Display options
Share it on

Mol Cell Biochem. 2022 Jan;477(1):307-317. doi: 10.1007/s11010-021-04271-6. Epub 2021 Oct 30.

miR-874-3p mitigates cisplatin resistance through modulating NF-κB/inhibitor of apoptosis protein signaling pathway in epithelial ovarian cancer cells.

Molecular and cellular biochemistry

Ying Wang, Chenming Yan, Junxia Qi, Chunyan Liu, Juan Yu, Huabin Wang

Affiliations

  1. Department of Obstetrics and Gynecology, Sichuan Tianfu New Area People's Hospital, Chengdu, China.
  2. Department of Obstetrics and Gynecology, Cixian People's Hospital, Cixian, China.
  3. Department of Obstetrics and Gynecology, Handan PuHui Obstetrics and Gynecology Hospital, Handan, China.
  4. Department of Gynecology, Jintang County Maternity and Child Health Hospital, No. 6, Jinquan Road, Jintang County, Chengdu, China. [email protected].

PMID: 34716858 DOI: 10.1007/s11010-021-04271-6

Abstract

The resistance to cisplatin, the most common platinum chemotherapy drug, may confine the efficacy of treatment in epithelial ovarian cancer patients. Aberrant expression of inhibitor of apoptosis proteins set the stage for resistance to cisplatin in EOC; besides, chemosensitivity in EOC can be chalked up to dysregulation of specific miRNAs. Herein, we investigated whether there is a potential correlation between miR-874-3p and the X-chromosome-linked inhibitor of apoptosis, a member of the IAP protein family in cisplatin-resistant EOC cells. The lower expression of miR-874-3p was found in SKOV3-DDP cells; it was also in association with cisplatin-resistance in EOC cells. XIAP was found to contribute to developing platinum resistance and is an authentic target for miR-874-3p in SKOV3-DDP cells. Consistently, restoration of miR-874-3p expression reversed cisplatin resistance in such cells by modulating XIAP and NF-κB/Survivin signaling pathway. Besides, siRNA knock down of XIAP in SKOV3-DDP cells had an anti-migratory effect like those with miR-874 overexpression. Importantly, the enforced expression of XIAP rescued SKOV3-DDP cells from the cytotoxic effects of miR-874-3p. Finally, miR-874-3p sensitized EOC cells to cisplatin-induced apoptosis, at least in part, through targeting XIAP. The cytotoxic effects of miR-874-3p can be attributed to the targeting XIAP in cisplatin-resistant EOC cells. We believe that the combination of cisplatin with miR-874-3p may make a potential strategy to reverse cisplatin resistance.

© 2021. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.

