Skip to main content
SpringerLink
Log in

Prospects for the Use of Small Extracellular Vesicles as a Transport Vehicle through the Blood–Brain Barrier

  • REVIEW ARTICLES
  • Published:
Neurochemical Journal Aims and scope Submit manuscript

Abstract—Small extracellular vesicles (sEVs) are one of the most promising objects of research in neurobiology. This class of particles includes membrane vesicles up to 200 nm in size. The composition of sEVs includes proteins, lipids, nucleic acids, and low-molecular-weight metabolites. Due to structural features, sEVs are not absorbed by macrophages and can circulate in the blood for quite a long time compared to other nanoparticles. It is generally accepted that sEVs are secreted by all cells of the body and carry out intercellular signaling, which has not yet been elucidated in much detail. The ability of these nanoparticles to penetrate the blood–brain barrier allows us to consider them as promising vehicles for the transfer of drugs to the brain.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1.
Fig. 2.

REFERENCES

  1. Busatto, S., Morad, G., Guo, P., and Moses, M.A., FASEB Bioadv., 2021, vol. 3, pp. 665–675.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Thery, C., Witwer, K.W., Aikawa, E., Alcaraz, M.J., Anderson, J.D., Andriantsitohaina, R., Antoniou, A., Arab, T., Archer, F., Atkin-Smith, G.K., et al., J. Extracell. Ves., 2018, vol. 7, no. 1, p. 1535750.

    Article  Google Scholar 

  3. Kapogiannis, D., Mustapic, M., Shardell, M.D., Berkowitz, S.T., Diehl, T.C., Spangler, R.D., Tran, J., Lazaropoulos, M.P., Chawla, S., and Gulyani, S., JAMA Neurology, 2019, vol. 76, no. 11, pp. 1340–1351.

    Article  PubMed  PubMed Central  Google Scholar 

  4. Mustapic, M., Eitan, E., Werner, J.K., Berkowitz, S.T., Lazaropoulos, M.P., Tran, J., Goetzl, E.J., and Kapogiannis, D., Front. Neurosci., 2017, vol. 11, p. 278.

    Article  PubMed  PubMed Central  Google Scholar 

  5. Winston, C.N., Goetzl, E.J., Akers, J.C., Carter, B.S., Rockenstein, E.M., Galasko, D., Masliah, E., and Rissman, R.A., Alzheimer’s and Dementia: Diagnosis, Assessment and Disease Monitoring, 2016, vol. 3, pp. 63–72.

    PubMed  PubMed Central  Google Scholar 

  6. Goetzl, E.J., Kapogiannis, D., Schwartz, J.B., Lobach, I.V., Goetzl, L., Abner, E.L., Jicha, G.A., Karydas, A.M., Boxer, A., and Miller, B.L., FASEB J., 2016, vol. 30, no. 12, pp. 4141–4148.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Fiandaca, M.S., Kapogiannis, D., Mapstone, M., Boxer, A., Eitan, E., Schwartz, J.B., Abner, E.L., Petersen, R.C., Federoff, H.J., and Miller, B.L., Alzheimer’s & Dementia, 2015, vol. 11, no. 6, pp. 600–607.

    Article  Google Scholar 

  8. Ardashirova, N.S., Fedotova, E.Yu., and Illarioshkin, S.N., Neurochem. J., 2020, vol. 14, no. 2, pp. 127–132.

    Article  CAS  Google Scholar 

  9. Shi, M., Liu, C., Cook, T.J., Bullock, K.M., Zhao, Y., Ginghina, C., Li, Y., Aro, P., Dator, R., and He, C., Acta Neuropat., vol. 128, no. 5, pp. 639–650.

  10. Shi, M., Kovac, A., Korff, A., Cook, T.J., Ginghina, C., Bullock, K.M., Yang, L., Stewart, T., Zheng, D., and Aro, P., Alzheimer’s & Dementia, 2016, vol. 12, no. 11, pp. 1125–1131.

    Article  Google Scholar 

  11. Hamlett, E.D., Goetzl, E.J., Ledreux, A., Vasilevko, V., Boger, H.A., LaRosa, A., Clark, D., Carroll, S.L., Carmona-Iragui, M., and Fortea, J., Alzheimer’s & Dementia, 2017, vol. 13, no. 5, pp. 541–549.

