1,399
Views
27
CrossRef citations to date
0
Altmetric
Research Paper

Methylation-mediated repression of MiR-424/503 cluster promotes proliferation and migration of ovarian cancer cells through targeting the hub gene KIF23

, , , , , & show all
Pages 1601-1618 | Received 18 Jan 2019, Accepted 10 May 2019, Published online: 09 Jun 2019

References

  • Bray F, Ferlay J, Soerjomataram I, et al. Global Cancer Statistics 2018: GLOBOCAN Estimates of Incidence and Mortality Worldwide for 36 Cancers in 185 Countries. CA Cancer J Clin. 2018 Sep 12 PubMed PMID: 30207593; eng. DOI:10.3322/caac.21492.
  • Fu X, Li Y, Alvero A, et al. MicroRNA-222-3p/GNAI2/AKT axis inhibits epithelial ovarian cancer cell growth and associates with good overall survival. Oncotarget. 2016 Dec 6;7(49):80633–80654. PubMed PMID: 27811362; PubMed Central PMCID: PMC5348346. eng.
  • Pan C, Stevic I, Müller V, et al. Exosomal microRNAs as tumor markers in epithelial ovarian cancer. Mol Oncol. 2018 Nov;12(11):1935–1948. . PubMed PMID: 30107086; PubMed Central PMCID: PMC6210043. eng.
  • Zhong Y, Yang S, Wang W, et al. The interaction of Lin28A/Rho associated coiled-coil containing protein kinase2 accelerates the malignancy of ovarian cancer. Oncogene. 2018 Sep 28 PubMed PMID: 30266988; eng. 10.1038/s41388-018-0512-9.
  • Bast RC Jr., Hennessy B, Mills GB. The biology of ovarian cancer: new opportunities for translation [Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov’t Review]. Nat Rev Cancer. 2009 Jun;9(6):415–428. . PubMed PMID: 19461667; PubMed Central PMCID: PMC2814299. eng.
  • Naora H, Montell DJ. Ovarian cancer metastasis: integrating insights from disparate model organisms [Review]. Nat Rev Cancer. 2005 May;5(5):355–366. . PubMed PMID: 15864277; eng.
  • Arvizo RR, Saha S, Wang E, et al. Inhibition of tumor growth and metastasis by a self-therapeutic nanoparticle [Research Support, N.I.H., Extramural]. Proc Natl Acad Sci U S A. 2013 Apr 23:110(17): 6700–6705. PubMed PMID: 23569259; PubMed Central PMCID: PMC3637766. eng.
  • Dragosavac S, Derchain S, Caserta NMG, et al. Staging recurrent ovarian cancer with (18)FDG PET/CT. Oncol Lett. 2013 Feb;5(2):593–597. . PubMed PMID: 23420711; PubMed Central PMCID: PMC3573129. eng.
  • Klopp AH, Zhang Y, Solley T, et al. Omental adipose tissue-derived stromal cells promote vascularization and growth of endometrial tumors [Research Support, N.I.H., Extramural]. Clin Cancer Res off J Am Assoc Cancer Res. 2012 Feb 1;18(3):771–782. PubMed PMID: 22167410; PubMed Central PMCID: PMC3481843. eng.
  • Kolonin MG. Progenitor cell mobilization from extramedullary organs [Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov’t Review]. Methods Mol Biol. 2012;904:243–252. PubMed PMID: 22890937; eng.
  • Miki H, Okada Y, Hirokawa N. Analysis of the kinesin superfamily: insights into structure and function [Research Support, Non-U.S. Gov’t Review]. Trends Cell Biol. 2005 Sep;15(9):467–476. . PubMed PMID: 16084724; eng.
  • Huszar D, Theoclitou ME, Skolnik J, et al. Kinesin motor proteins as targets for cancer therapy [Review]. Cancer Metastasis Rev. 2009 Jun;28(1–2):197–208. . PubMed PMID: 19156502; eng.
  • Hamam R, Hamam D, Alsaleh KA, et al. Circulating microRNAs in breast cancer: novel diagnostic and prognostic biomarkers [Review Research Support, Non-U.S. Gov’t]. Cell Death Dis. 2017 Sep 7;8(9):e3045. . PubMed PMID: 28880270; PubMed Central PMCID: PMC5636984. eng.
