Cited by 283Neuroscience and Neuropharmacology ResearchAlzheimer's disease research and treatmentsReceptor Mechanisms and Signaling

The DOI matches its Crossref record; 74 of the 74 references it cites were found in a registry or an index.

Secreted amyloid-β precursor protein functions as a GABA B R1a ligand to modulate synaptic transmission

Open access

Rice, Heather C., de Malmazet, Daniel, Schreurs, An, Frere, Samuel, Van Molle, Inge, Volkov, Alexander N., Creemers, Eline, Vertkin, Irena, Nys, Julie, Ranaivoson, Fanomezana M., Comoletti, Davide, Savas, Jeffrey N., Remaut, Han, Balschun, Detlef, Wierda, Keimpe D., Slutsky, Inna, Farrow, Karl, De Strooper, Bart, de Wit, Joris·2019·Science

DOI 10.1126/science.aao4827PMC PMC6366617

Open this paper in CoChat — free account

Abstract

A physiological function for sAPP? Although the pathological role of the amyloid-β precursor protein (APP) in Alzheimer's disease is well studied, the physiological role of this protein has remained elusive. Rice et al. found that the secreted ectodomain of APP (sAPP) binds to GABA B R1a, the metabotropic receptor for the inhibitory neurotransmitter γ-aminobutyric acid (GABA) (see the Perspective by Korte). Binding suppressed synaptic vesicle release and modulated synaptic transmission and plasticity in mice. A short, 17–amino acid peptide in APP bound to GABA B R1a's sushi 1 domain, conferring structure to this unstructured domain. Therapeutics targeting this interaction could potentially benefit a range of neurological disorders in which GABA signaling is implicated. Science , this issue p. eaao4827 ; see also p. 123

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

Crossref · 10.1126/science.aao4827

Cites

74 of 74 references verified0 citation errors · 0 not checkable

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?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

NMRPipe: A multidimensional spectral processing system based on UNIX pipes
Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J., & Bax, A. (1995) · Journal of Biomolecular NMR · doi:10.1007/bf00197809 · Cited by 15,961
Crystallography & NMR System: A New Software Suite for Macromolecular Structure Determination
Brünger, A. T., Adams, P. D., Clore, G. M., DeLano, W. L., Gros, P., Grosse‐Kunstleve, R. W., Jiang, J., Kuszewski, J. J., Nilges, M., Pannu, N., et al. (1998) · Acta Crystallographica Section D Biological Crystallography · doi:10.1107/s0907444998003254 · Cited by 15,723
An approach to correlate tandem mass spectral data of peptides with amino acid sequences in a protein database
Eng, J. K., McCormack, A. L., & Yates, J. R. (1994) · Journal of the American Society for Mass Spectrometry · doi:10.1016/1044-0305(94)80016-2 · Cited by 6,484
Large-scale analysis of the yeast proteome by multidimensional protein identification technology
Washburn, M. P., Wolters, D. A., & Yates, J. R. (2001) · Nature Biotechnology · doi:10.1038/85686 · Cited by 4,768
The precursor of Alzheimer's disease amyloid A4 protein resembles a cell-surface receptor
Kang, J., Lemaire, H.-G., Unterbeck, A., Salbaum, J. M., Masters, C. L., Grzeschik, K.-H., Multhaup, G., Beyreuther, K., & Müller-Hill, B. (1987) · Nature · doi:10.1038/325733a0 · Cited by 4,619
The CCPN data model for NMR spectroscopy: Development of a software pipeline
Vranken, W., Boucher, W., Stevens, T. J., Fogh, R. H., Pajon, A., Llinás, M., Ulrich, E. L., Markley, J. L., Ionides, J., & Laue, E. D. (2005) · Proteins Structure Function and Bioinformatics · doi:10.1002/prot.20449 · Cited by 3,222
The Xplor-NIH NMR molecular structure determination package
Schwieters, C. D., Kuszewski, J. J., Tjandra, N., & Clore, G. M. (2003) · Journal of Magnetic Resonance · doi:10.1016/s1090-7807(02)00014-9 · Cited by 2,371
Direct analysis of protein complexes using mass spectrometry
Link, A. J., Eng, J. K., Schieltz, D. M., Carmack, E., Mize, G. J., Morris, D. R., Garvik, B. M., & Yates, J. R. (1999) · Nature Biotechnology · doi:10.1038/10890 · Cited by 2,218
Evaluation of Multidimensional Chromatography Coupled with Tandem Mass Spectrometry (LC/LC−MS/MS) for Large-Scale Protein Analysis: The Yeast Proteome
Peng, J., Elias, J. E., Thoreen, C. C., Licklider, L., & Gygi, S. P. (2002) · Journal of Proteome Research · doi:10.1021/pr025556v · Cited by 1,652
APP Processing and Synaptic Function
Kamenetz, F., Tomita, T., Hsieh, H., Seabrook, G., Borchelt, D., Iwatsubo, T., Sisodia, S., & Malinow, R. (2003) · Neuron · doi:10.1016/s0896-6273(03)00124-7 · Cited by 1,644

Flagged first, then by citations

Show all 74 references

Research works printed but not linked: 2

10.1021/pr025556v · DOI
M. P. Williamson “The Transferred NOE ” in Modern Magnetic Resonance G. A. Webb Ed. (Springer 2008).

