Local and global influences on protein turnover in neurons and glia

eLife - Tập 7
Aline Ricarda Dörrbaum1,2, Lisa Kochen2, Julian D. Langer2,3, Erin M. Schuman2
1Faculty of Biological Sciences, Goethe University Frankfurt, Frankfurt, Germany
2Max Planck Institute for Brain Research, Frankfurt, Germany
3Max Planck Institute of Biophysics, Frankfurt, Germany

Tóm tắt

Regulation of protein turnover allows cells to react to their environment and maintain homeostasis. Proteins can show different turnover rates in different tissue, but little is known about protein turnover in different brain cell types. We used dynamic SILAC to determine half-lives of over 5100 proteins in rat primary hippocampal cultures as well as in neuron-enriched and glia-enriched cultures ranging from <1 to >20 days. In contrast to synaptic proteins, membrane proteins were relatively shorter-lived and mitochondrial proteins were longer-lived compared to the population. Half-lives also correlate with protein functions and the dynamics of the complexes they are incorporated in. Proteins in glia possessed shorter half-lives than the same proteins in neurons. The presence of glia sped up or slowed down the turnover of neuronal proteins. Our results demonstrate that both the cell-type of origin as well as the nature of the extracellular environment have potent influences on protein turnover.

Từ khóa


Tài liệu tham khảo

Aakalu, 2001, Dynamic visualization of local protein synthesis in hippocampal neurons, Neuron, 30, 489, 10.1016/S0896-6273(01)00295-1

Adam-Vizi, 2006, Bioenergetics and the formation of mitochondrial reactive oxygen species, Trends in Pharmacological Sciences, 27, 639, 10.1016/j.tips.2006.10.005

Ahmad, 2002, The histone variant H3.3 marks active chromatin by replication-independent nucleosome assembly, Molecular Cell, 9, 1191, 10.1016/S1097-2765(02)00542-7

Alvarez-Castelao, 2017, Cell-type-specific metabolic labeling of nascent proteomes in vivo, Nature Biotechnology, 35, 1196, 10.1038/nbt.4016

Bachmair, 1986, In vivo half-life of a protein is a function of its amino-terminal residue, Science, 234, 179, 10.1126/science.3018930

Beck, 2017, The nuclear pore complex: understanding its function through structural insight, Nature Reviews Molecular Cell Biology, 18, 73, 10.1038/nrm.2016.147

Bertram, 2017, Cryo-EM Structure of a Pre-catalytic Human Spliceosome Primed for Activation, Cell, 170, 701, 10.1016/j.cell.2017.07.011

Boisvert, 2012, A quantitative spatial proteomics analysis of proteome turnover in human cells, Molecular & Cellular Proteomics, 11, M111.011429, 10.1074/mcp.M111.011429

Cagalinec, 2013, Principles of the mitochondrial fusion and fission cycle in neurons, Journal of Cell Science, 126, 2187, 10.1242/jcs.118844

Cambridge, 2011, Systems-wide proteomic analysis in mammalian cells reveals conserved, functional protein turnover, Journal of Proteome Research, 10, 5275, 10.1021/pr101183k

Cohen, 2013, Metabolic turnover of synaptic proteins: kinetics, interdependencies and implications for synaptic maintenance, PLoS One, 8, e63191, 10.1371/journal.pone.0063191

Cox, 2008, MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification, Nature Biotechnology, 26, 1367, 10.1038/nbt.1511

Daigle, 2001, Nuclear pore complexes form immobile networks and have a very low turnover in live mammalian cells, The Journal of Cell Biology, 154, 71, 10.1083/jcb.200101089

Dieterich, 2006, Selective identification of newly synthesized proteins in mammalian cells using bioorthogonal noncanonical amino acid tagging (BONCAT), PNAS, 103, 9482, 10.1073/pnas.0601637103

