Diagnostic Value of Potential MicroRNAs in CRC: A Meta-Analysis

Author(s): Sofia Fathi*, Fadila Guessous and Mehdi Karkouri

Volume 11, Issue 3, 2022

Published on: 16 September, 2022

Page: [190 - 205] Pages: 16

DOI: 10.2174/2211536611666220523103316

Price: $65


Background: MicroRNAs (miRNAs) are small noncoding RNA molecules involved in the post-transcriptional regulation of genes. Deregulated expression of miRNAs is involved in different pathogenic mechanisms, particularly colorectal cancer (CRC) carcinogenesis. Due to their stability and accessibility, circulating miRNAs represent a new family of biomarkers with great potential. Therefore, certain miRNAs can be used as diagnostic biomarkers in CRC.

Objective: This systematic analysis aimed to explore the individual efficacy of the most investigated blood-based miRNAs for CRC diagnosis, namely miR-21, miR-29a and miR-92a.

Methods: Articles were retrieved from databases such as PubMed and Google Scholar, and studies designed to evaluate the diagnostic value of microRNAs in CRC were then selected. We subsequently explored the diagnostic accuracy of each miRNA using parameters such as (SE, SPE, PLR, NLR). The meta-analysis was performed using the Review Manager (Revman) 5.4 software and the Meta Disc software.

Results: Our results suggested that serum miR-21 levels showed great potential as a diagnostic molecular marker. The overall pooled results for sensitivity, specificity, area under the curve (AUC), PLR, and NLR were 78%, 91%, 0.9519, 8.12 and 0.17, respectively.

Conclusion: miRNAs have become increasingly important in the diagnosis of CRC. Based on these findings, circulating miR-21 levels may have a potential value for early detection and might be used as a novel diagnostic biomarker for CRC.

Keywords: Colorectal, cancer, microRNA, serum, diagnostic, biomarker, miR-29a, miR-92a, miR-21, meta-analysis.

