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miRNAs as short non-coding RNAs in regulating doxorubicin resistance

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Journal of Cell Communication and Signaling Aims and scope

Abstract

The treatment of cancer patients has been prohibited by chemoresistance. Doxorubicin (DOX) is an anti-tumor compound disrupting proliferation and triggering cell cycle arrest via inhibiting activity of topoisomerase I and II. miRNAs are endogenous RNAs localized in cytoplasm to reduce gene level. Abnormal expression of miRNAs changes DOX cytotoxicity. Overexpression of tumor-promoting miRNAs induces DOX resistance, while tumor-suppressor miRNAs inhibit DOX resistance. The miRNA-mediated regulation of cell death and hallmarks of cancer can affect response to DOX chemotherapy in tumor cells. The transporters such as P-glycoprotein are regulated by miRNAs in DOX chemotherapy. Upstream mediators including lncRNAs and circRNAs target miRNAs in affecting capacity of DOX. The response to DOX chemotherapy can be facilitated after administration of agents that are mostly phytochemicals including curcumol, honokiol and ursolic acid. These agents can regulate miRNA expression increasing DOX’s cytotoxicity. Since delivery of DOX alone or in combination with other drugs and genes can cause synergistic impact, the nanoparticles have been introduced for drug sensitivity.

Graphical abstract

The non-coding RNAs determine the response of tumor cells to doxorubicin chemotherapy. microRNAs play a key role in this case and they can be sponged by lncRNAs and circRNAs, showing interaction among non-coding RNAs in the regulation of doxorubicin sensitivity.

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Abbreviations

DOX:

Doxorubicin

ROS:

Reactive oxygen species

EMT:

Epithelial-to-mesenchymal transition

P-gp:

P-glycoprotein

miRNAs:

MicroRNAs

ncRNAs:

Non-coding RNAs

mRNA:

Messenger RNA

pri-miRNA:

Primary miRNA

pre-miRNA:

Precursor miRNA

RISC:

RNA-induced silencing complex

EVs:

Extracellular vesicles

SCLC:

Small-cell lung cancer

NSCLC:

Non-small cell lung cancer

AGR2:

Anterior gradient 2

HMGB1:

High mobility group box 1

lncRNAs:

Long non-coding RNAs

circRNAs:

Circular RNAs

References

  • Al-Momany B, Hammad H, Ahram M (2021) Dihydrotestosterone induces chemo-resistance of triple-negative breast MDA-MB-231 cancer cells towards doxorubicin independent of ABCG2 and miR-328-3p. Curr Mol Pharmacol 14(5):860–870

    CAS  PubMed  Google Scholar 

  • Alshaer W et al (2019) Downregulation of STAT3, β-catenin, and notch-1 by single and combinations of siRNA treatment enhance chemosensitivity of wild type and doxorubicin resistant MCF7 breast cancer cells to doxorubicin. Int J Mol Sci 20(15):3696

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ashrafizadeh M et al (2022) Exosomes as promising nanostructures in diabetes mellitus: from insulin sensitivity to ameliorating diabetic complications. Int J Nanomed 17:1229

    CAS  Google Scholar 

  • Ashrafizadeh M et al (2023) A bioinformatics analysis, pre-clinical and clinical conception of autophagy in pancreatic cancer: complexity and simplicity in crosstalk. Pharmacol Res 194:106822

    CAS  PubMed  Google Scholar 

  • Atteia HH et al (2021) Thymoquinone upregulates miR-125a-5p, attenuates STAT3 activation, and potentiates doxorubicin antitumor activity in murine solid Ehrlich carcinoma. J Biochem Mol Toxicol 35(12):e22924

    CAS  PubMed  Google Scholar 

  • Ayyildiz A et al (2021) Co-administration of apigenin with doxorubicin enhances anti-migration and antiproliferative effects via PI3K/PTEN/AKT pathway in prostate cancer cells. Exp Oncol 43(2):125–134

    CAS  PubMed  Google Scholar 

  • Baixauli F, López-Otín C, Mittelbrunn M (2014) Exosomes and autophagy: coordinated mechanisms for the maintenance of cellular fitness. Front Immunol 5:403

    PubMed  PubMed Central  Google Scholar 

  • Bao L et al (2012) Increased expression of P-glycoprotein and doxorubicin chemoresistance of metastatic breast cancer is regulated by miR-298. Am J Pathol 180(6):2490–2503

    CAS  PubMed  PubMed Central  Google Scholar 

  • Batist G et al (2002) Myocet (liposome-encapsulated doxorubicin citrate): a new approach in breast cancer therapy. Expert Opin Pharmacother 3(12):1739–1751

    CAS  PubMed  Google Scholar 

  • Buchholz TA et al (2002) Global gene expression changes during neoadjuvant chemotherapy for human breast cancer. Cancer J 8(6):461–468

    PubMed  Google Scholar 

  • Cao Y et al (2021) LncRNA MALAT1 mediates doxorubicin resistance of hepatocellular carcinoma by regulating miR-3129-5p/Nova1 axis. Mol Cell Biochem 476(1):279–292

    CAS  PubMed  Google Scholar 

  • Carvalho C et al (2009) Doxorubicin: the good, the bad and the ugly effect. Curr Med Chem 16(25):3267–3285

    CAS  PubMed  Google Scholar 

  • Chang H-I, Yeh M-K (2012) Clinical development of liposome-based drugs: formulation, characterization, and therapeutic efficacy. Int J Nanomed 7:49

    CAS  Google Scholar 

  • Chen Y et al (2017) miR-27b-3p suppresses cell proliferation, migration and invasion by targeting LIMK1 in colorectal cancer. Int J Clin Exp Pathol 10(9):9251–9261

    PubMed  PubMed Central  Google Scholar 

  • Chen D et al (2018a) miR-27b-3p inhibits proliferation and potentially reverses multi-chemoresistance by targeting CBLB/GRB2 in breast cancer cells. Cell Death Dis 9(2):188

    PubMed  PubMed Central  Google Scholar 

  • Chen J et al (2018b) miR-21-5p confers doxorubicin resistance in gastric cancer cells by targeting PTEN and TIMP3. Int J Mol Med 41(4):1855–1866

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chen M et al (2018c) miR-590-5p suppresses hepatocellular carcinoma chemoresistance by targeting YAP1 expression. EBioMedicine 35:142–154

    PubMed  PubMed Central  Google Scholar 

  • Chen W et al (2019) Delivery of miR-212 by chimeric peptide-condensed supramolecular nanoparticles enhances the sensitivity of pancreatic ductal adenocarcinoma to doxorubicin. Biomaterials 192:590–600