    Article  Google Scholar 

  12. Sproviero, D., la Salvia, S., Giannini, M., Crippa, V., Gagliardi, S., Bernuzzi, S., Diamanti, L., Ceroni, M., Pansarasa, O., and Poletti, A., Front. Neurosci, 2018, vol. 12, p. 487.

    Article  PubMed  PubMed Central  Google Scholar 

  13. Ivanova, M.V., Chekanova, E.O., Belugin, B.V., Dolzhikova, I.V., Tutykhina, I.L., and Zakharova, M.N., Neurochem. J., 2020, vol. 14, no. 3, pp. 321–327.

    Article  CAS  Google Scholar 

  14. Martinez, B. and Peplow, P.V., Neural Regeneration Res., 2020, vol. 15, no. 4, pp. 606–619.

    Article  Google Scholar 

  15. Mycko, M.P. and Baranzini, S.E., Mult. Sclerosis J., 2020, vol. 26, no. 5, pp. 599–604.

    Article  Google Scholar 

  16. Ebrahimkhani, S., Beadnall, H.N., Wang, C., Suter, C.M., Barnett, M.H., Buckland, M.E., and Vafaee, F., Mol. Neurobiol., 2020, vol. 57, no. 2, pp. 1245–1258.

    Article  CAS  PubMed  Google Scholar 

  17. Xin, H., Wang, F., Li, Y., Lu, Q.-E., Cheung, W.L., Zhang, Y., Zhang, Z.G., and Chopp, M., Cell Transpl., 2017, vol. 26, no. 2, pp. 243–257.

    Article  Google Scholar 

  18. Chen, Y., Song, Y., Huang, J., Qu, M., Zhang, Y., Geng, J., Zhang, Z., Liu, J., and Yang, G.-Y., Front. Neurol., 2017, vol. 8, p. 57.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Song, Y., Li, Z., He, T., Qu, M., Jiang, L., Li, W., Shi, X., Pan, J., Zhang, L., and Wang, Y., Theranostics, 2019, vol. 9, no. 10, pp. 2910–2923.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Yakovlev, A.A., Neurochem. J., 2022, vol. 16, no. 2, pp. 121–129.

    Article  Google Scholar 

  21. Choi, J., Kim, S.Y., Kim, H., Lim, B.C., Hwang, H., Chae, J.H., Kim, K.J., Oh, S., Kim, E.Y., and Shin, J.-S., BMC Neurol., 2020, vol. 20, no. 1, p. 85.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Kumar, S., Vijayan, M., Bhatti, J.S., and Reddy, P.H., Prog. Mol. Biol. Transl. Sci., 2017, p. 146.

  23. Nasca, C., Dobbin, J., Bigio, B., Watson, K., de Angelis, P., Kautz, M., Cochran, A., Mathe, A.A., Kocsis, J.H., and Lee, F.S., Mol. Psychiatry, 2021, vol. 26, no. 9, pp. 5140–5149.

    Article  CAS  PubMed  Google Scholar 

  24. Gruzdev, S.K., Yakovlev, A.A., Druzhkova, T.A., Guekht, A.B., and Gulyaeva, N.V., Cell. Mol. Neurobiol., 2019, vol. 39, no. 6, pp. 729–750.

    Article  CAS  PubMed  Google Scholar 

  25. Yakovlev, A.A., Druzhkova, T.A., Nikolaev, R.V., Kuznetsova, V.E., Gruzdev, S.K., Guekht, A.B., and Gulyaeva, N.V., Neurochem. J., 2019, vol. 13, no. 4, pp. 385–390.

    Article  CAS  Google Scholar 

  26. Ceylan, D., Tufekci, K.U., Keskinoglu, P., Genc, S., and Ozerdem, A., J. Affect. D., vol. 262, 2020, pp. 99–107.

  27. Amoah, S.K., Rodriguez, B.A., Logothetis, C.N., Chander, P., Sellgren, C.M., Weick, J.P., Sheridan, S.D., Jantzie, L.L., Webster, M.J., and Mellios, N., Neuropsychopharmacology, 2020, vol. 45, no. 4, pp. 656–665.

    Article  CAS  PubMed  Google Scholar 

  28. Ma, Y., Li, C., Huang, Y., Wang, Y., Xia, X., and Zheng, J.C., Cell Comm. Signal, 2019, vol. 17, no. 1, p. 96.

    Article  Google Scholar 

  29. Sharma, G., Modgil, A., Layek, B., Arora, K., Sun, C., Law, B., and Singh, J., J. Control. Release, 2013, vol. 167, no. 1, pp. 1–10.

