Polyphenols in Parkinson’s Disease: A Systematic Review of In Vivo Studies
Abstract
:1. Introduction
2. Studies in Animal Models
2.1. Pure Compounds
2.1.1. 6−hydroxydopamine Model
2.1.2. N-methyl-4-phenyl-1,2,3,6-tetrahydropyridine Model
2.1.3. Rotenone Model
2.1.4. Lipopolysaccharide Model
2.1.5. Homocysteine Model
2.2. Beverages and Extracts
3. Epidemiological Studies
4. The Permeability of Polyphenols Across the Blood-Brain Barrier
5. Polyphenols and the Microbiota–Gut–Brain Axis
6. Summary and Conclusions
Author Contributions
Conflicts of Interest
Abbreviations
4-HNE | 4-hydroxynonenal |
6-OHDA | 6-Hydroxydopamine |
AChE | Acetylcholinesterase |
AKT | serine/threonine protein kinase |
ARE | Antioxidant responsive element |
Bax | Bcl-2-like protein 4 |
Bcl-2 | B-cell lymphoma 2 |
BDNF | Brain-derived neurotrophic factor. |
b.w. | Body weight |
CaMKII | Ca2+/calmodulin-dependent protein kinase II |
Casp-3 | Caspase-3 |
Casp-8 | Caspase-8 |
Casp-9 | Caspase-9 |
CAT | Catalase |
CHIP | C terminus Hsp70 interacting protein |
CNS | Central nervous system |
COI | Cytochrome c oxidase I |
COX-2 | Cyclooxygenase-2 |
CUR | Curcumin |
DA | Dopamine |
DARPP-32 | Dopamine- and cAMP-regulated phosphoprotein |
DAT | Dopamine transporter |
DJ-1 | Protein deglycase |
DOPAC | 3,4-dihydroxyphenylacetic acid |
EC | (−)-Epicatechin |
ECG | Epicatechin gallate |
EGC | (−)-Epigallocatechin |
EGCG | Epigallocatechin-3-gallate |
ERK | Extracellular signal-regulated kinase protein-serine/threonine kinase |
FA | Ferulic acid |
GAPDH | Glyceraldehyde 3-phosphate dehydrogenase |
GABA | Gamma-aminobutyric acid |
GCLC | Glutamate cysteine ligase catalytic subunit |
GCLM | Glutamate cysteine ligase modifier subunit |
GDNF | Glial cell-derived neurotrophic factor |
GFAP | Glial fibrillary acidic protein |
GLu | Glutamate (or Glutamic acid) |
GPx | Glutathione peroxidase |
GR | Glutathione reductase |
GRP-78 | 78 kDa Glucose-regulated protein |
GS | Glutamine synthetase |
GSH | Reduced glutathione |
GSSG | Oxidized glutathione |
GTPs | Green tea polyphenols |
Hcy | Homocysteine |
HO-1 | Heme oxygenase-1 |
Hsp70s | The 70 kDa heat shock proteins |
HVA | Homovanillic acid |
Iba1 | Ionised calcium binding adapter molecule 1 |
i.p. | Intraperitoneally |
IL-1β | Interleukin 1 beta |
IL-6 | Interleukin 6 |
IL-10 | Interleukin 10 |
iNOS | Inducible nitric oxide synthase |
JNK | c-Jun N-terminal kinase |
JSE | Juglandis Semen extract |
L-DOPA | l-3,4-dihydroxyphenylalanine |
LPS | Lipopolysaccharide |
MAO | Monoamine oxidase |
MAPK | Mitogen-activated protein kinase |
MB | Maneb |
MDA | Malondialdehyde |
MMPs | N-methyl-4-phenyl-1,2,3,6-tetrahydropyridine |
MPTP | Mitochondrial transmembrane potentials |
mTORC1 | Mammalian target of rapamycin complex 1 |
