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Dual-functional extracellular vesicles enable synergistic treatment via m6A reader YTHDF1-targeting epigenetic regulation and chemotherapy

Du, Rong, You, Qing, Liu, Jingyi, Wang, Chen, Zhu, Ling, Yang, Yanlian·2023·Nano Research
DOI 10.1007/s12274-023-6105-0
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Abstract

Chemotherapy remains one of the most prevailing strategies for cancer treatment. However, its treatment effect is hampered by drug resistance, nonspecific tumor targeting, and severe toxic side effects. Combination chemotherapy with synergistic effect has become an attractive tumor therapy. N6-methyladenosine (m6A) regulators determine the fate of m6A-modified transcripts and play vital roles in cancer development and drug resistance. Gene therapy such as small interfering RNA (siRNA) is a promising strategy to reduce the abnormal gene expression of m6A regulators. However, its poor selectivity and high systemic toxicity necessitate the use of delivery vectors to target specific cells and tissues. Here, we constructed a dual-functional targeted nanodrug platform for the synergetic m6A-associated epigenetic regulation and chemotherapy of ovarian cancer. We encapsulated siRNA targeting the m6A reader YT521-B homology (YTH) N6-methyladenosine RNA-binding protein 1 (YTHDF1) and docetaxel (DTX), the first-line chemotherapeutic agent of ovarian cancer, into mesenchymal stem cell-derived small extracellular vesicles (MsEVs). This nanosystem exhibits significant tumor targeting and endo/lysosomal escape of siYTHDF1. It effectively depletes YTHDF1 and suppresses the protein translation of eukaryotic translation initiation factor 3 subunit C (EIF3C) in an m6A-dependent manner. The combination of YTHDF1-targeting epigenetic regulation significantly enhances the anti-tumor effect of DTX…

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Research works printed but not linked: 64

  1. Xiao, C.; Fan, T.; Tian, H.; Zheng, Y. J.; Zhou, Z.; Li, S. F.; Li, C. X.; He, J. H3K36 trimethylation-mediated biological functions in cancer. Clin. Epigenetics 2021, 13, 199. · DOI · Paper page
  2. Dawson, M. A.; Kouzarides, T. Cancer epigenetics: From mechanism to therapy. Cell 2012, 150, 12–27. · DOI · Paper page
  3. Jones, P. A.; Baylin, S. B. The epigenomics of cancer. Cell 2007, 128, 683–692. · DOI · Paper page
  4. Chen, M. N.; Wei, L.; Law, C. T.; Tsang, F. H. C.; Shen, J. K.; Cheng, C. L. H.; Tsang, L. H.; Ho, D. W. H.; Chiu, D. K. C.; Lee, J. M. F. et al. RNA N6-methyladenosine methyltransferase-like 3 promotes liver cancer progression through YTHDF2-dependent posttranscriptional silencing of SOCS2. Hepatology 2018, 67, 2254–2270. · DOI
  5. Zhang, L.; Volinia, S.; Bonome, T.; Calin, G. A.; Greshock, J.; Yang, N.; Liu, C. G.; Giannakakis, A.; Alexiou, P.; Hasegawa, K. et al. Genomic and epigenetic alterations deregulate microRNA expression in human epithelial ovarian cancer. Proc. Natl. Acad. Sci. USA 2008, 105, 7004–7009. · DOI
