{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,15]],"date-time":"2026-10-15T20:20:22Z","timestamp":1792095622088,"version":"4.4.0"},"reference-count":52,"publisher":"American Chemical Society (ACS)","issue":"8","license":[{"start":{"date-parts":[[2026,6,29]],"date-time":"2026-06-29T00:00:00Z","timestamp":1782691200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by-nc-nd\/4.0\/"}],"funder":[{"DOI":"10.13039\/na","name":"Tianjin Education Commission for Higher Education","doi-asserted-by":"publisher","award":["2023ZD023"],"award-info":[{"award-number":["2023ZD023"]}],"id":[{"id":"10.13039\/na","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/na","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["82203542"],"award-info":[{"award-number":["82203542"]}],"id":[{"id":"10.13039\/na","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/na","name":"Tianjin Key Medical Discipline (Specialty) Construction Project","doi-asserted-by":"publisher","award":["TJYXZDXK-009A"],"award-info":[{"award-number":["TJYXZDXK-009A"]}],"id":[{"id":"10.13039\/na","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2026,8,7]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>Colorectal cancer (CRC) exhibits profound molecular heterogeneity according to primary tumor location, but spatially resolved assessment is limited by interindividual variability. Here, to minimize interindividual genetic confounding, we performed an exploratory single-case spatial metabolomics study (MALDI-MSI) on a rare case of synchronous bilateral tumors from one patient. This was complemented by untargeted metabolomics (UHPLC-HRMS\/MS) on tumor and matched normal tissues from a cohort of 30 CRC patients with different anatomical sites and histologies. As an observational finding in this single case, the left-sided colon cancer (LCC) showed distinct metabolite distribution features from the tumor core to the invasive margin, whereas in right-sided colon cancer (RCC), metabolic differences were more closely associated with a histological subtype. UHPLC-HRMS\/MS showed that, among tubular adenocarcinomas, LCC exhibited enrichments in ether lipid and phosphatidylcholine metabolism, whereas RCC preferred nucleotide and fatty acid metabolism. Furthermore, right-sided mucinous adenocarcinomas displayed unique sphingolipid alterations, consistent with a possible desaturase-associated shift from apoptosis-promoting pathways toward structural functions compared with the tubular subtype. Collectively, these findings underscore the potential influence of primary tumor location and histology on a microenvironmental metabolic architecture, offering exploratory insights for future hypothesis testing on location- and histology-dependent tumor adaptation.<\/jats:p>","DOI":"10.1021\/acs.jproteome.5c01260","type":"journal-article","created":{"date-parts":[[2026,6,29]],"date-time":"2026-06-29T06:36:50Z","timestamp":1782715010000},"page":"4018-4036","source":"Crossref","is-referenced-by-count":1,"title":["Integrated\nSpatial and Bulk Untargeted Metabolomics\nCharacterize Location- and Histology-Associated Metabolic Heterogeneity\nin Colorectal Cancer"],"prefix":"10.1021","volume":"25","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-8148-8305","authenticated-orcid":true,"given":"Junfeng","family":"Wang","sequence":"first","affiliation":[{"name":"Tianjin Key Laboratory of Digestive Cancer , , ,","place":["Tianjin, China, 300060"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0008-3050-5786","authenticated-orcid":true,"given":"Jinjin","family":"Gao","sequence":"additional","affiliation":[{"name":"Tianjin Key Laboratory of Digestive Cancer , , ,","place":["Tianjin, China, 300060"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jia","family":"Liu","sequence":"additional","affiliation":[{"name":"Tianjin Key Laboratory of Digestive Cancer , , ,","place":["Tianjin, China, 300060"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dongzhi","family":"Hu","sequence":"additional","affiliation":[{"name":"Tianjin