Blocking the apolipoprotein E/amyloid-β interaction as a potential therapeutic approach for Alzheimer's disease

Sadowski, Martin J.; Pankiewicz, Joanna; Scholtzova, Henrieta; Mehta, Pankaj D.; Prelli, Frances; Quartermain, David; Wisniewski, Thomas

doi:10.1073/pnas.0604011103

Cited by 167Alzheimer's disease research and treatmentsDementia and Cognitive Impairment ResearchNeuroinflammation and Neurodegeneration Mechanisms

Blocking the apolipoprotein E/amyloid-β interaction as a potential therapeutic approach for Alzheimer's disease

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Sadowski, Martin J., Pankiewicz, Joanna, Scholtzova, Henrieta, Mehta, Pankaj D., Prelli, Frances, Quartermain, David, Wisniewski, Thomas·2006·Proceedings of the National Academy of Sciences

DOI 10.1073/pnas.0604011103PMC PMC1654132

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Abstract

The amyloid-β (Aβ) cascade hypothesis of Alzheimer's disease (AD) maintains that accumulation of Aβ peptide constitutes a critical event in the early disease pathogenesis. The direct binding between Aβ and apolipoprotein E (apoE) is an important factor implicated in both Aβ clearance and its deposition in the brain's parenchyma and the walls of meningoencephalic vessels as cerebral amyloid angiopathy. With the aim of testing the effect of blocking the apoE/Aβ interaction in vivo as a potential novel therapeutic target for AD pharmacotherapy, we have developed Aβ12-28P, which is a blood-brain-barrier-permeable nontoxic, and nonfibrillogenic synthetic peptide homologous to the apoE binding site on the full-length Aβ. Aβ12-28P binds with high affinity to apoE, preventing its binding to Aβ, but has no direct effect on Aβ aggregation. Aβ12-28P shows a strong pharmacological effect in vivo . Its systemic administration resulted in a significant reduction of Aβ plaques and cerebral amyloid angiopathy burden and a reduction of the total brain level of Aβ in two AD transgenic mice models. The treatment did not affect the levels of soluble Aβ fraction or Aβ oligomers, indicating that inhibition of the apoE/Aβ interaction in vivo has a net effect of increasing Aβ clearance over deposition and at the same time does not create conditions favoring formation of toxic oligomers. Furthermore, behavioral studies demonstrated that treatment with Aβ12-28P prevents a memory deficit in transgenic animals. These findings provide evidence of another therapeutic approach for AD.

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The authors previously used Aβ12-28P to successfully reduce Aβ plaque load and cerebral amyloid angiopathy in APP SW and APP SW/PS1 M146L AD model mice.
“We have used Ab12-28P in the past to successfully reduce Ab plaques load and CAA in APP SW and APP SW /PS1 M146L AD model mice.22”
From Blocking the Interaction between Apolipoprotein E and Aβ Reduces Intraneuronal Accumulation of Aβ and Inhibits Synaptic Degeneration (2013) · cites this paper as [22]
The Results and Discussion report reduced Aβ deposits in both APPSWE and APPSWE/PS1 mice and a 68.4% reduction in CAA burden in APPSWE mice. They explicitly say CAA treatment effects could not be reliably assessed in APPSWE/PS1 mice, so the claim overextends that finding to the second model. (LLM, conf=0.90)
Experimental — accuracy not yet measured
Antagonizing the apoE/Aβ interaction with a small peptide decreased Aβ pathology in the mouse brain.
“One study found that antagonizing the apoE/Aβ interaction with a small peptide decreased Aβ pathology in the mouse brain”
From Human ApoE isoforms differentially regulate brain amyloid-β peptide clearance (2011) · cites this paper as [57]
A similar strategy preventing the interaction between apoE and Aβ has already been successfully used to attenuate Aβ toxicity and amyloid deposition.
“A similar strategy preventing the interaction between apoE and Aβ has already been successfully used to attenuate Aβ toxicity and amyloid deposition (Sadowski et al., 2006).”
From Anti-apoE immunotherapy inhibits amyloid accumulation in a transgenic mouse model of Aβ amyloidosis (2012) · cites this paper as Sadowski et al., 2006
Aβ12-28P inhibits apoE4/Aβ binding with KI = 12.9 nM and neutralizes the promoting effect of apoE on Aβ fibrillization in vitro, but has no effect on self-assembly of Aβ in the absence of apoE.
“Aβ12-28P inhibits apoE4/Aβ binding with KI = 12.9 nM and neutralizes the promoting effect of apoE on Aβ fibrillization in vitro, but has no effect on self-assembly of Aβ in the absence of apoE [15].”
From Blocking the apoE/Aβ interaction ameliorates Aβ-related pathology in APOE ε2 and ε4 targeted replacement Alzheimer model mice (2014) · cites this paper as [15]
Aβ12-28P exerts an effect on serum cholesterol metabolism in addition to targeting the apoE/Aβ interaction in the brain.
“Consistently with our previously published observations [15] these results indicate that Aβ12-28P exerts an effect on serum cholesterol metabolism in addition to targeting the apoE/Aβ interaction in the brain.”
From Blocking the apoE/Aβ interaction ameliorates Aβ-related pathology in APOE ε2 and ε4 targeted replacement Alzheimer model mice (2014) · cites this paper as [15]

ApoE affects Aβ accumulation by modulating both Aβ aggregation and clearance.
“There is compelling evidence showing that apoE affects A␤ accumulation by modulating both A␤ aggregation (Ma et al., 1994;Wisniewski et al., 1994) and clearance (Sadowski et al., 2006;Deane et al., 2008;Jiang et al., 2008;Castellano et al., 2011)”
From Anti-ApoE Antibody Given after Plaque Onset Decreases Aβ Accumulation and Improves Brain Function in a Mouse Model of Aβ Amyloidosis (2014) · cites this paper as Sadowski et al., 2006
Blocking the interaction between apoE and Aβ results in decreased amyloidosis.
“Conversely, blocking the interaction between apoE and A␤ (Sadowski et al., 2006) and decreasing the apoE level by overexpressing low-density lipoprotein receptor (Kim et al., 2009) or haploinsufficiency of apoE (Bales et al., 1999;Holtzman et al., 2000;Kim et al., 2011;Bien-Ly et al., 2012) results in decreased amyloidosis.”
From Anti-ApoE Antibody Given after Plaque Onset Decreases Aβ Accumulation and Improves Brain Function in a Mouse Model of Aβ Amyloidosis (2014) · cites this paper as Sadowski et al., 2006
Aβ12-28P reduces the load of Aβ plaques and CAA when systemically administered to APPSW Tg mice.
“As we have previously shown, Ab12-28P inhibits ApoE4/Ab binding with K I Z 12.9 nmol/L, neutralizes the promoting effect of ApoE on Ab fibrillization in vitro, and reduces the load of Ab plaques and CAA when systemically administered to APP SW Tg mice.22”
From Blocking the Interaction between Apolipoprotein E and Aβ Reduces Intraneuronal Accumulation of Aβ and Inhibits Synaptic Degeneration (2013) · cites this paper as [22]
Aβ12-28P inhibits ApoE4/Aβ binding with Ki = 12.9 nmol/L.
“As we have previously shown, Ab12-28P inhibits ApoE4/Ab binding with K I Z 12.9 nmol/L, neutralizes the promoting effect of ApoE on Ab fibrillization in vitro, and reduces the load of Ab plaques and CAA when systemically administered to APP SW Tg mice.22”
From Blocking the Interaction between Apolipoprotein E and Aβ Reduces Intraneuronal Accumulation of Aβ and Inhibits Synaptic Degeneration (2013) · cites this paper as [22]
Aβ12-28P neutralizes the promoting effect of ApoE on Aβ fibrillization in vitro.
“As we have previously shown, Ab12-28P inhibits ApoE4/Ab binding with K I Z 12.9 nmol/L, neutralizes the promoting effect of ApoE on Ab fibrillization in vitro, and reduces the load of Ab plaques and CAA when systemically administered to APP SW Tg mice.22”
From Blocking the Interaction between Apolipoprotein E and Aβ Reduces Intraneuronal Accumulation of Aβ and Inhibits Synaptic Degeneration (2013) · cites this paper as [22]
The degree of co-localization between apoE and Aβ deposition appeared to decrease in brains carrying the APOE3-Jac variant compared to those from APOE3.
“As apoE co-deposits with Aβ in the amyloid plaques (13–15), we examined and found that the degree of co-localization between apoE and Aβ deposition appeared to decrease in the brains carrying APOE3-Jac variant compared to those from APOE3 (Fig. S1C–F).”
From APOE3 -Jacksonville (V236E) variant reduces self-aggregation and risk of dementia (2021) · cites this paper as [14]

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Kim, J., Eltorai, A. E. M., Jiang, H., Liao, F., Verghese, P. B., Kim, J., Stewart, F. R., Basak, J. M., & Holtzman, D. M. (2012) · Journal of Experimental Medicine · doi:10.1084/jem.20121274 · Cited by 160 · see citing works
“ApoE appears to affect A accumulation by modulating both A aggregation and clearance (Ma et al., 1994; Wisniewski et al., 1994; Castano et al., 1995; Sadowski et al., 2006; Deane et al., 2008; Jiang et al., 2008; Castellano et al., 2011).”
Background
Low-density lipoprotein receptor overexpression enhances the rate of brain-to-blood Aβ clearance in a mouse model of β-amyloidosis
Castellano, J. M., Deane, R., Gottesdiener, A. J., Verghese, P. B., Stewart, F. R., West, T., Paoletti, A. C., Kasper, T. R., DeMattos, R. B., Zlokovic, B. V., et al. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1206446109 · Cited by 154 · see citing works
Apolipoprotein E and Alzheimer's disease: molecular mechanisms and therapeutic opportunities
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The Binding of Apolipoprotein E to Oligomers and Fibrils of Amyloid-β Alters the Kinetics of Amyloid Aggregation
Garai, K., Verghese, P. B., Baban, B., Holtzman, D. M., & Frieden, C. (2014) · Biochemistry · doi:10.1021/bi5008172 · Cited by 145 · see citing works
Peptide‐Based Molecular Strategies To Interfere with Protein Misfolding, Aggregation, and Cell Degeneration
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Apolipoprotein E in Synaptic Plasticity and Alzheimer’s Disease: Potential Cellular and Molecular Mechanisms
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“For example, an A 12- 28 synthetic peptide, which contains the apoE-binding site, reduced cerebral A accumulation in animal models of A amyloidosis (Kuszczyk et al., 2013; Pankiewicz et al., 2014; Sadowski et al., 2004; 2006).”
Background
Why is the amyloid beta peptide of Alzheimer’s disease neurotoxic?
Rauk, A. (2008) · Dalton Transactions · doi:10.1039/b718601k · Cited by 139 · see citing works
Advances in the pathogenesis of Alzheimer’s disease: a re-evaluation of amyloid cascade hypothesis
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Strategies for the Inhibition of Protein Aggregation in Human Diseases
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Immunotherapy Reduces Vascular Amyloid- in PDAPP Mice
Schroeter, S., Khan, K., Barbour, R., Doan, M., Chen, M., Guido, T., Gill, D., Basi, G., Schenk, D., Seubert, P., et al. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.2377-07.2008 · Cited by 133 · see citing works
Anti-ApoE Antibody Given after Plaque Onset Decreases Aβ Accumulation and Improves Brain Function in a Mouse Model of Aβ Amyloidosis
Liao, F., Hori, Y., Hudry, E., Bauer, A. Q., Jiang, H., Mahan, T. E., Lefton, K. B., Zhang, T. J., Dearborn, J. T., Kim, J., et al. (2014) · The Journal of Neuroscience · doi:10.1523/jneurosci.0646-14.2014 · Cited by 128 · see citing works
“…evidence showing that apoE affects A accumulation by modulating both A aggregation (Ma et al., 1994; Wisniewski et al., 1994) and clearance (Sadowski et al., 2006; Deane et al., 2008; Jiang et al., 2008; Castellano et al., 2011) and it also colocalizes with A plaques (Namba et al., 1991).”
