Protoplasmic Perivascular Astrocytes Play a Crucial Role in the Development of Enlarged Perivascular Spaces in Obesity, Metabolic Syndrome, and Type 2 Diabetes Mellitus
Abstract
:1. Introduction
2. Metabolic Disorders: Obesity, Metabolic Syndrome (MetS), Type 2 Diabetes Mellitus (T2DM), and Global Aging
3. Postcapillary Venule Perivascular Unit (PVU), Normal Perivascular Spaces (PVS), and Transformation to Pathological Enlarged Perivascular Spaces (EPVS)
4. Protoplasmic Perivascular Astrocyte Endfeet (pvACef) Play a Crucial Role in the Development of the Perivascular Unit (PVU) and Enlarged Perivascular Spaces (EPVS)
5. Perivascular Astrocyte Endfeet (pvACef)
6. Perisynaptic Astrocyte Endfeet (psACef), Aquaporin-4 (AQP4), Impaired Synaptic Transmission and Synaptopathy
7. Impaired Perivascular Astrocyte Endfeet (pvACef), AQP4, Glymphatic System (GS), and Clearance of Metabolic Waste (MW) Associated with Cerebral Small Vessel Disease (SVD)
8. Conclusions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
Abbreviations
References
- Mishra, A.; Reynolds, J.P.; Chen, Y.; Gourine, A.V.; Rusakov, D.A.; Attwell, D. Astrocytes mediate neurovascular signaling to capillary pericytes but not to arterioles. Nat. Neurosci. 2016, 19, 1619–1627. [Google Scholar] [CrossRef] [PubMed]
- Shulyatnikova, T.; Hayden, M.R. Why Are Perivascular Spaces Important? Medicina 2023, 59, 917. [Google Scholar] [CrossRef] [PubMed]
- Hayden, M.R. Brain Endothelial Cells Play a Central Role in the Development of Enlarged Perivascular Spaces in the Metabolic Syndrome. Medicina 2023, 59, 1124. [Google Scholar] [CrossRef] [PubMed]
- Yu, L.; Hu, X.; Li, H.; Zhao, Y. Perivascular Spaces, Glymphatic System and MR. Front. Neurol. 2022, 13, 844938. [Google Scholar] [CrossRef] [PubMed]
- McConnell, H.L.; Kersch, C.N.; Woltjer, R.L.; Neuwelt, E.A. The Translational Significance of the Neurovascular Unit. J. Biol. Chem. 2017, 292, 762–770. [Google Scholar] [CrossRef] [PubMed]
- Petzold, G.C.; Murthy, V.N. Role of astrocytes in neurovascular coupling. Neuron 2011, 71, 782–797. [Google Scholar] [CrossRef]
- Hayden, M.R.; Grant, D.G.; Aroor, A.A.; DeMarco, V.G. Ultrastructural Remodeling of the Neurovascular Unit in the Female Diabetic db/db Model—Part I: Astrocyte. Neuroglia 2018, 1, 220–244. [Google Scholar] [CrossRef]
- Verkhratsky, A.; Butt, A.M. Neuroglia: Function and Pathology, 1st ed.; Academic Press: London, UK, 2023. [Google Scholar]
- Verkhratsky, A.; Nedergaard, M. Astroglial cradle in the life of the synapse. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2014, 369, 20130595. [Google Scholar] [CrossRef]
- Verkhratsky, A.; Nedergaard, M. Physiology of Astroglia. Physiol. Rev. 2018, 98, 239–389. [Google Scholar] [CrossRef]
- Verkhratsky, A. Astrocytes: The Housekeepers and Guardians of the CNS. Adv. Neurobiol. 2021, 26, 21–53. [Google Scholar] [CrossRef]
- Hayden, M.R.; Banks, W.A.; Shah, G.N.; Gu, Z.; Sowers, J.R. Cardiorenal metabolic syndrome and diabetic cognopathy. Cardiorenal Med. 2013, 3, 265–282. [Google Scholar] [CrossRef]
- Hayden, M.R. Hypothesis: Neuroglia Activation Due to Increased Peripheral and CNS Proinflammatory Cytokines/Chemokines with Neuroinflammation May Result in Long COVID. Neuroglia 2021, 2, 7–35. [Google Scholar] [CrossRef]
