Development of Novel Therapeutics Targeting the Blood–Brain Barrier: From Barrier to Carrier
Open accessAbstract
The blood–brain barrier (BBB) is a highly specialized neurovascular unit, initially described as an intact barrier to prevent toxins, pathogens, and potentially harmful substances from entering the brain. An intact BBB is also critical for the maintenance of normal neuronal function. In cerebral vascular diseases and neurological disorders, the BBB can be disrupted, contributing to disease progression. While restoration of BBB integrity serves as a robust biomarker of better clinical outcomes, the restrictive nature of the intact BBB presents a major hurdle for delivery of therapeutics into the brain. Recent studies show that the BBB is actively engaged in crosstalk between neuronal and the circulatory systems, which defines another important role of the BBB: as an interfacing conduit that mediates communication between two sides of the BBB. This role has been subject to extensive investigation for brain‐targeted drug delivery and shows promising results. The dual roles of the BBB make it a unique target for drug development. Here, recent developments and novel strategies to target the BBB for therapeutic purposes are reviewed, from both barrier and carrier perspectives.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
A major impediment to effective pharmacological treatment of CNS disorders is the blood-brain barrier (BBB).
“When it comes to pharmacological drugs, a major impediment to effective treatment is the BBB [102].”
From Extracellular vesicles as nanotheranostic platforms for targeted neurological disorder interventions (2024) · cites this paper as [102]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Astrocyte-endothelial interactions at the blood-brain barrier
Abbott, N. J., Rönnbäck, L., & Hansson, E. (2006) · Nature Reviews Neuroscience · doi:10.1038/nrn1824 · Cited by 5,595 · see citing works
Neurovascular pathways to neurodegeneration in Alzheimer’s disease and other disorders
Zlokovic, B. V. (2011) · Nature Reviews Neuroscience · doi:10.1038/nrn3114 · Cited by 2,969 · see citing works
Blood-brain barrier breakdown in the aging human hippocampus
Montagne, A., Barnes, S. R., Sweeney, M. D., Halliday, M. R., Sagare, A. P., Zhao, Z., Toga, A. W., Jacobs, R. E., Liu, C. Y., Amezcua, L., et al. (2015) · Neuron · doi:10.1016/j.neuron.2014.12.032 · Cited by 2,102 · see citing works
A molecular atlas of cell types and zonation in the brain vasculature
Vanlandewijck, M., He, L., Mäe, M. A., Andrae, J., Ando, K., Del Gaudio, F., Nahar, K., Lebouvier, T., Laviña, B., Gouveia, L., et al. (2018) · Nature · doi:10.1038/nature25739 · Cited by 2,074 · see citing works
Size-selective loosening of the blood-brain barrier in claudin-5–deficient mice
Nitta, T., Hata, M., Gotoh, S., Seo, Y., Sasaki, H., Hashimoto, N., Furuse, M., & Tsukita, S. (2003) · The Journal of Cell Biology · doi:10.1083/jcb.200302070 · Cited by 1,917 · see citing works
Intravascular AAV9 preferentially targets neonatal neurons and adult astrocytes
Foust, K. D., Nurre, E., Montgomery, C. L., Hernandez, A., Chan, C. M., & Kaspar, B. K. (2009) · Nature Biotechnology · doi:10.1038/nbt.1515 · Cited by 1,456 · see citing works
VEGF enhances angiogenesis and promotes blood–brain barrier leakage in the ischemic brain
Zhang, Z. G., Zhang, L., Jiang, Q., Zhang, R., Davies, K., Powers, C., Bruggen, N. V., & Chopp, M. (2000) · Journal of Clinical Investigation · doi:10.1172/jci9369 · Cited by 1,296 · see citing works
Human Gut Microbiota from Autism Spectrum Disorder Promote Behavioral Symptoms in Mice
Sharon, G., Cruz, N. J., Kang, D.-W., Gandal, M. J., Wang, B., Kim, Y.-M., Zink, E. M., Casey, C. P., Taylor, B. C., Lane, C. J., et al. (2019) · Cell · doi:10.1016/j.cell.2019.05.004 · Cited by 1,182 · see citing works
Pericytes of the neurovascular unit: key functions and signaling pathways
Sweeney, M. D., Ayyadurai, S., & Zlokovic, B. V. (2016) · Nature Neuroscience · doi:10.1038/nn.4288 · Cited by 1,125 · see citing works
Social stress induces neurovascular pathology promoting depression
Menard, C., Pfau, M. L., Hodes, G. E., Kana, V., Wang, V. X., Bouchard, S., Takahashi, A., Flanigan, M. E., Aleyasin, H., LeClair, K. B., et al. (2017) · Nature Neuroscience · doi:10.1038/s41593-017-0010-3 · Cited by 1,028 · see citing works
Dual microglia effects on blood brain barrier permeability induced by systemic inflammation
Haruwaka, K., Ikegami, A., Tachibana, Y., Ohno, N., Konishi, H., Hashimoto, A., Matsumoto, M., Kato, D., Ono, R., Kiyama, H., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-13812-z · Cited by 923 · see citing works
Large-scale generation of functional mRNA-encapsulating exosomes via cellular nanoporation
Yang, Z., Shi, J., Xie, J., Wang, Y., Sun, J., Liu, T., Zhao, Y., Zhao, X., Wang, X., Ma, Y., et al. (2019) · Nature Biomedical Engineering · doi:10.1038/s41551-019-0485-1 · Cited by 744 · see citing works
History and progress of hypotheses and clinical trials for Alzheimer’s disease
Liu, P.-P., Xie, Y., Meng, X.-Y., & Kang, J.-S. (2019) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-019-0063-8 · Cited by 723 · see citing works
GLUT1 reductions exacerbate Alzheimer's disease vasculo-neuronal dysfunction and degeneration
Winkler, E. A., Nishida, Y., Sagare, A. P., Rege, S. V., Bell, R. D., Perlmutter, D., Sengillo, J. D., Hillman, S., Kong, P., Nelson, A. R., et al. (2015) · Nature Neuroscience · doi:10.1038/nn.3966 · Cited by 689 · see citing works
Cirrito, J. R. (2005) · Journal of Clinical Investigation · doi:10.1172/jci25247 · Cited by 660 · see citing works
Banks, W. A., Sharma, P., Bullock, K. M., Hansen, K. M., Ludwig, N., & Whiteside, T. L. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21124407 · Cited by 561 · see citing works
Self-citationEndothelial LRP1 transports amyloid-β1–42 across the blood-brain barrier
Storck, S. E., Meister, S., Nahrath, J., Meißner, J. N., Schubert, N., Di Spiezio, A., Baches, S., Vandenbroucke, R. E., Bouter, Y., Prikulis, I., et al. (2015) · Journal of Clinical Investigation · doi:10.1172/jci81108 · Cited by 477 · see citing works
Altered Gut Microbiota in a Mouse Model of Alzheimer’s Disease
Zhang, L., Wang, Y., Xiayu, X., Shi, C., Chen, W., Song, N., Fu, X., Zhou, R., Xu, Y.-F., Huang, L., et al. (2017) · Journal of Alzheimer s Disease · doi:10.3233/jad-170020 · Cited by 449 · see citing works
Macrophages at CNS interfaces: Ontogeny and function in health and disease
Kierdorf, K., Masuda, T., Jordão, M. J. C., & Prinz, M. (2019) · Nature Reviews Neuroscience · doi:10.1038/s41583-019-0201-x · Cited by 416 · see citing works
Recirculating Intestinal IgA-Producing Cells Regulate Neuroinflammation via IL-10
Rojas, O. L., Pröbstel, A.-K., Porfilio, E. A., Wang, A. A., Charabati, M., Sun, T., Lee, D. S. W., Galicia, G., Ramaglia, V., Ward, L. A., et al. (2019) · Cell · doi:10.1016/j.cell.2018.11.035 · Cited by 382 · see citing works
Therapeutic bispecific antibodies cross the blood-brain barrier in nonhuman primates
Yu, Y. J., Atwal, J. K., Zhang, Y., Tong, R. K., Wildsmith, K. R., Tan, C., Bien-Ly, N., Hersom, M., Maloney, J. A., Meilandt, W. J., et al. (2014) · Science Translational Medicine · doi:10.1126/scitranslmed.3009835 · Cited by 371 · see citing works
Overexpression of ABCA1 reduces amyloid deposition in the PDAPP mouse model of Alzheimer disease
Wahrle, S. E., Jiang, H., Parsadanian, M., Kim, J., Li, A., Knoten, A., Jain, S., Hirsch-Reinshagen, V., Wellington, C. L., Bales, K. R., et al. (2008) · Journal of Clinical Investigation · doi:10.1172/jci33622 · Cited by 370 · see citing works
Noninvasive hippocampal blood-brain barrier opening in Alzheimer's disease with focused ultrasound.
