Blood-Brain Barrier Alterations and Edema Formation in Different Brain Mass Lesions
Status PubMed-not-MEDLINE Language English Country Switzerland Media electronic-ecollection
Document type Journal Article, Review
PubMed
35910247
PubMed Central
PMC9334679
DOI
10.3389/fncel.2022.922181
Knihovny.cz E-resources
- Keywords
- blood-brain barrier, brain abscess, brain edema, brain lymphoma, brain metastasis, glioblastoma multiforme,
- Publication type
- Journal Article MeSH
- Review MeSH
Differential diagnosis of brain lesion pathologies is complex, but it is nevertheless crucial for appropriate clinical management. Advanced imaging methods, including diffusion-weighted imaging and apparent diffusion coefficient, can help discriminate between brain mass lesions such as glioblastoma, brain metastasis, brain abscesses as well as brain lymphomas. These pathologies are characterized by blood-brain barrier alterations and have been extensively studied. However, the changes in the blood-brain barrier that are observed around brain pathologies and that contribute to the development of vasogenic brain edema are not well described. Some infiltrative brain pathologies such as glioblastoma are characterized by glioma cell infiltration in the brain tissue around the tumor mass and thus affect the nature of the vasogenic edema. Interestingly, a common feature of primary and secondary brain tumors or tumor-like brain lesions characterized by vasogenic brain edema is the formation of various molecules that lead to alterations of tight junctions and result in blood-brain barrier damage. The resulting vasogenic edema, especially blood-brain barrier disruption, can be visualized using advanced magnetic resonance imaging techniques, such as diffusion-weighted imaging and apparent diffusion coefficient. This review presents a comprehensive overview of blood-brain barrier changes contributing to the development of vasogenic brain edema around glioblastoma, brain metastases, lymphomas, and abscesses.
1st Department of Pathology St Anne's University Hospital Brno Czechia
Department of Neurosurgery St Anne's University Hospital Brno Czechia
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Abbott N. J., Rönnbäck L., Hansson E. (2006). Astrocyte-endothelial interactions at the blood-brain barrier. Nat. Rev. Neurosci. 7 41–53. 10.1038/nrn1824 PubMed DOI
Ahir B. K., Engelhard H. H., Lakka S. S. (2020). Tumor Development and Angiogenesis in Adult Brain Tumor: glioblastoma. Mol. Neurobiol. 57 2461–2478. 10.1007/s12035-020-01892-8 PubMed DOI PMC
Aho R., Ekfors T., Haltia M., Kalimo H. (1993). Pathogenesis of primary central nervous system lymphoma: invasion of malignant lymphoid cells into and within the brain parenchyme. Acta Neuropathol. 86 71–76. 10.1007/BF00454901 PubMed DOI
Allt G., Lawrenson J. G. (2001). Pericytes: cell biology and pathology. Cells Tissues Organs 169 1–11. 10.1159/000047855 PubMed DOI
Almiron Bonnin D. A., Havrda M. C., Lee M. C., Liu H., Zhang Z., Nguyen L. N., et al. (2018). Secretion-mediated STAT3 activation promotes self-renewal of glioma stem-like cells during hypoxia. Oncogene 37 1107–1118. 10.1038/onc.2017.404 PubMed DOI PMC
Ampawong S., Luplertlop N. (2019). Experimental Scedosporiosis Induces Cerebral Oedema Associated with Abscess regarding Aquaporin-4 and Nrf-2 Depletions. Biomed. Res. Int. 2019:6076571. 10.1155/2019/6076571 PubMed DOI PMC
Angara K., Borin T. F., Arbab A. S. (2017). Vascular Mimicry: a Novel Neovascularization Mechanism Driving Anti-Angiogenic Therapy (AAT) Resistance in Glioblastoma. Transl. Oncol. 10 650–660. 10.1016/j.tranon.2017.04.007 PubMed DOI PMC
Apte R. S., Chen D. S., Ferrara N. (2019). VEGF in Signaling and Disease: beyond Discovery and Development. Cell 176 1248–1264. 10.1016/j.cell.2019.01.021 PubMed DOI PMC
Archie S. R., Al Shoyaib A., Cucullo L. (2021). Blood-Brain Barrier Dysfunction in CNS Disorders and Putative Therapeutic Targets: an Overview. Pharmaceutics 13:1779. 10.3390/pharmaceutics13111779 PubMed DOI PMC
Argaw A. T., Gurfein B. T., Zhang Y., Zameer A., John G. R. (2009). VEGF-mediated disruption of endothelial CLN-5 promotes blood-brain barrier breakdown. Proc. Natl. Acad. Sci. U S A 106 1977–1982. 10.1073/pnas.0808698106 PubMed DOI PMC
Armulik A., Genové G., Betsholtz C. (2011). Pericytes: developmental, physiological, and pathological perspectives, problems, and promises. Dev. Cell 21 193–215. 10.1016/j.devcel.2011.07.001 PubMed DOI
Arvanitis C. D., Ferraro G. B., Jain R. K. (2020). The blood-brain barrier and blood-tumour barrier in brain tumours and metastases. Nat. Rev. Cancer 20 26–41. 10.1038/s41568-019-0205-x PubMed DOI PMC
Atzori M. G., Tentori L., Ruffini F., Ceci C., Lisi L., Bonanno E., et al. (2017). The anti-vascular endothelial growth factor receptor-1 monoclonal antibody D16F7 inhibits invasiveness of human glioblastoma and glioblastoma stem cells. J. Exp. Clin. Cancer Res. 36:106. 10.1186/s13046-017-0577-2 PubMed DOI PMC
Aurrand-Lions M., Johnson-Leger C., Wong C., Du Pasquier L., Imhof B. A. (2001). Heterogeneity of endothelial junctions is reflected by differential expression and specific subcellular localization of the three JAM family members. Blood 98 3699–3707. 10.1182/blood.v98.13.3699 PubMed DOI
Badaut J., Ashwal S., Obenaus A. (2011). Aquaporins in cerebrovascular disease: a target for treatment of brain edema? Cerebrovasc. Dis. 31 521–531. 10.1159/000324328 PubMed DOI PMC
