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Research progress in membrane fusion-based hybrid exosomes for drug delivery systems

Liu, Anqi, Yang, Gang, Liu, Yuehua, Liu, Tingjiao·2022·Frontiers in Bioengineering and Biotechnology
DOI 10.3389/fbioe.2022.939441PMC PMC9424752
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Abstract

Liposomes are the earliest and most widely used nanoparticles for targeted drug delivery. Exosomes are nanosized membrane-bound particles and important mediators of intercellular communication. Combining liposomes and exosomes using various membrane fusion methods gives rise to a novel potential drug delivery system called membrane fusion-based hybrid exosomes (MFHE). These novel MFHEs not only exhibit potential advantageous features, such as high drug loading rate and targeted cellular uptake via surface modification, but are also endowed with high biocompatibility and low immunogenicity. Here, we provide an overview of MFHEs’ various preparation methods, characterization strategies, and their applications for disease treatment and scientific research.

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FIGURE 1 Membrane fusion-based hybrid exosome preparation and applications.
FIGURE 1 Membrane fusion-based hybrid exosome preparation and applications.CC BY · PubMed Central
FIGURE 2 Characterization of membrane fusion-based hybrid exosomes. (A) FRET assay to characterize membrane fusion (Thorsteinsson et al., 2020) (B) Immunomagnetic bead method to characterize membrane fusion (Lv et al., 2020) (C) TEM & confocal fluorescence microscopy analysis to visualize membrane fusion (Singh et al., 2021).
FIGURE 2 Characterization of membrane fusion-based hybrid exosomes. (A) FRET assay to characterize membrane fusion (Thorsteinsson et al., 2020) (B) Immunomagnetic bead method to characterize membrane fusion (Lv et al., 2020) (C) TEM & confocal fluorescence microscopy analysis to visualize membrane fusion (Singh et al., 2021).CC BY · PubMed Central
FIGURE 3 Applications of membrane fusion-based hybrid exosomes. (A) Characterization of the therapeutic benefits of MFHE (G/D-gETL NPs) treatment in patient-derived mPC tumor xenografts (Lv et al., 2020) (B) The antitumor activity of MFHEs (miR497/TP-HENPs) in vivo (Li et al., 2022) (C) MFHEs carrying antagomir-188 are able to reverse aging-related bone loss (Hu et al., 2021).
FIGURE 3 Applications of membrane fusion-based hybrid exosomes. (A) Characterization of the therapeutic benefits of MFHE (G/D-gETL NPs) treatment in patient-derived mPC tumor xenografts (Lv et al., 2020) (B) The antitumor activity of MFHEs (miR497/TP-HENPs) in vivo (Li et al., 2022) (C) MFHEs carrying antagomir-188 are able to reverse aging-related bone loss (Hu et al., 2021).CC BY · PubMed Central

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Research works printed but not linked: 80

  1. Abri Aghdam, 2019, Recent advances on thermosensitive and pH-sensitive liposomes employed in controlled release, J. Control. Release, 315, 1, 10.1016/j.jconrel.2019.09.018 · DOI
  2. Allmang, 1999, Functions of the exosome in rRNA, snoRNA and snRNA synthesis, EMBO J., 18, 5399, 10.1093/emboj/18.19.5399 · DOI
  3. Alvarez-Erviti, 2011, Delivery of siRNA to the mouse brain by systemic injection of targeted exosomes, Nat. Biotechnol., 29, 341, 10.1038/nbt.1807 · DOI · Paper page
  4. Antimisiaris, 2018, Exosomes and exosome-inspired vesicles for targeted drug delivery, Pharmaceutics, 10, 218, 10.3390/pharmaceutics10040218 · DOI
