Login Register Cart 0
Generic placeholder image

Current Pharmaceutical Design

Editor-in-Chief

ISSN (Print): 1381-6128
ISSN (Online): 1873-4286

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe
Review Article

Deciphering Potential Role of Hippo Signaling Pathway in Breast Cancer: A Comprehensive Review

Author(s): Hunayna Bhavnagari, Apexa Raval and Franky Shah*

Volume 29, Issue 44, 2023

Published on: 21 December, 2023

Page: [3505 - 3518] Pages: 14

DOI: 10.2174/0113816128274418231215054210

Price: $65

Open Access Journals Promotions 2
Abstract

Breast cancer is a heterogeneous disease and a leading malignancy around the world. It is a vital cause of untimely mortality among women. Drug resistance is the major challenge for effective cancer therapeutics. In contrast, cancer stem cells (CSCs) are one of the reasons for drug resistance, tumor progression, and metastasis. The small population of CSCs present in each tumor has the ability of self-renewal, differentiation, and tumorigenicity. CSCs are often identified and enriched using a variety of cell surface markers (CD44, CD24, CD133, ABCG2, CD49f, LGR5, SSEA-3, CD70) that exert their functions by different regulatory networks, i.e., Notch, Wnt/β-catenin, hedgehog (Hh), and Hippo signaling pathways. Particularly the Hippo signaling pathway is the emerging and very less explored cancer stem cell pathway. Here, in this review, the Hippo signaling molecules are elaborated with respect to their ability of stemness as epigenetic modulators and how these molecules can be targeted for better cancer treatment and to overcome drug resistance.

Keywords: Breast cancer, cancer stem cell, heterogeneous disease, drug resistance, epigenetic modulators, Hippo signaling pathway.

