Oxidative Stress, Mitochondrial Dysfunction, and Neuroprotection of Polyphenols with Respect to Resveratrol in Parkinson’s Disease
Abstract
:1. Introduction
2. Mitochondrial Biology
2.1. Mitochondria and ROS Generation
2.2. Mitochondrial Oxidative Stress and Antioxidative Systems
2.3. Oxidative Stress and Mitochondrial Dysfunction
2.4. Oxidative Stress and Cell Death
3. Parkinson’s Disease, Oxidative Stress, and Mitochondrial Dysfunction
4. Polyphenols and Their Properties
4.1. Resveratrol’s Neuroprotective Effects against Parkinson’s Disease
4.2. Clinical Trials of Resveratrol on Neurodegenerative Diseases
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
Glossary
AD | Alzheimer’s disease | MPTP | 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine |
ADP | Adenosine diphosphate | mtDNA | Mitochondrial DNA |
AMPK | 5′-adenosine monophosphate (AMP)-activated protein kinase | mTOR/mTORC1 | Mammalian target of rapamycin/ mammalian target of rapamycin complex I |
APAF1 | Apoptotic peptidase-activating factor 1 | nDNA | Nucleus DNA |
ATP | Adenosine triphosphate | NCLX | Na+/Ca2+ exchanger |
ATP13A2 | Atpase type13a2 | NF-κB | Nuclear factor kappa-light-chain-enhancer of activated B cells |
BAK | Bcl2-antagonist/killer | NOX | Nicotinamide adenine dinucleotide phosphate oxidase |
BAX | Bcl-2-associated x protein | NRF | Nuclear respiratory factor |
Ca2+ | Calcium | 6-OHDA | 6-hydroxydopamine |
CoQ | Co-enzyme q | OM | Outer membrane |
CR | Caloric restriction | OXPHOS | Oxidative phosphorylation |
CVD | Cardiovascular diseases | PD | Parkinson’s disease |
DJ-1 | Daisuke-junko-1 | PGC | Peroxisome proliferator-activated receptors (PPAR) γ coactivator |
ER | Endoplasmic reticulum | PINK1 | Phosphatase and tensin homologue (PTEN)-induced putative kinase 1 |
ERK1/2 | Extracellular signal-regulated kinase 1/2 | POLG1 | Polymerase gamma 1 |
ETC | Electric transport chain | PPAR | Peroxisome proliferator-activated receptor |
FBXO7 | F-box only protein 7 | PRX | Peroxiredoxin |
GPX | Gsh peroxidase | Redox | Reduction-oxidization |
GR | Glutathione reductase | ROS | Reactive oxygen species |
GSSG | Glutathione disulfide | rRNA | Ribosomal rna |
GSH | Glutathione | SOD | Superoxide dismutase |
IM | Inner membrane | (mt)SSB | (Mitochondrial) single-stranded binding protein |
IMS | Intermembrane space | SIRT-1 | Sirtuin-1 |
LRRK2 | Leucine rich repeat kinase 2 | SNpc | Substantia nigra pars compacta |
MCU | Mitochondrial Ca2+ uniporter | TCA | Tricarboxylic acid |
ΔΨm | Mitochondrial membrane potential | TFAM | Mitochondrial transcription factor A |
MOA | Monoamine oxidase | TRX | Thioredoxin |
MOMP | Mitochondrial outer membrane permeabilization | ULK1 | Unc-51 like autophagy activating kinase 1 |
mPTP | Mitochondrial permeability transition pore | VPS35 | Vacuolar protein sorting 35 |
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Symbol | Locus | Gene Name | Inheritance | Disease | Pathological Effects on the Mitochondria | Ref. |
---|---|---|---|---|---|---|
PARK1 PARK4 | 4q21-22 | SNCA | AD | EOPD | Mutant SNCA aggregates more easily, binds to mitochondrial membranes, inhibits Complex I activity damages mitochondrial structures, and causes mitochondrial toxicity. | [138,139,140] |
PARK2 | 6q25.2-q27 | Parkin | AR | EOPD | Point mutations in parkin can inhibit its ability to interact with E2 and other protein substrates, ubiquitinate substrates, and translocate to depolarized mitochondria and induce mitophagy. | [141,142] |
PARK3 | 2p13 | Unknown | AD | Classical PD | Unconfirmed, but may be a risk factor | [143] |