Rezai, A. R., Ranjan, M., D’Haese, P.-F., Haut, M. W., Carpenter, J., Najib, U., Mehta, R. I., Chazen, J. L., Zibly, Z., Yates, J. R., et al. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2002571117 · Cited by 365 · see citing works
Molecular adaptations of the blood–brain barrier promote stress resilience vs. depression
Dudek, K. A., Dion-Albert, L., Lebel, M., LeClair, K., Labrecque, S., Tuck, E., Ferrer Perez, C., Golden, S. A., Tamminga, C., Turecki, G., et al. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1914655117 · Cited by 361 · see citing works
Kloepper, J., Riedemann, L., Amoozgar, Z., Seano, G., Susek, K., Yu, V., Dalvie, N., Amelung, R. L., Datta, M., Song, J. W., et al. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1525360113 · Cited by 357 · see citing works
Kang, D. E., Pietrzik, C. U., Baum, L., Chevallier, N., Merriam, D. E., Kounnas, M. Z., Wagner, S. L., Troncoso, J. C., Kawas, C. H., Katzman, R., et al. (2000) · Journal of Clinical Investigation · doi:10.1172/jci11013 · Cited by 354 · see citing works
Krishna, V., Sammartino, F., & Rezai, A. (2018) · JAMA Neurology · doi:10.1001/jamaneurol.2017.3129 · Cited by 289 · see citing works
Senatorov, V. V., Friedman, A. R., Milikovsky, D. Z., Ofer, J., Saar-Ashkenazy, R., Charbash, A., Jahan, N., Chin, G., Mihaly, E., Lin, J. M., et al. (2019) · Science Translational Medicine · doi:10.1126/scitranslmed.aaw8283 · Cited by 257 · see citing works
Regulation of ABC efflux transporters at blood-brain barrier in health and neurological disorders
Qosa, H., Miller, D. S., Pasinelli, P., & Trotti, D. (2015) · Brain Research · doi:10.1016/j.brainres.2015.07.005 · Cited by 249 · see citing works
Transcriptional and epigenomic landscapes of CNS and non-CNS vascular endothelial cells
Sabbagh, M. F., Heng, J. S., Luo, C., Castanon, R. G., Nery, J. R., Rattner, A., Goff, L. A., Ecker, J. R., & Nathans, J. (2018) · eLife · doi:10.7554/elife.36187 · Cited by 245 · see citing works
Nanotechnology-based strategies for siRNA brain delivery for disease therapy
Zheng, M., Tao, W., Zou, Y., Farokhzad, O. C., & Shi, B. (2018) · Trends in biotechnology · doi:10.1016/j.tibtech.2018.01.006 · Cited by 210 · see citing works
Self-citationShi, M., Kovac, A., Korff, A., Cook, T. J., Ginghina, C., Bullock, K. M., Yang, L., Stewart, T., Zheng, D., Aro, P., et al. (2016) · Alzheimer's & Dementia · doi:10.1016/j.jalz.2016.04.003 · Cited by 206 · see citing works
Self-citationPersidsky, Y., Heilman, D., Haorah, J., Zelivyanskaya, M., Persidsky, R., Weber, G. A., Shimokawa, H., Kaibuchi, K., & Ikezu, T. (2006) · Blood · doi:10.1182/blood-2005-11-4721 · Cited by 200 · see citing works
Nanotechnology—novel therapeutics for CNS disorders
Srikanth, M., & Kessler, J. A. (2012) · Nature Reviews Neurology · doi:10.1038/nrneurol.2012.76 · Cited by 198 · see citing works
Howard, R., Zubko, O., Bradley, R., Harper, E., Pank, L., O’Brien, J., Fox, C., Tabet, N., Livingston, G., Bentham, P., et al. (2020) · JAMA Neurology · doi:10.1001/jamaneurol.2019.3762 · Cited by 194 · see citing works
Deo, A. K., Borson, S., Link, J. M., Domino, K., Eary, J. F., Ke, B., Richards, T. L., Mankoff, D. A., Minoshima, S., O’Sullivan, F., et al. (2014) · Journal of Nuclear Medicine · doi:10.2967/jnumed.113.130161 · Cited by 193 · see citing works
Casas, A. I., Geuss, E., Kleikers, P. W. M., Mencl, S., Herrmann, A. M., Buendia, I., Egea, J., Meuth, S. G., Lopez, M. G., Kleinschnitz, C., et al. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1705034114 · Cited by 152 · see citing works
Miner, J. J., Daniels, B. P., Shrestha, B., Proenca-Modena, J. L., Lew, E. D., Lazear, H. M., Gorman, M. J., Lemke, G., Klein, R. S., & Diamond, M. S. (2015) · Nature Medicine · doi:10.1038/nm.3974 · Cited by 152 · see citing works
Fung, K. Y., Wang, C., Nyegaard, S., Heit, B., Fairn, G. D., & Lee, W. L. (2017) · Frontiers in Physiology · doi:10.3389/fphys.2017.00841 · Cited by 129 · see citing works
Chronic inflammation in multiple sclerosis - seeing what was always there
Matthews, P. M. (2019) · Nature Reviews Neurology · doi:10.1038/s41582-019-0240-y · Cited by 128 · see citing works
Aβ peptide immunization restores blood‐brain barrier integrity in Alzheimer disease
Dickstein, D. L., Biron, K. E., Ujiie, M., Pfeifer, C. G., Jeffries, A. R., & Jefferies, W. A. (2006) · The FASEB Journal · doi:10.1096/fj.05-3956com · Cited by 111 · see citing works
McCarty, D. M., DiRosario, J., Gulaid, K., Muenzer, J., & Fu, H. (2009) · Gene Therapy · doi:10.1038/gt.2009.85 · Cited by 105 · see citing works
Flagged first, then by citations
Research works printed but not linked: 286
- [2]L. Stern, R. Gautier, Arch. Int. Physiol. 1921, 17, 138.
- [3]P. A. Stewart, M. J. Wiley, Dev Biol 1981, 84, 183. 7250491
- [4]C. Iadecola, Neuron 2017, 96, 17. 28957666 PMC5657612
- [5]C. F. Cho, J. M. Wolfe, C. M. Fadzen, D. Calligaris, K. Hornburg, E. A. Chiocca, N. Y. R. Agar, B. L. Pentelute, S. E. Lawler, Nat. Commun. 2017, 8, 15623. 28585535 PMC5467173
- [6]E. S. Lippmann, S. M. Azarin, J. E. Kay, R. A. Nessler, H. K. Wilson, A. Al‐Ahmad, S. P. Palecek, E. V. Shusta, Nat. Biotechnol. 2012, 30, 783. 22729031 PMC3467331
- [7]A. Herland, A. D. van der Meer, E. A. FitzGerald, T. E. Park, J. J. Sleeboom, D. E. Ingber, PLoS One 2016, 11, e0150360. 26930059 PMC4773137
- [8]A. Ben‐Zvi, B. Lacoste, E. Kur, B. J. Andreone, Y. Mayshar, H. Yan, C. Gu, Nature 2014, 509, 507. 24828040 PMC4134871
- [9]M. Demeule, N. Beaudet, A. Regina, E. Besserer‐Offroy, A. Murza, P. Tetreault, K. Belleville, C. Che, A. Larocque, C. Thiot, R. Beliveau, J. M. Longpre, E. Marsault, R. Leduc, J. E. Lachowicz, S. L. Gonias, J. P. Castaigne, P. Sarret, J. Clin. Invest. 2014, 124, 1199. 24531547 PMC3934173
- [10]J. Niewoehner, B. Bohrmann, L. Collin, E. Urich, H. Sade, P. Maier, P. Rueger, J. O. Stracke, W. Lau, A. C. Tissot, H. Loetscher, A. Ghosh, P. O. Freskgard, Neuron 2014, 81, 49. 24411731