- Oberheim, N.A.; Takano, T.; Han, X.; He, W.; Lin, J.H.C.; Wang, F.; Xu, Q.; Wyatt, J.D.; Pilcher, W.; Ojemann, J.G.; et al. Uniquely hominid features of adult human astrocytes. J. Neurosci. 2009, 29, 3276–3287. [Google Scholar] [CrossRef] [PubMed]
- Scemes, E.; Spray, D.C. Chapter: The astrocytic syncytium. In Non-Neural Cells in the Nervous System: Function and Dysfunction; Hertz, L., Ed.; Elsevier: New York, NY, USA, 2004; Volume 31, pp. 165–179. [Google Scholar]
- Abbott, N.J.; Rönnbäck, L.; Hansson, E. Astrocyte-endothelial interactions at the blood-brain barrier. Nat. Rev. Neurosci. 2006, 7, 41–53. [Google Scholar] [CrossRef] [PubMed]
- Iliff, J.; Wang, M.; Liao, Y.; Plogg, B.A.; Peng, W.; Gundersen, G.A.; Benveniste, H.; Vates, E.; Deane, R.; Goldman, S.A.; et al. A Paravascular Pathway Facilitates CSF Flow Through the Brain Parenchyma and the Clearance of Interstitial Solutes, Including Amyloid β. Sci. Transl. Med. 2012, 4, 147ra111. [Google Scholar] [CrossRef] [PubMed]
- Chung, W.S.; Allen, N.J.; Eroglu, C. Astrocytes Control Synapse Formation, Function, and Elimination. Cold Spring Harb. Perspect. Biol. 2015, 7, a020370. [Google Scholar] [CrossRef] [PubMed]
- Taoufik, E.; Kouroupi, G.; Zygogianni, Q.; Matsas, R. Synaptic dysfunction in neurodegenerative and neurodevelopmental diseases: An overview of induced pluripotent stem-cell-based disease models. Open Biol. 2018, 8, 180138. [Google Scholar] [CrossRef]
- Oksanen, M.; Lehtonen, S.; Jaronen, M.; Goldsteins, G.; Hämäläinen, R.H.; Koistinaho, J. Astrocyte alterations in neurodegenerative pathologies and their modeling in human induced pluripotent stem cell platforms. Cell. Mol. Life Sci. 2019, 76, 2739–2760. [Google Scholar] [CrossRef]
- Hayden, M.R. Type 2 Diabetes Mellitus Increases the Risk of Late-Onset Alzheimer’s Disease: Ultrastructural Remodeling of the Neurovascular Unit and Diabetic Gliopathy. Brain Sci. 2019, 9, 262. [Google Scholar] [CrossRef]
- Gerdes, E.O.W.; Zhu, Y.; Weigand, B.M.; Tripathi, U.; Burns, T.C.; Tchkonia, T.J.; Kirkland, J.L. Cellular senescence in aging and age-related diseases: Implications for neurodegenerative diseases. Int. Rev. Neurobiol. 2020, 155, 203–234. [Google Scholar] [CrossRef]
- Seshadri, S.; Wolf, P.A. Lifetime risk of stroke and dementia: Current concepts, and estimates from the Framingham Study. Lancet Neurol. 2007, 6, 1106–1114. [Google Scholar] [CrossRef] [PubMed]
- Qi, Y.; Lin, M.; Yang, Y.; Li, Y. Relationship of Visceral Adipose Tissue with Dilated Perivascular Spaces. Front. Neurosci. 2020, 14, 583557. [Google Scholar] [CrossRef] [PubMed]
- Lee, T.H.; Yau, S.Y. From Obesity to Hippocampal Neurodegeneration: Pathogenesis and Non-Pharmacological Interventions. Int. J. Mol. Sci. 2021, 22, 201. [Google Scholar] [CrossRef] [PubMed]
- Wu, D.; Yang, X.; Zhong, P.; Ye, X.; Li, C.; Liu, X. Insulin Resistance Is Independently Associated with Enlarged Perivascular Space in the Basal Ganglia in Nondiabetic Healthy Elderly Population. Am. J. Alzheimer’s Dis. Other Dement. 2020, 35, 1533317520912126. [Google Scholar] [CrossRef] [PubMed]
- Craft, S. The role of metabolic disorders in Alzheimer’s disease and vascular dementia: Two roads converged. Arch. Neurol. 2009, 66, 300–305. [Google Scholar] [CrossRef]
