Extracellular Vesicle-Mediated Transfer of a Novel Long Noncoding RNA TUC339: A Mechanism of Intercellular Signaling in Human Hepatocellular Cancer
Open accessAbstract
Although the expression of long noncoding RNA (lncRNA) is altered in hepatocellular cancer (HCC), their biological effects are poorly defined. We have identified lncRNA with highly conserved sequences, ultraconserved lncRNA (ucRNA) that are transcribed and altered in expression in HCC. Extracellular vesicles, such as exosomes and microvesicles, are released from tumor cells and can transfer biologically active proteins and RNA across cells. We sought to identify the role of vesicle-mediated transfer of ucRNA as a mechanism by which these novel lncRNA could influence intercellular signaling with potential for environmental modulation of tumor cell behavior. HCC-derived extracellular vesicles could be isolated from cells in culture and taken up by adjacent cells. The expression of several ucRNA was dramatically altered within extracellular vesicles compared to that in donor cells. The most highly significantly expressed ucRNA in HCC cell-derived extracellular vesicles was cloned and identified as a 1,198-bp ucRNA, termed TUC339. TUC339 was functionally implicated in modulating tumor cell growth and adhesion. Suppression of TUC339 by siRNA reduced HCC cell proliferation, clonogenic growth, and growth in soft agar. Thus, intercellular transfer of TUC339 represents a unique signaling mechanism by which tumor cells can promote HCC growth and spread. These findings expand the potential roles of ucRNA in HCC, support the existence of selective mechanisms for lncRNA export from cells,…
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TUC339 is a long non-coding RNA that is selectively released in EV from hepatocellular cancer cells and is implicated in modulating tumor cell behavior.
“We also analyzed expression of TUC339, a long non-coding RNA that is selectively released in EV from hepatocellular cancer cells and is foundationally implicated in modulating tumor cell behavior (15).”
From Analysis of Extracellular RNA by Digital PCR (2014) · cites this paper as [15]
Cites
Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources
Huang, D. W., Sherman, B. T., & Lempicki, R. A. (2009) · Nature Protocols · doi:10.1038/nprot.2008.211 · Cited by 35,890 · see citing works
Huang, D. W., Sherman, B. T., & Lempicki, R. A. (2009) · Nucleic Acids Research · doi:10.1093/nar/gkn923 · Cited by 14,108 · see citing works
Mapping and quantifying mammalian transcriptomes by RNA-Seq
Mortazavi, A., Williams, B. A., McCue, K., Schaeffer, L., & Wold, B. (2008) · Nature Methods · doi:10.1038/nmeth.1226 · Cited by 13,696 · 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
Long non-coding RNAs: insights into functions
Mercer, T. R., Dinger, M. E., & Mattick, J. S. (2009) · Nature Reviews Genetics · doi:10.1038/nrg2521 · Cited by 5,654 · see citing works
Prediction of complete gene structures in human genomic DNA
Burge, C., & Karlin, S. (1997) · Journal of Molecular Biology · doi:10.1006/jmbi.1997.0951 · Cited by 4,211 · see citing works
Pan, Q., Shai, O., Lee, L. J., Frey, B. J., & Blencowe, B. J. (2008) · Nature Genetics · doi:10.1038/ng.259 · Cited by 3,951 · 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
Ultraconserved Elements in the Human Genome
Bejerano, G., Pheasant, M., Makunin, I., Stephen, S., Kent, W. J., Mattick, J. S., & Haussler, D. (2004) · Science · doi:10.1126/science.1098119 · Cited by 1,732 · see citing works
