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Open Access 01-12-2021 | Breast Cancer | Review

Utilizing the Hippo pathway as a therapeutic target for combating endocrine-resistant breast cancer

Authors: Jing Chen, Runlan Wan, Qinqin Li, Zhenghuan Rao, Yanlin Wang, Lei Zhang, Alexander Tobias Teichmann

Published in: Cancer Cell International | Issue 1/2021

Abstract

Drug resistance is always a great obstacle in any endocrine therapy of breast cancer. Although the combination of endocrine therapy and targeted therapy has been shown to significantly improve prognosis, refractory endocrine resistance is still common. Dysregulation of the Hippo pathway is often related to the occurrence and the development of many tumors. Targeted therapies of this pathway have played important roles in the study of triple negative breast cancer (TNBC). Targeting the Hippo pathway in combination with chemotherapy or other targeted therapies has been shown to significantly improve specific antitumor effects and reduce cancer antidrug resistance. Further exploration has shown that the Hippo pathway is closely related to endocrine resistance, and it plays a “co-correlation point” role in numerous pathways involving endocrine resistance, including related pathways in breast cancer stem cells (BCSCs). Agents and miRNAs targeting the components of the Hippo pathway are expected to significantly enhance the sensitivity of breast cancer cells to endocrine therapy. This review initially explains the possible mechanism of the Hippo pathway in combating endocrine resistance, and it concludes by recommending endocrine therapy in combination with therapies targeting the Hippo pathway in the study of endocrine-resistant breast cancers.

Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, 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. https://doi.org/10.3322/caac.21492.CrossRefPubMed

Effects of chemotherapy and hormonal therapy for early breast cancer on recurrence and 15-year survival: an overview of the randomised trials. The Lancet. 2005;365(9472):1687–717. https://doi.org/10.1016/s0140-6736(05)66544-0.

Pennery E. The role of endocrine therapies in reducing risk of recurrence in postmenopausal women with hormone receptor-positive breast cancer. Eur J Oncol Nurs. 2008;12(3):233–43. https://doi.org/10.1016/j.ejon.2008.01.007.CrossRefPubMed

Giuliano M, Schettini F, Rognoni C, Milani M, Jerusalem G, Bachelot T, et al. Endocrine treatment versus chemotherapy in postmenopausal women with hormone receptor-positive, HER2-negative, metastatic breast cancer: a systematic review and network meta-analysis. Lancet Oncol. 2019;20(10):1360–9. https://doi.org/10.1016/S1470-2045(19)30420-6.CrossRefPubMed

Li Z, Razavi P, Li Q, Toy W, Liu B, Ping C, et al. Loss of the FAT1 tumor suppressor promotes resistance to CDK4/6 inhibitors via the Hippo pathway. Cancer Cell. 2018;34(6):893-905e8. https://doi.org/10.1016/j.ccell.2018.11.006.CrossRefPubMedPubMedCentral

Pancholi S, Ribas R, Simigdala N, Schuster E, Nikitorowicz-Buniak J, Ressa A, et al. Tumour kinome re-wiring governs resistance to palbociclib in oestrogen receptor positive breast cancers, highlighting new therapeutic modalities. Oncogene. 2020;39(25):4781–97. https://doi.org/10.1038/s41388-020-1284-6.CrossRefPubMedPubMedCentral

Baselga J, Campone M, Piccart M, Burris HA 3rd, Rugo HS, Sahmoud T, et al. Everolimus in postmenopausal hormone-receptor-positive advanced breast cancer. N Engl J Med. 2012;366(6):520–9. https://doi.org/10.1056/NEJMoa1109653.CrossRefPubMed

Park YH, Kim TY, Kim GM, Kang SY, Park IH, Kim JH, et al. Palbociclib plus exemestane with gonadotropin-releasing hormone agonist versus capecitabine in premenopausal women with hormone receptor-positive, HER2-negative metastatic breast cancer (KCSG-BR15-10): a multicentre, open-label, randomised, phase 2 trial. Lancet Oncol. 2019;20(12):1750–9. https://doi.org/10.1016/S1470-2045(19)30565-0.CrossRefPubMed

Hortobagyi GN, Stemmer SM, Burris HA, Yap YS, Sonke GS, Paluch-Shimon S, et al. Ribociclib as first-line therapy for HR-positive, advanced breast cancer. N Engl J Med. 2016;375(18):1738–48. https://doi.org/10.1056/NEJMoa1609709.CrossRefPubMed

10.

Johnston SRD, Harbeck N, Hegg R, Toi M, Martin M, Shao ZM, et al. Abemaciclib combined with endocrine therapy for the adjuvant treatment of HR+, HER2−, node-positive, high-risk, early breast cancer (monarchE). J Clin Oncol. 2020;38(34):3987–98. https://doi.org/10.1200/jco.20.02514.CrossRefPubMedPubMedCentral

11.

Andre F, Ciruelos E, Rubovszky G, Campone M, Loibl S, Rugo HS, et al. Alpelisib for PIK3CA-mutated, hormone receptor-positive advanced breast cancer. N Engl J Med. 2019;380(20):1929–40. https://doi.org/10.1056/NEJMoa1813904.CrossRefPubMed

12.

Piva M, Domenici G, Iriondo O, Rabano M, Simoes BM, Comaills V, et al. Sox2 promotes tamoxifen resistance in breast cancer cells. EMBO Mol Med. 2014;6(1):66–79. https://doi.org/10.1002/emmm.201303411.CrossRefPubMed

13.

Dubrovska A, Hartung A, Bouchez LC, Walker JR, Reddy VA, Cho CY, et al. CXCR4 activation maintains a stem cell population in tamoxifen-resistant breast cancer cells through AhR signalling. Br J Cancer. 2012;107(1):43–52. https://doi.org/10.1038/bjc.2012.105.CrossRefPubMedPubMedCentral

14.

Liu H, Zhang HW, Sun XF, Guo XH, He YN, Cui SD, et al. Tamoxifen-resistant breast cancer cells possess cancer stem-like cell properties. Chin Med J (Engl). 2013;126(16):3030–4. https://doi.org/10.3760/cma.j.issn.0366-6999.20130227.CrossRef

15.

El-Sheemy M, Hussain I, Rea C, Arif K. The role of Nanog expression in tamoxifen-resistant breast cancer cells. OncoTargets Ther. 2015;8:1327–34. https://doi.org/10.2147/ott.S67835.CrossRef

16.

Domenici G, Aurrekoetxea-Rodriguez I, Simoes BM, Rabano M, Lee SY, Millan JS, et al. A Sox2-Sox9 signalling axis maintains human breast luminal progenitor and breast cancer stem cells. Oncogene. 2019;38(17):3151–69. https://doi.org/10.1038/s41388-018-0656-7.CrossRefPubMedPubMedCentral

17.