BackgroundInfluential
APOE-amyloid interaction: Therapeutic targets
Wısnıewskı, T., & Drummond, E. (2020) · Neurobiology of Disease · doi:10.1016/j.nbd.2020.104784 · Cited by 125 · see citing works
Amyloid-β fibrillogenesis: Structural insight and therapeutic intervention
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Current therapeutic targets for the treatment of Alzheimer’s disease
Grill, J. D., & Cummings, J. L. (2010) · Expert Review of Neurotherapeutics · doi:10.1586/ern.10.29 · Cited by 121 · see citing works
Memantine leads to behavioral improvement and amyloid reduction in Alzheimer's‐disease‐model transgenic mice shown as by micromagnetic resonance imaging
Scholtzova, H., Wadghiri, Y. Z., Douadi, M., Sigurdsson, E. M., Li, Y., Quartermain, D., Banerjee, P., & Wısnıewskı, T. (2008) · Journal of Neuroscience Research · doi:10.1002/jnr.21713 · Cited by 119 · see citing works
Self-citation
Targeting dysregulated lipid metabolism for the treatment of Alzheimer's disease and Parkinson's disease: Current advancements and future prospects
Tong, B., Ba, Y., Li, Z., Yang, C., Su, K., Qi, H., Zhang, D., Liu, X., Wu, Y., Chen, Y., et al. (2024) · Neurobiology of Disease · doi:10.1016/j.nbd.2024.106505 · Cited by 117 · see citing works
Soluble apoE/Aβ complex: mechanism and therapeutic target for APOE4-induced AD risk
Tai, L. M., Mehra, S., Shete, V., Estus, S., Rebeck, G. W., Bu, G., & LaDu, M. J. (2014) · Molecular Neurodegeneration · doi:10.1186/1750-1326-9-2 · Cited by 116 · see citing works
Detection of Amyloid Plaques Targeted by Bifunctional USPIO in Alzheimer’s Disease Transgenic Mice Using Magnetic Resonance Microimaging
Wadghiri, Y. Z., Li, J., Wang, J., Hoang, D. M., Sun, Y., Xu, H., Tsui, W., Li, Y., Boutajangout, A., Wang, A., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0057097 · Cited by 114 · see citing works
APOE3 -Jacksonville (V236E) variant reduces self-aggregation and risk of dementia
Liu, C.-C., Murray, M. E., Li, X., Zhao, N., Wang, N., Heckman, M. G., Shue, F., Martens, Y., Li, Y., Raulin, A.-C., et al. (2021) · Science Translational Medicine · doi:10.1126/scitranslmed.abc9375 · Cited by 108 · see citing works
Animal models of dementia and cognitive dysfunction
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Mouse Models to Study the Effect of Cardiovascular Risk Factors on Brain Structure and Cognition
Bink, D. I., Ritz, K., Aronica, E., van der Weerd, L., & Daemen, M. J. A. P. (2013) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.2013.140 · Cited by 95 · see citing works
Traumatic Brain Injury Exacerbates Neurodegenerative Pathology: Improvement with an Apolipoprotein E-Based Therapeutic
Laskowitz, D. T., Song, P., Wang, H., Mace, B. E., Sullivan, P. M., Vitek, M. P., & Dawson, H. N. (2010) · Journal of Neurotrauma · doi:10.1089/neu.2010.1396 · Cited by 90 · see citing works
Blocking the Interaction between Apolipoprotein E and Aβ Reduces Intraneuronal Accumulation of Aβ and Inhibits Synaptic Degeneration
Kuszczyk, M. A., Sanchez, S., Pankiewicz, J., Kim, J., Duszczyk, M., Guridi, M., Asuni, A. A., Sullivan, P. M., Holtzman, D. M., & Sadowski, M. J. (2013) · The American Journal of Pathology · doi:10.1016/j.ajpath.2013.01.034 · Cited by 89 · see citing works
“Ab peptides were synthesized on solid-phase support and purified by reverse-phase high-pressure liquid chromatography, as previously described.(16,22) Full-length sequences of Ab1-40, Ab1-42, and Ab1-40 amino-terminally tagged with 5,6-carboxyfluorescein (FITC-Ab1-40) were synthesized with L-amino acids, whereas end-p…”
MethodSelf-citation
Apolipoprotein E, Amyloid-β, and Blood-Brain Barrier Permeability in Alzheimer Disease
Donahue, J. E., & Johanson, C. E. (2008) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/nen.0b013e31816a0dc8 · Cited by 86 · see citing works
Amyloid Clearance as a Treatment Target Against Alzheimer's Disease
Kurz, A., & Perneczky, R. (2011) · Journal of Alzheimer s Disease · doi:10.3233/jad-2011-102139 · Cited by 83 · see citing works
Murine models of Alzheimer's disease and their use in developing immunotherapies
Wısnıewskı, T., & Sigurdsson, E. M. (2010) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2010.05.004 · Cited by 80 · see citing works