Baldwin A. C., Kielian T. (2004). Persistent immune activation associated with a mouse model of Staphylococcus aureus-induced experimental brain abscess. J. Neuroimmunol. 151 24–32. 10.1016/j.jneuroim.2004.02.002 PubMed DOI
Ballabh P., Braun A., Nedergaard M. (2004). The blood-brain barrier: an overview: structure, regulation, and clinical implications. Neurobiol. Dis. 16 1–13. 10.1016/j.nbd.2003.12.016 PubMed DOI
Begley D. J., Brightman M. W. (2003). ““Structural and functional aspects of the blood-brain barrier,”,” in Peptide Transport and Delivery into the Central Nervous System Progress in Drug Research, eds Prokai L., Prokai-Tatrai K. (Basel: Birkhäuser; ), 39–78. 10.1007/978-3-0348-8049-7_2 PubMed DOI
Berghoff A. S., Fuchs E., Ricken G., Mlecnik B., Bindea G., Spanberger T., et al. (2016). Density of tumor-infiltrating lymphocytes correlates with extent of brain edema and overall survival time in patients with brain metastases. Oncoimmunology 5:e1057388. 10.1080/2162402X.2015.1057388 PubMed DOI PMC
Berghoff A. S., Rajky O., Winkler F., Bartsch R., Furtner J., Hainfellner J. A., et al. (2013). Invasion patterns in brain metastases of solid cancers. Neuro. Oncol. 15 1664–1672. 10.1093/neuonc/not112 PubMed DOI PMC
Birner P., Piribauer M., Fischer I., Gatterbauer B., Marosi C., Ambros P. F., et al. (2003). Vascular patterns in glioblastoma influence clinical outcome and associate with variable expression of angiogenic proteins: evidence for distinct angiogenic subtypes. Brain Pathol. 13 133–143. 10.1111/j.1750-3639.2003.tb00013.x PubMed DOI PMC
Bloch O., Papadopoulos M. C., Manley G. T., Verkman A. S. (2005). Aquaporin-4 gene deletion in mice increases focal edema associated with staphylococcal brain abscess. J. Neurochem. 95 254–262. 10.1111/j.1471-4159.2005.03362.x PubMed DOI
Brantley E. C., Nabors L. B., Gillespie G. Y., Choi Y.-H., Palmer C. A., Harrison K., et al. (2008). Loss of PIAS3 Expression in Glioblastoma Multiforme Tumors: implications for STAT-3 Activation and Gene Expression. Clin. Cancer Res. 14 4694–4704. 10.1158/1078-0432.CCR-08-0618 PubMed DOI PMC
Broholm H., Rubin I., Kruse A., Braendstrup O., Schmidt K., Skriver E. B., et al. (2003). Nitric oxide synthase expression and enzymatic activity in human brain tumors. Clin. Neuropathol. 22 273–281. PubMed
Buonfiglioli A., Hambardzumyan D. (2021). Macrophages and microglia: the cerberus of glioblastoma. Acta Neuropathol. Commun. 9:54. 10.1186/s40478-021-01156-z PubMed DOI PMC
Calimeri T., Marcucci F., Corti A. (2021). Overcoming the blood-brain barrier in primary central nervous system lymphoma: a review on new strategies to solve an old problem. Ann. Lymphoma 5 10.21037/aol-20-54 DOI
Carlson M. R. J., Pope W. B., Horvath S., Braunstein J. G., Nghiemphu P., Tso C.-L., et al. (2007). Relationship between survival and edema in malignant gliomas: role of vascular endothelial growth factor and neuronal pentraxin 2. Clin. Cancer Res. 13 2592–2598. 10.1158/1078-0432.CCR-06-2772 PubMed DOI
Chen L., Lin Z.-X., Lin G.-S., Zhou C.-F., Chen Y.-P., Wang X.-F., et al. (2015). Classification of microvascular patterns via cluster analysis reveals their prognostic significance in glioblastoma. Hum. Pathol. 46 120–128. 10.1016/j.humpath.2014.10.002 PubMed DOI
Chen Z., Herting C. J., Ross J. L., Gabanic B., Puigdelloses Vallcorba M., Szulzewsky F., et al. (2020). Genetic driver mutations introduced in identical cell-of-origin in murine glioblastoma reveal distinct immune landscapes but similar response to checkpoint blockade. Glia 68 2148–2166. 10.1002/glia.23883 PubMed DOI PMC
Chi O. Z., Liu X., Weiss H. R. (1999). Effects of cyclic GMP on microvascular permeability of the cerebral cortex. Microvasc. Res. 58 35–40. 10.1006/mvre.1999.2152 PubMed DOI
Coureuil M., Lécuyer H., Bourdoulous S., Nassif X. (2017). A journey into the brain: insight into how bacterial pathogens cross blood-brain barriers. Nat. Rev. Microbiol. 15 149–159. 10.1038/nrmicro.2016.178 PubMed DOI
Cramer S. P., Larsson H. B. (2014). Accurate Determination of Blood–Brain Barrier Permeability Using Dynamic Contrast-Enhanced T1-Weighted MRI: a Simulation and in vivo Study on Healthy Subjects and Multiple Sclerosis Patients. J. Cereb. Blood Flow Metab. 34 1655–1665. 10.1038/jcbfm.2014.126 PubMed DOI PMC
Dahlberg D., Ivanovic J., Hassel B. (2016). Toxic levels of ammonia in human brain abscess. J. Neurosurg. 124 854–860. 10.3171/2015.1.JNS142582 PubMed DOI
Dahlberg D., Mariussen E., Goverud I. L., Tønjum T., Mæhlen J., Antal E.-A., et al. (2015b). Staphylococcal α-hemolysin is neurotoxic and causes lysis of brain cells in vivo and in vitro. Neurotoxicology 48 61–67. 10.1016/j.neuro.2015.03.001 PubMed DOI
Dahlberg D., Ivanovic J., Mariussen E., Hassel B. (2015a). High extracellular levels of potassium and trace metals in human brain abscess. Neurochem. Int. 82 28–32. 10.1016/j.neuint.2015.02.003 PubMed DOI
Dalby T., Wohl E., Dinsmore M., Unger Z., Chowdhury T., Venkatraghavan L. (2021). Pathophysiology of Cerebral Edema—A Comprehensive Review. J. Neuroanaesth. Crit. Care 08 163–172. 10.1055/s-0040-1721165 DOI
Davies D. C. (2002). Blood-brain barrier breakdown in septic encephalopathy and brain tumours. J. Anat. 200 639–646. 10.1046/j.1469-7580.2002.00065.x PubMed DOI PMC
Del Zoppo G. J., Milner R., Mabuchi T., Hung S., Wang X., Koziol J. A. (2006). Vascular matrix adhesion and the blood-brain barrier. Biochem. Soc. Trans. 34 1261–1266. 10.1042/BST0341261 PubMed DOI
Díaz-Flores L., Gutiérrez R., González-Gómez M., García M.-D.-P., Díaz-Flores L., González-Marrero I., et al. (2021). Disproportion in Pericyte/Endothelial Cell Proliferation and Mechanisms of Intussusceptive Angiogenesis Participate in Bizarre Vessel Formation in Glioblastoma. Cells 10:2625. 10.3390/cells10102625 PubMed DOI PMC
