Outlooks of Using Small Extracellular Vesicles as a Transport Vehicle through the Blood–Brain Barrier


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Abstract

The review summarizes the results of recent studies on the mechanisms mediating the crossing by small extracellular vesicles through blood-brain barrier (BBB). The kinds of vesicular transport through the BBB, including receptor-mediated and adsorptive-mediated transcytosis, are considered. The possibilities of optimizing the penetration of vesicles into the parenchyma of the brain through the BBB are shown.

About the authors

L. G. Khaspekov

Research Center of Neurology

Email: nchjournal@gmail.com
Russia, Moscow

A. A. Yakovlev

Institute of Higher Nervous Activity and Neurophysiology RAS; Scientific and Practical Psychoneurological Center named after Z.P. Solovy’ov DZM

Email: nchjournal@gmail.com
Russia, Moscow; Russia, Moscow

References

  1. Busatto S., Morad G., Guo P., Moses M.A. // FASEB Bioadv. 2021. V. 3. P. 665–675.
  2. Théry 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. V. 7. № 1. 1535750
  3. Kapogiannis D., Mustapic M., Shardell M.D., Berkowitz S.T., Diehl T.C., Spangler R.D., Tran J., Lazaropoulos M.P., Chawla S., Gulyani S. // JAMA Neurology. 2019. V. 76. № 11. P. 1340–1351.
  4. Mustapic M., Eitan E., Werner J.K., Berkowitz S.T., Lazaropoulos M.P., Tran J., Goetzl E.J., Kapogiannis D. // Front. Neurosci. 2017. V. 11. 278.
  5. Winston C.N., Goetzl E.J., Akers J.C., Carter B.S., Rockenstein E.M., Galasko D., Masliah E., Rissman R.A. // Alzheimer’s and Dementia: Diagnosis, Assessment and Disease Monitoring. 2016. V. 3. P. 63–72.
  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., Miller B.L. // FASEB J. 2016. V. 30. № 12. P. 4141–4148.
  7. Fiandaca M.S., Kapogiannis D., Mapstone M., Boxer A., Eitan E., Schwartz J.B., Abner E.L., Petersen R.C., Federoff H.J., Miller B.L. // Alzheimer’s Dem. 2015. V. 11. № 6. P. 600–607.
  8. Ardashirova N.S., Fedotova E.Yu., Illarioshkin S.N. // Neurochem. J. 2020. V. 14. № 2. P. 127-132.
  9. Shi M., Liu C., Cook T.J., Bullock K.M., Zhao Y., Ginghina C., Li Y., Aro P., Dator R., He C. // Acta Neuropath. 2014. V. 128. № 5. P. 639–650.
  10. Shi M., Kovac A., Korff A., Cook T.J., Ginghina C., Bullock K.M., Yang L., Stewart T., Zheng D., Aro P. // Alzheimer’s & Dementia. 2016. V. 12. № 11. P. 1125–1131.
  11. Hamlett E.D., Goetzl E.J., Ledreux A., Vasilevko V., Boger H.A., LaRosa A., Clark D., Carroll S.L., Carmona-Iragui M., Fortea J. // Alzheimer’s & Dementia. 2017. V. 13. № 5. P. 541–549.
  12. Sproviero D., la Salvia S., Giannini M., Crippa V., Gagliardi S., Bernuzzi S., Diamanti L., Ceroni M., Pansarasa O., Poletti A. // Front. Neurosci. 2018. V. 12. 487.
  13. Ivanova M.V., Chekanova E.O., Belugin B.V., Dolzhikova I.V, Tutykhina I.L., Zakharova M.N. // Neurochem. J. 2020. V. 14. № 3. P. 321–327.
  14. Martinez B., Peplow P.V. // Neural Regeneration Res. 2020. V. 15. № 4. P. 606–619.