Key Laboratory of Digestive Cancer , , ,","place":["Tianjin, China, 300060"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0008-2645-594X","authenticated-orcid":true,"given":"Yang","family":"Zhan","sequence":"additional","affiliation":[{"name":"Tianjin Key Laboratory of Digestive Cancer , , ,","place":["Tianjin, China, 300060"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"316","published-online":{"date-parts":[[2026,6,29]]},"reference":[{"issue":"1","key":"2026080709090193900_cit1","doi-asserted-by":"publisher","first-page":"12","DOI":"10.3322\/caac.21820","article-title":"Cancer statistics, 2024","volume":"74","author":"Siegel","year":"2024","journal-title":"Ca-Cancer J. Clin."},{"issue":"15_suppl","key":"2026080709090193900_cit2","doi-asserted-by":"publisher","first-page":"LBA3","DOI":"10.1200\/jco.2014.32.15_suppl.lba3","article-title":"CALGB\/SWOG\n80405: Phase III trial of irinotecan\/5-FU\/leucovorin (FOLFIRI) or\noxaliplatin\/5-FU\/leucovorin (mFOLFOX6) with bevacizumab (BV) or cetuximab\n(CET) for patients (pts) with KRAS wild-type (wt) untreated metastatic\nadenocarcinoma of the colon or rectum (MCRC)","volume":"32","author":"Venook","year":"2014","journal-title":"J. Clin. Oncol."},{"issue":"9","key":"2026080709090193900_cit3","doi-asserted-by":"publisher","first-page":"1607","DOI":"10.1007\/s00432-014-1678-3","article-title":"Left-sided primary tumors are associated with favorable\nprognosis in patients with KRAS codon 12\/13 wild-type metastatic colorectal\ncancer treated with cetuximab plus chemotherapy: an analysis of the\nAIO KRK-0104 trial","volume":"140","author":"von Einem","year":"2014","journal-title":"J. Cancer Res. Clin. Oncol."},{"issue":"10","key":"2026080709090193900_cit4","doi-asserted-by":"publisher","first-page":"1261","DOI":"10.1200\/JCO.2010.30.1366","article-title":"Value of mismatch repair,\nKRAS, and BRAF mutations in predicting recurrence and benefits from\nchemotherapy in colorectal cancer","volume":"29","author":"Hutchins","year":"2011","journal-title":"J. Clin.\nOncol."},{"issue":"2","key":"2026080709090193900_cit5","doi-asserted-by":"publisher","first-page":"117","DOI":"10.1158\/2159-8290.CD-11-0315","article-title":"Cancers of the colon and rectum:\nidentical or fraternal twins?","volume":"2","author":"Hong","year":"2012","journal-title":"Cancer Discov."},{"issue":"2","key":"2026080709090193900_cit6","doi-asserted-by":"publisher","first-page":"211","DOI":"10.1001\/jamaoncol.2016.4227","article-title":"Prognostic\nSurvival Associated With Left-Sided vs Right-Sided Colon Cancer: A\nSystematic Review and Meta-analysis","volume":"3","author":"Petrelli","year":"2017","journal-title":"JAMA Oncol."},{"key":"2026080709090193900_cit7","doi-asserted-by":"publisher","first-page":"1662464","DOI":"10.3389\/fcell.2025.1662464","article-title":"Metabolic\nreprogramming and immunosenescence in colorectal cancer: mechanisms\nand therapeutic implications","volume":"13","author":"Zhu","year":"2025","journal-title":"Front. Cell Dev.\nBiol."},{"issue":"1","key":"2026080709090193900_cit8","doi-asserted-by":"publisher","first-page":"160","DOI":"10.1186\/s13045-022-01358-5","article-title":"Warburg effect\nin colorectal cancer: the emerging roles\nin tumor microenvironment and therapeutic implications","volume":"15","author":"Zhong","year":"2022","journal-title":"J. Hematol. Oncol."},{"key":"2026080709090193900_cit9","doi-asserted-by":"publisher","first-page":"216384","DOI":"10.1016\/j.canlet.2023.216384","article-title":"Multi-omic analysis\nreveals metabolic pathways that characterize right-sided colon cancer\nliver metastasis","volume":"574","author":"Morris","year":"2023","journal-title":"Cancer Lett."},{"issue":"2 D","key":"2026080709090193900_cit10","doi-asserted-by":"publisher","DOI":"10.6004\/jnccn.2024.0029","article-title":"Colon Cancer, Version 3.2024, NCCN Clinical Practice Guidelines in\nOncology","volume":"22","author":"Benson","year":"2024","journal-title":"J. Natl. 