Dobrogowska D. H., Lossinsky A. S., Tarnawski M., Vorbrodt A. W. (1998). Increased blood-brain barrier permeability and endothelial abnormalities induced by vascular endothelial growth factor. J. Neurocytol. 27 163–173. 10.1023/a:1006907608230 PubMed DOI
Dore-Duffy P., LaManna J. C. (2007). Physiologic angiodynamics in the brain. Antioxid. Redox Signal 9 1363–1371. 10.1089/ars.2007.1713 PubMed DOI
Edwards D. N., Bix G. J. (2019). Roles of blood-brain barrier integrins and extracellular matrix in stroke. Am. J. Physiol.-Cell Physiol. 316 C252–C263. 10.1152/ajpcell.00151.2018 PubMed DOI PMC
Engelhardt B., Sorokin L. (2009). The blood-brain and the blood-cerebrospinal fluid barriers: function and dysfunction. Semin. Immunopathol. 31 497–511. 10.1007/s00281-009-0177-0 PubMed DOI
Esen N., Tanga F. Y., DeLeo J. A., Kielian T. (2004). Toll-like receptor 2 (TLR2) mediates astrocyte activation in response to the Gram-positive bacterium Staphylococcus aureus. J. Neurochem. 88 746–758. 10.1046/j.1471-4159.2003.02202.x PubMed DOI
Fernández-Cortés M., Delgado-Bellido D., Oliver F. J. (2019). Vasculogenic Mimicry: become an Endothelial Cell “But Not So Much.”. Front. Oncol. 9:803. 10.3389/fonc.2019.00803 PubMed DOI PMC
Fitzgerald D. P., Palmieri D., Hua E., Hargrave E., Herring J. M., Qian Y., et al. (2008). Reactive glia are recruited by highly proliferative brain metastases of breast cancer and promote tumor cell colonization. Clin. Exp. Metastasis 25 799–810. 10.1007/s10585-008-9193-z PubMed DOI PMC
Gabrusiewicz K., Ellert-Miklaszewska A., Lipko M., Sielska M., Frankowska M., Kaminska B. (2011). Characteristics of the alternative phenotype of microglia/macrophages and its modulation in experimental gliomas. PLoS One 6:e23902. 10.1371/journal.pone.0023902 PubMed DOI PMC
Gorelick P. B., Furie K. L., Iadecola C., Smith E. E., Waddy S. P., Lloyd-Jones D. M., et al. (2017). Defining Optimal Brain Health in Adults: a Presidential Advisory From the American Heart Association/American Stroke Association. Stroke 48:e284–e303. 10.1161/STR.0000000000000148 PubMed DOI PMC
Greenberg D. A., Jin K. (2005). From angiogenesis to neuropathology. Nature 438 954–959. 10.1038/nature04481 PubMed DOI
Guzman R., Altrichter S., El-Koussy M., Gralla J., Weis J., Barth A., et al. (2008). Contribution of the apparent diffusion coefficient in perilesional edema for the assessment of brain tumors. J. Neuroradiol. 35 224–229. 10.1016/j.neurad.2008.02.003 PubMed DOI
Hambardzumyan D., Gutmann D. H., Kettenmann H. (2016). The role of microglia and macrophages in glioma maintenance and progression. Nat. Neurosci. 19 20–27. 10.1038/nn.4185 PubMed DOI PMC
Han J., Alvarez-Breckenridge C. A., Wang Q.-E., Yu J. (2015). TGF-β signaling and its targeting for glioma treatment. Am. J. Cancer Res. 5 945–955. PubMed PMC
Hashimoto Y., Campbell M. (2020). Tight junction modulation at the blood-brain barrier: current and future perspectives. Biochim. Biophys. Acta Biomembr. 1862:183298. 10.1016/j.bbamem.2020.183298 PubMed DOI
Hassel B., Dahlberg D., Mariussen E., Goverud I. L., Antal E.-A., Tønjum T., et al. (2014). Brain infection with Staphylococcus aureus leads to high extracellular levels of glutamate, aspartate, γ-aminobutyric acid, and zinc. J. Neurosci. Res. 92 1792–1800. 10.1002/jnr.23444 PubMed DOI
Hawkins B. T., Davis T. P. (2005). The blood-brain barrier/neurovascular unit in health and disease. Pharmacol. Rev. 57 173–185. 10.1124/pr.57.2.4 PubMed DOI
Herting C. J., Chen Z., Maximov V., Duffy A., Szulzewsky F., Shayakhmetov D. M., et al. (2019). Tumour-associated macrophage-derived interleukin-1 mediates glioblastoma-associated cerebral oedema. Brain 142 3834–3851. 10.1093/brain/awz331 PubMed DOI PMC
Holley M. M., Kielian T. (2012). Th1 and Th17 cells regulate innate immune responses and bacterial clearance during central nervous system infection. J. Immunol. 188 1360–1370. 10.4049/jimmunol.1101660 PubMed DOI PMC
Hood J. D., Frausto R., Kiosses W. B., Schwartz M. A., Cheresh D. A. (2003). Differential αv integrin–mediated Ras-ERK signaling during two pathways of angiogenesis. J. Cell Biol. 162 933–943. 10.1083/jcb.200304105 PubMed DOI PMC
Hubbard J. A., Szu J. I., Binder D. K. (2018). The role of aquaporin-4 in synaptic plasticity, memory and disease. Brain Res. Bull. 136 118–129. 10.1016/j.brainresbull.2017.02.011 PubMed DOI
Iorio-Morin C., Gahide G., Morin C., Vanderweyen D., Roy M.-A., St-Pierre I., et al. (2020). Management of Primary Central Nervous System Lymphoma Using Intra-Arterial Chemotherapy With Osmotic Blood-Brain Barrier Disruption: retrospective Analysis of the Sherbrooke Cohort. Front. Oncol. 10:543648. 10.3389/fonc.2020.543648 PubMed DOI PMC
Ishihara H., Kubota H., Lindberg R. L. P., Leppert D., Gloor S. M., Errede M., et al. (2008). Endothelial Cell Barrier Impairment Induced by Glioblastomas and Transforming Growth Factor β2 Involves Matrix Metalloproteinases and Tight Junction Proteins. J. Neuropathol. Exp. Neurol. 67 435–448. 10.1097/NEN.0b013e31816fd622 PubMed DOI
Kang E. J., Major S., Jorks D., Reiffurth C., Offenhauser N., Friedman A., et al. (2013). Blood-brain barrier opening to large molecules does not imply blood-brain barrier opening to small ions. Neurobiol. Dis. 52 204–218. 10.1016/j.nbd.2012.12.007 PubMed DOI