  6. Calin, G. A.; Croce, C. M. MicroRNA signatures in human cancers. Nat. Rev. Cancer 2006, 6, 857–866. · DOI
  7. Wang, X.; Lu, Z. K.; Gomez, A.; Hon, G. C.; Yue, Y. N.; Han, D. L.; Fu, Y.; Parisien, M.; Dai, Q.; Jia, G. F. et al. N6-methyladenosine-dependent regulation of messenger RNA stability. Nature 2014, 505, 117–120. · DOI · Paper page
  8. Jin, D.; Guo, J. W.; Wu, Y.; Du, J.; Yang, L. J.; Wang, X. H.; Di, W. H.; Hu, B. G.; An, J. J.; Kong, L. Q. et al. RETRACTED ARTICLE: m6A mRNA methylation initiated by METTL3 directly promotes YAP translation and increases YAP activity by regulating the MALAT1-miR-1914-3p-YAP axis to induce NSCLC drug resistance and metastasis. J. Hematol. Oncol. 2019, 12, 135. · DOI
  9. Huang, H. L.; Weng, H. Y.; Chen, J. J. m6A modification in coding and non-coding RNAs: Roles and therapeutic implications in cancer. Cancer Cell 2020, 37, 270–288. · DOI
  10. Wang, X.; Zhao, B. S.; Roundtree, I. A.; Lu, Z. K.; Han, D. L.; Ma, H. H.; Weng, X. C.; Chen, K.; Shi, H. L.; He, C. N6-methyladenosine modulates messenger RNA translation efficiency. Cell 2015, 161, 1388–1399. · DOI · Paper page
  11. Liu, T.; Wei, Q. L.; Jin, J.; Luo, Q. Y.; Liu, Y.; Yang, Y.; Cheng, C. M.; Li, L. F.; Pi, J. N.; Si, Y. M. et al. The m6A reader YTHDF1 promotes ovarian cancer progression via augmenting EIF3C translation. Nucleic Acids Res. 2020, 48, 3816–3831. · DOI
  12. Emmanuel, R.; Weinstein, S.; Landesman-Milo, D.; Peer, D. eIF3c: A potential therapeutic target for cancer. Cancer Lett. 2013, 336, 158–166. · DOI
  13. Wen, F.; Wu, Z. Y.; Nie, L.; Zhang, Q. Z.; Qin, Y. K.; Zhou, Z. L.; Wu, J. J.; Zhao, X.; Tan, J.; Sawmiller, D. et al. Eukaryotic initiation factor 3, subunit C silencing inhibits cell proliferation and promotes apoptosis in human ovarian cancer cells. Biosci. Rep. 2019, 39, BSR20191124. · DOI
  14. Nishizawa, Y.; Konno, M.; Asai, A.; Koseki, J.; Kawamoto, K.; Miyoshi, N.; Takahashi, H.; Nishida, N.; Haraguchi, N.; Sakai, D. et al. Oncogene c-Myc promotes epitranscriptome m6A reader YTHDF1 expression in colorectal cancer. Oncotarget 2018, 9, 7476–7486. · DOI
  15. Chen, P.; Liu, X. Q.; Lin, X.; Gao, L. Y.; Zhang, S.; Huang, X. Targeting YTHDF1 effectively re-sensitizes cisplatin-resistant colon cancer cells by modulating GLS-mediated glutamine metabolism. Mol. Ther. Oncolytics 2021, 20, 228–239. · DOI
  16. Hao, L.; Wang, J. M.; Liu, B. Q.; Yan, J.; Li, C.; Jiang, J. Y.; Zhao, F. Y.; Qiao, H. Y.; Wang, H. Q. m6A-YTHDF1-mediated TRIM29 upregulation facilitates the stem cell-like phenotype of cisplatin-resistant ovarian cancer cells. Biochim. Biophys. Acta (BBA)-Mol. Cell Res. 2021, 1868, 118878. · DOI
  17. Li, Z. J.; Teng, M. Z.; Jiang, Y. B.; Zhang, L. T.; Luo, X.; Liao, Y. H.; Yang, B. YTHDF1 negatively regulates treponema pallidum-induced inflammation in THP-1 macrophages by promoting SOCS3 translation in an m6A-dependent manner. Front. Immunol. 2022, 13, 857727. · DOI · Paper page
