Impaired ketogenesis in Leydig Cells drives testicular aging

Nat Commun. 2025 May 7;16(1):4224. doi: 10.1038/s41467-025-59591-8.

Abstract

Testicular aging commonly leads to testosterone deficiency and impaired spermatogenesis, yet the underlying mechanisms remain elusive. Here, we show that Leydig cells are particularly vulnerable to aging processes in testis. Single-cell RNA sequencing identifies the expression of Hmgcs2, the gene encoding rate-limiting enzyme of ketogenesis, decreases significantly in Leydig cells from aged mice. Additionally, the concentrations of ketone bodies β-hydroxybutyric acid and acetoacetic acid in young testes are substantially higher than that in serum, but significantly diminish in aged testes. Silencing of Hmgcs2 in young Leydig cells drives cell senescence and accelerated testicular aging. Mechanistically, β-hydroxybutyric acid upregulates the expression of Foxo3a by facilitating histone acetylation, thereby mitigating Leydig cells senescence and promoting testosterone production. Consistently, enhanced ketogenesis by genetic manipulation or oral β-hydroxybutyric acid supplementation alleviates Leydig cells senescence and ameliorates testicular aging in aged mice. These findings highlight defective ketogenesis as a pivotal factor in testicular aging, suggesting potential therapeutic avenues for addressing age-related testicular dysfunction.

MeSH terms

  • 3-Hydroxybutyric Acid / metabolism
  • 3-Hydroxybutyric Acid / pharmacology
  • Acetylation
  • Aging* / metabolism
  • Animals
  • Cellular Senescence / drug effects
  • Forkhead Box Protein O3 / genetics
  • Forkhead Box Protein O3 / metabolism
  • Histones / metabolism
  • Hydroxymethylglutaryl-CoA Synthase / genetics
  • Hydroxymethylglutaryl-CoA Synthase / metabolism
  • Ketone Bodies* / biosynthesis
  • Ketone Bodies* / metabolism
  • Leydig Cells* / drug effects
  • Leydig Cells* / metabolism
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Testis* / cytology
  • Testis* / metabolism
  • Testosterone / metabolism

Substances

  • Testosterone
  • Forkhead Box Protein O3
  • 3-Hydroxybutyric Acid
  • Ketone Bodies
  • FoxO3 protein, mouse
  • Histones
  • Hydroxymethylglutaryl-CoA Synthase