Alpha-lipoic acid supplementation corrects pathological alterations in cellular models of pantothenate kinase-associated neurodegeneration with residual PANK2 expression levels

Orphanet J Rare Dis. 2023 Apr 12;18(1):80. doi: 10.1186/s13023-023-02687-5.

Abstract

Background: Neurodegeneration with brain iron accumulation (NBIA) disorders are a group of neurodegenerative diseases that have in common the accumulation of iron in the basal nuclei of the brain which are essential components of the extrapyramidal system. Frequent symptoms are progressive spasticity, dystonia, muscle rigidity, neuropsychiatric symptoms, and retinal degeneration or optic nerve atrophy. One of the most prevalent subtypes of NBIA is Pantothenate kinase-associated neurodegeneration (PKAN). It is caused by pathogenic variants in the gene of pantothenate kinase 2 (PANK2) which encodes the enzyme responsible for the first reaction on the coenzyme A (CoA) biosynthesis pathway. Thus, deficient PANK2 activity induces CoA deficiency as well as low expression levels of 4'-phosphopantetheinyl proteins which are essential for mitochondrial metabolism.

Methods: This study is aimed at evaluating the role of alpha-lipoic acid (α-LA) in reversing the pathological alterations in fibroblasts and induced neurons derived from PKAN patients. Iron accumulation, lipid peroxidation, transcript and protein expression levels of PANK2, mitochondrial ACP (mtACP), 4''-phosphopantetheinyl and lipoylated proteins, as well as pyruvate dehydrogenase (PDH) and Complex I activity were examined.

Results: Treatment with α-LA was able to correct all pathological alterations in responsive mutant fibroblasts with residual PANK2 enzyme expression. However, α-LA had no effect on mutant fibroblasts with truncated/incomplete protein expression. The positive effect of α-LA in particular pathogenic variants was also confirmed in induced neurons derived from mutant fibroblasts.

Conclusions: Our results suggest that α-LA treatment can increase the expression levels of PANK2 and reverse the mutant phenotype in PANK2 responsive pathogenic variants. The existence of residual enzyme expression in some affected individuals raises the possibility of treatment using high dose of α-LA.

Keywords: 4′-phosphopantetheinylation; Acyl carrier protein; Coenzyme A; Induced neurons; Mitochondria; PANK2; PKAN; Pantothenate kinase; Pantothenate kinase-associated neurodegeneration; α-lipoic acid.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Dietary Supplements
  • Humans
  • Iron / metabolism
  • Mitochondria / metabolism
  • Neurodegenerative Diseases* / genetics
  • Pantothenate Kinase-Associated Neurodegeneration* / drug therapy
  • Pantothenate Kinase-Associated Neurodegeneration* / genetics
  • Pantothenate Kinase-Associated Neurodegeneration* / metabolism
  • Phosphotransferases (Alcohol Group Acceptor) / genetics
  • Phosphotransferases (Alcohol Group Acceptor) / metabolism
  • Thioctic Acid* / metabolism
  • Thioctic Acid* / therapeutic use

Substances

  • Iron
  • pantothenate kinase
  • Phosphotransferases (Alcohol Group Acceptor)
  • Thioctic Acid