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Pandey"],"technology_type":["Mass Spectrometry","Bottom-up proteomics"],"disease":["Cholangiocarcinoma"],"software":[""],"submitter_keywords":["Phosphoproteomics","Lc-ms/ms","Multiomics","Dimensional reduction","Hierarchical all-against-all","Cholangiocarcinoma"],"full_dataset_link":["https://www.ebi.ac.uk/pride/archive/projects/PXD059245"],"tissue":["Liver","Bile Duct"],"sample_protocol":["Frozen tissues were pulverized using a cryoPREP device  (CP02, Covaris). The powder was lysed in lysis buffer (8 M urea in 20 mM HEPES, 1 mM sodium orthovanadate, 2.5 mM sodium pyrophosphate, 1 mM β-glycerophosphate) and sonicated using a tip sonicator (Branson, SFX550). Lysates were reduced and alkylated using dithiothreitol (D9163, Sigma) and iodoacetamide (I1149, Sigma), respectively. Extracted proteins were diluted using 20 mM HEPES to a final concentration of 1 M urea and TPCK-treated trypsin (LS003744, Worthington) was added with 1:50 enzyme to protein ratio and kept for incubation at 37 °C for overnight. Digests were acidified and subjected to desalt using Sep-Pak C18 cartridge (Waters). Eluted peptides were lyophilized and subjected to tandem mass tag (A44520, Thermo Fisher Scientific) labeling following the manufacturer’s instruction. TMT labeled peptides were fractionated by high pH reversed phase liquid chromatography on Dionex Ultimate 3000 liquid chromatography system  (Thermo Fisher Scientific) using a Xbridge column (4.6 mm x 50 cm x 3.5µm,  Waters) with a 2 hr. A total of 96 fractions were collected and concatenated into 24 fractions. Around 10 µg equivalent of each fraction was set aside for global proteome analysis and the rest of each sample was concentrated into 12 fractions and dried prior to phosphopeptide enrichment. IMAC-based phosphopeptide enrichment was performed using Fe(III)-NTA resin on an AssayMap Bravo (Agilent Technologies)  following the manufacture instruction. For enrichment of phosphotyrosine peptides, immunoaffinity purification was performed. Lyophilized peptides were reconstituted in IAP buffer (50 mM MOPS, 10 mM sodium phosphate, 50 mM NaCl) followed by incubation with anti-phosphotyrosine antibody beads (pY1000, Cell Signaling Technology) at 4 °C for 1 hr following the manufacturer’s instruction. For label-free kinome profiling, we used our in-house developed kinobead platform. Frozen human and PDX tissue samples were suspended in modified RIPA buffer containing HALT protease and phosphatase inhibitor cocktail (100x, Thermo Fisher Scientific), as well as 1 mM phenylmethylsulfonyl fluoride. Tissues were homogenized on ice using a hand-held homogenizer and clarified by centrifugation at 4°C and 21,000 Xg for 20 min. 40 µl of a 50% slurry of our optimized kinobead mixture in 20% aq. ethanol were prepared for each kinase enrichment experiment. The beads were washed twice with 400 µl modified RIPA buffer and 600 µg of protein in lysate was added. The mixture was incubated on a tube rotator for 3h at 4°C and then the beads were pelleted rapidly at 2000 Xg on a benchtop centrifuge. After removal of the supernatant, the beads were rapidly washed twice with 400 µl of ice-cold mod. Freshly prepared denaturing buffer (8M urea, 100 mM Tris, pH 8.5) containing 5 mM tris(2-carboxyethyl)phosphine hydrochloride and 10 mM chloroacetamide, were added and the slurry agitated on a thermomixer at 1400 rpm for 30 min. The mixture was diluted 2-fold with 100 mM triethylamine bicarbonate, the pH adjusted to 8-9 by addition 1 N aq. NaOH; 2 µg LysC were added, and the mixture agitated on a thermomixer at 1400 rpm at 37°C for 2 h. Then, the mixture was diluted another 2-fold with 100 mM TEAB, 2 µg MS-grade trypsin (Thermo Fisher Scientific) were added, and the mixture agitated on a thermomixer at 1400 rpm at 37°C overnight. LC-MS/MS data of TMT-labeled peptides were acquired on Orbitrap Fusion Eclipse mass spectrometer (Thermo Fisher Scientific) coupled to Ultimate 3000 liquid