miR-216b-5p promotes late apoptosis/necroptosis in trastuzumab-resistant SK-BR-3 cells

Istar Burcu Dolapci, (Ankara Üniversitesi, Biyoteknoloji Enstitüsü, Ankara, Türkiye)
Senem NOYAN, (Ankara Üniversitesi, Biyoteknoloji Enstitüsü, Ankara, Türkiye)
AYSEGUL YUCEL POLAT, (Ankara Üniversitesi, Biyoteknoloji Enstitüsü, Ankara, Türkiye)
Hakan Gurdal, (Ankara Üniversitesi, Tıp Fakültesi, Tıbbi Farmakoloji Anabilim Dalı, Ankara, Türkiye)
Bala Gur Dedeoglu (Ankara Üniversitesi, Biyoteknoloji Enstitüsü, Ankara, Türkiye)
Turkish Journal of Biology
8 0
Yıl: 2023 Cilt: 47 Sayı: 3 Sayfa Aralığı: 199 - 207 Metin Dili: İngilizce DOI: 10.55730/1300-0152.2655 İndeks Tarihi: 28-07-2023

miR-216b-5p promotes late apoptosis/necroptosis in trastuzumab-resistant SK-BR-3 cells

Öz:
Breast cancer is the most common cancer in women. The human epidermal growth factor receptor 2 (HER2) overexpressing subtype is related to poor prognosis with an aggressive phenotype and is reported as one of the most commonly seen subtypes. Trastuzumab is prevalently used as a treatment method for HER2+ breast cancer however, resistance to the drug frequently occurs following the treatment. MicroRNAs (miRNAs) are 19–23 nucleotide long small RNAs, which regulate gene expression at post- transcriptional level and studies show that there are differentially expressed miRNAs between drug sensitive and resistant groups, indicating that they might have some key roles in drug effectiveness. In this study, the aim is to find out the role of miR-216b-5p in trastuzumab resistance. SK-BR-3 cells developed resistance to trastuzumab after continuous treatment with increasing concentrations of the drug for 6 months. To investigate the effect of miR-216b-5p on cancer cell behavior in resistance state, proliferation, motility, and invasion capacities of these resistant cells were analyzed by xCELLigence real-time cell analyzer. To further understand the molecular mechanisms underlying the regulation of resistant SK-BR-3 cells by miR-216b-5p, microarray analysis was performed. Apoptosis analysis was also performed since the pathway enrichment analysis pointed out cell death related pathways. The proliferation, motility, and invasion capacities of the miR-216b-5p transfected resistant cells were diminished compared to sensitive cells. We identified the necroptosis signaling pathway as the result of microarray and pathway enrichment analyses. STAT1, IRF9, and PKR were validated as the significant elements of the pathway, which are also the putative targets of miR-216b-5p. Our apoptosis analysis showed that a significant amount of trastuzumab resistant SK-BR-3 cells entered to late apoptosis/necrosis stage upon miR- 216b-5p overexpression, it could be concluded that reexpression of miR-216b-5p sensitizes trastuzumab resistance through necroptosis in breast cancer.
