Generic placeholder image

Current Medicinal Chemistry

Editor-in-Chief

ISSN (Print): 0929-8673
ISSN (Online): 1875-533X

Systematic Review Article

Gastric Cancer and Circulating microRNAs: An Updated Systematic Review and Diagnostic Meta-Analysis

Author(s): Amir Hossein Aalami, Farnoosh Aalami and Amirhossein Sahebkar*

Volume 30, Issue 33, 2023

Published on: 28 December, 2022

Page: [3798 - 3814] Pages: 17

DOI: 10.2174/0929867330666221121155905

Price: $65

Abstract

Background: Circulating microRNAs (miRNAs, miRs) are now used as noninvasive diagnostic indicators in various malignancies.

Objective: Our objective is to use a meta-analysis to assess the diagnostic performance of circulating miRNAs in gastric cancer.

Methods: We reviewed databases and methodically obtained papers for analysis until October 15th, 2021. The random-effect meta-analysis was performed to construct pooled diagnostic parameters. To detect the causes of heterogeneity, spearman threshold effect analysis and subgroup analysis were performed. The I2 and Chi-square tests were also used to examine the heterogeneity. The subgroup analyses were conducted based on sample types (serum/plasma/blood), normalized genes (U6, miR-16, and miR-39), qPCR mastermix (SYBR and Taqman), and country. Finally, the publication bias was estimated using Egger's funnel plot asymmetry test.

Results: A total of 40 articles covering 73 studies (59 microRNAs) were included, containing 11,022 participants (6,324 cases and 4,698 controls). The overall pooled sensitivity, specificity, positive likelihood ratio (PLR), negative likelihood ratio (NLR), diagnostic odds ratio (DOR), and area under the curve (AUC) were 0.75 (95% CI: 0.74-0.77), 0.79 (95% CI: 0.78-0.80), 4.081 (95% CI: 3.43-4.85), 0.28 (95% CI: 0.25-0.32), 16.08 (95% CI: 12.34-20.95), and 0.877 (CI: 0.84-0.90), respectively. We conducted a subgroup analysis of diagnostic values, which revealed that serum type, U6 reference gene, SYBR mastermix, and East Asian Countries (China and Japan) had better diagnostic value.

Conclusion: Circulating miRs can serve as diagnostic biomarkers for gastric cancer. However, specific miRNAs still need to be discovered in diagnosing gastric cancer, especially early screening.

Keywords: Gastric cancer, circulating miRNAs, diagnosis, biomarker, meta-analysis, non-invasive diagnostic indicators.