  15. Mycko M.P., Baranzini S.E. // Mult. Sclerosis J. 2020. V. 26. № 5. P. 599–604.
  16. Ebrahimkhani S., Beadnall H.N., Wang C., Suter C.M., Barnett M.H., Buckland M.E., Vafaee F. // Mol. Neurobiol. 2020. V. 57. № 2. P. 1245–1258.
  17. Xin H., Wang F., Li Y., Lu Q.-E., Cheung W.L., Zhang Y., Zhang Z.G., Chopp M. // Cell Transpl. 2017. V. 26. № 2. P. 243–257.
  18. Chen Y., Song Y., Huang J., Qu M., Zhang Y., Geng J., Zhang Z., Liu J., Yang G.-Y. // Front. Neurol. 2017. V. 8. 57.
  19. Song Y., Li Z., He T., Qu M., Jiang L., Li W., Shi X., Pan J., Zhang L., Wang Y. // Theranostics. 2019. V. 9. № 10. P. 2910–2923.
  20. Yakovlev A.A. // Neurochem. J. 2022. V. 16. № 2. P. 121–129.
  21. Choi J., Kim S.Y., Kim H., Lim B.C., Hwang H., Chae J.H., Kim K.J., Oh S., Kim E.Y., Shin J.-S. // BMC Neurol. 2020. V. 20. № 1. P. 85.
  22. Kumar S., Vijayan M., Bhatti J.S., Reddy P.H. // Prog. Mol. Biol. Transl. Sci. 2017. 146:47-94.
  23. Nasca C., Dobbin J., Bigio B., Watson K., de Angelis P., Kautz M., Cochran A., Mathé A.A., Kocsis J.H., Lee F.S. // Mol. Psychiatry. 2021. V. 26. № 9. P. 5140–5149.
  24. Gruzdev S.K., Yakovlev A.A., Druzhkova T.A., Guekht A.B., Gulyaeva N.V. // Cell. Mol. Neurobiol. 2019. V. 39. № 6. P. 729–750
  25. Yakovlev A.A., Druzhkova T.A., Nikolaev R.V., Kuznetsova V.E., Gruzdev S.K., Guekht A.B., Gulyaeva N.V. // Neurochem. J. 2019. V. 13. № 4. P. 385–390.
  26. Ceylan D., Tufekci K.U., Keskinoglu P., Genc S., Ozerdem A. // J. Affect. Dis. 2020. V. 262. P. 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., Mellios N. // Neuropsychopharmacology. 2020. V. 45. № 4. P. 656–665.
  28. Ma Y., Li C., Huang Y., Wang Y., Xia X., Zheng J.C. // Cell Comm. Signal. 2019. V. 17. № 1. 96.
  29. Sharma G., Modgil A., Layek B., Arora K., Sun C., Law B., Singh J. // J. Control. Release. 2013. V. 167. № 1. P. 1–10.
  30. Gómez-Molina C., Sandoval M., Henzi R., Ramírez J.P., Varas-Godoy M., Luarte A., Lafourcade C.A., Lopez-Verrilli A., Smalla K.H., Kaehne T. // Int. J. Neuropsychopharmacol. 2019. V. 22. № 3. P. 232–246
  31. Belhadj Z., He B., Deng H., Song S., Zhang H., Wang X., Dai W., Zhang Q. // J. Extracell. Ves. 2020. V. 9. № 1. 1806444.
  32. Kamerkar S., Lebleu V.S., Sugimoto H., Yang S., Ruivo C.F., Melo S.A., Lee J.J., Kalluri R. // Nature. 2017. V. 546. № 7659. P. 498–503
  33. Shi M., Sheng L., Stewart T., Zabetian C.P., Zhang J. // Prog. Neurobiol. 2019. V. 175. P. 96–106.
  34. Banks W.A., Sharma P., Bullock K.M., Hansen K.M., Ludwig N., Whiteside T.L. // Int. J. Mol. Sci. 2020. V. 21. № 12. P. 1–21.
  35. Tkach M., Théry C. // Cell. 2016. V. 164. № 6. P. 1226–1232.
  36. Patil S.M., Sawant S.S., Kunda N.K. // Eur. J. Pharm. Biopharm. 2020. V. 154. P. 259–269.
  37. Heidarzadeh M., Gürsoy-Özdemir Y., Kaya M., Eslami Abriz A., Zarebkohan A., Rahbarghazi R., Sokullu E. // Cell Biosci. 2021. V. 11. № 1. 142.
  38. Dardet J.P., Serrano N., András I.E., Toborek M. // Front. Drug Deliv. 2022. V. 2.