    CAS  PubMed  Google Scholar 

  • Chen S et al (2021a) MiR-199b-5p promotes gastric cancer progression by regulating HHIP expression. Front Oncol 11:728393

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chen Q et al (2021b) MiR-873-5p targets THUMPD1 to inhibit gastric cancer cell behavior and chemoresistance. J Gastrointest Oncol 12(5):2061–2072

    PubMed  PubMed Central  Google Scholar 

  • Dai H et al (2019) MicroRNA-222 promotes drug resistance to doxorubicin in breast cancer via regulation of miR-222/bim pathway. Biosci Rep 39(7):BSR2019

    Google Scholar 

  • Dai G et al (2021) Expression of miR-187 and miR-509-3p in serum of primary hepatocellular carcinoma patients and its evaluation of prognosis. J BUON 26(4):1340–1345

    PubMed  Google Scholar 

  • Deng Z et al (2017) Exosomes miR-126a released from MDSC induced by DOX treatment promotes lung metastasis. Oncogene 36(5):639–651

    CAS  PubMed  Google Scholar 

  • Ding J et al (2018) MiR-223 promotes the doxorubicin resistance of colorectal cancer cells via regulating epithelial-mesenchymal transition by targeting FBXW7. Acta Biochim Biophys Sin (shanghai) 50(6):597–604

    CAS  PubMed  Google Scholar 

  • Dou D et al (2020) CircUBE2D2 (hsa_circ_0005728) promotes cell proliferation, metastasis and chemoresistance in triple-negative breast cancer by regulating miR-512-3p/CDCA3 axis. Cancer Cell Int 20:454

    CAS  PubMed  PubMed Central  Google Scholar 

  • Doublier S et al (2012) HIF-1 activation induces doxorubicin resistance in MCF7 3-D spheroids via P-glycoprotein expression: a potential model of the chemo-resistance of invasive micropapillary carcinoma of the breast. BMC Cancer 12:4

    CAS  PubMed  PubMed Central  Google Scholar 

  • Du F et al (2019) miR-137 alleviates doxorubicin resistance in breast cancer through inhibition of epithelial-mesenchymal transition by targeting DUSP4. Cell Death Dis 10(12):922

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fan YP et al (2017) MiR-375 and doxorubicin co-delivered by liposomes for combination therapy of hepatocellular carcinoma. Mol Ther Nucleic Acids 7:181–189

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fang J et al (2020) A nanomicelle with miR-34a and doxorubicin reverses the drug resistance of cisplatin in esophageal carcinoma cells by inhibiting SIRT1 signal pathway. Transl Cancer Res 9(7):4131–4140

    CAS  PubMed  PubMed Central  Google Scholar 

  • Farago AF et al (2019) ATLANTIS: a phase III study of lurbinectedin/doxorubicin versus topotecan or cyclophosphamide/doxorubicin/vincristine in patients with small-cell lung cancer who have failed one prior platinum-containing line. Future Oncol 15(3):231–239

    CAS  PubMed  Google Scholar 

  • Gajda E et al (2020) Combinatory treatment with miR-7-5p and drug-loaded cubosomes effectively impairs cancer cells. Int J Mol Sci 21(14):5039

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gao AM, Zhang XY, Ke ZP (2017) Apigenin sensitizes BEL-7402/ADM cells to doxorubicin through inhibiting miR-101/Nrf2 pathway. Oncotarget 8(47):82085–82091

    PubMed  PubMed Central  Google Scholar 

  • Gao AM et al (2018) Apigenin sensitizes hepatocellular carcinoma cells to doxorubic through regulating miR-520b/ATG7 axis. Chem Biol Interact 280:45–50

    CAS  PubMed  Google Scholar 

  • Gao M et al (2020a) Orphan nuclear receptor RORγ confers doxorubicin resistance in prostate cancer. Cell Biol Int 44(10):2170–2176

    CAS  PubMed  Google Scholar 

  • Gao H et al (2020b) Exosomal transfer of macrophage-derived miR-223 confers doxorubicin resistance in gastric cancer. Onco Targets Ther 13:12169–12179

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gao J et al (2021a) Curcumol increases the sensitivity of colon cancer to 5-FU by regulating Wnt/β-catenin signaling. Transl Cancer Res 10(5):2437–2450

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gao X, Jiang Y, Li Y (2021b) Inhibitory effect of miR-140-5p on doxorubicin resistance of hepatocellular carcinoma. Exp Ther Med 21(5):507

    CAS  PubMed  PubMed Central  Google Scholar 

  • Garg M et al (2020) The pleiotropic role of transcription factor STAT3 in oncogenesis and its targeting through natural products for cancer prevention and therapy. Med Res Rev 41:1291

    Google Scholar 

  • Gorshkov A et al (2022) Exosomes as natural nanocarriers for RNA-based therapy and prophylaxis. Nanomaterials (Basel) 12(3):524

    CAS  PubMed  Google Scholar 

  • Guan X et al (2021) Curcumol inhibits EBV-positive Nasopharyngeal carcinoma migration and invasion by targeting nucleolin. Biochem Pharmacol 192:114742

    CAS  PubMed  Google Scholar 

  • Guarnerio J et al (2016) Oncogenic role of fusion-circRNAs derived from cancer-associated chromosomal translocations. Cell 165(2):289–302

    CAS  PubMed  Google Scholar 

  • Guo B et al (2011) Individualized liposomal doxorubicin-based treatment in elderly patients with non-Hodgkin’s lymphoma. Oncol Res Treat 34(4):184–188

    CAS  Google Scholar 

  • Guo Q et al (2021) Doxorubicin-loaded natural daptomycin micelles with enhanced targeting and anti-tumor effect in vivo. Eur J Med Chem 222:113582

    CAS  PubMed  Google Scholar 

  • Han B et al (2019) The microRNA miR-181c enhances chemosensitivity and reduces chemoresistance in breast cancer cells via down-regulating osteopontin. Int J Biol Macromol 125:544–556

    CAS  PubMed  Google Scholar 

  • Hashemi M et al (2022) Long non-coding RNA (lncRNA) H19 in human cancer: from proliferation and metastasis to therapy. Pharmacol Res 184:106418

    CAS  PubMed  Google Scholar 

  • Hilmer SN et al (2004) The hepatic pharmacokinetics of doxorubicin and liposomal doxorubicin. Drug Metab Dispos 32(8):794–799