Anahtar Kelime: miR-216b-5p breast cancer trastuzumab resistance

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  • Cataldo A, Romero-Cordoba S, Plantamura I, Cosentino G, Hidalgo-Miranda A et al. (2020). miR-302b as a combinatorial therapeutic approach to improve cisplatin chemotherapy efficacy in human triple-negative breast cancer.” Cancers 12 (8). https://doi.org/10.3390/cancers12082261
  • Cilek EE, Ozturk H, Gur Dedeoglu B (2017). Construction of miRNA-miRNA networks revealing the complexity of miRNA- mediated mechanisms in trastuzumab treated breast cancer cell lines.” PloS one 12 (10): e0185558. https://doi.org/10.1371/ journal.pone.0185558
  • Egeli U, Tezcan G, Cecener G, Tunca B, Demirdogen Sevinc E et al. (2016). miR-216b targets FGFR1 and confers sensitivity to dadiotherapy in pancreatic ductal adenocarcinoma patients without EGFR or KRAS mutation. Pancreas 45 (9): 1294–1302. https://doi.org/10.1097/MPA.0000000000000640
  • Ferino A, Miglietta G, Picco R, Vogel S, Wengel J et al. (2018). MicroRNA therapeutics: design of single-stranded miR- 216b mimics to target KRAS in pancreatic cancer cells. RNA Biology 15 (10): 1273–1285. https://doi.org/10.1080/15476286 .2018.1526536
  • Floros KV, Lochmann TL, Hu B, Monterrubio C, Hughes MT et al. (2018). Coamplification of miR-4728 protects HER2- amplified breast cancers from targeted therapy. Proceedings of the National Academy of Sciences of the United States of America 115 (11): E2594–2603. https://doi.org/10.1073/ pnas.1717820115
  • Fragomeni, SM, Sciallis A, Jeruss JS (2018). Molecular subtypes and local-regional control of breast cancer. Surgical Oncology Clinics of North America 27 (1): 95–120. https://doi. org/10.1016/j.soc.2017.08.005
  • Rao F, Jing-Shan T (2020). miR-126 reduces trastuzumab resistance by targeting PIK3R2 and regulating AKT/MTOR pathway in breast cancer cells. Journal of Cellular and Molecular Medicine 24 (13): 7600–7608. https://doi.org/10.1111/jcmm.15396
  • Gabos Z, Sinha R, Hanson J, Chauhan N, Hugh J et al, (2006). Prognostic significance of human epidermal growth factor receptor positivity for the development of brain metastasis after newly diagnosed breast cancer. Journal of clinical oncology : official journal of the American Society of Clinical Oncology 24 (36): 5658–5663. https://doi.org/10.1200/JCO.2006.07.0250
  • Goldhirsch A, Winer EP, Coates AS, Gelber RD, Piccart-Gebhart M et al. (2013). Personalizing the treatment of women with early breast cancer: Highlights of the St Gallen international expert consensus on the primary therapy of early breast cancer 2013. Annals of oncology : official journal of the European Society for Medical Oncology 24 (9): 2206–2223. https://doi. org/10.1093/annonc/mdt303
  • Goldman MJ, Craft B, Hastie M, Repečka K, McDade F et al. (2020). Visualizing and interpreting cancer genomics data via the xena platform. Nature Biotechnology 38 (6): 675–678. https://doi. org/10.1038/s41587-020-0546-8
  • Gong C, Yao Y, Wang Y, Liu B, Wu W et al. (2011). Up-regulation of miR-21 mediates resistance to trastuzumab therapy for breast cancer. The Journal of Biological Chemistry 286 (21): 19127– 19137. https://doi.org/10.1074/jbc.M110.216887
  • Grimaldi AM, Salvatore M, Incoronato M (2021). miRNA- based therapeutics in breast cancer: a systematic review. Frontiers in Oncology 11: 668464. https://doi.org/10.3389/ fonc.2021.668464
