. Cancer Inst., 2006, 98(24), 1777-1785.
[http://dx.doi.org/10.1093/jnci/djj495] [PMID: 17179479]
[23]
Farnie, G.; Clarke, R.B. Mammary stem cells and breast cancer--role of Notch signalling. Stem Cell Rev., 2007, 3(2), 169-175.
[http://dx.doi.org/10.1007/s12015-007-0023-5] [PMID: 17873349]
[24]
Li, Y.; Zhang, T.; Korkaya, H.; Liu, S.; Lee, H.F.; Newman, B.; Yu, Y.; Clouthier, S.G.; Schwartz, S.J.; Wicha, M.S.; Sun, D. Sulforaphane, a dietary component of broccoli/broccoli sprouts, inhibits breast cancer stem cells. Clin. Cancer Res., 2010, 16(9), 2580-2590.
[http://dx.doi.org/10.1158/1078-0432.CCR-09-2937] [PMID: 20388854]
[25]
Park, S.; Kim, J.; Kim, Y. Mulberry leaf extract inhibits cancer cell stemness in neuroblastoma. Nutr. Cancer, 2012, 64(6), 889-898.
[http://dx.doi.org/10.1080/01635581.2012.707280] [PMID: 22860924]
[26]
Lin, C.H.; Shen, Y.A.; Hung, P.H.; Yu, Y.B.; Chen, Y.J. Epigallocathechin gallate, polyphenol present in green tea, inhibits stem-like characteristics and epithelial-mesenchymal transition in nasopharyngeal cancer cell lines. BMC Complement. Altern. Med., 2012, 12, 201.
[http://dx.doi.org/10.1186/1472-6882-12-201] [PMID: 23110507]
[27]
Pádua, D.; Rocha, E.; Gargiulo, D.; Ramos, A.A. Bioactive compounds from brown seaweeds: Phloroglucinol, fucoxanthin and fucoidan as promising therapeutic agents against breast cancer. Phytochem. Lett., 2015, 14, 91-98.
[http://dx.doi.org/10.1016/j.phytol.2015.09.007]
[28]
Murad, H.; Hawat, M.; Ekhtiar, A.; AlJapawe, A.; Abbas, A.; Darwish, H.; Sbenati, O.; Ghannam, A. Induction of G1-phase cell cycle arrest and apoptosis pathway in MDA-MB-231 human breast cancer cells by sulfated polysaccharide extracted from Laurencia papillosa. Cancer Cell Int., 2016, 16, 39.
[http://dx.doi.org/10.1186/s12935-016-0315-4] [PMID: 27231438]
[29]
Lee, J.C.; Hou, M.F.; Huang, H.W.; Chang, F.R.; Yeh, C.C.; Tang, J.Y.; Chang, H.W. Marine algal natural products with anti-oxidative, anti-inflammatory, and anti-cancer properties. Cancer Cell Int., 2013, 13(1), 55.
[http://dx.doi.org/10.1186/1475-2867-13-55] [PMID: 23724847]
[30]
Silva, T.H.; Alves, A.; Popa, E.G.; Reys, L.L.; Gomes, M.E.; Sousa, R.A.; Silva, S.S.; Mano, J.F.; Reis, R.L. Marine algae sulfated polysaccharides for tissue engineering and drug delivery approaches. Biomatter, 2012, 2(4), 278-289.
[http://dx.doi.org/10.4161/biom.22947] [PMID: 23507892]
[31]
Mohamed, S.F.; Agili, F.A. Antiviral sulphated polysaccharide from brown algae Padina pavonia characterization and structure elucidation. Int. J. Chemtech Res., 2013, 5, 1469-1476.
[32]
Queiroz, K.C.; Assis, C.F.; Medeiros, V.P.; Rocha, H.A.; Aoyama, H.; Ferreira, C.V.; Leite, E.L. Cytotoxicity effect of algal polysaccharides on HL60 cells. Biochemistry (Mosc.), 2006, 71(12), 1312-1315.
[http://dx.doi.org/10.1134/S0006297906120042] [PMID: 17223782]
[33]
Maruyama, H.; Tamauchi, H.; Hashimoto, M.; Nakano, T. Antitumor activity and immune response of Mekabu fucoidan extracted from Sporophyll of Undaria pinnatifida. in vivo, 2003, 17(3), 245-249.
