Exosomes as carriers transporting long non‑coding RNAs: Molecular characteristics and their function in cancer (Review)
- Authors:
- Damian Kołat
- Raneem Hammouz
- Andrzej K. Bednarek
- Elżbieta Płuciennik
-
Affiliations: Faculty of Biomedical Sciences and Postgraduate Education, Medical University of Łódź, 90‑752 Łódź, Poland, Department of Molecular Carcinogenesis, Medical University of Łódź, 90‑752 Łódź, Poland - Published online on: June 5, 2019 https://doi.org/10.3892/mmr.2019.10340
- Pages: 851-862
-
Copyright : © Kołat et al. This is an open access article distributed under the terms of Creative Commons Attribution License [CC BY 4.0].
This article is mentioned in:
Abstract
Pan BT and Johnstone RM: Fate of the transferrin receptor during maturation of sheep reticulocytes in vitro: Selective externalization of the receptor. Cell. 33:967–978. 1983. View Article : Google Scholar : PubMed/NCBI | |
Johnstone RM, Adam M, Hammond JR, Orr L and Turbide C: Vesicle formation during reticulocyte maturation. Association of plasma membrane activities with released vesicles (exosomes). J Boil Chem. 262:9412–9420. 1987. | |
Yu S, Cao H, Shen B and Feng J: Tumor-derived exosomes in cancer progression and treatment failure. Oncotarget. 6:37151–37168. 2015. View Article : Google Scholar : PubMed/NCBI | |
Isola AL and Chen S: Exosomes: The link between GPCR activation and metastatic potential? Front Genet. 7:562016. View Article : Google Scholar : PubMed/NCBI | |
Ciardiello C, Cavallini L, Spinelli C, Yang J, Reis-Sobreiro M, de Candia P, Minciacchi VR and Di Vizio D: Focus on extracellular vesicles: New frontiers of cell-to-cell communication in cancer. Int J Mol Sci. 17:1752016. View Article : Google Scholar : PubMed/NCBI | |
Taverna S, Giallombardo M, Gil-Bazo I, Carreca AP, Castiglia M, Chacartegui J, Araujo A, Alessandro R, Pauwels P, Peeters M and Rolfo C: Exosomes isolation and characterization in serum is feasible in non-small cell lung cancer patients: Critical analysis of evidence and potential role in clinical practice. Oncotarget. 7:28748–28760. 2016. View Article : Google Scholar : PubMed/NCBI | |
Fu H, Yang H, Zhang X and Xu W: The emerging roles of exosomes in tumor-stroma interaction. J Cancer Res Clin Oncol. 142:1897–1907. 2016. View Article : Google Scholar : PubMed/NCBI | |
Soung YH, Nguyen T, Cao H, Lee J and Chung J: Emerging roles of exosomes in cancer invasion and metastasis. BMB Rep. 49:18–25. 2016. View Article : Google Scholar : PubMed/NCBI | |
Rahman MA, Barger JF, Lovat F, Gao M, Otterson GA and Nana-Sinkam P: Lung cancer exosomes as drivers of epithelial mesenchymal transition. Oncotarget. 7:54852–54866. 2016. View Article : Google Scholar : PubMed/NCBI | |
Wang Y, Yi J, Chen X, Zhang Y, Xu M and Yang Z: The regulation of cancer cell migration by lung cancer cell-derived exosomes through TGF-β and IL-10. Oncol Lett. 11:1527–1530. 2016. View Article : Google Scholar : PubMed/NCBI | |
Bobrie A and Thery C: Unraveling the physiological functions of exosome secretion by tumors. Oncoimmunology. 2:e225652013. View Article : Google Scholar : PubMed/NCBI | |
De Toro J, Herschlik L, Waldner C and Mongini C: Emerging roles of exosomes in normal and pathological conditions: New insights for diagnosis and therapeutic applications. Front Immunol. 6:2032015. View Article : Google Scholar : PubMed/NCBI | |