    CAS  PubMed  Google Scholar 

  • Hong KS et al (2019) Calponin 3 regulates cell invasion and doxorubicin resistance in gastric cancer. Gastroenterol Res Pract 2019:3024970

    PubMed  PubMed Central  Google Scholar 

  • Hsieh PL et al (2020) Soy isoflavone genistein impedes cancer stemness and mesenchymal transition in head and neck cancer through activating miR-34a/RTCB Axis. Nutrients 12(7):1924

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hu G et al (2018) miR-125b regulates the drug-resistance of breast cancer cells to doxorubicin by targeting HAX-1. Oncol Lett 15(2):1621–1629

    PubMed  Google Scholar 

  • Hu XY et al (2022) Cancer drug resistance related microRNAs: recent advances in detection methods. Analyst 147(12):2615–2632

    CAS  PubMed  Google Scholar 

  • Huang J et al (2012) HMGB1 promotes drug resistance in osteosarcoma. Cancer Res 72(1):230–238

    CAS  PubMed  Google Scholar 

  • Indrieri A et al (2020) The pervasive role of the miR-181 family in development, neurodegeneration, and cancer. Int J Mol Sci 21(6):2092

    CAS  PubMed  PubMed Central  Google Scholar 

  • Iwai N et al (2018) Oncogenic miR-96-5p inhibits apoptosis by targeting the caspase-9 gene in hepatocellular carcinoma. Int J Oncol 53(1):237–245

    CAS  PubMed  Google Scholar 

  • Jain N, Das B, Mallick B (2022) miR-197-5p increases doxorubicin-mediated anticancer cytotoxicity of HT1080 fibrosarcoma cells by decreasing drug efflux. DNA Repair (amst) 109:103259

    CAS  PubMed  Google Scholar 

  • Ji, Y., et al., circ_0002060 Enhances Doxorubicin Resistance in Osteosarcoma by Regulating the miR-198/ABCB1 Axis. Cancer Biother Radiopharm, 2020.

  • Jiang CF et al (2021) TBX15/miR-152/KIF2C pathway regulates breast cancer doxorubicin resistance via promoting PKM2 ubiquitination. Cancer Cell Int 21(1):542

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jin Y et al (2020) miR-199a-5p is involved in doxorubicin resistance of non-small cell lung cancer (NSCLC) cells. Eur J Pharmacol 878:173105

    CAS  PubMed  Google Scholar 

  • Kalfert D et al (2020) Multifunctional roles of miR-34a in cancer: a review with the emphasis on head and neck squamous cell carcinoma and thyroid cancer with clinical implications. Diagnostics 10(8):563

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kang X et al (2017) DUSP4 promotes doxorubicin resistance in gastric cancer through epithelial-mesenchymal transition. Oncotarget 8(55):94028–94039

    PubMed  PubMed Central  Google Scholar 

  • Kanojia D et al (2022) Transcriptome analysis identifies TODL as a novel lncRNA associated with proliferation, differentiation, and tumorigenesis in liposarcoma through FOXM1. Pharmacol Res 185:106462

    CAS  PubMed  Google Scholar 

  • Keizer H et al (1990) Doxorubicin (adriamycin): a critical review of free radical-dependent mechanisms of cytotoxicity. Pharmacol Ther 47(2):219–231

    CAS  PubMed  Google Scholar 

  • Kheradmand P, Vallian Boroojeni S, Esmaeili-Mahani S (2021) MiR-221 expression level correlates with insulin-induced doxorubicin resistance in MCF-7 breast cancer cells. Cell J 23(3):329–334

    PubMed  PubMed Central  Google Scholar 

  • Korać P, Antica M, Matulić MJB (2021) MiR-7 in cancer development. Biomedicines 9(3):325

    PubMed  PubMed Central  Google Scholar 

  • Kowal J, Tkach M, Théry C (2014) Biogenesis and secretion of exosomes. Curr Opin Cell Biol 29:116–125

    CAS  PubMed  Google Scholar 

  • Lai J et al (2019) MiR-7-5p-mediated downregulation of PARP1 impacts DNA homologous recombination repair and resistance to doxorubicin in small cell lung cancer. BMC Cancer 19(1):602

    PubMed  PubMed Central  Google Scholar 

  • Li R et al (2016) miR-223/FBW7 axis regulates doxorubicin sensitivity through epithelial mesenchymal transition in non-small cell lung cancer. Am J Transl Res 8(6):2512–2524

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li Y et al (2018a) MiR-770 suppresses the chemo-resistance and metastasis of triple negative breast cancer via direct targeting of STMN1. Cell Death Dis 9(1):14

    PubMed  PubMed Central  Google Scholar 

  • Li S et al (2018b) Down-regulation of miR-210-3p encourages chemotherapy resistance of renal cell carcinoma via modulating ABCC1. Cell Biosci 8:9

    PubMed  PubMed Central  Google Scholar 

  • Li X et al (2020) Circ_0003998 enhances doxorubicin resistance in hepatocellular carcinoma by regulating miR-218-5p/EIF5A2 pathway. Diagn Pathol 15(1):141

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li Z et al (2021a) STAT5a confers doxorubicin resistance to breast cancer by regulating ABCB1. Front Oncol 11:697950

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li H et al (2021b) miR-940 is a new biomarker with tumor diagnostic and prognostic value. Mol Ther Nucleic Acids 25:53–66

    PubMed  PubMed Central  Google Scholar 

  • Li QK et al (2021c) Circ-sirt1 inhibits growth and invasion of gastric cancer by sponging miR-132-3p/miR-212-3p and upregulating sirt1 expression. Neoplasma 68(4):780–787

    CAS  PubMed  Google Scholar 

  • Li Z et al (2021d) LINC01977 promotes breast cancer progression and chemoresistance to doxorubicin by targeting miR-212-3p/GOLM1 axis. Front Oncol 11:657094

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li R et al (2021e) LINC01116 promotes doxorubicin resistance in osteosarcoma by epigenetically silencing miR-424-5p and inducing epithelial-mesenchymal transition. Front Pharmacol 12:632206

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li M et al (2022) miR-205 reverses MDR-1 mediated doxorubicin resistance via PTEN in human liver cancer HepG2 cells. Cell J 24(3):112–119

    PubMed  PubMed Central  Google Scholar 

  • Liang Y et al (2019) circKDM4C suppresses tumor progression and attenuates doxorubicin resistance by regulating miR-548p/PBLD axis in breast cancer. Oncogene 38(42):6850–6866

