Histone lactylation-regulated METTL3 promotes ferroptosis via m6A-modification on ACSL4 in sepsis-associated lung injury

Redox Biol. 2024 Aug:74:103194. doi: 10.1016/j.redox.2024.103194. Epub 2024 May 16.

Abstract

Elevated lactate levels are a significant biomarker of sepsis and are positively associated with sepsis-related mortality. Sepsis-associated lung injury (ALI) is a leading cause of poor prognosis in clinical patients. However, the underlying mechanisms of lactate's involvement in sepsis-associated ALI remain unclear. In this study, we demonstrate that lactate regulates N6-methyladenosine (m6A) modification levels by facilitating p300-mediated H3K18la binding to the METTL3 promoter site. The METTL3-mediated m6A modification is enriched in ACSL4, and its mRNA stability is regulated through a YTHDC1-dependent pathway. Furthermore, short-term lactate stimulation upregulates ACSL4, which promotes mitochondria-associated ferroptosis. Inhibition of METTL3 through knockdown or targeted inhibition effectively suppresses septic hyper-lactate-induced ferroptosis in alveolar epithelial cells and mitigates lung injury in septic mice. Our findings suggest that lactate induces ferroptosis via the GPR81/H3K18la/METTL3/ACSL4 axis in alveolar epithelial cells during sepsis-associated ALI. These results reveal a histone lactylation-driven mechanism inducing ferroptosis through METTL3-mediated m6A modification. Targeting METTL3 represents a promising therapeutic strategy for patients with sepsis-associated ALI.

Keywords: Ferroptosis; Histone lactylation; N6- methyladenosine; Sepsis-associated acute lung injury.

MeSH terms

  • Acute Lung Injury / etiology
  • Acute Lung Injury / genetics
  • Acute Lung Injury / metabolism
  • Acute Lung Injury / pathology
  • Adenosine / analogs & derivatives
  • Adenosine / metabolism
  • Animals
  • Coenzyme A Ligases* / genetics
  • Coenzyme A Ligases* / metabolism
  • Disease Models, Animal
  • Ferroptosis*
  • Humans
  • Lactic Acid / metabolism
  • Lung Injury / etiology
  • Lung Injury / genetics
  • Lung Injury / metabolism
  • Lung Injury / pathology
  • Male
  • Methyltransferases* / genetics
  • Methyltransferases* / metabolism
  • Mice
  • Sepsis* / complications
  • Sepsis* / metabolism

Substances

  • Methyltransferases
  • Mettl3 protein, mouse
  • Coenzyme A Ligases
  • N-methyladenosine
  • METTL3 protein, human
  • Adenosine
  • Acsl4 protein, mouse
  • Lactic Acid