A proposed method for the relative quantification of levels of circulating microRNAs in the plasma of gastric cancer patients Corrigendum in /10.3892/ol.2017.7626

Suárez‑Arriaga,Mayra‑Cecilia; Torres,Javier; Camorlinga‑Ponce,Margarita; Gómez‑Delgado,Alejandro; Piña‑Sánchez,Patricia; Valdez‑Salazar,Hilda‑Alicia; Ribas‑Aparicio,Rosa‑María; Fuentes‑Pananá,Ezequiel  M.; Ruiz‑Tachiquín,Martha‑Eugenia

doi:10.3892/ol.2017.5816

A proposed method for the relative quantification of levels of circulating microRNAs in the plasma of gastric cancer patients

Corrigendum in: /10.3892/ol.2017.7626

Authors:
- Mayra‑Cecilia Suárez‑Arriaga
- Javier Torres
- Margarita Camorlinga‑Ponce
- Alejandro Gómez‑Delgado
- Patricia Piña‑Sánchez
- Hilda‑Alicia Valdez‑Salazar
- Rosa‑María Ribas‑Aparicio
- Ezequiel M. Fuentes‑Pananá
- Martha‑Eugenia Ruiz‑Tachiquín
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Affiliations: Medical Research Unit in Human Genetics, Pediatrics Hospital ‘Dr Silvestre Frenk Freud’, XXI Century National Medical Center, Mexican Institute of Social Security, 06720 Mexico City, Mexico, Medical Research Unit in Infectious and Parasitic Diseases, Pediatrics Hospital ‘Dr Silvestre Frenk Freud’, XXI Century National Medical Center, Mexican Institute of Social Security, 06720 Mexico City, Mexico, Medical Research Unit in Oncological Diseases, Oncology Hospital, XXI Century National Medical Center, Mexican Institute of Social Security, 06720 Mexico City, Mexico, Department of Microbiology, National School of Biological Sciences, National Polytechnic Institute, 11340 Mexico City, Mexico, Virology and Cancer Research Unit, Children's Hospital of Mexico ‘Federico Gómez’, 06720 Mexico City, Mexico
Published online on: March 7, 2017 https://doi.org/10.3892/ol.2017.5816
Pages: 3109-3117
Copyright: © Suárez‑Arriaga et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

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Abstract

Gastric cancer (GC) is the fifth most common type of malignancy and the third leading cause of cancer-associated mortality worldwide. It is necessary to identify novel methods aimed at improving the early diagnosis and treatment of GC. MicroRNA expression profiles in the plasma of patients with GC have demonstrated a potential use in the opportune diagnosis of this neoplasm. However, there are currently no standardized targets for use in the normalization of microRNA Cq values for different neoplasms. The present study tested two normalization approaches while analyzing plasma derived from patients with GC and non‑atrophic gastritis. The first method utilized a panel of small nucleolar RNAs (snoRNAs) and a small nuclear RNA (snRNA) provided by a commercial array. The second normalization approach involved the use of hsa‑miR‑18a‑5p and hsa‑miR‑29a‑3p, which were identified by a stability analysis of the samples being tested. The results revealed that the snoRNAs and snRNA were not expressed in all samples tested. Only the stable microRNAs allowed a narrow distribution of the data and enabled the identification of specific downregulation of hsa‑miR‑200c‑3p and hsa‑miR‑26b‑5p in patients with GC. hsa‑miR‑200c‑3p and hsa-miR-26b-5p have been previously linked to cancer, and a Kyoto Encyclopedia of Genes and Genomes analysis demonstrated that these microRNAs were associated with cell adhesion, cell cycle and cancer pathways.