Kim KM, Abdelmohsen K, Mustapic M, Kapogiannis D and Gorospe M: RNA in extracellular vesicles. Wiley Interdiscip Rev RNA. 8:2017. View Article : Google Scholar | |
Neviani P and Fabbri M: Exosomic microRNAs in the tumor microenvironment. Front Med (Lausanne). 2:472015.PubMed/NCBI | |
Martin F, Roth DM, Jans DA, Pouton CW, Partridge LJ, Monk PN and Moseley GW: Tetraspanins in viral infections: A fundamental role in viral biology? J Virol. 79:10839–10851. 2005. View Article : Google Scholar : PubMed/NCBI | |
Baietti MF, Zhang Z, Mortier E, Melchior A, Degeest G, Geeraerts A, Ivarsson Y, Depoortere F, Coomans C, Vermeiren E, et al: Syndecan-syntenin-ALIX regulates the biogenesis of exosomes. Nat Cell Biol. 14:677–685. 2012. View Article : Google Scholar : PubMed/NCBI | |
Fares J, Kashyap R and Zimmermann P: Syntenin: Key player in cancer exosome biogenesis and uptake? Cell Adh Migr. 11:124–126. 2017. View Article : Google Scholar : PubMed/NCBI | |
Ghossoub R, Lembo F, Rubio A, Gaillard CB, Bouchet J, Vitale N, Slavík J, Machala M and Zimmermann P: Syntenin-ALIX exosome biogenesis and budding into multivesicular bodies are controlled by ARF6 and PLD2. Nat Commun. 5:34772014. View Article : Google Scholar : PubMed/NCBI | |
Shim S: Role and regulation of ESCRT-III In multivesiculr body biogenesis. All Theses and Dissertations (ETDs). 3232009. | |
Roxrud I, Stenmark H and Malerod L: ESCRT & Co. Biol Cell. 102:293–318. 2010. View Article : Google Scholar : PubMed/NCBI | |
Votteler J and Sundquist WI: Virus budding and the ESCRT pathway. Cell Host Microbe. 14:232–241. 2013. View Article : Google Scholar : PubMed/NCBI | |
Amano M, Nakayama M and Kaibuchi K: Rho-kinase/ROCK: A key regulator of the cytoskeleton and cell polarity. Cytoskeleton (Hoboken). 67:545–554. 2010. View Article : Google Scholar : PubMed/NCBI | |
Roucourt B, Meeussen S, Bao J, Zimmermann P and David G: Heparanase activates the syndecan-syntenin-ALIX exosome pathway. Cell Res. 25:412–428. 2015. View Article : Google Scholar : PubMed/NCBI | |
Roma-Rodrigues C, Fernandes AR and Baptista PV: Exosome in tumour microenvironment: Overview of the crosstalk between normal and cancer cells. Biomed Res Int. 2014:1794862014. View Article : Google Scholar : PubMed/NCBI | |
Gezer U, Ozgur E, Cetinkaya M, Isin M and Dalay N: Long non-coding RNAs with low expression levels in cells are enriched in secreted exosomes. Cell Biol Int. 38:1076–1079. 2014.PubMed/NCBI | |
Schageman J, Zeringer E, Li M, Barta T, Lea K, Gu J, Magdaleno S, Setterquist R and Vlassov AV: The complete exosome workflow solution: From isolation to characterization of RNA cargo. Biomed Res Int. 2013:2539572013. View Article : Google Scholar : PubMed/NCBI | |
Batagov AO, Kuznetsov VA and Kurochkin IV: Identification of nucleotide patterns enriched in secreted RNAs as putative cis-acting elements targeting them to exosome nano-vesicles. BMC Genomics. 3 (Suppl 12):S182011. View Article : Google Scholar | |
Okazaki Y, Furuno M, Kasukawa T, Adachi J, Bono H, Kondo S, Nikaido I, Osato N, Saito R, Suzuki H, et al: Analysis of the mouse transcriptome based on functional annotation of 60,770 full-length cDNAs. Nature. 420:563–573. 2002. View Article : Google Scholar : PubMed/NCBI | |