  39. Kalluri R., LeBleu V.S. // Science. 2020. V. 367. № 6478. eaau6977.
  40. Matsumoto J., Stewart T., Banks W.A., Zhang J. // Curr. Pharm. Des. 2017. V. 23. № 40. P. 6206–6214.
  41. Tian T., Zhu Y.-L., Hu F.-H., Wang Y.-Y., Huang N.-P., Xiao Z.-D. // J. Cell. Physiol. 2013. V. 228. № 7. P. 1487–1495.
  42. Toth A.E., Holst M.R., Nielsen M.S. // Curr. Pharm. Des. 2020. V. 26. № 13. P. 1405–1416.
  43. Haqqani A.S., Thom G., Burrell M., Delaney C.E., Brunette E., Baumann E., Sodja C., Jezierski A., Webster C., Stanimirovic D.B. // J. Neurochem. 2018. V. 146. № 6. P. 735–752.
  44. Patel M.M., Patel B.M. // CNS Drugs. 2017. V. 31. № 2. P. 109–133.
  45. Banks W.A., Sharma P., Bullock K.M., Hansen K.M., Ludwig N., Whiteside T.L. // Int. J. Mol. Sci. 2020. V. 21. № 12. P. 1–21.
  46. Saint-Pol J., Gosselet F., Duban-Deweer S., Pottiez G., Karamanos Y. // Cells. 2020. V. 9. № 4. 851.
  47. Krämer-Albers E.-M., Bretz N., Tenzer S., Winterstein C., Möbius W., Berger H., Nave K.-A., Schild H., Trotter J. // Proteomics Clin. Appl. 2007. V. 1. № 11. P. 1446–1461.
  48. Wang G., Dinkins M., He Q., Zhu G., Poirier C., Campbell A., Mayer-Proschel M., Bieberich E. // J. Biol. Chem. 2012. V. 287. № 25. P. 21384–21395.
  49. Xin H., Li Y., Buller B., Katakowski M., Zhang Y., Wang X., Shang X., Zhang Z.G., Chopp M. // Stem Cells. 2012. V. 30. № 7. P. 1556–1564.
  50. Zhang Y., Kim M.S., Jia B., Yan J., Zuniga-Hertz J.P., Han C., Cai D. // Nature. 2017. V. 548. № 7665. P. 52–57.
  51. Fitzner D., Schnaars M., van Rossum D., Krishnamoorthy G., Dibaj P., Bakhti M., Regen T., Hanisch U.-K., Simons M. // J. Cell Sci. 2011. V. 124. № 3. P. 447–458.
  52. Frühbeis C., Fröhlich D., Kuo W.P., Amphornrat J., Thilemann S., Saab A.S., Kirchhoff F., Möbius W., Goebbels S., Nave K.-A. // PLoS Biol. 2013. V. 11. № 7. e1001604.
  53. Morel L., Regan M., Higashimori H., Ng S.K., Esau C., Vidensky S., Rothstein J., Yang Y. // J. Biol. Chemistry. 2013. V. 288. № 10. P. 7105–7116.
  54. Frühbeis C., Fröhlich D., Kuo W.P., Krämer-Albers E.-M. // Front. Cell. Neurosci. 2013. V. 7. 182.
  55. Budnik V., Ruiz-Cañada C., Wendler F. // Nat. Rev. Neurosci. 2016. V. 17. № 3. P. 160–172.
  56. Fitzner D., Schnaars M., van Rossum D., Krishnamoorthy G., Dibaj P., Bakhti M., Regen T., Hanisch U.-K., Simons M. // J. Cell Sci. 2011. V. 124. № 3. P. 447–458.
  57. Budnik V., Ruiz-Cañada C., Wendler F. // Nat. Rev. Neurosci. 2016. V. 17. № 3. P. 160–172.
  58. Fauré J., Lachenal G., Court M., Hirrlinger J., Chatellard-Causse C., Blot B., Grange J., Schoehn G., Goldberg Y., Boyer V. // Mol. Cell. Neurosci. 2006. V. 31. № 4. P. 642–648.
  59. Zhang J., Li S., Li L., Li M., Guo C., Yao J., Mi S. // Genom. Proteom. Bioinform. 2015. V. 13. № 1. P. 17–24.
  60. Shetgaonkar G.G., Marques S.M., DCruz C.E.M., Vibhavari R.J.A., Kumar L., Shirodkar R.K. // Drug Deliv. Transl. Res. 2022. V. 12. № 5. P. 1047–1079.
  61. Qu M., Lin Q., Huang L., Fu Y., Wang L., He S., Fu Y., Yang S., Zhang Z., Zhang L. // J. Control. Release. 2018. V. 287. P. 156–166.