  5. Armstrong, 2018, Strategic design of extracellular vesicle drug delivery systems, Adv. drug Deliv. Rev., 130, 12, 10.1016/j.addr.2018.06.017 · DOI · Paper page
  6. Balint, 2014, Conductive polymers: Towards a smart biomaterial for tissue engineering, Acta biomater., 10, 2341, 10.1016/j.actbio.2014.02.015 · DOI
  7. Cheng, 2021, Gene-engineered exosomes-thermosensitive liposomes hybrid nanovesicles by the blockade of CD47 signal for combined photothermal therapy and cancer immunotherapy, Biomaterials, 275, 120964, 10.1016/j.biomaterials.2021.120964 · DOI
  8. Conner, 2003, Regulated portals of entry into the cell, Nature, 422, 37, 10.1038/nature01451 · DOI
  9. Contreras-Naranjo, 2017, Microfluidics for exosome isolation and analysis: Enabling liquid biopsy for personalized medicine, Lab. Chip, 17, 3558, 10.1039/c7lc00592j · DOI
  10. Costa, 2014, Freeze-anneal-thaw cycling of unilamellar liposomes: Effect on encapsulation efficiency, Pharm. Res., 31, 97, 10.1007/s11095-013-1135-z · DOI
  11. de Jong, 2019, Drug delivery with extracellular vesicles: From imagination to innovation, Acc. Chem. Res., 52, 1761, 10.1021/acs.accounts.9b00109 · DOI
  12. Dissanayake, 2021, Measurement of the size and concentration and zeta potential of extracellular vesicles using nanoparticle tracking analyzer, Methods Mol. Biol. Clift. N.J.), 2273, 207, 10.1007/978-1-0716-1246-0_15 · DOI
  13. Dosio, 2016, Hyaluronic acid for anticancer drug and nucleic acid delivery, Adv. drug Deliv. Rev., 97, 204, 10.1016/j.addr.2015.11.011 · DOI
  14. Evers, 2021, Functional siRNA delivery by extracellular vesicle-liposome hybrid nanoparticles, Adv. Healthc. Mater., 11, 2101202, 10.1002/adhm.202101202 · DOI
  15. Farooqi, 2018, Exosome biogenesis, bioactivities and functions as new delivery systems of natural compounds, Biotechnol. Adv., 36, 328, 10.1016/j.biotechadv.2017.12.010 · DOI · Paper page
  16. Filipe, 2010, Critical evaluation of Nanoparticle Tracking Analysis (NTA) by NanoSight for the measurement of nanoparticles and protein aggregates, Pharm. Res., 27, 796, 10.1007/s11095-010-0073-2 · DOI · Paper page
  17. George, 2019, Lung transplantation for idiopathic pulmonary fibrosis, Lancet. Respir. Med., 7, 271, 10.1016/s2213-2600(18)30502-2 · DOI
  18. Guimarães, 2021, Design of liposomes as drug delivery system for therapeutic applications, Int. J. Pharm., 601, 120571, 10.1016/j.ijpharm.2021.120571 · DOI
  19. Gustafson, 2015, Nanoparticle uptake: The phagocyte problem, Nano today, 10, 487, 10.1016/j.nantod.2015.06.006 · DOI
  20. Hartjes, 2019, Extracellular vesicle quantification and characterization: Common methods and emerging approaches, Bioengineering, 6, 7, 10.3390/bioengineering6010007 · DOI
  21. Hu, 2021, Exosome-guided bone targeted delivery of Antagomir-188 as an anabolic therapy for bone loss, Bioact. Mater., 6, 2905, 10.1016/j.bioactmat.2021.02.014 · DOI
  22. Jhan, 2020, Engineered extracellular vesicles with synthetic lipids via membrane fusion to establish efficient gene delivery, Int. J. Pharm., 573, 118802, 10.1016/j.ijpharm.2019.118802 · DOI
  23. Ji, 2022, Clodronate-nintedanib-loaded exosome-liposome hybridization enhances the liver fibrosis therapy by inhibiting Kupffer cell activity, Biomater. Sci., 10, 702, 10.1039/d1bm01663f · DOI
  24. Jiang, 2018, Arginine, glycine, aspartic acid peptide-modified paclitaxel and curcumin co-loaded liposome for the treatment of lung cancer: In vitro/vivo evaluation, Ijn, 2561, 10.2147/ijn.S157746 · DOI