    CAS  PubMed  Google Scholar 

  • Liang X et al (2021) Nucleolin-targeting AS1411 aptamer-modified micelle for the co-delivery of doxorubicin and miR-519c to improve the therapeutic efficacy in hepatocellular carcinoma treatment. Int J Nanomedicine 16:2569–2584

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lin XJ et al (2020) miR-936 suppresses cell proliferation, invasion, and drug resistance of laryngeal squamous cell carcinoma and targets GPR78. Front Oncol 10:60

    PubMed  PubMed Central  Google Scholar 

  • Liu XQ et al (2012) Therapeutic delivery of siRNA silencing HIF-1 alpha with micellar nanoparticles inhibits hypoxic tumor growth. Mol Pharm 9(10):2863–2874

    CAS  PubMed  Google Scholar 

  • Liu T, Guo J, Zhang X (2019a) MiR-202-5p/PTEN mediates doxorubicin-resistance of breast cancer cells via PI3K/Akt signaling pathway. Cancer Biol Ther 20(7):989–998

    CAS  PubMed  PubMed Central  Google Scholar 

  • Liu X et al (2019b) Exosomal transfer of miR-501 confers doxorubicin resistance and tumorigenesis via targeting of BLID in gastric cancer. Cancer Lett 459:122–134

    CAS  PubMed  Google Scholar 

  • Liu C et al (2019c) MiR-124 reversed the doxorubicin resistance of breast cancer stem cells through STAT3/HIF-1 signaling pathways. Cell Cycle 18(18):2215–2227

    CAS  PubMed  PubMed Central  Google Scholar 

  • Liu Y et al (2019d) CKLF1 enhances inflammation-mediated carcinogenesis and prevents doxorubicin-induced apoptosis via IL6/STAT3 signaling in HCC. Clin Cancer Res 25(13):4141–4154

    CAS  PubMed  Google Scholar 

  • Liu J et al (2021) The biology, function, and applications of exosomes in cancer. Acta Pharm Sin B 11(9):2783–2797

    CAS  PubMed  PubMed Central  Google Scholar 

  • Long QZ et al (2015) miR-124 represses FZD5 to attenuate P-glycoprotein-mediated chemo-resistance in renal cell carcinoma. Tumour Biol 36(9):7017–7026

    CAS  PubMed  Google Scholar 

  • Long J et al (2018) Maintenance of stemness by miR-589-5p in hepatocellular carcinoma cells promotes chemoresistance via STAT3 signaling. Cancer Lett 423:113–126

    CAS  PubMed  Google Scholar 

  • Lou Y et al (2010) Isolation and identification of phase 1 metabolites of curcumol in rats. Drug Metab Dispos 38(11):2014–2022

    CAS  PubMed  Google Scholar 

  • Lovitt CJ, Shelper TB, Avery VM (2018) Doxorubicin resistance in breast cancer cells is mediated by extracellular matrix proteins. BMC Cancer 18(1):41

    PubMed  PubMed Central  Google Scholar 

  • Lu L et al (2018) miR-505 enhances doxorubicin-induced cytotoxicity in hepatocellular carcinoma through repressing the Akt pathway by directly targeting HMGB1. Biomed Pharmacother 104:613–621

    CAS  PubMed  Google Scholar 

  • Lu J et al (2021a) CircNUP98 suppresses the maturation of miR-519a-3p in glioblastoma. Front Neurol 12:679745

    PubMed  PubMed Central  Google Scholar 

  • Lu M et al (2021b) Notoginsenoside R1 counteracts mesenchymal stem cell-evoked oncogenesis and doxorubicin resistance in osteosarcoma cells by blocking IL-6 secretion-induced JAK2/STAT3 signaling. Invest New Drugs 39(2):416–425

    CAS  PubMed  Google Scholar 

  • Lu Q et al (2021c) Ursolic acid enhances cytotoxicity of doxorubicin-resistant triple-negative breast cancer cells via ZEB1-AS1/miR-186–5p/ABCC1 axis. Cancer Biother Radiopharm 37:673

    PubMed  Google Scholar 

  • Ma XL et al (2021) Doxorubicin-induced novel circRNA_0004674 facilitates osteosarcoma progression and chemoresistance by upregulating MCL1 through miR-142-5p. Cell Death Discov 7(1):309

    CAS  PubMed  PubMed Central  Google Scholar 

  • Manvati MKS et al (2020) Association of miR-760 with cancer: an overview. Gene 747:144648

    CAS  PubMed  Google Scholar 

  • Marina NM et al (2002) Dose escalation and pharmacokinetics of pegylated liposomal doxorubicin (doxil) in children with solid tumors: a pediatric oncology group study. Clin Cancer Res 8(2):413–418

    CAS  PubMed  Google Scholar 

  • Meldolesi J (2018) Exosomes and ectosomes in intercellular communication. Curr Biol 28(8):R435-r444

    CAS  PubMed  Google Scholar 

  • Meng RY et al (2021) Ursolic acid accelerates paclitaxel-induced cell death in esophageal cancer cells by suppressing Akt/FOXM1 signaling cascade. Int J Mol Sci 22(21):11486

    CAS  PubMed  PubMed Central  Google Scholar 

  • Meredith A-M, Dass CR (2016) Increasing role of the cancer chemotherapeutic doxorubicin in cellular metabolism. J Pharm Pharmacol 68(6):729–741

    CAS  PubMed  Google Scholar 

  • Mi H et al (2018) miR-381 induces sensitivity of breast cancer cells to doxorubicin by inactivation of MAPK signaling via FYN. Eur J Pharmacol 839:66–75

    CAS  PubMed  Google Scholar 

  • Minotti G et al (2004) Anthracyclines: molecular advances and pharmacologic developments in antitumor activity and cardiotoxicity. Pharmacol Rev 56(2):185–229

    CAS  PubMed  Google Scholar 

  • Mirzaei S et al (2022) Advances in understanding the role of P-gp in doxorubicin resistance: molecular pathways, therapeutic strategies, and prospects. Drug Discovery Today 27(2):436–455

    CAS  PubMed  Google Scholar 

  • Mirzaei S et al (2023) Resveratrol augments doxorubicin and cisplatin chemotherapy: a novel therapeutic strategy. Curr Mol Pharmacol 16:280–306

    CAS  PubMed  Google Scholar 

  • Naba NM et al (2020) Doxorubicin inhibits miR-140 expression and upregulates PD-L1 expression in HCT116 cells, opposite to its effects on MDA-MB-231 cells. Turk J Biol 44(1):15–23

