Abstract
Colorectal cancer (CRC) is a multifactorial disease commonly diagnosed worldwide, with high mortality rates. Several studies demonstrate important associations between differential expression of micro-RNAs (miRs) and the prognosis of CRC. The present study aimed to identify differentially expressed tissue miRs associated with prognostic factors in CRC patients, through a systematic review of the Literature. Using the PubMed database, Cochrane Library and Web of Science, studies published in English evaluating miRs differentially expressed in tumor tissue and significantly associated with the prognostic aspects of CRC were selected. All the included studies used RT-PCR (Taqman or SYBR Green) for miR expression analysis and the period of publication was from 2009 to 2018. A total of 115 articles accomplished the inclusion criteria and were included in the review. The studies investigated the expression of 100 different miRs associated with prognostic aspects in colorectal cancer patients. The most frequent oncogenic miRs investigated were miR-21, miR-181a, miR-182, miR-183, miR-210 and miR-224 and the hyperexpression of these miRs was associated with distant metastasis, lymph node metastasis and worse survival in patients with CRC. The most frequent tumor suppressor miRs were miR-126, miR-199b and miR-22 and the hypoexpression of these miRs was associated with distant metastasis, worse prognosis and a higher risk of disease relapse (worse disease-free survival). Specific tissue miRs are shown to be promising prognostic biomarkers in patients with CRC, given their strong association with the prognostic aspects of these tumors, however, new studies are necessary to establish the sensibility and specificity of the individual miRs in order to use them in clinical practice.
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References
INCA (2017) Estimativa 2018-Incidência de câncer no Brasil. Instituto Nacional de Câncer José Alencar Gomes da Silva, Rio de Janerio, p 130
Mayer RJ, Wolpin BM (2009) Systemic treatment of colorectal cancer. Gastroenterology 134(5):1296–1310
Erickson BA, Olawaire AB, Adriana Bermudez ECG, DGM (2017) American Joint Committee on Cancer Staging Manual, 8th edn. Cervix uteri, pp. 649–659
Wilhelmsen M, Kring T, Jorgensen LN, Madsen MR, Jess P, Bulut O et al (2014) Determinants of recurrence after intended curative resection for colorectal cancer. Scand J Gastroenterol 49(12):1399–1408
Siegel R, DeSantis C, Virgo K, Stein K, Mariotto A, Smith T et al (2012) Cancer treatment and survivorship statistics, 2012. CA Cancer J Clin 62(4):220–241
Destri GL, Rubino AS, Latino R, Giannone F, Lanteri R, Scilletta B et al (2015) Preoperative carcinoembryonic antigen and independent prognostic factor still reliable. Int Surg 100:617–625
Pardini B, Rosa F, Naccarati A, Vymetalkova V, Ye Y, Wu X et al (2015) Polymorphisms in microRNA genes as predictors of clinical outcomes in colorectal cancer patients. Carcinogenesis 36(1):82–86
Hansen TF, Christensen RDP, Andersen RF, Sørensen FB, Johnsson A, Jakobsen A (2013) MicroRNA-126 and epidermal growth factor-like domain 7-an angiogenic couple of importance in metastatic colorectal cancer. Results from the Nordic ACT trial. Br J Cancer 109(5):1243–1251
Rasmussen MH, Jensen NF, Tarpgaard LS, Qvortrup C, Rømer MU, Stenvang J et al (2013) High expression of microRNA-625-3p is associated with poor response to first-line oxaliplatin based treatment of metastatic colorectal cancer. Mol Oncol 7(3):1–10
Masuda T, Hayashi N, Kuroda Y, Ito S, Educhi H, Mimori K (2017) MicroRNAs as biomarkers in colorectal cancer. Cancers 9(124):1–15
Toiyama Y, Hur K, Tanaka K, Inoue Y, Kusunoki M, Boland CR et al (2014) Serum miR-200c is a novel prognostic and metastasis-predictive biomarker in patients with colorectal cancer. Ann Surg 259(4):735–743
Gregory RI, Shiekhattar R, Gregory RI, Shiekhattar R (2005) MicroRNA biogenesis and cancer. Cancer 9:3509–3512
