Development, maintenance and disruption of the blood-brain barrier

Obermeier, Birgit; Daneman, Richard; Ransohoff, Richard M

doi:10.1038/nm.3407

Cited by 2,452Barrier Structure and Function StudiesDrug Transport and Resistance MechanismsCerebrospinal fluid and hydrocephalus

Development, maintenance and disruption of the blood-brain barrier

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Obermeier, Birgit, Daneman, Richard, Ransohoff, Richard M·2013·Nature Medicine

DOI 10.1038/nm.3407PMC PMC4080800

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Abstract

The interface between the blood circulation and the neural tissue features unique characteristics that are encompassed by the term 'blood-brain barrier' (BBB). The main functions of this barrier, namely maintenance of brain homeostasis, regulation of influx and efflux transport, and protection from harm, are determined by its specialized multicellular structure. Every constituent cell type makes an indispensable contribution to the BBB's integrity. But if one member of the BBB fails, and as a result the barrier breaks down, there can be dramatic consequences and neuroinflammation and neurodegeneration can occur. In this Review, we highlight recently gained mechanistic insights into the development and maintenance of the BBB. We then discuss how BBB disruption can cause or contribute to neurological disease. Finally, we examine how this knowledge can be used to explore new possibilities for BBB repair.

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The breakdown of the BBB is mainly due to the disruption of TJs, such as claudin-5.
“The breakdown of the BBB is mainly due to the disruption of TJs, such as claudin-5 [42, 43].”
From Chronic stress-induced depression requires the recruitment of peripheral Th17 cells into the brain (2022) · cites this paper as [43]
The “Links between the BBB and disease” section says BBB breakdown can involve disrupted tight junctions, and its ischemic-stroke subsection associates reduced claudin-5 expression with increased BBB permeability. But the review also identifies impaired transport processes and says the mechanisms of breakdown are manifold; it does not establish that tight-junction disruption is the main cause. (LLM, conf=0.88)
Experimental — accuracy not yet measured
The blood-brain barrier prevents the transfer of most small-molecule drugs and macromolecules into the brain.
“it prevents the transfer of most of small-molecule drugs and macromolecules (e.g., peptides, gene drugs, and protein drugs) into the brain (1–6).”
From Neurotransmitter-derived lipidoids (NT-lipidoids) for enhanced brain delivery through intravenous injection (2020) · cites this paper as [4]
The Introduction says the BBB’s tight junctions and low transcytosis greatly limit movement of molecules into the brain. It does not specifically establish that most small-molecule drugs or macromolecular drugs, including the examples in the citing sentence, are prevented from entering. (LLM, conf=0.82)
Experimental — accuracy not yet measured
Together with microglia, astrocytes constitute the principal defensive system of the CNS and respond to damage-related stimuli including Aβ and glutamate overload in a process known as astrocyte reactivity.
“Together with microglia, astrocytes constitute the principal defensive system of the CNS [37], responding to numerous damage‐related stimuli [6, 7, 8, 9] including amyloid β peptides (Aβ) and glutamate overload, in a process known as astrocyte reactivity [15, 37, 38, 39, 40].”
From Gliovascular alterations in sporadic and familial Alzheimer's disease: <scp>APOE3</scp> Christchurch homozygote glioprotection (2023) · cites this paper as [7]
The section ‘The role of astrocytes in BBB regulation’ says astrocytes control immune reactions, and ‘BBB compromise in chronic neurodegeneration: ALS’ reports that microglia and astrocytes become activated after tissue injury. These passages support a defensive role and an activation response, but do not call the two cell types the CNS’s principal defensive system or identify the response as ‘astrocyte reactivity.’ The cited paper also does not substantiate Aβ or glutamate overload as triggers in this account. (LLM, conf=0.82)
Experimental — accuracy not yet measured
Astrocyte reactivity has frequently been associated with neuroinflammation, unfavorable glial scar formation, glutamate dyshomeostasis, altered coverage of synapses and blood vessels, and BBB breakout.