  25. Jiang, 2008, Nanoparticle-mediated cellular response is size-dependent, Nat. Nanotech, 3, 145, 10.1038/nnano.2008.30 · DOI
  26. Kannavou, 2021, Engineered versus hybrid cellular vesicles as efficient drug delivery systems: A comparative study with brain targeted vesicles, Drug Deliv. Transl. Res., 11, 547, 10.1007/s13346-021-00900-1 · DOI
  27. Kumar Pramanik, 2017, Physicochemical characterizations of functional hybrid liposomal nanocarriers formed using photo-sensitive lipids, Sci. Rep., 7, 46257, 10.1038/srep46257 · DOI
  28. Lentz, 2007, PEG as a tool to gain insight into membrane fusion, Eur. Biophys. J., 36, 315, 10.1007/s00249-006-0097-z · DOI
  29. Li, 2015, Folate-polydiacetylene-liposome for tumor targeted drug delivery and fluorescent tracing, Colloids Surfaces B Biointerfaces, 134, 235, 10.1016/j.colsurfb.2015.07.008 · DOI
  30. Li, 2022, Exosome-liposome hybrid nanoparticle codelivery of TP and miR497 conspicuously overcomes chemoresistant ovarian cancer, J. Nanobiotechnol, 20, 50, 10.1186/s12951-022-01264-5 · DOI · Paper page
  31. Li, 2019, A nuclear targeted Dox-aptamer loaded liposome delivery platform for the circumvention of drug resistance in breast cancer, Biomed. Pharmacother., 117, 109072, 10.1016/j.biopha.2019.109072 · DOI
  32. Li, 2021, Artificial exosomes for translational nanomedicine, J. Nanobiotechnol, 19, 242, 10.1186/s12951-021-00986-2 · DOI · Paper page
  33. Lin, 2018, Exosome-liposome hybrid nanoparticles deliver CRISPR/Cas9 system in MSCs, Adv. Sci., 5, 1700611, 10.1002/advs.201700611 · DOI · Paper page
  34. Liu, 2021, Targeted liposomal drug delivery: A nanoscience and biophysical perspective, Nanoscale Horiz., 6, 78, 10.1039/d0nh00605j · DOI
  35. Lu, 2020, Bioinspired exosome-like therapeutics and delivery nanoplatforms, Biomaterials, 242, 119925, 10.1016/j.biomaterials.2020.119925 · DOI
  36. Lu, 2010, Intraperitoneal therapy for peritoneal cancer, Future Oncol., 6, 1625, 10.2217/fon.10.100 · DOI
  37. Lv, 2020, Thermosensitive exosome-liposome hybrid nanoparticle‐mediated chemoimmunotherapy for improved treatment of metastatic peritoneal cancer, Adv. Sci., 7, 2000515, 10.1002/advs.202000515 · DOI
  38. Ma, 2022, A cascade synergetic strategy induced by photothermal effect based on platelet exosome nanoparticles for tumor therapy, Biomaterials, 282, 121384, 10.1016/j.biomaterials.2022.121384 · DOI
  39. Midekessa, 2020, Zeta potential of extracellular vesicles: Toward understanding the attributes that determine colloidal stability, ACS omega, 5, 16701, 10.1021/acsomega.0c01582 · DOI
  40. Millard, 2018, mTHPC-loaded extracellular vesicles outperform liposomal and free mTHPC formulations by an increased stability, drug delivery efficiency and cytotoxic effect in tridimensional model of tumors, Drug Deliv., 25, 1790, 10.1080/10717544.2018.1513609 · DOI
  41. Mitchell, 2021, Engineering precision nanoparticles for drug delivery, Nat. Rev. Drug DiscovDrug Discov., 20, 101, 10.1038/s41573-020-0090-8 · DOI · Paper page
  42. Moghimipour, 2018, Folic acid-modified liposomal drug delivery strategy for tumor targeting of 5-fluorouracil, Eur. J. Pharm. Sci., 114, 166, 10.1016/j.ejps.2017.12.011 · DOI
  43. Murphy, 2019, Extracellular vesicle-based therapeutics: Natural versus engineered targeting and trafficking, Exp. Mol. Med., 51, 1, 10.1038/s12276-019-0223-5 · DOI
  44. Ning, 2021, Liposome-mediated detection of SARS-CoV-2 RNA-positive extracellular vesicles in plasma, Nat. Nanotechnol., 16, 1039, 10.1038/s41565-021-00939-8 · DOI