Graphical Abstract
Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 2018; 68(6): 394-424.
[] [PMID: 30207593]
Messersmith WA. Systemic management of colorectal cancer. J Natl Compr Canc Netw 2017; 15(5S): 699-702.
[] [PMID: 28515248]
Grady WM, Pritchard CC. Molecular alterations and biomarkers in colorectal cancer. Toxicol Pathol 2014; 42(1): 124-39.
[] [PMID: 24178577]
Esquela-Kerscher A, Slack FJ. Oncomirs - microRNAs with a role in cancer. Nat Rev Cancer 2006; 6(4): 259-69.
[] [PMID: 16557279]
Drusco A, Croce CM. MicroRNAs and cancer: A long story for short RNAs. Adv Cancer Res 2017; 135: 1-24.
[] [PMID: 28882219]
Lee RC, Feinbaum RL, Ambros V. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 1993; 75(5): 843-54.
[] [PMID: 8252621]
Kim VN. MicroRNA biogenesis: Coordinated cropping and dicing. Nat Rev Mol Cell Biol 2005; 6(5): 376-85.
[] [PMID: 15852042]
Ha M, Kim VN. Regulation of microRNA biogenesis. Nat Rev Mol Cell Biol 2014; 15(8): 509-24.
[] [PMID: 25027649]
Brodersen P, Voinnet O. Revisiting the principles of microRNA target recognition and mode of action. Nat Rev Mol Cell Biol 2009; 10(2): 141-8.
[] [PMID: 19145236]
Okamura K, Liu N, Lai EC. Distinct mechanisms for microRNA strand selection by Drosophila argonautes. Mol Cell 2009; 36(3): 431-44.
[] [PMID: 19917251]
Cancer Genome Atlas Network. Comprehensive molecular characterization of human colon and rectal cancer. Nature 2012; 487(7407): 330-7.
[] [PMID: 22810696]
Noubissi FK, Elcheva I, Bhatia N, et al. CRD-BP mediates stabilization of betaTrCP1 and c-myc mRNA in response to beta-catenin signal-ling. Nature 2006; 441(7095): 898-901.
[] [PMID: 16778892]
Tetsu O, McCormick F. Beta-catenin regulates expression of cyclin D1 in colon carcinoma cells. Nature 1999; 398(6726): 422-6.
[] [PMID: 10201372]
Nagel R, le Sage C, Diosdado B, et al. Regulation of the adenomatous polyposis coli gene by the miR-135 family in colorectal cancer. Cancer Res 2008; 68(14): 5795-802.
[] [PMID: 18632633]
Zhang G-J, Li L-F, Yang G-D, et al. MiR-92a promotes stem cell-like properties by activating Wnt/β-catenin signaling in colorectal cancer. Oncotarget 2017; 8(60): 101760-70.
[] [PMID: 29254202]
Sansal I, Sellers WR. The biology and clinical relevance of the PTEN tumor suppressor pathway. J Clin Oncol 2004; 22(14): 2954-63.
[] [PMID: 15254063]
Maehama T, Dixon JE. The tumor suppressor, PTEN/MMAC1, dephosphorylates the lipid second messenger, phosphatidylinositol 3,4,5-trisphosphate. J Biol Chem 1998; 273(22): 13375-8.
[] [PMID: 9593664]
Sun Y, Tian H, Wang L. Effects of PTEN on the proliferation and apoptosis of colorectal cancer cells via the phosphoinositol-3-kinase/Akt pathway. Oncol Rep 2015; 33(4): 1828-36.
[] [PMID: 25683168]
Wu Y, Song Y, Xiong Y, et al. MicroRNA-21 (Mir-21) promotes cell growth and invasion by repressing tumor suppressor PTEN in colo-rectal cancer. Cell Physiol Biochem 2017; 43(3): 945-58.
[] [PMID: 28957811]
Pellatt AJ, Mullany LE, Herrick JS, et al. The TGFβ-signaling pathway and colorectal cancer: associations between dysregulated genes and miRNAs. J Transl Med 2018; 16(1): 191.
[] [PMID: 29986714]
Sokolova V, Fiorino A, Zoni E, et al. The effects of miR-20a on p21: Two mechanisms blocking growth arrest in TGF-β-responsive colon carcinoma. J Cell Physiol 2015; 230(12): 3105-14.
[] [PMID: 26012475]
