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Review

Exosomes as Crucial Emerging Tools for Intercellular Communication with Therapeutic Potential in Ovarian Cancer

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Article: FSO833 | Received 09 Jun 2022, Accepted 15 Feb 2023, Published online: 06 Mar 2023

References

  • LePage C , ProvencherD , MaugardCM , OuelletV , Mes-MassonA-M. Signature of a silent killer: expression profiling in epithelial ovarian cancer. Expert Rev. Mol. Diagn.4(2), 157–167 (2004).
  • CoticchiaCM , YangJ , MosesMA. Ovarian cancer biomarkers: current options and future promise. J. Natl Compr. Canc. Netw.6(8), 795–802 (2008).
  • ReidBM , PermuthJB , SellersTA. Epidemiology of ovarian cancer: a review. Cancer Biol. Med.14(1), 9–32 (2017).
  • MatulonisUA , SoodAK , FallowfieldL , HowittBE , SehouliJ , KarlanBY. Ovarian cancer. Nat. Rev. Dis. Primer.2, 16061 (2016).
  • AgarwalR , KayeSB. Ovarian cancer: strategies for overcoming resistance to chemotherapy. Nat. Rev. Cancer.3(7), 502–516 (2003).
  • SankaranarayananR , FerlayJ. Worldwide burden of gynaecological cancer: the size of the problem. Best Pract. Res. Clin. Obstet. Gynaecol.20(2), 207–225 (2006).
  • SungH , FerlayJ , SiegelRLet al.Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J. Clin.71(3), 209–249 Doi: 10.3322/caac.21660 (2021).
  • KurmanRJ , ShihI-M. The origin and pathogenesis of epithelial ovarian cancer: a proposed unifying theory. Am. J. Surg. Pathol.34(3), 433–443 (2010).
  • BristowRE , KarlanBY , ChiDS. Surgery for Ovarian Cancer: Principles and Practice.CRC Press, London (2010).
  • TorreLA , TrabertB , DeSantisCEet al.Ovarian cancer statistics, 2018: Ovarian Cancer Statistics, 2018. CA Cancer J. Clin.68(4), 284–296 (2018).
  • ShenJ , ZhuX , FeiJ , ShiP , YuS , ZhouJ. Advances of exosome in the development of ovarian cancer and its diagnostic and therapeutic prospect. OncoTargets Ther.11, 2831–2841 (2018).
  • ZhangW , PengP , OuX , ShenK , WuX. Ovarian cancer circulating extracelluar vesicles promote coagulation and have a potential in diagnosis: an iTRAQ based proteomic analysis. BMC Cancer19(1), 1095 (2019).
  • JacobsI , BastRC. The CA 125 tumour-associated antigen: a review of the literature. Hum. Reprod. Oxf. Engl.4(1), 1–12 (1989).
  • DaoudE , BodorG. CA-125 concentrations in malignant and nonmalignant disease. Clin. Chem.37(11), 1968–1974 (1991).
  • CollinsWP , BourneTH , CampbellS. Screening strategies for ovarian cancer. Curr. Opin. Obstet. Gynecol.10(1), 33–39 (1998).
  • KitawakiJ , IshiharaH , KoshibaHet al.Usefulness and limits of CA-125 in diagnosis of endometriosis without associated ovarian endometriomas. Hum. Reprod. Oxf. Engl.20(7), 1999–2003 (2005).
  • Van GorpT , CadronI , DespierreEet al.HE4 and CA125 as a diagnostic test in ovarian cancer: prospective validation of the risk of ovarian malignancy algorithm. Br. J. Cancer104(5), 863–870 (2011).
  • SarojiniS , TamirA , LimHet al.Early detection biomarkers for ovarian cancer. J. Oncol.2012, 709049 (2012).
  • MooreRG , MillerMC , SteinhoffMMet al.Serum HE4 levels are less frequently elevated than CA125 in women with benign gynecologic disorders. Am. J. Obstet. Gynecol.206(4), 351.e1–351.e8 (2012).
  • Norouzi-BaroughL , SarookhaniMR , SharifiM , MoghbelinejadS , JangjooS , SalehiR. Molecular mechanisms of drug resistance in ovarian cancer. J. Cell. Physiol.233(6), 4546–4562 (2018).