chromatography system (Thermo Fisher Scientific). The peptides were loaded onto a trap column (PepMap C18, 2cm x 100µm, 100 Å) at a flow rate of 20 µl/min and separated on EASY-Spray column (PepMap RSCL C18, 75 µm x 50 cm, 100 Å) at a flow rate of 300 nL/min. Solvent A (0.1% formic acid in water) and solvent B (0.1% formic acid in acetonitrile) were used for generating gradient (3-40%) over 135 min. Mass spectrometry data were acquired in data-dependent acquisition mode with cycle time of 2 sec. MS scan and MS/MS scan were acquired with resolution of 120,000 and 30,000, respectively. Precursor ions were isolated under 0.7 m/z isolation width and fragmented with normalized collision energy of 35.  For label-free protein quantification, peptide samples of 200 ng were analyzed on a timsTOF Pro 2 – nanoElute 2 LC-MS system (Bruker). Peptides were separated in on 15 cm long, 150 µm inner diameter PepSep columns packed with 1.5 µm diameter C18 beads in 45 min LC gradients (5-30% B) at flow rates of 0.5 µL/min. LC solvents were A (0.1% formic acid in water) and B (0.1% formic acid in acetonitrile). MS data were acquired in data-independent acquisition mode using the diaPASEF method."],"repository":["Pride"],"quantification_method":[""],"modification":[""],"data_protocol":["MS raw files were processed in MaxQuant software version 1.6.17.0. Peptides were searched using the Andromeda search engine against the human UniProt protein database. TMT on lysine and peptide n-terminal and cysteine carbamidomethylation were set as fixed modifications and N-terminal acetylation and methionine oxidation were set at as variable modifications. For processing data of phosphorylated peptides, phosphorylation on serine, threonine and tyrosine were additionally considered as set as variable modifications.  Searches were performed with a false discovery rate of 1% for both peptides and proteins using a target-decoy approach.  Peptide length was to at least 7 amino acids long and MS2 match tolerance was set to 0.02 Da. Enzyme specificity was set to trypsin and a maximum of two missed cleavages were allowed.  For label-free experiments, MS raw files were computed using DIA-NN v.1.9.1 in library-free mode. Both the human  protein database downloaded from UniProt on 07.14.2023 (UP000005640) and the mouse protein database downloaded from uniport on 07.14.2023 (UP000000589) were use the DIA-NN search."],"omics_type":["Proteomics"],"labhead":["Akhilesh Pandey"],"instrument_platform":[""],"labhead_affiliation":["Department of Laboratory Medicine and Pathology, Mayo Clinic"],"submission_type":["PARTIAL"],"species":["Homo Sapiens (human)"],"submitter_mail":["pandey.akhilesh@mayo.edu"],"publication":["41020779 Mun DG, Jessen E, Tomlinson JL, Carlson D, Budhraja R, Alva-Ruiz R, Abdelrahman A, Watkins R, Gregory L, McCabe C, Wang C, Graham RP, Woods K, Golkowski M, Baker M, Gores GJ, Ilyas SI, Conboy C, Larson EL, Sample JW, Ozmert EH, Kandasamy RK, Borad MJ, Roberts L, Andersen J, Pandey A, Smoot RL, Smoot RL. Multiomics combined with machine learning defines unique molecular subtypes of cholangiocarcinoma and identifies TNK1 as a therapeutic target. Hepatology. 2025 10.1097/hep.0000000000001535"],"submitter_affiliation":["Department of Laboratory Medicine and Pathology, Mayo Clinic, Rochester, MN 55905"],"submitter_country":["United States"],"pubmed_abstract":["<h4>Background and aims</h4>Cholangiocarcinoma (CCA) is one of the most lethal cancers, characterized by molecular heterogeneity and treatment resistance. To uncover new biological signals and therapeutic opportunities, we employed multiomic characterization combined with machine learning.