Molecular characterization of chromophobe renal cell carcinoma reveals mTOR pathway alterations in patients with poor outcome

Chromophobe renal cell carcinoma (chRCC) is a histologically and molecularly distinct class of rare renal tumor. TCGA studies revealed low mutational burden, with only TP53 and PTEN recurrently mutated, and discovered alterations in TERT promoter and in the electron transport chain Complex I genes....

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Published inModern pathology Vol. 33; no. 12; pp. 2580 - 2590
Main Authors Roldan-Romero, Juan María, Santos, María, Lanillos, Javier, Caleiras, Eduardo, Anguera, Georgia, Maroto, Pablo, García-Donas, Jesús, de Velasco, Guillermo, Martinez-Montes, Ángel Mario, Calsina, Bruna, Monteagudo, María, Letón, Rocío, Leandro-García, Luis Javier, Montero-Conde, Cristina, Cascón, Alberto, Robledo, Mercedes, Rodriguez-Antona, Cristina
Format Journal Article
LanguageEnglish
Published New York Elsevier Inc 01.12.2020
Nature Publishing Group US
Elsevier Limited
Subjects
13/105
13/51
38/23
631/1647/514/2254
692/308/575
692/420/2489/68
692/53/2422
Adult
Aged
Aged, 80 and over
Biomarkers, Tumor - analysis
Biomarkers, Tumor - genetics
Carcinoma, Renal Cell - chemistry
Carcinoma, Renal Cell - genetics
Carcinoma, Renal Cell - pathology
Carcinoma, Renal Cell - therapy
DNA Mutational Analysis
Electron transport chain
Female
Genetic Predisposition to Disease
Genomics
High-Throughput Nucleotide Sequencing
Humans
Immunohistochemistry
Kidney cancer
Kidney Neoplasms - chemistry
Kidney Neoplasms - genetics
Kidney Neoplasms - pathology
Kidney Neoplasms - therapy
Laboratory Medicine
Leukocytes (eosinophilic)
Male
Medical prognosis
Medicine
Medicine & Public Health
Metastases
Metastasis
Middle Aged
Mitochondria
Mutation
p53 Protein
Pathology
Phenotype
Phosphorylation
PTEN Phosphohydrolase - analysis
PTEN protein
Renal cell carcinoma
Ribosomal Protein S6 Kinases - analysis
Survival analysis
Telomeres
Therapeutic targets
TOR protein
TOR Serine-Threonine Kinases - genetics
Tuberous Sclerosis Complex 1
Tuberous Sclerosis Complex 1 Protein - genetics
Tuberous Sclerosis Complex 2
Tuberous Sclerosis Complex 2 Protein - analysis
Tuberous Sclerosis Complex 2 Protein - genetics
Tumor Suppressor Protein p53 - genetics
Tumors
Online AccessGet full text
ISSN0893-3952
1530-0285
1530-0285
DOI10.1038/s41379-020-0607-z

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Abstract Chromophobe renal cell carcinoma (chRCC) is a histologically and molecularly distinct class of rare renal tumor. TCGA studies revealed low mutational burden, with only TP53 and PTEN recurrently mutated, and discovered alterations in TERT promoter and in the electron transport chain Complex I genes. However, knowledge on drug targetable genes is limited and treatments at metastatic stage do not follow a molecular rationale. In a large series of 92 chRCC enriched with metastatic cases, we performed an in-depth characterization of mTOR pathway alterations through targeted NGS and immunohistochemistry (IHC) of phospho-S6, tuberin, and PTEN. Mutations in mitochondria, telomere maintenance and other renal cancer related genes and p53 IHC, were also assessed. The impact on metastasis development and disease specific survival was determined, using TCGA-KICH series (n = 65) for validation. mTOR pathway mutations (MTOR, TSC1, TSC2) were present in 17% of primary tumors, most of them being classified as pathogenic. Mutations were associated with positive IHC staining of phospho-S6 and PTEN (P = 0.009 and P = 0.001, respectively) and with chRCC eosinophilic variant (P = 0.039), supporting a biological relevance of the pathway. mTOR pathway mutations were associated with worse clinical outcomes. Survival analysis gave a hazard ratio of 5.5 (P = 0.027), and this association was confirmed in TCGA-KICH (HR = 10.3, P = 0.006). TP53 mutations were enriched in metastatic cases (P = 0.018), and mutations in telomere maintenance genes showed a trend in the same direction. p53 IHC staining pattern was associated with the underlying TP53 defect, and negative PTEN IHC staining (82% of cases) suggested PTEN loss as a chRCC hallmark. In conclusion, our study provides with novel genomic knowledge in chRCC and identifies novel markers of poor survival. Furthermore, this is the first study showing that mTOR pathway mutations correlate with poor prognosis, and may help to identify patients with increased sensitivity to mTOR inhibitors.
