Cited by 2,061Alzheimer's disease research and treatmentsDementia and Cognitive Impairment ResearchNeuroinflammation and Neurodegeneration Mechanisms

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Amyloid Precursor Protein Processing and Alzheimer's Disease

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O'Brien, Richard J., Wong, Philip C.·2011·Annual Review of Neuroscience

DOI 10.1146/annurev-neuro-061010-113613PMC PMC3174086

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Abstract

Alzheimer's disease (AD), the leading cause of dementia worldwide, is characterized by the accumulation of the β-amyloid peptide (Aβ) within the brain along with hyperphosphorylated and cleaved forms of the microtubule-associated protein tau. Genetic, biochemical, and behavioral research suggest that physiologic generation of the neurotoxic Aβ peptide from sequential amyloid precursor protein (APP) proteolysis is the crucial step in the development of AD. APP is a single-pass transmembrane protein expressed at high levels in the brain and metabolized in a rapid and highly complex fashion by a series of sequential proteases, including the intramembranous γ-secretase complex, which also process other key regulatory molecules. Why Aβ accumulates in the brains of elderly individuals is unclear but could relate to changes in APP metabolism or Aβ elimination. Lessons learned from biochemical and genetic studies of APP processing will be crucial to the development of therapeutic targets to treat AD.

