Proto-oncogene c-Myb potentiates cisplatin resistance of ovarian cancer cells by downregulating lncRNA NKILA and modulating cancer stemness and LIN28A-let7 axis.
Humans
Cisplatin
/ pharmacology
RNA, Long Noncoding
/ genetics
Female
Ovarian Neoplasms
/ genetics
Drug Resistance, Neoplasm
/ genetics
MicroRNAs
/ genetics
Cell Line, Tumor
Proto-Oncogene Proteins c-myb
/ metabolism
Proto-Oncogene Mas
Down-Regulation
RNA-Binding Proteins
/ metabolism
Neoplastic Stem Cells
/ metabolism
Gene Expression Regulation, Neoplastic
/ drug effects
Antineoplastic Agents
/ pharmacology
Signal Transduction
/ drug effects
Cell Proliferation
/ drug effects
Cisplatin resistance
LIN28A
Let-7
NKILA
Ovarian cancer
c-Myb
Journal
Journal of ovarian research
ISSN: 1757-2215
Titre abrégé: J Ovarian Res
Pays: England
ID NLM: 101474849
Informations de publication
Date de publication:
14 May 2024
14 May 2024
Historique:
received:
08
05
2023
accepted:
30
04
2024
medline:
15
5
2024
pubmed:
15
5
2024
entrez:
14
5
2024
Statut:
epublish
Résumé
Ovarian cancer is a major gynecological cancer that has poor prognosis associated mainly to its late diagnosis. Cisplatin is an FDA approved ovarian cancer therapy and even though the therapy is initially promising, the patients mostly progress to resistance against cisplatin. The underlying mechanisms are complex and not very clearly understood. Using two different paired cell lines representing cisplatin-sensitive and the cisplatin-resistant ovarian cancer cells, the ES2 and the A2780 parental and cisplatin-resistant cells, we show an elevated proto-oncogene c-Myb in resistant cells. We further show down-regulated lncRNA NKILA in resistant cells with its de-repression in resistant cells when c-Myb is silenced. NKILA negatively correlates with cancer cell and invasion but has no effect on cellular proliferation or cell cycle. C-Myb activates NF-κB signaling which is inhibited by NKILA. The cisplatin resistant cells are also marked by upregulated stem cell markers, particularly LIN28A and OCT4, and downregulated LIN28A-targeted let-7 family miRNAs. Whereas LIN28A and downregulated let-7s individually de-repress c-Myb-mediated cisplatin resistance, the ectopic expression of let-7s attenuates LIN28A effects, thus underlying a c-Myb-NKILA-LIN28A-let-7 axis in cisplatin resistance of ovarian cancer cells that needs to be further explored for therapeutic intervention.
Identifiants
pubmed: 38745302
doi: 10.1186/s13048-024-01429-w
pii: 10.1186/s13048-024-01429-w
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
102Subventions
Organisme : Bethune Program of Jilin University
ID : 2020B07
Organisme : Health Commission of Jilin Province Health Technology Capacity Improvement Project
ID : 2022LC123
Informations de copyright
© 2024. The Author(s).
Références
Stuart GC, Kitchener H, Bacon M, duBois A, Friedlander M, Ledermann J, Marth C, Thigpen T, Trimble E, participants of 4th Ovarian Cancer Consensus C et al. 2010 Gynecologic Cancer InterGroup (GCIG) consensus statement on clinical trials in ovarian cancer: report from the Fourth Ovarian Cancer Consensus Conference. Int J Gynecol Cancer 2011, 21(4):750-755.
Wang Y, Wang Z, Zhang Z, Wang H, Peng J, Hong L. Burden of ovarian cancer in China from 1990 to 2030: A systematic analysis and comparison with the global level. Front Public Health. 2023;11:1136596.
pubmed: 36860393
pmcid: 9969192
doi: 10.3389/fpubh.2023.1136596
Siegel RL, Miller KD, Wagle NS, Jemal A. Cancer statistics, 2023. CA Cancer J Clin. 2023;73(1):17–48.
pubmed: 36633525
doi: 10.3322/caac.21763
Doubeni CA, Doubeni AR, Myers AE. Diagnosis and management of ovarian cancer. Am Fam Phys. 2016;93(11):937–44.
