Abstract

The photodynamic (PD) effect has been reported to be efficient for the opening of the blood-brain barrier (BBB), which provides a new informative platform for developing perspective strategies towards brain disease therapy and drug delivery. However, this method is usually performed via craniotomy due to high scattering of the turbid skull. In this work, we employed a newly-developed optical clearing skull window for investigating non-invasive PD-induced BBB opening to high weight molecules and 100-nm fluid-phase liposomes containing ganglioside GM1. The results demonstrated that the BBB permeability to the Evans blue albumin complex is related to laser doses. By in vivo two-photon imaging and ex vivo confocal imaging with specific markers of the BBB, we noticed PD-related extravasation of rhodamine-dextran and liposomes from the vessels into the brain parenchyma. The PD induced an increase in oxidative stress associated with mild hypoxia and changes in the expression of tight junction (CLND-5 and ZO-1) and adherens junction (VE-cadherin) proteins, which might be one of the mechanisms underlying the PD-related BBB opening for liposomes. Our experiments indicate that optical clearing skull window will be a promising tool for non-invasive PD-related BBB opening for high weight molecules and liposomes that provides a novel useful tool for brain drug delivery and treatment of brain diseases.

© 2018 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

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2018 (3)

X. Dong, “Current strategies for brain drug delivery,” Theranostics 8(6), 1481–1493 (2018).
[Crossref] [PubMed]

Y. J. Zhao, T. T. Yu, C. Zhang, Z. Li, Q. M. Luo, T. H. Xu, and D. Zhu, “Skull optical clearing window for in vivo imaging of the mouse cortex at synaptic resolution:erratum,” Light Sci. Appl. 7(1), 6 (2018).
[Crossref] [PubMed]

C. Zhang, W. Feng, Y. Zhao, T. Yu, P. Li, T. Xu, Q. Luo, and D. Zhu, “A large, switchable optical clearing skull window for cerebrovascular imaging,” Theranostics 8(10), 2696–2708 (2018).
[Crossref] [PubMed]

2017 (9)

M. Agrawal, D. K. Ajazuddin, D. K. Tripathi, S. Saraf, S. Saraf, S. G. Antimisiaris, S. Mourtas, M. Hammarlund-Udenaes, and A. Alexander, “Recent advancements in liposomes targeting strategies to cross blood-brain barrier (BBB) for the treatment of Alzheimer’s disease,” J. Control. Release 260, 61–77 (2017).
[Crossref] [PubMed]

Z. Belhadj, C. Zhan, M. Ying, X. Wei, C. Xie, Z. Yan, and W. Lu, “Multifunctional targeted liposomal drug delivery for efficient glioblastoma treatment,” Oncotarget 8(40), 66889–66900 (2017).
[Crossref] [PubMed]

W. Stummer, H. Stepp, O. D. Wiestler, and U. Pichlmeier, “Randomized, prospective double-blinded study comparing 3 different doses of 5-aminolevulinic acid for fluorescence-guided resections of malignant gliomas,” Neurosurgery 81(2), 230–239 (2017).
[Crossref] [PubMed]

Z. I. Kovacs, S. Kim, N. Jikaria, F. Qureshi, B. Milo, B. K. Lewis, M. Bresler, S. R. Burks, and J. A. Frank, “Disrupting the blood-brain barrier by focused ultrasound induces sterile inflammation,” Proc. Natl. Acad. Sci. U.S.A. 114(1), E75–E84 (2017).
[Crossref] [PubMed]

M. M. Patel and B. M. Patel, “Crossing the blood-brain barrier: recent advances in drug delivery to the brain,” CNS Drugs 31(2), 109–133 (2017).
[Crossref] [PubMed]

V. Kiviniemi, V. Korhonen, J. Kortelainen, S. Rytky, T. Keinänen, T. Tuovinen, M. Isokangas, E. Sonkajärvi, T. Siniluoto, J. Nikkinen, S. Alahuhta, O. Tervonen, T. Turpeenniemi-Hujanen, T. Myllylä, O. Kuittinen, and J. Voipio, “Real-time monitoring of human blood-brain barrier disruption,” PLoS One 12(3), e0174072 (2017).
[Crossref] [PubMed]