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APOE distribution in world populations with new data from India and the UK
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Expression of human apolipoprotein E reduces amyloid-β deposition in a mouse model of Alzheimer's disease
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Cortical dysplasia resembling human type 2 lissencephaly in mice lacking all three APP family members
Herms, J. W., Anliker, B., Heber, S., Ring, S., Fuhrmann, M., Kretzschmar, H. A., Sisodia, S. S., & Müller, U. (2004) · The EMBO Journal · doi:10.1038/sj.emboj.7600390 · Cited by 343
Protein Kinase C-dependent α-Secretase Competes with β-Secretase for Cleavage of Amyloid-β Precursor Protein in the Trans-Golgi Network
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Loss of apolipoprotein E receptor LR11 in Alzheimer disease
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Obesity‐related leptin regulates Alzheimer's Aβ
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“Pathways that may mediate this effect include leptin’s ability to affect Aβ production and clearance (Fewlass et al. 2004, Greco et al. 2009b) and its ability to alter dendritic morphology and synaptic density (O’Malley et al. 2007).”
Background
Putative function of ADAM9, ADAM10, and ADAM17 as APP -secretase
Asai, M., Hattori, C., Szabó, B., Sasagawa, N., Maruyama, K., Tanuma, S.-I., & Ishiura, S. (2003) · Biochemical and Biophysical Research Communications · doi:10.1016/s0006-291x(02)02999-6 · Cited by 303
Reduction of Soluble Aβ and Tau, but Not Soluble Aβ Alone, Ameliorates Cognitive Decline in Transgenic Mice with Plaques and Tangles
Oddo, S., Vasilevko, V., Caccamo, A., Kitazawa, M., Cribbs, D. H., & LaFerla, F. M. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m608485200 · Cited by 298
Alteration of BACE1-dependent NRG1/ErbB4 signaling and schizophrenia-like phenotypes in BACE1 -null mice
Savonenko, A. V., Melnikova, T., Laird, F. M., Stewart, K.-A., Price, D. L., & Wong, P. C. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0710373105 · Cited by 290
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Defective Neuromuscular Synapses in Mice Lacking Amyloid Precursor Protein (APP) and APP-Like Protein 2
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Demonstration by FRET of BACE interaction with the amyloid precursor protein at the cell surface and in early endosomes
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Alzheimer-like neurodegeneration in aged antinerve growth factor transgenic mice
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Lipidation of apolipoprotein E influences its isoform-specific interaction with Alzheimer's amyloid β peptides
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Effects of voluntary and forced exercise on plaque deposition, hippocampal volume, and behavior in the Tg2576 mouse model of Alzheimer's disease
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Phosphorylation-dependent Regulation of the Interaction of Amyloid Precursor Protein with Fe65 Affects the Production of β-Amyloid
Ando, K., Iijima, K., Elliott, J. I., Kirino, Y., & Suzuki, T. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m104059200 · Cited by 261
Increase of synaptic density and memory retention by a peptide representing the trophic domain of the amyloid beta/A4 protein precursor.
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Adult neuron survival strategies — slamming on the brakes
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The up‐regulation of BACE1 mediated by hypoxia and ischemic injury: role of oxidative stress and HIF1α
Guglielmotto, M., Aragno, M., Autelli, R., Giliberto, L., Novo, E., Colombatto, S., Danni, O., Parola, M., Smith, M. A., Perry, G. L., et al. (2008) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2008.05858.x · Cited by 245
Age-Related Distribution of Neuropathologic Changes in the Cerebral Cortex of Patients With Down's Syndrome
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Reversal of Alzheimer’s-like pathology and behavior in human APP transgenic mice by mutation of Asp664
Galvan, V., Gorostiza, O. F., Banwait, S., Ataie, M., Logvinova, A. V., Sitaraman, S., Carlson, E., Sagi, S. A., Chevallier, N., Jin, K., et al. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0509695103 · Cited by 239
Increased proNGF Levels in Subjects with Mild Cognitive Impairment and Mild Alzheimer Disease
Peng, S., Wuu, J., Mufson, E. J., & Fahnestock, M. L. (2004) · Journal of Neuropathology & Experimental Neurology · doi:10.1093/jnen/63.6.641 · Cited by 236
Atherosclerosis, dementia, and Alzheimer disease in the Baltimore Longitudinal Study of aging cohort
Dolan, H., Crain, B. J., Troncoso, J. C., Resnick, S. M., Zonderman, A. B., & O’Brien, R. (2010) · Annals of Neurology · doi:10.1002/ana.22055 · Cited by 235
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Amyloid β-Protein Toxicity and the Pathogenesis of Alzheimer Disease
Yankner, B. A., & Lu, T. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.r800018200 · Cited by 229
Impact of APOE genotype on neuropathologic and neurochemical markers of Alzheimer disease
Tiraboschi, P., Hansen, L. A., Masliah, E., Alford, M., Thal, L. J., & Corey-Bloom, J. (2004) · Neurology · doi:10.1212/01.wnl.0000128091.92139.0f · Cited by 226
Binding of F-spondin to amyloid-β precursor protein: a candidate amyloid-β precursor protein ligand that modulates amyloid-β precursor protein cleavage
Ho, A., & Südhof, T. C. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0308655100 · Cited by 224
Axonal Transport, Amyloid Precursor Protein, Kinesin-1, and the Processing Apparatus: Revisited
Lazarov, O., Morfini, G. A., Lee, E. B., Farah, M. H., Szodorai, A., DeBoer, S. R., Koliatsos, V. E., Kins, S., Lee, V. M. ‐., Wong, P. C., et al. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.3089-04.2005 · Cited by 223
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Leptin Reduces Pathology and Improves Memory in a Transgenic Mouse Model of Alzheimer's Disease
Greco, S. J., Bryan, K. J., Sarkar, S., Zhu, X., Smith, M. A., Ashford, J. W., Johnston, J. M., Tezapsidis, N., & Casadesús, G. (2010) · Journal of Alzheimer s Disease · doi:10.3233/jad-2010-1308 · Cited by 220
