دورية أكاديمية

Activity dependent dissociation of the Homer1 interactome.

التفاصيل البيبلوغرافية
العنوان: Activity dependent dissociation of the Homer1 interactome.
المؤلفون: Stillman M; Center for Integrative Brain Research, Seattle Children's Research Institute, Seattle, WA, USA.; Dartmouth-Hitchcock Medical Center Psychiatry Residency Program, Dartmouth, NH, USA., Lautz JD; Center for Integrative Brain Research, Seattle Children's Research Institute, Seattle, WA, USA., Johnson RS; Department of Genome Sciences, University of Washington, Seattle, WA, USA., MacCoss MJ; Department of Genome Sciences, University of Washington, Seattle, WA, USA., Smith SEP; Center for Integrative Brain Research, Seattle Children's Research Institute, Seattle, WA, USA. seps@uw.edu.; Department of Pediatrics, University of Washington, Seattle, WA, USA. seps@uw.edu.; Graduate Program in Neuroscience, University of Washington, Seattle, WA, USA. seps@uw.edu.
المصدر: Scientific reports [Sci Rep] 2022 Feb 25; Vol. 12 (1), pp. 3207. Date of Electronic Publication: 2022 Feb 25.
نوع المنشور: Journal Article; Research Support, N.I.H., Extramural; Research Support, Non-U.S. Gov't
اللغة: English
بيانات الدورية: Publisher: Nature Publishing Group Country of Publication: England NLM ID: 101563288 Publication Model: Electronic Cited Medium: Internet ISSN: 2045-2322 (Electronic) Linking ISSN: 20452322 NLM ISO Abbreviation: Sci Rep Subsets: MEDLINE
أسماء مطبوعة: Original Publication: London : Nature Publishing Group, copyright 2011-
مواضيع طبية MeSH: Neurons*/metabolism , Synapses*/metabolism, Animals ; Cerebral Cortex/metabolism ; Homer Scaffolding Proteins/genetics ; Homer Scaffolding Proteins/metabolism ; Mice ; Mice, Knockout ; Microfilament Proteins/metabolism ; Nerve Tissue Proteins/genetics ; Nerve Tissue Proteins/metabolism
مستخلص: Neurons encode information by rapidly modifying synaptic protein complexes, which changes the strength of specific synaptic connections. Homer1 is abundantly expressed at glutamatergic synapses, and is known to alter its binding to metabotropic glutamate receptor 5 (mGlu5) in response to synaptic activity. However, Homer participates in many additional known interactions whose activity-dependence is unclear. Here, we used co-immunoprecipitation and label-free quantitative mass spectrometry to characterize activity-dependent interactions in the cerebral cortex of wildtype and Homer1 knockout mice. We identified a small, high-confidence protein network consisting of mGlu5, Shank2 and 3, and Homer1-3, of which only mGlu5 and Shank3 were significantly reduced following neuronal depolarization. We identified several other proteins that reduced their co-association in an activity-dependent manner, likely mediated by Shank proteins. We conclude that Homer1 dissociates from mGlu5 and Shank3 following depolarization, but our data suggest that direct Homer1 interactions in the cortex may be more limited than expected.
(© 2022. The Author(s).)
References: Brakeman, P. R. et al. Homer: A protein that selectively binds metabotropic glutamate receptors. Nature 386(6622), 284–288 (1997). (PMID: 906928710.1038/386284a0)
Szumlinski, K. K., Kalivas, P. W. & Worley, P. F. Homer proteins: Implications for neuropsychiatric disorders. Curr. Opin. Neurobiol. 16(3), 251–257 (2006). (PMID: 1670493210.1016/j.conb.2006.05.002)
Hayashi, M. K. et al. The postsynaptic density proteins Homer and Shank form a polymeric network structure. Cell 137(1), 159–171 (2009). (PMID: 19345194268091710.1016/j.cell.2009.01.050)
Tu, J. C. et al. Homer binds a novel proline-rich motif and links group 1 metabotropic glutamate receptors with IP3 receptors. Neuron 21(4), 717–726 (1998). (PMID: 980845910.1016/S0896-6273(00)80589-9)
Li, Z. et al. Homer tetramer promotes actin bundling activity of drebrin. Structure 27(1), 27-38.e4 (2019). (PMID: 3050377810.1016/j.str.2018.10.011)
Shiraishi-Yamaguchi, Y. & Furuichi, T. The Homer family proteins. Genome Biol. 8(2), 206 (2007). (PMID: 17316461185240810.1186/gb-2007-8-2-206)
