MicroRNAs as Biomarkers in Colorectal Cancer
Abstract
:1. Introduction
2. Methods
3. Biomarkers for the Early Detection and Prediction of Prognosis in CRC
3.1. miRs in Tumor Tissues
3.2. miRs in Stool
3.3. miRs in Serum/Plasma
4. Biomarkers for Prediction of Drug Efficacy
5. Limitations
5.1. Conflicting Functions of miRs
5.2. Sensitivity/Specificity
5.3. Internal Control
6. Development of Novel Diagnostic Methods Using miRs
7. Conclusions
Acknowledgments
Author Contributions
Conflicts of Interest
References
- The Cancer Genome Atlas Network. Comprehensive molecular characterization of human colon and rectal cancer. Nature 2012, 487, 330–337. [Google Scholar]
- Uchi, R.; Takahashi, Y.; Niida, A.; Shimamura, T.; Hirata, H.; Sugimachi, K.; Sawada, G.; Iwaya, T.; Kurashige, J.; Shinden, Y.; et al. Integrated multiregional analysis proposing a new model of colorectal cancer evolution. PLoS Genet. 2016, 12, e1005778. [Google Scholar] [CrossRef] [PubMed]
- Chu, C.Y.; Rana, T.M. Small RNAs: Regulators and guardians of the genome. J. Cell. Physiol. 2007, 213, 412–419. [Google Scholar] [CrossRef] [PubMed]
- Bartel, D.P. MicroRNAs: Genomics, biogenesis, mechanism, and function. Cell 2004, 116, 281–297. [Google Scholar] [CrossRef]
- Lin, S.; Gregory, R.I. MicroRNA biogenesis pathways in cancer. Nat. Rev. Cancer 2015, 15, 321–333. [Google Scholar] [CrossRef] [PubMed]
- Michael, M.Z.; SM, O.C.; van Holst Pellekaan, N.G.; Young, G.P.; James, R.J. Reduced accumulation of specific microRNAs in colorectal neoplasia. Mol. Cancer Res. 2003, 1, 882–891. [Google Scholar] [PubMed]
- Zavoral, M.; Suchanek, S.; Zavada, F.; Dusek, L.; Muzik, J.; Seifert, B.; Fric, P. Colorectal cancer screening in Europe. World J. Gastroenterol. 2009, 15, 5907–5915. [Google Scholar] [CrossRef] [PubMed]
- Altobelli, E.; Lattanzi, A.; Paduano, R.; Varassi, G.; di Orio, F. Colorectal cancer prevention in Europe: Burden of disease and status of screening programs. Prev. Med. 2014, 62, 132–141. [Google Scholar] [CrossRef] [PubMed]
- Sovich, J.L.; Sartor, Z.; Misra, S. Developments in screening tests and strategies for colorectal cancer. Biomed. Res. Int. 2015, 2015, 326728. [Google Scholar] [CrossRef] [PubMed]
- Van Rijn, J.C.; Reitsma, J.B.; Stoker, J.; Bossuyt, P.M.; van Deventer, S.J.; Dekker, E. Polyp miss rate determined by tandem colonoscopy: A systematic review. Am. J. Gastroenterol. 2006, 101, 343–350. [Google Scholar] [CrossRef] [PubMed]
- Leufkens, A.M.; van Oijen, M.G.; Vleggaar, F.P.; Siersema, P.D. Factors influencing the miss rate of polyps in a back-to-back colonoscopy study. Endoscopy 2012, 44, 470–475. [Google Scholar] [CrossRef] [PubMed]
- Dong, Y.; Wu, W.K.; Wu, C.W.; Sung, J.J.; Yu, J.; Ng, S.S. MicroRNA dysregulation in colorectal cancer: A clinical perspective. Br. J. Cancer 2011, 104, 893–898. [Google Scholar] [CrossRef] [PubMed]
- Ren, A.; Dong, Y.; Tsoi, H.; Yu, J. Detection of miRNA as non-invasive biomarkers of colorectal cancer. Int. J. Mol. Sci. 2015, 16, 2810–2823. [Google Scholar] [CrossRef] [PubMed]
- Akao, Y.; Nakagawa, Y.; Naoe, T. MicroRNAs 143 and 145 are possible common onco-microRNAs in human cancers. Oncol. Rep. 2006, 16, 845–850. [Google Scholar] [CrossRef] [PubMed]
- Schee, K.; Boye, K.; Abrahamsen, T.W.; Fodstad, O.; Flatmark, K. Clinical relevance of microRNA miR-21, miR-31, miR-92a, miR-101, miR-106a, and miR-145 in colorectal cancer. BMC Cancer 2012, 12, 505. [Google Scholar] [CrossRef] [PubMed]
- Xuan, Y.; Yang, H.; Zhao, L.; Lau, W.B.; Lau, B.; Ren, N.; Hu, Y.; Yi, T.; Zhao, X.; Zhou, S.; et al. MicroRNAs in colorectal cancer: Small molecules with big functions. Cancer Lett. 2015, 360, 89–105. [Google Scholar] [CrossRef] [PubMed]
- Shen, W.W.; Zeng, Z.; Zhu, W.X.; Fu, G.H. MiR-142–3p functions as a tumor suppressor by targeting CD133, ABCG2, and LGR5 in colon cancer cells. J. Mol. Med. 2013, 91, 989–1000. [Google Scholar] [CrossRef] [PubMed]
- Schetter, A.J.; Okayama, H.; Harris, C.C. The role of microRNAs in colorectal cancer. Cancer J. 2012, 18, 244–252. [Google Scholar] [CrossRef] [PubMed]
- Yang, I.P.; Tsai, H.L.; Miao, Z.F.; Huang, C.W.; Kuo, C.H.; Wu, J.Y.; Wang, W.M.; Juo, S.H.; Wang, J.Y. Development of a deregulating microRNA panel for the detection of early relapse in postoperative colorectal cancer patients. J. Transl. Med. 2016, 14, 108. [Google Scholar] [CrossRef] [PubMed]
- Bovell, L.C.; Shanmugam, C.; Putcha, B.D.; Katkoori, V.R.; Zhang, B.; Bae, S.; Singh, K.P.; Grizzle, W.E.; Manne, U. The prognostic value of microRNAs varies with patient race/ethnicity and stage of colorectal cancer. Clin. Cancer Res. 2013, 19, 3955–3965. [Google Scholar] [CrossRef] [PubMed]
- Cheng, D.; Zhao, S.; Tang, H.; Zhang, D.; Sun, H.; Yu, F.; Jiang, W.; Yue, B.; Wang, J.; Zhang, M.; et al. MicroRNA-20a-5p promotes colorectal cancer invasion and metastasis by downregulating SMAD4. Oncotarget 2016, 7, 45199–45213. [Google Scholar] [CrossRef] [PubMed]