<h4>Approach and results</h4>We profiled all anatomical CCA subtypes using whole exome sequencing, mRNA sequencing, and proteome/phosphoproteome analysis. Integrative dimensional reduction revealed RNA, protein, and phosphoprotein features driving tumor heterogeneity, enabling clustering. Machine learning algorithms identified molecular features for each cluster and mapped external datasets and patient-derived xenograft (PDX) models onto these clusters. Kinase enrichment analysis highlighted targetable kinases active in each cluster. In vivo validation was performed in cluster-specific PDX models using the selective TNK1 inhibitor, TP-5801. We identified 3 molecular clusters with distinct pathway characterization: immunomodulatory (cluster 1), metabolic (cluster 2), and gene regulation/cellular fate (cluster 3). Cluster assignment was independent of anatomic subtype but correlated with overall survival following curative-intent resection. We also identified multiomic features and pathways linked to overall survival and lymph node metastases, crucial for patient treatment selection. Kinase enrichment analysis pinpointed TNK1 as a highly active kinase in the metabolic cluster. Treatment with TP-5801 significantly reduced tumor growth in a metabolic PDX model, but not in models representing the other clusters. Combining internal data with publicly available datasets, we identified the immunomodulatory cluster as most responsive to gemcitabine/cisplatin therapy, confirmed in vivo using cluster-specific PDX models.<h4>Conclusions</h4>Integrated multiomic characterization provides translational insights by defining unique molecular subtypes associated both with therapeutic response and overall clinical outcomes. This approach identified TNK1 as a previously unrecognized therapeutic target in a defined subset of CCA tumors."],"pubmed_title":["Multiomics combined with machine learning defines unique molecular subtypes of cholangiocarcinoma and identifies TNK1 as a therapeutic target."],"pubmed_authors":["Mun Dong-Gi DG, Jessen Erik E, Tomlinson Jennifer L JL, Carlson Danielle D, Budhraja Rohit R, Alva-Ruiz Roberto R, Abdelrahman Amro A, Watkins Ryan R, Gregory Lindsey L, McCabe Chantal C, Wang Chen C, Graham Rondell P RP, Woods Kathryn K, Golkowski Martin M, Baker Marshall M, Gores Gregory J GJ, Ilyas Sumera I SI, Conboy Caitlin C, Larson Ellen L EL, Sample Jack W JW, Ozmert Enis H EH, Kandasamy Richard K RK, Borad Mitesh J MJ, Roberts Lewis L, Andersen Joshua J, Pandey Akhilesh A, Smoot Rory L RL, Smoot Rory L RL"],"additional_accession":[]},"is_claimable":false,"name":"Integrated multiomic analysis of cholangiocarcinoma defines novel molecular subtypes associated with clinical outcome and identifies TNK1 as a therapeutic target","description":"Despite remarkable advances in cancer genomics and targeted therapy, cholangiocarcinoma (CCA) is still one of the deadliest cancers. Current translational approaches have focused on genomic alterations, while leaving proteomic alterations, that may more directly pinpoint therapeutic targets, unexplored. To address these knowledge gaps, we performed multiomic characterization of all three CCA subtypes, using whole exome sequencing, mRNA sequencing, and proteome/phosphoproteome profiling. Integrative dimensional reduction approaches revealed RNA, protein and phosphoprotein features driving tumor heterogeneity. These features defined three molecular clusters associated with unique pathways: immunomodulatory (cluster 1), metabolic (cluster 2), and chromosomal stability/apoptosis (cluster 3). We observed that cluster assignment was not related to anatomic subtype but was associated with overall survival after curative-intent resection. Further, we utilized a hierarchical all-against-all approach, which identified multi-omic features and pathways associated with overall survival and lymph node metastases, clinically relevant endpoints for selecting patient treatments. Kinase enrichment analysis of molecular features identified non-receptor tyrosine protein kinase TNK1 as a highly active kinase for cluster 2. We developed a radial support vector machine model that mapped to multiomically-characterized patient derived xenograft (PDX) models resulting in the selection of PDX models for each cluster. Importantly, we confirmed that treating