- Cai, Y.; Chen, B.; Zeng, X.; Xie, M.; Wei, X.; Cai, J. Glutathione. Front. Neurol. 2022, 13, 782286. [Google Scholar] [CrossRef]
- Tiehuis, A.M.; van der Graaf, Y.; Mali, W.P.; Vincken, K.; Muller, M.; Geerlings, M.I.; SMART Study Group. Diabetes Metabolic syndrome, prediabetes, and brain abnormalities on MRI in patients with manifest arterial disease: The SMART-MR study. Diabetes Care 2014, 37, 2515–2521. [Google Scholar] [CrossRef]
- Munia, O.B. Association of Type 2 Diabetes Mellitus with Perivascular Spaces and Cerebral Amyloid Angiopathy in Alzheimer’s Disease: Insights from MRI Imaging. Dement. Neurocogn. Disord. 2023, 22, 87–99. [Google Scholar] [CrossRef]
- Choi, E.Y.; Park, Y.W.; Lee, M.; Kim, M.; Lee, C.S.; Ahn, S.S.; Kim, J.; Lee, S.K. Magnetic Resonance Imaging-Visible Perivascular Spaces in the Basal Ganglia Are Associated with the Diabetic Retinopathy Stage and Cognitive Decline in Patients with Type 2 Diabetes. Front. Aging Neurosci. 2021, 13, 666495. [Google Scholar] [CrossRef]
- Zhao, H.; Wang, F.; Luo, G.H.; Lei, H.; Peng, F.; Ren, Q.P.; Chen, W.; Wu, Y.F.; Yin, L.C.; Liu, J.C.; et al. Assessment of structural brain changes in patients with type 2 diabetes mellitus using the MRI-based brain atrophy and lesion index. Neural Regen. Res. 2022, 17, 618–624. [Google Scholar] [CrossRef]
- Zebarth, J.; Kamal, R.; Perlman, G.; Ouk, M.; Xiong, L.Y.; Yu, D.; Lin, W.Z.; Ramirez, J.; Masellis, M.; Goubran, M.; et al. Perivascular spaces mediate a relationship between diabetes and other cerebral small vessel disease markers in cerebrovascular and neurodegenerative diseases. J. Stroke Cebrovasc. Dis. 2023, 32, 107273. [Google Scholar] [CrossRef] [PubMed]
- Jiang, Q.; Zhang, L.; Ding, G.; Davoodi-Boid, E.; Li, Q.; Li, L.; Sadry, N.; Nedergaard, M.; Chopp, M.; Zhang, Z. Impairment of the glymphatic system after diabetes. J. Cereb. Blood Flow Metab. 2017, 37, 1326–1337. [Google Scholar] [CrossRef] [PubMed]
- Biessels, G.J.; Staekenborg, S.; Brunner, E.; Brayne, C.; Scheltens, P. Risk of dementia in diabetes mellitus: A systemic review. Lancet Neurol. 2006, 5, 64–74. [Google Scholar] [CrossRef] [PubMed]
- Ott, A.; Stolk, R.P.; van Harskamp, F.; Hofman, H.A.; Breteler, M.M.B. Diabetes mellitus and risk of dementia: The Rotterdam study. Neurology 1999, 53, 1037–1942. [Google Scholar] [CrossRef]
- Cukierman, T.; Gerstein, H.C.; Williamson, J.D. Cognitive decline and dementia in diabetes—Systematic overview of prospective observational studies. Diabetologia 2005, 48, 2460–2469. [Google Scholar] [CrossRef]
- Jacobson, A.M.; Musen, G.; Ryan, C.M.; Silver, N.; Cleary, P.; Waberski, B.; Burwood, A.; Weinger, K.; Bayless, M.; Dahms, W.; et al. Long-term effect of diabetes and its treatment on cognitive function. N. Engl. J. Med. 2007, 356, 1842–1852. [Google Scholar]
- McCrimmon, R.J.; Ryan, C.M.; Frier, B.M. Diabetes and cognitive dysfunction. Lancet 2012, 379, 2291–2299. [Google Scholar] [CrossRef]
- Zou, Q.; Wang, M.; Wei, X.; Li, W. Prevalence and Risk Factors for Enlarged Perivascular Spaces in Young Adults from a Neurology Clinic-Based Cohort. Brain Sci. 2022, 12, 1164. [Google Scholar] [CrossRef]
