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The zebrafish were provided by Professor Jose Cibelli's group at the Department of Animal Science at Michigan State University. All animal-related experiments were performed using a protocol approved by the Institutional Animal Care and Use Committee of Michigan State University. Following euthanasia with tricaine overdose (0.4%), whole brains were carefully extracted using standard microdissection techniques and placed individually on small aluminum foil squares (approximately 1.5 cm²). Each brain was immediately flash-frozen by immersion in liquid nitrogen for approximately 30 seconds to preserve tissue integrity and structural morphology during subsequent regional dissection. The rapid freezing protocol was employed to minimize protein degradation and maintain the architectural integrity of distinct brain regions, which is necessary for accurate anatomical separation. The frozen brains were then transferred to a pre-chilled dissection surface consisting of 100 mm petri dishes filled with water and frozen to maintain a consistent low temperature during manipulation. Using pre-chilled microdissection tools (forceps, scalpels, and micro-scissors maintained on ice) under an illuminated dissecting microscope, each frozen brain was manually dissected into four distinct neuroanatomical regions based on established zebrafish brain atlas landmarks: telencephalon, combined habenula-optic tectum, cerebellum, and medulla. The olfactory bulbs were excluded from analysis due to insufficient tissue volume for downstream proteomic analysis. The habenula and optic tectum were combined as a single sample due to the technical challenges associated with accurately separating these closely associated midline structures without compromising sample integrity. Dissected regions of the same anatomical type were pooled from all five fish into individual pre-labeled 5 mL round-bottom tubes maintained on ice throughout the procedure. All pooled samples were immediately stored at -80°C until protein extraction and subsequent analysis by CZE-MS/MS analysis. This pooling strategy ensured sufficient protein yield for comprehensive proteomics characterization. Sample Preparation for CZE-MS/MS For protein extraction, adult zebrafish brain regions (telencephalon, combined habenula-optic tectum, cerebellum, and medulla) were lysed in a solution containing 8 M urea and 100 mM ABC at pH 8.0, with the addition of complete protease inhibitor mixture and PhosSTOP phosphatase inhibitors. Brain tissue homogenization was performed using a Fisher Scientific Homogenizer 150, followed by ice sonication with a VWR Scientific Branson Sonifier 250 to enhance protein solubilization. Following centrifugation at 16,000 × g for 10 minutes at 15°C, lipids and cellular debris were removed, and the protein-rich supernatant was recovered. Protein quantification was accomplished using a bicinchoninic acid (BCA) assay from Fisher Scientific (Pittsburgh, PA). Prior to CZE-MS/MS analysis, zebrafish brain proteins underwent reduction with 5 mM DTT for 30 minutes at 37°C. Buffer exchange and urea removal were performed using an Amicon Ultra Centrifugal Filter with a 10 kDa molecular weight cutoff (MWCO). The filter was first conditioned by adding 200 µL of 10 mM ammonium acetate (pH 6.9) and centrifuging at 14,000 × g for 15 min. The sample was then loaded onto a Microcon-10 kDa centrifugal filter (Sigma-Aldrich) and centrifuged at 14,000 × g for 20 min to facilitate urea removal. To ensure complete buffer exchange, the retained sample was subjected to three sequential washes with 10 mM ammonium acetate (pH 6.9), each followed by centrifugation under the same conditions. The retained proteoform sample was reconstituted in 30-40 µL of 10 mM ammonium acetate (pH 6.9) for downstream analysis. Final protein quantification was conducted using a BCA kit according to the manufacturer's instructions. The proteoform samples were subjected to CZE-MS/MS