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/PXD054766/submission_042726_v2.px"]},"type":"primary"},"statusCode":"OK","statusCodeValue":200}],"scores":null,"additional":{"labhead_mail":["tukiet.lam@yale.edu"],"submitter":["TuKiet Lam"],"technology_type":["Data-dependent acquisition","Mass Spectrometry","Bottom-up proteomics"],"disease":["Neuronal Ceroid Lipofuscinosis 3"],"software":[""],"submitter_keywords":[""],"full_dataset_link":["https://www.ebi.ac.uk/pride/archive/projects/PXD054766"],"tissue":["Brain"],"sample_protocol":["LC-MS/MS data acquisition for mouse lipofuscin samplesPurified lipofuscin fractions were diluted with PBS and pelleted, then washed in ultrapure distilled H2O (RPI) to remove sucrose and protease inhibitors (6000 x g, 10 min, 4°C). The washed lipofuscin pellet was frozen at -80°C prior to mass spectrometry. Label-Free Quantification Mass Spectrometry (LFQ-MS) was performed at the Yale Mass Spectrometry & Proteomics Resource of the W.M. Keck Foundation Biotechnology Resource Laboratory with the support of the Yale/NIDA Neuroproteomics Center.Total brain homogenate samples were diluted with 300 μL RIPA buffer (Thermo Scientific, 89901) containing 1× Halt protease/phosphatase inhibitor cocktail (Thermo Scientific, 78447). The samples were sonicated at 10 amps for two rounds of 15 sec with 1 sec on/off pulses, storing the samples on ice between rounds. The samples were then centrifuged (14,600 x g, 10 min, 4 °C) to clear insoluble debris prior to protein precipitation using chloroform/methanol/water. Lipofuscin pellets and total brain homogenate protein precipitates were dissolved in 0.1% RapiGest SF (Waters Corporation, SKU: 186001861) in 50mM ammonium bicarbonate, reduced with DTT (final concentration of 4.5 mM, 37°C, 30 min.) and alkylated with iodoacetamide (final concentration of 10 mM, room temperature, 30 min., in the dark). Reduced and alkylated proteins were then treated with PNGase (37°C, overnight, Promega, V4831) followed by digestion with Lys-C (1:50 enzyme:protein ratio; 37°C, 6.5 hours) and subsequently with trypsin (1:50 enzyme:protein ratio; 37°C, overnight). The solution was then acidified with trifluoroacetic acid (TFA final concentration of 0.95%; 37°C, 45 min.; Thermo Fisher Scientific, 28901) and centrifuged (14,600 g, room temperature, 10 min.) to crash out the RapiGest SF hydrolysis products. The supernatant was transferred to a new tube, spiked with Pierce Retention Time Calibration Mixture (Thermo Fisher Scientific, 88321), and diluted with 0.1% TFA in 98:2% water:acetonitrile prior to injecting on the mass spectrometer.LFQ-MS was performed on a Thermo Scientific Q-Exactive plus Mass spectrometer connected to a Waters nanoACQUITY UPLC system equipped with a Waters SymmetryR C18 180 μm × 20 mm trap column and a 1.7-μm, 75 μm × 250 mm nanoACQUITY UPLC column (35°C). 5 μl of each 0.05 μg/μl digest were injected in block randomized order (each biological replicate injected in technical triplicate). To ensure a high level of identification and quantitation integrity, a resolution of 70,000 was utilized for MS and 20 MS/MS spectra were acquired per MS scan using higher-energy collisional dissociation (HCD). All MS (Profile) and MS/MS (centroid) peaks were detected in the Orbitrap. Trapping was carried out for 3 min at 5 μl/min in 99.5% Buffer A (0.1% FA in water) and 0.5% Buffer B (0.1% FA in acetonitrile (ACN)) prior to eluting with linear gradients that reached 25% B at 140 min, 40% B at 165 min, and 90% B at 170 min. Four blanks (2x 100% ACN wash, then 2x Buffer A wash) were injected after each sample to ensure against sample carryover.LC-MS/MS data acquisition for human total brain homogenate and lipofuscin samplesLC-MS/MS data were acquired on a Thermo Scientific Q Exactive HF-X mass spectrometer coupled to a Waters M-Class UPLC system. Peptides were loaded onto a nanoEase M/Z Symmetry C18 trap column (100 A, 5 μm, 180 μm × 20 mm) (Waters, 186008821) at a flow rate of 5 μL/min, 0.5% B for 3 min and separated using a peptide BEH C18 