Song M, Cui M, Liu K. Therapeutic strategies to overcome cisplatin resistance in ovarian cancer. Eur J Med Chem. 2022;232:114205.
pubmed: 35217497
doi: 10.1016/j.ejmech.2022.114205
Dasari S, Tchounwou PB. Cisplatin in cancer therapy: molecular mechanisms of action. Eur J Pharmacol. 2014;740:364–78.
pubmed: 25058905
pmcid: 4146684
doi: 10.1016/j.ejphar.2014.07.025
Zon A, Bednarek I. Cisplatin in ovarian cancer treatment-known limitations in therapy force new solutions. Int J Mol Sci. 2023;24(8):7585.
Helm CW, States JC. Enhancing the efficacy of cisplatin in ovarian cancer treatment - could arsenic have a role. J Ovarian Res. 2009;2:2.
pubmed: 19144189
pmcid: 2636805
doi: 10.1186/1757-2215-2-2
Li J, Feng Q, Kim JM, Schneiderman D, Liston P, Li M, Vanderhyden B, Faught W, Fung MF, Senterman M, et al. Human ovarian cancer and cisplatin resistance: possible role of inhibitor of apoptosis proteins. Endocrinology. 2001;142(1):370–80.
pubmed: 11145600
doi: 10.1210/endo.142.1.7897
Ortiz M, Wabel E, Mitchell K, Horibata S. Mechanisms of chemotherapy resistance in ovarian cancer. Cancer Drug Resist. 2022;5(2):304–16.
pubmed: 35800369
pmcid: 9255249
Marchetti C, De Felice F, Romito A, Iacobelli V, Sassu CM, Corrado G, Ricci C, Scambia G, Fagotti A. Chemotherapy resistance in epithelial ovarian cancer: Mechanisms and emerging treatments. Semin Cancer Biol. 2021;77:144–66.
pubmed: 34464704
doi: 10.1016/j.semcancer.2021.08.011
Wang J, Wu GS. Role of autophagy in cisplatin resistance in ovarian cancer cells. J Biol Chem. 2014;289(24):17163–73.
pubmed: 24794870
pmcid: 4059157
doi: 10.1074/jbc.M114.558288
Minerva, Bhat A, Verma S, Chander G, Jamwal RS, Sharma B, Bhat A, Katyal T, Kumar R, Shah R. Cisplatin-based combination therapy for cancer. J Cancer Res Ther. 2023;19(3):530–6.
pubmed: 37470570
doi: 10.4103/jcrt.jcrt_792_22
Wu Z, Jiang S, Chen Y. Non-coding RNA and Drug resistance in cholangiocarcinoma. Noncoding RNA Res. 2024;9(1):194–202.
pubmed: 38125756
doi: 10.1016/j.ncrna.2023.11.003
Abdi E, Latifi-Navid S, Panahi A: Long noncoding RNA polymorphisms in gynecological cancers. Per Med. 2023;21(1):59–68.
Usman M, Li A, Wu D, Qinyan Y, Yi LX, He G, Lu H. The functional role of lncRNAs as ceRNAs in both ovarian processes and associated diseases. Noncoding RNA Res. 2024;9(1):165–77.
pubmed: 38075201
doi: 10.1016/j.ncrna.2023.11.008
Bai L, Wang A, Zhang Y, Xu X, Zhang X. Knockdown of MALAT1 enhances chemosensitivity of ovarian cancer cells to cisplatin through inhibiting the Notch1 signaling pathway. Exp Cell Res. 2018;366(2):161–71.
pubmed: 29548748
doi: 10.1016/j.yexcr.2018.03.014
Wang Y, Wang X, Han L, Hu D. LncRNA MALAT1 Regulates the Progression and Cisplatin Resistance of Ovarian Cancer Cells via Modulating miR-1271-5p/E2F5 Axis. Cancer Manag Res. 2020;12:9999–10010.
