4,028
Views
54
CrossRef citations to date
0
Altmetric
Back Matter

PD-L1 is overexpressed on breast cancer stem cells through notch3/mTOR axis

, , , & ORCID Icon
Article: 1729299 | Received 12 May 2019, Accepted 06 Jan 2020, Published online: 03 Mar 2020

References

  • Siegel RL, Miller KD, Jemal A. Cancer statistics, 2019. CA Cancer J Clin. 2019;69:7-34.
  • Schmid P, Adams S, Rugo HS, Schneeweiss A, Barrios CH, Iwata H, Diéras V, Hegg R, Im S-A, Shaw Wright G, et al. Atezolizumab and Nab-Paclitaxel in advanced triple-negative breast cancer. N Engl J Med. 2018;379:2108–11. doi:10.1056/NEJMoa1809615.
  • Nicolini A, Giardino R, Carpi A, Ferrari P, Anselmi L, Colosimo S, Conte M, Fini M, Giavaresi G, Berti P, et al. Metastatic breast cancer: an updating. Biomed Pharmacother. 2006;60:548–556. doi:10.1016/j.biopha.2006.07.086.
  • 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. 2008;133:704–715. doi:10.1016/j.cell.2008.03.027.
  • Ghebeh H, Al-Alwan M. Do cancer stem cells have an immunomodulatory role different from the bulk of tumor cells? Carcinog Mutagen. 2013;S14:1–5.
  • Reiman JM, Knutson KL, Radisky DC. Immune promotion of epithelial-mesenchymal transition and generation of breast cancer stem cells. Cancer Res. 2010;70:3005–3008. doi:10.1158/0008-5472.CAN-09-4041.
  • Akalay I, Janji B, Hasmim M, Noman MZ, Andre F, De Cremoux P, Bertheau P, Badoual C, Vielh P, Larsen AK, et al. Epithelial-to-mesenchymal transition and autophagy induction in breast carcinoma promote escape from T cell-mediated lysis. Cancer Res. 2013;73:2418–2427. doi:10.1158/0008-5472.CAN-12-2432.
  • Dongre A, Rashidian M, Reinhardt F, Bagnato A, Keckesova Z, Ploegh HL, Weinberg RA. Epithelial-to-mesenchymal transition contributes to immunosuppression in breast carcinomas. Cancer Res. 2017;77:3982–3989. doi:10.1158/0008-5472.CAN-16-3292.
  • Alsuliman A, Colak D, Al-Harazi O, Fitwi H, Tulbah A, Al-Tweigeri T, Al-Alwan M, Ghebeh H. Bidirectional crosstalk between PD-L1 expression and epithelial to mesenchymal transition: significance in claudin-low breast cancer cells. Mol Cancer. 2015;14:149. doi:10.1186/s12943-015-0421-2.
  • Almozyan S, Colak D, Mansour F, Alaiya A, Al-Harazi O, Qattan A, Al-Mohanna F, Al-Alwan M, Ghebeh H. PD-L1 promotes OCT4 and Nanog expression in breast cancer stem cells by sustaining PI3K/AKT pathway activation. Int J Cancer. 2017;141:1402–1412. doi:10.1002/ijc.v141.7.
  • Lu H, Clauser KR, Tam WL, Frose J, Ye X, Eaton EN, Reinhardt F, Donnenberg VS, Bhargava R, Carr SA, et al. A breast cancer stem cell niche supported by juxtacrine signalling from monocytes and macrophages. Nat Cell Biol. 2014;16:1105–1117. doi:10.1038/ncb3041.
  • Chen CF, Dou XW, Liang YK, Lin HY, Bai JW, Zhang XX, Wei X-L, Li Y-C, Zhang G-J. Notch3 overexpression causes arrest of cell cycle progression by inducing Cdh1 expression in human breast cancer cells. Cell Cycle. 2016;15:432–440. doi:10.1080/15384101.2015.1127474.
  • Casey SC, Tong L, Li Y, Do R, Walz S, Fitzgerald KN, Gouw AM, Baylot V, Gutgemann I, Eilers M, et al. MYC regulates the antitumor immune response through CD47 and PD-L1. Science. 2016;352:227–231. doi:10.1126/science.aac9935.