  • DoubeniCA , DoubeniAR , MyersAE. Diagnosis and management of ovarian cancer. Am. Fam. Physician93(11), 937–944 (2016).
  • Ovarian Cancer – Cancer Stat Facts [ Internet]. Available from: https://seer.cancer.gov/statfacts/html/ovary.html
  • AlharbiM , ZuñigaF , ElfekyOet al.The potential role of miRNAs and exosomes in chemotherapy in ovarian cancer. Endocr. Relat. Cancer.25(12), R663–R685 (2018).
  • ChenM , JinY , BiY , YinJ , WangY , PanL. A survival analysis comparing women with ovarian low-grade serous carcinoma to those with high-grade histology. OncoTargets Ther.7, 1891–1899 (2014).
  • KurmanRJ , ShihI-M. The Dualistic Model of Ovarian Carcinogenesis. Am. J. Pathol.186(4), 733–747 (2016).
  • AluloskiI , TanturovskiM , JovanovicRet al.Survival of Advanced Stage High-Grade Serous Ovarian Cancer Patients in the Republic of Macedonia. Open Access Maced. J. Med. Sci.5(7), 904–908 (2017).
  • ShimizuA , SawadaK , KimuraT. Pathophysiological Role and Potential Therapeutic Exploitation of Exosomes in Ovarian Cancer. Cells.9(4), 814 (2020).
  • ChengL , WuS , ZhangK , QingY , XuT. A comprehensive overview of exosomes in ovarian cancer: emerging biomarkers and therapeutic strategies. J. Ovarian Res.10(1), 73 (2017).
  • DilsizN. Role of exosomes and exosomal microRNAs in cancer. Future Sci. OA.6(4), FSO465 (2020).
  • KellerS , RidingerJ , RuppA-K , JanssenJW , AltevogtP. Body fluid derived exosomes as a novel template for clinical diagnostics. J. Transl. Med.9(1), 86 (2011).
  • CaiJ , GongL , LiG , GuoJ , YiX , WangZ. Exosomes in ovarian cancer ascites promote epithelial–mesenchymal transition of ovarian cancer cells by delivery of miR-6780b-5p. Cell Death Dis.12(2), 210 (2021).
  • TaiY , ChenK , HsiehJ , ShenT. Exosomes in cancer development and clinical applications. Cancer Sci.109(8), 2364–2374 (2018).
  • RashedMH , BayraktarE , HelalGKet al.Exosomes: from garbage bins to promising therapeutic targets. Int. J. Mol. Sci.18(3), 538 (2017).
  • JohnstoneRM. The Jeanne Manery-Fisher Memorial Lecture 1991. Maturation of reticulocytes: formation of exosomes as a mechanism for shedding membrane proteins. Biochem. Cell Biol. Biochim. Biol. Cell.70(3–4), 179–190 (1992).
  • DoyleL , WangM. Overview of extracellular vesicles, their origin, composition, purpose, and methods for exosome isolation and analysis. Cells.8(7), 727 (2019).
  • ZhangY , LiuY , LiuH , TangWH. Exosomes: biogenesis, biologic function and clinical potential. Cell Biosci.9, 19 (2019).
  • GurunathanS , KangM-H , JeyarajM , QasimM , KimJ-H. Review of the isolation, characterization, biological function, and multifarious therapeutic approaches of exosomes. Cells8(4), 307 (2019).
  • IbrahimA , MarbánE. Exosomes: fundamental biology and roles in cardiovascular physiology. Annu. Rev. Physiol.78, 67–83 (2016).
  • LeeAH , KohIL , DawsonMR. The role of exosome heterogeneity in epithelial ovarian cancer. Adv. Cancer Biol. - Metastasis.4, 100040 (2022).
  • ColomboM , RaposoG , ThéryC. Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles. Annu. Rev. Cell Dev. Biol.30(1), 255–289 (2014).
  • HuangT , DengC-X. Current progresses of exosomes as cancer diagnostic and prognostic biomarkers. Int. J. Biol. Sci.15(1), 1–11 (2019).
  • DaiJ , SuY , ZhongSet al.Exosomes: key players in cancer and potential therapeutic strategy. Signal Transduct. Target. Ther.5(1), 1–10 (2020).