Next »
[1]
Sung H, Ferlay J, Siegel RL, et al. Global cancer statistics 2020: Globocan estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 2021; 71(3): 209-49.
[http://dx.doi.org/10.3322/caac.21660] [PMID: 33538338]
[2]
Wu L, Yang X. Targeting the Hippo pathway for breast cancer therapy. Cancers 2018; 10(11): 422.
[http://dx.doi.org/10.3390/cancers10110422] [PMID: 30400599]
[3]
Ricardo S, Vieira AF, Gerhard R, et al. Breast cancer stem cell markers CD44, CD24 and ALDH1: Expression distribution within intrinsic molecular subtype. J Clin Pathol 2011; 64(11): 937-46.
[http://dx.doi.org/10.1136/jcp.2011.090456] [PMID: 21680574]
[4]
Rabinovich I, Sebastião APM, Lima RS, et al. Cancer stem cell markers ALDH1 and CD44+/CD24- phenotype and their prognosis impact in invasive ductal carcinoma. Eur J Histochem 2018; 62(3): 62.
[http://dx.doi.org/10.4081/ejh.2018.2943] [PMID: 30362671]
[5]
Albini A, Bruno A, Gallo C, Pajardi G, Noonan DM, Dallaglio K. Cancer stem cells and the tumor microenvironment: Interplay in tumor heterogeneity. Connect Tissue Res 2015; 56(5): 414-25.
[http://dx.doi.org/10.3109/03008207.2015.1066780] [PMID: 26291921]
[6]
Tanei T, Morimoto K, Shimazu K, et al. Association of breast cancer stem cells identified by aldehyde dehydrogenase 1 expression with resistance to sequential Paclitaxel and epirubicin-based chemotherapy for breast cancers. Clin Cancer Res 2009; 15(12): 4234-41.
[http://dx.doi.org/10.1158/1078-0432.CCR-08-1479] [PMID: 19509181]
[7]
Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci 2003; 100(7): 3983-8.
[http://dx.doi.org/10.1073/pnas.0530291100] [PMID: 12629218]
[8]
Yoshida GJ, Saya H. Therapeutic strategies targeting cancer stem cells. Cancer Sci 2016; 107(1): 5-11.
[http://dx.doi.org/10.1111/cas.12817] [PMID: 26362755]
[9]
Shipitsin M, Campbell LL, Argani P, et al. Molecular definition of breast tumor heterogeneity. Cancer Cell 2007; 11(3): 259-73.
[http://dx.doi.org/10.1016/j.ccr.2007.01.013] [PMID: 17349583]
[10]
Wright MH, Calcagno AM, Salcido CD, Carlson MD, Ambudkar SV, Varticovski L. Brca1 breast tumors contain distinct CD44+/CD24- and CD133+cells with cancer stem cell characteristics. Breast Cancer Res 2008; 10(1): R10.
[http://dx.doi.org/10.1186/bcr1855] [PMID: 18241344]
[11]
Wang D, Cai C, Dong X, et al. Identification of multipotent mammary stem cells by protein C receptor expression. Nature 2015; 517(7532): 81-4.
[http://dx.doi.org/10.1038/nature13851] [PMID: 25327250]
[12]
Leccia F, Del Vecchio L, Mariotti E, et al. ABCG2, a novel antigen to sort luminal progenitors of BRCA1- Breast cancer cells. Mol Cancer 2014; 13(1): 213.
[http://dx.doi.org/10.1186/1476-4598-13-213] [PMID: 25216750]
[13]
Cheung SKC, Chuang PK, Huang HW, et al. Stage-specific embryonic antigen-3 (SSEA-3) and β3GalT5 are cancer specific and significant markers for breast cancer stem cells. Proc Natl Acad Sci USA 2016; 113(4): 960-5.
[http://dx.doi.org/10.1073/pnas.1522602113] [PMID: 26677875]
[14]
Liu L, Yin B, Yi Z, et al. Breast cancer stem cells characterized by CD70 expression preferentially metastasize to the lungs. Breast Cancer 2018; 25(6): 706-16.
[http://dx.doi.org/10.1007/s12282-018-0880-6] [PMID: 29948958]
[15]
Akbarzadeh M, Maroufi NF, Tazehkand AP, et al. Current approaches in identification and isolation of cancer stem cells. J Cell Physiol 2019; 234(9): 14759-72.
[http://dx.doi.org/10.1002/jcp.28271] [PMID: 30741412]
[16]
Pattabiraman DR, Weinberg RA. Tackling the cancer stem cells - What challenges do they pose? Nat Rev Drug Discov 2014; 13(7): 497-512.
[http://dx.doi.org/10.1038/nrd4253] [PMID: 24981363]
[17]
Beça FF, Caetano P, Gerhard R, et al. Cancer stem cells markers CD44, CD24 and ALDH1 in breast cancer special histological types. J Clin Pathol 2013; 66(3): 187-91.
[http://dx.doi.org/10.1136/jclinpath-2012-201169] [PMID: 23112116]
[18]
Pham PV, Phan NLC, Nguyen NT, et al. Differentiation of breast cancer stem cells by knockdown of CD44: Promising differentiation therapy. J Transl Med 2011; 9(1): 209.
[http://dx.doi.org/10.1186/1479-5876-9-209] [PMID: 22152097]
[19]
Bensimon J, Altmeyer-Morel S, Benjelloun H, Chevillard S, Lebeau J. CD24−/low stem-like breast cancer marker defines the radiation-resistant cells involved in memorization and transmission of radiation-induced genomic instability. Oncogene 2013; 32(2): 251-8.
[http://dx.doi.org/10.1038/onc.2012.31] [PMID: 22330142]
[20]
Muzio G, Maggiora M, Paiuzzi E, Oraldi M, Canuto RA. Aldehyde dehydrogenases and cell proliferation. Free Radic Biol Med 2012; 52(4): 735-46.
[http://dx.doi.org/10.1016/j.freeradbiomed.2011.11.033] [PMID: 22206977]
[21]