[1]
Talebi, A.; Borumandnia, N.; Doosti, H.; Abbasi, S.; Pourhoseingholi, M.A.; Agah, S.; Tabaeian, S.P. Development of web-based dynamic nomogram to predict survival in patients with gastric cancer: A population-based study. Sci. Rep., 2022, 12(1), 4580.
[http://dx.doi.org/10.1038/s41598-022-08465-w] [PMID: 35301382]
[2]
Kotzev, A.I.; Draganov, P.V. Carbohydrate antigen 19-9, carcinoembryonic antigen, and carbohydrate antigen 72-4 in gastric cancer: is the old band still playing? Gastrointest. Tumors, 2018, 5(1-2), 1-13.
[http://dx.doi.org/10.1159/000488240] [PMID: 30574476]
[3]
Ma, H.; He, Z.; Chen, J.; Zhang, X.; Song, P. Identifying of biomarkers associated with gastric cancer based on 11 topological analysis methods of CytoHubba. Sci. Rep., 2021, 11(1), 1331.
[http://dx.doi.org/10.1038/s41598-020-79235-9] [PMID: 33446695]
[4]
Hosseini Mojahed, F.; Aalami, A.H.; Pouresmaeil, V.; Amirabadi, A.; Qasemi Rad, M.; Sahebkar, A. Clinical evaluation of the diagnostic role of MicroRNA-155 in breast cancer. Int. J. Genomics, 2020, 2020, 9514831.
[http://dx.doi.org/10.1155/2020/9514831] [PMID: 32964011]
[5]
Aalami, A.H.; Abdeahad, H.; Shoghi, A.; Mesgari, M.; Amirabadi, A.; Sahebkar, A. Brain tumors and circulating micrornas: A systematic review and diagnostic meta-analysis. Expert Rev. Mol. Diagn., 2022, 22(2), 201-211.
[http://dx.doi.org/10.1080/14737159.2022.2019016] [PMID: 34906021]
[6]
Liu, X.; Ma, R.; Yi, B.; Riker, A.I.; Xi, Y. MicroRNAs are involved in the development and progression of gastric cancer. Acta Pharmacol. Sin., 2021, 42(7), 1018-1026.
[http://dx.doi.org/10.1038/s41401-020-00540-0] [PMID: 33037405]
[7]
Qasemi Rad, M.; Pouresmaeil, V.; Hosseini Mojahed, F.; Amirabadi, A.; Aalami, A.H. Clinicopathological utility of miR-203a-3p in diagnosing colorectal cancer. Mol. Biol. Rep., 2022, 49(7), 6975-6985.
[http://dx.doi.org/10.1007/s11033-022-07465-3] [PMID: 35511316]
[8]
Oliveira, A.; Castanhole-Nunes, M.; Biselli-Chicote, P.; Pavarino, É.; Silva, R.; Silva, R.; Goloni-Bertollo, E.M. Differential expression of angiogenesis-related miRNAs and VEGFA in cirrhosis and hepatocellular carcinoma. Arch. Med. Sci., 2020, 16(5), 1150-1157.
[http://dx.doi.org/10.5114/aoms.2020.97967] [PMID: 32864004]
[9]
Huang, F.; Tang, W.; Lei, Y. MicroRNA-107 promotes apoptosis of acute myelocytic leukemia cells by targeting RAD51. Arch. Med. Sci., 2021, 17(4), 1044-1055.
[http://dx.doi.org/10.5114/aoms.2020.92860] [PMID: 34336032]
[10]
Pu, R.; Pu, M.; Huang, H.; Cui, Y. MicroRNA 144 inhibits cell migration and invasion and regulates inflammatory cytokine secretion through targeting toll like receptor 2 in non-small cell lung cancer. Arch. Med. Sci., 2021, 17(4), 1028-1037.
[http://dx.doi.org/10.5114/aoms.2020.93084] [PMID: 34336030]
[11]
Wang, H.; Liu, G.; Li, T.; Wang, N.; Wu, J.; Zhi, H. MiR-330-3p functions as a tumor suppressor that regulates glioma cell proliferation and migration by targeting CELF1. Arch. Med. Sci., 2020, 16(5), 1166-1175.
[http://dx.doi.org/10.5114/aoms.2020.95027] [PMID: 32864006]
[12]
Zhang, H.; Bao, J.; Zhao, S.; Huo, Z.; Li, B. MicroRNA-490-3p suppresses hepatocellular carcinoma cell proliferation and migration by targeting the aurora kinase A gene (AURKA). Arch. Med. Sci., 2020, 16(2), 395-406.
[http://dx.doi.org/10.5114/aoms.2019.91351] [PMID: 32190151]
[13]
Zhao, M.; Wang, K.; Shang, J.; Liang, Z.; Zheng, W.; Gu, J. MiR-345-5p inhibits tumorigenesis of papillary thyroid carcinoma by targeting SETD7. Arch. Med. Sci., 2020, 16(4), 888-897.
[http://dx.doi.org/10.5114/aoms.2019.83823] [PMID: 32542092]
[14]
Zhihong, Z.; Rubin, C.; Liping, L.; Anpeng, M.; Hui, G.; Yanting, W.; Zhenxiu, S. MicroRNA-1179 regulates proliferation and chemosensitivity of human ovarian cancer cells by targeting the PTEN-mediated PI3K/AKT signaling pathway. Arch. Med. Sci., 2020, 16(4), 907-914.
[http://dx.doi.org/10.5114/aoms.2019.86798] [PMID: 32542094]
[15]
