Circulating Exosomal microRNAs as Biomarkers of Colon Cancer
Open accessAbstract
PURPOSE: Exosomal microRNAs (miRNAs) have been attracting major interest as potential diagnostic biomarkers of cancer. The aim of this study was to characterize the miRNA profiles of serum exosomes and to identify those that are altered in colorectal cancer (CRC). To evaluate their use as diagnostic biomarkers, the relationship between specific exosomal miRNA levels and pathological changes of patients, including disease stage and tumor resection, was examined. EXPERIMENTAL DESIGN: Microarray analyses of miRNAs in exosome-enriched fractions of serum samples from 88 primary CRC patients and 11 healthy controls were performed. The expression levels of miRNAs in the culture medium of five colon cancer cell lines were also compared with those in the culture medium of a normal colon-derived cell line. The expression profiles of miRNAs that were differentially expressed between CRC and control sample sets were verified using 29 paired samples from post-tumor resection patients. The sensitivities of selected miRNAs as biomarkers of CRC were evaluated and compared with those of known tumor markers (CA19-9 and CEA) using a receiver operating characteristic analysis. The expression levels of selected miRNAs were also validated by quantitative real-time RT-PCR analyses of an independent set of 13 CRC patients. RESULTS: The serum exosomal levels of seven miRNAs (let-7a, miR-1229, miR-1246, miR-150, miR-21, miR-223, and miR-23a) were significantly higher in primary CRC patients, even those with early stage disease, than in healthy controls, and were significantly down-regulated after surgical resection of tumors. These miRNAs were also secreted at significantly higher levels by colon cancer cell lines than by a normal colon-derived cell line. The high sensitivities of the seven selected exosomal miRNAs were confirmed by a receiver operating characteristic analysis. CONCLUSION: Exosomal miRNA signatures appear to mirror pathological changes of CRC patients and several miRNAs are promising biomarkers for non-invasive diagnosis of the disease.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
microRNA's presence in exosomes has been reported in different cells and cancer types.
“microRNA's presence in exosomes have been already reported in different cells and cancer types (44–50).”
From Potential Therapeutic Effects of Exosomes Packed With a miR-21-Sponge Construct in a Rat Model of Glioblastoma (2019) · cites this paper as [48]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
1 retracted
RETRACTED: MicroRNA signatures of tumor-derived exosomes as diagnostic biomarkers of ovarian cancer
Taylor, D. D., & Gerçel-Taylor, Ç. (2008) · Gynecologic Oncology · doi:10.1016/j.ygyno.2008.04.033 · Cited by 2,289 · see citing works
RetractedAnalysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2−ΔΔCT Method
Livak, K. J., & Schmittgen, T. D. (2001) · Methods · doi:10.1006/meth.2001.1262 · Cited by 180,860 · see citing works
Jemal, A., Bray, F., Ferlay, J., Ward, E., & Forman, D. (2011) · CA A Cancer Journal for Clinicians · doi:10.3322/caac.20107 · Cited by 54,708 · see citing works
Valadi, H., Ekström, K., Bossios, A., Sjöstrand, M., Lee, J. J., & Lötvall, J. O. (2007) · Nature Cell Biology · doi:10.1038/ncb1596 · Cited by 12,834 · see citing works
MicroRNA expression profiles classify human cancers
Lü, J., Getz, G. A., Miska, E. A., Alvarez-Saavedra, E., Lamb, J., Peck, D., Sweet-Cordero, A., Ebert, B. L., Mak, R. H., Ferrando, A. A., et al. (2005) · Nature · doi:10.1038/nature03702 · Cited by 9,497 · see citing works
Oncomirs — microRNAs with a role in cancer
Esquela‐Kerscher, A., & Slack, F. J. (2006) · Nature reviews. Cancer · doi:10.1038/nrc1840 · Cited by 7,038 · see citing works
Skog, J., Würdinger, T., van Rijn, S., Meijer, D. H., Gainche, L., Curry, W. T., Carter, B. S., Krichevsky, A. M., & Breakefield, X. O. (2008) · Nature Cell Biology · doi:10.1038/ncb1800 · Cited by 5,001 · see citing works
Causes and consequences of microRNA dysregulation in cancer
Croce, C. M. (2009) · Nature Reviews Genetics · doi:10.1038/nrg2634 · Cited by 3,003 · see citing works
MicroRNA dysregulation in cancer: diagnostics, monitoring and therapeutics. A comprehensive review
Iorio, M. V., & Croce, C. M. (2012) · EMBO Molecular Medicine · doi:10.1002/emmm.201100209 · Cited by 1,738 · see citing works
Atkin, W. S., Edwards, R., Kralj‐Hans, I., Wooldrage, K., Hart, A. R., Northover, J. M. A., Parkin, D. M., Wardle, J., Duffy, S. W., & Cuzick, J. M. (2010) · The Lancet · doi:10.1016/s0140-6736(10)60551-x · Cited by 1,618 · see citing works
ASCO 2006 Update of Recommendations for the Use of Tumor Markers in Gastrointestinal Cancer
Locker, G. Y., Hamilton, S. R., Harris, J. E., Jessup, J. M., Kemeny, N. E., Macdonald, J. S., Somerfield, M. R., Hayes, D. F., & Bast, R. C. (2006) · Journal of Clinical Oncology · doi:10.1200/jco.2006.08.2644 · Cited by 1,592 · see citing works
Exosomes: proteomic insights and diagnostic potential
Simpson, R. J., Lim, J. W., Moritz, R. L., & Mathivanan, S. (2009) · Expert Review of Proteomics · doi:10.1586/epr.09.17 · Cited by 1,113 · see citing works
MicroRNAs accurately identify cancer tissue origin
Rosenfeld, N., Aharonov, R., Meiri, E., Rosenwald, S., Spector, Y., Zepeniuk, M., Benjamin, H., Shabes, N., Tabak, S., Levy, A., et al. (2008) · Nature Biotechnology · doi:10.1038/nbt1392 · Cited by 971 · see citing works
Plasma microRNAs are promising novel biomarkers for early detection of colorectal cancer
Huang, Z., Huang, D., Ni, S., Peng, Z., Sheng, W., & Du, X. (2009) · International Journal of Cancer · doi:10.1002/ijc.25007 · Cited by 957 · see citing works
Classification of human colorectal adenocarcinoma cell lines.