Genetic variation in microRNA networks: the implications for cancer research
Ryan, B. M., Robles, A. I., & Harris, C. C. (2010) · Nature reviews. Cancer · doi:10.1038/nrc2867 · Cited by 1,253 · see citing works
Exosomes: A Common Pathway for a Specialized Function
van Niel, G., Porto-Carreiro, I., Simoes, S., & Raposo, G. (2006) · The Journal of Biochemistry · doi:10.1093/jb/mvj128 · Cited by 922 · see citing works
Panzitt, K., Tschernatsch, M. M. O., Guelly, C., Moustafa, T., Stradner, M. H., Strohmaier, H. M., Buck, C. R., Denk, H., Schroeder, R., Trauner, M. A., et al. (2006) · Gastroenterology · doi:10.1053/j.gastro.2006.08.026 · Cited by 771 · see citing works
Ultraconserved Regions Encoding ncRNAs Are Altered in Human Leukemias and Carcinomas
Calin, G. A., Liu, C., Ferracin, M., Hyslop, T., Spizzo, R., Sevignani, C., Fabbri, M., Cimmino, A., Lee, E. J., Wojcik, S. E., et al. (2007) · Cancer Cell · doi:10.1016/j.ccr.2007.07.027 · Cited by 714 · see citing works
The H19 Non-Coding RNA Is Essential for Human Tumor Growth
Matouk, I., de-Groot, N., Mezan, S., Ayesh, S. K., Abu-lail, R., Hochberg, A., & Galun, E. (2007) · PLoS ONE · doi:10.1371/journal.pone.0000845 · Cited by 649 · see citing works
microRNA-29 can regulate expression of the long non-coding RNA gene MEG3 in hepatocellular cancer
Braconi, C., Kogure, T., Valeri, N., Huang, N., Nuovo, G., Costinean, S., Negrini, M., Miotto, E., Croce, C. M., & Patel, T. (2011) · Oncogene · doi:10.1038/onc.2011.193 · Cited by 642 · see citing works
Self-citationLai, M.-C., Yang, Z., Zhou, L., Zhu, Q., Xie, H., Zhang, F., Wu, L., Chen, L.-M., & Zheng, S. (2011) · Medical Oncology · doi:10.1007/s12032-011-0004-z · Cited by 596 · see citing works
Kogure, T., Lin, W.-L., Yan, I. K., Braconi, C., & Patel, T. (2011) · Hepatology · doi:10.1002/hep.24504 · Cited by 551 · see citing works
Self-citationSharp, P. A. (2009) · Cell · doi:10.1016/j.cell.2009.02.007 · Cited by 452 · see citing works
Tumor-Released Microvesicles as Vehicles of Immunosuppression
Valenti, R., Huber, V., Iero, M., Filipazzi, P., Parmiani, G., & Rivoltini, L. (2007) · Cancer Research · doi:10.1158/0008-5472.can-07-0520 · Cited by 409 · see citing works
Micromechanical control of cell–cell interactions
Hui, E. E., & Bhatia, S. N. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0608660104 · Cited by 392 · see citing works
Mohamed, J. S., Gaughwin, P. M., Lim, B., Robson, P., & Lipovich, L. (2009) · RNA · doi:10.1261/rna.1441510 · Cited by 335 · see citing works
Braconi, C., Valeri, N., Kogure, T., Gasparini, P., Huang, N., Nuovo, G. J., Terracciano, L., Croce, C. M., & Patel, T. C. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1011098108 · Cited by 214 · see citing works
Self-citationHighly upregulated in liver cancer noncoding RNA is overexpressed in hepatic colorectal metastasis
Matouk, I., Abbasi, I., Hochberg, A., Galun, E., Dweik, H., & Akkawi, M. (2009) · European Journal of Gastroenterology & Hepatology · doi:10.1097/meg.0b013e328306a3a2 · Cited by 190 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Biological properties of extracellular vesicles and their physiological functions
Yáñez‐Mó, M., Siljander, P. R. ‐., Andreu, Z., Bedina Zavec, A., Borràs, F. E., Buzas, E. I., Buzas, K., Casal, E., Cappello, F., Carvalho, J., et al. (2015) · Journal of Extracellular Vesicles · doi:10.3402/jev.v4.27066 · Cited by 5,926 · see citing works
Exosomes: biogenesis, biologic function and clinical potential
Zhang, Y., Liu, Y., Liu, H., & Tang, W. H. (2019) · Cell & Bioscience · doi:10.1186/s13578-019-0282-2 · Cited by 2,119 · see citing works
