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ORIGINAL RESEARCH

Ovo Like Zinc Finger 2 (OVOL2) Suppresses Breast Cancer Stem Cell Traits and Correlates with Immune Cells Infiltration

ORCID Icon, & ORCID Icon
Pages 211-227 | Published online: 04 Dec 2023

References

  • 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. doi:10.3322/caac.21492
  • Smalley M, Piggott L, Clarkson R. Breast cancer stem cells: obstacles to therapy. Cancer Lett. 2013;338(1):57–62.
  • Takebe N, Harris PJ, Warren RQ, Ivy SP. Targeting cancer stem cells by inhibiting Wnt, Notch, and Hedgehog pathways. Nat Rev Clin Oncol. 2011;8(2):97–106.
  • Jones RJ, Matsui W. Cancer stem cells: from bench to bedside. Biol Blood Marrow Transplant. 2007;13(Suppl 1):47–52.
  • Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci U S A. 2003;100(7):3983–3988.
  • Morrison BJ, Schmidt CW, Lakhani SR, Reynolds BA, Lopez JA. Breast cancer stem cells: implications for therapy of breast cancer. Breast Cancer Res. 2008;10(4):210.
  • Dontu G, Abdallah WM, Foley JM, et al. In vitro propagation and transcriptional profiling of human mammary stem/progenitor cells. Genes Dev. 2003;17(10):1253–1270.
  • Ponti D, Zaffaroni N, Capelli C, Daidone MG. Breast cancer stem cells: an overview. Eur J Cancer. 2006;42(9):1219–1224.
  • Kohandel M. Mesenchymal traits and cancer stem cells in mammospheres: chicken or egg? Cell Cycle. 2012;11(24):4498.
  • Larionova I, Cherdyntseva N, Liu T, Patysheva M, Rakina M, Kzhyshkowska J. Interaction of tumor-associated macrophages and cancer chemotherapy. Oncoimmunology. 2019;8(7):1596004. doi:10.1080/2162402X.2019.1596004
  • Nalio Ramos R, Missolo-Koussou Y, Gerber-Ferder Y, et al. Tissue-resident FOLR2(+) macrophages associate with CD8(+) T cell infiltration in human breast cancer. Cell. 2022;185(7):1189–1207 e1125. doi:10.1016/j.cell.2022.02.021
  • Ali HR, Chlon L, Pharoah PD, Markowetz F, Caldas C. Patterns of immune infiltration in breast cancer and their clinical implications: a gene-expression-based retrospective study. PLoS Med. 2016;13(12):e1002194.
  • Li B, Dai Q, Li L, Nair M, Mackay DR, Dai X. Ovol2, a mammalian homolog of Drosophila ovo: gene structure, chromosomal mapping, and aberrant expression in blind-sterile mice. Genomics. 2002;80(3):319–325.
  • Mackay DR, Hu M, Li B, Rheaume C, Dai X. The mouse Ovol2 gene is required for cranial neural tube development. Dev Biol. 2006;291(1):38–52.
  • Unezaki S, Horai R, Sudo K, Iwakura Y, Ito S. Ovol2/Movo, a homologue of Drosophila ovo, is required for angiogenesis, heart formation and placental development in mice. Genes Cells. 2007;12(6):773–785.
  • Watanabe K, Villarreal-Ponce A, Sun P, et al. Mammary morphogenesis and regeneration require the inhibition of EMT at terminal end buds by Ovol2 transcriptional repressor. Dev Cell. 2014;29(1):59–74.
  • Hayashi M, Shinozuka Y, Shigenobu S, et al. Conserved role of Ovo in germline development in mouse and Drosophila. Sci Rep. 2017;7:40056.
  • Ye GD, Sun GB, Jiao P, et al. OVOL2, an inhibitor of WNT signaling, reduces invasive activities of human and mouse cancer cells and is down-regulated in human colorectal tumors. Gastroenterology. 2016;150(3):659–671 e616.
