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Citations to this article

Human blood-brain barrier receptors for Alzheimer's amyloid-beta 1- 40. Asymmetrical binding, endocytosis, and transcytosis at the apical side of brain microvascular endothelial cell monolayer.
J B Mackic, … , B Frangione, B V Zlokovic
J B Mackic, … , B Frangione, B V Zlokovic
Published August 15, 1998
Citation Information: J Clin Invest. 1998;102(4):734-743. https://doi.org/10.1172/JCI2029.
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Human blood-brain barrier receptors for Alzheimer's amyloid-beta 1- 40. Asymmetrical binding, endocytosis, and transcytosis at the apical side of brain microvascular endothelial cell monolayer.

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Abstract

A soluble monomeric form of Alzheimer's amyloid-beta (1-40) peptide (sAbeta1-40) is present in the circulation and could contribute to neurotoxicity if it crosses the brain capillary endothelium, which comprises the blood-brain barrier (BBB) in vivo. This study characterizes endothelial binding and transcytosis of a synthetic peptide homologous to human sAbeta1-40 using an in vitro model of human BBB. 125I-sAbeta1-40 binding to the brain microvascular endothelial cell monolayer was time dependent, polarized to the apical side, and saturable with high- and low-affinity dissociation constants of 7.8+/-1.2 and 52.8+/-6.2 nM, respectively. Binding of 125I-sAbeta1-40 was inhibited by anti-RAGE (receptor for advanced glycation end products) antibody (63%) and by acetylated low density lipoproteins (33%). Consistent with these data, transfected cultured cells overexpressing RAGE or macrophage scavenger receptor (SR), type A, displayed binding and internalization of 125I-sAbeta1-40. The internalized peptide remains intact > 94%. Transcytosis of 125I-sAbeta1-40 was time and temperature dependent, asymmetrical from the apical to basolateral side, saturable with a Michaelis constant of 45+/-9 nM, and partially sensitive to RAGE blockade (36%) but not to SR blockade. We conclude that RAGE and SR mediate binding of sAbeta1-40 at the apical side of human BBB, and that RAGE is also involved in sAbeta1-40 transcytosis.

Authors

J B Mackic, M Stins, J G McComb, M Calero, J Ghiso, K S Kim, S D Yan, D Stern, A M Schmidt, B Frangione, B V Zlokovic

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JM Englert, LE Hanford, N Kaminski, JM Tobolewski, RJ Tan, CL Fattman, L Ramsgaard, TJ Richards, I Loutaev, PP Nawroth, M Kasper, A Bierhaus, TD Oury
The American Journal of Pathology 2008
RAGE recycles at the plasma membrane in S100B secretory vesicles and promotes Schwann cells morphological changes
L Perrone, G Peluso, MA Melone
Journal of Cellular Physiology 2008
The role of the cell surface LRP and soluble LRP in blood-brain barrier Abeta clearance in Alzheimer's disease
R Deane, A Sagare, BV Zlokovic
Current pharmaceutical design 2008
Apolipoprotein E, Amyloid-??, and Blood-Brain Barrier Permeability in Alzheimer Disease
JE Donahue, CE Johanson
Journal of Neuropathology and Experimental Neurology 2008
Effects of ginkgo biloba extract EGb761 on expression of RAGE and LRP-1 in cerebral microvascular endothelial cells under chronic hypoxia and hypoglycemia
FL Yan, Y Zheng, FD Zhao
Acta Neuropathologica 2008
Clearance mechanisms of Alzheimer's amyloid-β peptide: implications for therapeutic design and diagnostic tests
KA Bates, G Verdile, QX Li, D Ames, P Hudson, CL Masters, RN Martins
Molecular Psychiatry 2008
The role of peptides in blood-brain barrier nanotechnology
M Teixidó, E Giralt
Journal of Peptide Science 2008
Receptor for Advanced Glycation End Products Is Subjected to Protein Ectodomain Shedding by Metalloproteinases
L Zhang, M Bukulin, E Kojro, A Roth, VV Metz, F Fahrenholz, PP Nawroth, A Bierhaus, R Postina
The Journal of biological chemistry 2008
Drug Addiction
RS Rapaka, W Sadée
2008
Heat shock proteins and amateur chaperones in amyloid-Beta accumulation and clearance in Alzheimer's disease
MM Wilhelmus, RM de Waal, MM Verbeek
Molecular Neurobiology 2007
Protein Misfolding, Aggregation, and Conformational Diseases
VN Uversky, AL Fink
2007
Dissociation of ERK and Akt signaling in endothelial cell angiogenic responses to beta-amyloid
J Magrane, RA Christensen, KM Rosen, V Veereshwarayya, HW Querfurth
Experimental Cell Research 2006
Transport pathways for clearance of human Alzheimer's amyloid beta-peptide and apolipoproteins E and J in the mouse central nervous system
RD Bell, AP Sagare, AE Friedman, GS Bedi, DM Holtzman, R Deane, BV Zlokovic
Journal of Cerebral Blood Flow & Metabolism 2006
Major Involvement of Low-Density Lipoprotein Receptor-Related Protein 1 in the Clearance of Plasma Free Amyloid β-Peptide by the Liver
C Tamaki, S Ohtsuki, T Iwatsubo, T Hashimoto, K Yamada, C Yabuki, T Terasaki
Pharmaceutical Research 2006
Mechanism of Cerebral β-Amyloid Angiopathy: Murine and Cellular Models
MC Herzig, WE Nostrand, M Jucker
Brain Pathology 2006
The −374 T/A polymorphism in the gene encoding RAGE is associated with diabetic nephropathy and retinopathy in type 1 diabetic patients
E Lindholm, E Bakhtadze, M Sjögren, CM Cilio, E Agardh, L Groop, CD Agardh
Diabetologia 2006
CNS drug delivery: Opioid peptides and the blood-brain barrier
KA Witt, TP Davis
The AAPS Journal 2006
RAGE, LRP-1, and amyloid-beta protein in Alzheimer’s disease
JE Donahue, SL Flaherty, CE Johanson, JA Duncan, GD Silverberg, MC Miller, R Tavares, W Yang, Q Wu, E Sabo, V Hovanesian, EG Stopa
Acta Neuropathologica 2006
ε-Glycation, APP and Aβ in ageing and Alzheimer disease: A hypothesis
HP Schmitt
Medical Hypotheses 2006
Understanding RAGE, the receptor for advanced glycation end products
A Bierhaus, PM Humpert, M Morcos, T Wendt, T Chavakis, B Arnold, DM Stern, PP Nawroth
Journal of Molecular Medicine 2005
Evaluation of rage isoforms, ligands, and signaling in the brain
Q Ding, JN Keller
Biochimica et Biophysica Acta (BBA) - Molecular Cell Research 2005
Colloidal carriers and blood–brain barrier (BBB) translocation: A way to deliver drugs to the brain?
E Garcia-Garcia, K Andrieux, S Gil, P Couvreur
International Journal of Pharmaceutics 2005
Permeability Studies on In Vitro Blood–Brain Barrier Models: Physiology, Pathology, and Pharmacology
MA Deli, CS Ábrahám, Y Kataoka, M Niwa
Cellular and Molecular Neurobiology 2005
Role of the MEOX2 homeobox gene in neurovascular dysfunction in Alzheimer disease
Z Wu, H Guo, N Chow, J Sallstrom, RD Bell, R Deane, AI Brooks, S Kanagala, A Rubio, A Sagare, D Liu, F Li, D Armstrong, T Gasiewicz, R Zidovetzki, X Song, F Hofman, BV Zlokovic
Nature Medicine 2005
International Review of Neurobiology
ZT Bloomgarden
International review of neurobiology 2005
The Blood-Brain Barrier and Its Microenvironment: Basic Physiology to Neurological Disease
H Wolburg, A Warth
The Blood-Brain Barrier and Its Microenvironment: Basic Physiology to Neurological Disease 2005
The choroid plexus removes beta-amyloid from brain cerebrospinal fluid
JS Crossgrove, GJ Li, W Zheng
Experimental biology and medicine (Maywood, N.J.) 2005
RAGE and amyloid beta interactions: Atomic force microscopy and molecular modeling
MO Chaney, WB Stine, TA Kokjohn, YM Kuo, C Esh, A Rahman, DC Luehrs, AM Schmidt, D Stern, SD Yan, AE Roher
Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease 2005
The Choroid Plexus Removes β-Amyloid from Brain Cerebrospinal Fluid
JS Crossgrove, GJ Li, W Zheng
Experimental biology and medicine (Maywood, N.J.) 2005
Physiological Roles of Amyloid-?? and Implications for its Removal in Alzheimer???s Disease:
GM Bishop, SR Robinson
Drugs & Aging 2004
LRP/Amyloid β-Peptide Interaction Mediates Differential Brain Efflux of Aβ Isoforms
R Deane, Z Wu, A Sagare, J Davis, SD Yan, K Hamm, F Xu, M Parisi, B LaRue, HW Hu, P Spijkers, H Guo, X Song, PJ Lenting, WE van Nostrand, BV Zlokovic
Neuron 2004
Method for measurement of the blood–brain barrier permeability in the perfused mouse brain: application to amyloid-β peptide in wild type and Alzheimer’s Tg2576 mice
B LaRue, E Hogg, A Sagare, S Jovanovic, L Maness, C Maurer, R Deane, BV Zlokovic
Journal of Neuroscience Methods 2004
Blood-Spinal Cord and Brain Barriers in Health and Disease
E Anderson, L Ryan, H Xiong, S Swindells, J Zheng, HE Gendelman
Blood-Spinal Cord and Brain Barriers in Health and Disease 2004
Peripheral treatment with enoxaparin, a low molecular weight heparin, reduces plaques and beta-amyloid accumulation in a mouse model of Alzheimer's disease
L Bergamaschini, E Rossi, C Storini, S Pizzimenti, M Distaso, C Perego, AD Luigi, C Vergani, MG de Simoni
The Journal of neuroscience : the official journal of the Society for Neuroscience 2004
Systemic Catabolism of Alzheimer's Aβ40 and Aβ42
J Ghiso, M Shayo, M Calero, D Ng, Y Tomidokoro, S Gandy, A Rostagno, B Frangione
The Journal of biological chemistry 2004
Amyloid β(1–42) and its β(25–35) fragment induce activation and membrane translocation of cytosolic phospholipase A2 in bovine retina capillary pericytes
CD Anfuso, G Assero, G Lupo, A Nicotra, G Cannavò, RP Strosznajder, P Rapisarda, R Pluta, M Alberghina
Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids 2004
RAGE mediates amyloid-β peptide transport across the blood-brain barrier and accumulation in brain
R Deane, SD Yan, RK Submamaryan, B LaRue, S Jovanovic, E Hogg, D Welch, L Manness, C Lin, J Yu, H Zhu, J Ghiso, B Frangione, A Stern, AM Schmidt, DL Armstrong, B Arnold, B Liliensiek, P Nawroth, F Hofman, M Kindy, D Stern, B Zlokovic
Nature Medicine 2003
International Textbook of Diabetes Mellitus
RA DeFronzo, L Mandarino, E Ferrannini
International Textbook of Diabetes Mellitus 2003
THEROLE OFDRUGTRANSPORTERS AT THEBLOOD-BRAINBARRIER
AG Boer, IC der Sandt, PJ Gaillard
Annual Review of Pharmacology and Toxicology 2003
A simple method for isolation and characterization of mouse brain microvascular endothelial cells
Z Wu, FM Hofman, BV Zlokovic
Journal of Neuroscience Methods 2003
Alzheimer’s Disease
DS Vohora, LC Mishra
Scientific Basis for Ayurvedic Therapies 2003
T HE R OLE OF D RUG T RANSPORTERS AT THE B LOOD -B RAIN B ARRIER
AG Boer, IC der Sandt, PJ Gaillard
Annual Review of Pharmacology and Toxicology 2003
Transcytosis: Crossing Cellular Barriers
PL Tuma, AL Hubbard
Physiological reviews 2003
Activated protein C blocks p53-mediated apoptosis in ischemic human brain endothelium and is neuroprotective
T Cheng, D Liu, JH Griffin, JA Fernández, F Castellino, ED Rosen, K Fukudome, BV Zlokovic
Nature Medicine 2003
Amyloid Peptide-Induced Cytokine and Chemokine Expression in THP-1 Monocytes Is Blocked by Small Inhibitory RNA Duplexes for Early Growth Response-1 Messenger RNA
RK Giri, SK Selvaraj, VK Kalra
Journal of immunology (Baltimore, Md. : 1950) 2003
Sporadic and Familial Cerebral Amyloid Angiopathies
T Revesz, JL Holton, T Lashley, G Plant, A Rostagno, J Ghiso, B Frangione
Brain Pathology 2002
Human antibodies against amyloid β peptide: A potential treatment for Alzheimer's disease: Human Antibodies against Amyloid β Peptide
R Dodel, H Hampel, C Depboylu, S Lin, F Gao, S Schock, S Jäckel, X Wei, K Buerger, C Höft, B Hemmer, HJ Möller, M Farlow, WH Oertel, N Sommer, Y Du
Annals of Neurology 2002
Circulating amyloid-β peptide crosses the blood–brain barrier in aged monkeys and contributes to Alzheimer's disease lesions
JB Mackic, J Bading, J Ghiso, L Walker, T Wisniewski, B Frangione, BV Zlokovic
Vascular Pharmacology 2002
Cyclooxygenase-2-positive macrophages infiltrate the Alzheimer's disease brain and damage the blood-brain barrier
M Fiala, QN Liu, J Sayre, V Pop, V Brahmandam, MC Graves, HV Vinters
European Journal of Clinical Investigation 2002
Heparin attenuates cytotoxic and inflammatory activity of Alzheimer amyloid-β in vitro
L Bergamaschini, C Donarini, E Rossi, AD Luigi, C Vergani, MG de Simoni
Neurobiology of Aging 2002
Intracellular accumulation of β-amyloid1–42 in neurons is facilitated by the α7 nicotinic acetylcholine receptor in Alzheimer’s disease
RG Nagele, MR D’Andrea, WJ Anderson, HY Wang
Neuroscience 2002
Universes in Delicate Balance
RH Miller, S Robinson
Universes in Delicate Balance 2002
BSE: a consequence of cattle feeding with glycated molecules host-unknown?
J Boratyński, A Górski
Medical Hypotheses 2002
Aβ 42 -induced Increase in Neprilysin Is Associated with Prevention of Amyloid Plaque Formation in Vivo
MH Mohajeri, MA Wollmer, RM Nitsch
The Journal of biological chemistry 2002
Antibodies to β-Amyloid Decrease the Blood-to-Brain Transfer of β-Amyloid Peptide 1
W Pan, B Solomon, LM Maness, AJ Kastin
Experimental biology and medicine (Maywood, N.J.) 2002
Diabetes and advanced glycation endproducts
H Vlassara, MR Palace
Journal of Internal Medicine 2002
Effect of endothelial cell polarity on β-amyloid-induced migration of monocytes across normal and AD endothelium
R Giri, S Selvaraj, CA Miller, F Hofman, SD Yan, D Stern, BV Zlokovic, VK Kalra
American journal of physiology. Cell physiology 2002
Noninvasive Imaging of Peripherally Injected Alzheimer's Disease Type Synthetic Aβ Amyloid In Vivo
JR Marshall, ER Stimson, JR Ghilardi, HV Vinters, PW Mantyh, JE Maggio
Bioconjugate Chemistry 2002
The AGE-receptor in the pathogenesis of diabetic complications
H Vlassara
Diabetes/Metabolism Research and Reviews 2001
Peptide drug modifications to enhance bioavailability and blood-brain barrier permeability
KA Witt, TJ Gillespie, JD Huber, RD Egleton, TP Davis
Peptides 2001
α2-Macroglobulin-Mediated Degradation of Amyloid β1–42: A Mechanism to Enhance Amyloid β Catabolism
D Lauer, A Reichenbach, G Birkenmeier
Experimental Neurology 2001
Bacterial invasion and transcytosis in transfected human brain microvascular endothelial cells
MF Stins, J Badger, KS Kim
Microbial Pathogenesis 2001
Neuroinflammatory Mechanisms in Alzheimer’s Disease Basic and Clinical Research
J Rogers
2001
The chemokine receptor CCR2 mediates the binding and internalization of monocyte chemoattractant protein-1 along brain microvessels
K A Dzenko, A V Andjelkovic, W A Kuziel, J S Pachter
The Journal of neuroscience : the official journal of the Society for Neuroscience 2001
The Chemokine Receptor CCR2 Mediates the Binding and Internalization of Monocyte Chemoattractant Protein-1 along Brain Microvessels
Dzenko KA, Andjelkovic AV, Kuziel WA, Pachter JS
Journal of Neuroscience 2001
Clearance of Alzheimer's amyloid beta1-40 peptide from brain by low-density lipoprotein receptor-related protein-1 at the blood-brain barrier
Masayoshi Shibata, Shinya Yameda,Ram Kumar, Miguel Calero,ar, James Bading, Blas Frangione, David Holtzman, Carol A. Miller, Dudley K. Strickland,Jorge Ghiso, Berislav V. Zlokovic
Journal of Clinical Investigation 2000
Apolipoprotein J (clusterin) and Alzheimer's disease
M Calero, A Rostagno, E Matsubara, B Zlokovic, B Frangione, J Ghiso
Microscopy Research and Technique 2000
Mechanisms of Cerebrovascular Amyloid Deposition: Lessons from Mouse Models
P Burgermeister, ME Calhoun, DT Winkler, M Jucker
Annals of the New York Academy of Sciences 2000
Improved bioavailability to the brain of glycosylated Met-enkephalin analogs
RD Egleton, SA Mitchell, JD Huber, J Janders, D Stropova, R Polt, HI Yamamura, VJ Hruby, TP Davis
Brain Research 2000
The biology of the receptor for advanced glycation end products and its ligands
A M Schmidt, S D Yan, S F Yan, D M Stern
Biochimica et Biophysica Acta 2000
Cellular cofactors potentiating induction of stress and cytotoxicity by amyloid beta-peptide
S D Yan, A Roher, M Chaney, B Zlokovic, A M Schmidt, D Stern
Biochimica et Biophysica Acta 2000
β-Amyloid-induced migration of monocytes across human brain endothelial cells involves RAGE and PECAM-1
R Giri, Y Shen, M Stins, SD Yan, AM Schmidt, D Stern, KS Kim, B Zlokovic, VK Kalra
American journal of physiology. Cell physiology 2000
Clearance of amyloid β-peptide from brain: transport or metabolism?
BV Zlokovic, S Yamada, D Holtzman, J Ghiso, B Frangione
Nature Medicine 2000
Differential Regulation of Leptin Transport by the Choroid Plexus and Blood-Brain Barrier and High Affinity Transport Systems for Entry into Hypothalamus and Across the Blood-Cerebrospinal Fluid Barrier*
BV Zlokovic, S Jovanovic, W Miao, S Samara, S Verma, CL Farrell
Endocrinology 2000
Reply to: 'Clearance of amyloid β-peptide from brain: transport or metabolism?'
N Iwata, S Tsubuki, E Hama, Y Takaki, K Shirotani, TC Saido
Nature Medicine 2000
Cerebral Amyloid Angiopathy in Alzheimer’s Disease and Related Disorders
MM Verbeek, RM de Waal, HV Vinters
2000
Pentosan polysulfate regulates scavenger receptor-mediated, but not fluid-phase, endocytosis in immortalized cerebral endothelial cells
M A Deli, C S Abrahám, H Takahata, S Katamine, M Niwa
Cellular and Molecular Neurobiology 2000
Cellular Cofactors for Amyloid β-Peptide-Induced Cell Stress
SD Yan, A Roher, AM Schmidt, DM Stern
The American Journal of Pathology 1999
Cellular cofactors for amyloid beta-peptide-induced cell stress. Moving from cell culture to in vivo
SD Yan, A Roher, AM Schmidt, DM Stern
The American Journal of Pathology 1999
RAGE Mediates a Novel Proinflammatory Axis
MA Hofmann, S Drury, C Fu, W Qu, A Taguchi, Y Lu, C Avila, N Kambham, A Bierhaus, P Nawroth, MF Neurath, T Slattery, D Beach, J McClary, M Nagashima, J Morser, D Stern, AM Schmidt
Cell 1999
The evolution of Alzheimer disease, the reproductive schedule, and apoE isoforms☆
CE Finch, RM Sapolsky
Neurobiology of Aging 1999
Neuroprotective approaches in experimental models of β-Amyloid neurotoxicity: Relevance to Alzheimer's disease
T Harkany, T Hortobágyi, M Sasvári, C Kónya, B Penke, PG Luiten, N Csaba
Progress in Neuro-Psychopharmacology and Biological Psychiatry 1999
cDNA cloning of a novel secreted isoform of the human receptor for advanced glycation end products and characterization of cells co-expressing cell-surface scavenger receptors and Swedish mutant amyloid precursor protein
P Malherbe, JG Richards, H Gaillard, A Thompson, C Diener, A Schuler, G Huber
Molecular Brain Research 1999
Cereport (RMP-7) increases the permeability of human brain microvascular endothelial cell monolayers
J B Mackic, M Stins, S Jovanovic, K S Kim, R T Bartus, B V Zlokovic
Pharmaceutical Research 1999

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