PARK5 | 4p13 | UCHL1 | AD | Classical PD | Mutations in UCHL1 can lead to impaired ubiquitin proteasome system (UPS), accumulation of damaged proteins, and formation of Lewy bodies. | [144,145,146,147] |
PARK6 | 1p35-p36 | PINK1 | AR | EOPD | Mutations at PINK1 impair mitophagy and mitochondrial quality control by disrupting activation and recruitment of parkin to the mitochondria and the normal phosphorylation of proteins that facilitate mitophagy. | [142,148] |
PARK7 | 1p36 | DJ-1 | AR | EOPD | Mutations in DJ-1 cause mitochondria damage from oxidative stress, loss of ability to prevent α-synuclein fibrillation, and increased likelihood of mitochondria depolarization and fragmentation. | [149] |
PARK8 | 12q12 | LRRK2 | AD | Classical PD | Mutations in LRRK2 result in increased mitochondrial fragmentation, increased basal activity, increased susceptibility to oxidative damage, and the disruption of mitophagy. | [150,151] |
PARK9 | 1p36 | ATP13A2 | AR | Kufor-Rakeb syndrome; atypical dementia with spasticity, dementia, and supranuclear glaze palsy | Mutations in ATP13A2 have been associated with reduced ATP production, increased mitochondrial fragmentation, increased ROS production, increased glycolysis (which aggravates mitochondrial dysfunction), and defective mitophagy. | [132,144,152,153,154,155,156] |
PARK10 | 1p32 | Unknown | Risk factor | Classical PD | Confirmed susceptible locus, but unknown pathology | [143] |
PARK11 | 2q36-27 | Unknown, not GIGYF2 | AD | Late-onset PD | May be a risk factor, but not independently confirmed | [143] |
PARK12 | Xq21-q25 | Unknown | Risk factor | Classical PD | Confirmed susceptible locus; may be possible risk factor; pathology unknown | [143] |
PARK13 | 2p12 | HTRA2 | AD or risk factor | Classical PD | HTRA2 mutations could possibly lead to insufficient protein degradation, atypical mitochondrial morphology and function, and increased mitochondrial susceptibility to oxidative stress. | [144,157,158,159] |
PARK14 | 22q13.1 | PLA2G6 | AR | Early-onset dystonia–parkinsonism | PLA2G6 participates in the regulation of Ca2+ within the cell. Impaired PLA2G6-dependent store-operated Ca2+ signaling causes autophagy dysfunction, while increased influx of Ca2+ into the mitochondria is associated with oxidative stress. | [144,160] |
PARK15 | 22q12-q13 | FBXO7 | AR | Early-onset parkinsonian-pyramidal syndrome | Mutations in the FBXO7 gene can cause protein aggregation in the mitochondria and inhibition of mitophagy and ROS generation. | [143,161,162] |
PARK16 | 1q32 | Unknown | Risk factor | Classical PD | Confirmed susceptibility locus | [143] |
PARK17 | 16q11.2 | VPS35 | AD | Classical PD | Mutations in VPS35 lead to increased mitochondrial fission/fragmentation. | [161,163] |
PARK18 | 3q27.1 | EIF4G1 | AD | Classical PD | The exact mechanism of this mutation has yet to be understood. | [143,161] |
PARK19 | 1p31.3 | DNAJC6 | AR | Juvenile onset, atypical PD | DNAJC6 encodes HPS40 Auxilin, but the mechanism of the mutation is not yet understood. | [164,165] |
PARK20 | 21q22.11 | SYNJ1 | AR | Juvenile onset, atypical PD | SYNJ1 results in an increase in oxidative stress and change in mitochondrial morphology | [164,166] |
PARK21 | 3q22.1 | DNAJC13 | AD | Late-onset PD | Mutations in DNAJC13 disrupts normal endosomal trafficking and results in α-synuclein aggregation in the lysosomes. | [164,167,168] |
