ArticleCell2019
Integrated Proteogenomic Characterization of Clear Cell Renal Cell Carcinoma.
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Article in Cell, 2019. The graph could read no effect estimate from its abstract, so it casts no vote on the map. An erratum has been issued. Cited by 459 papers, 1 of them a synthesis that pooled it.
0numbers the graph read from it
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459citing papers in PubMed, 1 pooled it
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What it found
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The abstract states no effect estimate the extractor could read, or names no intervention and outcome on the map, so this paper lights no cell and moves no belief. It is still indexed, cited and linked below.
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Trials whose registry record cites this paper, or whose number appears in the abstract. A trial that started after this paper was published is citing it as background, not reporting it.
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Who cites it
459 citing papers in PubMed, 1 synthesis or guideline pooled it.
- Molecular biomarkers in metastatic clear cell renal cell carcinoma treated with first-line immune combinations: a systematic review of phase III randomized clinical trials by Meet-URO group.Cancer metastasis reviews · 2026Pooled it
- Pan-Cancer Quantification of Driver Alteration Transmission Across Molecular Layers Reveals Limited Propagation to Protein Abundance.International journal of cancer · 2026Article
- SLC39-driven zinc influx orchestrates pleiotropic tumor-immune system cross-talk to establish immune suppression in colorectal cancer.Science advances · 2026Article
- Integrated multi-omics analysis reveals the molecular landscape and therapeutic strategies in Chinese cervical cancer patients.PLoS biology · 2026Article
- Integrated metabolomics data analysis to generate mechanistic hypotheses with MetaProViz.Molecular systems biology · 2026Article
- Complex assembly and activity states as multifaceted protein attributes explaining phenotypic variability.Molecular systems biology · 2026Article
- Machine learning and multi-omics clustering to map cellular rewiring and immune evasion in ccRCC.Human genomics · 2026Article
- Effective tumor kinetics inferred from single routine H&E biopsies enable counterfactual virtual radiotherapy trials.medRxiv : the preprint server for health sciences · 2026Article
- Renal cell carcinoma: molecular understanding and therapeutic development.Cell death and differentiation · 2026Review
- Current Advances of Treatments, Therapeutic Targets, Biomarkers, Novel Drugs, and Machine Learning for Hypopharyngeal Squamous Cell Carcinoma.World journal of otorhinolaryngology - head and neck surgery · 2026Review
- SPOP-mediated ZMYND8 ubiquitination and phase separation exclusion drives mTOR inhibitor resistance in kidney cancer.Nature communications · 2026Article
- Distinct endogenous retroviruses are expressed in mutational subtypes of clear cell renal cell carcinoma and are linked to improved clinical outcomes.Cell reports · 2026Article
- The Deubiquitinating Enzyme USP9X Regulates the Protein Stability of the FAM49B in Clear Cell Renal Cell Carcinoma.Journal of proteome research · 2026Article
- Urinary proteome and metabolome uncover tumor microenvironment and cellular metabolism changes of renal clear cell carcinoma.British journal of cancer · 2026Article
- Nuclear PML expression as a prognostic biomarker in localised clear cell renal cell carcinoma.BJUI compass · 2026Article
- Article
- Absolute quantitative proteomics guides patient-stratified drug repurposing in clear cell and papillary renal cell carcinoma.bioRxiv : the preprint server for biology · 2026Article
- Bimodality in pan-cancer proteomics reveals new opportunities for biomarker discovery.Genome biology · 2026Article
- Loss of the USP22 deubiquitylase confers resistance to chemotherapy in small cell lung cancer.Nature communications · 2026Article
- Attenuation of EGFR-Mediated Cellular Signaling by Sialidase-Mediated Desialylation.Research square · 2026Article
399 more citing papers are in PubMed but not listed here.
Corrections and comments
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Authors and funding
81 authors.
David J ClarkDepartment of Pathology, Johns Hopkins University, Baltimore, MD 21231, USA.
Saravana M DhanasekaranDepartment of Pathology, University of Michigan, Ann Arbor, MI 48109, USA.
Francesca PetraliaDepartment of Genetics and Genomic Sciences and Icahn Institute for Data Science and Genomic Technology, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
Jianbo PanDepartment of Pathology, Johns Hopkins University, Baltimore, MD 21231, USA.
Xiaoyu SongDepartment of Population Health Science and Policy, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA; Tisch Cancer Institute, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
Yingwei HuDepartment of Pathology, Johns Hopkins University, Baltimore, MD 21231, USA.
Felipe da Veiga LeprevostDepartment of Pathology, University of Michigan, Ann Arbor, MI 48109, USA.
Boris RevaDepartment of Genetics and Genomic Sciences and Icahn Institute for Data Science and Genomic Technology, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
Tung-Shing M LihDepartment of Pathology, Johns Hopkins University, Baltimore, MD 21231, USA.
Hui-Yin ChangDepartment of Pathology, University of Michigan, Ann Arbor, MI 48109, USA.
Weiping MaDepartment of Genetics and Genomic Sciences and Icahn Institute for Data Science and Genomic Technology, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
Chen HuangLester and Sue Smith Breast Center, Baylor College of Medicine, Houston, TX 77030, USA.
Christopher J RickettsUrologic Oncology Branch, Center for Cancer Research, National Cancer Institute, National Institutes of Health, Bethesda, MD 20892, USA.
Lijun ChenDepartment of Pathology, Johns Hopkins University, Baltimore, MD 21231, USA.
Azra KrekDepartment of Genetics and Genomic Sciences and Icahn Institute for Data Science and Genomic Technology, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
Yize LiWashington University School of Medicine, St. Louis, MO 63110, USA.
Dmitry RykunovDepartment of Genetics and Genomic Sciences and Icahn Institute for Data Science and Genomic Technology, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
Qing Kay LiDepartment of Pathology, Johns Hopkins University, Baltimore, MD 21231, USA.
Lin S ChenDepartment of Public Health Sciences, University of Chicago, Chicago, IL 60637, USA.
Umut OzbekDepartment of Population Health Science and Policy, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA; Tisch Cancer Institute, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
Suhas VasaikarDepartment of Translational Molecular Pathology, MD Anderson Cancer Center, Houston, TX 77030, USA.
Yige WuWashington University School of Medicine, St. Louis, MO 63110, USA.
Seungyeul YooDepartment of Genetics and Genomic Sciences and Icahn Institute for Data Science and Genomic Technology, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
Shrabanti ChowdhuryDepartment of Genetics and Genomic Sciences and Icahn Institute for Data Science and Genomic Technology, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
Matthew A WyczalkowskiWashington University School of Medicine, St. Louis, MO 63110, USA.
Jiayi JiDepartment of Population Health Science and Policy, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA; Tisch Cancer Institute, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
Michael SchnaubeltDepartment of Pathology, Johns Hopkins University, Baltimore, MD 21231, USA.
Andy KongDepartment of Pathology, University of Michigan, Ann Arbor, MI 48109, USA.
Sunantha SethuramanWashington University School of Medicine, St. Louis, MO 63110, USA.
Dmitry M AvtonomovDepartment of Pathology, University of Michigan, Ann Arbor, MI 48109, USA.
Minghui AoDepartment of Pathology, Johns Hopkins University, Baltimore, MD 21231, USA.
Antonio ColapricoDepartment of Public Health Sciences, University of Miami Miller School of Medicine, Miami, FL 33136, USA.
Song CaoWashington University School of Medicine, St. Louis, MO 63110, USA.
Kyung-Cho ChoDepartment of Pathology, Johns Hopkins University, Baltimore, MD 21231, USA.
Selim KalayciDepartment of Genetics and Genomic Sciences and Icahn Institute for Data Science and Genomic Technology, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
Shiyong MaDepartment of Pathology, Johns Hopkins University, Baltimore, MD 21231, USA.
Wenke LiuInstitute for Systems Genetics and Department of Biochemistry and Molecular Pharmacology, New York University School of Medicine, New York, NY 10016, USA.
Kelly RugglesDepartment of Medicine, New York University School of Medicine, New York, NY 10016, USA.
Anna CalinawanDepartment of Genetics and Genomic Sciences and Icahn Institute for Data Science and Genomic Technology, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
Zeynep H GümüşDepartment of Genetics and Genomic Sciences and Icahn Institute for Data Science and Genomic Technology, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
Daniel GeiszlerDepartment of Computational Medicine and Bioinformatics, University of Michigan, Ann Arbor, MI 48109, USA.
Emily KawalerInstitute for Systems Genetics and Department of Biochemistry and Molecular Pharmacology, New York University School of Medicine, New York, NY 10016, USA.
Guo Ci TeoDepartment of Pathology, University of Michigan, Ann Arbor, MI 48109, USA.
Bo WenLester and Sue Smith Breast Center, Baylor College of Medicine, Houston, TX 77030, USA.
Yuping ZhangDepartment of Pathology, University of Michigan, Ann Arbor, MI 48109, USA.
