Research progress of Hippo signaling pathway in triple negative breast cancer_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

QIAN Shuangqiang , HOU Lingmi , CHEN Jingtai , PU Hongyu ,  GAO Yanchun

Department of Thyroid and Breast Surgery, Affiliated Hospital of North Sichuan Medical College, Nanchong, Sichuan 637000, P. R. China;

Corresponding author：

GAO Yanchun, Email: boyang11111@163.com

Keywords：

Hippo signal pathway; triple negative breast cancer; progress; treatment

DOI：

10.7507/1007-9424.202109025

Video：

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Abstract Full text Figures/Tables Video References Cited by

Objective To summarize the research progress of Hippo signaling pathway in triple negative breast cancer (TNBC). Method Literatures about studies the role of Hippo signaling pathway in cancer stem cells, epithelial-mesenchymal transformation, tumorigenesis and development, distant metastasis, treatment resistance, and treatment strategies were retrieved. Results In TNBC, overexpression of Yes-associated protein and PDZ-binding motif could promote the development of tumor stem cells, induce epithelial-mesenchymal transformation of TNBC cells, and promote tumor development, distant metastasis, and chemotherapy resistance. Conclusion Hippo/Yes-associated protein axis plays an important role in carcinogenesis and progression of TNBC, and targeting Hippo signaling pathway might be a potential therapeutic target for TNBC.

Citation： QIAN Shuangqiang, HOU Lingmi, CHEN Jingtai, PU Hongyu, GAO Yanchun. Research progress of Hippo signaling pathway in triple negative breast cancer. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2022, 29(7): 965-970. doi: 10.7507/1007-9424.202109025 Copy