Hammond SM (2015) An overview of microRNAs. Adv Drug Deliv Rev 87:3–14
Falzone L, Scola L, Zanghì A, Biondi A, Di CA, Libra M et al (2018) Integrated analysis of colorectal cancer microRNA datasets: identification of microRNAs associated with tumor development. Aging 10(5):1000–1014
Lee Y, Ahn C, Han J, Choi H, Kim J, Yim J et al (2003) The nuclear RNase III Drosha initiates microRNA processing. Nature 425(6956):415–419
MacFarlane L-A, Murphy R (2010) MicroRNA: biogenesis, function and role in cancer. Curr Genom 11(7):537–561
Jonas S, Izaurralde E (2015) Towards a molecular understanding of microRNA-mediated gene silencing. Nat Rev Genet 16(7):421–433. https://doi.org/10.1038/nrg3965
Moutinho C, Esteller M (2017) MicroRNAs and epigenetics. Adv Cancer Res 135:189–220. https://doi.org/10.1016/bs.acr.2017.06.003
Calin GA, Croce CM (2006) MicroRNA signatures in human cancers. Nat Rev Cancer 6(11):857–866
Zhang B, Pan X, Cobb GP, Anderson TA (2007) MicroRNAs as oncogenes and tumor suppressors. Dev Biol 302(1):1–12
Siegel R, Desantis C, Jemal A (2014) Colorectal cancer statistics. CA Cancer J Clin 64(1):104–117
Xi Y, Formentini A, Chien M, Weir DB, Russo JJ, Ju J et al (2007) Prognostic values of microRNAs in colorectal cancer. Biomark Insights 1(251):113–121
Gao S, Zhao Z-Y, Wu R, Zhang Y, Zhang Z-Y (2018) Prognostic value of microRNAs in colorectal cancer: a meta-analysis. Cancer Manag 10:907–929
Thomas J, Ohtsuka M, Pichler M, Ling H (2015) MicroRNAs: clinical relevance in colorectal cancer. Int J Mol Sci 16(12):28063–28076
Michael MZ, O’Connor SM, van Holst Pellekaan NG, Young GP, James RJ (2003) Reduced accumulation of specific microRNAs in colorectal neoplasia. Mol Cancer Res 1(12):882–891
Gao J, Li N, Dong Y, Li S, Xu L, Li X et al (2015) MiR-34a-5p suppresses colorectal cancer metastasis and predicts recurrence in patients with stage II/III colorectal cancer. Oncogene 34(31):4142–4152
Zhou T, Zhang GJ, Zhou H, Xiao HX, Li Y (2014) Overexpression of microRNA-183 in human colorectal cancer and its clinical significance. Eur J Gastroenterol Hepatol 26(2):229–233
Binderup HG, Madsen JS, Helweg Heegaard NH, Houlind K, Andersen RF, Brasen CL (2018) Quantification of microRNA levels in plasma: impact of preanalytical and analytical conditions. PLoS ONE 13(7):1
Ahmed FE, NaC A, Gouda MM, Vos PW, Bonnerup C (2018) RT-qPCR for fecal mature microRNA quantification and validation. Color Cancer Methods Protoc Methods Mol Biol 165:203–215
Fuessel S, Lohse-Fischer A, Van DV, Solomo K, Erdmann K, Wirth MP (2018) Quantification of microRNAs in urine-derived specimens susanne. Urothelial Carcinom Methods Protoc Methods Mol Biol 1655(16):201–226
Wentz-Hunter KK, Potashkin JA (2011) The role of miRNAs as key regulators in the neoplastic microenvironment. Mol Biol Int 2011:1–8
Radovich M, Sood AK, Armaiz-Pena GN, Rodriguez-Aguayo C, Zhang W, Pradeep S et al (2014) Hypoxia-mediated downregulation of miRNA biogenesis promotes tumour progression. Nat Commun 5(1):1–13. https://doi.org/10.1038/ncomms6202
Hennessy E, Driscoll LO (2011) MicroRNA expression analysis: techniques suitable for studies of intercellular and extracellular microRNA. Gene expression profiling: methods and protocols. Methods Mol Biol 784:99–107
Mima K, Nishihara R, Yang J, Dou R, Masugi Y, Shi YY et al (2016) MicroRNA MIR21 (miR-21) and PTGS2 expression in colorectal cancer and patient survival. Clin Cancer Res 22(15):3841–3848
Fukushima Y, Iinuma H, Tsukamoto M, Matsuda K, Hashiguchi Y (2015) Clinical significance of microRNA-21 as a biomarker in each Dukes’ stage of colorectal cancer. Oncol Rep 33(2):573–582
Chen T-H, Wang K-L, Liu C-N, Lee H, Lin C-C, Huang C-C et al (2013) The prognostic significance of APC gene mutation and miR-21 expression in advanced-stage colorectal cancer. Color Dis 15(11):1367–1374