- Troili, F.; Cipollini, V.; Moci, M.; Morena, E.; Palotai, M.; Rinaldi, V.; Romano, C.; Ristori, G.; Giubilei, F.; Salvetti, M.; et al. Perivascular Unit: This Must Be the Place. The Anatomical Crossroad Between the Immune Vascular and Nervous System. Front. Neuroanat. 2020, 14, 17. [Google Scholar] [CrossRef]
- Hayden, M.R. Pericytes and Resident Perivascular Macrophages Play a Key Role in the Development of Enlarged Perivascular Spaces in Obesity, Metabolic Syndrome and Type 2 Diabetes Mellitus. J. Alzheimer’s Neurodegener. Dis. 2023, 9, 062. [Google Scholar]
- Okar, S.V.; Hu, F.; Shinohara, R.T.; Beck, E.S.; Reich, D.S.; Ineichen, B.V. The etiology and evolution of magnetic resonance imaging-visible perivascular spaces: Systematic review and meta-analysis. Front. Neurosci. 2023, 17, 1038011. [Google Scholar] [CrossRef]
- Hayden, M.R. Brain Injury: Response to Injury Wound-Healing Mechanisms and Enlarged Perivascular Spaces in Obesity, Metabolic Syndrome and Type 2 Diabetes Mellitus. Medicina 2023, 59, 1337. [Google Scholar] [CrossRef]
- Tucsek, Z.; Toth, P.; Tarantini, S.; Sosnowska, D.; Gautam, T.; Warrington, J.P.; Giles, C.B.; Wren, J.D.; Koller, A.; Ballabh, P.; et al. Aging Exacerbates Obesity-induced Cerebromicrovascular Rarefaction, Neurovascular Uncoupling, and Cognitive Decline in Mice. J. Gerontol. Ser. A 2014, 69, 1339–1352. [Google Scholar] [CrossRef]
- Paavonsalo, S.; Hariharan, S.; Lackman, M.H.; Karaman, S. Capillary Rarefaction in Obesity and Metabolic Diseases—Organ-Specificity and Possible Mechanisms. Cells 2020, 9, 2683. [Google Scholar] [CrossRef]
- Chantler, P.D.; Shrader, C.D.; Tabone, L.E.; D’Audiffret, A.C.; Huseynova, K.; Brooks, S.D.; Branyan, K.W.; Grogg, K.A.; Frisbee, J.C. Cerebral Cortical Microvascular Rarefaction in Metabolic Syndrome is Dependent on Insulin Resistance and Loss of Nitric Oxide Bioavailability. Microcirculation 2015, 22, 435–445. [Google Scholar] [CrossRef]
- Wardlaw, J.M.; Smith, E.E.; Biessels, G.J.; Cordonnier, C.; Fazekas, F.; Frayne, R.; Lindley, R.I.; O’Brien, J.T.; Barkhof, F.; Benavente, O.R.; et al. Neuroimaging standards for research into small vessel disease and its contribution to ageing and neurodegeneration. Lancet Neurol. 2013, 12, 822–838. [Google Scholar] [CrossRef]
- Owens, T.; Bechmann, I.; Engelhardt, B. Perivascular spaces and the two steps to neuroinflammation. J. Neuropathol. Exp. Neurol. 2008, 67, 1113–1121. [Google Scholar] [CrossRef]
- Hayden, M.R. The Brain Endothelial Cell Glycocalyx Plays a Crucial Role in The Development of Enlarged Perivascular Spaces in Obesity, Metabolic Syndrome and Type 2 Diabetes Mellitus. Life 2023, 13, 1955. [Google Scholar] [CrossRef]
- Banks, W.A.; Gray, A.M.; Erickson, M.A.; Salameh, T.S.; Damodarasamy, M.; Sheibani, N.; Meabon, J.S.; Wing, E.E.; Morofuji, Y.; Cook, D.G.; et al. Lipopolysaccharide-induced blood-brain barrier disruption: Roles of cyclooxygenase, oxidative stress, neuroinflammation, and elements of the neurovascular unit. J. Neuroinflamm. 2015, 12, 223. [Google Scholar] [CrossRef]
- Peng, X.; Luo, Z.; He, S.; Zhang, L.; Li, Y. Blood-Brain Barrier Disruption by Lipopolysaccharide and Sepsis-Associated Encephalopathy. Front. Cell. Infect. Microbiol. 2021, 11, 768108. [Google Scholar] [CrossRef]