Kapranov P, Cheng J, Dike S, Nix DA, Duttagupta R, Willingham AT, Stadler PF, Hertel J, Hackermüller J, Hofacker IL, et al: RNA maps reveal new RNA classes and a possible function for pervasive transcription. Science. 316:1484–1488. 2007. View Article : Google Scholar : PubMed/NCBI | |
Perkel JM: Visiting ‘noncodarnia’. Biotechniques. 54:301 303–304. 2013. View Article : Google Scholar | |
Wang KC and Chang HY: Molecular mechanisms of long noncoding RNAs. Mol Cell. 43:904–914. 2011. View Article : Google Scholar : PubMed/NCBI | |
Sato-Kuwabara Y, Melo SA, Soares FA and Calin GA: The fusion of two worlds: Non-coding RNAs and extracellular vesicles-diagnostic and therapeutic implications (Review). Int J Oncol. 46:17–27. 2015. View Article : Google Scholar : PubMed/NCBI | |
Bolha L, Ravnik-Glavac M and Glavac D: Long noncoding RNAs as biomarkers in cancer. Dis Markers. 2017:72439682017. View Article : Google Scholar : PubMed/NCBI | |
Hewson C and Morris KV: Form and function of exosome-associated long non-coding RNAs in cancer. Curr Top Microbiol Immunol. 394:41–56. 2016.PubMed/NCBI | |
Zhao J, Ohsumi TK, Kung JT, Ogawa Y, Grau DJ, Sarma K, Song JJ, Kingston RE, Borowsky M and Lee JT: Genome-wide identification of polycomb-associated RNAs by RIP-seq. Mol Cell. 40:939–953. 2010. View Article : Google Scholar : PubMed/NCBI | |
Shih JW and Kung HJ: Long non-coding RNA and tumor hypoxia: New players ushered toward an old arena. J Biomed Sci. 24:532017. View Article : Google Scholar : PubMed/NCBI | |
Berrondo C, Flax J, Kucherov V, Siebert A, Osinski T, Rosenberg A, Fucile C, Richheimer S and Beckham CJ: Expression of the long non-coding RNA HOTAIR correlates with disease progression in bladder cancer and is contained in bladder cancer patient urinary exosomes. PLoS One. 11:e01472362016. View Article : Google Scholar : PubMed/NCBI | |
Yan TH, Lu SW, Huang YQ, Que GB, Chen JH, Chen YP, et al: Upregulation of the long noncoding RNA HOTAIR predicts recurrence in stage Ta/T1 bladder cancer. Tumour biology: the journal of the International Society for Oncodevelopmental Biology and Medicine. 2014.35(10): 10249–57. View Article : Google Scholar : PubMed/NCBI | |
Xie Z, Chen X, Li J, Guo Y, Li H, Pan X, Jiang J, Liu H and Wu B: Salivary HOTAIR and PVT1 as novel biomarkers for early pancreatic cancer. Oncotarget. 7:25408–25419. 2016.PubMed/NCBI | |
Wang J, Zhang X, Ji C, Zhang L, Di Y, Lou W, Zhang X and X J: Novel implications of exosomes and lncRNAs in the diagnosis and treatment of pancreatic cancer. Novel Implications of Exosomes in Diagnosis and Treatment of Cancer and Infectious Diseases. Wang J; IntechOpen, : 2017, https://www.intechopen.com/books/novel-implications-of-exosomes-in-diagnosis-and-treatment-of-cancer-and-infectious-diseases/novel-implications-of-exosomes-and-lncrnas-in-the-diagnosis-and-treatment-of-pancreatic-cancer09th–May. 2019 View Article : Google Scholar | |
Song J, Kim D, Han J, Kim Y, Lee M and Jin EJ: PBMC and exosome-derived Hotair is a critical regulator and potent marker for rheumatoid arthritis. Clin Exp Med. 15:121–126. 2015. View Article : Google Scholar : PubMed/NCBI | |
