TINF2 is a haploinsufficient tumor suppressor that limits telomere length

Elife. 2020 Dec 1:9:e61235. doi: 10.7554/eLife.61235.

Abstract

Telomere shortening is a presumed tumor suppressor pathway that imposes a proliferative barrier (the Hayflick limit) during tumorigenesis. This model predicts that excessively long somatic telomeres predispose to cancer. Here, we describe cancer-prone families with two unique TINF2 mutations that truncate TIN2, a shelterin subunit that controls telomere length. Patient lymphocyte telomeres were unusually long. We show that the truncated TIN2 proteins do not localize to telomeres, suggesting that the mutations create loss-of-function alleles. Heterozygous knock-in of the mutations or deletion of one copy of TINF2 resulted in excessive telomere elongation in clonal lines, indicating that TINF2 is haploinsufficient for telomere length control. In contrast, telomere protection and genome stability were maintained in all heterozygous clones. The data establish that the TINF2 truncations predispose to a tumor syndrome. We conclude that TINF2 acts as a haploinsufficient tumor suppressor that limits telomere length to ensure a timely Hayflick limit.

Keywords: TIN2; cancer biology; cancer predisposition; human; telomere length.

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

  • Cell Line
  • Female
  • Genes, Tumor Suppressor*
  • HEK293 Cells
  • Heterozygote
  • Humans
  • Loss of Function Mutation
  • Male
  • Neoplasms / genetics
  • Telomere / genetics*
  • Telomere / pathology
  • Telomere Shortening / genetics*
  • Telomere-Binding Proteins / genetics
  • Telomere-Binding Proteins / physiology*
  • Telomeric Repeat Binding Protein 1 / metabolism
  • Tumor Suppressor Proteins

Substances

  • TINF2 protein, human
  • Telomere-Binding Proteins
  • Telomeric Repeat Binding Protein 1
  • Tumor Suppressor Proteins