  • Troiano G, Boldrup L, Ardito F, et al. Circulating miRNAs from blood, plasma or serum as promising clinical biomarkers in oral squamous cell carcinoma: A systematic review of current findings [Review]. Oral Oncol. 2016 Dec;63:30–37. PubMed PMID: 27938997; eng.
  • Li J, Hu K, Gong G, et al. Upregulation of MiR-205 transcriptionally suppresses SMAD4 and PTEN and contributes to human ovarian cancer progression. Sci Rep. 2017 Feb 1;7:41330.
  • Esquela-Kerscher A, Slack FJ. Oncomirs - microRNAs with a role in cancer. Nat Rev Cancer. 2006 Apr;6(4):259–269. . PubMed PMID: 16557279; eng.
  • Sun X, Zhang J, Mukhopadhyay P. Dysfunctional miRNA-Mediated Regulation in Chromophobe Renal Cell Carcinoma. PubMed PMID: 27258182; PubMed Central PMCID: PMC4892590. eng PloS One. 2016;116:e0156324.
  • Chen Y, Min L, Ren C, et al. miRNA-148a serves as a prognostic factor and suppresses migration and invasion through Wnt1 in non-small cell lung cancer. PloS One. 2017;12(2):e0171751. PubMed PMID: 28199399; PubMed Central PMCID: PMC5310808. eng.
  • Sathyapalan T, David R, Gooderham NJ, et al. Increased expression of circulating miRNA-93 in women with polycystic ovary syndrome may represent a novel, non-invasive biomarker for diagnosis [Research Support, Non-U.S. Gov’t]. Sci Rep. 2015 Nov 19;5:16890.
  • Li J, Li L, Li Z, et al. The role of miR-205 in the VEGF-mediated promotion of human ovarian cancer cell invasion. Gynecol Oncol. 2015 Apr;137(1):125–133. . PubMed PMID: 25597268; eng.
  • Wu Q, Ren X, Zhang Y, et al. MiR-221-3p targets ARF4 and inhibits the proliferation and migration of epithelial ovarian cancer cells. Biochem Biophys Res Commun. 2018 Mar 18;497(4):1162–1170. PubMed PMID: 28057486; eng.
  • Nones K, Waddell N, Song S, et al. Genome-wide DNA methylation patterns in pancreatic ductal adenocarcinoma reveal epigenetic deregulation of SLIT-ROBO, ITGA2 and MET signaling. Int J Cancer. 2014 Sep 1;135(5):1110–1118. PubMed PMID: 24500968; eng.
  • Yang G, Chang B, Yang F, et al. Aurora kinase A promotes ovarian tumorigenesis through dysregulation of the cell cycle and suppression of BRCA2 [Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov’t]. Clin Cancer Res off J Am Assoc Cancer Res. 2010 Jun 15;16(12):3171–3181. PubMed PMID: 20423983; PubMed Central PMCID: PMC2930838. eng.
  • Davidson B, Nymoen DA, Elgaaen BV, et al. BUB1 mRNA is significantly co-expressed with AURKA and AURKB mRNA in advanced-stage ovarian serous carcinoma [Research Support, Non-U.S. Gov’t]. Virchows Arch. 2014 Jun;464(6):701–707. PubMed PMID: 24756216; eng.
  • de Resende MF, Vieira S, Chinen LT, et al. Prognostication of prostate cancer based on TOP2A protein and gene assessment: TOP2A in prostate cancer [Research Support, Non-U.S. Gov’t]. J Transl Med. 2013 Feb 11;11:36. PubMed PMID: 23398928; PubMed Central PMCID: PMC3576277. eng. DOI: 10.1186/1479-5876-11-36
  • Cao Y, Zhang G, Wang P, et al. Clinical significance of UGT1A1 polymorphism and expression of ERCC1, BRCA1, TYMS, RRM1, TUBB3, STMN1 and TOP2A in gastric cancer. BMC Gastroenterol. 2017 Jan 5;17(1):2. PubMed PMID: 28056823; PubMed Central PMCID: PMC5217235. eng.
  • Zheng H, Li X, Chen C, et al. Quantum dot-based immunofluorescent imaging and quantitative detection of TOP2A and prognostic value in triple-negative breast cancer. Int J Nanomedicine. 2016;11:5519–5529. PubMed PMID: 27799773; PubMed Central PMCID: PMC5085300. eng.