  18. Cortes, J. E.; Pazdur, R. Docetaxel. J. Clin. Oncol. 1995, 13, 2643–2655. · DOI · Paper page
  19. Zahedi, P.; De Souza, R.; Huynh, L.; Piquette-Miller, M.; Allen, C. Combination drug delivery strategy for the treatment of multidrug resistant ovarian cancer. Mol. Pharm. 2011, 8, 260–269. · DOI
  20. Chen, Y. Y.; Tai, Y. C. Hsa_circ_0006404 and hsa_circ_0000735 regulated ovarian cancer response to docetaxel treatment via regulating p-GP expression. Biochem. Genet. 2022, 60, 395–414. · DOI
  21. Qiu, L. Y.; Wang, J. K.; Chen, M.; Chen, F. Y.; Tu, W. L. Exosomal microRNA-146a derived from mesenchymal stem cells increases the sensitivity of ovarian cancer cells to docetaxel and taxane via a LAMC2-mediated PI3K/Akt axis. Int. J. Mol. Med. 2020, 46, 609–620. · DOI · Paper page
  22. Bai, X. W.; Wong, C. C.; Pan, Y. S.; Chen, H. R.; Liu, W. X.; Zhai, J. N.; Kang, W.; Shi, Y.; Yamamoto, M.; Tsukamoto, T. et al. Loss of YTHDF1 in gastric tumors restores sensitivity to antitumor immunity by recruiting mature dendritic cells. J. Immunother. Cancer 2022, 10, e003663. · DOI
  23. Han, D. L.; Liu, J.; Chen, C. Y.; Dong, L. H.; Liu, Y.; Chang, R. B.; Huang, X. N.; Liu, Y. Y.; Wang, J. Y.; Dougherty, U. et al. Anti-tumour immunity controlled through mRNA m6A methylation and YTHDF1 in dendritic cells. Nature 2019, 566, 270–274. · DOI · Paper page
  24. Shi, Y. F.; Du, L. M.; Lin, L. Y.; Wang, Y. Tumour-associated mesenchymal stem/stromal cells: Emerging therapeutic targets. Nat. Rev. Drug Discov. 2017, 16, 35–52. · DOI
  25. Quante, M.; Tu, S. P.; Tomita, H.; Gonda, T.; Wang, S. S. W.; Takashi, S.; Baik, G. H.; Shibata, W.; DiPrete, B.; Betz, K. S. et al. Bone marrow-derived myofibroblasts contribute to the mesenchymal stem cell niche and promote tumor growth. Cancer Cell 2011, 19, 257–272. · DOI
  26. Ren, G. W.; Zhao, X.; Wang, Y.; Zhang, X.; Chen, X. D.; Xu, C. L.; Yuan, Z. R.; Roberts, A. I.; Zhang, L. Y.; Zheng, B. et al. CCR2-dependent recruitment of macrophages by tumor-educated mesenchymal stromal cells promotes tumor development and is mimicked by TNFα. Cell Stem Cell 2012, 11, 812–824. · DOI
  27. Jung, Y.; Kim, J. K.; Shiozawa, Y.; Wang, J. C.; Mishra, A.; Joseph, J.; Berry, J. E.; McGee, S.; Lee, E.; Sun, H. L. et al. Recruitment of mesenchymal stem cells into prostate tumours promotes metastasis. Nat. Commun. 2013, 4, 1795. · DOI
  28. Zhang, F. S.; Guo, J. S.; Zhang, Z. H.; Qian, Y. P.; Wang, G.; Duan, M. Q.; Zhao, H. Y.; Yang, Z.; Jiang, X. F. Mesenchymal stem cell-derived exosome: A tumor regulator and carrier for targeted tumor therapy. Cancer Lett. 2022, 526, 29–40. · DOI · Paper page
  29. Fitts, C. A.; Ji, N.; Li, Y. S.; Tan, C. Exploiting exosomes in cancer liquid biopsies and drug delivery. Adv. Healthc. Mater. 2019, 8, 1801268. · DOI