NF-кB | Nuclear factor-кB |
nNOS | Nuclear nitric oxide synthase |
NO | Nitric oxide |
Nrf2 | Nuclear factor (erythroid-derived 2)-like 2 |
NQO1 | NAD(P)H: quinone oxidoreductase 1 |
(p) | probenocid |
p-4E-BP1 | Phosphorylated 4E-binding protein 1 |
p38 | MAP Kinase (MAPK), CSBP Cytokinin-Specific Binding Protein or RK |
PARP | Poly(ADP-ribose) polymerase |
PCA | Protocatechuic acid |
PCs | Protein carbonyls |
PD | Parkinson disease |
PGE2 | Prostaglandin E2 |
PI3K | phosphoinositide 3-kinase |
PKC | Protein kinase C |
PLA2 | Phospholipases A2 |
p.o. | Orally |
PQ | Resveratrol |
RES | Paraquat |
ROS | Reactive oxygen species |
ROT | Rotenone |
SA | Syringic acid |
SIL | Silibinin |
SNpc | Substantia nigra pars compacta |
SOD | Superoxide dismutase |
TBARS | Thiobarbituric acid reactive substances |
TH | Tyrosine hydroxylase |
TNF-α | Tumor necrosis factor alpha |
TRAP | Total reactive antioxidant potential |
Trx | Thioredoxin |
TF | Theaflavin |
TPs | Tea polyphenols |
TrkB | Tropomyosin receptor kinase B |
TUNEL | Terminal deoxynucleotidyl transferase dUTP nick end labeling |
UA | Urolithin A |
VMAT2 | Vesicular monoamine transporter-2 |
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Compound, Route and Dosage | Species (Sex) | Neurotoxin | Neuroprotective Effects | References |
---|---|---|---|---|
Naringenin (50 mg/kg; p.o.) 4-day pre-treatment | Sprague- Dawley rats (male) | 6-OHDA | ↑TH-positive cells ↑DA, DOPAC, and HVA | Zbarsky et al. 2005 [14] |
Naringenin (70 mg/kg; p.o.) 4-day pre-treatment | C57BL/6 mice (male) | 6-OHDA | ↑rotational behavior ↑TH-positive neurons ↑DA, DOPAC, and HVA ↑protein expression of NRf2, HO-1, GCLC, GCLM, HO-1 ↑GSH ↓ROS ↑protein expression of JNK and p38 | Lou et al. 2014 [15] |
Naringin (80 mg/kg; i.p.) 1-day pre-treatment and 6-day post-treatment | C57BL/6 mice (male) | 6-OHDA | ↑TH-positive neurons ↓Iba1-positive microglia ↓IL-1β positive microglia ↓6-OHDA—inducedp-4E-BP1 | Kim et al. 2016 [16] |
Hesperidin (50 mg/kg; p.o.) 28-day post-treatment | aged C57BL/6 mice (female) | 6-OHDA | ↓time spent immobile (antidepressant-like activity) ↑spatial learning and memory skill ↑DA, DOPAC and HVA ↑GSH level and TRAP ↑CAT and GPx activity ↓ROS levels ↓6-OHDA—induced GR activity | Antunes et al. 2014 [17] |
Hesperetin (50 mg/kg; p.o.) 1-week post-treatment | Wistar rats (male) | 6-OHDA | ↑rotational behavior ↑motor balance and coordination ↓MDA ↑GSH ↑CAT ↑Bcl-2 ↓GFAP expression and DNA fragmentation | Kiasalari et al. 2016 [18] |
Quercetin (50 mg/kg; i.g.) 4-day pre-treatment | Sprague-Dawley rats (male) | 6-OHDA | No effects | Zbarsky et al. 2005 [14] |
Quercetin (50–200 mg/kg; i.p.) once a day for one week before and for one week after the 6-OHDA-infusion (100 mg/kg; i.p.) twice a day for one week before and for one week after the 6-OHDA-infusion | Wistar rats (male) | 6-OHDA | No effects | Kääriäinen et al. 2008 [19] |
