An emerging role of radiation‑induced exosomes in hepatocellular carcinoma progression and radioresistance (Review)
- Authors:
- Qing Fan
- Yue Yu
- Yueling Zhou
- Sheng Zhang
- Chunli Wu
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Affiliations: Department of General Surgery, The Fourth Affiliated Hospital of China Medical University, Shenyang, Liaoning 110032, P.R. China, Department of Radiation Oncology, The Fourth Affiliated Hospital of China Medical University, Shenyang, Liaoning 110032, P.R. China - Published online on: March 9, 2022 https://doi.org/10.3892/ijo.2022.5336
- Article Number: 46
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Copyright: © Fan et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
This article is mentioned in:
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 |
|
Llovet JM, Zucman-Rossi J, Pikarsky E, Sangro B, Schwartz M, Sherman M and Gores G: Hepatocellular carcinoma. Nat Rev Dis Primers. 2:160182016. View Article : Google Scholar : PubMed/NCBI | |
|
Villanueva A: Hepatocellular carcinoma. N Engl J Med. 380:1450–1462. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Nair H, Simoes EA, Rudan I, Gessner BD, Azziz-Baumgartner E, Zhang JSF, Feikin DR, Mackenzie GA, Moiïsi JC, Roca A, et al: Global and regional burden of hospital admissions for severe acute lower respiratory infections in young children in 2010: A systematic analysis. Lancet. 381:1380–1390. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Global Burden of Disease Liver Cancer Collaboration; Akinyemiju T, Abera S, Ahmed M, Alam N, Alemayohu MA, Allen C, Al-Raddadi R, Alvis-Guzman N, Amoako Y, et al: The burden of primary liver cancer and underlying etiologies from 1990 to 2015 at the global, regional, and national level: Results from the global burden of disease study 2015. JAMA Oncol. 3:1683–1691. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Llovet JM, Kelley RK, Villanueva A, Singal AG, Pikarsky E, Roayaie S, Lencioni R, Koike K, Zucman-Rossi J and Finn RS: Hepatocellular carcinoma. Nat Rev Dis Primers. 7:62021. View Article : Google Scholar : PubMed/NCBI | |
|
Liu J and Fan D: Hepatitis B in China. Lancet. 369:1582–1583. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Laursen L: A preventable cancer. Nature. 516:S2–S3. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
European Association for the study of the Liver and European Organisation for research and treatment of Cancer: EASL-EORTC clinical practice guidelines: Management of hepatocellular carcinoma. J Hepatol. 56:908–943. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Ishizawa T, Hasegawa K, Aoki T, Takahashi M, Inoue Y, Sano K, Imamura H, Sugawara Y, Kokudo N and Makuuchi M: Neither multiple tumors nor portal hypertension are surgical contraindications for hepatocellular carcinoma. Gastroenterology. 134:1908–1916. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Yu Y and Feng M: Radiotherapy for hepatocellular carcinoma. Semin Radiat Oncol. 28:277–287. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Bang A and Dawson LA: Radiotherapy for HCC: Ready for prime time? JHEP Rep. 1:131–137. 2019. View Article : Google Scholar | |
|
Ohri N, Dawson LA, Krishnan S, Seong J, Cheng JC, Sarin SK, Kinkhabwala M, Ahmed MM, Vikram B, Coleman CN and Guha C: Radiotherapy for hepatocellular carcinoma: New indications and directions for future study. J Natl Cancer Inst. 108:djw1332016. View Article : Google Scholar : PubMed/NCBI | |
|
Ni J, Bucci J, Malouf D, Knox M, Graham P and Li Y: Exosomes in cancer radioresistance. Front Oncol. 9:8692019. View Article : Google Scholar : PubMed/NCBI | |
|
