Expression analysis of progesterone‑regulated miRNAs in cells derived from human glioblastoma
- Authors:
- Diana Elisa Velázquez‑Vázquez
- Aylin Del Moral‑Morales
- Jenie Marian Cruz‑Burgos
- Eduardo Martínez‑Martínez
- Mauricio Rodríguez‑Dorantes
- Ignacio Camacho‑Αrroyo
-
Affiliations: Unidad de Investigación en Reproducción Humana, Instituto Nacional de Perinatología‑Facultad de Química, Universidad Nacional Autónoma de México, Mexico City 04510, Mexico, Oncogenomics Laboratory, The National Institute of Genomic Medicine, Mexico City 14610, Mexico, Laboratory of Cell Communication and Extracellular Vesicles, The National Institute of Genomic Medicine, Mexico City 14610, Mexico - Published online on: April 22, 2021 https://doi.org/10.3892/mmr.2021.12114
- Article Number: 475
-
Copyright: © Velázquez‑Vázquez et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
This article is mentioned in:
Abstract
Wen PY and Kesari S: Malignant gliomas in adults. N Engl J Med. 359:492–507. 2008. View Article : Google Scholar : PubMed/NCBI | |
Urbanska K, Sokolowska J, Szmidt M and Sysa P: Glioblastoma multiforme-An overview. Contemp Oncol (Pozn). 18:307–312. 2014.PubMed/NCBI | |
Weller M, Wick W, Aldape K, Brada M, Berger M, Pfister SM, Nishikawa R, Rosenthal M, Wen PY, Stupp R and Reifenberger G: Glioma. Nat Rev Dis Primers. 1:150172015. View Article : Google Scholar : PubMed/NCBI | |
Ostrom QT, Gittleman H, Liao P, Vecchione-Koval T, Wolinsky Y, Kruchko C and Barnholtz-Sloan JS: CBTRUS statistical report: Primary brain and other central nervous system tumors diagnosed in the United States in 2010–2014. Neuro Oncol. 19 (Suppl 5):v1–v88. 2017. View Article : Google Scholar : PubMed/NCBI | |
Ciafrè SA, Galardi S, Mangiola A, Ferracin M, Liu CG, Sabatino G, Negrini M, Maira G, Croce CM and Farace MG: Extensive modulation of a set of microRNAs in primary glioblastoma. Biochem Biophys Res Commun. 334:1351–1358. 2005. View Article : Google Scholar | |
Novakova J, Slaby O, Vyzula R and Michalek J: MicroRNA involvement in glioblastoma pathogenesis. Biochem Biophys Res Commun. 386:1–5. 2009. View Article : Google Scholar : PubMed/NCBI | |
Aldaz B, Sagardoy A, Nogueira L, Guruceaga E, Grande L, Huse JT, Aznar MA, Díez-Valle R, Tejada-Solís S, Alonso MM, et al: Involvement of miRNAs in the differentiation of human glioblastoma multiforme stem-like cells. PLoS One. 8:e770982013. View Article : Google Scholar : PubMed/NCBI | |
Alfardus H, Mcintyre A and Smith S: MicroRNA regulation of glycolytic metabolism in glioblastoma. Biomed Res Int. 2017:91573702017. View Article : Google Scholar : PubMed/NCBI | |
Mercatelli N, Galardi S and Ciafrè SA: MicroRNAs as multifaceted players in glioblastoma multiforme. Int Rev Cell Mol Biol. 333:269–323. 2017. View Article : Google Scholar : PubMed/NCBI | |
Sana J, Busek P, Fadrus P, Besse A, Radova L, Vecera M, Reguli S, Stollinova Sromova L, Hilser M, Lipina R, et al: Identification of microRNAs differentially expressed in glioblastoma stem-like cells and their association with patient survival. Sci Rep. 8:28362018. View Article : Google Scholar : PubMed/NCBI | |
