Telomere Dysfunction Induces Sirtuin Repression that Drives Telomere-Dependent Disease

Cell Metab. 2019 Jun 4;29(6):1274-1290.e9. doi: 10.1016/j.cmet.2019.03.001. Epub 2019 Mar 28.

Abstract

Telomere shortening is associated with stem cell decline, fibrotic disorders, and premature aging through mechanisms that are incompletely understood. Here, we show that telomere shortening in livers of telomerase knockout mice leads to a p53-dependent repression of all seven sirtuins. P53 regulates non-mitochondrial sirtuins (Sirt1, 2, 6, and 7) post-transcriptionally through microRNAs (miR-34a, 26a, and 145), while the mitochondrial sirtuins (Sirt3, 4, and 5) are regulated in a peroxisome proliferator-activated receptor gamma co-activator 1 alpha-/beta-dependent manner at the transcriptional level. Administration of the NAD(+) precursor nicotinamide mononucleotide maintains telomere length, dampens the DNA damage response and p53, improves mitochondrial function, and, functionally, rescues liver fibrosis in a partially Sirt1-dependent manner. These studies establish sirtuins as downstream targets of dysfunctional telomeres and suggest that increasing Sirt1 activity alone or in combination with other sirtuins stabilizes telomeres and mitigates telomere-dependent disorders.

Keywords: liver disease; metabolism; p53; sirtuins; telomeres.

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

  • Animals
  • Cells, Cultured
  • Down-Regulation / drug effects
  • Down-Regulation / genetics
  • Embryo, Mammalian
  • Female
  • Gene Expression Regulation, Enzymologic / drug effects
  • HEK293 Cells
  • Humans
  • Liver / drug effects
  • Liver / metabolism
  • Liver / pathology
  • Liver Cirrhosis / genetics*
  • Liver Cirrhosis / pathology
  • Liver Cirrhosis / prevention & control
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Mitochondria, Liver / drug effects
  • Mitochondria, Liver / metabolism
  • Nicotinamide Mononucleotide / pharmacology
  • Sirtuin 1 / genetics
  • Sirtuin 1 / metabolism
  • Sirtuins / genetics*
  • Sirtuins / metabolism
  • Telomerase / genetics
  • Telomerase / metabolism
  • Telomere Homeostasis / drug effects
  • Telomere Homeostasis / physiology
  • Telomere Shortening / drug effects
  • Telomere Shortening / genetics
  • Telomere Shortening / physiology*

Substances

  • Nicotinamide Mononucleotide
  • Telomerase
  • Tert protein, mouse
  • Sirtuin 1
  • Sirtuins