  • BlancL , VidalM. New insights into the function of Rab GTPases in the context of exosomal secretion. Small GTPases.9(1–2), 95–106 (2018).
  • PegtelDM , GouldSJ. Exosomes. Annu. Rev. Biochem.88(1), 487–514 (2019).
  • LamKCK , LamMKN , ChimCS , ChanGCF , LiJCB. The functional role of surface molecules on extracellular vesicles in cancer, autoimmune diseases, and coagulopathy. J. Leukoc. Biol.108(5), 1565–1573 (2020).
  • MeldolesiJ. Exosomes and ectosomes in intercellular communication. Curr. Biol.28(8), R435–R444 (2018).
  • MulcahyLA , PinkRC , CarterDRF. Routes and mechanisms of extracellular vesicle uptake. J. Extracell. Vesicles.3 (2014).
  • SubraC , GrandD , LaulagnierKet al.Exosomes account for vesicle-mediated transcellular transport of activatable phospholipases and prostaglandins. J. Lipid Res.51(8), 2105–2120 (2010).
  • LiuC , SuC. Design strategies and application progress of therapeutic exosomes. Theranostics.9(4), 1015–1028 (2019).
  • BeckerA , ThakurBK , WeissJM , KimHS , PeinadoH , LydenD. Extracellular vesicles in cancer: cell-to-cell mediators of metastasis. Cancer Cell.30(6), 836–848 (2016).
  • McAndrewsKM , KalluriR. Mechanisms associated with biogenesis of exosomes in cancer. Mol. Cancer18(1), 52 (2019).
  • FriedlP , AlexanderS. Cancer invasion and the microenvironment: plasticity and reciprocity. Cell147(5), 992–1009 (2011).
  • HanahanD , WeinbergRA. Hallmarks of cancer: the next generation. Cell144(5), 646–674 (2011).
  • ZhangW , LiuY , JiangJ , TangY , TangY , LiangX. Extracellular vesicle long non–coding RNA-mediated crosstalk in the tumor microenvironment: tiny molecules, huge roles. Cancer Sci.111(8), 2726–2735 (2020).
  • HuiL , ChenY. Tumor microenvironment: sanctuary of the devil. Cancer Lett.368(1), 7–13 (2015).
  • Roma-RodriguesC , MendesR , BaptistaPV , FernandesAR. Targeting tumor microenvironment for cancer therapy. Int. J. Mol. Sci.20(4), 840 (2019).
  • LiI , NabetBY. Exosomes in the tumor microenvironment as mediators of cancer therapy resistance. Mol. Cancer18(1), 32 (2019).
  • ConigliaroA , CicchiniC. Exosome-mediated signaling in epithelial to mesenchymal transition and tumor progression. J. Clin. Med.8(1), 26 (2019).
  • LiK , ChenY , LiA , TanC , LiuX. Exosomes play roles in sequential processes of tumor metastasis. Int. J. Cancer144(7), 1486–1495 (2019).
  • AlfonsiR , GrassiL , SignoreM , BonciD. The double face of exosome-carried microRNAs in cancer immunomodulation. Int. J. Mol. Sci.19(4), 1183 (2018).
  • LeBleuVS , KalluriR. Exosomes as a multicomponent biomarker platform in cancer. Trends Cancer6(9), 767–774 (2020).
  • GuoS , DengC-X. Effect of stromal cells in tumor microenvironment on metastasis initiation. Int. J. Biol. Sci.14(14), 2083–2093 (2018).
  • KuboN , ArakiK , KuwanoH , ShirabeK. Cancer-associated fibroblasts in hepatocellular carcinoma. World J. Gastroenterol.22(30), 6841–6850 (2016).
  • MuW , RanaS , ZöllerM. Host matrix modulation by tumor exosomes promotes motility and invasiveness. Neoplasia N. Y. N.15(8), 875–887 (2013).
  • HendrixA , MaynardD , PauwelsPet al.Effect of the secretory small GTPase Rab27B on breast cancer growth, invasion, and metastasis. J. Natl Cancer Inst.102(12), 866–880 (2010).
  • LuoZ , WangQ , LauWBet al.Tumor microenvironment: the culprit for ovarian cancer metastasis?Cancer Lett.377(2), 174–182 (2016).
