AMP Kinase Activation is Selectively Disrupted in the Ventral Midbrain of Mice Deficient in Parkin or PINK1 Expression

Neuromolecular Med. 2019 Mar;21(1):25-32. doi: 10.1007/s12017-018-8517-7. Epub 2018 Nov 8.

Abstract

Parkinson's disease (PD) is a prevalent neurodegenerative movement disorder that is characterized pathologically by the progressive loss of dopaminergic (DA) neurons in the substantia nigra pars compacta (SNpc) of the midbrain. Despite intensive research, the etiology of PD remains poorly understood. Interestingly, recent studies have implicated neuronal energy dysregulation as one of the key perpetrators of the disease. Supporting this, we have recently demonstrated that pharmacological or genetic activation of AMP kinase (AMPK), a master regulator of cellular energy homeostasis, rescues the pathological phenotypes of Drosophila models of PD. However, little is known about the role of AMPK in the mammalian brain. As an initial attempt to clarify this, we examined the expression of AMPK in rodent brains and found that phospho-AMPK (pAMPK) is disproportionately distributed in the adult mouse brain, being high in the ventral midbrain where the SN resides and relatively lower in regions such as the cortex-reflecting perhaps the unique energy demands of midbrain DA neurons. Importantly, the physiologically higher level of midbrain pAMPK is significantly reduced in aged mice and also in Parkin-deficient mice; the loss of function of which in humans causes recessive Parkinsonism. Not surprisingly, the expression of PGC-1α, a downstream target of AMPK activity, and a key regulator of mitochondrial biogenesis, mirrors the expression pattern of pAMPK. Similar observations were made with PINK1-deficient mice. Finally, we showed that metformin administration restores the level of midbrain pAMPK and PGC-1α expression in Parkin-deficient mice. Taken together, our results suggest that the disruption of AMPK-PGC-1α axis in the brains of individuals with Parkin or PINK1 mutations may be a precipitating factor of PD, and that pharmacological AMPK activation may represent a neuroprotective strategy for the disease.

Keywords: AMP kinase; Mitochondria; PGC-1α; PINK1; Parkin; Parkinson’s disease.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenylate Kinase / metabolism*
  • Aging / metabolism
  • Animals
  • Dopaminergic Neurons / metabolism
  • Dopaminergic Neurons / pathology
  • Drug Evaluation, Preclinical
  • Energy Metabolism
  • Enzyme Activation
  • Gene Expression Regulation / drug effects
  • Male
  • Mesencephalon / enzymology*
  • Metformin / pharmacology
  • Metformin / therapeutic use
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Nerve Tissue Proteins / deficiency
  • Nerve Tissue Proteins / genetics
  • Nerve Tissue Proteins / metabolism*
  • Organ Specificity
  • Parkinson Disease Associated Proteins / deficiency
  • Parkinson Disease Associated Proteins / genetics
  • Parkinson Disease Associated Proteins / metabolism*
  • Pars Compacta / enzymology
  • Peroxisome Proliferator-Activated Receptor Gamma Coactivator 1-alpha / biosynthesis
  • Peroxisome Proliferator-Activated Receptor Gamma Coactivator 1-alpha / genetics
  • Phosphorylation
  • Protein Kinases / deficiency*
  • Protein Kinases / genetics
  • Protein Processing, Post-Translational / drug effects
  • Ubiquitin-Protein Ligases / deficiency*
  • Ubiquitin-Protein Ligases / genetics

Substances

  • Nerve Tissue Proteins
  • Parkinson Disease Associated Proteins
  • Peroxisome Proliferator-Activated Receptor Gamma Coactivator 1-alpha
  • Ppargc1a protein, mouse
  • Metformin
  • Ubiquitin-Protein Ligases
  • parkin protein
  • Protein Kinases
  • PTEN-induced putative kinase
  • Adenylate Kinase