“Hence, astrocyte reactivity has frequently been associated with neuroinflammation, unfavorable glial scar formation [7, 8, 9, 37, 38, 43, 48, 49], glutamate dyshomeostasis [43, 50, 51], altered coverage of synapses and blood vessels, and BBB breakout [38, 42, 43, 45, 46, 47].”
From Gliovascular alterations in sporadic and familial Alzheimer's disease: <scp>APOE3</scp> Christchurch homozygote glioprotection (2023) · cites this paper as [7]
The sections on epilepsy and ALS link astrocytic inflammatory activity with increased BBB permeability and describe reduced astrocyte glutamate transport and swollen perivascular end-feet. They do not establish the full claimed association of astrocyte reactivity with unfavorable glial scars or altered synaptic coverage, and the BBB findings are presented in specific disease contexts rather than as a general consequence of reactivity. (LLM, conf=0.85)
Experimental — accuracy not yet measured
Treatment with glucocorticoids offers blood-brain barrier protection.
“Treatment with glucocorticoids also offers BBB protection (446).”
From Blood-Brain Barrier: From Physiology to Disease and Back (2019) · cites this paper as [446]

Treatment of central nervous system diseases is severely constrained by the blood-brain barrier.
“The treatment of central nervous system (CNS) diseases, such as neurodegenerative disorders, brain tumors, brain infections, and stroke, is severely constrained by the blood-brain barrier (BBB) because it prevents the transfer of most of small-molecule drugs and macromolecules (e.g., peptides, gene drugs, and protein drugs) into the brain (1–6).”
From Neurotransmitter-derived lipidoids (NT-lipidoids) for enhanced brain delivery through intravenous injection (2020) · cites this paper as [4]
Astrocytic processes surround most of the vascular surface and regulate blood-brain barrier permeability by modulating tight junction proteins such as claudin-5 and endothelial proteins such as vimentin.
“Astrocytic processes surround most of the vascular surface, regulating the blood–brain barrier (BBB) permeability [6, 7, 8, 9]—by modulating tight junction proteins such as claudin‐5 [10], or endothelial proteins such vimentin, which is associated with the stability of cerebral vasculature [11]—and integrate neuronal activity with blood flow [1, 2, 3, 4, 5, 12, 13, 14, 15, 16, 17, 18, 19, 20].”
From Gliovascular alterations in sporadic and familial Alzheimer's disease: <scp>APOE3</scp> Christchurch homozygote glioprotection (2023) · cites this paper as [7]
The third shared process, geneM26/isoM22, is downregulated and enriched for endothelial and pericyte genes, with hubs including blood-brain barrier markers ITIH5, SLC38A5, ABCB1, and GPR124.
“The third biological process, geneM26/isoM22 (Fig 5C), is downregulated, and enriched for endothelial and pericyte genes, with hubs that represent markers of the blood-brain barrier, including ITIH5, SLC38A5, ABCB1, and GPR124, a critical regulator of brain-specific angiogenesis (53, 54).”
From Transcriptome-wide isoform-level dysregulation in ASD, schizophrenia, and bipolar disorder (2018) · cites this paper as [54]
The third shared process, geneM26/isoM22, is downregulated and enriched for endothelial and pericyte genes, with hubs including blood-brain barrier markers ITIH5, SLC38A5, ABCB1, and GPR124.
“The third biological process, geneM26/isoM22 (Fig 5C), is downregulated, and enriched for endothelial and pericyte genes, with hubs that represent markers of the blood-brain barrier, including ITIH5, SLC38A5, ABCB1, and GPR124, a critical regulator of brain-specific angiogenesis (53, 54).”
From Transcriptome-wide isoform-level dysregulation in ASD, schizophrenia, and bipolar disorder (2018) · cites this paper as [53]
The brain inflammatory response to antigen infiltration triggered by activated microglia may result in aberrant expression of several chemokines, leading to alterations in BBB permeability.
“the brain inflammatory response to antigen infiltration (virus, bacteria or fungus) triggered by activated microglia may result in aberrant expression of several chemokines, leading to alterations in BBB permeability (Buckner et al., 2006; Obermeier et al., 2013).”