  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., Moses M.A. // ACS Nano. 2019. V. 13. № 12. P. 13853–13865.
  63. Pulgar V.M. // Front. Neurosci. 2019. V. 12. 1019
  64. Terstappen G.C., Meyer A.H., Bell R.D., Zhang W. // Nat. Rev. Drug Discov. 2021. V. 20. № 5. P. 362–383.
  65. Azarmi M., Maleki H., Nikkam N., Malekinejad H. // Int. J. Pharm. 2020. V. 586. 119582.
  66. Uchida Y., Ohtsuki S., Katsukura Y., Ikeda C., Suzuki T., Kamiie J., Terasaki T. // J. Neurochem. 2011. V. 117. № 2. P. 333–345.
  67. Zuchero Y.J.Y., Chen X., Bien-Ly N., Bumbaca D., Tong R.K., Gao X., Zhang S., Hoyte K., Luk W., Huntley M.A. // Neuron. 2016. V. 89. № 1. P. 70–82.
  68. Karatas H., Aktas Y., Gursoy-Ozdemir Y., Bodur E., Yemisci M., Caban S., Vural A., Pinarbasli O., Capan Y., Fernandez-Megia E. // J. Neurosci. 2009. V. 29. № 44. P. 13761–13769.
  69. Sonoda H., Morimoto H., Yoden E., Koshimura Y., Kinoshita M., Golovina G., Takagi H., Yamamoto R., Minami K., Mizoguchi A. // Mol. Ther. 2018. V. 26. № 5. P. 1366–1374.
  70. Spencer B.J., Verma I.M. // Proc Natl Acad Sci U S A. 2007. V. 104. № 18. P. 7594–7599.
  71. Wagner S., Zensi A., Wien S.L., Tschickardt S.E., Maier W., Vogel T., Worek F., Pietrzik C.U., Kreuter J., von Briesen H. // PLoS One. 2012. V. 7. № 3. e32568.
  72. Spencer B., Trinh I., Rockenstein E., Mante M., Florio J., Adame A., El-Agnaf O.M.A., Kim C., Masliah E., Rissman R.A. // Neurobiol. Dis. 2019. V. 127. P. 163–177.
  73. Zhang W., Liu Q.Y., Haqqani A.S., Leclerc S., Liu Z., Fauteux F., Baumann E., Delaney C.E., Ly D., Star A.T. // Fluids Barriers CNS. 2020. V. 17. № 1. 47.
  74. Pardridge W.M., Kang Y.-S., Buciak J.L., Yang J. // Pharm. Res. 1995. V. 12. № 6. P. 807–816.
  75. Boado R.J., Pardridge W.M. // Mol. Pharmaceutics. 2017. V. 14. № 4. P. 1271–1277.
  76. Pardridge W.M., Boado R.J., Giugliani R., Schmidt M. // BioDrugs. 2018. V. 32. № 2. P. 169–176.
  77. Feral C.C., Nishiya N., Fenczik C.A., Stuhlmann H., Slepak M., Ginsberg M.H. // Proc Natl Acad Sci U S A. 2005. V. 102. № 2. P. 355–360.
  78. Xie F., Xie F., Qin, Yuan, Tang, Zhang, Fan, Chen, Hai, Yao, et al. // Int. J. Nanomedicine. 2012. V. 7. P. 163–175.
  79. Guo Y., Zhang Y., Li J., Zheng Y., Lu Y., Jiang X., He X., Ma H., An S., Jiang C. // ACS Appl. Mater. Interfaces. 2015. V. 7. № 9. P. 5444–5453.
  80. Webb R.L., Kaiser E.E., Scoville S.L., Thompson T.A., Fatima S., Pandya C., Sriram K., Swetenburg R.L., Vaibhav K., Arbab A.S. // Transl. Stroke Res. 2018. V. 9. № 5. P. 530–539.
  81. Yang T., Martin P., Fogarty B., Brown A., Schurman K., Phipps R., Yin V.P., Lockman P., Bai S. // Pharm. Res. 2015. V. 32. № 6. P. 2003–2014.
  82. Record M., Subra C., Silvente-Poirot S., Poirot M. // Biochem. Pharmacol. 2011. V. 81. № 10. P. 1171–1182.
  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., Ségaliny A. // Cell. Mol. Bioengineering. 2016. V. 9. № 4. P. 509–529.
