The Genomic Landscape of Renal Oncocytoma Identifies a Metabolic Barrier to Tumorigenesis

Cell Rep. 2015 Dec 1;13(9):1895-908. doi: 10.1016/j.celrep.2015.10.059. Epub 2015 Nov 19.

Abstract

Oncocytomas are predominantly benign neoplasms possessing pathogenic mitochondrial mutations and accumulation of respiration-defective mitochondria, characteristics of unknown significance. Using exome and transcriptome sequencing, we identified two main subtypes of renal oncocytoma. Type 1 is diploid with CCND1 rearrangements, whereas type 2 is aneuploid with recurrent loss of chromosome 1, X or Y, and/or 14 and 21, which may proceed to more aggressive eosinophilic chromophobe renal cell carcinoma (ChRCC). Oncocytomas activate 5' adenosine monophosphate-activated protein kinase (AMPK) and Tp53 (p53) and display disruption of Golgi and autophagy/lysosome trafficking, events attributed to defective mitochondrial function. This suggests that the genetic defects in mitochondria activate a metabolic checkpoint, producing autophagy impairment and mitochondrial accumulation that limit tumor progression, revealing a novel tumor-suppressive mechanism for mitochondrial inhibition with metformin. Alleviation of this metabolic checkpoint in type 2 by p53 mutations may allow progression to eosinophilic ChRCC, indicating that they represent higher risk.

Keywords: cancer genomics; cancer metabolism; lysosome; mitochondria; oncocytoma.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • AMP-Activated Protein Kinases / genetics
  • AMP-Activated Protein Kinases / metabolism
  • Adenoma, Oxyphilic / genetics
  • Adenoma, Oxyphilic / metabolism
  • Adenoma, Oxyphilic / pathology*
  • Autophagy / drug effects
  • Carcinoma, Renal Cell / genetics
  • Carcinoma, Renal Cell / metabolism
  • Carcinoma, Renal Cell / pathology
  • Cathepsins / metabolism
  • Cell Transformation, Neoplastic*
  • Cyclin D1 / genetics
  • Cyclin D1 / metabolism
  • DNA Copy Number Variations
  • Female
  • Golgi Apparatus / metabolism
  • Humans
  • Karyotype
  • Kidney / metabolism
  • Kidney / pathology
  • Kidney Neoplasms / genetics
  • Kidney Neoplasms / metabolism
  • Kidney Neoplasms / pathology*
  • Lysosomal Membrane Proteins / metabolism
  • Lysosomes / metabolism
  • Male
  • Metformin / pharmacology
  • Mitochondria / drug effects
  • Mitochondria / metabolism
  • Sequence Analysis, RNA
  • Transcriptome
  • Tumor Suppressor Protein p53 / genetics
  • Tumor Suppressor Protein p53 / metabolism

Substances

  • CCND1 protein, human
  • LAMP1 protein, human
  • Lysosomal Membrane Proteins
  • Tumor Suppressor Protein p53
  • Cyclin D1
  • Metformin
  • AMP-Activated Protein Kinases
  • Cathepsins

Supplementary concepts

  • Oncocytoma, renal

Associated data

  • SRA/SRP051509