[PMID: 12929574]
[34]
Rocha, H.A.; Franco, C.R.; Trindade, E.S.; Veiga, S.S.; Leite, E.L.; Nader, H.B.; Dietrich, C.P. Fucan inhibits Chinese hamster ovary cell (CHO) adhesion to fibronectin by binding to the extracellular matrix. Planta Med., 2005, 71(7), 628-633.
[http://dx.doi.org/10.1055/s-2005-871268] [PMID: 16041648]
[35]
Matloub, A.A.; Elsouda, S.S.M.; El-Senousy, W.M.; Hamed, M.; Aly, H.; Ali, S.A.; Mohammed, R.S.; Mahmoud, K.; El-Hallouty, S.; Ibrahim, N.A.; Awad, N.A.; El-Rafaie, H.M. In vitro antiviral, cytotoxic, antioxidant and hypolipidemic activites of polysaccharide isolated from marine algae. IJPPR, 2015, 7, 1099-1111.
[36]
Dai, X.; Cheng, H.; Bai, Z.; Li, J. Breast Cancer Cell Line Classification and Its Relevance with Breast Tumor Subtyping. J. Cancer, 2017, 8(16), 3131-3141.
[http://dx.doi.org/10.7150/jca.18457] [PMID: 29158785]
[37]
Comşa, Ş.; Cîmpean, A.M.; Raica, M. The Story of MCF-7 Breast Cancer Cell Line: 40 years of Experience in Research. Anticancer Res., 2015, 35(6), 3147-3154.
[PMID: 26026074]
[38]
Matloub, A.A.; Aglan, H.A.; Mohamed El Souda, S.S.; Aboutabl, M.E.; Maghraby, A.S.; Ahmed, H.H. Influence of bioactive sulfated polysaccharide-protein complexes on hepatocarcinogenesis, angiogenesis and immunomodulatory activities. Asian Pac. J. Trop. Med., 2016, 9(12), 1200-1211.
[http://dx.doi.org/10.1016/j.apjtm.2016.11.004] [PMID: 27955748]
[39]
Mosmann, T. Rapid colorimetric assay for cellular growth and survival: Application to proliferation and cytotoxicity assays. J. Immunol. Methods, 1983, 65(1-2), 55-63.
[http://dx.doi.org/10.1016/0022-1759(83)90303-4] [PMID: 6606682]
[40]
Livak, K.J.; Schmittgen, T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)). Method. Methods, 2001, 25(4), 402-408.
[http://dx.doi.org/10.1006/meth.2001.1262] [PMID: 11846609]
[41]
Yang, Y.; Liu, D.; Wu, J.; Chen, Y.; Wang, S. In vitro antioxidant activities of sulfated polysaccharide fractions extracted from Corallina officinalis. Int. J. Biol. Macromol., 2011, 49(5), 1031-1037.
[http://dx.doi.org/10.1016/j.ijbiomac.2011.08.026] [PMID: 21896282]
[42]
Raposo, M.F.; de Morais, R.M.; Bernardo de Morais, A.M. Bioactivity and applications of sulphated polysaccharides from marine microalgae. Mar. Drugs, 2013, 11(1), 233-252.
[http://dx.doi.org/10.3390/md11010233] [PMID: 23344113]
[43]
Gheda, S.; El-Sheekh, M.; Abou-Zeid, A. In vitro anticancer activity of polysaccharide extracted from red alga Jania rubens against breast and colon cancer cell lines. Asian Pac. J. Trop. Med., 2018, 11, 583-589.
[http://dx.doi.org/10.4103/1995-7645.244523]
[44]
Wang, J.; Wu, H.J.; Zhou, C.Z.; Wang, H. Sulfated polysaccharide-protein complex sensitizes doxorubicin-induced apoptosis of breast cancer cells in vitro andin vivo. Exp. Ther. Med., 2016, 12(4), 2169-2176.
[http://dx.doi.org/10.3892/etm.2016.3574] [PMID: 27698706]
[45]
Liao, N.; Zhong, J.; Zhang, R.; Ye, X.; Zhang, Y.; Wang, W.; Wang, Y.; Chen, S.; Liu, D.; Liu, R. Protein-Bound Polysaccharide from Corbicula fluminea Inhibits Cell Growth in MCF-7 and MDA-MB-231 Human Breast Cancer Cells. PLoS One, 2016, 11(12), e0167889.
[http://dx.doi.org/10.1371/journal.pone.0167889] [PMID: 27959954]
[46]
Chang, K.Y.; Yang, J.R. Analysis and prediction of highly effective antiviral peptides based on random forests. PLoS One, 2013, 8(8), e70166.