C. Poon, D. McMahon, and K. Hynynen, “Noninvasive and targeted delivery of therapeutics to the brain using focused ultrasound,” Neuropharmacology 120, 20–37 (2017).
[Crossref] [PubMed]

P. S. Fishman and V. Frenkel, “Focused ultrasound: an emerging therapeutic modality for neurologic disease,” Neurotherapeutics 14(2), 393–404 (2017).
[Crossref] [PubMed]

O. Semyachkina-Glushkovskaya, J. Kurths, E. Borisova, S. Sokolovski, V. Mantareva, I. Angelov, A. Shirokov, N. Navolokin, N. Shushunova, A. Khorovodov, M. Ulanova, M. Sagatova, I. Agranivich, O. Sindeeva, A. Gekalyuk, A. Bodrova, and E. Rafailov, “Photodynamic opening of blood-brain barrier,” Biomed. Opt. Express 8(11), 5040–5048 (2017).
[Crossref] [PubMed]

2016 (5)

H. Ito and H. Matsui, “Mitochondrial reactive oxygen species and photodynamic therapy,” Laser Ther. 25(3), 193–199 (2016).
[Crossref] [PubMed]

D. S. Hersh, A. S. Wadajkar, N. Roberts, J. G. Perez, N. P. Connolly, V. Frenkel, J. A. Winkles, G. F. Woodworth, and A. J. Kim, “Evolving drug delivery strategies to overcome the blood brain barrier,” Curr. Pharm. Des. 22(9), 1177–1193 (2016).
[Crossref] [PubMed]

L. Zhang, A. A. Habib, and D. Zhao, “Phosphatidylserine-targeted liposome for enhanced glioma-selective imaging,” Oncotarget 7(25), 38693–38706 (2016).
[Crossref] [PubMed]

D. B. Vieira and L. F. Gamarra, “Getting into the brain: liposome-based strategies for effective drug delivery across the blood-brain barrier,” Int. J. Nanomedicine 11, 5381–5414 (2016).
[Crossref] [PubMed]

S. Genheden and L. A. Eriksson, “Estimation of liposome penetration barriers of drug molecules with all-atom and coarse-grained models,” J. Chem. Theory Comput. 12(9), 4651–4661 (2016).
[Crossref] [PubMed]

2015 (5)

D. Silberberg, N. P. Anand, K. Michels, and R. N. Kalaria, “Brain and other nervous system disorders across the lifespan - global challenges and opportunities,” Nature 527(7578), S151–S154 (2015).
[Crossref] [PubMed]

N. Liu, X. Cui, D. M. Bryant, G. H. Glover, and A. L. Reiss, “Inferring deep-brain activity from cortical activity using functional near-infrared spectroscopy,” Biomed. Opt. Express 6(3), 1074–1089 (2015).
[Crossref] [PubMed]

O. Semyachkina-Glushkovskaya, A. Pavlov, J. Kurths, E. Borisova, A. Gisbrecht, O. Sindeeva, A. Abdurashitov, A. Shirokov, N. Navolokin, E. Zinchenko, A. Gekalyuk, M. Ulanova, D. Zhu, Q. Luo, and V. Tuchin, “Optical monitoring of stress-related changes in the brain tissues and vessels associated with hemorrhagic stroke in newborn rats,” Biomed. Opt. Express 6(10), 4088–4097 (2015).
[Crossref] [PubMed]

H. L. Wang and T. W. Lai, “Optimization of Evans blue quantitation in limited rat tissue samples,” Sci. Rep. 4(1), 6588 (2015).
[Crossref] [PubMed]

Z. Geng, X. Tong, and H. Jia, “Reactive oxygen species (ROS) mediates non-freezing cold injury of rat sciatic nerve,” Int. J. Clin. Exp. Med. 8(9), 15700–15707 (2015).
[PubMed]

2014 (2)

J. P. M. Jämbeck, E. S. E. Eriksson, A. Laaksonen, A. P. Lyubartsev, and L. A. Eriksson, “Molecular dynamics studies of liposomes as carriers for photosensitizing drugs: development, validation, and simulations with a coarse-grained model,” J. Chem. Theory Comput. 10(1), 5–13 (2014).
[Crossref] [PubMed]

J. Wang, Y. Zhang, P. C. Li, Q. M. Luo, and D. Zhu, “Review: tissue optical clearing window for blood flow monitoring,” IEEE J. Sel. Top. Quant. 20, 6801112 (2014).