- Schetter, A.J.; Leung, S.Y.; Sohn, J.J.; Zanetti, K.A.; Bowman, E.D.; Yanaihara, N.; Yuen, S.T.; Chan, T.L.; Kwong, D.L.; Au, G.K.; et al. MicroRNA expression profiles associated with prognosis and therapeutic outcome in colon adenocarcinoma. JAMA 2008, 299, 425–436. [Google Scholar] [CrossRef] [PubMed]
- Mima, K.; Nishihara, R.; Yang, J.; Dou, R.; Masugi, Y.; Shi, Y.; da Silva, A.; Cao, Y.; Song, M.; Nowak, J.; et al. MicroRNA miR21 (miR-21) and PTGS2 expression in colorectal cancer and patient survival. Clin. Cancer Res. 2016, 22, 3841–3848. [Google Scholar] [CrossRef] [PubMed]
- Peng, Q.; Zhang, X.; Min, M.; Zou, L.; Shen, P.; Zhu, Y. 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 2017, 8, 44893–44909. [Google Scholar] [CrossRef] [PubMed]
- Chen, Z.; Liu, H.; Jin, W.; Ding, Z.; Zheng, S.; Yu, Y. Tissue microRNA-21 expression predicted recurrence and poor survival in patients with colorectal cancer—A meta-analysis. Onco. Targets Ther. 2016, 9, 2615–2624. [Google Scholar] [PubMed]
- Xia, S.S.; Zhang, G.J.; Liu, Z.L.; Tian, H.P.; He, Y.; Meng, C.Y.; Li, L.F.; Wang, Z.W.; Zhou, T. MicroRNA-22 suppresses the growth, migration and invasion of colorectal cancer cells through a sp1 negative feedback loop. Oncotarget 2017, 8, 36266–36278. [Google Scholar] [CrossRef] [PubMed]
- Ke, T.W.; Wei, P.L.; Yeh, K.T.; Chen, W.T.; Cheng, Y.W. MiR-92a promotes cell metastasis of colorectal cancer through PTEN-mediated PI3K/AKT pathway. Ann. Surg. Oncol. 2015, 22, 2649–2655. [Google Scholar] [CrossRef] [PubMed]
- Shibuya, H.; Iinuma, H.; Shimada, R.; Horiuchi, A.; Watanabe, T. Clinicopathological and prognostic value of microRNA-21 and microRNA-155 in colorectal cancer. Oncology 2010, 79, 313–320. [Google Scholar] [CrossRef] [PubMed]
- Han, H.B.; Gu, J.; Zuo, H.J.; Chen, Z.G.; Zhao, W.; Li, M.; Ji, D.B.; Lu, Y.Y.; Zhang, Z.Q. Let-7c functions as a metastasis suppressor by targeting MMP11 and PBX3 in colorectal cancer. J. Pathol. 2012, 226, 544–555. [Google Scholar] [CrossRef] [PubMed]
- Hansen, T.F.; Kjaer-Frifeldt, S.; Morgenthaler, S.; Blondal, T.; Lindebjerg, J.; Jakobsen, A.; Sorensen, F.B. The prognostic value of microRNA-126 and microvessel density in patients with stage ii colon cancer: Results from a population cohort. J. Transl. Med. 2014, 12, 254. [Google Scholar] [CrossRef] [PubMed]
- Colangelo, T.; Fucci, A.; Votino, C.; Sabatino, L.; Pancione, M.; Laudanna, C.; Binaschi, M.; Bigioni, M.; Maggi, C.A.; Parente, D.; et al. MicroRNA-130b promotes tumor development and is associated with poor prognosis in colorectal cancer. Neoplasia 2013, 15, 1086–1099. [Google Scholar] [CrossRef] [PubMed]
- Mokutani, Y.; Uemura, M.; Munakata, K.; Okuzaki, D.; Haraguchi, N.; Takahashi, H.; Nishimura, J.; Hata, T.; Murata, K.; Takemasa, I.; et al. Down-regulation of microRNA-132 is associated with poor prognosis of colorectal cancer. Ann. Surg. Oncol. 2016, 23, 599–608. [Google Scholar] [CrossRef] [PubMed]
- Liu, X.; Duan, B.; Dong, Y.; He, C.; Zhou, H.; Sheng, H.; Gao, H.; Zhang, X. MicroRNA-139–3p indicates a poor prognosis of colon cancer. Int. J. Clin. Exp. Pathol. 2014, 7, 8046–8052. [Google Scholar] [PubMed]
- Xiao, G.; Tang, H.; Wei, W.; Li, J.; Ji, L.; Ge, J. Aberrant expression of microRNA-15a and microRNA-16 synergistically associates with tumor progression and prognosis in patients with colorectal cancer. Gastroenterol. Res. Pract. 2014, 2014, 364549. [Google Scholar] [CrossRef] [PubMed]
- Zhou, T.; Zhang, G.J.; Zhou, H.; Xiao, H.X.; Li, Y. Overexpression of microRNA-183 in human colorectal cancer and its clinical significance. Eur. J. Gastroenterol. Hepatol. 2014, 26, 229–233. [Google Scholar] [CrossRef] [PubMed]
- Wang, X.; Wang, J.; Ma, H.; Zhang, J.; Zhou, X. Downregulation of miR-195 correlates with lymph node metastasis and poor prognosis in colorectal cancer. Med. Oncol. 2012, 29, 919–927. [Google Scholar] [CrossRef] [PubMed]
- Ge, J.; Chen, Z.; Li, R.; Lu, T.; Xiao, G. Upregulation of microRNA-196a and microRNA-196b cooperatively correlate with aggressive progression and unfavorable prognosis in patients with colorectal cancer. Cancer Cell. Int. 2014, 14, 128. [Google Scholar] [CrossRef] [PubMed]
- Liang, Y.; Yang, W.; Zhu, Y.; Yuan, Y. Prognostic role of microRNA-203 in various carcinomas: Evidence from a meta-analysis involving 13 studies. Springerplus 2016, 5, 1538. [Google Scholar] [CrossRef] [PubMed]
- Karaayvaz, M.; Pal, T.; Song, B.; Zhang, C.; Georgakopoulos, P.; Mehmood, S.; Burke, S.; Shroyer, K.; Ju, J. Prognostic significance of miR-215 in colon cancer. Clin. Colorectal Cancer 2011, 10, 340–347. [Google Scholar] [CrossRef] [PubMed]
- Liao, W.T.; Li, T.T.; Wang, Z.G.; Wang, S.Y.; He, M.R.; Ye, Y.P.; Qi, L.; Cui, Y.M.; Wu, P.; Jiao, H.L.; et al. MicroRNA-224 promotes cell proliferation and tumor growth in human colorectal cancer by repressing PHLPP1 and PHLPP2. Clin. Cancer. Res. 2013, 19, 4662–4672. [Google Scholar] [CrossRef] [PubMed]