Markman B, Javier Ramos F, Capdevila J, Tabernero J. EGFR and KRAS in colorectal cancer. Adv Clin Chem 2010; 51: 71-119.
[] [PMID: 20857619]
Xing Y, Jing H, Zhang Y, Suo J, Qian M. MicroRNA-141-3p affected proliferation, chemosensitivity, migration and invasion of colorectal cancer cells by targeting EGFR. Int J Biochem Cell Biol 2020; 118: 105643.
[] [PMID: 31704502]
Nishida N, Yokobori T, Mimori K, et al. MicroRNA miR-125b is a prognostic marker in human colorectal cancer. Int J Oncol 2011; 38(5): 1437-43.
[PMID: 21399871]
Le MTN, Shyh-Chang N, Khaw SL, et al. Conserved regulation of p53 network dosage by microRNA-125b occurs through evolving miR-NA-target gene pairs. PLoS Genet 2011; 7(9): e1002242.
[] [PMID: 21935352]
He L, He X, Lim LP, et al. A microRNA component of the p53 tumour suppressor network. Nature 2007; 447(7148): 1130-4.
[] [PMID: 17554337]
Ruepp A, Kowarsch A, Schmidl D, et al. PhenomiR: A knowledgebase for microRNA expression in diseases and biological processes. Genome Biol 2010; 11(1): R6.
[] [PMID: 20089154]
Chautard R, Ibrahim S, Gueguinou M, Lecomte T, Raoul W. Micro-ARN et cancer colorectal Hépato-Gastro Oncol Dig. 2019. [cited 2022 Jan 25]; Available from:
Lee H, Han S, Kwon CS, Lee D. Biogenesis and regulation of the let-7 miRNAs and their functional implications. Protein Cell 2016; 7(2): 100-13.
[] [PMID: 26399619]
Wang J, Huang SK, Zhao M, et al. Identification of a circulating microRNA signature for colorectal cancer detection. PLoS One 2014; 9(4): e87451.
[] [PMID: 24709885]
Margetis N, Kotsinas A, Mariolis-Sapsakos T. The promising role of let-7 microRNA in colorectal cancer: Practical points for clinicians. Clin Oncol 2018; 3: 8.
Shenouda SK, Alahari SK. MicroRNA function in cancer: Oncogene or a tumor suppressor? Cancer Metastasis Rev 2009; 28(3-4): 369-78.
[] [PMID: 20012925]
Lanza G, Ferracin M, Gafà R, et al. mRNA/microRNA gene expression profile in microsatellite unstable colorectal cancer. Mol Cancer 2007; 6(1): 54.
[] [PMID: 17716371]
Lu J, Getz G, Miska EA, et al. MicroRNA expression profiles classify human cancers. Nature 2005; 435(7043): 834-8.
[] [PMID: 15944708]
Deng J, Lei W, Fu J-C, Zhang L, Li J-H, Xiong J-P. Targeting miR-21 enhances the sensitivity of human colon cancer HT-29 cells to chemoradiotherapy in vitro. Biochem Biophys Res Commun 2014; 443(3): 789-95.
[] [PMID: 24275137]
Asangani IA, Rasheed SA, Nikolova DA, et al. MicroRNA-21 (miR-21) post-transcriptionally downregulates tumor suppressor Pdcd4 and stimulates invasion, intravasation and metastasis in colorectal cancer. Oncogene 2008; 27(15): 2128-36.
[] [PMID: 17968323]
Ma Y, Qin C, Li L, Miao R, Jing C, Cui X. MicroRNA-21 promotes cell proliferation by targeting tumor suppressor TET1 in colorectal cancer. Int J Clin Exp Pathol 2018; 11(3): 1439-45.
[PMID: 31938241]
Li J, Liang H, Bai M, et al. MiR-135b promotes cancer progression by targeting Transforming Growth Factor Beta Receptor II (TGFBR2) in colorectal cancer. PLoS One 2015; 10(6): e0130194.
[] [PMID: 26061281]
Zhou W, Li X, Liu F, et al. MiR-135a promotes growth and invasion of colorectal cancer via metastasis suppressor 1 in vitro. Acta Biochim Biophys Sin (Shanghai) 2012; 44(10): 838-46.
[] [PMID: 23017832]
Ke T-W, Wei P-L, Yeh K-T, Chen WT-L, Cheng Y-W. MiR-92a promotes cell metastasis of colorectal cancer through PTEN-Mediated PI3K/AKT pathway. Ann Surg Oncol 2015; 22(8): 2649-55.