  • Wu RS, Hong JJ, Wu JF, et al. OVOL2 antagonizes TGF-beta signaling to regulate epithelial to mesenchymal transition during mammary tumor metastasis. Oncotarget. 2017;8(24):39401–39416.
  • Roca H, Hernandez J, Weidner S, et al. Transcription factors OVOL1 and OVOL2 induce the mesenchymal to epithelial transition in human cancer. PLoS One. 2013;8(10):e76773.
  • Liu J, Wu Q, Wang Y, et al. Ovol2 induces mesenchymal-epithelial transition via targeting ZEB1 in osteosarcoma. Onco Targets Ther. 2018;11:2963–2973.
  • Hong T, Watanabe K, Ta CH, Villarreal-Ponce A, Nie Q, Dai X. An Ovol2-Zeb1 mutual inhibitory circuit governs bidirectional and multi-step transition between epithelial and mesenchymal states. Plos Comput Biol. 2015;11(11):e1004569.
  • Haensel D, Sun P, MacLean AL, et al. An Ovol2-Zeb1 transcriptional circuit regulates epithelial directional migration and proliferation. EMBO Rep. 2019;20(1):e46273.
  • Wang ZH, Li Z, Hu M, et al. Ovol2 gene inhibits the epithelial-to-mesenchymal transition in lung adenocarcinoma by transcriptionally repressing Twist1. Gene. 2017;600:1–8.
  • Bhat-Nakshatri P, Appaiah H, Ballas C, et al. SLUG/SNAI2 and tumor necrosis factor generate breast cells with CD44+/CD24- phenotype. BMC Cancer. 2010;10:411.
  • Creighton CJ, Li X, Landis M, et al. Residual breast cancers after conventional therapy display mesenchymal as well as tumor-initiating features. Proc Natl Acad Sci U S A. 2009;106(33):13820–13825.
  • Li T, Fu J, Zeng Z, et al. TIMER2.0 for analysis of tumor-infiltrating immune cells. Nucleic Acids Res. 2020;48(W1):W509–W514.
  • Jezequel P, Gouraud W, Ben Azzouz F, et al. bc-GenExMiner 4.5: new mining module computes breast cancer differential gene expression analyses. Database (Oxford). 2021;2021:baab007.
  • Chandrashekar DS, Karthikeyan SK, Korla PK, et al. UALCAN: an update to the integrated cancer data analysis platform. Neoplasia. 2022;25:18–27.
  • Vasaikar SV, Straub P, Wang J, Zhang B. LinkedOmics: analyzing multi-omics data within and across 32 cancer types. Nucleic Acids Res. 2018;46(D1):D956–D963.
  • Chen EY, Tan CM, Kou Y, et al. Enrichr: interactive and collaborative HTML5 gene list enrichment analysis tool. Bmc Bioinformatics. 2013;14:128.
  • Kuleshov MV, Jones MR, Rouillard AD, et al. Enrichr: a comprehensive gene set enrichment analysis web server 2016 update. Nucleic Acids Res. 2016;44(W1):W90–97.
  • Nagy A, Lanczky A, Menyhart O, Gyorffy B. Validation of miRNA prognostic power in hepatocellular carcinoma using expression data of independent datasets. Sci Rep. 2018;8(1):9227.
  • Cai WY, Wei TZ, Luo QC, et al. The Wnt-beta-catenin pathway represses let-7 microRNA expression through transactivation of Lin28 to augment breast cancer stem cell expansion. J Cell Sci. 2013;126(Pt 13):2877–2889.
  • Perou CM, Sorlie T, Eisen MB, et al. Molecular portraits of human breast tumours. Nature. 2000;406(6797):747–752.
  • Sorlie T, Tibshirani R, Parker J, et al. Repeated observation of breast tumor subtypes in independent gene expression data sets. Proc Natl Acad Sci U S A. 2003;100(14):8418–8423.
  • Cancer Genome Atlas N. Comprehensive molecular portraits of human breast tumours. Nature. 2012;490(7418):61–70.
  • Yin L, Duan JJ, Bian XW, Yu SC. Triple-negative breast cancer molecular subtyping and treatment progress. Breast Cancer Res. 2020;22(1):61.
  • Luo M, Clouthier SG, Deol Y, et al. Breast cancer stem cells: current advances and clinical implications. Methods Mol Biol. 2015;1293:1–49.
  • Al-Ejeh F, Smart CE, Morrison BJ, et al. Breast cancer stem cells: treatment resistance and therapeutic opportunities. Carcinogenesis. 2011;32(5):650–658.
  • Martin TA, Mason MD, Jiang WG. Tight junctions in cancer metastasis. Front Biosci (Landmark Ed). 2011;16:898–936.
  • Kohn KW, Zeeberg BM, Reinhold WC, Pommier Y. Gene expression correlations in human cancer cell lines define molecular interaction networks for epithelial phenotype. PLoS One. 2014;9(6):e99269.
  • Cao M, Nie W, Li J, et al. MicroRNA-495 induces breast cancer cell migration by targeting JAM-A. Protein Cell. 2014;5(11):862–872.
  • Raleigh DR, Marchiando AM, Zhang Y, et al. Tight junction-associated MARVEL proteins marveld3, tricellulin, and occludin have distinct but overlapping functions. Mol Biol Cell. 2010;21(7):1200–1213.
  • Warzecha CC, Sato TK, Nabet B, Hogenesch JB, Carstens RP. ESRP1 and ESRP2 are epithelial cell-type-specific regulators of FGFR2 splicing. Mol Cell. 2009;33(5):591–601.
  • Kikuchi M, Yamashita K, Waraya M, et al. Epigenetic regulation of ZEB1-RAB25/ESRP1 axis plays a critical role in phenylbutyrate treatment-resistant breast cancer. Oncotarget. 2016;7(2):1741–1753.
  • Mooney SM, Talebian V, Jolly MK, et al. The GRHL2/ZEB feedback loop-A key axis in the regulation of EMT in breast cancer. J Cell Biochem. 2017;118(9):2559–2570.
  • Riethdorf S, Frey S, Santjer S, et al. Diverse expression patterns of the EMT suppressor grainyhead-like 2 (GRHL2) in normal and tumour tissues. Int J Cancer. 2016;138(4):949–963.
  • Thiery JP, Acloque H, Huang RY, Nieto MA. Epithelial-mesenchymal transitions in development and disease. Cell. 2009;139(5):871–890.
  • Huber MA, Kraut N, Beug H. Molecular requirements for epithelial-mesenchymal transition during tumor progression. Curr Opin Cell Biol. 2005;17(5):548–558.
  • Mani SA, Guo W, Liao MJ, et al. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell. 2008;133(4):704–715.
  • Maqbool M, Bekele F, Fekadu G. Treatment strategies against triple-negative breast cancer: an updated review. Breast Cancer (Dove Med Press). 2022;14:15–24.
  • Wellner U, Schubert J, Burk UC, et al. The EMT-activator ZEB1 promotes tumorigenicity by repressing stemness-inhibiting microRNAs. Nat Cell Biol. 2009;11(12):1487–1495.
  • Singh A, Settleman J. EMT, cancer stem cells and drug resistance: an emerging axis of evil in the war on cancer. Oncogene. 2010;29(34):4741–4751.
  • Chiu WT, Huang YF, Tsai HY, et al. FOXM1 confers to epithelial-mesenchymal transition, stemness and chemoresistance in epithelial ovarian carcinoma cells. Oncotarget. 2015;6(4):2349–2365.
  • Dighe AS, Richards E, Old LJ, Schreiber RD. Enhanced in vivo growth and resistance to rejection of tumor cells expressing dominant negative IFN gamma receptors. Immunity. 1994;1(6):447–456.
