{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,24]],"date-time":"2026-09-24T01:37:55Z","timestamp":1790213875738,"version":"4.1.0"},"reference-count":53,"publisher":"Elsevier BV","issue":"12","license":[{"start":{"date-parts":[[2023,12,1]],"date-time":"2023-12-01T00:00:00Z","timestamp":1701388800000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/tdm\/userlicense\/1.0\/"},{"start":{"date-parts":[[2023,12,1]],"date-time":"2023-12-01T00:00:00Z","timestamp":1701388800000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/legal\/tdmrep-license"},{"start":{"date-parts":[[2023,11,14]],"date-time":"2023-11-14T00:00:00Z","timestamp":1699920000000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100014013","name":"UK Research and Innovation","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100014013","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100000266","name":"Engineering and Physical Sciences Research Council","doi-asserted-by":"publisher","award":["EP\/W02909X\/1"],"award-info":[{"award-number":["EP\/W02909X\/1"]}],"id":[{"id":"10.13039\/501100000266","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100006041","name":"Innovate UK","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100006041","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100004330","name":"GlaxoSmithKline","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100004330","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["cell.com","elsevier.com","sciencedirect.com"],"crossmark-restriction":true},"short-container-title":["Cell Reports Medicine"],"published-print":{"date-parts":[[2023,12]]},"DOI":"10.1016\/j.xcrm.2023.101313","type":"journal-article","created":{"date-parts":[[2023,12,19]],"date-time":"2023-12-19T10:44:54Z","timestamp":1702982694000},"page":"101313","update-policy":"https:\/\/doi.org\/10.1016\/elsevier_cm_policy","source":"Crossref","is-referenced-by-count":12,"title":["Cross-linking breast tumor transcriptomic states and tissue histology"],"prefix":"10.1016","volume":"4","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-5358-9478","authenticated-orcid":false,"given":"Muhammad","family":"Dawood","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mark","family":"Eastwood","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mostafa","family":"Jahanifar","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lawrence","family":"Young","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Asa","family":"Ben-Hur","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kim","family":"Branson","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Louise","family":"Jones","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nasir","family":"Rajpoot","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Fayyaz ul Amir Afsar","family":"Minhas","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"78","reference":[{"key":"10.1016\/j.xcrm.2023.101313_bib1","doi-asserted-by":"crossref","first-page":"31","DOI":"10.1158\/2159-8290.CD-21-1059","article-title":"Hallmarks of Cancer: New Dimensions","volume":"12","author":"Hanahan","year":"2022","journal-title":"Cancer Discov."},{"key":"10.1016\/j.xcrm.2023.101313_bib2","doi-asserted-by":"crossref","first-page":"375","DOI":"10.1002\/path.4847","article-title":"The molecular basis of breast cancer pathological phenotypes","volume":"241","author":"Heng","year":"2017","journal-title":"J.\u00a0Pathol."},{"key":"10.1016\/j.xcrm.2023.101313_bib3","doi-asserted-by":"crossref","first-page":"1160","DOI":"10.1200\/JCO.2008.18.1370","article-title":"Supervised Risk Predictor of Breast Cancer Based on Intrinsic Subtypes","volume":"27","author":"Parker","year":"2009","journal-title":"J.\u00a0Clin. Oncol."},{"key":"10.1016\/j.xcrm.2023.101313_bib4","doi-asserted-by":"crossref","first-page":"714","DOI":"10.1158\/1055-9965.EPI-13-1023","article-title":"Intrinsic Subtypes from PAM50 Gene Expression Assay in a Population-Based Breast Cancer Cohort: Differences by Age, Race, and Tumor Characteristics","volume":"23","author":"Sweeney","year":"2014","journal-title":"Cancer Epidemiol. Biomarkers Prev."