Creighton CJ, Li X, Landis M, Dixon JM, Neumeister VM, Sjolund A, et al. Residual breast cancers after conventional therapy display mesenchymal as well as tumor-initiating features. Proc Nat Acad Sci. 2009;106(33):13820–5. https://doi.org/10.1073/pnas.0905718106.CrossRefPubMedPubMedCentral

18.

Simoes BM, O’Brien CS, Eyre R, Silva A, Yu L, Sarmiento-Castro A, et al. Anti-estrogen resistance in human breast tumors is driven by JAG1-NOTCH4-dependent cancer stem cell activity. Cell Rep. 2015;12(12):1968–77. https://doi.org/10.1016/j.celrep.2015.08.050.CrossRefPubMedPubMedCentral

19.

Sansone P, Ceccarelli C, Berishaj M, Chang Q, Rajasekhar VK, Perna F, et al. Self-renewal of CD133(hi) cells by IL6/Notch3 signalling regulates endocrine resistance in metastatic breast cancer. Nat Commun. 2016;7:10442. https://doi.org/10.1038/ncomms10442.CrossRefPubMedPubMedCentral

20.

Gelsomino L, Panza S, Giordano C, Barone I, Gu G, Spina E, et al. Mutations in the estrogen receptor alpha hormone binding domain promote stem cell phenotype through notch activation in breast cancer cell lines. Cancer Lett. 2018;428:12–20. https://doi.org/10.1016/j.canlet.2018.04.023.CrossRefPubMed

21.

Deng H, Zhang XT, Wang ML, Zheng HY, Liu LJ, Wang ZY. ER-alpha36-mediated rapid estrogen signaling positively regulates ER-positive breast cancer stem/progenitor cells. PLoS ONE. 2014;9(2):e88034. https://doi.org/10.1371/journal.pone.0088034.CrossRefPubMedPubMedCentral

22.

Ma R, Karthik GM, Lovrot J, Haglund F, Rosin G, Katchy A, et al. Estrogen receptor beta as a therapeutic target in breast cancer stem cells. J Natl Cancer Inst. 2017;109(3):1–14. https://doi.org/10.1093/jnci/djw236.CrossRefPubMed

23.

Chan YT, Lai AC, Lin RJ, Wang YH, Wang YT, Chang WW, et al. GPER-induced signaling is essential for the survival of breast cancer stem cells. Int J Cancer. 2020;146(6):1674–85. https://doi.org/10.1002/ijc.32588.CrossRefPubMed

24.

Eden JA. Human breast cancer stem cells and sex hormones. Menopause. 2010;17(4):801–10. https://doi.org/10.1097/gme.0b013e3181d3cdd7.CrossRefPubMed

25.

Shipitsin M, Campbell LL, Argani P, Weremowicz S, Bloushtain-Qimron N, Yao J, et al. Molecular definition of breast tumor heterogeneity. Cancer Cell. 2007;11(3):259–73. https://doi.org/10.1016/j.ccr.2007.01.013.CrossRefPubMed

26.

Liu S, Ginestier C, Charafe-Jauffret E, Foco H, Kleer CG, Merajver SD, et al. BRCA1 regulates human mammary stem/progenitor cell fate. Proc Natl Acad Sci USA. 2008;105(5):1680–5. https://doi.org/10.1073/pnas.0711613105.CrossRefPubMedPubMedCentral

27.

Buckley NE, Nic An tSaoir CB, Blayney JK, Oram LC, Crawford NT, D’Costa ZC, et al. BRCA1 is a key regulator of breast differentiation through activation of Notch signalling with implications for anti-endocrine treatment of breast cancers. Nucleic Acids Res. 2013;41(18):8601–14. https://doi.org/10.1093/nar/gkt626.CrossRefPubMedPubMedCentral

28.

Ojo D, Wei F, Liu Y, Wang E, Zhang H, Lin X, et al. Factors promoting tamoxifen resistance in breast cancer via stimulating breast cancer stem cell expansion. Curr Med Chem. 2015;22(19):2360–74. https://doi.org/10.2174/0929867322666150416095744.CrossRefPubMed

29.

Chen C, Baumann WT, Clarke R, Tyson JJ. Modeling the estrogen receptor to growth factor receptor signaling switch in human breast cancer cells. FEBS Lett. 2013;587(20):3327–34. https://doi.org/10.1016/j.febslet.2013.08.022.CrossRefPubMedPubMedCentral

30.

Massarweh S, Schiff R. Resistance to endocrine therapy in breast cancer: exploiting estrogen receptor/growth factor signaling crosstalk. Endocr Relat Cancer. 2006;13(Suppl 1):S15-24. https://doi.org/10.1677/erc.1.01273.CrossRefPubMed

31.

Martinez-Revollar G, Garay E, Martin-Tapia D, Nava P, Huerta M, Lopez-Bayghen E, et al. Heterogeneity between triple negative breast cancer cells due to differential activation of Wnt and PI3K/AKT pathways. Exp Cell Res. 2015;339(1):67–80. https://doi.org/10.1016/j.yexcr.2015.10.006.CrossRefPubMed

32.

Schlange T, Matsuda Y, Lienhard S, Huber A, Hynes NE. Autocrine WNT signaling contributes to breast cancer cell proliferation via the canonical WNT pathway and EGFR transactivation. Breast Cancer Res. 2007;9(5):R63. https://doi.org/10.1186/bcr1769.CrossRefPubMedPubMedCentral

33.

O’Brien CS, Howell SJ, Farnie G, Clarke RB. Resistance to endocrine therapy: are breast cancer stem cells the culprits? J Mam Gland Biol Neoplasia. 2009;14(1):45–54. https://doi.org/10.1007/s10911-009-9115-y.CrossRef

34.

Manupati K, Dhoke NR, Debnath T, Yeeravalli R, Guguloth K, Saeidpour S, et al. Inhibiting epidermal growth factor receptor signalling potentiates mesenchymal–epithelial transition of breast cancer stem cells and their responsiveness to anticancer drugs. Febs J. 2017;284(12):1830–54. https://doi.org/10.1111/febs.14084.CrossRefPubMed

35.

Roop RP, Ma CX. Endocrine resistance in breast cancer: molecular pathways and rational development of targeted therapies. Future Oncol. 2012;8(3):273–92. https://doi.org/10.2217/fon.12.8.CrossRefPubMed

36.

Johnston S, Basik M, Hegg R, Lausoontornsiri W, Grzeda L, Clemons M, et al. Inhibition of EGFR, HER2, and HER3 signaling with AZD8931 in combination with anastrozole as an anticancer approach: phase II randomized study in women with endocrine-therapy-naive advanced breast cancer. Breast Cancer Res Treat. 2016;160(1):91–9. https://doi.org/10.1007/s10549-016-3979-5.CrossRefPubMed

37.

Burstein HJ, Cirrincione CT, Barry WT, Chew HK, Tolaney SM, Lake DE, et al. Endocrine therapy with or without inhibition of epidermal growth factor receptor and human epidermal growth factor receptor 2: a randomized, double-blind, placebo-controlled phase III trial of fulvestrant with or without lapatinib for postmenopausal women with hormone receptor-positive advanced breast cancer-CALGB 40302 (Alliance). J Clin Oncol. 2014;32(35):3959–66. https://doi.org/10.1200/JCO.2014.56.7941.CrossRefPubMedPubMedCentral

38.