AbstractList Chromophobe renal cell carcinoma (chRCC) is a histologically and molecularly distinct class of rare renal tumor. TCGA studies revealed low mutational burden, with only TP53 and PTEN recurrently mutated, and discovered alterations in TERT promoter and in the electron transport chain Complex I genes. However, knowledge on drug targetable genes is limited and treatments at metastatic stage do not follow a molecular rationale. In a large series of 92 chRCC enriched with metastatic cases, we performed an in-depth characterization of mTOR pathway alterations through targeted NGS and immunohistochemistry (IHC) of phospho-S6, tuberin, and PTEN. Mutations in mitochondria, telomere maintenance and other renal cancer related genes and p53 IHC, were also assessed. The impact on metastasis development and disease specific survival was determined, using TCGA-KICH series (n = 65) for validation. mTOR pathway mutations (MTOR, TSC1, TSC2) were present in 17% of primary tumors, most of them being classified as pathogenic. Mutations were associated with positive IHC staining of phospho-S6 and PTEN (P = 0.009 and P = 0.001, respectively) and with chRCC eosinophilic variant (P = 0.039), supporting a biological relevance of the pathway. mTOR pathway mutations were associated with worse clinical outcomes. Survival analysis gave a hazard ratio of 5.5 (P = 0.027), and this association was confirmed in TCGA-KICH (HR = 10.3, P = 0.006). TP53 mutations were enriched in metastatic cases (P = 0.018), and mutations in telomere maintenance genes showed a trend in the same direction. p53 IHC staining pattern was associated with the underlying TP53 defect, and negative PTEN IHC staining (82% of cases) suggested PTEN loss as a chRCC hallmark. In conclusion, our study provides with novel genomic knowledge in chRCC and identifies novel markers of poor survival. Furthermore, this is the first study showing that mTOR pathway mutations correlate with poor prognosis, and may help to identify patients with increased sensitivity to mTOR inhibitors.Chromophobe renal cell carcinoma (chRCC) is a histologically and molecularly distinct class of rare renal tumor. TCGA studies revealed low mutational burden, with only TP53 and PTEN recurrently mutated, and discovered alterations in TERT promoter and in the electron transport chain Complex I genes. However, knowledge on drug targetable genes is limited and treatments at metastatic stage do not follow a molecular rationale. In a large series of 92 chRCC enriched with metastatic cases, we performed an in-depth characterization of mTOR pathway alterations through targeted NGS and immunohistochemistry (IHC) of phospho-S6, tuberin, and PTEN. Mutations in mitochondria, telomere maintenance and other renal cancer related genes and p53 IHC, were also assessed. The impact on metastasis development and disease specific survival was determined, using TCGA-KICH series (n = 65) for validation. mTOR pathway mutations (MTOR, TSC1, TSC2) were present in 17% of primary tumors, most of them being classified as pathogenic. Mutations were associated with positive IHC staining of phospho-S6 and PTEN (P = 0.009 and P = 0.001, respectively) and with chRCC eosinophilic variant (P = 0.039), supporting a biological relevance of the pathway. mTOR pathway mutations were associated with worse clinical outcomes. Survival analysis gave a hazard ratio of 5.5 (P = 0.027), and this association was confirmed in TCGA-KICH (HR = 10.3, P = 0.006). TP53 mutations were enriched in metastatic cases (P = 0.018), and mutations in telomere maintenance genes showed a trend in the same direction. p53 IHC staining pattern was associated with the underlying TP53 defect, and negative PTEN IHC staining (82% of cases) suggested PTEN loss as a chRCC hallmark. In conclusion, our study provides with novel genomic knowledge in chRCC and identifies novel markers of poor survival. Furthermore, this is the first study showing that mTOR pathway mutations correlate with poor prognosis, and may help to identify patients with increased sensitivity to mTOR inhibitors.