Quercetin (30 mg/kg; i.p.) 14-day post-treatment | Sprague-Dawley rats (male) | 6-OHDA | ↑DA ↑neuronal density of striatum ↑Nissl-stained neurons ↓PCs ↓LPO ↑GSH | Haleagrahara et al. 2011 [20] |
Rutin (25 mg/kg; p.o.) 3-week pre-treatment | Wistar rats (male) | 6-OHDA | ↑motor co-ordination ↑working performance ↑DA and DOPAC ↓TNF-α and IL-1β ↓NO ↓TBARS, H2O2, and PCs ↑GSH ↑GPx, GR, SOD and CAT activity | Khan et al. 2012 [21] |
Troxerutin (150 mg/kg; p.o.) 1-week pre-treatment | Wistar rats (male) | 6-OHDA | ↑motor function ↑numbers of TH-positive ↑Nissl positive neurons ↑DA and DOPAC ↓MDA, ROS, NO2 ↓GFAP ↓TBARS, H2O2, and PCs ↓DNA fragmentation ↑GPx, GR, SOD and CAT activity | Baluchnejadmojarad et al. 2017 [22] |
Myricitrin (60 mg/kg; i.p.) 1-day pre-treatment and 6-day post-treatment | C57BL/6 mice (male) | 6-OHDA | ↑motor function ↑TH-positive neurons ↓Iba1-positive microglia ↓TNF-α-positive microglia ↑TH activity ↑p-4E-BP1 and p-TH levels ↑mTORC1 | Kim et al. 2016 [16] |
Myricetin (5 µl of solution 0.5 mg/mL injected into lateral cerebral ventricle) 7-day post-treatment | Wistar rats (female) | 6-OHDA | ↑TH-positive neurons ↓iron-staining cells ↑DA, DOPAC and HVA ↑TH and GAPDH mRNA | Ma et al. 2007 [23] |
Genistein (10 mg/kg; i.p.) a single dose 1 h before surgery | Sprague–Dawley rats (male) | 6-OHDA | ↑rotational behavior ↑Nissl-stained neurons | Baluchnejadmojarad et al. 2009 [24] |
Puerarin (0.12 mg/kg; i.p.) 10-day co-treatment t | Sprague–Dawley rats (male) | 6-OHDA | ↑TH-positive cells ↑DA, DOPAC and HVA ↓degeneration of DAargic neurons ↓apoptosis (TUNEL assay) ↓Bax protein expression ↑GDNF protein expression | Zhu et al. 2010 [25] |
Baicalein (200 mg/kg; i.g.) 1-week pre-treatment | Sprague–Dawley rats (male) | 6-OHDA | ↓muscle tremor ↑GABA level ↓ GLu level ↓COI mRNA expression ↓GABA-T protein expression ↑GS protein expression | Yu et al. 2012 [26] |
Tangeretin (20 mg/kg; p.o.) 4-day pre-treatment | Sprague-Dawley rats (male) | 6-OHDA | ↑TH-positive cells ↑DA | Datla et al. 2001 [27] |
EGCG (1 and 2 mg/kg; p.o.) 14-day pre-treatment | Sprague–Dawley rats (female) | 6-OHDA | ↓postural abnormalities ↑ability to cross a narrow beam | Leaver et al. 2009 [28] |
Pelargonidin (10 and/or 20 mg/kg; p.o.) 1 day before and on the day of surgery. | Wistar rats (male) | 6-OHDA | ↑rotational behavior ↑SN neurons ↓TBARS | Roghani et al. 2010 [29] |
RES (10, 20 and 40 mg/kg; i.g.) 10-week post-treatment | Sprague–Dawley rats (male) | 6-OHDA | ↑rotational behavior ↓COX-2 and TNF-α mRNA ↓COX-2 protein | Jin et al. 2008 [30] |