  • Marzec M, Zhang Q, Goradia A, Raghunath PN, Liu X, Paessler M, Wang HY, Wysocka M, Cheng M, Ruggeri BA, et al. Oncogenic kinase NPM/ALK induces through STAT3 expression of immunosuppressive protein CD274 (PD-L1, B7-H1). Proc Natl Acad Sci U S A. 2008;105:20852–20857. doi:10.1073/pnas.0810958105.
  • Parsa AT, Waldron JS, Panner A, Crane CA, Parney IF, Barry JJ, Cachola KE, Murray JC, Tihan T, Jensen MC, et al. Loss of tumor suppressor PTEN function increases B7-H1 expression and immunoresistance in glioma. Nat Med. 2007;13:84–88. doi:10.1038/nm1517.
  • Lee Y, Shin JH, Longmire M, Wang H, Kohrt HE, Chang HY, Sunwoo JB. CD44+ cells in head and neck squamous cell carcinoma suppress T-cell-mediated immunity by selective constitutive and inducible expression of PD-L1. Clin Cancer Res. 2016;22:3571–3581. doi:10.1158/1078-0432.CCR-15-2665.
  • Yang YP, Wu K, Zhao ED, Li W, Shi L, Xie GC, JIANG B, WANG Y, LI R, ZHANG P, et al. B7-H1 enhances proliferation ability of gastric cancer stem-like cells as a receptor. Oncol Lett. 2015;9:1833–1838. doi:10.3892/ol.2015.2949.
  • Chan SM, Weng AP, Tibshirani R, Aster JC, Utz PJ. Notch signals positively regulate activity of the mTOR pathway in T-cell acute lymphoblastic leukemia. Blood. 2007;110:278–286. doi:10.1182/blood-2006-08-039883.
  • Schatton T, Murphy GF, Frank NY, Yamaura K, Waaga-Gasser AM, Gasser M, Zhan Q, Jordan S, Duncan LM, Weishaupt C, et al. Identification of cells initiating human melanomas. Nature. 2008;451:345–349. doi:10.1038/nature06489.
  • 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;100:3983–3988. doi:10.1073/pnas.0530291100.
  • 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. 2007;1:555–567. doi:10.1016/j.stem.2007.08.014.
  • Bocci F, Jolly MK, George JT, Levine H, Onuchic JN. A mechanism-based computational model to capture the interconnections among epithelial-mesenchymal transition, cancer stem cells and Notch-Jagged signaling. Oncotarget. 2018;9:29906–29920. doi:10.18632/oncotarget.v9i52.
  • Liu S, Cong Y, Wang D, Sun Y, Deng L, Liu Y, Martin-Trevino R, Shang L, McDermott S, Landis M, et al. Breast cancer stem cells transition between epithelial and mesenchymal states reflective of their normal counterparts. Stem Cell Rep. 2014;2:78–91. doi:10.1016/j.stemcr.2013.11.009.
  • Bolos V, Mira E, Martinez-Poveda B, Luxan G, Canamero M, Martinez AC, Mañes S, de la Pompa JL. Notch activation stimulates migration of breast cancer cells and promotes tumor growth. Breast Cancer Res. 2013;15:R54. doi:10.1186/bcr3447.
  • Farnie G, Clarke RB, Spence K, Pinnock N, Brennan K, Anderson NG, Bundred NJ. Novel cell culture technique for primary ductal carcinoma in situ: role of Notch and epidermal growth factor receptor signaling pathways. J Natl Cancer Inst. 2007;99:616–627. doi:10.1093/jnci/djk133.
  • Stylianou S, Clarke RB, Brennan K. Aberrant activation of notch signaling in human breast cancer. Cancer Res. 2006;66:1517–1525. doi:10.1158/0008-5472.CAN-05-3054.
  • Pan TT, Liu ZJ, Yin JY, Zhou TY, Liu JL, Qu HP. Notch signaling pathway was involved in regulating programmed cell death 1 expression during sepsis-induced immunosuppression. Mediat Inflamm. 2015;2015:1–9. doi:10.1155/2015/539841.
  • Mathieu M, Cotta-Grand N, Daudelin JF, Thebault P, Labrecque N. Notch signaling regulates PD-1 expression during CD8(+) T-cell activation. Immunol Cell Biol. 2013;91:82–88. doi:10.1038/icb.2012.53.