},{"key":"10.1016\/j.xcrm.2023.101313_bib5","doi-asserted-by":"crossref","first-page":"721","DOI":"10.1200\/JCO.2007.15.1068","article-title":"Development of the 21-gene assay and its application in clinical practice and clinical trials","volume":"26","author":"Sparano","year":"2008","journal-title":"J.\u00a0Clin. Oncol."},{"key":"10.1016\/j.xcrm.2023.101313_bib6","doi-asserted-by":"crossref","first-page":"1183","DOI":"10.1093\/jnci\/djj329","article-title":"Validation and Clinical Utility of a 70-Gene Prognostic Signature for Women With Node-Negative Breast Cancer","volume":"98","author":"Buyse","year":"2006","journal-title":"J.\u00a0Natl. Cancer Inst."},{"key":"10.1016\/j.xcrm.2023.101313_bib7","doi-asserted-by":"crossref","first-page":"57","DOI":"10.1038\/nrg2484","article-title":"RNA-Seq: a revolutionary tool for transcriptomics","volume":"10","author":"Wang","year":"2009","journal-title":"Nat. Rev. Genet."},{"key":"10.1016\/j.xcrm.2023.101313_bib8","doi-asserted-by":"crossref","first-page":"377","DOI":"10.1038\/nmeth.1315","article-title":"mRNA-Seq whole-transcriptome analysis of a single cell","volume":"6","author":"Tang","year":"2009","journal-title":"Nat. Methods"},{"key":"10.1016\/j.xcrm.2023.101313_bib9","doi-asserted-by":"crossref","first-page":"1096","DOI":"10.1038\/nmeth.2639","article-title":"Smart-seq2 for sensitive full-length transcriptome profiling in single cells","volume":"10","author":"Picelli","year":"2013","journal-title":"Nat. Methods"},{"key":"10.1016\/j.xcrm.2023.101313_bib10","doi-asserted-by":"crossref","first-page":"9","DOI":"10.1038\/s41592-020-01033-y","article-title":"Method of the Year: spatially resolved transcriptomics","volume":"18","author":"Marx","year":"2021","journal-title":"Nat. Methods"},{"key":"10.1016\/j.xcrm.2023.101313_bib11","doi-asserted-by":"crossref","first-page":"78","DOI":"10.1126\/science.aaf2403","article-title":"Visualization and analysis of gene expression in tissue sections by spatial transcriptomics","volume":"353","author":"St\u00e5hl","year":"2016","journal-title":"Science"},{"key":"10.1016\/j.xcrm.2023.101313_bib12","doi-asserted-by":"crossref","first-page":"586","DOI":"10.1038\/s41587-020-0472-9","article-title":"Multiplex digital spatial profiling of proteins and RNA in fixed tissue","volume":"38","author":"Merritt","year":"2020","journal-title":"Nat. Biotechnol."},{"key":"10.1016\/j.xcrm.2023.101313_bib13","series-title":"Joint European Conference on Machine Learning and Knowledge Discovery in Databases","first-page":"437","article-title":"All You Need is Color: Image based Spatial Gene Expression Prediction using Neural Stain Learning","author":"Dawood","year":"2021"},{"key":"10.1016\/j.xcrm.2023.101313_bib14","doi-asserted-by":"crossref","first-page":"827","DOI":"10.1038\/s41551-020-0578-x","article-title":"Integrating spatial gene expression and breast tumour morphology via deep learning","volume":"4","author":"He","year":"2020","journal-title":"Nat. Biomed. Eng."},{"key":"10.1016\/j.xcrm.2023.101313_bib15","doi-asserted-by":"crossref","first-page":"3877","DOI":"10.1038\/s41467-020-17678-4","article-title":"A deep learning model to predict RNA-Seq expression of tumours from whole slide images","volume":"11","author":"Schmauch","year":"2020","journal-title":"Nat. Commun."},{"key":"10.1016\/j.xcrm.2023.101313_bib16","doi-asserted-by":"crossref","first-page":"5115","DOI":"10.1158\/0008-5472.CAN-21-0482","article-title":"Predicting Molecular Phenotypes from Histopathology Images: A Transcriptome-Wide Expression\u2013Morphology Analysis in Breast Cancer","volume":"81","author":"Wang","year":"2021","journal-title":"Cancer Res."},{"key":"10.1016\/j.xcrm.2023.101313_bib17","doi-asserted-by":"crossref","first-page":"304","DOI":"10.1038\/s42003-023-04583-x","article-title":"Learning to predict RNA sequence expressions from whole slide images with applications for search and classification","volume":"6","author":"Alsaafin","year":"2023","journal-title":"Commun. Biol."