  45. Ou, 2021, Extracellular Vesicle (EV) biohybrid systems for cancer therapy: Recent advances and future perspectives, Seminars cancer Biol., 74, 45, 10.1016/j.semcancer.2021.02.006 · DOI
  46. Owensiii, 2006, Opsonization, biodistribution, and pharmacokinetics of polymeric nanoparticles, Int. J. Pharm., 307, 93, 10.1016/j.ijpharm.2005.10.010 · DOI · Paper page
  47. Paliwal, 2015, A review of mechanistic insight and application of pH-sensitive liposomes in drug delivery, Drug Deliv., 22, 231, 10.3109/10717544.2014.882469 · DOI
  48. Panahi, 2017, Recent advances on liposomal nanoparticles: Synthesis, characterization and biomedical applications, Artif. cells, nanomedicine, Biotechnol., 45, 788, 10.1080/21691401.2017.1282496 · DOI
  49. Piffoux, 2018, Modification of extracellular vesicles by fusion with liposomes for the design of personalized biogenic drug delivery systems, ACS Nano, 12, 6830, 10.1021/acsnano.8b02053 · DOI
  50. Rayamajhi, 2019, Macrophage-derived exosome-mimetic hybrid vesicles for tumor targeted drug delivery, Acta biomater., 94, 482, 10.1016/j.actbio.2019.05.054 · DOI · Paper page
  51. Reshke, 2020, Reduction of the therapeutic dose of silencing RNA by packaging it in extracellular vesicles via a pre-microRNA backbone, Nat. Biomed. Eng., 4, 52, 10.1038/s41551-019-0502-4 · DOI
  52. Rozo, 2020, Biophysical analysis of lipidic nanoparticles, Methods, 180, 45, 10.1016/j.ymeth.2020.05.001 · DOI
  53. Schindler, 2019, Exosomal delivery of doxorubicin enables rapid cell entry and enhanced in vitro potency, PloS one, 14, e0214545, 10.1371/journal.pone.0214545 · DOI
  54. Sercombe, 2015, Advances and challenges of liposome assisted drug delivery, Front. Pharmacol., 6, 286, 10.3389/fphar.2015.00286 · DOI
  55. Shah, 2020, Liposomes: Advancements and innovation in the manufacturing process, Adv. drug Deliv. Rev., 102, 10.1016/j.addr.2020.07.002 · DOI
  56. Simons, 2009, Exosomes - vesicular carriers for intercellular communication, Curr. Opin. Cell Biol., 21, 575, 10.1016/j.ceb.2009.03.007 · DOI
  57. Singh, 2021, Transplantation of engineered exosomes derived from bone marrow mesenchymal stromal cells ameliorate diabetic peripheral neuropathy under electrical stimulation, Bioact. Mater., 6, 2231, 10.1016/j.bioactmat.2021.01.008 · DOI
  58. Skotland, 2020, An emerging focus on lipids in extracellular vesicles, Adv. drug Deliv. Rev., 159, 308, 10.1016/j.addr.2020.03.002 · DOI
  59. Storm, 1998, Doxorubicin entrapped in sterically stabilized liposomes: Effects on bacterial blood clearance capacity of the mononuclear phagocyte system, Clin. cancer Res. official J. Am. Assoc. Cancer Res., 4, 111
  60. Sun, 2021, Clodronate-loaded liposomal and fibroblast-derived exosomal hybrid system for enhanced drug delivery to pulmonary fibrosis, Biomaterials, 271, 120761, 10.1016/j.biomaterials.2021.120761 · DOI
  61. Sutaria, 2017, Achieving the promise of therapeutic extracellular vesicles: The devil is in details of therapeutic loading, Pharm. Res., 34, 1053, 10.1007/s11095-017-2123-5 · DOI · Paper page
  62. Szebeni, 2015, Complement activation as a bioequivalence issue relevant to the development of generic liposomes and other nanoparticulate drugs, Biochem. biophysical Res. Commun., 468, 490, 10.1016/j.bbrc.2015.06.177 · DOI
  63. Tang, 2018, PEGylated liposomes as delivery systems for Gambogenic acid: Characterization and in vitro/in vivo evaluation, Colloids Surfaces B Biointerfaces, 172, 26, 10.1016/j.colsurfb.2018.08.022 · DOI