  • Hildebrand D, Uhle F, Sahin D, Krauser U, Weigand MA, Heeg K. The interplay of notch signaling and STAT3 in TLR-activated human primary monocytes. Front Cell Infect Microbiol. 2018;8:241. doi:10.3389/fcimb.2018.00241.
  • Castagnoli L, Cancila V, Cordoba-Romero SL, Faraci S, Talarico G, Belmonte B, Iorio MV, Milani M, Volpari T, Chiodoni C, et al. WNT signaling modulates PD-L1 expression in the stem cell compartment of triple-negative breast cancer. Oncogene. 2019;38:4047–4060. doi:10.1038/s41388-019-0700-2.
  • Hsu JM, Xia W, Hsu YH, Chan LC, Yu WH, Cha JH, Chen CT, Liao HW, Kuo CW, Khoo KH, et al. STT3-dependent PD-L1 accumulation on cancer stem cells promotes immune evasion. Nat Commun. 2018;9:1908. doi:10.1038/s41467-018-04313-6.
  • Shi W, Harris AL. Notch signaling in breast cancer and tumor angiogenesis: cross-talk and therapeutic potentials. J Mammary Gland Biol Neoplasia. 2006;11:41–52. doi:10.1007/s10911-006-9011-7.
  • Choy L, Hagenbeek TJ, Solon M, French D, Finkle D, Shelton A, Venook R, Brauer MJ, Siebel CW. Constitutive NOTCH3 signaling promotes the growth of basal breast cancers. Cancer Res. 2017;77:1439–1452. doi:10.1158/0008-5472.CAN-16-1022.
  • Ghebeh H, Tulbah A, Mohammed S, Elkum N, Bin Amer SM, Al-Tweigeri T, Dermime S. Expression of B7-H1 in breast cancer patients is strongly associated with high proliferative Ki-67-expressing tumor cells. Int J Cancer. 2007;121:751–758. doi:10.1002/(ISSN)1097-0215.
  • Yamaguchi N, Oyama T, Ito E, Satoh H, Azuma S, Hayashi M, Shimizu K, Honma R, Yanagisawa Y, Nishikawa A, et al. NOTCH3 signaling pathway plays crucial roles in the proliferation of ErbB2-negative human breast cancer cells. Cancer Res. 2008;68:1881–1888. doi:10.1158/0008-5472.CAN-07-1597.
  • Guo S, Liu M, Gonzalez-Perez RR. Role of Notch and its oncogenic signaling crosstalk in breast cancer. Biochim Biophys Acta. 2011;1815:197–213. doi:10.1016/j.bbcan.2010.12.002.
  • Lafkas D, Rodilla V, Huyghe M, Mourao L, Kiaris H, Fre S. Notch3 marks clonogenic mammary luminal progenitor cells in vivo. J Cell Biol. 2013;203:47–56. doi:10.1083/jcb.201307046.
  • Sansone P, Storci G, Giovannini C, Pandolfi S, Pianetti S, Taffurelli M, Santini D, Ceccarelli C, Chieco P, Bonafé M, et al. p66Shc/Notch-3 interplay controls self-renewal and hypoxia survival in human stem/progenitor cells of the mammary gland expanded in vitro as mammospheres. Stem Cells. 2007;25:807–815. doi:10.1634/stemcells.2006-0442.
  • Leontovich AA, Jalalirad M, Salisbury JL, Mills L, Haddox C, Schroeder M, Tuma A, Guicciardi ME, Zammataro L, Gambino MW, et al. NOTCH3 expression is linked to breast cancer seeding and distant metastasis. Breast Cancer Res. 2018;20:105. doi:10.1186/s13058-018-1020-0.
  • Hu S, Fu W, Li T, Yuan Q, Wang F, Lv G, Lv Y, Fan X, Shen Y, Lin F, et al.  Antagonism of EGFR and Notch limits resistance to EGFR inhibitors and radiation by decreasing tumor-initiating cell frequency. Sci Transl Med. 2017;9
  • Fu W, Lei C, Yu Y, Liu S, Li T, Lin F, Fan X, Shen Y, Ding M, Tang Y, et al. EGFR/Notch antagonists enhance the response to inhibitors of the PI3K-Akt pathway by decreasing tumor-initiating cell frequency. Clin Cancer Res. 2019;25:2835–2847. doi:10.1158/1078-0432.CCR-18-2732.