LNCcation: lncRNA localization and function
Bridges, M. C., Daulagala, A. C., & Kourtidis, A. (2021) · Journal of Cell Biology · doi:10.1083/jcb.202009045 · Cited by 1,556 · see citing works
Exosome-based liquid biopsies in cancer: opportunities and challenges
Wang, Y., Hurley, J. D., Roberts, D., Chakrabortty, S. K., Enderle, D., Noerholm, M., Breakefield, X. O., & Skog, J. (2021) · Annals of Oncology · doi:10.1016/j.annonc.2021.01.074 · Cited by 871 · 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
Stem Cell-Derived Exosomes as Nanotherapeutics for Autoimmune and Neurodegenerative Disorders
Riazifar, M., Mohammadi, M. R., Pone, E. J., Yeri, A., Lässer, C., Segaliny, A. I., McIntyre, L. L., Shelke, G. V., Hutchins, E., Hamamoto, A., et al. (2019) · ACS Nano · doi:10.1021/acsnano.9b01004 · Cited by 551 · see citing works
Exosomes: From Garbage Bins to Promising Therapeutic Targets
Rashed, M. H., Bayraktar, E., Helal, G. K., Abd‐Ellah, M. F., Amero, P., Chávez‐Reyes, A., & Rodriguez‐Aguayo, C. (2017) · International Journal of Molecular Sciences · doi:10.3390/ijms18030538 · Cited by 525 · see citing works
Clinical utility of circulating non-coding RNAs — an update
Anfossi, S., Babayan, A., Pantel, K., & Călin, G. A. (2018) · Nature Reviews Clinical Oncology · doi:10.1038/s41571-018-0035-x · Cited by 453 · see citing works
Conigliaro, A., Costa, V., Dico, A. L., Saieva, L., Buccheri, S., Dieli, F., Manno, M., Raccosta, S., Mancone, C., Tripodi, M., et al. (2015) · Molecular Cancer · doi:10.1186/s12943-015-0426-x · Cited by 435 · see citing works
Epigenetic regulation in the tumor microenvironment: molecular mechanisms and therapeutic targets
Yang, J., Xu, J., Wang, W. T., Zhang, B., Yu, X., & Shi, S. (2023) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-023-01480-x · Cited by 404 · see citing works
Xiao, J., Pan, Y., Li, X. H., Yang, X. Y., Feng, Y. L., Tan, H. H., Jiang, L., Feng, J., & Yu, X. Y. (2016) · Cell Death & Disease · doi:10.1038/cddis.2016.181 · Cited by 373 · see citing works
Goody, P. R., Hosen, M. R., Christmann, D., Niepmann, S. T., Zietzer, A., Adam, M., Bönner, F., Zimmer, S., Nickenig, G., & Jansen, F. (2020) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.119.313067 · Cited by 339 · see citing works
Xu, Z., Chen, Y., Ma, L., Chen, Y., Liu, J., Guo, Y., Yu, T., Zhang, L., Zhu, L., & Shu, Y. (2022) · Molecular Therapy · doi:10.1016/j.ymthe.2022.01.046 · Cited by 325 · see citing works
Circular RNA: a novel biomarker and therapeutic target for human cancers
Lei, B., Tian, Z., Fan, W., & Ni, B. (2019) · International Journal of Medical Sciences · doi:10.7150/ijms.28047 · Cited by 315 · see citing works
Circulating long non-coding RNAs in cancer: current status and future perspectives
Qi, P., Zhou, X.-Y., & Du, X. (2016) · Molecular Cancer · doi:10.1186/s12943-016-0524-4 · Cited by 313 · see citing works
Iraci, N., Leonardi, T., Gessler, F., Vega, B., & Pluchino, S. (2016) · International Journal of Molecular Sciences · doi:10.3390/ijms17020171 · Cited by 301 · see citing works
Takahashi, K., Yan, I. K., Wood, J. D., Haga, H., & Patel, T. C. (2014) · Molecular Cancer Research · doi:10.1158/1541-7786.mcr-13-0636 · Cited by 281 · see citing works
Self-citationTrophic Effects of Mesenchymal Stem Cells in Tissue Regeneration
Fu, Y., Karbaat, L., Wu, L., Leijten, J., Both, S. K., & Karperien, M. (2017) · Tissue Engineering Part B Reviews · doi:10.1089/ten.teb.2016.0365 · Cited by 276 · see citing works
Long noncoding RNAs: a potential novel class of cancer biomarkers