  30. Herrmann, I. K.; Wood, M. J. A.; Fuhrmann, G. Extracellular vesicles as a next-generation drug delivery platform. Nat. Nanotechnol. 2021, 16, 748–759. · DOI · Paper page
  31. Yeo, R. W. Y.; Lai, R. C.; Zhang, B.; Tan, S. S.; Yin, Y. J.; Teh, B. J.; Lim, S. K. Mesenchymal stem cell: An efficient mass producer of exosomes for drug delivery. Adv. Drug Deliv. Rev. 2013, 65, 336–341. · DOI · Paper page
  32. Li, W. Z.; Shao, B.; Liu, C. L.; Wang, H. Y.; Zheng, W. S.; Kong, W. Y.; Liu, X. R.; Xu, G. B.; Wang, C.; Li, H. P. et al. Noninvasive diagnosis and molecular phenotyping of breast cancer through microbead-assisted flow cytometry detection of tumor-derived extracellular vesicles. Small Methods 2018, 2, 1800122. · DOI
  33. Théry, C.; Zitvogel, L.; Amigorena, S. Exosomes: Composition, biogenesis and function. Nat. Rev. Immunol. 2002, 2, 569–579. · DOI
  34. Riazifar, M.; Mohammadi, M. R.; Pone, E. J.; Yeri, A.; Lässer, C.; Segaliny, A. I.; McIntyre, L. L.; Shelke, G. V.; Hutchins, E.; Hamamoto, A. et al. Stem cell-derived exosomes as nanotherapeutics for autoimmune and neurodegenerative disorders. ACS Nano 2019, 13, 6670–6688. · DOI · Paper page
  35. Melzer, C.; Rehn, V.; Yang, Y. Y.; Bähre, H.; von der Ohe, J.; Hass, R. Taxol-loaded MSC-derived exosomes provide a therapeutic vehicle to target metastatic breast cancer and other carcinoma cells. Cancers 2019, 11, 798. · DOI
  36. Kalluri, R.; LeBleu, V. S. The biology, function, and biomedical applications of exosomes. Science 2020, 367, eaau6977. · DOI · Paper page
  37. Cheng, Q.; Wei, T.; Farbiak, L.; Johnson, L. T.; Dilliard, S. A.; Siegwart, D. J. Selective organ targeting (SORT) nanoparticles for tissue-specific mRNA delivery and CRISPR-Cas gene editing. Nat. Nanotechnol. 2020, 15, 313–320. · DOI · Paper page
  38. Blanco, E.; Shen, H. F.; Ferrari, M. Principles of nanoparticle design for overcoming biological barriers to drug delivery. Nat. Biotechnol. 2015, 33, 941–951. · DOI · Paper page
  39. Yang, Z. G.; Xie, J.; Zhu, J.; Kang, C.; Chiang, C.; Wang, X. M.; Wang, X. B.; Kuang, T. R.; Chen, F.; Chen, Z. et al. Functional exosome-mimic for delivery of siRNA to cancer: In vitro and in vivo evaluation. J. Control. Release 2016, 243, 160–171. · DOI
  40. Usman, W. M.; Pham, T. C.; Kwok, Y. Y.; Vu, L. T.; Ma, V.; Peng, B. Y.; Chan, Y. S.; Wei, L. K.; Chin, S. M.; Azad, A. et al. Efficient RNA drug delivery using red blood cell extracellular vesicles. Nat. Commun. 2018, 9, 2359. · DOI · Paper page
  41. Li, C. H.; Zhou, J. H.; Wu, Y. D.; Dong, Y. L.; Du, L. L.; Yang, T. R.; Wang, Y. H.; Guo, S.; Zhang, M. J.; Hussain, A. et al. Core role of hydrophobic core of polymeric nanomicelle in endosomal escape of siRNA. Nano Lett. 2021, 21, 3680–3689. · DOI
  42. Juliane, N.; Szoka, F. C. Nucleic acid delivery: The missing pieces of the puzzle. Acc. Chem. Res. 2012, 45, 1153–1162. · DOI
