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Research Article

Study on tumour cell-derived hybrid exosomes as dasatinib nanocarriers for pancreatic cancer therapy

, ORCID Icon, , , , , , , , , , & ORCID Icon show all
Pages 532-546 | Received 22 May 2023, Accepted 23 Sep 2023, Published online: 05 Oct 2023

References

  • Siegel RL, Miller KD, Fuchs HE, et al. Cancer statistics, 2022. CA Cancer J Clin. 2022;72(1):7–33. doi: 10.3322/caac.21708.
  • Seo YD, Katz MH. Preoperative therapy for pancreatic adenocarcinoma-precision beyond anatomy. Cancer. 2022;128(16):3041–3056. doi: 10.1002/cncr.34273.
  • Gaianigo N, Melisi D, Carbone C. EMT and treatment resistance in pancreatic cancer. Cancers. 2017;9(9):122. doi: 10.3390/cancers9090122.
  • Yu S, Zhang C, Xie KP. Therapeutic resistance of pancreatic cancer: roadmap to its reversal. Biochim Biophys Acta Rev Cancer. 2021;1875(1):188461. doi: 10.1016/j.bbcan.2020.188461.
  • Chen X, Liang H, Zhang J, et al. Secreted microRNAs: a new form of intercellular communication. Trends Cell Biol. 2012;22(3):125–132. doi: 10.1016/j.tcb.2011.12.001.
  • Kumar D, Gupta D, Shankar S, et al. Biomolecular characterization of exosomes released from cancer stem cells: possible implications for biomarker and treatment of cancer. Oncotarget. 2015;6(5):3280–3291. doi: 10.18632/oncotarget.2462.
  • Lee JE, Moon PG, Lee IK, et al. Proteomic analysis of extracellular vesicles released by adipocytes of Otsuka Long-Evans Tokushima fatty (OLETF) rats. Protein J. 2015;34(3):220–235. doi: 10.1007/s10930-015-9616-z.
  • Zhang HG, Grizzle WE. Exosomes: a novel pathway of local and distant intercellular communication that facilitates the growth and metastasis of neoplastic lesions. Am J Pathol. 2014;184(1):28–41. doi: 10.1016/j.ajpath.2013.09.027.
  • Khongkow M, Yata T, Boonrungsiman S, et al. Surface modification of gold nanoparticles with neuron-targeted exosome for enhanced blood-brain barrier penetration. Sci Rep. 2019;9(1):8278. doi: 10.1038/s41598-019-44569-6.
  • Wang J, Chen P, Dong Y, et al. Designer exosomes enabling tumor targeted efficient chemo/gene/photothermal therapy. Biomaterials. 2021;276:121056. doi: 10.1016/j.biomaterials.2021.121056.
  • Cheng G, Li W, Ha L, et al. Self-assembly of extracellular vesicle-like metal-organic framework nanoparticles for protection and intracellular delivery of biofunctional proteins. J Am Chem Soc. 2018;140(23):7282–7291. doi: 10.1021/jacs.8b03584.
  • Yong T, Zhang X, Bie N, et al. Tumor exosome-based nanoparticles are efficient drug carriers for chemotherapy. Nat Commun. 2019;10(1):3838. doi: 10.1038/s41467-019-11718-4.
  • Sancho-Albero M, Martín-Pardillos A, Lujan L, et al. Exosomes loaded with ultrasmall Pt nanoparticles: a novel low-toxicity alternative to cisplatin. J Nanobiotechnology. 2022;20(1):473. doi: 10.1186/s12951-022-01675-4.
  • Mo J, Da X, Li Q, et al. The study of exosomes-encapsulated mPEG-PLGA polymer drug-loaded particles for targeted therapy of liver cancer. J Oncol. 2022;2022:4234116–4234110. doi: 10.1155/2022/4234116.
  • Cheng L, Zhang X, Tang J, et al. Gene-engineered exosomes-thermosensitive liposomes hybrid nanovesicles by the blockade of CD47 signal for combined photothermal therapy and cancer immunotherapy. Biomaterials. 2021;275:120964. doi: 10.1016/j.biomaterials.2021.120964.
  • Sato YT, Umezaki K, Sawada S, et al. Engineering hybrid exosomes by membrane fusion with liposomes. Sci Rep. 2016;6(1):21933. doi: 10.1038/srep21933.