Ginestier C, Hur MH, Charafe-Jauffret E, et al. 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): 555-67.
[http://dx.doi.org/10.1016/j.stem.2007.08.014] [PMID: 18371393]
[22]
Pires BRB, De Amorim ÍSS, Souza LD, Rodrigues JA, Mencalha AL. Targeting cellular signaling pathways in breast cancer stem cells and its implication for cancer treatment. Anticancer Res 2016; 36(11): 5681-92.
[http://dx.doi.org/10.21873/anticanres.11151] [PMID: 27793889]
[23]
Yang L, Shi P, Zhao G, et al. Targeting cancer stem cell pathways for cancer therapy. Signal Transduct Target Ther 2020; 5(1): 8.
[http://dx.doi.org/10.1038/s41392-020-0110-5] [PMID: 32296030]
[24]
Piersma B, Bank RA, Boersema M. Signaling in fibrosis: TGF-β, WNT, and YAP/TAZ converge. Front Med 2015; 2: 59.
[http://dx.doi.org/10.3389/fmed.2015.00059] [PMID: 26389119]
[25]
Sun SG, Wu S, Zhang L. The discovery and expansion of Hippo signaling pathway in Drosophila model. Yi Chuan 2017; 39(7): 537-45.
[PMID: 28757469]
[26]
Yamauchi T, Moroishi T. Hippo pathway in mammalian adaptive immune system. Cells 2019; 8(5): 398.
[http://dx.doi.org/10.3390/cells8050398] [PMID: 31052239]
[27]
Watt KI, Harvey KF, Gregorevic P. Regulation of tissue growth by the mammalian Hippo signaling pathway. Front Physiol 2017; 8: 942.
[http://dx.doi.org/10.3389/fphys.2017.00942] [PMID: 29225579]
[28]
Yang Z, Hata Y. What is the Hippo pathway? Is the Hippo pathway conserved in Caenorhabditis elegans? J Biochem 2013; 154(3): 207-9.
[http://dx.doi.org/10.1093/jb/mvt060] [PMID: 23843471]
[29]
Yu FX, Zhao B, Guan KL. Hippo pathway in organ size control, tissue homeostasis, and cancer. Cell 2015; 163(4): 811-28.
[http://dx.doi.org/10.1016/j.cell.2015.10.044] [PMID: 26544935]
[30]
Yu FX, Mo JS, Guan KL. Upstream regulators of the Hippo pathway. Cell Cycle 2012; 11(22): 4097-8.
[http://dx.doi.org/10.4161/cc.22322] [PMID: 23075495]
[31]
Yu FX, Zhao B, Panupinthu N, et al. Regulation of the Hippo-YAP pathway by G-protein-coupled receptor signaling. Cell 2012; 150(4): 780-91.
[http://dx.doi.org/10.1016/j.cell.2012.06.037] [PMID: 22863277]
[32]
Cai H, Xu Y. The role of LPA and YAP signaling in long-term migration of human ovarian cancer cells. Cell Commun Signal 2013; 11(1): 31.
[http://dx.doi.org/10.1186/1478-811X-11-31] [PMID: 23618389]
[33]
Cheng JC, Wang EY, Yi Y, Thakur A, Tsai SH, Hoodless PA. S1P stimulates proliferation by upregulating CTGF Expression through S1PR2-Mediated YAP Activation. Mol Cancer Res 2018; 16(10): 1543-55.
[http://dx.doi.org/10.1158/1541-7786.MCR-17-0681] [PMID: 29903770]
[34]
Gong R, Hong AW, Plouffe SW, et al. Opposing roles of conventional and novel PKC isoforms in Hippo-YAP pathway regulation. Cell Res 2015; 25(8): 985-8.
[http://dx.doi.org/10.1038/cr.2015.88] [PMID: 26206313]
[35]
Striedinger K, VandenBerg SR, Baia GS, McDermott MW, Gutmann DH, Lal A. The neurofibromatosis 2 tumor suppressor gene product, merlin, regulates human meningioma cell growth by signaling through YAP. Neoplasia 2008; 10(11): 1204-12.
[http://dx.doi.org/10.1593/neo.08642] [PMID: 18953429]
[36]
Luo J, Yu FX. GPCR-Hippo signaling in cancer. Cells 2019; 8(5): 426.
[http://dx.doi.org/10.3390/cells8050426] [PMID: 31072060]
[37]
Galan JA, Avruch J. MST1/MST2 protein kinases: Regulation and physiologic roles. Biochemistry 2016; 55(39): 5507-19.
[http://dx.doi.org/10.1021/acs.biochem.6b00763] [PMID: 27618557]
[38]
Hong AW, Meng Z, Guan KL. The Hippo pathway in intestinal regeneration and disease. Nat Rev Gastroenterol Hepatol 2016; 13(6): 324-37.
[http://dx.doi.org/10.1038/nrgastro.2016.59] [PMID: 27147489]
[39]
Britschgi A, Duss S, Kim S, et al. The Hippo kinases LATS1 and 2 control human breast cell fate via crosstalk with ERα. Nature 2017; 541(7638): 541-5.
[http://dx.doi.org/10.1038/nature20829] [PMID: 28068668]
[40]
Cobbaut M, Karagil S, Bruno L, et al. Dysfunctional mechanotransduction through the YAP/TAZ/Hippo pathway as a feature of Chronic disease. Cells 2020; 9(1): 151.
[http://dx.doi.org/10.3390/cells9010151] [PMID: 31936297]
[41]
Piccolo S, Dupont S, Cordenonsi M. The biology of YAP/TAZ: Hippo signaling and beyond. Physiol Rev 2014; 94(4): 1287-312.
[http://dx.doi.org/10.1152/physrev.00005.2014] [PMID: 25287865]
[42]
Holden J, Cunningham C. Targeting the Hippo pathway and cancer through the tead family of transcription factors. Cancers 2018; 10(3): 81.
[http://dx.doi.org/10.3390/cancers10030081] [PMID: 29558384]
[43]
Hamaratoglu F, Willecke M, Kango-Singh M, et al. The tumour- suppressor genes NF2/Merlin and Expanded act through Hippo signalling to regulate cell proliferation and apoptosis. Nat Cell Biol 2006; 8(1): 27-36.