Toiyama Y, Takahashi M, Hur K, Nagasaka T, Tanaka K, Inoue Y et al (2013) Serum miR-21 as a diagnostic and prognostic biomarker in colorectal cancer. J Natl Cancer Inst 105(12):849–859
Wu Y, Song Y, Xiong Y, Wang X, Xu K, Han B et al (2017) MicroRNA-21 (Mir-21) promotes cell growth and invasion by repressing tumor suppressor PTEN in colorectal cancer. Cell Physiol Biochem 43(3):945–958
Shibuya H, Iinuma H, Shimada R, Horiuchi A, Watanabe T (2010) Clinicopathological and prognostic value of microRNA-21 and microRNA-155 in colorectal cancer. Oncology 79:313–320
Ji D, Chen Z, Li M, Zhan T, Yao Y, Zhang Z et al (2014) MicroRNA-181a promotes tumor growth and liver metastasis in colorectal cancer by targeting the tumor suppressor WIF-1. Mol Cancer 13(1):86
Nishimura J, Handa R, Yamamoto H, Tanaka F, Shibata K, Mimori K et al (2012) microRNA-181a is associated with poor prognosis of colorectal cancer. Oncol Rep 28(6):2221–2226
Li Z, Wang H, Xu Z, Sun Y, Han J (2016) Expression and mechanism of microRNA-181a on incidence and survival in late liver metastases of colorectal cancer. Oncol Rep 35(3):1403–1408
Xiao G, Tang H, Wei W, Li J, Ji L, Ge J (2014) Aberrant expression of microRNA-15a and microRNA-16 synergistically associates with tumor progression and prognosis in patients with colorectal cancer. Gastroenterol Res Pract 2014:364549
Diamantopoulos MA, Kontos CK, Kerimis D, Papadopoulos IN, Scorilas A (2017) Upregulated miR-16 expression is an independent indicator of relapse and poor overall survival of colorectal adenocarcinoma patients. Clin Chem Lab Med 55(5):737–747
Qian J, Jiang B, Li M, Chen J, Fang M (2013) Prognostic significance of microRNA-16 expression in human colorectal cancer. World J Surg 37(12):2944–2949
Guo Y, Li X, Lin C, Zhang Y, Hu G, Zhou J et al (2015) MicroRNA-133b inhibits connective tissue growth factor in colorectal cancer and correlates with the clinical stage of the disease. Mol Med Rep 11(4):2805–2812
Ellermeier C, Vang S, Cleveland K, Durand W, Resnick MB, Brodsky AS (2014) Prognostic microRNA expression signature from examination of colorectal primary and metastatic tumors. Anticancer Res 34(8):3957–3968
Akçakaya P, Ekelund S, Kolosenko I, Caramuta S, Özata D, Xie H et al (2011) miR-185 and miR-133b deregulation is associated with overall survival and metastasis in colorectal cancer. Int J Oncol 39(2):311–318
Liu Y, Zhou Y, Feng X, Yang P, Yang J, Ping A et al (2014) Low expression of microRNA-126 is associated with. Wiley Period 53:358–365
Wang LL, Du LT, Li J, Liu YM, Qu AL, Yang YM et al (2014) Decreased expression of miR-133a correlates with poor prognosis in colorectal cancer patients. World J Gastroenterol 20(32):11340–11346
Wan TMH, Lam CSC, Ng L, Chow AKM, Wong SKM, Li HS et al (2014) The clinicopathological significance of miR-133a in colorectal cancer. Dis Mark 2014:919283
Rapti SM, Kontos CK, Papadopoulos IN, Scorilas A (2014) Enhanced miR-182 transcription is a predictor of poor overall survival in colorectal adenocarcinoma patients. Clin Chem Lab Med 52(8):1217–1227
Liu H, Du L, Wen Z, Yang Y, Li J, Wang L et al (2013) Up-regulation of miR-182 expression in colorectal cancer tissues and its prognostic value. Int J Colorectal Dis 28(5):697–703
Chen Y, Song W (2018) Wnt/catenin β1/microRNA 183 predicts recurrence and prognosis of patients with colorectal cancer. Oncol Lett 15(4):4451–4456
Cristóbal I, Caramés C, Rincón R, Manso R, Madoz-Gúrpide J, Torrejón B et al (2017) Downregulation of microRNA-199b predicts unfavorable prognosis and emerges as a novel therapeutic target which contributes to PP2A inhibition in metastatic colorectal cancer. Oncotarget 8(25):40169–40180
Shen ZZ-LZ, Wang B, Jiang KK-WK, Ye CC-XC, Cheng C, Yan Y-CYY-CY et al (2016) Downregulation of miR-199b is associated with distant metastasis in colorectal cancer via activation of SIRT1 and inhibition of CREB/KISS1 signaling. Oncotarget 7(23):35092–35105