    Article  CAS  PubMed  Google Scholar 

  30. Gomez-Molina, C., Sandoval, M., Henzi, R., Ramirez, J.P., Varas-Godoy, M., Luarte, A., Lafourcade, C.A., Lopez-Verrilli, A., Smalla, K.H., and Kaehne, T., Int. J. Neuropsychopharmacol., 2019, vol. 22, no. 3, pp. 232–246.

    Article  CAS  PubMed  Google Scholar 

  31. Belhadj, Z., He, B., Deng, H., Song, S., Zhang, H., Wang, X., Dai, W., and Zhang, Q., J. Extracell. Ves., 2020, vol. 9, no. 1, p. 1806444.

    Article  CAS  Google Scholar 

  32. Kamerkar, S., Lebleu, V.S., Sugimoto, H., Yang, S., Ruivo, C.F., Melo, S.A., Lee, J.J., and Kalluri, R., Nature, 2017, vol. 546, no. 7659, pp. 498–503.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Shi, M., Sheng, L., Stewart, T., Zabetian, C.P., and Zhang, J., Prog. Neurobiol., 2019, vol. 175, pp. 96–106.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Banks, W.A., Sharma, P., Bullock, K.M., Hansen, K.M., Ludwig, N., and Whiteside, T.L., Int. J. Mol. Sci., 2020, vol. 21, no. 12, pp. 1–21.

    Google Scholar 

  35. Tkach, M. and Thery, C., Cell, 2016, vol. 164, no. 6, pp. 1226–1232.

    Article  CAS  PubMed  Google Scholar 

  36. Patil, S.M., Sawant, S.S., and Kunda, N.K., Eur. J. Pharm. Biopharm, 2020, vol. 154, pp. 259–269.

    Article  CAS  PubMed  Google Scholar 

  37. Heidarzadeh, M., Gursoy-Ozdemir, Y., Kaya, M., Eslami, AbrizA., Zarebkohan, A., Rahbarghazi, R., and Sokullu, E., Cell Biosci., 2021, vol. 11, no. 1, p. 142.

    Article  PubMed  PubMed Central  Google Scholar 

  38. Dardet, J.P., Serrano, N., Andras, I.E., and Toborek, M., Front. Drug Deliv., 2022, vol. 2.

    Google Scholar 

  39. Kalluri, R. and LeBleu, V.S., Science, 2020, vol. 367, no. 6478, p. eaau6977.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Matsumoto, J., Stewart, T., Banks, W.A., and Zhang, J., Curr. Pharm. Des., 2017, vol. 23, no. 40, pp. 6206–6214.

    Article  CAS  PubMed  Google Scholar 

  41. Tian, T., Zhu, Y.-L., Hu, F.-H., Wang, Y.-Y., Huang, N.-P., and Xiao, Z.-D., J. Cell Physiol., 2013, vol. 228, no. 7, pp. 1487–1495.

    Article  CAS  PubMed  Google Scholar 

  42. Toth, A.E., Holst, M.R., and Nielsen, M.S., Curr. Pharm. Des., 2020, vol. 26, no. 13, pp. 1405–1416.

    Article  CAS  PubMed  Google Scholar 

  43. Haqqani, A.S., Thom, G., Burrell, M., Delaney, C.E., Brunette, E., Baumann, E., Sodja, C., Jezierski, A., Webster, C., and Stanimirovic, D.B., J. Neurochem., 2018, vol. 146, no. 6, pp. 735–752.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Patel, M.M. and Patel, B.M., CNS Drugs, 2017, vol. 31, no. 2, pp. 109–133.

    Article  CAS  PubMed  Google Scholar 

  45. Banks, W.A., Sharma, P., Bullock, K.M., Hansen, K.M., Ludwig, N., and Whiteside, T.L., Int. J. Mol. Sci., 2020, vol. 21, no. 12, pp. 1–21.

    Google Scholar 

  46. Saint-Pol, J., Gosselet, F., Duban-Deweer, S., Pottiez, G., and Karamanos, Y., Cells, 2020, vol. 9, no. 4, p. 851.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Kramer-Albers, E.-M., Bretz, N., Tenzer, S., Winterstein, C., Mobius, W., Berger, H., Nave, K.-A., Schild, H., and Trotter, J., Proteomics Clin. Appl., 2007, vol. 1, no. 11, pp. 1446–1461.