  • Kang K, Nho CW, Kim ND, et al. Daurinol, a catalytic inhibitor of topoisomerase IIalpha, suppresses SNU-840 ovarian cancer cell proliferation through cell cycle arrest in S phase [Research Support, Non-U.S. Gov’t]. Int J Oncol. 2014 Aug;45(2):558–566. PubMed PMID: 24841075; eng.
  • Glotzer M. The molecular requirements for cytokinesis [Research Support, Non-U.S. Gov’t Review]. Science. 2005 Mar 18;307(5716):1735–1739. . PubMed PMID: 15774750; eng.
  • Neef R, Klein UR, Kopajtich R, et al. Cooperation between mitotic kinesins controls the late stages of cytokinesis [Comparative Study Research Support, Non-U.S. Gov’t]. Curr Biol. 2006 Feb 7;16(3):301–307. . PubMed PMID: 16461284; eng.
  • Wu WD, Yu KW, Zhong N, et al. Roles and mechanisms of Kinesin-6 KIF20A in spindle organization during cell division. Eur J Cell Biol. 2018 Dec 16. PubMed PMID: 30579662; eng. 10.1016/j.ejcb.2018.12.002
  • Kamimoto T, Zama T, Aoki R, et al. Identification of a novel kinesin-related protein, KRMP1, as a target for mitotic peptidyl-prolyl isomerase Pin1. J Biol Chem. 2001 Oct 5;276(40):37520–37528. . PubMed PMID: 11470801; eng.
  • Nislow C, Sellitto C, Kuriyama R, et al. A monoclonal antibody to a mitotic microtubule-associated protein blocks mitotic progression. J Cell Biol. 1990 Aug;111(2):511–522. PubMed PMID: 2199459; PubMed Central PMCID: PMC2116221. eng.
  • Zhao X, Zhou LL, Li X, et al. Overexpression of KIF20A confers malignant phenotype of lung adenocarcinoma by promoting cell proliferation and inhibiting apoptosis. Cancer Med. 2018 Sep;7(9):4678–4689. . PubMed PMID: 30105795; PubMed Central PMCID: PMC6143951. eng.
  • Sablin EP. Kinesins and microtubules: their structures and motor mechanisms. Curr Opin Cell Biol. 2000 Feb;12(1):35–41. PubMed PMID: 10679355; eng.
  • Kline-Smith SL, Walczak CE. Mitotic spindle assembly and chromosome segregation: refocusing on microtubule dynamics [Research Support, Non-U.S. Gov’t Research Support, U.S. Gov’t, P.H.S. Review]. Mol Cell. 2004 Aug 13;15(3):317–327. . PubMed PMID: 15304213; eng.
  • Bandres E, Agirre X, Bitarte N, et al. Epigenetic regulation of microRNA expression in colorectal cancer. Int J Cancer. 2009 Dec 1;125(11):2737–2743. . PubMed PMID: 19521961; eng.
  • He Y, Cui Y, Wang W, et al. Hypomethylation of the hsa-miR-191 locus causes high expression of hsa-mir-191 and promotes the epithelial-to-mesenchymal transition in hepatocellular carcinoma. Neoplasia (New York, NY). 2011 Sep;13(9):841-IN23. PubMed PMID: 21969817; PubMed Central PMCID: PMC3182276. eng.
  • Minor J, Wang X, Zhang F, et al. Methylation of microRNA-9 is a specific and sensitive biomarker for oral and oropharyngeal squamous cell carcinomas. Oral Oncol. 2012 Jan;48(1):73–78. PubMed PMID: 22133638; PubMed Central PMCID: PMC3291120. eng.
  • de Souza Rocha Simonini P, Breiling A, Gupta N, et al. Epigenetically deregulated microRNA-375 is involved in a positive feedback loop with estrogen receptor alpha in breast cancer cells. Cancer Res. 2010 Nov 15;70(22):9175–9184. PubMed PMID: 20978187; eng.
  • Kunej T, Godnic I, Ferdin J, et al. Epigenetic regulation of microRNAs in cancer: an integrated review of literature. Mutat Res. 2011 Dec 1;717(1–2):77–84. . PubMed PMID: 21420983; eng.
  • Green RA, Paluch E, Oegema K. Cytokinesis in animal cells [Research Support, Non-U.S. Gov’t Review]. Annu Rev Cell Dev Biol. 2012;28:29–58. PubMed PMID: 22804577; eng.