Leibovitz, A., Stinson, J. C., McCombs, W. B., McCoy, C. E., Mazur, K. C., & Mabry, N. D. (1976) · PubMed · Cited by 949 · see citing works
Ng, E. K. O., Chong, W. W. S., Jin, H., Lam, E. K. Y., Shin, V. Y., Yu, J., Poon, T. C. W., Ng, S. S. M., & Sung, J. J. Y. (2009) · Gut · doi:10.1136/gut.2008.167817 · Cited by 936 · see citing works
Serum miR-21 as a Diagnostic and Prognostic Biomarker in Colorectal Cancer
Toiyama, Y., Takahashi, M., Hur, K., Nagasaka, T., Tanaka, K., Inoue, Y., Kusunoki, M., Boland, C. R., & Goel, A. (2013) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/djt101 · Cited by 500 · see citing works
Cheng, H., Zhang, L., Cogdell, D. E., Zheng, H., Schetter, A. J., Nykter, M., Harris, C. C., Chen, K., Hamilton, S. R., & Zhang, W. (2011) · PLoS ONE · doi:10.1371/journal.pone.0017745 · Cited by 431 · see citing works
Exosomal miRNAs: Biological Properties and Therapeutic Potential
Hu, G., Drescher, K. M., & Chen, X. (2012) · Frontiers in Genetics · doi:10.3389/fgene.2012.00056 · Cited by 389 · see citing works
Swarup, V., & Rajeswari, M. R. (2007) · FEBS Letters · doi:10.1016/j.febslet.2007.01.051 · Cited by 379 · see citing works
Pu, X., Huang, G., Guo, H., Guo, C., Li, H., Shen, Y., Ling, S., Jiang, L., Tian, Y., & Lin, T. (2010) · Journal of Gastroenterology and Hepatology · doi:10.1111/j.1440-1746.2010.06417.x · Cited by 289 · see citing works
Takeshita, N., Hoshino, I., Mori, M., Akutsu, Y., Hanari, N., Yoneyama, Y., Ikeda, N., Isozaki, Y., Maruyama, T., Akanuma, N., et al. (2013) · British Journal of Cancer · doi:10.1038/bjc.2013.8 · Cited by 263 · see citing works
Exosome-Like Vesicles with Dipeptidyl Peptidase IV in Human Saliva
Ogawa, Y., Kanai‐Azuma, M., Akimoto, Y., Kawakami, H., & Yanoshita, R. (2008) · Biological and Pharmaceutical Bulletin · doi:10.1248/bpb.31.1059 · Cited by 259 · see citing works
Madhavan, D., Zucknick, M., Wallwiener, M., Ćuk, K., Modugno, C., Scharpff, M., Schott, S., Heil, J., Turchinovich, A. A., Yang, R., et al. (2012) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-12-1407 · Cited by 248 · see citing works
MicroRNA Signatures: Novel Biomarker for Colorectal Cancer?
Luo, X., Burwinkel, B., Tao, S., & Brenner, H. (2011) · Cancer Epidemiology Biomarkers & Prevention · doi:10.1158/1055-9965.epi-11-0035 · Cited by 242 · see citing works
Si, H., Sun, X., Chen, Y., Cao, Y., Chen, S., Wang, H., & Hu, C. (2012) · Journal of Cancer Research and Clinical Oncology · doi:10.1007/s00432-012-1315-y · Cited by 236 · see citing works
Clinical impact of circulating miR-221 in plasma of patients with pancreatic cancer
Kawaguchi, T., Komatsu, S., Ichikawa, D., Morimura, R., Tsujiura, M., Konishi, H., Takeshita, H., Nagata, H., Arita, T., Hirajima, S., et al. (2013) · British Journal of Cancer · doi:10.1038/bjc.2012.546 · Cited by 212 · see citing works
Köberle, V., Pleli, T., Schmithals, C., Alonso, E. A., Haupenthal, J., Bonig, H. B., Peveling‐Oberhag, J., Biondi, R. M., Zeuzem, S., Kronenberger, B., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0075184 · Cited by 194 · see citing works
MiR-181d acts as a tumor suppressor in glioma by targeting K-ras and Bcl-2
Wang, X., Shi, Z., Wang, X.-R., Cao, L., Wang, Y., Zhang, J., Yin, Y., Luo, H., Kang, C., Liu, N., et al. (2011) · Journal of Cancer Research and Clinical Oncology · doi:10.1007/s00432-011-1114-x · Cited by 132 · see citing works
Determination of the levels of urokinase and its receptor in human colon carcinoma cell lines.
