The phosphotyrosine interaction domains of X11 and FE65 bind to distinct sites on the YENPTY motif of amyloid precursor protein
Open accessAbstract
The phosphotyrosine interaction (PI) domains (also known as the PTB, or phosphotyrosine binding, domains) of Shc and IRS-1 are recently described domains that bind peptides phosphorylated on tyrosine residues. The PI/PTB domains differ from Src homology 2 (SH2) domains in that their binding specificity is determined by residues that lie amino terminal and not carboxy terminal to the phosphotyrosine. Recently, it has been appreciated that other cytoplasmic proteins also contain PI domains. We now show that the PI domain of X11 and one of the PI domains of FE65, two neuronal proteins, bind to the cytoplasmic domain of the amyloid precursor protein ((beta)APP). (beta)APP is an integral transmembrane glycoprotein whose cellular function is unknown. One of the processing pathways of (beta)APP leads to the secretion of A(beta), the major constituent of the amyloid deposited in the brain parenchyma and vessel walls of Alzheimer's disease patients. We have found that the X11 PI domain binds a YENPTY motif in the intracellular domain of (beta)APP that is strikingly similar to the NPXY motifs that bind the Shc and IRS-1 PI/PTB domains. However, unlike the case for binding of the Shc PI/PTB domain, tyrosine phosphorylation of the YENPTY motif is not required for the binding of (beta)APP to X11 or FE65. The binding site of the FE65 PI domain appears to be different from that of X11, as mutations within the YENPTY motif differentially affect the binding of X11 and FE65. Using site-directed mutagenesis, we have identified a crucial residue within the PI domain involved in X11 and FE65 binding to (beta)APP. The binding of X11 or FE65 PI domains to residues of the YENPTY motif of (beta)APP identifies PI domains as general protein interaction domains and may have important implications for the processing of (beta)APP.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The text we found for this paper looks like another document, so the self-check wasn’t run.
Cites
High-Efficiency Transformation of Mammalian Cells by Plasmid DNA
Chen, C., & Okayama, H. (1987) · Molecular and Cellular Biology · doi:10.1128/mcb.7.8.2745 · Cited by 5,374 · see citing works
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 · see citing works
Amyloid plaque core protein in Alzheimer disease and Down syndrome.
Masters, C. L., Simms, G., Weinman, N. A., Multhaup, G., McDonald, B. L., & Beyreuther, K. (1985) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.82.12.4245 · Cited by 4,431 · see citing works
Protein modules and signalling networks
Pawson, T. (1995) · Nature · doi:10.1038/373573a0 · Cited by 2,420 · see citing works
Domain Interaction Between NMDA Receptor Subunits and the Postsynaptic Density Protein PSD-95
Kornau, H., Schenker, L. T., Kennedy, M. B., & Seeburg, P. H. (1995) · Science · doi:10.1126/science.7569905 · Cited by 1,882 · see citing works
Alzheimer's disease and Down's syndrome: Sharing of a unique cerebrovascular amyloid fibril protein
Glenner, G. G., & Wong, C. W. (1984) · Biochemical and Biophysical Research Communications · doi:10.1016/0006-291x(84)91209-9 · Cited by 1,693 · see citing works
The SH2 and SH3 domain-containing protein GRB2 links receptor tyrosine kinases to ras signaling
Lowenstein, E. J., Daly, R. J., Batzer, A., Li, W., Margolis, B. L., Lammers, R., Ullrich, A., Skolnik, E. Y., Bar‐Sagi, D., & Schlessinger, J. (1992) · Cell · doi:10.1016/0092-8674(92)90167-b · Cited by 1,632 · see citing works
Self-citationBrenman, J. E., Chao, D. S., Gee, S., McGee, A. W., Craven, S. E., Santillano, D. R., Wu, Z., Huang, F., Xia, H., Peters, M. F., et al. (1996) · Cell · doi:10.1016/s0092-8674(00)81053-3 · Cited by 1,596 · see citing works
