Loss of CD24 promotes radiation‑ and chemo‑resistance by inducing stemness properties associated with a hybrid E/M state in breast cancer cells

Bontemps,Isaline; Lallemand,Celine; Biard,Denis; Dechamps,Nathalie; Kortulewski,Thierry; Bourneuf,Emmanuelle; Siberchicot,Capucine; Boussin,François; Chevillard,Sylvie; Campalans,Anna; Lebeau,Jerome

doi:10.3892/or.2022.8441

Loss of CD24 promotes radiation‑ and chemo‑resistance by inducing stemness properties associated with a hybrid E/M state in breast cancer cells

Authors:
- Isaline Bontemps
- Celine Lallemand
- Denis Biard
- Nathalie Dechamps
- Thierry Kortulewski
- Emmanuelle Bourneuf
- Capucine Siberchicot
- François Boussin
- Sylvie Chevillard
- Anna Campalans
- Jerome Lebeau
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Affiliations: Laboratory of Experimental Cancerology, Institute of Cellular and Molecular Radiobiology, Genetic Stability Stem Cells and Radiation, François Jacob Institute of Biology, French Alternative Energies and Atomic Energy Commission (CEA), Paris University and Paris‑Saclay University, F‑92265 Fontenay‑aux‑Roses, France, Unit of Prion Disorders and Related Infectious Agents, François Jacob Institute of Biology, CEA, Paris‑Saclay University, F‑92265 Fontenay‑aux‑Roses, France, Laboratory of Radiopathology, Institute of Cellular and Molecular Radiobiology, Genetic Stability Stem Cells and Radiation, François Jacob Institute of Biology, CEA, French National Health and Medical Research Institute U1274, Paris University and Paris‑Saclay University, F‑92265 Fontenay‑aux‑Roses, France
Published online on: November 7, 2022 https://doi.org/10.3892/or.2022.8441
Article Number: 4
Copyright: © Bontemps et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

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Abstract

Cancer stem cells (CSCs) serve an essential role in failure of conventional antitumor therapy. In breast cancer, CD24^‑/low/CD44⁺ phenotype and high aldehyde dehydrogenase activity are associated with CSC subtypes. Furthermore, CD24^‑/low/CD44⁺ pattern is also characteristic of mesenchymal cells generated by epithelial‑mesenchymal transition (EMT). CD24 is a surface marker expressed in numerous types of tumor, however, its biological functions and role in cancer progression and treatment resistance remain poorly documented. Loss of CD24 expression in breast cancer cells is associated with radiation resistance and control of oxidative stress. Reactive oxygen species (ROS) mediate the effects of anticancer drugs as well as ionizing radiation; therefore, the present study investigated if CD24 mediates radiation‑ and chemo‑resistance of breast cancer cells. Using a HMLE breast cancer cell model, CD24 expression has been artificially modulated and it was observed that loss of CD24 expression induced stemness properties associated with acquisition of a hybrid E/M phenotype. CD24^‑/low cells were more radiation‑ and chemo‑resistant than CD24⁺ cells. The resistance was associated with lower levels of ROS; CD24 controlled ROS levels via regulation of mitochondrial function independently of antioxidant activity. Together, these results suggested a key role of CD24 in de‑differentiation of breast cancer cells and promoting acquisition of therapeutic resistance properties.

