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Blood−brain barrier breakdown and neovascularization processes after stroke and traumatic brain injury
Open accessAbstract
PURPOSE OF REVIEW: Angiogenesis or vascular reorganization plays a role in recovery after stroke and traumatic brain injury (TBI). In this review, we have focused on two major events that occur during stroke and TBI from a vascular perspective - what is the process and time course of blood-brain barrier (BBB) breakdown? and how does the surrounding vasculature recover and facilitate repair? RECENT FINDINGS: Despite differences in the primary injury, the BBB changes overlap between stroke and TBI. Disruption of BBB involves a series of events: formation of caveolae, trans and paracellular disruption, tight junction breakdown and vascular disruption. Confounding factors that need careful assessment and standardization are the severity, duration and extent of the stroke and TBI that influences BBB disruption. Vascular repair proceeds through long-term neovascularization processes: angiogenesis, arteriogenesis and vasculogenesis. Enhancing each of these processes may impart beneficial effects in endogenous recovery. SUMMARY: Our understanding of BBB breakdown acutely after the cerebrovascular injury has come a long way; however, we lack a clear understanding of the course of BBB disruption and BBB recovery and the evolution of individual cellular events associated with BBB change. Neovascularization responses have been widely studied in stroke for their role in functional recovery but the role of vascular reorganization after TBI in recovery is much less defined.
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“BBB dysfunction is a prominent pathological feature of both ischemic and hemorrhagic stroke and is typically associated with poor outcome (307, 312, 482).”
From Blood-Brain Barrier: From Physiology to Disease and Back (2019) · cites this paper as [482]
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“In preclinical models of ischemic stroke, opening of BBB has been shown to be a biphasic phenomenon (482).”
From Blood-Brain Barrier: From Physiology to Disease and Back (2019) · cites this paper as [482]
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“For instance, it has been suggested that an increase of the blood-brain barrier (BBB) permeability could be determined by severe stress and/or traumatic brain injury [35,36].”
From C-Reactive protein as a biomarker for major depressive disorder? (2022) · cites this paper as [35]
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Cites
Heart Disease and Stroke Statistics—2015 Update: A Report From the American Heart Association
Mozaffarian, D., Benjamin, E. J., Go, A. S., Arnett, D. K., Blaha, M. J., Cushman, M., de Ferranti, S., Després, J.-P., Fullerton, H. J., Howard, V. J., et al. (2015) · Circulation · doi:10.1161/cir.0000000000000152 · Cited by 5,797
Angiogenesis in health and disease
Carmeliet, P. (2003) · Nature Medicine · doi:10.1038/nm0603-653 · Cited by 4,379
The Blood-Brain Barrier in Health and Chronic Neurodegenerative Disorders
Zlokovic, B. V. (2008) · Neuron · doi:10.1016/j.neuron.2008.01.003 · Cited by 3,280
Pericytes regulate the blood–brain barrier
Armulik, A., Genové, G., Mäe, M., Nisancioglu, M. H., Wallgard, E., Niaudet, C., He, L., Norlin, J., Lindblom, P., Strittmatter, K., et al. (2010) · Nature · doi:10.1038/nature09522 · Cited by 2,843
Development, maintenance and disruption of the blood-brain barrier
Obermeier, B., Daneman, R., & Ransohoff, R. M. (2013) · Nature Medicine · doi:10.1038/nm.3407 · Cited by 2,452
Ghajar, J. (2000) · The Lancet · doi:10.1016/s0140-6736(00)02689-1 · Cited by 2,244
Pathophysiology of traumatic brain injury
Werner, C., & Engelhard, K. (2007) · British Journal of Anaesthesia · doi:10.1093/bja/aem131 · Cited by 1,712
Animal models of traumatic brain injury
Xiong, Y., Mahmood, A., & Chopp, M. (2013) · Nature reviews. Neuroscience · doi:10.1038/nrn3407 · Cited by 1,456
The New Neurometabolic Cascade of Concussion
Giza, C. C., & Hovda, D. A. (2014) · Neurosurgery · doi:10.1227/neu.0000000000000505 · Cited by 1,353
The Neurometabolic Cascade of Concussion.
Giza, C. C., & Hovda, D. A. (2001) · PubMed Central · Cited by 1,342
Cited by
Sorted by citations
Blood-Brain Barrier: From Physiology to Disease and Back
Sweeney, M. D., Zhao, Z., Montagne, A., Nelson, A. R., & Zlokovic, B. V. (2019) · Physiological Reviews · doi:10.1152/physrev.00050.2017 · Cited by 2,312
Blood-brain barrier dysfunction and recovery after ischemic stroke
Jiang, X., Andjelkovic, A. V., Zhu, L., Yang, T., Bennett, M. V. L., Chen, J., Keep, R. F., & Shi, Y. (2017) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2017.10.001 · Cited by 967
Organotypic vasculature: From descriptive heterogeneity to functional pathophysiology
Augustin, H. G., & Koh, G. Y. (2017) · Science · doi:10.1126/science.aal2379 · Cited by 790
Abdullahi, W., Tripathi, D. K., & Ronaldson, P. T. (2018) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00095.2018 · Cited by 623
“Such barrier breakdown leads to a significant increase in paracellular permeability at the level of the cerebral microvasculature, a remarkable pathological feature of stroke (68, 115).”