Karnati H. K., Panigrahi M., Shaik N. A., Greig N. H., Bagadi S. A. R., Kamal M., et al. (2014). Down Regulated Expression of Claudin-1 and Claudin-5 and Up Regulation of B-Catenin: association with Human Glioma Progression. CNS Neurol. Disord. Drug Targets 13 1413–1426. 10.2174/1871527313666141023121550 PubMed DOI PMC
Keaney J., Campbell M. (2015). The dynamic blood-brain barrier. FEBS J. 282 4067–4079. 10.1111/febs.13412 PubMed DOI
Kickingereder P., Sahm F., Wiestler B., Roethke M., Heiland S., Schlemmer H.-P., et al. (2014). Evaluation of microvascular permeability with dynamic contrast-enhanced MRI for the differentiation of primary CNS lymphoma and glioblastoma: radiologic-pathologic correlation. AJNR Am. J. Neuroradiol. 35 1503–1508. 10.3174/ajnr.A3915 PubMed DOI PMC
Kielian T. (2004). Immunopathogenesis of brain abscess. J. Neuroinflamm. 1:16. 10.1186/1742-2094-1-16 PubMed DOI PMC
Kielian T., Barry B., Hickey W. F. (2001). CXC chemokine receptor-2 ligands are required for neutrophil-mediated host defense in experimental brain abscesses. J. Immunol. 166 4634–4643. 10.4049/jimmunol.166.7.4634 PubMed DOI
Kielian T., Esen N., Bearden E. D. (2005a). Toll-like receptor 2 (TLR2) is pivotal for recognition of S. aureus peptidoglycan but not intact bacteria by microglia. Glia 49 567–576. 10.1002/glia.20144 PubMed DOI PMC
Kielian T., Haney A., Mayes P. M., Garg S., Esen N. (2005b). Toll-like receptor 2 modulates the pro-inflammatory milieu in Staphylococcus aureus-induced brain abscess. Infect. Immun. 73 7428–7435. 10.1128/IAI.73.11.7428-7435.2005 PubMed DOI PMC
Kielian T., Phulwani N. K., Esen N., Syed M., Md, Haney A. C., McCastlain K., et al. (2007). MyD88-Dependent Signals Are Essential for the Host Immune Response in Experimental Brain Abscess. J. Immunol. 178 4528–4537. 10.4049/jimmunol.178.7.4528 PubMed DOI PMC
Kim J.-E., Ryu H. J., Kang T.-C. (2013). Status Epilepticus Induces Vasogenic Edema via Tumor Necrosis Factor-α/ Endothelin-1-Mediated Two Different Pathways. PLoS One 8:e74458. 10.1371/journal.pone.0074458 PubMed DOI PMC
Kim J. Y., Ko A.-R., Hyun H.-W., Kang T.-C. (2015). ETB receptor-mediated MMP-9 activation induces vasogenic edema via ZO-1 protein degradation following status epilepticus. Neuroscience 304 355–367. 10.1016/j.neuroscience.2015.07.065 PubMed DOI
Klimas A., Drzazga Z., Kluczewska E., Hartel M. (2013). Regional ADC measurements during normal brain aging in the clinical range of b values: a DWI study. Clin. Imaging 37 637–644. 10.1016/j.clinimag.2013.01.013 PubMed DOI
Krebs S., Barasch J. G., Young R. J., Grommes C., Schöder H. (2021). Positron emission tomography and magnetic resonance imaging in primary central nervous system lymphoma-a narrative review. Ann. Lymph. 5:15. 10.21037/aol-20-52 PubMed DOI PMC
Kummer D., Ebnet K. (2018). Junctional Adhesion Molecules (JAMs): the JAM-Integrin Connection. Cells 7:E25. 10.3390/cells7040025 PubMed DOI PMC
Lai R., Rosenblum M. K., DeAngelis L. M. (2002). Primary CNS lymphoma: a whole-brain disease? Neurology 59 1557–1562. 10.1212/01.wnl.0000034256.20173.ea PubMed DOI
Lakomy R., Kazda T., Selingerova I., Poprach A., Pospisil P., Belanova R., et al. (2020). Real-World Evidence in Glioblastoma: stupp’s Regimen After a Decade. Front. Oncol. 10:840. 10.3389/fonc.2020.00840 PubMed DOI PMC
Lan Y.-L., Wang X., Lou J.-C., Ma X.-C., Zhang B. (2017). The potential roles of aquaporin 4 in malignant gliomas. Oncotarget 8 32345–32355. 10.18632/oncotarget.16017 PubMed DOI PMC
Leinonen V., Vanninen R., Rauramaa T. (2018). ““Chapter 4 - Raised intracranial pressure and brain edema,”,” in Handbook of Clinical Neurology Neuropathology, eds Kovacs G. G., Alafuzoff I. (Amsterdam: Elsevier; ), 25–37. 10.1016/B978-0-12-802395-2.00004-3 PubMed DOI
Li W., Chen Z., Chin I., Chen Z., Dai H. (2018). The Role of VE-cadherin in Blood-brain Barrier Integrity Under Central Nervous System Pathological Conditions. Curr. Neuropharmacol. 16 1375–1384. 10.2174/1570159X16666180222164809 PubMed DOI PMC
Liebner S., Fischmann A., Rascher G., Duffner F., Grote E. H., Kalbacher H., et al. (2000). Claudin-1 and claudin-5 expression and tight junction morphology are altered in blood vessels of human glioblastoma multiforme. Acta Neuropathol. 100 323–331. 10.1007/s004010000180 PubMed DOI
Lin C., McGough R., Aswad B., Block J. A., Terek R. (2004). Hypoxia induces HIF-1alpha and VEGF expression in chondrosarcoma cells and chondrocytes. J. Orthop. Res. 22 1175–1181. 10.1016/j.orthres.2004.03.002 PubMed DOI
Lin G.-S., Chen Y.-P., Lin Z.-X., Wang X.-F., Zheng Z.-Q., Chen L. (2014). STAT3 serine 727 phosphorylation influences clinical outcome in glioblastoma. Int. J. Clin. Exp. Pathol. 7 3141–3149. PubMed PMC
Lin Z. X., Yang L. J., Huang Q., Lin J. H., Ren J., Chen Z. B., et al. (2008). Inhibition of tumor-induced edema by antisense VEGF is mediated by suppressive vesiculo-vacuolar organelles (VVO) formation. Cancer Sci. 99 2540–2546. 10.1111/j.1349-7006.2008.00974.x PubMed DOI PMC
Liu X., Zhang Q., Mu Y., Zhang X., Sai K., Pang J. C.-S., et al. (2011). Clinical significance of vasculogenic mimicry in human gliomas. J. Neurooncol. 105 173–179. 10.1007/s11060-011-0578-5 PubMed DOI PMC
Lo W. D., Wolny A., Boesel C. (1994). Blood-brain barrier permeability in staphylococcal cerebritis and early brain abscess. J. Neurosurg. 80 897–905. 10.3171/jns.1994.80.5.0897 PubMed DOI
Loeffler S., Fayard B., Weis J., Weissenberger J. (2005). Interleukin-6 induces transcriptional activation of vascular endothelial growth factor (VEGF) in astrocytes in vivo and regulates VEGF promoter activity in glioblastoma cells via direct interaction between STAT3 and Sp1. Int. J. Cancer 115 202–213. 10.1002/ijc.20871 PubMed DOI