Smith IE, Walsh G, Skene A, Llombart A, Mayordomo JI, Detre S, et al. A phase II placebo-controlled trial of neoadjuvant anastrozole alone or with gefitinib in early breast cancer. J Clin Oncol. 2007;25(25):3816–22. https://doi.org/10.1200/JCO.2006.09.6578.CrossRefPubMed

39.

Green MD, Francis PA, Gebski V, Harvey V, Karapetis C, Chan A, et al. Gefitinib treatment in hormone-resistant and hormone receptor-negative advanced breast cancer. Ann Oncol. 2009;20(11):1813–7. https://doi.org/10.1093/annonc/mdp202.CrossRefPubMed

40.

Tryfonidis K, Basaran G, Bogaerts J, Debled M, Dirix L, Thery JC, et al. A European Organisation for Research and Treatment of Cancer randomized, double-blind, placebo-controlled, multicentre phase II trial of anastrozole in combination with gefitinib or placebo in hormone receptor-positive advanced breast cancer (NCT00066378). Eur J Cancer. 2016;53:144–54. https://doi.org/10.1016/j.ejca.2015.10.012.CrossRefPubMed

41.

Fukui F, Hayashi SI, Yamaguchi Y. Heregulin controls ERalpha and HER2 signaling in mammospheres of ERalpha-positive breast cancer cells and interferes with the efficacy of molecular targeted therapy. J Steroid Biochem Mol Biol. 2020;201:105698. https://doi.org/10.1016/j.jsbmb.2020.105698.CrossRefPubMed

42.

Hardt O, Wild S, Oerlecke I, Hofmann K, Luo S, Wiencek Y, et al. Highly sensitive profiling of CD44+/CD24− breast cancer stem cells by combining global mRNA amplification and next generation sequencing: evidence for a hyperactive PI3K pathway. Cancer Lett. 2012;325(2):165–74. https://doi.org/10.1016/j.canlet.2012.06.010.CrossRefPubMed

43.

Karthik GM, Ma R, Lövrot J, Kis LL, Lindh C, Blomquist L, et al. mTOR inhibitors counteract tamoxifen-induced activation of breast cancer stem cells. Cancer Lett. 2015;367(1):76–87. https://doi.org/10.1016/j.canlet.2015.07.017.CrossRefPubMed

44.

Lu PW, Li L, Wang F, Gu YT. Inhibitory role of large intergenic noncoding RNA-ROR on tamoxifen resistance in the endocrine therapy of breast cancer by regulating the PI3K/Akt/mTOR signaling pathway. J Cell Physiol. 2019;234(2):1904–12. https://doi.org/10.1002/jcp.27066.CrossRefPubMed

45.

Beelen K, Hoefnagel LD, Opdam M, Wesseling J, Sanders J, Vincent AD, et al. PI3K/AKT/mTOR pathway activation in primary and corresponding metastatic breast tumors after adjuvant endocrine therapy. Int J Cancer. 2014;135(5):1257–63. https://doi.org/10.1002/ijc.28769.CrossRefPubMedPubMedCentral

46.

Yin L, Zhang XT, Bian XW, Guo YM, Wang ZY. Disruption of the ER-α36-EGFR/HER2 positive regulatory loops restores tamoxifen sensitivity in tamoxifen resistance breast cancer cells. PLoS ONE. 2014;9(9):e107369. https://doi.org/10.1371/journal.pone.0107369.CrossRefPubMedPubMedCentral

47.

Deng H, Zhang XT, Wang ML, Zheng HY, Liu LJ, Wang ZY. ER-α36-mediated rapid estrogen signaling positively regulates ER-positive breast cancer stem/progenitor cells. PLoS ONE. 2014;9(2):e88034. https://doi.org/10.1371/journal.pone.0088034.CrossRefPubMedPubMedCentral

48.

Kang L, Guo Y, Zhang X, Meng J, Wang ZY. A positive cross-regulation of HER2 and ER-α36 controls ALDH1 positive breast cancer cells. J Steroid Biochem Mol Biol. 2011;127(3–5):262–8. https://doi.org/10.1016/j.jsbmb.2011.08.011.CrossRefPubMedPubMedCentral

49.

Zhao L, Qiu T, Jiang D, Xu H, Zou L, Yang Q, et al. SGCE promotes breast cancer stem cells by stabilizing EGFR. Adv Sci (Weinh). 2020;7(14):1903700. https://doi.org/10.1002/advs.201903700.CrossRefPubMedPubMedCentral

50.

Arpino G, Green SJ, Allred DC, Lew D, Martino S, Osborne CK, et al. HER-2 amplification, HER-1 expression, and tamoxifen response in estrogen receptor-positive metastatic breast cancer: a southwest oncology group study. Clin Cancer Res. 2004;10(17):5670–6. https://doi.org/10.1158/1078-0432.Ccr-04-0110.CrossRefPubMed

51.

Jeong Y, Bae SY, You D, Jung SP, Choi HJ, Kim I, et al. EGFR is a therapeutic target in hormone receptor-positive breast cancer. Cell Physiol Biochem. 2019;53(5):805–19. https://doi.org/10.33594/000000174.CrossRefPubMed

52.

Berardi DE, Raffo D, Todaro LB, Simian M. Laminin modulates the stem cell population in LM05-E murine breast cancer cells through the activation of the MAPK/ERK pathway. Cancer Res Treat. 2017;49(4):869–79. https://doi.org/10.4143/crt.2016.378.CrossRefPubMed

53.

Xu C, Sun X, Qin S, Wang H, Zheng Z, Xu S, et al. Let-7a regulates mammosphere formation capacity through Ras/NF-κB and Ras/MAPK/ERK pathway in breast cancer stem cells. Cell Cycle. 2015;14(11):1686–97. https://doi.org/10.1080/15384101.2015.1030547.CrossRefPubMedPubMedCentral

54.

Xu M, Ren Z, Wang X, Comer A, Frank JA, Ke ZJ, et al. ErbB2 and p38γ MAPK mediate alcohol-induced increase in breast cancer stem cells and metastasis. Mol Cancer. 2016;15(1):52. https://doi.org/10.1186/s12943-016-0532-4.CrossRefPubMedPubMedCentral

55.

Rhodes LV, Short SP, Neel NF, Salvo VA, Zhu Y, Elliott S, et al. Cytokine receptor CXCR4 mediates estrogen-independent tumorigenesis, metastasis, and resistance to endocrine therapy in human breast cancer. Cancer Res. 2011;71(2):603–13. https://doi.org/10.1158/0008-5472.CAN-10-3185.CrossRefPubMed

56.

