Advances in understanding the role and mechanisms of tumor stem cells in HER2-positive breast cancer treatment resistance (Review)
- Authors:
- Linfei Xu
- Fang Han
- Liang Zhu
- Wenli Ding
- Kexin Zhang
- Chengxia Kan
- Ningning Hou
- Qinying Li
- Xiaodong Sun
-
Affiliations: Department of Endocrinology and Metabolism, Affiliated Hospital of Weifang Medical University, Weifang, Shandong 261031, P.R. China, Department of Pathology, Affiliated Hospital of Weifang Medical University, Weifang, Shandong 261031, P.R. China - Published online on: February 28, 2023 https://doi.org/10.3892/ijo.2023.5496
- Article Number: 48
-
Copyright: © Xu et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
This article is mentioned in:
Abstract
Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A and Bray F: Global Cancer Statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 71:209–249. 2021. View Article : Google Scholar : PubMed/NCBI | |
Sorlie T, Tibshirani R, Parker J, Hastie T, Marron JS, Nobel A, Deng S, Johnsen H, Pesich R, Geisler S, et al: Repeated observation of breast tumor subtypes in independent gene expression data sets. Proc Natl Acad Sci USA. 100:8418–8423. 2003. View Article : Google Scholar : PubMed/NCBI | |
Hugh J, Hanson J, Cheang MC, Nielsen TO, Perou CM, Dumontet C, Reed J, Krajewska M, Treilleux I, Rupin M, et al: Breast cancer subtypes and response to docetaxel in node-positive breast cancer: Use of an immunohistochemical definition in the BCIRG 001 trial. J Clin Oncol. 27:1168–1176. 2009. View Article : Google Scholar : PubMed/NCBI | |
Prat A, Cheang MC, Martín M, Parker JS, Carrasco E, Caballero R, Tyldesley S, Gelmon K, Bernard PS, Nielsen TO, et al: Prognostic significance of progesterone receptor-positive tumor cells within immunohistochemically defined luminal A breast cancer. J Clin Oncol. 31:203–209. 2013. View Article : Google Scholar | |
Raj-Kumar PK, Liu J, Hooke JA, Kovatich AJ, Kvecher L, Shriver CD and Hu H: PCA-PAM50 improves consistency between breast cancer intrinsic and clinical subtyping reclassifying a subset of luminal A tumors as luminal B. Sci Rep. 9:79562019. View Article : Google Scholar : PubMed/NCBI | |
Nagini S: Breast cancer: Current molecular therapeutic targets and new players. Anticancer Agents Med Chem. 17:152–163. 2017. View Article : Google Scholar | |
Burstein HJ: The distinctive nature of HER2-positive breast cancers. N Engl J Med. 353:1652–1654. 2005. View Article : Google Scholar : PubMed/NCBI | |
Pernas S, Barroso-Sousa R and Tolaney SM: Optimal treatment of early stage HER2-positive breast cancer. Cancer. 124:4455–4466. 2018. View Article : Google Scholar : PubMed/NCBI | |
Pellat A, Vaquero J and Fouassier L: Role of ErbB/HER family of receptor tyrosine kinases in cholangiocyte biology. Hepatology. 67:762–773. 2018. View Article : Google Scholar | |
Reschke M, Mihic-Probst D, van der Horst EH, Knyazev P, Wild PJ, Hutterer M, Meyer S, Dummer R, Moch H and Ullrich A: HER3 is a determinant for poor prognosis in melanoma. Clin Cancer Res. 14:5188–5197. 2008. View Article : Google Scholar : PubMed/NCBI | |
Saglam O, Xiong Y, Marchion DC, Strosberg C, Wenham RM, Johnson JJ, Saeed-Vafa D, Cubitt C, Hakam A and Magliocco AM: ERBB4 expression in ovarian serous carcinoma resistant to platinum-based therapy. Cancer Control. 24:89–95. 2017. View Article : Google Scholar : PubMed/NCBI | |
Wang Z: ErbB receptors and cancer. Methods Mol Biol. 1652:3–35. 2017. View Article : Google Scholar : PubMed/NCBI | |
Watanabe S, Yonesaka K, Tanizaki J, Nonagase Y, Takegawa N, Haratani K, Kawakami H, Hayashi H, Takeda M, Tsurutani J and Nakagawaet K: Targeting of the HER2/HER3 signaling axis overcomes ligand-mediated resistance to trastuzumab in HER2-positive breast cancer. Cancer Med. 8:1258–1268. 2019. View Article : Google Scholar : PubMed/NCBI | |
Cronin KA, Harlan LC, Dodd KW, Abrams JS and Ballard-Barbash R: Population-based estimate of the prevalence of HER-2 positive breast cancer tumors for early stage patients in the US. Cancer Invest. 28:963–968. 2010. View Article : Google Scholar : PubMed/NCBI | |
Von Minckwitz G, Huang CS, Mano MS, Loibl S, Mamounas EP, Untch M, Wolmark N, Rastogi P, Schneeweiss A, Redondo A, et al: Trastuzumab Emtansine for residual invasive HER2-positive breast cancer. N Engl J Med. 380:617–628. 2019. View Article : Google Scholar | |
Saura C, Oliveira M, Feng YH, Dai MS, Chen SW, Hurvitz SA, Kim SB, Moy B, Delaloge S, Gradishar W, et al: Neratinib plus capecitabine versus lapatinib plus capecitabine in HER2-positive metastatic breast cancer previously treated with ≥2 HER2-directed regimens: Phase III NALA trial. J Clin Oncol. 38:3138–3149. 2020. View Article : Google Scholar : PubMed/NCBI | |