- [11]M. Vanlandewijck, L. He, M. A. Mae, J. Andrae, K. Ando, F. Del Gaudio, K. Nahar, T. Lebouvier, B. Lavina, L. Gouveia, Y. Sun, E. Raschperger, M. Rasanen, Y. Zarb, N. Mochizuki, A. Keller, U. Lendahl, C. Betsholtz, Nature 2018, 554, 475. 29443965
- [12]R. N. Munji, A. L. Soung, G. A. Weiner, F. Sohet, B. D. Semple, A. Trivedi, K. Gimlin, M. Kotoda, M. Korai, S. Aydin, A. Batugal, A. C. Cabangcala, P. G. Schupp, M. C. Oldham, T. Hashimoto, L. J. Noble‐Haeusslein, R. Daneman, Nat. Neurosci. 2019, 22, 1892. 31611708 PMC6858546
- [13]T. S. Reese, M. J. Karnovsky, J. Cell Biol. 1967, 34, 207. 6033532 PMC2107213
- [14]N. M. O'Brown, S. J. Pfau, C. Gu, Genes Dev. 2018, 32, 466. 29692355 PMC5959231
- [15]B. J. Andreone, B. W. Chow, A. Tata, B. Lacoste, A. Ben‐Zvi, K. Bullock, A. A. Deik, D. D. Ginty, C. B. Clish, C. Gu, Neuron 2017, 94, 581. 28416077 PMC5474951
- [16]N. M. O'Brown, S. G. Megason, C. Gu, eLife 2019, 8, e47326. 31429822 PMC6726461
- [17]K. A. Dudek, L. Dion‐Albert, M. Lebel, K. LeClair, S. Labrecque, E. Tuck, C. Ferrer Perez, S. A. Golden, C. Tamminga, G. Turecki, N. Mechawar, S. J. Russo, C. Menard, Proc. Natl. Acad. Sci. U. S. A. 2020, 117, 3326. 31974313 PMC7022213
- [18]M. D. Sweeney, K. Kisler, A. Montagne, A. W. Toga, B. V. Zlokovic, Nat. Neurosci. 2018, 21, 1318. 30250261 PMC6198802
- [19]Y. Yang, G. A. Rosenberg, Stroke 2011, 42, 3323. 21940972 PMC3584169
- [20]C. D. Arvanitis, G. B. Ferraro, R. K. Jain, Nat. Rev. Cancer 2020, 20, 26. 31601988 PMC8246629
- [21]C. Menard, M. L. Pfau, G. E. Hodes, V. Kana, V. X. Wang, S. Bouchard, A. Takahashi, M. E. Flanigan, H. Aleyasin, K. B. LeClair, W. G. Janssen, B. Labonte, E. M. Parise, Z. S. Lorsch, S. A. Golden, M. Heshmati, C. Tamminga, G. Turecki, M. Campbell, Z. A. Fayad, C. Y. Tang, M. Merad, S. J. Russo, Nat. Neurosci. 2017, 20, 1752. 29184215 PMC5726568
- [22]A. Q. Chen, Z. Fang, X. L. Chen, S. Yang, Y. F. Zhou, L. Mao, Y. P. Xia, H. J. Jin, Y. N. Li, M. F. You, X. X. Wang, H. Lei, Q. W. He, B. Hu, Cell Death Dis. 2019, 10, 487. 31221990 PMC6586814
- [23]M. D. Sweeney, A. Montagne, A. P. Sagare, D. A. Nation, L. S. Schneider, H. C. Chui, M. G. Harrington, J. Pa, M. Law, D. J. J. Wang, R. E. Jacobs, F. N. Doubal, J. Ramirez, S. E. Black, M. Nedergaard, H. Benveniste, M. Dichgans, C. Iadecola, S. Love, P. M. Bath, H. S. Markus, R. A. Salman, S. M. Allan, T. J. Quinn, R. N. Kalaria, D. J. Werring, R. O. Carare, R. M. Touyz, S. C. R. Williams, M. A. Moskowitz, Z. S. Katusic, S. E. Lutz, O. Lazarov, R. D. Minshall, J. Rehman, et al., Alzheimers Dement. 2019, 15, 158.30642436
- [24]A. Montagne, S. R. Barnes, M. D. Sweeney, M. R. Halliday, A. P. Sagare, Z. Zhao, A. W. Toga, R. E. Jacobs, C. Y. Liu, L. Amezcua, M. G. Harrington, H. C. Chui, M. Law, B. V. Zlokovic, Neuron 2015, 85, 296. 25611508 PMC4350773
- [25]H. Hu, E. A. Hone, E. A. P. Provencher, S. A. Sprowls, I. Farooqi, D. R. Corbin, S. N. Sarkar, J. M. Hollander, P. R. Lockman, J. W. Simpkins, X. Ren, Sci. Rep. 2020, 10, 3233. 32094435 PMC7040038
- [26]D. L. Dickstein, K. E. Biron, M. Ujiie, C. G. Pfeifer, A. R. Jeffries, W. A. Jefferies, FASEB J. 2006, 20, 426. 16507760
- [27]L. Buttler, M. T. Jordao, M. G. Fragas, A. Ruggeri, A. Ceroni, L. C. Michelini, Front. Physiol. 2017, 8, 1048. 29311978 PMC5733101
- [28]J. J. Miner, B. P. Daniels, B. Shrestha, J. L. Proenca‐Modena, E. D. Lew, H. M. Lazear, M. J. Gorman, G. Lemke, R. S. Klein, M. S. Diamond, Nat. Med. 2015, 21, 1464. 26523970 PMC4674389
- [29]R. Cecchelli, V. Berezowski, S. Lundquist, M. Culot, M. Renftel, M. P. Dehouck, L. Fenart, Nat. Rev. Drug Discovery 2007, 6, 650. 17667956
- [30]Z. Cheng, J. Zhang, H. Liu, Y. Li, Y. Zhao, E. Yang, Drug Metab. Dispos. 2010, 38, 1355. 20427691
- [31]J. N. Sarkaria, L. S. Hu, I. F. Parney, D. H. Pafundi, D. H. Brinkmann, N. N. Laack, C. Giannini, T. C. Burns, S. H. Kizilbash, J. K. Laramy, K. R. Swanson, T. J. Kaufmann, P. D. Brown, N. Y. R. Agar, E. Galanis, J. C. Buckner, W. F. Elmquist, Neuro‐Oncology 2018, 20, 184. 29016900 PMC5777482
- [32]S. Sindhwani, A. M. Syed, J. Ngai, B. R. Kingston, L. Maiorino, J. Rothschild, P. MacMillan, Y. Zhang, N. U. Rajesh, T. Hoang, J. L. Y. Wu, S. Wilhelm, A. Zilman, S. Gadde, A. Sulaiman, B. Ouyang, Z. Lin, L. Wang, M. Egeblad, W. C. W. Chan, Nat. Mater. 2020, 19, 566. 31932672
- [33]A. Abrahao, Y. Meng, M. Llinas, Y. Huang, C. Hamani, T. Mainprize, I. Aubert, C. Heyn, S. E. Black, K. Hynynen, N. Lipsman, L. Zinman, Nat. Commun. 2019, 10, 4373. 31558719 PMC6763482
- [34]P. W. Janowicz, G. Leinenga, J. Gotz, R. M. Nisbet, Sci. Rep. 2019, 9, 9255. 31239479 PMC6592925
- [35]D. J. Lundy, K. J. Lee, I. C. Peng, C. H. Hsu, J. H. Lin, K. H. Chen, Y. W. Tien, P. C. H. Hsieh, ACS Nano 2019, 13, 97. 30532951
- [36]W. A. Banks, Nat. Rev. Drug Discovery 2016, 15, 275. 26794270
- [37]M. D. Sweeney, S. Ayyadurai, B. V. Zlokovic, Nat. Neurosci. 2016, 19, 771. 27227366 PMC5745011
- [38]N. J. Abbott, L. Ronnback, E. Hansson, Nat. Rev. Neurosci. 2006, 7, 41. 16371949
- [39]R. Cabezas, M. Avila, J. Gonzalez, R. S. El‐Bacha, E. Baez, L. M. Garcia‐Segura, J. C. Jurado Coronel, F. Capani, G. P. Cardona‐Gomez, G. E. Barreto, Front. Cell. Neurosci. 2014, 8, 211. 25136294 PMC4120694
- [40]K. Kierdorf, T. Masuda, M. J. C. Jordao, M. Prinz, Nat. Rev. Neurosci. 2019, 20, 547. 31358892
- [41]M. W. B. T. S. Reese, J. Cell Biol. 1969, 40, 648. 5765759 PMC2107650
- [42]M. F. Sabbagh, J. S. Heng, C. Luo, R. G. Castanon, J. R. Nery, A. Rattner, L. A. Goff, J. R. Ecker, J. Nathans, eLife. 2018, 7, e36187. 30188322 PMC6126923
- [43]D. Paul, A. E. Cowan, S. Ge, J. S. Pachter, Microvasc. Res. 2013, 86, 1. 23261753 PMC3570614
- [44]C. Greene, N. Hanley, M. Campbell, Fluids Barriers CNS 2019, 16, 3. 30691500 PMC6350359
- [45]P. Berndt, L. Winkler, J. Cording, O. Breitkreuz‐Korff, A. Rex, S. Dithmer, V. Rausch, R. Blasig, M. Richter, A. Sporbert, H. Wolburg, I. E. Blasig, R. F. Haseloff, Cell. Mol. Life Sci. 2019, 76, 1987. 30734065 PMC11105330
- [46]S. Tietz, B. Engelhardt, J. Cell Biol. 2015, 209, 493. 26008742 PMC4442813
- [47]D. Feng, J. A. Nagy, K. Pyne, H. F. Dvorak, A. M. Dvorak, J. Histochem. Cytochem. 2004, 52, 87. 14688220
- [48]Y. Wallez, P. Huber, Biochim. Biophys. Acta 2008, 1778, 794. 17961505
- [49]M. G. Lampugnani, Cold Spring Harbor Perspect. Med. 2012, 2, a006528. PMC3475402 23028127
- [50]G. Bazzoni, E. Dejana, Physiol. Rev. 2004, 84, 869. 15269339
- [51]A. Taddei, C. Giampietro, A. Conti, F. Orsenigo, F. Breviario, V. Pirazzoli, M. Potente, C. Daly, S. Dimmeler, E. Dejana, Nat. Cell Biol. 2008, 10, 923. 18604199
- [52]W. A. Banks, BMC Neurol. 2009, 9, S3. 19534732 PMC2697631
- [53]A. Hoffmann, T. Dege, R. Kunze, A. S. Ernst, H. Lorenz, L. I. Bohler, T. Korff, H. H. Marti, S. Heiland, M. Bendszus, X. Helluy, M. Pham, Stroke 2018, 49, 1479. 29760276
- [54]D. Knowland, A. Arac, K. J. Sekiguchi, M. Hsu, S. E. Lutz, J. Perrino, G. K. Steinberg, B. A. Barres, A. Nimmerjahn, D. Agalliu, Neuron 2014, 82, 603. 24746419 PMC4016169
- [55]N. Bien‐Ly, Y. J. Yu, D. Bumbaca, J. Elstrott, C. A. Boswell, Y. Zhang, W. Luk, Y. Lu, M. S. Dennis, R. M. Weimer, I. Chung, R. J. Watts, J. Exp. Med. 2014, 211, 233. 24470444 PMC3920563
- [56]M. A. Erickson, K. Dohi, W. A. Banks, NeuroImmunoModulation 2012, 19, 121. 22248728 PMC3707010
- [57]H. Wolburg, K. Wolburg‐Buchholz, B. Engelhardt, Acta Neuropathol. 2005, 109, 181. 15549331
- [58]D. L. Kenney‐Jung, A. Vezzani, R. J. Kahoud, R. G. LaFrance‐Corey, M. L. Ho, T. W. Muskardin, E. C. Wirrell, C. L. Howe, E. T. Payne, Ann. Neurol. 2016, 80, 939. 27770579 PMC5225882
- [59]W. Lu, Curr. Pharm. Biotechnol. 2012, 13, 2340. 23016640
- [60]B. Oller‐Salvia, M. Sanchez‐Navarro, E. Giralt, M. Teixido, Chem. Soc. Rev. 2016, 45, 4690. 27188322
- [61]M. Demeule, J. Poirier, J. Jodoin, Y. Bertrand, R. R. Desrosiers, C. Dagenais, T. Nguyen, J. Lanthier, R. Gabathuler, M. Kennard, W. A. Jefferies, D. Karkan, S. Tsai, L. Fenart, R. Cecchelli, R. Beliveau, J. Neurochem. 2002, 83, 924. 12421365
- [62]L. Huang, K. L. Chambliss, X. Gao, I. S. Yuhanna, E. Behling‐Kelly, S. Bergaya, M. Ahmed, P. Michaely, K. Luby‐Phelps, A. Darehshouri, L. Xu, E. A. Fisher, W. P. Ge, C. Mineo, P. W. Shaul, Nature 2019, 569, 565. 31019307 PMC6631346
- [63]K. Y. Fung, C. Wang, S. Nyegaard, B. Heit, G. D. Fairn, W. L. Lee, Front. Physiol. 2017, 8, 841. 29163190 PMC5670330
- [64]L. N. Nguyen, D. Ma, G. Shui, P. Wong, A. Cazenave‐Gassiot, X. Zhang, M. R. Wenk, E. L. Goh, D. L. Silver, Nature 2014, 509, 503. 24828044
- [65]J. P. Hindley, E. Jones, K. Smart, H. Bridgeman, S. N. Lauder, B. Ondondo, S. Cutting, K. Ladell, K. K. Wynn, D. Withers, D. A. Price, A. Ager, A. J. Godkin, A. M. Gallimore, Cancer Res. 2012, 72, 5473. 22962270 PMC3491872
- [66]M. Kaksonen, A. Roux, Nat. Rev. Mol. Cell Biol. 2018, 19, 313. 29410531
- [67]S. E. Lutz, J. R. Smith, D. H. Kim, C. V. L. Olson, K. Ellefsen, J. M. Bates, S. P. Gandhi, D. Agalliu, Cell Rep. 2017, 21, 2104. 29166603 PMC5728697
- [68]S. Ayloo, C. Gu, Curr. Opin. Neurobiol. 2019, 57, 32. 30708291 PMC6629499
- [69]H. N. Yassine, Q. Feng, J. Chiang, L. M. Petrosspour, A. N. Fonteh, H. C. Chui, M. G. Harrington, J. Am. Heart Assoc. 2016, 5, e002886. 26873692 PMC4802440
- [70]S. E. Storck, S. Meister, J. Nahrath, J. N. Meissner, N. Schubert, A. Di Spiezio, S. Baches, R. E. Vandenbroucke, Y. Bouter, I. Prikulis, C. Korth, S. Weggen, A. Heimann, M. Schwaninger, T. A. Bayer, C. U. Pietrzik, J. Clin. Invest. 2016, 126, 123. 26619118 PMC4701557
- [71]H. Qosa, D. S. Miller, P. Pasinelli, D. Trotti, Brain Res. 2015, 1628, 298. 26187753 PMC4681613
- [72]A. Noack, B. Gericke, M. von Kockritz‐Blickwede, A. Menze, S. Noack, I. Gerhauser, F. Osten, H. Y. Naim, W. Loscher, Proc. Natl. Acad. Sci. U. S. A. 2018, 115, E9590. 30254169 PMC6187170
- [73]N. Strazielle, J. F. Ghersi‐Egea, Front. Neurosci. 2015, 9, 21. 25698917 PMC4318338
- [74]M. D. Sweeney, A. P. Sagare, B. V. Zlokovic, Nat. Rev. Neurol. 2018, 14, 133. 29377008 PMC5829048
- [75]D. Shlosberg, M. Benifla, D. Kaufer, A. Friedman, Nat. Rev. Neurol. 2010, 6, 393. 20551947 PMC3625732
- [76]C. P. Profaci, R. N. Munji, R. S. Pulido, R. Daneman, J. Exp. Med. 2020, 217, e20190062. 32211826 PMC7144528
- [77]M. T. Mohammadi, G. A. Dehghani, Pathol., Res. Pract. 2014, 210, 985. 24996562
- [78]F. Shimizu, K. L. Schaller, G. P. Owens, A. C. Cotleur, D. Kellner, Y. Takeshita, B. Obermeier, T. J. Kryzer, Y. Sano, T. Kanda, V. A. Lennon, R. M. Ransohoff, J. L. Bennett, Sci. Transl. Med. 2017, 9, 397. PMC5585784 28679661
- [79]J. Keaney, D. M. Walsh, T. O'Malley, N. Hudson, D. E. Crosbie, T. Loftus, F. Sheehan, J. McDaid, M. M. Humphries, J. J. Callanan, F. M. Brett, M. A. Farrell, P. Humphries, M. Campbell, Sci. Adv. 2015, 1, e1500472. 26491725 PMC4610013
- [80]D. A. Nation, M. D. Sweeney, A. Montagne, A. P. Sagare, L. M. D'Orazio, M. Pachicano, F. Sepehrband, A. R. Nelson, D. P. Buennagel, M. G. Harrington, T. L. S. Benzinger, A. M. Fagan, J. M. Ringman, L. S. Schneider, J. C. Morris, H. C. Chui, M. Law, A. W. Toga, B. V. Zlokovic, Nat. Med. 2019, 25, 270. 30643288 PMC6367058
- [81]H. J. van de Haar, S. Burgmans, J. F. Jansen, M. J. van Osch, M. A. van Buchem, M. Muller, P. A. Hofman, F. R. Verhey, W. H. Backes, Radiology 2016, 281, 527. 27243267
- [82]A. Montagne, D. A. Nation, A. P. Sagare, G. Barisano, M. D. Sweeney, A. Chakhoyan, M. Pachicano, E. Joe, A. R. Nelson, L. M. D'Orazio, D. P. Buennagel, M. G. Harrington, T. L. S. Benzinger, A. M. Fagan, J. M. Ringman, L. S. Schneider, J. C. Morris, E. M. Reiman, R. J. Caselli, H. C. Chui, J. Tcw, Y. Chen, J. Pa, P. S. Conti, M. Law, A. W. Toga, B. V. Zlokovic, Nature 2020, 581, 71. 32376954 PMC7250000