analytical column (130 A, 1.7 μm, 75 μm × 250 mm) (Waters, 186008795) (35 °C). The compositions of mobile phases A and B were 0.1% formic acid in water and 0.1% formic acid in ACN, respectively. The peptides were eluted at a flow rate of 300 nL/min with a gradient starting at 3% B, increasing to 6% B over 2 min, then to 25% B over 173 min and 40% B over 20 min. The gradient was then ramped to 90% B over 5 min and held for 10 min before the column was equilibrated to starting conditions. Precursor MS1 scans (profile) were collected from 350-1500 m/z at a resolution of 120,000. The AGC target was set to 3 × 106 and the maximum injection time was 50 ms. Data-dependent MS2 scans (top 20; centroid) were collected from 200-2000 m/z at a resolution of 30,000. Precursors with 2 ≤ z ≤ 7 were selected for HCD fragmentation with a collision energy setting of 30% and an isolation window of 1.4 m/z. The AGC target was set to 1 × 105 and the maximum injection time was 50 ms. Dynamic exclusion was enabled with an exclusion duration of 20 s. Four blank injections were performed between sample injections to minimize carryover."],"repository":["Pride"],"quantification_method":[""],"modification":[""],"data_protocol":["As previously [33, 101], chromatographic/spectral alignment, mass spectral peak picking and filtering (ion signal > 3X standard deviation of noise), and quantification of proteins and peptides were performed with Progenesis QI software (Nonlinear Dynamics, version 4.2). A normalization factor was calculated to account for sample load and ionization differences across technical triplicate injections. An in-house Mascot search engine (2.7) was used to carry out protein identification against the Swiss Protein database with taxonomy restricted to Mus musculus. Two missed tryptic cleavages were allowed, precursor mass tolerance was set to 10 ppm, and fragment mass tolerance was set to 0.02 Da. The protein identification significance threshold was set based on a False Discovery Rate (FDR) of 2%. Protein abundances were calculated from the sum of all non-conflicting peptide ion ID assignments for a specific protein on each run, then normalized to Pierce Retention Time Calibration Mixture and spectral counts. Proteins with 2+ unique peptides and a confidence score > 39 were included in the lipofuscin proteome for further analysis. Proteins are listed in UniProt Protein ID nomenclature.Proteomics data analysis for mouse lipofuscin samplesProtein abundance comparisons were considered significant with a fold-change of 1.5 and a p-value < 0.05 by two-tailed unpaired t-test. Ingenuity Pathway Analysis (IPA; Qiagen) was conducted to determine represented canonical pathways. Organelle enrichment was determined by annotating proteomic data by primary localization in the Human Protein Atlas [95] and quantifying the annotated proteins per category/total detected proteins in lipofuscin versus the expected whole brain ratio in the Human Protein Atlas. Mitochondrial compartment annotation (MOM: mitochondrial outer membrane; IMS: intermembrane space; MIM: mitochondrial inner membrane) was performed using MitoCarta 3.0 [80] as a reference. The ratios of proteins from each mitochondrial compartment/total proteins were compared by two-tailed unpaired t-test for lipofuscin vs. mitochondrial isolates from different brain regions (spinalcord, brainstem, cerebellum, cerebrum) detailed in MitoCarta 3.0. Lysosomal compartment annotation was performed using combined lysosomal proteome datasets [2, 18, 52]. Proteins capable of S-acylation were annotated with our previously published proteome of S-acylated proteins isolated from WT and Ppt1-/- 2-month brain and synaptosomes [33].Proteomics data analysis for human total brain homogenate/lipofuscin samplesProtein identification and label-free quantification (LFQ) were performed in Proteome Discoverer (Thermo Fisher Scientific, version 3.2.0.450) using standard processing and consensus workflows. Briefly, precursor masses were recalibrated before data were searched against the