From The impact of microglial activation on blood-brain barrier in brain diseases (2014) · cites this paper as Obermeier et al., 2013
Neuroinflammation is a key component of cell death cascades in stroke, with microglial cells and peripheral leukocytes, especially neutrophils and monocytes/macrophages, as main players.
“One of the key components of the cell death cascades in stroke is neuroinflammation, where the main players are microglial cells and the peripheral leukocytes, especially neutrophils and monocytes/macrophages.”
From The impact of microglial activation on blood-brain barrier in brain diseases (2014) · cites this paper as Obermeier et al., 2013
MMPs are further stimulated by NK-κB and HIF-1α and disrupt tight junction proteins (ZO-1, claudin-5 and occludin), rendering the BBB leaky; these downstream effects are reverted by blocking NOS.
“MMPs are further stimulated by NK-κB and HIF-1α and disrupt TJ proteins (as ZO-1, claudin-5 and occludin), rendering the BBB leaky, downstream effects which were shown to be reverted by blocking NOS (Yang and Rosenberg, 2011; Gu et al., 2012; Obermeier et al., 2013).”
From The impact of microglial activation on blood-brain barrier in brain diseases (2014) · cites this paper as Obermeier et al., 2013
The early opening (12-48 h) of the BBB is mainly caused by oxidative stress, with ROS as the most important mediator.
“The early opening (12–48 h) of the BBB is mainly caused by oxidative stress, being ROS the most important mediator.”
From The impact of microglial activation on blood-brain barrier in brain diseases (2014) · cites this paper as Obermeier et al., 2013
In the early phase, release of cytokine pools trapped by BBB ECM (molecule trapping) activates glial and endothelial cells and contributes to recruitment of peripheral immune cells.
“Another phenomenon observed in this early phase is the release of cytokine pools that were trapped by BBB ECM (“molecule trapping”), that activate glial and ECs and contribute to the recruitment of peripheral immune cells (Obermeier et al., 2013).”
From The impact of microglial activation on blood-brain barrier in brain diseases (2014) · cites this paper as Obermeier et al., 2013
ROS activate latent MMP-2 minutes after ischemic insult and are produced by microglia and astrocytes through the HIF-1α pathway.
“They activate the latent MMP-2 min after the ischemic insult, and are produced by microglia and astrocytes through the HIF-1α pathway (Yang and Rosenberg, 2011; Obermeier et al., 2013).”
From The impact of microglial activation on blood-brain barrier in brain diseases (2014) · cites this paper as Obermeier et al., 2013
Brain vascular endothelial cells connect with each other through junction proteins and are enveloped by surrounding pericytes and astrocytes to form the blood-brain barrier.
“Brain vascular endothelial cells (ECs) connect with each other through junction proteins and are enveloped by surrounding pericytes and astrocytes to form the blood-brain barrier (BBB)1,2,3,4.”
From Neurons secrete miR-132-containing exosomes to regulate brain vascular integrity (2017) · cites this paper as [4]
The blood-brain barrier restricts material exchange between the brain and blood vessels to maintain homeostasis of the brain microenvironment.
“The BBB restricts material exchange between the brain and blood vessels to maintain the homeostasis of the brain microenvironment, which is crucial for the normal development and function of the central nervous system (CNS)1,2,3,4.”
From Neurons secrete miR-132-containing exosomes to regulate brain vascular integrity (2017) · cites this paper as [4]
Wnt and Sonic Hedgehog pathways were found to be implicated in neural regulation of brain vasculature.
“several signaling pathways, in particular the Wnt and Sonic Hedgehog (Shh) pathways, were found to be implicated in this neural regulation4,5.”
