GLUT1 reductions exacerbate Alzheimer's disease vasculo-neuronal dysfunction and degeneration

Winkler et al . show that the glucose transporter GLUT1 in brain endothelium is necessary for the maintenance of proper brain capillary networks and blood-brain barrier integrity. The study also shows that loss of GLUT1 in a mouse model of Alzheimer's disease accelerates BBB breakdown, perfusio...

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Published in	Nature neuroscience Vol. 18; no. 4; pp. 521 - 530
Main Authors	Winkler, Ethan A, Nishida, Yoichiro, Sagare, Abhay P, Rege, Sanket V, Bell, Robert D, Perlmutter, David, Sengillo, Jesse D, Hillman, Sara, Kong, Pan, Nelson, Amy R, Sullivan, John S, Zhao, Zhen, Meiselman, Herbert J, Wenby, Rosalinda B, Soto, Jamie, Abel, E Dale, Makshanoff, Jacob, Zuniga, Edward, De Vivo, Darryl C, Zlokovic, Berislav V
Format	Journal Article
Language	English
Published	New York Nature Publishing Group US 01.04.2015 Nature Publishing Group
Subjects	13/51 14 14/19 14/69 38 38/109 42 42/44 631/378/1341 82 Alzheimer Disease - metabolism Alzheimer Disease - pathology Alzheimer Disease - physiopathology Alzheimer's disease Amyloid beta-Peptides - metabolism Animal Genetics and Genomics Animals Behavioral Sciences Biological Techniques Biomedicine Blood-brain barrier Blood-Brain Barrier - metabolism Blood-Brain Barrier - pathology Blood-Brain Barrier - physiopathology Brain research Cerebrovascular Circulation - physiology Dextrose Disease Models, Animal Endothelium Endothelium, Vascular - metabolism Endothelium, Vascular - pathology Endothelium, Vascular - physiopathology Glucose Glucose Transporter Type 1 - deficiency Medicine Mice Mice, Inbred C57BL Mice, Transgenic Neurobiology Neurodegeneration Neurons Neurosciences Peptides Physiological aspects New York Los Angeles California Iowa San Francisco California United States > US Iowa City Iowa California
Online Access	Get full text
ISSN	1097-6256 1546-1726
DOI	10.1038/nn.3966

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Abstract	Winkler et al . show that the glucose transporter GLUT1 in brain endothelium is necessary for the maintenance of proper brain capillary networks and blood-brain barrier integrity. The study also shows that loss of GLUT1 in a mouse model of Alzheimer's disease accelerates BBB breakdown, perfusion and metabolic stress resulting in behavioral deficits, elevated amyloid beta levels and neurodegeneration. The glucose transporter GLUT1 at the blood-brain barrier (BBB) mediates glucose transport into the brain. Alzheimer's disease is characterized by early reductions in glucose transport associated with diminished GLUT1 expression at the BBB. Whether GLUT1 reduction influences disease pathogenesis remains, however, elusive. Here we show that GLUT1 deficiency in mice overexpressing amyloid β-peptide (Aβ) precursor protein leads to early cerebral microvascular degeneration, blood flow reductions and dysregulation and BBB breakdown, and to accelerated amyloid β-peptide (Aβ) pathology, reduced Aβ clearance, diminished neuronal activity, behavioral deficits, and progressive neuronal loss and neurodegeneration that develop after initial cerebrovascular degenerative changes. We also show that GLUT1 deficiency in endothelium, but not in astrocytes, initiates the vascular phenotype as shown by BBB breakdown. Thus, reduced BBB GLUT1 expression worsens Alzheimer's disease cerebrovascular degeneration, neuropathology and cognitive function, suggesting that GLUT1 may represent a therapeutic target for Alzheimer's disease vasculo-neuronal dysfunction and degeneration.