RES (20 mg/kg; i.g.) 14-day post-treatment treatment | Wistar rats (male) | 6-OHDA | ↑rotational behavior ↑total nigral cells and DA neurons ↑total antioxidant capacity ↓number of apoptotic nigral cells ↓ROS | Wang et al. 2011 [31] |
RES (20 mg/kg; i.p.) 15-day pre-treatment | Wistar rats (male) | 6-OHDA | ↑rotational behaviour, motor coordination ↑TH-positive cells ↑DA, DOPAC ↓TBARS, PCs ↓PLA2, COX-2 protein ↑activity of GSH, SOD, CAT, GPx, GR ↑Na+/K+-ATPase activity | Khan et al. 2010 [32] |
Piceid (50 mg/kg; p.o.), 14-day co-treatment | Sprague-Dawley rats (male) | 6-OHDA | ↓motor defects ↓MDA ↑SOD activity | Chen et al. 2015 [33] |
CUR (200 mg/kg; i.g.) twice a day, 24-day pre-treatment | Wistar rats (female) | 6-OHDA | ↑TH-positive cells ↑DA, DOPAC and HVA ↓iron-stained cells | Du et al. 2012 [34] |
CUR (200 mg/kg; i.p.) 7-day post-treatment | ICR mice (male) | 6-OHDA | ↑TH-positive cells ↓GFAP, Iba1 protein ↑SOD1 level | Tripanichkul et al. 2013 [35] |
CA (20 mg/kg; p.o.) 3 times per week, 3-week pre-treatment | Wistar rats (male) | 6-OHDA | ↑locomotor time and distance traveled ↓TBARS ↑GSH ↑GCLC, GCLM, GR, and SOD protein ↓phosphorylated JNK and p38 protein (↓activation) ↑Bcl-2/Bax ↑cleaved caspase-3/caspase-3 and cleaved PARP/PARP | Wu et al. 2015 [36] |
SA (20 mg/kg; p.o.) 2-day pre-treatment | Wistar rats (male) | 6-OHDA | ↑rotational behavior ↑Nissl-stained, TH-positive and total SN neurons ↓iron-stained cells ↓MDA and nitrite level | Zare et al. 2015 [37] |
Ellagic acid (50 mg/kg; i.g) 10-day post-treatment | Wistar rats (male) | 6-OHDA | ↓motor deficiencies ↓IL-1β and TNF-α protein | Farbood et al. 2015 [38] |
Delta 9-tetrahydrocannabinol (3 mg/kg; i.p.) 2-week post-treatment | Sprague-Dawley rats (male) | 6-OHDA | ↑DA ↑TH mRNA and activity | Lastres-Becker et al. 2005 [39] |
EGCG (2 and 10 mg/kg; p.o.) 10-day pre-treatment | C57-BL mice (male) | MPTP | ↑DA ↑TH level and activity ↓MPTP-induced activity of SOD and CAT | Levites et al. 2001 [40] |
EGCG (2 mg/kg; p.o.) 10-day pre-treatment | C57-BL mice (male) | MPTP | ↑DA ↑TH level and activity ↓α-synuclein ↓Bcl-2, Bax protein ↑PKCα protein | Mandel et al. 2004 [41] |
EGCG (25 mg/kg; p.o.) 1-day pre-treatment and 5-day co-treatment | C57B6 mice (male) | MPTP | ↑TH-positive neurons ↑DA, DOPAC and HVA ↑TH activity ↓nNOS mRNAs, nNOS level and activity | Choi et al. 2002 [42] |
EGCG (25 mg/kg; p.o.) 7-day post-treatment | C57 black mice (male) | MPTP | ↑rotational behaviour ↑DA and DOPAC ↓PCs ↑ferroportin protein | Xu et al. 2017 [43] |
EGCG (10 mg/kg; i.g.) 14-day post-treatment | C57/BL6 mice (male) | MPTP | ↑DA, DOPAC and HVA ↑Ras expression | Reznichenko et al. 2010 [44] |
EGCG (10 , 50 mg/kg; i.p.) 10-day pre-treatment and 4-day co-treatment | C57Bl/6 mice (male) | MPTP | ↑TH-positive neurons ↓iNOS expression | Kim et al. 2010 [45] |
