The NAD+ Precursor Nicotinamide Riboside Rescues Mitochondrial Defects and Neuronal Loss in iPSC derived Cortical Organoid of Alpers' Disease

Int J Biol Sci. 2024 Jan 25;20(4):1194-1217. doi: 10.7150/ijbs.91624. eCollection 2024.

Abstract

Alpers' syndrome is an early-onset neurodegenerative disorder usually caused by biallelic pathogenic variants in the gene encoding the catalytic subunit of polymerase-gamma (POLG), which is essential for mitochondrial DNA (mtDNA) replication. The disease is progressive, incurable, and inevitably it leads to death from drug-resistant status epilepticus. The neurological features of Alpers' syndrome are intractable epilepsy and developmental regression, with no effective treatment; the underlying mechanisms are still elusive, partially due to lack of good experimental models. Here, we generated the patient derived induced pluripotent stem cells (iPSCs) from one Alpers' patient carrying the compound heterozygous mutations of A467T (c.1399G>A) and P589L (c.1766C>T), and further differentiated them into cortical organoids and neural stem cells (NSCs) for mechanistic studies of neural dysfunction in Alpers' syndrome. Patient cortical organoids exhibited a phenotype that faithfully replicated the molecular changes found in patient postmortem brain tissue, as evidenced by cortical neuronal loss and depletion of mtDNA and complex I (CI). Patient NSCs showed mitochondrial dysfunction leading to ROS overproduction and downregulation of the NADH pathway. More importantly, the NAD+ precursor nicotinamide riboside (NR) significantly ameliorated mitochondrial defects in patient brain organoids. Our findings demonstrate that the iPSC model and brain organoids are good in vitro models of Alpers' disease; this first-in-its-kind stem cell platform for Alpers' syndrome enables therapeutic exploration and has identified NR as a viable drug candidate for Alpers' disease and, potentially, other mitochondrial diseases with similar causes.

Keywords: Alpers' disease; NAD+; NR; cortical organoids; induced pluripotent stem cells; mitochondrial function.

MeSH terms

  • DNA Polymerase gamma
  • DNA, Mitochondrial / genetics
  • Diffuse Cerebral Sclerosis of Schilder*
  • Humans
  • Induced Pluripotent Stem Cells*
  • Mitochondrial Diseases*
  • Mutation
  • NAD / genetics
  • Niacinamide / analogs & derivatives*
  • Pyridinium Compounds*

Substances

  • DNA Polymerase gamma
  • NAD
  • nicotinamide-beta-riboside
  • DNA, Mitochondrial
  • Niacinamide
  • Pyridinium Compounds