  • He J, Sun M, Geng H, Tian S (2019). Long non-coding RNA Linc00518 promotes paclitaxel resistance of the human prostate cancer by sequestering miR-216b-5p. Biology of the Cell 111 (2): 39–50. https://doi.org/10.1111/boc.201800054
  • He S, Liao B, Deng Y, Su C, Tuo J et al. (2017). miR-216b inhibits cell proliferation by targeting FOXM1 in cervical cancer cells and is associated with better prognosis. BMC Cancer 17 (1): 673. https://doi.org/10.1186/s12885-017-3650-5
  • Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ et al. (2003). Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics (Oxford, England) 4 (2): 249–264. https://doi.org/10.1093/ biostatistics/4.2.249
  • Kanehisa M, Goto S (2000). KEGG: Kyoto Encyclopedia of Genes and Genomes. Nucleic Acids Research 28 (1): 27–30. https:// doi.org/10.1093/nar/28.1.27
  • Leva GD, Croce CM (2010). Roles of small RNAs in tumor formation. Trends in Molecular Medicine 16 (6): 257–267. https://doi. org/10.1016/j.molmed.2010.04.001
  • Lin S, Gregory RI (2015). MicroRNA biogenesis pathways in cancer. Nature Reviews Cancer 15 (6): 321–333. https://doi. org/10.1038/nrc3932
  • Liu Y, Niu Z, Lin X, Tian Y (2017). miR-216b increases cisplatin sensitivity in ovarian cancer cells by targeting PARP1. Cancer Gene Therapy 24 (5): 208–214. https://doi.org/10.1038/cgt.2017.6
  • Luo L, Zhang Z, Qiu N, Ling L, Jia X et al. (2021). Disruption of FOXO3a-miRNA feedback inhibition of IGF2/IGF-1R/IRS1 signaling confers herceptin resistance in HER2-positive breast cancer. Nature Communications 12 (1): 2699. https://doi. org/10.1038/s41467-021-23052-23059
  • Jing M, Zhou Z (2020). Downregulation of miR-302b is associated with poor prognosis and tumor progression of breast cancer. Breast cancer (Tokyo, Japan) 27 (2): 291–298. https://doi. org/10.1007/s12282-019-01022-w
  • McComb S, Cessford E, Alturki NA, Joseph J, Shutinoski B et al. (2014). Type-I interferon signaling through ISGF3 complex is required for sustained Rip3 activation and necroptosis in macrophages. Proceedings of the National Academy of Sciences of the United States of America 111 (31): E3206-E3213. https:// doi.org/10.1073/pnas.1407068111
  • Menbari MN, Rahimi K, Ahmadi A, Elyasi A, Darvishi N et al. (2019). miR-216b-5p inhibits cell proliferation in human breast cancer by down-regulating HDAC8 expression. Life Sciences 237: 116945. https://doi.org/10.1016/j.lfs.2019.116945
  • Mendell, JT, Olson EN (2012). MicroRNAs in stress signaling and human disease. Cell 148 (6): 1172–1187. https://doi. org/10.1016/j.cell.2012.02.005
  • Noyan S, Andac Ozketen A, Gurdal H, Gur Dedeoglu B (2021). miR-770-5p regulates EMT and invasion in TNBC cells by targeting DNMT3A. Cellular Signalling 83: 109996. https:// doi.org/10.1016/j.cellsig.2021.109996
  • Oliveros JC (2007). VENNY. an interactive tool for comparing lists with venn diagrams. http://bioinfogp.cnb.csic.es/tools/venny?/ index.html. (June 29, 2013)
  • Jhih-Kai P, Cheng-Han L, Yao-Lung, Luo-Ping G, Hui-Chuan C et al. (2021). miR-211 determines brain metastasis specificity through SOX11/NGN2 axis in triple-negative breast cancer. Oncogene 40 (9): 1737–51. https://doi.org/10.1038/s41388- 021-01654-3