Ceballos-Chávez M, Subtil-Rodríguez A, Giannopoulou EG, Soronellas D, Vázquez-Chávez E, Vicent GP, Elemento O, Beato M and Reyes JC: The chromatin remodeler CHD8 is required for activation of progesterone receptor-dependent enhancers. PLoS Genet. 11:e10051742015. View Article : Google Scholar | |
Helsen C and Claessens F: Looking at nuclear receptors from a new angle. Mol Cell Endocrinol. 382:97–106. 2013. View Article : Google Scholar : PubMed/NCBI | |
Jacobsen BM and Horwitz KB: Progesterone receptors, their isoforms and progesterone regulated transcription. Mol Cell Endocrinol. 357:18–29. 2012. View Article : Google Scholar : PubMed/NCBI | |
González-Agüero G, Gutiérrez AA, González-Espinosa D, Solano JD, Morales R, González-Arenas A, Cabrera-Muñoz E and Camacho-Arroyo I: Progesterone effects on cell growth of U373 and D54 human astrocytoma cell lines. Endocrine. 32:129–135. 2007. View Article : Google Scholar | |
Piña-Medina AG, Hansberg-Pastor V, González-Arenas A, Cerbón M and Camacho-Arroyo I: Progesterone promotes cell migration, invasion and cofilin activation in human astrocytoma cells. Steroids. 105:19–25. 2016. View Article : Google Scholar | |
Germán-Castelán L, Manjarrez-Marmolejo J, González-Arenas A, González-Morán MG and Camacho-Arroyo I: Progesterone induces the growth and infiltration of human astrocytoma cells implanted in the cerebral cortex of the rat. Biomed Res Int. 2014:3931742014. View Article : Google Scholar | |
González-Arenas A, Cabrera-Wrooman A, Díaz NF, González- García TK, Salido-Guadarrama I, Rodríguez-Dorantes M and Camacho-Arroyo I: Progesterone receptor subcellular localization and gene expression profile in human astrocytoma cells are modified by progesterone. Nucl Recept Res. 1:1–10. 2014. View Article : Google Scholar | |
Zamora-Sánchez CJ, Hansberg-Pastor V, Salido-Guadarrama I, Rodríguez-Dorantes M and Camacho-Arroyo I: Allopregnanolone promotes proliferation and differential gene expression in human glioblastoma cells. Steroids. 119:36–42. 2017. View Article : Google Scholar | |
Zamora-Sánchez CJ, Del Moral-Morales A, Hernández-Vega AM, Hansberg-Pastor V, Salido-Guadarrama I, Rodríguez-Dorantes M and Camacho-Arroyo I: Allopregnanolone alters the gene expression profile of human glioblastoma cells. Int J Mol Sci. 19:8642018. View Article : Google Scholar | |
Hernández-Hernández OT, González-García TK and Camacho-Arroyo I: Progesterone receptor and SRC-1 participate in the regulation of VEGF, EGFR and cyclin D1 expression in human astrocytoma cell lines. J Steroid Biochem Mol Biol. 132:127–134. 2012. View Article : Google Scholar | |
Wendler A, Keller D, Albrecht C, Peluso JJ and Wehiling M: Involvement of let-7/miR-98 microRNAs in the regulation of progesterone receptor membrane component 1 expression in ovarian cancer cells. Oncol Rep. 25:273–279. 2011.PubMed/NCBI | |
Cittelly DM, Finlay-Schultz J, Howe EN, Spoelstra NS, Axlund SD, Hendricks P, Jacobsen BM, Sartorius CA and Richer JK: Progestin suppression of miR-29 potentiates dedifferentiation of breast cancer cells via KLF4. Oncogene. 32:2555–2564. 2013. View Article : Google Scholar : PubMed/NCBI | |
Rivas MA, Venturutti L, Huang YW, Schillaci R, Huang TH and Elizalde PV: Downregulation of the tumor-suppressor miR-16 via progestin-mediated oncogenic signaling contributes to breast cancer development. Breast Cancer Res. 14:R772012. View Article : Google Scholar : PubMed/NCBI | |