Lev, S., Moreno, H., Martinez, R., Canoll, P., Peles, E., Musacchio, J. M., Plowman, G. D., Rudy, B., & Schlessinger, J. (1995) · Nature · doi:10.1038/376737a0 · Cited by 1,381 · see citing works
A novel transforming protein (SHC) with an SH2 domain is implicated in mitogenic signal transduction
Pelicci, G., Lanfrancone, L., Grignani, F., McGlade, J. C., Cavallo, F., Forni, G., Nicoletti, I., Grignani, F., Pawson, T. J., & Pelicci, P. G. (1992) · Cell · doi:10.1016/0092-8674(92)90536-l · Cited by 1,326 · see citing works
Doyle, D., Lee, A., Lewis, J. H., Kim, E., Sheng, M., & MacKinnon, R. (1996) · Cell · doi:10.1016/s0092-8674(00)81307-0 · Cited by 1,170 · see citing works
Evidence that production and release of amyloid beta-protein involves the endocytic pathway
Koo, E. H., & Squazzo, S. L. (1994) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)32449-3 · Cited by 989 · see citing works
Rozakis-Adcock, M., McGlade, J. C., Mbamalu, G., Pelicci, G., Daly, R. J., Li, W., Batzer, A., Thomas, S. Μ., Brugge, J. S., Pelicci, P. G., et al. (1992) · Nature · doi:10.1038/360689a0 · Cited by 973 · see citing works
Brenman, J. E., Chao, D. S., Xia, H., Aldape, K. D., & Bredt, D. S. (1995) · Cell · doi:10.1016/0092-8674(95)90471-9 · Cited by 953 · see citing works
Chen, W. J., Goldstein, J. L., & Brown, M. S. (1990) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)39742-x · Cited by 936 · see citing works
Specific Motifs Recognized by the SH2 Domains of Csk, 3BP2, fps/fes, GRB-2, HCP, SHC, Syk, and Vav
Songyang, Z., Shoelson, S. E., McGlade, J. C., Olivier, P., Pawson, T. J., Bustelo, X. R., Barbacid, M., Sabe, H., Hanafusa, H., Yi, T., et al. (1994) · Molecular and Cellular Biology · doi:10.1128/mcb.14.4.2777 · Cited by 881 · see citing works
Staub, O., Dho, S. E., Henry, P., Correa, J., Ishikawa, T., McGlade, J. C., & Rotin, D. (1996) · The EMBO Journal · doi:10.1002/j.1460-2075.1996.tb00593.x · Cited by 842 · see citing works
Margolis, B. L., Rhee, S. G., Felder, S., Mervič, M., Lyall, R. M., Levitzki, A., Ullrich, A., Zilberstein, A., & Schlessinger, J. (1989) · Cell · doi:10.1016/0092-8674(89)90047-0 · Cited by 753 · see citing works
Self-citationFAP-1: A Protein Tyrosine Phosphatase That Associates with Fas
Sato, T., Irie, S., Kitada, S., & Reed, J. C. (1995) · Science · doi:10.1126/science.7536343 · Cited by 683 · see citing works
Waksman, G., Kominos, D., Robertson, S. C., Pant, N., Baltimore, D., Birge, R. B., Cowburn, D., Hanafusa, H., Mayer, B. J., Overduin, M., et al. (1992) · Nature · doi:10.1038/358646a0 · Cited by 675 · see citing works
Control of Daughter Cell Fates during Asymmetric Division: Interaction of Numb and Notch
Guo, M., Jan, L. Y., & Jan, Y. N. (1996) · Neuron · doi:10.1016/s0896-6273(00)80278-0 · Cited by 673 · see citing works
Skolnik, E. Y., Margolis, B. L., Mohammadi, M., Lowenstein, E. J., Fischer, R., Dreps, A., Ullrich, A., & Schlessinger, J. (1991) · Cell · doi:10.1016/0092-8674(91)90410-z · Cited by 627 · see citing works
Self-citationChen, H. I., & Sudol, M. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.17.7819 · Cited by 557 · see citing works
An Alternative to SH2 Domains for Binding Tyrosine-Phosphorylated Proteins
Kavanaugh, W. M., & Williams, L. T. (1994) · Science · doi:10.1126/science.7527937 · Cited by 499 · see citing works
Hierarchy of Binding Sites for Grb2 and Shc on the Epidermal Growth Factor Receptor
Batzer, A., Rotin, D., Ureña, J. M., Skolnik, E. Y., & Schlessinger, J. (1994) · Molecular and Cellular Biology · doi:10.1128/mcb.14.8.5192 · Cited by 479 · see citing works
beta-Amyloid peptide and a 3-kDa fragment are derived by distinct cellular mechanisms.