Chromophobe renal cell carcinoma (chRCC) is a histologically and molecularly distinct class of rare renal tumor. TCGA studies revealed low mutational burden, with only TP53 and PTEN recurrently mutated, and discovered alterations in TERT promoter and in the electron transport chain Complex I genes. However, knowledge on drug targetable genes is limited and treatments at metastatic stage do not follow a molecular rationale. In a large series of 92 chRCC enriched with metastatic cases, we performed an in-depth characterization of mTOR pathway alterations through targeted NGS and immunohistochemistry (IHC) of phospho-S6, tuberin, and PTEN. Mutations in mitochondria, telomere maintenance and other renal cancer related genes and p53 IHC, were also assessed. The impact on metastasis development and disease specific survival was determined, using TCGA-KICH series (n = 65) for validation. mTOR pathway mutations (MTOR, TSC1, TSC2) were present in 17% of primary tumors, most of them being classified as pathogenic. Mutations were associated with positive IHC staining of phospho-S6 and PTEN (P = 0.009 and P = 0.001, respectively) and with chRCC eosinophilic variant (P = 0.039), supporting a biological relevance of the pathway. mTOR pathway mutations were associated with worse clinical outcomes. Survival analysis gave a hazard ratio of 5.5 (P = 0.027), and this association was confirmed in TCGA-KICH (HR = 10.3, P = 0.006). TP53 mutations were enriched in metastatic cases (P = 0.018), and mutations in telomere maintenance genes showed a trend in the same direction. p53 IHC staining pattern was associated with the underlying TP53 defect, and negative PTEN IHC staining (82% of cases) suggested PTEN loss as a chRCC hallmark. In conclusion, our study provides with novel genomic knowledge in chRCC and identifies novel markers of poor survival. Furthermore, this is the first study showing that mTOR pathway mutations correlate with poor prognosis, and may help to identify patients with increased sensitivity to mTOR inhibitors.
Chromophobe renal cell carcinoma (chRCC) is a histologically and molecularly distinct class of rare renal tumor. TCGA studies revealed low mutational burden, with only TP53 and PTEN recurrently mutated, and discovered alterations in TERT promoter and in the electron transport chain Complex I genes. However, knowledge on drug targetable genes is limited and treatments at metastatic stage do not follow a molecular rationale. In a large series of 92 chRCC enriched with metastatic cases, we performed an in-depth characterization of mTOR pathway alterations through targeted NGS and immunohistochemistry (IHC) of phospho-S6, tuberin, and PTEN. Mutations in mitochondria, telomere maintenance and other renal cancer related genes and p53 IHC, were also assessed. The impact on metastasis development and disease specific survival was determined, using TCGA-KICH series ( n  = 65) for validation. mTOR pathway mutations ( MTOR, TSC1 , TSC2 ) were present in 17% of primary tumors, most of them being classified as pathogenic. Mutations were associated with positive IHC staining of phospho-S6 and PTEN ( P  = 0.009 and P  = 0.001, respectively) and with chRCC eosinophilic variant ( P  = 0.039), supporting a biological relevance of the pathway. mTOR pathway mutations were associated with worse clinical outcomes. Survival analysis gave a hazard ratio of 5.5 ( P  = 0.027), and this association was confirmed in TCGA-KICH (HR = 10.3, P  = 0.006). TP53 mutations were enriched in metastatic cases ( P  = 0.018), and mutations in telomere maintenance genes showed a trend in the same direction. p53 IHC staining pattern was associated with the underlying TP53 defect, and negative PTEN IHC staining (82% of cases) suggested PTEN loss as a chRCC hallmark. In conclusion, our study provides with novel genomic knowledge in chRCC and identifies novel markers of poor survival. Furthermore, this is the first study showing that mTOR pathway mutations correlate with poor prognosis, and may help to identify patients with increased sensitivity to mTOR inhibitors.