Machein M. R., Kullmer J., Fiebich B. L., Plate K. H., Warnke P. C. (1999). Vascular endothelial growth factor expression, vascular volume, and, capillary permeability in human brain tumors. Neurosurgery 44 732–740. 10.1097/00006123-199904000-00022 PubMed DOI
Mak K. M., Mei R. (2017). Basement Membrane Type IV Collagen and Laminin: an Overview of Their Biology and Value as Fibrosis Biomarkers of Liver Disease. Anat. Rec. 300 1371–1390. 10.1002/ar.23567 PubMed DOI
Marcelis L., Antoranz A., Delsupehe A.-M., Biesemans P., Ferreiro J. F., Debackere K., et al. (2020). In-depth characterization of the tumor microenvironment in central nervous system lymphoma reveals implications for immune-checkpoint therapy. Cancer Immunol. Immunother. 69 1751–1766. 10.1007/s00262-020-02575-y PubMed DOI PMC
Mathisen G. E., Johnson J. P. (1997). Brain abscess. Clin. Infect. Dis. 25 763–779. 10.1086/515541 PubMed DOI
Mayhan W. G. (1999). VEGF increases permeability of the blood-brain barrier via a nitric oxide synthase/cGMP-dependent pathway. Am. J. Physiol. 276 C1148–C1153. 10.1152/ajpcell.1999.276.5.C1148 PubMed DOI
Maza S., Kiewe P., Munz D. L., Korfel A., Hamm B., Jahnke K., et al. (2009). First report on a prospective trial with yttrium-90-labeled ibritumomab tiuxetan (Zevalin) in primary CNS lymphoma. Neuro. Oncol. 11 423–429. 10.1215/15228517-2008-108 PubMed DOI PMC
Mei X., Chen Y.-S., Zhang Q.-P., Chen F.-R., Xi S.-Y., Long Y.-K., et al. (2020). Association between glioblastoma cell-derived vessels and poor prognosis of the patients. Cancer Commun. 40 211–221. 10.1002/cac2.12026 PubMed DOI PMC
Meşe G., Richard G., White T. W. (2007). Gap junctions: basic structure and function. J. Invest. Dermatol. 127 2516–2524. 10.1038/sj.jid.5700770 PubMed DOI
Mitic L. L., Van Itallie C. M., Anderson J. M. (2000). Molecular physiology and pathophysiology of tight junctions I. Tight junction structure and function: lessons from mutant animals and proteins. Am. J. Physiol. Gastrointest. Liver Physiol. 279 G250–G254. 10.1152/ajpgi.2000.279.2.G250 PubMed DOI
Molnár P. P., O’Neill B. P., Scheithauer B. W., Groothuis D. R. (1999). The blood-brain barrier in primary CNS lymphomas: ultrastructural evidence of endothelial cell death. Neuro. Oncol. 1 89–100. 10.1093/neuonc/1.2.89 PubMed DOI PMC
Mou K., Chen M., Mao Q., Wang P., Ni R., Xia X., et al. (2010). AQP-4 in peritumoral edematous tissue is correlated with the degree of glioma and with expression of VEGF and HIF-alpha. J. Neurooncol. 100 375–383. 10.1007/s11060-010-0205-x PubMed DOI
Muoio V., Persson P. B., Sendeski M. M. (2014). The neurovascular unit - concept review. Acta Physiol. 210 790–798. 10.1111/apha.12250 PubMed DOI
Na W., Shin J. Y., Lee J. Y., Jeong S., Kim W.-S., Yune T. Y., et al. (2017). Dexamethasone suppresses JMJD3 gene activation via a putative negative glucocorticoid response element and maintains integrity of tight junctions in brain microvascular endothelial cells. J. Cereb. Blood Flow Metab. 37 3695–3708. 10.1177/0271678X17701156 PubMed DOI PMC
Nakagawa S., Deli M. A., Nakao S., Honda M., Hayashi K., Nakaoke R., et al. (2007). Pericytes from brain microvessels strengthen the barrier integrity in primary cultures of rat brain endothelial cells. Cell Mol. Neurobiol. 27 687–694. 10.1007/s10571-007-9195-4 PubMed DOI PMC
Noell S., Wolburg-Buchholz K., Mack A. F., Ritz R., Tatagiba M., Beschorner R., et al. (2012). Dynamics of expression patterns of AQP4, dystroglycan, agrin and matrix metalloproteinases in human glioblastoma. Cell Tissue Res. 347 429–441. 10.1007/s00441-011-1321-4 PubMed DOI
Obenaus A., Ashwal S. (2008). Magnetic resonance imaging in cerebral ischemia: focus on neonates. Neuropharmacology 55 271–280. 10.1016/j.neuropharm.2008.06.010 PubMed DOI
Ostrom Q. T., Cioffi G., Waite K., Kruchko C., Barnholtz-Sloan J. S. (2021). CBTRUS Statistical Report: primary Brain and Other Central Nervous System Tumors Diagnosed in the United States in 2014-2018. Neuro. Oncol. 23 iii1–iii105. 10.1093/neuonc/noab200 PubMed DOI PMC
Ou A., Ott M., Fang D., Heimberger A. B. (2021). The Role and Therapeutic Targeting of JAK/STAT Signaling in Glioblastoma. Cancers 13:437. 10.3390/cancers13030437 PubMed DOI PMC
Papadopoulos M. C., Saadoun S., Woodrow C. J., Davies D. C., Costa-Martins P., Moss R. F., et al. (2001). Occludin expression in microvessels of neoplastic and non-neoplastic human brain. Neuropathol. Appl. Neurobiol. 27 384–395. 10.1046/j.0305-1846.2001.00341.x PubMed DOI
Papadopoulos M. C., Verkman A. S. (2007). Aquaporin-4 and brain edema. Pediatr. Nephrol. 22 778–784. 10.1007/s00467-006-0411-0 PubMed DOI PMC
Park M.-W., Kim C.-H., Cheong J.-H., Bak K.-H., Kim J.-M., Oh S.-J. (2006). Occludin Expression in Brain Tumors and its Relevance to Peritumoral Edema and Survival. Cancer Res. Treat. 38 139–143. 10.4143/crt.2006.38.3.139 PubMed DOI PMC
Preusser M., Heinzl H., Gelpi E., Schonegger K., Haberler C., Birner P., et al. (2006). Histopathologic assessment of hot-spot microvessel density and vascular patterns in glioblastoma: poor observer agreement limits clinical utility as prognostic factors: a translational research project of the European Organization for Research and Treatment of Cancer Brain Tumor Group. Cancer 107 162–170. 10.1002/cncr.21973 PubMed DOI
Pun P. B. L., Lu J., Moochhala S. (2009). Involvement of ROS in BBB dysfunction. Free Radic. Res. 43 348–364. 10.1080/10715760902751902 PubMed DOI