  • YuanD , GuoT , ZhuDet al.Exosomal lncRNA ATB derived from ovarian cancer cells promotes angiogenesis via regulating miR-204-3p/TGFβR2 axis. Cancer Manag. Res.14, 327–337 (2022).
  • HeL , ZhuW , ChenQet al.Ovarian cancer cell-secreted exosomal miR-205 promotes metastasis by inducing angiogenesis. Theranostics.9(26), 8206–8220 (2019).
  • WuQ , WuX , YingXet al.Suppression of endothelial cell migration by tumor associated macrophage-derived exosomes is reversed by epithelial ovarian cancer exosomal lncRNA. Cancer Cell Int.17, 62 (2017).
  • ZhangY , CaiH , ChenS , SunD , ZhangD , HeY. Exosomal transfer of miR-124 inhibits normal fibroblasts to cancer-associated fibroblasts transition by targeting sphingosine kinase 1 in ovarian cancer. J. Cell. Biochem.120(8), 13187–13201 (2019).
  • YingX , WuQ , WuXet al.Epithelial ovarian cancer-secreted exosomal miR-222-3p induces polarization of tumor-associated macrophages. Oncotarget.7(28), 43076–43087 (2016).
  • ChenX , ZhouJ , LiX , WangX , LinY , WangX. Exosomes derived from hypoxic epithelial ovarian cancer cells deliver microRNAs to macrophages and elicit a tumor-promoted phenotype. Cancer Lett.435, 80–91 (2018).
  • YokoiA , YoshiokaY , YamamotoYet al.Malignant extracellular vesicles carrying MMP1 mRNA facilitate peritoneal dissemination in ovarian cancer. Nat. Commun.8, 14470 (2017).
  • YoshimuraA , SawadaK , NakamuraKet al.Exosomal miR-99a-5p is elevated in sera of ovarian cancer patients and promotes cancer cell invasion by increasing fibronectin and vitronectin expression in neighboring peritoneal mesothelial cells. BMC Cancer.18(1), 1065 (2018).
  • NakamuraK , SawadaK , KinoseYet al.Exosomes promote ovarian cancer cell invasion through transfer of CD44 to peritoneal mesothelial cells. Mol. Cancer Res. MCR.15(1), 78–92 (2017).
  • KrugmannJ , SchwarzCL , MelcherBet al.Malignant ascites occurs most often in patients with high-grade serous papillary ovarian cancer at initial diagnosis: a retrospective analysis of 191 women treated at Bayreuth Hospital, 2006-2015. Arch. Gynecol. Obstet.299(2), 515–523 (2019).
  • KippsE , TanDSP , KayeSB. Meeting the challenge of ascites in ovarian cancer: new avenues for therapy and research. Nat. Rev. Cancer.13(4), 273–282 (2013).
  • KimS , KimB , SongYS. Ascites modulates cancer cell behavior, contributing to tumor heterogeneity in ovarian cancer. Cancer Sci.107(9), 1173–1178 (2016).
  • ChafferCL , WeinbergRA. A perspective on cancer cell metastasis. Science331(6024), 1559–1564 (2011).
  • FidlerIJ. The organ microenvironment and cancer metastasis. Differ. Res. Biol. Divers.70(9–10), 498–505 (2002).
  • KimH , LeeS , ShinEet al.The emerging roles of exosomes as EMT regulators in cancer. Cells.9(4), 861 (2020).
  • VuT , DattaPK. Regulation of EMT in colorectal cancer: a culprit in metastasis. Cancers (Basel).9(12), 171 (2017).
  • PastushenkoI , BlanpainC. EMT transition states during tumor progression and metastasis. Trends Cell Biol.29(3), 212–226 (2019).
  • JordanNV , JohnsonGL , AbellAN. Tracking the intermediate stages of epithelial–mesenchymal transition in epithelial stem cells and cancer. Cell Cycle Georget. Tex.10(17), 2865–2873 (2011).
  • GrigoreAD , JollyMK , JiaD , Farach-CarsonMC , LevineH. Tumor budding: the name is EMT. Partial EMT. J. Clin. Med.5(5), E51 (2016).
  • AggarwalV , MontoyaCA , DonnenbergVS , SantS. Interplay between tumor microenvironment and partial EMT as the driver of tumor progression. iScience.24(2), 102113 (2021).