[] [PMID: 25515201]
Zhang G, Zhou H, Xiao H, Liu Z, Tian H, Zhou T. MicroRNA-92a functions as an oncogene in colorectal cancer by targeting PTEN. Dig Dis Sci 2014; 59(1): 98-107.
[] [PMID: 24026406]
Wei Q-D, Zheng W-B, Sun K, Xue Q, Yang C-Z, Li G-X. MiR-92a promotes the invasion and migration of colorectal cancer by targeting RECK. Int J Clin Exp Pathol 2019; 12(5): 1565-77.
[PMID: 31933974]
Nishida N, Nagahara M, Sato T, et al. Microarray analysis of colorectal cancer stromal tissue reveals upregulation of two oncogenic miR-NA clusters. Clin Cancer Res 2012; 18(11): 3054-70.
[] [PMID: 22452939]
Gao F, Wang W. MicroRNA-96 promotes the proliferation of colorectal cancer cells and targets tumor protein p53 inducible nuclear pro-tein 1, forkhead box protein O1 (FOXO1) and FOXO3a. Mol Med Rep 2015; 11(2): 1200-6.
[] [PMID: 25369914]
Yue C, Chen J, Li Z, Li L, Chen J, Guo Y. MicroRNA-96 promotes occurrence and progression of colorectal cancer via regulation of the AMPKα2-FTO-m6A/MYC axis. J Exp Clin Cancer Res 2020; 39(1): 240.
[] [PMID: 33183350]
Chen E, Li Q, Wang H, Yang F, Min L, Yang J. MiR-92a promotes tumorigenesis of colorectal cancer, a transcriptomic and functional based study. Biomed Pharmacother Biomedecine Pharmacother 2018; 106: 1370-7.
[] [PMID: 30119209]
Zhang Y, Wang X, Wang Z, Tang H, Fan H, Guo Q. miR-182 promotes cell growth and invasion by targeting forkhead box F2 transcription factor in colorectal cancer. Oncol Rep 2015; 33(5): 2592-8.
[] [PMID: 25738520]
Peng H, Pan X, Su Q, Zhu L-S, Ma G-D. MiR-372-3p promotes tumor progression by targeting LATS2 in colorectal cancer. Eur Rev Med Pharmacol Sci 2019; 23(19): 8332-44.
[PMID: 31646563]
Yamashita S, Yamamoto H, Mimori K, et al. MicroRNA-372 is associated with poor prognosis in colorectal cancer. Oncology 2012; 82(4): 205-12.
[] [PMID: 22456107]
Wang LQ, Yu P, Li B, et al. MiR-372 and miR-373 enhance the stemness of colorectal cancer cells by repressing differentiation signaling pathways. Mol Oncol 2018; 12(11): 1949-64.
[] [PMID: 30171794]
Tang W, Zhu Y, Gao J, et al. MicroRNA-29a promotes colorectal cancer metastasis by regulating matrix metalloproteinase 2 and E-cadherin via KLF4. Br J Cancer 2014; 110(2): 450-8.
[] [PMID: 24281002]
Ma Q, Wang Y, Zhang H, Wang F. MiR-1290 contributes to colorectal cancer cell proliferation by targeting INPP4B. Oncol Res 2018; 26(8): 1167-74.
[] [PMID: 28915933]
Ye L, Jiang T, Shao H, et al. MiR-1290 is a biomarker in DNA-mismatch-repair-deficient colon cancer and promotes resistance to 5-fluorouracil by directly targeting hMSH2. Mol Ther Nucleic Acids 2017; 7: 453-64.
[] [PMID: 28624221]
Liu W, Qian K, Wei X, et al. MiR 27a promotes proliferation, migration, and invasion of colorectal cancer by targeting FAM172A and acts as a diagnostic and prognostic biomarker. Oncol Rep 2017; 37(6): 3554-64.
[] [PMID: 28440497]
Chen W, Tong K, Yu J. MicroRNA-130a is upregulated in colorectal cancer and promotes cell growth and motility by directly targeting forkhead box F2. Mol Med Rep 2017; 16(4): 5241-8.
[] [PMID: 28849155]
Liu L, Nie J, Chen L, et al. The oncogenic role of microRNA-130a/301a/454 in human colorectal cancer via targeting Smad4 expression. PLoS One 2013; 8(2): e55532.
[] [PMID: 23393589]