    Article  PubMed  Google Scholar 

  48. Wang, G., Dinkins, M., He, Q., Zhu, G., Poirier, C., Campbell, A., Mayer-Proschel, M., and Bieberich, E., J. Biol. Chem., 2012, vol. 287, no. 25, pp. 21384–21395.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Xin, H., Li, Y., Buller, B., Katakowski, M., Zhang, Y., Wang, X., Shang, X., Zhang, Z.G., and Chopp, M., Stem Cells, 2012, vol. 30, no. 7, pp. 1556–1564.

    Article  CAS  PubMed  Google Scholar 

  50. Zhang, Y., Kim, M.S., Jia, B., Yan, J., Zuniga-Hertz, J.P., Han, C., and Cai, D., Nature, 2017, vol. 548, no. 7665, pp. 52–57.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Fitzner, D., Schnaars, M., van Rossum, D., Krishnamoorthy, G., Dibaj, P., Bakhti, M., Regen, T., Hanisch, U.-K., and Simons, M., J. Cell Sci., 2011, vol. 124, no. 3, pp. 447–458.

    Article  CAS  PubMed  Google Scholar 

  52. Fruhbeis, C., Frohlich, D., Kuo, W.P., Amphornrat, J., Thilemann, S., Saab, A.S., Kirchhoff, F., Mobius, W., Goebbels, S., and Nave, K.-A., PLoS Biol., 2013, vol. 11, no. 7, p. e1001604.

    Article  PubMed  PubMed Central  Google Scholar 

  53. Morel, L., Regan, M., Higashimori, H., Ng, S.K., Esau, C., Vidensky, S., Rothstein, J., and Yang, Y., J. Biol. Chemistry, 2013, vol. 288, no. 10, pp. 7105–7116.

    Article  CAS  Google Scholar 

  54. Fruhbeis, C., Frohlich, D., Kuo, W.P., and Kramer-Albers, E.-M., Front. Cell. Neurosci., 2013, vol. 7, p. 182.

    Article  PubMed  PubMed Central  Google Scholar 

  55. Budnik, V., Ruiz-Canada, C., and Wendler, F., Nat. Rev. Neurosci., 2016, vol. 17, no. 3, pp. 160–172.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Fitzner, D., Schnaars, M., van Rossum, D., Krishnamoorthy, G., Dibaj, P., Bakhti, M., Regen, T., Hanisch, U.-K., and Simons, M., J. Cell Sci., 2011, vol. 124, no. 3, pp. 447–458.

    Article  CAS  PubMed  Google Scholar 

  57. Budnik, V., Ruiz-Canada, C., and Wendler, F., Nat. Rev. Neurosci., 2016, vol. 17, no. 3, pp. 160–172.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Faure, J., Lachenal, G., Court, M., Hirrlinger, J., Chatellard-Causse, C., Blot, B., Grange, J., Schoehn, G., Goldberg, Y., and Boyer, V., Mol. Cell. Neurosci., 2006, vol. 31, no. 4, pp. 642–648.

    Article  CAS  PubMed  Google Scholar 

  59. Zhang, J., Li, S., Li, L., Li, M., Guo, C., Yao, J., and Mi, S., Genom. Proteom. Bioinform., 2015, vol. 13, no. 1, pp. 17–24.

    Article  CAS  Google Scholar 

  60. Shetgaonkar, G.G., Marques, S.M., DCruz, C.E.M., Vibhavari, R.J.A., Kumar, L., and Shirodkar, R.K., Drug Deliv. Transl. Res., 2022, vol. 12, no. 5, pp. 1047–1079.

    Article  CAS  PubMed  Google Scholar 

  61. Qu, M., Lin, Q., Huang, L., Fu, Y., Wang, L., He, S., Fu, Y., Yang, S., Zhang, Z., and Zhang, L., J. Control. Release, 2018, vol. 287, pp. 156–166.

    Article  CAS  PubMed  Google Scholar 

  62. Morad, G., Carman, C.V., Hagedorn, E.J., Perlin, J.R., Zon, L.I., Mustafaoglu, N., Park, T.-E., Ingber, D.E., Daisy, C.C., and Moses, M.A., ACS Nano, vol. 13, no. 12, pp. 13853–13865.