Zhang G, Xia S, Tian H, Liu Z, Zhou T (2012) Clinical significance of miR-22 expression in patients with colorectal cancer. Med Oncol 29(5):3108–3112
Xia S-S, Zhang G-J, Liu Z-L, Tian H-P, He Y, Meng C-Y et al (2017) MicroRNA-22 suppresses the growth, migration and invasion of colorectal cancer cells through a Sp1 negative feedback loop. Oncotarget 8(22):36266–36278
Adamopoulos PG, Kontos CK, Rapti SM, Papadopoulos IN, Scorilas A (2015) MiR-224 overexpression is a strong and independent prognosticator of short-term relapse and poor overall survival in colorectal adenocarcinoma. Int J Oncol 46(2):849–859
Liao WT, Li TT, Wang ZG, Wang SY, He MR, Ye YP et al (2013) microRNA-224 promotes cell proliferation and tumor growth in human colorectal cancer by repressing PHLPP1 and PHLPP2. Clin Cancer Res 19(17):4662–4672
Kerimis D, Kontos CK, Christodoulou S, Papadopoulos IN, Scorilas A (2017) Elevated expression of miR-24-3p is a potentially adverse prognostic factor in colorectal adenocarcinoma. Clin Biochem 50(6):285–292. https://doi.org/10.1016/j.clinbiochem.2016.11.034
Gao Y, Liu Y, Du L, Li J, Qu A, Zhang X et al (2015) Down-regulation of miR-24-3p in colorectal cancer is associated with malignant behavior. Med Oncol 32(1):362
Nagano Y, Toiyama Y, Okugawa Y, Imaoka H, Fujikawa H, Yasuda H et al (2016) MicroRNA-7 is associated with malignant potential and poor prognosis in human colorectal cancer. Anticancer Res 36(12):6521–6526
Suto T, Yokobori T, Yajima R, Morita H, Fujii T, Yamaguchi S et al (2015) MicroRNA-7 expression in colorectal cancer is associated with poor prognosis and regulates cetuximab sensitivity via EGFR regulation. Carcinogenesis 36(3):338–345
Ge J, Chen Z, Li R, Lu T, Xiao G (2014) Upregulation of microRNA-196a and microRNA-196b cooperatively correlate with aggressive progression and unfavorable prognosis in patients with colorectal cancer. Cancer Cell Int 14(1):1–8
Li H, Dai S, Zhen T, Shi H, Zhang F, Yang Y et al (2014) Clinical and biological significance of miR-378a-3p and miR-378a-5p in colorectal cancer. Eur J Cancer 50(6):1207–1221. https://doi.org/10.1016/j.ejca.2013.12.010
Wang CJ, Zhou ZG, Wang L, Yang L, Zhou B, Gu J et al (2009) Clinicopathological significance of microRNA-31, -143 and -145 expression in colorectal cancer. Dis Mark 26(1):27–34
Fang L, Li H, Wang L, Hu J, Jin T, Wang J et al (2014) MicroRNA-17-5p promotes chemotherapeutic drug resistance and tumour metastasis of colorectal cancer by repressing PTEN expression. Oncotarget 5(10):2974–2987
Sun HB, Chen X, Ji H, Wu T, Lu HW, Zhang Y et al (2014) MiR-494 is an independent prognostic factor and promotes cell migration and invasion in colorectal cancer by directly targeting PTEN. Int J Oncol 45(6):2486–2494
Zhang GJ, Li Y, Zhou H, Xiao HX, Zhou T (2014) miR-20a is an independent prognostic factor in colorectal cancer and is involved in cell metastasis. Mol Med Rep 10(1):283–291
Cheng D, Zhao S, Tang H, Zhang D, Sun H, Yu F et al (2016) MicroRNA-20a-5p promotes colorectal cancer invasion and metastasis by downregulating Smad4. Oncotarget 7(29):45199–45213
Gao S-J, Chen L, Lu W, Zhang L, Wang L, Zhu H-H (2018) miR-888 functions as an oncogene and predicts poor prognosis in colorectal cancer. Oncol Lett 15:9101–9109
Nishida N, Yokobori T, Mimori K, Sudo T, Tanaka F, Shibata K et al (2011) MicroRNA miR-125b is a prognostic marker in human colorectal cancer. Int J Oncol 38(5):1437–1443
Ma W, Liu B, Li J, Jiang J, Zhou R, Huang L et al (2018) MicroRNA-302c represses epithelial–mesenchymal transition and metastasis by targeting transcription factor AP-4 in colorectal cancer. Biomed Pharmacother 105:670–676. https://doi.org/10.1016/j.biopha.2018.06.025
Tong F, Ying Y, Pan H, Zhao W, Li H, Zhan X (2018) Microrna-466 (Mir-466) functions as a tumor suppressor and prognostic factor in colorectal cancer (CRC). Bosn J Basic Med Sci 18(3):252–259
Zhang L, Xie F, Tang C, Xu W, Ding X, Liang J (2017) miR-340 suppresses tumor growth and enhances chemosensitivity of colorectal cancer by targeting RLIP76. Eur Rev Med Pharmacol Sci 21:2875–2886