},{"key":"10.1016\/j.xcrm.2023.101313_bib18","series-title":"Handbook of Systems Biology Concepts and Insights","first-page":"45","article-title":"Interactome Networks","author":"Carvunis","year":"2013"},{"key":"10.1016\/j.xcrm.2023.101313_bib19","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1038\/s41540-020-00168-0","article-title":"Gene co-expression in the interactome: moving from correlation toward causation via an integrated approach to disease module discovery","volume":"7","author":"Paci","year":"2021","journal-title":"NPJ Syst. Biol. Appl."},{"key":"10.1016\/j.xcrm.2023.101313_bib20","doi-asserted-by":"crossref","first-page":"12","DOI":"10.1186\/s12920-017-0245-6","article-title":"Comprehensive discovery of subsample gene expression components by information explanation: therapeutic implications in cancer","volume":"10","author":"Pepke","year":"2017","journal-title":"BMC Med. Genomics"},{"key":"10.1016\/j.xcrm.2023.101313_bib21","doi-asserted-by":"crossref","first-page":"595","DOI":"10.1038\/nri1901","article-title":"The biology of interleukin-2 and interleukin-15: implications for cancer therapy and vaccine design","volume":"6","author":"Waldmann","year":"2006","journal-title":"Nat. Rev. Immunol."},{"key":"10.1016\/j.xcrm.2023.101313_bib22","doi-asserted-by":"crossref","first-page":"2246","DOI":"10.1161\/ATVBAHA.115.305289","article-title":"Plasma Levels of Soluble Interleukin-2 Receptor \u03b1","volume":"35","author":"Durda","year":"2015","journal-title":"Arterioscler. Thromb. Vasc. Biol."},{"key":"10.1016\/j.xcrm.2023.101313_bib23","doi-asserted-by":"crossref","first-page":"67","DOI":"10.1186\/s12943-017-0634-7","article-title":"TRIM8 restores p53 tumour suppressor function by blunting N-MYC activity in chemo-resistant tumours","volume":"16","author":"Mastropasqua","year":"2017","journal-title":"Mol. Cancer"},{"key":"10.1016\/j.xcrm.2023.101313_bib24","doi-asserted-by":"crossref","first-page":"812","DOI":"10.1016\/j.immuni.2018.03.023","article-title":"The Immune Landscape of Cancer","volume":"48","author":"Thorsson","year":"2018","journal-title":"Immunity"},{"key":"10.1016\/j.xcrm.2023.101313_bib25","doi-asserted-by":"crossref","first-page":"1298","DOI":"10.55563\/clinexprheumatol\/ret1kg","article-title":"Increased expression of interferon regulated and antiviral response genes in CD31+\/CD102+ lung microvascular endothelial cells from systemic sclerosis patients with end-stage interstitial lung disease","volume":"39","author":"Piera-Velazquez","year":"2021","journal-title":"Clin. Exp. Rheumatol."},{"key":"10.1016\/j.xcrm.2023.101313_bib26","article-title":"Molecular analysis of TCGA breast cancer histologic types","volume":"1","author":"Thennavan","year":"2021","journal-title":"Cell Genom."},{"key":"10.1016\/j.xcrm.2023.101313_bib27","doi-asserted-by":"crossref","first-page":"181","DOI":"10.1016\/j.celrep.2018.03.086","article-title":"Spatial Organization and Molecular Correlation of Tumor-Infiltrating Lymphocytes Using Deep Learning on Pathology Images","volume":"23","author":"Saltz","year":"2018","journal-title":"Cell Rep."},{"key":"10.1016\/j.xcrm.2023.101313_bib28","doi-asserted-by":"crossref","DOI":"10.1016\/j.media.2022.102486","article-title":"SlideGraph+: Whole slide image level graphs to predict HER2 status in breast cancer","volume":"80","author":"Lu","year":"2022","journal-title":"Med. Image Anal."},{"key":"10.1016\/j.xcrm.2023.101313_bib29","doi-asserted-by":"crossref","first-page":"555","DOI":"10.1038\/s41551-020-00682-w","article-title":"Data-efficient and weakly supervised computational pathology on whole-slide images","volume":"5","author":"Lu","year":"2021","journal-title":"Nat. Biomed. Eng."},{"key":"10.1016\/j.xcrm.2023.101313_bib30","doi-asserted-by":"crossref","first-page":"1301","DOI":"10.1038\/s41591-019-0508-1","article-title":"Clinical-grade computational pathology using weakly supervised deep learning on whole slide images","volume":"25","author":"Campanella","year":"2019","journal-title":"Nat. Med."