Ehlers, 2003, Activity level controls postsynaptic composition and signaling via the ubiquitin-proteasome system, Nature Neuroscience, 6, 231, 10.1038/nn1013

Gibbs, 2014, The eukaryotic N-end rule pathway: conserved mechanisms and diverse functions, Trends in Cell Biology, 24, 603, 10.1016/j.tcb.2014.05.001

Goldberg, 2014, LocTree3 prediction of localization, Nucleic Acids Research, 42, W350, 10.1093/nar/gku396

Gomes, 2008, High levels of Fis1, a pro-fission mitochondrial protein, trigger autophagy, Biochimica et Biophysica Acta (BBA) - Bioenergetics, 1777, 860, 10.1016/j.bbabio.2008.05.442

Holt, 2013, The central dogma decentralized: new perspectives on RNA function and local translation in neurons, Neuron, 80, 648, 10.1016/j.neuron.2013.10.036

Jin, 2018, The where, what, and when of membrane protein degradation in neurons, Developmental Neurobiology, 78, 283, 10.1002/dneu.22534

Kang, 1996, A requirement for local protein synthesis in neurotrophin-induced hippocampal synaptic plasticity, Science, 273, 1402, 10.1126/science.273.5280.1402

Kucharczyk, 2009, Mitochondrial ATP synthase disorders: molecular mechanisms and the quest for curative therapeutic approaches, Biochimica Et Biophysica Acta (BBA) - Molecular Cell Research, 1793, 186, 10.1016/j.bbamcr.2008.06.012

Lin, 2016, Architecture of the symmetric core of the nuclear pore, Science, 352, aaf1015, 10.1126/science.aaf1015

Magistretti, 1999, Astrocytes Couple Synaptic Activity to Glucose Utilization in the Brain, Physiology, 14, 177, 10.1152/physiologyonline.1999.14.5.177

Martin-Perez, 2017, Determinants and regulation of protein turnover in yeast, Cell Systems, 5, 283, 10.1016/j.cels.2017.08.008

Mason, 2017, Lactate shuttles in Neuroenergetics-Homeostasis, allostasis and beyond, Frontiers in Neuroscience, 11, 43, 10.3389/fnins.2017.00043

Mathieson, 2018, Systematic analysis of protein turnover in primary cells, Nature Communications, 9, 689, 10.1038/s41467-018-03106-1

McShane, 2016, Kinetic analysis of protein stability reveals age-dependent degradation, Cell, 167, 803, 10.1016/j.cell.2016.09.015

Mi, 2013, Large-scale gene function analysis with the PANTHER classification system, Nature Protocols, 8, 1551, 10.1038/nprot.2013.092

O'Shea, 2013, pLogo: a probabilistic approach to visualizing sequence motifs, Nature Methods, 10, 1211, 10.1038/nmeth.2646

Peña, 2017, Eukaryotic ribosome assembly, transport and quality control, Nature Structural & Molecular Biology, 24, 689, 10.1038/nsmb.3454

Price, 2010, Analysis of proteome dynamics in the mouse brain, PNAS, 107, 14508, 10.1073/pnas.1006551107

Pulk, 2010, Ribosome reactivation by replacement of damaged proteins, Molecular Microbiology, 75, 801, 10.1111/j.1365-2958.2009.07002.x

Purdy, 2014, Function and dynamics of macromolecular complexes explored by integrative structural and computational biology, Current Opinion in Structural Biology, 27, 138, 10.1016/j.sbi.2014.08.006

Rabut, 2004, Mapping the dynamic organization of the nuclear pore complex inside single living cells, Nature Cell Biology, 6, 1114, 10.1038/ncb1184

Rappsilber, 2007, Protocol for micro-purification, enrichment, pre-fractionation and storage of peptides for proteomics using StageTips, Nature Protocols, 2, 1896, 10.1038/nprot.2007.261

Rosenberg, 2014, The roles of protein expression in synaptic plasticity and memory consolidation, Frontiers in Molecular Neuroscience, 7, 86, 10.3389/fnmol.2014.00086