Stiegelbauer V, Vychytilova-Faltejskova P, Karbiener M, Pehserl AM, Reicher A, Resel M et al (2017) MiR-196b-5p regulates colorectal cancer cell migration and metastases through interaction with HOXB7 and GALNT5. Clin Cancer Res 23(17):5255–5266
Wen L, Li Y, Jiang Z, Zhang Y, Yang B, Han F (2017) MiR-944 inhibits cell migration and invasion by targeting MACC1 in colorectal cancer. Oncol Rep 37(6):3415–3422
Yan L, Qiu J, Yao J (2017) Downregulation of microRNA-30d promotes cell proliferation and invasion by targeting LRH-1 in colorectal carcinoma. Int J Mol Med 39(6):1371–1380
He Z, Yu L, Luo S, Li M, Li J, Li Q et al (2017) miR-296 inhibits the metastasis and epithelial-mesenchymal transition of colorectal cancer by targeting S100A4. BMC Cancer 17(1):1–10
Wang Y-X, Chen Y-R, Liu S-S, Ye Y-P, Jiao H-L, Wang S-Y et al (2016) MiR-384 inhibits human colorectal cancer metastasis by targeting KRAS and CDC42. Oncotarget 7(51):84826–84838
Wu L, Shi B, Huang K, Fan G (2015) MicroRNA-128 suppresses cell growth and metastasis in colorectal carcinoma by targeting IRS1. Oncol Rep 34(5):2797–2805
Liao W, Gu C, Huang A, Yao J, Sun R (2016) MicroRNA-33b inhibits tumor cell growth and is associated with prognosis in colorectal cancer patients. Clin Transl Oncol 18(5):449–456
Qu YL, Wang HF, Sun ZQ, Tang Y, Han XN, Yu XB et al (2015) Up-regulated miR-155-5p promotes cell proliferation, invasion and metastasis in colorectal carcinoma. Int J Clin Exp Pathol 8(6):6988–6994
Kai Y, Qiang C, Xinxin P, Miaomiao Z, Kuailu L (2015) Decreased miR-154 expression and its clinical significance in human colorectal cancer. World J Surg Oncol 13(195):615–619. https://doi.org/10.1186/s12957-015-0607-5
Xu K, Liu X, Mao X, Xue L, Wang R, Chen L et al (2015) MicroRNA-149 suppresses colorectal cancer cell migration and invasion by directly targeting forkhead box transcription factor FOXM1. Cell Physiol Biochem 35(2):499–515
Wang B, Shen ZL, Gao ZD, Zhao G, Wang CY, Yang Y et al (2015) MiR-194, commonly repressed in colorectal cancer, suppresses tumor growth by regulating the MAP4K4/c-Jun/MDM2 signaling pathway. Cell Cycle 14(7):1046–1058
Chen P, Xi Q, Wang Q, Wei P (2014) Downregulation of microRNA-100 correlates with tumor progression and poor prognosis in colorectal cancer. Med Oncol 31(10):1–6
Sun ZF, Zhang Z, Liu Z, Qiu B, Liu K, Dong G (2014) MicroRNA-335 inhibits invasion and metastasis of colorectal cancer by targeting ZEB2. Med Oncol 31(6):982
Yu H, Gao G, Jiang L, Guo L, Lin M, Jiao X et al (2013) Decreased expression of miR-218 is associated with poor prognosis in patients with colorectal cancer. Int J Clin Exp Pathol 6(12):2904–2911
Tao Y, Ma C, Fan Q, Wang Y, Han T, Sun C (2018) MicroRNA-1296 facilitates proliferation, migration and invasion of colorectal cancer cells by targeting SFPQ. J Cancer 9(13):2317–2326
Chen W, Tong K, Yu J (2017) MicroRNA-130a is upregulated in colorectal cancer and promotes cell growth and motility by directly targeting forkhead box F2. Mol Med Rep 16(4):5241–5248
Rapti SM, Kontos CK, Papadopoulos IN, Scorilas A (2016) High miR-96 levels in colorectal adenocarcinoma predict poor prognosis, particularly in patients without distant metastasis at the time of initial diagnosis. Tumor Biol 37(9):11815–11824. https://doi.org/10.1007/s13277-016-5023-0
Ma W, Yu Q, Jiang J, Du X, Huang L, Zhao L et al (2016) miR-517a is an independent prognostic marker and contributes to cell migration and invasion in human colorectal cancer. Oncol Lett 11(1):2583–2589
Zhang GJ, Li JS, Zhou H, Xiao HX, Li Y, Zhou T (2015) MicroRNA-106b promotes colorectal cancer cell migration and invasion by directly targeting DLC1. J Exp Clin Cancer Res 34(1):1–11
Perez-Carbonell L, Sinicrope FA, Alberts SR, Oberg AL, Balaguer F, Castells A et al (2015) MiR-320e is a novel prognostic biomarker in colorectal cancer. Br J Cancer 113(1):83–90. https://doi.org/10.1038/bjc.2015.168