Rauch S. M., Huen K., Miller M. C., Chaudry H., Lau M., Sanes J. R., et al. (2011). Changes in Brain β-Amyloid Deposition and Aquaporin 4 Levels in Response to Altered Agrin Expression in Mice. J. Neuropathol. Exp. Neurol. 70 1124–1137. 10.1097/NEN.0b013e31823b0b12 PubMed DOI PMC
Rempe R. G., Hartz A. M., Bauer B. (2016). Matrix metalloproteinases in the brain and blood–brain barrier: versatile breakers and makers. J. Cereb. Blood Flow Metab. 36 1481–1507. 10.1177/0271678X16655551 PubMed DOI PMC
Rite I., Machado A., Cano J., Venero J. L. (2008). Intracerebral VEGF injection highly upregulates AQP4 mRNA and protein in the perivascular space and glia limitans externa. Neurochem. Int. 52 897–903. 10.1016/j.neuint.2007.10.004 PubMed DOI
Roberts W. G., Palade G. E. (1995). Increased microvascular permeability and endothelial fenestration induced by vascular endothelial growth factor. J. Cell Sci. 108 2369–2379. 10.1242/jcs.108.6.2369 PubMed DOI
Rosińska S., Gavard J. (2021). Tumor Vessels Fuel the Fire in Glioblastoma. Int. J. Mol. Sci. 22:6514. 10.3390/ijms22126514 PubMed DOI PMC
Ruggieri S., Tamma R., Resta N., Albano F., Coccaro N., Loconte D., et al. (2017). Stat3-positive tumor cells contribute to vessels neoformation in primary central nervous system lymphoma. Oncotarget 8 31254–31269. 10.18632/oncotarget.16115 PubMed DOI PMC
Saadoun S., Papadopoulos M. C., Bell B. A., Krishna S., Davies D. C. (2002a). The aquaporin-4 water channel and brain tumour oedema. J. Anat. 200 523–534. 10.1046/j.1469-7580.2002.00047_16.x DOI
Saadoun S., Papadopoulos M. C., Davies D. C., Krishna S., Bell B. A. (2002b). Aquaporin-4 expression is increased in oedematous human brain tumours. J. Neurol. Neurosurg. Psychiatr. 72 262–265. 10.1136/jnnp.72.2.262 PubMed DOI PMC
Saadoun S., Papadopoulos M. C., Krishna S. (2003). Water transport becomes uncoupled from K+ siphoning in brain contusion, bacterial meningitis, and brain tumours: immunohistochemical case review. J. Clin. Pathol. 56 972–975. 10.1136/jcp.56.12.972 PubMed DOI PMC
Sehm T., Fan Z., Ghoochani A., Rauh M., Engelhorn T., Minakaki G., et al. (2016). Sulfasalazine impacts on ferroptotic cell death and alleviates the tumor microenvironment and glioma-induced brain edema. Oncotarget 7 36021–36033. 10.18632/oncotarget.8651 PubMed DOI PMC
Shevtsov M. A., Nikolaev B. P., Yakovleva L. Y., Dobrodumov A. V., Zhakhov A. V., Mikhrina A. L., et al. (2015). Recombinant interleukin-1 receptor antagonist conjugated to superparamagnetic iron oxide nanoparticles for theranostic targeting of experimental glioblastoma. Neoplasia 17 32–42. 10.1016/j.neo.2014.11.001 PubMed DOI PMC
Shi S., Cheng J., Zhang C., Liang T., Zhang Y., Sun Y., et al. (2020). Peripheral Blood Occludin Level as a Biomarker for Perioperative Cerebral Edema in Patients with Brain Tumors. Dis. Markers 2020 8813535. 10.1155/2020/8813535 PubMed DOI PMC
Shweiki D., Itin A., Soffer D., Keshet E. (1992). Vascular endothelial growth factor induced by hypoxia may mediate hypoxia-initiated angiogenesis. Nature 359 843–845. 10.1038/359843a0 PubMed DOI
Simard J. M., Chen M., Tarasov K. V., Bhatta S., Ivanova S., Melnitchenko L., et al. (2006). Newly expressed SUR1-regulated NC(Ca-ATP) channel mediates cerebral edema after ischemic stroke. Nat. Med. 12 433–440. 10.1038/nm1390 PubMed DOI PMC
Simard J. M., Geng Z., Woo S. K., Ivanova S., Tosun C., Melnichenko L., et al. (2009). Glibenclamide reduces inflammation, vasogenic edema, and caspase-3 activation after subarachnoid hemorrhage. J. Cereb. Blood Flow Metab. 29 317–330. 10.1038/jcbfm.2008.120 PubMed DOI PMC
Simone L., Pisani F., Mola M. G., De Bellis M., Merla G., Micale L., et al. (2019). AQP4 Aggregation State Is a Determinant for Glioma Cell Fate. Cancer Res. 79 2182–2194. 10.1158/0008-5472.CAN-18-2015 PubMed DOI
Solár P., Zamani A., Lakatosová K., Joukal M. (2022). The blood–brain barrier and the neurovascular unit in subarachnoid hemorrhage: molecular events and potential treatments. Fluids Barriers CNS 19 1–79. 10.1186/s12987-022-00312-4 PubMed DOI PMC
Song Y., Liu B., Guan M., Liu M. (2018). Successful treatment using apatinib in intractable brain edema: a case report and literatures review. Cancer Biol. Ther. 19 1093–1096. 10.1080/15384047.2018.1491502 PubMed DOI PMC
Soussain C., Muldoon L. L., Varallyay C., Jahnke K., DePaula L., Neuwelt E. A. (2007). Characterization and magnetic resonance imaging of a rat model of human B-cell central nervous system lymphoma. Clin. Cancer Res. 13 2504–2511. 10.1158/1078-0432.CCR-06-2379 PubMed DOI
Spanberger T., Berghoff A. S., Dinhof C., Ilhan-Mutlu A., Magerle M., Hutterer M., et al. (2013). Extent of peritumoral brain edema correlates with prognosis, tumoral growth pattern. HIF1a expression and angiogenic activity in patients with single brain metastases. Clin. Exp. Metastas. 30 357–368. 10.1007/s10585-012-9542-9 PubMed DOI
Stamatovic S. M., Johnson A. M., Keep R. F., Andjelkovic A. V. (2016). Junctional proteins of the blood-brain barrier: new insights into function and dysfunction. Tissue Barriers 4 e1154641. 10.1080/21688370.2016.1154641 PubMed DOI PMC
Steiner H.-H., Karcher S., Mueller M. M., Nalbantis E., Kunze S., Herold-Mende C. (2004). Autocrine pathways of the vascular endothelial growth factor (VEGF) in glioblastoma multiforme: clinical relevance of radiation-induced increase of VEGF levels. J. Neurooncol. 66 129–138. 10.1023/b:neon.0000013495.08168.8f PubMed DOI