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nair R et al (2014) Extracellular vesicles derived from preosteoblasts influence embryonic stem cell differentiation. Stem Cells Dev 23(14):1625

    CAS  PubMed  Google Scholar 

  • O’Connor R (2007) The pharmacology of cancer resistance. Anticancer Res 27(3A):1267–1272

    CAS  PubMed  Google Scholar 

  • Ong CP et al (2019) Honokiol: a review of its anticancer potential and mechanisms. Cancers 12(1):48

    PubMed  PubMed Central  Google Scholar 

  • Pan L et al (2021) Curcumin inhibits prostate cancer progression by regulating the miR-30a-5p/PCLAF axis. Exp Ther Med 22(3):969

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pandya G et al (2020) The implication of long non-coding RNAs in the diagnosis, pathogenesis and drug resistance of pancreatic ductal adenocarcinoma and their possible therapeutic potential. Biochim Biophys Acta (BBA) Rev Cancer 187(2):188423

    Google Scholar 

  • Pang X et al (2019) Foxo3a-dependent miR-633 regulates chemotherapeutic sensitivity in gastric cancer by targeting fas-associated death domain. RNA Biol 16(2):233–248

    PubMed  PubMed Central  Google Scholar 

  • Papa A, Pandolfi PP (2019) The PTEN−PI3K axis in cancer. Biomolecules 9(4):153

    CAS  PubMed  PubMed Central  Google Scholar 

  • Peer D et al (2007) Nanocarriers as an emerging platform for cancer therapy. Nano-Enabled Med Appl 2(12):751–760

    CAS  Google Scholar 

  • Qin T et al (2022) Luteolin attenuates the chemoresistance of osteosarcoma through inhibiting the PTN/β-catenin/MDR1 signaling axis by upregulating miR-384. J Bone Oncol 34:100429

    PubMed  PubMed Central  Google Scholar 

  • Qin Y et al (2023) Autophagy and cancer drug resistance in dialogue: pre-clinical and clinical evidence. Cancer Lett 570:216307

    CAS  PubMed  Google Scholar 

  • Rajput A et al (2022) Exosomes as new generation vehicles for drug delivery: biomedical applications and future perspectives. Molecules 27(21):7289

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rawat L, Nayak V (2021) Ursolic acid disturbs ROS homeostasis and regulates survival-associated gene expression to induce apoptosis in intestinal cancer cells. Toxicol Res (camb) 10(3):369–375

    PubMed  Google Scholar 

  • Ruggiero A et al (2013) Myocardial performance index and biochemical markers for early detection of doxorubicin-induced cardiotoxicity in children with acute lymphoblastic leukaemia. Int J Clin Oncol 18(5):927–933

    CAS  PubMed  Google Scholar 

  • Safaei S et al (2022) miR-200c increases the sensitivity of breast cancer cells to doxorubicin through down regulating MDR1 gene. Exp Mol Pathol 125:104753

    CAS  PubMed  Google Scholar 

  • Schmitt AM, Chang H (2016) Long noncoding RNAs in cancer pathways. Cancer Cells 29(4):452–463

    CAS  Google Scholar 

  • Sengupta S et al (2017) Activation of tumor suppressor LKB1 by honokiol abrogates cancer stem-like phenotype in breast cancer via inhibition of oncogenic Stat3. Oncogene 36(41):5709–5721

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shabna A et al (2023) Long non-coding RNAs: Fundamental regulators and emerging targets of cancer stem cells. Biochim Biophys Acta (BBA) Rev Cancer 1878(3):188899

    CAS  Google Scholar 

  • Shang J et al (2019) CircPAN3 mediates drug resistance in acute myeloid leukemia through the miR-153-5p/miR-183-5p-XIAP axis. Exp Hematol 70:42-54.e3

    CAS  PubMed  Google Scholar 

  • Sharma S et al (2017) Enhanced efficacy of anti-miR-191 delivery through stearylamine liposome formulation for the treatment of breast cancer cells. Int J Pharm 530(1–2):387–400

    CAS  PubMed  Google Scholar 

  • Shen SJ et al (2020) MicroRNA-27b-3p promotes tumor progression and metastasis by inhibiting peroxisome proliferator-activated receptor gamma in triple-negative breast cancer. Front Oncol 10:1371

    PubMed  PubMed Central  Google Scholar 

  • Sheng W et al (2021) Curcumol inhibits the malignant progression of prostate cancer and regulates the PDK1/AKT/mTOR pathway by targeting miR-9. Oncol Rep 46(5):1

    Google Scholar 

  • Shi X et al (2020) circRNAs and exosomes: a mysterious frontier for human cancer. Mol Ther Nucleic Acids 19:384–392

    CAS  PubMed  Google Scholar 

  • Shi P, Song H, Ding X (2021a) Reduced expression of circRNA hsa_circ_001888 in gastric cancer and its clinical significance. J Clin Lab Anal 35(9):e23953

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shi Y et al (2021b) Dextran-polylactide micelles loaded with doxorubicin and DiR for image-guided chemo-photothermal tumor therapy. Int J Biol Macromol 187:296–308

    CAS  PubMed  Google Scholar 

  • Sohail M et al (2021) Research progress in strategies to improve the efficacy and safety of doxorubicin for cancer chemotherapy. Expert Rev Anticancer Ther 21(12):1385–1398

    CAS  PubMed  Google Scholar 

  • Song Z et al (2021a) Exosomal miR-4443 promotes cisplatin resistance in non-small cell lung carcinoma by regulating FSP1 m6A modification-mediated ferroptosis. Life Sci 276:119399

    CAS  PubMed  Google Scholar 

  • Song F et al (2021b) Resveratrol inhibits the migration, invasion and epithelial-mesenchymal transition in liver cancer cells through up- miR-186-5p expression. Zhejiang Da Xue Xue Bao Yi Xue Ban 50(5):582–590

    PubMed  PubMed Central  Google Scholar 

  • Sousa D, Lima RT, Vasconcelos M (2015) Intercellular transfer of cancer drug resistance traits by extracellular vesicles. Trends Mol Med 21(10):595–608

    CAS  PubMed  Google Scholar 

  • Suebsoonthron J et al (2017) Inhibition of WNT signaling reduces differentiation and induces sensitivity to doxorubicin in human malignant neuroblastoma SH-SY5Y cells. Anticancer Drugs 28(5):469–479

    CAS  PubMed  Google Scholar 

  • Sun S, Fang H (2021) Curcumin inhibits ovarian cancer progression by regulating circ-PLEKHM3/miR-320a/SMG1 axis. J Ovarian Res 14(1):158

