Abstract
The heroin analogue 1-methyl-4-phenylpyridinium, MPP(+), both in vitro and in vivo, produces death of dopaminergic substantia nigral cells by inhibiting the mitochondrial NADH dehydrogenase multienzyme complex, producing a syndrome indistinguishable from Parkinson's disease. Similarly, a fragment of amyloid protein, Abeta(1-42), is lethal to hippocampal cells, producing recent memory deficits characteristic of Alzheimer's disease. Here we show that addition of 4 mM d-beta-hydroxybutyrate protected cultured mesencephalic neurons from MPP(+) toxicity and hippocampal neurons from Abeta(1-42) toxicity. Our previous work in heart showed that ketone bodies, normal metabolites, can correct defects in mitochondrial energy generation. The ability of ketone bodies to protect neurons in culture suggests that defects in mitochondrial energy generation contribute to the pathophysiology of both brain diseases. These findings further suggest that ketone bodies may play a therapeutic role in these most common forms of human neurodegeneration.
MeSH Terms
1-Methyl-4-phenylpyridinium/antagonists & inhibitors,toxicity
3-Hydroxybutyric Acid/pharmacology
Alzheimer Disease
Amyloid beta-Peptides/antagonists & inhibitors,toxicity
Animals
Cells, Cultured
Culture Media, Serum-Free
Embryo, Mammalian
Hippocampus/cytology
Humans
Ketone Bodies/pharmacology
Mesencephalon/cytology
Microtubule-Associated Proteins/analysis
Models, Neurological
Neurons/cytology,drug effects
Parkinson Disease
Peptide Fragments/antagonists & inhibitors,toxicity
Rats
Tyrosine 3-Monooxygenase/analysis
Chemicals
Amyloid beta-Peptides
Culture Media, Serum-Free
Ketone Bodies
Microtubule-Associated Proteins
Peptide Fragments
amyloid beta-protein (1-42)
Tyrosine 3-Monooxygenase
1-Methyl-4-phenylpyridinium
3-Hydroxybutyric Acid
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Kashiwaya Y
Division of Neurology, Tottori University Faculty of Medicine, Yonago, 683-8503 Tottori, Japan.
Takeshima T
Mori N
Nakashima K
Clarke K
Veech R L
References (32)
32 references, click to expand
-
Beta-secretase cleavage of Alzheimer's amyloid precursor protein by the transmembrane aspartic protease BACE.
Science. 1999 Oct 22;286(5440):735-41
PMID: 10531052
-
Cognitive changes and modified processing of amyloid precursor protein in the cortical and hippocampal system after cholinergic synapse loss and muscarinic receptor activation.
Proc Natl Acad Sci U S A. 1999 Oct 12;96(21):12108-13
PMID: 10518584
-
Hydroperoxide metabolism in mammalian organs.
Physiol Rev. 1979 Jul;59(3):527-605
PMID: 37532
-
Prevalence of Alzheimer's disease in a community population of older persons. Higher than previously reported.
JAMA. 1989 Nov 10;262(18):2551-6
PMID: 2810583
-
Alzheimer's disease: the amyloid cascade hypothesis.
Science. 1992 Apr 10;256(5054):184-5
PMID: 1566067
-
Efficacy of the ketogenic diet for intractable seizure disorders: review of 58 cases.
Epilepsia. 1992 Nov-Dec;33(6):1132-6
PMID: 1464275
-
The amyloid precursor protein in ischemic brain injury and chronic hypoperfusion.
Ann N Y Acad Sci. 1993 Sep 24;695:190-3
PMID: 8239281
-
Characterization of the inhibitory mechanism of 1-methyl-4-phenylpyridinium and 4-phenylpyridine analogs in inner membrane preparations.
J Biol Chem. 1994 Feb 4;269(5):3167-74
PMID: 8106350
-
Inhibition of energy metabolism alters the processing of amyloid precursor protein and induces a potentially amyloidogenic derivative.
J Biol Chem. 1994 May 6;269(18):13623-8
PMID: 8175797
-
Mesencephalic type 1 astrocytes rescue dopaminergic neurons from death induced by serum deprivation.