Salarinia, R.; Sahebkar, A.; Peyvandi, M.; Reza Mirzaei, H.; Reza Jaafari, M.; Matbou Riahi, M.; Ebrahimnejad, H.; Sadri Nahand, J.; Hadjati, J.; Ostadi Asrami, M.; Fadaei, S.; Salehi, R.; Mirzaei, H. Epi-drugs and epi-mirs: Moving beyond current cancer therapies. Curr. Cancer Drug Targets, 2016, 16(9), 773-788.
[http://dx.doi.org/10.2174/1568009616666151207110143] [PMID: 26638884]
[16]
Azarbarzin, S.; Safaralizadeh, R.; Khojasteh, M.B.; Baghbanzadeh, A.; Baradaran, B. Current perspectives on the dysregulated microRNAs in gastric cancer. Mol. Biol. Rep., 2020, 47(9), 7253-7264.
[http://dx.doi.org/10.1007/s11033-020-05720-z] [PMID: 32776162]
[17]
Chang, J.; Liu, S.; Li, B.; Huo, Z.; Wang, X.; Zhang, H. MiR-338-3p improved lung adenocarcinoma by AKAP12 suppression. Arch. Med. Sci., 2021, 17(2), 462-473.
[http://dx.doi.org/10.5114/aoms.2019.90913] [PMID: 33747281]
[18]
Chen, Z.; Gao, Y.; Gao, S.; Song, D.; Feng, Y. MiR-135b-5p promotes viability, proliferation, migration and invasion of gastric cancer cells by targeting Krüppel-like factor 4 (KLF4). Arch. Med. Sci., 2020, 16(1), 167-176.
[http://dx.doi.org/10.5114/aoms.2019.87761] [PMID: 32051721]
[19]
Krupa, R.; Malecki, W.; Czarny, P.; Strycharz, J.; Jablkowski, M.; Kordek, R.; Szemraj, J.; Sliwinski, T. MicroRNA profile and iron-related gene expression in hepatitis C-related hepatocellular carcinoma: A preliminary study. Arch. Med. Sci., 2021, 17(5), 1175-1183.
[http://dx.doi.org/10.5114/aoms.2019.86613] [PMID: 34522246]
[20]
Li, H.; Liu, D.; Liu, L.; Huang, S.; Ma, A.; Zhang, X. The role of HOTAIR/miR-152-3p/LIN28B in regulating the progression of endometrial squamous carcinoma. Arch. Med. Sci., 2021, 17(2), 434-448.
[http://dx.doi.org/10.5114/aoms.2019.89632] [PMID: 33747279]
[21]
Aalami, A.H.; Abdeahad, H.; Mesgari, M.; Sahebkar, A. MicroRNA-223 in gastrointestinal cancers: A systematic review and diagnostic meta-analysis. Eur. J. Clin. Invest., 2021, 51(2), e13448.
[http://dx.doi.org/10.1111/eci.13448] [PMID: 33244751]
[22]
Aalami, A.H.; Abdeahad, H.; Mesgari, M. Circulating miR-21 as a potential biomarker in human digestive system carcinoma: A systematic review and diagnostic meta- analysis. Biomarkers, 2021, 26(2), 103-113.
[http://dx.doi.org/10.1080/1354750X.2021.1875504] [PMID: 33434077]
[23]
Fattahi, S.; Nikbakhsh, N.; Ranaei, M.; Sabour, D.; Akhavan-Niaki, H. Association of sonic hedgehog signaling pathway genes IHH, BOC, RAB23a and MIR195-5p, MIR509-3-5p, MIR6738-3p with gastric cancer stage. Sci. Rep., 2021, 11(1), 1-12.
[PMID: 33414495]
[24]
Ahadi, A. Dysregulation of miRNAs as a signature for diagnosis and prognosis of gastric cancer and their involvement in the mechanism underlying gastric carcinogenesis and progression. IUBMB Life, 2020, 72(5), 884-898.
[http://dx.doi.org/10.1002/iub.2259] [PMID: 32078236]
[25]
Ghafouri-Fard, S.; Vafaee, R.; Shoorei, H.; Taheri, M. MicroRNAs in gastric cancer: Biomarkers and therapeutic targets. Gene, 2020, 757, 144937.
[http://dx.doi.org/10.1016/j.gene.2020.144937] [PMID: 32640300]
[26]
Kipkeeva, F.; Muzaffarova, T.; Korotaeva, A.; Nikulin, M.; Grishina, K.; Mansorunov, D.; Apanovich, P.; Karpukhin, A. MicroRNA in gastric cancer development: Mechanisms and biomarkers. Diagnostics, 2020, 10(11), 891.
[http://dx.doi.org/10.3390/diagnostics10110891] [PMID: 33142817]
[27]
Fathullahzadeh, S.; Mirzaei, H.; Honardoost, M.A.; Sahebkar, A.; Salehi, M. Circulating microRNA-192 as a diagnostic biomarker in human chronic lymphocytic leukemia. Cancer Gene Ther., 2016, 23(10), 327-332.
[http://dx.doi.org/10.1038/cgt.2016.34] [PMID: 27659777]
[28]
Ghandadi, M.; Sahebkar, A. MicroRNA-34a and its target genes: Key factors in cancer multidrug resistance. Curr. Pharm. Des., 2016, 22(7), 933-939.
[http://dx.doi.org/10.2174/1381612822666151209153729] [PMID: 26648462]
[29]
Kim, Y.J.; Jeong, S.; Jung, W.Y.; Choi, J.W.; Hwang, K.C.; Kim, S.W.; Lee, Y.C. miRNAs as potential biomarkers for the progression of gastric cancer inhibit CREBZF and regulate migration of gastric adenocarcinoma cells. Int. J. Med. Sci., 2020, 17(6), 693-701.
