The Impact of Cancer-Derived Exosomes on the Epigenetic Regulation of Recipient Cells

Nuray VAROLa
aGazi University Faculty of Medicine, Department of Medical Biology and Genetics, Ankara, Türkiye

Varol N. The impact of cancer-derived exosomes on the epigenetic regulation of recipient cells. In: Yar Sağlam AS, ed. Innovative Approaches in Cancer Diagnosis and Treatment. 1st ed. Ankara: Türkiye Klinikleri; 2024. p.38-43.

Makale Dili: EN

ABSTRACT
Cancer cells have a dynamic cross-talk between tumor microenvironment and cancer cells. This communication is essential in reprogramming the recipient cell and/or microenvironments. Exosomes are a subset of extracellular vesicles that act as multi-molecular messengers by transferring exosomal cargo biomolecules, including proteins,lipids, DNA, mRNAs, and non-coding RNAs. The role of exosomes is dynamic and specific to cancer type and stage. Cancer-derived exosomes are pivotal in regulating tumor growth, angiogenesis, metastasis, drug resistance, and spread in recipient cells. As a result, in this chapter, we attempted to summarize how cancer-derived exosomes induce the initiation and progression of cancer by epigenetically reprogramming the recipient cell and microenvironments.

Keywords: Exosomes; epigenesis, genetic; biomarkers, tumor

Referanslar

  1. Dilsiz N. Role of exosomes and exosomal microRNAs in cancer. Future Sci OA. 2020;6(4):FSO465. [Crossref]  [PubMed]  [PMC]
  2. Liu YJ, Wang C. A review of the regulatory mechanisms of extracellular vesicles-mediated intercellular communication. Cell Commun Signal. 2023;21(1):77. [Crossref]  [PubMed]  [PMC]
  3. Guille C, Johnson E, Douglas E, Aujla R, Boyars L, Kruis R, et al. A Pilot Study Examining Access to and Satisfaction with Maternal Mental Health and Substance Use Disorder Treatment via Telemedicine. Telemed Rep. 2022;3(1):24-9. [Crossref]  [PubMed]  [PMC]
  4. Chiodoni C, Di Martino MT, Zazzeroni F, Caraglia M, Donadelli, Meschini S, Leonetti C, Scotlandi K. Correction to: Cell communication and signaling: how to turn bad language into positive one. J Exp Clin Cancer Res. 2019;38(1):425. [Crossref]  [PubMed]  [PMC]
  5. Catoni C, Di Paolo V, Rossi E, Quintieri L, Zamarchi R. Cell-Secreted Vesicles: Novel Opportunities in Cancer Diagnosis, Monitoring and Treatment Diagnostics (Basel). 2021;11(6):1118. [Crossref]  [PubMed]  [PMC]
  6. Dai J, YSu Y, Zhong S, Cong L, Liu B, Yang J, et al. Exosomes: key players in cancer and potential therapeutic strategy. Signal Transduct Target Ther. 2020;5(1):145. [Crossref]  [PubMed]  [PMC]
  7. Zhou S, Abdouh M, Arena V, Arena M, Arena GO. Reprogramming Malignant Cancer Cells toward a Benign Phenotype following Exposure to Human Embryonic Stem Cell Microenvironment. PLoS One. 2017;12(1):e0169899. [Crossref]  [PubMed]  [PMC]
  8. Tomasetti M, Lee W, Santarelli L, Neuzil J. Exosome-derived microRNAs in cancer metabolism: possible implications in cancer diagnostics and therapy. Exp Mol Med. 2017;49(1):e285. [Crossref]  [PubMed]  [PMC]
  9. Hanahan D. Hallmarks of Cancer: New Dimensions. Cancer Discov. 2022;12(1):31-46. [Crossref]  [PubMed]
  10. Liu QW, He Y, Xu WW. Molecular functions and therapeutic applications of exosomal noncoding RNAs in cancer. Exp Mol Med. 2022;54(3):216-25. [Crossref]  [PubMed]  [PMC]
  11. Li C, Ni YQ, Xu H, Xiang QY, Zhao Y, Zhan JK, et al. Roles and mechanisms of exosomal non-coding RNAs in human health and diseases. Signal Transduct Target Ther. 2021;6(1):383. [Crossref]  [PubMed]  [PMC]
  12. Kinoshita T, Yip KW, Spence T, Liu FF. MicroRNAs in extracellular vesicles: potential cancer biomarkers. J Hum Genet. 2017;62(1):67-74. [Crossref]  [PubMed]
  13. Lunavat TR, Cheng L, Kim DK, Bhadury J, Jang SC, Lässer C, et al. Small RNA deep sequencing discriminates subsets of extracellular vesicles released by melanoma cells--Evidence of unique microRNA cargos. RNA Biol. 2015;12(8):810-23. [Crossref]  [PubMed]  [PMC]