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): 209-249.
2.	Wu L, Yang X. Targeting the Hippo pathway for breast cancer therapy. Cancers (Basel), 2018, 10(11): 422. doi: 10.3390/cancers10110422.
3.	Zhao B, Lei QY, Guan KL. The Hippo-YAP pathway: new connections between regulation of organ size and cancer. Curr Opin Cell Biol, 2008, 20(6): 638-646.
4.	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. doi: 10.3389/fonc.2021.609743.
5.	Díaz-Martín J, López-García MÁ, Romero-Pérez L, et al. Nuclear TAZ expression associates with the triple-negative phenotype in breast cancer. Endocr Relat Cancer, 2015, 22(3): 443-454.
6.	Yu FX, Zhao B, Guan KL. Hippo pathway in organ size control, tissue homeostasis, and cancer. Cell, 2015, 163(4): 811-828.
7.	Moroishi T, Hansen CG, Guan KL. The emerging roles of YAP and TAZ in cancer. Nat Rev Cancer, 2015, 15(2): 73-79.
8.	Mo JS, Park HW, Guan KL. The Hippo signaling pathway in stem cell biology and cancer. EMBO Rep, 2014, 15(6): 642-656.
9.	Zhao B, Wei X, Li W, et al. Inactivation of YAP oncoprotein by the Hippo pathway is involved in cell contact inhibition and tissue growth control. Genes Dev, 2007, 21(21): 2747-2761.
10.	Liu CY, Zha ZY, Zhou X, et al. The Hippo tumor pathway promotes TAZ degradation by phosphorylating a phosphodegron and recruiting the SCFβ-TrCP E3 ligase. J Biol Chem, 2010, 285(48): 37159-37169.
11.	Zhao B, Ye X, Yu J, et al. TEAD mediates YAP-dependent gene induction and growth control. Genes Dev, 2008, 22(14): 1962-1971.
12.	Koontz LM, Liu-Chittenden Y, Yin F, et al. The Hippo effector Yorkie controls normal tissue growth by antagonizing scalloped-mediated default repression. Dev Cell, 2013, 25(4): 388-401.
13.	Vici P, Ercolani C, Di Benedetto A, et al. Topographic expression of the Hippo transducers TAZ and YAP in triple-negative breast cancer treated with neoadjuvant chemotherapy. J Exp Clin Cancer Res, 2016, 35: 62. doi: 10.1186/s13046-016-0338-7.
14.	Nassar D, Blanpain C. Cancer stem cells: basic concepts and therapeutic implications. Annu Rev Pathol, 2016, 11: 47-76.
15.	Park JH, Shin JE, Park HW. The role of Hippo pathway in cancer stem cell biology. Mol Cells, 2018, 41(2): 83-92.
16.	Samanta S, Sun H, Goel HL, et al. IMP3 promotes stem-like properties in triple-negative breast cancer by regulating SLUG. Oncogene, 2016, 35(9): 1111-1121.
17.	Samanta S, Guru S, Elaimy AL, et al. IMP3 stabilization of WNT5B mRNA facilitates TAZ activation in breast cancer. Cell Rep, 2018, 23(9): 2559-2567.
18.	Gao Y, Chen X, He Q, et al. Adipocytes promote breast tumorigenesis through TAZ-dependent secretion of Resistin. Proc Natl Acad Sci USA, 2020, 117(52): 33295-33304.
19.	Sun HL, Men JR, Liu HY, et al. FOXM1 facilitates breast cancer cell stemness and migration in YAP1-dependent manner. Arch Biochem Biophys, 2020, 685: 108349. doi: 10.1016/j.abb.2020.108349.
20.	Liu S, Cong Y, Wang D, et al. Breast cancer stem cells transition between epithelial and mesenchymal states reflective of their normal counterparts. Stem Cell Reports, 2013, 2(1): 78-91.
21.	Sulaiman A, McGarry S, Li L, et al. Dual inhibition of Wnt and Yes-associated protein signaling retards the growth of triple-negative breast cancer in both mesenchymal and epithelial states. Mol Oncol, 2018, 12(4): 423-440.
22.	Rajabi H, Kufe D. MUC1-C oncoprotein integrates a program of EMT, epigenetic reprogramming and immune evasion in human carcinomas. Biochim Biophys Acta Rev Cancer, 2017, 1868(1): 117-122.