BackgroundChen, A., Fang, Z. H., Chen, X.-L., Yang, S., Zhou, Y., Mao, L., Xia, Y., Jin, H., Li, Y., You, M., et al. (2019) · Cell Death and Disease · doi:10.1038/s41419-019-1716-9 · Cited by 559
Lochhead, J. J., Yang, J., Ronaldson, P. T., & Davis, T. P. (2020) · Frontiers in Physiology · doi:10.3389/fphys.2020.00914 · Cited by 445
Bao, Q., Hu, P., Xu, Y., Cheng, T., Wei, C., Pan, L., & Shi, J. (2018) · ACS Nano · doi:10.1021/acsnano.8b01994 · Cited by 391
Bernardo-Castro, S., Sousa, J. A., Brás, A., Cecília, C., Rodrigues, B., Almendra, L., Machado, C., Santo, G., da Silva, F. A. D. A., Ferreira, L., et al. (2020) · Frontiers in Neurology · doi:10.3389/fneur.2020.594672 · Cited by 395
“This process implies an immature BBB (139), hence the risk of developing HT.”
BackgroundSulhan, S., Lyon, K. A., Shapiro, L. A., & Huang, J. H. (2018) · Journal of Neuroscience Research · doi:10.1002/jnr.24331 · Cited by 353
Blood-brain barrier regulation in psychiatric disorders
Kealy, J., Greene, C., & Campbell, M. (2018) · Neuroscience Letters · doi:10.1016/j.neulet.2018.06.033 · Cited by 318
Blood-Brain Barrier Dysfunction in CNS Disorders and Putative Therapeutic Targets: An Overview
Archie, S. R., Shoyaib, A. A., & Cucullo, L. (2021) · Pharmaceutics · doi:10.3390/pharmaceutics13111779 · Cited by 244
Astrocytic tight junctions control inflammatory CNS lesion pathogenesis
Horng, S., Therattil, A., Moyon, S., Gordon, A., Kim, K., Argaw, A. T., Hara, Y., Mariani, J. N., Sawai, S., Flodby, P., et al. (2017) · Journal of Clinical Investigation · doi:10.1172/jci91301 · Cited by 221
Cao, G., Jiang, N., Hu, Y., Zhang, Y., Wang, G., Yin, M., Ma, X., Zhou, K., Qi, J., Yu, B., et al. (2016) · International Journal of Molecular Sciences · doi:10.3390/ijms17091418 · Cited by 191
“As a highly specialized endothelial tissue, the function of the BBB is modulated by the cerebral microvascular endothelium, which can prevent peripheral leukocyte recruitment into the brain parenchyma [4].”
BackgroundC-Reactive protein as a biomarker for major depressive disorder?
Orsolini, L., Pompili, S., Tempia Valenta, S., Salvi, V., & Volpe, U. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23031616 · Cited by 171
“For instance, it has been suggested that an increase of the blood-brain barrier (BBB) permeability could be determined by severe stress and/or traumatic brain injury [35,36].”
BackgroundPrecision drug delivery to the central nervous system using engineered nanoparticles
Gao, J., Xia, Z. J., Gunasekar, S., Jiang, C., Karp, J. M., & Joshi, N. (2024) · Nature Reviews Materials · doi:10.1038/s41578-024-00695-w · Cited by 173
“Other acute assaults, such as TBI and ischaemic stroke, can also breach the BBB for a short window of time, which forms a valuable therapeutic window for the efficient penetration of drug-loaded NPs 97,98 .”
Mitochondria-Endoplasmic Reticulum Contacts in Reactive Astrocytes Promote Vascular Remodeling
Göbel, J., Engelhardt, E., Pelzer, P., Sakthivelu, V., Jahn, H. M., Jevtic, M., Folz‐Donahue, K., Kukat, C., Schauss, A. C., Frese, C. K., et al. (2020) · Cell Metabolism · doi:10.1016/j.cmet.2020.03.005 · Cited by 160
He, R., Jiang, Y., Shi, Y., Liang, J., & Zhao, L. (2020) · Materials Science and Engineering C · doi:10.1016/j.msec.2020.111314 · Cited by 147
Chen, S., Shao, L., & Ma, L. (2021) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2021.716825 · Cited by 154
Sorby‐Adams, A., Marcoionni, A., Dempsey, E., Woenig, J. A., & Turner, R. J. (2017) · International Journal of Molecular Sciences · doi:10.3390/ijms18081788 · Cited by 150
“Alterations in BBB permeability have been well-documented following TBI [44,45], with the exact temporal profile of such changes highly variable depending upon the type of injury.”