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1	Marusyk A, Almendro V and Polyak K: Intra-tumour heterogeneity: A looking glass for cancer? Nat Rev Cancer. 12:323–334. 2012. View Article : Google Scholar : PubMed/NCBI
2	Pece S, Tosoni D, Confalonieri S, Mazzarol G, Vecchi M, Ronzoni S, Bernard L, Viale G, Pelicci PG and Di Fiore PP: Biological and molecular heterogeneity of breast cancers correlates with their cancer stem cell content. Cell. 140:62–73. 2010. View Article : Google Scholar : PubMed/NCBI
3	Batlle E and Clevers H: Cancer stem cells revisited. Nat Med. 23:1124–1134. 2017. View Article : Google Scholar : PubMed/NCBI
4	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
5	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 : PubMed/NCBI
6	Hwang-Verslues WW, Kuo WH, Chang PH, Pan CC, Wang HH, Tsai ST, Jeng YM, Shew JY, Kung JT, Chen CH, et al: Multiple lineages of human breast cancer stem/progenitor cells identified by profiling with stem cell markers. PLoS One. 4:e83772009. View Article : Google Scholar : PubMed/NCBI
7	Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, Zhou AY, Brooks M, Reinhard F, Zhang CC, Shipitsin M, et al: The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell. 133:704–715. 2008. View Article : Google Scholar : PubMed/NCBI
8	Zhang R, Tu J and Liu S: Novel molecular regulators of breast cancer stem cell plasticity and heterogeneity. Semin Cancer Biol. 82:11–25. 2022. View Article : Google Scholar : PubMed/NCBI
9	Morel AP, Lièvre M, Thomas C, Hinkal G, Ansieau S and Puisieux A: Generation of breast cancer stem cells through epithelial-mesenchymal transition. PLoS One. 3:e28882008. View Article : Google Scholar : PubMed/NCBI
10	Konge J, Leteurtre F, Goislard M, Biard D, Morel-Altmeyer S, Vaurijoux A, Gruel G, Chevillard S and Lebeau J: Breast cancer stem cell-like cells generated during TGFβ-induced EMT are radioresistant. Oncotarget. 9:23519–23531. 2018. View Article : Google Scholar : PubMed/NCBI
11	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. 2013. View Article : Google Scholar : PubMed/NCBI
12	Pastushenko I and Blanpain C: EMT transition states during tumor progression and metastasis. Trends Cell Biol. 29:212–226. 2019. View Article : Google Scholar : PubMed/NCBI
13	Pasani S, Sahoo S and Jolly MK: Hybrid E/M phenotype(s) and stemness: A mechanistic connection embedded in network topology. J Clin Med. 10:602020. View Article : Google Scholar : PubMed/NCBI
14	Kröger C, Afeyan A, Mraz J, Eaton EN, Reinhardt F, Khodor YL, Thiru P, Bierie B, Ye X, Burge CB and Weinberg RA: Acquisition of a hybrid E/M state is essential for tumorigenicity of basal breast cancer cells. Proc Natl Acad Sci USA. 116:7353–7362. 2019. View Article : Google Scholar : PubMed/NCBI
15	Luo M, Brooks M and Wicha MS: Epithelial-mesenchymal plasticity of breast cancer stem cells: Implications for metastasis and therapeutic resistance. Curr Pharm Des. 21:1301–1310. 2015. View Article : Google Scholar : PubMed/NCBI
16	Phillips TM, McBride WH and Pajonk F: The response of CD24(−/low)/CD44+ breast cancer-initiating cells to radiation. J Natl Cancer Inst. 98:1777–1785. 2006. View Article : Google Scholar : PubMed/NCBI
17	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
18	Kamble D, Mahajan M, Dhat R and Sitasawad S: Keap1-Nrf2 pathway regulates ALDH and contributes to radioresistance in breast cancer stem cells. Cells. 10:832021. View Article : Google Scholar : PubMed/NCBI
19	Tanei T, Morimoto K, Shimazu K, Kim SJ, Tanji Y, Taguchi T, Tamaki Y and Noguchi S: Association of breast cancer stem cells identified by aldehyde dehydrogenase 1 expression with resistance to sequential Paclitaxel and epirubicin-base chemotherapy for breast cancers. Clin Cancer Res. 15:4234–4241. 2009. View Article : Google Scholar : PubMed/NCBI