Sorted by citations

Alzheimer disease
Knopman, D. S., Amieva, H., Petersen, R. C., Chételat, G., Holtzman, D. M., Hyman, B. T., Nixon, R. A., & Jones, D. T. (2021) · Nature Reviews Disease Primers · doi:10.1038/s41572-021-00269-y · Cited by 2,606
The Amyloid-β Pathway in Alzheimer’s Disease
Hampel, H., Hardy, J., Blennow, K., Chen, C., Perry, G., Kim, S. H., Villemagne, V. L., Aisen, P., Vendruscolo, M., Iwatsubo, T., et al. (2021) · Molecular Psychiatry · doi:10.1038/s41380-021-01249-0 · Cited by 1,952
The β-Secretase BACE1 in Alzheimer’s Disease
Hampel, H., Vassar, R., De Strooper, B., Hardy, J., Willem, M., Singh, N., Zhou, J., Yan, R., Vanmechelen, E., De Vos, A., et al. (2021) · Biological Psychiatry · doi:10.1016/j.biopsych.2020.02.001 · Cited by 694
Bidirectional relationship between sleep and Alzheimer’s disease: role of amyloid, tau, and other factors
Wang, C., & Holtzman, D. M. (2020) · Neuropsychopharmacology · doi:10.1038/s41386-019-0478-5 · Cited by 615
Lipid metabolism and Alzheimer's disease: clinical evidence, mechanistic link and therapeutic promise
Yin, F. (2023) · The FEBS Journal · doi:10.1111/febs.16344 · Cited by 441
Pathological mechanisms and therapeutic strategies for Alzheimer’s disease
Tam, K. Y., & Ju, Y. (2021) · Neural Regeneration Research · doi:10.4103/1673-5374.320970 · Cited by 422
Amyloid-beta peptide and tau protein crosstalk in Alzheimer’s disease
Villegas, S., Roda, A., Serra-Mir, G., Montoliu-Gaya, L., & Tiessler, L. (2022) · Neural Regeneration Research · doi:10.4103/1673-5374.332127 · Cited by 306
Regulation of beta-amyloid production in neurons by astrocyte-derived cholesterol
Wang, H., Kulas, J. A., Wang, C., Holtzman, D. M., Ferris, H. A., & Hansen, S. B. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2102191118 · Cited by 301
GABAergic dysfunction in excitatory and inhibitory (E/I) imbalance drives the pathogenesis of Alzheimer's disease
Bi, D., Wen, L., Wu, Z., & Shen, Y. (2020) · Alzheimer's & Dementia · doi:10.1002/alz.12088 · Cited by 232
Amyloidosis in Alzheimer’s Disease: Pathogeny, Etiology, and Related Therapeutic Directions
Ma, C., Hong, F., & Yang, S. (2022) · Molecules · doi:10.3390/molecules27041210 · Cited by 243
GABAergic Inhibitory Interneuron Deficits in Alzheimer’s Disease: Implications for Treatment
Xu, Y., Zhao, M., Han, Y., & Zhang, H. (2020) · Frontiers in Neuroscience · doi:10.3389/fnins.2020.00660 · Cited by 203
A single-nuclei RNA sequencing study of Mendelian and sporadic AD in the human brain
Del-Aguila, J. L., Li, Z., Dube, U., Mihindukulasuriya, K. A., Budde, J. P., Fernandez, M. V., Ibanez, L., Bradley, J., Wang, F., Bergmann, K., et al. (2019) · Alzheimer's Research & Therapy · doi:10.1186/s13195-019-0524-x · Cited by 183
Stimulation of neural stem cell differentiation by circularly polarized light transduced by chiral nanoassemblies
Qu, A., Sun, M., Kim, J., Xu, L., Hao, C., Ma, W., Wu, X., Liu, X., Kuang, H., Kotov, N. A., et al. (2020) · Nature Biomedical Engineering · doi:10.1038/s41551-020-00634-4 · Cited by 172
Tipping the Scales: Peptide-Dependent Dysregulation of Neural Circuit Dynamics in Alzheimer’s Disease
Harris, S. S., Wolf, F., De Strooper, B., & Busche, M. A. (2020) · Neuron · doi:10.1016/j.neuron.2020.06.005 · Cited by 161
The basis of cellular and regional vulnerability in Alzheimer’s disease
Mrdjen, D., Fox, E. J., Bukhari, S. A., Montine, K. S., Bendall, S. C., & Montine, T. J. (2019) · Acta Neuropathologica · doi:10.1007/s00401-019-02054-4 · Cited by 162
Liver Dysfunction as a Novel Player in Alzheimer’s Progression: Looking Outside the Brain
Estrada, L. D., Ahumada, P., Cabrera, D., & Arab, J. P. (2019) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2019.00174 · Cited by 144
Physiology and pharmacology of amyloid precursor protein
Cho, Y., Bae, H., Okun, E., Arumugam, T. V., & Jo, D. (2022) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2022.108122 · Cited by 150
Preclinical Models of Alzheimer's Disease: Relevance and Translational Validity
Mullane, K., & Williams, M. J. (2019) · Current Protocols in Pharmacology · doi:10.1002/cpph.57 · Cited by 127
Excitatory-inhibitory imbalance in Alzheimer's disease and therapeutic significance
Varela, E. V., Etter, G., & Williams, S. (2019) · Neurobiology of Disease · doi:10.1016/j.nbd.2019.04.010 · Cited by 122