Romero-Cordoba S, Rodriguez-Cuevas S, Rebollar-Vega R, Quintanar-Jurado V, Maffuz-Aziz A, Jimenez-Sanchez G, Bautista-Piña V, Arellano-Llamas R and Hidalgo-Miranda A: Identification and pathway analysis of microRNAs with no previous involvement in breast cancer. PLoS One. 7:e319042012. View Article : Google Scholar : PubMed/NCBI | |
Cochrane DR, Jacobsen BM, Connaghan KD, Howe EN, Bain DL and Richer JK: Progestin regulated miRNAs that mediate progesterone receptor action in breast cancer. Mol Cell Endocrinol. 355:15–24. 2012. View Article : Google Scholar : PubMed/NCBI | |
Finlay-Schultz J, Cittelly DM, Hendricks P, Patel P, Kabos P, Jacobsen BM, Richer JK and Sartorius CA: Progesterone downregulation of miR-141 contributes to expansion of stem-like breast cancer cells through maintenance of progesterone receptor and Stat5a. Oncogene. 34:3676–3687. 2015. View Article : Google Scholar : PubMed/NCBI | |
Fletcher CE, Dart DA and Bevan CL: Interplay between steroid signalling and microRNAs: Implications for hormone-dependent cancers. Endocr Relat Cancer. 21:R409–R429. 2014. View Article : Google Scholar : PubMed/NCBI | |
Godbole M, Chandrani P, Gardi N, Dhamne H, Patel K, Yadav N, Gupta S, Badwe R and Dutt A: miR-129-2 mediates down-regulation of progesterone receptor in response to progesterone in breast cancer cells. Cancer Biol Ther. 18:801–805. 2017. View Article : Google Scholar : PubMed/NCBI | |
McFall T, McKnight B, Rosati R, Kim S, Huang Y, Viola-Villegas N and Ratnam M: Progesterone receptor A promotes invasiveness and metastasis of luminal breast cancer by suppressing regulation of critical microRNAs by estrogen. J Biol Chem. 293:1163–1177. 2018. View Article : Google Scholar : PubMed/NCBI | |
Nie L, Zhao YB, Pan JL, Lei Y, Liu M, Long Y, Zhang JH, Hu Y, Xu MQ, Yuan DZ and Yue LM: Progesterone-Induced miR-152 inhibits the proliferation of endometrial epithelial cells by downregulating WNT-1. Reprod Sci. 24:1444–1453. 2017. View Article : Google Scholar : PubMed/NCBI | |
Smyth GK: limma: Linear models for microarray data. Bioinformatics and Computational Biology Solutions Using R and Bioconductor. Gentleman R, Carey VJ, Huber W, Irizarry RA and Dudoit S: Springer; New York, NY: pp. 397–420. 2005, View Article : Google Scholar | |
R Core Team: R: A language and environment for statistical computing. R Foundation for Statistical Computing; Vienna, Austria: 2018, http://www.R-project.org/ | |
Karagkouni D, Paraskevopoulou MD, Chatzopoulos S, Vlachos IS, Tastsoglou S, Kanellos I, Papadimitriou D, Kavakiotis I, Maniou S, Skoufos G, et al: DIANA-TarBase v8: A decade-long collection of experimentally supported miRNA-gene interactions. Nucleic Acids Res. 46(D1): D239–D245. 2018. View Article : Google Scholar : PubMed/NCBI | |
Dweep H, Gretz N and Sticht C: MiRWalk database for miRNA-target interactions. Methods Mol Biol. 1182:289–305. 2014. View Article : Google Scholar : PubMed/NCBI | |
Paraskevopoulou MD, Georgakilas G, Kostoulas N, Vlachos IS, Vergoulis T, Reczko M, Filippidis C, Dalamagas T and Hatzigeorgiou AG: DIANA-microT web server v5.0: Service integration into miRNA functional analysis workflows. Nucleic Acids Res. 41((Web Server Issue)): W169–W73. 2013. View Article : Google Scholar : PubMed/NCBI | |