2013 (5)

S. J. Madsen, H. M. Gach, S. J. Hong, F. A. Uzal, Q. Peng, and H. Hirschberg, “Increased nanoparticle-loaded exogenous macrophage migration into the brain following PDT-induced blood-brain barrier disruption,” Lasers Surg. Med. 45(8), 524–532 (2013).
[PubMed]

D. Zhu, K. V. Larin, Q. Luo, and V. V. Tuchin, “Recent progress in tissue optical clearing,” Laser Photonics Rev. 7(5), 732–757 (2013).
[Crossref] [PubMed]

I. Karaiskos, L. Galani, F. Baziaka, and H. Giamarellou, “Intraventricular and intrathecal colistin as the last therapeutic resort for the treatment of multidrug-resistant and extensively drug-resistant Acinetobacter baumannii ventriculitis and meningitis: a literature review,” Int. J. Antimicrob. Agents 41(6), 499–508 (2013).
[Crossref] [PubMed]

S. Mitragotri, “Devices for overcoming biological barriers: The use of physical forces to disrupt the barriers,” Adv. Drug Deliv. Rev. 65(1), 100–103 (2013).
[Crossref] [PubMed]

J. K. Hebda, H. M. Leclair, S. Azzi, C. Roussel, M. G. Scott, N. Bidère, and J. Gavard, “The C-terminus region of β-arrestin1 modulates VE-cadherin expression and endothelial cell permeability,” Cell Commun. Signal. 11(1), 37 (2013).
[Crossref] [PubMed]

2012 (2)

J. Wang, Y. Zhang, T. H. Xu, Q. M. Luo, and D. Zhu, “An innovative transparent cranial window based on skull optical clearing,” Laser Phys. Lett. 9(6), 469–473 (2012).
[Crossref]

N. R. Kuznetsova, C. Sevrin, D. Lespineux, N. V. Bovin, E. L. Vodovozova, T. Mészáros, J. Szebeni, and C. Grandfils, “Hemocompatibility of liposomes loaded with lipophilic prodrugs of methotrexate and melphalan in the lipid bilayer,” J. Control. Release 160(2), 394–400 (2012).
[Crossref] [PubMed]

2011 (1)

M. R. Hara, J. J. Kovacs, E. J. Whalen, S. Rajagopal, R. T. Strachan, W. Grant, A. J. Towers, B. Williams, C. M. Lam, K. Xiao, S. K. Shenoy, S. G. Gregory, S. Ahn, D. R. Duckett, and R. J. Lefkowitz, “A stress response pathway regulates DNA damage through β2-adrenoreceptors and β-arrestin-1,” Nature 477(7364), 349–353 (2011).
[Crossref] [PubMed]

2010 (4)

N. J. Abbott, A. A. K. Patabendige, D. E. M. Dolman, S. R. Yusof, and D. J. Begley, “Structure and function of the blood-brain barrier,” Neurobiol. Dis. 37(1), 13–25 (2010).
[Crossref] [PubMed]

S. V. Dhuria, L. R. Hanson, and W. H. Frey, “Intranasal Delivery to the Central Nervous System: Mechanisms and Experimental Considerations,” J. Pharm. Sci. 99(4), 1654–1673 (2010).
[Crossref] [PubMed]

J. Huppert, D. Closhen, A. Croxford, R. White, P. Kulig, E. Pietrowski, I. Bechmann, B. Becher, H. J. Luhmann, A. Waisman, and C. R. W. Kuhlmann, “Cellular mechanisms of IL-17-induced blood-brain barrier disruption,” FASEB J. 24(4), 1023–1034 (2010).
[Crossref] [PubMed]

S. J. Madsen and H. Hirschberg, “Site-specific opening of the blood-brain barrier,” J. Biophotonics 3(5-6), 356–367 (2010).
[Crossref] [PubMed]

2008 (2)

H. Hirschberg, F. A. Uzal, D. Chighvinadze, M. J. Zhang, Q. Peng, and S. J. Madsen, “Disruption of the blood-brain barrier following ALA-mediated photodynamic therapy,” Lasers Surg. Med. 40(8), 535–542 (2008).
[Crossref] [PubMed]

Z. Petrásek and P. Schwille, “Photobleaching in two-photon scanning fluorescence correlation spectroscopy,” ChemPhysChem 9(1), 147–158 (2008).
[Crossref] [PubMed]

2007 (3)

S. S. Hu, H. B. Cheng, Y. R. Zheng, R. Y. Zhang, W. Yue, and H. Zhang, “Effects of photodynamic therapy on the ultrastructure of glioma cells,” Biomed. Environ. Sci. 20(4), 269–273 (2007).
[PubMed]

I. A. Boldyrev, X. Zhai, M. M. Momsen, H. L. Brockman, R. E. Brown, and J. G. Molotkovsky, “New BODIPY lipid probes for fluorescence studies of membranes,” J. Lipid Res. 48(7), 1518–1532 (2007).
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H. T. Xu, F. Pan, G. Yang, and W. B. Gan, “Choice of cranial window type for in vivo imaging affects dendritic spine turnover in the cortex,” Nat. Neurosci. 10(5), 549–551 (2007).
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2006 (1)

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2005 (1)

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2004 (1)

P. Ballabh, A. Braun, and M. Nedergaard, “The blood-brain barrier: an overview: Structure, regulation, and clinical implications,” Neurobiol. Dis. 16(1), 1–13 (2004).
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2002 (1)

M. Mora, M. L. Sagristá, D. Trombetta, F. P. Bonina, A. De Pasquale, and A. Saija, “Design and characterization of liposomes containing long-chain N-acylPEs for brain delivery: Penetration of liposomes incorporating GM1 into the rat brain,” Pharm. Res. 19(10), 1430–1438 (2002).
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2000 (1)

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1988 (1)

A. Gabizon and D. Papahadjopoulos, “Liposome formulations with prolonged circulation time in blood and enhanced uptake by tumors,” Proc. Natl. Acad. Sci. U.S.A. 85(18), 6949–6953 (1988).
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1980 (1)

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1979 (1)

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N. J. Abbott, A. A. K. Patabendige, D. E. M. Dolman, S. R. Yusof, and D. J. Begley, “Structure and function of the blood-brain barrier,” Neurobiol. Dis. 37(1), 13–25 (2010).
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P. Ballabh, A. Braun, and M. Nedergaard, “The blood-brain barrier: an overview: Structure, regulation, and clinical implications,” Neurobiol. Dis. 16(1), 1–13 (2004).
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I. Karaiskos, L. Galani, F. Baziaka, and H. Giamarellou, “Intraventricular and intrathecal colistin as the last therapeutic resort for the treatment of multidrug-resistant and extensively drug-resistant Acinetobacter baumannii ventriculitis and meningitis: a literature review,” Int. J. Antimicrob. Agents 41(6), 499–508 (2013).
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N. J. Abbott, A. A. K. Patabendige, D. E. M. Dolman, S. R. Yusof, and D. J. Begley, “Structure and function of the blood-brain barrier,” Neurobiol. Dis. 37(1), 13–25 (2010).
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M. Mora, M. L. Sagristá, D. Trombetta, F. P. Bonina, A. De Pasquale, and A. Saija, “Design and characterization of liposomes containing long-chain N-acylPEs for brain delivery: Penetration of liposomes incorporating GM1 into the rat brain,” Pharm. Res. 19(10), 1430–1438 (2002).
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Bovin, N. V.