The GABAB Receptor—Structure, Ligand Binding and Drug Development
Evenseth, L. S. M., Gabrielsen, M., & Sylte, I. (2020) · Molecules · doi:10.3390/molecules25133093 · Cited by 118
Molecular mechanisms of metabotropic GABA B receptor function
Shaye, H., Stauch, B., Gati, C., & Cherezov, V. (2021) · Science Advances · doi:10.1126/sciadv.abg3362 · Cited by 115
Alzheimer’s disease beyond amyloid: Can the repetitive failures of amyloid-targeted therapeutics inform future approaches to dementia drug discovery?
Mullane, K., & Williams, M. J. (2020) · Biochemical Pharmacology · doi:10.1016/j.bcp.2020.113945 · Cited by 109
Structural and Biophysical Mechanisms of Class C G Protein-Coupled Receptor Function
Ellaithy, A., González‐Maeso, J., Logothetis, D. E., & Levitz, J. (2020) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2020.07.008 · Cited by 98
Brain foods - the role of diet in brain performance and health
Ekstrand, B., Scheers, N., Rasmussen, M. K., Young, J. F., Ross, A. B., & Landberg, R. (2020) · Nutrition Reviews · doi:10.1093/nutrit/nuaa091 · Cited by 115
The Role of the GABAergic System in Diseases of the Central Nervous System
Zhang, W., Xiong, B., Zhang, L.-Q., Huang, X., Yuan, X., Tian, Y., & Tian, X. (2021) · Neuroscience · doi:10.1016/j.neuroscience.2021.06.037 · Cited by 97
Trafficking and proteolytic processing of amyloid precursor protein and secretases in Alzheimer's disease development: An up-to-date review
Yuksel, M., & Tacal, Ö. (2019) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2019.172415 · Cited by 99
Modulation of Brain Hyperexcitability: Potential New Therapeutic Approaches in Alzheimer’s Disease
Toniolo, S., Sen, A., & Husain, M. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21239318 · Cited by 97
Small heat shock proteins in neurodegenerative diseases
Vendredy, L., Adriaenssens, E., & Timmerman, V. (2020) · Cell Stress and Chaperones · doi:10.1007/s12192-020-01101-4 · Cited by 99
Emerging Alternative Proteinases in APP Metabolism and Alzheimer’s Disease Pathogenesis: A Focus on MT1-MMP and MT5-MMP
García-González, L., Pilat, D., Baranger, K., & Rivera, S. (2019) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2019.00244 · Cited by 88
Neurophysiological biomarkers using transcranial magnetic stimulation in Alzheimer’s disease and mild cognitive impairment: A systematic review and meta-analysis
Mimura, Y., Nishida, H., Nakajima, S., Tsugawa, S., Morita, S., Yoshida, K., Tarumi, R., Ogyu, K., Wada, M., Kurose, S., et al. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.12.003 · Cited by 86
Synaptic dysfunction in early phases of Alzheimer's Disease
Pelucchi, S., Gardoni, F., Luca, M. D., & Marcello, E. E. (2022) · Handbook of clinical neurology · doi:10.1016/b978-0-12-819410-2.00022-9 · Cited by 93
Neuropathological assessment of the Alzheimer spectrum
Jellinger, K. A. (2020) · Journal of Neural Transmission · doi:10.1007/s00702-020-02232-9 · Cited by 85
Proteotoxicity and Neurodegenerative Diseases
Ruz, C., Alcantud, J. L., Montero, F. V., Durán, R., & Bandrés‐Ciga, S. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21165646 · Cited by 83
Physiological Roles of β-amyloid in Regulating Synaptic Function: Implications for AD Pathophysiology
Cai, W., Li, L., Sang, S., Pan, X., & Zhong, C. (2023) · Neuroscience Bulletin · doi:10.1007/s12264-022-00985-9 · Cited by 83
An Insight into Cellular and Molecular Mechanisms Underlying the Pathogenesis of Neurodegeneration in Alzheimer’s Disease
Ratan, Y., Rajput, A., Maleysm, S., Pareek, A., Jain, V. K., Pareek, A., Kaur, R., & Singh, G. (2023) · Biomedicines · doi:10.3390/biomedicines11051398 · Cited by 89
Modeling the β-secretase cleavage site and humanizing amyloid-beta precursor protein in rat and mouse to study Alzheimer’s disease
Serneels, L., T’Syen, D., Pérez‐Benito, L., Theys, T., Holt, M. G., & Strooper, B. D. (2020) · Molecular Neurodegeneration · doi:10.1186/s13024-020-00399-z · Cited by 78
Targeting receptor complexes: a new dimension in drug discovery
Ishoey, M., Clemmensen, L. S., Bredt, D. S., Bettler, B., & Strømgaard, K. (2020) · Nature Reviews Drug Discovery · doi:10.1038/s41573-020-0086-4 · Cited by 79