Proapoptotic Effects of Tau Cleavage Product Generated by Caspase-3
Chung, C.-W., Song, Y.-H., Kim, I.-K., Yoon, W. J., Ryu, B. R., Jo, D., Woo, H., Kwon, Y.-K., Kim, H., Gwag, B.-J., et al. (2001) · Neurobiology of Disease · doi:10.1006/nbdi.2000.0335 · Cited by 211
Involvement of the Interaction between p21 and Proliferating Cell Nuclear Antigen for the Maintenance of G2/M Arrest after DNA Damage
Ando, T., Kawabe, T., Ohara, H., Ducommun, B., Itoh, M., & Okamoto, T. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m106460200 · Cited by 202
Cleavage of Alzheimer's Amyloid Precursor Protein by α-Secretase Occurs at the Surface of Neuronal Cells
Parvathy, S., Hussain, I., Karran, E. H., Turner, A. J., & Hooper, N. M. (1999) · Biochemistry · doi:10.1021/bi9906827 · Cited by 200
Leptin regulates tau phosphorylation and amyloid through AMPK in neuronal cells
Greco, S. J., Sarkar, S., Johnston, J. M., & Tezapsidis, N. (2009) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2009.01.041 · Cited by 190
cAMP-dependent Protein Kinase Phosphorylation of EVL, a Mena/VASP Relative, Regulates Its Interaction with Actin and SH3 Domains
Lambrechts, A., Kwiatkowski, A. V., Lanier, L. M., Bear, J. E., Vandekerckhove, J. S., Ampè, C., & Gertler, F. B. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.m006274200 · Cited by 188
Leptin promotes rapid dynamic changes in hippocampal dendritic morphology
O’Malley, D., MacDonald, N., Mizielinska, S., Connolly, C. N., Irving, A. J., & Harvey, J. (2007) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2007.05.001 · Cited by 186
Reduction of cortical TrkA but not p75NTR protein in early‐stage Alzheimer's disease
Counts, S., Nadeem, M., Wuu, J., Ginsberg, S. D., Saragovi, H. U., & Mufson, E. J. (2004) · Annals of Neurology · doi:10.1002/ana.20233 · Cited by 183
SorLA/LR11 regulates processing of amyloid precursor protein via interaction with adaptors GGA and PACS-1
Schmidt, V., Sporbert, A., Rohe, M., Reimer, T., Rehm, A., Andersen, O. M., & Willnow, T. E. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m705073200 · Cited by 181
γ-secretases: from cell biology to therapeutic strategies
Bergmans, B. A., & Strooper, B. D. (2010) · The Lancet Neurology · doi:10.1016/s1474-4422(09)70332-1 · Cited by 179
β-Secretase Processing in the Trans-Golgi Network Preferentially Generates Truncated Amyloid Species That Accumulate in Alzheimer’s Disease Brain
Huse, J. T., Liu, K., Pijak, D. S., Carlin, D., Lee, V. M.-Y., & Doms, R. W. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m111141200 · Cited by 176
FE65 Constitutes the Functional Link between the Low-Density Lipoprotein Receptor-Related Protein and the Amyloid Precursor Protein
Pietrzik, C. U., Yoon, I.-S., Jaeger, S., Busse, T., Weggen, S., & Koo, E. H. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.5451-03.2004 · Cited by 173
Fasciclin II Signals New Synapse Formation through Amyloid Precursor Protein and the Scaffolding Protein dX11/Mint
Ashley, J., Packard, M. C., Ataman, B., & Budnik, V. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.1144-05.2005 · Cited by 164
Adaptor Protein Sorting Nexin 17 Regulates Amyloid Precursor Protein Trafficking and Processing in the Early Endosomes
Lee, J., Retamal, C., Cuitiño, L., Caruano-Yzermans, A., Shin, J.-E., van Kerkhof, P., Marzolo, M.-P., & Bu, G. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m800642200 · Cited by 162
Dynamics of β-Amyloid Reductions in Brain, Cerebrospinal Fluid, and Plasma of β-Amyloid Precursor Protein Transgenic Mice Treated with a γ-Secretase Inhibitor
Barten, D. M., Guss, V. L., Corsa, J. A., Loo, A., Hansel, S. B., Zheng, M., Munoz, B., Srinivasan, K., Wang, B., Robertson, B. J., et al. (2005) · The Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.104.075408 · Cited by 159
Activation and Functional Characterization of the Mosaic Receptor SorLA/LR11
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Presenilin diversifies its portfolio
Parks, A. L., & Curtis, D. (2007) · Trends in Genetics · doi:10.1016/j.tig.2007.01.008 · Cited by 154
The Fe65 Adaptor Protein Interacts through Its PID1 Domain with the Transcription Factor CP2/LSF/LBP1
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Interaction of the Cytosolic Domains of sorLA/LR11 with the Amyloid Precursor Protein (APP) and β-Secretase β-Site APP-Cleaving Enzyme
Spoelgen, R., von Arnim, C. A. F., Thomas, A. V., Peltan, I. D., Koker, M., Deng, A., Irizarry, M. C., Andersen, O. M., Willnow, T. E., & Hyman, B. T. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.3882-05.2006 · Cited by 148
Lack of Pathology in a Triple Transgenic Mouse Model of Alzheimer’s Disease after Overexpression of the Anti-Apoptotic Protein Bcl-2
Rohn, T. T., Vyas, V., Hernandez-Estrada, T., Nichol, K. E., Christie, L.-A., & Head, E. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.5620-07.2008 · Cited by 146
The FE65 proteins and Alzheimer's disease
McLoughlin, D. M., & Miller, C. C. J. (2007) · Journal of Neuroscience Research · doi:10.1002/jnr.21532 · Cited by 138
Genetics of Alzheimer's disease: recent advances
Avramopoulos, D. (2009) · Genome Medicine · doi:10.1186/gm34 · Cited by 136
Variations in the neuropathology of familial Alzheimer’s disease
Shepherd, C. E., McCann, H., & Halliday, G. M. (2009) · Acta Neuropathologica · doi:10.1007/s00401-009-0521-4 · Cited by 135
Decreased levels of BDNF protein in Alzheimer temporal cortex are independent of BDNF polymorphisms
Lee, J. E., Fukumoto, H., Orne, J. D., Klucken, J., Raju, S., Vanderburg, C. R., Irizarry, M. C., Hyman, B. T., & Ingelsson, M. (2005) · Experimental Neurology · doi:10.1016/j.expneurol.2005.01.026 · Cited by 124
It all sticks together—the APP-related family of proteins and Alzheimer's disease
Bayer, T. A., Cappai, R., Masters, C. L., Beyreuther, K. T., & Multhaup, G. (1999) · Molecular Psychiatry · doi:10.1038/sj.mp.4000552 · Cited by 121
Glycogen Synthase Kinase 3β Induces Caspase-cleaved Tau Aggregation in Situ
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An inherited variable poly-T repeat genotype in TOMM40 in Alzheimer disease