Barker HE, Paget JT, Khan AA and Harrington KJ: The tumour microenvironment after radiotherapy: Mechanisms of resistance and recurrence. Nat Rev Cancer. 15:409–425. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Chan R, Sethi P, Jyoti A, McGarry R and Upreti M: Investigating the radioresistant properties of lung cancer stem cells in the context of the tumor microenvironment. Radiat Res. 185:169–181. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Swartz MA, Iida N, Roberts EW, Sangaletti S, Wong MH, Yull FE, Coussens LM and DeClerck YA: Tumor microenvironment complexity: Emerging roles in cancer therapy. Cancer Res. 72:2473–2480. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Son B, Lee S, Youn H, Kim E, Kim W and Youn B: The role of tumor microenvironment in therapeutic resistance. Oncotarget. 8:3933–3945. 2017. View Article : Google Scholar : | |
|
Kalluri R and LeBleu VS: The biology, function, and biomedical applications of exosomes. Science. 367:eaau69772020. View Article : Google Scholar : | |
|
Jeppesen DK, Fenix AM, Franklin JL, Higginbotham JN, Zhang Q, Zimmerman LJ, Liebler DC, Ping J, Liu Q, Evans R, et al: Reassessment of exosome composition. Cell. 177:428–445.e18. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Tai YL, Chen KC, Hsieh JT and Shen TL: Exosomes in cancer development and clinical applications. Cancer Sci. 109:2364–2374. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Dai J, Su Y, Zhong S, Cong L, Liu B, Yang J, Tao Y, He Z, Chen C and Jiang Y: Exosomes: Key players in cancer and potential therapeutic strategy. Signal Transduct Target Ther. 5:1452020. View Article : Google Scholar : PubMed/NCBI | |
|
van Niel G, D'Angelo G and Raposo G: Shedding light on the cell biology of extracellular vesicles. Nat Rev Mol Cell Biol. 19:213–228. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Sato S, Zhu XL and Sly WS: Carbonic anhydrase Isozymes IV and II in urinary membranes from carbonic anhydrase II-deficient patients. Proc Natl Acad Sci USA. 87:6073–6076. 1990. View Article : Google Scholar : PubMed/NCBI | |
|
Zhang L and Yu D: Exosomes in cancer development, metastasis, and immunity. Biochim Biophys Acta Rev Cancer. 1871:455–468. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Pegtel DM and Gould SJ: Exosomes. Annu Rev Biochem. 88:487–514. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Chen W, Mao Y, Liu C, Wu H and Chen S: Exosome in hepatocellular carcinoma: An update. J Cancer. 12:2526–2536. 2021. View Article : Google Scholar : PubMed/NCBI | |
|
Wang HB, Lu ZM and Zhao XX: Tumorigenesis, diagnosis, and therapeutic potential of exosomes in liver cancer. J Hematol Oncol. 12:1332019. View Article : Google Scholar : PubMed/NCBI | |
|
Keerthikumar S, Chisanga D, Ariyaratne D, Al Saffar H, Anand S, Zhao K, Samuel M, Pathan M, Jois M, Chilamkurti N, et al: ExoCarta: A Web-Based compendium of exosomal cargo. J Mol Biol. 428:688–692. 2016. View Article : Google Scholar : | |
|
Nabet BY, Qiu Y, Shabason JE, Wu TJ, Yoon T, Kim BC, Benci JL, DeMichele AM, Tchou J, Marcotrigiano J and Minn AJ: Exosome RNA unshielding couples stromal activation to pattern recognition receptor signaling in cancer. Cell. 170:352–366.e13. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Li I and Nabet BY: Exosomes in the tumor microenvironment as mediators of cancer therapy resistance. Mol Cancer. 18:322019. 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 | |
|