- Takeyama, H.; Yamamoto, H.; Yamashita, S.; Wu, X.; Takahashi, H.; Nishimura, J.; Haraguchi, N.; Miyake, Y.; Suzuki, R.; Murata, K.; et al. Decreased miR-340 expression in bone marrow is associated with liver metastasis of colorectal cancer. Mol. Cancer Ther. 2014, 13, 976–985. [Google Scholar] [CrossRef] [PubMed]
- Gao, J.; Li, N.; Dong, Y.; Li, S.; Xu, L.; Li, X.; Li, Y.; Li, Z.; Ng, S.S.; Sung, J.J.; et al. MiR-34a-5p suppresses colorectal cancer metastasis and predicts recurrence in patients with stage II/III colorectal cancer. Oncogene 2015, 34, 4142–4152. [Google Scholar] [CrossRef] [PubMed]
- Perez-Carbonell, L.; Sinicrope, F.A.; Alberts, S.R.; Oberg, A.L.; Balaguer, F.; Castells, A.; Boland, C.R.; Goel, A. MiR-320e is a novel prognostic biomarker in colorectal cancer. Br. J. Cancer. 2015, 113, 83–90. [Google Scholar] [CrossRef] [PubMed]
- Diaz, R.; Silva, J.; Garcia, J.M.; Lorenzo, Y.; Garcia, V.; Pena, C.; Rodriguez, R.; Munoz, C.; Garcia, F.; Bonilla, F.; et al. Deregulated expression of miR-106a predicts survival in human colon cancer patients. Genes Chromosomes Cancer 2008, 47, 794–802. [Google Scholar] [CrossRef] [PubMed]
- Ma, Y.; Zhang, P.; Wang, F.; Zhang, H.; Yang, J.; Peng, J.; Liu, W.; Qin, H. MiR-150 as a potential biomarker associated with prognosis and therapeutic outcome in colorectal cancer. Gut 2012, 61, 1447–1453. [Google Scholar] [CrossRef] [PubMed]
- Weissmann-Brenner, A.; Kushnir, M.; Lithwick Yanai, G.; Aharonov, R.; Gibori, H.; Purim, O.; Kundel, Y.; Morgenstern, S.; Halperin, M.; Niv, Y.; et al. Tumor microRNA-29a expression and the risk of recurrence in stage II colon cancer. Int. J. Oncol. 2012, 40, 2097–2103. [Google Scholar] [PubMed]
- Yamashita, S.; Yamamoto, H.; Mimori, K.; Nishida, N.; Takahashi, H.; Haraguchi, N.; Tanaka, F.; Shibata, K.; Sekimoto, M.; Ishii, H.; et al. MicroRNA-372 is associated with poor prognosis in colorectal cancer. Oncology 2012, 82, 205–212. [Google Scholar] [CrossRef] [PubMed]
- Iwaya, T.; Yokobori, T.; Nishida, N.; Kogo, R.; Sudo, T.; Tanaka, F.; Shibata, K.; Sawada, G.; Takahashi, Y.; Ishibashi, M.; et al. Downregulation of miR-144 is associated with colorectal cancer progression via activation of mTOR signaling pathway. Carcinogenesis 2012, 33, 2391–2397. [Google Scholar] [CrossRef] [PubMed]
- Nishimura, J.; Handa, R.; Yamamoto, H.; Tanaka, F.; Shibata, K.; Mimori, K.; Takemasa, I.; Mizushima, T.; Ikeda, M.; Sekimoto, M.; et al. MicroRNA-181a is associated with poor prognosis of colorectal cancer. Oncol. Rep. 2012, 28, 2221–2226. [Google Scholar] [CrossRef] [PubMed]
- Menendez, P.; Padilla, D.; Villarejo, P.; Palomino, T.; Nieto, P.; Menendez, J.M.; Rodriguez-Montes, J.A. Prognostic implications of serum microRNA-21 in colorectal cancer. J. Surg. Oncol. 2013, 108, 369–373. [Google Scholar] [CrossRef] [PubMed]
- Sun, Y.; Liu, Y.; Cogdell, D.; Calin, G.A.; Sun, B.; Kopetz, S.; Hamilton, S.R.; Zhang, W. Examining plasma microRNA markers for colorectal cancer at different stages. Oncotarget 2016, 7, 11434–11449. [Google Scholar] [CrossRef] [PubMed]
- Jinushi, T.; Shibayama, Y.; Kinoshita, I.; Oizumi, S.; Jinushi, M.; Aota, T.; Takahashi, T.; Horita, S.; Dosaka-Akita, H.; Iseki, K. Low expression levels of microRNA-124–5p correlated with poor prognosis in colorectal cancer via targeting of SMC4. Cancer Med. 2014, 3, 1544–1552. [Google Scholar] [CrossRef] [PubMed]
- Cheng, H.; Zhang, L.; Cogdell, D.E.; Zheng, H.; Schetter, A.J.; Nykter, M.; Harris, C.C.; Chen, K.; Hamilton, S.R.; Zhang, W. Circulating plasma miR-141 is a novel biomarker for metastatic colon cancer and predicts poor prognosis. PLoS ONE 2011, 6, e17745. [Google Scholar] [CrossRef] [PubMed]
- Lv, Z.C.; Fan, Y.S.; Chen, H.B.; Zhao, D.W. Investigation of microRNA-155 as a serum diagnostic and prognostic biomarker for colorectal cancer. Tumour. Biol. 2015, 36, 1619–1625. [Google Scholar] [CrossRef] [PubMed]
- Toiyama, Y.; Hur, K.; Tanaka, K.; Inoue, Y.; Kusunoki, M.; Boland, C.R.; Goel, A. Serum mir-200c is a novel prognostic and metastasis-predictive biomarker in patients with colorectal cancer. Ann. Surg. 2014, 259, 735–743. [Google Scholar] [CrossRef] [PubMed]
- Yu, H.; Gao, G.; Jiang, L.; Guo, L.; Lin, M.; Jiao, X.; Jia, W.; Huang, J. Decreased expression of miR-218 is associated with poor prognosis in patients with colorectal cancer. Int. J. Clin. Exp. Pathol. 2013, 6, 2904–2911. [Google Scholar] [PubMed]
- Pu, X.X.; Huang, G.L.; Guo, H.Q.; Guo, C.C.; Li, H.; Ye, S.; Ling, S.; Jiang, L.; Tian, Y.; Lin, T.Y. Circulating miR-221 directly amplified from plasma is a potential diagnostic and prognostic marker of colorectal cancer and is correlated with p53 expression. J. Gastroenterol. Hepatol. 2010, 25, 1674–1680. [Google Scholar] [CrossRef] [PubMed]