AbstractList	The glucose transporter GLUT1 at the blood-brain barrier (BBB) mediates glucose transport into the brain. Alzheimer's disease is characterized by early reductions in glucose transport associated with diminished GLUT1 expression at the BBB. Whether GLUT1 reduction influences disease pathogenesis remains, however, elusive. Here we show that GLUT1 deficiency in mice overexpressing amyloid β-peptide (Aβ) precursor protein leads to early cerebral microvascular degeneration, blood flow reductions and dysregulation and BBB breakdown, and to accelerated amyloid β-peptide (Aβ) pathology, reduced Aβ clearance, diminished neuronal activity, behavioral deficits, and progressive neuronal loss and neurodegeneration that develop after initial cerebrovascular degenerative changes. We also show that GLUT1 deficiency in endothelium, but not in astrocytes, initiates the vascular phenotype as shown by BBB breakdown. Thus, reduced BBB GLUT1 expression worsens Alzheimer's disease cerebrovascular degeneration, neuropathology and cognitive function, suggesting that GLUT1 may represent a therapeutic target for Alzheimer's disease vasculo-neuronal dysfunction and degeneration. The glucose transporter GLUT1 at the blood-brain barrier (BBB) mediates glucose transport into the brain. Alzheimer's disease is characterized by early reductions in glucose transport associated with diminished GLUT1 expression at the BBB. Whether GLUT1 reduction influences disease pathogenesis remains, however, elusive. Here we show that GLUT1 deficiency in mice overexpressing amyloid beta -peptide (A beta ) precursor protein leads to early cerebral microvascular degeneration, blood flow reductions and dysregulation and BBB breakdown, and to accelerated amyloid beta -peptide (A beta ) pathology, reduced A beta clearance, diminished neuronal activity, behavioral deficits, and progressive neuronal loss and neurodegeneration that develop after initial cerebrovascular degenerative changes. We also show that GLUT1 deficiency in endothelium, but not in astrocytes, initiates the vascular phenotype as shown by BBB breakdown. Thus, reduced BBB GLUT1 expression worsens Alzheimer's disease cerebrovascular degeneration, neuropathology and cognitive function, suggesting that GLUT1 may represent a therapeutic target for Alzheimer's disease vasculo-neuronal dysfunction and degeneration. Winkler et al . show that the glucose transporter GLUT1 in brain endothelium is necessary for the maintenance of proper brain capillary networks and blood-brain barrier integrity. The study also shows that loss of GLUT1 in a mouse model of Alzheimer's disease accelerates BBB breakdown, perfusion and metabolic stress resulting in behavioral deficits, elevated amyloid beta levels and neurodegeneration. The glucose transporter GLUT1 at the blood-brain barrier (BBB) mediates glucose transport into the brain. Alzheimer's disease is characterized by early reductions in glucose transport associated with diminished GLUT1 expression at the BBB. Whether GLUT1 reduction influences disease pathogenesis remains, however, elusive. Here we show that GLUT1 deficiency in mice overexpressing amyloid β-peptide (Aβ) precursor protein leads to early cerebral microvascular degeneration, blood flow reductions and dysregulation and BBB breakdown, and to accelerated amyloid β-peptide (Aβ) pathology, reduced Aβ clearance, diminished neuronal activity, behavioral deficits, and progressive neuronal loss and neurodegeneration that develop after initial cerebrovascular degenerative changes. We also show that GLUT1 deficiency in endothelium, but not in astrocytes, initiates the vascular phenotype as shown by BBB breakdown. Thus, reduced BBB GLUT1 expression worsens Alzheimer's disease cerebrovascular degeneration, neuropathology and cognitive function, suggesting that GLUT1 may represent a therapeutic target for Alzheimer's disease vasculo-neuronal dysfunction and degeneration.
Audience	Academic
Author	Zhao, Zhen Sagare, Abhay P Hillman, Sara Zlokovic, Berislav V Bell, Robert D Rege, Sanket V Abel, E Dale Makshanoff, Jacob Nelson, Amy R Sullivan, John S Meiselman, Herbert J Zuniga, Edward Perlmutter, David Sengillo, Jesse D Kong, Pan Soto, Jamie De Vivo, Darryl C Winkler, Ethan A Nishida, Yoichiro Wenby, Rosalinda B
Author_xml	– sequence: 1 givenname: Ethan A surname: Winkler fullname: Winkler, Ethan A organization: Zilkha Neurogenetic Institute, Keck School of Medicine, University of Southern California, Department of Neurological Surgery, University of California San Francisco – sequence: 2 givenname: Yoichiro surname: Nishida fullname: Nishida, Yoichiro organization: Center for Neurodegenerative and Vascular Brain Disorders, University of Rochester School of Medicine & Dentistry, Rochester, Department of Neurology and Neurological Science, Graduate School, Tokyo Medical and Dental University – sequence: 3 givenname: Abhay P surname: Sagare fullname: Sagare, Abhay P organization: Zilkha Neurogenetic Institute, Keck School of Medicine, University of Southern California – sequence: 4 givenname: Sanket V surname: Rege fullname: Rege, Sanket V organization: Zilkha Neurogenetic Institute, Keck School of Medicine, University of Southern California – sequence: 5 givenname: Robert D surname: Bell fullname: Bell, Robert D organization: Center for Neurodegenerative and Vascular Brain Disorders, University of Rochester School of Medicine & Dentistry, Rochester – sequence: 6 givenname: David surname: Perlmutter fullname: Perlmutter, David organization: Center for Neurodegenerative and Vascular Brain Disorders, University of Rochester School of Medicine & Dentistry, Rochester – sequence: 7 givenname: Jesse D surname: Sengillo fullname: Sengillo, Jesse D organization: Zilkha Neurogenetic Institute, Keck School of Medicine, University of Southern California, Center for Neurodegenerative and Vascular Brain Disorders, University of Rochester School of Medicine & Dentistry, Rochester – sequence: 8 givenname: Sara surname: Hillman fullname: Hillman, Sara organization: Center for Neurodegenerative and Vascular Brain Disorders, University of Rochester School of Medicine & Dentistry, Rochester – sequence: 9 givenname: Pan surname: Kong fullname: Kong, Pan organization: Zilkha Neurogenetic Institute, Keck School of Medicine, University of Southern California – sequence: 10 givenname: Amy R surname: Nelson fullname: Nelson, Amy R organization: Zilkha Neurogenetic Institute, Keck School of Medicine, University of Southern California – sequence: 11 givenname: John S surname: Sullivan fullname: Sullivan, John S organization: Zilkha Neurogenetic Institute, Keck School of Medicine, University of Southern California – sequence: 12 givenname: Zhen surname: Zhao fullname: Zhao, Zhen organization: Zilkha Neurogenetic Institute, Keck School of Medicine, University of Southern California – sequence: 13 givenname: Herbert J surname: Meiselman fullname: Meiselman, Herbert J organization: Department of Physiology and Biophysics, Keck School of Medicine, University of Southern California – sequence: 14 givenname: Rosalinda B surname: Wenby fullname: Wenby, Rosalinda B organization: Department of Physiology and Biophysics, Keck School of Medicine, University of Southern California – sequence: 15 givenname: Jamie surname: Soto fullname: Soto, Jamie organization: Fraternal Order of Eagles Diabetes Research Center, University of Iowa, Division of Endocrinology and Metabolism, Carver College of Medicine, University of Iowa – sequence: 16 givenname: E Dale surname: Abel fullname: Abel, E Dale organization: Fraternal Order of Eagles Diabetes Research Center, University of Iowa, Division of Endocrinology and Metabolism, Carver College of Medicine, University of Iowa – sequence: 17 givenname: Jacob surname: Makshanoff fullname: Makshanoff, Jacob organization: Zilkha Neurogenetic Institute, Keck School of Medicine, University of Southern California – sequence: 18 givenname: Edward surname: Zuniga fullname: Zuniga, Edward organization: Zilkha Neurogenetic Institute, Keck School of Medicine, University of Southern California – sequence: 19 givenname: Darryl C surname: De Vivo fullname: De Vivo, Darryl C organization: Colleen Giblin Laboratories for Pediatric Neurology Research, Columbia University – sequence: 20 givenname: Berislav V surname: Zlokovic fullname: Zlokovic, Berislav V email: zlokovic@usc.edu organization: Zilkha Neurogenetic Institute, Keck School of Medicine, University of Southern California, Department of Physiology and Biophysics, Keck School of Medicine, University of Southern California
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/25730668$$D View this record in MEDLINE/PubMed
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Snippet	Winkler et al . show that the glucose transporter GLUT1 in brain endothelium is necessary for the maintenance of proper brain capillary networks and... The glucose transporter GLUT1 at the blood-brain barrier (BBB) mediates glucose transport into the brain. Alzheimer's disease is characterized by early...
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SubjectTerms	13/51 14 14/19 14/69 38 38/109 42 42/44 631/378/1341 82 Alzheimer Disease - metabolism Alzheimer Disease - pathology Alzheimer Disease - physiopathology Alzheimer's disease Amyloid beta-Peptides - metabolism Animal Genetics and Genomics Animals Behavioral Sciences Biological Techniques Biomedicine Blood-brain barrier Blood-Brain Barrier - metabolism Blood-Brain Barrier - pathology Blood-Brain Barrier - physiopathology Brain research Cerebrovascular Circulation - physiology Dextrose Disease Models, Animal Endothelium Endothelium, Vascular - metabolism Endothelium, Vascular - pathology Endothelium, Vascular - physiopathology Glucose Glucose Transporter Type 1 - deficiency Medicine Mice Mice, Inbred C57BL Mice, Transgenic Neurobiology Neurodegeneration Neurons Neurosciences Peptides Physiological aspects
Title	GLUT1 reductions exacerbate Alzheimer's disease vasculo-neuronal dysfunction and degeneration
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