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sun X et al (2020) Long noncoding RNA OIP5-AS1 mediates resistance to doxorubicin by regulating miR-137-3p/PTN axis in osteosarcoma. Biomed Pharmacother 128:110201

    CAS  PubMed  Google Scholar 

  • Tacar O et al (2013) Doxorubicin: an update on anticancer molecular action, toxicity and novel drug delivery systems. J Pharm Pharmacol 65(2):157–170

    CAS  PubMed  Google Scholar 

  • Tanaka N et al (2021) Identification of miR-199–5p and miR-199–3p target genes: paxillin facilities cancer cell aggressiveness in head and neck squamous cell carcinoma. Genes (basel) 12(12):1910

    CAS  PubMed  Google Scholar 

  • Tang X et al (2021) Dual ATP/reduction-responsive polyplex to achieve the co-delivery of doxorubicin and miR-23b for the cancer treatment. Colloids Surf B Biointerfaces 206:111955

    CAS  PubMed  Google Scholar 

  • Tao L et al (2020) MiR-451a attenuates doxorubicin resistance in lung cancer via suppressing epithelialmesenchymal transition (EMT) through targeting c-Myc. Biomed Pharmacother 125:109962

    CAS  PubMed  Google Scholar 

  • Teng X et al (2015) Mesenchymal stem cell-derived exosomes improve the microenvironment of infarcted myocardium contributing to angiogenesis and anti-inflammation. Cell Physiol Biochem 37(6):2415–2424

    CAS  PubMed  Google Scholar 

  • Théry C, Zitvogel L, Amigorena S (2002) Exosomes: composition, biogenesis and function. Nature Rev Immunol 2(8):569–579

    Google Scholar 

  • Tian ZC, Wang JQ, Ge H (2020) Apatinib ameliorates doxorubicin-induced migration and cancer stemness of osteosarcoma cells by inhibiting Sox2 via STAT3 signalling. J Orthop Translat 22:132–141

    PubMed  Google Scholar 

  • Tong R et al (2020) Inhibition of miR-574-5p suppresses cell growth and metastasis and enhances chemosensitivity by targeting RNA binding protein QKI in cervical cancer cells. Naunyn Schmiedebergs Arch Pharmacol 393(6):951–966

    CAS  PubMed  Google Scholar 

  • Tran QH et al (2021) Melatonin and doxorubicin synergistically enhance apoptosis via autophagy-dependent reduction of AMPKα1 transcription in human breast cancer cells. Exp Mol Med 53(9):1413–1422

    CAS  PubMed  PubMed Central  Google Scholar 

  • Walsh N et al (2009) Expression of multidrug resistance markers ABCB1 (MDR-1/P-gp) and ABCC1 (MRP-1) in renal cell carcinoma. BMC Urol 9(1):1–7

    Google Scholar 

  • Wang Y et al (2017) An ATP-responsive codelivery system of doxorubicin and MiR-34a to synergistically inhibit cell proliferation and migration. Mol Pharm 14(7):2323–2332

    CAS  PubMed  Google Scholar 

  • Wang H et al (2018) HOTAIR enhanced paclitaxel and doxorubicin resistance in gastric cancer cells partly through inhibiting miR-217 expression. J Cell Biochem 119(9):7226–7234

    CAS  PubMed  Google Scholar 

  • Wang Y et al (2019a) Exosomal circRNAs: biogenesis, effect and application in human diseases. Mol Cancer 18(1):116

    PubMed  PubMed Central  Google Scholar 

  • Wang H et al (2019b) Downregulation of miR-222-3p reverses doxorubicin-resistance in LoVo cells through upregulating forkhead box protein P2 (FOXP2) Protein. Med Sci Monit 25:2169–2178

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang S et al (2020a) Interactions between lncRNA TUG1 and miR-9-5p modulate the resistance of breast cancer cells to doxorubicin by regulating eIF5A2. Onco Targets Ther 13:13159–13170

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang S et al (2020b) Exosomal CircPRRX1 enhances doxorubicin resistance in gastric cancer by regulating MiR-3064-5p/PTPN14 signaling. Yonsei Med J 61(9):750–761

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang B et al (2020c) LncRNA NORAD accelerates the progression and doxorubicin resistance of neuroblastoma through up-regulating HDAC8 via sponging miR-144-3p. Biomed Pharmacother 129:110268

    CAS  PubMed  Google Scholar 

  • Wang L et al (2020d) Long non-coding RNA LINC00426 contributes to doxorubicin resistance by sponging miR-4319 in osteosarcoma. Biol Direct 15(1):11

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang JD et al (2021) Exosomal HMGB1 promoted cancer malignancy. Cancers (basel) 13(4):877

    CAS  PubMed  Google Scholar 

  • Wang Y et al (2021a) MiR-200c-3p aggravates gastric cell carcinoma via KLF6. Genes Genomics 43(11):1307–1316

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang L et al (2021b) The LINC00922 aggravates ovarian cancer progression via sponging miR-361-3p. J Ovarian Res 14(1):77

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Q et al (2021c) Hsa_circ_0092276 promotes doxorubicin resistance in breast cancer cells by regulating autophagy via miR-348/ATG7 axis. Transl Oncol 14(8):101045

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang S et al (2021d) Ursolic acid inhibits breast cancer metastasis by suppressing glycolytic metabolism via activating SP1/Caveolin-1 signaling. Front Oncol 11:745584

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang J et al (2021e) Curcumol simultaneously induces both apoptosis and autophagy in human nasopharyngeal carcinoma cells. Phytother Res 35(12):7004–7017

    CAS  PubMed  Google Scholar 

  • Wang D, Zhang X, Xu B (2021f) PEGylated doxorubicin prodrug-forming reduction-sensitive micelles with high drug loading and improved anticancer therapy. Front Bioeng Biotechnol 9:781982

    PubMed  PubMed Central  Google Scholar 

  • Wardhani BWK et al (2021) TGF-β-induced TMEPAI promotes epithelial-mesenchymal transition in doxorubicin-treated triple-negative breast cancer cells via SMAD3 and PI3K/AKT pathway alteration. Breast Cancer (dove Med Press) 13:529–538

    PubMed  Google Scholar 

  • Wei W et al (2020) CircSAMD4A contributes to cell doxorubicin resistance in osteosarcoma by regulating the miR-218-5p/KLF8 axis. Open Life Sci 15(1):848–859