Piccart M, Procter M, Fumagalli D, de Azambuja E, Clark E, Ewer MS, Restuccia E, Jerusalem G, Dent S, Reaby L, et al: Adjuvant Pertuzumab and trastuzumab in early HER2-positive breast cancer in the APHINITY trial: 6 Years' follow-up. J Clin Oncol. 39:1448–1457. 2021. View Article : Google Scholar : PubMed/NCBI | |
Nader-Marta G, Martins-Branco D and de Azambuja E: How we treat patients with metastatic HER2-positive breast cancer. ESMO Open. 7:1003432022. View Article : Google Scholar : PubMed/NCBI | |
Figueroa-Magalhães MC, Jelovac D, Connolly R and Wolff AC: Treatment of HER2-positive breast cancer. Breast. 23:128–136. 2014. View Article : Google Scholar | |
Qiu Y, Yang L, Liu H and Luo X: Cancer stem cell-targeted therapeutic approaches for overcoming trastuzumab resistance in HER2-positive breast cancer. Stem Cells. 39:1125–1136. 2021. View Article : Google Scholar : PubMed/NCBI | |
Zhang Y: The root cause of drug resistance in HER2-positive breast cancer and the therapeutic approaches to overcoming the resistance. Pharmacol Ther. 218:1076772021. View Article : Google Scholar : | |
Ross JS, Slodkowska EA, Symmans WF, Pusztai L, Ravdin PM and Hortobagyi GN: The HER-2 receptor and breast cancer: Ten years of targeted anti-HER-2 therapy and personalized medicine. Oncologist. 14:320–368. 2009. View Article : Google Scholar : PubMed/NCBI | |
Lambertini M, Pondé NF, Solinas C and de Azambuja E: Adjuvant trastuzumab: A 10-year overview of its benefit. Expert Rev Anticancer Ther. 17:61–74. 2017. View Article : Google Scholar | |
Valabrega G, Montemurro F and Aglietta M: Trastuzumab: Mechanism of action, resistance and future perspectives in HER2-overexpressing breast cancer. Ann Oncol. 18:977–984. 2007. View Article : Google Scholar : PubMed/NCBI | |
McCormack PL: Pertuzumab: A review of its use for first-line combination treatment of HER2-positive metastatic breast cancer. Drugs. 73:1491–1502. 2013. View Article : Google Scholar : PubMed/NCBI | |
Xia W, Mullin RJ, Keith BR, Liu LH, Ma H, Rusnak DW, Owens G, Alligood KJ and Spector NL: Anti-tumor activity of GW572016: A dual tyrosine kinase inhibitor blocks EGF activation of EGFR/erbB2 and downstream Erk1/2 and AKT pathways. Oncogene. 21:6255–6263. 2002. View Article : Google Scholar : PubMed/NCBI | |
Hegde PS, Rusnak D, Bertiaux M, Alligood K, Strum J, Gagnon R and Gilmer TM: Delineation of molecular mechanisms of sensitivity to lapatinib in breast cancer cell lines using global gene expression profiles. Mol Cancer Ther. 6:1629–1640. 2007. View Article : Google Scholar : PubMed/NCBI | |
Rabindran SK, Discafani CM, Rosfjord EC, Baxter M, Floyd MB, Golas J, Hallett WA, Johnson BD, Nilakantan R, Overbeek E, et al: Antitumor activity of HKI-272, an orally active, irreversible inhibitor of the HER-2 tyrosine kinase. Cancer Res. 64:3958–3965. 2004. View Article : Google Scholar : PubMed/NCBI | |
Mohd Nafi SN, Generali D, Kramer-Marek G, Gijsen M, Strina C, Cappelletti M, Andreis D, Haider S, Li JL, Bridges E, et al: Nuclear HER4 mediates acquired resistance to trastuzumab and is associated with poor outcome in HER2 positive breast cancer. Oncotarget. 5:5934–5949. 2014. View Article : Google Scholar : PubMed/NCBI | |
Kourie HR, Chaix M, Gombos A, Aftimos P and Awada A: Pharmacodynamics, pharmacokinetics and clinical efficacy of neratinib in HER2-positive breast cancer and breast cancer with HER2 mutations. Expert Opin Drug Metab Toxicol. 12:947–957. 2016. View Article : Google Scholar : PubMed/NCBI | |
Borges VF, Ferrario C, Aucoin N, Falkson C, Khan Q, Krop I, Welch S, Conlin A, Chaves J, Bedard PL, et al: Tucatinib combined with Ado-trastuzumab emtansine in advanced ERBB2/HER2-positive metastatic breast cancer: A phase 1b clinical trial. JAMA Oncol. 4:1214–1220. 2018. View Article : Google Scholar : PubMed/NCBI | |
Kulukian A, Lee P, Taylor J, Rosler R, de Vries P, Watson D, Forero-Torres A and Peterson S: Preclinical activity of HER2-selective tyrosine kinase inhibitor tucatinib as a single agent or in combination with trastuzumab or docetaxel in solid tumor models. Mol Cancer Ther. 19:976–987. 2020. View Article : Google Scholar : PubMed/NCBI | |
Murthy RK, Loi S, Okines A, Paplomata E, Hamilton E, Hurvitz SA, Lin NU, Borges V, Abramson V, Anders C, et al: Tucatinib, trastuzumab, and capecitabine for HER2-positive metastatic breast cancer. N Engl J Med. 382:597–609. 2020. View Article : Google Scholar | |
Junttila TT, Li G, Parsons K, Phillips GL and Sliwkowski MX: Trastuzumab-DM1 (T-DM1) retains all the mechanisms of action of trastuzumab and efficiently inhibits growth of lapatinib insensitive breast cancer. Breast Cancer Res Treat. 128:347–356. 2011. View Article : Google Scholar | |
Li G, Guo J, Shen BQ, Yadav DB, Sliwkowski MX, Crocker LM, Lacap JA and Phillips G: Mechanisms of acquired resistance to trastuzumab emtansine in breast cancer cells. Mol Cancer Ther. 17:1441–1453. 2018. View Article : Google Scholar : PubMed/NCBI | |