  • Lin Y, Wu J, Gu W, et al. Exosome-liposome hybrid nanoparticles deliver CRISPR/Cas9 system in MSCs. Adv Sci. 2018;5:1700611. doi: 10.1002/advs.201700611.
  • Rayamajhi S, Nguyen TDT, Marasini R, et al. Macrophage-derived exosome-mimetic hybrid vesicles for tumor targeted drug delivery. Acta Biomater. 2019;94:482–494. doi: 10.1016/j.actbio.2019.05.054.
  • Sun L, Fan M, Huang D, et al. Clodronate-loaded liposomal and fibroblast-derived exosomal hybrid system for enhanced drug delivery to pulmonary fibrosis. Biomaterials. 2021;271:120761. doi: 10.1016/j.biomaterials.2021.120761.
  • Piffoux M, Silva AKA, Wilhelm C, et al. Modification of extracellular vesicles by fusion with liposomes for the design of personalized biogenic drug delivery systems. ACS Nano. 2018;12(7):6830–6842. doi: 10.1021/acsnano.8b02053.
  • Lutz MP, Esser IB, Flossmann-Kast BB, et al. Overexpression and activation of the tyrosine kinase src in human pancreatic carcinoma. Biochem Biophys Res Commun. 1998;243(2):503–508. doi: 10.1006/bbrc.1997.8043.
  • Mahajan K, Coppola D, Chen YA, et al. Ack1 tyrosine kinase activation correlates with pancreatic cancer progression. Am J Pathol. 2012;180(4):1386–1393. doi: 10.1016/j.ajpath.2011.12.028.
  • Duong HQ, Yi YW, Kang HJ, et al. Combination of dasatinib and gemcitabine reduces the ALDH1A1 expression and the proliferation of gemcitabine-resistant pancreatic cancer MIA PaCa-2 cells. Int J Oncol. 2014;44(6):2132–2138. doi: 10.3892/ijo.2014.2357.
  • Morton JP, Karim SA, Graham K, et al. Dasatinib inhibits the development of metastases in a mouse model of pancreatic ductal adenocarcinoma. Gastroenterology. 2010;139(1):292–303. doi: 10.1053/j.gastro.2010.03.034.
  • Ma L, Wei J, Su GH, et al. Dasatinib can enhance paclitaxel and gemcitabine inhibitory activity in human pancreatic cancer cells. Cancer Biol Ther. 2019;20(6):855–865. doi: 10.1080/15384047.2019.1579956.
  • Zhang Y, Zeng X, Wang H, et al. Dasatinib self-assembled nanoparticles decorated with hyaluronic acid for targeted treatment of tumors to overcome multidrug resistance. Drug Deliv. 2021;28(1):670–679. doi: 10.1080/10717544.2021.1905751.
  • Dong C, Li B, Li Z, et al. Dasatinib-loaded albumin nanoparticles possess diminished endothelial cell barrier disruption and retain potent antileukemia cell activity. Oncotarget. 2016;7(31):49699–49709. doi: 10.18632/oncotarget.10435.
  • Zeng F, Ju RJ, Liu L, et al. Efficacy in treating lung metastasis of invasive breast cancer with functional vincristine plus dasatinib liposomes. Pharmacology. 2018;101(1-2):43–53. doi: 10.1159/000480737.
  • Qian X, Xie F, Cui D. Exploring purification methods of exosomes from different biological samples. Biomed Res Int. 2023;2023:2336536. doi: 10.1155/2023/2336536.
  • Xu L, Faruqu FN, Lim YM, et al. Exosome-mediated RNAi of PAK4 prolongs survival of pancreatic cancer mouse model after loco-regional treatment. Biomaterials. 2021;264:120369. doi: 10.1016/j.biomaterials.2020.120369.
  • Behroozi F, Abdkhodaie MJ, Abandansari HS, et al. Engineering folate-targeting diselenide-containing triblock copolymer as a redox-responsive shell-sheddable micelle for antitumor therapy in vivo. Acta Biomater. 2018;76:239–256. doi: 10.1016/j.actbio.2018.05.031.