Haass, C., Hung, A. Y., Schlossmacher, M. G., Teplow, D. B., & Selkoe, D. J. (1993) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)53650-4 · Cited by 465 · see citing works
Schlessinger, J. (1994) · Current Opinion in Genetics & Development · doi:10.1016/0959-437x(94)90087-6 · Cited by 454 · see citing works
Buxbaum, J. D., Gandy, S., Cicchetti, P., Ehrlich, M. E., Czernik, A. J., Fracasso, R. P., Ramabhadran, T. V., Unterbeck, A., & Greengard, P. (1990) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.87.15.6003 · Cited by 450 · see citing works
Characterization of a novel protein‐binding module — the WW domain
Sudol, M., Chen, H. I., Bougeret, C., Einbond, A., & Peer Bork, B. (1995) · FEBS Letters · doi:10.1016/0014-5793(95)00550-s · Cited by 381 · see citing works
Gustafson, T. A., He, W., Craparo, A., Schaub, C. D., & O’Neill, T. J. (1995) · Molecular and Cellular Biology · doi:10.1128/mcb.15.5.2500 · Cited by 374 · see citing works
Structure and ligand recognition of the phosphotyrosine binding domain of Shc
Zhou, M., Ravichandran, K. S., Olejniczak, E. T., Petros, A. M., Meadows, R. P., Sattler, M., Harlan, J. E., Wade, W. S., Burakoff, S. J., & Fesik, S. W. (1995) · Nature · doi:10.1038/378584a0 · Cited by 364 · see citing works
Sudol, M., Bork, P., Einbond, A., Kastury, K., Druck, T., Negrini, M., Huebner, K., & Lehman, D. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.24.14733 · Cited by 342 · see citing works
Blaikie, P., Immanuel, D., Wu, J., Li, N., Yajnik, V., & Margolis, B. L. (1994) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)31593-x · Cited by 335 · see citing works
Self-citationMargolis, B. L., Li, N., Koch, A., Mohammadi, M., Hurwitz, D. R., Zilberstein, A., Ullrich, A., Pawson, T. J., & Schlessinger, J. (1990) · The EMBO Journal · doi:10.1002/j.1460-2075.1990.tb07887.x · Cited by 296 · see citing works
Self-citationFiore, F., Zambrano, N., Minopoli, G., Donini, V., Duilio, A., & Russo, T. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.52.30853 · Cited by 294 · see citing works
Cutler, R. L., Liu, L., Damen, J. E., & Krystal, G. (1993) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(20)80558-4 · Cited by 228 · see citing works
PTB Domains of IRS-1 and Shc Have Distinct but Overlapping Binding Specificities
Wolf, G., Trüb, T., Ottinger, E. A., Groninga, L., Lynch, A., White, M. F., Miyazaki, M., Lee, J., & Shoelson, S. E. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.46.27407 · Cited by 220 · see citing works
Nordstedt, C., Caporaso, G. L., Thyberg, J., Gandy, S., & Greengard, P. (1993) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)54194-6 · Cited by 208 · see citing works
Characterization of Sorting Signals in the β-Amyloid Precursor Protein Cytoplasmic Domain
Lai, A., Sisodia, S. S., & Trowbridge, I. S. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.8.3565 · Cited by 194 · see citing works
A phosphotyrosine interaction domain
Peer Bork, B., & Margolis, B. L. (1995) · Cell · doi:10.1016/0092-8674(95)90347-x · Cited by 191 · see citing works
Self-citationvan der Geer, P., Wiley, S. E., Lai, V. K.-M., Olivier, J. P., Gish, G. D., Stephens, R. M., Kaplan, D. R., Shoelson, S. E., & Pawson, T. J. (1995) · Current Biology · doi:10.1016/s0960-9822(95)00081-9 · Cited by 173 · see citing works
Margolis, B. L., Silvennoinen, O., Comoglio, F., et al. (1992) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.89.19.8894 · Cited by 171 · see citing works
Self-citationCraparo, A., O’Neill, T. J., & Gustafson, T. A. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.26.15639 · Cited by 168 · see citing works
Growth Hormone-promoted Tyrosyl Phosphorylation of SHC Proteins and SHC Association with Grb2
VanderKuur, J. A., Allevato, G., Billestrup, N., Norstedt, G., & Carter‐Su, C. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.13.7587 · Cited by 160 · see citing works
Strooper, B. D., Umans, L., Leuven, F. V., & BERGHE, H. V. D. (1993) · The Journal of Cell Biology · doi:10.1083/jcb.121.2.295 · Cited by 152 · see citing works
Shc Binding to Nerve Growth Factor Receptor Is Mediated by the Phosphotyrosine Interaction Domain
Đikić, I., Batzer, A., Blaikie, P., Obermeier, A., Ullrich, A., Schlessinger, J., & Margolis, B. L. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.25.15125 · Cited by 141 · see citing works
Self-citationpGSTag--a versatile bacterial expression plasmid for enzymatic labeling of recombinant proteins.