N. R. Kuznetsova, C. Sevrin, D. Lespineux, N. V. Bovin, E. L. Vodovozova, T. Mészáros, J. Szebeni, and C. Grandfils, “Hemocompatibility of liposomes loaded with lipophilic prodrugs of methotrexate and melphalan in the lipid bilayer,” J. Control. Release 160(2), 394–400 (2012).
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P. Ballabh, A. Braun, and M. Nedergaard, “The blood-brain barrier: an overview: Structure, regulation, and clinical implications,” Neurobiol. Dis. 16(1), 1–13 (2004).
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Z. I. Kovacs, S. Kim, N. Jikaria, F. Qureshi, B. Milo, B. K. Lewis, M. Bresler, S. R. Burks, and J. A. Frank, “Disrupting the blood-brain barrier by focused ultrasound induces sterile inflammation,” Proc. Natl. Acad. Sci. U.S.A. 114(1), E75–E84 (2017).
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I. A. Boldyrev, X. Zhai, M. M. Momsen, H. L. Brockman, R. E. Brown, and J. G. Molotkovsky, “New BODIPY lipid probes for fluorescence studies of membranes,” J. Lipid Res. 48(7), 1518–1532 (2007).
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I. A. Boldyrev, X. Zhai, M. M. Momsen, H. L. Brockman, R. E. Brown, and J. G. Molotkovsky, “New BODIPY lipid probes for fluorescence studies of membranes,” J. Lipid Res. 48(7), 1518–1532 (2007).
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Burks, S. R.

Z. I. Kovacs, S. Kim, N. Jikaria, F. Qureshi, B. Milo, B. K. Lewis, M. Bresler, S. R. Burks, and J. A. Frank, “Disrupting the blood-brain barrier by focused ultrasound induces sterile inflammation,” Proc. Natl. Acad. Sci. U.S.A. 114(1), E75–E84 (2017).
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S. S. Hu, H. B. Cheng, Y. R. Zheng, R. Y. Zhang, W. Yue, and H. Zhang, “Effects of photodynamic therapy on the ultrastructure of glioma cells,” Biomed. Environ. Sci. 20(4), 269–273 (2007).
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H. Hirschberg, F. A. Uzal, D. Chighvinadze, M. J. Zhang, Q. Peng, and S. J. Madsen, “Disruption of the blood-brain barrier following ALA-mediated photodynamic therapy,” Lasers Surg. Med. 40(8), 535–542 (2008).
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J. Huppert, D. Closhen, A. Croxford, R. White, P. Kulig, E. Pietrowski, I. Bechmann, B. Becher, H. J. Luhmann, A. Waisman, and C. R. W. Kuhlmann, “Cellular mechanisms of IL-17-induced blood-brain barrier disruption,” FASEB J. 24(4), 1023–1034 (2010).
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D. S. Hersh, A. S. Wadajkar, N. Roberts, J. G. Perez, N. P. Connolly, V. Frenkel, J. A. Winkles, G. F. Woodworth, and A. J. Kim, “Evolving drug delivery strategies to overcome the blood brain barrier,” Curr. Pharm. Des. 22(9), 1177–1193 (2016).
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J. Huppert, D. Closhen, A. Croxford, R. White, P. Kulig, E. Pietrowski, I. Bechmann, B. Becher, H. J. Luhmann, A. Waisman, and C. R. W. Kuhlmann, “Cellular mechanisms of IL-17-induced blood-brain barrier disruption,” FASEB J. 24(4), 1023–1034 (2010).
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De Pasquale, A.

M. Mora, M. L. Sagristá, D. Trombetta, F. P. Bonina, A. De Pasquale, and A. Saija, “Design and characterization of liposomes containing long-chain N-acylPEs for brain delivery: Penetration of liposomes incorporating GM1 into the rat brain,” Pharm. Res. 19(10), 1430–1438 (2002).
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S. V. Dhuria, L. R. Hanson, and W. H. Frey, “Intranasal Delivery to the Central Nervous System: Mechanisms and Experimental Considerations,” J. Pharm. Sci. 99(4), 1654–1673 (2010).
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Dolman, D. E. M.

