Resolvin E1 attenuates doxorubicin-induced cardiac fibroblast senescence: A key role for IL-1β

Biochim Biophys Acta Mol Basis Dis. 2022 Nov 1;1868(11):166525. doi: 10.1016/j.bbadis.2022.166525. Epub 2022 Aug 18.

Abstract

Cardiac fibroblasts (CFs) undergo senescence in reaction to different stressors, leading to a poor prognosis of cardiac disease. Doxorubicin (Doxo) is an antineoplastic drug with strong cardiotoxic effects, which induces IL-1β secretion and thus, triggers a potent pro-inflammatory response. Doxo induces CFs senescence; however, the mechanisms are not fully understood. Different pharmacological strategies have been used to eliminate senescent cells by inducing their apoptosis or modifying their secretome. However, Resolvin E1 (RvE1), a lipid derivative resolutive mediator with potent anti-inflammatory effects has not been used before to prevent CFs senescence. CFs were isolated from adult male C57BL/6J mice and subsequently stimulated with Doxo, in the presence or absence of RvE1. Senescence-associated β-galactosidase activity (SA-β-gal), γ-H2A.X, p53, p21, and senescence-associated secretory phenotype (SASP) were evaluated. The involvement of the NLRP3 inflammasome/interleukin-1 receptor (IL-1R) signaling pathway on CFs senescence was studied using an NLRP3 inhibitor (MCC950) and an endogenous IL-1R antagonist (IR1A). Doxo is able to trigger CFs senescence, as evidenced by an increase of γ-H2A.X, p53, p21, and SA-β-gal, and changes in the SASP profile. These Doxo effects were prevented by RvE1. Doxo triggers IL-1β secretion, which was dependent on NLRP3 activation. Doxo-induced CFs senescence was partially blocked by MCC950 and IR1A. In addition, IL-1β also triggered CFs senescence, as evidenced by the increase of γ-H2A.X, p53, p21, SA-β-gal activity, and SASP. All these effects were also prevented by RvE1 treatment. CONCLUSION: These data show the anti-senescent role of RvE1 in Doxo-induced CFs senescence, which could be mediated by reducing IL-1β secretion.

Keywords: Cardiac fibroblasts; Doxorubicin; Interleukin-1β; Resolvin E1; Senescence.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Anti-Inflammatory Agents / pharmacology
  • Cellular Senescence
  • Doxorubicin / pharmacology
  • Eicosapentaenoic Acid / analogs & derivatives
  • Eicosapentaenoic Acid / pharmacology
  • Fibroblasts / metabolism
  • Furans
  • Indenes
  • Inflammasomes* / metabolism
  • Interleukin-1beta / metabolism*
  • Male
  • Mice
  • Mice, Inbred C57BL
  • NLR Family, Pyrin Domain-Containing 3 Protein / metabolism
  • Receptors, Interleukin-1 / metabolism
  • Sulfonamides
  • Tumor Suppressor Protein p53 / metabolism
  • beta-Galactosidase / metabolism
  • beta-Galactosidase / pharmacology

Substances

  • Anti-Inflammatory Agents
  • Furans
  • IL1B protein, mouse
  • Indenes
  • Inflammasomes
  • Interleukin-1beta
  • NLR Family, Pyrin Domain-Containing 3 Protein
  • Receptors, Interleukin-1
  • Sulfonamides
  • Tumor Suppressor Protein p53
  • N-(1,2,3,5,6,7-hexahydro-S-indacen-4-ylcarbamoyl)-4-(2-hydroxy-2-propanyl)-2-furansulfonamide
  • Doxorubicin
  • Eicosapentaenoic Acid
  • beta-Galactosidase
  • 5S,12R,18R-trihydroxy-6Z,8E,10E,14Z,16E-eicosapentaenoic acid