  • Liljeholm M, Irvine AF, Vikberg AL, et al. Congenital dyserythropoietic anemia type III (CDA III) is caused by a mutation in kinesin family member, KIF23. Blood. 2013 Jun 6;121(23):4791–4799. . PubMed PMID: 23570799; eng.
  • Vasiliev JM, Gelfand IM, Domnina LV, et al. Effect of colcemid on the locomotory behaviour of fibroblasts. J Embryol Exp Morphol. 1970 Nov;24(3):625–640. PubMed PMID: 4923996; eng.
  • Sun L, Zhang C, Yang Z, et al. KIF23 is an independent prognostic biomarker in glioma, transcriptionally regulated by TCF-4. Oncotarget. 2016 Apr 26;7(17):24646–24655. . PubMed PMID: 27013586; PubMed Central PMCID: PMC5029730. eng.
  • Takahashi S, Fusaki N, Ohta S, et al. Downregulation of KIF23 suppresses glioma proliferation [Research Support, Non-U.S. Gov’t]. J Neurooncol. 2012 Feb;106(3):519–529. . PubMed PMID: 21904957; eng.
  • Kato T, Wada H, Patel P, et al. Overexpression of KIF23 predicts clinical outcome in primary lung cancer patients. Lung Cancer. 2016 Feb;92:53–61. PubMed PMID: 26775597; eng.
  • Iltzsche F, Simon K, Stopp S, et al. An important role for Myb-MuvB and its target gene KIF23 in a mouse model of lung adenocarcinoma [Research Support, Non-U.S. Gov’t]. Oncogene. 2017 Jan 5;36(1):110–121. PubMed PMID: 27212033; eng.
  • Rissland Olivia S, Hong S-J, Bartel David P. MicroRNA Destabilization Enables Dynamic Regulation of the miR-16 Family in Response to Cell-Cycle Changes. Mol Cell. 2011;43(6):993–1004.
  • Li Y, Li W, Ying Z, et al. Metastatic heterogeneity of breast cancer cells is associated with expression of a heterogeneous TGFbeta-activating miR424-503 gene cluster. Cancer Res. 2014 Nov 1;74(21):6107–6118. . PubMed PMID: 25164015; eng.
  • De Mariano M, Stigliani S, Moretti S, et al. A genome-wide microRNA profiling indicates miR-424-5p and miR-503-5p as regulators of ALK expression in neuroblastoma. Oncotarget. 2017 Aug 22;8(34):56518–56532. . PubMed PMID: 28915608; PubMed Central PMCID: PMC5593579. eng.
  • Liu J, Gu Z, Tang Y, et al. Tumour-suppressive microRNA-424-5p directly targets CCNE1 as potential prognostic markers in epithelial ovarian cancer. PubMed PMID: 29228869; PubMed Central PMCID: PMC5914728. eng Cell Cycle. 2018;173:309–318.
  • Wu X, Ruan Y, Jiang H, et al. MicroRNA-424 inhibits cell migration, invasion, and epithelial mesenchymal transition by downregulating doublecortin-like kinase 1 in ovarian clear cell carcinoma. Int J Biochem Cell Biol. 2017 Apr;85:66–74. PubMed PMID: 28161486; eng.
  • Caporali A, Emanueli C. MicroRNA-503 and the extended microRNA-16 family in angiogenesis [Research Support, Non-U.S. Gov’t Review]. Trends Cardiovasc Med. 2011 Aug;21(6):162–166. . PubMed PMID: 22814423; PubMed Central PMCID: PMC3407871. eng.
  • Soto-Reyes E, Gonzalez-Barrios R, Cisneros-Soberanis F, et al. Disruption of CTCF at the miR-125b1 locus in gynecological cancers. BMC Cancer. 2012 Jan 25;12:40. PubMed PMID: 22277129; PubMed Central PMCID: PMC3297514. eng.
  • Wu CT, Lin WY, Chang YH, et al. DNMT1-dependent suppression of microRNA424 regulates tumor progression in human bladder cancer. Oncotarget. 2015 Sep 15;6(27):24119–24131. . PubMed PMID: 26090723; PubMed Central PMCID: PMC4695174. eng.
  • Jin C, Li M, Ouyang Y, et al. MiR-424 functions as a tumor suppressor in glioma cells and is down-regulated by DNA methylation. J Neurooncol. 2017 Jun;133(2):247–255. . PubMed PMID: 28508328; eng.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.