PRDM10 RCC: A Birt-Hogg-Dubé-like Syndrome Associated With Lipoma and Highly Penetrant, Aggressive Renal Tumors Morphologically Resembling Type 2 Papillary Renal Cell Carcinoma

Urology. 2023 Sep:179:58-70. doi: 10.1016/j.urology.2023.04.035. Epub 2023 Jun 16.

Abstract

Objective: To characterize the clinical manifestations and genetic basis of a familial cancer syndrome in patients with lipomas and Birt-Hogg-Dubé-like clinical manifestations including fibrofolliculomas and trichodiscomas and kidney cancer.

Methods: Genomic analysis of blood and renal tumor DNA was performed. Inheritance pattern, phenotypic manifestations, and clinical and surgical management were documented. Cutaneous, subcutaneous, and renal tumor pathologic features were characterized.

Results: Affected individuals were found to be at risk for a highly penetrant and lethal form of bilateral, multifocal papillary renal cell carcinoma. Whole genome sequencing identified a germline pathogenic variant in PRDM10 (c.2029 T>C, p.Cys677Arg), which cosegregated with disease. PRDM10 loss of heterozygosity was identified in kidney tumors. PRDM10 was predicted to abrogate expression of FLCN, a transcriptional target of PRDM10, which was confirmed by tumor expression of GPNMB, a TFE3/TFEB target and downstream biomarker of FLCN loss. In addition, a sporadic papillary RCC from the TCGA cohort was identified with a somatic PRDM10 mutation.

Conclusion: We identified a germline PRDM10 pathogenic variant in association with a highly penetrant, aggressive form of familial papillary RCC, lipomas, and fibrofolliculomas/trichodiscomas. PRDM10 loss of heterozygosity and elevated GPNMB expression in renal tumors indicate that PRDM10 alteration leads to reduced FLCN expression, driving TFE3-induced tumor formation. These findings suggest that individuals with Birt-Hogg-Dubé-like manifestations and subcutaneous lipomas, but without a germline pathogenic FLCN variant, should be screened for germline PRDM10 variants. Importantly, kidney tumors identified in patients with a pathogenic PRDM10 variant should be managed with surgical resection instead of active surveillance.

MeSH terms

  • Basic Helix-Loop-Helix Leucine Zipper Transcription Factors
  • Birt-Hogg-Dube Syndrome* / complications
  • Birt-Hogg-Dube Syndrome* / genetics
  • Birt-Hogg-Dube Syndrome* / pathology
  • Carcinoma, Renal Cell* / complications
  • Carcinoma, Renal Cell* / genetics
  • DNA-Binding Proteins
  • Humans
  • Kidney Neoplasms* / genetics
  • Kidney Neoplasms* / pathology
  • Lipoma* / complications
  • Lipoma* / genetics
  • Membrane Glycoproteins
  • Proto-Oncogene Proteins / genetics
  • Proto-Oncogene Proteins / metabolism
  • Skin Neoplasms*
  • Transcription Factors / genetics

Substances

  • Proto-Oncogene Proteins
  • Transcription Factors
  • Basic Helix-Loop-Helix Leucine Zipper Transcription Factors
  • PRDM10 protein, human
  • DNA-Binding Proteins
  • GPNMB protein, human
  • Membrane Glycoproteins

Supplementary concepts

  • Papillary renal cell carcinoma, sporadic