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SRIVASTAVA"],"technology_type":["Data-dependent acquisition","Mass Spectrometry"],"disease":["Alzheimer's Disease"],"software":[""],"submitter_keywords":["Mitochondria","Synaptosome","Excitatory neuron","Cognitive resilience","Neuroinflammation","Mapk signaling","Alzheimer's disease","Synapse vulnerability","Native-state proteomics"],"full_dataset_link":["https://www.ebi.ac.uk/pride/archive/projects/PXD068874"],"tissue":["Brain","Excitatory Synapse"],"sample_protocol":["After decapitation, each mouse brain was gently homogenized with 16-strokes at 800 rpm in 10 volumes of Medium I (0.32 M sucrose, 5 mM HEPES pH 7.5, and 0.1 mM EDTA) containing protease and phosphatase inhibitors. The bulk brain homogenate (H) was first centrifuged at 1,000 x g for 10 min to give a pellet (P1) containing nuclear and cell debris. Supernatant (S1) was then centrifuged at 12,000 x g for 20 min to produce the crude synaptosomal pellet (P2). The P2 pellet was resuspended in 500 µL Medium I and sonicated on ice until completely dissolved. Equal volumes of bulk brain homogenates and P2 fractions were diluted in 8 M urea lysis buffer (10mM TRIS, 100mM NaH2PO4, pH 8.5) with protease and phosphatase inhibitors, sonicated on ice, and centrifuged at 18,000 x g for 10 min at 4˚C. Biotinylated proteins were captured by streptavidin magnetic beads incubating 41.5 µL beads per 500 µg of protein in 500 µL RIPA buffer (50 mM Tris, 150 mM NaCl, 0.1% SDS, 0.5% sodium deoxycholate, 1% Triton X-100) for 1h at 4˚C with rotation. After incubation, beads were then washed sequentially at RT 2x with RIPA buffer for 8 min/each, 1x with 1 M KCl for 8 min, 1x with 0.1 M Na2CO3, 1x with 2 M urea in 10mM Tris-HCl (pH 8.0) for 10 sec, 2x with RIPA buffer for 8 min/each and 4x PBS. Finally, beads were then recovered on a magnetic rack, PBS was removed completely and further diluted in 100 µL PBS. For on-bead digestion of proteins from streptavidin-enriched pulldown samples, beads were washed with PBS and then resuspended in 225 μL of 50 mM ammonium bicarbonate. About 1 mM DTT was added to reduce samples for 30 min on a shaker at RT. About 5 mM iodoacetamide was added to alkylate cysteines for 30 min on a rotor at RT, protected from light. Proteins were digested overnight with 0.5 μg of lysyl on a shaker at RT. Next day, proteins were further digested by 1 μg trypsin overnight on a shaker at RT. Samples were acidified to 1% formic acid and 0.1% TFA, desalted using HLB columns, and dried using cold vacuum centrifugation. To prepare inputs via in-solution digestion, 50 µg of protein were reduced with 5 mM DTT at RT for 30 min and alkylated by 10 mM IAA in the dark for 30 min. Samples were then digested overnight with 1 µg of Lys-C at RT on a shaker. Samples were further diluted 7-fold with 50 mM ABC and digested overnight with 1 µg of trypsin at RT on a shaker. The peptide solutions were acidified to a final concentration of 1% FA and 0.1% TFA, desalted with HLB columns, and dried down in a vacuum centrifuge. Dried peptides were resuspended in loading buffer (0.1% FA and 0.03% TFA in water), then analyzed by liquid chromatography and MS as previously described."],"repository":["Pride"],"quantification_method":[""],"modification":[""],"data_protocol":["RAW files from LC–MS/MS were searched in MaxQuant (version 2.7.3.0). Data processing was performed in Perseus, where proteinGroups.txt tables were filtered to remove contaminants, reverse hits, and identifications by site only. LFQ intensities were log2 transformed, proteins not consistently quantified across replicates were excluded, and missing