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wen C et al (2019) Curcumin reverses doxorubicin resistance via inhibition the efflux function of ABCB4 in doxorubicin-resistant breast cancer cells. Mol Med Rep 19(6):5162–5168

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wise HM, Hermida MA, Leslie NR (2017) Prostate cancer, PI3K, PTEN and prognosis. Clin Sci (lond) 131(3):197–210

    CAS  PubMed  Google Scholar 

  • Wu X et al (2018) The many faces of long noncoding RNAs in cancer. Antioxid Redox Signal 29(9):922–935

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wu M et al (2021) Hsa_circRNA_002144 promotes growth and metastasis of colorectal cancer through regulating miR-615-5p/LARP1/mTOR pathway. Carcinogenesis 42(4):601–610

    CAS  PubMed  Google Scholar 

  • Xi L et al (2021) Circular RNA circCSPP1 knockdown attenuates doxorubicin resistance and suppresses tumor progression of colorectal cancer via miR-944/FZD7 axis. Cancer Cell Int 21(1):153

    CAS  PubMed  PubMed Central  Google Scholar 

  • Xia M et al (2021) MiR-194-5p enhances the sensitivity of nonsmall-cell lung cancer to doxorubicin through targeted inhibition of hypoxia-inducible factor-1. World J Surg Oncol 19(1):174

    PubMed  PubMed Central  Google Scholar 

  • Xie X et al (2019) Polymeric hybrid nanomicelles for cancer theranostics: an efficient and precise anticancer strategy for the codelivery of doxorubicin/miR-34a and magnetic resonance imaging. ACS Appl Mater Interfaces 11(47):43865–43878

    CAS  PubMed  Google Scholar 

  • Xie C et al (2020) Circular RNA hsa_circ_0003496 contributes to tumorigenesis and chemoresistance in osteosarcoma through targeting (microRNA) miR-370/Krüppel-like factor 12 axis. Cancer Manag Res 12:8229–8240

    CAS  PubMed  PubMed Central  Google Scholar 

  • Xie X et al (2021) A circular RNA, circSMARCA5, inhibits prostate cancer proliferative, migrative, and invasive capabilities via the miR-181b-5p/miR-17-3p-TIMP3 axis. Aging (albany NY) 13(15):19908–19919

    CAS  PubMed  Google Scholar 

  • Xin X et al (2022) MiR-376a-3p increases cell apoptosis in acute myeloid leukemia by targeting MT1X. Cancer Biol Ther 23(1):234–242

    CAS  PubMed  PubMed Central  Google Scholar 

  • Xu Y et al (2018) miR-27b-3p is involved in doxorubicin resistance of human anaplastic thyroid cancer cells via targeting peroxisome proliferator-activated receptor gamma. Basic Clin Pharmacol Toxicol 123(6):670–677

    CAS  PubMed  Google Scholar 

  • Xu Y et al (2021) miR-34a inhibits melanoma growth by targeting ZEB1. Aging (albany NY) 13(11):15538–15547

    CAS  PubMed  Google Scholar 

  • Xue H et al (2017) Delivery of miR-375 and doxorubicin hydrochloride by lipid-coated hollow mesoporous silica nanoparticles to overcome multiple drug resistance in hepatocellular carcinoma. Int J Nanomed 12:5271–5287

    CAS  Google Scholar 

  • Yang L et al (2012) Down-regulation of osteopontin expression by RNA interference affects cell proliferation and chemotherapy sensitivity of breast cancer MDA-MB-231 cells. Mol Med Rep 5(2):373–376

    CAS  PubMed  Google Scholar 

  • Yang X et al (2017) miR-200b regulates epithelial-mesenchymal transition of chemo-resistant breast cancer cells by targeting FN1. Discov Med 24(131):75–85

    PubMed  Google Scholar 

  • Yang X et al (2019) MiR-27b-3p promotes migration and invasion in colorectal cancer cells by targeting HOXA10. Biosci Rep 39(12):BSR20191087

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yang Q et al (2021) Chemotherapy-elicited exosomal miR-378a-3p and miR-378d promote breast cancer stemness and chemoresistance via the activation of EZH2/STAT3 signaling. J Exp Clin Cancer Res 40(1):120

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yi X et al (2021) Honokiol antagonizes doxorubicin resistance in human breast cancer via miR-188-5p/FBXW7/c-Myc pathway. Cancer Chemother Pharmacol 87(5):647–656

    CAS  PubMed  Google Scholar 

  • Yin TF et al (2021) Identification of the circRNA-miRNA-mRNA regulatory network and its prognostic effect in colorectal cancer. World J Clin Cases 9(18):4520–4541

    PubMed  PubMed Central  Google Scholar 

  • Yuan J et al (2021) CircPRDM2 contributes to doxorubicin resistance of osteosarcoma by elevating EZH2 via sponging miR-760. Cancer Manag Res 13:4433–4445

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yue X et al (2020) LncRNA MALAT1 promotes breast cancer progression and doxorubicin resistance via regulating miR-570-3p. Biomed J 44:S296

    PubMed  PubMed Central  Google Scholar 

  • Zang H et al (2020) Overcoming acquired resistance of EGFR-mutant NSCLC cells to the third generation EGFR inhibitor, osimertinib, with the natural product honokiol. Mol Oncol 14(4):882–895

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zangouei AS, Alimardani M, Moghbeli M (2021) MicroRNAs as the critical regulators of doxorubicin resistance in breast tumor cells. Cancer Cell Int 21(1):213

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zanoaga O et al (2021) The Role of miR-155 in nutrition: modulating cancer-associated inflammation. Nutrients 13(7):2245

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zeng C et al (2020) Curcumol enhances the sensitivity of doxorubicin in triple-negative breast cancer via regulating the miR-181b-2-3p-ABCC3 axis. Biochem Pharmacol 174:113795

    CAS  PubMed  Google Scholar 

  • Zhang Y et al (2019) miR-135b-5p enhances doxorubicin-sensitivity of breast cancer cells through targeting anterior gradient 2. J Exp Clin Cancer Res 38(1):26

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang M et al (2020a) LncRNA XIST promotes chemoresistance of breast cancer cells to doxorubicin by sponging miR-200c-3p to upregulate ANLN. Clin Exp Pharmacol Physiol 47(8):1464–1472

    CAS  PubMed  Google Scholar 

  • Zhang J et al (2020b) LncRNA SNHG15 contributes to doxorubicin resistance of osteosarcoma cells through targeting the miR-381-3p/GFRA1 axis. Open Life Sci 15(1):871–883