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Rev."},{"key":"2026080709090193900_cit17","doi-asserted-by":"publisher","first-page":"1213273","DOI":"10.3389\/fonc.2023.1213273","article-title":"Spatial metabolomics\nin head and neck tumors: a review","volume":"13","author":"Zheng","year":"2023","journal-title":"Front. Oncol."},{"key":"2026080709090193900_cit18","doi-asserted-by":"publisher","first-page":"1054233","DOI":"10.3389\/fonc.2022.1054233","article-title":"When cancer drug resistance\nmeets metabolomics (bulk, single-cell\nand\/or spatial): Progress, potential, and perspective","volume":"12","author":"Zhang","year":"2023","journal-title":"Front. Oncol."},{"issue":"7","key":"2026080709090193900_cit19","doi-asserted-by":"publisher","first-page":"429","DOI":"10.1038\/s41571-023-00766-x","article-title":"Gut microbiota in colorectal\ncancer development and therapy","volume":"20","author":"Wong","year":"2023","journal-title":"Nat. Rev. Clin.\nOncol."},{"issue":"21","key":"2026080709090193900_cit20","doi-asserted-by":"publisher","first-page":"5317","DOI":"10.3390\/cancers14215317","article-title":"Gut Microbiota\nand Tumor Immune Escape: A New Perspective for Improving Tumor Immunotherapy","volume":"14","author":"He","year":"2022","journal-title":"Cancers (Basel)"},{"issue":"16","key":"2026080709090193900_cit21","doi-asserted-by":"publisher","DOI":"10.1172\/jci.insight.148028","article-title":"PLA2G4A promotes right-sided\ncolorectal cancer progression by inducing CD39+\u03b3\u03b4 Treg\npolarization","volume":"6","author":"Zhan","year":"2021","journal-title":"JCI Insight"},{"issue":"11","key":"2026080709090193900_cit22","doi-asserted-by":"publisher","first-page":"2126","DOI":"10.3390\/molecules24112126","article-title":"Design, Synthesis and Antibacterial\nActivity of Coumarin-1,2,3-triazole Hybrids Obtained from Natural\nFurocoumarin Peucedanin","volume":"24","author":"Lipeeva","year":"2019","journal-title":"Molecules"},{"issue":"D1","key":"2026080709090193900_cit23","doi-asserted-by":"publisher","first-page":"D672","DOI":"10.1093\/nar\/gkae909","article-title":"KEGG: biological\nsystems database as a model of the real world","volume":"53","author":"Kanehisa","year":"2025","journal-title":"Nucleic Acids Res."},{"issue":"1","key":"2026080709090193900_cit24","doi-asserted-by":"publisher","first-page":"27","DOI":"10.1093\/nar\/28.1.27","article-title":"KEGG: kyoto encyclopedia of genes and genomes","volume":"28","author":"Kanehisa","year":"2000","journal-title":"Nucleic Acids Res."},{"issue":"11","key":"2026080709090193900_cit25","doi-asserted-by":"publisher","first-page":"1947","DOI":"10.1002\/pro.3715","article-title":"Toward understanding\nthe origin and evolution of cellular organisms","volume":"28","author":"Kanehisa","year":"2019","journal-title":"Protein Sci."},{"issue":"8","key":"2026080709090193900_cit26","doi-asserted-by":"publisher","first-page":"1432","DOI":"10.1038\/s41591-021-01406-6","article-title":"Gut microbiota signatures are associated\nwith toxicity to combined CTLA-4 and PD-1 blockade","volume":"27","author":"Andrews","year":"2021","journal-title":"Nat. Med."},{"issue":"17","key":"2026080709090193900_cit27","doi-asserted-by":"publisher","first-page":"15411","DOI":"10.1021\/acs.jmedchem.4c00989","article-title":"Examining\nHemin and\nits Derivatives: Induction of Heme-Oxygenase-1 Activity and Oxidative\nStress in Breast Cancer Cells through Collaborative Experimental Analysis\nand Molecular Dynamics Simulations","volume":"67","author":"Alsharabasy","year":"2024","journal-title":"J. Med.\nChem."