Yarmishyn, A. A., & Kurochkin, I. V. (2015) · Frontiers in Genetics · doi:10.3389/fgene.2015.00145 · Cited by 273 · see citing works
Regulation of Macrophage Activation and Polarization by HCC-Derived Exosomal lncRNA TUC339
Li, X., Lei, Y., Wu, M., & Li, N. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19102958 · Cited by 254 · see citing works
Berrondo, C., Flax, J. D., Kucherov, V., Siebert, A. L., Osinski, T. L., Rosenberg, A. F., Fucile, C., Richheimer, S., & Beckham, C. J. (2016) · PLoS ONE · doi:10.1371/journal.pone.0147236 · Cited by 267 · see citing works
Transcriptome of Extracellular Vesicles: State-of-the-Art
Turchinovich, A. A., Drapkina, O. M., & Tonevitsky, A. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.00202 · Cited by 254 · see citing works
Extracellular vesicles as circulating cancer biomarkers: opportunities and challenges
Lane, R. E., Korbie, D. J., Hill, M. M. C., & Trau, M. (2018) · Clinical and Translational Medicine · doi:10.1186/s40169-018-0192-7 · Cited by 245 · 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
Fang, S., Tian, H., Li, X., Jin, D., Li, X., Kong, J., Yang, C., Yang, X., Lu, Y., Luo, Y., et al. (2017) · PLoS ONE · doi:10.1371/journal.pone.0175050 · Cited by 234 · see citing works
Takahashi, K., Yan, I. K., Haga, H., & Patel, T. C. (2014) · Journal of Cell Science · doi:10.1242/jcs.141069 · Cited by 231 · see citing works
Self-citationEmerging roles of exosomes during epithelial–mesenchymal transition and cancer progression
Greening, D. W., Gopal, S. K., Mathias, R. A., Liu, L., Sheng, J., Zhu, H., & Simpson, R. J. (2015) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2015.02.008 · Cited by 220 · see citing works
Long noncoding RNAs (lncRNAs) and the molecular hallmarks of aging
Grammatikakis, I., Panda, A., Abdelmohsen, K., & Gorospe, M. (2014) · Aging · doi:10.18632/aging.100710 · Cited by 207 · see citing works
Barbagallo, C., Brex, D., Caponnetto, A., Cirnigliaro, M., Scalia, M., Magnano, A., Caltabiano, R., Barbagallo, D., Biondi, A., Cappellani, A., et al. (2018) · Molecular Therapy — Nucleic Acids · doi:10.1016/j.omtn.2018.05.009 · Cited by 222 · see citing works
Therapeutic and Diagnostic Translation of Extracellular Vesicles in Cardiovascular Diseases
Sahoo, S., Adamiak, M., Mathiyalagan, P., Kenneweg, F., Kafert-Kasting, S., & Thum, T. (2021) · Circulation · doi:10.1161/circulationaha.120.049254 · Cited by 212 · see citing works
Long non-coding RNAs as novel targets for therapy in hepatocellular carcinoma
Parasramka, M. A., Maji, S., Matsuda, A., Yan, I. K., & Patel, T. C. (2016) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2016.03.004 · Cited by 209 · see citing works
Self-citationKoeck, E. S., Iordanskaia, T., Sevilla, S., Ferrante, S. C., Hubal, M. J., Freishtat, R. J., & Nadler, E. P. (2014) · Journal of Surgical Research · doi:10.1016/j.jss.2014.06.050 · Cited by 210 · see citing works
Non-coding RNAs regulation of macrophage polarization in cancer
Mohapatra, S., Pioppini, C., Özpolat, B., & Călin, G. A. (2021) · Molecular Cancer · doi:10.1186/s12943-021-01313-x · Cited by 206 · see citing works
LncRNAs regulate metabolism in cancer
Lin, W., Zhou, Q., Wang, C., Zhu, L., Bi, C., Zhang, S., Wang, X., & Jin, H. (2020) · International Journal of Biological Sciences · doi:10.7150/ijbs.40769 · Cited by 202 · see citing works
Self-citationLang, H., Hu, G., Zhang, B., Kuang, W., Chen, Y., Wu, L., & Xu, G. (2017) · Oncology Reports · doi:10.3892/or.2017.5742 · Cited by 201 · see citing works
Circulating lncRNA H19 in plasma as a novel biomarker for breast cancer
