Low-Level Laser Treatment Induces the Blood-Brain Barrier Opening and the Brain Drainage System Activation: Delivery of Liposomes into Mouse Glioblastoma.

blood-brain barrier brain drainage system glioblastoma infrared low-intensity laser treatment liposomes

Journal

Pharmaceutics
ISSN: 1999-4923
Titre abrégé: Pharmaceutics
Pays: Switzerland
ID NLM: 101534003

Informations de publication

Date de publication:
08 Feb 2023
Historique:
received: 16 01 2023
revised: 30 01 2023
accepted: 02 02 2023
entrez: 25 2 2023
pubmed: 26 2 2023
medline: 26 2 2023
Statut: epublish

Résumé

The progress in brain diseases treatment is limited by the blood-brain barrier (BBB), which prevents delivery of the vast majority of drugs from the blood into the brain. In this study, we discover unknown phenomenon of opening of the BBBB (BBBO) by low-level laser treatment (LLLT, 1268 nm) in the mouse cortex. LLLT-BBBO is accompanied by activation of the brain drainage system contributing effective delivery of liposomes into glioblastoma (GBM). The LLLT induces the generation of singlet oxygen without photosensitizers (PSs) in the blood endothelial cells and astrocytes, which can be a trigger mechanism of BBBO. LLLT-BBBO causes activation of the ABC-transport system with a temporal decrease in the expression of tight junction proteins. The BBB recovery is accompanied by activation of neuronal metabolic activity and stabilization of the BBB permeability. LLLT-BBBO can be used as a new opportunity of interstitial PS-free photodynamic therapy (PDT) for modulation of brain tumor immunity and improvement of immuno-therapy for GBM in infants in whom PDT with PSs, radio- and chemotherapy are strongly limited, as well as in adults with a high allergic reaction to PSs.

Identifiants

pubmed: 36839889
pii: pharmaceutics15020567
doi: 10.3390/pharmaceutics15020567
pmc: PMC9966329
pii:
doi:

Types de publication

Journal Article

Langues

eng

Subventions

Organisme : EU's H2020 FET OPEN NEUROPA
ID : 863214
Organisme : Grant from the Russian Ministry of Science and High Education
ID : 075-15-2022-1094
Organisme : NIGMS NIH HHS
ID : P20 GM109089
Pays : United States
Organisme : NIH HHS
ID : R21NS091600 and R01 NS112808
Pays : United States
Organisme : Russian Science Foundation
ID : 21-75-10088; 23-25-00296; 21-74-20177
Organisme : NINDS NIH HHS
ID : R01 NS112808
Pays : United States

