Lipopolysaccharide alters the blood–brain barrier transport of amyloid β protein: A mechanism for inflammation in the progression of Alzheimer’s disease
Open accessAbstract
Alzheimer's disease (AD) brains are characterized by accumulation of amyloid beta protein (Abeta) and neuroinflammation. Increased blood-to-brain influx and decreased brain-to-blood efflux across the blood-brain barrier (BBB) have been proposed as mechanisms for Abeta accumulation. Epidemiological studies suggest that the nonsteroidal anti-inflammatory drug (NSAID) indomethacin slows the progression of AD. We hypothesized that inflammation alters BBB handling of Abeta. Mice treated with lipopolysaccharide (LPS) had increased brain influx and decreased brain efflux of Abeta, recapitulating the findings in AD. Neither influx nor efflux was mediated by LPS acting directly on BBB cells. Increased influx was mediated by a blood-borne factor, indomethacin-independent, blocked by the triglyceride triolein, and not related to expression of the blood-to-brain transporter of Abeta, RAGE. Serum levels of IL-6, IL-10, IL-13, and MCP-1 mirrored changes in Abeta influx. Decreased efflux was blocked by indomethacin and accompanied by decreased protein expression of the brain-to-blood transporter of Abeta, LRP-1. LPS paradoxically increased expression of neuronal LRP-1, a major source of Abeta. Thus, inflammation potentially increases brain levels of Abeta by three mechanisms: increased influx, decreased efflux, and increased neuronal production.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
High plasma levels of endotoxin can increase permeability of the blood-brain barrier, allowing toxic plasma components, including amyloid β and α-synuclein into the brain.
“High plasma levels of endotoxin can increase permeability of the blood-brain barrier, allowing toxic plasma components, including amyloid β and α-synuclein into the brain [49–51].”
From The endotoxin hypothesis of neurodegeneration (2019) · cites this paper as [51]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Colowick, S. P., Joshi, M. D., Jagannathan, & KAPLAN, N. O. (1966) · Cited by 26,137 · see citing works
The Amyloid Hypothesis of Alzheimer’s Disease: Progress and Problems on the Road to Therapeutics
Hardy, J., & Selkoe, D. J. (2002) · Science · doi:10.1126/science.1072994 · Cited by 13,864 · see citing works
Amyloid oligomers exacerbate tau pathology in a mouse model of tauopathy
Selenica, M.-L. B., Brownlow, M., Jimenez, J. P., Lee, D. C., Pena, G., Dickey, C. A., Gordon, M. N., & Morgan, D. (2013) · Neurodegenerative Diseases · doi:10.1159/000337230 · Cited by 10,359 · see citing works
Graphical Evaluation of Blood-to-Brain Transfer Constants from Multiple-Time Uptake Data
Patlak, C. S., Blasberg, R. G., & Fenstermacher, J. D. (1983) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.1983.1 · Cited by 3,565 · see citing works
Systemic LPS causes chronic neuroinflammation and progressive neurodegeneration
Qin, L., Wu, X., Block, M. L., Liu, Y., Breese, G. R., Hong, J., Knapp, D. J., & Crews, F. T. (2007) · Glia · doi:10.1002/glia.20467 · Cited by 2,144 · see citing works
RAGE mediates amyloid-β peptide transport across the blood-brain barrier and accumulation in brain
Deane, R., Du Yan, S., Submamaryan, R. K., LaRue, B., Jovanovic, S., Hogg, E., Welch, D., Manness, L., Lin, C., Yu, J., et al. (2003) · Nature Medicine · doi:10.1038/nm890 · Cited by 1,426 · see citing works
Shibata, M., Yamada, S., Kumar, S. R., Calero, M., Bading, J., Frangione, B., Holtzman, D. M., Miller, C. A., Strickland, D. K., Ghiso, J., et al. (2000) · Journal of Clinical Investigation · doi:10.1172/jci10498 · Cited by 1,413 · see citing works
Evidence of oxidative damage in Alzheimer's disease brain: central role for amyloid β-peptide
Butterfield, D. A., Drake, J., Pocernich, C., & Castegna, A. (2001) · Trends in Molecular Medicine · doi:10.1016/s1471-4914(01)02173-6 · Cited by 1,114 · see citing works
LRP/Amyloid β-Peptide Interaction Mediates Differential Brain Efflux of Aβ Isoforms
Deane, R., Wu, Z., Sagare, A., Davis, J., Du Yan, S., Hamm, K., Xu, F., Parisi, M., LaRue, B., Hu, H. W., et al. (2004) · Neuron · doi:10.1016/j.neuron.2004.07.017 · Cited by 828 · see citing works
Lillis, A. P., Duyn, L. B. V., Murphy-Ullrich, J. E., & Strickland, D. K. (2008) · Physiological Reviews · doi:10.1152/physrev.00033.2007 · Cited by 702 · see citing works
Bell, R. D., Sagare, A. P., Friedman, A. E., Bedi, G. S., Holtzman, D. M., Deane, R., & Zlokovic, B. V. (2007) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/sj.jcbfm.9600419 · Cited by 670 · see citing works
Transport of α-Aminoisobutyric Acid across Brain Capillary and Cellular Membranes
Blasberg, R. G., Fenstermacher, J. D., & Patlak, C. S. (1983) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.1983.2 · Cited by 517 · see citing works
Triglycerides Induce Leptin Resistance at the Blood-Brain Barrier
Banks, W. A., Coon, A. B., Robinson, S. M., Moinuddin, A., Shultz, J. M., Nakaoke, R., & Morley, J. E. (2004) · Diabetes · doi:10.2337/diabetes.53.5.1253 · Cited by 512 · see citing works