Tu, J. C. et al. Coupling of mGluR/Homer and PSD-95 complexes by the Shank family of postsynaptic density proteins. Neuron 23(3), 583–592 (1999). (PMID: 1043326910.1016/S0896-6273(00)80810-7)
Monteiro, P. & Feng, G. SHANK proteins: Roles at the synapse and in autism spectrum disorder. Nat. Rev. Neurosci. 18(3), 147–157 (2017). (PMID: 2817964110.1038/nrn.2016.183)
Dosemeci, A., Weinberg, R. J., Reese, T. S. & Tao-Cheng, J.-H. The postsynaptic density: There is more than meets the eye. Front. Synaptic Neurosci. 8, 23 (2016). (PMID: 27594834499054410.3389/fnsyn.2016.00023)
Sugiyama, Y., Kawabata, I., Sobue, K. & Okabe, S. Determination of absolute protein numbers in single synapses by a GFP-based calibration technique. Nat. Methods 2(9), 677–684 (2005). (PMID: 1611863810.1038/nmeth783)
Guo, W., Ceolin, L., Collins, K. A., Perroy, J. & Huber, K. M. Elevated CaMKIIα and hyperphosphorylation of Homer mediate circuit dysfunction in a fragile X syndrome mouse model. Cell Rep. 13(10), 2297–2311 (2015). (PMID: 26670047468500810.1016/j.celrep.2015.11.013)
Bottai, D. et al. Synaptic activity-induced conversion of intronic to exonic sequence in Homer 1 immediate early gene expression. J. Neurosci. Off. J. Soc. Neurosci. 22(1), 167–175 (2002). (PMID: 10.1523/JNEUROSCI.22-01-00167.2002)
Clifton, N. E., Trent, S., Thomas, K. L. & Hall, J. Regulation and function of activity-dependent homer in synaptic plasticity. Mol. Neuropsychiatry 5(3), 147–161 (2019). (PMID: 313126366597914)
Diering, G. H. et al. Homer1a drives homeostatic scaling-down of excitatory synapses during sleep. Science 355(6324), 511–515 (2017). (PMID: 28154077538271110.1126/science.aai8355)
Moutin, E. et al. Restoring glutamate receptosome dynamics at synapses rescues autism-like deficits in Shank3-deficient mice. Mol. Psychiatry 30, 1–14 (2021).
Moutin, E. et al. Dynamic remodeling of scaffold interactions in dendritic spines controls synaptic excitability. J. Cell Biol. 198(2), 251–263 (2012). (PMID: 22801779341041710.1083/jcb.201110101)
Perroy, J. et al. Direct interaction enables cross-talk between ionotropic and group I metabotropic glutamate receptors. J. Biol. Chem. 283(11), 6799–6805 (2008). (PMID: 1818239210.1074/jbc.M705661200)
Aloisi, E. et al. Altered surface mGluR5 dynamics provoke synaptic NMDAR dysfunction and cognitive defects in Fmr1 knockout mice. Nat. Commun. 8, 1103 (2017). (PMID: 29062097565365310.1038/s41467-017-01191-2)
Bear, M. F., Huber, K. M. & Warren, S. T. The mGluR theory of fragile X mental retardation. Trends Neurosci. 27(7), 370–377 (2004). (PMID: 1521973510.1016/j.tins.2004.04.009)
Lautz, J. D., Brown, E. A., Williams VanSchoiack, A. A. & Smith, S. E. P. Synaptic activity induces input-specific rearrangements in a targeted synaptic protein interaction network. J. Neurochem. 146(5), 540–559 (2018). (PMID: 29804286615082310.1111/jnc.14466)
Heavner, W. E. et al. Remodeling of the Homer–Shank interactome mediates homeostatic plasticity. Sci. Signal. 14(681), eabd7325 (2021). (PMID: 33947797830086010.1126/scisignal.abd7325)
Lautz, J. D. et al. Synaptic signaling networks encode experience by assuming stimulus-specific and brain-region-specific states. Cell Rep. 37, 110076 (2021). (PMID: 34852231872236110.1016/j.celrep.2021.110076)
Menche, J. et al. Uncovering disease–disease relationships through the incomplete human interactome. Science 347(6224), 1257601 (2015). (PMID: 25700523443574110.1126/science.1257601)
Lundby, A. et al. Oncogenic mutations rewire signaling pathways by switching protein recruitment to phosphotyrosine sites. Cell 179(2), 543-560.e26 (2019). (PMID: 3158508710.1016/j.cell.2019.09.008)
Goulding, S. P., Szumlinski, K. K., Contet, C., MacCoss, M. J. & Wu, C. C. A mass spectrometry-based proteomic analysis of Homer2-interacting proteins in the mouse brain. J. Proteomics 166, 127–137 (2017). (PMID: 28728878572263310.1016/j.jprot.2017.07.008)
Ting, J. T. et al. Preparation of acute brain slices using an optimized N-methyl-D-glucamine protective recovery method. J. Vis. Exp. JoVE. 132, e53825 (2018).