pubmed: 33116856
pmcid: 7567574
doi: 10.2147/CMAR.S261979
Taheri M, Shoorei H, Tondro Anamag F, Ghafouri-Fard S, Dinger ME. LncRNAs and miRNAs participate in determination of sensitivity of cancer cells to cisplatin. Exp Mol Pathol. 2021;123:104602.
pubmed: 33422487
doi: 10.1016/j.yexmp.2021.104602
Liu S, Lei H, Luo F, Li Y, Xie L. The effect of lncRNA HOTAIR on chemoresistance of ovarian cancer through regulation of HOXA7. Biol Chem. 2018;399(5):485–97.
pubmed: 29455183
doi: 10.1515/hsz-2017-0274
Wang Y, Wang H, Song T, Zou Y, Jiang J, Fang L, Li P. HOTAIR is a potential target for the treatment of cisplatin-resistant ovarian cancer. Mol Med Rep. 2015;12(2):2211–6.
pubmed: 25824616
doi: 10.3892/mmr.2015.3562
Zhang Y, Ai H, Fan X, Chen S, Wang Y, Liu L. Knockdown of long non-coding RNA HOTAIR reverses cisplatin resistance of ovarian cancer cells through inhibiting miR-138-5p-regulated EZH2 and SIRT1. Biol Res. 2020;53(1):18.
pubmed: 32349783
pmcid: 7191713
doi: 10.1186/s40659-020-00286-3
Miao JT, Gao JH, Chen YQ, Chen H, Meng HY, Lou G: LncRNA ANRIL affects the sensitivity of ovarian cancer to cisplatin via regulation of let-7a/HMGA2 axis. Biosci Rep. 2019;39(7):BSR20182101.
Zhang D, Ding L, Li Y, Ren J, Shi G, Wang Y, Zhao S, Ni Y, Hou Y. Midkine derived from cancer-associated fibroblasts promotes cisplatin-resistance via up-regulation of the expression of lncRNA ANRIL in tumour cells. Sci Rep. 2017;7(1):16231.
pubmed: 29176691
pmcid: 5701200
doi: 10.1038/s41598-017-13431-y
Chen L, Wang J, Liu Q. Long noncoding RNAs as therapeutic targets to overcome chemoresistance in ovarian cancer. Front Cell Dev Biol. 2022;10:999174.
pubmed: 36105363
pmcid: 9464811
doi: 10.3389/fcell.2022.999174
Lipsick JS. The C-MYB story–is it definitive? Proc Natl Acad Sci U S A. 2010;107(40):17067–8.
pubmed: 20858731
pmcid: 2951432
doi: 10.1073/pnas.1012402107
Ciciro Y, Sala A. MYB oncoproteins: emerging players and potential therapeutic targets in human cancer. Oncogenesis. 2021;10(2):19.
pubmed: 33637673
pmcid: 7910556
doi: 10.1038/s41389-021-00309-y
Srivastava SK, Khan MA, Anand S, Zubair H, Deshmukh SK, Patel GK, Singh S, Andrews J, Wang B, Carter JE, et al. MYB interacts with androgen receptor, sustains its ligand-independent activation and promotes castration resistance in prostate cancer. Br J Cancer. 2022;126(8):1205–14.
pubmed: 34837075
doi: 10.1038/s41416-021-01641-1
Salomoni P, Perrotti D, Martinez R, Franceschi C, Calabretta B. Resistance to apoptosis in CTLL-2 cells constitutively expressing c-Myb is associated with induction of BCL-2 expression and Myb-dependent regulation of bcl-2 promoter activity. Proc Natl Acad Sci U S A. 1997;94(7):3296–301.
pubmed: 9096387
pmcid: 20363
doi: 10.1073/pnas.94.7.3296
Zhang XY, Li YF, Ma H, Gao YH. Regulation of MYB mediated cisplatin resistance of ovarian cancer cells involves miR-21-wnt signaling axis. Sci Rep. 2020;10(1):6893.
pubmed: 32327705
pmcid: 7181810
doi: 10.1038/s41598-020-63396-8
Tan WX, Sun G, Shangguan MY, Gui Z, Bao Y, Li YF, Jia ZH. Novel role of lncRNA CHRF in cisplatin resistance of ovarian cancer is mediated by miR-10b induced EMT and STAT3 signaling. Sci Rep. 2020;10(1):14768.