  84. Yuan D., Zhao Y., Banks W.A., Bullock K.M., Haney M., Batrakova E., Kabanov A.V. // Biomaterials. 2017. V. 142. P. 1–12.
  85. Hu G.W., Li Q., Niu X., Hu B., Liu J., Zhou S.M., Guo S.C., Lang H.L., Zhang C.Q., Wang Y. // Stem Cell Res. Ther. 2015. V. 6. № 1. 10.
  86. Zhou W., Fong M.Y., Min Y., Somlo G., Liu L., Palomares M.R., Yu Y., Chow A., O’Connor S., Chin A.R. // Cancer Cell. 2014. V. 25. № 4. P. 501-515.
  87. Pivoraitė U., Jarmalavičiūtė A., Tunaitis V., Ramanauskaitė G., Vaitkuvienė A., Kašėta V., Biziulevičienė G., Venalis A., Pivoriūnas A. // Inflammation. 2015. V. 38. № 5. P. 1933–1941.
  88. Wardlaw J.M., Doubal F.N., Valdes-Hernandez M., Wang X., Chappell F.M., Shuler K., Armitage P.A., Carpenter T.C., Dennis M.S. // Stroke. 2013. V. 44. № 2. P. 525–527.
  89. Xu B., Zhang Y., Du X.-F., Li J., Zi H.-X., Bu J.-W., Yan Y., Han H., Du J.-L. // Cell Res. 2017. V. 27. № 7. P. 882–897.
  90. Haney M.J., Klyachko N.L., Zhao Y., Gupta R., Plotnikova E.G., He Z., Patel T., Piroyan A., Sokolsky M., Kabanov A.V. // J. Control. Release. 2015. V. 207. P. 18–30.
  91. Kim G., Kim M., Lee Y., Byun J.W., Hwang D.W., Lee M. // J. Control. Release. 2020. V. 317. P. 273–281.
  92. Liu Y., Fu N., Su J., Wang X., Li X. // BioMed Res. Int. 2019. V. 2019. 4273290.
  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., Liu J.-R. // FASEB J. 2018. V. 32. № 2. P. 654–668.
  94. Xu M., Feng T., Liu B., Qiu F., Xu Y., Zhao Y., Zheng Y. // Theranostics. 2021. V. 11. № 18. P. 8926–8944.
  95. Choi H., Choi K., Kim D.-H., Oh B.-K., Yim H., Jo S., Choi C. // Pharmaceutics. 2022. V. 14. № 3. 672.
  96. Malekian F., Shamsian A., Kodam S.P., Ullah M. // J. Physiol. 2022. May 16. https://doi.org/10.1113/JP282799
  97. Alvarez-Erviti L., Seow Y., Yin H., Betts C., Lakhal S., Wood M.J.A. // Nat. Biotechnol. 2011. V. 29. № 4. P. 341–345.
  98. Salunkhe S., Dheeraj, Basak M., Chitkara D., Mittal A. // J. Control. Release. 2020. V. 326. P. 599–614.
  99. Gopalan D., Pandey A., Udupa N., Mutalik S. // J. Control. Release. 2020. V. 319. P. 183–200.
  100. Xu R., Greening D.W., Chen M., Rai A., Ji H., Takahashi N., Simpson R.J. // Proteomics. 2019. V. 19. № 8. e1900121.
  101. Khongkow M., Yata T., Boonrungsiman S., Ruktanonchai U.R., Graham D., Namdee K. // Sci. Rep. 2019. V. 9. № 1. 8278.
  102. Zhao C., Wang H., Xiong C., Liu Y. // Biochem. Biophys. Res. Commun. 2018. V. 502. № 3. P. 324–331.
  103. Jia G., Han Y., An Y., Ding Y., He C., Wang X., Tang Q. // Biomaterials. 2018. V. 178. P. 302–316.
  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., Tannous B.A. // Biomaterials. 2018. V. 150. P. 137–149.
  105. Alyautdin R., Khalin I., Nafeeza M.I., Haron M.H., Kuznetsov D. // Int. J. Nanomedicine. 2014. V. 9. № 1. P. 795–811.
  106. El-Andaloussi S., Lee Y., Lakhal-Littleton S., Li J., Seow Y., Gardiner C., Alvarez-Erviti L., Sargent I.L., Wood M.J.A. // Nat. Prot. 2012. V. 7. № 12. P. 2112–2126.

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