},{"issue":"15","key":"2026080709090193900_cit28","doi-asserted-by":"publisher","first-page":"3714","DOI":"10.3390\/cancers14153714","article-title":"Reprogrammed\nLipid Metabolism and the Lipid-Associated Hallmarks of Colorectal\nCancer","volume":"14","author":"Salita","year":"2022","journal-title":"Cancers (Basel)"},{"issue":"2","key":"2026080709090193900_cit29","doi-asserted-by":"publisher","first-page":"192","DOI":"10.3390\/diagnostics15020192","article-title":"Clinical Outcome Differences in Mucinous Versus Non-Mucinous\nColonic Adenocarcinoma: A Comparative Study","volume":"15","author":"Cote","year":"2025","journal-title":"Diagnostics"},{"issue":"1","key":"2026080709090193900_cit30","doi-asserted-by":"publisher","first-page":"13","DOI":"10.1186\/s40880-019-0361-0","article-title":"Mucinous colorectal adenocarcinoma:\nclinical pathology and treatment options","volume":"39","author":"Luo","year":"2019","journal-title":"Cancer\nCommun."},{"issue":"1","key":"2026080709090193900_cit31","doi-asserted-by":"publisher","first-page":"85","DOI":"10.1038\/s42003-023-04441-w","article-title":"Single-cell profiling\nreveals differences between human classical adenocarcinoma and mucinous\nadenocarcinoma","volume":"6","author":"Hu","year":"2023","journal-title":"Commun. Biol."},{"issue":"1","key":"2026080709090193900_cit32","doi-asserted-by":"publisher","first-page":"39","DOI":"10.1016\/j.molonc.2013.08.010","article-title":"Chemical\nmapping of the colorectal cancer microenvironment via MALDI imaging\nmass spectrometry (MALDI-MSI) reveals novel cancer-associated field\neffects","volume":"8","author":"Mirnezami","year":"2014","journal-title":"Mol. Oncol."},{"key":"2026080709090193900_cit33","doi-asserted-by":"publisher","first-page":"1089090","DOI":"10.3389\/fonc.2023.1089090","article-title":"Spatially resolved\ntranscriptomics revealed local invasion-related\ngenes in colorectal cancer","volume":"13","author":"Liu","year":"2023","journal-title":"Front. Oncol."},{"issue":"1","key":"2026080709090193900_cit34","doi-asserted-by":"publisher","first-page":"111929","DOI":"10.1016\/j.celrep.2022.111929","article-title":"Spatial and single-cell transcriptomics\ndecipher the\ncellular environment containing HLA-G+ cancer cells and SPP1+ macrophages\nin colorectal cancer","volume":"42","author":"Ozato","year":"2023","journal-title":"Cell Rep."},{"issue":"2","key":"2026080709090193900_cit35","doi-asserted-by":"publisher","first-page":"72","DOI":"10.1007\/s10142-024-01356-5","article-title":"Targeting nucleotide\nmetabolic pathways in colorectal cancer by integrating scRNA-seq,\nspatial transcriptome, and bulk RNA-seq data","volume":"24","author":"Zhao","year":"2024","journal-title":"Funct. Integr. Genomics"},{"issue":"3","key":"2026080709090193900_cit36","doi-asserted-by":"publisher","first-page":"411","DOI":"10.6004\/jnccn.2017.0038","article-title":"Right Versus\nLeft Colon Cancer Biology:\nIntegrating the Consensus Molecular Subtypes","volume":"15","author":"Lee","year":"2017","journal-title":"J. Natl. Compr. Cancer Network"},{"issue":"6","key":"2026080709090193900_cit37","doi-asserted-by":"publisher","first-page":"847","DOI":"10.1136\/gutjnl-2011-300865","article-title":"Assessment of colorectal cancer molecular\nfeatures along bowel subsites challenges the conception of distinct\ndichotomy of proximal versus distal colorectum","volume":"61","author":"Yamauchi","year":"2012","journal-title":"Gut"},{"issue":"1","key":"2026080709090193900_cit38","doi-asserted-by":"publisher","first-page":"116","DOI":"10.1038\/s41698-025-00892-y","article-title":"Multidimensional differences of right-\nand left-sided colorectal cancer and their impact on targeted therapies","volume":"9","author":"Abdel Hamid","year":"2025","journal-title":"npj Precis. Oncol."},{"issue":"1","key":"2026080709090193900_cit39","doi-asserted-by":"publisher","first-page":"35","DOI":"10.1038\/s44303-024-00041-3","article-title":"MALDI imaging combined\nwith two-photon microscopy reveals local differences in the heterogeneity\nof colorectal cancer","volume":"2","author":"Bharti","year":"2024","journal-title":"Npj Imaging"},{"key":"2026080709090193900_cit40","doi-asserted-by":"publisher","first-page":"1589943","DOI":"10.3389\/fimmu.2025.1589943","article-title":"Driving innovations\nin cancer research through spatial metabolomics: a bibliometric review\nof trends and hotspot","volume":"16","author":"Chen","year":"2025","journal-title":"Front. Immunol."