EGCG (25 , 50 mg/kg/day; i.g.) 1-day pre-treatment and 20-day post-treatment | C57BL/6 mice (male) | MPTP | ↓motor coordination ↑TH-positive neurons ↓CD3+CD4+/CD3+CD8+ T cells ↓TNF-α and IL-6 protein in plasma | Zhou et al. 2018 [46] |
Acacetin (10 mg/kg; p.o) 3-day co-treatment | C57BL/6 mice (male) | MPTP | ↓movement impairment ↑TH-positive neurons ↓damage in DAergic cells ↑DA ↓iNOS mRNA and COX-2 mRNA | Kim et al. 2012 [47] |
Baicalein (10 mg/kg; i.g.) 5-day co-treatment | C57BL/6 mice (male) | MPTP | ↓motor dysfunction ↓MPTP-induced glutamatergic transmission, presynaptic glutamate release and upregulation of synaptic GluR1 subunit | Xue et al. 2014 [48] |
Baicalein (1 and 10 mg/kg; i.g.) 7-day pre-treatment | C57BL/6 mice (male) | MPTP | ↓motor dysfunction ↑TH-positive neurons ↓GFAP, Iba1 protein ↓phosphorylated ERK and JNK- ↓activation | Lee et al. 2014 [49] |
7,8-dihydroxyflavone (5, 20, 40, and 100 mg/kg; i.p) 7-day pre-and 7-day co-treatment | B57/BL mice (male) | MPTP | ↑TH-positive neurons ↑TrkB activity ↓caspase-3 protein | Jang et al. 2010 [50] |
Tangeretin (10 mg/kg; i.p.) 4-day pre-treatment | C57BL/6 mice (male) | MPTP | ↑TH-positive neurons ↑DA ↑GRP-78 protein | Takano et al. 2007 [51] |
Nobiletin (10 mg/kg; i.p.) 1-day pre-treatment and 6-day-post-treatment | Sprague Dawley (SD) rats (female) | MPTP | ↑TH-positive neurons ↑DA ↓Iba1 protein and IL-1β ↑GDNF protein | Jeong et al. 2015 [52] |
Nobiletin (50 mg/kg; i.p.) 14-day post-treatment | C57BL/6 mice (male) | MPTP | ↓motor and cognitive impairment ↑Ca2+/calmodulin-dependent protein kinase II (CaMKII) ↑DARPP-32, dopamine- and cAMP-regulated phosphoprotein-32 | Yabuki et al. 2014 [53] |
Naringin (8 and 800 mg/kg; i.p) 1-day pre-and 6-day post-treatment | Sprague Dawley (SD) rats (female) | MPTP | ↑TH-positive neurons ↑GDNF protein ↑mTORC1 activity ↓TNF-α protein | Leem et al. 2014 [54] |
Kaempferol (25, 50 and 100 mg/kg; p.o) 14-day pre-treatment | C57BL/6 mice (male) | MPTP | ↑Motor behavioral ↑TH-positive neurons ↑DA and DOPAC ↓MDA ↑activity of SOD and GPx | Li and Pu 2011 [55] |
Quercetin (100, 200 mg/kg; p.o.) 10-day pre-treatment and 4-day co-treatment | C57BL/6 mice (male) | MPTP | ↑motor balance and coordination ↑DA ↑GPx, SOD activity ↑Na+, K+-ATPase ↓4-HNE ↑AChE activity | Lv et al. 2012 [56] |
Morin (5, 20, 40, and 100 mg/kg; i.p) 5-day pre-and 5-day co-treatment | B57/BL mice (male) | MPTP | ↓cataleptic time (bar test) and ↑ number of steps (drag test) ↑DA ↑TH-positive neurons | Zhang et al. 2010 [57] |
Silibinin (1 or 10 mg/kg; i.p.) 5-day co-treatment | C57BL/6 mice (male) | MPTP | ↓Motor dysfunction ↓DAergic neuron damage | Lee et al. 2015 [58] |
Silibinin (50, 100 mg/kg; i.p.) 5-day co-treatment | Sprague Dawley (female) | MPTP | ