Extensive genotype-phenotype heterogeneity in renal cell carcinoma - a proof-of-concept study

BackgroundRenal cell carcinoma (RCC) is characterized by a high degree of genomic but also functional intratumoral heterogeneity (ITH). Mutations in VHL, chromatin remodeling genes such as SETD2 and genes that regulate the PI3K/AKT/mTOR pathway have been identified as recurrent drivers despite genom...

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Main Authors: Jakob Wieke, Christina Jurcic, Adam Kaczorowski, Sarah Böning, Martina Kirchner, Constantin Schwab, Viktoria Schütz, Markus Hohenfellner, Anette Duensing, Albrecht Stenzinger, Stefan Duensing
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Language:English
Published: Frontiers Media S.A. 2025-04-01
Series:Frontiers in Oncology
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Online Access:https://www.frontiersin.org/articles/10.3389/fonc.2025.1551077/full
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author Jakob Wieke
Christina Jurcic
Adam Kaczorowski
Sarah Böning
Martina Kirchner
Constantin Schwab
Viktoria Schütz
Markus Hohenfellner
Anette Duensing
Albrecht Stenzinger
Stefan Duensing
author_facet Jakob Wieke
Christina Jurcic
Adam Kaczorowski
Sarah Böning
Martina Kirchner
Constantin Schwab
Viktoria Schütz
Markus Hohenfellner
Anette Duensing
Albrecht Stenzinger
Stefan Duensing
author_sort Jakob Wieke
collection DOAJ
description BackgroundRenal cell carcinoma (RCC) is characterized by a high degree of genomic but also functional intratumoral heterogeneity (ITH). Mutations in VHL, chromatin remodeling genes such as SETD2 and genes that regulate the PI3K/AKT/mTOR pathway have been identified as recurrent drivers despite genomic ITH. Whether and to what extent these mutations shape functional ITH including the formation of spatial niches is incompletely understood. Herein, we analyze the correlation between mutational drivers and their functional proxies in a spatially defined manner.MethodsA total of 23 RCCs were analyzed by panel next-generation sequencing followed by immunohistochemistry for five functional proxies for key genetic alterations including the expression of CD31, GLUT1, phospho-mTOR S2448, H3K36me3 and Ki-67. Antibody stainings were scored semiquantitatively in the tumor periphery and the tumor center.ResultsUnexpectedly, the presence of a VHL mutation was not found to correlate with its functional proxies including the expression of CD31/microvessel density or the expression of the glucose transporter GLUT1. Likewise, there was no correlation between the presence of activating mutations in genes of the PI3K/AKT/mTOR pathway and the expression of activated phospho-mTOR S2448. Furthermore, mutations in the methyltransferase gene SETD2 were not found to correlate with the expression level of its downstream target H3K36me3. Lastly, there was no correlation between the expression of the proliferation marker Ki-67 and the number of driver mutations.ConclusionThis proof-of-concept study adds genotype-phenotype heterogeneity as additional layer of complexity to the known genomic and functional ITH in RCC.
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spelling doaj-art-caa5890e35a84d1ba448001ea1a2b6382025-08-20T02:18:34ZengFrontiers Media S.A.Frontiers in Oncology2234-943X2025-04-011510.3389/fonc.2025.15510771551077Extensive genotype-phenotype heterogeneity in renal cell carcinoma - a proof-of-concept studyJakob Wieke0Christina Jurcic1Adam Kaczorowski2Sarah Böning3Martina Kirchner4Constantin Schwab5Viktoria Schütz6Markus Hohenfellner7Anette Duensing8Albrecht Stenzinger9Stefan Duensing10Molecular Urooncology, Department of Urology, University Hospital Heidelberg, Heidelberg, GermanyMolecular Urooncology, Department of Urology, University Hospital Heidelberg, Heidelberg, GermanyMolecular Urooncology, Department of Urology, University Hospital Heidelberg, Heidelberg, GermanyMolecular Urooncology, Department of Urology, University Hospital Heidelberg, Heidelberg, GermanyInstitute of Pathology, University Hospital Heidelberg, Heidelberg, GermanyInstitute of Pathology, University Hospital Heidelberg, Heidelberg, GermanyDepartment of Urology, University Hospital Heidelberg, and National Center for Tumor Diseases (NCT), Heidelberg, GermanyDepartment of Urology, University Hospital Heidelberg, and National Center for Tumor Diseases (NCT), Heidelberg, GermanyPrecision Oncology of Urological Malignancies, Department of Urology, University Hospital Heidelberg, Heidelberg, GermanyInstitute of Pathology, University Hospital Heidelberg, Heidelberg, GermanyMolecular Urooncology, Department of Urology, University Hospital Heidelberg, Heidelberg, GermanyBackgroundRenal cell carcinoma (RCC) is characterized by a high degree of genomic but also functional intratumoral heterogeneity (ITH). Mutations in VHL, chromatin remodeling genes such as SETD2 and genes that regulate the PI3K/AKT/mTOR pathway have been identified as recurrent drivers despite genomic ITH. Whether and to what extent these mutations shape functional ITH including the formation of spatial niches is incompletely understood. Herein, we analyze the correlation between mutational drivers and their functional proxies in a spatially defined manner.MethodsA total of 23 RCCs were analyzed by panel next-generation sequencing followed by immunohistochemistry for five functional proxies for key genetic alterations including the expression of CD31, GLUT1, phospho-mTOR S2448, H3K36me3 and Ki-67. Antibody stainings were scored semiquantitatively in the tumor periphery and the tumor center.ResultsUnexpectedly, the presence of a VHL mutation was not found to correlate with its functional proxies including the expression of CD31/microvessel density or the expression of the glucose transporter GLUT1. Likewise, there was no correlation between the presence of activating mutations in genes of the PI3K/AKT/mTOR pathway and the expression of activated phospho-mTOR S2448. Furthermore, mutations in the methyltransferase gene SETD2 were not found to correlate with the expression level of its downstream target H3K36me3. Lastly, there was no correlation between the expression of the proliferation marker Ki-67 and the number of driver mutations.ConclusionThis proof-of-concept study adds genotype-phenotype heterogeneity as additional layer of complexity to the known genomic and functional ITH in RCC.https://www.frontiersin.org/articles/10.3389/fonc.2025.1551077/fullrenal cell carcinomatumor heterogeneitygenotypephenotypeVHLmTOR
spellingShingle Jakob Wieke
Christina Jurcic
Adam Kaczorowski
Sarah Böning
Martina Kirchner
Constantin Schwab
Viktoria Schütz
Markus Hohenfellner
Anette Duensing
Albrecht Stenzinger
Stefan Duensing
Extensive genotype-phenotype heterogeneity in renal cell carcinoma - a proof-of-concept study
Frontiers in Oncology
renal cell carcinoma
tumor heterogeneity
genotype
phenotype
VHL
mTOR
title Extensive genotype-phenotype heterogeneity in renal cell carcinoma - a proof-of-concept study
title_full Extensive genotype-phenotype heterogeneity in renal cell carcinoma - a proof-of-concept study
title_fullStr Extensive genotype-phenotype heterogeneity in renal cell carcinoma - a proof-of-concept study
title_full_unstemmed Extensive genotype-phenotype heterogeneity in renal cell carcinoma - a proof-of-concept study
title_short Extensive genotype-phenotype heterogeneity in renal cell carcinoma - a proof-of-concept study
title_sort extensive genotype phenotype heterogeneity in renal cell carcinoma a proof of concept study
topic renal cell carcinoma
tumor heterogeneity
genotype
phenotype
VHL
mTOR
url https://www.frontiersin.org/articles/10.3389/fonc.2025.1551077/full
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