BackgroundEmerging links between cerebrovascular and neurodegenerative diseases—a special role for pericytes
Lendahl, U., Nilsson, P., & Betsholtz, C. (2019) · EMBO Reports · doi:10.15252/embr.201948070 · Cited by 148
“BBB disruptions occur in TBI [122,123], which may contribute to the more long-term neurological problems in TBI.”
Zhang, Q., Liu, C., Shi, R., Zhou, S., Shan, H., Deng, L., Chen, T., Guo, Y., Zhang, Z., Yang, G., et al. (2022) · Aging and Disease · doi:10.14336/ad.2021.1029 · Cited by 138
“It is well established that the BBB is disrupted after ischemic stroke, which contributes to the development of brain injury and subsequent neurological impairment [19, 20].”
BackgroundPlanas, A. M. (2024) · Glia · doi:10.1002/glia.24501 · Cited by 144
“However, this pattern varies depending on stroke severity and the specific stroke models (Prakash & Carmichael, 2015).”
BackgroundSperring, C. P., Savage, W., Argenziano, M., Leifer, V. P., Alexander, J. E., Echlov, N., Spinazzi, E. F., & Connolly, E. S. (2023) · Stroke · doi:10.1161/strokeaha.123.044240 · Cited by 138
Celorrio, M., Abellanas, M. A., Rhodes, J., Goodwin, V. M., Moritz, J., Vadivelu, S., Wang, L., Rodgers, R., Xiao, S., Anabayan, I., et al. (2021) · Acta Neuropathologica Communications · doi:10.1186/s40478-021-01137-2 · Cited by 122
“It is well-characterized that BBB permeability increases after TBI [56].”
BackgroundRevisiting the blood-brain barrier: A hard nut to crack in the transportation of drug molecules
Harilal, S., Jose, J., Parambi, D. G. T., Kumar, R., Unnikrishnan, M. K., Uddin, M. S., Mathew, G. E., Pratap, R., Marathakam, A., & Mathew, B. (2020) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2020.03.018 · Cited by 127
Fan, F., Lü, Y., Li, R., Zou, X., Li, N., Meng, X., Zhang, Y., & Wang, X. (2020) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2020.110458 · Cited by 116
Wang, Y., Guan, X., Gao, C., Ruan, W., Zhao, S., Kai, G., Li, F., & Pang, T. (2021) · Pharmacological Research · doi:10.1016/j.phrs.2021.105640 · Cited by 109
Biomarkers for acute diagnosis and management of stroke in neurointensive care units
Glushakova, O., Glushakov, A. V., Miller, E. R., Valadka, A. B., & Hayes, R. (2016) · Brain Circulation · doi:10.4103/2394-8108.178546 · Cited by 112
“Of interest are studies of CNS-specifi c biomarker dynamics performed in TBI, which share several common features with strokes including brain ischemia, parenchymal brain hemorrhage, and SAH often coexisting at varied degrees; comparisons of the biomarker profiles between these two acute insults would provide valuable…”
BackgroundAl-Ahmady, Z. S., Jasim, D. A., Ahmad, S. S., Wong, R., Haley, M., Coutts, G., Schießl, I., Allan, S. M., & Kostarelos, K. (2019) · ACS Nano · doi:10.1021/acsnano.9b01808 · Cited by 109
PDGFR-β restores blood-brain barrier functions in a mouse model of focal cerebral ischemia
Shen, J., Xu, G., Zhu, R., Yuan, J., Ishii, Y., Hamashima, T., Matsushima, T., Yamamoto, S., Takatsuru, Y., Nabekura, J., et al. (2018) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1177/0271678x18769515 · Cited by 105
Chen, Z., Xu, Q.-Q., Shan, C.-S., Shi, Y., Wang, Y., Chang, R. C., & Zheng, G. (2019) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2019/2936737 · Cited by 101
Hutchings, G., Janowicz, K., Moncrieff, L., Dompé, C., Strauss, E., Kocherova, I., Nawrocki, M. J., Kruszyna, Ł., Wąsiatycz, G., Antosik, P., et al. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21113790 · Cited by 97
Liang, Y., Song, P., Chen, W., Xie, X., Luo, R., Su, J.-H., Zhu, Y., Xu, J., Liu, R., Zhu, P., et al. (2021) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2020.540669 · Cited by 94
Zarriello, S., Tuazon, J. P., Corey, S., Schimmel, S. J., Rajani, M., Gorsky, A., Abraham, D. I., Hammock, B. D., & Borlongan, C. V. (2018) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2018.11.001 · Cited by 92
“In some pathogenic processes, such as in stroke and TBI, inflammation can also cause increased permeability of the BBB, allowing harmful blood products to enter the brain parenchyma (Prakash and Carmichael, 2015).”
BackgroundOzga, J. E., Povroznik, J. M., Engler-Chiurazzi, E. B., & Haar, C. V. (2018) · Behavioural Pharmacology · doi:10.1097/fbp.0000000000000430 · Cited by 96
“Parsing these metabolic changes is further compounded by disruption of the blood–brain barrier (Stowe et al., 2000; Hay et al., 2015; Prakash and Carmichael, 2015), potentially resulting in higher than normal drug concentrations, and/or other interfering proteins reaching neural tissue as blood–brain barrier permeabil…”
BackgroundZhu, J., Li, Z., Ji, Z., Wu, Y., He, Y., Liu, K., Chang, Y., Peng, Y., Lin, Z., Wang, S., et al. (2021) · Brain Pathology · doi:10.1111/bpa.13006 · Cited by 83
“The disassembly and reassembly of endothelial TJs are considered to account for the featured dynamics of BBB disruption (4, 6).”
BackgroundThe peripheral immune response after stroke—A double edge sword for blood‐brain barrier integrity
Li, Y., Zhu, Z., Huang, T., Zhou, Y., Wang, X., Yang, L., Chen, Z., Yu, W., & Li, P. (2018) · CNS Neuroscience & Therapeutics · doi:10.1111/cns.13081 · Cited by 84
Traumatic Brain Injury: A Comprehensive Review of Biomechanics and Molecular Pathophysiology
Orr, T. J., Lesha, E., Kramer, A. H., Cecia, A. F., Dugan, J. E., Schwartz, B., & Einhaus, S. L. (2024) · World Neurosurgery · doi:10.1016/j.wneu.2024.01.084 · Cited by 96
Structural and Functional Remodeling of the Brain Vasculature Following Stroke
Andrade, M. F., Raman‐Nair, J., & Lacoste, B. (2020) · Frontiers in Physiology · doi:10.3389/fphys.2020.00948 · Cited by 82
Mascaro, A. L. A., Conti, E., Lai, S., Giovanna, A. P. D., Spalletti, C., Alia, C., Panarese, A., Scaglione, A., Sacconi, L., Micera, S., et al. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.08.062 · Cited by 75
“The reason could be that the region of active neovascularization acts as a niche for enhanced neuronal remodeling and tissue repair (Prakash and Carmichael, 2015; Shen et al., 2008).”
BackgroundLi, Q., Ding, D., Wang, X., Sun, Y., & Wu, J. (2021) · Experimental Neurology · doi:10.1016/j.expneurol.2021.113645 · Cited by 75
Age‐related small vessel disease: a potential contributor to neurodegeneration in multiple sclerosis
Geraldes, R., Esiri, M. M., DeLuca, G. C., & Palace, J. A. (2016) · Brain Pathology · doi:10.1111/bpa.12460 · Cited by 77
Liu, B., Li, Y., Han, Y., Wang, S., Yang, H., Zhao, Y., Li, P., & Wang, Y. (2021) · Phytomedicine · doi:10.1016/j.phymed.2021.153660 · Cited by 74
Lippert, T., & Borlongan, C. V. (2019) · CNS Neuroscience & Therapeutics · doi:10.1111/cns.13124 · Cited by 76
Zhang, X., Wang, L., Han, Z., Dong, J., Pang, D., Fu, Y., & Li, L. (2020) · Journal of Neuroinflammation · doi:10.1186/s12974-020-01780-x · Cited by 69
Phosphodiesterase Type 4 Inhibition in CNS Diseases
Blokland, A., Heckman, P. R. A., Vanmierlo, T., Schreiber, R., Paes, D., & Prickaerts, J. (2019) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2019.10.006 · Cited by 70
“The sustained increase in BBB permeability and the subsequent leakage of inflammatory cells and humoral factors can lead to long-lasting impairments in BBB integrity [72]”
BackgroundExploiting BBB disruption for the delivery of nanocarriers to the diseased CNS
Umlauf, B. J., & Shusta, E. V. (2019) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2019.01.013 · Cited by 67
“While hemorrhagic stroke is by definition a breach of the BBB, ischemic stroke induces BBB disruption in a complex, multi-phasic manner[16].”
BackgroundJiang, Y., Lin, L., Liu, N., Wang, Q., Yuan, J., Li, Y., Chung, K. K., Guo, S., Yu, Z., & Wang, X. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21030824 · Cited by 66
“Enormous clinical and experimental investigations have demonstrated that BBB integrity disruption is a key cerebral vascular pathology primarily mediating acute brain injury after ischemic stroke [29,30] and associated with poor prognosis poststroke [31].”
BackgroundDl-3-n-butylphthalide Reduces Neurovascular Inflammation and Ischemic Brain Injury in Mice
Yang, C., Guo, A., Li, Y., Shi, K., Shi, F., & Li, M. (2019) · Aging and Disease · doi:10.14336/ad.2019.0608 · Cited by 66
“The interaction among the cerebrovascular endothelium, leukocytes, and platelets exacerbates thrombosis and cerebrovascular dysfunction, leading to infarct expansion and worsened neurological outcome [10-16].”