Références

Cancers (Basel). 2021 Jul 13;13(14):
pubmed: 34298721
Front Oncol. 2020 Sep 18;10:563840
pubmed: 33072591
Aging Dis. 2020 Feb 1;11(1):200-211
pubmed: 32010493
Pharmaceutics. 2022 Dec 22;15(1):
pubmed: 36678667
Clin J Oncol Nurs. 2016 Oct 1;20(5 Suppl):S2-8
pubmed: 27668386
J Biophotonics. 2019 Apr;12(4):e201800330
pubmed: 30485699
Proc Biol Sci. 2020 Dec 23;287(1941):20202337
pubmed: 33323086
Brain Sci. 2020 Jan 31;10(2):
pubmed: 32024010
Pharmaceutics. 2020 Nov 17;12(11):
pubmed: 33213076
Pediatr Blood Cancer. 2008 Dec;51(6):806-11
pubmed: 18802947
J Vis Exp. 2013 May 12;(75):e50326
pubmed: 23712122
J Biophotonics. 2018 Aug;11(8):e201700287
pubmed: 29380947
Microvasc Res. 2013 Nov;90:199-205
pubmed: 23978334
Biomed Opt Express. 2017 Oct 17;8(11):5040-5048
pubmed: 29188101
Am J Clin Oncol. 2018 Mar;41(3):307-312
pubmed: 26808258
Cell Commun Signal. 2013 May 28;11(1):37
pubmed: 23714586
Neurochem Res. 2002 Feb;27(1-2):89-96
pubmed: 11926280
J Cereb Blood Flow Metab. 2017 Mar;37(3):762-775
pubmed: 28155574
Lasers Surg Med. 2005 Apr;36(4):307-14
pubmed: 15739174
Expert Rev Clin Pharmacol. 2021 Mar;14(3):357-381
pubmed: 33554678
J Clin Oncol. 1998 Jul;16(7):2486-93
pubmed: 9667268
Nature. 2019 Feb;566(7745):548-552
pubmed: 30760924
Int J Mol Sci. 2019 Mar 02;20(5):
pubmed: 30832361
Methods Mol Biol. 2018;1732:507-517
pubmed: 29480496
Tsitologiia. 2015;57(10):710-3
pubmed: 26863769
Biomed Opt Express. 2019 Sep 16;10(10):5182-5197
pubmed: 31646040
Biomed Opt Express. 2018 Sep 14;9(10):4850-4862
pubmed: 30319907
Lasers Surg Med. 2013 Oct;45(8):524-32
pubmed: 24037939
Comput Struct Biotechnol J. 2022 Dec 15;21:758-768
pubmed: 36698965
J Neurosurg. 2020 Jan 24;:1-11
pubmed: 31978877
Mol Neurobiol. 2018 Aug;55(8):6601-6636
pubmed: 29327206
Free Radic Biol Med. 2021 Feb 1;163:306-313
pubmed: 33359431
Wiley Interdiscip Rev Syst Biol Med. 2013 Jan-Feb;5(1):111-24
pubmed: 23209022
Photobiomodul Photomed Laser Surg. 2019 Oct;37(10):581-595
pubmed: 31553265
J Dtsch Dermatol Ges. 2021 Jan;19(1):19-29
pubmed: 33491908
Drug Deliv. 2019 Dec;26(1):551-565
pubmed: 31928355
J Nanobiotechnology. 2022 Sep 15;20(1):412
pubmed: 36109754
Biochim Biophys Acta Biomembr. 2018 Nov;1860(11):2337-2347
pubmed: 29864406
Pharmaceutics. 2022 Nov 26;14(12):
pubmed: 36559105
Front Cell Neurosci. 2014 Dec 12;8:418
pubmed: 25565956
J Neurosci Res. 2018 Apr;96(4):731-743
pubmed: 29131369
Cancers (Basel). 2021 Nov 17;13(22):
pubmed: 34830908
Sci Adv. 2019 Jan 11;5(1):eaau8355
pubmed: 30746463
J Neurooncol. 2019 Feb;141(3):479-486
pubmed: 30644008
Cancer. 1995 Nov 1;76(9):1685-6
pubmed: 8635080
Cancer. 1995 Feb 15;75(4):1045-50
pubmed: 7842407
Sci Rep. 2013 Dec 12;3:3484
pubmed: 24336590
Front Surg. 2020 Jan 21;6:81
pubmed: 32039232
Acta Pharm Sin B. 2018 Jan;8(1):85-96
pubmed: 29872625
JAMA Oncol. 2018 Sep 1;4(9):1254-1262
pubmed: 29931168
Pharmaceuticals (Basel). 2021 Jul 26;14(8):
pubmed: 34451820
Lasers Surg Med. 2019 Sep;51(7):625-633
pubmed: 30811633
Nat Rev Cancer. 2020 Jan;20(1):26-41
pubmed: 31601988
J Neurooncol. 2021 May;152(3):501-514
pubmed: 33743128
Sci Rep. 2019 Oct 15;9(1):14815
pubmed: 31616011
Nat Rev Clin Oncol. 2012 May 29;9(7):400-13
pubmed: 22641364
Biomed Environ Sci. 2007 Aug;20(4):269-73
pubmed: 17948759
J Biophotonics. 2010 Jun;3(5-6):356-67
pubmed: 20162563
Sci Rep. 2014 Oct 10;4:6588
pubmed: 25300427
Front Oncol. 2022 Oct 13;12:1010188
pubmed: 36313687
Pediatrics. 2016 Jun;137(6):
pubmed: 27217478
Int J Mol Sci. 2022 Mar 10;23(6):
pubmed: 35328396
Arch Immunol Ther Exp (Warsz). 2021 Mar 27;69(1):8
pubmed: 33772646
Prog Neurol Surg. 2018;32:1-13
pubmed: 29990969
Expert Rev Mol Med. 2011 May 13;13:e17
pubmed: 21676290
Ann Med Surg (Lond). 2022 Mar 23;77:103231
pubmed: 35638044
J Neurosurg. 2013 Oct;119(4):845-52
pubmed: 23952800
Sci Adv. 2019 Feb 27;5(2):eaav5447
pubmed: 30820460
J Neurosurg. 2017 Jul;127(1):111-122
pubmed: 27715437
Front Oncol. 2021 May 26;11:666734
pubmed: 34123831
Nature. 2011 Aug 21;477(7364):349-53
pubmed: 21857681
J Cereb Blood Flow Metab. 1983 Mar;3(1):1-7
pubmed: 6822610
Cancers (Basel). 2019 Mar 08;11(3):
pubmed: 30857221
J Nanobiotechnology. 2021 Sep 26;19(1):289
pubmed: 34565383
Onco Targets Ther. 2019 Feb 22;12:1497-1508
pubmed: 30863116
Neuro Oncol. 2013 Aug;15(8):1058-67
pubmed: 23460322
Front Oncol. 2012 Aug 24;2:105
pubmed: 22937526
Pflugers Arch. 2020 Sep;472(9):1299-1343
pubmed: 32789766
AAPS J. 2021 Oct 28;23(6):114
pubmed: 34713363
J Exp Med. 2007 Oct 1;204(10):2349-62
pubmed: 17846148
Neuroscience. 2000;100(3):617-27
pubmed: 11098125
Neuro Oncol. 2018 Jan 22;20(2):184-191
pubmed: 29016900
Radiother Oncol. 1997 Jun;43(3):235-46
pubmed: 9215782
Lasers Med Sci. 2015 May;30(4):1357-65
pubmed: 25794592
Photochem Photobiol. 2020 Mar;96(2):280-294
pubmed: 32003006
Lasers Surg Med. 2008 Oct;40(8):535-42
pubmed: 18798293