  • PastushenkoI , BrisebarreA , SifrimAet al.Identification of the tumour transition states occurring during EMT. Nature556(7702), 463–468 (2018).
  • YangJ , AntinP , BerxGet al.Guidelines and definitions for research on epithelial–mesenchymal transition. Nat. Rev. Mol. Cell Biol.21(6), 341–352 (2020).
  • LoretN , DenysH , TummersP , BerxG. The role of epithelial-to-mesenchymal plasticity in ovarian cancer progression and therapy resistance. Cancers.11(6), 838 (2019).
  • SaitohM. Involvement of partial EMT in cancer progression. J. Biochem. (Tokyo).164(4), 257–264 (2018).
  • PolyakK , WeinbergRA. Transitions between epithelial and mesenchymal states: acquisition of malignant and stem cell traits. Nat. Rev. Cancer.9(4), 265–273 (2009).
  • ZhangY , HuangS , GuoY , LiL. MiR-1294 confers cisplatin resistance in ovarian Cancer cells by targeting IGF1R. Biomed. Pharmacother. Biomedecine Pharmacother.106, 1357–1363 (2018).
  • Al-AidaroosAQO , YuenHF , GuoKet al.Metastasis-associated PRL-3 induces EGFR activation and addiction in cancer cells. J. Clin. Invest.123(8), 3459–3471 (2013).
  • EscreventeC , KellerS , AltevogtP , CostaJ. Interaction and uptake of exosomes by ovarian cancer cells. BMC Cancer.11, 108 (2011).
  • WangS , SuX , XuMet al.Exosomes secreted by mesenchymal stromal/stem cell-derived adipocytes promote breast cancer cell growth via activation of Hippo signaling pathway. Stem Cell Res. Ther.10(1), 117 (2019).
  • NamRK , BenatarT , WallisCJDet al.MiR-301a regulates E-cadherin expression and is predictive of prostate cancer recurrence. The Prostate.76(10), 869–884 (2016).
  • XiaY , WeiK , HuL-Qet al.Exosome-mediated transfer of miR-1260b promotes cell invasion through Wnt/β–catenin signaling pathway in lung adenocarcinoma. J. Cell. Physiol.235(10), 6843–6853 (2020).
  • LuC , ShanZ , HongJ , YangL. MicroRNA-92a promotes epithelial–mesenchymal transition through activation of PTEN/PI3K/AKT signaling pathway in non-small cell lung cancer metastasis. Int. J. Oncol.51(1), 235–244 (2017).
  • QuZ , FengJ , PanH , JiangY , DuanY , FaZ. Exosomes derived from HCC cells with different invasion characteristics mediated EMT through TGF-β/Smad signaling pathway. OncoTargets Ther.12, 6897–6905 (2019).
  • XiaoD , BarryS , KmetzDet al.Melanoma cell-derived exosomes promote epithelial–mesenchymal transition in primary melanocytes through paracrine/autocrine signaling in the tumor microenvironment. Cancer Lett.376(2), 318–327 (2016).
  • LiW , ZhangX , WangJet al.TGFβ1 in fibroblasts-derived exosomes promotes epithelial–mesenchymal transition of ovarian cancer cells. Oncotarget.8(56), 96035–96047 (2017).
  • CrowJ , AtayS , BanskotaS , ArtaleB , SchmittS , GodwinAK. Exosomes as mediators of platinum resistance in ovarian cancer. Oncotarget.8(7), 11917–11936 (2017).
  • KosakaN , KogureA , YamamotoTet al.Exploiting the message from cancer: the diagnostic value of extracellular vesicles for clinical applications. Exp. Mol. Med.51(3), 1–9 (2019).
  • SilvaJ , GarciaV , RodriguezMet al.Analysis of exosome release and its prognostic value in human colorectal cancer. Genes. Chromosomes Cancer.51(4), 409–418 (2012).
  • TangMKS , WongAST. Exosomes: emerging biomarkers and targets for ovarian cancer. Cancer Lett.367(1), 26–33 (2015).
  • MeloSA , LueckeLB , KahlertCet al.Glypican-1 identifies cancer exosomes and detects early pancreatic cancer. Nature523(7559), 177–182 (2015).