[http://dx.doi.org/10.1038/ncb1339] [PMID: 16341207]
[44]
Sansores-Garcia L, Bossuyt W, Wada KI, et al. Modulating F-actin organization induces organ growth by affecting the Hippo pathway. EMBO J 2011; 30(12): 2325-35.
[http://dx.doi.org/10.1038/emboj.2011.157] [PMID: 21556047]
[45]
Yousefi H, Delavar MR, Piroozian F, et al. Hippo signaling pathway: A comprehensive gene expression profile analysis in breast cancer. Biomed Pharmacother 2022; 151: 113144.
[http://dx.doi.org/10.1016/j.biopha.2022.113144] [PMID: 35623167]
[46]
Hiemer SE, Szymaniak AD, Varelas X. The transcriptional regulators TAZ and YAP direct transforming growth factor β-induced tumorigenic phenotypes in breast cancer cells. J Biol Chem 2014; 289(19): 13461-74.
[http://dx.doi.org/10.1074/jbc.M113.529115] [PMID: 24648515]
[47]
Li Y, Hibbs MA, Gard AL, Shylo NA, Yun K. Genome-wide analysis of N1ICD/RBPJ targets in vivo reveals direct transcriptional regulation of Wnt, SHH, and Hippo pathway effectors by Notch1. Stem Cells 2012; 30(4): 741-52.
[http://dx.doi.org/10.1002/stem.1030] [PMID: 22232070]
[48]
Kim W, Khan SK, Gvozdenovic-Jeremic J, et al. Hippo signaling interactions with Wnt/β-catenin and Notch signaling repress liver tumorigenesis. J Clin Invest 2016; 127(1): 137-52.
[http://dx.doi.org/10.1172/JCI88486] [PMID: 27869648]
[49]
Fernandez-L A, Northcott PA, Dalton J, et al. YAP1 is amplified and up-regulated in hedgehog-associated medulloblastomas and mediates Sonic hedgehog-driven neural precursor proliferation. Genes Dev 2009; 23(23): 2729-41.
[http://dx.doi.org/10.1101/gad.1824509] [PMID: 19952108]
[50]
Liu J, Li J, Chen H, et al. Metformin suppresses proliferation and invasion of drug-resistant breast cancer cells by activation of the Hippo pathway. J Cell Mol Med 2020; 24(10): 5786-96.
[http://dx.doi.org/10.1111/jcmm.15241] [PMID: 32281270]
[51]
Vališ K, Novák P. Targeting ERK-Hippo interplay in cancer therapy. Int J Mol Sci 2020; 21(9): 3236.
[http://dx.doi.org/10.3390/ijms21093236] [PMID: 32375238]
[52]
Miranda MZ, Bialik JF, Speight P, et al. TGF-β1 regulates the expression and transcriptional activity of TAZ protein via a Smad3-independent, myocardin-related transcription factor-mediated mechanism. J Biol Chem 2017; 292(36): 14902-20.
[http://dx.doi.org/10.1074/jbc.M117.780502] [PMID: 28739802]
[53]
Wang Y, Tu K, Liu D, et al. p300 acetyltransferase is a cytoplasm-to-nucleus shuttle for SMAD2/3 and TAZ nuclear transport in transforming growth factor β–stimulated hepatic stellate cells. Hepatology 2019; 70(4): 1409-23.
[http://dx.doi.org/10.1002/hep.30668] [PMID: 31004519]
[54]
Pefani DE, Pankova D, Abraham AG, et al. TGF-β targets the Hippo pathway scaffold RASSF1A to facilitate YAP/SMAD2 nuclear translocation. mol cell 2016; 63(1): 156-66.
[http://dx.doi.org/10.1016/j.molcel.2016.05.012] [PMID: 27292796]
[55]
Seo WI, Park S, Gwak J, et al. Wnt signaling promotes androgen-independent prostate cancer cell proliferation through up-regulation of the Hippo pathway effector YAP. Biochem Biophys Res Commun 2017; 486(4): 1034-9.
[http://dx.doi.org/10.1016/j.bbrc.2017.03.158] [PMID: 28366633]
[56]
Yang D, Zhang N, Li M, Hong T, Meng W, Ouyang T. The Hippo signaling pathway: The trader of tumor microenvironment. Front Oncol 2021; 11: 772134.
[http://dx.doi.org/10.3389/fonc.2021.772134] [PMID: 34858852]
[57]
Kim S, Jho E. Merlin, a regulator of Hippo signaling, regulates Wnt/β-catenin signaling. BMB Rep 2016; 49(7): 357-8.
[http://dx.doi.org/10.5483/BMBRep.2016.49.7.104] [PMID: 27345717]
[58]
Akladios B, Mendoza Reinoso V, Cain JE, et al. Positive regulatory interactions between YAP and Hedgehog signalling in skin homeostasis and BCC development in mouse skin in vivo. PLoS One 2017; 12(8): e0183178.
[http://dx.doi.org/10.1371/journal.pone.0183178] [PMID: 28820907]
[59]
Slemmons KK, Crose LES, Riedel S, Sushnitha M, Belyea B, Linardic CM. A Novel Notch–YAP circuit drives stemness and tumorigenesis in embryonal rhabdomyosarcoma. Mol Cancer Res 2017; 15(12): 1777-91.
[http://dx.doi.org/10.1158/1541-7786.MCR-17-0004] [PMID: 28923841]
[60]
Zhang X, Liu X, Luo J, et al. Notch3 inhibits epithelial–mesenchymal transition by activating Kibra-mediated Hippo/YAP signaling in breast cancer epithelial cells. Oncogenesis 2016; 5(11): e269.
[http://dx.doi.org/10.1038/oncsis.2016.67] [PMID: 27841855]
[61]
DeRan M, Yang J, Shen CH, et al. Energy stress regulates Hippo-YAP signaling involving AMPK-mediated regulation of angiomotin-like 1 protein. Cell Rep 2014; 9(2): 495-503.
[http://dx.doi.org/10.1016/j.celrep.2014.09.036] [PMID: 25373897]
[62]