Lautz, J. D. et al. Activity-dependent changes in synaptic protein complex composition are consistent in different detergents despite differential solubility. Sci. Rep. 9(1), 10890 (2019). (PMID: 31350430665971210.1038/s41598-019-46690-y)
Szklarczyk, D. et al. The STRING database in 2021: Customizable protein-protein networks, and functional characterization of user-uploaded gene/measurement sets. Nucleic Acids Res. 49(D1), D605–D612 (2021). (PMID: 3323731110.1093/nar/gkaa1074)
Tao-Cheng, J. H., Dosemeci, A., Gallant, P. E., Smith, C. & Reese, T. Activity induced changes in the distribution of Shanks at hippocampal synapses. Neuroscience 168(1), 11–17 (2010). (PMID: 2034701510.1016/j.neuroscience.2010.03.041)
Naisbitt, S. et al. Shank, a novel family of postsynaptic density proteins that binds to the NMDA receptor/PSD-95/GKAP complex and cortactin. Neuron 23(3), 569–582 (1999). (PMID: 1043326810.1016/S0896-6273(00)80809-0)
MacGillavry, H. D., Kerr, J. M., Kassner, J., Frost, N. A. & Blanpied, T. A. Shank–cortactin interactions control actin dynamics to maintain flexibility of neuronal spines and synapses. Eur. J. Neurosci. 43(2), 179–193 (2016). (PMID: 2654783110.1111/ejn.13129)
Uruno, T. et al. Activation of Arp2/3 complex-mediated actin polymerization by cortactin. Nat. Cell Biol. 3(3), 259–266 (2001). (PMID: 1123157510.1038/35060051)
Weaver, A. M. et al. Cortactin promotes and stabilizes Arp2/3-induced actin filament network formation. Curr. Biol. CB. 11(5), 370–374 (2001). (PMID: 1126787610.1016/S0960-9822(01)00098-7)
Kang, J., Park, H. & Kim, E. IRSp53/BAIAP2 in dendritic spine development, NMDA receptor regulation, and psychiatric disorders. Neuropharmacology 100, 27–39 (2016). (PMID: 2627584810.1016/j.neuropharm.2015.06.019)
Choi, J. et al. Regulation of dendritic spine morphogenesis by insulin receptor substrate 53, a downstream effector of Rac1 and Cdc42 small GTPases. J. Neurosci. Soc. Neurosci. 25(4), 869–879 (2005). (PMID: 10.1523/JNEUROSCI.3212-04.2005)
Soltau, M., Richter, D. & Kreienkamp, H.-J. The insulin receptor substrate IRSp53 links postsynaptic shank1 to the small G-protein cdc42. Mol. Cell. Neurosci. 21(4), 575–583 (2002). (PMID: 1250459110.1006/mcne.2002.1201)
Bockmann, J., Kreutz, M. R., Gundelfinger, E. D. & Böckers, T. M. ProSAP/Shank postsynaptic density proteins interact with insulin receptor tyrosine kinase substrate IRSp53. J. Neurochem. 83(4), 1013–1017 (2002). (PMID: 1242137510.1046/j.1471-4159.2002.01204.x)
Wessel, D. & Flügge, U. I. A method for the quantitative recovery of protein in dilute solution in the presence of detergents and lipids. Anal. Biochem. 138(1), 141–143 (1984). (PMID: 673183810.1016/0003-2697(84)90782-6)
Amodei, D. et al. Improving precursor selectivity in data-independent acquisition using overlapping windows. J. Am. Soc. Mass Spectrom. 30(4), 669–684 (2019). (PMID: 30671891644582410.1007/s13361-018-2122-8)
Searle, B. C. et al. Chromatogram libraries improve peptide detection and quantification by data independent acquisition mass spectrometry. Nat. Commun. 9(1), 5128 (2018). (PMID: 30510204627745110.1038/s41467-018-07454-w)
Gessulat, S. et al. Prosit: Proteome-wide prediction of peptide tandem mass spectra by deep learning. Nat. Methods 16(6), 509–518 (2019). (PMID: 3113376010.1038/s41592-019-0426-7)
MacLean, B. et al. Skyline: An open source document editor for creating and analyzing targeted proteomics experiments. Bioinformatics Oxf. Engl. 26(7), 966–968 (2010). (PMID: 10.1093/bioinformatics/btq054)
معلومات مُعتمدة: P41 GM103533 United States GM NIGMS NIH HHS; R01 MH113545 United States MH NIMH NIH HHS; R01 MH121487 United States MH NIMH NIH HHS
المشرفين على المادة: 0 (Homer Scaffolding Proteins)
0 (Homer1 protein, mouse)
0 (Microfilament Proteins)
0 (Nerve Tissue Proteins)
0 (Shank2 protein, mouse)
0 (Shank3 protein, mouse)
تواريخ الأحداث: Date Created: 20220226 Date Completed: 20220412 Latest Revision: 20221024
رمز التحديث: 20240829
مُعرف محوري في PubMed: PMC8881602
DOI: 10.1038/s41598-022-07179-3
PMID: 35217690
قاعدة البيانات: MEDLINE
الوصف
تدمد:2045-2322
DOI:10.1038/s41598-022-07179-3