20	Palomeras S, Ruiz-Martínez S and Puig T: Targeting breast cancer stem cells to overcome treatment resistance. Molecules. 23:21932018. View Article : Google Scholar : PubMed/NCBI
21	García-Heredia JM and Carnero A: Role of mitochondria in cancer stem cell resistance. Cells. 9:16932020. View Article : Google Scholar : PubMed/NCBI
22	Bensimon J, Altmeyer-Morel S, Benjelloun H, Chevillard S and Lebeau J: CD24(−/low) stem-like breast cancer marker defines the radiation-resistant cells involved in memorization and transmission of radiation-induced genomic instability. Oncogene. 32:251–258. 2013. View Article : Google Scholar : PubMed/NCBI
23	Bensimon J, Biard D, Paget V, Goislard M, Morel-Altmeyer S, Konge J, Chevillard S and Lebeau J: Forced extinction of CD24 stem-like breast cancer marker alone promotes radiation resistance through the control of oxidative stress. Mol Carcinog. 55:245–254. 2016. View Article : Google Scholar : PubMed/NCBI
24	Diehn M, Cho RW, Lobo NA, Kalisky T, Dorie MJ, Kulp AN, Qian D, Lam JS, Ailles LE, Wong M, et al: Association of reactive oxygen species levels and radioresistance in cancer stem cells. Nature. 458:780–783. 2009. View Article : Google Scholar : PubMed/NCBI
25	Lee JH, Kim SH, Lee ES and Kim YS: CD24 overexpression in cancer development and progression: A meta-analysis. Oncol Rep. 22:1149–1156. 2009.PubMed/NCBI
26	Altevogt P, Sammar M, Hüser L and Kristiansen G: Novel insights into the function of CD24: A driving force in cancer. Int J Cancer. 148:546–559. 2021. View Article : Google Scholar : PubMed/NCBI
27	Kristiansen G, Machado E, Bretz N, Rupp C, Winzer KJ, König AK, Moldenhauer G, Marmé F, Costa J and Altevogt P: Molecular and clinical dissection of CD24 antibody specificity by a comprehensive comparative analysis. Lab Invest. 90:1102–1116. 2010. View Article : Google Scholar : PubMed/NCBI
28	Weber E, Lehmann HP, Beck-Sickinger AG, Wawrzynczak EJ, Waibel R, Folkers G and Stahel RA: Antibodies to the protein core of the small cell lung cancer workshop antigen cluster-w4 and to the leucocyte workshop antigen CD24 recognize the same short protein sequence leucine-alanine-proline. Clin Exp Immunol. 93:279–285. 1993. View Article : Google Scholar : PubMed/NCBI
29	Riley PA: Free radicals in biology: Oxidative stress and the effects of ionizing radiation. Int J Radiat Biol. 65:27–33. 1994. View Article : Google Scholar : PubMed/NCBI
30	Mohiuddin M and Kasahara K: Cisplatin activates the growth inhibitory signaling pathways by enhancing the production of reactive oxygen species in non-small cell lung cancer carrying an EGFR exon 19 deletion. Cancer Genomics Proteomics. 18 (3 Suppl):S471–S486. 2021. View Article : Google Scholar : PubMed/NCBI
31	Mosca L, Ilari A, Fazi F, Assaraf YG and Colotti G: Taxanes in cancer treatment: Activity, chemoresistance and its overcoming. Drug Resist Updat. 54:1007422021. View Article : Google Scholar : PubMed/NCBI
32	Pan X, Zhang X, Sun H, Zhang J, Yan M and Zhang H: Autophagy inhibition promotes 5-fluorouraci-induced apoptosis by stimulating ROS formation in human non-small cell lung cancer A549 cells. PLoS One. 8:e566792013. View Article : Google Scholar : PubMed/NCBI
33	Elenbaas B, Spirio L, Koerner F, Fleming MD, Zimonjic DB, Donaher JL, Popescu NC, Hahn WC and Weinberg RA: Human breast cancer cells generated by oncogenic transformation of primary mammary epithelial cells. Genes Dev. 15:50–65. 2001. View Article : Google Scholar : PubMed/NCBI