Clancy C, Joyce MR, Kerin MJ. The use of circulating microRNAs as diagnostic biomarkers in colorectal cancer. Cancer Biomark Sect Dis Markers 2015; 15(2): 103-13.
[] [PMID: 25547322]
Yang Y-P, Ting W-C, Chen L-M, Lu T-L, Bao B-Y. Polymorphisms in microRNA binding sites predict colorectal cancer survival. Int J Med Sci 2017; 14(1): 53-7.
[] [PMID: 28138309]
Inoue A, Yamamoto H, Uemura M, et al. MicroRNA-29b is a Novel Prognostic Marker in Colorectal Cancer. Ann Surg Oncol 2015; 22(S3) (Suppl. 3): S1410-8.
[] [PMID: 25472644]
Liu H, Cheng X-H. MiR-29b reverses oxaliplatin-resistance in colorectal cancer by targeting SIRT1. Oncotarget 2018; 9(15): 12304-15.
[] [PMID: 29552311]
Ding D, Li C, Zhao T, Li D, Yang L, Zhang B. LncRNA H19/miR-29b-3p/PGRN axis promoted epithelial-mesenchymal transition of colo-rectal cancer cells by acting on Wnt Signaling. Mol Cells 2018; 41(5): 423-35.
[PMID: 29754471]
Wang B, Li W, Liu H, et al. MiR-29b suppresses tumor growth and metastasis in colorectal cancer via downregulating Tiam1 expression and inhibiting epithelial-mesenchymal transition. Cell Death Dis 2014; 5(7): e1335.
[] [PMID: 25032858]
Zhao H-J, Ren L-L, Wang Z-H, et al. MiR-194 deregulation contributes to colorectal carcinogenesis via targeting AKT2 pathway. Theranostics 2014; 4(12): 1193-208.
[] [PMID: 25285168]
Sun B, Fang Y-T, Jin D-J, et al. MiR-194 inhibits the proliferation of SW620 colon cancer stem cells through downregulation of SSH2 expression. Cancer Manag Res 2019; 11: 10229-38.
[] [PMID: 31824193]
Liu X-H, Wang J, Dong Y-H. The inhibitory effect of miR-375 targeting sp1 in colorectal cancer cell proliferation. Eur Rev Med Pharmacol Sci 2018; 22(2): 405-11.
[PMID: 29424897]
Mao Q, Quan T, Luo B, Guo X, Liu L, Zheng Q. MiR-375 targets KLF4 and impacts the proliferation of colorectal carcinoma. Tumour Biol 2016; 37(1): 463-71.
[] [PMID: 26224477]
Wang Y, Tang Q, Li M, Jiang S, Wang X. MicroRNA-375 inhibits colorectal cancer growth by targeting PIK3CA. Biochem Biophys Res Commun 2014; 444(2): 199-204.
[] [PMID: 24440701]
Xu L, Wen T, Liu Z, et al. MicroRNA-375 suppresses human colorectal cancer metastasis by targeting Frizzled 8. Oncotarget 2016; 7(26): 40644-56.
[] [PMID: 27276676]
Li X, Ding Y, Liu N, Sun Q, Zhang J. MicroRNA 760 inhibits cell proliferation and invasion of colorectal cancer by targeting the SP1 mediated PTEN/AKT signalling pathway. Mol Med Rep 2017; 16(6): 9692-700.
[] [PMID: 29039575]
Cao L, Liu Y, Wang D, et al. MiR-760 suppresses human colorectal cancer growth by targeting BATF3/AP-1/cyclinD1 signaling. J Exp Clin Cancer Res 2018; 37(1): 83.
[] [PMID: 29661228]
Fan J, Zhang W, Wu Y, Wan P, Guo Q, Zhang Y. miR 124 inhibits cell growth through targeting IQGAP1 in colorectal cancer. Mol Med Rep 2018; 18(6): 5270-8.
[] [PMID: 30272357]
Xie X-Q, Wang M-J, Li Y, et al. MiR-124 intensified oxaliplatin-based chemotherapy by targeting CAPN2 in colorectal cancer. Mol Ther Oncolytics 2020; 17: 320-31.
[] [PMID: 32382656]
Zhou L, Xu Z, Ren X, Chen K, Xin S. MicroRNA-124 (MiR-124) inhibits cell proliferation, metastasis and invasion in colorectal cancer by downregulating Rho-Associated Protein Kinase 1(ROCK1). Cell Physiol Biochem 2016; 38(5): 1785-95.
[] [PMID: 27159971]
Zhang J, Lu Y, Yue X, et al. MiR-124 suppresses growth of human colorectal cancer by inhibiting STAT3. PLoS One 2013; 8(8): e70300.
[] [PMID: 23940556]