Liu M, Zhi Q, Wang W, Zhang Q, Fang T, Ma Q (2015) Up-regulation of miR-592 correlates with tumor progression and poor prognosis in patients with colorectal cancer. Biomed Pharmacother 69:214–220. https://doi.org/10.1016/j.biopha.2014.12.001
Wang X, Kuang Y, Shen X, Zhou H, Chen Y, Han Y et al (2014) Evaluation of miR-720 prognostic significance in patients with colorectal cancer. Tumor Biol 36(2):719–727
Chu D, Zheng J, Li J, Li Y, Zhang J, Zhao Q et al (2014) MicroRNA-630 is a prognostic marker for patients with colorectal cancer. Tumor Biol 35(10):9787–9792
Qu A, Du L, Yang Y, Liu H, Li J, Wang L et al (2014) Hypoxia-inducible MiR-210 is an independent prognostic factor and contributes to metastasis in colorectal cancer. PLoS ONE 9(3):e90952
Li X, Yang C, Wang X, Zhang J, Zhang R, Liu R (2014) The expression of miR-25 is increased in colorectal cancer and is associated with patient prognosis. Med Oncol 31(1):781
Qin S, Zhu Y, Ai F, Li Y, Bai B, Yao W et al (2014) MicroRNA-191 correlates with poor prognosis of colorectal carcinoma and plays multiple roles by targeting tissue inhibitor of metalloprotease 3 S. Neoplasma 61(1):27–34
Zhou T, Zhang G, Liu Z, Xia S, Tian H (2013) Overexpression of miR-92a correlates with tumor metastasis and poor prognosis in patients with colorectal cancer. Int J Color Dis 28(11):19–24
Wang N, Liu W (2018) Increased expression of miR-552 acts as a potential predictor biomarker for poor prognosis of colorectal cancer. Eur Rev Med Pharmacol Sci 22:412–416
Liu TP, Huang CC, Yeh KT, Ke TW, Wei PL, Yang JR et al (2016) Down-regulation of let-7a-5p predicts lymph node metastasis and prognosis in colorectal cancer: implications for chemotherapy. Surg Oncol 25(4):429–434. https://doi.org/10.1016/j.suronc.2016.05.016
Mokutani Y, Uemura M, Munakata K, Okuzaki D, Haraguchi N, Takahashi H et al (2016) Down-regulation of microRNA-132 is associated with poor prognosis of colorectal cancer. Ann Surg Oncol 23:599–608
Sun P, Sun D, Wang X, Liu T, Ma Z, Duan L (2015) miR-206 is an independent prognostic factor and inhibits tumor invasion and migration in colorectal cancer. Cancer Biomark 15(4):391–396
Zhang G, Zhou H, Xiao H, Li Y, Zhou T (2014) MiR-378 is an independent prognostic factor and inhibits cell growth and invasion in colorectal cancer. BMC Cancer 14(1):109. https://doi.org/10.1186/1471-2407-14-109
Song Y, Xu Y, Wang Z, Chen Y, Yue Z, Gao P et al (2012) MicroRNA-148b suppresses cell growth by targeting cholecystokinin-2 receptor in colorectal cancer. Int J Cancer 131(5):1042–1051
Bin L, Zhang M, Lixia L, Aimin Z, Hua Y, Yanhong S et al (2016) Down-regulation of miRNA-30c predicts poor prognosis in colorectal cancer patients. Rev Rom Med Lab 24(4):369–375
Lin M, Duan B, Hu J, Yu H, Sheng H, Gao H et al (2017) Decreased expression of miR-193a-3p is associated with poor prognosis in colorectal cancer. Oncol Lett 14(1):1061–1067
Li J, Du L, Yang Y, Wang C, Liu H, Wang L et al (2013) MiR-429 is an independent prognostic factor in colorectal cancer and exerts its anti-apoptotic function by targeting SOX2. Cancer Lett 329(1):84–90. https://doi.org/10.1016/j.canlet.2012.10.019
Cui BH, Hong X (2018) Mir-6852 serves as a prognostic biomarker in colorectal cancer and inhibits tumor growth and metastasis by targeting tcf7. Exp Ther Med 16(2):879–885
Wang L, Jiang C, Li D, Ge X, Shi Z, Li C et al (2016) MicroRNA-497 inhibits tumor growth and increases chemosensitivity to 5-fluorouracil treatment by targeting KSR1. Oncotarget 7(3):2660–2671
Zhang P, Ji DB, Han HB, Shi YF, Du CZ, Gu J (2014) Downregulation of miR-193a-5p correlates with lymph node metastasis and poor prognosis in colorectal cancer. World J Gastroenterol 20(34):12241–12248
Orang AV, Safaralizadeh R, Hosseinpour Feizi MA, Somi MH (2014) Diagnostic and prognostic value of miR-205 in colorectal cancer. Asian Pac J Cancer Prev 15(9):4033–4037