SwissProt Homo sapiens database (downloaded June, 2025) and a database of common contaminant proteins (301 entries). The Sequest HT search engine was employed and trypsin was selected as the enzyme. The precursor and fragment mass tolerances were set to 10 ppm and 0.02 Da, respectively, and peptides with lengths between 6-30 amino acids and up to two missed cleavages were allowed. Oxidation of methionine and deamidation of asparagine were set as variable modifications and carbamidomethylation of cysteine was set as a fixed modification. PSM-level false discovery rates (FDRs) were estimated using Percolator. The Minora algorithm was used for feature detection and quantification was performed using unique and razor peptides. Normalization between files was based on total peptide amount and protein abundance ratios between conditions were calculated based on pairwise peptide ratios. Background-based t-tests were performed to identify significant differences in protein abundances between conditions. Peptide- and protein-level FDR thresholds were set to 1% and only master proteins with at least two unique peptides were considered for downstream analysis. Proteins capable of S-acylation were annotated by comparison with mouse homologues from our previously published proteome of S-acylated proteins isolated from WT and Ppt1-/- 2-month brain and synaptosomes [33]."],"omics_type":["Proteomics"],"labhead":["TuKiet Lam"],"instrument_platform":[""],"submission_type":["PARTIAL"],"labhead_affiliation":["Keck MS & Proteomics Resource Yale School of Medicine"],"species":["Mus Musculus (mouse)"],"publication":["10.1007/S00401-026-03012-7"],"submitter_mail":["tukiet.lam@yale.edu"],"submitter_affiliation":["Yale University"],"submitter_country":["United States"],"additional_accession":[]},"is_claimable":false,"name":"Lipofuscin accumulation in aging and CLN1 is associated with deficient de-S-acylation, lysomitochondrial dysfunction, and lipid dyshomeostasis","description":"Lipofuscin is an autofluorescent material that accrues in brain tissues with age and in Neuronal Ceroid Lipofuscinosis (NCL), a neurodegenerative disease with pediatric onset. The distribution, composition, and organellar origin of lipofuscin have remained unclear despite its widespread presence in aged tissues and involvement in neurodegeneration. Here, we elucidate lipofuscin composition in mouse and human brain and assemble a reference neuroanatomical atlas of lipofuscin accumulation with age and NCL (Type 1; CLN1) progression across 425 fine brain regions. We identify a primary role of the lysosomal-mitochondrial axis in the formation of lipofuscin pathology via multimodal mass spectrometry, ultrastructural analyses,and assays of cellular and enzymatic metabolism. We find the protein and lipid composition of age and CLN1 lipofuscin to be remarkably similar. Dissection of implicated molecular pathways reveals protein Sacylation and unsaturated lipid homeostasis as central processes involved in lipofuscin deposition during aging and CLN1. Notably, >95% of lipofuscin resident proteins can be S-acylated and many are substrates of the enzyme PPT1, validating a seminal hypothesis that CLN1 lipofuscin contains these lipid-modified proteins. Further, we discover deficient de-S-acylation is correlated with lipofuscin load in healthy aging, as the specific de-S-acylation enzyme activity of PPT1 is found to decline with advancing age. Finally, we identify lipid metabolite biomarkers of lipofuscin, including long-chain polyunsaturated fatty acids, bis(monoacylglycerol)phosphate (BMP), and oxidized phosphatidylethanolamine (OxPE) lipid species. Overall, we provide a comprehensive redefinition of lipofuscin neuropathology and a resource for studying aging, lysosomal storage disorders, and