- Tsai, H.L.; Yang, I.P.; Huang, C.W.; Ma, C.J.; Kuo, C.H.; Lu, C.Y.; Juo, S.H.; Wang, J.Y. Clinical significance of microRNA-148a in patients with early relapse of stage II stage and III colorectal cancer after curative resection. Transl. Res. 2013, 162, 258–268. [Google Scholar] [CrossRef] [PubMed]
- Yuan, D.; Li, K.; Zhu, K.; Yan, R.; Dang, C. Plasma miR-183 predicts recurrence and prognosis in patients with colorectal cancer. Cancer Biol. Ther. 2015, 16, 268–275. [Google Scholar] [CrossRef] [PubMed]
- Schou, J.V.; Rossi, S.; Jensen, B.V.; Nielsen, D.L.; Pfeiffer, P.; Hogdall, E.; Yilmaz, M.; Tejpar, S.; Delorenzi, M.; Kruhoffer, M.; et al. MiR-345 in metastatic colorectal cancer: A non-invasive biomarker for clinical outcome in non-kras mutant patients treated with 3rd line cetuximab and irinotecan. PLoS ONE 2014, 9, e99886. [Google Scholar] [CrossRef] [PubMed]
- Matsumura, T.; Sugimachi, K.; Iinuma, H.; Takahashi, Y.; Kurashige, J.; Sawada, G.; Ueda, M.; Uchi, R.; Ueo, H.; Takano, Y.; et al. Exosomal microRNA in serum is a novel biomarker of recurrence in human colorectal cancer. Br. J. Cancer 2015, 113, 275–281. [Google Scholar] [CrossRef] [PubMed]
- Hur, K.; Toiyama, Y.; Okugawa, Y.; Ide, S.; Imaoka, H.; Boland, C.R.; Goel, A. Circulating microRNA-203 predicts prognosis and metastasis in human colorectal cancer. Gut 2017, 66, 654–665. [Google Scholar] [CrossRef] [PubMed]
- Takano, Y.; Masuda, T.; Iinuma, H.; Yamaguchi, R.; Sato, K.; Tobo, T.; Hirata, H.; Kuroda, Y.; Nambara, S.; Hayashi, N.; et al. Circulating exosomal microRNA-203 is associated with metastasis possibly via inducing tumor-associated macrophages in colorectal cancer. Oncotarget 2017. [Google Scholar] [CrossRef]
- Lee, J.K.; Liles, E.G.; Bent, S.; Levin, T.R.; Corley, D.A. Accuracy of fecal immunochemical tests for colorectal cancer: Systematic review and meta-analysis. Ann. Intern. Med. 2014, 160, 171. [Google Scholar] [CrossRef] [PubMed]
- Ahmed, F.E.; Jeffries, C.D.; Vos, P.W.; Flake, G.; Nuovo, G.J.; Sinar, D.R.; Naziri, W.; Marcuard, S.P. Diagnostic microRNA markers for screening sporadic human colon cancer and active ulcerative colitis in stool and tissue. Cancer Genom. Proteom. 2009, 6, 281–295. [Google Scholar]
- Ahmed, F.E.; Ahmed, N.C.; Vos, P.W.; Bonnerup, C.; Atkins, J.N.; Casey, M.; Nuovo, G.J.; Naziri, W.; Wiley, J.E.; Mota, H.; et al. Diagnostic microRNA markers to screen for sporadic human colon cancer in stool: I. Proof of principle. Cancer Genom. Proteom. 2013, 10, 93–113. [Google Scholar]
- Li, J.M.; Zhao, R.H.; Li, S.T.; Xie, C.X.; Jiang, H.H.; Ding, W.J.; Du, P.; Chen, W.; Yang, M.; Cui, L. Down-regulation of fecal miR-143 and miR-145 as potential markers for colorectal cancer. Saudi Med. J. 2012, 33, 24–29. [Google Scholar] [PubMed]
- Link, A.; Balaguer, F.; Shen, Y.; Nagasaka, T.; Lozano, J.J.; Boland, C.R.; Goel, A. Fecal microRNAs as novel biomarkers for colon cancer screening. Cancer Epidemiol. Biomarkers Prev. 2010, 19, 1766–1774. [Google Scholar] [CrossRef] [PubMed]
- Wu, C.W.; Ng, S.S.; Dong, Y.J.; Ng, S.C.; Leung, W.W.; Lee, C.W.; Wong, Y.N.; Chan, F.K.; Yu, J.; Sung, J.J. Detection of miR-92a and miR-21 in stool samples as potential screening biomarkers for colorectal cancer and polyps. Gut 2012, 61, 739–745. [Google Scholar] [CrossRef] [PubMed]
- Wu, C.W.; Ng, S.C.; Dong, Y.; Tian, L.; Ng, S.S.; Leung, W.W.; Law, W.T.; Yau, T.O.; Chan, F.K.; Sung, J.J.; et al. Identification of microRNA-135b in stool as a potential noninvasive biomarker for colorectal cancer and adenoma. Clin. Cancer Res. 2014, 20, 2994–3002. [Google Scholar] [CrossRef] [PubMed]
- Zhu, Y.; Xu, A.; Li, J.; Fu, J.; Wang, G.; Yang, Y.; Cui, L.; Sun, J. Fecal miR-29a and miR-224 as the noninvasive biomarkers for colorectal cancer. Cancer Biomark. 2016, 16, 259–264. [Google Scholar] [CrossRef] [PubMed]
- Koga, Y.; Yasunaga, M.; Takahashi, A.; Kuroda, J.; Moriya, Y.; Akasu, T.; Fujita, S.; Yamamoto, S.; Baba, H.; Matsumura, Y. MicroRNA expression profiling of exfoliated colonocytes isolated from feces for colorectal cancer screening. Cancer Prev. Res. 2010, 3, 1435–1442. [Google Scholar] [CrossRef] [PubMed]
- Yau, T.O.; Wu, C.W.; Dong, Y.; Tang, C.M.; Ng, S.S.; Chan, F.K.; Sung, J.J.; Yu, J. MicroRNA-221 and microRNA-18a identification in stool as potential biomarkers for the non-invasive diagnosis of colorectal carcinoma. Br. J. Cancer 2014, 111, 1765–1771. [Google Scholar] [CrossRef] [PubMed]
- Giraldez, M.D.; Lozano, J.J.; Ramirez, G.; Hijona, E.; Bujanda, L.; Castells, A.; Gironella, M. Circulating microRNAs as biomarkers of colorectal cancer: Results from a genome-wide profiling and validation study. Clin. Gastroenterol. Hepatol. 2013, 11, 681–688. [Google Scholar] [CrossRef] [PubMed]