PARK22 | 7p11.2 | CHCHD2 | AD | Late-onset PD | Deficiency in CHCHD2 leads to reduced cytochrome c oxidase (COX) activity, decreased mitochondrial membrane potential, increased ROS production, and increased mitochondrial fragmentation. | [169,170] |
PARK23 | 15q22 | VPS13C | AR | EOPD, rapid progression | Mutations in the VPS13C gene have been associated with reduced mitochondrial membrane potential, increased mitochondrial fragmentation, and upregulated PINK1/parkin-dependent mitophagy. | [161,171] |
Type of Study | Sample | Purpose | Dose | Duration | Completion Date | Main Results | Ref. |
---|---|---|---|---|---|---|---|
DBRCT, crossover, placebo-controlled phase I | 20 healthy part. | To study resveratrol pharmacokinetics when taken together with levodopa | BIA 6-512 (trans-RSV) 25 mg, 50 mg, 100 mg dose | 11 weeks | 23 July 2004 | Not Posted | NCT: NCT03091543 |
DBRCT, placebo-controlled phase I | 80 healthy part. | To study the tolerability and pharmacokinetics of resveratrol and its effects on levodopa | Oral BIA 6-512 (trans-RSV) 25 mg, 50 mg, 100 mg dose | 17 weeks | 28 February 2005 | Not Posted | NCT: NCT03091868 |
Single-center, open-label, RCT, two-way crossover | 24 healthy part. | To study the effect of food on resveratrol pharmacokinetics | Oral BIA 6-512 400 mg dose following a breakfast (Test) or at least 8 h of fasting (Reference) | 7 weeks | 7 July 2005 | Not Posted | NCT: NCT03095092 |
DBRCT, crossover, placebo-controlled phase I | 40 healthy part. | To study the safety and tolerability of different doses of BIA 6-512 six times a day and to characterize the pharmacokinetics of BIA 6-512 | Oral BIA 6-512 (25, 50, 100, or 150 mg dose) six times a day/4 h intervals | 11 weeks | 29 July 2005 | Not Posted | NCT: NCT03093389 |
DBRCT, placebo-controlled phase I | 25 part. | To compare the pharmacokinetic profile of BIA 6-512 in healthy young and old subjects | Oral BIA 6-512 200 mg every 8 h | 5 weeks | 2 March 2006 | Not Posted | NCT: NCT03095105 |
Single-center, open-label, RCT, two-way crossover | 39 healthy part. | To investigate the effects of BIA 6-512 at steady state on the pharmacokinetics of levodopa when administered with levodopa/benserazide with or without entacapone | Oral BIA 6-512 (25, 50, 75, and 100 mg) plus a single dose of immediate release levodopa/benserazide 200/50 mg with or without a single dose of entacapone 200 mg | 7 weeks | 11 July 2006 | Not Posted | NCT: NCT03094156 |
DBRCT, crossover, placebo-controlled phase I | 38 healthy part. | To investigate the effects of BIA 6-512 at steady state on the pharmacokinetics of levodopa when administered with levodopa/benserazide with or without nebicapone | Oral BIA 6-512 (25, 50, 75, and 100 mg) plus a single dose of immediate release levodopa/benserazide 200/50 mg with or without a single dose of nebicapone 150 mg | 13 weeks | 20 October 2006 | Not Posted | NCT: NCT03097211 |
Type of Study | Sample | Purpose | Dose | Duration | Main Results | Completion Date | Ref. |
---|---|---|---|---|---|---|---|
DBRCT, placebo-controlled parallel | 102 early affected Huntington disease (HD) patients | To study the therapeutic potential of RSV on the caudate volume of HD patients | RSV 40 mg twice a day | 1 year | Not Posted | October 2019 | NCT: NCT02336633 |
DBRCT, placebo-controlled Phase II | 120 patients with mild to moderate dementia most likely due to AD | To study the impact on biomarkers of RSV treatment in patients with mild to moderate AD | Oral RSV 500 mg OD with dose escalation of up to 1000 mg BID | 52 weeks | RSV is safe and well tolerated with nausea, weight loss, and diarrhea as side effects. No benefit on biomarkers CSF Aβ40 and Aβ42, etc. [239,263] Increased brain volume loss | March 2014 | NCT: NCT01504854 |