34	Lombardo Y, de Giorgio A, Coombes CR, Stebbing J and Castellano L: Mammosphere formation assay from human breast cancer tissues and cell lines. J Vis Exp. 526712015.PubMed/NCBI
35	Biard DS, Despras E, Sarasin A and Angulo JF: Development of new EBV-based vectors for stable expression of small interfering RNA to mimick human syndromes: Application to NER gene silencing. Mol Cancer Res. 3:519–529. 2005. View Article : Google Scholar : PubMed/NCBI
36	Vert JP, Foveau N, Lajaunie C and Vandenbrouck Y: An accurate and interpretable model for siRNA efficacy prediction. BMC Bioinformatics. 7:5202006. View Article : Google Scholar : PubMed/NCBI
37	Meijering E, Dzyubachyk O and Smal I: Methods for cell and particle tracking. Methods Enzymol. 504:183–200. 2012. View Article : Google Scholar : PubMed/NCBI
38	Gorelik R and Gautreau A: Quantitative and unbiased analysis of directional persistence in cell migration. Nat Protoc. 9:1931–1943. 2014. View Article : Google Scholar : PubMed/NCBI
39	Pastushenko I, Brisebarre A, Sifrim A, Fioramonti M, Revenco T, Boumahdi S, Van Keymeulen A, Brown D, Moers V, Lemaire S, et al: Identification of the tumour transition states occurring during EMT. Nature. 556:463–468. 2018. View Article : Google Scholar : PubMed/NCBI
40	Yoh KE, Regunath K, Guzman A, Lee SM, Pfister NT, Akanni O, Kaufman LJ, Prives C and Prywes R: Repression of p63 and induction of EMT by mutant Ras in mammary epithelial cells. Proc Natl Acad Sci USA. 113:E6107–E6116. 2016. View Article : Google Scholar : PubMed/NCBI
41	Bocci F, Tripathi SC, Vilchez Mercedes SA, George JT, Casabar JP, Wong PK, Hanash SM, Levine H, Onuchic JN and Jolly MK: NRF2 activates a partial epithelial-mesenchymal transition and is maximally present in a hybrid epithelial/mesenchymal phenotype. Integr Biol (Camb). 11:251–263. 2019. View Article : Google Scholar : PubMed/NCBI
42	Kim D, Choi B, Ryoo I and Kwak MK: High NRF2 level mediates cancer stem cell-like properties of aldehyde dehydrogenase (ALDH)-high ovarian cancer cells: Inhibitory role of all-trans retinoic acid in ALDH/NRF2 signaling. Cell Death Dis. 9:8962018. View Article : Google Scholar : PubMed/NCBI
43	Tang JY, Ou-Yang F, Hou MF, Huang HW, Wang HR, Li KT, Fayyaz S, Shu CW and Chang HW: Oxidative stress-modulating drugs have preferential anticancer effects-involving the regulation of apoptosis, DNA damage, endoplasmic reticulum stress, autophagy, metabolism, and migration. Semin Cancer Biol. 58:109–117. 2019. View Article : Google Scholar : PubMed/NCBI
44	Peiris-Pagès M, Martinez-Outschoorn UE, Pestell RG, Sotgia F and Lisanti MP: Cancer stem cell metabolism. Breast Cancer Res. 18:552016. View Article : Google Scholar : PubMed/NCBI
45	Bhatia S, Monkman J, Blick T, Pinto C, Waltham M, Nagaraj SH and Thompson EW: Interrogation of phenotypic plasticity between epithelial and mesenchymal states in breast cancer. J Clin Med. 8:8932019. View Article : Google Scholar : PubMed/NCBI
46	Gupta PB, Fillmore CM, Jiang G, Shapira SD, Tao K, Kuperwasser C and Lander ES: Stochastic state transitions give rise to phenotypic equilibrium in populations of cancer cells. Cell. 146:633–644. 2011. View Article : Google Scholar : PubMed/NCBI
47	Ruscetti M, Dadashian EL, Guo W, Mulholland DJ, Park JW, Tran LM, Kobayashi N, Bianchi-Frias D, Xing Y, Nelson PS and Wu H: HDAC inhibition impedes epithelial-mesenchymal plasticity and suppresses metastatic, castration-resistant prostate cancer. Oncogene. 35:3781–3795. 2016. View Article : Google Scholar : PubMed/NCBI