Heng BC, Zhang X, Aubel D, et al. An overview of signaling pathways regulating YAP/TAZ activity. Cell Mol Life Sci 2021; 78(2): 497-512.
[http://dx.doi.org/10.1007/s00018-020-03579-8] [PMID: 32748155]
[63]
Guo S, Liu M, Gonzalez-Perez RR. Role of Notch and its oncogenic signaling crosstalk in breast cancer. Biochim Biophys Acta 2011; 1815(2): 197-213.
[PMID: 21193018]
[64]
Azzolin L, Panciera T, Soligo S, et al. YAP/TAZ incorporation in the β-catenin destruction complex orchestrates the Wnt response. Cell 2014; 158(1): 157-70.
[http://dx.doi.org/10.1016/j.cell.2014.06.013] [PMID: 24976009]
[65]
Meng Z, Moroishi T, Mottier-Pavie V, et al. MAP4K family kinases act in parallel to MST1/2 to activate LATS1/2 in the Hippo pathway. Nat Commun 2015; 6(1): 8357.
[http://dx.doi.org/10.1038/ncomms9357] [PMID: 26437443]
[66]
Ahmed AA, Mohamed AD, Gener M, Li W, Taboada E. YAP and the Hippo pathway in pediatric cancer. Mol Cell Oncol 2017; 4(3): e1295127.
[http://dx.doi.org/10.1080/23723556.2017.1295127] [PMID: 28616573]
[67]
Piccolo D, Crisman G, Schoinas S, Altamura D, Peris K. Computer-automated ABCD versus dermatologists with different degrees of experience in dermoscopy. Eur J Dermatol 2014; 24(4): 477-81.
[http://dx.doi.org/10.1684/ejd.2014.2320] [PMID: 24721784]
[68]
Yao CB, Zhou X, Chen CS, Lei QY. The regulatory mechanisms and functional roles of the Hippo signaling pathway in breast cancer. Yi Chuan 2017; 39(7): 617-29.
[PMID: 28757476]
[69]
Li YW, Shen H, Frangou C, et al. Characterization of TAZ domains important for the induction of breast cancer stem cell properties and tumorigenesis. Cell Cycle 2015; 14(1): 146-56.
[http://dx.doi.org/10.4161/15384101.2014.967106] [PMID: 25602524]
[70]
Overholtzer M, Zhang J, Smolen GA, et al. Transforming properties of YAP, a candidate oncogene on the chromosome 11q22 amplicon. Proc Natl Acad Sci 2006; 103(33): 12405-10.
[http://dx.doi.org/10.1073/pnas.0605579103] [PMID: 16894141]
[71]
Chan SW, Lim CJ, Guo K, et al. A role for TAZ in migration, invasion, and tumorigenesis of breast cancer cells. Cancer Res 2008; 68(8): 2592-8.
[http://dx.doi.org/10.1158/0008-5472.CAN-07-2696] [PMID: 18413727]
[72]
Cordenonsi M, Zanconato F, Azzolin L, et al. The Hippo transducer TAZ confers cancer stem cell-related traits on breast cancer cells. Cell 2011; 147(4): 759-72.
[http://dx.doi.org/10.1016/j.cell.2011.09.048] [PMID: 22078877]
[73]
Sun HL, Men JR, Liu HY, Liu MY, Zhang HS. FOXM1 facilitates breast cancer cell stemness and migration in YAP1-dependent manner. Arch Biochem Biophys 2020; 685: 108349.
[http://dx.doi.org/10.1016/j.abb.2020.108349] [PMID: 32209309]
[74]
Chan JKK, Yap LH. The anatomical basis of desensitisation in breast reconstruction: Comment on ‘Burn after breast reconstruction’ by Delfino S., et al. [Burns 34 (2008) 873–877]. Burns 2009; 35(7): 1050-2.
[http://dx.doi.org/10.1016/j.burns.2008.12.016] [PMID: 19477596]
[75]
Qin F, Tian J, Zhou D, Chen L. Mst1 and Mst2 kinases: Regulations and diseases. Cell Biosci 2013; 3(1): 31.
[http://dx.doi.org/10.1186/2045-3701-3-31] [PMID: 23985272]
[76]
Li X, Wang W, Wang J, et al. Proteomic analyses reveal distinct chromatin-associated and soluble transcription factor complexes. Mol Syst Biol 2015; 11(1): 775.
[http://dx.doi.org/10.15252/msb.20145504] [PMID: 25609649]
[77]
Huh H, Kim D, Jeong HS, Park H. Regulation of TEAD transcription factors in cancer biology. Cells 2019; 8(6): 600.
[http://dx.doi.org/10.3390/cells8060600] [PMID: 31212916]
[78]
Okusaka T, Ikeda M, Fukutomi A, et al. Response to Y. Sasaki et al.: Is repeating FOLFIRINOX in the original dosage and treatment schedule tolerable in Japanese patients with pancreatic cancer? Cancer Sci 2015; 106(8): 1101-2.
[http://dx.doi.org/10.1111/cas.12709] [PMID: 26268894]
[79]
Esteller M, Herman JG. Cancer as an epigenetic disease: DNA methylation and chromatin alterations in human tumours. J Pathol 2002; 196(1): 1-7.
[http://dx.doi.org/10.1002/path.1024] [PMID: 11748635]
[80]
Carlos-Reyes Á, López-González JS, Meneses-Flores M, et al. Dietary compounds as epigenetic modulating agents in cancer. Front Genet 2019; 10: 79.
[http://dx.doi.org/10.3389/fgene.2019.00079] [PMID: 30881375]
[81]
Liu CC, Lin JH, Hsu TW, et al. IL-6 enriched lung cancer stem- like cell population by inhibition of cell cycle regulators via DNMT1 upregulation. Int J Cancer 2015; 136(3): 547-59.
[http://dx.doi.org/10.1002/ijc.29033] [PMID: 24947242]
[82]
Morita R, Hirohashi Y, Suzuki H, et al. DNA methyltransferase 1 is essential for initiation of the colon cancers. Exp Mol Pathol 2013; 94(2): 322-9.
[http://dx.doi.org/10.1016/j.yexmp.2012.10.004] [PMID: 23064049]
[83]