Knock-in models related to Alzheimer’s disease: synaptic transmission, plaques and the role of microglia
Benítez, D. P., Jiang, S., Wood, J. I., Wang, R., Hall, C. M., Peerboom, C., Wong, N. S. M., Stringer, K. M., Vitanova, K. S., Smith, V. C., et al. (2021) · Molecular Neurodegeneration · doi:10.1186/s13024-021-00457-0 · Cited by 81
Amyloid, APP, and Electrical Activity of the Brain
Hefter, D., Ludewig, S., Draguhn, A., & Körte, M. (2019) · The Neuroscientist · doi:10.1177/1073858419882619 · Cited by 83
Dissociation of somatostatin and parvalbumin interneurons circuit dysfunctions underlying hippocampal theta and gamma oscillations impaired by amyloid β oligomers in vivo
Chung, H., Park, K., Jang, H. J., Kohl, M. M., & Kwag, J. (2020) · Brain Structure and Function · doi:10.1007/s00429-020-02044-3 · Cited by 85
Deciphering the neuroprotective and neurogenic potential of soluble amyloid precursor protein alpha (sAPPα)
Dar, N. J., & Glazner, G. W. (2020) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-019-03404-x · Cited by 77
Presynaptic failure in Alzheimer's disease
Barthet, G., & Mulle, C. (2020) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2020.101801 · Cited by 74
An Expanded Narrative Review of Neurotransmitters on Alzheimer’s Disease: The Role of Therapeutic Interventions on Neurotransmission
Akyuz, E., Arulsamy, A., Aslan, F. S., Sarisözen, B., Guney, B., Hekimoglu, A., Yilmaz, B. N., Retinasamy, T., & Shaikh, M. F. (2025) · Molecular Neurobiology · doi:10.1007/s12035-024-04333-y · Cited by 69
Amyloid-β Peptide Impact on Synaptic Function and Neuroepigenetic Gene Control Reveal New Therapeutic Strategies for Alzheimer’s Disease
Karisetty, B. C., Bhatnagar, A., Armour, E. M., Beaver, M., Zhang, H., & Elefant, F. (2020) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2020.577622 · Cited by 67
Beyond the Ligand: Extracellular and Transcellular G Protein–Coupled Receptor Complexes in Physiology and Pharmacology
Dunn, H. A., Orlandi, C., & Martemyanov, K. A. (2019) · Pharmacological Reviews · doi:10.1124/pr.119.018044 · Cited by 66
Amyloid-β plaque formation and reactive gliosis are required for induction of cognitive deficits in App knock-in mouse models of Alzheimer’s disease
Sakakibara, Y., Sekiya, M., Saito, T., Saido, T. C., & Iijima, K. M. (2019) · BMC Neuroscience · doi:10.1186/s12868-019-0496-6 · Cited by 65
Glia: A major player in glutamate–GABA dysregulation‐mediated neurodegeneration
Sood, A., Kumari, P., Fernandes, V., Khatri, D. K., & Singh, S. B. (2021) · Journal of Neuroscience Research · doi:10.1002/jnr.24977 · Cited by 60
Functional and Phenotypic Diversity of Microglia: Implication for Microglia-Based Therapies for Alzheimer’s Disease
Xu, Y., Au, N. P. B., & Ma, C. H. E. (2022) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2022.896852 · Cited by 68
Super-resolution microscopy: a closer look at synaptic dysfunction in Alzheimer disease
Padmanabhan, P., Kneynsberg, A., & Götz, J. (2021) · Nature reviews. Neuroscience · doi:10.1038/s41583-021-00531-y · Cited by 59
Does HIV infection contribute to increased beta-amyloid synthesis and plaque formation leading to neurodegeneration and Alzheimer’s disease?
Fülöp, T., Witkowski, J. M., Larbi, A., Khalil, A., Herbein, G., & Frost, E. H. (2019) · Journal of NeuroVirology · doi:10.1007/s13365-019-00732-3 · Cited by 59
Reversible GABAergic dysfunction involved in hippocampal hyperactivity predicts early-stage Alzheimer disease in a mouse model
Li, Y., Zhu, K., Li, N., Wang, X., Xiao, X., Li, L., Li, L., He, Y., Zhang, J., Wo, J., et al. (2021) · Alzheimer s Research & Therapy · doi:10.1186/s13195-021-00859-8 · Cited by 51
Long-term voluntary exercise inhibited AGE/RAGE and microglial activation and reduced the loss of dendritic spines in the hippocampi of APP/PS1 transgenic mice
Wang, Y., Zhou, Y., Jiang, L. H., Wang, S., Zhu, L., Zhang, S., Yang, H., He, Q., Liu, L., Xie, Y., et al. (2023) · Experimental Neurology · doi:10.1016/j.expneurol.2023.114371 · Cited by 56
Symptomatic, Genetic, and Mechanistic Overlaps between Autism and Alzheimer’s Disease
Nadeem, M. S., Hosawi, S. B. I., Alshehri, S., Ghoneim, M. M., Imam, S. S., Murtaza, B. N., & Kazmi, I. A. (2021) · Biomolecules · doi:10.3390/biom11111635 · Cited by 60