analysis."],"repository":["Pride"],"quantification_method":[""],"modification":[""],"data_protocol":["Data analysis was performed using Xcalibur software (Thermo Fisher Scientific, version 4.5) to extract proteoform intensities and migration times. Electropherograms were exported from Xcalibur and further processed in Inkscape (version 1.3.2) to generate the final figures. Proteoform identification and quantification from MS RAW files of zebrafish brain regions were conducted using the TopPIC pipeline (Top-down mass spectrometry-based Proteoform Identification and Characterization)5. Initially, RAW files were converted to mzML format using the MSConvert tool 6 . Monoisotopic masses and proteoform features were extracted from precursor and fragment isotope clusters using TopFD (Top-down mass spectrometry Feature Detection, version 1.7.8)7. The resulting mass spectra and feature data were saved in .msalign and text formats, respectively. The database search was conducted via TopPIC (version 1.7.8), allowing for a maximum of one unexpected mass shift per proteoform. The precursor and fragment mass error tolerances were set to 10 ppm, and unidentified mass shifts were limited to a maximum of 500 Da. A target-decoy approach was applied to estimate false discovery rates (FDRs), and identifications were filtered at 1% FDR at the proteoform-spectrum match (PrSM) level and 5% FDR at the proteoform level 8,9. Label-free quantification of the identified proteoforms was performed using TopDiff (Top-down mass spectrometry-based identification of Differentially expressed proteoforms, version 1.7.8) under default parameters 10. The analysis was conducted using the software's default parameters. The TopDiff software is part of the TopPIC suite package (https://www.toppic.org/software/toppic/index.html). To determine the differentially expressed proteoforms between zebrafish brain regions (telencephalon, combined habenula-optic tectum, cerebellum, and medulla), the quantified proteoforms were further analyzed by the Perseus software11"],"omics_type":["Proteomics"],"labhead":["Liangliang Sun"],"instrument_platform":[""],"submission_type":["PARTIAL"],"labhead_affiliation":["Department of Chemistry Michigan State University"],"species":["Danio Rerio (zebrafish) (brachydanio Rerio)"],"publication":["41995712 Falamarzi Askarani M, Poulos W, Rahimzadeh Dashtaki M, Fang F, Cibelli JB, Sun L. Top-Down Proteomics of Zebrafish Brain Regions Using Capillary Zone Electrophoresis-Tandem Mass Spectrometry. J Proteome Res. 2026 25(5):2546-2557 10.1021/acs.jproteome.6c00007"],"submitter_mail":["colonros@msu.edu"],"submitter_affiliation":["Michigan State University"],"submitter_country":["United States"],"pubmed_abstract":["Understanding region-specific proteoform profiles in the brain is crucial for deciphering neural function and identifying therapeutic targets. Zebrafish (Danio rerio) is a valuable vertebrate model for neuroscience research due to its substantial conservation of brain structure and function with that of mammals. We present a label-free quantitative top-down proteomics (TDP) analysis of distinct zebrafish brain regions using microdissection and capillary zone electrophoresis-tandem mass spectrometry (CZE-MS/MS). We analyzed four anatomically distinct regions─telencephalon (Tele), combined habenula-optic tectum (Tec/Hab), cerebellum (Cer), and medulla (Med)─identifying 1,050 proteoforms from 336 proteins. Only 89 proteoforms (5.1%) were shared across all regions, demonstrating substantial proteoform heterogeneity. Quantitative comparisons of proteoform intensity between any two brain regions revealed drastic proteoform abundance differences. Interestingly, proteoforms of the same genes (i.e., <i>sncb, calm1a, mbpa, pcp4l1, apoa2</i>, and <i>nefma</i>) showed opposite expression patterns between brain regions, indicating potential proteoform-specific functions. Nearly 153 neuropeptides were identified using a recently published neuropeptide prediction algorithm with a prediction probability of over 75%, and some neuropeptide