- Luo, X.; Stock, C.; Burwinkel, B.; Brenner, H. Identification and evaluation of plasma microRNAs for early detection of colorectal cancer. PLoS ONE 2013, 8, e62880. [Google Scholar] [CrossRef] [PubMed]
- Jiang, J.X.; Zhang, N.; Liu, Z.M.; Wang, Y.Y. Detection of microRNA-21 expression as a potential screening biomarker for colorectal cancer: A meta-analysis. Asian Pac. J. Cancer Prev. 2014, 15, 7583–7588. [Google Scholar] [CrossRef] [PubMed]
- Yu, W.; Wang, Z.; Shen, L.I.; Wei, Q. Circulating microRNA-21 as a potential diagnostic marker for colorectal cancer: A meta-analysis. Mol. Clin. Oncol. 2016, 4, 237–244. [Google Scholar] [CrossRef] [PubMed]
- Zhu, M.; Huang, Z.; Zhu, D.; Zhou, X.; Shan, X.; Qi, L.W.; Wu, L.; Cheng, W.; Zhu, J.; Zhang, L.; et al. A panel of microRNA signature in serum for colorectal cancer diagnosis. Oncotarget 2017, 8, 17081–17091. [Google Scholar] [CrossRef] [PubMed]
- Fang, Z.; Tang, J.; Bai, Y.; Lin, H.; You, H.; Jin, H.; Lin, L.; You, P.; Li, J.; Dai, Z.; et al. Plasma levels of microRNA-24, microRNA-320a, and microRNA-423–5p are potential biomarkers for colorectal carcinoma. J. Exp. Clin. Cancer Res. 2015, 34, 86. [Google Scholar] [CrossRef] [PubMed]
- 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, 118–126. [Google Scholar] [CrossRef] [PubMed]
- Nugent, M.; Miller, N.; Kerin, M.J. Circulating miR-34a levels are reduced in colorectal cancer. J. Surg. Oncol. 2012, 106, 947–952. [Google Scholar] [CrossRef] [PubMed]
- Xu, L.; Li, M.; Wang, M.; Yan, D.; Feng, G.; An, G. The expression of microRNA-375 in plasma and tissue is matched in human colorectal cancer. BMC Cancer 2014, 14, 714. [Google Scholar] [CrossRef] [PubMed]
- Wang, S.; Xiang, J.; Li, Z.; Lu, S.; Hu, J.; Gao, X.; Yu, L.; Wang, L.; Wang, J.; Wu, Y.; et al. A plasma microRNA panel for early detection of colorectal cancer. Int. J. Cancer 2015, 136, 152–161. [Google Scholar] [CrossRef] [PubMed]
- Ng, E.K.; Chong, W.W.; Jin, H.; Lam, E.K.; Shin, V.Y.; Yu, J.; Poon, T.C.; Ng, S.S.; Sung, J.J. Differential expression of microRNAs in plasma of patients with colorectal cancer: A potential marker for colorectal cancer screening. Gut 2009, 58, 1375–1381. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wang, J.; Huang, S.K.; Zhao, M.; Yang, M.; Zhong, J.L.; Gu, Y.Y.; Peng, H.; Che, Y.Q.; Huang, C.Z. Identification of a circulating microRNA signature for colorectal cancer detection. PLoS ONE 2014, 9, e87451. [Google Scholar] [CrossRef] [PubMed]
- Zanutto, S.; Pizzamiglio, S.; Ghilotti, M.; Bertan, C.; Ravagnani, F.; Perrone, F.; Leo, E.; Pilotti, S.; Verderio, P.; Gariboldi, M.; et al. Circulating miR-378 in plasma: A reliable, haemolysis-independent biomarker for colorectal cancer. Br. J. Cancer 2014, 110, 1001–1007. [Google Scholar] [CrossRef] [PubMed]
- Wang, Q.; Huang, Z.; Ni, S.; Xiao, X.; Xu, Q.; Wang, L.; Huang, D.; Tan, C.; Sheng, W.; Du, X. Plasma miR-601 and miR-760 are novel biomarkers for the early detection of colorectal cancer. PLoS ONE 2012, 7, e44398. [Google Scholar] [CrossRef] [PubMed]
- Zheng, G.; Du, L.; Yang, X.; Zhang, X.; Wang, L.; Yang, Y.; Li, J.; Wang, C. Serum microRNA panel as biomarkers for early diagnosis of colorectal adenocarcinoma. Br. J. Cancer 2014, 111, 1985–1992. [Google Scholar] [CrossRef] [PubMed]
- Chang, P.Y.; Chen, C.C.; Chang, Y.S.; Tsai, W.S.; You, J.F.; Lin, G.P.; Chen, T.W.; Chen, J.S.; Chan, E.C. MicroRNA-223 and microRNA-92a in stool and plasma samples act as complementary biomarkers to increase colorectal cancer detection. Oncotarget 2016, 7, 10663–10675. [Google Scholar] [CrossRef] [PubMed]
- Yau, T.O.; Wu, C.W.; Tang, C.M.; Chen, Y.; Fang, J.; Dong, Y.; Liang, Q.; Ng, S.S.; Chan, F.K.; Sung, J.J.; et al. MicroRNA-20a in human faeces as a non-invasive biomarker for colorectal cancer. Oncotarget 2016, 7, 1559–1568. [Google Scholar] [CrossRef] [PubMed]
- Kalimutho, M.; Del Vecchio Blanco, G.; Di Cecilia, S.; Sileri, P.; Cretella, M.; Pallone, F.; Federici, G.; Bernardini, S. Differential expression of miR-144* as a novel fecal-based diagnostic marker for colorectal cancer. J. Gastroenterol. 2011, 46, 1391–1402. [Google Scholar] [CrossRef] [PubMed]
- Hunter, M.P.; Ismail, N.; Zhang, X.; Aguda, B.D.; Lee, E.J.; Yu, L.; Xiao, T.; Schafer, J.; Lee, M.L.; Schmittgen, T.D.; et al. Detection of microRNA expression in human peripheral blood microvesicles. PLoS ONE 2008, 3, e3694. [Google Scholar] [CrossRef] [PubMed]
- Chen, X.; Ba, Y.; Ma, L.; Cai, X.; Yin, Y.; Wang, K.; Guo, J.; Zhang, Y.; Chen, J.; Guo, X.; et al. Characterization of microRNAs in serum: A novel class of biomarkers for diagnosis of cancer and other diseases. Cell. Res. 2008, 18, 997–1006. [Google Scholar] [CrossRef] [PubMed]
- Colombo, M.; Raposo, G.; Thery, C. Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles. Annu. Rev. Cell. Dev. Biol. 2014, 30, 255–289. [Google Scholar] [CrossRef] [PubMed]