  63. Pulgar, V.M., Front. Neurosci., 2019, vol. 12, p. 1019.

    Article  PubMed  PubMed Central  Google Scholar 

  64. Terstappen, G.C., Meyer, A.H., Bell, R.D., and Zhang, W., Nat. Rev. Drug Discov., 2021, vol. 20, no. 5, pp. 362–383.

    Article  CAS  PubMed  Google Scholar 

  65. Azarmi, M., Maleki, H., Nikkam, N., and Malekinejad, H., Int. J. Pharm., 2020, vol. 586, p. 119582.

    Article  CAS  PubMed  Google Scholar 

  66. Uchida, Y., Ohtsuki, S., Katsukura, Y., Ikeda, C., Suzuki, T., Kamiie, J., and Terasaki, T., J. Neurochem., 2011, vol. 117, no. 2, pp. 333–345.

    Article  CAS  PubMed  Google Scholar 

  67. Zuchero, Y.J.Y., Chen, X., Bien-Ly, N., Bumbaca, D., Tong, R.K., Gao, X., Zhang, S., Hoyte, K., Luk, W., and Huntley, M.A., Neuron, 2016, vol. 89, no. 1, pp. 70–82.

    Article  CAS  PubMed  Google Scholar 

  68. Karatas, H., Aktas, Y., Gursoy-Ozdemir, Y., Bodur, E., Yemisci, M., Caban, S., Vural, A., Pinarbasli, O., Capan, Y., and Fernandez-Megia, E., J. Neurosci., 2009, vol. 29, no. 44, pp. 13761–13769.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Sonoda, H., Morimoto, H., Yoden, E., Koshimura, Y., Kinoshita, M., Golovina, G., Takagi, H., Yamamoto, R., Minami, K., and Mizoguchi, A., Mol. Ther., 2018, vol. 26, no. 5, pp. 1366–1374.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Spencer, B.J. and Verma, I.M., Proc. Natl. Acad. Sci. U S A, 2007, vol. 104, no. 18, pp. 7594–7599.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Wagner, S., Zensi, A., Wien, S.L., Tschickardt, S.E., Maier, W., Vogel, T., Worek, F., Pietrzik, C.U., Kreuter, J., and von Briesen, H., PLoS One, 2012, vol. 7, no. 3, p. e32568.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Spencer, B., Trinh, I., Rockenstein, E., Mante, M., Florio, J., Adame, A., El-Agnaf, O.M.A., Kim, C., Masliah, E., and Rissman, R.A., Neurobiol. D., 2019, vol. 127, pp. 163–177.

  73. Zhang, W., Liu, Q.Y., Haqqani, A.S., Leclerc, S., Liu, Z., Fauteux, F., Baumann, E., Delaney, C.E., Ly, D., and Star, A.T., Fluids Barriers CN, 2020, vol. 17, no. 1, p. 47.

  74. Pardridge, W.M., Kang, Y.-S., Buciak, J.L., and Yang, J., Pharm. Res., 1995, vol. 12, no. 6, pp. 807–816.

    Article  CAS  PubMed  Google Scholar 

  75. Boado, R.J. and Pardridge, W.M., Mol. Pharmaceutics, 2017, vol. 14, no. 4, pp. 1271–1277.

    Article  CAS  Google Scholar 

  76. Pardridge, W.M., Boado, R.J., Giugliani, R., and Schmidt, M., BioDrugs, 2018, vol. 32, no. 2, pp. 169–176.

    Article  CAS  PubMed  Google Scholar 

  77. Feral, C.C., Nishiya, N., Fenczik, C.A., Stuhlmann, H., Slepak, M., and Ginsberg, M.H., Proc. Natl. Acad. Sci. U S A, 2005, vol. 102, no. 2, pp. 355–360.

    Article  CAS  PubMed  Google Scholar 

  78. Xie, F., Yao, N., Qin, Y., Zhang, Q., Chen, H., Yuan, M., Tang, J., Li, X., Fan, W., Zhang, Q., Wu, Y., Hai, L., and He, Q., Int. J. Nanomedicine, 2012, vol. 7, pp. 163–175.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Guo, Y., Zhang, Y., Li, J., Zheng, Y., Lu, Y., Jiang, X., He, X., Ma, H., An, S., and Jiang, C., ACS Appl. Mater. Interfaces, 2015, vol. 7, no. 9, pp. 5444–5453.

    Article  CAS  PubMed  Google Scholar 

  80. Webb, R.L., Kaiser, E.E., Scoville, S.L., Thompson, T.A., Fatima, S., Pandya, C., Sriram, K., Swetenburg, R.L., Vaibhav, K., and Arbab, A.S., Transl. Stroke Res., 2018, vol. 9, no. 5, pp. 530–539.

