Replenishing IRAK-M expression in retinal pigment epithelium attenuates outer retinal degeneration

Sci Transl Med. 2024 Jun 5;16(750):eadi4125. doi: 10.1126/scitranslmed.adi4125. Epub 2024 Jun 5.

Abstract

Chronic inflammation is a constitutive component of many age-related diseases, including age-related macular degeneration (AMD). Here, we identified interleukin-1 receptor-associated kinase M (IRAK-M) as a key immunoregulator in retinal pigment epithelium (RPE) that declines during the aging process. Rare genetic variants of IRAK3, which encodes IRAK-M, were associated with an increased likelihood of developing AMD. In human samples and mouse models, IRAK-M abundance in the RPE declined with advancing age or exposure to oxidative stress and was further reduced in AMD. Irak3-knockout mice exhibited an increased incidence of outer retinal degeneration at earlier ages, which was further exacerbated by oxidative stressors. The absence of IRAK-M led to a disruption in RPE cell homeostasis, characterized by compromised mitochondrial function, cellular senescence, and aberrant cytokine production. IRAK-M overexpression protected RPE cells against oxidative or immune stressors. Subretinal delivery of adeno-associated virus (AAV)-expressing human IRAK3 rescued light-induced outer retinal degeneration in wild-type mice and attenuated age-related spontaneous retinal degeneration in Irak3-knockout mice. Our data show that replenishment of IRAK-M in the RPE may redress dysregulated pro-inflammatory processes in AMD, suggesting a potential treatment for retinal degeneration.

MeSH terms

  • Animals
  • Cellular Senescence
  • Humans
  • Interleukin-1 Receptor-Associated Kinases* / genetics
  • Interleukin-1 Receptor-Associated Kinases* / metabolism
  • Macular Degeneration / genetics
  • Macular Degeneration / metabolism
  • Macular Degeneration / pathology
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout*
  • Mitochondria / metabolism
  • Oxidative Stress*
  • Retinal Degeneration* / genetics
  • Retinal Degeneration* / metabolism
  • Retinal Degeneration* / pathology
  • Retinal Pigment Epithelium* / metabolism
  • Retinal Pigment Epithelium* / pathology

Substances

  • Interleukin-1 Receptor-Associated Kinases
  • IRAK3 protein, human
  • Irak3 protein, mouse