- Mirzaei, H.; Sahebkar, A.; Jaafari, M.R.; Goodarzi, M.; Mirzaei, H.R. Diagnostic and therapeutic potential of exosomes in cancer: The beginning of a new tale? J. Cell. Physiol. 2016, 232, 3251–3260. [Google Scholar] [CrossRef] [PubMed]
- Silva, J.; Garcia, V.; Rodriguez, M.; Compte, M.; Cisneros, E.; Veguillas, P.; Garcia, J.M.; Dominguez, G.; Campos-Martin, Y.; Cuevas, J.; et al. Analysis of exosome release and its prognostic value in human colorectal cancer. Genes Chromosomes Cancer. 2012, 51, 409–418. [Google Scholar] [CrossRef] [PubMed]
- Hollis, M.; Nair, K.; Vyas, A.; Chaturvedi, L.S.; Gambhir, S.; Vyas, D. MicroRNAs potential utility in colon cancer: Early detection, prognosis, and chemosensitivity. World J. Gastroenterol. 2015, 21, 8284–8292. [Google Scholar] [CrossRef] [PubMed]
- Merhautova, J.; Demlova, R.; Slaby, O. MicroRNA-based therapy in animal models of selected gastrointestinal cancers. Front. Pharmacol. 2016, 7, 329. [Google Scholar] [CrossRef] [PubMed]
- Zhu, L.; Fang, J. The structure and clinical roles of microRNA in colorectal cancer. Gastroenterol. Res. Pract. 2016, 2016, 1360348. [Google Scholar] [CrossRef] [PubMed]
- Xie, T.; Huang, M.; Wang, Y.; Wang, L.; Chen, C.; Chu, X. MicroRNAs as regulators, biomarkers and therapeutic targets in the drug resistance of colorectal cancer. Cell. Physiol. Biochem. 2016, 40, 62–76. [Google Scholar] [CrossRef] [PubMed]
- Hansen, T.F.; Andersen, C.L.; Nielsen, B.S.; Spindler, K.L.; Sorensen, F.B.; Lindebjerg, J.; Brandslund, I.; Jakobsen, A. Elevated microRNA-126 is associated with high vascular endothelial growth factor receptor 2 expression levels and high microvessel density in colorectal cancer. Oncol. Lett. 2011, 2, 1101–1106. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Suto, T.; Yokobori, T.; Yajima, R.; Morita, H.; Fujii, T.; Yamaguchi, S.; Altan, B.; Tsutsumi, S.; Asao, T.; Kuwano, H. MicroRNA-7 expression in colorectal cancer is associated with poor prognosis and regulates cetuximab sensitivity via EGFR regulation. Carcinogenesis 2015, 36, 338–345. [Google Scholar] [CrossRef] [PubMed]
- Igarashi, H.; Kurihara, H.; Mitsuhashi, K.; Ito, M.; Okuda, H.; Kanno, S.; Naito, T.; Yoshii, S.; Takahashi, H.; Kusumi, T.; et al. Association of microRNA-31–5p with clinical efficacy of anti-EGFR therapy in patients with metastatic colorectal cancer. Ann. Surg. Oncol. 2015, 22, 2640–2648. [Google Scholar] [CrossRef] [PubMed]
- Cappuzzo, F.; Sacconi, A.; Landi, L.; Ludovini, V.; Biagioni, F.; D’Incecco, A.; Capodanno, A.; Salvini, J.; Corgna, E.; Cupini, S.; et al. MicroRNA signature in metastatic colorectal cancer patients treated with anti-EGFR monoclonal antibodies. Clin. Colorectal Cancer 2014, 13, 37–45. [Google Scholar] [CrossRef] [PubMed]
- Fang, L.; Li, H.; Wang, L.; Hu, J.; Jin, T.; Wang, J.; Yang, B.B. MicroRNA-17–5p promotes chemotherapeutic drug resistance and tumour metastasis of colorectal cancer by repressing PTEN expression. Oncotarget 2014, 5, 2974–2987. [Google Scholar] [CrossRef] [PubMed]
- Oue, N.; Anami, K.; Schetter, A.J.; Moehler, M.; Okayama, H.; Khan, M.A.; Bowman, E.D.; Mueller, A.; Schad, A.; Shimomura, M.; et al. High miR-21 expression from FFPE tissues is associated with poor survival and response to adjuvant chemotherapy in colon cancer. Int. J. Cancer 2014, 134, 1926–1934. [Google Scholar] [CrossRef] [PubMed]
- Qian, X.; Yu, J.; Yin, Y.; He, J.; Wang, L.; Li, Q.; Zhang, L.Q.; Li, C.Y.; Shi, Z.M.; Xu, Q.; et al. MicroRNA-143 inhibits tumor growth and angiogenesis and sensitizes chemosensitivity to oxaliplatin in colorectal cancers. Cell. Cycle 2013, 12, 1385–1394. [Google Scholar] [CrossRef] [PubMed]
- Takahashi, M.; Cuatrecasas, M.; Balaguer, F.; Hur, K.; Toiyama, Y.; Castells, A.; Boland, C.R.; Goel, A. The clinical significance of miR-148a as a predictive biomarker in patients with advanced colorectal cancer. PLoS ONE 2012, 7, e46684. [Google Scholar] [CrossRef] [PubMed]
- Song, Y.; Xu, Y.; Wang, Z.; Chen, Y.; Yue, Z.; Gao, P.; Xing, C.; Xu, H. MicroRNA-148b suppresses cell growth by targeting cholecystokinin-2 receptor in colorectal cancer. Int. J. Cancer 2012, 131, 1042–1051. [Google Scholar] [CrossRef] [PubMed]
- Bhangu, A.; Wood, G.; Brown, G.; Darzi, A.; Tekkis, P.; Goldin, R. The role of epithelial mesenchymal transition and resistance to neoadjuvant therapy in locally advanced rectal cancer. Colorectal Dis. 2014, 16, O133–O143. [Google Scholar] [CrossRef] [PubMed]
- Wan, L.Y.; Deng, J.; Xiang, X.J.; Zhang, L.; Yu, F.; Chen, J.; Sun, Z.; Feng, M.; Xiong, J.P. MiR-320 enhances the sensitivity of human colon cancer cells to chemoradiotherapy in vitro by targeting foxm1. Biochem. Biophys. Res. Commun. 2015, 457, 125–132. [Google Scholar] [CrossRef] [PubMed]
- Rasmussen, M.H.; Jensen, N.F.; Tarpgaard, L.S.; Qvortrup, C.; Romer, M.U.; Stenvang, J.; Hansen, T.P.; Christensen, L.L.; Lindebjerg, J.; Hansen, F.; et al. High expression of microRNA-625–3p is associated with poor response to first-line oxaliplatin based treatment of metastatic colorectal cancer. Mol. Oncol. 2013, 7, 637–646. [Google Scholar] [CrossRef] [PubMed]