Author Leandro-García, Luis Javier
García-Donas, Jesús
Santos, María
Letón, Rocío
Cascón, Alberto
Caleiras, Eduardo
Monteagudo, María
Montero-Conde, Cristina
Robledo, Mercedes
Martinez-Montes, Ángel Mario
Anguera, Georgia
Calsina, Bruna
Rodriguez-Antona, Cristina
Lanillos, Javier
Roldan-Romero, Juan María
de Velasco, Guillermo
Maroto, Pablo
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ContentType Journal Article
Copyright 2020 United States & Canadian Academy of Pathology
The Author(s), under exclusive licence to United States & Canadian Academy of Pathology 2020
The Author(s), under exclusive licence to United States & Canadian Academy of Pathology 2020.
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Snippet Chromophobe renal cell carcinoma (chRCC) is a histologically and molecularly distinct class of rare renal tumor. TCGA studies revealed low mutational burden,...
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13/51
38/23
631/1647/514/2254
692/308/575
692/420/2489/68
692/53/2422
Adult
Aged
Aged, 80 and over
Biomarkers, Tumor - analysis
Biomarkers, Tumor - genetics
Carcinoma, Renal Cell - chemistry
Carcinoma, Renal Cell - genetics
Carcinoma, Renal Cell - pathology
Carcinoma, Renal Cell - therapy
DNA Mutational Analysis
Electron transport chain
Female
Genetic Predisposition to Disease
Genomics
High-Throughput Nucleotide Sequencing
Humans
Immunohistochemistry
Kidney cancer
Kidney Neoplasms - chemistry
Kidney Neoplasms - genetics
Kidney Neoplasms - pathology
Kidney Neoplasms - therapy
Laboratory Medicine
Leukocytes (eosinophilic)
Male
Medical prognosis
Medicine
Medicine & Public Health
Metastases
Metastasis
Middle Aged
Mitochondria
Mutation
p53 Protein
Pathology
Phenotype
Phosphorylation
PTEN Phosphohydrolase - analysis
PTEN protein
Renal cell carcinoma
Ribosomal Protein S6 Kinases - analysis
Survival analysis
Telomeres
Therapeutic targets
TOR protein
TOR Serine-Threonine Kinases - genetics
Tuberous Sclerosis Complex 1
Tuberous Sclerosis Complex 1 Protein - genetics
Tuberous Sclerosis Complex 2
Tuberous Sclerosis Complex 2 Protein - analysis
Tuberous Sclerosis Complex 2 Protein - genetics
Tumor Suppressor Protein p53 - genetics
Tumors
Title Molecular characterization of chromophobe renal cell carcinoma reveals mTOR pathway alterations in patients with poor outcome
URI https://dx.doi.org/10.1038/s41379-020-0607-z
https://link.springer.com/article/10.1038/s41379-020-0607-z
https://www.ncbi.nlm.nih.gov/pubmed/32616874
https://www.proquest.com/docview/2473251202
https://www.proquest.com/docview/2420154908
Volume 33
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