Toh TB, Lim JJ, Chow EKH. Epigenetics in cancer stem cells. Mol Cancer 2017; 16(1): 29.
[http://dx.doi.org/10.1186/s12943-017-0596-9] [PMID: 28148257]
[84]
Wu Q, Li J, Sun S, et al. YAP/TAZ-mediated activation of serine metabolism and methylation regulation is critical for LKB1-deficient breast cancer progression. Biosci Rep 2017; 37(5): BSR20171072.
[http://dx.doi.org/10.1042/BSR20171072] [PMID: 28931725]
[85]
Bowman GD, Poirier MG. Post-translational modifications of histones that influence nucleosome dynamics. Chem Rev 2015; 115(6): 2274-95.
[http://dx.doi.org/10.1021/cr500350x] [PMID: 25424540]
[86]
Qing Y, Yin F, Wang W, et al. The Hippo effector Yorkie activates transcription by interacting with a histone methyltransferase complex through Ncoa6. eLife 2014; 3: e02564.
[http://dx.doi.org/10.7554/eLife.02564] [PMID: 25027438]
[87]
Oh H, Slattery M, Ma L, White KP, Mann RS, Irvine KD. Yorkie promotes transcription by recruiting a histone methyltransferase complex. Cell Rep 2014; 8(2): 449-59.
[http://dx.doi.org/10.1016/j.celrep.2014.06.017] [PMID: 25017066]
[88]
Hata S, Hirayama J, Kajiho H, et al. A novel acetylation cycle of transcription co-activator Yes-associated protein that is downstream of Hippo pathway is triggered in response to SN2 alkylating agents. J Biol Chem 2012; 287(26): 22089-98.
[http://dx.doi.org/10.1074/jbc.M111.334714] [PMID: 22544757]
[89]
Zhou D, Conrad C, Xia F, et al. Mst1 and Mst2 maintain hepatocyte quiescence and suppress hepatocellular carcinoma development through inactivation of the Yap1 oncogene. Cancer Cell 2009; 16(5): 425-38.
[http://dx.doi.org/10.1016/j.ccr.2009.09.026] [PMID: 19878874]
[90]
Bao Y, Nakagawa K, Yang Z, et al. A cell-based assay to screen stimulators of the Hippo pathway reveals the inhibitory effect of dobutamine on the YAP-dependent gene transcription. J Biochem 2011; 150(2): 199-208.
[http://dx.doi.org/10.1093/jb/mvr063] [PMID: 21586534]
[91]
Suh MR, Lee Y, Kim JY, et al. Human embryonic stem cells express a unique set of microRNAs. Dev Biol 2004; 270(2): 488-98.
[http://dx.doi.org/10.1016/j.ydbio.2004.02.019] [PMID: 15183728]
[92]
Houbaviy HB, Murray MF, Sharp PA. Embryonic stem cell-specific MicroRNAs. Dev Cell 2003; 5(2): 351-8.
[http://dx.doi.org/10.1016/S1534-5807(03)00227-2] [PMID: 12919684]
[93]
Yang X, Wang B, Chen W, Man X. MicroRNA-188 inhibits biological activity of lung cancer stem cells through targeting MDK and mediating the Hippo pathway. Exp Physiol 2020; 105(8): 1360-72.
[http://dx.doi.org/10.1113/EP088704] [PMID: 32592428]
[94]
Yoshida K, Yamamoto Y, Ochiya T. miRNA signaling networks in cancer stem cells. Regen Ther 2021; 17: 1-7.
[http://dx.doi.org/10.1016/j.reth.2021.01.004] [PMID: 33598508]
[95]
Yu F, Yao H, Zhu P, et al. let-7 regulates self renewal and tumorigenicity of breast cancer cells. Cell 2007; 131(6): 1109-23.
[http://dx.doi.org/10.1016/j.cell.2007.10.054] [PMID: 18083101]
[96]
Huang X, Tang F, Weng Z, Zhou M, Zhang Q. MiR-591 functions as tumor suppressor in breast cancer by targeting TCF4 and inhibits Hippo-YAP/TAZ signaling pathway. Cancer Cell Int 2019; 19(1): 108.
[http://dx.doi.org/10.1186/s12935-019-0818-x] [PMID: 31049030]
[97]
Du T, Wang D, Wan X, Xu J, Xiao Q, Liu B. Regulatory effect of microRNA-223-3p on breast cancer cell processes via the Hippo/Yap signaling pathway. Oncol Lett 2021; 22(1): 516.
[http://dx.doi.org/10.3892/ol.2021.12777] [PMID: 33986876]
[98]
Shi X, Zhu HR, Liu TT, Shen XZ, Zhu JM. The Hippo pathway in hepatocellular carcinoma: Non-coding RNAs in action. Cancer Lett 2017; 400: 175-82.
[http://dx.doi.org/10.1016/j.canlet.2017.04.032] [PMID: 28461246]
[99]
Liu X, Wang Y, Chen B, et al. Targeting the Hippo pathway in gastric cancer and other malignancies in the digestive system: From bench to bedside. Biomedicines 2022; 10(10): 2512.
[http://dx.doi.org/10.3390/biomedicines10102512] [PMID: 36289774]
[100]
Zygulska AL, Krzemieniecki K, Pierzchalski P. Hippo pathway - brief overview of its relevance in cancer. J Physiol Pharmacol 2017; 68(3): 311-35.
[PMID: 28820389]
[101]
Liu JY, Li YH, Lin HX, et al. Overexpression of YAP 1 contributes to progressive features and poor prognosis of human urothelial carcinoma of the bladder. BMC Cancer 2013; 13(1): 349.
[http://dx.doi.org/10.1186/1471-2407-13-349] [PMID: 23870412]
[102]
Wang Y, Dong Q, Zhang Q, Li Z, Wang E, Qiu X. Overexpression of yes-associated protein contributes to progression and poor prognosis of non-small-cell lung cancer. Cancer Sci 2010; 101(5): 1279-85.
[http://dx.doi.org/10.1111/j.1349-7006.2010.01511.x] [PMID: 20219076]
[103]