Boyd, D. D., Florent, G., Kim, P., & Brattain, M. G. (1988) · PubMed · Cited by 128 · see citing works
WiDr is a derivative of another colon adenocarcinoma cell line, HT-29
Chen, T. R., Drabkowski, D., Hay, R. J., Macy, M. L., & Peterson, W. (1987) · Cancer Genetics and Cytogenetics · doi:10.1016/0165-4608(87)90267-6 · Cited by 115 · see citing works
Tsuchiya, N., Izumiya, M., Ogata‐Kawata, H., Okamoto, K., Fujiwara, Y., Nakai, M., Okabe, A., Schetter, A. J., Bowman, E. D., Midorikawa, Y., et al. (2011) · Cancer Research · doi:10.1158/0008-5472.can-10-2475 · Cited by 113 · see citing works
Self-citationCirculating microRNAs in serum: novel biomarkers for patients with bladder cancer?
Scheffer, A.-R., Holdenrieder, S., Kristiansen, G., von Ruecker, A., Müller, S. C., & Ellinger, J. (2012) · World Journal of Urology · doi:10.1007/s00345-012-1010-2 · Cited by 111 · see citing works
Evidence for colorectal cancer screening
Bretthauer, M. (2010) · Best Practice & Research Clinical Gastroenterology · doi:10.1016/j.bpg.2010.06.005 · Cited by 69 · see citing works
Primary and long term epithelial cell cultures from human fetal normal colonic mucosa
Siddiqui, K. M., & Chopra, D. P. (1984) · In Vitro · doi:10.1007/bf02619632 · Cited by 65 · see citing works
An, J., Pan, Y., Yan, Z. P., Li, W., Cui, J., Yuan, J., Tian, L., Xing, R., & Lu, Y. (2013) · Journal of Cellular Biochemistry · doi:10.1002/jcb.24565 · Cited by 51 · see citing works
Izumiya, M., Okamoto, K., Tsuchiya, N., & Nakagama, H. (2010) · Carcinogenesis · doi:10.1093/carcin/bgq112 · Cited by 30 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Exosome and Exosomal MicroRNA: Trafficking, Sorting, and Function
Zhang, J., Li, S., Li, L., Li, M., Guo, C., Yao, J., & Mi, S. (2015) · Genomics Proteomics & Bioinformatics · doi:10.1016/j.gpb.2015.02.001 · Cited by 2,189 · see citing works
Extracellular Vesicles in Cancer: Cell-to-Cell Mediators of Metastasis
Becker, A., Thakur, B. K., Weiss, J. M., Kim, H. S., Peinado, H., & Lyden, D. (2016) · Cancer Cell · doi:10.1016/j.ccell.2016.10.009 · Cited by 2,003 · see citing works
Extracellular vesicles in cancer — implications for future improvements in cancer care
Xu, R., Rai, A., Chen, M., Suwakulsiri, W., Greening, D. W., & Simpson, R. J. (2018) · Nature Reviews Clinical Oncology · doi:10.1038/s41571-018-0036-9 · Cited by 1,435 · see citing works
Quantitative and stoichiometric analysis of the microRNA content of exosomes
Chevillet, J. R., Kang, Q., Ruf, I. K., Briggs, H., Vojtech, L. N., Hughes, S. M., Cheng, H. H., Arroyo, J. D., Meredith, E. K., Gallichotte, E. N., et al. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1408301111 · Cited by 1,105 · see citing works
Epigenetics of colorectal cancer: biomarker and therapeutic potential
Jung, G., Hernández-Illán, E., Moreira, L., Balaguer, F., & Goel, A. (2020) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/s41575-019-0230-y · Cited by 813 · see citing works
Epigenetic Alterations in Colorectal Cancer: Emerging Biomarkers
Okugawa, Y., Grady, W. M., & Goel, A. (2015) · Gastroenterology · doi:10.1053/j.gastro.2015.07.011 · Cited by 782 · see citing works
Exosomes in cancer: small particle, big player
Zhang, X., Yuan, X., Shi, H., Wu, L., Qian, H., & Xu, W. (2015) · Journal of Hematology & Oncology · doi:10.1186/s13045-015-0181-x · Cited by 783 · see citing works
Tumor-Derived Exosomes and Their Role in Cancer Progression
Whiteside, T. L. (2016) · Advances in clinical chemistry · doi:10.1016/bs.acc.2015.12.005 · Cited by 762 · see citing works
A microfluidics-based in vitro model of the gastrointestinal human–microbe interface
Shah, P., Fritz, J. V., Glaab, E., Desai, M. S., Greenhalgh, K., Frachet, A., Niegowska, M., Estes, M., Jäger, C., Seguin-Devaux, C., et al. (2016) · Nature Communications · doi:10.1038/ncomms11535 · Cited by 660 · see citing works
Plasma exosome microRNAs are indicative of breast cancer
Hannafon, B. N., Trigoso, Y. D., Calloway, C. L., Zhao, Y. D., Lum, D. H., Welm, A. L., Zhao, Z. J., Blick, K. E., Dooley, W. C., & Ding, W. (2016) · Breast Cancer Research · doi:10.1186/s13058-016-0753-x · Cited by 603 · see citing works
The importance of exosomal PDL1 in tumour immune evasion
Daassi, D., Mahoney, K. M., & Freeman, G. J. (2020) · Nature Reviews Immunology · doi:10.1038/s41577-019-0264-y · Cited by 598 · see citing works
