TERT Promoter Mutations Increase Tumor Aggressiveness by Altering TERT mRNA Splicing in Papillary Thyroid Carcinoma

J Clin Endocrinol Metab. 2024 Sep 16;109(10):e1827-e1838. doi: 10.1210/clinem/dgae220.

Abstract

Context: Telomerase reverse transcriptase promoter (TERT-p) mutations, which upregulate TERT expression, are strongly associated with tumor aggressiveness and worse prognosis in papillary thyroid carcinomas (PTCs). TERT expression is also observed in a proportion of PTCs without TERT-p mutations, but such tumors show less aggressiveness and better prognosis than TERT-p mutation-positive tumors.

Objective: TERT has multiple splicing variants whose relationships with the TERT-p status and clinicopathological characteristics remain poorly understood. We examined the relationship between the TERT-p mutational status, the TERT splicing pattern, and clinicopathological features.

Methods: We investigated the expression of 2 major variants, α deletion (dA) and β deletion (dB), in a series of 207 PTCs operated on between November 2001 and March 2020 in Nagasaki University Hospital and Kuma Hospital.

Results: The TERT-p mutations were found in 33 cases, and among 174 mutation-negative cases, 24 showed TERT expression. All cases were classified into 3 groups: the TERT-p mutation-negative/expression-negative group (mut-/exp-), the TERT-p mutation-negative/expression-positive group (mut-/exp+), and the TERT-p mutation-positive group (mut+/exp+). The +A+B/dB ratio in mut+/exp+ was significantly higher than that in mut-/exp+ PTCs. Analysis with clinicopathological data revealed that +A+B expression was associated with higher PTC aggressiveness, whereas dB expression counteracted this effect. Functional in vitro study demonstrated that dB strongly inhibited cell growth, migration, and clonogenicity, suggesting its tumor-suppressive role.

Conclusion: These results provide evidence that the TERT-p mutations alter the expression of different TERT splice variants, which, in turn, associates with different tumor aggressiveness.

Keywords: TERT expression; TERT promoter mutation; aggressiveness; papillary thyroid carcinoma; splicing.

MeSH terms

  • Adult
  • Aged
  • Female
  • Gene Expression Regulation, Neoplastic
  • Humans
  • Male
  • Middle Aged
  • Mutation*
  • Neoplasm Invasiveness / genetics
  • Prognosis
  • Promoter Regions, Genetic*
  • RNA Splicing*
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • Telomerase* / genetics
  • Telomerase* / metabolism
  • Thyroid Cancer, Papillary* / genetics
  • Thyroid Cancer, Papillary* / metabolism
  • Thyroid Cancer, Papillary* / pathology
  • Thyroid Neoplasms* / genetics
  • Thyroid Neoplasms* / metabolism
  • Thyroid Neoplasms* / pathology
  • Young Adult

Substances

  • Telomerase
  • TERT protein, human
  • RNA, Messenger