- Erickson, M.A.; Shylyatnikova, T.; Banks, W.A.; Hayden, M.R. Ultrastructural Remodeling of the Blood-Brain Barrier and Neurovascular Unit by Lipopolysaccharide-Induced Neuroinflammation. Int. J. Mol. Sci. 2023, 24, 1640. [Google Scholar] [CrossRef]
- Kugler, E.C.; Greenwood, J.; MacDonald, R.B. The “Neuro-Glial-Vascular” Unit: The Role of Glia in Neurovascular Unit Formation and Dysfunction. Front. Cell Dev. Biol. 2021, 9, 732820. [Google Scholar] [CrossRef]
- Yuan, M.; Wang, Y.; Wang, S.; Huang, Z.; Jin, F.; Zou, Q.; Li, J.; Pu, Y.; Cai, Z. Bioenergetic Impairment in the Neuro-Glia-Vascular Unit: An Emerging Physiopathology during Aging. Aging Dis. 2021, 12, 2080–2095. [Google Scholar] [CrossRef]
- Hayden, M.R. Hypothesis: Astrocyte Foot Processes Detachment from the Neurovascular Unit in Female Diabetic Mice May Impair Modulation of Information Processing-Six Degrees of Separation. Brain Sci. 2019, 9, 83. [Google Scholar] [CrossRef]
- Díaz-Castro, B.; Robel, S.; Mishra, A. Astrocyte Endfeet in Brain Function and Pathology: Open Questions. Annu. Rev. Neurosci. 2023, 46, 101–121. [Google Scholar] [CrossRef]
- Milner, R.; Hung, S.; Wang, X.; Spatz, M.; del Zoppo, G.J. The rapid decrease in astrocyte-associated dystroglycan expression by focal cerebral ischemia is protease-dependent. J. Cereb. Blood Flow Metab. 2008, 28, 812–823. [Google Scholar] [CrossRef]
- Baeten, K.M.; Akassoglou, K. Extracellular Matrix and Matrix Receptors in Blood-Brain Barrier Formation and Stroke. Dev. Neurobiol. 2011, 71, 1018–1039. [Google Scholar] [CrossRef]
- Thomsen, M.S.; Routhe, L.J.; Moos, T. The vascular basement membrane in the healthy and pathological brain. J. Cereb. Blood Flow Metab. 2017, 37, 3300–3317. [Google Scholar] [CrossRef]
- Zaccaria, M.L.; Di Tommaso, F.; Brancaccio, A.; Paggi, P.; Petrucci, T.C. Dystroglycan distribution in adult mouse brain: A light and electron microscopy study. Neuroscience 2001, 104, 311–324. [Google Scholar] [CrossRef]
- Winder, S.J. The complexities of dystroglycan. Trends Biochem. Sci. 2001, 26, 118–124. [Google Scholar] [CrossRef]
- Figiel, I.; Bączyńska, E.; Wójtowicz, T.; Magnowska, M.; Buszka, A.; Bijata, M.; Włodarczyk, J. The cell adhesion protein dystroglycan affects the structural remodeling of dendritic spines. Sci. Rep. 2022, 12, 2506. [Google Scholar] [CrossRef]
- Mazaré, N.; Oudart, M.; Cohen-Salmon, M. Local translation in perisynaptic and perivascular astrocytic processes—A means to ensure astrocyte molecular and functional polarity? J. Cell Sci. 2021, 134, jcs251629. [Google Scholar] [CrossRef]
- Nagelhus, E.A.; Ottersen, O.P. Physiological Roles of Aquaporin-4 in Brain. Physiol. Rev. 2013, 93, 1543–1562. [Google Scholar] [CrossRef]
- Scharfman, H.E.; Binder, D.K. Aquaporin-4 water channels and synaptic plasticity in the hippocampus. Neurochem. Int. 2013, 63, 702–711. [Google Scholar] [CrossRef]
- Skucas, V.A.; Mathews, I.B.; Yang, J.; Cheng, Q.; Treister, A.; Duffy, A.M.; Verkman, A.S.; Hempstead, B.L.; Wood, M.A.; Binder, D.K.; et al. Impairment of select forms of spatial memory and neurotrophin-dependent synaptic plasticity by deletion of glial aquaporin-4. J. Neurosci. 2011, 31, 6392–6397. [Google Scholar] [CrossRef]