Jeong W, Kim SB, Sohn BH, et al. Activation of YAP1 is associated with poor prognosis and response to taxanes in ovarian cancer. Anticancer Res 2014; 34(2): 811-7.
[PMID: 24511017]
[104]
Song M, Cheong JH, Kim H, Noh SH, Kim H. Nuclear expression of Yes-associated protein 1 correlates with poor prognosis in intestinal type gastric cancer. Anticancer Res 2012; 32(9): 3827-34.
[PMID: 22993325]
[105]
Cha YJ, Bae SJ, Kim D, et al. High nuclear expression of yes-associated protein 1 correlates with metastasis in patients with breast cancer. Front Oncol 2021; 11: 609743.
[http://dx.doi.org/10.3389/fonc.2021.609743] [PMID: 33718163]
[106]
Wang Z, Kong Q, Su P, et al. Regulation of Hippo signaling and triple negative breast cancer progression by an ubiquitin ligase RNF187. Oncogenesis 2020; 9(3): 36.
[http://dx.doi.org/10.1038/s41389-020-0220-5] [PMID: 32198343]
[107]
Xu MZ, Yao TJ, Lee NPY, et al. Yes-associated protein is an independent prognostic marker in hepatocellular carcinoma. Cancer 2009; 115(19): 4576-85.
[http://dx.doi.org/10.1002/cncr.24495] [PMID: 19551889]
[108]
Salcedo Allende MT, Zeron-Medina J, Hernandez J, et al. Overexpression of yes associated protein 1, an independent prognostic marker in patients with pancreatic ductal adenocarcinoma, correlated with liver metastasis and poor prognosis. Pancreas 2017; 46(7): 913-20.
[http://dx.doi.org/10.1097/MPA.0000000000000867] [PMID: 28697132]
[109]
Poma AM, Torregrossa L, Bruno R, Basolo F, Fontanini G. Hippo pathway affects survival of cancer patients: extensive analysis of TCGA data and review of literature. Sci Rep 2018; 8(1): 10623.
[http://dx.doi.org/10.1038/s41598-018-28928-3] [PMID: 30006603]
[110]
Lin XY, Cai FF, Wang MH, et al. Mammalian sterile 20-like kinase 1 expression and its prognostic significance in patients with breast cancer. Oncol Lett 2017; 14(5): 5457-63.
[http://dx.doi.org/10.3892/ol.2017.6852] [PMID: 29098035]
[111]
Yu J, Zhai X, Li X, et al. Identification of MST1 as a potential early detection biomarker for colorectal cancer through a proteomic approach. Sci Rep 2017; 7(1): 14265.
[http://dx.doi.org/10.1038/s41598-017-14539-x] [PMID: 29079854]
[112]
Wei Z, Wang Y, Li Z, et al. Overexpression of Hippo pathway effector TAZ in tongue squamous cell carcinoma: Correlation with clinicopathological features and patients’ prognosis. J Oral Pathol Med 2013; 42(10): 747-54.
[http://dx.doi.org/10.1111/jop.12062] [PMID: 23551691]
[113]
Andl T, Zhou L, Yang K, Kadekaro AL, Zhang Y. YAP and WWTR1: New targets for skin cancer treatment. Cancer Lett 2017; 396: 30-41.
[http://dx.doi.org/10.1016/j.canlet.2017.03.001] [PMID: 28279717]
[114]
Darbankhales S, Mirfakhraie R, Ghahremani H, et al. Effects of quinacrine on expression of Hippo signaling pathway components (LATS1, LATS2, and YAP) in human breast cancer stem cells. Asian Pac J Cancer Prev 2020; 21(11): 3171-6.
[http://dx.doi.org/10.31557/APJCP.2020.21.11.3171] [PMID: 33247672]
[115]
Hou L, Chen L, Fang L. Scutellarin inhibits proliferation, invasion, and tumorigenicity in human breast cancer cells by regulating Hippo-YAP signaling pathway. Med Sci Monit 2017; 23: 5130-8.
[http://dx.doi.org/10.12659/MSM.904492] [PMID: 29079722]
[116]
Bartucci M, Dattilo R, Moriconi C, et al. TAZ is required for metastatic activity and chemoresistance of breast cancer stem cells. Oncogene 2015; 34(6): 681-90.
[http://dx.doi.org/10.1038/onc.2014.5] [PMID: 24531710]
[117]
Giovinazzi S, Lindsay CR, Morozov VM, et al. Regulation of mitosis and taxane response by Daxx and Rassf1. Oncogene 2012; 31(1): 13-26.
[http://dx.doi.org/10.1038/onc.2011.211] [PMID: 21643015]
[118]
Jin X, Zhu L, Xiao S, et al. MST1 inhibits the progression of breast cancer by regulating the Hippo signaling pathway and may serve as a prognostic biomarker. Mol Med Rep 2021; 23(5): 383.
[http://dx.doi.org/10.3892/mmr.2021.12022] [PMID: 33760220]
[119]
Li S, Zhang X, Zhang R, et al. Hippo pathway contributes to cisplatin resistant-induced EMT in nasopharyngeal carcinoma cells. Cell Cycle 2017; 16(17): 1601-10.
[http://dx.doi.org/10.1080/15384101.2017.1356508] [PMID: 28749195]
[120]
Tan S, Bian X, Wu B, Chen X. RASSF6 Is downregulated in human bladder cancers and regulates doxorubicin sensitivity and mitochondrial membrane potential via the Hippo signaling pathway. OncoTargets Ther 2019; 12: 9189-200.
[http://dx.doi.org/10.2147/OTT.S217041] [PMID: 31807003]
[121]
Lin CH, Pelissier FA, Zhang H, et al. Microenvironment rigidity modulates responses to the HER2 receptor tyrosine kinase inhibitor lapatinib via YAP and TAZ transcription factors. Mol Biol Cell 2015; 26(22): 3946-53.
[http://dx.doi.org/10.1091/mbc.E15-07-0456] [PMID: 26337386]
[122]