23.	Li P, Mao X, Ren Y, et al. Epithelial cell polarity determinant CRB3 in cancer development. Int J Biol Sci, 2015, 11(1): 31-37.
24.	Alam M, Bouillez A, Tagde A, et al. MUC1-C represses the crumbs complex polarity factor CRB3 and downregulates the Hippo pathway. Mol Cancer Res, 2016, 14(12): 1266-1276.
25.	Quinn HM, Vogel R, Popp O, et al. YAP and β-catenin cooperate to drive oncogenesis in basal breast cancer. Cancer Res, 2021, 81(8): 2116-2127.
26.	Wang Z, Katsaros D, Biglia N, et al. Low expression of WWC1, a tumor suppressor gene, is associated with aggressive breast cancer and poor survival outcome. FEBS Open Bio, 2019, 9(7): 1270-1280.
27.	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.doi: 10.1038/oncsis.2016.67.
28.	Liu X, Li C, Zhang R, et al. The EZH2- H3K27me3-DNMT1 complex orchestrates epigenetic silencing of the wwc1 gene, a Hippo/YAP pathway upstream effector, in breast cancer epithelial cells. Cell Signal, 2018, 51: 243-256.
29.	Thirunavukkarasan M, Wang C, Rao A, et al. Short-chain fatty acid receptors inhibit invasive phenotypes in breast cancer cells. PLoS One, 2017, 12(10): e0186334. doi: 10.1371/journal.pone.0186334.
30.	Dang DK, Makena MR, Llongueras JP, et al. A Ca²⁺-ATPase regulates E-cadherin biogenesis and epithelial-mesenchymal transition in breast cancer cells. Mol Cancer Res, 2019, 17(8): 1735-1747.
31.	王加琪, 张一帆, 张研, 等. microRNA-200 家族在三阴性乳腺癌中的研究进展. 中国普外基础与临床杂志, 2019, 26(8): 1002-1006.
32.	Feldker N, Ferrazzi F, Schuhwerk H, et al. Genome-wide cooperation of EMT transcription factor ZEB1 with YAP and AP-1 in breast cancer. EMBO J, 2020, 39(17): e103209. doi: 10.15252/embj.2019103209.
33.	Ye S, Xu Y, Wang L, et al. Estrogen-related receptor α (ERRα) and G protein-coupled estrogen receptor (GPER) synergistically indicate poor prognosis in patients with triple-negative breast cancer. Onco Targets Ther, 2020, 13: 8887-8899.
34.	Huang R, Li J, Pan F, et al. 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.
35.	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. doi: 10.1038/s41389-020-0220-5.
36.	Zhou R, Ding Y, Xue M, et al. RNF181 modulates Hippo signaling and triple negative breast cancer progression. Cancer Cell Int, 2020, 20: 291. doi: 10.1186/s12935-020-01397-3.
37.	Liu Y, Su P, Zhao W, et al. ZNF213 negatively controls triple negative breast cancer progression via Hippo/YAP signaling. Cancer Sci, 2021, 112(7): 2714-2727.
38.	Kedan A, Verma N, Saroha A, et al. PYK2 negatively regulates the Hippo pathway in TNBC by stabilizing TAZ protein. Cell Death Dis, 2018, 9(10): 985. doi: 10.1038/s41419-018-1005-z.
39.	Mussell A, Shen H, Chen Y, et al. USP1 regulates TAZ protein stability through ubiquitin modifications in breast cancer. Cancers (Basel), 2020, 12(11): 3090. doi: 10.3390/cancers12113090.
40.	Guo X, Zhao Y, Yan H, et al. Single tumor-initiating cells evade immune clearance by recruiting type Ⅱ macrophages. Genes Dev, 2017, 31(3): 247-259.
41.	Zhang Y, Fan Y, Jing X, et al. OTUD5-mediated deubiquitination of YAP in macrophage promotes M2 phenotype polarization and favors triple-negative breast cancer progression. Cancer Lett, 2021, 504: 104-115.
42.	Rigiracciolo DC, Nohata N, Lappano R, 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.
43.	Jiang K, Liu P, Xu H, et al. SASH1 suppresses triple-negative breast cancer cell invasion through YAP-ARHGAP42-actin axis. Oncogene, 2020, 39(27): 5015-5030.
44.	Li Y, Hua K, Jin J, et al. miR-497 inhibits proliferation and invasion in triple-negative breast cancer cells via YAP1. Oncol Lett, 2021, 22(2): 580. doi: 10.3892/ol.2021.12841.