  • Vesely MD, Kershaw MH, Schreiber RD, Smyth MJ. Natural innate and adaptive immunity to cancer. Annu Rev Immunol. 2011;29:235–271.
  • Harlin H, Meng Y, Peterson AC, et al. Chemokine expression in melanoma metastases associated with CD8+ T-cell recruitment. Cancer Res. 2009;69(7):3077–3085.
  • Araujo JM, Gomez AC, Aguilar A, et al. Effect of CCL5 expression in the recruitment of immune cells in triple negative breast cancer. Sci Rep. 2018;8(1):4899.
  • Luo N, Sugiura A, Balko JM. Therapeutic potential of DNA methyltransferase inhibitors with immune checkpoint inhibitor therapy in breast cancer. Cell Stress. 2018;2(3):69–71.
  • Hakulinen J, Meri S. Complement-mediated killing of microtumors in vitro. Am J Pathol. 1998;153(3):845–855.
  • Li F, Cheng Y, Lu J, Hu R, Wan Q, Feng H. Photodynamic therapy boosts anti-glioma immunity in mice: a dependence on the activities of T cells and complement C3. J Cell Biochem. 2011;112(10):3035–3043.
  • Su S, Liao J, Liu J, et al. Blocking the recruitment of naive CD4(+) T cells reverses immunosuppression in breast cancer. Cell Res. 2017;27(4):461–482.
  • Huang Y, Ma C, Zhang Q, et al. CD4+ and CD8+ T cells have opposing roles in breast cancer progression and outcome. Oncotarget. 2015;6(19):17462–17478.
  • Wu L, Saxena S, Goel P, Prajapati DR, Wang C, Singh RK. Breast Cancer Cell-Neutrophil Interactions Enhance Neutrophil Survival and Pro-Tumorigenic Activities. Cancers (Basel. 2020;12(10):e46273.
  • Ward R, Sims AH, Lee A, et al. Monocytes and macrophages, implications for breast cancer migration and stem cell-like activity and treatment. Oncotarget. 2015;6(16):14687–14699.
  • Palucka K, Coussens LM, O’Shaughnessy J. Dendritic cells, inflammation, and breast cancer. Cancer J. 2013;19(6):511–516.
  • Solis-Castillo LA, Garcia-Romo GS, Diaz-Rodriguez A, et al. Tumor-infiltrating regulatory T cells, CD8/Treg ratio, and cancer stem cells are correlated with lymph node metastasis in patients with early breast cancer. Breast Cancer. 2020;27(5):837–849.
  • Lappano R, Rigiracciolo DC, Belfiore A, Maggiolini M, De Francesco EM. Cancer associated fibroblasts: role in breast cancer and potential as therapeutic targets. Expert Opin Ther Targets. 2020;24(6):559–572.
  • Ingthorsson S, Sigurdsson V, Fridriksdottir A Jr., et al. Endothelial cells stimulate growth of normal and cancerous breast epithelial cells in 3D culture. BMC Res Notes. 2010;3:184.
  • Lee E, Pandey NB, Popel AS. Lymphatic endothelial cells support tumor growth in breast cancer. Sci Rep. 2014;4:5853.
  • Poncin A, Onesti CE, Josse C, et al. Immunity and breast cancer: focus on eosinophils. Biomedicines. 2021;9(9):3.
  • Gatault S, Legrand F, Delbeke M, Loiseau S, Capron M. Involvement of eosinophils in the anti-tumor response. Cancer Immunol Immunother. 2012;61(9):1527–1534.
  • Carretero R, Sektioglu IM, Garbi N, Salgado OC, Beckhove P, Hammerling GJ. Eosinophils orchestrate cancer rejection by normalizing tumor vessels and enhancing infiltration of CD8(+) T cells. Nat Immunol. 2015;16(6):609–617.