Jin, X., Chen, Y., Chen, H., Fei, S., Chen, D., Cai, X., Liu, L., Lin, B., Su, H., Zhao, L., et al. (2017) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-17-0577 · Cited by 560 · see citing works
MicroRNAome genome: A treasure for cancer diagnosis and therapy
Berindan‐Neagoe, I., Monroig-Bosque, P. D. C., Pasculli, B., & Călin, G. A. (2014) · CA A Cancer Journal for Clinicians · doi:10.3322/caac.21244 · Cited by 521 · see citing works
Boriachek, K., Islam, M. N., Möller, A., Salomón, C., Nguyen, N., Hossain, M. S. A., Yamauchi, Y., & Shiddiky, M. J. A. (2017) · Small · doi:10.1002/smll.201702153 · Cited by 499 · see citing works
Exosomal microRNA in serum is a novel biomarker of recurrence in human colorectal cancer
Matsumura, T., Sugimachi, K., Iinuma, H., Takahashi, Y., Kurashige, J., Sawada, G., Ueda, M., Uchi, R., Ueo, H., Takano, Y., et al. (2015) · British Journal of Cancer · doi:10.1038/bjc.2015.201 · Cited by 491 · see citing works
Mutant p53 cancers reprogram macrophages to tumor supporting macrophages via exosomal miR-1246
Cooks, T., Pateras, I. S., Jenkins, L. M. M., Patel, K., Robles, A. I., Morris, J., Forshew, T., Appella, E., Gorgoulis, V. G., & Harris, C. C. (2018) · Nature Communications · doi:10.1038/s41467-018-03224-w · Cited by 483 · see citing works
Evidence-Based Clinical Use of Nanoscale Extracellular Vesicles in Nanomedicine
Fais, S., O’Driscoll, L., Borras, F. E., Buzas, E., Camussi, G., Cappello, F., Carvalho, J., Cordeiro da Silva, A., Del Portillo, H., El Andaloussi, S., et al. (2016) · ACS Nano · doi:10.1021/acsnano.5b08015 · Cited by 481 · see citing works
Predicting miRNA–disease association based on inductive matrix completion
Chen, X., Wang, L., Qu, J., Guan, N., & Li, J. (2018) · Bioinformatics · doi:10.1093/bioinformatics/bty503 · Cited by 468 · see citing works
Exosomes as miRNA Carriers: Formation–Function–Future
Yu, X., Odenthal, M., & Fries, J. W. U. (2016) · International Journal of Molecular Sciences · doi:10.3390/ijms17122028 · Cited by 434 · see citing works
Circulating MicroRNAs in Cancer: Potential and Challenge
Cui, M., Wang, H., Yao, X., Zhang, D., Xie, Y., Cui, R., & Zhang, X. (2019) · Frontiers in Genetics · doi:10.3389/fgene.2019.00626 · Cited by 424 · see citing works
Roles and mechanisms of exosomal non-coding RNAs in human health and diseases
Li, C., Ni, Y., Xu, H., Xiang, Q., Zhao, Y. Q., Zhan, J., He, J., Li, S., & Liu, Y. (2021) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-021-00779-x · Cited by 407 · see citing works
Brief update on endocytosis of nanomedicines
Patel, S., Kim, J., Herrera‐Barrera, M., Mukherjee, A., Kabanov, A. V., & Sahay, G. (2019) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2019.08.004 · Cited by 402 · see citing works
Effects of exosomes on pre-metastatic niche formation in tumors
Guo, Y., Ji, X., Liu, J., Fan, D., Zhou, Q., Chen, C., Wang, W., Wang, G., Wang, H., Yuan, W., et al. (2019) · Molecular Cancer · doi:10.1186/s12943-019-0995-1 · Cited by 402 · see citing works
Extracellular vesicles as biomarkers and therapeutic targets for cancer
Urabe, F., Kosaka, N., Ito, K., Kimura, T., Egawa, S., & Ochiya, T. (2019) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00280.2019 · Cited by 400 · see citing works
WBSMDA: Within and Between Score for MiRNA-Disease Association prediction
Chen, X., Yan, C. C., Zhang, X., You, Z., Deng, L., Liu, Y., Zhang, Y., & Dai, Q. (2016) · Scientific Reports · doi:10.1038/srep21106 · Cited by 376 · see citing works
Exosomes in Cancer Diagnostics
Soung, Y. H., Ford, S. K., Zhang, V., & Chung, J. (2017) · Cancers · doi:10.3390/cancers9010008 · Cited by 365 · see citing works
Versatile roles of extracellular vesicles in cancer
Kosaka, N., Yoshioka, Y., Fujita, Y., & Ochiya, T. (2016) · Journal of Clinical Investigation · doi:10.1172/jci81130 · Cited by 347 · see citing works
Circulating miRNAs: Roles in cancer diagnosis, prognosis and therapy
Cheng, G. (2014) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2014.09.001 · Cited by 335 · see citing works
Nakase, I., & Futaki, S. (2015) · Scientific Reports · doi:10.1038/srep10112 · Cited by 297 · see citing works
An, T.-X., Qin, S., Xu, Y., Tang, Y., Huang, Y., Situ, B., Inal, J., & Zheng, L. (2015) · Journal of Extracellular Vesicles · doi:10.3402/jev.v4.27522 · Cited by 262 · see citing works
EGBMMDA: Extreme Gradient Boosting Machine for MiRNA-Disease Association prediction