- González-Marrero, I.; Hernández-Abad, L.G.; González-Gómez, M.; Soto-Viera, M.; Carmona-Calero, E.M.; Castañeyra-Ruiz, L.; Castañeyra-Perdomo, A. Altered Expression of AQP1 and AQP4 in Brain Barriers and Cerebrospinal Fluid May Affect Cerebral Water Balance during Chronic Hypertension. Int. J. Mol. Sci. 2022, 23, 12277. [Google Scholar] [CrossRef]
- Li, Y.K.; Wang, F.; Wang, W.; Luo, Y.; Wu, P.F.; Xiao, J.L.; Hu, Z.L.; Jin, Y.; Hu, G.; Chen, J.G. Neuropsychopharmacology Aquaporin-4 deficiency impairs synaptic plasticity and associative fear memory in the lateral amygdala: Involvement of downregulation of glutamate transporter-1 expression. Neuropsychopharmacology 2012, 37, 1867–1878. [Google Scholar] [CrossRef]
- Papadopoulos, M.C.; Verkman, A.S. Aquaporin 4 and neuromyelitis optica. Lancet Neurol. 2012, 11, 535–544. [Google Scholar] [CrossRef]
- Jarius, S.; Paul, F.; Weinshenker, B.G.; Levy, M.; Kim, H.J.; Wildemann, B. Neuromyelitis optica. Nat. Rev. Dis. Primers 2020, 6, 85. [Google Scholar] [CrossRef]
- Mader, S.; Brimberg, L. Aquaporin-4 Water Channel in the Brain and Its Implication for Health and Disease. Cells 2019, 8, 90. [Google Scholar] [CrossRef]
- Huda, S.; Whittman, D.; Bhojak, M.; Chamberlain, J.; Noonan, C.; Jacob, A.; Kneen, R. Neuromyelitis optica spectrum disorders. Clin. Med. 2019, 19, 169–176. [Google Scholar] [CrossRef] [PubMed]
- Gomolka, R.S.; Hablitz, L.M.; Mestre, H.; Giannetto, M.; Du, T.; Hauglund, N.L.; Xie, L.; Peng, W.; Martinez, P.M.; Nedergaard, M.; et al. Loss of aquaporin-4 results in glymphatic system dysfunction via brain-wide interstitial fluid stagnation. eLife 2023, 12, e82232. [Google Scholar] [CrossRef] [PubMed]
- Teng, Z.; Wang, A.; Wang, P.; Wang, R.; Wang, W.; Han, H. The Effect of Aquaporin-4 Knockout on Interstitial Fluid Flow and the Structure of the Extracellular Space in the Deep Brain. Aging Dis. 2018, 9, 808–816. [Google Scholar] [CrossRef] [PubMed]
- Nielsen, S.; Nagelhus, E.A.; Amiry-Moghaddam, M.; Bourgue, C.; Agre, P.; Ottersen, O.P. Specialized Membrane Domains for Water Transport in Glial Cells: High-Resolution Immunogold Cytochemistry of Aquaporin-4 in Rat Brain. J. Neurosci. 1997, 17, 171–180. [Google Scholar] [CrossRef] [PubMed]
- Mestre, H.; Kostrikov, S.; Mehta, R.I.; Nedergaard, M. Perivascular Spaces, Glymphatic Dysfunction, and Small Vessel Disease. Clin. Sci. 2017, 131, 2257–2274. [Google Scholar] [CrossRef]
- Kress, B.T.; Iliff, J.J.; Xia, M.; Wang, M.; Wei, H.S.; Zeppenfeld, D.; Xie, L.; Kang, H.; Xu, Q.; Liew, J.A.; et al. Impairment of paravascular clearance pathways in the aging brain. Ann. Neurol. 2014, 76, 845–861. [Google Scholar] [CrossRef]
- Wang, M.; Ding, F.; Deng, S.; Guo, X.; Wang, W.; Iliff, J.J.; Nedergaard, M. Focal solute trapping and global glymphatic pathway impairment in a murine model of multiple microinfarcts. J. Neurosci. 2017, 37, 2870–2877. [Google Scholar] [CrossRef]
- Gaberel, T.; Gakuba, C.; Goulay, R.; Martinez De Lizarrondo, S.; Hanouz, J.L.; Emery, E.; Touze, E.; Vivien, D.; Gauberti, M. Impaired glymphatic perfusion after strokes revealed by contrast-enhanced MRI: A new target for fibrinolysis? Stroke 2014, 45, 3092–3096. [Google Scholar] [CrossRef]
- Peng, W.; Achariyar, T.M.; Li, B.; Liao, Y.; Mestre, H.; Hitomi, E.; Regan, S.; Kasper, T.; Peng, S.; Ding, F.; et al. Suppression of glymphatic fluid transport in a mouse model of Alzheimer’s disease. Neurobiol. Dis. 2016, 93, 215–225. [Google Scholar] [CrossRef]