Ridder K, Keller S, Dams M, Rupp AK, Schlaudraff J, Del Turco D, Starmann J, Macas J, Karpova D, Devraj K, et al: Extracellular vesicle-mediated transfer of genetic information between the hematopoietic system and the brain in response to inflammation. PLoS Biol. 12:–e1001874. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Skotland T, Sandvig K and Llorente A: Lipids in exosomes: Current knowledge and the way forward. Prog Lipid Res. 66:30–41. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Li WH, Li CY, Zhou T, Liu X, Liu X, Li X and Chen D: Role of exosomal proteins in cancer diagnosis. Mol Cancer. 16:1452017. View Article : Google Scholar : PubMed/NCBI | |
|
Cai J, Han Y, Ren HM, Chen C, He D, Zhou L, Eisner GM, Asico LD, Jose PA and Zeng C: Extracellular vesicle-mediated transfer of donor genomic DNA to recipient cells is a novel mechanism for genetic influence between cells. J Mol Cell Biol. 5:227–238. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Thakur BK, Zhang H, Becker A, Matei I, Huang Y, Costa-Silva B, Zheng Y, Hoshino A, Brazier H, Xiang J, et al: Double-stranded DNA in exosomes: A novel biomarker in cancer detection. Cell Res. 24:766–769. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Wong CM, Tsang FHC and Ng IOL: Non-coding RNAs in hepatocellular carcinoma: Molecular functions and pathological implications. Nat Rev Gastro Hepat. 15:137–151. 2018. View Article : Google Scholar | |
|
He M, Qin H, Poon TC, Sze SC, Ding X, Co NN, Ngai SM, Chan TF and Wong N: Hepatocellular carcinoma-derived exosomes promote motility of immortalized hepatocyte through transfer of oncogenic proteins and RNAs. Carcinogenesis. 36:1008–1018. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Wang S, Xu M, Li X, Su X, Xiao X, Keating A and Zhao RC: Exosomes released by hepatocarcinoma cells endow adipocytes with tumor-promoting properties. J Hematol Oncol. 11:822018. View Article : Google Scholar : PubMed/NCBI | |
|
Lee HY, Chen CK, Ho CM, Lee SS, Chang CY, Chen KJ and Jou YS: EIF3C-enhanced exosome secretion promotes angiogenesis and tumorigenesis of human hepatocellular carcinoma. Oncotarget. 9:13193–13205. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Wang S, Chen G, Lin X, Xing X, Cai Z, Liu X and Liu J: Role of exosomes in hepatocellular carcinoma cell mobility alteration. Oncol Lett. 14:8122–8131. 2017.PubMed/NCBI | |
|
Zhang J, Lu S, Zhou Y, Meng K, Chen Z, Cui Y, Shi Y, Wang T and He QY: Motile hepatocellular carcinoma cells preferentially secret sugar metabolism regulatory proteins via exosomes. Proteomics. 17:17001032017. View Article : Google Scholar | |
|
Conde-Vancells J, Rodriguez-Suarez E, Gonzalez E, Berisa A, Gil D, Embade N, Valle M, Luka Z, Elortza F, Wagner C, et al: Candidate biomarkers in exosome-like vesicles purified from rat and mouse urine samples. Proteom Clin Appl. 4:416–425. 2010. View Article : Google Scholar | |
|
Fu Q, Zhang Q, Lou Y, Yang J, Nie G, Chen Q, Chen Y, Zhang J, Wang J, Wei T, et al: Primary tumor-derived exosomes facilitate metastasis by regulating adhesion of circulating tumor cells via SMAD3 in liver cancer. Oncogene. 37:6105–6118. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Ye L, Zhang Q, Cheng Y, Chen X, Wang G, Shi M, Zhang T, Cao Y, Pan H, Zhang L, et al: Tumor-derived exosomal HMGB1 fosters hepatocellular carcinoma immune evasion by promoting TIM-1 + regulatory B cell expansion. J Immunother Cancer. 6:1452018. View Article : Google Scholar | |
|
Wang X, Shen H, Zhangyuan G, Huang R, Zhang W, He Q, Jin K, Zhuo H, Zhang Z, Wang J, et al: 14-3-3ζ delivered by hepatocellular carcinoma-derived exosomes impaired anti-tumor function of tumor-infiltrating T lymphocytes. Cell Death Dis. 9:1592018. View Article : Google Scholar | |
|