Stenzel W., Dahm J., Sanchez-Ruiz M., Miletic H., Hermann M., Courts C., et al. (2005a). Regulation of the inflammatory response to Staphylococcus aureus-induced brain abscess by interleukin-10. J. Neuropathol. Exp. Neurol. 64 1046–1057. 10.1097/01.jnen.0000189836.48704.ca PubMed DOI
Stenzel W., Soltek S., Miletic H., Hermann M. M., Körner H., Sedgwick J. D., et al. (2005b). An essential role for tumor necrosis factor in the formation of experimental murine Staphylococcus aureus-induced brain abscess and clearance. J. Neuropathol. Exp. Neurol. 64 27–36. 10.1093/jnen/64.1.27 PubMed DOI
Stenzel W., Soltek S., Schlüter D., Deckert M. (2004). The intermediate filament GFAP is important for the control of experimental murine Staphylococcus aureus-induced brain abscess and Toxoplasma encephalitis. J. Neuropathol. Exp. Neurol. 63 631–640. 10.1093/jnen/63.6.631 PubMed DOI
Stokum J. A., Kwon M. S., Woo S. K., Tsymbalyuk O., Vennekens R., Gerzanich V., et al. (2018). SUR1-TRPM4 and AQP4 form a heteromultimeric complex that amplifies ion/water osmotic coupling and drives astrocyte swelling. Glia 66 108–125. 10.1002/glia.23231 PubMed DOI PMC
Stupp R., Mason W. P., van den Bent M. J., Weller M., Fisher B., Taphoorn M. J. B., et al. (2005). Radiotherapy plus Concomitant and Adjuvant Temozolomide for Glioblastoma. N. Engl. J. Med. 352 987–996. 10.1056/NEJMoa043330 PubMed DOI
Suh C. H., Kim H. S., Jung S. C., Kim S. J. (2018). Diffusion-Weighted Imaging and Diffusion Tensor Imaging for Differentiating High-Grade Glioma from Solitary Brain Metastasis: a Systematic Review and Meta-Analysis. Am. J. Neuroradiol. 39 1208–1214. 10.3174/ajnr.A5650 PubMed DOI PMC
Sweeney M. D., Zhao Z., Montagne A., Nelson A. R., Zlokovic B. V. (2019). Blood-Brain Barrier: from Physiology to Disease and Back. Physiol. Rev. 99 21–78. 10.1152/physrev.00050.2017 PubMed DOI PMC
Takata K., Matsuzaki T., Tajika Y. (2004). Aquaporins: water channel proteins of the cell membrane. Prog. Histochem. Cytochem. 39 1–83. 10.1016/j.proghi.2004.03.001 PubMed DOI
Takeuchi H., Hashimoto N., Kitai R., Kubota T., Kikuta K. (2010). Proliferation of vascular smooth muscle cells in glioblastoma multiforme. J. Neurosurg. 113 218–224. 10.3171/2009.10.JNS08631 PubMed DOI
Takeuchi H., Matsuda K., Kitai R., Sato K., Kubota T. (2007). Angiogenesis in primary central nervous system lymphoma (PCNSL). J. Neurooncol. 84 141–145. 10.1007/s11060-007-9363-x PubMed DOI
Tamura R., Ohara K., Sasaki H., Morimoto Y., Yoshida K., Toda M. (2018). Histopathological vascular investigation of the peritumoral brain zone of glioblastomas. J. Neurooncol. 136 233–241. 10.1007/s11060-017-2648-9 PubMed DOI
Tan A. C., Ashley D. M., López G. Y., Malinzak M., Friedman H. S., Khasraw M. (2020). Management of glioblastoma: state of the art and future directions. CA Cancer J. Clin. 70 299–312. 10.3322/caac.21613 PubMed DOI
Thompson E. M., Pishko G. L., Muldoon L. L., Neuwelt E. A. (2013). Inhibition of SUR1 Decreases the Vascular Permeability of Cerebral Metastases. Neoplasia 15 535–543. 10.1593/neo.13164 PubMed DOI PMC
Toh C. H., Siow T. Y. (2021). Factors Associated With Dysfunction of Glymphatic System in Patients With Glioma. Front. Oncol. 11:744318. 10.3389/fonc.2021.744318 PubMed DOI PMC
Toh C. H., Siow T. Y., Castillo M. (2021). Peritumoral Brain Edema in Metastases May Be Related to Glymphatic Dysfunction. Front. Oncol. 11:4144. 10.3389/fonc.2021.725354 PubMed DOI PMC
Tran T. T., Mahajan A., Chiang V. L., Goldberg S. B., Nguyen D. X., Jilaveanu L. B., et al. (2019). Perilesional edema in brain metastases: potential causes and implications for treatment with immune therapy. J. Immunother. Cancer 7:200. 10.1186/s40425-019-0684-z PubMed DOI PMC
Trembath D. G., Davis E. S., Rao S., Bradler E., Saada A. F., Midkiff B. R., et al. (2020). Brain Tumor Microenvironment and Angiogenesis in Melanoma Brain Metastases. Front. Oncol. 10:604213. 10.3389/fonc.2020.604213 PubMed DOI PMC
Utsuki S., Oka H., Sato S., Shimizu S., Suzuki S., Tanizaki Y., et al. (2007). Histological examination of false positive tissue resection using 5-aminolevulinic acid-induced fluorescence guidance. Neurol. Med. Chir. 47 210–213. 10.2176/nmc.47.210 PubMed DOI
Van Itallie C. M., Anderson J. M. (2004). The role of claudins in determining paracellular charge selectivity. Proc. Am. Thorac. Soc. 1 38–41. 10.1513/pats.2306013 PubMed DOI
Vaquero J., Zurita M., Morales C. (2001). Possible Role for Vascular Permeability Factor in the Pathophysiology of Vasogenic Oedema Associated to Brain Abscess. Acta Neurochir. 143 1039–1040. 10.1007/s007010170009 PubMed DOI
Vazana U., Veksler R., Pell G. S., Prager O., Fassler M., Chassidim Y., et al. (2016). Glutamate-Mediated Blood-Brain Barrier Opening: implications for Neuroprotection and Drug Delivery. J. Neurosci. 36 7727–7739. 10.1523/JNEUROSCI.0587-16.2016 PubMed DOI PMC
Verkman A. S., Ratelade J., Rossi A., Zhang H., Tradtrantip L. (2011). Aquaporin-4: orthogonal array assembly, CNS functions, and role in neuromyelitis optica. Acta Pharmacol. Sin. 32 702–710. 10.1038/aps.2011.27 PubMed DOI PMC
Vestweber D. (2008). VE-cadherin: the major endothelial adhesion molecule controlling cellular junctions and blood vessel formation. Arterioscler. Thromb. Vasc. Biol. 28 223–232. 10.1161/ATVBAHA.107.158014 PubMed DOI
Wahl M., Unterberg A., Baethmann A., Schilling L. (1988). Mediators of blood-brain barrier dysfunction and formation of vasogenic brain edema. J. Cereb. Blood Flow Metab. 8 621–634. 10.1038/jcbfm.1988.109 PubMed DOI
Wallenfang T., Bohl J., Kretzschmar K. (1980). Evolution of brain abscess in cats formation of capsule and resolution of brain edema. Neurosurg. Rev. 3 101–111. 10.1007/BF01644062 PubMed DOI