  • 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. 2015;21:2084–2095. doi:10.1158/1078-0432.CCR-14-2808.
  • Sugimoto K, Maekawa Y, Kitamura A, Nishida J, Koyanagi A, Yagita H, Kojima H, Chiba S, Shimada M, Yasutomo K, et al. Notch2 signaling is required for potent antitumor immunity in vivo. The Journal of Immunology. 2010;184:4673–4678. doi:10.4049/jimmunol.0903661.
  • Janghorban M, Xin L, Rosen JM, Zhang XH. Notch signaling as a regulator of the tumor immune response: to target or not to target? Front Immunol. 2018;9:1649.
  • Ayaz F, Osborne BA. Non-canonical notch signaling in cancer and immunity. Front Oncol. 2014;4:345. doi:10.3389/fonc.2014.00345.
  • Guest RV, Boulter L, Dwyer BJ, Kendall TJ, Man T-Y, Minnis-Lyons SE, Lu W-Y, Robson AJ, Gonzalez SF, Raven A, et al. Notch3 drives development and progression of cholangiocarcinoma. Proc Natl Acad Sci U S A. 2016;113:12250–12255. doi:10.1073/pnas.1600067113.
  • Pelullo M, Quaranta R, Talora C, Checquolo S, Cialfi S, Felli MP, Te Kronnie G, Borga C, Besharat ZM, Palermo R, et al. Notch3/Jagged1 circuitry reinforces notch signaling and sustains T-ALL. Neoplasia. 2014;16:1007–1017. doi:10.1016/j.neo.2014.10.004.
  • Boareto M, Jolly MK, Lu M, Onuchic JN, Clementi C, Ben-Jacob E. Jagged-delta asymmetry in Notch signaling can give rise to a sender/receiver hybrid phenotype. Proc Natl Acad Sci U S A. 2015;112:E402–9. doi:10.1073/pnas.1416287112.
  • Li D, Masiero M, Banham AH, Harris AL. The notch ligand JAGGED1 as a target for anti-tumor therapy. Front Oncol. 2014;4:254. doi:10.3389/fonc.2014.00254.
  • Jin S, Mutvei AP, Chivukula IV, Andersson ER, Ramskold D, Sandberg R, Lee KL, Kronqvist P, Mamaeva V, Östling P, et al. Non-canonical Notch signaling activates IL-6/JAK/STAT signaling in breast tumor cells and is controlled by p53 and IKKalpha/IKKbeta. Oncogene. 2013;32:4892–4902. doi:10.1038/onc.2012.517.
  • Fillmore CM, Kuperwasser C. Human breast cancer cell lines contain stem-like cells that self-renew, give rise to phenotypically diverse progeny and survive chemotherapy. Breast Cancer Res. 2008;10:R25. doi:10.1186/bcr1982.
  • Ghebeh H, Sleiman GM, Manogaran PS, Al-Mazrou A, Barhoush E, Al-Mohanna FH, Tulbah A, Al-Faqeeh K, Adra CN. Profiling of normal and malignant breast tissue show CD44high/CD24low phenotype as a predominant stem/progenitor marker when used in combination with Ep-CAM/CD49f markers. BMC Cancer. 2013;13:289. doi:10.1186/1471-2407-13-289.
  • Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods. 2001;25:402–408. doi:10.1006/meth.2001.1262.
  • Dontu G, Abdallah WM, Foley JM, Jackson KW, Clarke MF, Kawamura MJ, Wicha MS. In vitro propagation and transcriptional profiling of human mammary stem/progenitor cells. Gene Dev. 2003;17:1253–1270. doi:10.1101/gad.1061803.
  • Al-Alwan M, Olabi S, Ghebeh H, Barhoush E, Tulbah A, Al-Tweigeri T, Ajarim D, Adra C. Fascin is a key regulator of breast cancer invasion that acts via the modification of metastasis-associated molecules. PLoS One. 2011;6:e27339. doi:10.1371/journal.pone.0027339.