Agarwal V, Bell GW, Nam JW and Bartel DP: Predicting effective microRNA target sites in mammalian mRNAs. Elife. 4:e050052015. View Article : Google Scholar : PubMed/NCBI | |
Chen EY, Tan CM, Kou Y, Duan Q, Wang Z, Meirelles GV, Clark NR and Ma'ayan A: Enrichr: Interactive and collaborative HTML5 gene list enrichment analysis tool. BMC Bioinformatics. 14:1282013. View Article : Google Scholar : PubMed/NCBI | |
Gene Ontology Consortium, . Gene ontology consortium: Going forward. Nucleic Acids Res. 43((Database issue)): D1049–D1056. 2015.PubMed/NCBI | |
Kanehisa M, Furumichi M, Tanabe M, Sato Y and Morishima K: KEGG: New perspectives on genomes, pathways, diseases and drugs. Nucleic Acids Res. 45(D1): D353–D361. 2017. View Article : Google Scholar : PubMed/NCBI | |
Szklarczyk D, Morris JH, Cook H, Kuhn M, Wyder S, Simonovic M, Santos A, Doncheva NT, Roth A, Bork P, et al: The STRING database in 2017: Quality-controlled protein-protein association networks, made broadly accessible. Nucleic Acids Res. 45(D1): D362–D368. 2017. View Article : Google Scholar : PubMed/NCBI | |
Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B and Ideker T: Cytoscape: A software environment for integrated models of biomolecular interaction networks. Genome Res. 13:2498–2504. 2003. View Article : Google Scholar : PubMed/NCBI | |
Tang Z, Li C, Kang B, Gao G, Li C and Zhang Z: GEPIA: A web server for cancer and normal gene expression profiling and interactive analyses. Nucleic Acids Res. 45((W1)): W98–W102. 2017. View Article : Google Scholar : PubMed/NCBI | |
Edgar R, Domrachev M and Lash AE: Gene expression omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res. 30:207–210. 2002. View Article : Google Scholar : PubMed/NCBI | |
Lowery AJ, Miller N, Devaney A, McNeill RE, Davoren PA, Lemetre C, Benes V, Schmidt S, Blake J, Ball G and Kerin MJ: MicroRNA signatures predict oestrogen receptor, progesterone receptor and HER2/neu receptor status in breast cancer. Breast Cancer Res. 11:R272009. View Article : Google Scholar : PubMed/NCBI | |
Maillot G, Lacroix-Triki M, Pierredon S, Gratadou L, Schmidt S, Bénès V, Roché H, Dalenc F, Auboeuf D, Millevoi S and Vagner S: Widespread estrogen-dependent repression of microRNAs involved in breast tumor cell growth. Cancer Res. 69:8332–8340. 2009. View Article : Google Scholar : PubMed/NCBI | |
Sun R, Fu X, Li Y, Xie Y and Mao Y: Global gene expression analysis reveals reduced abundance of putative microRNA targets in human prostate tumours. BMC Genomics. 10:932009. View Article : Google Scholar : PubMed/NCBI | |
Ribas J, Ni X, Haffner M, Wentzel EA, Salmasi AH, Chowdhury WH, Kudrolli TA, Yegnasubramanian S, Luo J, Rodriguez R, et al: miR-21: An androgen receptor-regulated microRNA that promotes hormone-dependent and hormone-independent prostate cancer growth. Cancer Res. 69:7165–7169. 2009. View Article : Google Scholar : PubMed/NCBI | |
Cadepond F, Ulmann A and Baulieu EE: RU486 (MIFEPRISTONE): Mechanisms of action and clinical uses. Annu Rev Med. 48:129–156. 1997. View Article : Google Scholar : PubMed/NCBI | |