From Neurons secrete miR-132-containing exosomes to regulate brain vascular integrity (2017) · cites this paper as [4]

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Microvascular protection is essential for successful neuroprotection in stroke
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Neurological autoimmunity targeting aquaporin-4
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The Potential of Mesenchymal Stromal Cells as a Novel Cellular Therapy for Multiple Sclerosis
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Blood—Brain Barrier Disruption is More Severe in Neuromyelitis Optica than in Multiple Sclerosis and Correlates with Clinical Disability
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Targeting metabolic inflammation in Parkinson’s disease: Implications for prospective therapeutic strategies
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Effector Functions of Antiaquaporin‐4 Autoantibodies in Neuromyelitis Optica
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Reactive Oxygen Species (ROS)-Based Nanomedicine
Yang, B., Chen, Y., & Shi, J. (2019) · Chemical Reviews · doi:10.1021/acs.chemrev.8b00626 · Cited by 2,453 · see citing works
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 2,294 · see citing works
The blood–brain barrier: Structure, regulation and drug delivery
Wu, D., Chen, Q., Chen, X., Han, F., Chen, Z., & Wang, Y. (2023) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-023-01481-w · Cited by 1,906 · see citing works
“The integrity of BBB could be breached by the intrinsic properties of the pathogens.(232) Directed evolution and capsid engineering have been developed to engineer a number of BBB-crossing AAVs.”
Background
Establishment and Dysfunction of the Blood-Brain Barrier
Zhao, Z., Nelson, A. R., Betsholtz, C., & Zlokovic, B. V. (2015) · Cell · doi:10.1016/j.cell.2015.10.067 · Cited by 1,670 · see citing works
Nanoparticle-mediated brain drug delivery: Overcoming blood–brain barrier to treat neurodegenerative diseases
Saraiva, C., Praça, C., Ferreira, R., Santos, T., Ferreira, L., & Bernardino, L. (2016) · Journal of Controlled Release · doi:10.1016/j.jconrel.2016.05.044 · Cited by 1,609 · see citing works
A polarizing question: do M1 and M2 microglia exist?
Ransohoff, R. M. (2016) · Nature Neuroscience · doi:10.1038/nn.4338 · Cited by 1,573 · see citing works
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Type I interferons and microbial metabolites of tryptophan modulate astrocyte activity and central nervous system inflammation via the aryl hydrocarbon receptor
Rothhammer, V., Mascanfroni, I. D., Bunse, L., Takenaka, M. C., Kenison, J. E., Mayo, L., Chao, C.-C., Patel, B., Yan, R., Blain, M., et al. (2016) · Nature Medicine · doi:10.1038/nm.4106 · Cited by 1,559 · see citing works
Transcriptome-wide isoform-level dysregulation in ASD, schizophrenia, and bipolar disorder
Gandal, M. J., Zhang, P., Hadjimichael, E., Walker, R. L., Chen, C., Liu, S., Won, H., van Bakel, H., Varghese, M., Wang, Y., et al. (2018) · Science · doi:10.1126/science.aat8127 · Cited by 1,247 · see citing works
Overcoming the blood–brain tumor barrier for effective glioblastoma treatment
van Tellingen, O., Yetkin-Arik, B., de Gooijer, M. C., Wesseling, P., Wurdinger, T., & de Vries, H. E. (2015) · Drug Resistance Updates · doi:10.1016/j.drup.2015.02.002 · Cited by 1,035 · see citing works
Astrocyte Crosstalk in CNS Inflammation
Linnerbauer, M., Wheeler, M. A., & Quintana, F. J. (2020) · Neuron · doi:10.1016/j.neuron.2020.08.012 · Cited by 989 · see citing works
Engineering of human brain organoids with a functional vascular-like system
Çakır, B., Xiang, Y., Tanaka, Y., Kural, M. H., Parent, M. J., Kang, Y., Chapeton, K., Patterson, B., Yuan, Y., He, C., et al. (2019) · Nature Methods · doi:10.1038/s41592-019-0586-5 · Cited by 959 · see citing works
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 946 · 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
A human brain vascular atlas reveals diverse mediators of Alzheimer’s risk
Yang, A. C., Vest, R. T., Kern, F., Lee, D. P., Agam, M., Maat, C. A., Losada, P. M., Chen, M. B., Schaum, N., Khoury, N., et al. (2022) · Nature · doi:10.1038/s41586-021-04369-3 · Cited by 797 · see citing works
Organotypic vasculature: From descriptive heterogeneity to functional pathophysiology
Augustin, H. G., & Koh, G. Y. (2017) · Science · doi:10.1126/science.aal2379 · Cited by 762 · see citing works
The blood–brain barrier in health and disease: Important unanswered questions
Profaci, C. P., Munji, R. N., Pulido, R. S., & Daneman, R. (2020) · The Journal of Experimental Medicine · doi:10.1084/jem.20190062 · Cited by 777 · see citing works
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The blood-brain barrier in aging and neurodegeneration
Knox, E. G., Aburto, M. R., Clarke, G., Cryan, J. F., & O’Driscoll, C. M. (2022) · Molecular Psychiatry · doi:10.1038/s41380-022-01511-z · Cited by 738 · see citing works
“The disruption mechanisms of oxidative stress include oxidative damage to cellular components (protein oxidation, lipid peroxidation, and DNA damage), activation of matrix metalloproteinases, cytoskeleton reorganization, modulation of tight junction proteins, and upregulation of inflammatory mediators [81, 86, 87].”