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A β42 is the predominant form of amyloid b -protein in the brains of short-term survivors of head injury
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Cerebral Ischemia and Alzheimer's Disease: The Expression of Amyloid-β and Apolipoprotein E in Human Hippocampus
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Distinct Pools of β-Amyloid in Alzheimer Disease–Affected Brain: A Clinicopathologic Study
Steinerman, J. R., Irizarry, M., Scarmeas, N., Raju, S., Brandt, J., Albert, M., Blacker, D., Hyman, B., & Stern, Y. (2008) · Archives of Neurology · doi:10.1001/archneur.65.7.906 · Cited by 104
Epidermal Growth Factor Receptor and Notch Pathways Participate in the Tumor Suppressor Function of γ-Secretase
Li, T., Wen, H., Brayton, C. F., Das, P., Smithson, L. A., Fauq, A. H., Fan, X., Crain, B. J., Price, D. L., Golde, T. E., et al. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m703649200 · Cited by 96
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The role of glycogen synthase kinase 3 in the early stages of Alzheimers’ disease
Hernández, F., & Ávila, J. (2008) · FEBS Letters · doi:10.1016/j.febslet.2008.10.026 · Cited by 88
Nerve growth factor as a paradigm of neurotrophins related to Alzheimer's disease
Calissano, P., Matrone, C., & Amadoro, G. (2010) · Developmental Neurobiology · doi:10.1002/dneu.20759 · Cited by 88
The Neuronal Adaptor Protein X11α Reduces Aβ Levels in the Brains of Alzheimer's APPswe Tg2576 Transgenic Mice
Lee, J., Lau, K., Perkinton, M. S., Standen, C. L., Shemilt, S. J. A., Mercken, L., Cooper, J. D., McLoughlin, D. M., & Miller, C. C. J. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m300503200 · Cited by 83
Moderate Reduction of γ-Secretase Attenuates Amyloid Burden and Limits Mechanism-Based Liabilities
Li, T., Wen, H., Brayton, C. F., Laird, F. M., Ma, G., Peng, S., Placanica, L., Wu, T. C., Crain, B. J., Price, D. L., et al. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.2152-07.2007 · Cited by 80
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Amyloid precursor protein increases cortical neuron size in transgenic mice
Oh, E. S., Savonenko, A. V., King, J. F., Fangmark Tucker, S. M., Rudow, G. L., Xu, G., Borchelt, D. R., & Troncoso, J. C. (2009) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2007.12.024 · Cited by 75
Presenilin-Dependent γ-Secretase on Plasma Membrane and Endosomes Is Functionally Distinct
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Age, Alzheimer's disease and dementia in the Baltimore Longitudinal Study of Ageing
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Visualization of APP dimerization and APP‐Notch2 heterodimerization in living cells using bimolecular fluorescence complementation
Chen, C.-D., Oh, S., Hinman, J. D., & Abraham, C. R. (2006) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2006.03705.x · Cited by 65
Caspases as therapeutic targets in Alzheimer's disease: is it time to "cut" to the chase?
Rohn, T. T., & Head, E. (2009) · PubMed Central · Cited by 63
Physiological Mouse Brain Aβ Levels Are Not Related to the Phosphorylation State of Threonine-668 of Alzheimer's APP
Sano, Y., Nakaya, T., Pedrini, S., Takeda, S., Iijima‐Ando, K., Iijima, K., Mathews, P. M., Itohara, S., Gandy, S., & Suzuki, T. (2006) · PLoS ONE · doi:10.1371/journal.pone.0000051 · Cited by 63
X11 Proteins Regulate the Translocation of Amyloid β-Protein Precursor (APP) into Detergent-resistant Membrane and Suppress the Amyloidogenic Cleavage of APP by β-Site-cleaving Enzyme in Brain
Saito, Y., Sano, Y., Vassar, R. J., Gandy, S., Nakaya, T., Yamamoto, T., & Suzuki, T. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m801353200 · Cited by 63
Aβ Immunotherapy: Lessons Learned for Potential Treatment of Alzheimer’s Disease
Schenk, D. B., Seubert, P. A., Grundman, M., & Black, R. (2005) · Neurodegenerative Diseases · doi:10.1159/000090365 · Cited by 60
A Dominant Role for FE65 (APBB1) in Nuclear Signaling
Yang, Z., Cool, B. H., Martin, G. M., & Hu, Q. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m508445200 · Cited by 59
The hydrophobic environment of Met35 of Alzheimer's Aβ(1–42) is important for the neurotoxic and oxidative properties of the peptide
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Expression and analysis of heparin‐binding regions of the amyloid precursor protein of Alzheimer's disease
Mok, S. S., Sberna, G., Heffernan, D., et al. (1997) · FEBS Letters · doi:10.1016/s0014-5793(97)01146-0 · Cited by 58
Identification of Caspase-6-Mediated Processing of the Valosin Containing Protein (p97) in Alzheimer's Disease: A Novel Link to Dysfunction in Ubiquitin Proteasome System-Mediated Protein Degradation
Halawani, D., Tessier, S., Anzellotti, D., Bennett, D. A. A., Latterich, M., & LeBlanc, A. C. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.5874-09.2010 · Cited by 54
Modeling an Anti-Amyloid Combination Therapy for Alzheimer’s Disease
Chow, V. W., Savonenko, A. V., Melnikova, T., Kim, H., Price, D. L., Li, T., & Wong, P. C. (2010) · Science Translational Medicine · doi:10.1126/scitranslmed.3000337 · Cited by 53
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Caspase activation in transgenic mice with Alzheimer-like pathology: results from a pilot study utilizing the caspase inhibitor, Q-VD-OPh.
Rohn, T. T., Kokoulina, P., Eaton, C. R., & Poon, W. W. (2009) · PubMed Central · Cited by 36
Caspase activation without apoptosis: insight into Aβ initiation of neurodegeneration
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Mitogen-activated protein kinase is involved in N-methyl-d-aspartate receptor regulation of amyloid precursor protein cleavage
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X11α haploinsufficiency enhances Aβ amyloid deposition in Alzheimer's disease transgenic mice
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Chronic Leptin Supplementation Ameliorates Pathology and Improves Cognitive Performance in a Transgenic Mouse Model of Alzheimer's Disease.
Greco, S. J., Bryan, K. J., Sarkar, S., Zhu, X., Smith, M. A., Ashford, J. W., Johnston, J. M., Tezapsidis, N., & Casadesús, G. (2009) · PubMed · doi:10.3233/jad-2009-1308 · Cited by 14