Li M, Lu Y, Xu Y, Wang J, Zhang C, Du Y, Wang L, Li L, Wang B, Shen J, et al: Horizontal transfer of exosomal CXCR4 promotes murine hepatocarcinoma cell migration, invasion and lymphangiogenesis. Gene. 676:101–109. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Dai WJ, Wang YL, Yang TX, Wang J, Wu WC and Gu JX: Downregulation of exosomal CLEC3B in hepatocellular carcinoma promotes metastasis and angiogenesis via AMPK and VEGF signals. Cell Commun Signal. 17:1132019. View Article : Google Scholar : PubMed/NCBI | |
|
Qiu QC, Wang L, Jin SS, Liu GF, Liu J, Ma L, Mao RF, Ma YY, Zhao N, Chen M and Lin BY: CHI3L1 promotes tumor progression by activating TGF-β signaling pathway in hepatocellular carcinoma. Sci Rep. 8:150292018. View Article : Google Scholar | |
|
Gai X, Tang B, Liu F, Wu Y, Wang F, Jing Y, Huang F, Jin D, Wang L and Zhang H: mTOR/miR-145-regulated exosomal GOLM1 promotes hepatocellular carcinoma through augmented GSK-3 beta/MMPs. J Genet Genomics. 46:235–245. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Skotland T, Sagini K, Sandvig K and Llorente A: An emerging focus on lipids in extracellular vesicles. Adv Drug Deliv Rev. 159:308–321. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Skotland T, Ekroos K, Kauhanen D, Simolin H, Seierstad T, Berge V, Sandvig K and Llorente A: Molecular lipid species in urinary exosomes as potential prostate cancer biomarkers. Eur J Cancer. 70:122–132. 2017. View Article : Google Scholar | |
|
Lydic TA, Townsend S, Adda CG, Collins C, Mathivanan S and Reid GE: Rapid and comprehensive 'Shotgun' lipidome profiling of colorectal cancer cell derived exosomes. Methods. 87:83–95. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Trajkovic K, Hsu C, Chiantia S, Rajendran L, Wenzel D, Wieland F, Schwille P, Brügger B and Simons M: Ceramide triggers budding of exosome vesicles into multivesicular Endosomes. Science. 319:1244–1247. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Chapuy-Regaud S, Dubois M, Plisson-Chastang C, Bonnefois T, Lhomme S, Bertrand-Michel J, You B, Simoneau S, Gleizes PE, Flan B, et al: Characterization of the lipid envelope of exosome encapsulated HEV particles protected from the immune response. Biochimie. 141:70–79. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Haraszti RA, Didiot MC, Sapp E, Leszyk J, Shaffer SA, Rockwell HE, Gao F, Narain NR, DiFiglia M, Kiebish MA, et al: High-resolution proteomic and lipidomic analysis of exosomes and microvesicles from different cell sources. J Extracell Vesicles. 5:325702016. View Article : Google Scholar : PubMed/NCBI | |
|
Sadovska L, Eglitis J and Line A: Extracellular vesicles as biomarkers and therapeutic targets in breast cancer. Anticancer Res. 35:6379–6390. 2015.PubMed/NCBI | |
|
Alix-Panabieres C and Pantel K: Clinical applications of circulating tumor cells and circulating tumor DNA as liquid biopsy. Cancer Discov. 6:479–491. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Li X, Li C, Zhang L, Wu M, Cao K, Jiang F, Chen D, Li N and Li W: The significance of exosomes in the development and treatment of hepatocellular carcinoma. Mol Cancer. 19:12020. View Article : Google Scholar : PubMed/NCBI | |
|
Bernard V, Kim DU, San Lucas FA, Castillo J, Allenson K, Mulu FC, Stephens BM, Huang J, Semaan A, Guerrero PA, et al: Circulating nucleic acids are associated with outcomes of patients with pancreatic cancer. Gastroenterology. 156:108–118.e4. 2019. View Article : Google Scholar | |
|
Yan LL, Chen YH, Zhou JY, Zhao H, Zhang HH and Wang GQ: Diagnostic value of circulating cell-free DNA levels for hepatocellular carcinoma. Int J Infect Dis. 67:92–97. 2018. View Article : Google Scholar | |
|
Slack FJ and Chinnaiyan AM: The role of Non-coding RNAs in oncology. Cell. 179:1033–1055. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Ambros V: The functions of animal microRNAs. Nature. 431:350–355. 2004. View Article : Google Scholar : PubMed/NCBI | |