Jia Y, Zhou J, Luo X, Chen M, Chen Y, Wang J, et al. KLF4 overcomes tamoxifen resistance by suppressing MAPK signaling pathway and predicts good prognosis in breast cancer. Cell Signal. 2018;42:165–75. https://doi.org/10.1016/j.cellsig.2017.09.025.CrossRefPubMed

57.

Sakunrangsit N, Ketchart W. Plumbagin inhibits cancer stem-like cells, angiogenesis and suppresses cell proliferation and invasion by targeting Wnt/beta-catenin pathway in endocrine resistant breast cancer. Pharmacol Res. 2019;150:104517. https://doi.org/10.1016/j.phrs.2019.104517.CrossRefPubMed

58.

Fu Y, Wang Z, Luo C, Wang Y, Wang Y, Zhong X, et al. Downregulation of CXXC finger protein 4 leads to a tamoxifen-resistant phenotype in breast cancer cells through activation of the Wnt/beta-catenin pathway. Transl Oncol. 2020;13(2):423–40. https://doi.org/10.1016/j.tranon.2019.12.005.CrossRefPubMedPubMedCentral

59.

Zheng W, Duan B, Zhang Q, Ouyang L, Peng W, Qian F, et al. Vitamin D-induced vitamin D receptor expression induces tamoxifen sensitivity in MCF-7 stem cells via suppression of Wnt/beta-catenin signaling. Biosci Rep. 2018;38(6). 10.1042/BSR20180595.

60.

Zhou M, Hou Y, Yang G, Zhang H, Tu G, Du YE, et al. LncRNA-Hh strengthen cancer stem cells generation in twist-positive breast cancer via activation of hedgehog signaling pathway. Stem Cells. 2016;34(1):55–66. https://doi.org/10.1002/stem.2219.CrossRefPubMed

61.

Ramaswamy B, Lu Y, Teng Ky, Nuovo G, Li X, Shapiro CL, et al. Hedgehog signaling is a novel therapeutic target in tamoxifen-resistant breast cancer aberrantly activated by PI3K/AKT pathway. Cancer Res. 2012;72(19):5048–59. https://doi.org/10.1158/0008-5472.Can-12-1248.CrossRefPubMed

62.

Bhateja P, Cherian M, Majumder S, Ramaswamy B. The Hedgehog signaling pathway: a viable target in breast cancer? Cancers (Basel). 2019;11(8):1126. https://doi.org/10.3390/cancers11081126.CrossRefPubMedCentral

63.

Sansone P, Berishaj M, Rajasekhar VK, Ceccarelli C, Chang Q, Strillacci A, et al. Evolution of cancer stem-like cells in endocrine-resistant metastatic breast cancers is mediated by stromal microvesicles. Cancer Res. 2017;77(8):1927–41. https://doi.org/10.1158/0008-5472.CAN-16-2129.CrossRefPubMedPubMedCentral

64.

Lombardo Y, Faronato M, Filipovic A, Vircillo V, Magnani L, Coombes RC. Nicastrin and Notch4 drive endocrine therapy resistance and epithelial to mesenchymal transition in MCF7 breast cancer cells. Breast Cancer Res. 2014;16(3):R62. https://doi.org/10.1186/bcr3675.CrossRefPubMedPubMedCentral

65.

Wang Y, Yu Y, Tsuyada A, Ren X, Wu X, Stubblefield K, et al. Transforming growth factor-β regulates the sphere-initiating stem cell-like feature in breast cancer through miRNA-181 and ATM. Oncogene. 2011;30(12):1470–80. https://doi.org/10.1038/onc.2010.531.CrossRefPubMed

66.

Nie Z, Wang C, Zhou Z, Chen C, Liu R, Wang D. Transforming growth factor-beta increases breast cancer stem cell population partially through upregulating PMEPA1 expression. Acta Biochim Biophys Sin (Shanghai). 2016;48(2):194–201. https://doi.org/10.1093/abbs/gmv130.CrossRef

67.

Zavadova E, Vocka M, Spacek J, Konopasek B, Fucikova T, Petruzelka L. Cellular and humoral immunodeficiency in breast cancer patients resistant to hormone therapy. Neoplasma. 2014;61(01):90–8. https://doi.org/10.4149/neo_2014_013.CrossRefPubMed

68.

Sieuwerts AM, Inda MA, Smid M, van Ooijen H, van de Stolpe A, Martens JWM, et al. ER and PI3K pathway activity in primary ER positive breast cancer is associated with progression-free survival of metastatic patients under first-line tamoxifen. Cancers (Basel). 2020;12(4):802. https://doi.org/10.3390/cancers12040802.CrossRef

69.

Knabbe C, Lippman ME, Wakefield LM, Flanders KC, Kasid A, Derynck R, et al. Evidence that transforming growth factor-beta is a hormonally regulated negative growth factor in human breast cancer cells. Cell. 1987;48(3):417–28. https://doi.org/10.1016/0092-8674(87)90193-0.CrossRefPubMed

70.

Camargo FD, Gokhale S, Johnnidis JB, Fu D, Bell GW, Jaenisch R, et al. YAP1 increases organ size and expands undifferentiated progenitor cells. Curr Biol. 2007;17(23):2054–60. https://doi.org/10.1016/j.cub.2007.10.039.CrossRefPubMed

71.

Thompson BJ. YAP/TAZ: drivers of tumor growth, metastasis, and resistance to therapy. BioEssays. 2020;42(5):e1900162. https://doi.org/10.1002/bies.201900162.CrossRefPubMed

72.

Zanconato F, Cordenonsi M, Piccolo S. YAP/TAZ at the roots of cancer. Cancer Cell. 2016;29(6):783–803. https://doi.org/10.1016/j.ccell.2016.05.005.CrossRefPubMedPubMedCentral

73.

Song H, Mak KK, Topol L, Yun K, Hu J, Garrett L, et al. Mammalian Mst1 and Mst2 kinases play essential roles in organ size control and tumor suppression. Proc Natl Acad Sci USA. 2010;107(4):1431–6. https://doi.org/10.1073/pnas.0911409107.CrossRefPubMedPubMedCentral

74.

Hao Y, Chun A, Cheung K, Rashidi B, Yang X. Tumor suppressor LATS1 is a negative regulator of oncogene YAP. J Biol Chem. 2008;283(9):5496–509. https://doi.org/10.1074/jbc.M709037200.CrossRefPubMed

75.

Yang X, Li DM, Chen W, Xu T. Human homologue of Drosophila lats, LATS1, negatively regulate growth by inducing G(2)/M arrest or apoptosis. Oncogene. 2001;20(45):6516–23. https://doi.org/10.1038/sj.onc.1204817.CrossRefPubMed

76.

Ke H, Pei J, Ni Z, Xia H, Qi H, Woods T, et al. Putative tumor suppressor Lats2 induces apoptosis through downregulation of Bcl-2 and Bcl-x(L). Exp Cell Res. 2004;298(2):329–38. https://doi.org/10.1016/j.yexcr.2004.04.031.CrossRefPubMed

77.