  • Pei, ML, Zong Xia Z, Ting S (2020). Dysregulation of lnc-SNHG1 and miR-216b-5p correlate with chemoresistance and indicate poor prognosis of serous epithelial ovarian cancer. Journal of Ovarian Research 13 (1): 144. https://doi.org/10.1186/s13048-020-00750-4
  • Perou CM, Sørlie T, Eisen MB, van de Rijn M, Jeffrey SS et al. (2000). Molecular portraits of human breast tumours. Nature 406 (6797): 747–752. https://doi.org/10.1038/35021093
  • Pohlmann PR, Mayer IA, Mernaugh R (2009). Resistance to trastuzumab in breast cancer. Clinical Cancer Research 15 (24): 7479–7491. https://doi.org/10.1158/1078-0432.CCR-09-0636
  • Slamon DJ, Godolphin W, Jones LA, Holt JA, Wong SG et al. (1989). Studies of the HER-2/Neu proto-oncogene in human breast and ovarian cancer. Science (New York, N.Y.) 244 (4905): 707– 712. https://doi.org/10.1126/science.2470152
  • Sørlie T, Perou CM, Tibshirani R, Aas T, Geisler S et al. (2001). Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proceedings of the National Academy of Sciences of the United States of America 98 (19): 10869–10874. https://doi.org/10.1073/pnas.191367098
  • Thapa RJ, Nogusa S, Chen P, Maki JL, Lerro A et al. (2013). Interferon- induced RIP1/RIP3-mediated necrosis requires PKR and is licensed by FADD and caspases. Proceedings of the National Academy of Sciences of the United States of America 110 (33): E3109-E3118. https://doi.org/10.1073/pnas.1301218110
  • Wang J, Duncan D, Shi Z, Zhang B (2013). WEB-Based GEne SeT AnaLysis Toolkit (WebGestalt): update 2013. Nucleic Acids Research 41 (Web Server issue): 77–83. https://doi. org/10.1093/nar/gkt439
  • Wang L, Wang Y, Du X, Yao Y, Wang L et al. (2019). miR-216b suppresses cell proliferation, migration, invasion, and epithelial-mesenchymal transition by regulating FOXM1 expression in human non-small cell lung cancer. OncoTargets and Therapy 12: 2999–3009. https://doi.org/10.2147/OTT. S202523
  • Wang P, Ke L, Cai C, Dong F (2022). LINC01578 affects the radiation resistance of lung cancer cells through regulating microRNA- 216b-5p/TBL1XR1 axis. Bioengineered 13 (4): 10721–10733. https://doi.org/10.1080/21655979.2022.2051881
  • Xing Z, Li S, Xing J, Yu G, Wanget G et al. (2022). Silencing of LINC01963 enhances the chemosensitivity of prostate cancer cells to docetaxel by targeting the miR-216b-5p/TrkB axis. Laboratory Investigation; a Journal of Technical Methods and Pathology 102 (6): 602–12. https://doi.org/10.1038/s41374- 022-00736-4
  • Yao Y, Li Q, Wang H (2018). miR-216b suppresses colorectal cancer proliferation, migration, and invasion by targeting SRPK1. OncoTargets and Therapy 11: 1671–81. https://doi. org/10.2147/OTT.S161835.
  • Zhang B, Kirov S, Snoddy J (2005). WebGestalt: an integrated system for exploring gene sets in various biological contexts. Nucleic acids research 33(Web Server issue): W741-8. https://doi. org/10.1093/nar/gki475.
  • Zhang Z, Zhang H, Li C, Xiang Q, Xuet L et al. (2021). Circulating microRNAs as indicators in the prediction of neoadjuvant chemotherapy response in luminal B breast cancer. Thoracic Cancer 12 (24): 3396–3406. https://doi.org/10.1111/1759- 7714.14219. Epub 2021 Nov 9.
  • Zhao Y, Simon R (2008). BRB-ArrayTools data archive for human cancer gene expression: A unique and efficient data sharing resource. Cancer Informatics 6: 9–15. https://doi.org/10.4137/ cin.s448. Epub 2008 Apr 21.