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1	Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo M, Parkin DM, Forman D and Bray F: Cancer incidence and mortality worldwide: Sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer. 136:E359–E386. 2015. View Article : Google Scholar : PubMed/NCBI
2	Mitchell PS, Parkin RK, Kroh EM, Fritz BR, Wyman SK, Pogosova-Agadjanyan EL, Peterson A, Noteboom J, O'Briant KC, Allen A, et al: Circulating microRNAs as stable blood-based markers for cancer detection. Proc Natl Acad Sci USA. 105:10513–10518. 2008. View Article : Google Scholar : PubMed/NCBI
3	Creemers EE, Tijsen AJ and Pinto YM: Circulating MicroRNAs: Novel biomarkers and extracellular communicators in cardiovascular disease? Circ Res. 110:483–495. 2012. View Article : Google Scholar : PubMed/NCBI
4	Munker R and Calin GA: MicroRNA profiling in cancer. Clin Sci (Lond). 121:141–158. 2011. View Article : Google Scholar : PubMed/NCBI
5	Volinia S, Calin GA, Liu CG, Ambs S, Cimmino A, Petrocca F, Visone R, Iorio M, Roldo C, Ferracin M, et al: A microRNA expression signature of human solid tumors defines cancer gene targets. Proc Natl Acad Sci USA. 103:2257–2261. 2006. View Article : Google Scholar : PubMed/NCBI
6	Lu J, Getz G, Miska EA, Alvarez-Saavedra E, Lamb J, Peck D, Sweet-Cordero A, Ebert BL, Mak RH, Ferrando AA, et al: MicroRNA expression profiles classify human cancers. Nature. 435:834–838. 2005. View Article : Google Scholar : PubMed/NCBI
7	Jiang C, Chen X, Alattar M, Wei J and Liu H: MicroRNAs in tumorigenesis, metastasis, diagnosis and prognosis of gastric cancer. Cancer Gene Ther. 22:291–301. 2015. View Article : Google Scholar : PubMed/NCBI
8	Shrestha S, Hsu SD, Huang WY, Huang HY, Chen W, Weng SL and Huang HD: A systematic review of microRNA expression profiling studies in human gastric cancer. Cancer Med. 3:878–888. 2014. View Article : Google Scholar : PubMed/NCBI
9	Ueda T, Volinia S, Okumura H, Shimizu M, Taccioli C, Rossi S, Alder H, Liu CG, Oue N, Yasui W, et al: Relation between microRNA expression and progression and prognosis of gastric cancer: A microRNA expression analysis. Lancet Oncol. 11:136–146. 2010. View Article : Google Scholar : PubMed/NCBI
10	Wang R, Wen H, Xu Y, Chen Q, Luo Y, Lin Y, Luo Y and Xu A: Circulating microRNAs as a novel class of diagnostic biomarkers in gastrointestinal tumors detection: A meta-analysis based on 42 articles. PLoS One. 9:e1134012014. View Article : Google Scholar : PubMed/NCBI
11	Li B, Zhao Y, Guo G, Li W, Zhu ED, Luo X, Mao XH, Zou QM, Yu PW, Zuo QF, et al: Plasma microRNAs, miR-223, miR-21 and miR-218, as novel potential biomarkers for gastric cancer detection. PLoS One. 7:e416292012. View Article : Google Scholar : PubMed/NCBI
12	Gorur A, Fidanci Balci S, Dogruer Unal N, Ayaz L, Akbayir S, Yildirim Yaroglu H, Dirlik M, Serin MS and Tamer L: Determination of plasma microRNA for early detection of gastric cancer. Mol Biol Rep. 40:2091–2096. 2013. View Article : Google Scholar : PubMed/NCBI
13	Song MY, Pan KF, Su HJ, Zhang L, Ma JL, Li JY, Yuasa Y, Kang D, Kim YS and You WC: Identification of serum microRNAs as novel non-invasive biomarkers for early detection of gastric cancer. PLoS One. 7:e336082012. View Article : Google Scholar : PubMed/NCBI
14	Qiu X, Zhang J, Shi W, Liu S, Kang M, Chu H, Wu D, Tong N, Gong W, Tao G, et al: Circulating MicroRNA-26a in plasma and its potential diagnostic value in gastric cancer. PLoS One. 11:e01513452016. View Article : Google Scholar : PubMed/NCBI