[http://dx.doi.org/10.1371/journal.pone.0070166] [PMID: 23940542]
[47]
Li, X.; Kong, X.; Kong, X.; Wang, Y.; Yan, S.; Yang, Q. 53BP1 sensitizes breast cancer cells to 5-fluorouracil. PLoS One, 2013, 8(9), e74928.
[http://dx.doi.org/10.1371/journal.pone.0074928] [PMID: 24040364]
[48]
Fillmore, C.M.; Kuperwasser, C. Human breast cancer cell lines contain stem-like cells that self-renew, give rise to phenotypically diverse progeny and survive chemotherapy. Breast Cancer Res., 2008, 10(2), R25.
[http://dx.doi.org/10.1186/bcr1982] [PMID: 18366788]
[49]
Hu, B.; Yan, W.; Wang, M.; Cui, X.; Hu, Y.; Chen, Q.; Zhang, Y.; Qi, X.; Jiang, J. Huaier polysaccharide inhibits the stem-like characteristics of ERα-36high triple negative breast cancer cells via inactivation of the ERα-36 signaling pathway. Int. J. Biol. Sci., 2019, 15(7), 1358-1367.
[http://dx.doi.org/10.7150/ijbs.27360] [PMID: 31337967]
[50]
Sun, Y.; Sun, T.; Wang, F.; Zhang, J.; Li, C.; Chen, X.; Li, Q.; Sun, S. A polysaccharide from the fungi of Huaier exhibits anti-tumor potential and immunomodulatory effects. Carbohydr. Polym., 2013, 92(1), 577-582.
[http://dx.doi.org/10.1016/j.carbpol.2012.09.006] [PMID: 23218338]
[51]
Klose, J.; Trefz, S.; Wagner, T.; Steffen, L.; Preißendörfer Charrier, A.; Radhakrishnan, P.; Volz, C.; Schmidt, T.; Ulrich, A.; Dieter, S.M.; Ball, C.; Glimm, H.; Schneider, M. Salinomycin: Anti-tumor activity in a pre-clinical colorectal cancer model. PLoS One, 2019, 14(2), e0211916.
[http://dx.doi.org/10.1371/journal.pone.0211916] [PMID: 30763370]
[52]
Jung, J.W.; Park, S.B.; Lee, S.J.; Seo, M.S.; Trosko, J.E.; Kang, K.S. Metformin represses self-renewal of the human breast carcinoma stem cells via inhibition of estrogen receptor-mediated OCT4 expression. PLoS One, 2011, 6(11), e28068.
[http://dx.doi.org/10.1371/journal.pone.0028068] [PMID: 22132214]
[53]
Zhang, Y.; Eades, G.; Yao, Y.; Li, Q.; Zhou, Q. Estrogen receptor α signaling regulates breast tumor-initiating cells by down-regulating miR-140 which targets the transcription factor SOX2. J. Biol. Chem., 2012, 287(49), 41514-41522.
[http://dx.doi.org/10.1074/jbc.M112.404871] [PMID: 23060440]
[54]
Yi, H.; Cho, H.J.; Cho, S.M.; Jo, K.; Park, J.A.; Lee, S.H.; Chang, B.J.; Kim, J.S.; Shin, H.C. Effect of 5-FU and MTX on the Expression of Drug-resistance Related Cancer Stem Cell Markers in Non-small Cell Lung Cancer Cells. Korean J. Physiol. Pharmacol., 2012, 16(1), 11-16.
[http://dx.doi.org/10.4196/kjpp.2012.16.1.11] [PMID: 22416214]
[55]
Lu, C.S.; Shieh, G.S.; Wang, C.T.; Su, B.H.; Su, Y.C.; Chen, Y.C.; Su, W.C.; Wu, P.; Yang, W.H.; Shiau, A.L.; Wu, C.L. Chemotherapeutics-induced Oct4 expression contributes to drug resistance and tumor recurrence in bladder cancer. Oncotarget, 2017, 8(19), 30844-30858.
[http://dx.doi.org/10.18632/oncotarget.9602] [PMID: 27244887]
[56]
Xu, Z.Y.; Tang, J.N.; Xie, H.X.; Du, Y.A.; Huang, L.; Yu, P.F.; Cheng, X.D. 5-Fluorouracil chemotherapy of gastric cancer generates residual cells with properties of cancer stem cells. Int. J. Biol. Sci., 2015, 11(3), 284-294.