  14. Fabbri M, Paone A, Calore F, Galli R, Gaudio E, Santhanam R,et al. MicroRNAs bind to Toll-like receptors to induce prometastatic inflammatory response. Proc Natl Acad Sci USA. 2012;109(31):E2110-6. [Crossref]  [PubMed]  [PMC]
  15. Xue X, Wang X, Zhao Y, Hu R, Qin L. Exosomal miR-93 promotes proliferation and invasion in hepatocellular carcinoma by directly inhibiting TIMP2/TP53INP1/CDKN1A. Biochem Biophys Res Commun. 2018;502(4):515-21. [Crossref]  [PubMed]
  16. Zhuang G, Wu X, Jiang Z, Kasman I, Yao J, Guan Y, et al. Tumour-secreted miR-9 promotes endothelial cell migration and angiogenesis by activating the JAK-STAT pathway. EMBO J. 2012;31(17):3513-23. [Crossref]  [PubMed]  [PMC]
  17. Chen H, Li L, Wang S, Lei Y, Ge Q, Lv N, et al. Reduced miR-126 expression facilitates angiogenesis of gastric cancer through its regulation on VEGF-A. Oncotarget. 2014;5(23):11873-85. [Crossref]  [PubMed]  [PMC]
  18. Lee JK, Park SR, Jung BK, Jeon YK, Lee YS, Kim MK, et al. Exosomes derived from mesenchymal stem cells suppress angiogenesis by down-regulating VEGF expression in breast cancer cells. PLoS One. 2023;8(12):e84256. [Crossref]  [PubMed]  [PMC]
  19. Pakravan K, Babashas S, Sadeghizadeh, Mowla SJ, Mohammadi MM, Ataei F, et al. MicroRNA-100 shuttled by mesenchymal stem cell-derived exosomes suppresses in vitro angiogenesis through modulating the mTOR/HIF-1α/VEGF signaling axis in breast cancer cells. Cell Oncol (Dordr). 2027; 40(5):457-70. [Crossref]  [PubMed]
  20. Sun X, Lin F, ESun W, Zhu W, Fang D, Luo L, et al. Exosome-transmitted miRNA-335-5p promotes colorectal cancer invasion and metastasis by facilitating EMT via targeting RASA1. Mol Ther Nucleic Acids. 2021:24:164-74. [Crossref]  [PubMed]  [PMC]
  21. Le MTN, Hamar P, Guo C, Basar E, Henriques RP, Blaj L, et al. miR-200-containing extracellular vesicles promote breast cancer cell metastasis.J Clin Invest. 2014;124(12):5109-28. [Crossref]  [PubMed]  [PMC]
  22. Zhang X, Sai B, Wang F, Wang L, Wang Y, Zheng L, et al. Hypoxic BMSC-derived exosomal miRNAs promote metastasis of lung cancer cells via STAT3-induced EMT. Mol Cancer. 2019;18(1):40. [Crossref]  [PubMed]  [PMC]
  23. Bigagli E, Luceri C, Guasti D, Cinci L. Exosomes secreted from human colon cancer cells influence the adhesion of neighboring metastatic cells: Role of microRNA-210. Cancer Biol. Ther. 2016;17:1062-9. [Crossref]  [PubMed]  [PMC]
  24. Mattick JS, Amaral PP, Carninci P, Carpenter S, Chang HY, Chen LL, et al. Long non-coding RNAs: definitions, functions, challenges and recommendations. Nat Rev Mol Cell Biol. 2023;24(6):430-47. [Crossref]  [PubMed]  [PMC]
  25. Han S, Qi Y, Luo Y, Chen X, Liang. Exosomal Long Non-Coding RNA: Interaction Between Cancer Cells and Non-Cancer Cells. Front Oncol. 2021:10:617837. [Crossref]  [PubMed]  [PMC]
  26. Li B, Mao R, Liu C, Zhang W, Tang Y, Guo Z. LncRNA FAL1 promotes cell proliferation and migration by acting as a CeRNA of miR-1236 in hepatocellular carcinoma cells. Life Sci. 2018;197:122-29. [Crossref]  [PubMed]
  27. Zhang P, Zhou H, Lu K, Lu Y, Wang Y, Feng T. Exosome-mediated delivery of MALAT1 induces cell proliferation in breast cancer.Onco Targets Ther. 2018;11:291-99. [Crossref]  [PubMed]  [PMC]
  28. Lu Y, Chen L, Li L, Cao Y. Exosomes Derived from Brain Metastatic Breast Cancer Cells Destroy the Blood-Brain Barrier by Carrying lncRNA GS1-600G8.5.Biomed Res Int. 2020;2020:7461727. [Crossref]  [PubMed]  [PMC]
  29. Conigliaro A, Costa V, Lo Dico A, Saieva L, Buccheri S, Dieli F, et al. CD90+ liver cancer cells modulate endothelial cell phenotype through the release of exosomes containing H19 lncRNA. Mol Cancer. 2015;14:155. [Crossref]  [PubMed]  [PMC]