pubmed: 32901049
pmcid: 7478977
doi: 10.1038/s41598-020-71153-0
Liu R, Zeng Y, Zhou CF, Wang Y, Li X, Liu ZQ, Chen XP, Zhang W, Zhou HH. Long noncoding RNA expression signature to predict platinum-based chemotherapeutic sensitivity of ovarian cancer patients. Sci Rep. 2017;7(1):18.
pubmed: 28154416
pmcid: 5428368
doi: 10.1038/s41598-017-00050-w
Xu J, Wu J, Fu C, Teng F, Liu S, Dai C, Shen R, Jia X. Multidrug resistant lncRNA profile in chemotherapeutic sensitive and resistant ovarian cancer cells. J Cell Physiol. 2018;233(6):5034–43.
pubmed: 29219179
doi: 10.1002/jcp.26369
Vera O, Rodriguez-Antolin C, de Castro J, Karreth FA, Sellers TA. Ibanez de Caceres I: An epigenomic approach to identifying differential overlapping and cis-acting lncRNAs in cisplatin-resistant cancer cells. Epigenetics. 2018;13(3):251–63.
pubmed: 29436261
pmcid: 5997141
doi: 10.1080/15592294.2018.1436364
Li Q, Zhang J, Zhou J, Yang B, Liu P, Cao L, Jing L, Liu H. lncRNAs are novel biomarkers for differentiating between cisplatin-resistant and cisplatin-sensitive ovarian cancer. Oncol Lett. 2018;15(6):8363–70.
pubmed: 29805570
pmcid: 5950027
Hussen BM, Azimi T, Hidayat HJ, Taheri M, Ghafouri-Fard S. NF-KappaB interacting LncRNA: Review of its roles in neoplastic and non-neoplastic conditions. Biomed Pharmacother. 2021;139:111604.
pubmed: 33895520
doi: 10.1016/j.biopha.2021.111604
Funato T, Satou J, Kozawa K, Fujimaki S, Miura T, Kaku M. Use of c-myb antisense oligonucleotides to increase the sensitivity of human colon cancer cells to cisplatin. Oncol Rep. 2001;8(4):807–10.
pubmed: 11410788
Tian M, Tian D, Qiao X, Li J, Zhang L. Modulation of Myb-induced NF-kB -STAT3 signaling and resulting cisplatin resistance in ovarian cancer by dietary factors. J Cell Physiol. 2019;234(11):21126–34.
pubmed: 31037726
doi: 10.1002/jcp.28715
Xu QF, Tang YX, Wang X. LncRNA EBIC promoted proliferation, metastasis and cisplatin resistance of ovarian cancer cells and predicted poor survival in ovarian cancer patients. Eur Rev Med Pharmacol Sci. 2018;22(14):4440–7.
pubmed: 30058681
Li Z, Niu H, Qin Q, Yang S, Wang Q, Yu C, Wei Z, Jin Z, Wang X, Yang A, et al. lncRNA UCA1 Mediates Resistance to Cisplatin by Regulating the miR-143/FOSL2-Signaling Pathway in Ovarian Cancer. Mol Ther Nucleic Acids. 2019;17:92–101.
pubmed: 31234009
pmcid: 6595407
doi: 10.1016/j.omtn.2019.05.007
Wang DY, Li N, Cui YL. Long non-coding RNA CCAT1 sponges miR-454 to promote chemoresistance of ovarian cancer cells to cisplatin by regulation of surviving. Cancer Res Treat. 2020;52(3):798–814.
pubmed: 32124583
pmcid: 7373880
doi: 10.4143/crt.2019.498
Xiao L, Shi XY, Li ZL, Li M, Zhang MM, Yan SJ, Wei ZL. Downregulation of LINC01508 contributes to cisplatin resistance in ovarian cancer via the regulation of the Hippo-YAP pathway. J Gynecol Oncol. 2021;32(5): e77.