Apolipoprotein E: Essential Catalyst of the Alzheimer Amyloid Cascade
Potter, H., & Wısnıewskı, T. (2012) · International Journal of Alzheimer s Disease · doi:10.1155/2012/489428 · Cited by 80 · see citing works
Murine versus human apolipoprotein E4: differential facilitation of and co-localization in cerebral amyloid angiopathy and amyloid plaques in APP transgenic mouse models
Liao, F., Zhang, T. J., Jiang, H., Lefton, K. B., Robinson, G. O., Vassar, R., Sullivan, P. M., & Holtzman, D. M. (2015) · Acta Neuropathologica Communications · doi:10.1186/s40478-015-0250-y · Cited by 77 · see citing works
Amyloid β and Tau Alzheimer’s disease related pathology is reduced by Toll-like receptor 9 stimulation
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 77 · see citing works
Self-citation
Cerebral clearance of human amyloid‐β peptide (1–40) across the blood–brain barrier is reduced by self‐aggregation and formation of low‐density lipoprotein receptor‐related protein‐1 ligand complexes
Ito, S., Ohtsuki, S., Kamiie, J., Nezu, Y., & Terasaki, T. (2007) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2007.04938.x · Cited by 85 · see citing works
Computational Simulations of the Early Steps of Protein Aggregation
Wei, G., Mousseau, N., & Derreumaux, P. (2007) · Prion · doi:10.4161/pri.1.1.3969 · Cited by 67 · see citing works
Novel antidepressant effects of Paeonol alleviate neuronal injury with concomitant alterations in BDNF, Rac1 and RhoA levels in chronic unpredictable mild stress rats
Zhu, X.-L., Chen, J., Han, F., Pan, C., Zhuang, T.-T., Cai, Y., & Lu, Y.-P. (2018) · Psychopharmacology · doi:10.1007/s00213-018-4915-7 · Cited by 63 · see citing works
Blocking the apolipoprotein E/Amyloid β interaction in triple transgenic mice ameliorates Alzheimer's disease related amyloid β and tau pathology
Liu, S., Breitbart, A., Sun, Y., Mehta, P. D., Boutajangout, A., Scholtzova, H., & Wisniewski, T. (2014) · Journal of Neurochemistry · doi:10.1111/jnc.12484 · Cited by 60 · see citing works
Self-citation
Increased atherosclerosis and vascular inflammation in APP transgenic mice with apolipoprotein E deficiency
Tibolla, G., Norata, G. D., Meda, C., Arnaboldi, L., Uboldi, P., Piazza, F., Ferrarese, C., Corsini, A., Maggi, A. C., Vegeto, E., et al. (2009) · Atherosclerosis · doi:10.1016/j.atherosclerosis.2009.10.040 · Cited by 60 · see citing works
Blocking the apoE/Aβ interaction ameliorates Aβ-related pathology in APOE ε2 and ε4 targeted replacement Alzheimer model mice
Pankiewicz, J. E., Guridi, M., Kim, J., Asuni, A. A., Sanchez, S., Sullivan, P. M., Holtzman, D. M., & Sadowski, M. J. (2014) · Acta Neuropathologica Communications · doi:10.1186/s40478-014-0075-0 · Cited by 57 · see citing works
Self-citation
Targeting Apolipoprotein E/Amyloid β Binding by Peptoid CPO_Aβ17-21 P Ameliorates Alzheimer’s Disease Related Pathology and Cognitive Decline
Liu, S., Park, S.-A., Allington, G., Prelli, F. C., Sun, Y., Martá-Ariza, M., Scholtzova, H., Biswas, G. K., Brown, B., Verghese, P. B., et al. (2017) · Scientific Reports · doi:10.1038/s41598-017-08604-8 · Cited by 57 · see citing works
Self-citation
Cerebral Amyloid Angiopathy, Subcortical White Matter Disease and Dementia: Literature Review and Study in OPTIMA
Esiri, M. M., Chance, S. A., Joachim, C. L., Warden, D. R., Smallwood, A., Sloan, C., Christie, S., Wilcock, G. K., & Smith, A. D. (2014) · Brain Pathology · doi:10.1111/bpa.12221 · Cited by 55 · see citing works
Apolipoprotein E/Amyloid-β Complex Accumulates in Alzheimer Disease Cortical Synapses via Apolipoprotein E Receptors and Is Enhanced by APOE4
Bilousova, T. V., Melnik, M., Miyoshi, E., Gonzalez, B. L., Poon, W. W., Vinters, H. V., Miller, C. A., Corrada, M. M., Kawas, C. H., Hatami, A., et al. (2019) · American Journal Of Pathology · doi:10.1016/j.ajpath.2019.04.010 · Cited by 54 · see citing works
Molecular Insight into the Therapeutic Promise of TargetingAPOE4for Alzheimer’s Disease
Mamun, A. A., Uddin, M. S., Bashar, M. F. B., Zaman, S., Begum, Y., Bulbul, I. J., Islam, M. S., Sarwar, M. S., Mathew, B., Amran, M. S., et al. (2020) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2020/5086250 · Cited by 53 · see citing works
Brain Apolipoprotein E: an Important Regulator of Food Intake in Rats