  • Zhou Y, Yuan Y, Li L, Wang X, Quan Y et al. (2021). HER2-intronic miR-4728-5p facilitates HER2 expression and accelerates cell proliferation and migration by targeting EBP1 in breast cancer. PloS one 16 (2): e0245832. https://doi.org/10.1371/journal. pone.0245832
  • Zou J, Kuang W, Hu J, Rao H (2017). miR-216b promotes cell growth and enhances chemosensitivity of colorectal cancer by suppressing PDZ-binding kinase. Biochemical and biophysical research communications 488 (2): 247–52. https://doi. org/10.1016/j.bbrc.2017.03.162
APA Dolapci I, Noyan S, YUCEL POLAT A, Gurdal H, Gur Dedeoglu B (2023). miR-216b-5p promotes late apoptosis/necroptosis in trastuzumab-resistant SK-BR-3 cells. , 199 - 207. 10.55730/1300-0152.2655
Chicago Dolapci Istar Burcu,Noyan Senem,YUCEL POLAT AYSEGUL,Gurdal Hakan,Gur Dedeoglu Bala miR-216b-5p promotes late apoptosis/necroptosis in trastuzumab-resistant SK-BR-3 cells. (2023): 199 - 207. 10.55730/1300-0152.2655
MLA Dolapci Istar Burcu,Noyan Senem,YUCEL POLAT AYSEGUL,Gurdal Hakan,Gur Dedeoglu Bala miR-216b-5p promotes late apoptosis/necroptosis in trastuzumab-resistant SK-BR-3 cells. , 2023, ss.199 - 207. 10.55730/1300-0152.2655
AMA Dolapci I,Noyan S,YUCEL POLAT A,Gurdal H,Gur Dedeoglu B miR-216b-5p promotes late apoptosis/necroptosis in trastuzumab-resistant SK-BR-3 cells. . 2023; 199 - 207. 10.55730/1300-0152.2655
Vancouver Dolapci I,Noyan S,YUCEL POLAT A,Gurdal H,Gur Dedeoglu B miR-216b-5p promotes late apoptosis/necroptosis in trastuzumab-resistant SK-BR-3 cells. . 2023; 199 - 207. 10.55730/1300-0152.2655
IEEE Dolapci I,Noyan S,YUCEL POLAT A,Gurdal H,Gur Dedeoglu B "miR-216b-5p promotes late apoptosis/necroptosis in trastuzumab-resistant SK-BR-3 cells." , ss.199 - 207, 2023. 10.55730/1300-0152.2655
ISNAD Dolapci, Istar Burcu vd. "miR-216b-5p promotes late apoptosis/necroptosis in trastuzumab-resistant SK-BR-3 cells". (2023), 199-207. https://doi.org/10.55730/1300-0152.2655
APA Dolapci I, Noyan S, YUCEL POLAT A, Gurdal H, Gur Dedeoglu B (2023). miR-216b-5p promotes late apoptosis/necroptosis in trastuzumab-resistant SK-BR-3 cells. Turkish Journal of Biology, 47(3), 199 - 207. 10.55730/1300-0152.2655
Chicago Dolapci Istar Burcu,Noyan Senem,YUCEL POLAT AYSEGUL,Gurdal Hakan,Gur Dedeoglu Bala miR-216b-5p promotes late apoptosis/necroptosis in trastuzumab-resistant SK-BR-3 cells. Turkish Journal of Biology 47, no.3 (2023): 199 - 207. 10.55730/1300-0152.2655
MLA Dolapci Istar Burcu,Noyan Senem,YUCEL POLAT AYSEGUL,Gurdal Hakan,Gur Dedeoglu Bala miR-216b-5p promotes late apoptosis/necroptosis in trastuzumab-resistant SK-BR-3 cells. Turkish Journal of Biology, vol.47, no.3, 2023, ss.199 - 207. 10.55730/1300-0152.2655
AMA Dolapci I,Noyan S,YUCEL POLAT A,Gurdal H,Gur Dedeoglu B miR-216b-5p promotes late apoptosis/necroptosis in trastuzumab-resistant SK-BR-3 cells. Turkish Journal of Biology. 2023; 47(3): 199 - 207. 10.55730/1300-0152.2655
Vancouver Dolapci I,Noyan S,YUCEL POLAT A,Gurdal H,Gur Dedeoglu B miR-216b-5p promotes late apoptosis/necroptosis in trastuzumab-resistant SK-BR-3 cells. Turkish Journal of Biology. 2023; 47(3): 199 - 207. 10.55730/1300-0152.2655
IEEE Dolapci I,Noyan S,YUCEL POLAT A,Gurdal H,Gur Dedeoglu B "miR-216b-5p promotes late apoptosis/necroptosis in trastuzumab-resistant SK-BR-3 cells." Turkish Journal of Biology, 47, ss.199 - 207, 2023. 10.55730/1300-0152.2655
ISNAD Dolapci, Istar Burcu vd. "miR-216b-5p promotes late apoptosis/necroptosis in trastuzumab-resistant SK-BR-3 cells". Turkish Journal of Biology 47/3 (2023), 199-207. https://doi.org/10.55730/1300-0152.2655
Sayfa Oluşturulma Tarihi
24-04-2024 8:38

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