Long L, Huang G, Zhu H, Guo Y, Liu Y, Huo J (2013) Down-regulation of miR-138 promotes colorectal cancer metastasis via directly targeting TWIST2. J Transl Med 11(1):1–10
Lou X, Qi X, Zhang Y, Long H, Yang J (2013) Decreased expression of microRNA-625 is associated with tumor metastasis and poor prognosis in patients with colorectal cancer. J Surg Oncol 108(4):230–235
Meng X, Wu J, Pan C, Wang H, Ying X, Zhou Y et al (2013) Genetic and epigenetic down-regulation of microRNA-212 promotes colorectal tumor metastasis via dysregulation of MnSOD. Gastroenterology 145(2):426-436.e6. https://doi.org/10.1053/j.gastro.2013.04.004
Wang X, Wang J, Ma H, Zhang J, Zhou X (2012) Downregulation of miR-195 correlates with lymph node metastasis and poor prognosis in colorectal cancer. Med Oncol 29(34):919–927
Roh MS, Lee HW, Jung SB, Kim K, Lee EH, Mil P et al (2018) Expression of miR-200c and its clinicopathological significance in patients with colorectal cancer. Pathol Res Pract 214(3):350–355. https://doi.org/10.1016/j.prp.2018.01.005
Liu D-R, Guan Q-L, Gao M-T, Jiang L, Kang H-X (2016) miR-1260b is a potential prognostic biomarker in colorectal cancer. Med Sci Monit 22:2417–2423
Mo Z-H, Wu X-D, Li S, Fei B-Y, Zhang B (2014) Expression and clinical significance of MicroRNA-376a in colorectal cancer. Asian Pac J Cancer Prev 15(21):9265–9270
Wan D, He S, Xie B, Xu G, Gu W, Shen C et al (2013) Aberrant expression of miR-199a-3p and its clinical significance in colorectal cancers. Med Oncol 30(1):378
Nishida N, Yamashita S, Mimori K, Sudo T, Tanaka F, Shibata K et al (2012) MicroRNA-10b is a prognostic indicator in colorectal cancer and confers resistance to the chemotherapeutic agent 5-fluorouracil in colorectal cancer cells. Ann Surg Oncol 19(9):3065–3071
Yu L, Lu Y, Han X, Zhao W, Li J, Mao J et al (2016) microRNA-140-5p inhibits colorectal cancer invasion and metastasis by targeting ADAMTS5 and IGFBP5. Stem Cell Res Ther 7(1):1–11. https://doi.org/10.1186/s13287-016-0438-5
Li W, Chang J, Wang S, Liu X, Junjie P, Huang D et al (2015) miRNA-99b-5p suppresses liver metastasis of colorectal cancer by down-regulating mTOR. Oncotarget 6(27):24448–24462
Ress AL, Stiegelbauer V, Winter E, Schwarzenbacher D, Kiesslich T, Lax S et al (2015) MiR-96-5p influences cellular growth and is associated with poor survival in colorectal cancer patients. Mol Carcinog 54(11):1442–1450
Yamashita S, Yamamoto H, Mimori K, Nishida N, Takahashi H, Haraguchi N et al (2012) MicroRNA-372 is associated with poor prognosis in colorectal cancer. Oncology 82(4):205–212
Zhou C, Cui F, Li J, Wang D, Wei Y, Wu Y et al (2017) MiR-650 represses high-risk non-metastatic colorectal cancer progression via inhibition of AKT2/GSK3beta/E-cadherin pathway. Oncotarget 8(30):49534–49547
Wang ZS, Zhong M, Bian YH, Mu YF, Qin SL, Yu MH et al (2016) MicroRNA-187 inhibits tumor growth and invasion by directly targeting CD276 in colorectal cancer. Oncotarget 7(28):44266–44276
Hibino Y, Sakamoto N, Naito Y, Goto K, Oo HZ, Sentani K et al (2015) Significance of miR-148a in colorectal neoplasia: downregulation of miR-148a contributes to the carcinogenesis and cell invasion of colorectal cancer. Pathobiology 82(5):233–241
Wang B, Shen ZL, Jiang KW, Zhao G, You WC, Chao YY et al (2015) MicroRNA-217 functions as a prognosis predictor and inhibits colorectal cancer cell proliferation and invasion via an AEG-1 dependent mechanism. BMC Cancer 15(1):1–11
Inoue A, Yamamoto H, Uemura M, Nishimura J, Hata T, Takemasa I et al (2015) MicroRNA-29b is a novel prognostic marker in colorectal cancer. Ann Surg Oncol 22:1410–1418
Yin Y, Zhang B, Wang W, Fei B, Quan C, Zhang J et al (2014) MiR-204-5p inhibits proliferation and invasion and enhances chemotherapeutic sensitivity of colorectal cancer cells by downregulating RAB22A. Clin Cancer Res 20(23):6187–6699