[http://dx.doi.org/10.7150/ijms.42654] [PMID: 32218690]
[30]
Zhou, L.; Lu, Y.; Liu, J.; Long, S.; Liu, H.; Zhang, J.; Zhang, T. The role of miR-21/RECK in the inhibition of osteosarcoma by curcumin. Mol. Cell. Probes, 2020, 51, 101534.
[http://dx.doi.org/10.1016/j.mcp.2020.101534] [PMID: 32081769]
[31]
Li, J.; Wei, H.; Liu, Y.; Li, Q.; Guo, H.; Guo, Y.; Chang, Z. Curcumin inhibits hepatocellular carcinoma via regulating miR-21/TIMP3 Axis. Evid. Based Complement. Alternat. Med., 2020, 2020, 2892917.
[http://dx.doi.org/10.1155/2020/2892917] [PMID: 32724322]
[32]
Shen, Z.; Xu, X.; Lv, L.; Dai, H.; Chen, J.; Chen, B. miR-21 overexpression promotes esophageal squamous cell carcinoma invasion and migration by repressing tropomyosin 1. Gastroenterol. Res. Pract., 2020, 2020, 6478653.
[http://dx.doi.org/10.1155/2020/6478653] [PMID: 33193757]
[33]
Kangas, R.; Pöllänen, E.; Rippo, M.R.; Lanzarini, C.; Prattichizzo, F.; Niskala, P.; Jylhävä, J.; Sipilä, S.; Kaprio, J.; Procopio, A.D.; Capri, M.; Franceschi, C.; Olivieri, F.; Kovanen, V. Circulating miR-21, miR-146a and Fas ligand respond to postmenopausal estrogen-based hormone replacement therapy - A study with monozygotic twin pairs. Mech. Ageing Dev., 2014, 143-144, 1-8.
[http://dx.doi.org/10.1016/j.mad.2014.11.001] [PMID: 25448133]
[34]
Huang, S.X.; Fan, W.Y.; Wang, L.; Liu, H.; Wang, X.; Zhao, H.; Jiang, W.B. Maspin inhibits MCF‑7 cell invasion and proliferation by downregulating miR‑21 and increasing the expression of its target genes. Oncol. Lett., 2020, 19(4), 2621-2628.
[http://dx.doi.org/10.3892/ol.2020.11360] [PMID: 32218812]
[35]
Zhao, M.; Zhu, N.; Hao, F.; Song, Y.; Wang, Z.; Ni, Y.; Ding, L. The regulatory role of noncoding RNAs on programmed cell death 4 in inflammation and cancer. Front. Oncol., 2019, 9, 919.
[http://dx.doi.org/10.3389/fonc.2019.00919] [PMID: 31620370]
[36]
Chen, D.; Guo, Y.; Chen, Y.; Guo, Q.; Chen, J.; Li, Y.; Zheng, Q.; Jiang, M.; Xi, M.; Cheng, L. LncRNA growth arrest-specific transcript 5 targets miR-21 gene and regulates bladder cancer cell proliferation and apoptosis through PTEN. Cancer Med., 2020, 9(8), 2846-2858.
[http://dx.doi.org/10.1002/cam4.2664] [PMID: 32069387]
[37]
Zhuang, H.; Wang, H.; Yang, H.; Li, H. Exosome-encapsulated MicroRNA-21 from esophageal squamous cell carcinoma cells enhances angiogenesis of human umbilical venous endothelial cells by targeting SPRY1. Cancer Manag. Res., 2020, 12, 10651-10667.
[http://dx.doi.org/10.2147/CMAR.S259077] [PMID: 33149673]
[38]
Mohammadlou, M.; Abdollahi, M.; Hemati, M. Apoptotic effect of berberine via Bcl-2, ROR1, and mir-21 in patients with B-chronic lymphocytic leukemia. Phytother. Res., 2020, 35(4), 2025-2033.
[PMID: 33174291]
[39]
Nedaeinia, R.; Sharifi, M.; Avan, A.; Kazemi, M.; Rafiee, L.; Ghayour-Mobarhan, M.; Salehi, R. Locked nucleic acid anti-miR-21 inhibits cell growth and invasive behaviors of a colorectal adenocarcinoma cell line: LNA-anti-miR as a novel approach. Cancer Gene Ther., 2016, 23(8), 246-253.
[http://dx.doi.org/10.1038/cgt.2016.25] [PMID: 27364574]
[40]
Papagiannakopoulos, T.; Shapiro, A.; Kosik, K.S. MicroRNA-21 targets a network of key tumor-suppressive pathways in glioblastoma cells. Cancer Res., 2008, 68(19), 8164-8172.
[http://dx.doi.org/10.1158/0008-5472.CAN-08-1305] [PMID: 18829576]
[41]
Abe, S.; Matsuzaki, J.; Sudo, K.; Oda, I.; Katai, H.; Kato, K.; Takizawa, S.; Sakamoto, H.; Takeshita, F.; Niida, S.; Saito, Y.; Ochiya, T. A novel combination of serum microRNAs for the detection of early gastric cancer. Gastric Cancer, 2021, 24(4), 835-843.
[http://dx.doi.org/10.1007/s10120-021-01161-0] [PMID: 33743111]
[42]
Ahadi, A. A systematic review of microRNAs as potential biomarkers for diagnosis and prognosis of gastric cancer. Immunogenetics, 2021, 73(2), 155-161.