Zhang, K., Luo, Z., Zhang, Y., Zhang, L., Wu, L., Liu, L., Yang, J., Song, X., & Liu, J. (2016) · Cancer Biomarkers · doi:10.3233/cbm-160630 · Cited by 199 · see citing works
Weber, D. G., Johnen, G., Casjens, S., Bryk, O., Pesch, B., Jöckel, K., Kollmeier, J., & Brüning, T. (2013) · BMC Research Notes · doi:10.1186/1756-0500-6-518 · Cited by 196 · see citing works
Exosomal lncRNAs as new players in cell-to-cell communication
Dragomir, M. P., Chen, B., & Călin, G. A. (2018) · Translational Cancer Research · doi:10.21037/tcr.2017.10.46 · Cited by 194 · see citing works
Zhang, K., Shi, H., Xi, H., Wu, X., Cui, J., Gao, Y., Liang, W., Hu, C., Liu, Y., Li, J., et al. (2016) · Theranostics · doi:10.7150/thno.16044 · Cited by 192 · see citing works
Wu, L.-J., Zhang, X., Zhang, B., Shi, H., Yuan, X., Sun, Y., Pan, Z.-J., Qian, H., & Xu, W.-R. (2016) · Tumor Biology · doi:10.1007/s13277-016-5071-5 · Cited by 177 · see citing works
Long noncoding RNA in liver diseases
Takahashi, K., Yan, I., Haga, H., & Patel, T. (2014) · Hepatology · doi:10.1002/hep.27043 · Cited by 184 · see citing works
Self-citationHaga, H., Yan, I. K., Takahashi, K., Matsuda, A., & Patel, T. C. (2017) · Stem Cells Translational Medicine · doi:10.1002/sctm.16-0226 · Cited by 181 · see citing works
Self-citationProgress and Prospects of Long Noncoding RNAs (lncRNAs) in Hepatocellular Carcinoma
Li, C., Chen, J., Zhang, K., Feng, B., Wang, R., & Chen, L. (2015) · Cellular Physiology and Biochemistry · doi:10.1159/000430109 · Cited by 179 · see citing works
The therapeutic and diagnostic role of exosomes in cardiovascular diseases
Zamani, P., Fereydouni, N., Butler, A. E., Navashenaq, J. G., & Sahebkar, A. (2018) · Trends in Cardiovascular Medicine · doi:10.1016/j.tcm.2018.10.010 · Cited by 177 · see citing works
Lee, H., Zhang, D., Zhu, Z., Cruz, C. S. D., & Jin, Y. (2016) · Scientific Reports · doi:10.1038/srep35250 · Cited by 173 · see citing works
The Role of Extracellular Vesicles in the Hallmarks of Cancer and Drug Resistance
Xavier, C. P. R., Caires, H. R., Barbosa, M. A. G., Bergantim, R., Guimarães, J. E., & Vasconcelos, M. H. (2020) · Cells · doi:10.3390/cells9051141 · Cited by 175 · see citing works
Dong, L., Qi, P., Xu, M., Ni, S., Huang, D., Xu, Q., Weng, W., Tan, C., Sheng, W., Zhou, X., et al. (2015) · International Journal of Cancer · doi:10.1002/ijc.29484 · Cited by 167 · see citing works
RNA Biomarkers: Frontier of Precision Medicine for Cancer
Xi, X., Li, T., Huang, Y., Sun, J., Zhu, Y., Yang, Y., & Lu, Z. J. (2017) · Non-Coding RNA · doi:10.3390/ncrna3010009 · Cited by 160 · see citing works
Haga, H., Yan, I. K., Takahashi, K., Wood, J. D., Zubair, A. C., & Patel, T. C. (2015) · Journal of Extracellular Vesicles · doi:10.3402/jev.v4.24900 · Cited by 159 · see citing works
Self-citationTumor 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
Alzahrani, F. A., El‐Magd, M. A., Abdelfattah‐Hassan, A., Saleh, A. A., Saadeldin, I. M., El‐Shetry, E. S., Badawy, A. A., & Alkarim, S. (2018) · Stem Cells International · doi:10.1155/2018/8058979 · Cited by 157 · see citing works
Circulating RNAs as new biomarkers for detecting pancreatic cancer
Kishikawa, T. (2015) · World Journal of Gastroenterology · doi:10.3748/wjg.v21.i28.8527 · Cited by 152 · 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
The Clinical Relevance of Long Non-Coding RNAs in Cancer
da Silva, A. M., Bullock, M. D., & Călin, G. A. (2015) · Cancers · doi:10.3390/cancers7040884 · Cited by 150 · see citing works
