Beta cells deficient for Renalase counteract autoimmunity by shaping natural killer cell activity

Front Immunol. 2024 Jun 4:15:1403752. doi: 10.3389/fimmu.2024.1403752. eCollection 2024.

Abstract

Type 1 diabetes (T1D) arises from autoimmune-mediated destruction of insulin-producing pancreatic beta cells. Recent advancements in the technology of generating pancreatic beta cells from human pluripotent stem cells (SC-beta cells) have facilitated the exploration of cell replacement therapies for treating T1D. However, the persistent threat of autoimmunity poses a significant challenge to the survival of transplanted SC-beta cells. Genetic engineering is a promising approach to enhance immune resistance of beta cells as we previously showed by inactivating the Renalase (Rnls) gene. Here, we demonstrate that Rnls loss of function in beta cells shapes autoimmunity by mediating a regulatory natural killer (NK) cell phenotype important for the induction of tolerogenic antigen-presenting cells. Rnls-deficient beta cells mediate cell-cell contact-independent induction of hallmark anti-inflammatory cytokine Tgfβ1 in NK cells. In addition, surface expression of regulatory NK immune checkpoints CD47 and Ceacam1 is markedly elevated on beta cells deficient for Rnls. Altered glucose metabolism in Rnls mutant beta cells is involved in the upregulation of CD47 surface expression. These findings are crucial to better understand how genetically engineered beta cells shape autoimmunity, giving valuable insights for future therapeutic advancements to treat and cure T1D.

Keywords: CD47; Ceacam1; NK cell; Tgfβ1; autoimmunity; beta cell; transplantation; type 1 diabetes.

MeSH terms

  • Animals
  • Autoimmunity*
  • CD47 Antigen / genetics
  • CD47 Antigen / immunology
  • CD47 Antigen / metabolism
  • Diabetes Mellitus, Type 1* / immunology
  • Humans
  • Insulin-Secreting Cells* / immunology
  • Insulin-Secreting Cells* / metabolism
  • Killer Cells, Natural* / immunology
  • Killer Cells, Natural* / metabolism
  • Mice
  • Mice, Inbred NOD
  • Monoamine Oxidase
  • Transforming Growth Factor beta1 / metabolism

Substances

  • renalase
  • CD47 Antigen
  • Transforming Growth Factor beta1
  • Monoamine Oxidase