|
Bartel DP: MicroRNAs: Genomics, biogenesis, mechanism, and function. Cell. 116:281–297. 2004. View Article : Google Scholar : PubMed/NCBI | |
|
Vickers KC, Palmisano BT, Shoucri BM, Shamburek RD and Remaley AT: MicroRNAs are transported in plasma and delivered to recipient cells by high-density lipoproteins. Nat Cell Biol. 13:423–433. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Arroyo JD, Chevillet JR, Kroh EM, Ruf IK, Pritchard CC, Gibson DF, Mitchell PS, Bennett CF, Pogosova-Agadjanyan EL, Stirewalt DL, et al: Argonaute2 complexes carry a population of circulating microRNAs independent of vesicles in human plasma. Proc Natl Acad Sci USA. 108:5003–5008. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Zhang J, Li S, Li L, Li M, Guo C, Yao J and Mi S: Exosome and exosomal MicroRNA: Trafficking, sorting, and function. Genom Proteom Bioinf. 13:17–24. 2015. View Article : Google Scholar | |
|
Croce CM: Causes and consequences of microRNA dysregulation in cancer. Nat Rev Genet. 10:704–714. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Lee YR, Kim G, Tak WY, Jang SY, Kweon YO, Park JG, Lee HW, Han YS, Chun JM, Park SY and Hur K: Circulating exosomal noncoding RNAs as prognostic biomarkers in human hepatocellular carcinoma. Int J Cancer. 144:1444–1452. 2019. View Article : Google Scholar | |
|
Tian XP, Wang CY, Jin XH, Li M, Wang FW, Huang WJ, Yun JP, Xu RH, Cai QQ and Xie D: Acidic microenvironment Up-Regulates exosomal miR-21 and miR-10b in early-stage hepatocellular carcinoma to promote cancer cell proliferation and metastasis. Theranostics. 9:1965–1979. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Lin XJ, Chong YT, Guo ZW, Xie C, Yang XJ, Zhang Q, Li SP, Xiong Y, Yuan Y, Min J, et al: A serum microRNA classifier for early detection of hepatocellular carcinoma: A multicentre, retrospective, longitudinal biomarker identification study with a nested case-control study. Lancet Oncol. 16:804–815. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Lin XJ, Fang JH, Yang XJ, Zhang C, Yuan Y, Zheng L and Zhuang SM: Hepatocellular carcinoma cell-secreted exosomal MicroRNA-210 promotes angiogenesis in vitro and in vivo. Mol Ther Nucleic Acids. 11:243–252. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Cui Y, Xu HF, Liu MY, Xu YJ, He JC, Zhou Y and Cang SD: Mechanism of exosomal microRNA-224 in development of hepatocellular carcinoma and its diagnostic and prognostic value. World J Gastroentero. 25:1890–1898. 2019. View Article : Google Scholar | |
|
Statello L, Guo CJ, Chen LL and Huarte M: Gene regulation by long non-coding RNAs and its biological functions. Nat Rev Mol Cell Biol. 22:96–118. 2021. View Article : Google Scholar | |
|
Pathania AS and Challagundla KB: Exosomal long Non-coding RNAs: Emerging players in the tumor microenvironment. Mol Ther Nucleic Acids. 23:1371–1383. 2021. View Article : Google Scholar : PubMed/NCBI | |
|
Prensner JR and Chinnaiyan AM: The Emergence of lncRNAs in cancer biology. Cancer Discov. 1:391–407. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Bolha L, Ravnik-Glavac M and Glavac D: Long noncoding RNAs as biomarkers in cancer. Dis Markers. 2017:2017. 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 | |
|
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 | |
|
Chen SY, Teng SC, Cheng TH and Wu KJ: miR-1236 regulates hypoxia-induced epithelial-mesenchymal transition and cell migration/invasion through repressing SENP1 and HDAC3. Cancer Lett. 378:59–67. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Li BG, Mao R, Liu CF, Zhang WH, Tang Y and Guo Z: LncRNA FAL1 promotes cell proliferation and migration by acting as a CeRNA of miR-1236 in hepatocellular carcinoma cells. Life Sci. 197:122–129. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Yao ZC, Jia CC, Tai Y, Liang H, Zhong Z, Xiong Z, Deng M and Zhang Q: Serum exosomal long noncoding RNAs lnc-FAM72D3 and lnc-EPC14 as diagnostic biomarkers for hepatocellular carcinoma. Aging (Albany NY). 12:11843–11863. 2020. View Article : Google Scholar | |
|
Hou YC, Yu Z, Tam NL, Huang S, Sun C, Wang R, Zhang X, Wang Z, Ma Y, He X and Wu L: Exosome-related lncRNAs as predictors of HCC patient survival: A prognostic model. Am J Transl Res. 10:1648–1662. 2018.PubMed/NCBI | |
|
Zhang C, Yang X, Qi Q, Gao YH, Wei Q and Han SW: lncRNA-HEIH in serum and exosomes as a potential biomarker in the HCV-related hepatocellular carcinoma. Cancer Biomark. 21:651–659. 2018. View Article : Google Scholar | |
|
Xu H, Chen YM, Dong XY and Wang XJ: Serum exosomal long noncoding RNAs ENSG00000258332.1 and LINC00635 for the diagnosis and prognosis of hepatocellular carcinoma. Cancer Epidem Biomar. 27:710–716. 2018. View Article : Google Scholar | |
|
Sun L, Su Y, Liu X, Xu M, Chen X, Zhu Y, Guo Z, Bai T, Dong L, Wei C, et al: Serum and exosome long non coding RNAs as potential biomarkers for hepatocellular carcinoma. J Cancer. 9:2631–2639. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Ma X, Yuan T, Yang C, Wang Z, Zang Y, Wu L and Zhuang L: X-inactive-specific transcript of peripheral blood cells is regulated by exosomal Jpx and acts as a biomarker for female patients with hepatocellular carcinoma. Ther Adv Med Oncol. 9:665–677. 2017. View Article : Google Scholar | |
|
Zhuang LK, Yang YT, Ma X, Han B, Wang ZS, Zhao QY, Wu LQ and Qu ZQ: MicroRNA-92b promotes hepatocellular carcinoma progression by targeting Smad7 and is mediated by long non-coding RNA XIST. Cell Death Dis. 7:e22032016. 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 | |
|
Li X, Lei Y, Wu M and Li N: Regulation of macrophage activation and polarization by HCC-Derived Exosomal lncRNA TUC339. Int J Mol Sci. 19:29582018. View Article : Google Scholar : | |
|
Ma D, Gao X, Liu Z, Lu X, Ju H and Zhang N: Exosome-transferred long non-coding RNA ASMTL-AS1 contributes to malignant phenotypes in residual hepatocellular carcinoma after insufficient radiofrequency ablation. Cell Prolif. 53:e127952020. View Article : Google Scholar : PubMed/NCBI | |
|
Wang D, Xing N, Yang T, Liu J, Zhao H, He J, Ai Y and Yang J: Exosomal lncRNA H19 promotes the progression of hepatocellular carcinoma treated with Propofol via miR-520a-3p/LIMK1 axis. Cancer Med. 9:7218–7230. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Ji JF, Yamashita T, Budhu A, Forgues M, Jia HL, Li C, Deng C, Wauthier E, Reid LM, Ye QH, et al: Identification of MicroRNA-181 by genome-wide screening as a critical player in EpCAM-Positive hepatic cancer stem cells. Hepatology. 50:472–480. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Sanger HL, Klotz G, Riesner D, Gross HJ and Kleinschmidt AK: Viroids are single-stranded covalently closed circular RNA molecules existing as highly base-paired rod-like structures. Proc Natl Acad Sci USA. 73:3852–3856. 1976. View Article : Google Scholar : PubMed/NCBI | |
|
Seimiya T, Otsuka M, Iwata T, Shibata C, Tanaka E, Suzuki T and Koike K: Emerging roles of exosomal circular RNAs in cancer. Front Cell Dev Biol. 8:5683662020. View Article : Google Scholar : PubMed/NCBI | |
|
Wang Y, Liu J, Ma J, Sun T, Zhou Q, Wang W, Wang G, Wu P, Wang H, Jiang L, et al: Exosomal circRNAs: Biogenesis, effect and application in human diseases. Mol Cancer. 18:1162019. View Article : Google Scholar : PubMed/NCBI | |
|