  • QianZ , ShenQ , YangX , QiuY , ZhangW. The role of extracellular vesicles: an epigenetic view of the cancer microenvironment. BioMed Res. Int.2015, e649161 (2015).
  • WangH , HouL , LiA , DuanY , GaoH , SongX. Expression of serum exosomal microRNA-21 in human hepatocellular carcinoma. BioMed Res. Int.2014, 864894 (2014).
  • ZhangC , YangX , QiQ , GaoY , WeiQ , HanS. lncRNA-HEIH in serum and exosomes as a potential biomarker in the HCV-related hepatocellular carcinoma. Cancer Biomark. Sect. Dis. Markers.21(3), 651–659 (2018).
  • SaberSH , AliHEA , GaballaRet al.Exosomes are the driving force in preparing the soil for the metastatic seeds: lessons from the prostate cancer. Cells.9(3), E564 (2020).
  • AnastasiadouE , JacobLS , SlackFJ. Non-coding RNA networks in cancer. Nat. Rev. Cancer.18(1), 5–18 (2018).
  • WeiJ-W , HuangK , YangC , KangC-S. Non-coding RNAs as regulators in epigenetics. Oncol. Rep.37(1), 3–9 (2017).
  • HaM , KimVN. Regulation of microRNA biogenesis. Nat. Rev. Mol. Cell Biol.15(8), 509–524 (2014).
  • TreiberT , TreiberN , MeisterG. Regulation of microRNA biogenesis and its crosstalk with other cellular pathways. Nat. Rev. Mol. Cell Biol.20(1), 5–20 (2019).
  • YangF , NingZ , MaLet al.Exosomal miRNAs and miRNA dysregulation in cancer-associated fibroblasts. Mol. Cancer.16(1), 148 (2017).
  • ZhaoW , LiuY , ZhangC , DuanC. Multiple roles of exosomal long noncoding RNAs in cancers. BioMed Res. Int.2019, 1460572 (2019).
  • WeryM , KwapiszM , MorillonA. Noncoding RNAs in gene regulation. WIREs Syst. Biol. Med.3(6), 728–738 (2011).
  • QuesenberryPJ , AliottaJ , DeregibusMC , CamussiG. Role of extracellular RNA-carrying vesicles in cell differentiation and reprogramming. Stem Cell Res. Ther.6, 153 (2015).
  • RabinowitsG , Gerçel-TaylorC , DayJM , TaylorDD , KloeckerGH. Exosomal microRNA: a diagnostic marker for lung cancer. Clin. Lung Cancer.10(1), 42–46 (2009).
  • LinJ , LiJ , HuangBet al.Exosomes: novel biomarkers for clinical diagnosis. Sci. World J.2015, 1–8 (2015).
  • WangM , YuF , DingH , WangY , LiP , WangK. Emerging function and clinical values of exosomal MicroRNAs in cancer. Mol. Ther. - Nucleic Acids.16, 791–804 (2019).
  • ZhangP , ZhouH , LuK , LuY , WangY , FengT. Exosome-mediated delivery of MALAT1 induces cell proliferation in breast cancer. OncoTargets Ther.11, 291–299 (2018).
  • LangH-L , HuG-W , ChenYet al.Glioma cells promote angiogenesis through the release of exosomes containing long non-coding RNA POU3F3. Eur. Rev. Med. Pharmacol. Sci.21(5), 959–972 (2017).
  • TanakaY , KamoharaH , KinoshitaKet al.Clinical impact of serum exosomal microRNA-21 as a clinical biomarker in human esophageal squamous cell carcinoma. Cancer119(6), 1159–1167 (2013).
  • BryantRJ , PawlowskiT , CattoJWFet al.Changes in circulating microRNA levels associated with prostate cancer. Br. J. Cancer106(4), 768–774 (2012).
  • LeMTN , HamarP , GuoCet al.miR-200-containing extracellular vesicles promote breast cancer cell metastasis. J. Clin. Invest.124(12), 5109–5128 (2014).
  • RichardsKE , ZeleniakAE , FishelML , WuJ , LittlepageLE , HillR. Cancer-associated fibroblast exosomes regulate survival and proliferation of pancreatic cancer cells. Oncogene36(13), 1770–1778 (2017).