proteoforms showed brain-region-specific expression (i.e., <i>pyya, scg2a</i>, and <i>syn1</i>). Gene Ontology analysis of the differentially expressed proteoforms between regions revealed region-specific biological process enrichment, i.e., innate immune response and chromatin organization in Cer, actin organization in Med, microtubule-based processes in Tele, and axonogenesis in Tec/Hab. Comparing quantitative TDP and bottom-up proteomics data from the four zebrafish brain regions revealed substantial discrepancies between proteoform-specific and protein-group-specific data sets, highlighting the value of spatially resolved TDP of brains for better understanding of protein function in a proteoform-specific manner."],"pubmed_title":["Top-Down Proteomics of Zebrafish Brain Regions Using Capillary Zone Electrophoresis-Tandem Mass Spectrometry."],"pubmed_authors":["Falamarzi Askarani Mehrdad M, Poulos William W, Rahimzadeh Dashtaki Maryam M, Fang Fei F, Cibelli Jose B JB, Sun Liangliang L"],"additional_accession":[]},"is_claimable":false,"name":"Spatially-Resolved Top-Down Proteomics of Zebrafish Brain Using Capillary Zone Electrophoresis-Tandem Mass Spectrometry","description":"Understanding region-specific proteoform profiles in the brain is crucial for deciphering neural function and identifying potential therapeutic targets. Here, we present a comprehensive label-free quantitative top-down proteomics (TDP) analysis of distinct zebrafish brain regions using capillary zone electrophoresis-tandem mass spectrometry (CZE-MS/MS). We analyzed four anatomically distinct brain regions—telencephalon, combined habenula-optic tectum, cerebellum, and medulla isolated by manual dissection—identifying 1,746 proteoforms from 336 proteins. Only 89 proteoforms (5.1%) were shared across all brain regions, demonstrating substantial proteoform heterogeneity across the zebrafish brain. Quantitative analysis revealed region-specific expression patterns, with each comparison yielding 44-230 significantly differentially expressed proteoforms.  Notably, six genes (SNCB, CALM1a, MBPA, PCP4L1, APOA2, and NEFMA) exhibited bidirectional proteoform regulation, with distinct proteoforms showing opposing regional expression patterns. Gene Ontology analysis revealed region-specific enrichment of biological processes: innate immune response and chromatin organization in cerebellum, actin filament organization in tectum/habenula, microtubule-based processes in telencephalon, and axonogenesis in medulla. Comparative analysis with bottom-up proteomics (BUP) revealed substantial discrepancies, with 10.8-31.8% of differentially expressed proteoforms undetected at the protein group level, highlighting the unique value of proteoform-specific characterization. This study establishes a comprehensive proteoform atlas of zebrafish brain regions and demonstrates the critical importance of TDP for understanding region-specific neural function through post-translational modification patterns invisible to conventional proteomics approaches.","dates":{"publication":"2026-06-08","submission":"2025-11-19"},"accession":"PXD070925","cross_references":{"TAXONOMY":["NEWT:330879","NEWT:377960","NEWT:1131","NEWT:2042546","NEWT:259447","NEWT:295546","NCBITaxon:2719036","NEWT:1334565","NEWT:625351","NEWT:258594","NCBITaxon:1280","NEWT:112503","NEWT:1129","NEWT:309807","NEWT:59753","NEWT:89184","NEWT:309800","NEWT:281395","NEWT:1211601","NEWT:876138","NEWT:44271","NEWT:193516","NEWT:1073882","NEWT:6819","NEWT:475174","NEWT:428386","NEWT:1117","NEWT:498257","NEWT:10036","NEWT:32264","NEWT:1590","NEWT:10034","NEWT:33114","NEWT:661410","NEWT:638632","NEWT:224326","NEWT:376619","NCBITaxon:79857","NEWT:1096976","NEWT:3765","NEWT:3767","NEWT:1589","NEWT:135622","NEWT:672127","NEWT:35786","NEWT:1580","NEWT:399784","NEWT:96731","NEWT:656064","NEWT:1582","NEWT:1584","NEWT:36630","NEWT:1585","NEWT:383379","NEWT:418106","NCBITaxon:12721","NEWT:10029","NEWT:913645","NEWT:2492962","NEWT:641809","NEWT:1392488","NEWT:38815","NEWT:317447","NEWT