Auteurs

Oxana Semyachkina-Glushkovskaya (O)

Institute of Physics, Humboldt University, Newtonstrasse 15, 12489 Berlin, Germany.
Department of Biology, Saratov State University, Astrakhanskaya 82, 410012 Saratov, Russia.

Denis Bragin (D)

Lovelace Biomedical Research Institute, Albuquerque, NM 87108, USA.
Department of Neurology, University of New Mexico School of Medicine, Albuquerque, NM 87131, USA.

Olga Bragina (O)

Lovelace Biomedical Research Institute, Albuquerque, NM 87108, USA.

Sergey Socolovski (S)

Optoelectronics and Biomedical Photonics Group, Aston Institute of Photonic Technologies, Aston University, Birmingham B4 7ET, UK.

Alexander Shirokov (A)

Department of Biology, Saratov State University, Astrakhanskaya 82, 410012 Saratov, Russia.
Institute of Biochemistry and Physiology of Plants and Microorganisms, Russian Academy of Sciences, Prospekt Entuziastov 13, 410049 Saratov, Russia.

Ivan Fedosov (I)

Department of Biology, Saratov State University, Astrakhanskaya 82, 410012 Saratov, Russia.

Vasily Ageev (V)

Department of Biology, Saratov State University, Astrakhanskaya 82, 410012 Saratov, Russia.

Inna Blokhina (I)

Department of Biology, Saratov State University, Astrakhanskaya 82, 410012 Saratov, Russia.

Alexander Dubrovsky (A)

Department of Biology, Saratov State University, Astrakhanskaya 82, 410012 Saratov, Russia.

Valeria Telnova (V)

Department of Biology, Saratov State University, Astrakhanskaya 82, 410012 Saratov, Russia.

Andrey Terskov (A)

Department of Biology, Saratov State University, Astrakhanskaya 82, 410012 Saratov, Russia.

Alexander Khorovodov (A)

Department of Biology, Saratov State University, Astrakhanskaya 82, 410012 Saratov, Russia.

Daria Elovenko (D)

Department of Biology, Saratov State University, Astrakhanskaya 82, 410012 Saratov, Russia.

Arina Evsukova (A)

Department of Biology, Saratov State University, Astrakhanskaya 82, 410012 Saratov, Russia.

Maria Zhoy (M)

Department of Biology, Saratov State University, Astrakhanskaya 82, 410012 Saratov, Russia.

Ilana Agranovich (I)

Department of Biology, Saratov State University, Astrakhanskaya 82, 410012 Saratov, Russia.

Elena Vodovozova (E)

Shemyakin-Ovchinnikov Institute of Bioorganic Chemistry, Russian Academy of Sciences, Miklukho-Maklaya 16/10, 117997 Moscow, Russia.

Anna Alekseeva (A)

Shemyakin-Ovchinnikov Institute of Bioorganic Chemistry, Russian Academy of Sciences, Miklukho-Maklaya 16/10, 117997 Moscow, Russia.

Jürgen Kurths (J)

Institute of Physics, Humboldt University, Newtonstrasse 15, 12489 Berlin, Germany.
Department of Biology, Saratov State University, Astrakhanskaya 82, 410012 Saratov, Russia.
Potsdam Institute for Climate Impact Research, Department of Complexity Science, Telegrafenberg A31, 14473 Potsdam, Germany.

Edik Rafailov (E)

Optoelectronics and Biomedical Photonics Group, Aston Institute of Photonic Technologies, Aston University, Birmingham B4 7ET, UK.

Classifications MeSH