Chen, X., Li, H., Xie, D., & Zhao, Q. (2018) · Cell Death and Disease · doi:10.1038/s41419-017-0003-x · Cited by 276 · see citing works
Circulating biomarkers for early detection and clinical management of colorectal cancer
Marcuello, M., Vymetalkova, V. P., Neves, R. P., Durán-Sanchón, S., Vedeld, H. M., Tham, E., van Dalum, G., Flügen, G., García‐Barberán, V., Fijneman, R. J. A., et al. (2019) · Molecular Aspects of Medicine · doi:10.1016/j.mam.2019.06.002 · Cited by 279 · see citing works
Colorectal Cancer Liver Metastasis: Evolving Paradigms and Future Directions
Zarour, L. R., Anand, S., Billingsley, K. G., Bisson, W. H., Cercek, A., Clarke, M. F., Coussens, L. M., Gast, C. E., Geltzeiler, C. B., Hansen, L., et al. (2017) · Cellular and Molecular Gastroenterology and Hepatology · doi:10.1016/j.jcmgh.2017.01.006 · Cited by 273 · see citing works
Nakase, I., Kobayashi, N. B., Takatani‐Nakase, T., & Yoshida, T. (2015) · Scientific Reports · doi:10.1038/srep10300 · Cited by 271 · see citing works
The Origin and Functions of Exosomes in Cancer
Rajagopal, C., & Harikumar, K. (2018) · Frontiers in Oncology · doi:10.3389/fonc.2018.00066 · Cited by 252 · see citing works
Xu, R., Greening, D. W., Rai, A., Ji, H. L., & Simpson, R. J. (2015) · Methods · doi:10.1016/j.ymeth.2015.04.008 · Cited by 267 · see citing works
miRNAs: Potential as Biomarkers and Therapeutic Targets for Cancer
Chakrabortty, A., Patton, D. J., Smith, B. F., & Agarwal, P. (2023) · Genes · doi:10.3390/genes14071375 · Cited by 258 · see citing works
Let ‐ 7 as biomarker, prognostic indicator, and therapy for precision medicine in cancer
Chirshev, E., Oberg, K. C., Ioffe, Y., & Unternaehrer, J. (2019) · Clinical and Translational Medicine · doi:10.1186/s40169-019-0240-y · Cited by 252 · see citing works
Exosomal miRNAs as novel cancer biomarkers: Challenges and opportunities
Salehi, M., & Sharifi, M. (2018) · Journal of Cellular Physiology · doi:10.1002/jcp.26481 · Cited by 252 · see citing works
Sato-Kuwabara, Y., Melo, S. A., Soares, F. A., & Călin, G. A. (2014) · International Journal of Oncology · doi:10.3892/ijo.2014.2712 · Cited by 244 · see citing works
New Concepts in Cancer Biomarkers: Circulating miRNAs in Liquid Biopsies
Larrea, E., Solé, C., Manterola, L., Goicoechea, I., Armesto, M., Arestin, M., Caffarel, M. M., Araujo, A. M., Araiz, M., Fernández‐Mercado, M., et al. (2016) · International Journal of Molecular Sciences · doi:10.3390/ijms17050627 · Cited by 239 · see citing works
HGIMDA: Heterogeneous graph inference for miRNA-disease association prediction
Chen, X., Yan, C. C., Zhang, X., You, Z., Huang, Y., & Yan, G. (2016) · Oncotarget · doi:10.18632/oncotarget.11251 · Cited by 232 · see citing works
LRSSLMDA: Laplacian Regularized Sparse Subspace Learning for MiRNA-Disease Association prediction
Chen, X., & Li, H. (2017) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1005912 · Cited by 228 · see citing works
Guo, S., Chen, J., Chen, F., Zeng, Q., Liu, W., & Zhang, G. (2020) · Gut · doi:10.1136/gutjnl-2020-321187 · Cited by 227 · see citing works
Exosomal microRNAs (exomiRs): Small molecules with a big role in cancer
Bhome, R., Vecchio, F. D., Lee, G.-H., Bullock, M. D., Primrose, J. M., Sayan, E., & Mirnezami, A. H. (2018) · Cancer Letters · doi:10.1016/j.canlet.2018.02.002 · Cited by 224 · see citing works
Kanlikilicer, P., Bayraktar, R., Denizli, M., Rashed, M. H., Ivan, C., Aslan, B., Mitra, R., Karagoz, K., Bayraktar, E., Zhang, X., et al. (2018) · EBioMedicine · doi:10.1016/j.ebiom.2018.11.004 · Cited by 222 · see citing works
MicroRNAs as Peripheral Biomarkers in Aging and Age-Related Diseases
Kumar, S., Vijayan, M., Bhatti, J. S., & Reddy, P. H. (2017) · Progress in molecular biology and translational science · doi:10.1016/bs.pmbts.2016.12.013 · Cited by 216 · see citing works
Extracellular vesicle transfer of cancer pathogenic components
Fujita, Y., Yoshioka, Y., & Ochiya, T. (2016) · Cancer Science · doi:10.1111/cas.12896 · Cited by 212 · see citing works
Circulating exosomes and exosomal microRNAs as biomarkers in gastrointestinal cancer
Nedaeinia, R., Manian, M., Jazayeri, M. H., Ranjbar, M., Salehi, R., Sharifi, M., Mohaghegh, F., Goli, M., Jahednia, S. H., Avan, A., et al. (2016) · Cancer Gene Therapy · doi:10.1038/cgt.2016.77 · Cited by 211 · see citing works
Non-Exosomal and Exosomal Circulatory MicroRNAs: Which Are More Valid as Biomarkers?