Wilusz JE and Sharp PA: Molecular biology. A circuitous route to noncoding RNA. Science. 340:440–441. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Li SS, Yao JP, Xie MJ, Liu YN and Zheng M: Exosomal miRNAs in hepatocellular carcinoma development and clinical responses. J Hematol Oncol. 11:542018. View Article : Google Scholar : PubMed/NCBI | |
|
Geng X, Lin X, Zhang Y, Li Q, Guo Y, Fang C and Wang H: Exosomal circular RNA sorting mechanisms and their function in promoting or inhibiting cancer. Oncol Lett. 19:3369–3380. 2020.PubMed/NCBI | |
|
Zhang H, Deng T, Ge S, Liu Y, Bai M, Zhu K, Fan Q, Li J, Ning T, Tian F, et al: Exosome circRNA secreted from adipocytes promotes the growth of hepatocellular carcinoma by targeting deubiquitination-related USP7. Oncogene. 38:2844–2859. 2019. View Article : Google Scholar : | |
|
Chen W, Quan Y, Fan S, Wang H, Liang J, Huang L, Chen L, Liu Q, He P and Ye Y: Exosome-transmitted circular RNA hsa_ circ_0051443 suppresses hepatocellular carcinoma progression. Cancer Lett. 475:119–128. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Zhang PF, Wei CY, Huang XY, Peng R, Yang X, Lu JC, Zhang C, Gao C, Cai JB, Gao PT, et al: Circular RNA circTRIM33-12 acts as the sponge of MicroRNA-191 to suppress hepatocellular carcinoma progression. Mol Cancer. 18:1052019. View Article : Google Scholar : PubMed/NCBI | |
|
Chen SP, Liu BX, Xu J, Pei XF, Liao YJ, Yuan F and Zheng F: MiR-449a suppresses the epithelial-mesenchymal transition and metastasis of hepatocellular carcinoma by multiple targets. BMC Cancer. 15:7062015. View Article : Google Scholar : PubMed/NCBI | |
|
Wang GY, Liu W, Zou Y, Wang G, Deng Y, Luo J, Zhang Y, Li H, Zhang Q, Yang Y and Chen G: Three isoforms of exosomal circPTGR1 promote hepatocellular carcinoma metastasis via the miR449a-MET pathway. EBioMedicine. 40:432–445. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Zhang TT, Jing B, Bai YX, Zhang Y and Yu HY: Circular RNA circTMEM45A Acts as the Sponge of MicroRNA-665 to promote hepatocellular carcinoma progression. Mol Ther Nucleic Acids. 22:285–297. 2020. View Article : Google Scholar : PubMed/NCBI | |
|
Shyu AB, Wilkinson MF and van Hoof A: Messenger RNA regulation: To translate or to degrade. Embo J. 27:471–481. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Yu SL, Li YC, Liao Z, Wang Z, Wang Z, Li Y, Qian L, Zhao J, Zong H, Kang B, et al: Plasma extracellular vesicle long RNA profiling identifies a diagnostic signature for the detection of pancreatic ductal adenocarcinoma. Gut. 69:540–550. 2020. View Article : Google Scholar | |
|
Li Y, Zhao J, Yu S, Wang Z, He X, Su Y, Guo T, Sheng H, Chen J, Zheng Q, et al: Extracellular vesicles long RNA sequencing reveals abundant mRNA, circRNA, and lncRNA in human blood as potential biomarkers for cancer diagnosis. Clin Chem. 65:798–808. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Abd El Gwad A, Matboli M, El-Tawdi A, Habib EK, Shehata H, Ibrahim D and Tash F: Role of exosomal competing endogenous RNA in patients with hepatocellular carcinoma. J Cell Biochem. 119:8600–8610. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Xu H, Dong XY, Chen YM and Wang XJ: Serum exosomal hnRNPH1 mRNA as a novel marker for hepatocellular carci-noma. Clin Chem Lab Med. 56:479–484. 2018. View Article : Google Scholar | |
|
He R, Wang Z, Shi W, Yu L, Xia H, Huang Z, Liu S, Zhao X, Xu Y, Yam JWP and Cui Y: Exosomes in hepatocellular carcinoma microenvironment and their potential clinical application value. Biomed Pharmacother. 138:1115292021. View Article : Google Scholar : PubMed/NCBI | |
|