Evaluation and targeting of amyloid precursor protein (APP)/amyloid beta (Aβ) axis in amyloidogenic and non-amyloidogenic pathways: A time outside the tunnel
Al-Kuraishy, H. M., Jabir, M. S., Al-Gareeb, A. I., Albuhadily, A. K., Albukhaty, S., Sulaiman, G. M., & Batiha, G. E. (2023) · Ageing Research Reviews · doi:10.1016/j.arr.2023.102119 · Cited by 58
Contribution of GABAergic interneurons to amyloid-β plaque pathology in an APP knock-in mouse model
Rice, H. C., Marcassa, G., Chrysidou, I., Horré, K., Young‐Pearse, T. L., Müller, U., Saito, T., Saido, T. C., Vassar, R. J., de Wit, J., et al. (2020) · Molecular Neurodegeneration · doi:10.1186/s13024-019-0356-y · Cited by 51
Self-citation
Loss of all three APP family members during development impairs synaptic function and plasticity, disrupts learning, and causes an autism‐like phenotype
Steubler, V., Erdinger, S., Back, M. K., Ludewig, S., Fässler, D., Richter, M., Han, K., Slomianka, L., Amrein, I., von Engelhardt, J., et al. (2021) · The EMBO Journal · doi:10.15252/embj.2020107471 · Cited by 54
Differential microRNA expression analyses across two brain regions in Alzheimer’s disease
Dobricic, V., Schilling, M., Schulz, J., Zhu, L.-S., Zhou, C.-W., Fuß, J., Franzenburg, S., Zhu, L.-Q., Parkkinen, L., Lill, C. M., et al. (2022) · Translational Psychiatry · doi:10.1038/s41398-022-02108-4 · Cited by 48
Amyloid-Beta Mediates Homeostatic Synaptic Plasticity
Galanis, C., Fellenz, M., Becker, D., Bold, C. S., Lichtenthaler, S. F., Müller, U., Deller, T., & Vlachos, A. (2021) · Journal of Neuroscience · doi:10.1523/jneurosci.1820-20.2021 · Cited by 56
Opposite changes in APP processing and human Aβ levels in rats carrying either a protective or a pathogenic APP mutation
Tambini, M. D., Norris, K. A., & D'adamio, L. (2020) · eLife · doi:10.7554/elife.52612 · Cited by 48
Neurexins regulate presynaptic GABAB-receptors at central synapses
Luo, F., Sclip, A., Merrill, S. A., & Südhof, T. C. (2021) · Nature Communications · doi:10.1038/s41467-021-22753-5 · Cited by 50
Reduction in the neuronal surface of post and presynaptic GABABreceptors in the hippocampus in a mouse model of Alzheimer's disease
Martín‐Belmonte, A., Aguado, C., Alfaro‐Ruiz, R., Moreno‐Martínez, A. E., de la Ossa, L., Hernández, J. M., Buisson, A., Früh, S., Bettler, B., Shigemoto, R., et al. (2019) · Brain Pathology · doi:10.1111/bpa.12802 · Cited by 50
Brothers in Arms: ProBDNF/BDNF and sAPPα/Aβ-Signaling and Their Common Interplay with ADAM10, TrkB, p75NTR, Sortilin, and sorLA in the Progression of Alzheimer’s Disease
Eggert, S., Kins, S., Endres, K., & Brigadski, T. (2022) · Biological Chemistry · doi:10.1515/hsz-2021-0330 · Cited by 46
ELFN2 is a postsynaptic cell adhesion molecule with essential roles in controlling group III mGluRs in the brain and neuropsychiatric behavior
Dunn, H. A., Zucca, S., Dao, M. T., Orlandi, C., & Martemyanov, K. A. (2019) · Molecular Psychiatry · doi:10.1038/s41380-019-0512-3 · Cited by 46
Knockdown of Amyloid Precursor Protein: Biological Consequences and Clinical Opportunities
Gabriele, R. M. C., Abel, E., Fox, N. C., Wray, S., & Arber, C. (2022) · Frontiers in Neuroscience · doi:10.3389/fnins.2022.835645 · Cited by 44
Neuropathology of the Alzheimer's continuum: an update
Jellinger, K. A. (2020) · Free Neuropathology · doi:10.17879/freeneuropathology-2020-3050 · Cited by 52
Morphological and Molecular Profiling of Amyloid-β Species in Alzheimer’s Pathogenesis
Almeida, Z. L., Vaz, D. C., & Brito, R. M. M. (2024) · Molecular Neurobiology · doi:10.1007/s12035-024-04543-4 · Cited by 49
Next Generation Precision Medicine: CRISPR-mediated Genome Editing for the Treatment of Neurodegenerative Disorders
Raikwar, S. P., Kikkeri, N. S., Sakuru, R. C., Saeed, D., Zahoor, H., Premkumar, K., Mentor, S., Thangavel, R., Dubova, I., Ahmed, M. E., et al. (2019) · Journal of Neuroimmune Pharmacology · doi:10.1007/s11481-019-09849-y · Cited by 48
The Interaction Between Contactin and Amyloid Precursor Protein and Its Role in Alzheimer’s Disease
Bamford, R. A., Widagdo, J., Takamura, N., Eve, M., Anggono, V., & Oguro‐Ando, A. (2019) · Neuroscience · doi:10.1016/j.neuroscience.2019.10.006 · Cited by 47
The fusiform gyrus exhibits an epigenetic signature for Alzheimer’s disease