BackgroundSubacute Stroke Mimicking Cerebral Metastasis in 68Ga-PSMA-HBED-CC PET/CT
Noto, B., Vrachimis, A., Schäfers, M. A., Stegger, L., & Rahbar, K. (2016) · Clinical Nuclear Medicine · doi:10.1097/rlu.0000000000001291 · Cited by 62
Friend, S. F., Nachnani, R., Powell, S. B., & Risbrough, V. B. (2020) · European Journal of Neuroscience · doi:10.1111/ejn.15031 · Cited by 66
“Moreover, traumatic brain injury, one of the most substantial risk factors for PTSD (Prakash & Carmichael, 2015; Yurgil et al., 2014), is also associated with BBB permeability, allowing immune signaling factors, including CRP, to access the CNS. CRP itself can also induce BBB disruption by binding…”
BackgroundCharacterization of the Blood Brain Barrier Disruption in the Photothrombotic Stroke Model
Weber, R., Grönnert, L., Mulders, G., Maurer, M., Tackenberg, C., Schwab, M. E., & Rust, R. (2020) · Frontiers in Physiology · doi:10.3389/fphys.2020.586226 · Cited by 56
“Although considerable sex differences have been previously reported in clinical stroke pathology (Reeves et al., 2008) as well as BBB permeability (Castellazzi et al., 2020), we have not observed any differences in BBB disruption between the sex in the photothrombotic stroke model.”
BackgroundA Comprehensive View on MRI Techniques for Imaging Blood-Brain Barrier Integrity.
Elschot, E. P., Backes, W., Postma, A., van Oostenbrugge, R. V., Staals, J., Rouhl, R., & Jansen, J. (2020) · Investigative Radiology · doi:10.1097/rli.0000000000000723 · Cited by 54
“An altered BBB integrity after stroke can express itself in several ways and is related to the severity of the condition.(50) In ischemic stroke, the BBB gets disrupted because of the oxidative stress shortly after onset of ischemia.”
BackgroundThe Role of Substance P in Secondary Pathophysiology after Traumatic Brain Injury
Vink, R., Gabrielian, L., & Thornton, E. (2017) · Frontiers in Neurology · doi:10.3389/fneur.2017.00304 · Cited by 60
Jiang, Y., He, R., Shi, Y., Liang, J., & Zhao, L. (2020) · Life Sciences · doi:10.1016/j.lfs.2020.117987 · Cited by 60
Xu, Z., Shi, W., Xu, L., Shao, M., Chen, Z.-P., Zhu, G.-C., & Hou, Q. (2018) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.8b00298 · Cited by 59
Sex-Specific Immune Responses in Stroke
Banerjee, A., & McCullough, L. D. (2022) · Stroke · doi:10.1161/strokeaha.122.036945 · Cited by 57
Prabhakar, N. K., Khan, H., Grewal, A. K., & Singh, T. G. (2022) · International Immunopharmacology · doi:10.1016/j.intimp.2022.108902 · Cited by 60
Faisal, S. M., Comba, A., Varela, M. L., Argento, A. E., Brumley, E. K., Abel, C. C., Castro, M. G., & Lowenstein, P. R. (2022) · Frontiers in Oncology · doi:10.3389/fonc.2022.1005069 · Cited by 58
Signaling pathways in brain ischemia: Mechanisms and therapeutic implications
Lin, W., Zhao, X., Cheng, J., Li, L., Jiang, Q., Zhang, Y., & Han, F. (2023) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2023.108541 · Cited by 61
Cognitive impairment after traumatic brain injury: The role of MRI and possible pathological basis
Wang, M.-L., & Li, W. (2016) · Journal of the Neurological Sciences · doi:10.1016/j.jns.2016.09.049 · Cited by 57
Leiro, V., Santos, S. D., Lopes, C. D. F., & Pêgo, A. P. (2017) · Advanced Functional Materials · doi:10.1002/adfm.201700313 · Cited by 56
Mishra, A., Kumar, R., Mishra, J., Dutta, K., Ahlawat, P., Kumar, A., Dhanasekaran, S., Gupta, A. K., Sinha, S., Bishi, D. K., et al. (2023) · Journal of Drug Delivery Science and Technology · doi:10.1016/j.jddst.2023.104694 · Cited by 56
Stroke-induced damage on the blood–brain barrier
Xue, S., Zhou, X., Yang, Z., Si, X., & Sun, X. (2023) · Frontiers in Neurology · doi:10.3389/fneur.2023.1248970 · Cited by 58
“Opening of the BBB is a biphasic phenomenon in preclinical models of ischemic stroke (145).”