values were imputed from a normal distribution (width = 0.3, downshift = 1.8). Statistical analysis was conducted using unpaired two-sided Student’s t-tests, and significantly enriched proteins were visualized in volcano plots based on nominal p-values and log2 fold-changes."],"omics_type":["Proteomics"],"labhead":["UPASNA SRIVASTAVA"],"instrument_platform":[""],"labhead_affiliation":["Yale School of Medicine, Department of Neurolgy, Yale University"],"submission_type":["PARTIAL"],"species":["Mus Musculus (mouse)"],"submitter_mail":["upasna.srivastava@yale.edu"],"publication":["41953673 Espinosa-Garcia C, Srivastava U, Kumar P, Kour D, Malepati S, Tobin BR, Xiao H, Sunna S, Bowen CA, Cheng L, Bagchi P, Duong DM, Whitworth TJ, Liu X, Seyfried NT, Wood LB, Faundez V, Rangaraju S. Neuroinflammatory stress preferentially impacts synaptic MAPK signaling and mitochondria in excitatory neurons. Mol Neurodegener Adv. 2026 2(1):17 10.1186/s44477-026-00024-1"],"submitter_affiliation":["YALE UNIVERSITY"],"submitter_country":["United States"],"pubmed_abstract":["<h4>Background</h4>Understanding synapse-specific effects of neuroinflammation can provide mechanistic and therapeutically relevant insights across the spectrum of neurological diseases.<h4>Methods</h4>We applied neuron-specific proteomic biotinylation <i>in vivo</i>, differential centrifugation of brain for crude synaptosome enrichment (P2 fraction) and mass spectrometry (MS) analysis of biotinylated proteins to derive native-state proteomes of Camk2a-positive neurons and their corresponding P2 synaptic compartments. Next, in an <i>in vivo</i> model of systemic lipopolysaccharide (LPS) dosing, we examined the effects of neuroinflammation on whole neuron and synaptic compartments using a combination of MS, network analysis, confirmatory biochemical and ultrastructural assays and integrative approaches across our mouse-derived and existing human datasets.<h4>Results</h4>Ultrastructural and biochemical analyses of P2 fractions verified enrichment in synaptic elements, including synaptic vesicles and mitochondria. MS of biotinylated proteins from Camk2a-specific bulk brain homogenates (whole neuron) and P2 fractions (synaptosome) showed enrichment of > 1000 proteins, consistent with neuron-specific biotinylation, also confirmed by immunofluorescence microscopy. Camk2a-specific synaptic proteome revealed molecular signatures related to mitochondrial function, synaptic transmission, protein translation. LPS-treated mice displayed body weight loss and neuroinflammation, characterized by glial activation, increased pro-inflammatory cytokine levels and upregulated expression of Alzheimer's disease (AD)-related microglial genes. LPS-induced neuroinflammation exerted distinct effects on the synaptic proteome, including increased mitochondrial and reduced cytoskeletal-synaptic proteins, while suppressed synaptic MAPK signaling. Importantly, these changes were not observed at the whole neuron level, indicating unique vulnerability of the synapse to neuroinflammation. In line with synapse proteomic and signaling changes, LPS altered the ultrastructure of asymmetric synapses, suggesting dysregulation of excitatory neurotransmission. Co-expression network analysis of Camk2a neuronal proteins further resolved mitochondria- and synapse-specific protein modules, some of which were neuroinflammation-dependent. Neuroinflammation increased levels of a mitochondria-enriched module, and decreased levels of a pre-synaptic vesicle module, without impacting a post-synaptic membrane module. LPS-dependent mitochondrial and LPS-independent post-synaptic modules in mouse neurons mapped to post-mortem human AD brain proteomic modules which were decreased in cases with AD dementia and positively correlated to cognitive function, including pro-resilience markers for AD.