Shen, L., Tso, P., Woods, S. C., Clegg, D. J., Barber, K. L., Carey, K., & Liu, M. (2008) · Diabetes · doi:10.2337/db08-0291 · Cited by 52 · see citing works
In Silico Analysis of the Apolipoprotein E and the Amyloid β Peptide Interaction: Misfolding Induced by Frustration of the Salt Bridge Network
Luo, J., Maréchal, J., Wärmländer, S. K. T. S., Gräslund, A., & Perálvarez‐Marín, A. (2010) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1000663 · Cited by 51 · see citing works
Immunomodulation Targeting Abnormal Protein Conformation Reduces Pathology in a Mouse Model of Alzheimer's Disease
Goñi, F., Prelli, F. C., Ji, Y., Scholtzova, H., Yang, J., Sun, Y., Liang, F., Kascsak, R., Kascsak, R. J., Mehta, P. D., et al. (2010) · PLoS ONE · doi:10.1371/journal.pone.0013391 · Cited by 48 · see citing works
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Mouse models in neurological disorders: Applications of non-invasive imaging
Waerzeggers, Y., Monfared, P., Viel, T., Winkeler, A., & Jacobs, A. H. (2010) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2010.04.009 · Cited by 47 · see citing works
Current therapeutic strategy in Alzheimer's disease.
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Peroxiredoxin 6 mediates protective function of astrocytes in Aβ proteostasis
Pankiewicz, J. E., Diaz, J. R., Martá-Ariza, M., Lizińczyk, A. M., Franco, L. A., & Sadowski, M. J. (2020) · Molecular Neurodegeneration · doi:10.1186/s13024-020-00401-8 · Cited by 45 · see citing works
Self-citation
Immunomodulation targeting of both Aβ and tau pathological conformers ameliorates Alzheimer’s disease pathology in TgSwDI and 3xTg mouse models
Goñi, F., Herline, K., Peyser, D., Wong, K., Ji, Y., Sun, Y., Mehta, P., & Wisniewski, T. (2013) · Journal of Neuroinflammation · doi:10.1186/1742-2094-10-150 · Cited by 43 · see citing works
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Preventing β-amyloid fibrillization and deposition: β-sheet breakers and pathological chaperone inhibitors
Wısnıewskı, T., & Sadowski, M. J. (2008) · BMC Neuroscience · doi:10.1186/1471-2202-9-s2-s5 · Cited by 42 · see citing works
Self-citation
Using human induced pluripotent stem cells (hiPSCs) to investigate the mechanisms by which Apolipoprotein E (APOE) contributes to Alzheimer’s disease (AD) risk
Raman, S., Brookhouser, N., & Brafman, D. A. (2020) · Neurobiology of Disease · doi:10.1016/j.nbd.2020.104788 · Cited by 40 · see citing works
Chemical Cross-Linking/Mass Spectrometry Maps the Amyloid β Peptide Binding Region on Both Apolipoprotein E Domains
Deroo, S., Stengel, F., Mohammadi, A., Henry, N., Hubin, E., Krammer, E., Aebersold, R. H., & Raussens, V. (2014) · ACS Chemical Biology · doi:10.1021/cb500994j · Cited by 40 · see citing works
Binding studies of truncated variants of the Aβ peptide to the V-domain of the RAGE receptor reveal Aβ residues responsible for binding
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Therapeutic approaches for prion and Alzheimer's diseases
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Immunotherapeutic approaches for Alzheimer’s disease in transgenic mouse models
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Apolipoprotein E isoform-dependent effects on the processing of Alzheimer's amyloid-β
Chai, A. B., Lam, H. H. J., Kockx, M., & Gelissen, I. C. (2021) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2021.158980 · Cited by 39 · see citing works
Transthyretin Accelerates Vascular Aβ Deposition in a Mouse Model of Alzheimer's Disease
Wati, H., Kawarabayashi, T., Matsubara, E., Kasai, A., Hirasawa, T., Kubota, T., Harigaya, Y., Shoji, M., & Maeda, S. (2008) · Brain Pathology · doi:10.1111/j.1750-3639.2008.00166.x · Cited by 36 · see citing works
Extracellular Proteolysis of Apolipoprotein E (apoE) by Secreted Serine Neuronal Protease
Tamboli, I. Y., Heo, D., & Rebeck, G. W. (2014) · PLoS ONE · doi:10.1371/journal.pone.0093120 · Cited by 35 · see citing works
APOE Genotype Differentially Modulates Effects of Anti-Aβ, Passive Immunization in APP Transgenic Mice
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“standard enzymatic assay based on the Cholesterol E kit (Wako Diagnostics, Richmond, VA) as previously described [19, 24].”
MethodSelf-citation
Beyond Amyloid
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Up-regulation of apolipoprotein E by leptin in the hypothalamus of mice and rats
Shen, L., Tso, P., Wang, D. Q. ‐., Woods, S. C., Davidson, W. S., Sakai, R. R., & Liu, M. (2009) · Physiology & Behavior · doi:10.1016/j.physbeh.2009.05.013 · Cited by 32 · see citing works
Distinguishing Lewy body dementias from Alzheimer’s disease
Tarawneh, R. M., & Galvin, J. E. (2007) · Expert Review of Neurotherapeutics · doi:10.1586/14737175.7.11.1499 · Cited by 32 · see citing works
Mapping ApoE/Aβ binding regions to guide inhibitor discovery
Liu, Q. R., Wu, W., Fang, C.-L., Li, R., Liu, P., Lei, P., Hu, J., Sun, X., Zheng, Y.-Z., Zhao, Y., et al. (2011) · Molecular BioSystems · doi:10.1039/c1mb05019b · Cited by 29 · see citing works
Estrogen signalling and Alzheimer's disease: Decoding molecular mechanisms for therapeutic breakthrough
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Modulation of amyloid precursor protein expression reduces β‐amyloid deposition in a mouse model
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Self-citation
Isoform‐specific effects of apolipoprotein E on cognitive performance in targeted‐replacement mice overexpressing human APP
Kornecook, T. J., McKinney, A. P., Ferguson, M. T., & Dodart, J. (2009) · Genes Brain & Behavior · doi:10.1111/j.1601-183x.2009.00545.x · Cited by 29 · see citing works
Alterations in Lipid Levels of Mitochondrial Membranes Induced by Amyloid-ß: A Protective Role of Melatonin
Rosales‐Corral, S., López-Armas, G. D. C., Cruz-Ramos, J. A., Melnikov, V., Tan, D., Manchester, L. C., Munoz, R., & Reiter, R. J. (2012) · International Journal of Alzheimer s Disease · doi:10.1155/2012/459806 · Cited by 30 · see citing works
Potential Novel Approaches to Understand the Pathogenesis and Treat Alzheimer’s Disease
Drummond, E., Goñi, F., Liu, S., Prelli, F., Scholtzova, H., & Wısnıewskı, T. (2018) · Journal of Alzheimer s Disease · doi:10.3233/jad-179909 · Cited by 26 · see citing works
Self-citation
The Antidepressant Effects of Resveratrol are Accompanied by the Attenuation of Dendrite/Dendritic Spine Loss and the Upregulation of BDNF/p-cofilin1 Levels in Chronic Restraint Mice
Chen, J., Shen, J., Yu, Z.-H., Pan, C., Han, F., Zhu, X.-L., Xu, H., Xu, R.-T., Wei, T.-Y., & Lu, Y.-P. (2021) · Neurochemical Research · doi:10.1007/s11064-020-03200-1 · Cited by 26 · see citing works
Knowing Me, Knowing You: Can a Knowledge of Risk Factors for Alzheimer's Disease Prove Useful in Understanding the Pathogenesis of Parkinson's Disease?
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Aβ20–29 peptide blocking apoE/Aβ interaction reduces full-length Aβ42/40 fibril formation and cytotoxicity in vitro
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Novel derivative of Paeonol, Paeononlsilatie sodium, alleviates behavioral damage and hippocampal dendritic injury in Alzheimer's disease concurrent with cofilin1/phosphorylated-cofilin1 and RAC1/CDC42 alterations in rats
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Are apolipoprotein E fragments a promising new therapeutic target for Alzheimer’s disease?