- Schain, A.J.; Melo, A.; Strassman, A.M.; Burstein, R. Cortical spreading depression closes the paravascular space and impairs glymphatic flow: Implications for migraine headache. J. Neurosci. 2017, 37, 2904–2915. [Google Scholar] [CrossRef]
- Hachinski, V. Stroke and Potentially Preventable Dementias Proclamation: Updated World Stroke Day Proclamation. Stroke 2015, 46, 3039–3040. [Google Scholar] [CrossRef] [PubMed]
- Pantoni, L. Cerebral small vessel disease: From pathogenesis and clinical characteristics to therapeutic challenges. Lancet Neurol. 2010, 9, 689–701. [Google Scholar] [CrossRef] [PubMed]
- Wardlaw, J.M.; Beveniste, H.; Nedergaard, M.; Zlokovic, B.V.; Mestre, H.; Lee, H.; Doubal, F.N.; Brown, R.; Ramirez, J.; MacIntosh, B.J.; et al. Perivascular spaces in the brain: Anatomy, physiology and pathology. Nat. Rev. Neurol. 2020, 16, 137–153. [Google Scholar] [CrossRef] [PubMed]
- Joutel, A.; Monet-Leprêtre, M.; Gosele, C.; Baron-Menguy, C.; Hammes, A.; Schmidt, S.; Lemaire-Carrette, B.; Domenga, V.; Schedl, A.; Lacombe, P.; et al. Cerebrovascular dysfunction and microcirculation rarefaction precede white matter lesions in a mouse genetic model of cerebral ischemic small vessel disease. J. Clin. Investig. 2010, 120, 433–445. [Google Scholar] [CrossRef]
- Duperron, M.G.; Knol, M.J.; Le Grand, Q.; Evans, T.E.; Mishra, A.; Tsuchida, A.; Roshchupkin, G.; Konuma, T.; Trégouët, D.-A.; Romero, J.R.; et al. Genomics of perivascular space burden unravels early mechanisms of cerebral small vessel disease. Nat. Med. 2023, 29, 950–962. [Google Scholar] [CrossRef]
- Tarasoff-Conway, J.M.; Carare, R.O.; Osorio, R.S.; Glodzik, L.; Butler, T.; Fieremans, E.; Axel, L.; Rusinek, H.; Nicholson, C.; Zlokovic, B.V.; et al. Clearance systems in the brain—Implications for Alzheimer disease. Nat. Rev. Neurol. 2015, 11, 457–470. [Google Scholar] [CrossRef]
- Huentelman, M.J.; Talboom, J.S.; Lewis, C.R.; Chen, Z.; Barnes, C.A. Reinventing Neuroaging Research in the Digital Age. Trends Neurosci. 2020, 43, 17–23. [Google Scholar] [CrossRef]
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Hayden, M.R. Protoplasmic Perivascular Astrocytes Play a Crucial Role in the Development of Enlarged Perivascular Spaces in Obesity, Metabolic Syndrome, and Type 2 Diabetes Mellitus. Neuroglia 2023, 4, 307-328. https://doi.org/10.3390/neuroglia4040021
Hayden MR. Protoplasmic Perivascular Astrocytes Play a Crucial Role in the Development of Enlarged Perivascular Spaces in Obesity, Metabolic Syndrome, and Type 2 Diabetes Mellitus. Neuroglia. 2023; 4(4):307-328. https://doi.org/10.3390/neuroglia4040021
Chicago/Turabian StyleHayden, Melvin R. 2023. "Protoplasmic Perivascular Astrocytes Play a Crucial Role in the Development of Enlarged Perivascular Spaces in Obesity, Metabolic Syndrome, and Type 2 Diabetes Mellitus" Neuroglia 4, no. 4: 307-328. https://doi.org/10.3390/neuroglia4040021
APA StyleHayden, M. R. (2023). Protoplasmic Perivascular Astrocytes Play a Crucial Role in the Development of Enlarged Perivascular Spaces in Obesity, Metabolic Syndrome, and Type 2 Diabetes Mellitus. Neuroglia, 4(4), 307-328. https://doi.org/10.3390/neuroglia4040021