  43. Lu, H. T.; Zhang, Q. F.; He, S. S.; Liu, S.; Xie, Z. G.; Li, X. Y.; Huang, Y. B. Reduction-sensitive fluorinated-Pt(IV) universal transfection nanoplatform facilitating CT45-targeted CRISPR/dCas9 activation for synergistic and individualized treatment of ovarian cancer. Small 2021, 17, 2102494. · DOI
  44. Zhou, Z. J.; Lv, J. C.; Yu, H.; Han, J.; Yang, X.; Feng, D. X.; Wu, Q. K.; Yuan, B. R.; Lu, Q.; Yang, H. W. Mechanism of RNA modification N6-methyladenosine in human cancer. Mol. Cancer 2020, 19, 104. · DOI
  45. Chen, Z. Y.; Zhong, X. L.; Xia, M.; Zhong, J. The roles and mechanisms of the m6A reader protein YTHDF1 in tumor biology and human diseases. Mol. Ther. Nucleic Acids 2021, 26, 1270–1279. · DOI
  46. Mosca, L.; Ilari, A.; Fazi, F.; Assaraf, Y. G.; Colotti, G. Taxanes in cancer treatment: Activity, chemoresistance and its overcoming. Drug Resist. Updat. 2021, 54, 100742. · DOI
  47. Wanderley, C. W.; Colón, D. F.; Luiz, J. P. M.; Oliveira, F. F.; Viacava, P. R.; Leite, C. A.; Pereira, J. A.; Silva, C. M.; Silva, C. R.; Silva, R. L. et al. Paclitaxel reduces tumor growth by reprogramming tumor-associated macrophages to an M1 profile in a TLR4-dependent manner. Cancer Res. 2018, 78, 5891–5900. · DOI · Paper page
  48. Pan, X. P.; Hong, X. L.; Li, S. M.; Meng, P.; Xiao, F. METTL3 promotes adriamycin resistance in MCF-7 breast cancer cells by accelerating pri-microRNA-221-3p maturation in a m6A-dependent manner. Exp. Mol. Med. 2021, 53, 91–102. · DOI
  49. Feng, S. T.; Qiu, G. Q.; Yang, L. H.; Feng, L. H.; Fan, X.; Ren, F.; Huang, K. D.; Chen, Y. D. Omeprazole improves chemosensitivity of gastric cancer cells by m6A demethylase FTO-mediated activation of mTORC1 and DDIT3 up-regulation. Biosci. Rep. 2021, 41, BSR20200842. · DOI
  50. Shi, Y. L.; Fan, S. Q.; Wu, M. G.; Zuo, Z. X.; Li, X. Y.; Jiang, L. P.; Shen, Q. S.; Xu, P. F.; Zeng, L.; Zhou, Y. C. et al. YTHDF1 links hypoxia adaptation and non-small cell lung cancer progression. Nat. Commun. 2019, 10, 4892. · DOI
  51. Xu, J. J.; Wan, Z.; Tang, M. Y.; Lin, Z. J.; Jiang, S.; Ji, L.; Gorshkov, K.; Mao, Q. J.; Xia, S. J.; Cen, D. et al. N6-methyladenosine-modified CircRNA-SORE sustains sorafenib resistance in hepatocellular carcinoma by regulating β-catenin signaling. Mol. Cancer 2020, 19, 163. · DOI
  52. Zhang, Y.; Kang, M.; Zhang, B.; Meng, F. C.; Song, J.; Kaneko, H.; Shimamoto, F.; Tang, B. m6A modification-mediated CBX8 induction regulates stemness and chemosensitivity of colon cancer via upregulation of LGR5. Mol. Cancer 2019, 18, 185. · DOI
  53. Zhou, T. F.; Li, S. C.; Xiang, D. M.; Liu, J. Y.; Sun, W.; Cui, X. L.; Ning, B. F.; Li, X.; Cheng, Z.; Jiang, W. Q. et al. m6A RNA methylation-mediated HNF3γ reduction renders hepatocellular carcinoma dedifferentiation and sorafenib resistance. Signal Transduct. Target. Ther. 2020, 5, 296. · DOI