15	Zhu X, Lv M, Wang H and Guan W: Identification of circulating MicroRNAs as novel potential biomarkers for gastric cancer detection: A systematic review and meta-analysis. Dig Dis Sci. 59:911–919. 2014. View Article : Google Scholar : PubMed/NCBI
16	Mestdagh P, Van Vlierberghe P, De Weer A, Muth D, Westermann F, Speleman F and Vandesompele J: A novel and universal method for microRNA RT-qPCR data normalization. Genome Biol. 10:R642009. View Article : Google Scholar : PubMed/NCBI
17	Peltier HJ and Latham GJ: Normalization of microRNA expression levels in quantitative RT-PCR assays: Identification of suitable reference RNA targets in normal and cancerous human solid tissues. RNA. 14:844–852. 2008. View Article : Google Scholar : PubMed/NCBI
18	Sperveslage J, Hoffmeister M, Henopp T, Klöppel G and Sipos B: Establishment of robust controls for the normalization of miRNA expression in neuroendocrine tumors of the ileum and pancreas. Endocrine. 46:226–230. 2014. View Article : Google Scholar : PubMed/NCBI
19	Juzėnas S, Saltenienė V, Kupcinskas J, Link A, Kiudelis G, Jonaitis L, Jarmalaite S, Kupcinskas L, Malfertheiner P and Skieceviciene J: Analysis of deregulated microRNAs and their target genes in gastric cancer. PLoS One. 10:e01323272015. View Article : Google Scholar : PubMed/NCBI
20	Benz F, Roderburg C, Cardenas Vargas D, Vucur M, Gautheron J, Koch A, Zimmermann H, Janssen J, Nieuwenhuijsen L, Luedde M, et al: U6 is unsuitable for normalization of serum miRNA levels in patients with sepsis or liver fibrosis. Exp Mol Med. 45:e422013. View Article : Google Scholar : PubMed/NCBI
21	Zheng G, Wang H, Zhang X, Yang Y, Wang L, Du L, Li W, Li J, Qu A, Liu Y and Wang C: Identification and validation of reference genes for qPCR detection of serum microRNAs in colorectal adenocarcinoma patients. PLoS One. 8:e830252013. View Article : Google Scholar : PubMed/NCBI
22	van Beers EH, Joosse SA, Ligtenberg MJ, Fles R, Hogervorst FB, Verhoef S and Nederlof PM: A multiplex PCR predictor for aCGH success of FFPE samples. Br J Cancer. 94:333–337. 2006. View Article : Google Scholar : PubMed/NCBI
23	Andersen CL, Jensen JL and Ørntoft TF: Normalization of real-time quantitative reverse transcription-PCR data: A model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets. Cancer Res. 64:5245–5250. 2004. View Article : Google Scholar : PubMed/NCBI
24	Livak KJ and Schmittgen TD: Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) Method. Methods. 25:402–408. 2001. View Article : Google Scholar : PubMed/NCBI
25	Vlachos IS, Zagganas K, Paraskevopoulou MD, Georgakilas G, Karagkouni D, Vergoulis T, Dalamagas T and Hatzigeorgiou AG: DIANA-miRPath v3.0: Deciphering microRNA function with experimental support. Nucleic Acids Res. 43:W460–W466. 2015. View Article : Google Scholar : PubMed/NCBI
26	Pritchard CC, Cheng HH and Tewari M: MicroRNA profiling: Approaches and considerations. Nat Rev Genet. 13:358–369. 2012. View Article : Google Scholar : PubMed/NCBI
27	Wang XW, Wu Y, Wang D and Qin ZF: MicroRNA network analysis identifies key microRNAs and genes associated with precancerous lesions of gastric cancer. Genet Mol Res. 13:8695–8703. 2014. View Article : Google Scholar : PubMed/NCBI
28	Wong CM, Wei L, Au SL, Fan DN, Zhou Y, Tsang FH, Law CT, Lee JM, He X, Shi J, et al: MiR-200b/200c/429 subfamily negatively regulates Rho/ROCK signaling pathway to suppress hepatocellular carcinoma metastasis. Oncotarget. 6:13658–13670. 2015. View Article : Google Scholar : PubMed/NCBI
29	Hur K, Toiyama Y, Takahashi M, Balaguer F, Nagasaka T, Koike J, Hemmi H, Koi M, Boland CR and Goel A: MicroRNA-200c modulates epithelial-to-mesenchymal transition (EMT) in human colorectal cancer metastasis. Gut. 62:1315–1326. 2013. View Article : Google Scholar : PubMed/NCBI