Catalano RD, Yanaihara A, Evans AL, Rocha D, Prentice A, Saidi S, Print CG, Charnock-Jones DS, Sharkey AM and Smith SK: The effect of RU486 on the gene expression profile in an endometrial explant model. Mol Hum Reprod. 9:465–473. 2003. View Article : Google Scholar : PubMed/NCBI | |
Zhang Y, Sui R, Chen Y, Liang H, Shi J and Piao H: Downregulation of miR-485-3p promotes glioblastoma cell proliferation and migration via targeting RNF135. Exp Ther Med. 18:475–482. 2019.PubMed/NCBI | |
Yang W, Warrington NM, Taylor SJ, Whitmire P, Carrasco E, Singleton KW, Wu N, Lathia JD, Berens ME, Kim AH, et al: Sex differences in GBM revealed by analysis of patient imaging, transcriptome and survival data. Sci Transl Med. 11:eaao52532019. View Article : Google Scholar : PubMed/NCBI | |
Yang P, Kang W, Pan Y, Zhao X and Duan L: Overexpression of HOXC6 promotes cell proliferation and migration via MAPK signaling and predicts a poor prognosis in glioblastoma. Cancer Manag Res. 11:8167–8179. 2019. View Article : Google Scholar : PubMed/NCBI | |
Zhou L, Tang H, Wang F, Chen L, Ou S, Wu T, Xu J and Guo K: Bioinformatics analyses of significant genes, related pathways and candidate prognostic biomarkers in glioblastoma. Mol Med Rep. 18:4185–4196. 2018.PubMed/NCBI | |
Zhang S, Wan Y, Pan T, Gu X, Qian C, Sun G, Sun L, Xiang Y, Wang Z and Shi L: MicroRNA-21 inhibitor sensitizes human glioblastoma U251 stem cells to chemotherapeutic drug temozolomide. J Mol Neurosci. 47:346–356. 2012. View Article : Google Scholar : PubMed/NCBI | |
Nicolas S, Abdellatef S, Haddad MA, Fakhoury I and El-Sibai M: Hypoxia and EGF stimulation regulate VEGF expression in human glioblastoma multiforme (GBM) cells by differential regulation of the PI3K/Rho-GTPase and MAPK pathways. Cells. 8:13972019. View Article : Google Scholar : PubMed/NCBI | |
Shan ZN, Tian R, Zhang M, Gui ZH, Wu J, Ding M, Zhou XF and He J: MiR128-1 inhibits the growth of glioblastoma multiforme and glioma stem-like cells via targeting BMI1 and E2F3. Oncotarget. 7:78813–78826. 2016. View Article : Google Scholar : PubMed/NCBI | |
Wen L, Tan Y, Dai S, Zhu Y, Meng T, Yang X, Liu Y, Liu X, Yuan H and Hu F: VEGF-mediated tight junctions pathological fenestration enhances doxorubicin-loaded glycolipid-like nanoparticles traversing BBB for glioblastoma-targeting therapy. Drug Deliv. 24:1843–1855. 2017. View Article : Google Scholar : PubMed/NCBI | |
Bao S, Wu Q, Sathornsumetee S, Hao Y, Li Z, Hjelmeland AB, Shi Q, McLendon RE, Bigner DD and Rich JN: Stem cell-like glioma cells promote tumor angiogenesis through vascular endothelial growth factor. Cancer Res. 66:7843–7848. 2006. View Article : Google Scholar : PubMed/NCBI | |
Cui X, Xu Z, Zhao Z, Sui D, Ren X, Huang Q, Qin J, Hao L, Wang Z, Shen L and Lin S: Analysis of CD137l and IL-17 expression in tumor tissue as prognostic indicators for gliblastoma. Int J Biol Sci. 9:134–141. 2013. View Article : Google Scholar : PubMed/NCBI | |
Berenguer-Daizé C, Astorgues-Xerri L, Odore E, Cayol M, Cvitkovic E, Noel K, Bekradda M, MacKenzie S, Rezai K, Lokiec F, et al: OTX015 (MK-8628), a novel BET inhibitor, displays in vitro and in vivo antitumor effects alone and in combination with conventional therapies in glioblastoma models. Int J Cancer. 139:2047–2055. 2016. View Article : Google Scholar | |