Ruepp, 2010, CORUM: the comprehensive resource of mammalian protein complexes--2009, Nucleic Acids Research, 38, D497, 10.1093/nar/gkp914

Savas, 2012, Extremely long-lived nuclear pore proteins in the rat brain, Science, 335, 942, 10.1126/science.1217421

Schanzenbächer, 2018, Time- and polarity-dependent proteomic changes associated with homeostatic scaling at central synapses, eLife, 7, e33322, 10.7554/eLife.33322

Schanzenbächer, 2016, Nascent Proteome Remodeling following Homeostatic Scaling at Hippocampal Synapses, Neuron, 92, 358, 10.1016/j.neuron.2016.09.058

Schwartz, 2005, Transcriptional activation triggers deposition and removal of the histone variant H3.3, Genes & Development, 19, 804, 10.1101/gad.1259805

Sharma, 2015, Cell type- and brain region-resolved mouse brain proteome, Nature Neuroscience, 18, 1819, 10.1038/nn.4160

Sutton, 2006, Dendritic protein synthesis, synaptic plasticity, and memory, Cell, 127, 49, 10.1016/j.cell.2006.09.014

Tai, 2008, Ubiquitin, the proteasome and protein degradation in neuronal function and dysfunction, Nature Reviews Neuroscience, 9, 826, 10.1038/nrn2499

tom Dieck, 2015, Direct visualization of newly synthesized target proteins in situ, Nature Methods, 12, 411, 10.1038/nmeth.3319

Toyama, 2013, Identification of long-lived proteins reveals exceptional stability of essential cellular structures, Cell, 154, 971, 10.1016/j.cell.2013.07.037

Tuchev G. 2017. NeuroBits. GitHub. https://githubmolgenmpgde/MPIBR/NeuroBits.

Tyanova, 2016, The MaxQuant computational platform for mass spectrometry-based shotgun proteomics, Nature Protocols, 11, 2301, 10.1038/nprot.2016.136

Tyanova, 2016, The Perseus computational platform for comprehensive analysis of (prote)omics data, Nature Methods, 13, 731, 10.1038/nmeth.3901

Vinothkumar, 2016, Structure of the mitochondrial ATP synthase from Pichia angusta determined by electron cryo-microscopy, PNAS, 113, 12709, 10.1073/pnas.1615902113

Visscher, 2016, Proteome-wide Changes in Protein Turnover Rates in C. elegans Models of Longevity and Age-Related Disease, Cell Reports, 16, 3041, 10.1016/j.celrep.2016.08.025

Vizcaíno, 2013, The PRoteomics IDEntifications (PRIDE) database and associated tools: status in 2013, Nucleic Acids Research, 41, D1063, 10.1093/nar/gks1262

Voorhees, 2014, Structure of the mammalian ribosome-Sec61 complex to 3.4 Å resolution, Cell, 157, 1632, 10.1016/j.cell.2014.05.024

Warner, 2009, How common are extraribosomal functions of ribosomal proteins?, Molecular Cell, 34, 3, 10.1016/j.molcel.2009.03.006

Wiśniewski, 2009, Universal sample preparation method for proteome analysis, Nature Methods, 6, 359, 10.1038/nmeth.1322

Wohlgemuth, 2015, Studying macromolecular complex stoichiometries by peptide-based mass spectrometry, Proteomics, 15, 862, 10.1002/pmic.201400466

Wu, 1982, Patterns of histone variant synthesis can distinguish G0 from G1 cells, Cell, 31, 367, 10.1016/0092-8674(82)90130-1

Xue, 2012, Specialized ribosomes: a new frontier in gene regulation and organismal biology, Nature Reviews Molecular Cell Biology, 13, 355, 10.1038/nrm3359

Thông tin
Thông tin xuất bản

eLife

Tập 7

Thông tin tác giả