48	Meyer MJ, Fleming JM, Ali MA, Pesesky MW, Ginsburg E and Vonderhaar BK: Dynamic regulation of CD24 and the invasive, CD44posCD24neg phenotype in breast cancer cell lines. Breast Cancer Res. 11:R822009. View Article : Google Scholar : PubMed/NCBI
49	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
50	Xia F and Powell SN: The molecular basis of radiosensitivity and chemosensitivity in the treatment of breast cancer. Semin Radiat Oncol. 12:296–304. 2002. View Article : Google Scholar : PubMed/NCBI
51	Luce A, Courtin A, Levalois C, Altmeyer-Morel S, Romeo PH, Chevillard S and Lebeau J: Death receptor pathways mediate targeted and non-targeted effects of ionizing radiations in breast cancer cells. Carcinogenesis. 30:432–439. 2009. View Article : Google Scholar : PubMed/NCBI
52	Longley DB, Harkin DP and Johnston PG: 5-fluorouracil: Mechanisms of action and clinical strategies. Nat Rev Cancer. 3:330–338. 2003. View Article : Google Scholar : PubMed/NCBI
53	Tchounwou PB, Dasari S, Noubissi FK, Ray P and Kumar S: Advances in our understanding of the molecular mechanisms of action of cisplatin in cancer therapy. J Exp Pharmacol. 13:303–328. 2021. View Article : Google Scholar : PubMed/NCBI
54	Abu Samaan TM, Samec M, Liskova A, Kubatka P and Büsselberg D: Paclitaxel's mechanistic and clinical effects on breast cancer. Biomolecules. 9:7892019. View Article : Google Scholar : PubMed/NCBI
55	Pinto CA, Widodo E, Waltham M and Thompson EW: Breast cancer stem cells and epithelial mesenchymal plasticity-implications for chemoresistance. Cancer Lett. 341:56–62. 2013. View Article : Google Scholar : PubMed/NCBI
56	Bierie B, Pierce SE, Kroeger C, Stover DG, Pattabiraman DR, Thiru P, Liu Donaher J, Reinhardt F, Chaffer CL, Keckesova Z and Weinberg RA: Integrin-β4 identifies cancer stem cell-enriched populations of partially mesenchymal carcinoma cells. Proc Natl Acad Sci USA. 114:E2337–E2346. 2017. View Article : Google Scholar : PubMed/NCBI
57	Unternaehrer JJ, Zhao R, Kim K, Cesana M, Powers JT, Ratanasirintrawoot S, Onder T, Shibue T, Weinberg RA and Daley GQ: The epithelial-mesenchymal transition factor SNAIL paradoxically enhances reprogramming. Stem Cell Reports. 3:691–698. 2014. View Article : Google Scholar : PubMed/NCBI
58	Gingold JA, Fidalgo M, Guallar D, Lau Z, Sun Z, Zhou H, Faiola F, Huang X, Lee DF, Waghray A, et al: A genome-wide RNAi screen identifies opposing functions of Snai1 and Snai2 on the Nanog dependency in reprogramming. Mol Cell. 56:140–152. 2014. View Article : Google Scholar : PubMed/NCBI
59	Ma SY, Park JH, Jung H, Ha SM, Kim Y, Park DH, Lee DH, Lee S, Chu IH, Jung SY, et al: Snail maintains metastatic potential, cancer stem-like properties, and chemoresistance in mesenchymal mouse breast cancer TUBO-P2J cells. Oncol Rep. 38:1867–1876. 2017. View Article : Google Scholar : PubMed/NCBI
60	Roca H, Hernandez J, Weidner S, McEachin RC, Fuller D, Sud S, Schumann T, Wilkinson JE, Zaslavsky A, Li H, et al: Transcription factors OVOL1 and OVOL2 induce the mesenchymal to epithelial transition in human cancer. PLoS One. 8:e767732013. View Article : Google Scholar : PubMed/NCBI
61	Wu RS, Hong JJ, Wu JF, Yan S, Wu D, Liu N, Liu QF, Wu QW, Xie YY, Liu YJ, et al: OVOL2 antagonizes TGF-β signaling to regulate epithelial to mesenchymal transition during mammary tumor metastasis. Oncotarget. 8:39401–39416. 2017. View Article : Google Scholar : PubMed/NCBI
62	Hong T, Watanabe K, Ta CH, Villarreal-Ponce A, Nie Q and Dai X: An Ovol2-Zeb1 mutual inhibitory circuit governs bidirectional and multi-step transition between epithelial and mesenchymal states. PLoS Comput Biol. 11:e10045692015. View Article : Google Scholar : PubMed/NCBI