Ron, D., & Dressler, H. (1992) · PubMed · Cited by 136 · see citing works
Batzer, A., Blaikie, P., Nelson, K. N., Schlessinger, J., & Margolis, B. L. (1995) · Molecular and Cellular Biology · doi:10.1128/mcb.15.8.4403 · Cited by 133 · see citing works
Self-citationThe cloning of Grb10 reveals a new family of SH2 domain proteins.
Ooi, J., Yajnik, V., Immanuel, D., Gordon, M., Moskow, J. J., Buchberg, A. M., & Margolis, B. L. (1995) · PubMed · Cited by 128 · see citing works
Self-citationTartare‐Deckert, S., Sawka‐Verhelle, D., Murdaca, J., & OBBERGHEN, E. V. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.40.23456 · Cited by 114 · see citing works
Chen, Y., Grall, D., Salcini, A. E., Pelicci, P. G., Pouysségur, J., & Obberghen‐Schilling, E. V. (1996) · The EMBO Journal · doi:10.1002/j.1460-2075.1996.tb00441.x · Cited by 111 · see citing works
van der Geer, P., Wiley, S. E., Gish, G., Lai, V. K.-M., Stephens, R., White, M. F., Kaplan, D. R., & Pawson, T. J. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.3.963 · Cited by 100 · see citing works
Duilio, A., Zambrano, N., Mogavero, A. R., Ammendola, R., Cimino, F., & Russo, T. (1991) · Nucleic Acids Research · doi:10.1093/nar/19.19.5269 · Cited by 95 · see citing works
He, W., O’Neill, T. J., & Gustafson, T. A. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.40.23258 · Cited by 87 · see citing works
Charest, A., Wagner, J., Jacob, S. M., et al. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.14.8424 · Cited by 78 · see citing works
Duclos, F. J., Boschert, U., Sirugo, G., et al. (1993) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.90.1.109 · Cited by 70 · see citing works
Isakoff, S. J., Yu, Y.-P., Su, Y.-C., et al. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.8.3959 · Cited by 64 · see citing works
Expression of the Neuron-Specific FE65 Gene Marks the Development of Embryo Ganglionic Derivatives
Simeone, A., Duilio, A., Fiore, F., Acampora, D., Felice, C. D., Faraonio, R., Paolocci, F., Cimino, F., & Russo, T. (1994) · Developmental Neuroscience · doi:10.1159/000112088 · Cited by 36 · see citing works
Yajnik, V., Blaikie, P., Peer Bork, B., & Margolis, B. L. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.4.1813 · Cited by 36 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Amyloid Precursor Protein Processing and Alzheimer's Disease
O'Brien, R. J., & Wong, P. C. (2011) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-061010-113613 · Cited by 2,061 · see citing works
A Transcriptively Active Complex of APP with Fe65 and Histone Acetyltransferase Tip60
Cao, X., & Südhof, T. C. (2001) · Science · doi:10.1126/science.1058783 · Cited by 1,202 · see citing works
Borg, J.-P., Yang, Y., De Taddéo-Borg, M., Margolis, B., & Turner, R. S. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.24.14761 · Cited by 201 · see citing works
Self-citationMeyer, D., Liu, A., & Margolis, B. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.49.35113 · Cited by 126 · see citing works
Marzolo, M.-P., & Bu, G. (2009) · Seminars in Cell & Developmental Biology · doi:10.1016/j.semcdb.2008.10.005 · Cited by 122 · see citing works
Reelin: Neurodevelopmental Architect and Homeostatic Regulator of Excitatory Synapses
Wasser, C. R., & Herz, J. (2017) · Journal of Biological Chemistry · doi:10.1074/jbc.r116.766782 · Cited by 111 · see citing works
“of both Fe65 and X11 / (69), whereas ApoER2 binds a second PTB domain of”
BackgroundFunctional Roles of the Interaction of APP and Lipoprotein Receptors
Pohlkamp, T., Wasser, C. R., & Herz, J. (2017) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2017.00054 · Cited by 92 · see citing works
Del Prete, D., Rice, R. C., Rajadhyaksha, A. M., & D'Adamio, L. (2016) · Journal of Biological Chemistry · doi:10.1074/jbc.m116.733626 · Cited by 86 · see citing works
FE65 interaction with the ApoE receptor ApoEr2
Hoe, H.-S., Magill, L. A., Guenette, S., Fu, Z., Vicini, S., & Rebeck, G. W. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m600728200 · Cited by 69 · see citing works
Appoptosin is a Novel Pro-Apoptotic Protein and Mediates Cell Death in Neurodegeneration
Zhang, H., Zhang, Y.-W., Chen, Y., Huang, X., Zhou, F., Wang, W., Xian, B., Zhang, X., Masliah, E., Chen, Q., et al. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.3668-12.2012 · Cited by 68 · see citing works
Amyloid precursor protein mediates proinflammatory activation of monocytic lineage cells
Sondag, C. M., & Combs, C. K. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m313747200 · Cited by 56 · see citing works
Ikin, A. F., Sabo, S. L., Lanier, L. M., & Buxbaum, J. D. (2007) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2007.02.003 · Cited by 38 · see citing works
FE65 interacts with ADP-ribosylation factor 6 to promote neurite outgrowth
Cheung, H. N. M., Dunbar, C., Mórotz, G. M., Cheng, W. H., Chan, H. Y. E., Miller, C. C. J., & Lau, K. (2014) · The FASEB Journal · doi:10.1096/fj.13-232694 · Cited by 37 · see citing works
Minami, S. S., Sung, Y. M., Dumanis, S. B., Chi, S. H., Burns, M. P., Ann, E.-J., Suzuki, T., Turner, R. S., Park, H.-S., Pak, D. T. S., et al. (2010) · The FASEB Journal · doi:10.1096/fj.09-138123 · Cited by 28 · see citing works
- Authors
- Borg, J.-P., Ooi, J., Levy, E., & Margolis, B.
- Affiliations
- Howard Hughes Medical Institute (US)
- University of Michigan (US)
- Venue
- Molecular and Cellular Biology
- Publisher
- Informa UK Limited
- Published
- 1996-11
- Volume
- 16
- Issue
- 11
- Pages
- 6229-6241
- ISSN
- 0270-7306 (ISSN-L)
- 1098-5549
- PMC
- PMC231626
- OpenAlex
- W2162051767
- Cited by
- 477
- References
- 59
- Citations by year
- 2026: 1 · 2025: 1 · 2024: 4 · 2023: 12 · 2022: 5 · 2021: 8 · 2020: 3 · 2019: 9 · 2018: 5 · 2017: 13 · 2016: 8 · 2015: 6 · 2014: 5 · 2013: 16 · 2012: 19
- FWCI
- 16.86
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Molecular and Cellular Biology (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Howard Hughes Medical Institute
- National Institutes of Health (5r01ag011481-03)
- National Institute on Aging (AG11481)
- Topics
- Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protein Kinase Regulation and GTPase Signaling
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- X Window System, Fe65, amyloid precursor protein, NPXY motif, protein-protein binding, tyrosine phosphorylation, Alzheimer's disease, amyloid-beta, APP processing, neuronal proteins, binding site identification
- MeSH terms
- Alzheimer Disease, Amino Acid Sequence, Binding Sites, Brain, Cell Line, Friedreich Ataxia, Genetic Vectors, Humans, Kidney, Molecular Sequence Data, Nerve Tissue Proteins, Neurons, Nuclear Proteins, Recombinant Proteins, Transfection, Proto-Oncogene Proteins c-myc, Amyloid beta-Protein Precursor, src Homology Domains, Phosphotyrosine, Adaptor Proteins, Signal Transducing
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