- [83]M. Merlini, V. A. Rafalski, P. E. Rios Coronado, T. M. Gill, M. Ellisman, G. Muthukumar, K. S. Subramanian, J. K. Ryu, C. A. Syme, D. Davalos, W. W. Seeley, L. Mucke, R. B. Nelson, K. Akassoglou, Neuron 2019, 101, 1099. 30737131 PMC6602536
- [84]S. Y. Kim, M. Buckwalter, H. Soreq, A. Vezzani, D. Kaufer, Epilepsia 2012, 53, 37. 23134494 PMC3703535
- [85]R. Brauer, M. Herrero‐Zazo, D. J. Barlow, F. Gaughran, D. Taylor, L. M. Howard, J. Psychopharmacol. 2019, 33, 466. 30696331
- [86]H. Babbe, A. Roers, A. Waisman, H. Lassmann, N. Goebels, R. Hohlfeld, M. Friese, R. Schroder, M. Deckert, S. Schmidt, R. Ravid, K. Rajewsky, J. Exp. Med. 2000, 192, 393. 10934227 PMC2193223
- [87]C. L. Willis, R. B. Camire, S. A. Brule, D. E. Ray, Neuroscience 2013, 250, 773. 23845748 PMC4002262
- [88]B. K. Wacker, A. B. Freie, J. L. Perfater, J. M. Gidday, J. Cereb. Blood Flow Metab. 2012, 32, 1014. 22314269 PMC3367228
- [89]Y. Zhao, K. K. Ting, J. Li, V. C. Cogger, J. Chen, A. Johansson‐Percival, S. F. Ngiow, J. Holst, G. Grau, S. Goel, T. Muller, E. Dejana, G. McCaughan, M. J. Smyth, R. Ganss, M. A. Vadas, J. R. Gamble, Cancer Res. 2017, 77, 4434. 28655790
- [90]R. O. Smith, T. Ninchoji, E. Gordon, H. Andre, E. Dejana, D. Vestweber, A. Kvanta, L. Claesson‐Welsh, eLife 2020, 9, e54056. 32312382 PMC7188482
- [91]K. K. Ting, Y. Zhao, W. Shen, P. Coleman, M. Yam, T. Chan‐Ling, J. Li, T. Moller, M. Gillies, M. A. Vadas, J. R. Gamble, Diabetologia 2019, 62, 322. 30443753
- [92]J. Li, Y. Zhao, J. Choi, K. K. Ting, P. Coleman, J. Chen, V. C. Cogger, L. Wan, Z. Shi, T. Moller, X. Zheng, M. A. Vadas, J. R. Gamble, PLoS Biol. 2020, 18, e3000734. 32502201 PMC7299406
- [93]J. A. Young, K. K. Ting, J. Li, T. Moller, L. Dunn, Y. Lu, J. Moses, L. Prado‐Lourenco, L. M. Khachigian, M. Ng, P. A. Gregory, G. J. Goodall, A. Tsykin, I. Lichtenstein, C. N. Hahn, N. Tran, N. Shackel, J. G. Kench, G. McCaughan, M. A. Vadas, J. R. Gamble, Blood 2013, 122, 2911. 24009229
- [94]K. Hubner, P. Cabochette, R. Dieguez‐Hurtado, C. Wiesner, Y. Wakayama, K. S. Grassme, M. Hubert, S. Guenther, H. G. Belting, M. Affolter, R. H. Adams, B. Vanhollebeke, W. Herzog, Nat. Commun. 2018, 9, 4860. 30451830 PMC6242933
- [95]L. Maddaluno, N. Rudini, R. Cuttano, L. Bravi, C. Giampietro, M. Corada, L. Ferrarini, F. Orsenigo, E. Papa, G. Boulday, E. Tournier‐Lasserve, F. Chapon, C. Richichi, S. F. Retta, M. G. Lampugnani, E. Dejana, Nature 2013, 498, 492. 23748444
- [96]M. Mathiesen Janiurek, R. Soylu‐Kucharz, C. Christoffersen, K. Kucharz, M. Lauritzen, eLife 2019, 8, e49405. 31763978 PMC6877292
- [97]K. Yanagida, C. H. Liu, G. Faraco, S. Galvani, H. K. Smith, N. Burg, J. Anrather, T. Sanchez, C. Iadecola, T. Hla, Proc. Natl. Acad. Sci. U. S. A. 2017, 114, 4531. 28396408 PMC5410849
- [98]Z. Wang, K. Higashikawa, H. Yasui, Y. Kuge, Y. Ohno, A. Kihara, Y. A. Midori, K. Houkin, M. Kawabori, Transl. Stroke Res. 2020, 11, 1103. 32103462 PMC7496052
- [99]V. Brinkmann, A. Billich, T. Baumruker, P. Heining, R. Schmouder, G. Francis, S. Aradhye, P. Burtin, Nat. Rev. Drug Discovery 2010, 9, 883. 21031003
- [100]F. Ma, P. Sun, X. Zhang, M. H. Hamblin, K. J. Yin, Sci. Signaling 2020, 13, eaay5686. PMC7173187 32265338
- [101]K. Toyama, J. M. Spin, A. C. Deng, T. T. Huang, K. Wei, M. U. Wagenhauser, T. Yoshino, H. Nguyen, J. Mulorz, S. Kundu, U. Raaz, M. Adam, I. N. Schellinger, A. Jagger, P. S. Tsao, Arterioscler., Thromb., Vasc. Biol. 2018, 38, 1392. 29650692
- [102]B. Dalile, L. Van Oudenhove, B. Vervliet, K. Verbeke, Nat. Rev. Gastroenterol. Hepatol. 2019, 16, 461. 31123355
- [103]B. P. Daniels, D. W. Holman, L. Cruz‐Orengo, H. Jujjavarapu, D. M. Durrant, R. S. Klein, mBio 2014, 5, e01476. 25161189 PMC4173776
- [104]B. Bauer, A. M. Hartz, G. Fricker, D. S. Miller, Mol. Pharmacol. 2004, 66, 413. 15322232
- [105]M. Krohn, C. Lange, J. Hofrichter, K. Scheffler, J. Stenzel, J. Steffen, T. Schumacher, T. Bruning, A. S. Plath, F. Alfen, A. Schmidt, F. Winter, K. Rateitschak, A. Wree, J. Gsponer, L. C. Walker, J. Pahnke, J. Clin. Invest. 2011, 121, 3924. 21881209 PMC3195473
- [106]C. Moessinger, I. Nilsson, L. Muhl, M. Zeitelhofer, B. Heller Sahlgren, J. Skogsberg, U. Eriksson, EMBO Rep. 2020, 21, e49343. 32449307 PMC7332976
- [107]S. Debette, C. A. Ibrahim Verbaas, J. Bressler, M. Schuur, A. Smith, J. C. Bis, G. Davies, C. Wolf, V. Gudnason, L. B. Chibnik, Q. Yang, A. L. deStefano, D. J. de Quervain, V. Srikanth, J. Lahti, H. J. Grabe, J. A. Smith, L. Priebe, L. Yu, N. Karbalai, C. Hayward, J. F. Wilson, H. Campbell, K. Petrovic, M. Fornage, G. Chauhan, R. Yeo, R. Boxall, J. Becker, O. Stegle, K. A. Mather, V. Chouraki, Q. Sun, L. M. Rose, S. Resnick, et al., Biol. Psychiatry 2015, 77, 749. 25648963 PMC4513651
- [108]C. Chakraborty, A. R. Sharma, G. Sharma, M. Bhattacharya, S. S. Lee, Mol. Ther.–Nucleic Acids 2020, 19, 933. 32004864 PMC6994820
- [109]M. M. Mihaylova, D. S. Vasquez, K. Ravnskjaer, P. D. Denechaud, R. T. Yu, J. G. Alvarez, M. Downes, R. M. Evans, M. Montminy, R. J. Shaw, Cell 2011, 145, 607. 21565617 PMC3117637
- [110]F. Roudnicky, B. K. Kim, Y. Lan, R. Schmucki, V. Kuppers, K. Christensen, M. Graf, C. Patsch, M. Burcin, C. A. Meyer, P. D. Westenskow, C. A. Cowan, Sci. Rep. 2020, 10, 3886. 32127614 PMC7054428
- [111]R. D. Fontijn, O. L. Volger, J. O. Fledderus, A. Reijerkerk, H. E. de Vries, A. J. Horrevoets, Am. J. Physiol.: Heart Circ. Physiol. 2008, 294, H891. 18065521
- [112]Y. Yamazaki, M. Shinohara, M. Shinohara, A. Yamazaki, M. E. Murray, A. M. Liesinger, M. G. Heckman, E. R. Lesser, J. E. Parisi, R. C. Petersen, D. W. Dickson, T. Kanekiyo, G. Bu, Brain 2019, 142, 1077. 30770921 PMC6439325
- [113]B. V. Zlokovic, Nat. Rev. Neurosci. 2011, 12, 723. 22048062 PMC4036520
- [114]T. Nitta, M. Hata, S. Gotoh, Y. Seo, H. Sasaki, N. Hashimoto, M. Furuse, S. Tsukita, J. Cell Biol. 2003, 161, 653. 12743111 PMC2172943