45.	Wang Y, Liu S. LncRNA GHET1 promotes hypoxia-induced glycolysis, proliferation, and invasion in triple-negative breast cancer through the Hippo/YAP signaling pathway. Front Cell Dev Biol, 2021, 9: 643515. doi: 10.3389/fcell.2021.643515.
46.	Hu J, Ji C, Hua K, et al. Hsa_circ_0091074 regulates TAZ expression via microRNA-1297 in triple negative breast cancer cells. Int J Oncol, 2020, 56(5): 1314-1326.
47.	An P, Li J, Lu L, et al. Histone deacetylase 8 triggers the migration of triple negative breast cancer cells via regulation of YAP signals. Eur J Pharmacol, 2019, 845: 16-23.
48.	Deng Q, Jiang G, Wu Y, et al. GPER/Hippo-YAP signal is involved in bisphenol S induced migration of triple negative breast cancer (TNBC) cells. J Hazard Mater, 2018, 355: 1-9.
49.	Chen W, Bai Y, Patel C, et al. Autophagy promotes triple negative breast cancer metastasis via YAP nuclear localization. Biochem Biophys Res Commun, 2019, 520(2): 263-268.
50.	Liu J, Ye L, Li Q, et al. Synaptopodin-2 suppresses metastasis of triple-negative breast cancer via inhibition of YAP/TAZ activity. J Pathol, 2018, 244(1): 71-83.
51.	Gan L, Camarena V, Mustafi S, et al. Vitamin C inhibits triple-negative breast cancer metastasis by affecting the expression of YAP1 and synaptopodin 2. Nutrients, 2019, 11(12): 2997. doi: 10.3390/nu11122997.
52.	Wang G, Dong Y, Liu H, et al. Loss of miR-873 contributes to gemcitabine resistance in triple-negative breast cancer via targeting ZEB1. Oncol Lett, 2019, 18(4): 3837-3844.
53.	He Z, Zhao TT, Jin F, et al. Downregulation of RASSF6 promotes breast cancer growth and chemoresistance through regulation of Hippo signaling. Biochem Biophys Res Commun, 2018, 503(4): 2340-2347.
54.	Koh SB, Ross K, Isakoff SJ, et al. RASAL2 confers collateral MEK/EGFR dependency in chemoresistant triple-negative breast cancer. Clin Cancer Res, 2021, 27(17): 4883-4897.
55.	Elaimy AL, Amante JJ, Zhu LJ, et al. The VEGF receptor neuropilin 2 promotes homologous recombination by stimulating YAP/TAZ-mediated Rad51 expression. Proc Natl Acad Sci USA, 2019, 116(28): 14174-14180.
56.	Ma J, Fan Z, Tang Q, et al. Aspirin attenuates YAP and β-catenin expression by promoting β-TrCP to overcome docetaxel and vinorelbine resistance in triple-negative breast cancer. Cell Death Dis, 2020, 11(7): 530. doi: 10.1038/s41419-020-2719-2.
57.	Dai M, Yan G, Wang N, et al. In vivo genome-wide CRISPR screen reveals breast cancer vulnerabilities and synergistic mTOR/Hippo targeted combination therapy. Nat Commun, 2021, 12(1): 3055. doi: 10.1038/s41467-021-23316-4.
58.	Koohestanimobarhan S, Salami S, Imeni V, et al. Lipophilic statins antagonistically alter the major epithelial-to-mesenchymal transition signaling pathways in breast cancer stem-like cells via inhibition of the mevalonate pathway. J Cell Biochem, 2018 Sep 6. doi: 10.1002/jcb.27544.
59.	Pérez-Herrero E, Fernández-Medarde A. Advanced targeted therapies in cancer: drug nanocarriers, the future of chemotherapy. Eur J Pharm Biopharm, 2015, 93: 52-79.
60.	Sulaiman A, McGarry S, El-Sahli S, et al. Co-targeting bulk tumor and CSCs in clinically translatable TNBC patient-derived xenografts via combination nanotherapy. Mol Cancer Ther, 2019, 18(10): 1755-1764.
61.	El-Sahli S, Hua K, Sulaiman A, et al. A triple-drug nanotherapy to target breast cancer cells, cancer stem cells, and tumor vasculature. Cell Death Dis, 2021, 12(1): 8. doi: 10.1038/s41419-020-03308-w.