Nagai Y, Oitate M, Shiozawa H and Ando O: Comprehensive preclinical pharmacokinetic evaluations of trastuzumab deruxtecan (DS-8201a), a HER2-targeting antibody-drug conjugate, in cynomolgus monkeys. Xenobiotica. 49:1086–1096. 2019. View Article : Google Scholar | |
Ogitani Y, Aida T, Hagihara K, Yamaguchi J, Ishii C, Harada N, Soma M, Okamoto H, Oitate M, Arakawa S, et al: DS-8201a, A novel HER2-targeting ADC with a Novel DNA topoisomerase I inhibitor, demonstrates a promising antitumor efficacy with differentiation from T-DM1. Clin Cancer Res. 22:5097–5108. 2016. View Article : Google Scholar : PubMed/NCBI | |
Metzger-Filho O, Vora T and Awada A: Management of metastatic HER2-positive breast cancer progression after adjuvant trastuzumab therapy-current evidence and future trends. Expert Opin Investig Drugs. 19(Suppl 1): S31–S39. 2010. View Article : Google Scholar | |
Bonnet D and Dick JE: Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat Med. 3:730–737. 1997. View Article : Google Scholar : PubMed/NCBI | |
Kreso A and Dick JE: Evolution of the cancer stem cell model. Cell Stem Cell. 14:275–291. 2014. View Article : Google Scholar : PubMed/NCBI | |
Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ and Clarke MF: Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA. 100:3983–3988. 2003. View Article : Google Scholar : PubMed/NCBI | |
Kim YJ, Sung D, Oh E, Cho Y, Cho TM, Farrand L, Seo JH and Kim JY: Flubendazole overcomes trastuzumab resistance by targeting cancer stem-like properties and HER2 signaling in HER2-positive breast cancer. Cancer Lett. 412:118–130. 2018. View Article : Google Scholar | |
Seo AN, Lee HJ, Kim EJ, Jang MH, Kim YJ, Kim JH, Kim SW, Ryu HS, Park IA, Im SA, et al: Expression of breast cancer stem cell markers as predictors of prognosis and response to trastuzumab in HER2-positive breast cancer. Br J Cancer. 114:1109–1116. 2016. View Article : Google Scholar : PubMed/NCBI | |
Ricardo S, Vieira AF, Gerhard R, Leitão D, Pinto R, Cameselle-Teijeiro JF, Milanezi F, Schmitt F and Paredes J: Breast cancer stem cell markers CD44, CD24 and ALDH1: Expression distribution within intrinsic molecular subtype. J Clin Pathol. 64:937–946. 2011. View Article : Google Scholar : PubMed/NCBI | |
Li X, Lewis MT, Huang J, Gutierrez C, Osborne CK, Wu MF, Hilsenbeck SG, Pavlick A, Zhang X, Chamness GC, et al: Intrinsic resistance of tumorigenic breast cancer cells to chemotherapy. J Natl Cancer Inst. 100:672–679. 2008. View Article : Google Scholar : PubMed/NCBI | |
Bourguignon L: Matrix hyaluronan-CD44 interaction activates MicroRNA and LncRNA signaling associated with chemoresistance, invasion, and tumor progression. Front Oncol. 9:4922019. View Article : Google Scholar : PubMed/NCBI | |
Chen Y, Song J, Jiang Y, Yu C and Ma Z: Predictive value of CD44 and CD24 for prognosis and chemotherapy response in invasive breast ductal carcinoma. Int J Clin Exp Pathol. 8:11287–11295. 2015.PubMed/NCBI | |
Liu S, Cong Y, Wang D, Sun Y, Deng L, Liu Y, Martin-Trevino R, Shang L, McDermott SP, Landis MD, et al: Breast cancer stem cells transition between epithelial and mesenchymal states reflective of their normal counterparts. Stem Cell Reports. 2:78–91. 2014. View Article : Google Scholar : PubMed/NCBI | |
Oliveras-Ferraros C, Vazquez-Martin A, Martin-Castillo B, Cufí S, Del Barco S, Lopez-Bonet E, Brunet J and Menendez JA: Dynamic emergence of the mesenchymal CD44(pos)CD24(neg/low) phenotype in HER2-gene amplified breast cancer cells with de novo resistance to trastuzumab (Herceptin). Biochem Biophys Res Commun. 397:27–33. 2010. View Article : Google Scholar : PubMed/NCBI | |
Ginestier C, Hur MH, Charafe-Jauffret E, Monville F, Dutcher J, Brown M, Jacquemier J, Viens P, Kleer CG, Liu S, et al: ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome. Cell Stem Cell. 1:555–567. 2007. View Article : Google Scholar | |
Liu C, Qiang J, Deng Q, Xia J, Deng L, Zhou L, Wang D, He X, Liu Y, Zhao B, et al: ALDH1A1 activity in tumor-initiating cells remodels myeloid-derived suppressor cells to promote breast cancer progression. Cancer Res. 81:5919–5934. 2021. View Article : Google Scholar : PubMed/NCBI | |
Talukdar S, Bhoopathi P, Emdad L, Das S, Sarkar D and Fisher PB: Dormancy and cancer stem cells: An enigma for cancer therapeutic targeting. Adv Cancer Res. 141:43–84. 2019. View Article : Google Scholar : PubMed/NCBI | |
Duru N, Fan M, Candas D, Menaa C, Liu HC, Nantajit D, Wen Y, Xiao K, Eldridge A, Chromy BA, et al: HER2-associated radiore-sistance of breast cancer stem cells isolated from HER2-negative breast cancer cells. Clin Cancer Res. 18:6634–6647. 2012. View Article : Google Scholar : PubMed/NCBI | |
Shao J, Fan W, Ma B and Wu Y: Breast cancer stem cells expressing different stem cell markers exhibit distinct biological characteristics. Mol Med Rep. 14:4991–4998. 2016. View Article : Google Scholar : PubMed/NCBI | |