  • Zhang L, Lin Z, Chen Y, et al. Co-delivery of docetaxel and resveratrol by liposomes synergistically boosts antitumor efficiency against prostate cancer. Eur J Pharm Sci. 2022;174:106199. doi: 10.1016/j.ejps.2022.106199.
  • Xiong G, Wu Z, Yi J, et al. ADMETlab 2.0: an integrated online platform for accurate and comprehensive predictions of ADMET properties. Nucleic Acids Res. 2021;49(W1):W5–W14. doi: 10.1093/nar/gkab255.
  • Lipinski CA, Lombardo F, Dominy BW, et al. Experimental and computational approaches to estimate solubility and permeability in drug discovery and development settings. Adv Drug Deliv Rev. 2001;46(1-3):3–26. doi: 10.1016/s0169-409x(00)00129-0.
  • Trott O, Olson AJ. AutoDock vina: improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading. J Comput Chem. 2010;31(2):455–461. doi: 10.1002/jcc.21334.
  • Burley SK, Berman HM, Kleywegt GJ, et al. Protein data bank (PDB): the single global macromolecular structure archive. Methods Mol Biol. 2017;1607:627–641. doi: 10.1007/978-1-4939-7000-1_26.
  • Landrum G. RDKit: a software suite for cheminformatics, computational chemistry, and predictive modeling. Greg Landrum. 2013;8:31.
  • DeLano WL. Pymol: an open-source molecular graphics tool. CCP4 Newslett Pro Crystallogr. 2002;40(1):82–92.
  • Laskowski RA, Swindells MB. LigPlot+: multiple ligand-protein interaction diagrams for drug discovery. J Chem Inf Model. 2011;51(10):2778–2786. doi: 10.1021/ci200227u.
  • Chee CE, Krishnamurthi S, Nock CJ, et al. Phase II study of dasatinib (BMS-354825) in patients with metastatic adenocarcinoma of the pancreas. Oncologist. 2013;18(10):1091–1092. doi: 10.1634/theoncologist.2013-0255.
  • Cabrera E, Welch LC, Robinson MR, et al. Cryopreservation and the freeze–thaw stress response in yeast. Genes (Basel). 2020;11(8):835. doi: 10.3390/genes11080835.
  • Rudolph AS, Crowe JH. Membrane stabilization during freezing: the role of two natural cryoprotectants trehalose and proline. Cryobiology. 1985;22(4):367–377. doi: 10.1016/0011-2240(85)90184-1.
  • Costa AP, Xu X, Burgess DJ. Freeze-anneal-thaw cycling of unilamellar liposomes: effect on encapsulation efficiency. Pharm Res. 2014;31(1):97–103. doi: 10.1007/s11095-013-1135-z.
  • Siow LF, Rades T, Lim MH. Characterizing the freezing behavior of liposomes as a tool to understand the cryopreservation procedures. Cryobiology. 2007;55(3):210–221. doi: 10.1016/j.cryobiol.2007.08.002.
  • Meyuhas D, Nir S, Lichtenberg D. Aggregation of phospholipid vesicles by water-soluble polymers. Biophys J. 1996;71(5):2602–2612. doi: 10.1016/S0006-3495(96)79452-3.
  • Lentz BR, Lee J. Poly(ethylene glycol) (PEG) mediated fusion between pure lipid bilayers a mechanism in common with viral fusion and secretory vesicle release. Mol Membr Biol. 1999;16(4):279–296. doi: 10.1080/096876899294508.
  • Litschel T, Ganzinger KA, Movinkel T, et al. Freeze-thaw cycles induce content exchange between cell-sized lipid vesicles. New J Phys. 2018;20(5):055008. doi: 10.1088/1367-2630/aabb96.
  • Gurung S, Perocheau D, Touramanidou L, et al. The exosome journey: from biogenesis to uptake and intracellular signalling. Cell Commun Signal. 2021;19(1):47. doi: 10.1186/s12964-021-00730-1.
  • van Niel G, D'Angelo G, Raposo G. Shedding light on the cell biology of extracellular vesicles. Nat Rev Mol Cell Biol. 2018;19(4):213–228. doi: 10.1038/nrm.2017.125.
  • Donoso‐Quezada J, Ayala‐Mar S, González‐Valdez J. The role of lipids in exosome biology and intercellular communication: function, analytics and applications. Traffic. 2021;22(7):204–220. doi: 10.1111/tra.12803.