Stewart RA, Li DM, Huang H, Xu T. A genetic screen for modifiers of the lats tumor suppressor gene identifies C-terminal Src kinase as a regulator of cell proliferation in Drosophila. Oncogene. 2003;22(41):6436–44. https://doi.org/10.1038/sj.onc.1206820.CrossRefPubMed

78.

Bao Y, Nakagawa K, Yang Z, Ikeda M, Withanage K, Ishigami-Yuasa M, 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. https://doi.org/10.1093/jb/mvr063.CrossRefPubMed

79.

Zhao W, Wang M, Cai M, Zhang C, Qiu Y, Wang X, et al. Transcriptional co-activators YAP/TAZ: potential therapeutic targets for metastatic breast cancer. Biomed Pharmacother. 2021;133:110956. https://doi.org/10.1016/j.biopha.2020.110956.CrossRefPubMed

80.

Kim E, Kang JG, Kang MJ, Park JH, Kim YJ, Kweon TH, et al. O-GlcNAcylation on LATS2 disrupts the Hippo pathway by inhibiting its activity. Proc Natl Acad Sci USA. 2020;117(25):14259–69. https://doi.org/10.1073/pnas.1913469117.CrossRefPubMedPubMedCentral

81.

Raghunathan VK, Dreier B, Morgan JT, Tuyen BC, Rose BW, Reilly CM, et al. Involvement of YAP, TAZ and HSP90 in contact guidance and intercellular junction formation in corneal epithelial cells. PLoS ONE. 2014;9(10):e109811. https://doi.org/10.1371/journal.pone.0109811.CrossRefPubMedPubMedCentral

82.

Gill MK, Christova T, Zhang YY, Gregorieff A, Zhang L, Narimatsu M, et al. A feed forward loop enforces YAP/TAZ signaling during tumorigenesis. Nat Commun. 2018;9(1):3510. https://doi.org/10.1038/s41467-018-05939-2.CrossRefPubMedPubMedCentral

83.

Zhou D, Zhang Y, Wu H, Barry E, Yin Y, Lawrence E, et al. Mst1 and Mst2 protein kinases restrain intestinal stem cell proliferation and colonic tumorigenesis by inhibition of Yes-associated protein (Yap) overabundance. Proc Natl Acad Sci USA. 2011;108(49):E1312–20. https://doi.org/10.1073/pnas.1110428108.CrossRefPubMedPubMedCentral

84.

Ma Y, Yang Y, Wang F, Wei Q, Qin H. Hippo-YAP signaling pathway: a new paradigm for cancer therapy. Int J Cancer. 2015;137(10):2275–86. https://doi.org/10.1002/ijc.29073.CrossRefPubMed

85.

Clara JA, Monge C, Yang Y, Takebe N. Targeting signalling pathways and the immune microenvironment of cancer stem cells—a clinical update. Nat Rev Clin Oncol. 2020;17(4):204–32. https://doi.org/10.1038/s41571-019-0293-2.CrossRefPubMed

86.

Fallahi E, O’Driscoll NA, Matallanas D. The MST/Hippo pathway and cell death: a non-canonical affair. Genes (Basel). 2016;7(6):28. https://doi.org/10.3390/genes7060028.CrossRefPubMedCentral

87.

Azad T, Janse van Rensburg HJ, Lightbody ED, Neveu B, Champagne A, Ghaffari A, et al. A LATS biosensor screen identifies VEGFR as a regulator of the Hippo pathway in angiogenesis. Nat Commun. 2018;9(1):1061. https://doi.org/10.1038/s41467-018-03278-w.CrossRefPubMedPubMedCentral

88.

Cordenonsi M, Zanconato F, Azzolin L, Forcato M, Rosato A, Frasson C, et al. The Hippo transducer TAZ confers cancer stem cell-related traits on breast cancer cells. Cell. 2011;147(4):759–72. https://doi.org/10.1016/j.cell.2011.09.048.CrossRefPubMed

89.

Duss S, Britschgi A, Bentires-Alj M. Hippo inactivation feeds tumor-initiating cells. Breast Cancer Res. 2012;14(4):318. https://doi.org/10.1186/bcr3190.CrossRefPubMedPubMedCentral

90.

Liu J, Li J, Li P, Jiang Y, Chen H, Wang R, et al. DLG5 suppresses breast cancer stem cell-like characteristics to restore tamoxifen sensitivity by inhibiting TAZ expression. J Cell Mol Med. 2019;23(1):512–21. https://doi.org/10.1111/jcmm.13954.CrossRefPubMed

91.

Chang C, Goel HL, Gao H, Pursell B, Shultz LD, Greiner DL, et al. A laminin 511 matrix is regulated by TAZ and functions as the ligand for the alpha6Bbeta1 integrin to sustain breast cancer stem cells. Genes Dev. 2015;29(1):1–6. https://doi.org/10.1101/gad.253682.114.CrossRefPubMedPubMedCentral

92.

Bartucci M, Dattilo R, Moriconi C, Pagliuca A, Mottolese M, Federici G, et al. TAZ is required for metastatic activity and chemoresistance of breast cancer stem cells. Oncogene. 2015;34(6):681–90. https://doi.org/10.1038/onc.2014.5.CrossRefPubMed

93.

Li YW, Shen H, Frangou C, Yang N, Guo J, Xu B, 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. https://doi.org/10.4161/15384101.2014.967106.CrossRefPubMedPubMedCentral

94.

Zhang H, Lang TY, Zou DL, Zhou L, Lou M, Liu JS, et al. miR-520b promotes breast cancer stemness through Hippo/YAP signaling pathway. Onco Targets Ther. 2019;12:11691–700. https://doi.org/10.2147/OTT.S236607.CrossRefPubMedPubMedCentral

95.

Kim T, Yang SJ, Hwang D, Song J, Kim M, Kyum Kim S, et al. A basal-like breast cancer-specific role for SRF-IL6 in YAP-induced cancer stemness. Nat Commun. 2015;6:10186. https://doi.org/10.1038/ncomms10186.CrossRefPubMed

96.

Sorrentino G, Ruggeri N, Zannini A, Ingallina E, Bertolio R, Marotta C, et al. Glucocorticoid receptor signalling activates YAP in breast cancer. Nat Commun. 2017;8:14073. https://doi.org/10.1038/ncomms14073.CrossRefPubMedPubMedCentral

97.

Yang CE, Lee WY, Cheng HW, Chung CH, Mi FL, Lin CW. The antipsychotic chlorpromazine suppresses YAP signaling, stemness properties, and drug resistance in breast cancer cells. Chem Biol Interact. 2019;302:28–35. https://doi.org/10.1016/j.cbi.2019.01.033.CrossRefPubMed

98.

Britschgi A, Duss S, Kim S, Couto JP, Brinkhaus H, Koren S, et al. The Hippo kinases LATS1 and 2 control human breast cell fate via crosstalk with ERalpha. Nature. 2017;541(7638):541–5. https://doi.org/10.1038/nature20829.CrossRefPubMedPubMedCentral

99.