[http://dx.doi.org/10.1007/s00251-020-01201-6] [PMID: 33399935]
[43]
Page, M.J.; McKenzie, J.E.; Bossuyt, P.M.; Boutron, I.; Hoffmann, T.C.; Mulrow, C.D.; Shamseer, L.; Tetzlaff, J.M.; Moher, D. Updating guidance for reporting systematic reviews: Development of the PRISMA 2020 statement. J. Clin. Epidemiol., 2021, 134, 103-112.
[http://dx.doi.org/10.1016/j.jclinepi.2021.02.003] [PMID: 33577987]
[44]
Moher, D.; Shamseer, L.; Clarke, M.; Ghersi, D.; Liberati, A.; Petticrew, M.; Shekelle, P.; Stewart, L.A. Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015 statement. Syst. Rev., 2015, 4(1), 1.
[http://dx.doi.org/10.1186/2046-4053-4-1] [PMID: 25554246]
[45]
Moses, L.E.; Shapiro, D.; Littenberg, B. Combining independent studies of a diagnostic test into a summary roc curve: Data-analytic approaches and some additional considerations. Stat. Med., 1993, 12(14), 1293-1316.
[http://dx.doi.org/10.1002/sim.4780121403] [PMID: 8210827]
[46]
Furuya-Kanamori, L.; Kostoulas, P.; Doi, S.A.R. A new method for synthesizing test accuracy data outperformed the bivariate method. J. Clin. Epidemiol., 2021, 132, 51-58.
[http://dx.doi.org/10.1016/j.jclinepi.2020.12.015] [PMID: 33333166]
[47]
Higgins, J.P.T.; Thompson, S.G.; Deeks, J.J.; Altman, D.G. Measuring inconsistency in meta-analyses. BMJ, 2003, 327(7414), 557-560.
[http://dx.doi.org/10.1136/bmj.327.7414.557] [PMID: 12958120]
[48]
Liu, X.; Cai, H.; Wang, Y. Prognostic significance of tumour markers in Chinese patients with gastric cancer. ANZ J. Surg., 2014, 84(6), 448-453.
[http://dx.doi.org/10.1111/j.1445-2197.2012.06287.x] [PMID: 23013163]
[49]
Zhu, H.; Wu, H.; Liu, X.; Evans, B.R.; Medina, D.J.; Liu, C.G.; Yang, J.M. Role of MicroRNA miR-27a and miR-451 in the regulation of MDR1/P-glycoprotein expression in human cancer cells. Biochem. Pharmacol., 2008, 76(5), 582-588.
[http://dx.doi.org/10.1016/j.bcp.2008.06.007] [PMID: 18619946]
[50]
Liu, F.; Bu, Z.; Zhao, F.; Xiao, D. Increased T-helper 17 cell differentiation mediated by exosome-mediated microRNA-451 redistribution in gastric cancer infiltrated T cells. Cancer Sci., 2018, 109(1), 65-73.
[http://dx.doi.org/10.1111/cas.13429] [PMID: 29059496]
[51]
Wang, Q.X.; Zhu, Y.Q.; Zhang, H.; Xiao, J. Altered MiRNA expression in gastric cancer: A systematic review and meta-analysis. Cell. Physiol. Biochem., 2015, 35(3), 933-944.
[http://dx.doi.org/10.1159/000369750] [PMID: 25633747]
[52]
Zhang, B.G.; Li, J.F.; Yu, B.Q.; Zhu, Z.G.; Liu, B.Y.; Yan, M. microRNA-21 promotes tumor proliferation and invasion in gastric cancer by targeting PTEN. Oncol. Rep., 2012, 27(4), 1019-1026.
[http://dx.doi.org/10.3892/or.2012.1645] [PMID: 22267008]
[53]
Yamanaka, S.; Olaru, A.V.; An, F.; Luvsanjav, D.; Jin, Z.; Agarwal, R.; Tomuleasa, C.; Popescu, I.; Alexandrescu, S.; Dima, S.; Chivu-Economescu, M.; Montgomery, E.A.; Torbenson, M.; Meltzer, S.J.; Selaru, F.M. MicroRNA-21 inhibits Serpini1, a gene with novel tumour suppressive effects in gastric cancer. Dig. Liver Dis., 2012, 44(7), 589-596.
[http://dx.doi.org/10.1016/j.dld.2012.02.016] [PMID: 22464652]
[54]
Zhu, X.; Lv, M.; Wang, H.; Guan, W. Identification of circulating microRNAs as novel potential biomarkers for gastric cancer detection: A systematic review and meta-analysis. Dig. Dis. Sci., 2014, 59(5), 911-919.
[http://dx.doi.org/10.1007/s10620-013-2970-9] [PMID: 24337687]
[55]
Larner, A.J. The Q* index: A useful global measure of dementia screening test accuracy. Dement. Geriatr. Cogn. Disord. Extra, 2015, 5(2), 265-270.
[http://dx.doi.org/10.1159/000430784] [PMID: 26195982]
[56]
Naredo, E.; Uson, J.; Jiménez-Palop, M.; Martínez, A.; Vicente, E.; Brito, E.; Rodríguez, A.; Cornejo, F.J.; Castañeda, S.; Martínez, M.J.; Sanz, J.; Möller, I.; Batlle-Gualda, E.; Garrido, J.; Pascual, E. Ultrasound-detected musculoskeletal urate crystal deposition: Which joints and what findings should be assessed for diagnosing gout? Ann. Rheum. Dis., 2014, 73(8), 1522-1528.