  • LiL , LiC , WangSet al.Exosomes derived from hypoxic oral squamous cell carcinoma cells deliver miR-21 to normoxic cells to elicit a prometastatic phenotype. Cancer Res.76(7), 1770–1780 (2016).
  • ShanY , YouB , ShiSet al.Hypoxia-induced matrix metalloproteinase-13 expression in exosomes from nasopharyngeal carcinoma enhances metastases. Cell Death Dis.9(3), 382–382 (2018).
  • SinghR , PochampallyR , WatabeK , LuZ , MoY-Y. Exosome-mediated transfer of miR-10b promotes cell invasion in breast cancer. Mol. Cancer.13(1), 256 (2014).
  • Naderi-MeshkinH , LaiX , AmirkhahR , VeraJ , RaskoJ , SchmitzU. Exosomal lncRNAs and cancer: connecting the missing links. Bioinformatics.35(2), 352–360 (2019).
  • HewsonC , MorrisKV. Form and function of exosome-associated long non-coding RNAs in cancer. Curr. Top. Microbiol. Immunol.394, 41–56 (2016).
  • WangM , ZhouL , YuF , ZhangY , LiP , WangK. The functional roles of exosomal long non-coding RNAs in cancer. Cell. Mol. Life Sci.76(11), 2059–2076 (2019).
  • PanL , LiangW , FuMet al.Exosomes-mediated transfer of long noncoding RNA ZFAS1 promotes gastric cancer progression. J. Cancer Res. Clin. Oncol.143(6), 991–1004 (2017).
  • LiB , MaoR , LiuC , ZhangW , TangY , GuoZ. 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).
  • XuC-G , YangM-F , RenY-Q , WuC-H , WangL-Q. Exosomes mediated transfer of lncRNA UCA1 results in increased tamoxifen resistance in breast cancer cells. Eur Rev Med Pharmacol Sci.20, 7 (2016).
  • KrolJ , LoedigeI , FilipowiczW. The widespread regulation of microRNA biogenesis, function and decay. Nat. Rev. Genet.11(9), 597–610 (2010).
  • QiuJ-J , LinX-J , TangX-Y , ZhengT-T , LinY-Y , HuaK-Q. Exosomal metastasis-associated lung adenocarcinoma transcript 1 promotes angiogenesis and predicts poor prognosis in epithelial ovarian cancer. Int. J. Biol. Sci.14(14), 1960–1973 (2018).
  • LiZ , NiuH , QinQet al.lncRNA UCA1 mediates resistance to cisplatin by regulating the miR-143/FOSL2-signaling pathway in ovarian cancer. Mol. Ther. - Nucleic Acids.17, 92–101 (2019).
  • TangX , LiuS , LiuYet al.Circulating serum exosomal aHIF is a novel prognostic predictor for epithelial ovarian cancer – PubMed. Onco Targets Ther.12, 7699–7711 (2019).
  • TaylorDD , Gercel-TaylorC. MicroRNA signatures of tumor-derived exosomes as diagnostic biomarkers of ovarian cancer. Gynecol. Oncol.110(1), 13–21 (2008).
  • SuYY , SunL , GuoZRet al.Upregulated expression of serum exosomal miR-375 and miR-1307 enhance the diagnostic power of CA125 for ovarian cancer. J. Ovarian Res.12(1), 6 (2019).
  • PanC , StevicI , MüllerVet al.Exosomal microRNAs as tumor markers in epithelial ovarian cancer. Mol. Oncol.12(11), 1935–1948 (2018).
  • ZhangQ , LenT-Y , ZhangS-X , ZhaoQ-H , YangL-H. Exosomes transferring long non-coding RNA FAL1 to regulate ovarian cancer metastasis through the PTEN/AKT signaling pathway. Eur Rev Med Pharmacol Sci.24(21), 10921 (2020 Nov).
  • AuYeung CL , CoN-N , TsurugaTet al.Exosomal transfer of stroma-derived miR21 confers paclitaxel resistance in ovarian cancer cells through targeting APAF1. Nat. Commun.7, 11150 (2016).
  • Weiner-GorzelK , DempseyE , MilewskaMet al.Overexpression of the microRNA miR-433 promotes resistance to paclitaxel through the induction of cellular senescence in ovarian cancer cells. Cancer Med.4(5), 745–758 (2015).
