Background
The age-related decline in oocyte nicotinamide adenine dinucleotide (NAD⁺) is associated with impaired redox metabolism and reduced fertility. However, the cause of declining oocyte NAD⁺ remains unresolved. Given the central role of cumulus-cells in oocyte metabolism, we hypothesised that reproductive ageing disrupts cumulus–oocyte metabolic coupling, impairing oocyte NAD⁺ homeostasis.
Methods
Oocytes and cumulus-cells from cumulus–oocyte complexes (COCs) were analysed by targeted LC-MS/MS for NAD⁺/adenine metabolites, from young and reproductively aged mice, upon disrupted cumulus communication (carbenoxolone;CBX) or mechanical denudation (denuded oocytes; DO), or upon acute H₂O₂ exposure, ± the NAD⁺ precursor nicotinamide mononucleotide (NMN). Deuterium-labelled NMN (d4-NMN) LC-MS/MS tracing assessed NAD⁺ synthesis. Redox outcomes were assessed using CM-H₂DCFDA (reactive oxygen species;ROS), monochlorobimane (glutathione), and JC-1 (mitochondrial membrane potential). Cumulus-cells from 23 fertility patients were also analysed.
Results
We identified altered NAD⁺ metabolites in mouse oocytes (NADP, p=0.029; NADPH, p=0.024) and cumulus-cells (NAD⁺, p=0.006; NADP, p=0.007) with age, and in aged human cumulus-cells (NAM, p=0.004; meNAM, p=0.049). Disrupted COC communication impaired oocyte NAD⁺ homeostasis, increasing oocyte NMN (CBX, p=0.0002; DO, p=0.0003), reducing oocyte NAD⁺ (CBX, p<0.0001; DO, p<0.0001), and reducing d3-NAD⁺ synthesis (CBX, p=0.027; DO, p<0.0001). Altered adenine nucleotide turnover emerged as a potential contributor to impaired NAD⁺ metabolism (AMP: CBX, p=0.028; DO, p=0.004). Restoring NAD⁺ levels during in vitro maturation with NMN in intact COCs reduced ROS (age, p<0.0001; H₂O₂, p<0.0001), increased glutathione (age, p=0.001; ROS, p<0.0001), and improved mitochondrial membrane potential (age, p<0.0001; ROS, p=0.006) in aged and H₂O₂-exposed mouse oocytes, but did not reduce ROS in DOs, demonstrating that NAD⁺-dependent benefits rely on cumulus-cells.
Conclusion
These findings identify a new model of somatic–germline metabolic coupling for NAD⁺ biosynthesis, placing age-related deterioration in cumulus-cell-mediated metabolic support as a key driver of impaired oocyte NAD⁺ levels and redox dysregulation with ageing.