Self-citationStrategies to advance translational research into brain barriers
Neuwelt, E., Abbott, N. J., Abrey, L., Banks, W. A., Blakley, B., Davis, T., Engelhardt, B., Grammas, P., Nedergaard, M., Nutt, J., et al. (2008) · The Lancet Neurology · doi:10.1016/s1474-4422(07)70326-5 · Cited by 474 · see citing works
Self-citationFarr, S. A., Poon, H. F., Dogrukol‐Ak, D., Drake, J., Banks, W. A., Eyerman, E., Butterfield, D. A., & Morley, J. E. (2003) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2003.01580.x · Cited by 459 · see citing works
Self-citationKinetics of Neutral Amino Acid Transport Across the Blood‐Brain Barrier
Smith, Q. R., Momma, S., Aoyagi, M., & Rapoport, S. I. (1987) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1987.tb01039.x · Cited by 454 · see citing works
Zlokovic, B. V., Martel, C. L., Matsubara, E., McComb, J. G., Zheng, G., McCluskey, R. T., Frangione, B., & Ghiso, J. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.9.4229 · Cited by 430 · see citing works
Deane, R., Wu, Z., & Zlokovic, B. V. (2004) · Stroke · doi:10.1161/01.str.0000143452.85382.d1 · Cited by 392 · see citing works
Sheng, J. (2003) · Neurobiology of Disease · doi:10.1016/s0969-9961(03)00069-x · Cited by 388 · see citing works
Masliah, E., Sisk, A., Mallory, M. E., Mucke, L., Schenk, D., & Games, D. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-18-05795.1996 · Cited by 387 · see citing works
Presenilin: Running with Scissors in the Membrane
Selkoe, D. J., & Wolfe, M. S. (2007) · Cell · doi:10.1016/j.cell.2007.10.012 · Cited by 376 · see citing works
Clearing amyloid through the blood-brain barrier
Zlokovic, B. V. (2004) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2004.02385.x · Cited by 336 · see citing works
Perrière, N., Demeuse, P., García-García, E., Régina, A., Debray, M., Andreux, J. P., Couvreur, P., Scherrmann, J., Temsamani, J., Couraud, P., et al. (2005) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2004.03020.x · Cited by 330 · see citing works
Behavioral Effects of Cytokines
Larson, S. J., & Dunn, A. J. (2001) · Brain Behavior and Immunity · doi:10.1006/brbi.2001.0643 · Cited by 295 · see citing works
Drug Transfer Across the Blood‐Brain Barrier: Correlation Between In Vitro and In Vivo Models
Dehouck, M., Jolliet, P., Brée, F., Fruchart, J., Cecchelli, R., & Tillement, J. P. (1992) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1992.tb10055.x · Cited by 286 · see citing works
Release of cytokines by brain endothelial cells: A polarized response to lipopolysaccharide
Verma, S., Nakaoke, R., Dohgu, S., & Banks, W. A. (2005) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2005.10.005 · Cited by 267 · see citing works
Self-citationMatsumura, K., Cao, C., Ozaki, M., Morii, H., Nakadate, K., & Watanabe, Y. (1998) · The Journal of Neuroscience · doi:10.1523/jneurosci.18-16-06279.1998 · Cited by 247 · see citing works
Signaling through OX40 (CD134) breaks peripheral T-cell tolerance
Bansal‐Pakala, P., Jember, A. G.-H., & Croft, M. (2001) · Nature Medicine · doi:10.1038/90942 · Cited by 231 · see citing works
Effect of LPS on the permeability of the blood–brain barrier to insulin
Xaio, H., Banks, W. A., Niehoff, M. L., & Morley, J. E. (2001) · Brain Research · doi:10.1016/s0006-8993(00)03247-9 · Cited by 231 · see citing works
Self-citationPeripheral infection evokes exaggerated sickness behaviour in pre-clinical murine prion disease
Combrinck, M. I., Perry, V. H., & Cunningham, C. (2002) · Neuroscience · doi:10.1016/s0306-4522(02)00030-1 · Cited by 231 · see citing works
Ghersi‐Egea, J. ‐., Gorevic, P. D., Ghiso, J., Frangione, B., Patlak, C. S., & Fenstermacher, J. D. (1996) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.1996.67020880.x · Cited by 222 · cited 1× · see citing works
“Ab is transported by RAGE (receptor for advanced glycation end products) into (Martel et al., 1996; Bell et al., 2006; Deane et al., 2003; Maness et al., 1994) and by LRP-1 (low density lipoprotein receptor-related protein-1) out of (Banks et al., 2003; Deane et al., 2004a; Shibata et al., 2000; Ghersi-Egea et al., 19…”
BackgroundTownsend, K. P., & Praticò, D. (2005) · The FASEB Journal · doi:10.1096/fj.04-3620rev · Cited by 196 · see citing works
Deane, R., Sagare, A. P., & Zloković, B. V. (2008) · Current Pharmaceutical Design · doi:10.2174/138161208784705487 · Cited by 184 · see citing works
Banks, W. A., Clever, C. M., & Farrell, C. L. (2000) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.2000.278.6.e1158 · Cited by 168 · see citing works
Self-citationBanks, W., Burney, B. O., & Robinson, S. (2008) · Peptides · doi:10.1016/j.peptides.2008.07.001 · Cited by 155 · see citing works
Self-citationPoon, H. F., Castegna, A., Farr, S. A., Thongboonkerd, V., Lynn, B. C., Banks, W. A., Morley, J. E., Klein, J. B., & Butterfield, D. A. (2004) · Neuroscience · doi:10.1016/j.neuroscience.2004.04.046 · Cited by 155 · see citing works
Self-citationCardiovascular Risk Factors for Alzheimer's Disease
Rosendorff, C., Beeri, M. S., & Silverman, J. M. (2007) · The American Journal of Geriatric Cardiology · doi:10.1111/j.1076-7460.2007.06696.x · Cited by 151 · see citing works
Zloković, B. V. (1996) · Life Sciences · doi:10.1016/0024-3205(96)00310-4 · Cited by 138 · see citing works
Jaeger, L. B., Dohgu, S., Hwang, M. C., Farr, S., Murphy, M. P., Fleegal-DeMotta, M. A., Lynch, J. L., Robinson, S., Niehoff, M., Johnson, S. N., et al. (2009) · Journal of Alzheimer's Disease · doi:10.3233/jad-2009-1074 · Cited by 135 · see citing works
Self-citationDrosophila: the genetics of two major larval proteins
Akam, M. E., Roberts, D. B., Richards, G., & Ashburner, M. (1978) · Cell · doi:10.1016/0092-8674(78)90190-3 · Cited by 135 · see citing works
Urayama, A., & Banks, W. A. (2008) · Endocrinology · doi:10.1210/en.2008-0008 · Cited by 121 · see citing works
Self-citationPoon, H. F., Gururaj Joshi, A., Rukhsana Sultana, A., Farr, S. A., Banks, W. A., Morley, J. E., Calabrese, V., & Butterfield, D. A. (2004) · Brain Research · doi:10.1016/j.brainres.2004.05.048 · Cited by 119 · see citing works
Self-citationPassage of human amyloid β-protein 1–40 across the murine blood-brain barrier
Maness, L. M., Banks, W. A., Podlisny, M. B., Selkoe, D. J., & Kastin, A. J. (1994) · Life Sciences · doi:10.1016/0024-3205(94)00331-9 · Cited by 113 · see citing works
Self-citationCultured human and canine endothelial cells from brain microvessels
Gerhart, D. Z., Broderius, M. A., & Drewes, L. R. (1988) · Brain Research Bulletin · doi:10.1016/0361-9230(88)90047-0 · Cited by 113 · see citing works
LaMarre, J., Wolf, B. B., Kittler, E. L. W., Quesenberry, P. J., & Gonias, S. L. (1993) · Journal of Clinical Investigation · doi:10.1172/jci116283 · Cited by 99 · see citing works
Adsorptive Endocytosis of HIV-1gp120 by Blood–Brain Barrier Is Enhanced by Lipopolysaccharide
Banks, W. A., Kastin, A. J., Brennan, J. M., & Vallance, K. (1999) · Experimental Neurology · doi:10.1006/exnr.1998.7011 · Cited by 90 · see citing works
Self-citationBanks, W. A., Robinson, S. M., Verma, S., & Morley, J. E. (2003) · Neuroscience · doi:10.1016/s0306-4522(03)00474-3 · Cited by 90 · see citing works
Self-citationMarzolo, M., Rommy von Bernhardi, M., Bu, G., & Inestrosa, N. C. (2000) · Journal of Neuroscience Research · doi:10.1002/(sici)1097-4547(20000501)60:3 · Cited by 87 · see citing works
Endotoxin induces a delayed loss of TH-IR neurons in substantia nigra and motor behavioral deficits
Liu, Y., Qin, L., Wilson, B., Wu, X., Qian, L., Granholm, A.-C., Crews, F. T., & Hong, J.-S. (2008) · NeuroToxicology · doi:10.1016/j.neuro.2008.02.014 · Cited by 84 · see citing works
Martel, C. L., Mačkić, J. B., McComb, J. G., Ghiso, J. A., & Zloković, B. V. (1996) · Neuroscience Letters · doi:10.1016/s0304-3940(96)12462-9 · Cited by 82 · see citing works
Quantifying carrier-mediated transport of peptides from the brain to the blood
Banks, W. A., & Kastin, A. J. (1989) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/0076-6879(89)68047-0 · Cited by 81 · see citing works
Self-citationPoon, H. F., Farr, S. A., Banks, W. A., Pierce, W. M. J., Klein, J. B., Morley, J. E., & Butterfield, D. A. (2005) · Molecular Brain Research · doi:10.1016/j.molbrainres.2005.02.020 · Cited by 76 · see citing works
Self-citationShayo, M., McLay, R. N., Kastin, A. J., & Banks, W. A. (1997) · Life Sciences · doi:10.1016/s0024-3205(96)00685-6 · Cited by 70 · see citing works
Self-citationAlzheimer’s disease through the eye of a mouse
Morley, J. E., Farr, S. A., Kumar, V. B., & Banks, W. A. (2002) · Peptides · doi:10.1016/s0196-9781(01)00630-1 · Cited by 68 · see citing works
Self-citationBanks, W. A., Kastin, A. J., & Fasold, M. B. (1988) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(25)24453-6 · Cited by 66 · see citing works
Self-citationBanks, W. A., Dohgu, S., Lynch, J. L., Fleegal-DeMotta, M. A., Erickson, M. A., Nakaoke, R., & Vo, T. Q. (2008) · Endocrinology · doi:10.1210/en.2007-1091 · Cited by 57 · see citing works
Self-citationLaRue, B., Hogg, E., Sagare, A. P., Jovanovic, S. S., Maness, L. M., Maurer, C. R., Deane, R., & Zloković, B. V. (2004) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2004.04.026 · Cited by 57 · see citing works
Lymphocyte adhesion to brain capillary endothelial cells in vitro
de Vries, H. E., Moor, A. C. E., Blom-Roosemalen, M. C. M., de Boer, A. G., Breimer, D. D., van Berkel, T. J. C., & Kuiper, J. (1994) · Journal of Neuroimmunology · doi:10.1016/0165-5728(94)90155-4 · Cited by 56 · see citing works
Effects of lipopolysaccharide on leptin transport across the blood–brain barrier
Nonaka, N., Hileman, S. M., Shioda, S., Vo, T. Q., & Banks, W. A. (2004) · Brain Research · doi:10.1016/j.brainres.2004.04.066 · Cited by 49 · see citing works
Self-citationNonaka, N., Shioda, S., & Banks, W. A. (2004) · Experimental Neurology · doi:10.1016/j.expneurol.2004.09.013 · Cited by 48 · see citing works
Self-citationMeasurement of Efflux Rates from Brain to Blood
Banks, W. A., Fasold, M. B., & Kastin, A. J. (2003) · Humana Press eBooks · doi:10.1385/0-89603-399-6:353 · Cited by 40 · see citing works
Self-citationProduction of pure primary rat cerebral endothelial cell culture: a comparison of different methods.
Szabó, C. A., Deli, M. A., Ngo, T. K., & Joo, F. (1997) · PubMed · Cited by 40 · see citing works
Ontogeny of Insulin Binding in Different Regions of the Rat Brain
Marks, J. L., & Eastman, C. J. (1990) · Developmental Neuroscience · doi:10.1159/000111863 · Cited by 28 · see citing works
Flagged first, then by citations
1 of the 64 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Neurovascular pathways to neurodegeneration in Alzheimer’s disease and other disorders
Zlokovic, B. V. (2011) · Nature Reviews Neuroscience · doi:10.1038/nrn3114 · Cited by 2,969 · see citing works
The blood-brain barrier in systemic inflammation
Varatharaj, A., & Galea, I. (2017) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2016.03.010 · Cited by 1,172 · see citing works
A Meta-Analysis of Cytokines in Alzheimer's Disease
Swardfager, W., Lanctôt, K., Rothenburg, L., Wong, A., Cappell, J., & Herrmann, N. (2010) · Biological Psychiatry · doi:10.1016/j.biopsych.2010.06.012 · Cited by 1,108 · see citing works
The Gut Microbiota and Alzheimer’s Disease
Jiang, C., Li, G., Huang, P., Liu, Z., & Zhao, B. (2017) · Journal of Alzheimer's Disease · doi:10.3233/jad-161141 · Cited by 852 · see citing works
Neuroinflammation: The role and consequences
Lyman, M., Lloyd, D. G., Ji, X., Vizcaychipi, M. P., & Ma, D. (2013) · Neuroscience Research · doi:10.1016/j.neures.2013.10.004 · Cited by 740 · see citing works
Peripheral inflammation and blood–brain barrier disruption: effects and mechanisms
Huang, X., Hussain, B., & Chang, J. (2020) · CNS Neuroscience & Therapeutics · doi:10.1111/cns.13569 · Cited by 732 · see citing works
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. (2015) · Journal of Neuroinflammation · doi:10.1186/s12974-015-0434-1 · Cited by 636 · see citing works
Self-citationBasic mechanisms of neurodegeneration: a critical update
Jellinger, K. A. (2010) · Journal of Cellular and Molecular Medicine · doi:10.1111/j.1582-4934.2010.01010.x · Cited by 608 · see citing works
Neuroinflammation in Alzheimer disease
Heneka, M. T., van der Flier, W. M., Jessen, F., Hoozemanns, J., Thal, D. R., Boche, D., Brosseron, F., Teunissen, C., Zetterberg, H., Jacobs, A. H., et al. (2025) · Nature Reviews Immunology · doi:10.1038/s41577-024-01104-7 · Cited by 638 · see citing works
Zhu, X., Badawi, M. A., Pomeroy, S. M., Sutaria, D. S., Xie, Z., Baek, A., Jiang, J., Elgamal, O. A., Mo, X. M., Perle, K. L., et al. (2017) · Journal of Extracellular Vesicles · doi:10.1080/20013078.2017.1324730 · Cited by 588 · see citing works
Microglia, neuroinflammation, and beta-amyloid protein in Alzheimer’s disease
Cai, Z., Hussain, M. D., & Yan, L.-J. (2014) · International Journal of Neuroscience · doi:10.3109/00207454.2013.833510 · Cited by 583 · see citing works
Role of sleep deprivation in immune-related disease risk and outcomes
Garbarino, S., Lanteri, P., Bragazzi, N. L., Magnavita, N., & Scoditti, E. (2021) · Communications Biology · doi:10.1038/s42003-021-02825-4 · Cited by 617 · see citing works
Blood–Brain Barrier Dysfunction as a Cause and Consequence of Alzheimer's Disease
Erickson, M. A., & Banks, W. A. (2013) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.2013.135 · Cited by 572 · see citing works
Self-citationLipopolysaccharide-induced neuroinflammation as a bridge to understand neurodegeneration
Batista, C. R. A., Gomes, G. F., Candelario-Jalil, E., Fiebich, B. L., & de Oliveira, A. C. P. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20092293 · Cited by 529 · see citing works
The blood-brain barrier and immune function and dysfunction
Banks, W. A., & Erickson, M. A. (2010) · Neurobiology of Disease · doi:10.1016/j.nbd.2009.07.031 · Cited by 523 · see citing works
Self-citationThe endotoxin hypothesis of neurodegeneration
Brown, G. C. (2019) · Journal of Neuroinflammation · doi:10.1186/s12974-019-1564-7 · Cited by 457 · see citing works
The role of monocyte chemoattractant protein MCP1/CCL2 in neuroinflammatory diseases
Conductier, G., Blondeau, N., Guyon, A., Nahon, J., & Rovère, C. (2010) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2010.05.010 · Cited by 405 · see citing works
Erickson, M. A., & Banks, W. A. (2018) · Pharmacological Reviews · doi:10.1124/pr.117.014647 · Cited by 394 · see citing works
Self-citationRole of Blood-Brain Barrier in Alzheimer’s Disease
Cai, Z., Qiao, P.-F., Wan, C.-Q., Cai, M., Zhou, N.-K., & Li, Q. (2018) · Journal of Alzheimer's Disease · doi:10.3233/jad-180098 · Cited by 370 · see citing works
Systemic Immune Activation Leads to Neuroinflammation and Sickness Behavior in Mice
Biesmans, S., Meert, T. F., Bouwknecht, J. A., Acton, P. D., Davoodi, N., Haes, P. D., Kuijlaars, J., Langlois, X., Matthews, L. J. R., Donck, L. V., et al. (2013) · Mediators of Inflammation · doi:10.1155/2013/271359 · Cited by 382 · see citing works
Alzheimer’s disease and gut microbiota
Hu, X., Wang, T., & Jin, F. (2016) · Science China Life Sciences · doi:10.1007/s11427-016-5083-9 · Cited by 371 · see citing works
The Impact of Systemic Inflammation on Alzheimer’s Disease Pathology
Xie, J., Van Hoecke, L., & Vandenbroucke, R. E. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2021.796867 · Cited by 324 · see citing works
Neuroinflammation in Alzheimer’s Disease
Onyango, I. G., Jauregui, G. V., Čarná, M., Bennett, J. P., & Stokin, G. B. (2021) · Biomedicines · doi:10.3390/biomedicines9050524 · Cited by 330 · see citing works
Contributions of peripheral inflammation to seizure susceptibility: Cytokines and brain excitability
Riazi, K., Galic, M. A., & Pittman, Q. J. (2009) · Epilepsy Research · doi:10.1016/j.eplepsyres.2009.09.004 · Cited by 302 · see citing works
The blood-brain barrier in neuroimmunology: Tales of separation and assimilation
Banks, W. A. (2015) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2014.08.007 · Cited by 292 · see citing works
Self-citationOxidative stress and β-amyloid protein in Alzheimer’s disease
Cai, Z., Zhao, B., & Ratka, A. (2011) · NeuroMolecular Medicine · doi:10.1007/s12017-011-8155-9 · Cited by 279 · see citing works
Recent advances in our understanding of neurodegeneration
Jellinger, K. A. (2009) · Journal of Neural Transmission · doi:10.1007/s00702-009-0240-y · Cited by 274 · see citing works
Hay, J. R., Johnson, V. E., Young, A. M. H., Smith, D. H., & Stewart, W. B., Jr. (2015) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/nen.0000000000000261 · Cited by 265 · see citing works
Role of the Blood-Brain Barrier in Central Nervous System Insulin Resistance
Rhea, E. M., & Banks, W. A. (2019) · Frontiers in Neuroscience · doi:10.3389/fnins.2019.00521 · Cited by 263 · see citing works
Self-citationGut microbiota, immune development and function
Bengmark, S. (2012) · Pharmacological Research · doi:10.1016/j.phrs.2012.09.002 · Cited by 264 · see citing works
Erickson, M. A., & Banks, W. A. (2011) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2011.06.006 · Cited by 262 · see citing works
Self-citationHussain, B., Fang, C., & Chang, J. (2021) · Frontiers in Neuroscience · doi:10.3389/fnins.2021.688090 · Cited by 251 · see citing works
Targeting neuroinflammation in Alzheimer’s disease
Bronzuoli, M. R., Iacomino, A., Steardo, L., & Scuderi, C. (2016) · Journal of Inflammation Research · doi:10.2147/jir.s86958 · Cited by 255 · see citing works
Neuroinflammation: A Common Pathway in CNS Diseases as Mediated at the Blood-Brain Barrier
Erickson, M. A., Dohi, K., & Banks, W. A. (2012) · NeuroImmunoModulation · doi:10.1159/000330247 · Cited by 246 · see citing works
Self-citationGut reactions: how the blood-brain barrier connects the microbiome and the brain
Logsdon, A. F., Erickson, M. A., Rhea, E. M., Salameh, T. S., & Banks, W. A. (2018) · Experimental Biology and Medicine · doi:10.1177/1535370217743766 · Cited by 235 · see citing works
Self-citationBlood-Brain Barrier Dysfunction in CNS Disorders and Putative Therapeutic Targets: An Overview
Archie, S. R., Shoyaib, A. A., & Cucullo, L. (2021) · Pharmaceutics · doi:10.3390/pharmaceutics13111779 · Cited by 232 · see citing works
The links between the gut microbiome, aging, modern lifestyle and Alzheimer's disease
Askarova, S., Umbayev, B., Masoud, A.-R., Kaiyrlykyzy, A., Safarova, Y., Tsoy, A., Olzhayev, F., & Kushugulova, A. (2020) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2020.00104 · Cited by 208 · see citing works
Goyal, D., Ali, S. A., & Singh, R. K. (2020) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2020.110112 · Cited by 208 · see citing works
Cerebral microvascular endothelium and the pathogenesis of neurodegenerative diseases
Grammas, P., Martinez, J. M., & Miller, B. B. (2011) · Expert Reviews in Molecular Medicine · doi:10.1017/s1462399411001918 · Cited by 203 · see citing works
de Theije, C. G. M., Wu, J., da Silva, S. L., Kamphuis, P. J. G. H., Garssen, J., Korte, S. M., & Kraneveld, A. D. (2011) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2011.07.013 · Cited by 203 · see citing works
Age-Associated Changes in the Immune System and Blood–Brain Barrier Functions
Erickson, M. A., & Banks, W. A. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20071632 · Cited by 192 · see citing works
Self-citationLee, Y., Choi, D., Yun, Y., Han, S., Oh, K., & Hong, J. T. (2012) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2012.06.011 · Cited by 195 · see citing works
Complement in the pathogenesis of Alzheimer’s disease
Morgan, B. P. (2018) · Seminars in Immunopathology · doi:10.1007/s00281-017-0662-9 · Cited by 194 · see citing works
Drug delivery to the brain in Alzheimer's disease: Consideration of the blood–brain barrier
Banks, W. A. (2012) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2011.12.005 · Cited by 184 · see citing works
Self-citationExploiting microglial and peripheral immune cell crosstalk to treat Alzheimer’s disease
Dionisio-Santos, D. A., Olschowka, J. A., & O’Banion, M. K. (2019) · Journal of Neuroinflammation · doi:10.1186/s12974-019-1453-0 · Cited by 184 · see citing works
Kahn, M. S., Kranjac, D., Alonzo, C. A., Haase, J. H., Cedillos, R. O., McLinden, K. A., Boehm, G. W., & Chumley, M. J. (2012) · Behavioural Brain Research · doi:10.1016/j.bbr.2012.01.010 · Cited by 177 · see citing works
Teixeira, F. B., Saito, M. T., MATHEUS, F. C., Prediger, R. D., Yamada, E. S., Maia, C. D. S. F., & Lima, R. R. (2017) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2017.00327 · Cited by 175 · see citing works
Lipopolysaccharide-Induced Memory Impairment in Rats: a Model of Alzheimer’s Disease
ZAKARIA, R., WAN YAACOB, W. M. H., OTHMAN, Z., LONG, I., AHMAD, A. H., & AL-RAHBI, B. (2017) · Physiological Research · doi:10.33549/physiolres.933480 · Cited by 167 · see citing works
Versele, R., Sevin, E., Gosselet, F., Fénart, L., & Candela, P. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms231810235 · Cited by 172 · see citing works
Kim, Y., Hwang, C. J., Lee, H. P., Kim, C. S., Son, D. J., Ham, Y. W., Hellström, M., Han, S., Kim, H. S., Park, E. K., et al. (2017) · Neuropharmacology · doi:10.1016/j.neuropharm.2017.01.025 · Cited by 159 · see citing works
Role of Endogenous Lipopolysaccharides in Neurological Disorders
Kalyan, M., Hediyal, T. A., Sonali, S., Vichitra, C., Sunanda, T., Praveenraj, S. S., Ray, B., Gorantla, V. R., Rungratanawanich, W., Mahalakshmi, A. M., et al. (2022) · Cells · doi:10.3390/cells11244038 · Cited by 161 · see citing works
Periodontal disease as a possible cause for Alzheimer's disease
Kamer, A. R., Craig, R. G., Niederman, R., Fortea, J., & de Leon, M. J. (2020) · Periodontology 2000 · doi:10.1111/prd.12327 · Cited by 154 · see citing works
Oxidative/Nitrosative Stress and Immuno-inflammatory Pathways in Depression: Treatment Implications
Anderson, G., & Maes, M. H. J. (2014) · Current Pharmaceutical Design · doi:10.2174/13816128113196660738 · Cited by 147 · see citing works
Erickson, M. A., Hartvigson, P. E., Morofuji, Y., Owen, J. B., Butterfield, D. A., & Banks, W. A. (2012) · Journal of Neuroinflammation · doi:10.1186/1742-2094-9-150 · Cited by 145 · see citing works
Self-citationSagare, A. P., Deane, R., & Zloković, B. V. (2012) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2012.07.008 · Cited by 144 · see citing works
LRP1 mediates bidirectional transcytosis of amyloid-β across the blood-brain barrier
Pflanzner, T., Janko, M. C., André-Dohmen, B., Reuss, S., Weggen, S., Roebroek, A. J. M., Kuhlmann, C. R. W., & Pietrzik, C. U. (2011) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2010.05.025 · Cited by 141 · see citing works
Recent advances in drug delivery and targeting to the brain
Sethi, B., Kumar, V., Mahato, K., Coulter, D. W., & Mahato, R. I. (2022) · Journal of Controlled Release · doi:10.1016/j.jconrel.2022.08.051 · Cited by 134 · see citing works
The endotoxin hypothesis of Alzheimer’s disease
Brown, G. C., & Heneka, M. T. (2024) · Molecular Neurodegeneration · doi:10.1186/s13024-024-00722-y · Cited by 140 · see citing works
Emerging Roles of Pericytes in the Regulation of the Neurovascular Unit in Health and Disease
Hill, J. D., Rom, S., Ramirez, S. H., & Persidsky, Y. (2014) · Journal of Neuroimmune Pharmacology · doi:10.1007/s11481-014-9557-x · Cited by 134 · see citing works
Lee, Y., Choi, D., Choi, I. S., Kim, K. H., Kim, Y. H., Kim, H. M., Lee, K., Cho, W. G., Jung, J. K., Han, S., et al. (2012) · Journal of Neuroinflammation · doi:10.1186/1742-2094-9-35 · Cited by 133 · see citing works
Nanotoxicology and nanomedicine: The Yin and Yang of nano-bio interactions for the new decade
Bondarenko, O. M., Mortimer, M., Kahru, A., Feliu, N., Javed, I., Käkinen, A., Lin, S., Xia, T., Song, Y., Davis, T. P., et al. (2021) · Nano Today · doi:10.1016/j.nantod.2021.101184 · Cited by 125 · see citing works
Modulation of inflammation in transgenic models of Alzheimer’s disease
Birch, A. M., Katsouri, L., & Sastre, M. (2014) · Journal of Neuroinflammation · doi:10.1186/1742-2094-11-25 · Cited by 119 · see citing works
Honarvar, N. M., Saedisomeolia, A., Abdolahi, M., Shayeganrad, A., Sangsari, G. T., Rad, B. H., & Muench, G. W. (2016) · Journal of Molecular Neuroscience · doi:10.1007/s12031-016-0857-x · Cited by 121 · see citing works
Alquisiras-Burgos, I., Peralta-Arrieta, I., Alonso-Palomares, L. A., Zacapala-Gómez, A. E., Salmerón-Bárcenas, E. G., & Aguilera, P. (2021) · Molecular Neurobiology · doi:10.1007/s12035-020-02134-7 · Cited by 115 · see citing works
Zhao, M., Zhou, A., Xu, L., & Zhang, X. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2014.03.039 · Cited by 115 · see citing works
Association of inflammation and cognition in the elderly: A systematic review and meta-analysis
Leonardo, S., & Fregni, F. (2023) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2023.1069439 · Cited by 115 · see citing works
Osteoarthritis accelerates and exacerbates Alzheimer's disease pathology in mice
Kyrkanides, S., Tallents, R. H., Miller, J. H., Olschowka, M. E., Johnson, R. E., Yang, M., Olschowka, J. A., Brouxhon, S. M., & O’Banion, M. K. (2011) · Journal of Neuroinflammation · doi:10.1186/1742-2094-8-112 · Cited by 112 · see citing works
Sun, M., Ma, K., Wen, J., Wang, G., Zhang, C., Li, Q., Bao, X., & Wang, H. (2020) · Journal of Alzheimer’s Disease · doi:10.3233/jad-190872 · Cited by 113 · see citing works
The effect of systemic inflammation on human brain barrier function
Elwood, E., Lim, Z., Naveed, H., & Galea, I. (2016) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2016.10.020 · Cited by 109 · see citing works
Systemic and CNS Inflammation Crosstalk: Implications for Alzheimer’s Disease
Paouri, E., & Georgopoulos, S. (2019) · Current Alzheimer Research · doi:10.2174/1567205016666190321154618 · Cited by 108 · see citing works
Sansores‐España, L. D., Melgar‐Rodríguez, S., Sagredo-Olivares, K., Cafferata, E. A., Martínez-Aguilar, V. M., Vernal, R., Paula-Lima, A. C., & Díaz‐Zúñiga, J. (2021) · Frontiers in Aging · doi:10.3389/fragi.2021.781582 · Cited by 106 · see citing works
Zhao, Y., Li, Y., Zhao, J., Song, J., & Zhao, Y. (2016) · Reviews in the Neurosciences · doi:10.1515/revneuro-2015-0069 · Cited by 103 · see citing works
Impact of gut microbiota on neurological diseases: Diet composition and novel treatments
Larroya-García, A., Navas-Carrillo, D., & Orenes‐Piñero, E. (2018) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408398.2018.1484340 · Cited by 105 · see citing works
Conn, K. A., Borsom, E. M., & Cope, E. K. (2024) · Gut Microbes · doi:10.1080/19490976.2024.2371950 · Cited by 105 · see citing works
Gu, Y., Vorburger, R. S., Scarmeas, N., Luchsinger, J. A., Manly, J. J., Schupf, N., Mayeux, R. P., & Brickman, A. M. (2017) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2017.04.022 · Cited by 99 · see citing works
Erickson, M. A., Hansen, K. M., & Banks, W. A. (2012) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2012.07.003 · Cited by 100 · see citing works
Self-citationGut Inflammation in Association With Pathogenesis of Parkinson’s Disease
Chen, Q.-Q., Haikal, C., Li, W., & Li, J. (2019) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2019.00218 · Cited by 88 · see citing works
The gut microbiome and Alzheimer’s disease: Complex and bidirectional interactions
Tarawneh, R. M., & Penhos, E. (2022) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2022.104814 · Cited by 89 · see citing works
Scholtzova, H., Do, E., Dhakal, S., Sun, Y., Liu, S., Mehta, P. D., & Wisniewski, T. (2017) · The Journal of Neuroscience · doi:10.1523/jneurosci.1967-16.2016 · Cited by 82 · see citing works
Park, A.-M., & Tsunoda, I. (2022) · Inflammation and Regeneration · doi:10.1186/s41232-022-00224-8 · Cited by 82 · see citing works
Scholtzova, H., Chianchiano, P. E., Pan, J., Sun, Y., Goñi, F., Mehta, P. D., & Wısnıewskı, T. (2014) · Acta Neuropathologica Communications · doi:10.1186/s40478-014-0101-2 · Cited by 80 · see citing works
Divecha, Y. A., Rampes, S., Tromp, S., Boyanova, S., Fleckney, A. L., Fidanboylu, M., & Thomas, S. A. (2025) · Pharmacological Reviews · doi:10.1016/j.pharmr.2025.100052 · Cited by 79 · see citing works
Integrative neurobiology of metabolic diseases, neuroinflammation, and neurodegeneration
van Dijk, G., van Heijningen, S., Reijne, A. C., Nyakas, C., van der Zee, E. A., & Eisel, U. L. M. (2015) · Frontiers in Neuroscience · doi:10.3389/fnins.2015.00173 · Cited by 75 · see citing works
Dohgu, S., & Banks, W. A. (2013) · Fluids and Barriers of the CNS · doi:10.1186/2045-8118-10-23 · Cited by 74 · see citing works
Self-citationCui, B., Li, K., Gai, Z., She, X., Zhang, N., Xu, C.-X., Chen, X., An, G., Ma, Q., & Wang, R. (2015) · Scientific Reports · doi:10.1038/srep12943 · Cited by 74 · see citing works
Probiotics: Protecting Our Health from the Gut
Varela-Trinidad, G. U., Domínguez-Díaz, C., Solórzano-Castanedo, K., Íñiguez-Gutiérrez, L., Hernández-Flores, T. D. J., & Fafutis‐Morris, M. (2022) · Microorganisms · doi:10.3390/microorganisms10071428 · Cited by 78 · see citing works
Francois, A., Terro, F., Quellard, N., Fernandez, B., Chassaing, D., Janet, T., Bilan, A. R., Paccalin, M., & Page, G. (2014) · Molecular Brain · doi:10.1186/s13041-014-0056-z · Cited by 73 · see citing works
Gut Microbiota in Neurological Disorders
Grochowska, M., Laskus, T., & Radkowski, M. (2019) · Archivum Immunologiae et Therapiae Experimentalis · doi:10.1007/s00005-019-00561-6 · Cited by 73 · see citing works
Zhang, J., Chen, S., Hou, Z., Cai, J., Mingmin, D., & Shi, X. (2015) · PLoS ONE · doi:10.1371/journal.pone.0122572 · Cited by 72 · see citing works
Hilal, S., Ikram, M. A., Verbeek, M. M., Franco, O. H., Stoops, E., Vanderstichele, H., Niessen, W. J., & Vernooij, M. W. (2018) · Stroke · doi:10.1161/strokeaha.118.022317 · Cited by 71 · see citing works
The Neglected Role of Histamine in Alzheimer’s Disease
Naddafi, F., & Mirshafiey, A. (2013) · American Journal of Alzheimer s Disease & Other Dementias® · doi:10.1177/1533317513488925 · Cited by 71 · see citing works
Pirolli, N. H., Bentley, W. E., & Jay, S. M. (2021) · Advanced Biology · doi:10.1002/adbi.202000540 · Cited by 70 · see citing works
Wu, S., Wu, Q., Wang, J., Li, Y., Chen, B., Zhu, Z., Huang, R., Chen, M., Huang, A., Xie, Y., et al. (2022) · Journal of Agricultural and Food Chemistry · doi:10.1021/acs.jafc.1c08393 · Cited by 68 · see citing works
Marottoli, F. M., Katsumata, Y., Koster, K. P., Thomas, R., Fardo, D. W., & Tai, L. M. (2017) · ASN NEURO · doi:10.1177/1759091417719201 · Cited by 68 · see citing works
Pritchard, A. B., Fabian, Z., Lawrence, C. L., Morton, G., Crean, S., & Alder, J. E. (2022) · Journal of Alzheimer s Disease · doi:10.3233/jad-215054 · Cited by 70 · see citing works
Cal, R., Castellano, J., Revuelta‐López, E., Aledo, R., Barriga, M., Farré, J., Vilahur, G., Nasarre, L., Hove‐Madsen, L., Badimón, L., et al. (2012) · Cardiovascular Research · doi:10.1093/cvr/cvs136 · Cited by 66 · see citing works
Piracetam Attenuates LPS-Induced Neuroinflammation and Cognitive Impairment in Rats
Tripathi, A., Paliwal, P., & Krishnamurthy, S. (2017) · Cellular and Molecular Neurobiology · doi:10.1007/s10571-017-0468-2 · Cited by 65 · see citing works
Ma, L., Zhang, H., Liu, N., Wang, P.-Q., Guo, W.-Z., Fu, Q., Jiao, L.-B., Ma, Y.-Q., & Mi, W. (2016) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2016.02.001 · Cited by 60 · see citing works
Erickson, M. A., Shulyatnikova, T. V., Banks, W. A., & Hayden, M. R. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24021640 · Cited by 64 · see citing works
Self-citationGhosh, A., Birngruber, T., Sattler, W., Altendorfer‐Kroath, T., Ratzer, M., Sinner, F. M., & Pieber, T. R. (2014) · PLoS ONE · doi:10.1371/journal.pone.0098143 · Cited by 62 · see citing works
- Authors
- Jaeger, L. B., Dohgu, S., Sultana, R., Lynch, J. L., Owen, J. B., Erickson, M. A., Shah, G. N., Price, T. O., Fleegal-Demotta, M. A., Butterfiled, D. A., & Banks, W. A.
- Affiliations
- St. Louis VA Medical Center (US)
- University of Kentucky (US)
- Corresponding author
- Banks, William A.
- Venue
- Brain, Behavior, and Immunity
- Publisher
- Elsevier BV
- Published
- 2009-05
- Volume
- 23
- Issue
- 4
- Pages
- 507-517
- ISSN
- 0889-1591 (ISSN-L)
- PMC
- PMC2783557
- OpenAlex
- W2156015902
- Cited by
- 281
- References
- 64
- Citations by year
- 2026: 20 · 2025: 17 · 2024: 23 · 2023: 13 · 2022: 16 · 2021: 21 · 2020: 19 · 2019: 14 · 2018: 11 · 2017: 22 · 2016: 17 · 2015: 9 · 2014: 21 · 2013: 17 · 2012: 13
- FWCI
- 9.06
- Type
- journal article
- Language
- en
- Update notices
- erratum (2011-11-01)
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Brain Behavior and Immunity (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute on Aging (R01AG029839)
- National Institute of Neurological Disorders and Stroke (R01NS050547, R01NS051334)
- Topics
- Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
- Life Sciences › Neuroscience › Neurology › Barrier Structure and Function Studies
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Keywords
- Alzheimer's disease, amyloid-beta, blood-brain barrier, lipopolysaccharide, neuroinflammation, indomethacin, LRP1, RAGE, triolein, interleukins, MCP-1
- MeSH terms
- Receptor for Advanced Glycation End Products, Alzheimer Disease, Animals, Blood-Brain Barrier, Brain, Dose-Response Relationship, Drug, Indomethacin, Inflammation, Lipopolysaccharides, Male, Receptors, Immunologic, Receptors, LDL, Triolein, Blotting, Western, Cytokines, Amyloid beta-Peptides, Cyclooxygenase Inhibitors, Oxidative Stress, Disease Progression, Protein Transport, Tumor Suppressor Proteins, Low Density Lipoprotein Receptor-Related Protein-1, Mice
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review