},{"issue":"1","key":"2026080709090193900_cit41","doi-asserted-by":"publisher","first-page":"10","DOI":"10.1038\/s41698-023-00488-4","article-title":"Profiling the heterogeneity\nof colorectal cancer consensus molecular subtypes using spatial transcriptomics","volume":"8","author":"Valdeolivas","year":"2024","journal-title":"npj Precis. Oncol."},{"key":"2026080709090193900_cit42","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1155\/2023\/9328344","article-title":"Clinical Significance\nof Carnitine\nin the Treatment of Cancer: From Traffic to the Regulation","volume":"2023","author":"Farahzadi","year":"2023","journal-title":"Oxid. Med. Cell. Longev."},{"issue":"6","key":"2026080709090193900_cit43","first-page":"2477","article-title":"The role and\ntherapeutic implication of CPTs in fatty acid oxidation and cancers\nprogression","volume":"11","author":"Wang","year":"2021","journal-title":"Am. J. Cancer Res."},{"issue":"8","key":"2026080709090193900_cit44","doi-asserted-by":"publisher","first-page":"1630","DOI":"10.1038\/s42255-025-01330-w","article-title":"The source\nof dietary fat influences anti-tumour immunity in obese mice","volume":"7","author":"Kunkemoeller","year":"2025","journal-title":"Nat. Metab."},{"key":"2026080709090193900_cit45","doi-asserted-by":"publisher","first-page":"72","DOI":"10.1038\/s41420-018-0075-0","article-title":"Targeting sphingolipid\nmetabolism as an approach for combination therapies in haematological\nmalignancies","volume":"4","author":"Lewis","year":"2018","journal-title":"Cell Death Discov."},{"key":"2026080709090193900_cit46","doi-asserted-by":"publisher","first-page":"565316","DOI":"10.1155\/2011\/565316","article-title":"Apoptotic\nsphingolipid\nceramide in cancer therapy","volume":"2011","author":"Huang","year":"2011","journal-title":"J. Lipids"},{"issue":"5","key":"2026080709090193900_cit47","doi-asserted-by":"publisher","first-page":"692","DOI":"10.1016\/j.bbalip.2013.12.003","article-title":"The role of sphingomyelin and sphingomyelin synthases\nin cell death, proliferation and migration-from cell and animal models\nto human disorders","volume":"1841","author":"Taniguchi","year":"2014","journal-title":"Biochim. Biophys. Acta Gen.\nSubj."},{"key":"2026080709090193900_cit48","doi-asserted-by":"publisher","first-page":"61","DOI":"10.1016\/bs.acr.2018.04.009","article-title":"Role and Function\nof Sphingomyelin\nBiosynthesis in the Development of Cancer","volume":"140","author":"D\u2019Angelo","year":"2018","journal-title":"Adv.\nCancer Res."},{"issue":"3","key":"2026080709090193900_cit49","doi-asserted-by":"publisher","first-page":"175","DOI":"10.1038\/nrm.2017.107","article-title":"Sphingolipids and\ntheir metabolism in physiology and\ndisease","volume":"19","author":"Hannun","year":"2018","journal-title":"Nat. Rev. Mol. Cell Biol."},{"issue":"1","key":"2026080709090193900_cit50","doi-asserted-by":"publisher","first-page":"41","DOI":"10.1038\/nrd2465","article-title":"The role\nof histamine H1 and H4 receptors\nin allergic inflammation: the search for new antihistamines","volume":"7","author":"Thurmond","year":"2008","journal-title":"Nat. Rev. Drug Discov."},{"issue":"21","key":"2026080709090193900_cit51","doi-asserted-by":"publisher","first-page":"3577","DOI":"10.1158\/0008-5472.CAN-23-0025","article-title":"Matrix Stiffness Triggers Lipid Metabolic Cross-talk between Tumor\nand Stromal Cells to Mediate Bevacizumab Resistance in Colorectal\nCancer Liver Metastases","volume":"83","author":"Zheng","year":"2023","journal-title":"Cancer Res."},{"issue":"11","key":"2026080709090193900_cit52","doi-asserted-by":"publisher","first-page":"1350","DOI":"10.1038\/nm.3967","article-title":"The consensus molecular\nsubtypes of colorectal cancer","volume":"21","author":"Guinney","year":"2015","journal-title":"Nat. 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