Phenotypic variability and risk of malignancy in SDHC-linked paragangliomas: lessons from three unrelated cases with an identical germline mutation (p.Arg133*)

J Clin Endocrinol Metab. 2014 Mar;99(3):E489-96. doi: 10.1210/jc.2013-3486. Epub 2014 Jan 1.

Abstract

Context: Mutations in the four subunits of succinate dehydrogenase (SDH) are the cause for the hereditary paraganglioma (PGL) syndrome types 1-4 and are associated with multiple and recurrent pheochromocytomas and PGLs. SDHC mutations most frequently result in benign, nonfunctional head-and neck PGLs (HNPGLs). The malignant potential of SDHC mutations remains unclear to date.

Objectives: We report a patient with malignant PGL carrying a SDHC mutation and compare her case with two others of the same genotype but presenting with classic benign HNPGLs. Loss of heterozygosity (LOH) was demonstrated in the malignant PGL tissue.

Design: In three unrelated patients referred for routine genetic testing, SDHB, SDHC, and SDHD genes were sequenced, and gross deletions were excluded by multiplex ligation-dependent probe amplification (MLPA). LOH was determined by pyrosequencing-based allele quantification and SDHB immunohistochemistry.

Results: In a patient with a nonfunctioning thoracic PGL metastatic to the bone, the lungs, and mediastinal lymph nodes, we detected the SDHC mutation c.397C>T predicting a truncated protein due to a premature stop codon (p.Arg133*). We demonstrated LOH and loss of SDHB protein expression in the malignant tumor tissue. The two other patients also carried c.397C>T, p.Arg133*; they differed from each other with respect to their tumor characteristics, but both showed benign HNPGLs.

Conclusions: We describe the first case of a malignant PGL with distant metastases caused by a SDHC germline mutation. The present case shows that SDHC germline mutations can have highly variable phenotypes and may cause malignant PGL, although malignancy is probably rare.

Publication types

  • Case Reports
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Arginine / genetics
  • Female
  • Genetic Heterogeneity
  • Genetic Predisposition to Disease
  • Germ-Line Mutation*
  • Glomus Jugulare Tumor / genetics
  • Head and Neck Neoplasms / genetics
  • Head and Neck Neoplasms / pathology
  • Heart Neoplasms / genetics
  • Heart Neoplasms / secondary
  • Humans
  • Loss of Heterozygosity
  • Lumbar Vertebrae
  • Male
  • Membrane Proteins / genetics*
  • Middle Aged
  • Paraganglioma / genetics*
  • Paraganglioma / pathology
  • Phenotype
  • Risk Factors
  • Spinal Neoplasms / genetics*
  • Spinal Neoplasms / pathology

Substances

  • Membrane Proteins
  • SDHC protein, human
  • Arginine