DBRCT, placebo-controlled 2-period crossover, Phase II | 40 Friederich ataxia (FRDA) patients | To study the efficacy of RSV as a treatment for FRDA | 1 g micronized RSV or placebo twice daily for two 24 week periods | 52 weeks | Recruiting | Ongoing | NCT: NCT03933163 |
Non-randomized, parallel assignment, open label clinical Phase I and II | 27 FRDA patients (n = 15 will receive RSV) | To study the effects of RSV on frataxin levels in FRDA patients and to measure RSV’s effects on markers of oxidative stress, clinical measures of ataxia, and cardiac parameters | RSV 40 mg twice a day | 12 weeks | Not Posted | August 2012 | NCT: NCT01339884 |
Single center, multi-site, DBRCT, placebo-controlled Phase-3 Trial | 27 mild to moderate AD patients | To investigate the efficacy of RSV in delaying the progression of AD | RSV, glucose, and malate supp. delivered in grape juice | 12 months | RSV is safe and well-tolerated at low dose. No significant changes in AD Assessment Scale-cognitive subscale, Mini-Mental State Exam, etc. [239,262] | December 2010 | NCT: NCT00678431 |
Prospective, longitudinal, mixed, analytical, experimental, double-blind, placebo-controlled study | 100 amyotrophic lateral sclerosis (ALS) patients | To assess the clinical improvement of ALS patients treated with curcumin and RSV liposomed polyphenols with dutasteride | RSV 75 mg, curcumin 200 mg, and dutasteride 0.5 mg | 6 months | Not Yet Recruiting | Not Yet Recruiting | NCT: NCT04654689 |
RCT, parallel assignment, quadruple-blind, Phase I | 48 part. | To study the safety and CSF penetration of oral BDPP (grape seed polyphonic extract, RSV) in humans to assess possible benefits of BDPP to MCI | Low, moderate, and high dose of BDPP | 4 months | Recruiting | Ongoing | NCT: NCT02502253 |
RCT, crossover assignment, open label | 12 patients with hereditary spastic paraplegia (SPG5) | To study the efficacy of Xenbilox, Tahor, and RSV in decreasing oxysterols synthesis, reducing cholesterol proudction, regulating bile production, and/or providing neuroprotection | Xenbilox, Tahor, or resveratrol (80 mg for 2 months) | 2 months | Not Posted | 27 September 2017 | NCT: NCT02314208 |
RCT, crossover assignment, open label, Phase I | 12 patients with mild to moderate AD | To study the efficacy and safety of administering etanercept with nutritional supp. versus administering nutritional supp. alone | Nutritional supp. (curcum., luteol., theaflav., lip., acid, fish oil, quercet., resveratr.) with or without etanercept | 16 weeks | Not Posted | October 2015 | NCT: NCT01716637 |
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Kung, H.-C.; Lin, K.-J.; Kung, C.-T.; Lin, T.-K. Oxidative Stress, Mitochondrial Dysfunction, and Neuroprotection of Polyphenols with Respect to Resveratrol in Parkinson’s Disease. Biomedicines 2021, 9, 918. https://doi.org/10.3390/biomedicines9080918
Kung H-C, Lin K-J, Kung C-T, Lin T-K. Oxidative Stress, Mitochondrial Dysfunction, and Neuroprotection of Polyphenols with Respect to Resveratrol in Parkinson’s Disease. Biomedicines. 2021; 9(8):918. https://doi.org/10.3390/biomedicines9080918
Chicago/Turabian StyleKung, Heng-Chung, Kai-Jung Lin, Chia-Te Kung, and Tsu-Kung Lin. 2021. "Oxidative Stress, Mitochondrial Dysfunction, and Neuroprotection of Polyphenols with Respect to Resveratrol in Parkinson’s Disease" Biomedicines 9, no. 8: 918. https://doi.org/10.3390/biomedicines9080918