:4688","NEWT:7719","NEWT:5530","NEWT:868565","NEWT:135674","NEWT:79329","NEWT:30069","NEWT:12637","NEWT:59729","NEWT:2164133","NEWT:295105","NEWT:108061","NEWT:60711","NEWT:224308","NEWT:3347","NEWT:160621","NEWT:212790","NEWT:110368","NEWT:1310161","NEWT:77133","NEWT:145481","NEWT:1310165","NEWT:29058","NCBITaxon:79824","NEWT:410658","NEWT:5516","NEWT:44688","NEWT:44689","NEWT:498211","NEWT:347256","NEWT:5518","NEWT:398007","NEWT:1527468","NEWT:498217","NEWT:498216","NEWT:11320","NEWT:246196","NEWT:246197","NEWT:145458","NEWT:1310173","NEWT:44685","NEWT:161934","NEWT:156587","NEWT:1148","NEWT:5508","NEWT:3329","NEWT:419481","NEWT:5507","NEWT:410661","NEWT:1140","NCBITaxon:2157","NEWT:1143","NEWT:1287689","NEWT:1094343","NEWT:1462472","NEWT:1336795","NEWT:644042","NEWT:150808","NEWT:1182590","NEWT:3712","NEWT:3711","NEWT:3714","NCBITaxon:37162","NEWT:270643","NEWT:2065263","NEWT:177437","NEWT:10891","NEWT:10418","NEWT:118698","NEWT:1616117","NEWT:118696","NEWT:34865","NEWT:52283","NEWT:28174","NEWT:284812","NEWT:8175","NEWT:43330","NEWT:1603293","NEWT:44664","NEWT:43346","NEWT:3702","NEWT:1245466","NEWT:3704","NEWT:244366","NEWT:1246791","NEWT:176597","NEWT:118694","NEWT:2850","NEWT:118691","NEWT:34871","NEWT:33548","NEWT:52299","NEWT:8165","NEWT:96794","NEWT:3708","NEWT:332648","NEWT:44670","NEWT:926571","NEWT:536231","NEWT:376219","NEWT:219813","NEWT:1510","NEWT:460519","NEWT:1515","NEWT:572307","NEWT:1432138","NEWT:1424507","NEWT:1194599","NEWT:272844","NEWT:1348799","NEWT:33995","NEWT:55784","NEWT:1303443","NEWT:9483","NEWT:485","NEWT:56636","NEWT:2499525","NEWT:2853422","NEWT:487","NEWT:1538553","NEWT:1679718","NEWT:480","NEWT:67767","NEWT:46835","NEWT:109757","NEWT:582580","NEWT:1185650","NEWT:216778","NEWT:1502","NEWT:128017","NEWT:376686","NEWT:237610","NEWT:95486","EFO:0001352","NEWT:119562","NEWT:1883446","NEWT:1233435","NEWT:118223","NEWT:11757","NEWT:987059","NEWT:109760","NEWT:29031","NEWT:317047","NEWT:491","NEWT:460523","NEWT:45954","NEWT:235443","NEWT:1757312","NEWT:85694","NEWT:109786","NEWT:108458","NEWT:5936","NEWT:320637","NEWT:1078283","NEWT:3750","NEWT:983964","NEWT:11706","NEWT:32644","NEWT:527796","NEWT:499175","NEWT:109779","NEWT:3745","NEWT:1715989","NCBITaxon:4751","NEWT:3747","NEWT:1116234","NEWT:1255228","NEWT:410289","NEWT:373153","NEWT:1640278","NEWT:472","NEWT:940825","NEWT:529507","NEWT:1071661","NEWT:28128","NEWT:470","NEWT:5911","NEWT:748693","NCBITaxon:50557","NEWT:39251","NEWT:29491","NEWT:101841","NEWT:446","NEWT:153481","NEWT:2014887","NEWT:33952","NEWT:445","NEWT:153009","NEWT:261756","NEWT:166313","NEWT:63366","NEWT:63367","NEWT:215402","NEWT:1547","NEWT:1290454","NEWT:906914","NEWT:28141","NEWT:9031","NEWT:27292","NEWT:1050722","NEWT:3728","NEWT:108931","NEWT:1293497","NEWT:1055524","NEWT:150475","NEWT:267872","NEWT:381666","NEWT:172269","NEWT:9534","NEWT:2126348","NEWT:5180","NEWT:256737","NEWT:9541","NEWT:8694","NEWT:33936","NEWT:8692","NEWT:2903","NEWT:185579","NEWT:13076","NEWT:207340","NEWT:1006581","NEWT:8673","NEWT:33940","NEWT:550","NEWT:554","NEWT:451516","NEWT:552","NEWT:1325291","NEWT:42410","NEWT:36185","NEWT:1054211","NEWT:1225786","NEWT:771870","NEWT:51338","NEWT:575412","NEWT:28112","NEWT:49012","NEWT:6493","NEWT:10832","NEWT:6494","NEWT:6491","NEWT:507601","NEWT:520","NEWT:186441","NEWT:643680","NEWT:214092","NCBITaxon:6157","NEWT:13095","NEWT:162425","NEWT:104105","NEWT:216257","NEWT:9986","NEWT:8654","NEWT:8658","NEWT:1268063","NEWT:8657","NEWT:9983","NEWT:8655","NEWT:5147","NEWT:28108","NEWT:28104","NEWT:407821","NEWT:568703","NCBITaxon:2","NEWT:568708","NEWT:1613","NEWT:986","NEWT:52641","NEWT:28532","NEWT:353152","NEWT:298176","NEWT:353153","NEWT:227377","NEWT:1774284","NEWT:40674","NEWT:1194669","NEWT:51329","NEWT:443906","NEWT:13037","NEWT:519","NEWT:2510939","NEWT:7394","NEWT:6063","NEWT:1328388","NEWT:105487","NEWT:1548728","NEWT:667127","NEWT:9557","NEWT:377586","NEWT:300641","NEWT:39655","NEWT:9554","NEWT:38323","NEWT:475932","NEWT:256318","NEWT:206411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