Background
The biphasic function of microglia in ischemic stroke
Ma, Y., Wang, J., Wang, Y., & Yang, G. (2016) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2016.01.005 · Cited by 724 · see citing works
Peripheral inflammation and blood–brain barrier disruption: effects and mechanisms
Huang, X., Hussain, B., & Chang, J. (2020) · CNS Neuroscience & Therapeutics · doi:10.1111/cns.13569 · Cited by 732 · see citing works
3D self-organized microvascular model of the human blood-brain barrier with endothelial cells, pericytes and astrocytes
Campisi, M., Shin, Y., Osaki, T., Hajal, C., Chiono, V., & Kamm, R. D. (2018) · Biomaterials · doi:10.1016/j.biomaterials.2018.07.014 · Cited by 718 · see citing works
Function and therapeutic value of astrocytes in neurological diseases
Lee, H.-G., Wheeler, M. A., & Quintana, F. J. (2022) · Nature Reviews Drug Discovery · doi:10.1038/s41573-022-00390-x · Cited by 662 · see citing works
The role of peripheral immune cells in the CNS in steady state and disease
Prinz, M., & Priller, J. (2017) · Nature Neuroscience · doi:10.1038/nn.4475 · Cited by 657 · see citing works
The dynamic blood–brain barrier
Keaney, J., & Campbell, M. (2015) · The FEBS Journal · doi:10.1111/febs.13412 · Cited by 616 · see citing works
Macrophage exosomes as natural nanocarriers for protein delivery to inflamed brain
Yuan, D., Zhao, Y., Banks, W. A., Bullock, K. M., Haney, M., Batrakova, E., & Kabanov, A. V. (2017) · Biomaterials · doi:10.1016/j.biomaterials.2017.07.011 · Cited by 607 · see citing works
Interaction of Microglia and Astrocytes in the Neurovascular Unit
Liu, L., Liu, J., Bao, J.-S., Bai, Q.-Q., & Wang, G. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.01024 · Cited by 591 · see citing works
Claudin-5: gatekeeper of neurological function
Greene, C., Hanley, N., & Campbell, M. (2019) · Fluids and Barriers of the CNS · doi:10.1186/s12987-019-0123-z · Cited by 583 · see citing works
The impact of microglial activation on blood-brain barrier in brain diseases
da Fonseca, A. C. C., Matias, D., Garcia, C., Amaral, R., Geraldo, L. H., Freitas, C., & Lima, F. R. S. (2014) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2014.00362 · Cited by 572 · see citing works
A combination of ontogeny and CNS environment establishes microglial identity
Bennett, F. C., Bennett, M. L., Yaqoob, F., Mulinyawe, S. B., Grant, G. A., Hayden Gephart, M., Plowey, E. D., & Barres, B. A. (2018) · Neuron · doi:10.1016/j.neuron.2018.05.014 · Cited by 524 · see citing works
Neutrophil extracellular traps released by neutrophils impair revascularization and vascular remodeling after stroke
Kang, L., Yu, H., Yang, X., Zhu, Y., Bai, X., Wang, R., Cao, Y., Xu, H., Luo, H., Lu, L., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-16191-y · Cited by 546 · see citing works
Elucidation of Exosome Migration Across the Blood–Brain Barrier Model In Vitro
Chen, C. C., Liu, L., Ma, F., Wong, C. W., Guo, X. E., Chacko, J. V., Farhoodi, H. P., Zhang, S. X., Zimak, J., Ségaliny, A., et al. (2016) · Cellular and Molecular Bioengineering · doi:10.1007/s12195-016-0458-3 · Cited by 537 · see citing works
Immunomodulation by endothelial cells — partnering up with the immune system?