Jin X, Kim LJY, Wu Q, Wallace LC, Prager BC, Sanvoranart T, Gimple RC, Wang X, Mack SC, Miller TE, et al: Targeting glioma stem cells through combined BMI1 and EZH2 inhibition. Nat Med. 23:1352–1361. 2017. View Article : Google Scholar : PubMed/NCBI | |
Elango R, Vishnubalaji R, Manikandan M, Binhamdan SI, Siyal AA, Alshawakir YA, Alfayez M, Aldahmash A and Alajez NM: Concurrent targeting of BMI1 and CDK4/6 abrogates tumor growth in vitro and in vivo. Sci Rep. 9:136962019. View Article : Google Scholar : PubMed/NCBI | |
Peng G, Liao Y and Shen C: miRNA-429 inhibits astrocytoma proliferation and invasion by targeting BMI1. Pathol Oncol Res. 23:369–376. 2017. View Article : Google Scholar : PubMed/NCBI | |
Antonyak MA, Kenyon LC, Godwin AK, James DC, Emlet DR, Okamoto I, Tnani M, Holgado-Madruga M, Moscatello DK and Wong AJ: Elevated JNK activation contributes to the pathogenesis of human brain tumors. Oncogene. 21:5038–5046. 2002. View Article : Google Scholar : PubMed/NCBI | |
Tsuiki H, Tnani M, Okamoto I, Kenyon LC, Emlet DR, Holgado-Madruga M, Lanham IS, Joynes CJ, Vo KT and Wong AJ: Constitutively active forms of c-Jun NH2-terminal kinase are expressed in primary glial tumors. Cancer Res. 63:250–255. 2003.PubMed/NCBI | |
Cui J, Han SY, Wang C, Su W, Harshyne L, Holgado-Madruga M and Wong AJ: c-Jun NH(2)-terminal kinase 2alpha2 promotes the tumorigenicity of human glioblastoma cells. Cancer Res. 66:10024–10031. 2006. View Article : Google Scholar : PubMed/NCBI | |
Yu OM, Benitez JA, Plouffe SW, Ryback D, Klein A, Smith J, Greenbaum J, Delatte B, Rao A, Guan KL, et al: YAP and MRTF-A, transcriptional co-activators of RhoA-mediated gene expression, are critical for glioblastoma tumorigenicity. Oncogene. 37:5492–5507. 2018. View Article : Google Scholar : PubMed/NCBI | |
Liu G, Yan T, Li X, Sun J, Zhang B, Wang H and Zhu Y: Daam1 activates RhoA to regulate Wnt5a-induced glioblastoma cell invasion. Oncol Rep. 39:465–472. 2018.PubMed/NCBI | |
Kusaczuk M, Krętowski R, Naumowicz M, Stypułkowska A and Cechowska-Pasko M: Silica nanoparticle-induced oxidative stress and mitochondrial damage is followed by activation of intrinsic apoptosis pathway in glioblastoma cells. Int J Nanomedicine. 13:2279–2294. 2018. View Article : Google Scholar : PubMed/NCBI | |
Cholia RP, Kumari S, Kumar S, Kaur M, Kaur M, Kumar R, Dhiman M and Mantha AK: An in vitro study ascertaining the role of H2O2 and glucose oxidase in modulation of antioxidant potential and cancer cell survival mechanisms in glioblastoma U-87 MG cells. Metab Brain Dis. 32:1705–1716. 2017. View Article : Google Scholar : PubMed/NCBI | |
Tanaka H, Mizuno M, Katsumata Y, Ishikawa K, Kondo H, Hashizume H, Okazaki Y, Toyokuni S, Nakamura K, Yoshikawa N, et al: Oxidative stress-dependent and -independent death of glioblastoma cells induced by non-thermal plasma-exposed solutions. Sci Rep. 9:136572019. View Article : Google Scholar : PubMed/NCBI | |
Wang R, Zhang S, Chen X, Li N, Li J, Jia R, Pan Y and Liang H: EIF4A3-induced circular RNA MMP9 (circMMP9) acts as a sponge of miR-124 and promotes glioblastoma multiforme cell tumorigenesis. Mol Cancer. 17:1662018. View Article : Google Scholar : PubMed/NCBI |