Zhang R, Xia Y, Wang Z, Zheng J, Chen Y, Li X, Wang Y and Ming H: Serum long non coding RNA MALAT-1 protected by exosomes is up-regulated and promotes cell proliferation and migration in non-small cell lung cancer. Biochem Biophys Res Commun. 490:406–414. 2017. View Article : Google Scholar : PubMed/NCBI | |
Gutschner T, Hammerle M, Eissmann M, Hsu J, Kim Y, Hung G, Revenko A, Arun G, Stentrup M, Gross M, et al: The noncoding RNA MALAT1 is a critical regulator of the metastasis phenotype of lung cancer cells. Cancer Res. 73:1180–1189. 2013. View Article : Google Scholar : PubMed/NCBI | |
Huang JK, Ma L, Song WH, Lu BY, Huang YB, Dong HM, Ma XK, Zhu ZZ and Zhou R: LncRNA-MALAT1 promotes angiogenesis of thyroid cancer by modulating tumor-associated macrophage FGF2 protein secretion. J Cell Biochem. 118:4821–4830. 2017. View Article : Google Scholar : PubMed/NCBI | |
Askarian-Amiri ME, Crawford J, French JD, Smart CE, Smith MA, Clark MB, Ru K, Mercer TR, Thompson ER, Lakhani SR, et al: SNORD-host RNA Zfas1 is a regulator of mammary development and a potential marker for breast cancer. RNA. 17:878–891. 2011. View Article : Google Scholar : PubMed/NCBI | |
Pan L, Liang W, Fu M, Huang ZH, Li X, Zhang W, Zhang P, Qian H, Jiang PC, Xu WR and Zhang X: Exosomes-mediated transfer of long noncoding RNA ZFAS1 promotes gastric cancer progression. J Cancer Res Clin Oncol. 143:991–1004. 2017. View Article : Google Scholar : PubMed/NCBI | |
Zhou H, Wang F, Chen H, Tan Q, Qiu S, Chen S, Jing W, Yu M, Liang C, Ye S and Tu J: Increased expression of long-noncoding RNA ZFAS1 is associated with epithelial-mesenchymal transition of gastric cancer. Aging (Albany NY). 8:2023–2038. 2016. View Article : Google Scholar : PubMed/NCBI | |
Matouk IJ, Halle D, Raveh E, Gilon M, Sorin V and Hochberg A: The role of the oncofetal H19 lncRNA in tumor metastasis: Orchestrating the EMT-MET decision. Oncotarget. 7:3748–3765. 2016. View Article : Google Scholar : PubMed/NCBI | |
Conigliaro A, Costa V, Lo Dico A, Saieva L, Buccheri S, Dieli F, Manno M, Raccosta S, Mancone C, Tripodi M, et al: CD90+ liver cancer cells modulate endothelial cell phenotype through the release of exosomes containing H19 lncRNA. Mol Cancer. 14:1552015. View Article : Google Scholar : PubMed/NCBI | |
Kallen AN, Zhou XB, Xu J, Qiao C, Ma J, Yan L, Lu L, Liu C, Yi JS, Zhang H, et al: The imprinted H19 lncRNA antagonizes let-7 microRNAs. Mol Cell. 52:101–112. 2013. View Article : Google Scholar : PubMed/NCBI | |
George J and Patel T: Noncoding RNA as therapeutic targets for hepatocellular carcinoma. Semin Liver Dis. 35:63–74. 2015. View Article : Google Scholar : PubMed/NCBI | |
Lang HL, Hu GW, Chen Y, Liu Y, Tu W, Lu YM, Wu L and Xu GH: Glioma cells promote angiogenesis through the release of exosomes containing long non-coding RNA POU3F3. Eur Rev Med Pharmacol Sci. 21:959–972. 2017.PubMed/NCBI | |
Hu C, Chen M, Jiang R, Guo Y, Wu M and Zhang X: Exosome-related tumor microenvironment. Journal of Cancer. 2018.9(17): 3084–92. View Article : Google Scholar : PubMed/NCBI | |
Mitra SA, Mitra AP and Triche TJ: A central role for long non-coding RNA in cancer. Front Genet. 3:172012. View Article : Google Scholar : PubMed/NCBI | |