Amersfoort, J., Eelen, G., & Carmeliet, P. (2022) · Nature reviews. Immunology · doi:10.1038/s41577-022-00694-4 · Cited by 549 · see citing works
Biomarkers of traumatic injury are transported from brain to blood via the glymphatic system.
Plog, B. A., Dashnaw, M. L., Hitomi, E., Peng, W., Liao, Y., Lou, N., Deane, R., & Nedergaard, M. (2015) · The Journal of Neuroscience · doi:10.1523/jneurosci.3742-14.2015 · Cited by 525 · see citing works
Gut microbiota and dysbiosis in Alzheimer's disease: Implications for pathogenesis and treatment
Liu, S., Gao, J., Zhu, M., Liu, K., & Zhang, H.-L. (2020) · Molecular Neurobiology · doi:10.1007/s12035-020-02073-3 · Cited by 516 · see citing works
Engineering mesoporous silica nanoparticles for drug delivery: where are we after two decades?
Vallet‐Regí, M., Schüth, F., Lozano, D., Colilla, M., & Manzano, M. (2022) · Chemical Society Reviews · doi:10.1039/d1cs00659b · Cited by 524 · see citing works
Physiological blood–brain transport is impaired with age by a shift in transcytosis
Yang, A. C., Stevens, M. Y., Chen, M. B., Lee, D. P., Stähli, D., Gate, D., Contrepois, K., Chen, W., Iram, T., Zhang, L., et al. (2020) · Nature · doi:10.1038/s41586-020-2453-z · Cited by 477 · see citing works
Crossing the Blood-Brain Barrier: Advances in Nanoparticle Technology for Drug Delivery in Neuro-Oncology
Hersh, A. M., Alomari, S., & Tyler, B. M. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23084153 · Cited by 478 · see citing works
Microbiome–microglia connections via the gut–brain axis
Abdel-Haq, R., Schlachetzki, J. C. M., Glass, C. K., & Mazmanian, S. K. (2019) · Journal of Experimental Medicine · doi:10.1084/jem.20180794 · Cited by 471 · see citing works
“This process of brain colonization precedes the formation of the BBB, which eventually shields microglia from potentially toxic peripheral influences throughout both fetal development and adulthood (Obermeier et al., 2013).”