Jansen, F., Li, Q., Pfeifer, A., & Werner, N. (2017) · JACC Basic to Translational Science · doi:10.1016/j.jacbts.2017.08.004 · Cited by 146 · see citing works
Fatima, F., & Nawaz, M. (2017) · Non-Coding RNA · doi:10.3390/ncrna3010010 · Cited by 144 · see citing works
Identification of Cancer-Related Long Non-Coding RNAs Using XGBoost With High Accuracy
Zhang, X., Li, T., Wang, J., Li, J., Chen, L., & Liu, C. (2019) · Frontiers in Genetics · doi:10.3389/fgene.2019.00735 · Cited by 142 · see citing works
Sutaria, D. S., Badawi, M., Phelps, M. A., & Schmittgen, T. D. (2017) · Pharmaceutical Research · doi:10.1007/s11095-017-2123-5 · Cited by 140 · see citing works
Circulating biomarkers to monitor cancer progression and treatment
Rapisuwon, S., Vietsch, E. E., & Wellstein, A. (2016) · Computational and Structural Biotechnology Journal · doi:10.1016/j.csbj.2016.05.004 · Cited by 138 · see citing works
Li, Y., Zhao, Z., Liu, W., & Li, X. (2020) · Applied Biochemistry and Biotechnology · doi:10.1007/s12010-020-03244-7 · Cited by 137 · 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
Unpacking extracellular vesicles: RNA cargo loading and function
Dellar, E. R., Hill, C., Melling, G. E., Carter, D. R. F., & Baena-López, L. A. (2022) · Journal of Extracellular Biology · doi:10.1002/jex2.40 · Cited by 138 · see citing works
Exosome: Function and Role in Cancer Metastasis and Drug Resistance
Zhang, C., Ji, Q., Yang, Y., Li, Q., & Wang, Z. (2018) · Technology in Cancer Research & Treatment · doi:10.1177/1533033818763450 · Cited by 134 · see citing works
Exosomes in hepatocellular carcinoma: a new horizon
Chen, R., Xu, X., Tao, Y., Qian, Z., & Yu, Y. (2019) · Cell Communication and Signaling · doi:10.1186/s12964-018-0315-1 · Cited by 136 · see citing works
Exosomes and Their Role in Cancer Progression
Osaki, M., & Okada, F. (2019) · Yonago acta medica · doi:10.33160/yam.2019.06.002 · Cited by 134 · see citing works
The functional roles of exosomal long non-coding RNAs in cancer
Wang, M., Zhou, L., Yu, F., Zhang, Y., Li, P., & Wang, K. (2019) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-019-03018-3 · Cited by 132 · see citing works
Exosomes and Hepatocellular Carcinoma: From Bench to Bedside
Sasaki, R., Kanda, T., Yokosuka, O., Kato, N., Matsuoka, S., & Moriyama, M. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20061406 · Cited by 128 · see citing works
Sources and Functions of Extracellular Small RNAs in Human Circulation
Fritz, J. V., Heintz‐Buschart, A., Ghosal, A., Wampach, L., Etheridge, A., Galas, D. J., & Wilmes, P. (2016) · Annual Review of Nutrition · doi:10.1146/annurev-nutr-071715-050711 · Cited by 124 · see citing works
CD44/CD44v6 a Reliable Companion in Cancer-Initiating Cell Maintenance and Tumor Progression
Wang, Z., Zhao, K., Hackert, T., & Zöller, M. (2018) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2018.00097 · Cited by 123 · see citing works
Wu, Y., Yq, W., Weng, W.-W., Zhang, Q.-Y., Xq, Y., Gan, H.-L., Yang, Y.-S., Zhang, P.-P., Sun, M., Xu, M.-D., et al. (2016) · Oncogenesis · doi:10.1038/oncsis.2015.48 · Cited by 118 · see citing works
HCC-Derived Exosomes: Critical Player and Target for Cancer Immune Escape
Han, Q., Zhao, H., Yu, J., Yin, C., & Zhang, J. (2019) · Cells · doi:10.3390/cells8060558 · Cited by 119 · see citing works
Extracellular vesicles: Novel mediator for cell to cell communications in liver pathogenesis
Devhare, P. B., & Ray, R. B. (2017) · Molecular Aspects of Medicine · doi:10.1016/j.mam.2017.11.001 · Cited by 114 · see citing works