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): 209-249.
2. Wu L, Yang X. Targeting the Hippo pathway for breast cancer therapy. Cancers (Basel), 2018, 10(11): 422. doi: 10.3390/cancers10110422.
3. Zhao B, Lei QY, Guan KL. The Hippo-YAP pathway: new connections between regulation of organ size and cancer. Curr Opin Cell Biol, 2008, 20(6): 638-646.
4. 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. doi: 10.3389/fonc.2021.609743.
5. Díaz-Martín J, López-García MÁ, Romero-Pérez L, et al. Nuclear TAZ expression associates with the triple-negative phenotype in breast cancer. Endocr Relat Cancer, 2015, 22(3): 443-454.
6. Yu FX, Zhao B, Guan KL. Hippo pathway in organ size control, tissue homeostasis, and cancer. Cell, 2015, 163(4): 811-828.
7. Moroishi T, Hansen CG, Guan KL. The emerging roles of YAP and TAZ in cancer. Nat Rev Cancer, 2015, 15(2): 73-79.
8. Mo JS, Park HW, Guan KL. The Hippo signaling pathway in stem cell biology and cancer. EMBO Rep, 2014, 15(6): 642-656.
9. Zhao B, Wei X, Li W, et al. Inactivation of YAP oncoprotein by the Hippo pathway is involved in cell contact inhibition and tissue growth control. Genes Dev, 2007, 21(21): 2747-2761.
10. Liu CY, Zha ZY, Zhou X, et al. The Hippo tumor pathway promotes TAZ degradation by phosphorylating a phosphodegron and recruiting the SCFβ-TrCP E3 ligase. J Biol Chem, 2010, 285(48): 37159-37169.
11. Zhao B, Ye X, Yu J, et al. TEAD mediates YAP-dependent gene induction and growth control. Genes Dev, 2008, 22(14): 1962-1971.
12. Koontz LM, Liu-Chittenden Y, Yin F, et al. The Hippo effector Yorkie controls normal tissue growth by antagonizing scalloped-mediated default repression. Dev Cell, 2013, 25(4): 388-401.
13. Vici P, Ercolani C, Di Benedetto A, et al. Topographic expression of the Hippo transducers TAZ and YAP in triple-negative breast cancer treated with neoadjuvant chemotherapy. J Exp Clin Cancer Res, 2016, 35: 62. doi: 10.1186/s13046-016-0338-7.
14. Nassar D, Blanpain C. Cancer stem cells: basic concepts and therapeutic implications. Annu Rev Pathol, 2016, 11: 47-76.
15. Park JH, Shin JE, Park HW. The role of Hippo pathway in cancer stem cell biology. Mol Cells, 2018, 41(2): 83-92.
16. Samanta S, Sun H, Goel HL, et al. IMP3 promotes stem-like properties in triple-negative breast cancer by regulating SLUG. Oncogene, 2016, 35(9): 1111-1121.
17. Samanta S, Guru S, Elaimy AL, et al. IMP3 stabilization of WNT5B mRNA facilitates TAZ activation in breast cancer. Cell Rep, 2018, 23(9): 2559-2567.
18. Gao Y, Chen X, He Q, et al. Adipocytes promote breast tumorigenesis through TAZ-dependent secretion of Resistin. Proc Natl Acad Sci USA, 2020, 117(52): 33295-33304.
19. Sun HL, Men JR, Liu HY, et al. FOXM1 facilitates breast cancer cell stemness and migration in YAP1-dependent manner. Arch Biochem Biophys, 2020, 685: 108349. doi: 10.1016/j.abb.2020.108349.
20. Liu S, Cong Y, Wang D, et al. Breast cancer stem cells transition between epithelial and mesenchymal states reflective of their normal counterparts. Stem Cell Reports, 2013, 2(1): 78-91.
21. Sulaiman A, McGarry S, Li L, et al. Dual inhibition of Wnt and Yes-associated protein signaling retards the growth of triple-negative breast cancer in both mesenchymal and epithelial states. Mol Oncol, 2018, 12(4): 423-440.
22. Rajabi H, Kufe D. MUC1-C oncoprotein integrates a program of EMT, epigenetic reprogramming and immune evasion in human carcinomas. Biochim Biophys Acta Rev Cancer, 2017, 1868(1): 117-122.
23. Li P, Mao X, Ren Y, et al. Epithelial cell polarity determinant CRB3 in cancer development. Int J Biol Sci, 2015, 11(1): 31-37.