- Boisen, M.K.; Dehlendorff, C.; Linnemann, D.; Nielsen, B.S.; Larsen, J.S.; Osterlind, K.; Nielsen, S.E.; Tarpgaard, L.S.; Qvortrup, C.; Pfeiffer, P.; et al. Tissue microRNAs as predictors of outcome in patients with metastatic colorectal cancer treated with first line capecitabine and oxaliplatin with or without bevacizumab. PLoS ONE 2014, 9, e109430. [Google Scholar] [CrossRef] [PubMed]
- Hansen, T.F.; Carlsen, A.L.; Heegaard, N.H.; Sorensen, F.B.; Jakobsen, A. Changes in circulating microRNA-126 during treatment with chemotherapy and bevacizumab predicts treatment response in patients with metastatic colorectal cancer. Br. J. Cancer 2015, 112, 624–629. [Google Scholar] [CrossRef] [PubMed]
- Hu, J.; Cai, G.; Xu, Y.; Cai, S. The plasma microRNA miR-1914* and -1915 suppresses chemoresistant in colorectal cancer patients by down-regulating NFIX. Curr. Mol. Med. 2016, 16, 70–82. [Google Scholar] [CrossRef] [PubMed]
- Svoronos, A.A.; Engelman, D.M.; Slack, F.J. OncomiR or tumor suppressor? The duplicity of microRNAs in cancer. Cancer Res. 2016, 76, 3666–3670. [Google Scholar] [CrossRef] [PubMed]
- Bao, Y.; Guo, Y.; Li, Z.; Fang, W.; Yang, Y.; Li, X.; Li, Z.; Xiong, B.; Chen, Z.; Wang, J.; et al. MicroRNA profiling in MUC2 knockout mice of colitis-associated cancer model reveals epigenetic alterations during chronic colitis malignant transformation. PLoS ONE 2014, 9, e99132. [Google Scholar] [CrossRef] [PubMed]
- Zhu, L.; Wang, Z.; Fan, Q.; Wang, R.; Sun, Y. MicroRNA-27a functions as a tumor suppressor in esophageal squamous cell carcinoma by targeting Kras. Oncol. Rep. 2014, 31, 280–286. [Google Scholar] [CrossRef] [PubMed]
- Scheibner, K.A.; Teaboldt, B.; Hauer, M.C.; Chen, X.; Cherukuri, S.; Guo, Y.; Kelley, S.M.; Liu, Z.; Baer, M.R.; Heimfeld, S.; et al. MiR-27a functions as a tumor suppressor in acute leukemia by regulating 14–3-3theta. PLoS ONE 2012, 7, e50895. [Google Scholar] [CrossRef] [PubMed]
- Chintharlapalli, S.; Papineni, S.; Abdelrahim, M.; Abudayyeh, A.; Jutooru, I.; Chadalapaka, G.; Wu, F.; Mertens-Talcott, S.; Vanderlaag, K.; Cho, S.D.; et al. Oncogenic microRNA-27a is a target for anticancer agent methyl 2-cyano-3,11-dioxo-18beta-olean-1,12-dien-30-oate in colon cancer cells. Int. J. Cancer 2009, 125, 1965–1974. [Google Scholar] [CrossRef] [PubMed]
- Xiang, X.; Zhuang, X.; Ju, S.; Zhang, S.; Jiang, H.; Mu, J.; Zhang, L.; Miller, D.; Grizzle, W.; Zhang, H.G. MiR-155 promotes macroscopic tumor formation yet inhibits tumor dissemination from mammary fat pads to the lung by preventing EMT. Oncogene 2011, 30, 3440–3453. [Google Scholar] [CrossRef] [PubMed]
- Shi, J. Considering exosomal miR-21 as a biomarker for cancer. J. Clin. Med. 2016, 5, 42. [Google Scholar] [CrossRef] [PubMed]
- Shen, J.; Liu, Z.; Todd, N.W.; Zhang, H.; Liao, J.; Yu, L.; Guarnera, M.A.; Li, R.; Cai, L.; Zhan, M.; et al. Diagnosis of lung cancer in individuals with solitary pulmonary nodules by plasma microRNA biomarkers. BMC Cancer 2011, 11, 374. [Google Scholar] [CrossRef] [PubMed]
- Liu, J.; Gao, J.; Du, Y.; Li, Z.; Ren, Y.; Gu, J.; Wang, X.; Gong, Y.; Wang, W.; Kong, X. Combination of plasma microRNAs with serum CA19–9 for early detection of pancreatic cancer. Int. J. Cancer 2012, 131, 683–691. [Google Scholar] [CrossRef] [PubMed]
- Zhou, J.; Yu, L.; Gao, X.; Hu, J.; Wang, J.; Dai, Z.; Wang, J.F.; Zhang, Z.; Lu, S.; Huang, X.; et al. Plasma microRNA panel to diagnose hepatitis b virus-related hepatocellular carcinoma. J. Clin. Oncol. 2011, 29, 4781–4788. [Google Scholar] [CrossRef] [PubMed]
- Chen, W.; Cai, F.; Zhang, B.; Barekati, Z.; Zhong, X.Y. The level of circulating miRNA-10b and miRNA-373 in detecting lymph node metastasis of breast cancer: Potential biomarkers. Tumour. Biol. 2013, 34, 455–462. [Google Scholar] [CrossRef] [PubMed]
- Shimomura, A.; Shiino, S.; Kawauchi, J.; Takizawa, S.; Sakamoto, H.; Matsuzaki, J.; Ono, M.; Takeshita, F.; Niida, S.; Shimizu, C.; et al. Novel combination of serum microRNA for detecting breast cancer in the early stage. Cancer. Sci. 2016, 107, 326–334. [Google Scholar] [CrossRef] [PubMed]
- Ogata-Kawata, H.; Izumiya, M.; Kurioka, D.; Honma, Y.; Yamada, Y.; Furuta, K.; Gunji, T.; Ohta, H.; Okamoto, H.; Sonoda, H.; et al. Circulating exosomal microRNAs as biomarkers of colon cancer. PLoS ONE 2014, 9, e92921. [Google Scholar] [CrossRef] [PubMed]
- Xiang, M.; Zeng, Y.; Yang, R.; Xu, H.; Chen, Z.; Zhong, J.; Xie, H.; Xu, Y.; Zeng, X. U6 is not a suitable endogenous control for the quantification of circulating microRNAs. Biochem. Biophys. Res. Commun. 2014, 454, 210–214. [Google Scholar] [CrossRef] [PubMed]
- Yu, H.W.; Sze, D.M.; Cho, W.C. MicroRNAs involved in anti-tumour immunity. Int. J. Mol. Sci. 2013, 14, 5587–5607. [Google Scholar] [CrossRef] [PubMed]
