Blocking CTLA-4 promotes pressure overload-induced heart failure via activating Th17 cells

FASEB J. 2024 Aug 15;38(15):e23851. doi: 10.1096/fj.202400384R.

Abstract

Targeting cytotoxic T-lymphocyte-associated antigen-4 (CTLA-4) with specific antibody offers long-term benefits for cancer immunotherapy but can cause severe adverse effects in the heart. This study aimed to investigate the role of anti-CTLA-4 antibody in pressure overload-induced cardiac remodeling and dysfunction. Transverse aortic constriction (TAC) was used to induce cardiac hypertrophy and heart failure in mice. Two weeks after the TAC treatment, mice received anti-CTLA-4 antibody injection twice a week at a dose of 10 mg/kg body weight. The administration of anti-CTLA-4 antibody exacerbated TAC-induced decline in cardiac function, intensifying myocardial hypertrophy and fibrosis. Further investigation revealed that anti-CTLA-4 antibody significantly elevated systemic inflammatory factors levels and facilitated the differentiation of T helper 17 (Th17) cells in the peripheral blood of TAC-treated mice. Importantly, anti-CTLA-4 mediated differentiation of Th17 cells and hypertrophic phenotype in TAC mice were dramatically alleviated by the inhibition of interleukin-17A (IL-17A) by an anti-IL-17A antibody. Furthermore, the C-X-C motif chemokine receptor 4 (CXCR4) antagonist AMD3100, also reversed anti-CTLA-4-mediated cardiotoxicity in TAC mice. Overall, these results suggest that the administration of anti-CTLA-4 antibody exacerbates pressure overload-induced heart failure by activating and promoting the differentiation of Th17 cells. Targeting the CXCR4/Th17/IL-17A axis could be a potential therapeutic strategy for mitigating immune checkpoint inhibitors-induced cardiotoxicity.

Keywords: CTLA‐4; CXCR4; IL‐17A; Th17 cells; heart failure.

MeSH terms

  • Animals
  • CTLA-4 Antigen* / antagonists & inhibitors
  • CTLA-4 Antigen* / metabolism
  • Cardiomegaly / etiology
  • Cardiomegaly / metabolism
  • Cardiomegaly / pathology
  • Cell Differentiation
  • Heart Failure* / etiology
  • Heart Failure* / metabolism
  • Interleukin-17 / metabolism
  • Male
  • Mice
  • Mice, Inbred C57BL*
  • Receptors, CXCR4 / antagonists & inhibitors
  • Receptors, CXCR4 / metabolism
  • Th17 Cells* / immunology
  • Th17 Cells* / metabolism

Substances

  • CTLA-4 Antigen
  • Interleukin-17
  • Ctla4 protein, mouse
  • Receptors, CXCR4
  • CXCR4 protein, mouse