    Article  CAS  PubMed  Google Scholar 

  81. Yang, T., Martin, P., Fogarty, B., Brown, A., Schurman, K., Phipps, R., Yin, V.P., Lockman, P., and Bai, S., Pharm. Res., 2015, vol. 32, no. 6, pp. 2003–2014.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Record, M., Subra, C., Silvente-Poirot, S., and Poirot, M., Biochem. Pharmacol., 2011, vol. 81, no. 10, pp. 1171–1182.

    Article  CAS  PubMed  Google Scholar 

  83. Chen, C.C., Liu, L., Ma, F., Wong, C.W., Guo, X.E., Chacko, J.V., Farhoodi, H.P., Zhang, S.X., Zimak, J., and Segaliny, A., Cell. Mol. Bioengineering, 2016, vol. 9, no. 4, pp. 509–529.

    Article  CAS  Google Scholar 

  84. Yuan, D., Zhao, Y., Banks, W.A., Bullock, K.M., Haney, M., Batrakova, E., and Kabanov, A.V., Biomaterials, 2017, vol. 142, pp. 1–12.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Hu, G.W., Li, Q., Niu, X., Hu, B., Liu, J., Zhou, S.M., Guo, S.C., Lang, H.L., Zhang, C.Q., and Wang, Y., Stem Cell Res. Ther., 2015, vol. 6, no. 1, p. 10.

    Article  PubMed  PubMed Central  Google Scholar 

  86. Zhou, W., Fong, M.Y., Min, Y., Somlo, G., Liu, L., Palomares, M.R., Yu, Y., Chow, A., O’Connor, S., and Chin, A.R., Cancer Cell, 2014, vol. 25, no. 4, pp. 501–515.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Pivoraite, U., Jarmalaviciute, A., Tunaitis, V., Ramanauskaite, G., Vaitkuviene, A., Kaseta, V., Biziuleviciene, G., Venalis, A., and Pivoriunas, A., Inflammation, 2015, vol. 38, no. 5, pp. 1933–1941.

    Article  CAS  PubMed  Google Scholar 

  88. Wardlaw, J.M., Doubal, F.N., Valdes-Hernandez, M., Wang, X., Chappell, F.M., Shuler, K., Armitage, P.A., Carpenter, T.C., and Dennis, M.S., Stroke, 2013, vol. 44, no. 2, pp. 525–527.

    Article  PubMed  Google Scholar 

  89. Xu, B., Zhang, Y., Du, X.-F., Li, J., Zi, H.-X., Bu, J.-W., Yan, Y., Han, H., and Du, J.-L., Cell Res., 2017, vol. 27, no. 7, pp. 882–897.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Haney, M.J., Klyachko, N.L., Zhao, Y., Gupta, R., Plotnikova, E.G., He, Z., Patel, T., Piroyan, A., Sokolsky, M., and Kabanov, A.V., J. Control. Release, 2015, vol. 207, pp. 18–30.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Kim, G., Kim, M., Lee, Y., Byun, J.W., Hwang, D.W., and Lee, M., J. Control. Release, 2020, vol. 317, pp. 273–281.

    Article  CAS  PubMed  Google Scholar 

  92. Liu, Y., Fu, N., Su, J., Wang, X., and Li, X., BioMed Res. Int., 2019, vol. 2019, p. 4273290.

    PubMed  PubMed Central  Google Scholar 

  93. Cui, G.-H., Wu, J., Mou, F.-F., Xie, W.-H., Wang, F.-B., Wang, Q.-L., Fang, J., Xu, Y.-W., Dong, Y.-R., and Liu, J.-R., FASEB J., 2018, vol. 32, no. 2, pp. 654–668.

    Article  CAS  PubMed  Google Scholar 

  94. Xu, M., Feng, T., Liu, B., Qiu, F., Xu, Y., Zhao, Y., and Zheng, Y., Theranostics, 2021, vol. 11, no. 18, pp. 8926–8944.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Choi, H., Choi, K., Kim, D.-H., Oh, B.-K., Yim, H., Jo, S., and Choi, C., Pharmaceutics, 2022, vol. 14, no. 3, p. 672.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Malekian, F., Shamsian, A., Kodam, S.P., and Ullah, M., J. Physiol., 2022.https://doi.org/10.1113/JP282799

  97. Alvarez-Erviti, L., Seow, Y., Yin, H., Betts, C., Lakhal, S., and Wood, M.J.A., Nat. Biotechnol., 2011, vol. 29, no. 4, pp. 341–345.