J Neurosci. 1994 Aug;14(8):4769-79
PMID: 7913955
-
Control of glucose utilization in working perfused rat heart.
J Biol Chem. 1994 Oct 14;269(41):25502-14
PMID: 7929251
-
Astrocyte-dependent and -independent phases of the development and survival of rat embryonic day 14 mesencephalic, dopaminergic neurons in culture.
Neuroscience. 1994 Jun;60(3):809-23
PMID: 7936201
-
Insulin, ketone bodies, and mitochondrial energy transduction.
FASEB J. 1995 May;9(8):651-8
PMID: 7768357
-
Regulation of mitochondrial pyruvate dehydrogenase activity by tau protein kinase I/glycogen synthase kinase 3beta in brain.
Proc Natl Acad Sci U S A. 1996 Apr 2;93(7):2719-23
PMID: 8610107
-
Water-soluble Abeta (N-40, N-42) oligomers in normal and Alzheimer disease brains.
J Biol Chem. 1996 Feb 23;271(8):4077-81
PMID: 8626743
-
Altered beta-APP metabolism after head injury and its relationship to the aetiology of Alzheimer's disease.
Acta Neurochir Suppl. 1996;66:96-102
PMID: 8780805
-
Inhibition of NADH oxidation by 1-methyl-4-phenylpyridinium analogs as the basis for the prediction of the inhibitory potency of novel compounds.
J Biochem Toxicol. 1996;11(1):33-43
PMID: 8806050
-
Nontoxic amyloid beta peptide 1-42 suppresses acetylcholine synthesis. Possible role in cholinergic dysfunction in Alzheimer's disease.
J Biol Chem. 1997 Jan 24;272(4):2038-41
PMID: 8999897
-
Alzheimer's disease: genotypes, phenotypes, and treatments.
Science. 1997 Jan 31;275(5300):630-1
PMID: 9019820
-
Probing the ubiquinone reduction site of mitochondrial complex I using novel cationic inhibitors.
J Biol Chem. 1997 Jun 27;272(26):16176-83
PMID: 9195916
-
Substrate signaling by insulin: a ketone bodies ratio mimics insulin action in heart.
Am J Cardiol. 1997 Aug 4;80(3A):50A-64A
PMID: 9293956
-
Association between features of the insulin resistance syndrome and Alzheimer's disease independently of apolipoprotein E4 phenotype: cross sectional population based study.
BMJ. 1997 Oct 25;315(7115):1045-9
PMID: 9366728
-
Mitochondrial diseases in man and mouse.
Science. 1999 Mar 5;283(5407):1482-8
PMID: 10066162
-
Titrating the effects of mitochondrial complex I impairment in the cell physiology.
J Biol Chem. 1999 Jun 4;274(23):16188-97
PMID: 10347173
-
Bcl-2 family proteins regulate the release of apoptogenic cytochrome c by the mitochondrial channel VDAC.
Nature. 1999 Jun 3;399(6735):483-7
PMID: 10365962
-
Can biotechnology move us toward a sustainable society?
Nat Biotechnol. 1999 Jun;17(6):541-4
PMID: 10385316
-
New order from neurological disorders.
Nature. 1999 Jun 24;399(6738 Suppl):A3-5
PMID: 10392574
-
Translating cell biology into therapeutic advances in Alzheimer's disease.
Nature. 1999 Jun 24;399(6738 Suppl):A23-31
PMID: 10392577
-
Prospects for new restorative and neuroprotective treatments in Parkinson's disease.
Nature. 1999 Jun 24;399(6738 Suppl):A32-9
PMID: 10392578
-
Immunization with amyloid-beta attenuates Alzheimer-disease-like pathology in the PDAPP mouse.
Nature. 1999 Jul 8;400(6740):173-7
PMID: 10408445
-
Deficit of in vivo mitochondrial ATP production in patients with Friedreich ataxia.
Proc Natl Acad Sci U S A. 1999 Sep 28;96(20):11492-5
PMID: 10500204
-
Microchemical pathology of the cerebral cortex in pre-senile dementias.
Trans Am Neurol Assoc. 1964;89:15-6
PMID: 5828492