Kamal, N. N. S. B. N. M., & Shahidan, W. N. S. (2020) · Frontiers in Pharmacology · doi:10.3389/fphar.2019.01500 · Cited by 210 · see citing works
Tumor-derived extracellular vesicles: reliable tools for Cancer diagnosis and clinical applications
Rahbarghazi, R., Jabbari, N., Sani, N. A., Asghari, R., Salimi, L., Kalashani, S. A., Feghhi, M., Etemadi, T., Akbariazar, E., Mahmoudi, M., et al. (2019) · Cell Communication and Signaling · doi:10.1186/s12964-019-0390-y · Cited by 207 · see citing works
MicroRNAs: Potential candidates for diagnosis and treatment of colorectal cancer
Moridikia, A., Mirzaei, H., Sahebkar, A., & Salimian, J. (2017) · Journal of Cellular Physiology · doi:10.1002/jcp.25801 · Cited by 203 · see citing works
Signature of Circulating microRNAs in Patients with Acute Heart Failure
Ovchinnikova, E. S., Schmitter, D., Vegter, E. L., ter Maaten, J. M., Valente, M. A. E., Liu, L. C. Y., van der Harst, P., Pinto, Y. M., de Boer, R. A., Meyer, S., et al. (2015) · European Journal of Heart Failure · doi:10.1002/ejhf.332 · Cited by 199 · see citing works
MicroRNAs in the prognosis and therapy of colorectal cancer: From bench to bedside
To, K. K. W., Tong, C. W. S., Wu, M., & Cho, W. C. S. (2018) · World Journal of Gastroenterology · doi:10.3748/wjg.v24.i27.2949 · Cited by 195 · see citing works
Circulating exosomal miR-125a-3p as a novel biomarker for early-stage colon cancer
Wang, J., Yan, F., Zhao, Q., Zhan, F., Wang, R., Wang, L., Zhang, Y., & Huang, X. (2017) · Scientific Reports · doi:10.1038/s41598-017-04386-1 · Cited by 196 · see citing works
Exosomal microRNA-141 is upregulated in the serum of prostate cancer patients
Hao, X., Li, Z., Ma, Y., Wang, J., Zeng, X., Li, R., & Kang, W. (2015) · OncoTargets and Therapy · doi:10.2147/ott.s95565 · Cited by 192 · see citing works
Cavallari, I., Ciccarese, F., Sharova, E., Urso, L., Raimondi, V., Silic‐Benussi, M., D’Agostino, D. M., & Ciminale, V. (2021) · Cancers · doi:10.3390/cancers13235874 · Cited by 190 · see citing works
Octamer 4/microRNA‐1246 signaling axis drives Wnt/β‐catenin activation in liver cancer stem cells
Chai, S., Ng, K. Y., Tong, M., Lau, E. Y.-T., Lee, T. K., Chan, K. W., Yuan, Y., Cheung, T. T., Cheung, S., Wang, X., et al. (2016) · Hepatology · doi:10.1002/hep.28821 · Cited by 188 · see citing works
Exosomes as potential sources of biomarkers in colorectal cancer
Xiao, Y., Zhong, J., Zhong, B., Huang, J., Jiang, L., Jiang, Y., Yuan, J., Sun, J. G., Dai, L., Yang, C., et al. (2020) · Cancer Letters · doi:10.1016/j.canlet.2020.01.033 · Cited by 185 · see citing works
Exosomal microRNA miR-92a concentration in serum reflects human brown fat activity
Chen, Y., Buyel, J. J., Hanssen, M. J. W., Siegel, F., Pan, R., Naumann, J., Schell, M. J., van der Lans, A. A. J. J., Schlein, C., Fröhlich, H., et al. (2016) · Nature Communications · doi:10.1038/ncomms11420 · Cited by 181 · see citing works
Shinohara, H., Kuranaga, Y., Kumazaki, M., Sugito, N., Yoshikawa, Y., Takai, T., Taniguchi, K., Ito, Y., & Akao, Y. (2017) · The Journal of Immunology · doi:10.4049/jimmunol.1700167 · Cited by 177 · see citing works
Jia, S., Zhang, R., Li, Z., & Li, J. (2017) · Oncotarget · doi:10.18632/oncotarget.17184 · Cited by 172 · see citing works
Dejima, H., Iinuma, H., Kanaoka, R., Matsutani, N., & Kawamura, M. (2017) · Oncology Letters · doi:10.3892/ol.2017.5569 · Cited by 171 · see citing works
Exosomes and extracellular vesicles: Rethinking the essential values in cancer biology
Yokoi, A., & Ochiya, T. (2021) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2021.03.032 · Cited by 169 · see citing works
RKNNMDA: Ranking-based KNN for MiRNA-Disease Association prediction
Chen, X., Wu, Q.-F., & Yan, G. (2017) · RNA Biology · doi:10.1080/15476286.2017.1312226 · Cited by 165 · see citing works
Adaptive boosting-based computational model for predicting potential miRNA-disease associations
Zhao, Y. F., Chen, X., & Yin, J. (2019) · Bioinformatics · doi:10.1093/bioinformatics/btz297 · Cited by 165 · see citing works
In situ single step detection of exosome microRNA using molecular beacon
Lee, J. H., Kim, J. A., Kwon, M. H., Kang, J. Y., & Rhee, W. J. (2015) · Biomaterials · doi:10.1016/j.biomaterials.2015.03.014 · Cited by 159 · see citing works
Cancer-secreted exosomal miR-21-5p induces angiogenesis and vascular permeability by targeting KRIT1
He, Q., Ye, A., Ye, W., Liao, X., Qin, G.-Q., Xu, Y., Yin, Y., Luo, H., Yi, M., Xian, L., et al. (2021) · Cell Death and Disease · doi:10.1038/s41419-021-03803-8 · Cited by 159 · see citing works
Tumor cells derived-exosomes as angiogenenic agents: possible therapeutic implications