N. J. Abbott, A. A. K. Patabendige, D. E. M. Dolman, S. R. Yusof, and D. J. Begley, “Structure and function of the blood-brain barrier,” Neurobiol. Dis. 37(1), 13–25 (2010).
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X. Dong, “Current strategies for brain drug delivery,” Theranostics 8(6), 1481–1493 (2018).
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M. R. Hara, J. J. Kovacs, E. J. Whalen, S. Rajagopal, R. T. Strachan, W. Grant, A. J. Towers, B. Williams, C. M. Lam, K. Xiao, S. K. Shenoy, S. G. Gregory, S. Ahn, D. R. Duckett, and R. J. Lefkowitz, “A stress response pathway regulates DNA damage through β2-adrenoreceptors and β-arrestin-1,” Nature 477(7364), 349–353 (2011).
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J. P. M. Jämbeck, E. S. E. Eriksson, A. Laaksonen, A. P. Lyubartsev, and L. A. Eriksson, “Molecular dynamics studies of liposomes as carriers for photosensitizing drugs: development, validation, and simulations with a coarse-grained model,” J. Chem. Theory Comput. 10(1), 5–13 (2014).
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S. Genheden and L. A. Eriksson, “Estimation of liposome penetration barriers of drug molecules with all-atom and coarse-grained models,” J. Chem. Theory Comput. 12(9), 4651–4661 (2016).
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C. Zhang, W. Feng, Y. Zhao, T. Yu, P. Li, T. Xu, Q. Luo, and D. Zhu, “A large, switchable optical clearing skull window for cerebrovascular imaging,” Theranostics 8(10), 2696–2708 (2018).
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Z. I. Kovacs, S. Kim, N. Jikaria, F. Qureshi, B. Milo, B. K. Lewis, M. Bresler, S. R. Burks, and J. A. Frank, “Disrupting the blood-brain barrier by focused ultrasound induces sterile inflammation,” Proc. Natl. Acad. Sci. U.S.A. 114(1), E75–E84 (2017).
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P. S. Fishman and V. Frenkel, “Focused ultrasound: an emerging therapeutic modality for neurologic disease,” Neurotherapeutics 14(2), 393–404 (2017).
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D. S. Hersh, A. S. Wadajkar, N. Roberts, J. G. Perez, N. P. Connolly, V. Frenkel, J. A. Winkles, G. F. Woodworth, and A. J. Kim, “Evolving drug delivery strategies to overcome the blood brain barrier,” Curr. Pharm. Des. 22(9), 1177–1193 (2016).
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S. V. Dhuria, L. R. Hanson, and W. H. Frey, “Intranasal Delivery to the Central Nervous System: Mechanisms and Experimental Considerations,” J. Pharm. Sci. 99(4), 1654–1673 (2010).
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A. Gabizon and D. Papahadjopoulos, “Liposome formulations with prolonged circulation time in blood and enhanced uptake by tumors,” Proc. Natl. Acad. Sci. U.S.A. 85(18), 6949–6953 (1988).
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S. J. Madsen, H. M. Gach, S. J. Hong, F. A. Uzal, Q. Peng, and H. Hirschberg, “Increased nanoparticle-loaded exogenous macrophage migration into the brain following PDT-induced blood-brain barrier disruption,” Lasers Surg. Med. 45(8), 524–532 (2013).
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I. Karaiskos, L. Galani, F. Baziaka, and H. Giamarellou, “Intraventricular and intrathecal colistin as the last therapeutic resort for the treatment of multidrug-resistant and extensively drug-resistant Acinetobacter baumannii ventriculitis and meningitis: a literature review,” Int. J. Antimicrob. Agents 41(6), 499–508 (2013).
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D. B. Vieira and L. F. Gamarra, “Getting into the brain: liposome-based strategies for effective drug delivery across the blood-brain barrier,” Int. J. Nanomedicine 11, 5381–5414 (2016).
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H. T. Xu, F. Pan, G. Yang, and W. B. Gan, “Choice of cranial window type for in vivo imaging affects dendritic spine turnover in the cortex,” Nat. Neurosci. 10(5), 549–551 (2007).
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J. K. Hebda, H. M. Leclair, S. Azzi, C. Roussel, M. G. Scott, N. Bidère, and J. Gavard, “The C-terminus region of β-arrestin1 modulates VE-cadherin expression and endothelial cell permeability,” Cell Commun. Signal. 11(1), 37 (2013).
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I. Karaiskos, L. Galani, F. Baziaka, and H. Giamarellou, “Intraventricular and intrathecal colistin as the last therapeutic resort for the treatment of multidrug-resistant and extensively drug-resistant Acinetobacter baumannii ventriculitis and meningitis: a literature review,” Int. J. Antimicrob. Agents 41(6), 499–508 (2013).
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M. R. Hara, J. J. Kovacs, E. J. Whalen, S. Rajagopal, R. T. Strachan, W. Grant, A. J. Towers, B. Williams, C. M. Lam, K. Xiao, S. K. Shenoy, S. G. Gregory, S. Ahn, D. R. Duckett, and R. J. Lefkowitz, “A stress response pathway regulates DNA damage through β2-adrenoreceptors and β-arrestin-1,” Nature 477(7364), 349–353 (2011).
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M. R. Hara, J. J. Kovacs, E. J. Whalen, S. Rajagopal, R. T. Strachan, W. Grant, A. J. Towers, B. Williams, C. M. Lam, K. Xiao, S. K. Shenoy, S. G. Gregory, S. Ahn, D. R. Duckett, and R. J. Lefkowitz, “A stress response pathway regulates DNA damage through β2-adrenoreceptors and β-arrestin-1,” Nature 477(7364), 349–353 (2011).
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L. Zhang, A. A. Habib, and D. Zhao, “Phosphatidylserine-targeted liposome for enhanced glioma-selective imaging,” Oncotarget 7(25), 38693–38706 (2016).
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[Crossref] [PubMed]