[http://dx.doi.org/10.7150/ijbs.10248] [PMID: 25678847]
[57]
Coulombe, P.A.; Wong, P. Cytoplasmic intermediate filaments revealed as dynamic and multipurpose scaffolds. Nat. Cell Biol., 2001, 6(8), 699-706.
[http://dx.doi.org/10.1038/ncb0804-699] [PMID: 15303099]
[58]
Han, X.Y.; Wei, B.; Fang, J.F.; Zhang, S.; Zhang, F.C.; Zhang, H.B.; Lan, T.Y.; Lu, H.Q.; Wei, H.B. Epithelial-mesenchymal transition associates with maintenance of stemness in spheroid-derived stem-like colon cancer cells. PLoS One, 2013, 8(9), e73341.
[http://dx.doi.org/10.1371/journal.pone.0073341] [PMID: 24039918]
[59]
Hsu, H.Y.; Lin, T.Y.; Hwang, P.A.; Tseng, L.M.; Chen, R.H.; Tsao, S.M.; Hsu, J. Fucoidan induces changes in the epithelial to mesenchymal transition and decreases metastasis by enhancing ubiquitin-dependent TGFβ receptor degradation in breast cancer. Carcinogenesis, 2013, 34(4), 874-884.
[http://dx.doi.org/10.1093/carcin/bgs396] [PMID: 23275155]
[60]
Al Saleh, S.; Al Mulla, F.; Luqmani, Y.A. Estrogen receptor silencing induces epithelial to mesenchymal transition in human breast cancer cells. PLoS One, 2011, 6(6), e20610.
[http://dx.doi.org/10.1371/journal.pone.0020610] [PMID: 21713035]
[61]
Bouris, P.; Skandalis, S.S.; Piperigkou, Z.; Afratis, N.; Karamanou, K.; Aletras, A.J.; Moustakas, A.; Theocharis, A.D.; Karamanos, N.K. Estrogen receptor alpha mediates epithelial to mesenchymal transition, expression of specific matrix effectors and functional properties of breast cancer cells. Matrix Biol., 2015, 43, 42-60.
[http://dx.doi.org/10.1016/j.matbio.2015.02.008] [PMID: 25728938]
[62]
Nair, M.G.; Prabhu, J.S.; Korlimarla, A.; Rajarajan, S. P S, H.; Kaul, R.; Alexander, A.; Raghavan, R.; B S, S.; T S, S. miR-18a activates Wnt pathway in ER-positive breast cancer and is associated with poor prognosis. Cancer Med., 2020, 9(15), 5587-5597.
[http://dx.doi.org/10.1002/cam4.3183] [PMID: 32543775]
[63]
Terashima, M.; Sakai, K.; Togashi, Y.; Hayashi, H.; De Velasco, M.A.; Tsurutani, J.; Nishio, K. Synergistic antitumor effects of S-1 with eribulin in vitro and in vivo for triple-negative breast cancer cell lines. Springerplus, 2014, 3, 417.
[http://dx.doi.org/10.1186/2193-1801-3-417] [PMID: 25140293]
[64]
Zhang, W.; Feng, M.; Zheng, G.; Chen, Y.; Wang, X.; Pen, B.; Yin, J.; Yu, Y.; He, Z. Chemoresistance to 5-fluorouracil induces epithelial-mesenchymal transition via up-regulation of Snail in MCF7 human breast cancer cells. Biochem. Biophys. Res. Commun., 2012, 417(2), 679-685.
[http://dx.doi.org/10.1016/j.bbrc.2011.11.142] [PMID: 22166209]
[65]
Liu, S.; Dontu, G.; Wicha, M.S. Mammary stem cells, self-renewal pathways, and carcinogenesis. Breast Cancer Res., 2005, 7(3), 86-95.
[http://dx.doi.org/10.1186/bcr1021] [PMID: 15987436]
[66]
Yang, S.; Sun, S.; Xu, W.; Yu, B.; Wang, G.; Wang, H. Astragalus polysaccharide inhibits breast cancer cell migration and invasion by regulating epithelial mesenchymal transition via the Wnt/β catenin signaling pathway. Mol. Med. Rep., 2020, 21(4), 1819-1832.
[http://dx.doi.org/10.3892/mmr.2020.10983] [PMID: 32319619]
[67]
Sun, S.; Yang, S.; An, N.; Wang, G.; Xu, Q.; Liu, J.; Mao, Y. Astragalus polysaccharides inhibits cardiomyocyte apoptosis during diabetic cardiomyopathy via the endoplasmic reticulum stress pathway. J. Ethnopharmacol., 2019, 238, 111857.