Ahmadi, M., & Rezaie, J. (2020) · Journal of Translational Medicine · doi:10.1186/s12967-020-02426-5 · Cited by 158 · see citing works
Simultaneous and multiplexed detection of exosome microRNAs using molecular beacons
Lee, J. H., Kim, J. A., Jeong, S.-A., & Rhee, W. J. (2016) · Biosensors and Bioelectronics · doi:10.1016/j.bios.2016.06.058 · Cited by 157 · see citing works
Serum-based microRNA signatures in early diagnosis and prognosis prediction of colon cancer
Vychytilova‐Faltejskova, P., Radová, L., Šachlová, M., Košářová, Z., Slabá, K., Fabián, P., Grolich, T., Procházka, V., Kala, Z., Svoboda, M., et al. (2016) · Carcinogenesis · doi:10.1093/carcin/bgw078 · Cited by 156 · see citing works
Fang, Z., Tang, J. P., Bai, Y., Lin, H., You, H., Jin, H., Lin, L., You, P., Li, J., Zhang, D., et al. (2015) · Journal of Experimental & Clinical Cancer Research · doi:10.1186/s13046-015-0198-6 · Cited by 156 · see citing works
Extracellular vesicles as emerging targets in cancer: Recent development from bench to bedside
Wu, K., Xing, F., Wu, S.-Y., & Watabe, K. (2017) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2017.10.001 · Cited by 157 · see citing works
Emerging microRNA biomarkers for colorectal cancer diagnosis and prognosis
Chen, B., Xia, Z., Deng, Y., Yang, Y., Zhang, P., Zhu, H., Xu, N., & Liang, S. (2019) · Open Biology · doi:10.1098/rsob.180212 · Cited by 156 · see citing works
Diagnostic and Therapeutic Potential of Exosomes in Cancer: The Beginning of a New Tale?
Mirzaei, H., Sahebkar, A., Jaafari, M. R., Goodarzi, M., & Mirzaei, H. R. (2016) · Journal of Cellular Physiology · doi:10.1002/jcp.25739 · Cited by 155 · see citing works
Bhome, R., Goh, R. W., Bullock, M. D., Pillar, N., Thirdborough, S. M., Mellone, M., Mirnezami, R., Galea, D., Veselkov, K., Gu, Q., et al. (2017) · Aging · doi:10.18632/aging.101355 · Cited by 155 · see citing works
Exosomes: Isolation, characterization, and biomedical applications
Alzhrani, G. N., Alanazi, S. T., Alsharif, S. Y., Albalawi, A. M., Alsharif, A. A., Abdel‐Maksoud, M. S., & Elsherbiny, N. M. (2021) · Cell Biology International · doi:10.1002/cbin.11620 · Cited by 155 · see citing works
MicroRNAs, Long Noncoding RNAs, and Their Functions in Human Disease
Xue, M., Zhuo, Y., & Shan, B. (2017) · Methods in molecular biology · doi:10.1007/978-1-4939-7046-9_1 · Cited by 154 · see citing works
Methodologies to Isolate and Purify Clinical Grade Extracellular Vesicles for Medical Applications
Akbar, A., Malekian, F., Baghban, N., Kodam, S. P., & Ullah, M. (2022) · Cells · doi:10.3390/cells11020186 · Cited by 154 · see citing works
Exosomes: New players in cancer
Guo, W., Gao, Y., Li, N., Shao, F., Wang, C., Wang, P., Yang, Z., Li, R., & He, J. (2017) · Oncology Reports · doi:10.3892/or.2017.5714 · Cited by 151 · see citing works
Signaling by exosomal microRNAs in cancer
Falcone, G., Felsani, A., & D’Agnano, I. (2015) · Journal of Experimental & Clinical Cancer Research · doi:10.1186/s13046-015-0148-3 · Cited by 151 · see citing works
Yamada, N. O., Tsujimura, N., Kumazaki, M., Shinohara, H., Taniguchi, K., Nakagawa, Y., Naoe, T., & Akao, Y. (2014) · Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms · doi:10.1016/j.bbagrm.2014.09.002 · Cited by 150 · see citing works
Liao, J., Liu, R., SHI, Y.-J., Yin, L., & Pu, Y. (2016) · International Journal of Oncology · doi:10.3892/ijo.2016.3453 · Cited by 150 · see citing works
Exosomes, new biomarkers in early cancer detection
Jalalian, S. H., Ramezani, M., Jalalian, S. A., Abnous, K., & Taghdisi, S. M. (2019) · Analytical Biochemistry · doi:10.1016/j.ab.2019.02.013 · Cited by 147 · see citing works
MicroRNAs in the etiology of colorectal cancer: Pathways and clinical implications
Strubberg, A. M., & Madison, B. B. (2017) · Disease Models & Mechanisms · doi:10.1242/dmm.027441 · Cited by 147 · see citing works
MicroRNAs in extracellular vesicles: potential cancer biomarkers
Kinoshita, T., Yip, K. W., Spence, T., & Liu, F. (2016) · Journal of Human Genetics · doi:10.1038/jhg.2016.87 · Cited by 149 · see citing works
Yoshimura, A., Sawada, K., Nakamura, K., Kinose, Y., Nakatsuka, E., Kobayashi, M., Miyamoto, M., Ishida, K., Matsumoto, Y., Kodama, M., et al. (2018) · BMC Cancer · doi:10.1186/s12885-018-4974-5 · Cited by 145 · see citing works
Recent Progress in Detection and Profiling of Cancer Cell‐Derived Exosomes
Xiong, H., Huang, Z., Yang, Z., Lin, Q., Yang, B., Fang, X., Liu, B., Chen, H., & Kong, J. (2021) · Small · doi:10.1002/smll.202007971 · Cited by 144 · see citing works
Circulating Serum Exosomal miRNAs As Potential Biomarkers for Esophageal Adenocarcinoma