He L, Yuan L, Sun Y, Wang P, Zhang H, Feng X, et al. Glucocorticoid receptor signaling activates TEAD4 to promote breast cancer progression. Cancer Res. 2019;79(17):4399–411. https://doi.org/10.1158/0008-5472.Can-19-0012.CrossRefPubMed

100.

Wang Y, Liu J, Ying X, Lin PC, Zhou BP. Twist-mediated epithelial–mesenchymal transition promotes breast tumor cell invasion via inhibition of hippo pathway. Sci Rep. 2016;6:24606. https://doi.org/10.1038/srep24606.CrossRefPubMedPubMedCentral

101.

Zhu C, Li L, Zhang Z, Bi M, Wang H, Su W, et al. A Non-canonical role of YAP/TEAD is required for activation of estrogen-regulated enhancers in breast cancer. Mol Cell. 2019;75(4):791-806e8. https://doi.org/10.1016/j.molcel.2019.06.010.CrossRefPubMedPubMedCentral

102.

Rosswag S, Thiede G, Sleeman JP, Thaler S. RASSF1A suppresses estrogen-dependent breast cancer cell growth through inhibition of the yes-associated protein 1 (YAP1), inhibition of the forkhead box protein M1 (FOXM1), and activation of forkhead box transcription factor 3A (FOXO3A). Cancers (Basel). 2020;12(9):2689. https://doi.org/10.3390/cancers12092689.CrossRefPubMedCentral

103.

Zhou X, Wang S, Wang Z, Feng X, Liu P, Lv XB, et al. Estrogen regulates Hippo signaling via GPER in breast cancer. J Clin Invest. 2015;125(5):2123–35. https://doi.org/10.1172/JCI79573.CrossRefPubMedPubMedCentral

104.

Xu S, Zhu L, Liu Y, Wang X, Zhong Y, Su Y, et al. MPP, inhibitor of estrogen receptor α, affects YAP nuclear localization during mouse blastocyst formation and in Trophoblast Stem Cells. Chin J Histochem Cytochem. 2019;28(01):6–13. https://doi.org/10.16705/j.cnki.1004-1850.2019.01.002.CrossRef

105.

Chen W, Bai Y, Patel C, Geng F. Autophagy promotes triple negative breast cancer metastasis via YAP nuclear localization. Biochem Biophys Res Commun. 2019;520(2):263–8. https://doi.org/10.1016/j.bbrc.2019.09.133.CrossRefPubMed

106.

Feng X, Zhang M, Wang B, Zhou C, Mu Y, Li J, et al. CRABP2 regulates invasion and metastasis of breast cancer through hippo pathway dependent on ER status. J Exp Clin Cancer Res. 2019;38(1). https://doi.org/10.1186/s13046-019-1345-2.

107.

Tufail R, Jorda M, Zhao W, Reis I, Nawaz Z. Loss of Yes-associated protein (YAP) expression is associated with estrogen and progesterone receptors negativity in invasive breast carcinomas. Breast Cancer Res Treat. 2012;131(3):743–50. https://doi.org/10.1007/s10549-011-1435-0.CrossRefPubMed

108.

Zheng X, Han H, Liu GP, Ma YX, Pan RL, Sang LJ, et al. LncRNA wires up Hippo and Hedgehog signaling to reprogramme glucose metabolism. EMBO J. 2017;36(22):3325–35. https://doi.org/10.15252/embj.201797609.CrossRefPubMedPubMedCentral

109.

Li J, Feng X, Li C, Liu J, Li P, Wang R, et al. Downregulation of WW domain-containing oxidoreductase leads to tamoxifen-resistance by the inactivation of Hippo signaling. Exp Biol Med (Maywood). 2019;244(12):972–82. https://doi.org/10.1177/1535370219854678.CrossRef

110.

Wu X, Zhang X, Yu L, Zhang C, Ye L, Ren D, et al. Zinc finger protein 367 promotes metastasis by inhibiting the Hippo pathway in breast cancer. Oncogene. 2020;39(12):2568–82. https://doi.org/10.1038/s41388-020-1166-y.CrossRefPubMed

111.

Li L, Liu T, Li Y, Wu C, Luo K, Yin Y, et al. The deubiquitinase USP9X promotes tumor cell survival and confers chemoresistance through YAP1 stabilization. Oncogene. 2018;37(18):2422–31. https://doi.org/10.1038/s41388-018-0134-2.CrossRefPubMedPubMedCentral

112.

Dethlefsen C, Hansen LS, Lillelund C, Andersen C, Gehl J, Christensen JF, et al. Exercise-induced catecholamines activate the Hippo tumor suppressor pathway to reduce risks of breast cancer development. Cancer Res. 2017;77(18):4894–904. https://doi.org/10.1158/0008-5472.Can-16-3125.CrossRefPubMed

113.

Lehmann W, Mossmann D, Kleemann J, Mock K, Meisinger C, Brummer T, et al. ZEB1 turns into a transcriptional activator by interacting with YAP1 in aggressive cancer types. Nat Commun. 2016;7:10498. https://doi.org/10.1038/ncomms10498.CrossRefPubMedPubMedCentral

114.

Zheng L, Xiang C, Li X, Guo Q, Gao L, Ni H, et al. STARD13-correlated ceRNA network-directed inhibition on YAP/TAZ activity suppresses stemness of breast cancer via co-regulating Hippo and Rho-GTPase/F-actin signaling. J Hematol Oncol. 2018;11(1):72. https://doi.org/10.1186/s13045-018-0613-5.CrossRefPubMedPubMedCentral

115.

Zhu Q, Li J, Wu Q, Cheng Y, Zheng H, Zhan T, et al. Linc-OIP5 in the breast cancer cells regulates angiogenesis of human umbilical vein endothelial cells through YAP1/Notch/NRP1 signaling circuit at a tumor microenvironment. Biol Res. 2020;53(1):5. https://doi.org/10.1186/s40659-020-0273-0.CrossRefPubMedPubMedCentral

116.

Samanta S, Guru S, Elaimy AL, Amante JJ, Ou J, Yu J, et al. IMP3 stabilization of WNT5B mRNA facilitates TAZ activation in breast cancer. Cell Rep. 2018;23(9):2559–67. https://doi.org/10.1016/j.celrep.2018.04.113.CrossRefPubMedPubMedCentral

117.

Alam M, Bouillez A, Tagde A, Ahmad R, Rajabi H, Maeda T, et al. MUC1-C represses the crumbs complex polarity factor CRB3 and downregulates the Hippo pathway. Mol Cancer Res. 2016;14(12):1266–76. https://doi.org/10.1158/1541-7786.Mcr-16-0233.CrossRefPubMedPubMedCentral

118.