Song M, Yin Y, Zhang J, Zhang B, Bian Z, Quan C et al (2014) MiR-139-5p inhibits migration and invasion of colorectal cancer by downregulating AMFR and NOTCH1. Protein Cell 5(11):851–861
Jinushi T, Shibayama Y, Kinoshita I, Oizumi S, Jinushi M, Aota T et al (2014) Low expression levels of microRNA-124-5p correlated with poor prognosis in colorectal cancer via targeting of SMC4. Cancer Med 3(6):1544–1552
Wang MJ, Li Y, Wang R, Wang C, Yu YY, Yang L et al (2013) Downregulation of microRNA-124 is an independent prognostic factor in patients with colorectal cancer. Int J Colorectal Dis 28(2):183–189
Tsiakanikas P, Kontos CK, Kerimis D, Papadopoulos IN, Scorilas A (2018) High microRNA-28-5p expression in colorectal adenocarcinoma predicts short-term relapse of node-negative patients and poor overall survival of patients with non-metastatic disease. Clin Chem Lab Med 56(6):990–1000
Rapti SM, Kontos CK, Christodoulou S, Papadopoulos IN, Scorilas A (2017) miR-34a overexpression predicts poor prognostic outcome in colorectal adenocarcinoma, independently of clinicopathological factors with established prognostic value. Clin Biochem 50(16–17):918–924. https://doi.org/10.1016/j.clinbiochem.2017.06.004
Kontos CK, Tsiakanikas P, Avgeris M, Papadopoulos IN, Scorilas A (2017) miR-15a-5p, a novel prognostic biomarker, predicting recurrent colorectal adenocarcinoma. Mol Diagnosis Ther 21(4):453–464
Yamazaki N, Koga Y, Taniguchi H, Kojima M, Kanemitsu Y, Saito N et al (2017) High expression of miR-181c as a predictive marker of recurrence in stage II colorectal cancer. Oncotarget 8(4):6970–6983
Noguchi T, Toiyama Y, Kitajima T, Imaoka H, Hiro J, Saigusa S et al (2016) MiRNA-503 promotes tumor progression and is associated with early recurrence and poor prognosis in human colorectal cancer. Oncology 90(4):221–231
Sümbül AT, Göğebakan B, Bayram S, Batmacı CY, Öztuzcu S (2015) MicroRNA 211 expression is upregulated and associated with poor prognosis in colorectal cancer: a case–control study. Tumor Biol 36(12):9703–9709
Wu LZ, Mei YY, Tao DL, Dong Z, Li WL, Zhang X et al (2014) Overexpression of miR-223 correlates with tumor metastasis and poor prognosis in patients with colorectal cancer. Med Oncol 31(11):1–5
Yiu AJ, Yiu CY (2016) Biomarkers in colorectal cancer. Anticancer Res 36:1093–1338
Peng Q, Zhang X, Min M, Zou L, Shen P, Yaqun Z (2017) The clinical role of microRNA-21 as a promising biomarker in the diagnosis and prognosis of colorectal cancer: a systematic review and meta-analysis. Oncotarget 8(27):44893–44909
Shirafkan N, Mansoori B, Mohammadi A, Shomali N, Ghasbi M, Baradaran B (2018) MicroRNAs as novel biomarkers for colorectal cancer: new outlooks. Biomed Pharmacother 97:1319–1330. https://doi.org/10.1016/j.biopha.2017.11.046
Chung JH, Eng C (2005) Nuclear-cytoplasmic partitioning of phosphatase and tensin homologue deleted on chromosome 10 (PTEN) differentially regulates the cell cycle and apoptosis. Cancer Res 65(18):8096–8100
Zhang B, Halder SK, Kashikar ND, Cho Y, Datta A, David L et al (2010) Anti-metastatic role of Smad4 signaling in colorectal cancer bixiang. Gastroenterology 138(3):969–980
Oren M, Bentwich Z, Rosenfeld N, Raver-Shapira N, Moskovits N, Spector Y et al (2007) Transcriptional activation of miR-34a contributes to p53-mediated apoptosis. Mol Cell 26(5):731–743
Jones RP, Sutton PA, Evans JP, Clifford R, McAvoy A, Lewis J et al (2017) Specific mutations in KRAS codon 12 are associated with worse overall survival in patients with advanced and recurrent colorectal cancer. Br J Cancer 116(7):923–929. https://doi.org/10.1038/bjc.2017.37
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dos Santos, I.L., Penna, K.G.B.D., dos Santos Carneiro, M.A. et al. Tissue micro-RNAs associated with colorectal cancer prognosis: a systematic review. Mol Biol Rep 48, 1853–1867 (2021). https://doi.org/10.1007/s11033-020-06075-1
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DOI: https://doi.org/10.1007/s11033-020-06075-1