Chiam, K., Wang, T., Watson, D. I., Mayne, G. C., Irvine, T., Bright, T., Smith, L. T., White, I. A., Bowen, J. M., Keefe, D. M. K., et al. (2015) · Journal of Gastrointestinal Surgery · doi:10.1007/s11605-015-2829-9 · Cited by 144 · see citing works
Emerging Role of MicroRNAs as Liquid Biopsy Biomarkers in Gastrointestinal Cancers
Shigeyasu, K., Toden, S., Zumwalt, T. J., Okugawa, Y., & Goel, A. (2017) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-16-1676 · Cited by 145 · see citing works
Wendler, F., Favicchio, R., Simon, T. R., Alifrangis, C., Stebbing, J., & Giamas, G. (2016) · Oncogene · doi:10.1038/onc.2016.253 · Cited by 141 · see citing works
Li, B., Hong, J., Mei, H., Wang, Y., Yu, T., Zang, S., & Wu, Q. (2019) · Oncogene · doi:10.1038/s41388-019-0788-4 · Cited by 140 · see citing works
Exosomal miR-1229 derived from colorectal cancer cells promotes angiogenesis by targeting HIPK2
Hu, H., Yu, C.-H., Zhang, H., Zhang, S., Yu, W.-Y., Yang, Y., & Chen, Q. (2019) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2019.03.221 · Cited by 140 · see citing works
A panel of microRNA signature in serum for colorectal cancer diagnosis
Zhu, M., Huang, Z., Zhu, D., Xin Min, Z. H. O. U., Shan, X., Qi, L., Wu, L., Cheng, W., Zhu, J., Zhang, L., et al. (2017) · Oncotarget · doi:10.18632/oncotarget.15059 · Cited by 138 · see citing works
Luo, X.-J., Zhao, Q., Liu, J. S., Zheng, J., Qiu, M., Ju, H., & Xu, R. (2020) · Molecular Therapy · doi:10.1016/j.ymthe.2020.12.017 · Cited by 137 · see citing works
Biogenesis and Functions of Exosomes and Extracellular Vesicles
Dreyer, F. S., & Baur, A. S. (2016) · Methods in molecular biology · doi:10.1007/978-1-4939-3753-0_15 · Cited by 135 · see citing works
The future of blood-based biomarkers for the early detection of breast cancer
Loke, S. Y., & Lee, A. S. G. (2018) · European Journal of Cancer · doi:10.1016/j.ejca.2017.12.025 · Cited by 135 · see citing works
The potential of tumor-derived exosomes for noninvasive cancer monitoring
Whiteside, T. L. (2015) · Expert Review of Molecular Diagnostics · doi:10.1586/14737159.2015.1071666 · Cited by 134 · see citing works
Breast cancer: The translation of big genomic data to cancer precision medicine
Low, S., Zembutsu, H., & Nakamura, Y. (2017) · Cancer Science · doi:10.1111/cas.13463 · Cited by 136 · see citing works
Liquid biopsy for cancer screening, patient stratification and monitoring
Brock, G., Castellanos-Rizaldos, E., Hu, L., Coticchia, C. M., & Skog, J. (2018) · Translational Cancer Research · doi:10.21037/4546 · Cited by 131 · see citing works
- Authors
- Ogata-Kawata, H., Izumiya, M., Kurioka, D., Honma, Y., Yamada, Y., Furuta, K., Gunji, T., Ohta, H., Okamoto, H., Sonoda, H., Watanabe, M., Nakagama, H., Yokota, J., Kohno, T., & Tsuchiya, N.
- Affiliations
- University of Tokyo Hospital (JP)
- Yokohama National University (JP)
- National Cancer Center Hospital (JP)
- NTT Medical Center (JP)
- Shionogi (Japan) (JP)
- National Cancer Center Research Institute (JP)
- Institute of Predictive and Personalized Medicine of Cancer (ES)
- Corresponding author
- Tsuchiya, Naoto
- ORCID
- Venue
- PLoS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2014-04-04
- Volume
- 9
- Issue
- 4
- Pages
- e92921
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC3976275
- OpenAlex
- W1992970284
- Cited by
- 809
- References
- 37
- Citations by year
- 2026: 28 · 2025: 37 · 2024: 51 · 2023: 45 · 2022: 76 · 2021: 96 · 2020: 89 · 2019: 81 · 2018: 76 · 2017: 76 · 2016: 78 · 2015: 60 · 2014: 15
- FWCI
- 31.32
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS ONE (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
- Figshare (submittedVersion, cc-by)
- Funders
- National Institute of Biomedical Innovation
- Japan Society for the Promotion of Science (23300359, 24790683)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Extracellular vesicles in disease
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › MicroRNA in disease regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer-related molecular mechanisms research
- Keywords
- exosomal microRNAs, colorectal cancer, serum exosomes, diagnostic biomarkers, non-invasive diagnosis, miR-21, miR-223, miR-23a, miR-150, miR-1246, let-7a, tumor resection, CA19-9, carcinoembryonic antigen
- MeSH terms
- Adult, Aged, Colonic Neoplasms, Female, Humans, Male, Middle Aged, Tumor Cells, Cultured, Biomarkers, Tumor, Gene Expression Regulation, Neoplastic, Case-Control Studies, HT29 Cells, Gene Expression Profiling, MicroRNAs, HCT116 Cells, Cell Line, Tumor, Microarray Analysis, Exosomes
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review