Jiang S, Miao D, Wang M, Lv J, Wang Y, Tong J. MiR-30-5p suppresses cell chemoresistance and stemness in colorectal cancer through USP22/Wnt/β-catenin signaling axis. J Cell Mol Med 2019; 23(1): 630-40.
[] [PMID: 30338942]
Wei W, Yang Y, Cai J, et al. MiR-30a-5p suppresses tumor metastasis of human colorectal cancer by targeting ITGB3. Cell Physiol Biochem 2016; 39(3): 1165-76.
[] [PMID: 27576787]
Johnson SM, Grosshans H, Shingara J, et al. RAS is regulated by the let-7 microRNA family. Cell 2005; 120(5): 635-47.
[] [PMID: 15766527]
Han H-B, Gu J, Zuo H-J, et al. Let-7c functions as a metastasis suppressor by targeting MMP11 and PBX3 in colorectal cancer. J Pathol 2012; 226(3): 544-55.
[] [PMID: 21984339]
Li Z, Pan W, Shen Y, et al. IGF1/IGF1R and microRNA let-7e down-regulate each other and modulate proliferation and migration of colo-rectal cancer cells. Cell Cycle 2018; 17(10): 1212-9.
[] [PMID: 29886785]
Jones CM, Athanasiou T. Summary receiver operating characteristic curve analysis techniques in the evaluation of diagnostic tests. Ann Thorac Surg 2005; 79(1): 16-20.
[] [PMID: 15620907]
Grimes DA, Schulz KF. Refining clinical diagnosis with likelihood ratios. Lancet 2005; 365(9469): 1500-5.
[] [PMID: 15850636]
Ahmed Hassan E, El-Din Abd El-Rehim AS, Mohammed Kholef EF, Abd-Elgwad Elsewify W. Potential role of plasma miR-21 and miR-92a in distinguishing between irritable bowel syndrome, ulcerative colitis, and colorectal cancer. Gastroenterol Hepatol Bed Bench 2020; 13(2): 147-54.
[PMID: 32308936]
Bader El Din NG, Ibrahim MK, El-Shenawy R, et al. MicroRNAs expression profiling in Egyptian colorectal cancer patients. IUBMB Life 2020; 72(2): 275-84.
[] [PMID: 31512372]
Brunet Vega A, Pericay C, Moya I, et al. MicroRNA expression profile in stage III colorectal cancer: circulating miR-18a and miR-29a as promising biomarkers. Oncol Rep 2013; 30(1): 320-6.
[] [PMID: 23673725]
Elshafei A, Shaker O, Abd El-Motaal O, Salman T. The expression profiling of serum miR-92a, miR-375, and miR-760 in colorectal can-cer: An Egyptian study. Tumour Biol 2017; 39(6): 1010428317705765.
[] [PMID: 28618945]
Farouk S, Khairy A, Salem AM, Soliman AF, Bader El Din NG. Differential expression of miR-21, miR-23a, and miR-27a, and their diag-nostic significance in Egyptian colorectal cancer patients. Genet Test Mol Biomarkers 2020; 24(12): 825-34.
[] [PMID: 33290159]
Ghareib AF, Mohamed RH, Abd El-Fatah AR, Saadawy SF. Assessment of serum microRNA-21 gene expression for diagnosis and prog-nosis of colorectal cancer. J Gastrointest Cancer 2020; 51(3): 818-23.
[] [PMID: 31482406]
Giráldez MD, Lozano JJ, Ramírez G, et al. Circulating microRNAs as biomarkers of colorectal cancer: Results from a genome-wide profil-ing and validation study. Clin Gastroenterol Hepatol 2013; 11(6): 681-8.e3.
[] [PMID: 23267864]
Huang Z, Huang D, Ni S, Peng Z, Sheng W, Du X. Plasma microRNAs are promising novel biomarkers for early detection of colorectal cancer. Int J Cancer 2010; 127(1): 118-26.
[] [PMID: 19876917]
Jin X-H, Lu S, Wang A-F. Expression and clinical significance of miR-4516 and miR-21-5p in serum of patients with colorectal cancer. BMC Cancer 2020; 20(1): 241.
[] [PMID: 32293319]
Kanaan Z, Rai SN, Eichenberger MR, et al. Plasma miR-21: A potential diagnostic marker of colorectal cancer. Ann Surg 2012; 256(3): 544-51.
[] [PMID: 22868372]