Ma, D., Fetahu, I. S., Wang, M., Fang, R., Li, J., Liu, H., Gramyk, T., Iwanicki, I. J., Gu, S., Xu, W., et al. (2020) · Clinical Epigenetics · doi:10.1186/s13148-020-00916-3 · Cited by 46
Acteoside exerts neuroprotection effects in the model of Parkinson's disease via inducing autophagy: Network pharmacology and experimental study
Aimaiti, M., Wumaier, A., Aisa, Y., Zhang, Y., Xirepu, X., Aibaidula, Y., Lei, X., Chen, Q., Feng, X., & Mi, N. (2021) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2021.174136 · Cited by 43
GABAB Receptor Chemistry and Pharmacology: Agonists, Antagonists, and Allosteric Modulators
Nieto, A., Bailey, T., Kaczanowska, K., & McDonald, P. H. (2021) · Current topics in behavioral neurosciences · doi:10.1007/7854_2021_232 · Cited by 43
Regulation of beta-amyloid production in neurons by astrocyte-derived cholesterolPreprint
Wang, H., Kulas, J. A., Ferris, H. A., & Hansen, S. B. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.06.18.159632 · Cited by 43
The organizing principle of GABAB receptor complexes: Physiological and pharmacological implications
Fritzius, T., & Bettler, B. (2019) · Basic & Clinical Pharmacology & Toxicology · doi:10.1111/bcpt.13241 · Cited by 41
Therapeutic effects of phlorotannins in the treatment of neurodegenerative disorders
Kwon, S. Y., Kwon, O. I., Hwang, H. J., Shin, H., & Yang, S. (2023) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2023.1193590 · Cited by 43
Density of GABAB Receptors Is Reduced in Granule Cells of the Hippocampus in a Mouse Model of Alzheimer’s Disease
Martín‐Belmonte, A., Aguado, C., Alfaro‐Ruiz, R., Moreno‐Martínez, A. E., de la Ossa, L., Hernández, J. M., Buisson, A., Shigemoto, R., Fukazawa, Y., & Luján, R. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21072459 · Cited by 39
Hydrogen-rich water ameliorates neuropathological impairments in a mouse model of Alzheimer's disease through reducing neuroinflammation and modulating intestinal microbiota
Lin, Y., Shi, Q., Zhang, L., Yue, C.-P., He, Z.-J., Li, X.-X., He, Q., Liu, Q., & Du, X. (2021) · Neural Regeneration Research · doi:10.4103/1673-5374.317992 · Cited by 39
Finding memo: versatile interactions of the VPS10p-Domain receptors in Alzheimer’s disease
Salasova, A., Monti, G., Andersen, O. M., & Nykjaer, A. (2022) · Molecular Neurodegeneration · doi:10.1186/s13024-022-00576-2 · Cited by 42
Novel Therapeutic Strategies in Alzheimer’s Disease: Pitfalls and Challenges of Anti-Amyloid Therapies and Beyond
Tondo, G., Marchi, F. D., Bonardi, F., Menegon, F., Verrini, G., Aprile, D., Anselmi, M., Mazzini, L., & Comi, C. (2024) · Journal of Clinical Medicine · doi:10.3390/jcm13113098 · Cited by 45
An agnostic reevaluation of the amyloid cascade hypothesis of Alzheimer's disease pathogenesis: The role of APP homeostasis
Caselli, R. J., Knopman, D. S., & Bu, G. (2020) · Alzheimer s & Dementia · doi:10.1002/alz.12124 · Cited by 36
The Expression and Localisation of G-Protein-Coupled Inwardly Rectifying Potassium (GIRK) Channels Is Differentially Altered in the Hippocampus of Two Mouse Models of Alzheimer’s Disease
Alfaro‐Ruiz, R., Martín‐Belmonte, A., Aguado, C., Hernández, F., Moreno‐Martínez, A. E., Ávila, J., & Luján, R. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms222011106 · Cited by 32
The vexing complexity of the amyloidogenic pathway
Castro, M., Hadziselimovic, A., & Sanders, C. R. (2019) · Protein Science · doi:10.1002/pro.3606 · Cited by 40
Amyloidosis is associated with thicker myelin and increased oligodendrogenesis in the adult mouse brain
Ferreira, S., Pitman, K. A., Wang, S., Summers, B. S., Bye, N., Young, K. M., & Cullen, C. L. (2020) · Journal of Neuroscience Research · doi:10.1002/jnr.24672 · Cited by 38
Amyloid Precursor Protein (APP) Controls the Expression of the Transcriptional Activator Neuronal PAS Domain Protein 4 (NPAS4) and Synaptic GABA Release
Opsomer, R., Contino, S., Perrin, F., Gualdani, R., Tasiaux, B., Doyen, P. J., Vergouts, M., Vrancx, C., Doshina, A., Pierrot, N., et al. (2020) · eNeuro · doi:10.1523/eneuro.0322-19.2020 · Cited by 38
Herpes Zoster virus infection and the risk of developing dementia: A systematic review and meta-analysis
Elhalag, R. H., Motawea, K. R., Talat, N. E., Rouzan, S. S., Reyad, S. M., Elsayed, S. M., Chèbl, P., Abowafia, M., & Shah, J. (2023) · Medicine · doi:10.1097/md.0000000000034503 · Cited by 34