Pascut D, Pratama MY, Vo NVT, Masadah R and Tiribelli C: The Crosstalk between tumor cells and the microenvironment in hepatocellular carcinoma: The role of exosomal microRNAs and their clinical implications. Cancers (Basel). 12:8232020. View Article : Google Scholar | |
|
Wu Q, Zhou L, Lv D, Zhu X and Tang H: Exosome-mediated communication in the tumor microenvironment contributes to hepatocellular carcinoma development and progression. J Hematol Oncol. 12:532019. View Article : Google Scholar : PubMed/NCBI | |
|
Chen X, Chi H, Zhao X, Pan R, Wei Y and Han Y: Role of exosomes in immune microenvironment of hepatocellular carcinoma. J Oncol. 2022:25210252022. View Article : Google Scholar : PubMed/NCBI | |
|
Chen C, Luo F, Liu X, Lu L, Xu H, Yang Q, Xue J, Shi L, Li J, Zhang A and Liu Q: NF-kB-regulated exosomal miR-155 promotes the inflammation associated with arsenite carcinogenesis. Cancer Lett. 388:21–33. 2017. View Article : Google Scholar | |
|
Fang T, Lv H, Lv G, Li T, Wang C, Han Q, Yu L, Su B, Guo L, Huang S, et al: Tumor-derived exosomal miR-1247-3p induces cancer-associated fibroblast activation to foster lung metastasis of liver cancer. Nat Commun. 9:1912018. View Article : Google Scholar : PubMed/NCBI | |
|
Zhang Z, Li X, Sun W, Yue S, Yang J, Li J, Ma B, Wang J, Yang X, Pu M, et al: Loss of exosomal miR-320a from cancer-associated fibroblasts contributes to HCC proliferation and metastasis. Cancer Lett. 397:33–42. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Goessler UR, Hormann K and Riedel F: Tissue engineering with chondrocytes and function of the extracellular matrix (Review). Int J Mol Med. 13:505–513. 2004.PubMed/NCBI | |
|
Yáñez-Mó M, Siljander PR, Andreu Z, Zavec AB, Borràs FE, Buzas EI, Buzas K, Casal E, Cappello F, Carvalho J, et al: Biological properties of extracellular vesicles and their physiological functions. J Extracell Vesicles. 4:270662015. View Article : Google Scholar : PubMed/NCBI | |
|
Herrera MB, Fonsato V, Gatti S, Deregibus MC, Sordi A, Cantarella D, Calogero R, Bussolati B, Tetta C and Camussi G: Human liver stem cell-derived microvesicles accelerate hepatic regeneration in hepatectomized rats. J Cell Mol Med. 14:1605–1618. 2010. View Article : Google Scholar | |
|
Fonsato V, Collino F, Herrera MB, Cavallari C, Deregibus MC, Cisterna B, Bruno S, Romagnoli R, Salizzoni M, Tetta C and Camussi G: Human liver stem cell-derived microvesicles inhibit hepatoma growth in SCID mice by delivering antitumor microRNAs. Stem Cells. 30:1985–1998. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Fabregat I, Roncero C and Fernandez M: Survival and apoptosis: A dysregulated balance in liver cancer. Liver Int. 27:155–162. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Kountouras J, Zavos C and Chatzopoulos D: Apoptosis in hepatocellular carcinoma. Hepatogastroenterology. 50:242–249. 2003.PubMed/NCBI | |
|
Thery C, Witwer KW, Aikawa E, Alcaraz MJ, Anderson JD, Andriantsitohaina R, Antoniou A, Arab T, Archer F, Atkin-Smith GK, et al: Minimal information for studies of extra-cellular vesicles 2018 (MISEV2018): A position statement of the International Society for Extracellular Vesicles and update of the MISEV2014 guidelines. J Extracell Vesicles. 7:15357502018. View Article : Google Scholar | |
|
McAndrews KM and Kalluri R: Mechanisms associated with biogenesis of exosomes in cancer. Mol Cancer. 18:522019. View Article : Google Scholar : PubMed/NCBI | |
|
Sasaki R, Kanda T, Yokosuka O, Kato N, Matsuoka S and Moriyama M: Exosomes and hepatocellular carcinoma: From bench to bedside. Int J Mol Sci. 20:14062019. View Article : Google Scholar : | |
|
Hennequin C, Quero L and Rivera S: Radiosensitivity of hepatocellular carcinoma. Cancer Radiother. 15:39–42. 2011.In French. View Article : Google Scholar : PubMed/NCBI |