  30. Lu Y, Hou K, Li M, Wu X, Yuan S. Exosome-Delivered LncHEIH Promotes Gastric Cancer Progression by Upregulating EZH2 and Stimulating Methylation of the GSDME Promoter. Front Cell Dev Biol. 2020:8:571297. Retraction in: Front Cell Dev Biol. 2022;10:896056. [Crossref]  [PubMed]  [PMC]
  31. Chen C, Luo Y, He W, Zhao Y, Kong Y, Liu H, et al.Exosomal long noncoding RNA LNMAT2 promotes lymphatic metastasis in bladder cancer. J Clin Invest. 2020;130(1):404-21. [Crossref]  [PubMed]  [PMC]
  32. Zheng R, Du M, Wang X, Xu W, Liang J, Wang W. Exosome-transmitted long non-coding RNA PTENP1 suppresses bladder cancer progression. Mol Cancer. 2018;17(1):143. [Crossref]  [PubMed]  [PMC]
  33. Zhang N, Nan A, Chen L, Li X, Jia Y, Qui M, et al. Circular RNA circSATB2 promotes progression of non-small cell lung cancer cells. Mol Cancer. 2020;19(1):101. [Crossref]  [PubMed]  [PMC]
  34. Zhu C, Su Y, Liu L, Wang S, Liu Y, Wu J. Circular RNA hsa_circ_0004277 Stimulates Malignant Phenotype of Hepatocellular Carcinoma and Epithelial-Mesenchymal Transition of Peripheral Cells. Front Cell dev Biol. 2021; 8:585565. [Crossref]  [PubMed]  [PMC]
  35. Li T, Sun X, Chen L. Exosome circ_0044516 promotes prostate cancer cell proliferation and metastasis as a potential biomarker. J Cell Biochem. 2020;121(3):2118-26. [Crossref]  [PubMed]
  36. Yao W, Guo P, Mu Q, Wang Y. Exosome-Derived Circ-PVT1 Contributes to Cisplatin Resistance by Regulating Autophagy, Invasion, and Apoptosis Via miR-30a-5p/YAP1 Axis in Gastric Cancer Cells. Cancer Biother Radiopharm. 2021; 36(4):347-59. [Crossref]  [PubMed]
  37. Geng X, Zhang Y, Lin X, Zeng Z, Hu J, Hao L, et al. Exosomal circWDR62 promotes temozolomide resistance and malignant progression through regulation of the miR-370-3p/MGMT axis in glioma. Cell Death Dis. 2022; 13(7):596. [Crossref]  [PubMed]  [PMC]
  38. Lin J, Huang B, Liu J, Chen X, Chen XM, Xu YM, et al. Exosomes: novel biomarkers for clinical diagnosis. cientific World Journal. 2015; 2015:657086. [Crossref]  [PubMed]  [PMC]
  39. Keerthikumar S, Chisanga D, Ariyaratne D, Al saffar H, Anand S, Zhao K, et al. ExoCarte: A web-based compendium of exosamal Cargo. J Mol Biol. 2016;428(4):688-92. [Crossref]  [PubMed]  [PMC]
  40. Wang J, Yue BL, Huang YZ, Lan XY, Liu WJ, Chen H. Exosomal RNAs: Novel Potential Biomarkers for Diseases-A Review. Int J Mol sci. 2022;23(5):2461. [Crossref]  [PubMed]  [PMC]
  41. Shao X, Chung J, Lee K, Balaj L, Min C, Carter BS, et al. Chip-based analysis of exosomal mRNA mediating drug resistance in glioblastoma. Nat Commun. 2015;6:6999. [Crossref]  [PubMed]  [PMC]
  42. Cao YL, Zhuang T, Xing BH, Li Na, Li Q. Exosomal DNMT1 mediates cisplatin resistance in ovarian cancer. Cell Biochem Funct. 2017;35(6):296-303. [Crossref]  [PubMed]
  43. Li W, Li C, Zhou T, Liu X, Liu X, Li X, et al. Role of exosomal proteins in cancer diagnosis. Mol Cancer. 2017;16(1):145. [Crossref]  [PubMed]  [PMC]
  44. Raimondo F, Morosi L, Corbetta S, Chinello C, Brambilla P, Della MP, et al. Differential protein profiling of renal cell carcinoma urinary exosomes. Mol BioSyst. 2013; 9:1220-33. [Crossref]  [PubMed]
  45. Clark DJ, Fondrie WE, Yang A, Mao L. Triple SILAC quantitative proteomic analysis reveals differential abundance of cell signaling proteins between normal and lung cancer-derived exosomes. J Proteomics. 2016;133:161-9. [Crossref]  [PubMed]
  46. Wang X, Shen H, Zhangyuan G, Huang R, Zhang W, He Q, et al. 14-3-3ζ delivered by hepatocellular carcinoma-derived exosomes impaired anti-tumor function of tumor-infiltrating T lymphocytes. Cell Death Dis. 2018;9(2):159. [Crossref]  [PubMed]  [PMC]
  47. Kim H, Kim DW, Cho JY. Exploring the key Communicator role of exosomes in cancer microenvironment through proteomics. Proteome Sci. 2019;17:5. [Crossref]  [PubMed]  [PMC]