Lim SK, Lu SY, Kang SA, Tan HJ, Li Z, Adrian Wee ZN, et al. Wnt signaling promotes breast cancer by blocking ITCH-mediated degradation of YAP/TAZ transcriptional coactivator WBP2. Cancer Res. 2016;76(21):6278–89. https://doi.org/10.1158/0008-5472.CAN-15-3537.CrossRefPubMed

119.

Song H, Wu T, Xie D, Li D, Hua K, Hu J, et al. WBP2 downregulation inhibits proliferation by blocking YAP transcription and the EGFR/PI3K/Akt signaling pathway in triple negative breast cancer. Cell Physiol Biochem. 2018;48(5):1968–82. https://doi.org/10.1159/000492520.CrossRefPubMed

120.

Zhao Y, Montminy T, Azad T, Lightbody E, Hao Y, SenGupta S, et al. PI3K positively regulates YAP and TAZ in mammary tumorigenesis through multiple signaling pathways. Mol Cancer Res. 2018;16(6):1046–58. https://doi.org/10.1158/1541-7786.MCR-17-0593.CrossRefPubMed

121.

Yu S, Zhang M, Huang L, Ma Z, Gong X, Liu W, et al. ERK1 indicates good prognosis and inhibits breast cancer progression by suppressing YAP1 signaling. Aging (Albany NY). 2019;11(24):12295–314. https://doi.org/10.18632/aging.102572.CrossRefPubMedPubMedCentral

122.

Zhu Q, Le Scolan E, Jahchan N, Ji X, Xu A, Luo K. SnoN antagonizes the Hippo kinase complex to promote TAZ signaling during breast carcinogenesis. Dev Cell. 2016;37(5):399–412. https://doi.org/10.1016/j.devcel.2016.05.002.CrossRefPubMedPubMedCentral

123.

Ma B, Cheng H, Gao R, Mu C, Chen L, Wu S, et al. Zyxin-Siah2-Lats2 axis mediates cooperation between Hippo and TGF-beta signalling pathways. Nat Commun. 2016;7:11123. https://doi.org/10.1038/ncomms11123.CrossRefPubMedPubMedCentral

124.

Mota MSV, Jackson WP, Bailey SK, Vayalil P, Landar A, Rostas JW, et al. Deficiency of tumor suppressor Merlin facilitates metabolic adaptation by co-operative engagement of SMAD-Hippo signaling in breast cancer. Carcinogenesis. 2018;39(9):1165–75. https://doi.org/10.1093/carcin/bgy078.CrossRefPubMedPubMedCentral

125.

Rashidian J, Le Scolan E, Ji X, Zhu Q, Mulvihill MM, Nomura D, et al. Ski regulates Hippo and TAZ signaling to suppress breast cancer progression. Sci Signal. 2015;8(363):ra14. https://doi.org/10.1126/scisignal.2005735.CrossRefPubMedPubMedCentral

126.

Vici P, Mottolese M, Pizzuti L, Barba M, Sperati F, Terrenato I, et al. The Hippo transducer TAZ as a biomarker of pathological complete response in HER2-positive breast cancer patients treated with trastuzumab-based neoadjuvant therapy. Oncotarget. 2014;5(20):9619–25. https://doi.org/10.18632/oncotarget.2449.CrossRefPubMedPubMedCentral

127.

González-Alonso P, Zazo S, Martín-Aparicio E, Luque M, Chamizo C, Sanz-Álvarez M, et al. The Hippo pathway transducers YAP1/TEAD induce acquired resistance to trastuzumab in HER2-positive breast cancer. Cancers (Basel). 2020;12(5):1108. https://doi.org/10.3390/cancers12051108.CrossRefPubMedCentral

128.

Lin CH, Pelissier FA, Zhang H, Lakins J, Weaver VM, Park C, 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. https://doi.org/10.1091/mbc.E15-07-0456.CrossRefPubMedPubMedCentral

129.

Azad T, Nouri K, Janse van Rensburg HJ, Maritan SM, Wu L, Hao Y, et al. A gain-of-functional screen identifies the Hippo pathway as a central mediator of receptor tyrosine kinases during tumorigenesis. Oncogene. 2020;39(2):334–55. https://doi.org/10.1038/s41388-019-0988-y.CrossRefPubMed

130.

Turunen SP, von Nandelstadh P, Ohman T, Gucciardo E, Seashore-Ludlow B, Martins B, et al. FGFR4 phosphorylates MST1 to confer breast cancer cells resistance to MST1/2-dependent apoptosis. Cell Death Differ. 2019;26(12):2577–93. https://doi.org/10.1038/s41418-019-0321-x.CrossRefPubMedPubMedCentral

131.

Rigiracciolo DC, Nohata N, Lappano R, Cirillo F, Talia M, Scordamaglia D, et al. IGF-1/IGF-1R/FAK/YAP transduction signaling prompts growth effects in triple-negative breast cancer (TNBC) cells. Cells. 2020;9(4):1010. https://doi.org/10.3390/cells9041010.CrossRefPubMedCentral

132.

Wu L, Yang X. Targeting the Hippo pathway for breast cancer therapy. Cancers (Basel). 2018;10(11):422. https://doi.org/10.3390/cancers10110422.CrossRefPubMedCentral

133.

Huang R, Li J, Pan F, Zhang B, Yao Y. The activation of GPER inhibits cells proliferation, invasion and EMT of triple-negative breast cancer via CD151/miR-199a-3p bio-axis. Am J Transl Res. 2020;12(1):32–44.PubMedPubMedCentral

134.

Mayoral-Varo V, Calcabrini A, Sánchez-Bailón MP, Martín-Pérez J. miR205 inhibits stem cell renewal in SUM159PT breast cancer cells. PLoS ONE. 2017;12(11):e0188637. https://doi.org/10.1371/journal.pone.0188637.CrossRefPubMedPubMedCentral

135.

Zhang KJ, Hu Y, Luo N, Li X, Chen FY, Yuan JQ, et al. miR-574-5p attenuates proliferation, migration and EMT in triple-negative breast cancer cells by targeting BCL11A and SOX2 to inhibit the SKIL/TAZ/CTGF axis. Int J Oncol. 2020;56(5):1240–51. https://doi.org/10.3892/ijo.2020.4995.CrossRefPubMed

136.

Liu Y, Li M, Yu H, Piao H. lncRNA CYTOR promotes tamoxifen resistance inbreast cancer cells via sponging miR-125a-5p. Int J Mol Med. 2019;45(2):497–509. https://doi.org/10.3892/ijmm.2019.4428.CrossRefPubMedPubMedCentral

137.

Manavalan TT, Teng Y, Litchfield LM, Muluhngwi P, Al-Rayyan N, Klinge CM. Reduced expression of miR-200 family members contributes to antiestrogen resistance in LY2 human breast cancer cells. PLoS ONE. 2013;8(4):e62334. https://doi.org/10.1371/journal.pone.0062334.CrossRefPubMedPubMedCentral

138.