- [115]V. Braniste, M. Al‐Asmakh, C. Kowal, F. Anuar, A. Abbaspour, M. Toth, A. Korecka, N. Bakocevic, L. G. Ng, P. Kundu, B. Gulyas, C. Halldin, K. Hultenby, H. Nilsson, H. Hebert, B. T. Volpe, B. Diamond, S. Pettersson, Sci. Transl. Med. 2014, 6, 263ra158. PMC4396848 25411471
- [116]S. Gerhardt, M. H. Mohajeri, Nutrients 2018, 10, 708. PMC6024871 29857583
- [117]L. Zhang, Y. Wang, X. Xiayu, C. Shi, W. Chen, N. Song, X. Fu, R. Zhou, Y. F. Xu, L. Huang, H. Zhu, Y. Han, C. Qin, J. Alzheimer's Dis. 2017, 60, 1241. 29036812
- [118]G. Sharon, N. J. Cruz, D. W. Kang, M. J. Gandal, B. Wang, Y. M. Kim, E. M. Zink, C. P. Casey, B. C. Taylor, C. J. Lane, L. M. Bramer, N. G. Isern, D. W. Hoyt, C. Noecker, M. J. Sweredoski, A. Moradian, E. Borenstein, J. K. Jansson, R. Knight, T. O. Metz, C. Lois, D. H. Geschwind, R. Krajmalnik‐Brown, S. K. Mazmanian, Cell 2019, 177, 1600. 31150625 PMC6993574
- [119]E. G. Severance, R. H. Yolken, W. W. Eaton, Schizophr. Res. 2016, 176, 23. 25034760 PMC4294997
- [120]A. T. Tang, J. P. Choi, J. J. Kotzin, Y. Yang, C. C. Hong, N. Hobson, R. Girard, H. A. Zeineddine, R. Lightle, T. Moore, Y. Cao, R. Shenkar, M. Chen, P. Mericko, J. Yang, L. Li, C. Tanes, D. Kobuley, U. Vosa, K. J. Whitehead, D. Y. Li, L. Franke, B. Hart, M. Schwaninger, J. Henao‐Mejia, L. Morrison, H. Kim, I. A. Awad, X. Zheng, M. L. Kahn, Nature 2017, 545, 305. 28489816 PMC5757866
- [121]K. M. Maslowski, A. T. Vieira, A. Ng, J. Kranich, F. Sierro, D. Yu, H. C. Schilter, M. S. Rolph, F. Mackay, D. Artis, R. J. Xavier, M. M. Teixeira, C. R. Mackay, Nature 2009, 461, 1282. 19865172 PMC3256734
- [122]L. B. Jaeger, S. Dohgu, M. C. Hwang, S. A. Farr, M. P. Murphy, M. A. Fleegal‐DeMotta, J. L. Lynch, S. M. Robinson, M. L. Niehoff, S. N. Johnson, V. B. Kumar, W. A. Banks, J. Alzheimer's Dis. 2009, 17, 553. 19433890 PMC2802833
- [123]D. E. Kang, C. U. Pietrzik, L. Baum, N. Chevallier, D. E. Merriam, M. Z. Kounnas, S. L. Wagner, J. C. Troncoso, C. H. Kawas, R. Katzman, E. H. Koo, J. Clin. Invest. 2000, 106, 1159. 11067868 PMC301422
- [124]E. A. Winkler, Y. Nishida, A. P. Sagare, S. V. Rege, R. D. Bell, D. Perlmutter, J. D. Sengillo, S. Hillman, P. Kong, A. R. Nelson, J. S. Sullivan, Z. Zhao, H. J. Meiselman, R. B. Wendy, J. Soto, E. D. Abel, J. Makshanoff, E. Zuniga, D. C. De Vivo, B. V. Zlokovic, Nat. Neurosci. 2015, 18, 521. 25730668 PMC4734893
- [125]A. D. Mooradian, H. C. Chung, G. N. Shah, Neurobio. Aging 1997, 18, 469. 9390772
- [126]M. Coureuil, H. Lecuyer, S. Bourdoulous, X. Nassif, Nat. Rev. Microbiol. 2017, 15, 149. 28090076
- [127]H. Salimi, M. D. Cain, X. Jiang, R. A. Roth, W. L. Beatty, C. Sun, W. B. Klimstra, J. Hou, R. S. Klein, mBio 2020, 11, e02731. 32047126 PMC7018649
- [128]A. J. Ridley, Trends Cell Biol. 2006, 16, 522. 16949823
- [129]S. M. Armstrong, V. Khajoee, C. Wang, T. Wang, J. Tigdi, J. Yin, W. M. Kuebler, M. Gillrie, S. P. Davis, M. Ho, W. L. Lee, Am J Pathol 2012, 180, 1308. 22203054
- [130]S. Tiwary, J. E. Morales, S. C. Kwiatkowski, F. F. Lang, G. Rao, J. H. McCarty, Sci. Rep. 2018, 8, 8267. 29844613 PMC5974340
- [131]S. E. Wahrle, H. Jiang, M. Parsadanian, J. Kim, A. Li, A. Knoten, S. Jain, V. Hirsch‐Reinshagen, C. L. Wellington, K. R. Bales, S. M. Paul, D. M. Holtzman, J. Clin. Invest. 2008, 118, 671. 18202749 PMC2200302
- [132]A. H. Abuznait, A. Kaddoumi, ACS Chem. Neurosci. 2012, 3, 820. 23181169 PMC3504479
- [133]K. G. Mawuenyega, W. Sigurdson, V. Ovod, L. Munsell, T. Kasten, J. C. Morris, K. E. Yarasheski, R. J. Bateman, Science 2010, 330, 1774. 21148344 PMC3073454
- [134]J. R. Cirrito, R. Deane, A. M. Fagan, M. L. Spinner, M. Parsadanian, M. B. Finn, H. Jiang, J. L. Prior, A. Sagare, K. R. Bales, S. M. Paul, B. V. Zlokovic, D. Piwnica‐Worms, D. M. Holtzman, J. Clin. Invest. 2005, 115, 3285. 16239972 PMC1257538
- [135]S. Vogelgesang, I. Cascorbi, E. Schroeder, J. Pahnke, H. K. Kroemer, W. Siegmund, C. Kunert‐Keil, L. C. Walker, R. W. Warzok, Pharmacogenet. Genomics 2002, 12, 535. 12360104
- [136]D. M. van Assema, M. Lubberink, M. Bauer, W. M. van der Flier, R. C. Schuit, A. D. Windhorst, E. F. Comans, N. J. Hoetjes, N. Tolboom, O. Langer, M. Muller, P. Scheltens, A. A. Lammertsma, B. N. van Berckel, Brain 2012, 135, 181. 22120145
- [137]A. M. Hartz, D. S. Miller, B. Bauer, Mol. Pharmacol. 2010, 77, 715. 20101004 PMC2872973
- [138]V. Zoufal, T. Wanek, M. Krohn, S. Mairinger, T. Filip, M. Sauberer, J. Stanek, T. Pekar, M. Bauer, J. Pahnke, O. Langer, J. Cereb. Blood Flow Metab. 2020, 40, 150. 30354871 PMC6928546
- [139]E. A. Neuwelt, D. L. Goldman, S. A. Dahlborg, J. Crossen, F. Ramsey, S. Roman‐Goldstein, R. Braziel, B. Dana, J. Clin. Oncol. 1991, 9, 1580. 1875220
- [140]C. Chu, A. Jablonska, W. G. Lesniak, A. M. Thomas, X. Lan, R. M. Linville, S. Li, P. C. Searson, G. Liu, M. Pearl, M. G. Pomper, M. Janowski, T. Magnus, P. Walczak, J. Controlled Release 2020, 317, 312. 31751635
- [141]D. M. McCarty, J. DiRosario, K. Gulaid, J. Muenzer, H. Fu, Gene Ther. 2009, 16, 1340. 19587708 PMC4289609
- [142]B. Zunkeler, R. E. Carson, J. Olson, R. G. Blasberg, H. DeVroom, R. J. Lutz, S. C. Saris, D. C. Wright, W. Kammerer, N. J. Patronas, R. L. Dedrick, P. Herscovitch, E. H. Oldfield, J. Neurosurg. 1996, 85, 1056. 8929495
- [143]Z. Wang, Y. Zheng, F. Wang, J. Zhong, T. Zhao, Q. Xie, T. Zhu, F. Ma, Q. Tang, B. Zhou, J. Zhu, Sci. Adv. 2020, 6, eaay8627. 32523984 PMC7259944
- [144]R. E. Cannon, J. C. Peart, B. T. Hawkins, C. R. Campos, D. S. Miller, Proc. Natl. Acad. Sci. U. S. A. 2012, 109, 15930. 22949658 PMC3465435
- [145]B. Prager, S. F. Spampinato, R. M. Ransohoff, Trends Mol. Med. 2015, 21, 354. 25939882
- [146]Z. I. Kovacs, S. Kim, N. Jikaria, F. Qureshi, B. Milo, B. K. Lewis, M. Bresler, S. R. Burks, J. A. Frank, Proc. Natl. Acad. Sci. U. S. A. 2017, 114, E75. 27994152 PMC5224365