pubmed: 34132072
pmcid: 8362814
doi: 10.3802/jgo.2021.32.e77
Wu J, Ni X, Yu Z, Wu S, Liu Z. CRNDE inducing cisplatin resistance through SRSF1/TIA1 signaling pathway in ovarian cancer. Pathol Res Pract. 2022;235:153957.
pubmed: 35653925
doi: 10.1016/j.prp.2022.153957
Zhu Y, Yang L, Wang J, Li Y, Chen Y. SP1-induced lncRNA MCF2L-AS1 promotes cisplatin resistance in ovarian cancer by regulating IGF2BP1/IGF2/MEK/ERK axis. J Gynecol Oncol. 2022;33(6):e75.
pubmed: 36245227
pmcid: 9634094
doi: 10.3802/jgo.2022.33.e75
Yang T, Li S, Liu J, Yin D, Yang X, Tang Q. lncRNA-NKILA/NF-kappaB feedback loop modulates laryngeal cancer cell proliferation, invasion, and radioresistance. Cancer Med. 2018;7(5):2048–63.
pubmed: 29573243
pmcid: 5943486
doi: 10.1002/cam4.1405
Huang X, Yan Y, Gui A, Zhu S, Qiu S, Chen F, Liu W, Zuo J, Yang L: A Regulatory Loop Involving miR-200c and NF-kappaB Modulates Mortalin Expression and Increases Cisplatin Sensitivity in an Ovarian Cancer Cell Line Model. Int J Mol Sci. 2022;23(23):15300.
Lv C, Ren C, Yu Y, Yin H, Huang C, Yang G, Hong Y: Wentilactone A Reverses the NF-kappaB/ECM1 Signaling-Induced Cisplatin Resistance through Inhibition of IKK/IkappaB in Ovarian Cancer Cells. Nutrients. 2022;14(18):3790.
Knopfova L, Biglieri E, Volodko N, Masarik M, Hermanova M, Glaus Garzon JF, Ducka M, Kucirkova T, Soucek K, Smarda J, et al. Transcription factor c-Myb inhibits breast cancer lung metastasis by suppression of tumor cell seeding. Oncogene. 2018;37(8):1020–30.
pubmed: 29084208
doi: 10.1038/onc.2017.392
Heuser C, Gattinoni L. c-Myb redefines the hierarchy of stem-like T cells. Nat Immunol. 2022;23(10):1405–7.
pubmed: 36192534
doi: 10.1038/s41590-022-01319-7
Knopfova L, Benes P, Pekarcikova L, Hermanova M, Masarik M, Pernicova Z, Soucek K, Smarda J. c-Myb regulates matrix metalloproteinases 1/9, and cathepsin D: implications for matrix-dependent breast cancer cell invasion and metastasis. Mol Cancer. 2012;11:15.
pubmed: 22439866
pmcid: 3325857
doi: 10.1186/1476-4598-11-15
Wang X, Wang Y, Gou S. A platinum(II) complex HY1-Pt overcomes cisplatin-induced resistance and attenuates metastasis of epithelial ovarian cancer by cancer cell stemness inhibition. Int J Biochem Cell Biol. 2023;157:106395.
pubmed: 36871936
doi: 10.1016/j.biocel.2023.106395
Qiu C, Ma Y, Wang J, Peng S, Huang Y. Lin28-mediated post-transcriptional regulation of Oct4 expression in human embryonic stem cells. Nucleic Acids Res. 2010;38(4):1240–8.
pubmed: 19966271
doi: 10.1093/nar/gkp1071
Huang J, Lin H, Zhong M, Huang J, Sun S, Lin L, Chen Y. Role of Lin28A/let-7a/c-Myc Pathway in Growth and Malignant Behavior of Papillary Thyroid Carcinoma. Med Sci Monit. 2018;24:8899–909.
pubmed: 30531691
pmcid: 6296344
doi: 10.12659/MSM.908628
Balzeau J, Menezes MR, Cao S, Hagan JP. The LIN28/let-7 Pathway in Cancer. Front Genet. 2017;8:31.
pubmed: 28400788
pmcid: 5368188
doi: 10.3389/fgene.2017.00031