Liu L, Shen W, Zhu Z, Lin J, Fang Q, Ruan Y, et al. Combined inhibition of EGFR and c-ABL suppresses the growth of fulvestrant-resistant breast cancer cells through miR-375-autophagy axis. Biochem Biophys Res Commun. 2018;498(3):559–65. https://doi.org/10.1016/j.bbrc.2018.03.019.CrossRefPubMed

139.

Lu Y, Roy S, Nuovo G, Ramaswamy B, Miller T, Shapiro C, et al. Anti-microRNA-222 (anti-miR-222) and -181B suppress growth of tamoxifen-resistant xenografts in mouse by targeting TIMP3 protein and modulating mitogenic signal. J Biol Chem. 2011;286(49):42292–302. https://doi.org/10.1074/jbc.M111.270926.CrossRefPubMedPubMedCentral

140.

Sorrentino G, Ruggeri N, Specchia V, Cordenonsi M, Mano M, Dupont S, et al. Metabolic control of YAP and TAZ by the mevalonate pathway. Nat Cell Biol. 2014;16(4):357–66. https://doi.org/10.1038/ncb2936.CrossRefPubMed

141.

Liu J, Li J, Chen H, Wang R, Li P, Miao Y, 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. https://doi.org/10.1111/jcmm.15241.CrossRefPubMedPubMedCentral

142.

Wu D, Jia H, Zhang Z, Li S. Circ_0000511 accelerates the proliferation, migration and invasion, and restrains the apoptosis of breast cancer cells through the miR-326/TAZ axis. Int J Oncol. 2021;58(4):1. https://doi.org/10.3892/ijo.2021.5181.CrossRefPubMedPubMedCentral

143.

Liu Y, Zhang Q, Wu J, Zhang H, Li X, Zheng Z, et al. Long non-coding RNA A2M-AS1 promotes breast cancer progression by sponging microRNA-146b to Upregulate MUC19. Int J Gen Med. 2020;13:1305–16. https://doi.org/10.2147/ijgm.S278564.CrossRefPubMedPubMedCentral

144.

Hu J, Ji C, Hua K, Wang X, Deng X, Li J, et al. Hsa_circ_0091074 regulates TAZ expression via microRNA-1297 in triple negative breast cancer cells. Int J Oncol. 2020;56(5):1314–26. https://doi.org/10.3892/ijo.2020.5000.CrossRefPubMed

145.

Geng Z, Wang W, Chen H, Mao J, Li Z, Zhou J. Circ_0001667 promotes breast cancer cell proliferation and survival via Hippo signal pathway by regulating TAZ. Cell Biosci. 2019;9:104. https://doi.org/10.1186/s13578-019-0359-y.CrossRefPubMedPubMedCentral

146.

Liu Y, Li M, Yu H, Piao H. lncRNA CYTOR promotes tamoxifen resistance in breast cancer cells via sponging miR-125a-5p. Int J Mol Med. 2020;45(2):497–509. https://doi.org/10.3892/ijmm.2019.4428.CrossRefPubMed

147.

Qiao K, Ning S, Wan L, Wu H, Wang Q, Zhang X, et al. LINC00673 is activated by YY1 and promotes the proliferation of breast cancer cells via the miR-515–5p/MARK4/Hippo signaling pathway. J Exp Clin Cancer Res. 2019;38(1):418. https://doi.org/10.1186/s13046-019-1421-7.CrossRefPubMedPubMedCentral

148.

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;19:108. https://doi.org/10.1186/s12935-019-0818-x.CrossRefPubMedPubMedCentral

149.

Cheng X, Chen J, Huang Z. miR-372 promotes breast cancer cell proliferation by directly targeting LATS2. Exp Ther Med. 2018;15(3):2812–7. https://doi.org/10.3892/etm.2018.5761.CrossRefPubMedPubMedCentral

150.

Zhu HY, Bai WD, Ye XM, Yang AG, Jia LT. Long non-coding RNA UCA1 desensitizes breast cancer cells to trastuzumab by impeding miR-18a repression of Yes-associated protein 1. Biochem Biophys Res Commun. 2018;496(4):1308–13. https://doi.org/10.1016/j.bbrc.2018.02.006.CrossRefPubMed

151.

Xie D, Song H, Wu T, Li D, Hua K, Xu H, et al. MicroRNA-424 serves an anti-oncogenic role by targeting cyclin-dependent kinase 1 in breast cancer cells. Oncol Rep. 2018;40(6):3416–26. https://doi.org/10.3892/or.2018.6741.CrossRefPubMedPubMedCentral

152.

Hua K, Jin J, Zhao J, Song J, Song H, Li D, et al. miR-135b, upregulated in breast cancer, promotes cell growth and disrupts the cell cycle by regulating LATS2. Int J Oncol. 2016;48(5):1997–2006. https://doi.org/10.3892/ijo.2016.3405.CrossRefPubMed

153.

Hua K, Yang W, Song H, Song J, Wei C, Li D, et al. Up-regulation of miR-506 inhibits cell growth and disrupt the cell cycle by targeting YAP in breast cancer cells. Int J Clin Exp Med. 2015;8(8):12018–27.PubMedPubMedCentral

154.

Beillard E, Ong SC, Giannakakis A, Guccione E, Vardy LA, Voorhoeve PM. miR-Sens—a retroviral dual-luciferase reporter to detect microRNA activity in primary cells. RNA. 2012;18(5):1091–100. https://doi.org/10.1261/rna.031831.111.CrossRefPubMedPubMedCentral

155.

Fang L, Du WW, Yang W, Rutnam ZJ, Peng C, Li H, et al. MiR-93 enhances angiogenesis and metastasis by targeting LATS2. Cell Cycle. 2012;11(23):4352–65. https://doi.org/10.4161/cc.22670.CrossRefPubMedPubMedCentral

156.

Yu SJ, Hu JY, Kuang XY, Luo JM, Hou YF, Di GH, et al. MicroRNA-200a promotes anoikis resistance and metastasis by targeting YAP1 in human breast cancer. Clin Cancer Res. 2013;19(6):1389–99. https://doi.org/10.1158/1078-0432.CCR-12-1959.CrossRefPubMed

157.

Gao L, Bao Z, Deng H, Li X, Li J, Rong Z, et al. The beneficial androgenic action of steroidal aromatase inactivators in estrogen-dependent breast cancer after failure of nonsteroidal drugs. Cell Death Dis. 2019;10(7):494. https://doi.org/10.1038/s41419-019-1724-9.CrossRefPubMedPubMedCentral

Title: Utilizing the Hippo pathway as a therapeutic target for combating endocrine-resistant breast cancer
Authors: Jing Chen
Runlan Wan
Qinqin Li
Zhenghuan Rao
Yanlin Wang
Lei Zhang
Alexander Tobias Teichmann
Publication date: 01-12-2021
Publisher: BioMed Central
Keywords: Breast Cancer
Breast Cancer
Tamoxifen
Published in: Cancer Cell International / Issue 1/2021
Electronic ISSN: 1475-2867
DOI: https://doi.org/10.1186/s12935-021-01999-5

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