30	Hill L, Browne G and Tulchinsky E: ZEB/miR-200 feedback loop: At the crossroads of signal transduction in cancer. Int J Cancer. 132:745–754. 2013. View Article : Google Scholar : PubMed/NCBI
31	Li H, Xu L, Li C, Zhao L, Ma Y, Zheng H, Li Z, Zhang Y, Wang R, Liu Y and Qu X: Ubiquitin ligase Cbl-b represses IGF-I-induced epithelial mesenchymal transition via ZEB2 and microRNA-200c regulation in gastric cancer cells. Mol Cancer. 13:1362014. View Article : Google Scholar : PubMed/NCBI
32	Tang H, Deng M, Tang Y and Xie X, Guo J, Kong Y, Ye F, Su Q and Xie X: MiR-200b and miR-200c as prognostic factors and mediators of gastric cancer cell progression. Clin Cancer Res. 19:5602–5612. 2013. View Article : Google Scholar : PubMed/NCBI
33	Zhang HP, Sun FB and Li SJ: Serum miR-200c expression level as a prognostic biomarker for gastric cancer. Genet Mol Res. 14:15913–15920. 2015. View Article : Google Scholar : PubMed/NCBI
34	Gao J and Liu QG: The role of miR-26 in tumors and normal tissues (Review). Oncol Lett. 2:1019–1023. 2011.PubMed/NCBI
35	Kato M, Goto Y, Matsushita R, Kurozumi A, Fukumoto I, Nishikawa R, Sakamoto S, Enokida H, Nakagawa M, Ichikawa T and Seki N: MicroRNA-26a/b directly regulate La-related protein 1 and inhibit cancer cell invasion in prostate cancer. Int J Oncol. 47:710–718. 2015.PubMed/NCBI
36	Ramachandran K, Saikumar J, Bijol V, Koyner JL, Qian J, Betensky RA, Waikar SS and Vaidya VS: Human miRNome profiling identifies MicroRNAs differentially present in the urine after kidney injury. Clin Chem. 59:1742–1752. 2013. View Article : Google Scholar : PubMed/NCBI
37	Chen J, Zhang K, Xu Y, Gao Y, Li C, Wang R and Chen L: The role of microRNA-26a in human cancer progression and clinical application. Tumor Biol. 37:7095–7108. 2016. View Article : Google Scholar
38	Li H, Sun Q, Han B, Yu X, Hu B and Hu S: MiR-26b inhibits hepatocellular carcinoma cell proliferation, migration, and invasion by targeting EphA2. Int J Clin Exp Pathol. 8:4782–4790. 2015.PubMed/NCBI
39	Zheng WD, Zhou FL and Lin N: MicroRNA-26b inhibits osteosarcoma cell migration and invasion by down-regulating PFKFB3 expression. Genet Mol Res. 14:16872–16879. 2015. View Article : Google Scholar : PubMed/NCBI
40	Lin J, Zhang L, Huang H, Huang Y, Huang L, Wang J, Huang S, He L, Zhou Y, Jia W, et al: MiR-26b/KPNA2 axis inhibits epithelial ovarian carcinoma proliferation and metastasis through downregulating OCT4. Oncotarget. 6:23793–23806. 2015. View Article : Google Scholar : PubMed/NCBI
41	Xia M, Duan ML, Tong JH and Xu JG: MiR-26b suppresses tumor cell proliferation, migration and invasion by directly targeting COX-2 in lung cancer. Eur Rev Med Pharmacol Sci. 19:4728–4737. 2015.PubMed/NCBI
42	Xie J, Chen M, Zhou J, Mo MS, Zhu LH, Liu YP, Gui QJ, Zhang L and Li GQ: miR-7 inhibits the invasion and metastasis of gastric cancer cells by suppressing epidermal growth factor receptor expression. Oncol Rep. 31:1715–1722. 2014.PubMed/NCBI
43	Inoue T, Iinuma H, Ogawa E, Inaba T and Fukushima R: Clinicopathological and prognostic significance of microRNA-107 and its relationship to DICER1 mRNA expression in gastric cancer. Oncol Rep. 27:1759–1764. 2012.PubMed/NCBI
44	Cooney CA, Jousheghany F, Yao-Borengasser A, Phanavanh B, Gomes T, Kieber-Emmons AM, Siegel ER, Suva LJ, Ferrone S, Kieber-Emmons T and Monzavi-Karbassi B: Chondroitin sulfates play a major role in breast cancer metastasis: A role for CSPG4 and CHST11 gene expression in forming surface P-selectin ligands in aggressive breast cancer cells. Breast Cancer Res. 13:R582011. View Article : Google Scholar : PubMed/NCBI