    Article  CAS  PubMed  Google Scholar 

  98. Salunkhe, S., Dheeraj, BasakM., Chitkara, D., and Mittal, A., J. Control. Release, 2020, vol. 326, pp. 599–614.

    Article  CAS  PubMed  Google Scholar 

  99. Gopalan, D., Pandey, A., Udupa, N., and Mutalik, S., J. Control. Release, 2020, vol. 319, pp. 183–200.

    Article  CAS  PubMed  Google Scholar 

  100. Xu, R., Greening, D.W., Chen, M., Rai, A., Ji, H., Takahashi, N., and Simpson, R.J., Proteomics, 2019, vol. 19, no. 8, p. e1900121.

    Article  Google Scholar 

  101. Khongkow, M., Yata, T., Boonrungsiman, S., Ruktanonchai, U.R., Graham, D., and Namdee, K., Sci. Rep., vol. 9, no. 1, p. 8278.

  102. Zhao, C., Wang, H., Xiong, C., and Liu, Y., Biochem. Biophys. Res. Commun., 2018, vol. 502, no. 3, pp. 324–331.

    Article  CAS  PubMed  Google Scholar 

  103. Jia, G., Han, Y., An, Y., Ding, Y., He, C., Wang, X., and Tang, Q., Biomaterials, 2018, vol. 178, pp. 302–316.

    Article  CAS  PubMed  Google Scholar 

  104. Tian, T., Zhang, H.X., He, C.P., Fan, S., Zhu, Y.L., Qi, C., Huang, N.P., Xiao, Z.D., Lu, Z.H., and Tannous, B.A., Biomaterials, 2018, vol. 150, pp. 137–149.

    Article  CAS  PubMed  Google Scholar 

  105. Alyautdin, R., Khalin, I., Nafeeza, M.I., Haron, M.H., and Kuznetsov, D., Int. J. Nanomedicine, 2014, vol. 9, no. 1, pp. 795–811.

    CAS  PubMed  PubMed Central  Google Scholar 

  106. El-Andaloussi, S., Lee, Y., Lakhal-Littleton, S., Li, J., Seow, Y., Gardiner, C., Alvarez-Erviti, L., Sargent, I.L., and Wood, M.J.A., Nat. Prot., 2012, vol. 7, no. 12, pp. 2112–2126.

    Article  CAS  Google Scholar 

Download references

Funding

The work is supported by Government assignments of Institute of Higher Nervous Activity and Neurophysiology of the Russian Academy of Sciences and the Research Center of Neurology of the Ministry of Education and Science of the Russian Federation.

Author information

Authors and Affiliations

  1. Research Center of Neurology, Ministry of Science and Higher Education of the Russian Federation, Moscow, Russia

    L. G. Khaspekov

  2. Institute of Higher Nervous Activity and Neurophysiology, Russian Academy of Sciences, Moscow, Russia

    A. A. Yakovlev

  3. Soloviev Scientific and Practical Psychoneurological Center, Department of Health Care of Moscow, Moscow, Russia

    A. A. Yakovlev

Authors
  1. L. G. Khaspekov
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. A. Yakovlev
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to A. A. Yakovlev.

Ethics declarations

Conflict of interest. The authors declare that they have no conflict of interest.

Additional information

Corresponding author; address: ul. Butlerova 5a, Moscow, 117485 Russia; e-mail: al_yakovlev@ihna.ru. Abbreviations: AD, Alzheimer’s disease; PD, Parkinson’s disease; BBB, blood–brain barrier; RTF, transferrin receptor; sEV, small extracellular vesicles; EC, endothelial cells; AMT, adsorptively mediated transcytosis; BDNF, brain-derived neurotrophic factor; BMECs, brain microvascular endothelial cells; LDL-R, low density lipoprotein receptor; RMT, receptor-mediated transcytosis; siRNA, short interfering RNA.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Khaspekov, L.G., Yakovlev, A.A. Prospects for the Use of Small Extracellular Vesicles as a Transport Vehicle through the Blood–Brain Barrier. Neurochem. J. 17, 1–9 (2023). https://doi.org/10.1134/S1819712423010087

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1819712423010087

Keywords:

Abbreviations:

Search

Navigation