Barzegar Behrooz A, Syahir A and Ahmad S: CD133: Beyond a cancer stem cell biomarker. J Drug Target. 27:257–269. 2019. View Article : Google Scholar | |
Li Y, Chu J, Feng W, Yang M, Zhang Y, Zhang Y, Qin Y, Xu J, Li J, Vasilatos SN, et al: EPHA5 mediates trastuzumab resistance in HER2-positive breast cancers through regulating cancer stem cell-like properties. FASEB J. 33:4851–4865. 2019. View Article : Google Scholar : PubMed/NCBI | |
He X, Semenov M, Tamai K and Zeng X: LDL receptor-related proteins 5 and 6 in Wnt/beta-catenin signaling: Arrows point the way. Development. 131:1663–1677. 2004. View Article : Google Scholar : PubMed/NCBI | |
Wei B, Cao J, Tian JH, Yu CY, Huang Q, Yu JJ, Ma R, Wang J, Xu F and Wang LB: Mortalin maintains breast cancer stem cells stemness via activation of Wnt/GSK3β/β-catenin signaling pathway. Am J Cancer Res. 11:2696–2716. 2021. | |
Wu Y, Ginther C, Kim J, Mosher N, Chung S, Slamon D and Vadgama JV: Expression of Wnt3 activates Wnt/β-catenin pathway and promotes EMT-like phenotype in trastuzumab-resistant HER2-overexpressing breast cancer cells. Mol Cancer Res. 10:1597–1606. 2012. View Article : Google Scholar : PubMed/NCBI | |
Choi HJ, Jin S, Cho H, Won HY, An HW, Jeong GY, Park YU, Kim HY, Park MK, Son T, et al: CDK12 drives breast tumor initiation and trastuzumab resistance via WNT and IRS1-ErbB-PI3K signaling. EMBO Rep. 20:e480582019. View Article : Google Scholar : PubMed/NCBI | |
El Abbass KA, Abdellateif MS, Gawish AM, Zekri AN, Malash I and Bahnassy AA: The role of breast cancer stem cells and some related molecular biomarkers in metastatic and nonmetastatic breast cancer. Clin Breast Cancer. 20:e373–e384. 2020. View Article : Google Scholar : PubMed/NCBI | |
Shen Q and Reedijk M: Notch signaling and the breast cancer microenvironment. Adv Exp Med Biol. 1287:183–200. 2021. View Article : Google Scholar | |
Baker A, Wyatt D, Bocchetta M, Li J, Filipovic A, Green A, Peiffer DS, Fuqua S, Miele L, Albain KS and Osipo C: Notch-1-PTEN-ERK1/2 signaling axis promotes HER2+ breast cancer cell proliferation and stem cell survival. Oncogene. 37:4489–4504. 2018. View Article : Google Scholar : PubMed/NCBI | |
Pandya K, Wyatt D, Gallagher B, Shah D, Baker A, Bloodworth J, Zlobin A, Pannuti A, Green A, Ellis IO, et al: PKCα attenuates Jagged-1-mediated notch signaling in ErbB-2-positive breast cancer to reverse trastuzumab resistance. Clin Cancer Res. 22:175–186. 2016. View Article : Google Scholar | |
He M, Fu Y, Yan Y, Xiao Q, Wu H, Yao W, Zhao H, Zhao L, Jiang Q, Yu Z, et al: The Hedgehog signalling pathway mediates drug response of MCF-7 mammosphere cells in breast cancer patients. Clin Sci (Lond). 129:809–822. 2015. View Article : Google Scholar : PubMed/NCBI | |
Liu S, Duan X, Xu L, Ye J, Cheng Y, Liu Q, Zhang H, Zhang S, Zhu S, Li T and Liu Y: Nuclear Gli1 expression is associated with pathological complete response and event-free survival in HER2-positive breast cancer treated with trastuzumab-based neoadjuvant therapy. Tumour Biol. 37:4873–4881. 2016. View Article : Google Scholar | |
Gupta P, Gupta N, Fofaria NM, Ranjan A and Srivastava SK: HER2-mediated GLI2 stabilization promotes anoikis resistance and metastasis of breast cancer cells. Cancer Lett. 442:68–81. 2019. View Article : Google Scholar | |
Doheny D, Sirkisoon S, Carpenter RL, Aguayo NR, Regua AT, Anguelov M, Manore SG, Arrigo A, Jalboush SA, Wong GL, et al: Combined inhibition of JAK2-STAT3 and SMO-GLI1/tGLI1 pathways suppresses breast cancer stem cells, tumor growth, and metastasis. Oncogene. 39:6589–6605. 2020. View Article : Google Scholar : PubMed/NCBI | |
Guo Z, Guo A and Zhou C: Breast cancer stem cell-derived ANXA6-containing exosomes sustain paclitaxel resistance and cancer aggressiveness in breast cancer. Front Cell Dev Biol. 9:7187212021. View Article : Google Scholar : PubMed/NCBI | |
Yousefnia S, Seyed Forootan F, Seyed Forootan S, Nasr Esfahani MH, Gure AO and Ghaedi K: Mechanistic pathways of malignancy in breast cancer stem cells. Front Oncol. 10:4522020. View Article : Google Scholar : PubMed/NCBI | |
Zhao Q, Liu Y, Wang T, Yang Y, Ni H, Liu H, Guo Q, Xi T and Zheng L: MiR-375 inhibits the stemness of breast cancer cells by blocking the JAK2/STAT3 signaling. Eur J Pharmacol. 884:1733592020. View Article : Google Scholar : PubMed/NCBI | |
Hu Y, Guo R, Wei J, Zhou Y, Ji W, Liu J, Zhi X and Zhang J: Effects of PI3K inhibitor NVP-BKM120 on overcoming drug resistance and eliminating cancer stem cells in human breast cancer cells. Cell Death Dis. 6:e20202015. View Article : Google Scholar : PubMed/NCBI | |
Yang L, Shi P, Zhao G, Xu J, Peng W, Zhang J, Zhang G, Wang X, Dong Z, Chen F and Cui H: Targeting cancer stem cell pathways for cancer therapy. Signal Transduct Target Ther. 5:82020. View Article : Google Scholar : PubMed/NCBI | |
