Aldehydes alter TGF-β signaling and induce obesity and cancer

Cell Rep. 2024 Sep 24;43(9):114676. doi: 10.1016/j.celrep.2024.114676. Epub 2024 Aug 31.

Abstract

Obesity and fatty liver diseases-metabolic dysfunction-associated steatotic liver disease (MASLD) and metabolic dysfunction-associated steatohepatitis (MASH)-affect over one-third of the global population and are exacerbated in individuals with reduced functional aldehyde dehydrogenase 2 (ALDH2), observed in approximately 560 million people. Current treatment to prevent disease progression to cancer remains inadequate, requiring innovative approaches. We observe that Aldh2-/- and Aldh2-/-Sptbn1+/- mice develop phenotypes of human metabolic syndrome (MetS) and MASH with accumulation of endogenous aldehydes such as 4-hydroxynonenal (4-HNE). Mechanistic studies demonstrate aberrant transforming growth factor β (TGF-β) signaling through 4-HNE modification of the SMAD3 adaptor SPTBN1 (β2-spectrin) to pro-fibrotic and pro-oncogenic phenotypes, which is restored to normal SMAD3 signaling by targeting SPTBN1 with small interfering RNA (siRNA). Significantly, therapeutic inhibition of SPTBN1 blocks MASH and fibrosis in a human model and, additionally, improves glucose handling in Aldh2-/- and Aldh2-/-Sptbn1+/- mice. This study identifies SPTBN1 as a critical regulator of the functional phenotype of toxic aldehyde-induced MASH and a potential therapeutic target.

Keywords: ALDH2; CP: Cancer; CP: Metabolism; HCC; MASH; SMAD3; SPTBN1; TGF-β; cancer; liver disease; metabolic syndrome; reactive aldehydes.

MeSH terms

  • Aldehyde Dehydrogenase, Mitochondrial* / genetics
  • Aldehyde Dehydrogenase, Mitochondrial* / metabolism
  • Aldehydes* / metabolism
  • Animals
  • Humans
  • Male
  • Metabolic Syndrome / genetics
  • Metabolic Syndrome / metabolism
  • Metabolic Syndrome / pathology
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Neoplasms* / genetics
  • Neoplasms* / metabolism
  • Neoplasms* / pathology
  • Obesity* / metabolism
  • Obesity* / pathology
  • Signal Transduction*
  • Smad3 Protein* / metabolism
  • Spectrin / genetics
  • Spectrin / metabolism
  • Transforming Growth Factor beta* / metabolism

Substances

  • Transforming Growth Factor beta
  • Aldehydes
  • Aldehyde Dehydrogenase, Mitochondrial
  • Smad3 Protein
  • Spectrin
  • SPTBN1 protein, human
  • 4-hydroxy-2-nonenal