Chang, R., Folkerson, L. E., Sloan, D., Tomasek, J. S., Kitagawa, R. S., Choi, H. A., Wade, C. E., & Holcomb, J. B. (2016) · Surgery · doi:10.1016/j.surg.2016.08.023 · Cited by 55
Basement Membrane Changes in Ischemic Stroke
Kang, M., & Yao, Y. (2020) · Stroke · doi:10.1161/strokeaha.120.028928 · Cited by 59
Agoston, D. V., Vink, R., Helmy, A. E., Risling, M., Nelson, D., & Prins, M. L. (2019) · Journal of Neurotrauma · doi:10.1089/neu.2018.6261 · Cited by 52
“and extent of neovascularization after TBI observed in both rodent models and also in human TBI cases.(89) Newly formed, immature”
BackgroundZhang, B., Gao, Y., Li, Q., Sun, D., Dong, X., Li, X., Xin, W., & Zhang, J. (2019) · World Neurosurgery · doi:10.1016/j.wneu.2019.11.172 · Cited by 52
Fanxia, S., Lidan, J., Frank, H., Degos, V., Chen, S., & Su, H. (2018) · Aging and Disease · doi:10.14336/ad.2018.0205 · Cited by 51
“MMP-9, a member belonging to the family of matrix metalloproteinases (MMPs), has been suggested to be involved in the BBB breakdown in neurological disorders, including stroke [41, 42].”
BackgroundA three-dimensional neural spheroid model for capillary-like network formation
Boutin, M. E., Kramer, L., Livi, L. L., Brown, T. D., Moore, C. I., & Hoffman–Kim, D. (2017) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2017.01.014 · Cited by 51
Pu, H., Jiang, X., Wei, Z., Hong, D., Hassan, S., Zhang, W., Liu, J., Meng, H., Shi, Y., Chen, L., et al. (2017) · Cell Transplantation · doi:10.3727/096368916x693842 · Cited by 49
Mesenchymal stem cell therapies in brain disease
Sherman, L. S., Romagano, M. P., Williams, S. F., & Rameshwar, P. (2019) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2019.03.003 · Cited by 49
Time‐dependent dual effect of NLRP3 inflammasome in brain ischaemia
Palomino‐Antolín, A., Narros‐Fernández, P., Farré‐Alins, V., Sevilla‐Montero, J., Decouty‐Pérez, C., López-Rodríguez, A. B., Fernández, N., Monge, L., Casas, A. I., Calzada, M. J., et al. (2021) · British Journal of Pharmacology · doi:10.1111/bph.15732 · Cited by 48
Yu, J., Li, C., Ding, Q., Que, J., Liu, K., Wang, H., & Liao, S. (2017) · Frontiers in Neuroscience · doi:10.3389/fnins.2017.00700 · Cited by 49
“However, local newly-formed blood vessels with immature blood-brain barrier (BBB), which are characterized by high permeability, could also spark off neuronal loss due to the injury of extravasation of serum macromolecules and inflammatory factors to brain parenchyma (Abraham et al., 2002; Krueger et al., 2015; Prakas…”
BackgroundTime-dependent dual effect of microglia in ischemic stroke
Fan, P., Wang, S., Chu, S., & Chen, N. (2023) · Neurochemistry International · doi:10.1016/j.neuint.2023.105584 · Cited by 49
Restin, T., Kajdi, M.-E., Schläpfer, M., Z’graggen, B. R., Booy, C., Dumrese, C., & Beck‐Schimmer, B. (2017) · PLoS ONE · doi:10.1371/journal.pone.0184973 · Cited by 46
“Blood-brain barrier disruption is highly relevant in the pathogenesis of secondary brain damage after brain injury [12, 25].”
BackgroundQin, X., Wang, J., Chen, S., Liu, G., Wu, C., Lv, Q., He, X., Bai, X., Huang, W., & Liao, H. (2022) · Glia · doi:10.1002/glia.24146 · Cited by 46
“…with abnormal structural alternations of tight junctions (Jiang et al., 2018; Knowland et al., 2014; Krueger et al., 2019), and activation of matrix metalloproteinases (MMPs) causing degradation of endothelial tight junctions (Prakash & Carmichael, 2015; Zhang, Tang, et al., 2020), and so forth.”
BackgroundHyperbaric oxygen therapy: A new look on treating stroke and traumatic brain injury
Borlongan, C., Gonzales‐Portillo, B., Lippert, T., Nguyen, H., & Lee, J.-Y. (2019) · Brain Circulation · doi:10.4103/bc.bc_31_19 · Cited by 50
“[6‐8] Secondary cell death of stroke and TBI have been linked to the breakdown of the blood–brain barrier (BBB), which allows for inflammatory cytokines to cross the BBB and ultimately increase inflammatory response, thus damaging the outcomes.[9] Additional Address for correspondence: Dr.”