[http://dx.doi.org/10.1136/annrheumdis-2013-203487] [PMID: 23709244]
[57]
Li, B; Zhao, Y; Guo, G Plasma microRNAs, miR-223, miR-21 and miR-218, as novel potential biomarkers for gastric cancer detection. PLoS One, 2012, 7(7), e41629.
[http://dx.doi.org/10.1371/journal.pone.0041629]
[58]
Tsujiura, M.; Komatsu, S.; Ichikawa, D.; Shiozaki, A.; Konishi, H.; Takeshita, H.; Moriumura, R.; Nagata, H.; Kawaguchi, T.; Hirajima, S.; Arita, T.; Fujiwara, H.; Okamoto, K.; Otsuji, E. Circulating miR-18a in plasma contributes to cancer detection and monitoring in patients with gastric cancer. Gastric Cancer, 2015, 18(2), 271-279.
[http://dx.doi.org/10.1007/s10120-014-0363-1] [PMID: 24626859]
[59]
Kong, Y.; Ning, L.; Qiu, F.; Yu, Q.; Cao, B. Clinical significance of serum miR-25 as a diagnostic and prognostic biomarker in human gastric cancer. Cancer Biomark., 2019, 24(4), 477-483.
[http://dx.doi.org/10.3233/CBM-182213] [PMID: 30909187]
[60]
Wang, H.; Wang, L.; Wu, Z.; Sun, R.; Jin, H.; Ma, J.; Liu, L.; Ling, R.; Yi, J.; Wang, L.; Bian, J.; Chen, J.; Li, N.; Yuan, S.; Yun, J. Three dysregulated microRNAs in serum as novel biomarkers for gastric cancer screening. Med. Oncol., 2014, 31(12), 298.
[http://dx.doi.org/10.1007/s12032-014-0298-8] [PMID: 25367852]
[61]
Juzėnas, S.; Saltenienė, V.; Kupcinskas, J.; Link, A.; Kiudelis, G.; Jonaitis, L.; Jarmalaite, S.; Kupcinskas, L.; Malfertheiner, P.; Skieceviciene, J. Analysis of deregulated microRNAs and their target genes in gastric cancer. PLoS One, 2015, 10(7), e0132327.
[http://dx.doi.org/10.1371/journal.pone.0132327] [PMID: 26172537]
[62]
Aalami, AH; Pouresmaeil, V; Amirabadi, A; Mojahed, FH; Rad, MQ; Sahebkar, A Evaluation of the diagnostic properties of serum hsa-miR-223-5p in the detection of gastric cancer: A case-control study. Anti-Cancer Agents Med. Chem., 2020, 20(7), 800-808.
[63]
Wu, J.; Li, G.; Yao, Y.; Wang, Z.; Sun, W.; Wang, J. MicroRNA-421 is a new potential diagnosis biomarker with higher sensitivity and specificity than carcinoembryonic antigen and cancer antigen 125 in gastric cancer. Biomarkers, 2015, 20(1), 58-63.
[http://dx.doi.org/10.3109/1354750X.2014.992812] [PMID: 25510566]
[64]
Zhao, G.; Jiang, T.; Liu, Y.; Huai, G.; Lan, C.; Li, G.; Jia, G.; Wang, K.; Yang, M. Droplet digital PCR-based circulating microRNA detection serve as a promising diagnostic method for gastric cancer. BMC Cancer, 2018, 18(1), 676.
[http://dx.doi.org/10.1186/s12885-018-4601-5] [PMID: 29929476]
[65]
Valladares-Ayerbes, M.; Reboredo, M.; Medina-Villaamil, V.; Iglesias-Díaz, P.; Lorenzo-Patiño, M.J.; Haz, M.; Santamarina, I.; Blanco, M.; Fernández-Tajes, J.; Quindós, M.; Carral, A.; Figueroa, A.; Antón-Aparicio, L.M.; Calvo, L. Circulating miR-200c as a diagnostic and prognostic biomarker for gastric cancer. J. Transl. Med., 2012, 10(1), 186.
[http://dx.doi.org/10.1186/1479-5876-10-186] [PMID: 22954417]
[66]
Zhou, H.; Guo, J.M.; Lou, Y.R.; Zhang, X.J.; Zhong, F.D.; Jiang, Z.; Cheng, J.; Xiao, B.X. Detection of circulating tumor cells in peripheral blood from patients with gastric cancer using microRNA as a marker. J. Mol. Med., 2010, 88(7), 709-717.
[http://dx.doi.org/10.1007/s00109-010-0617-2] [PMID: 20349219]
[67]
Liu, X.; Kwong, A.; Sihoe, A.; Chu, K.M. Plasma miR-940 may serve as a novel biomarker for gastric cancer. Tumour Biol., 2016, 37(3), 3589-3597.
[http://dx.doi.org/10.1007/s13277-015-4019-5] [PMID: 26456959]
[68]
Emami, S.S.; Nekouian, R.; Akbari, A.; Faraji, A.; Abbasi, V.; Agah, S. Evaluation of circulating miR-21 and miR-222 as diagnostic biomarkers for gastric cancer. J. Cancer Res. Ther., 2019, 15(1), 115-119.
[PMID: 30880765]
[69]
Li, Y.; Sun, H.; Guan, J.; Ji, T.; Wang, X. Serum microRNA-381: A potential marker for early diagnosis of gastric cancer. Yonsei Med. J., 2019, 60(8), 720-726.
[http://dx.doi.org/10.3349/ymj.2019.60.8.720] [PMID: 31347326]
[70]