Sarah KeeganInstitute for Systems Genetics and Department of Biochemistry and Molecular Pharmacology, New York University School of Medicine, New York, NY 10016, USA.
Kai LiLester and Sue Smith Breast Center, Baylor College of Medicine, Houston, TX 77030, USA.
Feng ChenDepartments of Medicine and Cell Biology and Physiology, Washington University School of Medicine, St. Louis, MO 63110, USA.
Nathan EdwardsDepartment of Biochemistry and Cellular Biology, Georgetown University, Washington, DC 20007, USA.
Phillip M PierorazioBrady Urological Institute and Department of Urology, Johns Hopkins University, Baltimore, MD 21231, USA.
Xi Steven ChenDepartment of Public Health Sciences, University of Miami Miller School of Medicine, Miami, FL 33136, USA; Sylvester Comprehensive Cancer Center, University of Miami Miller School of Medicine, Miami, FL 33136, USA.
Christian P PavlovichBrady Urological Institute and Department of Urology, Johns Hopkins University, Baltimore, MD 21231, USA.
A Ari HakimiDepartment of Surgery, Urology Service, Memorial Sloan Kettering Cancer Center, New York, NY 10065, USA.
Gabriel BrominskiDepartment of Urology, Poznań University of Medical Sciences, Szwajcarska 3, Poznań 61-285, Poland.
James J HsiehDepartment of Medicine, Washington University School of Medicine, St. Louis, MO 63110, USA.
Andrzej AntczakDepartment of Urology, Poznań University of Medical Sciences, Szwajcarska 3, Poznań 61-285, Poland.
Tatiana OmelchenkoSloan Kettering Institute, Memorial Sloan Kettering Cancer Center, New York, NY 10065, USA.
Jan LubinskiDepartment of Genetics and Pathology, Pomeranian Medical University, Szczecin 71-252, Poland.
Maciej WiznerowiczInternational Institute for Molecular Oncology, Poznań 60-203, Poland; Poznań University of Medical Sciences, Poznan 60-701, Poland.
W Marston LinehanUrologic Oncology Branch, Center for Cancer Research, National Cancer Institute, National Institutes of Health, Bethesda, MD 20892, USA.
Christopher R KinsingerOffice of Cancer Clinical Proteomics Research, National Cancer Institute, Bethesda, MD 20892, USA.
Mathangi ThiagarajanFrederick National Laboratory for Cancer Research, Frederick, MD 21702, USA.
Emily S BojaOffice of Cancer Clinical Proteomics Research, National Cancer Institute, Bethesda, MD 20892, USA.
Mehdi MesriOffice of Cancer Clinical Proteomics Research, National Cancer Institute, Bethesda, MD 20892, USA.
Tara HiltkeOffice of Cancer Clinical Proteomics Research, National Cancer Institute, Bethesda, MD 20892, USA.
Ana I RoblesOffice of Cancer Clinical Proteomics Research, National Cancer Institute, Bethesda, MD 20892, USA.
Henry RodriguezOffice of Cancer Clinical Proteomics Research, National Cancer Institute, Bethesda, MD 20892, USA.
Jiang QianDepartment of Ophthalmology, Johns Hopkins University, Baltimore, MD 21231, USA.
David FenyöInstitute for Systems Genetics and Department of Biochemistry and Molecular Pharmacology, New York University School of Medicine, New York, NY 10016, USA.
Bing ZhangLester and Sue Smith Breast Center, Baylor College of Medicine, Houston, TX 77030, USA; Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX 77030, USA.
Li DingWashington University School of Medicine, St. Louis, MO 63110, USA.
Eric SchadtDepartment of Genetics and Genomic Sciences and Icahn Institute for Data Science and Genomic Technology, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA; Sema4, Stamford, CT 06902, USA.
Arul M ChinnaiyanDepartment of Pathology, University of Michigan, Ann Arbor, MI 48109, USA.
Zhen ZhangDepartment of Pathology, Johns Hopkins University, Baltimore, MD 21231, USA.
Gilbert S OmennDepartment of Computational Medicine and Bioinformatics, University of Michigan, Ann Arbor, MI 48109, USA; Department of Internal Medicine, Human Genetics, and School of Public Health, University of Michigan, Ann Arbor, MI 48109, USA.
Marcin CieslikDepartment of Pathology, University of Michigan, Ann Arbor, MI 48109, USA. Electronic address: mcieslik@med.mich.edu.
Daniel W ChanDepartment of Pathology, Johns Hopkins University, Baltimore, MD 21231, USA. Electronic address: dchan@jhmi.edu.