<h4>Conclusion</h4>Our findings using native-state proteomics of Camk2a neurons combined with synaptosome enrichment identify proteome-level mechanisms of early synaptic vulnerability to neuroinflammation relevant to AD.<h4>Graphical abstract</h4><h4>Supplementary information</h4>The online version contains supplementary material available at 10.1186/s44477-026-00024-1."],"pubmed_title":["Neuroinflammatory stress preferentially impacts synaptic MAPK signaling and mitochondria in excitatory neurons."],"pubmed_authors":["Espinosa-Garcia Claudia C, Srivastava Upasna U, Kumar Prateek P, Kour Dilpreet D, Malepati Sneha S, Tobin Brendan R BR, Xiao Hailian H, Sunna Sydney S, Bowen Christine A CA, Cheng Lihong L, Bagchi Pritha P, Duong Duc M DM, Whitworth Ted J TJ, Liu Xinran X, Seyfried Nicholas T NT, Wood Levi B LB, Faundez Victor V, Rangaraju Srikant S"],"additional_accession":[]},"is_claimable":false,"name":"Neuroinflammatory Stress Preferentially Impacts Synaptic MAPK Signaling and Mitochondria in Excitatory Neurons","description":"In this study, we have applied cell type-specific in vivo biotinylation of proteins (CIBOP) to label Camk2a excitatory neuronal proteomes, and imposed differential centrifugation to prepare synaptosome-enriched fractions, followed by proteomic analysis of biotinylated neuronal proteins. This approach allowed us to obtain the native-state proteome of crude synaptosomes containing presynaptic (mitochondria and synaptic vesicles) and postsynaptic compartments of excitatory neurons from mouse brain, while directly contrasting them with the whole neuronal proteome. Next, we used the systemic LPS-induced neuroinflammation model to activate microglia in an AD-relevant manner, and examined how the synaptic compartment of excitatory neurons responds to neuroinflammatory stress, in contrast with the somatodendritic compartment. We observed that the effects of neuroinflammation on the synaptic compartment were indeed distinct from the somatodendritic compartment, suggestive of compartment-specific effects of neuroinflammation.","dates":{"publication":"2026-04-13","submission":"2025-09-26"},"accession":"PXD068874","cross_references":{"TAXONOMY":["NEWT:108018","NEWT:377960","NEWT:1131","NEWT:190486","NEWT:2737160","NEWT:2042546","NEWT:148942","NEWT:295546","NEWT:258594","NEWT:1126","NEWT:1129","NEWT:89187","NEWT:309807","NEWT:89184","NEWT:309800","NEWT:57577","NEWT:156563","NEWT:1323429","NEWT:876138","NEWT:44271","NEWT:193516","NEWT:2315688","NEWT:44270","NEWT:592321","NEWT:1073882","NEWT:6819","NEWT:93217","NEWT:428386","NEWT:1117","NEWT:498257","NEWT:10036","NEWT:32264","NEWT:10034","NEWT:661410","NEWT:488003","NEWT:224326","NEWT:376619","NEWT:3765","NEWT:2433","NEWT:3767","NEWT:433727","NEWT:135622","NEWT:672127","NEWT:656061","NEWT:37965","NEWT:656064","NEWT:3760","NEWT:36630","NEWT:381198","NEWT:1176302","NEWT:418106","NEWT:10029","NEWT:913645","NEWT:641809","NEWT:44250","NEWT:77151","NEWT:317447","NEWT:698761","NEWT:5530","NEWT:868565","NEWT:135674","NEWT:1562698","NEWT:11308","NEWT:12637","NEWT:2164133","NEWT:1180","NEWT:2767846","NEWT:1343074","NEWT:314344","NEWT:108061","NEWT:224308","NEWT:3134131","NEWT:49928","NEWT:160621","NEWT:110368","NCBITaxon:5204","NEWT:1916073","NEWT:1303873","NEWT:1310161","NEWT:1230383","NEWT:77133","NEWT:160620","NCBITaxon:77643","NEWT:1310165","NEWT:114727","NEWT:5516","NEWT:498211","NEWT:347256","NEWT:5518","NEWT:398007","NEWT:1527468","NEWT:498217","NEWT:498216","NEWT:11320","NEWT:1410384","NEWT:1310173","NEWT:1072569","NEWT:1072568","NEWT:161934","NEWT:1148","NEWT:5508","NEWT:135666","NEWT:419481","NEWT:5507","NEWT:1140","NCBITaxon:2157","NEWT:2066563","NEWT:1143","NEWT:1336794","NEWT:1462472","NEWT:1336795","NEWT:644042","NEWT:709964","NEWT:3710","NEWT:3712","NEWT:3711","NEWT:3714","NEWT:65121","NEWT:3716","NEWT:3715","NEWT:2065263","NEWT:1549675","NEWT:177437","NEWT:9014","NEWT:10891","NEWT:118221","NEWT:34869","NEWT:226126","NEWT:1616117","NEWT:34865","NEWT:550537","NEWT:284812","NEWT:284811","NEWT:3701","NEWT:3702","NEWT:1245466","NEWT:3704","NEWT:1246791","NEWT:34875","NEWT:10882","NEWT:1431297","NEWT:9005","NEWT:34871","NEWT:9006","NEWT:33548","NEWT:1883426","NEWT:657321","NEWT:1423687","NEWT:657322","NEWT:10886","NEWT:3707","NEWT:3708","NEWT:536231","NEWT:219813","NEWT:1301262","NEWT:319224","NEWT:2305479","NEWT:215451","NEWT:460519","NEWT:272843","NEWT:272844","NEWT:1348799","NEWT:55784","NEWT:485","NEWT:223074","NEWT:2499525","NEWT:467144","NEWT:142786","NEWT:28196","NEWT:2853422","NEWT:487","NEWT:1679718","NEWT:387344","NEWT:657318","NEWT:480","NEWT:67767","NEWT:46835","NEWT:216778","NEWT:376686","NEWT:237610","EFO:0001352","NEWT:219809","NEWT:219808","NEWT:119562","NEWT:1883446","NEWT:1233435","NEWT:118223","NEWT:141469","NEWT:272831","NEWT:987059","NEWT:491","NEWT:422203","NEWT:460523","NEWT:2422","NEWT:2423","NEWT:85694","NEWT:85692","NEWT:911045","NEWT:3750","NEWT:85698","NEWT:291146","NEWT:233271","NEWT:3745","NEWT:1715989","NCBITaxon:4751","NEWT:3747","NEWT:278161","NEWT:415978","NEWT:410289","NEWT:191701","NEWT:9054","NEWT:472","NEWT:29459","NEWT:34839","NEWT:476","NEWT:28128","NEWT:470","NEWT:41122","NEWT:1328300","NEWT:748693","NEWT:106299","NCBITaxon:50557","NEWT:63363","NEWT:3735","NEWT:29491","NEWT:911022","NEWT:446","NEWT:153481","NEWT:714485","NEWT:445","NEWT:2003758","NEWT:29486","NEWT:63366","NEWT:63367","NEWT:29488","NEWT:215402","NEWT:3726","NEWT:1862567","NEWT:591090","NEWT:30455","NEWT:28141","NEWT:9030","NEWT:9031","NEWT:3728","NEWT:108931","NEWT:219799","NEWT:1325292","NEWT:219798","NEWT:548","NEWT:150475","NEWT:546","NEWT:1431340","NEWT:256737","NEWT:51350","NEWT:8694","NEWT:8692","NEWT:542","NEWT:394503","NEWT:13076","NEWT:219785","NEWT:451515","NEWT:8673","NEWT:550","NEWT:10804","NEWT:52694","NEWT:554","NEWT:451516","NEWT:552","NEWT:1325291","NEWT:42410","NEWT:40686","NEWT:1225786","NEWT:366497","NEWT:771870","NEWT:8665","NEWT:51338","NEWT:771875","NEWT:377142","NEWT:9995","NEWT:28112","NEWT:49012","NEWT:28110","NEWT:10832","NEWT:311339","NEWT:507601","NEWT:520","NEWT:64657","NEWT:186441","NEWT:2585209","NEWT:643680","NEWT:214092","NEWT:40697","NEWT:13095","NEWT:162425","NEWT:242124","NEWT:9986","NEWT:8654","NEWT:536","NEWT:8658","NEWT:1268063","NEWT:8657","NEWT:9983","NEWT:8655","NEWT:80833","NEWT:479096","NEWT:28108","NEWT:28104","NEWT:1114957","NEWT:568703","NEWT:568708","NEWT:51315","NEWT:52641","NEWT:353152","NEWT:116597","NEWT:353153","NEWT:116598","NEWT:227377","NEWT:1774284","NEWT:27689","NEWT:207769","NEWT:40674","NEWT:51329","NCBITaxon:1763","NEWT:443906","NEWT:6055","NEWT:13037","NEWT:518","NEWT:519","NEWT:941638","NEWT:511","NEWT:7394","NEWT:6063","NEWT:404330","NEWT:1328388","NEWT:13064","NEWT:529120","NEWT:7375","NEWT:300641","NEWT:39655","NEWT:206411","NEWT:80869","NEWT:214053","NEWT:80863","NEWT:665890","NEWT:52639","NEWT:52638","NEWT:8697","NEWT:861109","NEWT:8695","NEWT:1196866","NEWT:6039","NEWT:37003","NEWT:1045775","NEWT:510516","NEWT:1123869","NCBITaxon:1335626","NEWT:7370","NEWT:280406","NEWT:83906","NEWT:99488","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