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang N et al (2021a) Curcumin reverses doxorubicin resistance in colon cancer cells at the metabolic level. J Pharm Biomed Anal 201:114129

    CAS  PubMed  Google Scholar 

  • Zhang K et al (2021b) A two-miRNA signature of upregulated miR-185-5p and miR-362-5p as a blood biomarker for breast cancer. Pathol Res Pract 222:153458

    CAS  PubMed  Google Scholar 

  • Zhang H et al (2021c) miR-520b inhibits IGF-1R to increase doxorubicin sensitivity and promote cell apoptosis in breast cancer. Yakugaku Zasshi 141(3):415–426

    CAS  PubMed  Google Scholar 

  • Zhang Y et al (2021d) miR-381-3p attenuates doxorubicin resistance in human anaplastic thyroid carcinoma via targeting homeobox A9. Int J Exp Pathol 102(4–5):209–217

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Y, Tan X, Lu Y (2022) Exosomal transfer of circ_0006174 contributes to the chemoresistance of doxorubicin in colorectal cancer by depending on the miR-1205/CCND2 axis. J Physiol Biochem 78(1):39–50

    CAS  PubMed  Google Scholar 

  • Zhao P et al (2017a) MiR-375 delivered by lipid-coated doxorubicin-calcium carbonate nanoparticles overcomes chemoresistance in hepatocellular carcinoma. Nanomedicine 13(8):2507–2516

    CAS  PubMed  Google Scholar 

  • Zhao G et al (2017b) Targeted inhibition of HDAC8 increases the doxorubicin sensitivity of neuroblastoma cells via up regulation of miR-137. Eur J Pharmacol 802:20–26

    CAS  PubMed  Google Scholar 

  • Zheng Z et al (2006) An ancestral haplotype defines susceptibility to doxorubicin nephropathy in the laboratory mouse. J Am Soc Nephrol 17(7):1796–1800

    CAS  PubMed  Google Scholar 

  • Zheng Y et al (2016) MiR-181b promotes chemoresistance in breast cancer by regulating Bim expression. Oncol Rep 35(2):683–690

    CAS  PubMed  Google Scholar 

  • Zheng SZ et al (2019) MiR-34a overexpression enhances the inhibitory effect of doxorubicin on HepG2 cells. World J Gastroenterol 25(22):2752–2762

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou B et al (2018a) Long noncoding RNA SNHG12 mediates doxorubicin resistance of osteosarcoma via miR-320a/MCL1 axis. Biomed Pharmacother 106:850–857

    CAS  PubMed  Google Scholar 

  • Zhou Z et al (2018b) The long noncoding RNA D63785 regulates chemotherapy sensitivity in human gastric cancer by targeting miR-422a. Mol Ther Nucleic Acids 12:405–419

    PubMed  PubMed Central  Google Scholar 

  • Zhou Y et al (2019) miR-223 overexpression inhibits doxorubicin-induced autophagy by targeting FOXO3a and reverses chemoresistance in hepatocellular carcinoma cells. Cell Death Dis 10(11):843

    PubMed  PubMed Central  Google Scholar 

  • Zhou W, Liu Y, Wu X (2021) Down-regulation of circITCH promotes osteosarcoma development and resistance to doxorubicin via the miR-524/RASSF6 axis. J Gene Med 23(10):e3373

    CAS  PubMed  Google Scholar 

  • Zhu J, Zhang F (2021) Circular RNA VANGL1 knockdown suppressed viability, promoted apoptosis, and increased doxorubicin sensitivity through targeting miR-145-5p to regulate SOX4 in bladder cancer cells. Open Med (wars) 16(1):1010–1021

    CAS  PubMed  Google Scholar 

  • Zhu LB et al (2021) De novosynthesis of pH-responsive, self-assembled, and targeted polypeptide nano-micelles for enhanced delivery of doxorubicin. Nanotechnology 32(29):295707

    CAS  Google Scholar 

  • Zou Z et al (2017) miR-495 sensitizes MDR cancer cells to the combination of doxorubicin and taxol by inhibiting MDR1 expression. J Cell Mol Med 21(9):1929–1943

    CAS  PubMed  PubMed Central  Google Scholar 

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Authors and Affiliations

  1. Department of Biology, Faculty of Science, Islamic Azad University, Science and Research Branch, Tehran, Iran

    Sepideh Mirzaei

  2. Farhikhtegan Medical Convergence Sciences Research Center, Farhikhtegan Hospital Tehran Medical Sciences, Islamic Azad University, Tehran, Iran

    Sepideh Mirzaei, Mahshid Deldar Abad Paskeh, Maliheh Entezari, Elahe Sadat Hejazi, Shamin Rezaei, Amirabbas kakavand, Maryam Aboutalebi, Afshin Taheriazam & Mehrdad Hashemi

  3. Department of Genetics, Faculty of Advanced Science and Technology, Tehran Medical Sciences, Islamic Azad University, Tehran, Iran

    Mahshid Deldar Abad Paskeh, Maliheh Entezari & Mehrdad Hashemi

  4. Department of Ophthalmology, Fauclty of Medicine, Tehran Medical Sciences Islamic Azad University, Tehran, Iran

    Farhad Adhami Moghadam

  5. Department of Cell and Molecular Biology, Faculty of Biological Sciences, Islamic Azad University, Tonekabon Branch, Tonekabon, Iran

    Zeinab Khazaei Koohpar

  6. Department of Food Hygiene and Quality Control, Division of Epidemiology, Faculty of Veterinary Medicine, University of Tehran, Tehran, Iran

    Mohammad Arad Zandieh

  7. Faculty of Veterinary Medicine, Islamic Azad University, Science and Research Branch, Tehran, Iran

    Romina Rajabi

  8. Department of Biochemistry and Molecular Biology, Faculty of Veterinary Medicine, Shahid Chamran University of Ahvaz, Ahvaz, Iran

    Shokooh Salimimoghadam

  9. Department of Orthopedics, Faculty of Medicine, Tehran Medical Sciences, Islamic Azad University, Tehran, Iran

    Afshin Taheriazam

  10. Healthy Ageing Research Centre, Neyshabur University of Medical Sciences, Neyshabur, Iran

    Saeed Samarghandian

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Mirzaei, S., Paskeh, M.D.A., Moghadam, F.A. et al. miRNAs as short non-coding RNAs in regulating doxorubicin resistance. J. Cell Commun. Signal. 17, 1181–1202 (2023). https://doi.org/10.1007/s12079-023-00789-0

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