  • ZhuX , ShenH , YinXet al.Macrophages derived exosomes deliver miR-223 to epithelial ovarian cancer cells to elicit a chemoresistant phenotype. J. Exp. Clin. Cancer Res. CR.38(1), 81 (2019).
  • RaimondoS , SaievaL , CorradoCet al.Chronic myeloid leukemia-derived exosomes promote tumor growth through an autocrine mechanism. Cell Commun. Signal. CCS13, 8 (2015).
  • LogozziM , DeMilito A , LuginiLet al.High levels of exosomes expressing CD63 and caveolin-1 in plasma of melanoma patients. PLOS ONE4(4), e5219 (2009).
  • SkogJ , WürdingerT , van RijnSet al.Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat. Cell Biol.10(12), 1470–1476 (2008).
  • Al-NedawiK , MeehanB , MicallefJet al.Intercellular transfer of the oncogenic receptor EGFRvIII by microvesicles derived from tumour cells. Nat. Cell Biol.10(5), 619–624 (2008).
  • SteigedalTS , ToraskarJ , RedversRPet al.Nephronectin is correlated with poor prognosis in breast cancer and promotes metastasis via its integrin-binding motifs. Neoplasia N. Y. N.20(4), 387–400 (2018).
  • KhanS , BennitHF , TurayDet al.Early diagnostic value of survivin and its alternative splice variants in breast cancer. BMC Cancer.14, 176 (2014).
  • LiangB , PengP , ChenSet al.Characterization and proteomic analysis of ovarian cancer-derived exosomes. J. Proteomics.80, 171–182 (2013).
  • SzajnikM , DerbisM , LachMet al.Exosomes in plasma of patients with ovarian carcinoma: potential biomarkers of tumor progression and response to therapy. Gynecol. Obstet. Sunnyvale Calif.Suppl. 4, 003 (2013).
  • FengW , DeanDC , HornicekFJ , ShiH , DuanZ. Exosomes promote pre-metastatic niche formation in ovarian cancer. Mol. Cancer18(1), 24 (2019).
  • JayaseelanVP. Emerging role of exosomes as promising diagnostic tool for cancer. Cancer Gene Ther.27(6), 395–398 (2020).
  • XuM , FengT , LiuBet al.Engineered exosomes: desirable target-tracking characteristics for cerebrovascular and neurodegenerative disease therapies. Theranostics.11(18), 8926–8944 (2021).
  • Alvarez-ErvitiL , SeowY , YinH , BettsC , LakhalS , WoodMJA. Delivery of siRNA to the mouse brain by systemic injection of targeted exosomes. Nat. Biotechnol.29(4), 341–345 (2011).
  • Momen-HeraviF , BalaS , BukongT , SzaboG. Exosome-mediated delivery of functionally active miRNA-155 inhibitor to macrophages. Nanomedicine Nanotechnol. Biol. Med.10(7), 1517–1527 (2014).
  • KimMS , HaneyMJ , ZhaoYet al.Development of exosome-encapsulated paclitaxel to overcome MDR in cancer cells. Nanomedicine Nanotechnol. Biol. Med.12(3), 655–664 (2016).
  • LiH , YangC , ShiY , ZhaoL. Exosomes derived from siRNA against GRP78 modified bone-marrow-derived mesenchymal stem cells suppress Sorafenib resistance in hepatocellular carcinoma. J. Nanobiotechnology.16(1), 103 (2018).
  • LiS , WuY , DingFet al.Engineering macrophage-derived exosomes for targeted chemotherapy of triple-negative breast cancer – PubMed. Nanoscale.12(19), 10854–10862 (2020).
  • ZhuangX , XiangX , GrizzleWet al.Treatment of brain inflammatory diseases by delivering exosome encapsulated anti-inflammatory drugs from the nasal region to the brain. Mol. Ther. J. Am. Soc. Gene Ther.19(10), 1769–1779 (2011).
  • PinzaniP , D'ArgenioV , ReMDet al.Updates on liquid biopsy: current trends and future perspectives for clinical application in solid tumors. Clin. Chem. Lab. Med. CCLM.59(7), 1181–1200 (2021).