Background
Biodistribution, Clearance, and Long‐Term Fate of Clinically Relevant Nanomaterials
Bourquin, J., Milosevic, A. M., Hauser, D., Lehner, R., Blank, F., Petri‐Fink, A., & Rothen‐Rutishauser, B. (2018) · Advanced Materials · doi:10.1002/adma.201704307 · Cited by 470 · see citing works
Microbiota-derived metabolites as drivers of gut–brain communication
Ahmed, H., Leyrolle, Q., Koistinen, V., Kärkkäinen, O., Layé, S., Delzenne, N., & Hanhineva, K. (2022) · Gut Microbes · doi:10.1080/19490976.2022.2102878 · Cited by 462 · see citing works
Blood–brain barrier shuttle peptides: an emerging paradigm for brain delivery
Oller‐Salvia, B., Sánchez‐Navarro, M., Giralt, E., & Teixidò, M. (2016) · Chemical Society Reviews · doi:10.1039/c6cs00076b · Cited by 443 · see citing works
Aged blood impairs hippocampal neural precursor activity and activates microglia via brain endothelial cell VCAM1
Yousef, H., Czupalla, C. J., Lee, D., Chen, M. B., Burke, A. N., Zera, K. A., Zandstra, J., Berber, E., Lehallier, B., Mathur, V., et al. (2019) · Nature Medicine · doi:10.1038/s41591-019-0440-4 · Cited by 442 · see citing works
Neuronal regulation of the blood–brain barrier and neurovascular coupling
Kaplan, L., Chow, B. W., & Gu, C. (2020) · Nature reviews. Neuroscience · doi:10.1038/s41583-020-0322-2 · Cited by 431 · see citing works
Gut Microbiota Interact With the Brain Through Systemic Chronic Inflammation: Implications on Neuroinflammation, Neurodegeneration, and Aging
Mou, Y., Du, Y., Zhou, L., Yue, J., Hu, X., Liu, Y., Chen, S., Lin, X., Zhang, G., Xiao, H., et al. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.796288 · Cited by 432 · see citing works
Surface-Engineered Dendrimers in Gene Delivery
Jiepin, Y., Zhang, Q., Chang, H., & Cheng, Y. (2015) · Chemical Reviews · doi:10.1021/cr500542t · Cited by 432 · see citing works
Age-associated Physiological and Pathological Changes at the Blood-Brain Barrier: A Review
Erdő, F., Denes, L., & de Lange, E. (2017) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1177/0271678x16679420 · Cited by 426 · see citing works
The progress of gut microbiome research related to brain disorders
Zhu, S., Jiang, Y., Xu, K., Cui, M., Ye, W., Zhao, G., Jin, L., & Chen, X. (2020) · Journal of Neuroinflammation · doi:10.1186/s12974-020-1705-z · Cited by 419 · see citing works
Magnetic hyperthermia therapy for the treatment of glioblastoma: a review of the therapy’s history, efficacy and application in humans
Mahmoudi, K., Bouras, A., Bozec, D., Ivkov, R., & Hadjipanayis, C. G. (2018) · International Journal of Hyperthermia · doi:10.1080/02656736.2018.1430867 · Cited by 417 · see citing works
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Authors: Obermeier, B., Daneman, R., & Ransohoff, R. M.
Affiliations: Cleveland Clinic (US)
University of California, San Francisco (US)
Corresponding author: Ransohoff, Richard M
ORCID: Obermeier, Birgit
Daneman, Richard
Ransohoff, Richard M
Venue: Nature Medicine
Publisher: Springer Science and Business Media LLC
Published: 2013-12
Volume: 19
Issue: 12
Pages: 1584-1596
ISSN: 1078-8956 (ISSN-L)
1546-170X
DOI: 10.1038/nm.3407
PMC: PMC4080800
OpenAlex: W1995037165
Cited by: 2,452
References: 180
Citations by year: 2026: 168 · 2025: 256 · 2024: 264 · 2023: 254 · 2022: 271 · 2021: 251 · 2020: 224 · 2019: 181 · 2018: 172 · 2017: 159 · 2016: 108 · 2015: 91 · 2014: 52
FWCI: 8.07
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springer.com/tdm (tdm)
www.springer.com/tdm (vor)
Locations: Nature Medicine (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: National Institute of Neurological Disorders and Stroke (R21NS074820, K24NS051400)
Topics: Life Sciences › Neuroscience › Neurology › Barrier Structure and Function Studies
Health Sciences › Medicine › Oncology › Drug Transport and Resistance Mechanisms
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Cerebrospinal fluid and hydrocephalus
Keywords: blood-brain barrier, blood-brain barrier disruption, brain homeostasis, BBB repair, neuroinflammation, neurodegeneration, blood-brain barrier permeability, neurological disorders
MeSH terms: Animals, Blood Vessels, Blood-Brain Barrier, Brain, Humans, Nervous System Diseases, Neovascularization, Physiologic, Vascular Endothelial Growth Factor A, Wnt Signaling Pathway

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