},{"key":"10.1016\/j.xcrm.2023.101313_bib31","doi-asserted-by":"crossref","first-page":"192","DOI":"10.1016\/j.molonc.2010.04.004","article-title":"Histological types of breast cancer: How special are they?","volume":"4","author":"Weigelt","year":"2010","journal-title":"Mol. Oncol."},{"key":"10.1016\/j.xcrm.2023.101313_bib32","doi-asserted-by":"crossref","first-page":"321","DOI":"10.1016\/j.cell.2018.03.035","article-title":"Oncogenic Signaling Pathways in The Cancer Genome Atlas","volume":"173","author":"Sanchez-Vega","year":"2018","journal-title":"Cell"},{"key":"10.1016\/j.xcrm.2023.101313_bib33","doi-asserted-by":"crossref","first-page":"425","DOI":"10.1038\/s41392-021-00828-5","article-title":"Targeting PI3K\/Akt signal transduction for cancer therapy","volume":"6","author":"He","year":"2021","journal-title":"Sig Transduct Target Ther"},{"key":"10.1016\/j.xcrm.2023.101313_bib34","doi-asserted-by":"crossref","first-page":"1371","DOI":"10.1158\/1535-7163.MCT-21-0958","article-title":"YES1: A Novel Therapeutic Target and Biomarker in Cancer","volume":"21","author":"Garmendia","year":"2022","journal-title":"Mol. Cancer Ther."},{"key":"10.1016\/j.xcrm.2023.101313_bib35","doi-asserted-by":"crossref","first-page":"e1163462","DOI":"10.1080\/2162402X.2016.1163462","article-title":"Role of IL-2 in cancer immunotherapy","volume":"5","author":"Jiang","year":"2016","journal-title":"OncoImmunology"},{"key":"10.1016\/j.xcrm.2023.101313_bib36","doi-asserted-by":"crossref","first-page":"395","DOI":"10.1089\/bio.2014.0055","article-title":"Biobanking Sustainability\u2014Experiences of the Australian Breast Cancer Tissue Bank (ABCTB)","volume":"12","author":"Carpenter","year":"2014","journal-title":"Biopreserv. Biobank."},{"key":"10.1016\/j.xcrm.2023.101313_bib37","doi-asserted-by":"crossref","first-page":"291","DOI":"10.1016\/j.cell.2018.03.022","article-title":"Cell-of-Origin Patterns Dominate the Molecular Classification of 10,000 Tumors from 33 Types of Cancer","volume":"173","author":"Hoadley","year":"2018","journal-title":"Cell"},{"key":"10.1016\/j.xcrm.2023.101313_bib38","doi-asserted-by":"crossref","first-page":"61","DOI":"10.1038\/nature11412","article-title":"Comprehensive molecular portraits of human breast tumours","volume":"490","year":"2012","journal-title":"Nature"},{"key":"10.1016\/j.xcrm.2023.101313_bib39","doi-asserted-by":"crossref","first-page":"55","DOI":"10.1038\/nature18003","article-title":"Proteogenomics connects somatic mutations to signaling in breast cancer","volume":"534","author":"Mertins","year":"2016","journal-title":"Nature"},{"key":"10.1016\/j.xcrm.2023.101313_bib40","doi-asserted-by":"crossref","first-page":"346","DOI":"10.1038\/nature10983","article-title":"The genomic and transcriptomic architecture of 2,000 breast tumours reveals novel subgroups","volume":"486","author":"Curtis","year":"2012","journal-title":"Nature"},{"key":"10.1016\/j.xcrm.2023.101313_bib41","article-title":"The somatic mutation profiles of 2,433 breast cancers refines their genomic and transcriptomic landscapes","volume":"7","author":"Pereira","year":"2016","journal-title":"Nat. Commun."},{"key":"10.1016\/j.xcrm.2023.101313_bib42","doi-asserted-by":"crossref","first-page":"401","DOI":"10.1158\/2159-8290.CD-12-0095","article-title":"The cBio cancer genomics portal: an open platform for exploring multidimensional cancer genomics data","volume":"2","author":"Cerami","year":"2012","journal-title":"Cancer Discov."},{"key":"10.1016\/j.xcrm.2023.101313_bib43","doi-asserted-by":"crossref","first-page":"pl1","DOI":"10.1126\/scisignal.2004088","article-title":"Integrative analysis of complex cancer genomics and clinical profiles using the cBioPortal","volume":"6","author":"Gao","year":"2013","journal-title":"Sci. Signal."