neurodegeneration.","dates":{"publication":"2026-05-06","submission":"2024-08-09"},"accession":"PXD054766","cross_references":{"TAXONOMY":["NEWT:108018","NEWT:377960","NEWT:1131","NEWT:190486","NEWT:2042546","NEWT:148942","NEWT:295546","NEWT:258594","NEWT:1126","NEWT:1129","NEWT:89187","NEWT:309807","NEWT:89184","NEWT:309800","NEWT:1323429","NEWT:876138","NEWT:44271","NEWT:193516","NEWT:2315688","NEWT:592321","NEWT:1073882","NEWT:6819","NEWT:428386","NEWT:1117","NEWT:498257","NEWT:10036","NEWT:32264","NEWT:10034","NEWT:661410","NEWT:488003","NEWT:224326","NEWT:376619","NEWT:3765","NEWT:3767","NEWT:433727","NEWT:135622","NEWT:672127","NEWT:656061","NEWT:37965","NEWT:656064","NEWT:3760","NEWT:36630","NEWT:381198","NEWT:418106","NEWT:10029","NEWT:913645","NEWT:641809","NEWT:44250","NEWT:317447","NEWT:5530","NEWT:868565","NEWT:135674","NEWT:1562698","NEWT:12637","NEWT:2164133","NEWT:2767846","NEWT:1343074","NEWT:314344","NEWT:108061","NEWT:224308","NEWT:49928","NEWT:160621","NEWT:110368","NEWT:1916073","NEWT:1310161","NEWT:1230383","NEWT:77133","NEWT:1310165","NEWT:114727","NEWT:5516","NEWT:498211","NEWT:347256","NEWT:5518","NEWT:398007","NEWT:1527468","NEWT:498217","NEWT:498216","NEWT:11320","NEWT:1310173","NEWT:161934","NEWT:1148","NEWT:5508","NEWT:419481","NEWT:5507","NEWT:1140","NCBITaxon:2157","NEWT:2066563","NEWT:1143","NEWT:1462472","NEWT:1336795","NEWT:644042","NEWT:709964","NEWT:3712","NEWT:3711","NEWT:3714","NEWT:65121","NEWT:3715","NEWT:2065263","NEWT:1549675","NEWT:177437","NEWT:9014","NEWT:10891","NEWT:226126","NEWT:1616117","NEWT:34865","NEWT:28174","NEWT:550537","NEWT:284812","NEWT:3701","NEWT:3702","NEWT:1245466","NEWT:3704","NEWT:1246791","NEWT:9005","NEWT:34871","NEWT:9006","NEWT:33548","NEWT:1883426","NEWT:657321","NEWT:10886","NEWT:3708","NEWT:536231","NEWT:219813","NEWT:215451","NEWT:460519","NEWT:272843","NEWT:272844","NEWT:1348799","NEWT:55784","NEWT:485","NEWT:2499525","NEWT:142786","NEWT:2853422","NEWT:487","NEWT:1679718","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:460523","NEWT:85694","NEWT:85692","NEWT:911045","NEWT:3750","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:28128","NEWT:470","NEWT:41122","NEWT:1328300","NEWT:748693","NCBITaxon:50557","NEWT:3735","NEWT:29491","NEWT:911022","NEWT:446","NEWT:153481","NEWT:445","NEWT:2003758","NEWT:63366","NEWT:63367","NEWT:29488","NEWT:215402","NEWT:3726","NEWT:30455","NEWT:28141","NEWT:9030","NEWT:9031","NEWT:3728","NEWT:108931","NEWT:219799","NEWT:219798","NEWT:548","NEWT:150475","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:554","NEWT:451516","NEWT:552","NEWT:1325291","NEWT:42410","NEWT:1225786","NEWT:771870","NEWT:8665","NEWT:51338","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:8658","NEWT:1268063","NEWT:8657","NEWT:9983","NEWT:8655","NEWT:80833","NEWT:479096","NEWT:28108","NEWT:28104","NEWT:1114957","NEWT:568703","NEWT:568708","NEWT:52641","NEWT:353152","NEWT:353153","NEWT:227377","NEWT:1774284","NEWT:27689","NEWT:207769","NEWT:40674","NEWT:51329","NCBITaxon:1763","NEWT:443906","NEWT:13037","NEWT:519","NEWT:7394","NEWT:6063","NEWT:404330","NEWT:1328388","NEWT:13064","NEWT:300641","NEWT:39655","NEWT:38323","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:1045775","NEWT:1123869","NCBITaxon:1335626","NEWT:7370","NEWT:83906","NEWT:99488","NEWT:1134506","NEWT:255470","NEWT:762903","NEWT:27697","NEWT:86185","NEWT:9935","NEWT:266940","NEWT:287889","NEWT:1028307","NEWT:52603","NEWT:92867","NEWT:92866","NEWT:1344414","NEWT:202950","NEWT:741158","NEWT:1293091","NEWT:202956","NEWT:315750","NEWT:632957","NEWT:9925","NCBITaxon:9606","NEWT:1436183","NEWT:1479235","NEWT:4232","NEWT:9922","NEWT:416348","NEWT:105812","NEWT:11298","NEWT:4233","NEWT:4236","NEWT:398031","NEWT:196627","NEWT:523840","NEWT:1076878","NEWT:200308","NEWT:200302","NEWT:9913","NEWT:9915","NEWT:105841","NEWT:1170227","NEWT:2666255","NEWT:999810","NEWT:28995","NEWT:1392998","NEWT:1150621","NEWT:1085791","NEWT:745531","NEWT:226900","NEWT:231490","NEWT:590651","NEWT:449239","NEWT:244704","NEWT:9909","NEWT:9902","NEWT:430615","NEWT:563041","NEWT:36599","NEWT:41949","NEWT:9900","NEWT:326423","NEWT:326424","NEWT:13013","NEWT:749906","NEWT:418985","NEWT:749907","NEWT:431947","NEWT:142809","NEWT:1095183","NEWT:302409","NEWT:9979","NEWT:1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