  54. Sun, Y.; Dong, D.; Xia, Y. H.; Hao, L. Y.; Wang, W.; Zhao, C. H. YTHDF1 promotes breast cancer cell growth, DNA damage repair and chemoresistance. Cell Death Dis. 2022, 13, 230. · DOI
  55. Tang, B.; Yang, Y. H.; Kang, M.; Wang, Y. S.; Wang, Y.; Bi, Y.; He, S. Q.; Shimamoto, F. m6A demethylase ALKBH5 inhibits pancreatic cancer tumorigenesis by decreasing WIF-1 RNA methylation and mediating Wnt signaling. Mol. Cancer 2020, 19, 3. · DOI
  56. Naseri, Z.; Oskuee, R. K.; Jaafari, M. R.; Forouzandeh Moghadam, M. Exosome-mediated delivery of functionally active miRNA-142-3p inhibitor reduces tumorigenicity of breast cancer in vitro and in vivo. Int. J. Nanomedicine 2018, 13, 7727–7747. · DOI
  57. Jarad, G.; Miner, J. H. Update on the glomerular filtration barrier. Curr. Opin. Nephrol. Hypertens. 2009, 18, 226–232. · DOI
  58. Deleavey, G. F.; Damha, M. J. Designing chemically modified oligonucleotides for targeted gene silencing. Chem. Biol. 2012, 19, 937–954. · DOI
  59. Wei, H. X.; Chen, F.; Chen, J. Y.; Lin, H. F.; Wang, S. L.; Wang, Y. Q.; Wu, C. Y.; Lin, J. H.; Zhong, G. X. Mesenchymal stem cell derived exosomes as nanodrug carrier of doxorubicin for targeted osteosarcoma therapy via SDF1-CXCR4 axis. Int. J. Nanomedicine 2022, 17, 3483–3495. · DOI
  60. Sun, D. M.; Zhuang, X. Y.; Zhang, S. Q.; Deng, Z. B.; Grizzle, W.; Miller, D.; Zhang, H. G. Exosomes are endogenous nanoparticles that can deliver biological information between cells. Adv. Drug Deliv. Rev. 2013, 65, 342–347. · DOI
  61. Kamerkar, S.; LeBleu, V. S.; Sugimoto, H.; Yang, S. J.; Ruivo, C. F.; Melo, S. A.; Lee, J. J.; Kalluri, R. Exosomes facilitate therapeutic targeting of oncogenic KRAS in pancreatic cancer. Nature 2017, 546, 498–503. · DOI · Paper page
  62. Zhu, Y. N.; Li, J.; Yang, H.; Yang, X. Y.; Zhang, Y.; Yu, X. C.; Li, Y.; Chen, G. X.; Yang, Z. Z. The potential role of m6A reader YTHDF1 as diagnostic biomarker and the signaling pathways in tumorigenesis and metastasis in pan-cancer. Cell Death Discov. 2023, 9, 34. · DOI
  63. Lin, W. Z.; Chen, L.; Zhang, H. J.; Qiu, X. X.; Huang, Q. T.; Wan, F. Z.; Le, Z. Y.; Geng, S. K.; Zhang, A. L.; Qiu, S. F. et al. Tumor-intrinsic YTHDF1 drives immune evasion and resistance to immune checkpoint inhibitors via promoting MHC-I degradation. Nat. Commun. 2023, 14, 265. · DOI
  64. You, Q.; Wang, F.; Du, R.; Pi, J. N.; Wang, H. Y.; Huo, Y.; Liu, J. Y.; Wang, C.; Yu, J.; Yang, Y. L. et al. m6A reader YTHDF1-targeting engineered small extracellular vesicles for gastric cancer therapy via epigenetic and immune regulation. Adv. Mater. 2023, 35, 2204910. · DOI

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Metadata

Authors
Du, R., You, Q., Liu, J., Wang, C., Zhu, L., & Yang, Y.
Venue
Nano Research
Publisher
Tsinghua University Press
Published
2023-10-13
Volume
16
Issue
12
Pages
13309-13321
ISSN
  • 1998-0124
  • 1998-0000
DOI
10.1007/s12274-023-6105-0
Cited by
19
References
3
Language
en
Licence

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