Xing F, Kobayashi A, Okuda H, Watabe M, Pai SK, Pandey PR, Hirota S, Wilber A, Mo YY, Moore BE, et al: Reactive astrocytes promote the metastatic growth of breast cancer stem-like cells by activating Notch signalling in brain. EMBO Mol Med. 5:384–396. 2013. View Article : Google Scholar : PubMed/NCBI | |
Zhou N, Zhang Y, Zhang X, Lei Z, Hu R, Li H, Mao Y, Wang X, Irwin DM, Niu G and Tan H: Exposure of tumor-associated macrophages to apoptotic MCF-7 cells promotes breast cancer growth and metastasis. Int J Mol Sci. 16:11966–11982. 2015. View Article : Google Scholar : PubMed/NCBI | |
Ko YS, Rugira T, Jin H, Joo YN and Kim HJ: Radiotherapy-resistant breast cancer cells enhance tumor progression by enhancing premetastatic niche formation through the HIF-1α-LOX. Axis Int J Mol Sci. 21:80272020. View Article : Google Scholar | |
Mao Y, Zhang Y, Qu Q, Zhao M, Lou Y, Liu J, huang O, Chen X, Wu J and Shen K: Cancer-associated fibroblasts induce trastuzumab resistance in HER2 positive breast cancer cells. Mol Biosyst. 11:1029–1040. 2015. View Article : Google Scholar : PubMed/NCBI | |
Brown Y, Hua S and Tanwar PS: Extracellular matrix-mediated regulation of cancer stem cells and chemoresistance. Int J Biochem Cell Biol. 109:90–104. 2019. View Article : Google Scholar : PubMed/NCBI | |
Liu J, Shen JX, Wu HT, Li XL, Wen XF, Du CW and Zhang GJ: Collagen 1A1 (COL1A1) promotes metastasis of breast cancer and is a potential therapeutic target. Discov Med. 25:211–223. 2018.PubMed/NCBI | |
Hanker AB, Estrada MV, Bianchini G, Moore PD, Zhao J, Cheng F, Koch JP, Gianni L, Tyson DR, Sánchez V, et al: Extracellular matrix/integrin signaling promotes resistance to combined inhibition of HER2 and PI3K in HER2+ Breast Cancer. Cancer Res. 77:3280–3292. 2017. View Article : Google Scholar : PubMed/NCBI | |
Jokela TA and LaBarge MA: Integration of mechanical and ECM microenvironment signals in the determination of cancer stem cell states. Curr Stem Cell Rep. 7:39–47. 2021. View Article : Google Scholar : PubMed/NCBI | |
Li F, Xu J and Liu S: Cancer stem cells and neovascularization. Cells. 10:10702021. View Article : Google Scholar : PubMed/NCBI | |
Hori A, Shimoda M, Naoi Y, Kagara N, Tanei T, Miyake T, Shimazu K, Kim SJ and Noguchi S: Vasculogenic mimicry is associated with trastuzumab resistance of HER2-positive breast cancer. Breast Cancer Res. 21:882019. View Article : Google Scholar : PubMed/NCBI | |
Bussolati B, Grange C, Sapino A and Camussi G: Endothelial cell differentiation of human breast tumour stem/progenitor cells. J Cell Mol Med. 13:309–319. 2009. View Article : Google Scholar | |
McClements L, Yakkundi A, Papaspyropoulos A, Harrison H, Ablett MP, Jithesh PV, McKeen HD, Bennett R, Donley C, Kissenpfennig A, et al: Targeting treatment-resistant breast cancer stem cells with FKBPL and its peptide derivative, AD-01, via the CD44 pathway. Clin Cancer Res. 19:3881–3893. 2013. View Article : Google Scholar : PubMed/NCBI | |
Li M, Pan M, You C, Zhao F, Wu D, Guo M, Xu H, Shi F, Zheng D and Dou J: MiR-7 reduces the BCSC subset by inhibiting XIST to modulate the miR-92b/Slug/ESA axis and inhibit tumor growth. Breast Cancer Res. 22:262020. View Article : Google Scholar : PubMed/NCBI | |
Sandiford OA, Donnelly RJ, El-Far MH, Burgmeyer LM, Sinha G, Pamarthi SH, Sherman LS, Ferrer AI, DeVore DE, Patel SA, et al: Mesenchymal stem cell-secreted extracellular vesicles instruct stepwise dedifferentiation of breast cancer cells into dormancy at the bone marrow perivascular region. Cancer Res. 81:1567–1582. 2021. View Article : Google Scholar : PubMed/NCBI | |
Kim SY, Kang JW, Song X, Kim BK, Yoo YD, Kwon YT and Lee YJ: Role of the IL-6-JAK1-STAT3-Oct-4 pathway in the conversion of non-stem cancer cells into cancer stem-like cells. Cell Signal. 25:961–969. 2013. View Article : Google Scholar : PubMed/NCBI | |
Rodríguez CE, Berardi DE, Abrigo M, Todaro LB, Bal de Kier Joffé ED and Fiszman GL: Breast cancer stem cells are involved in Trastuzumab resistance through the HER2 modulation in 3D culture. J Cell Biochem. 119:1381–1391. 2018. View Article : Google Scholar | |
Maroufi NF, Amiri M, Dizaji BF, Vahedian V, Akbarzadeh M, Roshanravan N, Haiaty S, Nouri M and Rashidi MR: Inhibitory effect of melatonin on hypoxia-induced vasculogenic mimicry via suppressing epithelial-mesenchymal transition (EMT) in breast cancer stem cells. Eur J Pharmacol. 881:1732822020. View Article : Google Scholar : PubMed/NCBI | |
Lee KM, Giltnane JM, Balko JM, Schwarz LJ, Guerrero-Zotano AL, Hutchinson KE, Nixon MJ, Estrada MV, Sánchez V, Sanders ME, et al: MYC and MCL1 cooperatively promote chemotherapy-resistant breast cancer stem cells via regulation of mitochondrial oxidative phosphorylation. Cell Metab. 26:633–647. 2017. View Article : Google Scholar : PubMed/NCBI | |
Park SJ, Kim JG, Kim ND, Yang K, Shim JW and Heo K: Estradiol, TGF-β1 and hypoxia promote breast cancer stemness and EMT-mediated breast cancer migration. Oncol Lett. 11:1895–1902. 2016. View Article : Google Scholar : PubMed/NCBI | |