Braconi C, Valeri N, Kogure T, Gasparini P, Huang N, Nuovo GJ, Terracciano L, Croce CM and Patel T: Expression and functional role of a transcribed noncoding RNA with an ultraconserved element in hepatocellular carcinoma. Proc Natl Acad Sci USA. 108:786–791. 2011. View Article : Google Scholar : PubMed/NCBI | |
Kogure T, Yan IK, Lin WL and Patel T: Extracellular vesicle-mediated transfer of a novel long noncoding RNA TUC339: A mechanism of intercellular signaling in human hepatocellular cancer. Genes Cancer. 4:261–272. 2013. View Article : Google Scholar : PubMed/NCBI | |
Takahashi K, Yan IK, Kogure T, Haga H and Patel T: Extracellular vesicle-mediated transfer of long non-coding RNA ROR modulates chemosensitivity in human hepatocellular cancer. FEBS Open Bio. 4:458–467. 2014. View Article : Google Scholar : PubMed/NCBI | |
Li Y, Jiang B, Zhu H, Qu X, Zhao L, Tan Y, Jiang Y, Liao M and Wu X: Inhibition of long non-coding RNA ROR reverses resistance to Tamoxifen by inducing autophagy in breast cancer. Tumour Biol. 39:10104283177057902017. View Article : Google Scholar : PubMed/NCBI | |
Yang N, Li S, Li G, Zhang S, Tang X, Ni S, Jian X, Xu C, Zhu J and Lu M: The role of extracellular vesicles in mediating progression, metastasis and potential treatment of hepatocellular carcinoma. Oncotarget. 8:3683–3695. 2017.PubMed/NCBI | |
Takahashi K, Yan IK, Wood J, Haga H and Patel T: Involvement of extracellular vesicle long noncoding RNA (linc-VLDLR) in tumor cell responses to chemotherapy. Mol Cancer Res. 12:1377–1387. 2014. View Article : Google Scholar : PubMed/NCBI | |
Fritah S, Niclou SP and Azuaje F: Databases for lncRNAs: A comparative evaluation of emerging tools. RNA. 20:1655–1665. 2014. View Article : Google Scholar : PubMed/NCBI | |
Mourtada-Maarabouni M, Pickard MR, Hedge VL, Farzaneh F and Williams GT: GAS5, a non-protein-coding RNA, controls apoptosis and is downregulated in breast cancer. Oncogene. 28:195–208. 2009. View Article : Google Scholar : PubMed/NCBI | |
Lucafò M, Stocco G and Decorti GJTCR: Emerging molecular mechanisms underlying cancer metastasis: The rising role of the long non-coding RNA GAS5. Transl Cancer Res. 5 (Suppl 4):S827–S830. 2016. View Article : Google Scholar | |
Pickard MR, Mourtada-Maarabouni M and Williams GT: Long non-coding RNA GAS5 regulates apoptosis in prostate cancer cell lines. Biochim Biophys Acta. 1832:1613–1623. 2013. View Article : Google Scholar : PubMed/NCBI | |
Kino T, Hurt DE, Ichijo T, Nader N and Chrousos GP: Noncoding RNA gas5 is a growth arrest- and starvation-associated repressor of the glucocorticoid receptor. Sci Signal. 3:ra82010. View Article : Google Scholar : PubMed/NCBI | |
O'Leary VB, Hain S, Maugg D, Smida J, Azimzadeh O, Tapio S, Ovsepian SV and Atkinson MJ: Long non-coding RNA PARTICLE bridges histone and DNA methylation. Sci Rep. 7:17902017. View Article : Google Scholar : PubMed/NCBI | |
O'Leary VB, Ovsepian SV, Carrascosa LG, Buske FA, Radulovic V, Niyazi M, Moertl S, Trau M, Atkinson MJ and Anastasov N: PARTICLE, a triplex-forming long ncrna, regulates locus-specific methylation in response to low-dose irradiation. Cell Rep. 11:474–485. 2015. View Article : Google Scholar : PubMed/NCBI | |
Deng J, Tang J, Wang G and Zhu YS: Long non-coding RNA as potential biomarker for prostate cancer: Is it making a difference? Int J Environ Res Public Health. 14:E2702017. View Article : Google Scholar : PubMed/NCBI | |