24. Alam M, Bouillez A, Tagde A, et al. MUC1-C represses the crumbs complex polarity factor CRB3 and downregulates the Hippo pathway. Mol Cancer Res, 2016, 14(12): 1266-1276.
25. Quinn HM, Vogel R, Popp O, et al. YAP and β-catenin cooperate to drive oncogenesis in basal breast cancer. Cancer Res, 2021, 81(8): 2116-2127.
26. Wang Z, Katsaros D, Biglia N, et al. Low expression of WWC1, a tumor suppressor gene, is associated with aggressive breast cancer and poor survival outcome. FEBS Open Bio, 2019, 9(7): 1270-1280.
27. 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.doi: 10.1038/oncsis.2016.67.
28. Liu X, Li C, Zhang R, et al. The EZH2- H3K27me3-DNMT1 complex orchestrates epigenetic silencing of the wwc1 gene, a Hippo/YAP pathway upstream effector, in breast cancer epithelial cells. Cell Signal, 2018, 51: 243-256.
29. Thirunavukkarasan M, Wang C, Rao A, et al. Short-chain fatty acid receptors inhibit invasive phenotypes in breast cancer cells. PLoS One, 2017, 12(10): e0186334. doi: 10.1371/journal.pone.0186334.
30. Dang DK, Makena MR, Llongueras JP, et al. A Ca²⁺-ATPase regulates E-cadherin biogenesis and epithelial-mesenchymal transition in breast cancer cells. Mol Cancer Res, 2019, 17(8): 1735-1747.
31. 王加琪, 张一帆, 张研, 等. microRNA-200 家族在三阴性乳腺癌中的研究进展. 中国普外基础与临床杂志, 2019, 26(8): 1002-1006.
32. Feldker N, Ferrazzi F, Schuhwerk H, et al. Genome-wide cooperation of EMT transcription factor ZEB1 with YAP and AP-1 in breast cancer. EMBO J, 2020, 39(17): e103209. doi: 10.15252/embj.2019103209.
33. Ye S, Xu Y, Wang L, et al. Estrogen-related receptor α (ERRα) and G protein-coupled estrogen receptor (GPER) synergistically indicate poor prognosis in patients with triple-negative breast cancer. Onco Targets Ther, 2020, 13: 8887-8899.
34. Huang R, Li J, Pan F, et al. 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.
35. 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. doi: 10.1038/s41389-020-0220-5.
36. Zhou R, Ding Y, Xue M, et al. RNF181 modulates Hippo signaling and triple negative breast cancer progression. Cancer Cell Int, 2020, 20: 291. doi: 10.1186/s12935-020-01397-3.
37. Liu Y, Su P, Zhao W, et al. ZNF213 negatively controls triple negative breast cancer progression via Hippo/YAP signaling. Cancer Sci, 2021, 112(7): 2714-2727.
38. Kedan A, Verma N, Saroha A, et al. PYK2 negatively regulates the Hippo pathway in TNBC by stabilizing TAZ protein. Cell Death Dis, 2018, 9(10): 985. doi: 10.1038/s41419-018-1005-z.
39. Mussell A, Shen H, Chen Y, et al. USP1 regulates TAZ protein stability through ubiquitin modifications in breast cancer. Cancers (Basel), 2020, 12(11): 3090. doi: 10.3390/cancers12113090.
40. Guo X, Zhao Y, Yan H, et al. Single tumor-initiating cells evade immune clearance by recruiting type Ⅱ macrophages. Genes Dev, 2017, 31(3): 247-259.
41. Zhang Y, Fan Y, Jing X, et al. OTUD5-mediated deubiquitination of YAP in macrophage promotes M2 phenotype polarization and favors triple-negative breast cancer progression. Cancer Lett, 2021, 504: 104-115.
42. Rigiracciolo DC, Nohata N, Lappano R, 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.
43. Jiang K, Liu P, Xu H, et al. SASH1 suppresses triple-negative breast cancer cell invasion through YAP-ARHGAP42-actin axis. Oncogene, 2020, 39(27): 5015-5030.
44. Li Y, Hua K, Jin J, et al. miR-497 inhibits proliferation and invasion in triple-negative breast cancer cells via YAP1. Oncol Lett, 2021, 22(2): 580. doi: 10.3892/ol.2021.12841.