Takegawa N, Nonagase Y, Yonesaka K, Sakai K, Maenishi O, Ogitani Y, Tamura T, Nishio K, Nakagawa K and Tsurutani J: DS-8201a, a new HER2-targeting antibody-drug conjugate incorporating a novel DNA topoisomerase I inhibitor, overcomes HER2-positive gastric cancer T-DM1 resistance. Int J Cancer. 141:1682–1689. 2017. View Article : Google Scholar : PubMed/NCBI | |
Chen K, Huang YH and Chen JL: Understanding and targeting cancer stem cells: Therapeutic implications and challenges. Acta Pharmacol Sin. 34:732–740. 2013. View Article : Google Scholar : PubMed/NCBI | |
Zhang YS, Yang C, Han L, Liu L and Liu YJ: Expression of BCRP/ABCG2 Protein in invasive breast cancer and response to neoadjuvant chemotherapy. Oncol Res Treat. 45:94–101. 2022. View Article : Google Scholar | |
Němcová-Fürstová V, Kopperová D, Balušíková K, Ehrlichová M, Brynychová V, Václavíková R, Daniel P, Souček P and Kovář J: Characterization of acquired paclitaxel resistance of breast cancer cells and involvement of ABC transporters. Toxicol Appl Pharm. 310:215–228. 2016. View Article : Google Scholar | |
Shi RZ, He YF, Wen J, Niu YN, Gao Y, Liu LH, Zhang XP, Wang Y, Zhang XL, Zhang HF, et al: Epithelial cell adhesion molecule promotes breast cancer resistance protein-mediated multidrug resistance in breast cancer by inducing partial epithelial-mesenchymal transition. Cell Biol Int. 45:1644–1653. 2021. View Article : Google Scholar : PubMed/NCBI | |
Ye X, Bai W, Zhu H, Zhang X, Chen Y, Wang L, Yang A, Zhao J and Jia L: MiR-221 promotes trastuzumab-resistance and metastasis in HER2-positive breast cancers by targeting PTEN. BMB Rep. 47:268–273. 2014. View Article : Google Scholar : | |
Li X, Li Y, Yu X and Jin F: Identification and validation of stemness-related lncRNA prognostic signature for breast cancer. J Transl Med. 18:3312020. View Article : Google Scholar : PubMed/NCBI | |
Müller V, Oliveira-Ferrer L, Steinbach B, Pantel K and Schwarzenbach H: Interplay of lncRNA H19/miR-675 and lncRNA NEAT1/miR-204 in breast cancer. Mol Oncol. 13:1137–1149. 2019. View Article : Google Scholar : PubMed/NCBI | |
Zheng A, Song X, Zhang L, Zhao L, Mao X, Wei M and Jin F: Long non-coding RNA LUCAT1/miR-5582-3p/TCF7L2 axis regulates breast cancer stemness via Wnt/β-catenin pathway. J Exp Clin Cancer Res. 38:3052019. View Article : Google Scholar | |
Xu S, Kong D, Chen Q, Ping Y and Pang D: Oncogenic long noncoding RNA landscape in breast cancer. Mol Cancer. 16:1292017. View Article : Google Scholar : PubMed/NCBI | |
Pickard MR and Williams GT: Regulation of apoptosis by long non-coding RNA GAS5 in breast cancer cells: Implications for chemotherapy. Breast Cancer Res Treat. 145:359–370. 2014. View Article : Google Scholar : PubMed/NCBI | |
Ye XM, Zhu HY, Bai WD, Wang T, Wang L, Chen Y, Yang AG and Jia LT: Epigenetic silencing of miR-375 induces trastuzumab resistance in HER2-positive breast cancer by targeting IGF1R. BMC Cancer. 14:1342014. View Article : Google Scholar : PubMed/NCBI | |
Liu S, Sun Y, Hou Y, Yang L, Wan X, Qin Y, Liu Y, Wang R, Zhu P, Teng Y and Liuet M: A novel lncRNA ROPM-mediated lipid metabolism governs breast cancer stem cell properties. J Hematol Oncol. 14:1782021. View Article : Google Scholar : PubMed/NCBI | |
Peng F, Wang JH, Fan WJ, Meng YT, Li MM, Li TT, Cui B, Wang HF, Zhao Y, An F, et al: Glycolysis gatekeeper PDK1 repro-grams breast cancer stem cells under hypoxia. Oncogene. 37:1062–1074. 2018. View Article : Google Scholar | |
Fox DB, Garcia N, McKinney BJ, Lupo R, Noteware LC, Newcomb R, Liu J, Locasale JW, Hirschey MD and Alvarez JV: NRF2 activation promotes the recurrence of dormant tumour cells through regulation of redox and nucleotide metabolism. Nat Metab. 2:318–334. 2020. View Article : Google Scholar : PubMed/NCBI | |
Najafi M, Mortezaee K and Majidpoor J: Cancer stem cell (CSC) resistance drivers. Life Sci. 234:1167812019. View Article : Google Scholar : PubMed/NCBI | |
Abad E, Graifer D and Lyakhovich A: DNA damage response and resistance of cancer stem cells. Cancer Lett. 474:106–117. 2020. View Article : Google Scholar : PubMed/NCBI | |
Oh KS, Nam AR, Bang JH, Seo HR, Kim JM, Yoon J, Kim TY and Oh DY: A synthetic lethal strategy using PARP and ATM inhibition for overcoming trastuzumab resistance in HER2-positive cancers. Oncogene. 41:3939–3952. 2022. View Article : Google Scholar : PubMed/NCBI | |
Wengner AM, Scholz A and Haendler B: Targeting DNA damage response in prostate and breast cancer. Int J Mol Sci. 21:82732020. View Article : Google Scholar : PubMed/NCBI | |
Torres VI, Godoy JA and Inestrosa NC: Modulating Wnt signaling at the root: Porcupine and Wnt acylation. Pharmacol Ther. 198:34–45. 2019. View Article : Google Scholar : PubMed/NCBI | |