Hanson, L. R.

S. V. Dhuria, L. R. Hanson, and W. H. Frey, “Intranasal Delivery to the Central Nervous System: Mechanisms and Experimental Considerations,” J. Pharm. Sci. 99(4), 1654–1673 (2010).
[Crossref] [PubMed]

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M. R. Hara, J. J. Kovacs, E. J. Whalen, S. Rajagopal, R. T. Strachan, W. Grant, A. J. Towers, B. Williams, C. M. Lam, K. Xiao, S. K. Shenoy, S. G. Gregory, S. Ahn, D. R. Duckett, and R. J. Lefkowitz, “A stress response pathway regulates DNA damage through β2-adrenoreceptors and β-arrestin-1,” Nature 477(7364), 349–353 (2011).
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J. K. Hebda, H. M. Leclair, S. Azzi, C. Roussel, M. G. Scott, N. Bidère, and J. Gavard, “The C-terminus region of β-arrestin1 modulates VE-cadherin expression and endothelial cell permeability,” Cell Commun. Signal. 11(1), 37 (2013).
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Hersh, D. S.

D. S. Hersh, A. S. Wadajkar, N. Roberts, J. G. Perez, N. P. Connolly, V. Frenkel, J. A. Winkles, G. F. Woodworth, and A. J. Kim, “Evolving drug delivery strategies to overcome the blood brain barrier,” Curr. Pharm. Des. 22(9), 1177–1193 (2016).
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Hirschberg, H.

S. J. Madsen, H. M. Gach, S. J. Hong, F. A. Uzal, Q. Peng, and H. Hirschberg, “Increased nanoparticle-loaded exogenous macrophage migration into the brain following PDT-induced blood-brain barrier disruption,” Lasers Surg. Med. 45(8), 524–532 (2013).
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S. J. Madsen and H. Hirschberg, “Site-specific opening of the blood-brain barrier,” J. Biophotonics 3(5-6), 356–367 (2010).
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H. Hirschberg, F. A. Uzal, D. Chighvinadze, M. J. Zhang, Q. Peng, and S. J. Madsen, “Disruption of the blood-brain barrier following ALA-mediated photodynamic therapy,” Lasers Surg. Med. 40(8), 535–542 (2008).
[Crossref] [PubMed]

Hong, S. J.