45. Wang Y, Liu S. LncRNA GHET1 promotes hypoxia-induced glycolysis, proliferation, and invasion in triple-negative breast cancer through the Hippo/YAP signaling pathway. Front Cell Dev Biol, 2021, 9: 643515. doi: 10.3389/fcell.2021.643515.
46. Hu J, Ji C, Hua K, et al. Hsa_circ_0091074 regulates TAZ expression via microRNA-1297 in triple negative breast cancer cells. Int J Oncol, 2020, 56(5): 1314-1326.
47. An P, Li J, Lu L, et al. Histone deacetylase 8 triggers the migration of triple negative breast cancer cells via regulation of YAP signals. Eur J Pharmacol, 2019, 845: 16-23.
48. Deng Q, Jiang G, Wu Y, et al. GPER/Hippo-YAP signal is involved in bisphenol S induced migration of triple negative breast cancer (TNBC) cells. J Hazard Mater, 2018, 355: 1-9.
49. Chen W, Bai Y, Patel C, et al. Autophagy promotes triple negative breast cancer metastasis via YAP nuclear localization. Biochem Biophys Res Commun, 2019, 520(2): 263-268.
50. Liu J, Ye L, Li Q, et al. Synaptopodin-2 suppresses metastasis of triple-negative breast cancer via inhibition of YAP/TAZ activity. J Pathol, 2018, 244(1): 71-83.
51. Gan L, Camarena V, Mustafi S, et al. Vitamin C inhibits triple-negative breast cancer metastasis by affecting the expression of YAP1 and synaptopodin 2. Nutrients, 2019, 11(12): 2997. doi: 10.3390/nu11122997.
52. Wang G, Dong Y, Liu H, et al. Loss of miR-873 contributes to gemcitabine resistance in triple-negative breast cancer via targeting ZEB1. Oncol Lett, 2019, 18(4): 3837-3844.
53. He Z, Zhao TT, Jin F, et al. Downregulation of RASSF6 promotes breast cancer growth and chemoresistance through regulation of Hippo signaling. Biochem Biophys Res Commun, 2018, 503(4): 2340-2347.
54. Koh SB, Ross K, Isakoff SJ, et al. RASAL2 confers collateral MEK/EGFR dependency in chemoresistant triple-negative breast cancer. Clin Cancer Res, 2021, 27(17): 4883-4897.
55. Elaimy AL, Amante JJ, Zhu LJ, et al. The VEGF receptor neuropilin 2 promotes homologous recombination by stimulating YAP/TAZ-mediated Rad51 expression. Proc Natl Acad Sci USA, 2019, 116(28): 14174-14180.
56. Ma J, Fan Z, Tang Q, et al. Aspirin attenuates YAP and β-catenin expression by promoting β-TrCP to overcome docetaxel and vinorelbine resistance in triple-negative breast cancer. Cell Death Dis, 2020, 11(7): 530. doi: 10.1038/s41419-020-2719-2.
57. Dai M, Yan G, Wang N, et al. In vivo genome-wide CRISPR screen reveals breast cancer vulnerabilities and synergistic mTOR/Hippo targeted combination therapy. Nat Commun, 2021, 12(1): 3055. doi: 10.1038/s41467-021-23316-4.
58. Koohestanimobarhan S, Salami S, Imeni V, et al. Lipophilic statins antagonistically alter the major epithelial-to-mesenchymal transition signaling pathways in breast cancer stem-like cells via inhibition of the mevalonate pathway. J Cell Biochem, 2018 Sep 6. doi: 10.1002/jcb.27544.
59. Pérez-Herrero E, Fernández-Medarde A. Advanced targeted therapies in cancer: drug nanocarriers, the future of chemotherapy. Eur J Pharm Biopharm, 2015, 93: 52-79.
60. Sulaiman A, McGarry S, El-Sahli S, et al. Co-targeting bulk tumor and CSCs in clinically translatable TNBC patient-derived xenografts via combination nanotherapy. Mol Cancer Ther, 2019, 18(10): 1755-1764.
61. El-Sahli S, Hua K, Sulaiman A, et al. A triple-drug nanotherapy to target breast cancer cells, cancer stem cells, and tumor vasculature. Cell Death Dis, 2021, 12(1): 8. doi: 10.1038/s41419-020-03308-w.

CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Research progress of Hippo signaling pathway in triple negative breast cancer

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