with a selective TNK1 inhibitor significantly reduced tumor growth in a cluster 2 PDX, but not a cluster 1 or 3 PDX. Overall, we concluded that integrated multiomic characterization provides translational insights by defining unique molecular subtypes, identifying molecular features associated with clinical outcomes, and uncovering novel therapeutic targets.","dates":{"publication":"2026-06-29","submission":"2024-12-25"},"accession":"PXD059245","cross_references":{"TAXONOMY":["NEWT:330879","NEWT:377960","NEWT:1131","NEWT:35795","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:247480","NEWT:1211601","NEWT:876138","NEWT:44271","NEWT:193516","NEWT:2315688","NEWT:1073882","NEWT:6819","NEWT:475174","NEWT:111205","NEWT:1599","NEWT:428386","NEWT:1117","NEWT:498257","NEWT:10036","NEWT:32264","NEWT:12215","NEWT:1590","NEWT:10034","NEWT:33114","NEWT:1596","NEWT:661410","NEWT:638632","NEWT:224326","NEWT:376619","NCBITaxon:79857","NEWT:1096976","NEWT:3765","NEWT:3767","NEWT:1589","NEWT:135622","NEWT:4615","NEWT:672127","NEWT:35786","NEWT:1580","NEWT:399784","NEWT:96731","NEWT:656064","NEWT:1582","NEWT:3760","NEWT:1584","NEWT:36630","NEWT:1585","NEWT:383379","NEWT:381198","NEWT:418106","NCBITaxon:12721","NEWT:10029","NEWT:913645","NEWT:2492962","NEWT:641809","NEWT:1392488","NEWT:38815","NEWT:317447","NEWT:4688","NEWT:111225","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:49928","NEWT:3349","NEWT:160621","NEWT:212790","NEWT:110368","NEWT:55350","NEWT:1310161","NEWT:77133","NEWT:145481","NEWT:1310165","NEWT:29058","NCBITaxon:79824","NEWT:1912919","NEWT:410658","NEWT:5516","NEWT:44688","NEWT:44689","NEWT:370038","NEWT:498211","NEWT:345076","NEWT:347256","NEWT:5518","NEWT:398007","NEWT:1527468","NEWT:498217","NEWT:498216","NEWT:11320","NEWT:246196","NEWT:246197","NEWT:145458","NEWT:1310173","NEWT:200795","NEWT:2579791","NEWT:44685","NEWT:161934","NEWT:156587","NEWT:1148","NEWT:5508","NEWT:3329","NEWT:419481","NEWT:5507","NEWT:260499","NEWT:410661","NEWT:1140","NCBITaxon:2157","NEWT:2066563","NEWT:2649329","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:3715","NEWT:2065263","NEWT:177437","NEWT:717966","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:9006","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:2709072","NEWT:2499525","NEWT:2853422","NEWT:487","NEWT:1538553","NEWT:1679718","NEWT:480","NEWT:67767","NEWT:45972","NEWT:46835","NEWT:109757","NEWT:582580","NEWT:1185650","NEWT:216778","NEWT:294607","NEWT:1502","NEWT:128017","NEWT:2836","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:1509","NEWT:491","NEWT:460523","NEWT:45954","NEWT:235443","NEWT:1579","NEWT:1757312","NEWT:85694","NEWT:109786","NEWT:108458","NEWT:5936","NEWT:321967","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:415978","NEWT:1255228","NEWT:410289","NEWT:191701","NEWT:373153","NEWT:1640278","NEWT:472","NEWT:940825","NEWT:29459","NEWT:529507","NEWT:1071661","NEWT:28128","NEWT:470","NEWT:41122","NEWT:5911","NEWT:748693","NCBITaxon:50557","NEWT:39251","NEWT:29491","NEWT:101841","NEWT:446","NEWT:153481","NEWT:2014887","NEWT:33952","NEWT:11723","NEWT:445","NEWT:153009","NEWT:261756","NEWT:166313","NEWT:63366","NEWT:63367","NEWT:29488","NEWT:215402","NEWT:1547","NEWT:1290454","NEWT:3726","NEWT:906914","NEWT:81231006","NEWT:28141","NEWT:9031","NEWT:27292","NEWT:1050722","NEWT:3728","NEWT:108931","NEWT:1293497","NEWT:1055524","NEWT:548","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:542","NEWT:2903","NEWT:185579","NEWT:872227","NEWT:13076","NEWT:2587410","NEWT:207340","NEWT:1006581","NEWT:8673","NEWT:33940","NEWT:2126337","NEWT:550","NEWT:33941","NEWT:554","NEWT:451516","NEWT:552","NEWT:1325291","NEWT:42410","NEWT:36185","NEWT:1054211","NEWT:1225786","NEWT:771870","NEWT:51338","NEWT:9995","NEWT:575412","NEWT:28112","NEWT:49012","NEWT:6493","NEWT:10832","NEWT:6494","NEWT:6491","NEWT:507601","NEWT:520","NEWT:64657","NEWT:186441","NEWT:643680","NEWT:214092","NCBITaxon:6157","NEWT:13095"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