Yang Y, Li X, Wang T, Guo Q, Xi T and Zheng L: Emerging agents that target signaling pathways in cancer stem cells. J Hematol Oncol. 13:602020. View Article : Google Scholar : PubMed/NCBI | |
Jang GB, Hong IS, Kim RJ, Lee SY, Park SJ, Lee ES, Park JH, Yun CH, Chung JU, Lee KJ, et al: Wnt/β-Catenin small-molecule inhibitor CWP232228 preferentially inhibits the growth of breast cancer stem-like cells. Cancer Res. 75:1691–1702. 2015. View Article : Google Scholar : PubMed/NCBI | |
Gurney A, Axelrod F, Bond CJ, Cain J, Chartier C, Donigan L, Fischer M, Chaudhari A, Ji M, Kapoun AM, et al: Wnt pathway inhibition via the targeting of Frizzled receptors results in decreased growth and tumorigenicity of human tumors. Proc Natl Acad Sci USA. 109:11717–11722. 2012. View Article : Google Scholar : PubMed/NCBI | |
Mu J, Hui T, Shao B, Li L, Du Z, Lu L, Ye L, Li S, Li Q, Xiao Q, et al: Dickkopf-related protein 2 induces G0/G1 arrest and apoptosis through suppressing Wnt/β-catenin signaling and is frequently methylated in breast cancer. Oncotarget. 8:39443–39459. 2017. View Article : Google Scholar : PubMed/NCBI | |
An SM, Ding Q, Zhang J, Xie J and Li L: Targeting stem cell signaling pathways for drug discovery: Advances in the Notch and Wnt pathways. Sci China Life Sci. 57:575–580. 2014. View Article : Google Scholar : PubMed/NCBI | |
Schott AF, Landis MD, Dontu G, Griffith KA, Layman RM, Krop I, Paskett LA, Wong H, Dobrolecki LE, Lewis MT, et al: Preclinical and clinical studies of gamma secretase inhibitors with docetaxel on human breast tumors. Clin Cancer Res. 19:1512–1524. 2013. View Article : Google Scholar : PubMed/NCBI | |
Takebe N, Nguyen D and Yang SX: Targeting notch signaling pathway in cancer: Clinical development advances and challenges. Pharmacol Ther. 141:140–149. 2014. View Article : Google Scholar : | |
Yen WC, Fischer MM, Axelrod F, Bond C, Cain J, Cancilla B, Henner WR, Meisner R, Sato A, Shah J, et al: Targeting Notch signaling with a Notch2/Notch3 antagonist (tarextumab) inhibits tumor growth and decreases tumor-initiating cell frequency. Clin Cancer Res. 21:2084–2095. 2015. View Article : Google Scholar : PubMed/NCBI | |
Huang J, Hu W, Hu L, Previs RA, Dalton HJ, Yang XY, Sun Y, McGuire M, Rupaimoole R, Nagaraja AS, et al: Dll4 inhibition plus aflibercept markedly reduces ovarian tumor growth. Mol Cancer Ther. 15:1344–1352. 2016. View Article : Google Scholar : PubMed/NCBI | |
McKeage MJ, Kotasek D, Markman B, Hidalgo M, Millward MJ, Jameson MB, Harris DL, Stagg RJ, Kapoun AM, Xu L, et al: Phase IB Trial of the Anti-cancer stem cell DLL4-binding agent demcizumab with pemetrexed and carboplatin as First-line treatment of metastatic non-squamous NSCLC. Target Oncol. 13:89–98. 2018. View Article : Google Scholar | |
Silkenstedt E, Arenas F, Colom-Sanmartí B, Xargay-Torrent S, Higashi M, Giró A, Rodriguez V, Fuentes P, Aulitzky WE, van der Kuip H, et al: Notch1 signaling in NOTCH1-mutated mantle cell lymphoma depends on delta-like ligand 4 and is a potential target for specific antibody therapy. J Exp Clin Cancer Res. 38:4462019. View Article : Google Scholar : PubMed/NCBI | |
Hui M, Cazet A, Nair R, Watkins DN, O'Toole SA and Swarbrick A: The Hedgehog signalling pathway in breast development, carcinogenesis and cancer therapy. Breast Cancer Res. 15:2032013. View Article : Google Scholar : PubMed/NCBI | |
Clara JA, Monge C, Yang Y and Takebe N: Targeting signalling pathways and the immune microenvironment of cancer stem cells-a clinical update. Nat Rev Clin Oncol. 17:204–232. 2020. View Article : Google Scholar | |
Bhateja P, Cherian M, Majumder S and Ramaswamy B: The hedgehog signaling pathway: A viable target in breast cancer. Cancers (Basel). 11:11262019. View Article : Google Scholar | |
Liu C, Qi M, Li L, Yuan Y, Wu X and Fu J: Natural cordycepin induces apoptosis and suppresses metastasis in breast cancer cells by inhibiting the Hedgehog pathway. Food Funct. 11:2107–2116. 2020. View Article : Google Scholar : PubMed/NCBI | |
Takebe N, Harris PJ, Warren RQ and Ivy SP: Targeting cancer stem cells by inhibiting Wnt, Notch, and Hedgehog pathways. Nat Rev Clin Oncol. 8:97–106. 2011. View Article : Google Scholar | |
Sorrentino G, Ruggeri N, Specchia V, Cordenonsi M, Mano M, Dupont S, Manfrin A, Ingallina E, Sommaggio R, Piazza S, et al: Metabolic control of YAP and TAZ by the mevalonate pathway. Nat Cell Biol. 16:357–366. 2014. View Article : Google Scholar : PubMed/NCBI | |
Haque S and Morris JC: Transforming growth factor-β: A therapeutic target for cancer. Hum Vaccin Immunother. 13:1741–1750. 2017. View Article : Google Scholar : PubMed/NCBI | |
Wang T, Fahrmann JF, Lee H, Li YJ, Tripathi SC, Yue C, Zhang C, Lifshitz V, Song J, Yuan Y, et al: JAK/STAT3-regulated fatty acid β-oxidation is critical for breast cancer stem cell self-renewal and chemoresistance. Cell Metab. 27:136–150. 2018. View Article : Google Scholar | |