Liu-Chittenden Y, Huang B, Shim JS, et al. Genetic and pharmacological disruption of the TEAD–YAP complex suppresses the oncogenic activity of YAP. Genes Dev 2012; 26(12): 1300-5.
[http://dx.doi.org/10.1101/gad.192856.112] [PMID: 22677547]
[123]
Reik W, Dean W, Walter J. Epigenetic reprogramming in mammalian development. Science 2001; 293(5532): 1089-93.
[http://dx.doi.org/10.1126/science.1063443] [PMID: 11498579]
[124]
Hu Z, Rao B, Chen S, Duanmu J. Targeting tissue factor on tumour cells and angiogenic vascular endothelial cells by factor VII- targeted verteporfin photodynamic therapy for breast cancer in vitro and in vivo in mice. BMC Cancer 2010; 10(1): 235.
[http://dx.doi.org/10.1186/1471-2407-10-235] [PMID: 20504328]
[125]
Dasari VR, Carey DJ, Gogoi R. Synergistic enhancement of efficacy of platinum drugs with verteporfin in ovarian cancer cells. BMC Cancer 2020; 20(1): 273.
[http://dx.doi.org/10.1186/s12885-020-06752-1] [PMID: 32245422]
[126]
Yin J, Dong Q, Zheng M, et al. Antitumor activity of dobutamine on human osteosarcoma cells. Oncol Lett 2016; 11(6): 3676-80.
[http://dx.doi.org/10.3892/ol.2016.4479] [PMID: 27284371]
[127]
Messmer KJ, Abel SR. Verteporfin for age-related macular degeneration. Ann Pharmacother 2001; 35(12): 1593-8.
[http://dx.doi.org/10.1345/aph.10365] [PMID: 11793628]
[128]
Wei C, Li X. Verteporfin inhibits cell proliferation and induces apoptosis in different subtypes of breast cancer cell lines without light activation. BMC Cancer 2020; 20(1): 1042.
[http://dx.doi.org/10.1186/s12885-020-07555-0] [PMID: 33121449]
[129]
Brodowska K, Al-Moujahed A, Marmalidou A, et al. The clinically used photosensitizer Verteporfin (VP) inhibits YAP-TEAD and human retinoblastoma cell growth in vitro without light activation. Exp Eye Res 2014; 124: 67-73.
[http://dx.doi.org/10.1016/j.exer.2014.04.011] [PMID: 24837142]
[130]
Gibault F, Corvaisier M, Bailly F, Huet G, Melnyk P, Cotelle P. Non-photoinduced biological properties of verteporfin. Curr Med Chem 2016; 23(11): 1171-84.
[http://dx.doi.org/10.2174/0929867323666160316125048] [PMID: 26980565]
[131]
Calses PC, Crawford JJ, Lill JR, Dey A. Hippo pathway in cancer: Aberrant regulation and therapeutic opportunities. Trends Cancer 2019; 5(5): 297-307.
[http://dx.doi.org/10.1016/j.trecan.2019.04.001] [PMID: 31174842]
[132]
Bum-Erdene K, Zhou D, Gonzalez-Gutierrez G, et al. Small- molecule covalent modification of conserved cysteine leads to allosteric inhibition of the tead-yap protein-protein interaction. Cell Chem Biol 2019; 26(3): 378-389.e13.
[http://dx.doi.org/10.1016/j.chembiol.2018.11.010] [PMID: 30581134]
[133]
Madunić J, Madunić IV, Gajski G, Popić J, Garaj-Vrhovac V. Apigenin: A dietary flavonoid with diverse anticancer properties. Cancer Lett 2018; 413: 11-22.
[http://dx.doi.org/10.1016/j.canlet.2017.10.041] [PMID: 29097249]
[134]
Han Y. Analysis of the role of the Hippo pathway in cancer. J Transl Med 2019; 17(1): 116.
[http://dx.doi.org/10.1186/s12967-019-1869-4] [PMID: 30961610]
[135]
Li YW, Xu J, Zhu GY, et al. Apigenin suppresses the stem cell- like properties of triple-negative breast cancer cells by inhibiting YAP/TAZ activity. Cell Death Discov 2018; 4(1): 105.
[http://dx.doi.org/10.1038/s41420-018-0124-8] [PMID: 30479839]
[136]
Choi EJ, Kim GH. Apigenin causes G2/M arrest associated with the modulation of p21Cip1 and Cdc2 and activates p53-dependent apoptosis pathway in human breast cancer SK-BR-3 cells. J Nutr Biochem 2009; 20(4): 285-90.
[http://dx.doi.org/10.1016/j.jnutbio.2008.03.005] [PMID: 18656338]
[137]
Pobbati AV, Chan SW, Lee I, Song H, Hong W. Structural and functional similarity between the Vgll1-TEAD and the YAP-TEAD complexes. Structure 2012; 20(7): 1135-40.
[http://dx.doi.org/10.1016/j.str.2012.04.004] [PMID: 22632831]
[138]
Jiao S, Wang H, Shi Z, et al. A peptide mimicking VGLL4 function acts as a YAP antagonist therapy against gastric cancer. Cancer Cell 2014; 25(2): 166-80.
[http://dx.doi.org/10.1016/j.ccr.2014.01.010] [PMID: 24525233]
[139]
Panda AK, Chakraborty D, Sarkar I, Khan T, Sa G. New insights into therapeutic activity and anticancer properties of curcumin. J Exp Pharmacol 2017; 9: 31-45.
[http://dx.doi.org/10.2147/JEP.S70568] [PMID: 28435333]
[140]
Gao Y, Shi Q, Xu S, et al. Curcumin promotes KLF5 proteasome degradation through downregulating YAP/TAZ in bladder cancer cells. Int J Mol Sci 2014; 15(9): 15173-87.
[http://dx.doi.org/10.3390/ijms150915173] [PMID: 25170806]

Rights & Permissions Print Cite
Article Metrics
40
2
Wayfinder Image
Open Access Journals Promotions
World Antimicrobial Awareness Week
© 2024 Bentham Science Publishers | Privacy Policy