A Novel CCK Receptor GPR173 Mediates Potentiation of GABAergic Inhibition
He, L. S., Shi, H., Zhang, G., Peng, Y., Ghosh, A., Zhang, M., Hu, X., Liu, C., Shao, Y., Wang, S., et al. (2023) · Journal of Neuroscience · doi:10.1523/jneurosci.2035-22.2023 · Cited by 32
GABA and glutamate moderate beta-amyloid related functional connectivity in cognitively unimpaired old-aged adults
Quevenco, F. C., Schreiner, S. J., Preti, M. G., Bergen, J. M. G. V., Kirchner, T., Wyss, M. T., Steininger, S. C., Gietl, A. F., Leh, S. E., Buck, A., et al. (2019) · NeuroImage Clinical · doi:10.1016/j.nicl.2019.101776 · Cited by 31
Amyloid precursor protein and its interacting proteins in neurodevelopment
Chau, D. D., Ng, L. L.-H., Zhai, Y., & Lau, K. (2023) · Biochemical Society Transactions · doi:10.1042/bst20221527 · Cited by 34
Amyloid Precursor Protein (APP) and GABAergic Neurotransmission
Tang, B. L. (2019) · Cells · doi:10.3390/cells8060550 · Cited by 34
Controversial Properties of Amyloidogenic Proteins and Peptides: New Data in the COVID Era
Surguchov, A. P., Emamzadeh, F. N., Titova, M., & Surguchev, A. A. (2023) · Biomedicines · doi:10.3390/biomedicines11041215 · Cited by 33
Family C G-Protein-Coupled Receptors in Alzheimer’s Disease and Therapeutic Implications
Prà, I. D., Armato, U., & Chiarini, A. (2019) · Frontiers in Pharmacology · doi:10.3389/fphar.2019.01282 · Cited by 31
Somatostatin and the pathophysiology of Alzheimer’s disease
Almeida, V. N. (2024) · Ageing Research Reviews · doi:10.1016/j.arr.2024.102270 · Cited by 31
APP-Mediated Signaling Prevents Memory Decline in Alzheimer’s Disease Mouse Model
Deyts, C., Clutter, M., Pierce, N., Chakrabarty, P., Ladd, T. B., GODDI, A. A., Rosario, A. M., Cruz, P. E., Vetrivel, K. S., Wagner, S. L., et al. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.03.087 · Cited by 31
Disrupted neural correlates of anesthesia and sleep reveal early circuit dysfunctions in Alzheimer models
Zarhin, D., Atsmon, R., Ruggiero, A., Baeloha, H., Shoob, S., Scharf, O., Heim, L. R., Buchbinder, N., Shinikamin, O., Shapira, I., et al. (2022) · Cell Reports · doi:10.1016/j.celrep.2021.110268 · Cited by 32
Self-citation
Lack of APP and APLP2 in GABAergic Forebrain Neurons Impairs Synaptic Plasticity and Cognition
Mehr, A., Hick, M., Ludewig, S., Müller, M., Herrmann, U., von Engelhardt, J., Wolfer, D. P., Körte, M., & Müller, U. (2020) · Cerebral Cortex · doi:10.1093/cercor/bhaa025 · Cited by 30
Overexpression of wild-type human amyloid precursor protein alters GABAergic transmission
Kreis, A., Desloovere, J., Suelves, N., Pierrot, N., Yerna, X., Issa, F., Schakman, O., Gualdani, R., de Clippele, M., Tajeddine, N., et al. (2021) · Scientific Reports · doi:10.1038/s41598-021-97144-3 · Cited by 29
Infection‐induced endothelial amyloids impair memory
Balczon, R., Pittet, J., Wagener, B. M., Moser, S. A., Voth, S. B., Vorhees, C. V., Williams, M. T., Bridges, J. P., Alvarez, D. F., Koloteva, A., et al. (2019) · The FASEB Journal · doi:10.1096/fj.201900322r · Cited by 28
Amyloid-β1–43 cerebrospinal fluid levels and the interpretation of APP, PSEN1 and PSEN2 mutations
Perrone, F., Bjerke, M., Hens, E., Sieben, A., Timmers, M., Roeck, A. D., Vandenberghe, R. R., Sleegers, K., Martin, J., Deyn, P. P. D., et al. (2020) · Alzheimer s Research & Therapy · doi:10.1186/s13195-020-00676-5 · Cited by 28
MDGA1 negatively regulates amyloid precursor protein–mediated synapse inhibition in the hippocampus
Kim, J., Kim, S., Kim, H., Hwang, I.-W., Bae, S., Karki, S., Kim, D., Ogelman, R., Bang, G., Kim, J. Y., et al. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2115326119 · Cited by 29
Intercellular signaling by ectodomain shedding at the synapse
Martin‐de‐Saavedra, M. D., Santos, M. D., & Penzes, P. (2022) · Trends in Neurosciences · doi:10.1016/j.tins.2022.03.004 · Cited by 27
MT5-MMP promotes neuroinflammation, neuronal excitability and Aβ production in primary neuron/astrocyte cultures from the 5xFAD mouse model of Alzheimer’s disease
Pilat, D., Paumier, J.-M., García-González, L., Louis, L., Stephan, D., Manrique, C., Khrestchatisky, M., Di Pasquale, E., Baranger, K., & Rivera, S. (2022) · Journal of Neuroinflammation · doi:10.1186/s12974-022-02407-z · Cited by 28