Kosaka, N., Kogure, A., Yamamoto, T., Urabe, F., Usuba, W., Prieto‐Vila, M., & Ochiya, T. (2019) · Experimental & Molecular Medicine · doi:10.1038/s12276-019-0219-1 · Cited by 110 · see citing works
Chen, H., Zhang, C., Wang, H., & Zhao, L. (2021) · OncoImmunology · doi:10.1080/2162402x.2021.1887552 · Cited by 111 · see citing works
Shi, W., Wu, Q., Li, S., Yang, T., Liu, Z.-H., Tong, Y., Tuo, L., Wang, S., & Cao, X. (2015) · Tumor Biology · doi:10.1007/s13277-014-2863-3 · Cited by 108 · see citing works
Chen, J., Zhou, R.-P., Liang, Y.-M., Fu, X.-J., Wang, D.-R., & Wang, C. (2019) · The FASEB Journal · doi:10.1096/fj.201901610 · Cited by 97 · see citing works
The Role of Extracellular Vesicles: An Epigenetic View of the Cancer Microenvironment
Qian, Z., Shen, Q., Yang, X., Qiu, Y., & Zhang, W. (2015) · BioMed Research International · doi:10.1155/2015/649161 · Cited by 106 · see citing works
Droplet digital PCR improves urinary exosomal miRNA detection compared to real-time PCR
Wang, C., Ding, Q., Plant, P. J., Basheer, M. F., Yang, C., Tawedrous, E., Krizova, A., Boulos, C., Farag, M. S., Cheng, Y., et al. (2019) · Clinical Biochemistry · doi:10.1016/j.clinbiochem.2019.03.008 · Cited by 105 · see citing works
Sutaria, D. S., Jiang, J., Elgamal, O. A., Pomeroy, S. M., Badawi, M. A., Zhu, X., Pavlovicz, R. E., Azevedo‐Pouly, A. C. P., Chalmers, J. J., Li, C., et al. (2017) · Journal of Extracellular Vesicles · doi:10.1080/20013078.2017.1333882 · Cited by 104 · see citing works
Qiu, L., Tang, Q., Li, G., & Chen, K. (2017) · Life Sciences · doi:10.1016/j.lfs.2017.10.007 · Cited by 102 · see citing works
Wnt signalling modulates transcribed-ultraconserved regions in hepatobiliary cancers
Carotenuto, P., Fassan, M., Pandolfo, R., Lampis, A., Vicentini, C., Cascione, L., Paulus-Hock, V., Boulter, L., Guest, R. V., Quagliata, L., et al. (2016) · Gut · doi:10.1136/gutjnl-2016-312278 · Cited by 101 · see citing works
Self-citationLee, H., Abston, E. D., Zhang, D., Rai, A., & Jin, Y. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.00924 · Cited by 100 · see citing works
Yang, N., Li, S., Li, G., Zhang, S., Tang, X., Ni, S., Jian, X.-M., Xu, C., Zhu, J., & Lu, M. (2016) · Oncotarget · doi:10.18632/oncotarget.12465 · Cited by 101 · see citing works
Extracellular vesicle long noncoding RNA as potential biomarkers of liver cancer
Mohankumar, S., & Patel, T. C. (2015) · Briefings in Functional Genomics · doi:10.1093/bfgp/elv058 · Cited by 98 · see citing works
Self-citationHerpesviruses hijack host exosomes for viral pathogenesis
Sadeghipour, S., & Mathias, R. A. (2017) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2017.03.005 · Cited by 97 · see citing works
Ke, D., Li, H., Zhang, Y., An, Y., Fu, H., Fang, X., & Zheng, X. (2017) · Oncotarget · doi:10.18632/oncotarget.15628 · Cited by 94 · see citing works
Pancreatic cancer stem cell markers and exosomes - the incentive push
Heiler, S., Wang, Z., & Zöller, M. (2016) · World Journal of Gastroenterology · doi:10.3748/wjg.v22.i26.5971 · Cited by 91 · see citing works
Role of extracellular vesicles in liver diseases and their therapeutic potential
Kostallari, E., Valainathan, S. R., Biquard, L., Shah, V. H., & Rautou, P. (2021) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2021.05.026 · Cited by 92 · see citing works
New Insights into the Epigenetics of Hepatocellular Carcinoma
Wahid, B., Ali, A., Rafique, S., & Idrees, M. (2017) · BioMed Research International · doi:10.1155/2017/1609575 · Cited by 91 · see citing works
Extracellular RNAs: A New Awareness of Old Perspectives