Alexey I NesvizhskiiDepartment of Pathology, University of Michigan, Ann Arbor, MI 48109, USA. Electronic address: nesvi@med.umich.edu.
Pei WangDepartment of Genetics and Genomic Sciences and Icahn Institute for Data Science and Genomic Technology, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA. Electronic address: pei.wang@mssm.edu.
Hui ZhangDepartment of Pathology, Johns Hopkins University, Baltimore, MD 21231, USA. Electronic address: huizhang@jhu.edu.
Clinical Proteomic Tumor Analysis Consortium
Funding
X-RAY CRYSTALLOGRAPHYP30CA008748 · NCI · SLOAN-KETTERING INSTITUTE FOR CANCER RES · PI Hongbiao Carl Lekaye · 1985 to 2026
$347.4MThe Comprehensive Proteome Characterization Center at Johns Hopkins: High Precision Discovery and Confirmation of Genoproteomic TargetsU24CA210985 · NCI · JOHNS HOPKINS UNIVERSITY · PI CHAN, DANIEL WANYUI, ZHANG, HUI · 2016 to 2020
$5.3MPNNL Proteome Characterization CenterU24CA210955 · NCI · BATTELLE PACIFIC NORTHWEST LABORATORIES · PI LIU, TAO, SMITH, RICHARD D · 2016 to 2020
$5.3MiPGDAC, An Integrative Proteogenomic Data Analysis Center for CPTACU24CA210954 · NCI · BAYLOR COLLEGE OF MEDICINE · PI ZHANG, BING · 2016 to 2020
$4.9MSystems Biology based Proteogenomic Translator for Cancer Marker Discovery towards Precision MedicineU24CA210993 · NCI · ICAHN SCHOOL OF MEDICINE AT MOUNT SINAI · PI SCHADT, ERIC E, WANG, PEI · 2016 to 2020
$4.6MUniversity of Michigan Proteogenomics Data Analysis CenterU24CA210967 · NCI · UNIVERSITY OF MICHIGAN AT ANN ARBOR · PI CHINNAIYAN, ARUL M, DHANASEKARAN, SARAVANA M · 2016 to 2020
$4.1MProteogenomics of Cancer Training ProgramT32CA140044 · NCI · UNIVERSITY OF MICHIGAN AT ANN ARBOR · PI RAO, ARVIND, SARTOR, MAUREEN AGNES · 2010 to 2024
$3.9MProteogenomic Data Analysis for Cancer Systems Biology and Clinical TranslationU24CA210972 · NCI · NEW YORK UNIVERSITY SCHOOL OF MEDICINE · PI DING, LI, FENYO, DAVID · 2016 to 2020
$3.3MIntegrative multivariate association and genomic analysesR01GM108711 · NIGMS · UNIVERSITY OF CHICAGO · PI CHEN, LIN · 2014 to 2022
$3.1MNCI NIH HHS P30 CA008748NCI NIH HHS T32 CA140044NCI NIH HHS U24 CA210954NCI NIH HHS U24 CA210955NCI NIH HHS U24 CA210967NCI NIH HHS U24 CA210972NCI NIH HHS U24 CA210985NCI NIH HHS U24 CA210993NIGMS NIH HHS R01 GM108711
Abstract
To elucidate the deregulated functional modules that drive clear cell renal cell carcinoma (ccRCC), we performed comprehensive genomic, epigenomic, transcriptomic, proteomic, and phosphoproteomic characterization of treatment-naive ccRCC and paired normal adjacent tissue samples. Genomic analyses identified a distinct molecular subgroup associated with genomic instability. Integration of proteogenomic measurements uniquely identified protein dysregulation of cellular mechanisms impacted by genomic alterations, including oxidative phosphorylation-related metabolism, protein translation processes, and phospho-signaling modules. To assess the degree of immune infiltration in individual tumors, we identified microenvironment cell signatures that delineated four immune-based ccRCC subtypes characterized by distinct cellular pathways. This study reports a large-scale proteogenomic analysis of ccRCC to discern the functional impact of genomic alterations and provides evidence for rational treatment selection stemming from ccRCC pathobiology.
Indexed as
ProteogenomicsAdultAgedAged, 80 and overBiomarkers, TumorCarcinoma, Renal CellDisease-Free SurvivalExomeExome SequencingFemaleGene Expression Regulation, NeoplasticGenome, HumanHumansMaleMiddle AgedNeoplasm ProteinsBiomarkers, TumorNeoplasm ProteinsccRCCchromosomal translocationCPTACdrug targetsimmune infiltrationphosphoproteomicsproteogenomicsproteomicsrenal carcinomatumor microenvironment
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