  64. Thakral, 2013, Electrical stimulation as an adjunctive treatment of painful and sensory diabetic neuropathy, J. Diabetes Sci. Technol., 7, 1202, 10.1177/193229681300700510 · DOI
  65. Théry, 2015, Diagnosis by extracellular vesicles, Nature, 523, 161, 10.1038/nature14626 · DOI
  66. Thorsteinsson, 2020, FRET-based assay for the quantification of extracellular vesicles and other vesicles of complex composition, Anal. Chem., 92, 15336, 10.1021/acs.analchem.0c02271 · DOI
  67. Tran, 2020, Exosomes and nanoengineering: A match made for precision therapeutics, Adv. Mat., 32, 1904040, 10.1002/adma.201904040 · DOI
  68. Udugama, 2020, Diagnosing COVID-19: The disease and tools for detection, ACS Nano, 14, 3822, 10.1021/acsnano.0c02624 · DOI
  69. van der Koog, 2022, Liposomes and extracellular vesicles as drug delivery systems: A comparison of composition, pharmacokinetics, and functionalization, Adv. Healthc. Mater., 11, 2100639, 10.1002/adhm.202100639 · DOI
  70. Wang, 2021, Challenges in the development and establishment of exosome-based drug delivery systems, J. Control. Release, 329, 894, 10.1016/j.jconrel.2020.10.020 · DOI
  71. Wang, Fabrication of an aptamer-coated liposome complex for the detection and profiling of exosomes based on terminal deoxynucleotidyl transferase-mediated signal amplification, ACS Appl. Mat. Interfaces, 12, 322, 10.1021/acsami.9b18869 · DOI
  72. Wang, 2019, Bridging exosome and liposome through zirconium-phosphate coordination chemistry: A new method for exosome detection, Chem. Commun., 55, 2708, 10.1039/c9cc00220k · DOI
  73. Wang, Detection of SARS-CoV-2 in different types of clinical specimens, JAMA, 323, 1843, 10.1001/jama.2020.3786 · DOI
  74. Weber, 2019, Functionalization of liposomes with hydrophilic polymers results in macrophage uptake independent of the protein corona, Biomacromolecules, 20, 2989, 10.1021/acs.biomac.9b00539 · DOI
  75. Yang, 2018, Extracellular vesicles as a platform for membrane-associated therapeutic protein delivery, J. Extracell. vesicles, 7, 1440131, 10.1080/20013078.2018.1440131 · DOI
  76. Yang, 2021, Sorting sub-150-nm liposomes of distinct sizes by DNA-brick-assisted centrifugation, Nat. Chem., 13, 335, 10.1038/s41557-021-00667-5 · DOI
  77. Zahednezhad, 2019, Liposome and immune system interplay: Challenges and potentials, J. Control. Release, 305, 194, 10.1016/j.jconrel.2019.05.030 · DOI
  78. Zhang, 2017, Liposomes equipped with cell penetrating peptide BR2 enhances chemotherapeutic effects of cantharidin against hepatocellular carcinoma, Drug Deliv., 24, 986, 10.1080/10717544.2017.1340361 · DOI
  79. Zhao, 2015, Nanocarriers for delivery of siRNA and co-delivery of siRNA and other therapeutic agents, Nanomedicine, 10, 2199, 10.2217/nnm.15.61 · DOI
  80. Zhou, 2022, Tumour‐derived extracellular vesicle membrane hybrid lipid nanovesicles enhance siRNA delivery by tumour‐homing and intracellular freeway transportation, J Extracell. Vesicle, 11, e12198, 10.1002/jev2.12198 · DOI

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Metadata

Authors
Liu, A., Yang, G., Liu, Y., & Liu, T.
Venue
Frontiers in Bioengineering and Biotechnology
Publisher
Frontiers Media SA
Published
2022-08-16
Volume
10
ISSN
2296-4185
DOI
10.3389/fbioe.2022.939441
PMC
PMC9424752
Cited by
88
References
4
Licence
creativecommons.org/licenses/by/4.0/ (vor)
Funders
National Natural Science Foundation of China

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