Sadik, N., Cruz, L., Gurtner, A., Rodosthenous, R. S., Dusoswa, S. A., Ziegler, O., van Solinge, T. S., Wei, Z., Salvador, A. M., György, B., et al. (2018) · Methods in molecular biology · doi:10.1007/978-1-4939-7652-2_1 · Cited by 90 · see citing works
Extracellular vesicle associated long non-coding RNAs functionally enhance cell viability
Hewson, C., Capraro, D., Burdach, J., Whitaker, N. J., & Morris, K. V. (2016) · Non-coding RNA Research · doi:10.1016/j.ncrna.2016.06.001 · Cited by 90 · see citing works
Exosomes Regulate the Transformation of Cancer Cells in Cancer Stem Cell Homeostasis
Xu, J.-S., Liao, K.-L., & Zhou, W.-M. (2018) · Stem Cells International · doi:10.1155/2018/4837370 · Cited by 87 · see citing works
Diurnal Variations of Circulating Extracellular Vesicles Measured by Nano Flow Cytometry
Danielson, K., Estanislau, J., Tigges, J., Toxavidis, V., Camacho, V., Felton, E. J., Khoory, J. A., Kreimer, S. D., Ivanov, A. R., Mantel, P., et al. (2016) · PLoS ONE · doi:10.1371/journal.pone.0144678 · Cited by 84 · see citing works
Characters, functions and clinical perspectives of long non-coding RNAs
Wu, R., Su, Y., Wu, H., Dai, Y., Zhao, M., & Lu, Q. (2016) · Molecular Genetics and Genomics · doi:10.1007/s00438-016-1179-y · Cited by 84 · see citing works
LncRNAs as Chromatin Regulators in Cancer: From Molecular Function to Clinical Potential
Begolli, R., Sideris, N., & Giakountis, A. (2019) · Cancers · doi:10.3390/cancers11101524 · Cited by 84 · see citing works
Yu, J., Han, J., Zhang, J., Li, G., Liu, H., Cui, X., Xu, Y., Li, T., Liu, J., & Wang, C. (2016) · Medicine · doi:10.1097/md.0000000000004436 · Cited by 79 · see citing works
The Emerging Role of Long Non-Coding RNAs in the Metastasis of Hepatocellular Carcinoma
Chen, X., Tang, F. R., Arfuso, F., Cai, W.-Q., Ma, Z., Yang, J., & Sethi, G. (2019) · Biomolecules · doi:10.3390/biom10010066 · Cited by 79 · see citing works
Exosome-Based Treatment for Atherosclerosis
Heo, J., & Kang, H. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23021002 · Cited by 79 · see citing works
Papillary thyroid cancer–derived exosomes contain miRNA-146b and miRNA-222
Lee, J. C., Zhao, J., Gundara, J. S., Serpell, J. W., Bach, L. A., & Sidhu, S. B. (2015) · Journal of Surgical Research · doi:10.1016/j.jss.2015.02.027 · Cited by 79 · see citing works
- Authors
- Kogure, T., Yan, I. K., Lin, W.-L., & Patel, T.
- Affiliations
- Mayo Clinic (US)
- Mayo Clinic in Florida (US)
- Corresponding author
- Patel, T.
- Venue
- Genes & Cancer
- Publisher
- SAGE Publications
- Published
- 2013-07-01
- Volume
- 4
- Issue
- 7-8
- Pages
- 261-272
- ISSN
- 1947-6019 (ISSN-L)
- 1947-6027
- PMC
- PMC3807642
- OpenAlex
- W2118018590
- Cited by
- 303
- References
- 23
- Citations by year
- 2026: 3 · 2025: 5 · 2024: 13 · 2023: 16 · 2022: 28 · 2021: 31 · 2020: 37 · 2019: 32 · 2018: 31 · 2017: 30 · 2016: 37 · 2015: 25 · 2014: 14 · 2013: 1
- FWCI
- 11.51
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Genes & Cancer (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute of Diabetes and Digestive and Kidney Diseases (R01DK069370)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Extracellular vesicles in disease
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer-related molecular mechanisms research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › MicroRNA in disease regulation
- Keywords
- long non-coding RNA, extracellular vesicles, exosomes, microvesicles, hepatocellular carcinoma, intercellular RNA transfer, tumor cell proliferation, tumor cell adhesion, tumor microenvironment
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