BackgroundBrain‐targeting drug delivery systems
Liu, P., & Jiang, C. (2022) · Wiley Interdisciplinary Reviews Nanomedicine and Nanobiotechnology · doi:10.1002/wnan.1818 · Cited by 47
Matthiesen, I., Voulgaris, D., Nikolakopoulou, P., Winkler, T. E., & Herland, A. (2021) · Small · doi:10.1002/smll.202101785 · Cited by 44
Lu, H. J., Ashiqueali, R., Lin, C.-I., Walchale, A., Clendaniel, V., Matheson, R., Fisher, M., Lo, E. H., Selim, M. H., & Shehadah, A. (2022) · Molecular Neurobiology · doi:10.1007/s12035-022-03083-z · Cited by 43
You, Y., Liu, Y., Ma, C., Xu, J., Xie, L., Tong, S., Sun, Y., Ma, F., Huang, Y., Liu, J., et al. (2023) · Journal of Controlled Release · doi:10.1016/j.jconrel.2023.08.039 · Cited by 42
Zhou, Y., Li, Y., Jin, H., Wu, J., He, Q., Wang, X., Lei, H. C., & Hu, B. (2017) · The FASEB Journal · doi:10.1096/fj.201700786rr · Cited by 43
“Because the BBB disruption after stroke involves a series of pathologic process (7), understanding the cellular and molecular mechanisms underlying BBB damage after ischemic injury could effectively improve prognosis as well as clinical manage-”
BackgroundMethods of Mesenchymal Stem Cell Homing to the Blood–Brain Barrier
Conaty, P., Sherman, L. S., Naaldijk, Y., Ulrich, H., Stolzing, A., & Rameshwar, P. (2018) · Methods in molecular biology · doi:10.1007/978-1-4939-8697-2_6 · Cited by 42
Mittal, B., Malik, D., Sood, A., Singh, H., Basher, R. K., Shukla, J., Bhattacharya, A., & Singh, S. (2018) · Indian Journal of Nuclear Medicine · doi:10.4103/ijnm.ijnm_81_18 · Cited by 42
“[12] However, breach in blood–brain barrier may lead to nonspecific tracer accumulation in infarct/hemorrhage site due to increased permeability of tracer as well as the simultaneous occurrence of reparative processes (characterized by neovascularization) at these sites.[13] Hence, visualization of tracer avidity in s…”
BackgroundRoseborough, A. D., Zhu, Y., Zhao, L., Laviolette, S. R., Pasternak, S., & Whitehead, S. N. (2023) · Neurobiology of Disease · doi:10.1016/j.nbd.2023.106001 · Cited by 45
“Disruptions to the BBB can be acute in nature following neurological injury such as stroke and traumatic brain injury or can involve chronic impairment of its structural and functional integrity (Schoknecht and Shalev, 2012; Hay et al., 2015; Prakash and Carmichael, 2015).”
BackgroundInfluentialNeuroinflammation and acute ischemic stroke: impact on translational research and clinical care
Levinson, S., Pulli, B., & Heit, J. J. (2025) · Frontiers in Surgery · doi:10.3389/fsurg.2025.1501359 · Cited by 43
Fukuta, T., Oku, N., & Kogure, K. (2022) · Pharmaceutics · doi:10.3390/pharmaceutics14020361 · Cited by 41
“Following ischemic stroke, the I/R-induced increase in the permeability of the BBB has been shown to exhibit time-dependent and biphasic changes, whereby the increase in vascular permeability after I/R peaks once at 3–6 h (acute phase), with delayed BBB opening occurring at 48–72 h (subacute phase) [61,92].”
BackgroundCottier, K. E., Galloway, E. A., Calabrese, E., Tome, M. E., Liktor‐Busa, E., Kim, J., Davis, T. P., Vanderah, T. W., & Largent‐Milnes, T. M. (2018) · eNeuro · doi:10.1523/eneuro.0116-18.2018 · Cited by 38
“In conditions such as TBI and ischemic stroke, the integrity of the BBB is altered following injury (Prakash and Carmichael, 2015), although this loss of integrity is most often associated with trauma within the CNS rather than with CSD or headache.”
BackgroundBlood-brain barrier dysfunction as a potential therapeutic target for neurodegenerative disorders
Uprety, A. R., Kang, Y., & Kim, S. Y. (2021) · Archives of Pharmacal Research · doi:10.1007/s12272-021-01332-8 · Cited by 39
“MMP-9 expression is also significantly increased after stroke or TBI, both of which involve BBB breakdown, and the increased MMP-9 expression is likely to exacerbate the loss of TJ proteins and BBB dysfunction (reviewed in Prakash and Carmichael 2015).”
BackgroundWu, J., Zhao, Q., Chen, S., Xu, H., Zhang, R., Cai, D., Gao, Y., Peng, W., Chen, X., Yuan, S., et al. (2024) · Cancer Letters · doi:10.1016/j.canlet.2024.217266 · Cited by 40
Zhang, Y., Fan, F., Zeng, G., Zhou, L., Zhang, Y., Zhang, J., He, J., Zhang, T., Su, D., Yang, C., et al. (2016) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1177/0271678x16680221 · Cited by 36
“thrombolytic treatment.(4) In general, BBB is part of the Neurovascular Unit (NVU), within which the cell–cell and cell–matrix communications hold the normal structure and function of the brain.”