Wang X, Arai S, Song X, Reichart D, Du K, Pascual G, Tempst P, Rosenfeld MG, Glass CK and Kurokawa R: Induced ncRNAs allosterically modify RNA-binding proteins in cis to inhibit transcription. Nature. 454:126–130. 2008. View Article : Google Scholar : PubMed/NCBI | |
Di Liegro CM, Schiera G and Di Liegro I: Extracellular vesicle-associated RNA as a carrier of epigenetic information. Genes (Basel). 8:E2402017. View Article : Google Scholar : PubMed/NCBI | |
Hewson C, Capraro D, Burdach J, Whitaker N and Morris KV: Extracellular vesicle associated long non-coding RNAs functionally enhance cell viability. Noncoding RNA Res. 1:3–11. 2016. View Article : Google Scholar : PubMed/NCBI | |
Derrien T, Johnson R, Bussotti G, Tanzer A, Djebali S, Tilgner H, Guernec G, Martin D, Merkel A, Knowles DG, et al: The GENCODE v7 catalog of human long noncoding RNAs: Analysis of their gene structure, evolution, and expression. Genome Res. 22:1775–1789. 2012. View Article : Google Scholar : PubMed/NCBI | |
Yarmishyn AA and Kurochkin IV: Long noncoding RNAs: A potential novel class of cancer biomarkers. Front Genet. 6:1452015. View Article : Google Scholar : PubMed/NCBI | |
Shi T, Gao G and Cao Y: Long noncoding RNAs as novel biomarkers have a promising future in cancer diagnostics. Dis Markers. 2016:90851952016. View Article : Google Scholar : PubMed/NCBI | |
Akers JC, Gonda D, Kim R, Carter BS and Chen CC: Biogenesis of extracellular vesicles (EV): Exosomes, microvesicles, retrovirus-like vesicles, and apoptotic bodies. J Neurooncol. 113:1–11. 2013. View Article : Google Scholar : PubMed/NCBI | |
Silva A, Bullock M and Calin G: The clinical relevance of long non-coding RNAs in cancer. Cancers (Basel). 7:2169–2182. 2015. View Article : Google Scholar : PubMed/NCBI | |
Khurana R, Ranches G, Schafferer S, Lukasser M, Rudnicki M, Mayer G and Hüttenhofer A: Identification of urinary exosomal noncoding RNAs as novel biomarkers in chronic kidney disease. RNA. 23:142–152. 2017. View Article : Google Scholar : PubMed/NCBI | |
Takahashi K, Yan IK, Haga H and Patel T: Modulation of hypoxia-signaling pathways by extracellular linc-RoR. J Cell Sci. 127:1585–1594. 2014. View Article : Google Scholar : PubMed/NCBI | |
Gutschner T, Richtig G, Haemmerle M and Pichler M: From biomarkers to therapeutic targets-the promises and perils of long non-coding RNAs in cancer. Cancer Metastasis Rev. 37:83–105. 2018. View Article : Google Scholar : PubMed/NCBI | |
Rao AKDM, Rajkumar T and Mani S: Perspectives of long non-coding RNAs in cancer. Mol Boil Rep. 44:203–18. 2017. View Article : Google Scholar | |
Smaldone MC and Davies BJ: BC-819, a plasmid comprising the H19 gene regulatory sequences and diphtheria toxin A, for the potential targeted therapy of cancers. Curr Opin Mol Ther. 12:607–616. 2010.PubMed/NCBI | |
Liu J, Wan L, Lu K, Sun M, Pan X, Zhang P, Lu B, Liu G and Wang Z: The long noncoding RNA MEG3 contributes to cisplatin resistance of human lung adenocarcinoma. PLoS One. 10:e01145862015. View Article : Google Scholar : PubMed/NCBI | |
Wu R, Su Y, Wu H, Dai Y, Zhao M and Lu Q: Characters, functions and clinical perspectives of long non-coding RNAs. Mol Genet Genomics. 291:1013–1033. 2016. View Article : Google Scholar : PubMed/NCBI | |