[http://dx.doi.org/10.1016/j.jep.2019.111857] [PMID: 30959142]
[68]
Jin, Z.; Han, Y.X.; Han, X.R. Degraded iota-carrageenan can induce apoptosis in human osteosarcoma cells via the Wnt/β-catenin signaling pathway. Nutr. Cancer, 2013, 65(1), 126-131.
[http://dx.doi.org/10.1080/01635581.2013.741753] [PMID: 23368922]
[69]
Boo, H.J.; Hong, J.Y.; Kim, S.C.; Kang, J.I.; Kim, M.K.; Kim, E.J.; Hyun, J.W.; Koh, Y.S.; Yoo, E.S.; Kwon, J.M.; Kang, H.K. The anticancer effect of fucoidan in PC-3 prostate cancer cells. Mar. Drugs, 2013, 11(8), 2982-2999.
[http://dx.doi.org/10.3390/md11082982] [PMID: 23966032]
[70]
Fu, Y.; Zheng, S.; An, N.; Athanasopoulos, T.; Popplewell, L.; Liang, A.; Li, K.; Hu, C.; Zhu, Y. β-catenin as a potential key target for tumor suppression. Int. J. Cancer, 2011, 129(7), 1541-1551.
[http://dx.doi.org/10.1002/ijc.26102] [PMID: 21455986]
[71]
Ahmed, H.H.; El-Abhar, H.S.; Hassanin, E.A.K.; Abdelkader, N.F.; Shalaby, M.B. Punica granatum suppresses colon cancer through downregulation of Wnt/β-Catenin in rat model. Rev. Bras. Farmacogn., 2017, 27, 627-635.
[http://dx.doi.org/10.1016/j.bjp.2017.05.010]
[72]
Li, Z.; Sun, Y.; Qu, M.; Wan, H.; Cai, F.; Zhang, P. Inhibiting the MNK-eIF4E-β-catenin axis increases the responsiveness of aggressive breast cancer cells to chemotherapy. Oncotarget, 2017, 8(2), 2906-2915.
[http://dx.doi.org/10.18632/oncotarget.13772] [PMID: 27926520]
[73]
Dontu, G.; Jackson, K.W.; McNicholas, E.; Kawamura, M.J.; Abdallah, W.M.; Wicha, M.S. Role of Notch signaling in cell-fate determination of human mammary stem/progenitor cells. Breast Cancer Res., 2004, 6(6), R605-R615.
[http://dx.doi.org/10.1186/bcr920] [PMID: 15535842]
[74]
Wang, C.L.; Meng, M.; Liu, S.B.; Wang, L.R.; Hou, L.H.; Cao, X.H. A chemically sulfated polysaccharide from Grifola frondos induces HepG2 cell apoptosis by notch1-NF-κB pathway. Carbohydr. Polym., 2013, 95(1), 282-287.
[http://dx.doi.org/10.1016/j.carbpol.2013.02.057] [PMID: 23618270]
[75]
Nie, X.; Shi, B.; Ding, Y.; Tao, W. Preparation of a chemically sulfated polysaccharide derived from Grifola frondosa and its potential biological activities. Int. J. Biol. Macromol., 2006, 39(4-5), 228-233.
[http://dx.doi.org/10.1016/j.ijbiomac.2006.03.030] [PMID: 16822541]
[76]
Rizzo, P.; Miao, H.; D’Souza, G.; Osipo, C.; Song, L.L.; Yun, J.; Zhao, H.; Mascarenhas, J.; Wyatt, D.; Antico, G.; Hao, L.; Yao, K.; Rajan, P.; Hicks, C.; Siziopikou, K.; Selvaggi, S.; Bashir, A.; Bhandari, D.; Marchese, A.; Lendahl, U.; Qin, J.Z.; Tonetti, D.A.; Albain, K.; Nickoloff, B.J.; Miele, L. Cross-talk between notch and the estrogen receptor in breast cancer suggests novel therapeutic approaches. Cancer Res., 2008, 68(13), 5226-5235.
[http://dx.doi.org/10.1158/0008-5472.CAN-07-5744] [PMID: 18593923]
[77]
Li, L.Q.; Pan, D.; Zhang, S.W. -Y-Xie, D.; Zheng, X.L.; Chen, H. Autophagy regulates chemoresistance of gastric cancer stem cells via the Notch signaling pathway. Eur. Rev. Med. Pharmacol. Sci., 2018, 22(11), 3402-3407.
[PMID: 29917191]

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