Keywords: Chemoresistance; Cisplatin; EOC; XIAP; miR-874-3p

References

  1. Desai A, Xu J, Aysola K, Qin Y, Okoli C, Hariprasad R, Chinemerem U, Gates C, Reddy A, Danner O (2014) Epithelial ovarian cancer: an overview. World J Trans Med 3:1 - PubMed
  2. Gentry-Maharaj A, Menon U (2012) Screening for ovarian cancer in the general population. Best Pract Res Clin Obstet Gynaecol 26:243–256 - PubMed
  3. Guleria S, Jensen A, Toender A, Kjaer SK (2020) Risk of epithelial ovarian cancer among women with benign ovarian tumors: a follow-up study. Cancer Causes Control 31:25–31 - PubMed
  4. Pignata S, Cannella L, Leopardo D, Pisano C, Bruni GS, Facchini G (2011) Chemotherapy in epithelial ovarian cancer. Cancer Lett 303:73–83 - PubMed
  5. Kurman RJ, Shih I-M (2010) The Origin and pathogenesis of epithelial ovarian cancer-a proposed unifying theory. Am J Surg Pathol 34:433 - PubMed
  6. Lorusso D, Ceni V, Daniele G, Salutari V, Pietragalla A, Muratore M, Nero C, Ciccarone F and Scambia G (2020) Newly diagnosed ovarian cancer: which first-line treatment? Cancer Treat Rev. - PubMed
  7. Rathore R, McCallum JE, Varghese E, Florea A-M, Büsselberg D (2017) Overcoming chemotherapy drug resistance by targeting inhibitors of apoptosis proteins (IAPs). Apoptosis 22:898–919 - PubMed
  8. Chaudhary AK, Yadav N, Bhat TA, O’Malley J, Kumar S, Chandra D (2016) A potential role of X-linked inhibitor of apoptosis protein in mitochondrial membrane permeabilization and its implication in cancer therapy. Drug Discovery Today 21:38–47 - PubMed
  9. Zhang Y, Huang F, Luo Q, Wu X, Liu Z, Chen H, Huang Y (2018) Inhibition of XIAP increases carboplatin sensitivity in ovarian cancer. Onco Targets Ther 11:8751 - PubMed
  10. Altieri DC (2015) Survivin–the inconvenient IAP. Seminars in cell & developmental biology, Elsevier, pp. 91–96 - PubMed
  11. Peery RC, Liu J-Y, Zhang J-T (2017) Targeting survivin for therapeutic discovery: past, present, and future promises. Drug Discovery Today 22:1466–1477 - PubMed
  12. Arora V, Cheung HH, Plenchette S, Micali OC, Liston P, Korneluk RG (2007) Degradation of survivin by the X-linked inhibitor of apoptosis (XIAP)-XAF1 complex. J Biol Chem 282:26202–26209 - PubMed
  13. Boidot R, Végran F, Lizard-Nacol S (2014) Transcriptional regulation of the survivin gene. Mol Biol Rep 41:233–240 - PubMed
  14. Tracey L, Pérez-Rosado A, Artiga MJ, Camacho FI, Rodríguez A, Martínez N, Ruiz-Ballesteros E, Mollejo M, Martinez B, Cuadros M (2005) Expression of the NF-κB targets BCL2 and BIRC5/Survivin characterizes small B-cell and aggressive B-cell lymphomas, respectively. J Pathol 206:123–134 - PubMed
  15. Di Leva G, Garofalo M and Croce C (2013) MicroRNAs in Cancer. MicroRNAs in Cancer. MicroRNAs in Cancer. Ann Rev Pathol. - PubMed
  16. Babashah S, Soleimani M (2011) The oncogenic and tumour suppressive roles of microRNAs in cancer and apoptosis. Eur J Cancer 47:1127–1137 - PubMed
  17. Garofalo M, Croce CM (2013) MicroRNAs as therapeutic targets in chemoresistance. Drug Resist Updates 16:47–59 - PubMed
  18. Li Z, Hu S, Wang J, Cai J, Xiao L, Yu L, Wang Z (2010) MiR-27a modulates MDR1/P-glycoprotein expression by targeting HIPK2 in human ovarian cancer cells. Gynecol Oncol 119:125–130 - PubMed
  19. Livak KJ and Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCT method. Methods 25:402–408. - PubMed
  20. Agarwal V, Bell GW, Nam J-W and Bartel DP (2015) Predicting effective microRNA target sites in mammalian mRNAs. elife 4:e05005. - PubMed
  21. Ding X, Mohd A, Huang Z, Baba T, Bernardini M, Lyerly H, Berchuck A, Murphy S, Buermeyer A, Devi G (2009) MLH1 expression sensitises ovarian cancer cells to cell death mediated by XIAP inhibition. Br J Cancer 101:269–277 - PubMed
  22. Wang Y, Mao H, Hao Q, Wang Y, Yang Y, Shen L, Huang S, Liu P (2012) Association of expression of XIAP-associated factor 1 (XAF1) with clinicopathologic factors, overall survival, microvessel density and cisplatin-resistance in ovarian cancer. Regul Pept 178:36–42 - PubMed
  23. Xia Y, Shen S, Verma I (2014) NF-κB, an active player in human cancers. Cancer Immunol Res 2:823–830 - PubMed
  24. Lu M, Lin S-C, Huang Y, Kang YJ, Rich R, Lo Y-C, Myszka D, Han J, Wu H (2007) XIAP induces NF-κB activation via the BIR1/TAB1 interaction and BIR1 dimerization. Mol Cell 26:689–702 - PubMed
  25. Cui X, Shen D, Kong C, Zhang Z, Zeng Y, Lin X, Liu X (2017) NF-κB suppresses apoptosis and promotes bladder cancer cell proliferation by upregulating survivin expression in vitro and in vivo. Sci Rep 7:1–13 - PubMed