Li G, Wang Q, Li Z, Shen Y. Serum miR-21 and miR-210 as promising non-invasive biomarkers for the diagnosis and prognosis of colo-rectal cancer. Rev Esp Enferm Dig 2020; 112(11): 832-7.
[] [PMID: 33054296]
Liu G-H, Zhou Z-G, Chen R, et al. Serum miR-21 and miR-92a as biomarkers in the diagnosis and prognosis of colorectal cancer. Tumour Biol 2013; 34(4): 2175-81.
[] [PMID: 23625654]
Liu H-N, Liu T-T, Wu H, et al. Serum microRNA signatures and metabolomics have high diagnostic value in colorectal cancer using two novel methods. Cancer Sci 2018; 109(4): 1185-94.
[] [PMID: 29363233]
Luo X, Stock C, Burwinkel B, Brenner H. Identification and evaluation of plasma microRNAs for early detection of colorectal cancer. PLoS One 2013; 8(5): e62880.
[] [PMID: 23690963]
Ogata-Kawata H, Izumiya M, Kurioka D, et al. Circulating exosomal microRNAs as biomarkers of colon cancer. PLoS One 2014; 9(4): e92921.
[] [PMID: 24705249]
Hassan R, Omar M, Shehata M, et al. Role of serum miR-21 and miR-92a in colorectal cancer diagnosis as novel molecular biomarkers. Int J Cancer Biomed Res 2021; 5(1): 95-104.
Sabry D, El-Deek SEM, Maher M, et al. Role of miRNA-210, miRNA-21 and miRNA-126 as diagnostic biomarkers in colorectal carcino-ma: impact of HIF-1α-VEGF signaling pathway. Mol Cell Biochem 2019; 454(1-2): 177-89.
[] [PMID: 30357530]
Sazanov AA, Kiselyova EV, Zakharenko AA, Romanov MN, Zaraysky MI. Plasma and saliva miR-21 expression in colorectal cancer patients. J Appl Genet 2017; 58(2): 231-7.
[] [PMID: 27910062]
Shi Y, Liu Z. Serum miR-92a-1 is a novel diagnostic biomarker for colorectal cancer. J Cell Mol Med 2020; 24(15): 8363-7.
[] [PMID: 32562465]
Yamada A, Horimatsu T, Okugawa Y, et al. Serum miR-21, miR-29a, and miR-125b are promising biomarkers for the early detection of colorectal neoplasia. Clin Cancer Res 2015; 21(18): 4234-42.
[] [PMID: 26038573]
Ng EKO, Chong WWS, Jin H, et al. Differential expression of microRNAs in plasma of patients with colorectal cancer: A potential marker for colorectal cancer screening. Gut 2009; 58(10): 1375-81.
[] [PMID: 19201770]
Diosdado B, van de Wiel MA, Terhaar Sive Droste JS, et al. MiR-17-92 cluster is associated with 13q gain and c-myc expression during colorectal adenoma to adenocarcinoma progression. Br J Cancer 2009; 101(4): 707-14.
[] [PMID: 19672269]
Mogilyansky E, Rigoutsos I. The miR-17/92 cluster: A comprehensive update on its genomics, genetics, functions and increasingly im-portant and numerous roles in health and disease. Cell Death Differ 2013; 20(12): 1603-14.
[] [PMID: 24212931]
Liu M, Tang Q, Qiu M, et al. MiR-21 targets the tumor suppressor RhoB and regulates proliferation, invasion and apoptosis in colorectal cancer cells. FEBS Lett 2011; 585(19): 2998-3005.
[] [PMID: 21872591]
Toiyama Y, Takahashi M, Hur K, et al. Serum miR-21 as a diagnostic and prognostic biomarker in colorectal cancer. J Natl Cancer Inst 2013; 105(12): 849-59.
[] [PMID: 23704278]
Jiang H, Zhang G, Wu J-H, Jiang C-P. Diverse roles of miR-29 in cancer (review). Oncol Rep 2014; 31(4): 1509-16.
[] [PMID: 24573597]
Wang LG, Gu J. Serum microRNA-29a is a promising novel marker for early detection of colorectal liver metastasis. Cancer Epidemiol 2012; 36(1): e61-7.
[] [PMID: 22018950]

Rights & Permissions Print Export Cite as
© 2023 Bentham Science Publishers | Privacy Policy