Qi P, Zhou XY and Du X: Circulating long non-coding RNAs in cancer: Current status and future perspectives. Mol Cancer. 15:392016. View Article : Google Scholar : PubMed/NCBI | |
Schmidt O and Teis D: The ESCRT machinery. Curr Biol. 22:R116–R120. 2012. View Article : Google Scholar : PubMed/NCBI | |
Keller S, Sanderson MP, Stoeck A and Altevogt P: Exosomes: From biogenesis and secretion to biological function. Immunol Lett. 107:102–108. 2006. View Article : Google Scholar : PubMed/NCBI | |
Ruiz-Martinez M, Navarro A, Marrades RM, Vinolas N, Santasusagna S, Munoz C, Ramírez J, Molins L and Monzo M: YKT6 expression, exosome release, and survival in non-small cell lung cancer. Oncotarget. 7:51515–51524. 2016. View Article : Google Scholar : PubMed/NCBI | |
Hoshino A, Costa-Silva B, Shen TL, Rodrigues G, Hashimoto A, Tesic Mark M, Molina H, Kohsaka S, Di Giannatale A, Ceder S, et al: Tumour exosome integrins determine organotropic metastasis. Nature. 527:329–335. 2015. View Article : Google Scholar : PubMed/NCBI | |
Yang C and Robbins PD: The roles of tumor-derived exosomes in cancer pathogenesis. Clin Dev Immunol. 2011:8428492011. View Article : Google Scholar : PubMed/NCBI | |
Zhang A, Zhou N, Huang J, Liu Q, Fukuda K, Ma D, Lu Z, Bai C, Watabe K and Mo YY: The human long non-coding RNA-RoR is a p53 repressor in response to DNA damage. Cell Res. 23:340–350. 2013. View Article : Google Scholar : PubMed/NCBI | |
Qu L, Ding J, Chen C, Wu ZJ, Liu B, Gao Y, Chen W, Liu F, Sun W, Li XF, et al: Exosome-transmitted lncARSR promotes sunitinib resistance in renal cancer by acting as a competing endogenous RNA. Cancer Cell. 29:653–668. 2016. View Article : Google Scholar : PubMed/NCBI | |
Zhang J, Liu SC, Luo XH, Tao GX, Guan M, Yuan H and Hu DK: Exosomal long noncoding RNAs are differentially expressed in the cervicovaginal lavage samples of cervical cancer patients. J Clin Lab Anal. 30:1116–1121. 2016. View Article : Google Scholar : PubMed/NCBI | |
Zhang J, Yao T, Wang Y, Yu J, Liu Y and Lin Z: Long noncoding RNA MEG3 is downregulated in cervical cancer and affects cell proliferation and apoptosis by regulating miR-21. Cancer Boil Ther. 17:104–113. 2016. View Article : Google Scholar | |
Shao Y, Ye M, Li Q, Sun W, Ye G, Zhang X, Yang Y, Xiao B and Guo J: LncRNA-RMRP promotes carcinogenesis by acting as a miR-206 sponge and is used as a novel biomarker for gastric cancer. Oncotarget. 7:37812–37824. 2016. View Article : Google Scholar : PubMed/NCBI | |
Wang P, Wu T, Zhou H, Jin Q, He G, Yu H, Xuan L, Wang X, Tian L, Sun Y, et al: Long noncoding RNA NEAT1 promotes laryngeal squamous cell cancer through regulating miR-107/CDK6 pathway. J Exp Clin Cancer Res. 35:222016. View Article : Google Scholar : PubMed/NCBI | |
Xue M, Chen W, Xiang A, Wang R, Chen H, Pan J, Pang H, An H, Wang X, Hou H and Li X: Hypoxic exosomes facilitate bladder tumor growth and development through transferring long non-coding RNA-UCA1. Mol Cancer. 16:1432017. View Article : Google Scholar : PubMed/NCBI | |
Juni RP, Abreu RC and da Costa Martins PA: Regulation of microvascularization in heart failure-an endothelial cell, non-coding RNAs and exosome liaison. Noncoding RNA Res. 2:45–55. 2017. View Article : Google Scholar : PubMed/NCBI | |