Wang H.-C., Hsiao H.-H., Du J.-S., Cho S.-F., Yeh T.-J., Gau Y.-C., et al. (2021). Effect of Tumor Microenvironment and Angiogenesis on Clinical Outcomes of Primary Central Nervous System Lymphoma. BioMed. Res. Int. 2021:e3291762. 10.1155/2021/3291762 PubMed DOI PMC
Wang S.-Y., Ke Y.-Q., Lu G.-H., Song Z.-H., Yu L., Xiao S., et al. (2013). Vasculogenic mimicry is a prognostic factor for postoperative survival in patients with glioblastoma. J. Neurooncol. 112 339–345. 10.1007/s11060-013-1077-7 PubMed DOI
Wang X.-F., Lin G.-S., Lin Z.-X., Chen Y.-P., Chen Y., Zhang J.-D., et al. (2014). Association of pSTAT3-VEGF signaling pathway with peritumoral edema in newly diagnosed glioblastoma: an immunohistochemical study. Int. J. Clin. Exp. Pathol. 7 6133–6140. PubMed PMC
Warth A., Kröger S., Wolburg H. (2004). Redistribution of aquaporin-4 in human glioblastoma correlates with loss of agrin immunoreactivity from brain capillary basal laminae. Acta Neuropathol. 107 311–318. 10.1007/s00401-003-0812-0 PubMed DOI
Warth A., Simon P., Capper D., Goeppert B., Tabatabai G., Herzog H., et al. (2007). Expression pattern of the water channel aquaporin-4 in human gliomas is associated with blood-brain barrier disturbance but not with patient survival. J. Neurosci. Res. 85 1336–1346. 10.1002/jnr.21224 PubMed DOI
Wen L., Tan Y., Dai S., Zhu Y., Meng T., Yang X., et al. (2017). VEGF-mediated tight junctions pathological fenestration enhances doxorubicin-loaded glycolipid-like nanoparticles traversing BBB for glioblastoma-targeting therapy. Drug Deliv. 24 1843–1855. 10.1080/10717544.2017.1386731 PubMed DOI PMC
Wesseling P., Schlingemann R. O., Rietveld F. J., Link M., Burger P. C., Ruiter D. J. (1995). Early and extensive contribution of pericytes/vascular smooth muscle cells to microvascular proliferation in glioblastoma multiforme: an immuno-light and immuno-electron microscopic study. J. Neuropathol. Exp. Neurol. 54 304–310. 10.1097/00005072-199505000-00003 PubMed DOI
White M. L., Moore D. W., Zhang Y., Mark K. D., Greiner T. C., Bierman P. J. (2019). Primary central nervous system post-transplant lymphoproliferative disorders: the spectrum of imaging appearances and differential. Insights Imaging 10:46. 10.1186/s13244-019-0726-6 PubMed DOI PMC
Wolburg H., Noell S., Fallier-Becker P., Mack A. F., Wolburg-Buchholz K. (2012). The disturbed blood-brain barrier in human glioblastoma. Mol. Aspects Med. 33 579–589. 10.1016/j.mam.2012.02.003 PubMed DOI
Xu C., Wu X., Zhu J. (2013). VEGF promotes proliferation of human glioblastoma multiforme stem-like cells through VEGF receptor 2. Sci. WorldJ. 2013:417413. 10.1155/2013/417413 PubMed DOI PMC
Xu L., Nirwane A., Yao Y. (2018). Basement membrane and blood–brain barrier. Stroke Vasc. Neurol. 4 78–82. 10.1136/svn-2018-000198 PubMed DOI PMC
Xue Q., Cao L., Chen X.-Y., Zhao J., Gao L., Li S.-Z., et al. (2017). High expression of MMP9 in glioma affects cell proliferation and is associated with patient survival rates. Oncol. Lett. 13 1325–1330. 10.3892/ol.2017.5567 PubMed DOI PMC
Yang J., Li Q., Wang Z., Qi C., Han X., Lan X., et al. (2017). Multimodality MRI assessment of grey and white matter injury and blood-brain barrier disruption after intracerebral haemorrhage in mice. Sci. Rep. 7:40358. 10.1038/srep40358 PubMed DOI PMC
Yang J., Li W., He X., Zhang G., Yue L., Chai Y. (2015). VEGF Overexpression Is a Valuable Prognostic Factor for Non-Hodgkin’s Lymphoma Evidence from a Systemic Meta-Analysis. Dis. Mark 2015:786790. 10.1155/2015/786790 PubMed DOI PMC
Yang L., Wang X., Zhen S., Zhang S., Kang D., Lin Z. (2012). Aquaporin-4 upregulated expression in glioma tissue is a reaction to glioma-associated edema induced by vascular endothelial growth factor. Oncol. Rep. 28 1633–1638. 10.3892/or.2012.1973 PubMed DOI
Yang N., Ng Y. H., Pang Z. P., Südhof T. C., Wernig M. (2011). Induced neuronal cells: how to make and define a neuron. Cell Stem Cell 9 517–525. 10.1016/j.stem.2011.11.015 PubMed DOI PMC
Yeung P. K. K., Lo A. C. Y., Leung J. W. C., Chung S. S. M., Chung S. K. (2009). Targeted Overexpression of Endothelin-1 in Astrocytes Leads to More Severe Cytotoxic Brain Edema and Higher Mortality. J. Cereb. Blood Flow Metab. 29 1891–1902. 10.1038/jcbfm.2009.175 PubMed DOI
Zagzag D., Esencay M., Mendez O., Yee H., Smirnova I., Huang Y., et al. (2008). Hypoxia- and vascular endothelial growth factor-induced stromal cell-derived factor-1alpha/CXCR4 expression in glioblastomas: one plausible explanation of Scherer’s structures. Am. J. Pathol. 173 545–560. 10.2353/ajpath.2008.071197 PubMed DOI PMC
Zhang M., Olsson Y. (1995). Reactions of astrocytes and microglial cells around hematogenous metastases of the human brain. Expression of endothelin-like immunoreactivity in reactive astrocytes and activation of microglial cells. J. Neurol. Sci. 134 26–32. 10.1016/0022-510x(95)00227-9 PubMed DOI
Zhao B., Wang H., Wang X., Zhao H., Liu J. (2015). Multiple intracranial metastatic tumor case report and aquaporin water channel-related research. Cell Biochem. Biophys. 71 1015–1021. 10.1007/s12013-014-0303-z PubMed DOI
Zhao X., Sun Q., Dou C., Chen Q., Liu B. (2019). BMP4 inhibits glioblastoma invasion by promoting E-cadherin and claudin expression. Front. Biosci. 24:1060–1070. 10.2741/4768 PubMed DOI
Zhou J., Kong H., Hua X., Xiao M., Ding J., Hu G. (2008). Altered blood-brain barrier integrity in adult aquaporin-4 knockout mice. Neuroreport 19 1–5. 10.1097/WNR.0b013e3282f2b4eb PubMed DOI