},{"key":"10.1016\/j.xcrm.2023.101313_bib44","series-title":"2018 IEEE\/CVF Conference on Computer Vision and Pattern Recognition","first-page":"6848","article-title":"ShuffleNet: An Extremely Efficient Convolutional Neural Network for Mobile Devices","author":"Zhang","year":"2018"},{"key":"10.1016\/j.xcrm.2023.101313_bib45","doi-asserted-by":"crossref","first-page":"1045","DOI":"10.1007\/s10278-013-9622-7","article-title":"The Cancer Imaging Archive (TCIA): Maintaining and Operating a Public Information Repository","volume":"26","author":"Clark","year":"2013","journal-title":"J.\u00a0Digit. Imaging"},{"key":"10.1016\/j.xcrm.2023.101313_bib46","article-title":"Maximally Informative Hierarchical Representations of High-Dimensional Data","author":"Steeg","year":"2015","journal-title":"arXiv"},{"key":"10.1016\/j.xcrm.2023.101313_bib47","doi-asserted-by":"crossref","first-page":"W90","DOI":"10.1093\/nar\/gkw377","article-title":"Enrichr: a comprehensive gene set enrichment analysis web server 2016 update","volume":"44","author":"Kuleshov","year":"2016","journal-title":"Nucleic Acids Res."},{"key":"10.1016\/j.xcrm.2023.101313_bib48","doi-asserted-by":"crossref","first-page":"D380","DOI":"10.1093\/nar\/gkv1277","article-title":"STITCH 5: augmenting protein\u2013chemical interaction networks with tissue and affinity data","volume":"44","author":"Szklarczyk","year":"2016","journal-title":"Nucleic Acids Res."},{"key":"10.1016\/j.xcrm.2023.101313_bib49","series-title":"Trustworthy Machine Learning for Healthcare","first-page":"1","article-title":"Do Tissue Source Sites Leave Identifiable Signatures in Whole Slide Images Beyond Staining?","author":"Keller","year":"2023"},{"key":"10.1016\/j.xcrm.2023.101313_bib50","doi-asserted-by":"crossref","first-page":"211","DOI":"10.1007\/s11263-015-0816-y","article-title":"ImageNet Large Scale Visual Recognition Challenge","volume":"115","author":"Russakovsky","year":"2015","journal-title":"Int. J. Comput. Vis."},{"key":"10.1016\/j.xcrm.2023.101313_bib51","article-title":"Dynamic Graph CNN for Learning on Point Clouds","author":"Wang","year":"2019","journal-title":"arXiv"},{"key":"10.1016\/j.xcrm.2023.101313_bib52","series-title":"2021 IEEE\/CVF International Conference on Computer Vision Workshops (ICCVW)","first-page":"664","article-title":"ALBRT: Cellular Composition Prediction in Routine Histology Images","author":"Dawood","year":"2021"},{"key":"10.1016\/j.xcrm.2023.101313_bib53","article-title":"Stain-Robust Mitotic Figure\u00a0Detection for MIDOG 2022 Challenge","author":"Jahanifar","year":"2022","journal-title":"arXiv"}],"container-title":["Cell Reports Medicine"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S2666379123005074?httpAccept=text\/xml","content-type":"text\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S2666379123005074?httpAccept=text\/plain","content-type":"text\/plain","content-version":"vor","intended-application":"text-mining"}],"deposited":{"date-parts":[[2025,11,12]],"date-time":"2025-11-12T22:58:50Z","timestamp":1762988330000},"score":1,"resource":{"primary":{"URL":"https:\/\/linkinghub.elsevier.com\/retrieve\/pii\/S2666379123005074"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,12]]},"references-count":53,"journal-issue":{"issue":"12","published-print":{"date-parts":[[2023,12]]}},"alternative-id":["S2666379123005074"],"URL":"https:\/\/doi.org\/10.1016\/j.xcrm.2023.101313","relation":{},"ISSN":["2666-3791"],"issn-type":[{"value":"2666-3791","type":"print"}],"subject":[],"published":{"date-parts":[[2023,12]]},"assertion":[{"value":"Elsevier","name":"publisher","label":"This article is maintained by"},{"value":"Cross-linking breast tumor transcriptomic states and tissue histology","name":"articletitle","label":"Article Title"},{"value":"Cell Reports Medicine","name":"journaltitle","label":"Journal Title"},{"value":"https:\/\/doi.org\/10.1016\/j.xcrm.2023.101313","name":"articlelink","label":"CrossRef DOI link to publisher maintained version"},{"value":"article","name":"content_type","label":"Content Type"},{"value":"\u00a9 2023 The Authors.","name":"copyright","label":"Copyright"}],"article-number":"101313"}}