Authors: Rice, H. C., de Malmazet, D., Schreurs, A., Frere, S., Van Molle, I., Volkov, A. N., Creemers, E., Vertkin, I., Nys, J., Ranaivoson, F. M., Comoletti, D., Savas, J. N., Remaut, H., Balschun, D., Wierda, K. D., Slutsky, I., Farrow, K., De Strooper, B., & de Wit, J.
Affiliations: VIB-KU Leuven Center for Brain & Disease Research (BE)
Neuro-Electronics Research Flanders, Leuven, Belgium.
KU Leuven (BE)
Department of Physiology and Pharmacology, Sackler Faculty of Medicine and Sagol School of Neuroscience, Tel Aviv University, Tel Aviv, Israel.
VIB–VUB Structural Biology Research Center, Brussels, Belgium.
Vrije Universiteit Brussel (BE)
Tel Aviv University (IL)
Rutgers, The State University of New Jersey (US)
Northwestern University (US)
VIB-VUB Center for Structural Biology (BE)
IMEC (BE)
VIB Center for Brain & Disease Research, Leuven, Belgium.
ORCID: Rice, Heather C.
Schreurs, An
Frere, Samuel
Van Molle, Inge
Volkov, Alexander N.
Creemers, Eline
Vertkin, Irena
Ranaivoson, Fanomezana M.
Comoletti, Davide
Savas, Jeffrey N.
Remaut, Han
Balschun, Detlef
Wierda, Keimpe D.
Slutsky, Inna
Farrow, Karl
de Wit, Joris
Venue: Science
Publisher: American Association for the Advancement of Science (AAAS)
Published: 2019-01-11
Volume: 363
Issue: 6423
ISSN: 0036-8075 (ISSN-L)
1095-9203
DOI: 10.1126/science.aao4827
PMC: PMC6366617
OpenAlex: W2910128841
Cited by: 281
References: 74
Citations by year: 2026: 20 · 2025: 23 · 2024: 31 · 2023: 33 · 2022: 33 · 2021: 47 · 2020: 56 · 2019: 38
FWCI: 21.01
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Locations: Science (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Lirias (KU Leuven) (submittedVersion, other-oa)
UCL Discovery (University College London) (submittedVersion)
Open Access Victoria University of Wellington | Te Herenga Waka (Figshare) (submittedVersion, cc-by-nc-nd)
VUBIR (Vrije Universiteit Brussel) (submittedVersion)
Victoria University of Wellington
Funders: National Science Foundation (BRAIN EAGER MCB-1450895, IOS-1755189)
National Institutes of Health (RO1AG061787)
Robert Wood Johnson Foundation (74260)
Alzheimer's Association (AARF-16-442885)
European Research Council (724866, 311083)
Fonds Wetenschappelijk Onderzoek (G094616N, G.0D76.14)
Leuven Universiteit Fonds
Geneeskundige Stichting Koningin Elisabeth
KU Leuven Methusalem Grant
Vlaams Initiatief voor Netwerken voor Dementie Onderzoek (135043)
Stichting Voor Alzheimer Onderzoek (P#16011)
Agency for Innovation by Science and Technology (141698)
VUB onderzoeksfonds (SRP13)
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Alzheimer's disease research and treatments
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Receptor Mechanisms and Signaling
Keywords: GABAB receptors, synaptic transmission, synaptic plasticity, synaptic vesicle release, sushi domain, GABA signaling, Alzheimer's disease, therapeutic target
MeSH terms: Protein Domains, Amino Acid Sequence, Animals, Cells, Cultured, Hippocampus, Humans, Male, Membrane Proteins, Mice, Inbred BALB C, Mice, Inbred C57BL, Synaptic Transmission, Neuronal Plasticity, Neurons, Peptides, Protein Binding, Receptors, GABA-A, Synapses, Synaptic Vesicles, Amyloid beta-Protein Precursor, Mice, Knockout, Proteomics, Mice, HEK293 Cells

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

Secreted amyloid-β precursor protein functions as a GABA B R1a ligand to modulate synaptic transmission

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Claims other papers make about this one

Self-check

Citations

Cites

Cited by

Related

Metadata

Record

About these checks