- [147]A. R. Rezai, M. Ranjan, P. F. D'Haese, M. W. Haut, J. Carpenter, U. Najib, R. I. Mehta, J. L. Chazen, Z. Zibly, J. R. Yates, S. L. Hodder, M. Kaplitt, Proc. Natl. Acad. Sci. U. S. A. 2020, 117, 9180. 32284421 PMC7196825
- [148]S. H. Park, M. J. Kim, H. H. Jung, W. S. Chang, H. S. Choi, I. Rachmilevitch, E. Zadicario, J. W. Chang, J. Neurosurg. 2020, 134, 327. 31899873
- [149]A. K. Deo, S. Borson, J. M. Link, K. Domino, J. F. Eary, B. Ke, T. L. Richards, D. A. Mankoff, S. Minoshima, F. O'Sullivan, S. Eyal, P. Hsiao, K. Maravilla, J. D. Unadkat, J. Nucl. Med. 2014, 55, 1106. 24842892 PMC4691246
- [150]H. Thomas, H. M. Coley, Cancer Control 2003, 10, 159. 12712010
- [151]S. I. Rapoport, Cell. Mol. Neurobiol. 2000, 20, 217. 10696511 PMC11537517
- [152]E. M. Hiesiger, R. M. Voorhies, G. A. Basler, L. E. Lipschutz, J. B. Posner, W. R. Shapiro, Ann. Neurol. 1986, 19, 50. 3080944
- [153]E. A. Neuwelt, J. T. Diehl, L. H. Vu, S. A. Hill, A. J. Michael, E. P. Frenkel, Ann. Intern. Med. 1981, 94, 449. 6782926
- [154]L. Angelov, N. D. Doolittle, D. F. Kraemer, T. Siegal, G. H. Barnett, D. M. Peereboom, G. Stevens, J. McGregor, K. Jahnke, C. A. Lacy, N. A. Hedrick, E. Shalom, S. Ference, S. Bell, L. Sorenson, R. M. Tyson, M. Haluska, E. A. Neuwelt, J. Clin. Oncol. 2009, 27, 3503. 19451444 PMC2717756
- [155]Z. G. Zhang, L. Zhang, Q. Jiang, R. Zhang, K. Davies, C. Powers, N. Bruggen, M. Chopp, J. Clin. Invest. 2000, 106, 829. 11018070 PMC517814
- [156]F. Shimizu, Y. Sano, T. Takahashi, H. Haruki, K. Saito, M. Koga, T. Kanda, J. Neurol., Neurosurg. Psychiatry 2012, 83, 288. 22100760
- [157]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, E. Rafailov, Biomed. Opt. Express 2017, 8, 5040. 29188101 PMC5695951
- [158]D. Y. Zhang, C. Dmello, L. Chen, V. A. Arrieta, E. Gonzalez‐Buendia, J. R. Kane, L. P. Magnusson, A. Baran, C. D. James, C. Horbinski, A. Carpentier, C. Desseaux, M. Canney, M. Muzzio, R. Stupp, A. M. Sonabend, Clin. Cancer Res. 2020, 26, 477. 31831565 PMC7050644
- [159]S. N. Tabatabaei, H. Girouard, A. S. Carret, S. Martel, J. Controlled Release 2015, 206, 49. 25724273
- [160]N. Lipsman, Y. Meng, A. J. Bethune, Y. Huang, B. Lam, M. Masellis, N. Herrmann, C. Heyn, I. Aubert, A. Boutet, G. S. Smith, K. Hynynen, S. E. Black, Nat. Commun. 2018, 9, 2336. 30046032 PMC6060168
- [161]B. P. Mead, N. Kim, G. W. Miller, D. Hodges, P. Mastorakos, A. L. Klibanov, J. W. Mandell, J. Hirsh, J. S. Suk, J. Hanes, R. J. Price, Nano Lett. 2017, 17, 3533. 28511006 PMC5539956
- [162]V. Krishna, F. Sammartino, A. Rezai, JAMA Neurol. 2018, 75, 246. 29228074
- [163]N. M. Smith, I. Gachulincova, D. Ho, C. Bailey, C. A. Bartlett, M. Norret, J. Murphy, A. Buckley, P. J. Rigby, M. J. House, T. St Pierre, M. Fitzgerald, K. S. Iyer, S. A. Dunlop, Sci. Rep. 2016, 6, 22595. 26940762 PMC4778073
- [164]M. R. Jablonski, S. S. Markandaiah, D. Jacob, N. J. Meng, K. Li, V. Gennaro, A. C. Lepore, D. Trotti, P. Pasinelli, Ann. Clin. Transl. Neurol. 2014, 1, 996. 25574474 PMC4284125
- [165]D. G. Kim, M. S. Bynoe, J. Clin. Invest. 2016, 126, 1717. 27043281 PMC4855938
- [166]E. M. Kemper, A. E. van Zandbergen, C. Cleypool, H. A. Mos, W. Boogerd, J. H. Beijnen, O. van Tellingen, Clin. Cancer Res. 2003, 9, 2849. 12855665
- [167]Y. J. Yu, J. K. Atwal, Y. Zhang, R. K. Tong, K. R. Wildsmith, C. Tan, N. Bien‐Ly, M. Hersom, J. A. Maloney, W. J. Meilandt, D. Bumbaca, K. Gadkar, K. Hoyte, W. Luk, Y. Lu, J. A. Ernst, K. Scearce‐Levie, J. A. Couch, M. S. Dennis, R. J. Watts, Sci. Transl. Med. 2014, 6, 261ra154. 25378646
- [168]A. Galstyan, J. L. Markman, E. S. Shatalova, A. Chiechi, A. J. Korman, R. Patil, D. Klymyshyn, W. G. Tourtellotte, L. L. Israel, O. Braubach, V. A. Ljubimov, L. A. Mashouf, A. Ramesh, Z. B. Grodzinski, M. L. Penichet, K. L. Black, E. Holler, T. Sun, H. Ding, A. V. Ljubimov, J. Y. Ljubimova, Nat. Commun. 2019, 10, 3850. 31462642 PMC6713723
- [169]M. Baba, K. Itaka, K. Kondo, T. Yamasoba, K. Kataoka, J. Controlled Release 2015, 201, 41. 25599855
- [170]Y. Zou, X. Sun, Y. Wang, C. Yan, Y. Liu, J. Li, D. Zhang, M. Zheng, R. S. Chung, B. Shi, Adv. Mater. 2020, 2000416. 32374446
- [171]L. P. Wu, D. Ahmadvand, J. Su, A. Hall, X. Tan, Z. S. Farhangrazi, S. M. Moghimi, Nat. Commun. 2019, 10, 4635. 31604928 PMC6789111
- [172]M. Zheng, W. Tao, Y. Zou, O. C. Farokhzad, B. Shi, Trends Biotechnol. 2018, 36, 562. 29422412
- [173]C. P. Lai, X. O. Breakefield, Front. Physiol. 2012, 3, 228. 22754538 PMC3384085
- [174]J. Matsumoto, T. Stewart, L. Sheng, N. Li, K. Bullock, N. Song, M. Shi, W. A. Banks, J. Zhang, Acta Neuropathol. Commun. 2017, 5, 71. 28903781 PMC5598000
- [175]M. Shi, A. Kovac, A. Korff, T. J. Cook, C. Ginghina, K. M. Bullock, L. Yang, T. Stewart, D. Zheng, P. Aro, A. Atik, K. F. Kerr, C. P. Zabetian, E. R. Peskind, S. C. Hu, J. F. Quinn, D. R. Galasko, T. J. Montine, W. A. Banks, J. Zhang, Alzheimers Dement. 2016, 12, 1125. 27234211 PMC5107127
- [176]G. Morad, C. V. Carman, E. J. Hagedorn, J. R. Perlin, L. I. Zon, N. Mustafaoglu, T. E. Park, D. E. Ingber, C. C. Daisy, M. A. Moses, ACS Nano 2019, 13, 13853. 31479239 PMC7169949
- [177]W. A. Banks, P. Sharma, K. M. Bullock, K. M. Hansen, N. Ludwig, T. L. Whiteside, Int. J. Mol. Sci. 2020, 21, 4407. PMC7352415 32575812
- [178]D. Yuan, Y. Zhao, W. A. Banks, K. M. Bullock, M. Haney, E. Batrakova, A. V. Kabanov, Biomaterials 2017, 142, 1. 28715655 PMC5603188
- [179]M. Khongkow, T. Yata, S. Boonrungsiman, U. R. Ruktanonchai, D. Graham, K. Namdee, Sci. Rep. 2019, 9, 8278. 31164665 PMC6547645
- [180]L. Alvarez‐Erviti, Y. Seow, H. Yin, C. Betts, S. Lakhal, M. J. Wood, Nat. Biotechnol. 2011, 29, 341. 21423189
- [181]Z. G. Zhang, B. Buller, M. Chopp, Nat. Rev. Neurol. 2019, 15, 193. 30700824
- [182]X. Ren, Y. Zhao, F. Xue, Y. Zheng, H. Huang, W. Wang, Y. Chang, H. Yang, J. Zhang, Mol. Ther.–Nucleic Acids 2019, 17, 726. 31437653 PMC6709346
- [183]B. Xu, Y. Zhang, X. F. Du, J. Li, H. X. Zi, J. W. Bu, Y. Yan, H. Han, J. L. Du, Cell Res. 2017, 27, 882. 28429770 PMC5518987