S. J. Madsen, H. M. Gach, S. J. Hong, F. A. Uzal, Q. Peng, and H. Hirschberg, “Increased nanoparticle-loaded exogenous macrophage migration into the brain following PDT-induced blood-brain barrier disruption,” Lasers Surg. Med. 45(8), 524–532 (2013).
[PubMed]

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S. S. Hu, H. B. Cheng, Y. R. Zheng, R. Y. Zhang, W. Yue, and H. Zhang, “Effects of photodynamic therapy on the ultrastructure of glioma cells,” Biomed. Environ. Sci. 20(4), 269–273 (2007).
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F. Olson, C. A. Hunt, F. C. Szoka, W. J. Vail, and D. Papahadjopoulos, “Preparation of liposomes of defined size distribution by extrusion through polycarbonate membranes,” Biochim. Biophys. Acta 557(1), 9–23 (1979).
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J. Huppert, D. Closhen, A. Croxford, R. White, P. Kulig, E. Pietrowski, I. Bechmann, B. Becher, H. J. Luhmann, A. Waisman, and C. R. W. Kuhlmann, “Cellular mechanisms of IL-17-induced blood-brain barrier disruption,” FASEB J. 24(4), 1023–1034 (2010).
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C. Poon, D. McMahon, and K. Hynynen, “Noninvasive and targeted delivery of therapeutics to the brain using focused ultrasound,” Neuropharmacology 120, 20–37 (2017).
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V. Kiviniemi, V. Korhonen, J. Kortelainen, S. Rytky, T. Keinänen, T. Tuovinen, M. Isokangas, E. Sonkajärvi, T. Siniluoto, J. Nikkinen, S. Alahuhta, O. Tervonen, T. Turpeenniemi-Hujanen, T. Myllylä, O. Kuittinen, and J. Voipio, “Real-time monitoring of human blood-brain barrier disruption,” PLoS One 12(3), e0174072 (2017).
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Figures (5)

Fig. 1
Fig. 1 PD-induced opening of BBB through optical clearing skull window
Fig. 2
Fig. 2 The histological analysis of PD-related changes in the brain tissues and cerebral vessels. The black arrows show vasogenic edema.
Fig. 3
Fig. 3 The in vivo analysis of PD-induced BBB opening for rhodamine-dextran. (a) The timeline of the experiment. (b) and (c) are the same area imaged by 2PLSM before and after PD. (d) and (e) are the magnified images corresponding to the areas boxed in (b) and (c), respectively. (f) The bar graph of the average signal intensity inside (1-6) and outside (1’-6’) vessels.
Fig. 4
Fig. 4 The confocal imaging of non-invasive PD-induced BBB opening for GM1-liposomes with usage of markers of neurovascular unit: (a) liposomes distributions between the astrocytes labelled by antibodies of GFAP; (b) liposomes leakage outside the vascular endothelial cells labelled by antibodies of SMI; (c) liposomes distributions outside the basal membrane labelled by antibodies of laminin. Approximately 10-12 brain slices per animal (n = 6) were imaged. The white arrows show the sites of liposomes leakage.
Fig. 5
Fig. 5 Mechanisms underlying PD opening of BBB for GM1-liposomes. (a) The expression of TJ (CLDN-5 and ZO-1) and adhesion (VE-cadherin) proteins as well trans-membrane protein of cellular signalling system (ARRB1). ***-p<0.001, the comparison between PD-treated mice and untreated mice. (b) Schema of photodynamic opening of BBB: PD activates the internalization of CLND-5 and VE-cadherin that is accompanied by the loss of surface of these proteins in the space between vascular endothelial cells. (c) The PD-induced changes in the MDA level in the brain tissues. (d) The PD-induced changes in cerebral SpO2. *-p<0.05 the comparison between PD-treated mice and untreated mice.

Tables (1)

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Table 1 PD-induced BBB opening for the EBd albumin complex

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