63	Westcott JM, Camacho S, Nasir A, Huysman ME, Rahhal R, Dang TT, Riegel AT, Brekken RA and Pearson GW: ΔNp63-regulated epithelial-to-mesenchymal transition state heterogeneity confers a leader-follower relationship that drives collective invasion. Cancer Res. 80:3933–3944. 2020. View Article : Google Scholar : PubMed/NCBI
64	Jolly MK, Boareto M, Debeb BG, Aceto N, Farach-Carson MC, Woodward WA and Levine H: Inflammatory breast cancer: A model for investigating cluster-based dissemination. NPJ Breast Cancer. 3:1–8. 2017. View Article : Google Scholar : PubMed/NCBI
65	Ryoo I, Lee S and Kwak MK: Redox modulating NRF2: A potential mediator of cancer stem cell resistance. Oxid Med Cell Longev. 2016:24281532016. View Article : Google Scholar : PubMed/NCBI
66	Jia D, Tan Y, Liu H, Ooi S, Li L, Wright K, Bennett S, Addison CL and Wang L: Cardamonin reduces chemotherapy-enriched breast cancer stem-like cells in vitro and in vivo. Oncotarget. 7:771–785. 2016. View Article : Google Scholar : PubMed/NCBI
67	Vipparthi K, Hari K, Chakraborty P, Ghosh S, Patel AK, Ghosh A, Biswas NK, Sharan R, Arun P, Jolly MK and Singh S: Emergence of hybrid states of stem-like cancer cells correlates with poor prognosis in oral cancer. iScience. 25:1043172022. View Article : Google Scholar : PubMed/NCBI
68	Grosse-Wilde A, Kuestner RE, Skelton SM, MacIntosh E, d'Hérouël AF, Ertaylan G, Del Sol A, Skupin A and Huang S: Loss of inter-cellular cooperation by complete epithelial-mesenchymal transition supports favorable outcomes in basal breast cancer patients. Oncotarget. 9:20018–20033. 2018. View Article : Google Scholar : PubMed/NCBI
69	Gammon L, Biddle A, Heywood HK, Johannessen AC and Mackenzie IC: Sub-sets of cancer stem cells differ intrinsically in their patterns of oxygen metabolism. PLoS One. 8:e624932013. View Article : Google Scholar : PubMed/NCBI
70	Sciacovelli M and Frezza C: Metabolic reprogramming and epithelial-to-mesenchymal transition in cancer. FEBS J. 284:3132–3144. 2017. View Article : Google Scholar : PubMed/NCBI
71	Lee SY, Ju MK, Jeon HM, Lee YJ, Kim CH, Park HG, Han SI and Kang HS: Reactive oxygen species induce epithelial-mesenchymal transition, glycolytic switch, and mitochondrial repression through the Dlx-2/Snail signaling pathways in MCF-7 cells. Mol Med Rep. 20:2339–2346. 2019.PubMed/NCBI
72	Jia D, Park JH, Kaur H, Jung KH, Yang S, Tripathi S, Galbraith M, Deng Y, Jolly MK, Kaipparettu BA, et al: Towards decoding the coupled decision-making of metabolism and epithelial-to-mesenchymal transition in cancer. Br J Cancer. 124:1902–1911. 2021. View Article : Google Scholar : PubMed/NCBI
73	Fang X, Zheng P, Tang J and Liu Y: CD24: From A to Z. Cell Mol Immunol. 7:100–103. 2010. View Article : Google Scholar : PubMed/NCBI
74	Deng X, Apple S, Zhao H, Song J, Lee M, Luo W, Wu X, Chung D, Pietras RJ and Chang HR: CD24 expression and differential resistance to chemotherapy in triple-negative breast cancer. Oncotarget. 8:38294–38308. 2017. View Article : Google Scholar : PubMed/NCBI
75	Shen Y, Schmidt BUS, Kubitschke H, Morawetz EW, Wolf B, Käs JA and Losert W: Detecting heterogeneity in and between breast cancer cell lines. Cancer Converg. 4:12020. View Article : Google Scholar : PubMed/NCBI
76	Li W, Ma H, Zhang J, Zhu L, Wang C and Yang Y: Unraveling the roles of CD44/CD24 and ALDH1 as cancer stem cell markers in tumorigenesis and metastasis. Sci Rep. 7:138562017. View Article : Google Scholar : PubMed/NCBI
77	Gupta PB, Pastushenko I, Skibinski A, Blanpain C and Kuperwasser C: Phenotypic plasticity: Driver of cancer initiation, progression, and therapy resistance. Cell Stem Cell. 24:65–78. 2019. View Article : Google Scholar : PubMed/NCBI