- [184]Z. Yang, J. Shi, J. Xie, Y. Wang, J. Sun, T. Liu, Y. Zhao, X. Zhao, X. Wang, Y. Ma, V. Malkoc, C. Chiang, W. Deng, Y. Chen, Y. Fu, K. J. Kwak, Y. Fan, C. Kang, C. Yin, J. Rhee, P. Bertani, J. Otero, W. Lu, K. Yun, A. S. Lee, W. Jiang, L. Teng, B. Y. S. Kim, L. J. Lee, Nat. Biomed. Eng. 2020, 4, 69. 31844155 PMC7080209
- [185]R. Kojima, D. Bojar, G. Rizzi, G. C. Hamri, M. D. El‐Baba, P. Saxena, S. Auslander, K. R. Tan, M. Fussenegger, Nat. Commun. 2018, 9, 1305. 29610454 PMC5880805
- [186]P. Kumar, H. Wu, J. L. McBride, K. E. Jung, M. H. Kim, B. L. Davidson, S. K. Lee, P. Shankar, N. Manjunath, Nature 2007, 448, 39. 17572664
- [187]J. Yang, X. Zhang, X. Chen, L. Wang, G. Yang, Mol. Ther.–Nucleic Acids 2017, 7, 278. 28624203 PMC5415550
- [188]Y. Anraku, H. Kuwahara, Y. Fukusato, A. Mizoguchi, T. Ishii, K. Nitta, Y. Matsumoto, K. Toh, K. Miyata, S. Uchida, K. Nishina, K. Osada, K. Itaka, N. Nishiyama, H. Mizusawa, T. Yamasoba, T. Yokota, K. Kataoka, Nat. Commun. 2017, 8, 1001. 29042554 PMC5645389
- [189]M. Demeule, J. C. Currie, Y. Bertrand, C. Che, T. Nguyen, A. Regina, R. Gabathuler, J. P. Castaigne, R. Beliveau, J. Neurochem. 2008, 106, 1534. 18489712
- [190]Y. J. Zuchero, X. Chen, N. Bien‐Ly, D. Bumbaca, R. K. Tong, X. Gao, S. Zhang, K. Hoyte, W. Luk, M. A. Huntley, L. Phu, C. Tan, D. Kallop, R. M. Weimer, Y. Lu, D. S. Kirkpatrick, J. A. Ernst, B. Chih, M. S. Dennis, R. J. Watts, Neuron 2016, 89, 70. 26687840
- [191]Y. J. Yu, Y. Zhang, M. Kenrick, K. Hoyte, W. Luk, Y. Lu, J. Atwal, J. M. Elliott, S. Prabhu, R. J. Watts, M. S. Dennis, Sci. Transl. Med. 2011, 3, 84ra44. 21613623
- [192]K. B. Johnsen, M. Bak, P. J. Kempen, F. Melander, A. Burkhart, M. S. Thomsen, M. S. Nielsen, T. Moos, T. L. Andresen, Theranostics 2018, 8, 3416. 29930740 PMC6010987
- [193]K. B. Johnsen, M. Bak, F. Melander, M. S. Thomsen, A. Burkhart, P. J. Kempen, T. L. Andresen, T. Moos, J. Controlled Release 2019, 295, 237. 30633947
- [194]H. Guo, R. Wang, D. Wang, S. Wang, J. Zhou, Z. Chai, S. Yao, J. Li, L. Lu, Y. Liu, C. Xie, W. Lu, J. Controlled Release 2020, 320, 63. 31917294
- [195]J. Wen, D. Wu, M. Qin, C. Liu, L. Wang, D. Xu, H. V. Vinters, Y. Liu, E. Kranz, X. Guan, G. Sun, X. Sun, Y. Lee, O. Martinez‐Maza, D. Widney, Y. Lu, I. S. Y. Chen, M. Kamata, Nat. Biomed. Eng. 2019, 3, 706. 31384008 PMC6736720
- [196]J. A. Couch, Y. J. Yu, Y. Zhang, J. M. Tarrant, R. N. Fuji, W. J. Meilandt, H. Solanoy, R. K. Tong, K. Hoyte, W. Luk, Y. Lu, K. Gadkar, S. Prabhu, B. A. Ordonia, Q. Nguyen, Y. Lin, Z. Lin, M. Balazs, K. Scearce‐Levie, J. A. Ernst, M. S. Dennis, R. J. Watts, Sci. Transl. Med. 2013, 5, 183ra57. 23636093
- [197]X. Meng, Y. Zhao, B. Han, C. Zha, Y. Zhang, Z. Li, P. Wu, T. Qi, C. Jiang, Y. Liu, J. Cai, Nat. Commun. 2020, 11, 594. 32001707 PMC6992617
- [198]F. C. Lam, S. W. Morton, J. Wyckoff, T. L. Vu Han, M. K. Hwang, A. Maffa, E. Balkanska‐Sinclair, M. B. Yaffe, S. R. Floyd, P. T. Hammond, Nat. Commun. 2018, 9, 1991. 29777137 PMC5959860
- [199]B. E. Deverman, B. M. Ravina, K. S. Bankiewicz, S. M. Paul, D. W. Y. Sah, Nat. Rev. Drug Discovery 2018, 17, 641. 30093643
- [200]B. E. Deverman, P. L. Pravdo, B. P. Simpson, S. R. Kumar, K. Y. Chan, A. Banerjee, W. L. Wu, B. Yang, N. Huber, S. P. Pasca, V. Gradinaru, Nat. Biotechnol. 2016, 34, 204. 26829320 PMC5088052
- [201]D. Rosenblum, N. Joshi, W. Tao, J. M. Karp, D. Peer, Nat. Commun. 2018, 9, 1410. 29650952 PMC5897557
200 of 286 shown
Cited by
Sorted by citations
Blood–Brain Barrier Breakdown in Alzheimer’s Disease: Mechanisms and Targeted Strategies
Alkhalifa, A. E., Al-Ghraiybah, N. F., Odum, J., Shunnarah, J. G., Austin, N., & Kaddoumi, A. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms242216288 · Cited by 212 · see citing works
Extracellular vesicles as nanotheranostic platforms for targeted neurological disorder interventions
Choi, H. K., Chen, M., Goldston, L. L., & Lee, K.-B. (2024) · Nano Convergence · doi:10.1186/s40580-024-00426-5 · Cited by 26 · see citing works
In Situ Detection of Neuroinflammation Using Multicellular 3D Neurovascular‐Unit‐on‐a‐Chip
Choi, J., Choi, H. K., & Lee, K. (2023) · Advanced Functional Materials · doi:10.1002/adfm.202304382 · Cited by 21 · see citing works
- Authors
- Li, J., Zheng, M., Shimoni, O., Banks, W. A., Bush, A. I., Gamble, J. R., & Shi, B.
- Affiliations
- Henan University (CN)
- University of Technology Sydney (AU)
- University of Washington (US)
- The University of Melbourne (AU)
- The University of Sydney (AU)
- Corresponding author
- Shi, Bingyang
- ORCID
- Venue
- Advanced Science
- Publisher
- Wiley
- Published
- 2021-06-03
- Volume
- 8
- Issue
- 16
- Pages
- e2101090-e2101090
- ISSN
- 2198-3844 (ISSN-L)
- PMC
- PMC8373165
- OpenAlex
- W3165847087
- Cited by
- 202
- References
- 42
- Citations by year
- 2026: 28 · 2025: 54 · 2024: 47 · 2023: 33 · 2022: 31 · 2021: 9
- FWCI
- 3.54
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Advanced Science (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Minerva Access (University of Melbourne) (submittedVersion, cc-by)
- Funders
- National Natural Science Foundation of China (31640027)
- National Health and Medical Research Council (GNT1194825, GNT1166024, GNT1183057)
- NSW Ministry of Health
- Topics
- Life Sciences › Neuroscience › Neurology › Barrier Structure and Function Studies
- Health Sciences › Medicine › Oncology › Drug Transport and Resistance Mechanisms
- Physical Sciences › Materials Science › Biomaterials › Nanoparticle-Based Drug Delivery
- Keywords
- blood-brain barrier, blood-brain barrier disruption, brain drug delivery, neurovascular unit, neurological disorders, cerebrovascular disease
- MeSH terms
- Nanoparticle Drug Delivery System, Animals, Biological Transport, Blood-Brain Barrier, Drug Carriers, Humans, Drug Delivery Systems, Mice
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review