Shi, Y.; Wang, Z.; Zhu, X.; Chen, L.; Ma, Y.; Wang, J.; Yang, X.; Liu, Z. Exosomal miR-1246 in serum as a potential biomarker for early diagnosis of gastric cancer. Int. J. Clin. Oncol., 2020, 25(1), 89-99.
[http://dx.doi.org/10.1007/s10147-019-01532-9] [PMID: 31506750]
[71]
Tsujiura, M.; Ichikawa, D.; Komatsu, S.; Shiozaki, A.; Takeshita, H.; Kosuga, T.; Konishi, H.; Morimura, R.; Deguchi, K.; Fujiwara, H.; Okamoto, K.; Otsuji, E. Circulating microRNAs in plasma of patients with gastric cancers. Br. J. Cancer, 2010, 102(7), 1174-1179.
[http://dx.doi.org/10.1038/sj.bjc.6605608] [PMID: 20234369]
[72]
Qiu, X.; Zhang, J.; Shi, W.; Liu, S.; Kang, M.; Chu, H.; Wu, D.; Tong, N.; Gong, W.; Tao, G.; Zhao, Q.; Qiang, F.; Zhu, H.; Wu, Q.; Wang, M.; Zhang, Z. Circulating microRNA-26a in plasma and its potential diagnostic value in gastric cancer. PLoS One, 2016, 11(3), e0151345.
[http://dx.doi.org/10.1371/journal.pone.0151345] [PMID: 27010210]
[73]
Zhu, C.; Ren, C.; Han, J.; Ding, Y.; Du, J.; Dai, N.; Dai, J.; Ma, H.; Hu, Z.; Shen, H.; Xu, Y.; Jin, G. A five-microRNA panel in plasma was identified as potential biomarker for early detection of gastric cancer. Br. J. Cancer, 2014, 110(9), 2291-2299.
[http://dx.doi.org/10.1038/bjc.2014.119] [PMID: 24595006]
[74]
Zhang, J.; Song, Y.; Zhang, C.; Zhi, X.; Fu, H.; Ma, Y.; Chen, Y.; Pan, F.; Wang, K.; Ni, J.; Jin, W.; He, X.; Su, H.; Cui, D. Circulating MiR-16-5p and MiR-19b-3p as two novel potential biomarkers to indicate progression of gastric cancer. Theranostics, 2015, 5(7), 733-745.
[http://dx.doi.org/10.7150/thno.10305] [PMID: 25897338]
[75]
Konishi, H.; Ichikawa, D.; Komatsu, S.; Shiozaki, A.; Tsujiura, M.; Takeshita, H.; Morimura, R.; Nagata, H.; Arita, T.; Kawaguchi, T.; Hirashima, S.; Fujiwara, H.; Okamoto, K.; Otsuji, E. Detection of gastric cancer-associated microRNAs on microRNA microarray comparing pre- and post-operative plasma. Br. J. Cancer, 2012, 106(4), 740-747.
[http://dx.doi.org/10.1038/bjc.2011.588] [PMID: 22262318]
[76]
Li, C.; Li, J.F.; Cai, Q.; Qiu, Q.Q.; Yan, M.; Liu, B.Y.; Zhu, Z.G. miRNA-199a-3p in plasma as a potential diagnostic biomarker for gastric cancer. Ann. Surg. Oncol., 2013, 20(Suppl. 3), 397-405.
[http://dx.doi.org/10.1245/s10434-012-2600-3] [PMID: 22956063]
[77]
Song, M.; Pan, K.; Su, H.; Zhang, L.; Ma, J.; Li, J.; Yuasa, Y.; Kang, D.; Kim, Y.S.; You, W. Identification of serum microRNAs as novel non-invasive biomarkers for early detection of gastric cancer. PLoS One, 2012, 7(3), e33608.
[http://dx.doi.org/10.1371/journal.pone.0033608] [PMID: 22432036]
[78]
Huang, S.; Wang, J.; Li, J.; Luo, Q.; Zhao, M.; Zheng, L.; Dong, X.; Chen, C.; Che, Y.; Liu, P.; Qi, J.; Huang, C. Serum microRNA expression profile as a diagnostic panel for gastric cancer. Jpn. J. Clin. Oncol., 2016, 46(9), 811-818.
[http://dx.doi.org/10.1093/jjco/hyw085] [PMID: 27380811]
[79]
Liu, R.; Zhang, C.; Hu, Z.; Li, G.; Wang, C.; Yang, C.; Huang, D.; Chen, X.; Zhang, H.; Zhuang, R.; Deng, T.; Liu, H.; Yin, J.; Wang, S.; Zen, K.; Ba, Y.; Zhang, C.Y. A five-microRNA signature identified from genome-wide serum microRNA expression profiling serves as a fingerprint for gastric cancer diagnosis. Eur. J. Cancer, 2011, 47(5), 784-791.
[http://dx.doi.org/10.1016/j.ejca.2010.10.025] [PMID: 21112772]
[80]
Wang, N.; Wang, L.; Yang, Y.; Gong, L.; Xiao, B.; Liu, X. A serum exosomal microRNA panel as a potential biomarker test for gastric cancer. Biochem. Biophys. Res. Commun., 2017, 493(3), 1322-1328.
[http://dx.doi.org/10.1016/j.bbrc.2017.10.003] [PMID: 28986250]
[81]
Zeng, Q.; Jin, C.; Chen, W.; Xia, F.; Wang, Q.; Fan, F.; Du, J.; Guo, Y.; Lin, C.; Yang, K.; Li, J.; Peng, X.; Li, X.; Cao, K. Downregulation of serum miR-17 and miR-106b levels in gastric cancer and benign gastric diseases. Chin. J. Cancer Res., 2014, 26(6), 711-716.
[PMID: 25561770]
[82]
Li, F.; Guo, Y.; Liu, J.; Zhang, R. The significance of elevated plasma expression of microRNA 106b~25 clusters in gastric cancer. PLoS One, 2017, 12(5), e0178427.