  26. Altieri DC (2010) Survivin and IAP proteins in cell-death mechanisms. Biochemical Journal 430:199–205 - PubMed
  27. Rabik CA, Dolan ME (2007) Molecular mechanisms of resistance and toxicity associated with platinating agents. Cancer Treat Rev 33:9–23 - PubMed
  28. Wu M, Yuan S, Szporn AH, Gan L, Shtilbans V, Burstein DE (2005) Immunocytochemical detection of XIAP in body cavity effusions and washes. Mod Pathol 18:1618–1622 - PubMed
  29. Fernandez-Capetillo O, Chen H-T, Celeste A, Ward I, Romanienko PJ, Morales JC, Naka K, Xia Z, Camerini-Otero RD, Motoyama N (2002) DNA damage-induced G 2–M checkpoint activation by histone H2AX and 53BP1. Nat Cell Biol 4:993–997 - PubMed
  30. Arts H, Van Der Zee A, De Jong S, De Vries E (2000) Options for modulation of drug resistance in ovarian cancer. Int J Gynecol Cancer 10:47–52 - PubMed
  31. Gyrd-Hansen M, Meier P (2010) IAPs: from caspase inhibitors to modulators of NF-κB, inflammation and cancer. Nat Rev Cancer 10:561–574 - PubMed
  32. Altieri DC (2008) Survivin, cancer networks and pathway-directed drug discovery. Nat Rev Cancer 8:61–70 - PubMed
  33. Ghosh G, Wang VYF, Huang DB, Fusco A (2012) NF-κB regulation: lessons from structures. Immunol Rev 246:36–58 - PubMed
  34. Egodwin P, Baird A, Heavey S, Barr M, O’Byrne K, Gately K (2013) Targeting nuclear factor-Kappa B to overcome resistance to chemotherapy. Front Oncol 3:120 - PubMed
  35. Si W, Shen J, Zheng H, Fan W (2019) The role and mechanisms of action of microRNAs in cancer drug resistance. Clin Epigenetics 11:1–24 - PubMed
  36. Wang S, Li M-Y, Liu Y, Vlantis AC, Chan JY, Xue L, Hu B-G, Yang S, Chen M-X, Zhou S (2020) The role of microRNA in cisplatin resistance or sensitivity. Expert Opin Ther Targets 24:885–897 - PubMed
  37. Xia J-t, Chen L-z, Jian W-h, Wang K-B, Yang Y-z, He W-l, He Y-l, Chen D, Li W (2014) MicroRNA-362 induces cell proliferation and apoptosis resistance in gastric cancer by activation of NF-κB signaling. J Transl Med 12:1–12 - PubMed
  38. Jiang P, Jia W, Wei X, Zhang X, Wang C, Li B, Song T, Yang J, Zhu D, Meng Y (2017) MicroRNA-146a regulates cisplatin-resistance of non-small cell lung cancer cells by targeting NF-κB pathway. Int J Clin Exp Pathol 10:11545 - PubMed
  39. Huang R-s, Zheng Y-l, Zhao J, Chun X (2018) microRNA-381 suppresses the growth and increases cisplatin sensitivity in non-small cell lung cancer cells through inhibition of nuclear factor-κB signaling. Biomed Pharmacother 98:538–544 - PubMed
  40. Zhang L, Sun S, Li W, Feng Z, Xu X, Zhuang Q, Fang J (2015) Decreased expression of tumor suppressive miR-874 and its clinical significance in human osteosarcoma. Genet Mol Res 14:18315–18324 - PubMed
  41. Dong D, Gong Y, Zhang D, Bao H, Gu G (2016) miR-874 suppresses the proliferation and metastasis of osteosarcoma by targeting E2F3. Tumor Biol 37:6447–6455 - PubMed
  42. Fisher JN, Terao M, Fratelli M, Kurosaki M, Paroni G, Zanetti A, Gianni M, Bolis M, Lupi M, Tsykin A (2015) MicroRNA networks regulated by all-trans retinoic acid and Lapatinib control the growth, survival and motility of breast cancer cells. Oncotarget 6:13176 - PubMed
  43. Wang L, Gao W, Hu F, Xu Z, Wang F (2014) MicroRNA-874 inhibits cell proliferation and induces apoptosis in human breast cancer by targeting CDK9. FEBS Lett 588:4527–4535 - PubMed
  44. Jiang B, Li Z, Zhang W, Wang H, Zhi X, Feng J, Chen Z, Zhu Y, Yang L, Xu H (2014) miR-874 Inhibits cell proliferation, migration and invasion through targeting aquaporin-3 in gastric cancer. J Gastroenterol 49:1011–1025 - PubMed
  45. Kesanakurti D, Maddirela DR, Chittivelu S, Rao JS, Chetty C (2013) Suppression of tumor cell invasiveness and in vivo tumor growth by microRNA-874 in non-small cell lung cancer. Biochem Biophys Res Commun 434:627–633 - PubMed
  46. Que K, Tong Y, Que G, Li L, Lin H, Huang S, Wang R, Tang L (2017) Downregulation of miR-874-3p promotes chemotherapeutic resistance in colorectal cancer via inactivation of the Hippo signaling pathway. Oncol Rep 38:3376–3386 - PubMed
  47. Han J, Liu Z, Wang N, Pan W (2016) MicroRNA-874 inhibits growth, induces apoptosis and reverses chemoresistance in colorectal cancer by targeting X-linked inhibitor of apoptosis protein. Oncol Rep 36:542–550 - PubMed
  48. Ma H, Cao W, Ding M (2020) MicroRNA-31 weakens cisplatin resistance of medulloblastoma cells via NF-κB and PI3K/AKT pathways. BioFactors 46:831–838 - PubMed
  49. Ma Y, Zhou G, Li M, Hu D, Zhang L, Liu P, Lin K (2018) Long noncoding RNA DANCR mediates cisplatin resistance in glioma cells via activating AXL/PI3K/Akt/NF-κB signaling pathway. Neurochem Int 118:233–241 - PubMed

Publication Types