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Cross interactions between Apolipoprotein E and amyloid proteins in neurodegenerative diseases
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P4–254: The apolipoprotein E/Aβ interaction as a novel therapeutic target for Alzheimer's disease
Sadowski, M. J., Pankiewicz, J. E., Scholtzova, H., Wu, H., Prelli, F. C., Mehta, P. D., Quartermain, D., & Wısnıewskı, T. (2006) · Alzheimer s & Dementia · doi:10.1016/j.jalz.2006.05.1993
Self-citation
A Synthetic Peptide Blocking the Apolipoprotein E/β-Amyloid Binding Mitigates β-Amyloid Toxicity and Fibril Formation in Vitro and Reduces β-Amyloid Plaques in Transgenic Mice
Sadowski, M., Pankiewicz, J., Scholtzova, H., Ripellino, J. A., Li, Y., Schmidt, S. D., Mathews, P. M., Fryer, J. D., Holtzman, D. M., Sigurdsson, E. M., et al. (2004) · The American Journal of Pathology · doi:10.1016/s0002-9440(10)63355-x · Cited by 154 · see citing works
Self-citation
[P‐183]: Blocking the apolipoprotein E/amyloid‐B interaction reduces amyloid‐B load in AD transgenic mice
Sadowski, M. J., Pankiewicz, J. E., Scholtzova, H., Wen, P. H., Mehta, P. D., & Wısnıewskı, T. (2005) · Alzheimer s & Dementia · doi:10.1016/j.jalz.2005.06.243
Self-citation
Blocking the apolipoprotein E/Amyloid β interaction in triple transgenic mice ameliorates Alzheimer's disease related amyloid β and tau pathology
Liu, S., Breitbart, A., Sun, Y., Mehta, P. D., Boutajangout, A., Scholtzova, H., & Wisniewski, T. (2014) · Journal of Neurochemistry · doi:10.1111/jnc.12484 · Cited by 60 · see citing works
Self-citation
Blocking the Apolipoprotein E/Amyloid-β Interaction Reduces Fibrillar Vascular Amyloid Deposition and Cerebral Microhemorrhages in TgSwDI Mice
Yang, J., Ji, Y., Mehta, P. D., Bates, K. A., Sun, Y., & Wısnıewskı, T. (2011) · Journal of Alzheimer s Disease · doi:10.3233/jad-2011-101401 · Cited by 48 · see citing works
Self-citation

Authors: Sadowski, M. J., Pankiewicz, J., Scholtzova, H., Mehta, P. D., Prelli, F., Quartermain, D., & Wisniewski, T.
Affiliations: *Departments of Neurology,
New York State Institute for Basic Research in Developmental Disabilities, 1050 Forest Hill Road, Staten Island, NY 10314
ORCID: Sadowski, Martin J.
Scholtzova, Henrieta
Mehta, Pankaj D.
Prelli, Frances
Venue: Proceedings of the National Academy of Sciences
Publisher: National Academy of Sciences
Published: 2006-12-05
Volume: 103
Issue: 49
Pages: 18787-18792
ISSN: 0027-8424 (ISSN-L)
1091-6490
DOI: 10.1073/pnas.0604011103
PMC: PMC1654132
OpenAlex: W2004069543
Cited by: 167
References: 29
Citations by year: 2026: 6 · 2025: 3 · 2024: 5 · 2023: 3 · 2022: 3 · 2021: 7 · 2020: 8 · 2019: 8 · 2018: 6 · 2017: 7 · 2016: 5 · 2015: 5 · 2014: 16 · 2013: 13 · 2012: 16
FWCI: 8.19
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Locations: Proceedings of the National Academy of Sciences (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: National Institute on Aging (AG15408, R01AG015408, AG 20747, P30AG008051, R01AG020245, K08AG020747)
Topics: Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
Health Sciences › Medicine › Psychiatry and Mental health › Dementia and Cognitive Impairment Research
Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
Keywords: Alzheimer's disease, amyloid-beta, apolipoprotein E, synthetic peptides, amyloid-beta clearance, cerebral amyloid angiopathy, amyloid plaques, amyloid-beta oligomers, memory impairment, transgenic mouse model, blood-brain barrier permeability, therapeutic target
MeSH terms: Alzheimer Disease, Animals, Apolipoproteins E, Binding, Competitive, Female, Mice, Transgenic, Peptide Fragments, Amyloid beta-Peptides, Amyloid beta-Protein Precursor, Mice

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Blocking the apolipoprotein E/amyloid-β interaction as a potential therapeutic approach for Alzheimer's disease

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