[http://dx.doi.org/10.1371/journal.pone.0178427] [PMID: 28562634]
[83]
Chen, S.; Zhu, J.; Yu, F.; Tian, Y.; Ma, S.; Liu, X. Combination of miRNA and RNA functions as potential biomarkers for gastric cancer. Tumour Biol., 2015, 36(12), 9909-9918.
[http://dx.doi.org/10.1007/s13277-015-3756-9] [PMID: 26168960]
[84]
Jiang, X.; Wang, W.; Yang, Y.; Du, L.; Yang, X.; Wang, L.; Zheng, G.; Duan, W.; Wang, R.; Zhang, X.; Wang, L.; Chen, X.; Wang, C. Identification of circulating microRNA signatures as potential noninvasive biomarkers for prediction and prognosis of lymph node metastasis in gastric cancer. Oncotarget, 2017, 8(39), 65132-65142.
[http://dx.doi.org/10.18632/oncotarget.17789] [PMID: 29029418]
[85]
Liu, S.; Suo, J.; Wang, C.; Sun, X.; Wang, D.; He, L.; Zhang, Y.; Li, W. Prognostic significance of low miR-144 expression in gastric cancer. Cancer Biomark., 2017, 20(4), 547-552.
[http://dx.doi.org/10.3233/CBM-170351] [PMID: 28800316]
[86]
Liu, H.; Zhu, L.; Liu, B.; Yang, L.; Meng, X.; Zhang, W.; Ma, Y.; Xiao, H. Genome-wide microRNA profiles identify miR-378 as a serum biomarker for early detection of gastric cancer. Cancer Lett., 2012, 316(2), 196-203.
[http://dx.doi.org/10.1016/j.canlet.2011.10.034] [PMID: 22169097]
[87]
Tsai, M.M.; Wang, C.S.; Tsai, C.Y.; Huang, C.G.; Lee, K.F.; Huang, H.W.; Lin, Y.H.; Chi, H.C.; Kuo, L.M.; Lu, P.H.; Lin, K.H. Circulating microRNA-196a/b are novel biomarkers associated with metastatic gastric cancer. Eur. J. Cancer, 2016, 64, 137-148.
[http://dx.doi.org/10.1016/j.ejca.2016.05.007] [PMID: 27420607]
[88]
Hou, C.G.; Luo, X.Y.; Li, G. Diagnostic and prognostic value of serum microRNA-206 in patients with gastric cancer. Cell. Physiol. Biochem., 2016, 39(4), 1512-1520.
[http://dx.doi.org/10.1159/000447854] [PMID: 27614739]
[89]
Zheng, Y.; Cui, L.; Sun, W.; Zhou, H.; Yuan, X.; Huo, M.; Chen, J.; Lou, Y.; Guo, J. MicroRNA-21 is a new marker of circulating tumor cells in gastric cancer patients. Cancer Biomark., 2012, 10(2), 71-77.
[http://dx.doi.org/10.3233/CBM-2011-0231] [PMID: 22430134]
[90]
Wang, B.; Zhang, Q. The expression and clinical significance of circulating microRNA-21 in serum of five solid tumors. J. Cancer Res. Clin. Oncol., 2012, 138(10), 1659-1666.
[http://dx.doi.org/10.1007/s00432-012-1244-9] [PMID: 22638884]
[91]
Wu, J.; Li, G.; Wang, Z.; Yao, Y.; Chen, R.; Pu, X.; Wang, J. Circulating microRNA-21 is a potential diagnostic biomarker in gastric cancer. Dis. Markers, 2015, 2015, 435656.
[http://dx.doi.org/10.1155/2015/435656] [PMID: 26063956]
[92]
Fu, Z.; Qian, F.; Yang, X.; Jiang, H.; Chen, Y.; Liu, S. Circulating miR-222 in plasma and its potential diagnostic and prognostic value in gastric cancer. Med. Oncol., 2014, 31(9), 164.
[http://dx.doi.org/10.1007/s12032-014-0164-8] [PMID: 25129310]
[93]
Zhuang, K.; Han, K.; Tang, H.; Yin, X.; Zhang, J.; Zhang, X.; Zhang, L. Up-regulation of plasma miR-23b is associated with poor prognosis of gastric cancer. Med. Sci. Monit., 2016, 22, 356-361.
[http://dx.doi.org/10.12659/MSM.895428] [PMID: 26835790]
[94]
Zhang, W.H.; Gui, J.H.; Wang, C.Z.; Chang, Q.; Xu, S.P.; Cai, C.H.; Li, Y.N.; Tian, Y.P.; Yan, L.; Wu, B. The identification of miR-375 as a potential biomarker in distal gastric adenocarcinoma. Oncol. Res., 2012, 20(4), 139-147.
[http://dx.doi.org/10.3727/096504012X13522227232156] [PMID: 23461060]
[95]
Hung, P.S.; Chen, C.Y.; Chen, W.T.; Kuo, C.Y.; Fang, W.L.; Huang, K.H.; Chiu, P.C.; Lo, S.S. miR-376c promotes carcinogenesis and serves as a plasma marker for gastric carcinoma. PLoS One, 2017, 12(5), e0177346.
[http://dx.doi.org/10.1371/journal.pone.0177346] [PMID: 28486502]
[96]
Zhou, H.; Xiao, B.; Zhou, F.; Deng, H.; Zhang, X.; Lou, Y.; Gong, Z.; Du, C.; Guo, J. MiR-421 is a functional marker of circulating tumor cells in gastric cancer patients. Biomarkers, 2012, 17(2), 104-110.
[http://dx.doi.org/10.3109/1354750X.2011.614961] [PMID: 22263628]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy