Resolvin E1 attenuates doxorubicin-induced endothelial senescence by modulating NLRP3 inflammasome activation

Biochem Pharmacol. 2022 Jul:201:115078. doi: 10.1016/j.bcp.2022.115078. Epub 2022 May 10.

Abstract

Endothelial cell senescence contributes to chronic inflammation and endothelial dysfunction, while favoring cardiovascular disorders and frailty. Senescent cells acquire a pro-inflammatory secretory phenotype that further propagates inflammation and senescence to neighboring cells. Cell senescence can be provoked by plethora of stressors, including inflammatory molecules and chemotherapeutic drugs. Doxorubicin (Doxo) is a powerful anthracycline anticancer drug whose clinical application is constrained by a dose-limiting cardiovascular toxicity. We here investigated whether cell senescence can contribute to the vascular damage elicited by Doxo. In human umbilical vein endothelial cells (HUVEC) cultures, Doxo (10-100 nM) increased the number of SA-β-gal positive cells and the levels of γH2AX, p21 and p53, used as markers of senescence. Moreover, we identified Doxo-induced senescence to be mediated by the nucleotide-binding domain-like receptor protein 3 (NLRP3) inflammasome, a key player of the immune innate system capable of releasing interleukin (IL)-1β. In fact, IL-1β itself mimicked the stimulatory action of Doxo on both NLRP3 activation and cellular senescence, while the pharmacological blockade of IL-1 receptors markedly attenuated the pro-senescence effects of Doxo. In search of additional pharmacological strategies to attenuate Doxo-induced endothelial senescence, we identified resolvin E1 (RvE1), an endogenous pro-resolving mediator, as capable of reducing cell senescence induced by both Doxo and IL-1β by interfering with the increased expression of pP65, NLRP3, and pro-IL-1β proteins and with the formation of active NLRP3 inflammasome complexes. Overall, RvE1 and the blockade of the NLRP3 inflammasome-IL-1β axis may offer a novel therapeutic approach against Doxo-induced cardiovascular toxicity and subsequent sequelae.

Keywords: Doxorubicin; Endothelial senescence; Interleukin 1β; NLRP3 inflammasome; Resolvin E1; Vascular aging.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Cellular Senescence / drug effects
  • Doxorubicin* / pharmacology
  • Drug Interactions
  • Eicosapentaenoic Acid* / analogs & derivatives
  • Eicosapentaenoic Acid* / pharmacology
  • Human Umbilical Vein Endothelial Cells* / drug effects
  • Human Umbilical Vein Endothelial Cells* / immunology
  • Human Umbilical Vein Endothelial Cells* / metabolism
  • Humans
  • Inflammasomes* / drug effects
  • Inflammasomes* / immunology
  • Inflammasomes* / metabolism
  • Inflammation / chemically induced
  • Interleukin-1beta / metabolism
  • NLR Family, Pyrin Domain-Containing 3 Protein* / immunology
  • NLR Family, Pyrin Domain-Containing 3 Protein* / metabolism

Substances

  • Inflammasomes
  • Interleukin-1beta
  • NLR Family, Pyrin Domain-Containing 3 Protein
  • NLRP3 protein, human
  • Doxorubicin
  • Eicosapentaenoic Acid
  • 5S,12R,18R-trihydroxy-6Z,8E,10E,14Z,16E-eicosapentaenoic acid