BackgroundMotor tract reorganization after acute central nervous system injury: a translational perspective
Takase, H., & Regenhardt, R. W. (2020) · Neural Regeneration Research · doi:10.4103/1673-5374.300330 · Cited by 35
“Ischemic stroke, which comprises 80 – 90% of all human strokes, is characterized by a sudden reduction in local cerebral blood flow (Prakash and Carmichael, 2015).”
The secretome of endothelial progenitor cells: a potential therapeutic strategy for ischemic stroke
Bayraktutan, U., Alwjwaj, M., & Kadir, R. R. A. (2021) · Neural Regeneration Research · doi:10.4103/1673-5374.303012 · Cited by 36
“Oxidative stress and post-ischemic inflammation, characterized by excessive availabilities of reactive oxygen species (ROS) and inflammatory cytokines such as interleukin (IL)-1β, IL-18, IL-6 and tumor necrosis factor-α harm NVU by disrupting structural integrity of the tight junctions (del Zoppo and Hallenbeck, 2000;…”
BackgroundInfluentialPTSD, Immune System, and Inflammation
Pivac, N., Vuić, B., Šagud, M., Erjavec, G. N., Perković, M. N., Konjevod, M., Tudor, L., Štrac, D. Š., Uzun, S., Kozumplik, O., et al. (2023) · Advances in experimental medicine and biology · doi:10.1007/978-981-19-7376-5_11 · Cited by 38
Non‐Invasive Photoacoustic Cerebrovascular Monitoring of Early‐Stage Ischemic Strokes In Vivo
Kim, J., Kweon, J. Y., Choi, S., Jeon, H., Sung, M., Gao, R., Liu, C., Kim, C., & Ahn, Y. J. (2024) · Advanced Science · doi:10.1002/advs.202409361 · Cited by 35
Selvakumar, G. P., Ahmed, M. E., Thangavel, R., Kempuraj, D., Dubova, I., Raikwar, S. P., Zaheer, S. A., Iyer, S. S., & Zaheer, A. (2020) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2020.01.013 · Cited by 36
“Administration of MPTP enhances calpain 1 expression in WT and GMF-KO mice and probably due to neovascularization process, may lead to re-modeling the vessels in damaged brain region (Potz et al., 2016; Prakash and Carmichael, 2015).”
BackgroundPermeability of the Blood–Brain Barrier after Traumatic Brain Injury: Radiological Considerations
Amoo, M., O’Halloran, P. J., Henry, J. H., Husien, M. B., Brennan, P., Campbell, M., Caird, J., & Curley, G. F. (2021) · Journal of Neurotrauma · doi:10.1089/neu.2020.7545 · Cited by 36
“59,60 The delayed phase of BBB disruption is observed typically around day 3–7 after TBI.”
Extracellular vesicles as distinct biomarker reservoirs for mild traumatic brain injury diagnosis
Beard, K., Yang, Z., Haber, M., Flamholz, M., Diaz-Arrastia, R. R., Sandsmark, D. K., Meaney, D. F., & Issadore, D. (2021) · Brain Communications · doi:10.1093/braincomms/fcab151 · Cited by 36
Epigenetics and stroke: role of DNA methylation and effect of aging on blood–brain barrier recovery
Phillips, C. M., Stamatovic, S. M., Keep, R. F., & Andjelkovic, A. V. (2023) · Fluids and Barriers of the CNS · doi:10.1186/s12987-023-00414-7 · Cited by 35
“In poststroke BBB recovery, angiogenesis is a pivotal process [12, 24, 56].”
Background
Metadata
- Authors
- Prakash, R., & Carmichael, S. T.
- Affiliations
- University of California, Los Angeles (US)
- Corresponding author
- Prakash, Roshini
- Venue
- Current Opinion in Neurology
- Published
- 2015-12
- Volume
- 28
- Issue
- 6
- Pages
- 556-564
- ISSN
- 1350-7540 (ISSN-L)
- PMC
- PMC5267616
- OpenAlex
- W2341136898
- Cited by
- 296
- References
- 134
- Citations by year
- 2026: 16 · 2025: 27 · 2024: 32 · 2023: 29 · 2022: 33 · 2021: 38 · 2020: 36 · 2019: 31 · 2018: 24 · 2017: 19 · 2016: 11
- FWCI
- 1.44
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Current Opinion in Neurology (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- National Institute of Neurological Disorders and Stroke (R01NS081055, R01NS053957)
- Topics
- Life Sciences › Neuroscience › Neurology › Barrier Structure and Function Studies
- Health Sciences › Medicine › Clinical Neurology › Traumatic Brain Injury and Neurovascular Disturbances
- Health Sciences › Medicine › Clinical Neurology › Acute Ischemic Stroke Management
- Keywords
- blood-brain barrier disruption, neovascularization, stroke, traumatic brain injury, angiogenesis, arteriogenesis, vasculogenesis, vascular repair, caveolae, tight junction disruption, paracellular permeability, functional recovery
- MeSH terms
- Blood-Brain Barrier, Brain Injuries, Humans, Neovascularization, Physiologic, Stroke
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