- Lodish, H.F.; Zhou, B.; Liu, G.; Chen, C.Z. Micromanagement of the immune system by microRNAs. Nat. Rev. Immunol. 2008, 8, 120–130. [Google Scholar] [CrossRef] [PubMed]
- Xiao, C.; Rajewsky, K. MicroRNA control in the immune system: Basic principles. Cell 2009, 136, 26–36. [Google Scholar] [CrossRef] [PubMed]
- Li, X.; Nie, J.; Mei, Q.; Han, W.D. MicroRNAs: Novel immunotherapeutic targets in colorectal carcinoma. World J. Gastroenterol. 2016, 22, 5317–5331. [Google Scholar] [CrossRef] [PubMed]
Tissues | ||
microRNA | Population with Poor Prognosis * | References |
miR-7 | up | [19] |
miR-20a | up | [20,21] |
- | [22] | |
miR-21 | up | [23], Meta-analysis: [24,25] |
miR-22 | down | [26] |
miR-31 | - | [15] |
miR-92a | up | [27] |
- | [15] | |
miR-93 | down | [19] |
miR-101 | - | [15] |
miR-155 | up | [28] |
let-7c | down | [29] |
miR-126 | down | [30] |
miR-130b | up | [31] |
miR-132 | down | [32] |
miR-139-3p | down | [33] |
miR-15 | down | [34] |
miR-16 | down | [34] |
miR-181b | up | [20] |
- | [22] | |
miR-183 | up | [35] |
miR-195 | down | [19,36] |
miR-196a | up | [37] |
miR-196b | up | [37] |
miR-203 | up | [20] |
- | [22,38] | |
miR-215 | up | [39] |
miR-224 | up | [40] |
miR-340 | down | [41] |
miR-34-5p | down | [42] |
miR-320e | up | [43] |
miR-17-5p | up | [44] |
miR-106a | down | [44] |
up | [20] | |
- | [15] | |
miR-150 | down | [45] |
miR-29a | up | [46] |
miR-372 | up | [47] |
miR-141 | up | [19] |
miR-144 | down | [48] |
miR-145 | - | [15] |
miR-181a | up | [49] |
miR-494 | up | [19] |
Blood/Serum/Plasma | ||
microRNA | Population with Poor Prognosis * | References |
miR-21 | up | [50] |
miR-96 | up | [51] |
miR-124-5p | down | [52] |
miR-141 | up | [53] |
miR-155 | up | [54] |
miR-200b | up | [51] |
miR-200c | up | [55] |
miR-218 | down | [56] |
miR-221 | up | [57] |
miR-29a | up | [46] |
miR-148a | down | [58] |
miR-183 | up | [59] |
miR-345 | up | [60] |
miR-19a | up | [61] |
miR-203 | up | [62,63] |
Blood/Serum/Plasma | ||
microRNA | Population with CRC * | References |
miR-18a | up | [74,75] |
miR-19b | up | [74] |
miR-15a | up | [74] |
miR-21 | up | Meta-analysis: [24,76,77,78] |
miR-24 | down | [79] |
miR-29a | up | [74,75,80] |
miR-34a | down | [81] |
miR-375 | down | [82] |
miR-409-3p | up | [83] |
miR-7 | down | [83] |
miR-93 | down | [83] |
miR-17-3p | up | [84] |
let-7g | up | [85] |
miR-31 | down | [85] |
miR-181b | down | [85] |
miR-203 | down | [85] |
miR-378 | up | [86] |
miR-20a | up | [75] |
miR-143 | up | [75] |
miR-145 | up | [75] |
miR-133a | up | [75] |
miR-106b | up | [75] |
miR-335 | up | [74] |
miR-601 | down | [87] |
miR-223 | up | [88,89] |
miR-92 | up | [75,80,84,88,89] |
down | [85] | |
miR-760 | down | [87] |
miR-423-5p | down | [79] |
miR-320a | down | [79] |
miR-19a | up | [74,78,88] |
miR-425-5p | up | [78] |
miR-422a | down | [88] |
Stool | ||
microRNA | Population with CRC * | References |
miR-17-92 cluster | up | [72] |
miR-20a | up | [90] |
miR-21 | up | Meta-analysis: [76] |
miR-135 | up | [70,72] |
miR-144 * | up | [91] |
miR-29a | down | [71] |
miR-223 | up | [89] |
miR-221 | up | [73] |
miR-92a | up | [69,89] |
miR-224 | down | [71] |
Tissues | |||
Therapy | microRNA | Non-responders Pre-therapy * | References |
Anti-angiogenetic therapy | miR-126 | up | [101] |
Anti-EGFR therapy | miR-7 | down | [102] |
Chemotherapy | miR-31-5p | up | [103] |
Let-7c | down | [104] | |
miR-99a | down | [104] | |
miR-125b | down | [104] | |
miR-17-5p | up | [105] | |
miR-21 | up | [106] | |
miR-143 | down | [107] | |
miR-148a | down | [108] | |
miR-148b | down | [109] | |
miR-150 | down | [45] | |
miR-200c | down | [110] | |
miR-320 | down | [111] | |
miR-625-3p | up | [112] | |
miR-181b | up | [112] | |
miR-27b | up | [112] | |
miR-664-3p | down | [113] | |
miR-455-5p | up | [113] | |
miR-196b-5p | down | [113] | |
miR-592 | down | [113] | |
Blood/Serum/Plasma | |||
Therapy | microRNA | Non-responders Pre-therapy * | References |
Anti-angiogenetic therapy | miR-126 | up | [114] |
Anti-EGFR therapy | miR-345 | up | [60] |
Chemotherapy | miR-126 | up | [114] |
miR-143 | down | [107] | |
miR-345 | up | [60] | |
miR-1914 * | down | [115] | |
miR-1915 | down | [115] |
© 2017 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Masuda, T.; Hayashi, N.; Kuroda, Y.; Ito, S.; Eguchi, H.; Mimori, K. MicroRNAs as Biomarkers in Colorectal Cancer. Cancers 2017, 9, 124. https://doi.org/10.3390/cancers9090124
Masuda T, Hayashi N, Kuroda Y, Ito S, Eguchi H, Mimori K. MicroRNAs as Biomarkers in Colorectal Cancer. Cancers. 2017; 9(9):124. https://doi.org/10.3390/cancers9090124
Chicago/Turabian StyleMasuda, Takaaki, Naoki Hayashi, Yosuke Kuroda, Shuhei Ito, Hidetoshi Eguchi, and Koshi Mimori. 2017. "MicroRNAs as Biomarkers in Colorectal Cancer" Cancers 9, no. 9: 124. https://doi.org/10.3390/cancers9090124