  • Toda Y, Takata K, Nakagawa Y, et al. Effective internalization of U251-MG-secreted exosomes into cancer cells and characterization of their lipid components. Biochem Biophys Res Commun. 2015;456(3):768–773. doi: 10.1016/j.bbrc.2014.12.015.
  • Zhan Q, Yi K, Li X, et al. Phosphatidylcholine-engineered exosomes for enhanced tumor cell uptake and intracellular antitumor drug delivery. Macromol Biosci. 2021;21:e2100042. doi: 10.1002/mabi.202100042.
  • Smyth TJ, Redzic JS, Graner MW, et al. Examination of the specificity of tumor cell derived exosomes with tumor cells in vitro. Biochim Biophys Acta. 2014;1838(11):2954–2965. doi: 10.1016/j.bbamem.2014.07.026.
  • Mulcahy LA, Pink RC, Carter DR. Routes and mechanisms of extracellular vesicle uptake. J Extracell Vesicles. 2014;3(1):24641. doi: 10.3402/jev.v3.24641.
  • Escrevente C, Keller S, Altevogt P, et al. Interaction and uptake of exosomes by ovarian cancer cells. BMC Cancer. 2011;11(1):108. doi: 10.1186/1471-2407-11-108.
  • Rana S, Yue S, Stadel D, et al. Toward tailored exosomes: the exosomal tetraspanin web contributes to target cell selection. Int J Biochem Cell Biol. 2012;44(9):1574–1584. doi: 10.1016/j.biocel.2012.06.018.
  • Horibe S, Tanahashi T, Kawauchi S, et al. Mechanism of recipient cell-dependent differences in exosome uptake. BMC Cancer. 2018;18(1):47. doi: 10.1186/s12885-017-3958-1.
  • Parolini I, Federici C, Raggi C, et al. Microenvironmental pH is a key factor for exosome traffic in tumor cells. J Biol Chem. 2009;284(49):34211–34222. doi: 10.1074/jbc.M109.041152.
  • Lima LG, Ham S, Shin H, et al. Tumor microenvironmental cytokines bound to cancer exosomes determine uptake by cytokine receptor-expressing cells and biodistribution. Nat Commun. 2021;12(1):3543. doi: 10.1038/s41467-021-23946-8.
  • Verhoef JJ, Anchordoquy TJ. Questioning the use of PEGylation for drug delivery. Drug Deliv Transl Res. 2013;3(6):499–503. doi: 10.1007/s13346-013-0176-5.
  • Hong RL, Huang CJ, Tseng YL, et al. Direct comparison of liposomal doxorubicin with or without polyethylene glycol coating in C-26 tumor-bearing mice: is surface coating with polyethylene glycol beneficial? Clin Cancer Res. 1999;5(11):3645–3652.
  • Sadzuka Y, Kishi K, Hirota S, et al. Effect of polyethyleneglycol (PEG) chain on cell uptake of PEG-modified liposomes. J Liposome Res. 2003;13(2):157–172. doi: 10.1081/lpr-120020318.
  • Laulagnier K, Motta C, Hamdi S, et al. Mast cell- and dendritic cell-derived exosomes display a specific lipid composition and an unusual membrane organization. Biochem J. 2004;380(Pt 1):161–171. doi: 10.1042/BJ20031594.
  • Lv Q, Cheng L, Lu Y, et al. Thermosensitive exosome–liposome hybrid nanoparticle‐mediated chemoimmunotherapy for improved treatment of metastatic peritoneal cancer. Adv Sci. 2020;7:2000515. doi: 10.1002/advs.202000515.
  • Ci T, Li H, Chen G, et al. Cryo-shocked cancer cells for targeted drug delivery and vaccination. Sci Adv. 2020;6(50):eabc3013. doi: 10.1126/sciadv.abc3013.
  • Chen MM, Li J, Mills GB, et al. Predicting cancer cell line dependencies from the protein expression data of reverse-phase protein arrays. J Clin Oncol Clin Cancer Inform. 2020;4:357–366. doi: 10.1200/CCI.19.00144.
  • McGeary SE, Lin KS, Shi CY, et al. The biochemical basis of microRNA targeting efficacy. Science. 2019;366(6472):eaav1741. doi: 10.1126/science.aav1741.