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“78,111,112 115 However, FAD mutations are not necessarily linked to an increase in A β 42 levels or an elevation of A β 42 /A β 40 ratio.”
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Authors: O'Brien, R. J., & Wong, P. C.
Affiliations: Department of Neurology, Johns Hopkins Bayview Medical Center
Johns Hopkins University (US)
ORCID: Wong, Philip C.
Venue: Annual Review of Neuroscience
Publisher: Annual Reviews
Published: 2011-07-21
Volume: 34
Issue: 1
Pages: 185-204
ISSN: 0147-006X (ISSN-L)
1545-4126
DOI: 10.1146/annurev-neuro-061010-113613
PMC: PMC3174086
OpenAlex: W2129085204
Cited by: 2,061
References: 158
Citations by year: 2026: 118 · 2025: 182 · 2024: 227 · 2023: 194 · 2022: 197 · 2021: 225 · 2020: 185 · 2019: 143 · 2018: 144 · 2017: 105 · 2016: 91 · 2015: 76 · 2014: 70 · 2013: 63 · 2012: 33
FWCI: 5.83
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Locations: Annual Review of Neuroscience (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: National Institute on Aging (P50AG005146)
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › 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 precursor protein, APP processing, amyloid-beta, gamma-secretase, intramembrane proteolysis, tau hyperphosphorylation, amyloid accumulation, APP metabolism, therapeutic target
MeSH terms: Alzheimer Disease, Animals, Brain, Humans, Models, Biological, Amyloid beta-Protein Precursor, Amyloidogenic Proteins

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Amyloid Precursor Protein Processing and Alzheimer's Disease

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