Patel JS, Hu M, Sinha G, Walker ND, Sherman LS, Gallagher A and Rameshwar P: Non-coding RNA as mediators in microenvironment-breast cancer cell communication. Cancer Lett. 380:289–295. 2016. View Article : Google Scholar | |
Liu Y, Zhang P, Wu Q, Fang H, Wang Y, Xiao Y, Cong M, Wang T, He Y, Ma C, et al: Long non-coding RNA NR2F1-AS1 induces breast cancer lung metastatic dormancy by regulating NR2F1 and ΔNp63. Nat Commun. 12:52322021. View Article : Google Scholar | |
El Touny LH, Vieira A, Mendoza A, Khanna C, Hoenerhoff MJ and Green JE: Combined SFK/MEK inhibition prevents metastatic outgrowth of dormant tumor cells. J Clin Invest. 124:156–168. 2014. View Article : Google Scholar : | |
Puig I, Tenbaum SP, Chicote I, Arqués O, Martínez-Quintanilla J, Cuesta-Borrás E, Ramírez L, Gonzalo P, Soto A, Aguilar S, et al: TET2 controls chemoresistant slow-cycling cancer cell survival and tumor recurrence. J Clin Invest. 128:3887–3905. 2018. View Article : Google Scholar : PubMed/NCBI | |
Ma HP, Chang HL, Bamodu OA, Yadav VK, Huang TY, Wu A, Yeh CT, Tsai SH and Lee WH: Collagen 1A1 (COL1A1) is a reliable biomarker and putative therapeutic target for hepatocellular carcinogenesis and metastasis. Cancers (Basel). 11:7862019. View Article : Google Scholar : PubMed/NCBI | |
Chen Q, Xu L, Chen J, Yang Z, Liang C, Yang Y and Liu Z: Tumor vasculature normalization by orally fed erlotinib to modulate the tumor microenvironment for enhanced cancer nanomedicine and immunotherapy. Biomaterials. 148:69–80. 2017. View Article : Google Scholar : PubMed/NCBI | |
Kim JH, Verwilst P, Won M, Lee J, Sessler JL, Han J and Kim JS: A small molecule strategy for targeting cancer stem cells in hypoxic microenvironments and preventing tumorigenesis. J Am Chem Soc. 143:14115–14124. 2021. View Article : Google Scholar : PubMed/NCBI | |
Fico F and Santamaria-Martínez A: TGFBI modulates tumour hypoxia and promotes breast cancer metastasis. Mol Oncol. 14:3198–3210. 2020. View Article : Google Scholar : PubMed/NCBI | |
Jiang B, Zhu H, Tang L, Gao T, Zhou Y, Gong F, Tan Y, Xie L, Wu X and Li Y: Apatinib inhibits stem properties and malignant biological behaviors of breast cancer stem cells by blocking wnt/β-catenin signal pathway through down-regulating LncRNA ROR. Anticancer Agents Med Chem. 22:1723–1734. 2022. View Article : Google Scholar | |
Wu X, Zhang X, Sun L, Zhang H, Li L, Wang X, Li W, Su P, Hu J, Gao P and Zhou G: Progesterone negatively regulates BCRP in progesterone receptor-positive human breast cancer cells. Cell Physiol Biochem. 32:344–354. 2013. View Article : Google Scholar : PubMed/NCBI | |
Vannini I, Zoli W, Fabbri F, Ulivi P, Tesei A, Carloni S, Brigliadori G and Amadori D: Role of efflux Pump activity in Lapatinib/Caelyx combination in breast cancer cell lines. Anticancer Drugs. 20:918–925. 2009. View Article : Google Scholar : PubMed/NCBI | |
Karbownik A, Sobańska K, Płotek W, Grabowski T, Klupczynska A, Plewa S, Grześkowiak E and Szałek E: The influence of the coadministration of the p-glycoprotein modulator elacridar on the pharmacokinetics of lapatinib and its distribution in the brain and cerebrospinal fluid. Invest New Drugs. 38:574–583. 2020. View Article : Google Scholar : | |
Yi J, Chen S, Yi P, Luo J, Fang M, Du Y, Zou L and Fan P: Pyrotinib sensitizes 5-fluorouracil-resistant HER2 breast cancer cells to 5-fluorouracil. Oncol Res. 28:519–531. 2020. View Article : Google Scholar : PubMed/NCBI | |
Cufi S, Corominas-Faja B, Vazquez-Martin A, Oliveras-Ferraros C, Dorca J, Bosch-Barrera J, Martin-Castillo B and Menendez JA: Metformin-induced preferential killing of breast cancer initiating CD44+CD24-/low cells is sufficient to overcome primary resistance to trastuzumab in HER2+ human breast cancer xenografts. Oncotarget. 3:395–398. 2012. View Article : Google Scholar : PubMed/NCBI | |
Song CW, Lee H, Dings RP, Williams B, Powers J, Santos TD, Choi BH and Park HJ: Metformin kills and radiosensitizes cancer cells and preferentially kills cancer stem cells. Sci Rep. 2:3622012. View Article : Google Scholar : PubMed/NCBI | |
Singh JK, Simões BM, Clarke RB and Bundred NJ: Targeting IL-8 signalling to inhibit breast cancer stem cell activity. Expert Opin Ther Targets. 17:1235–1241. 2013. View Article : Google Scholar : PubMed/NCBI | |
Singh JK, Farnie G, Bundred NJ, Simões BM, Shergill A, Landberg G, Howell SJ and Clarke RB: Targeting CXCR1/2 significantly reduces breast cancer stem cell activity and increases the efficacy of inhibiting HER2 via HER2-dependent and -independent mechanisms. Clin Cancer Res. 19:643–656. 2013. View Article : Google Scholar | |
Kim HJ, Min A, Im SA, Jang H, Lee KH, Lau A, Lee M, Kim S, Yang Y, Kim J, et al: Anti-tumor activity of the ATR inhibitor AZD6738 in HER2 positive breast cancer cells. Int J Cancer. 140:109–119. 2017. View Article : Google Scholar |