Molecular Characterization of TFE3-rearranged Renal Cell Carcinoma, A Comparative Study with Papillary and Clear Cell Renal Cell Carcinomas - Beyond the Abstract

TFE3-rearranged renal cell carcinoma (rRCC) is a rare subtype of renal cell carcinoma. TFE3 fusion genes of this carcinoma can have a variety of gene fusion partners, including ASPL (ASPSCR1), EWSR1, CLTC, DVL2, FUBP1, GRIPAP1, KAT6A, KHDRBS2, KHSRP, LUC7L3, MED15, NEAT1, NONO, PARP14, PRCC, RBM10, SETD1B, SFPQ and ZC3H42.

The TFE3 gene fusions preserve functional domains of TFE3 proteins, suggesting that chimeric TFE3 proteins can function as oncogenic transcription factors. It was reported that the TFE3 fusion was sufficient for tumorigenesis in a mouse model. However, there is limited knowledge of co-alterations that occur along with TFE3 fusions. Although rRCC has a unique morphology, immunophenotype, and fusion gene, patients are typically treated with therapy developed for clear cell renal cell carcinoma (ccRCC). Furthermore, it is not uncommon for rRCC to be incorrectly diagnosed as ccRCC or papillary renal cell carcinoma (pRCC). In this study, we use a comprehensive molecular approach to compare the genomic, transcriptomic, and immunological landscape of rRCC, pRCC, and ccRCC.

Method and Specimens:
Next-generation sequencing of RNA (whole transcriptome) and DNA (592-gene panel or whole exome) for rRCC (N=20), pRCC (N=20), and ccRCC samples (N=392) was performed.

Results:
  1. rRCC patients were significantly younger and more frequently female (median 44.5 years (y), 75.0% female) as compared to pRCC (68.5 y, 25.0% female; p < 0.05) and ccRCC (62.0 y, 27.8% female; p < 0.05).
  2. A total of 8 unique fusion partners were observed, including a novel fusion with SRRM2::TFE3 in two patients.
  3. ccRCC exhibited significantly higher mutation rates of VHL (0% rRCC, 0% pRCC, 78.7% ccRCC; p<0.05) and PBMR1 (0% rRCC, 5.0% pRCC, 49.4% ccRCC; p<0.05). The genomic landscapes of rRCC were sparse with no mutations occurring with a prevalence higher than 10% other than pTERT (18.2% rRCC, 0% pRCC, 9.2% ccRCC).
  4. Gene set enrichment analysis showed rRCC are enriched in genes related to oxidative phosphorylation when compared to both ccRCC and pRCC.
  5. rRCC was associated with significantly fewer M1 macrophages (0.8%) as compared to pRCC (1.4%) and ccRCC (2.7%) (p < 0.05), suggesting a cold tumor immune microenvironment (TME). However, rRCC were more commonly PD-L1+ (rRCC 50%, pRCC 19.0%, ccRCC 12.2%; p < 0.05). The results suggest a potential benefit from immune checkpoint inhibitor (ICI) therapy.
Take home message:
rRCC patients were significantly younger and more frequently female compared to pRCC and ccRCC. rRCC didn’t have the commonly mutated genes found in pRCC and ccRCC. rRCC were more commonly PD-L1+, which suggests a potential benefit from immune checkpoint inhibitor therapy.

Written by: Shuanzeng Wei,1 Daniel M. Geynisman,2 Alexander Kutikov,3 Robert G. Uzzo3

  1. Department of Pathology, Fox Chase Cancer Center, Philadelphia, PA, USA
  2. Department of Oncology, Fox Chase Cancer Center, Philadelphia, PA, USA
  3. Department of Urology, Fox Chase Cancer Center, Philadelphia, PA, USA
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