Lu Z, Xiao Z, Liu F, Cui M, Li W, Yang Z, Li J, Ye L and Zhang X: Long non-coding RNA HULC promotes tumor angiogenesis in liver cancer by up-regulating sphingosine kinase 1 (SPHK1). Oncotarget. 7:241–254. 2016.PubMed/NCBI | |
Tan J, Qiu K, Li M and Liang Y: Double-negative feedback loop between long non-coding RNA TUG1 and miR-145 promotes epithelial to mesenchymal transition and radioresistance in human bladder cancer cells. FEBS Lett. 589:3175–3181. 2015. View Article : Google Scholar : PubMed/NCBI | |
Qin CF and Zhao FL: Long non-coding RNA TUG1 can promote proliferation and migration of pancreatic cancer via EMT pathway. Eur Rev Med Pharmacol Sci. 21:2377–2384. 2017.PubMed/NCBI | |
Li Z, Zhao L and Wang Q: Overexpression of long non-coding RNA HOTTIP increases chemoresistance of osteosarcoma cell by activating the Wnt/β-catenin pathway. Am J Transl Res. 8:2385–2393. 2016.PubMed/NCBI | |
Lang HL, Hu GW, Zhang B, Kuang W, Chen Y, Wu L and Xu GH: Glioma cells enhance angiogenesis and inhibit endothelial cell apoptosis through the release of exosomes that contain long non-coding RNA CCAT2. Oncol Rep. 38:785–798. 2017. View Article : Google Scholar : PubMed/NCBI | |
Liu T, Zhang X, Gao S, Jing F, Yang Y, Du L, Zheng G, Li P, Li C and Wang C: Exosomal long noncoding RNA CRNDE-h as a novel serum-based biomarker for diagnosis and prognosis of colorectal cancer. Oncotarget. 7:85551–85563. 2016. View Article : Google Scholar : PubMed/NCBI | |
Isin M, Uysaler E, Ozgur E, Koseoglu H, Sanli O, Yucel OB, Gezer U and Dalay N: Exosomal lncRNA-p21 levels may help to distinguish prostate cancer from benign disease. Front Genet. 6:1682015.PubMed/NCBI | |
Wang Y, Liu XJ and Yao XD: Function of PCA3 in prostate tissue and clinical research progress on developing a PCA3 score. Chin J Cancer Res. 26:493–500. 2014.PubMed/NCBI | |
Godinho M, Meijer D, Setyono-Han B, Dorssers LC and van Agthoven T: Characterization of BCAR4, a novel oncogene causing endocrine resistance in human breast cancer cells. J Cell Physiol. 226:1741–1749. 2011. View Article : Google Scholar : PubMed/NCBI | |
Jang SY, Kim G, Park SY, Lee YR, Kwon SH, Kim HS, Yoon JS, Lee JS, Kweon YO, Ha HT, et al: Clinical significance of lncRNA-ATB expression in human hepatocellular carcinoma. Oncotarget. 8:78588–78597. 2017. View Article : Google Scholar : PubMed/NCBI | |
Nie FQ, Sun M, Yang JS, Xie M, Xu TP, Xia R, Liu YW, Liu XH, Zhang EB, Lu KH and Shu YQ: Long noncoding RNA ANRIL promotes non-small cell lung cancer cell proliferation and inhibits apoptosis by silencing KLF2 and P21 expression. Mol Cancer Ther. 14:268–277. 2015. View Article : Google Scholar : PubMed/NCBI | |
Pang Q, Ge J, Shao Y, Sun W, Song H, Xia T, Xiao B and Guo J: Increased expression of long intergenic non-coding RNA LINC00152 in gastric cancer and its clinical significance. Tumour Biol. 35:5441–5447. 2014. View Article : Google Scholar : PubMed/NCBI | |
Xu N, Chen F, Wang F, Lu X, Wang X, Lv M and Lu C: Clinical significance of high expression of circulating serum lncRNA RP11-445H22.4 in breast cancer patients: A Chinese population-based study. Tumour Biol. 36:7659–7665. 2015. View Article : Google Scholar : PubMed/NCBI |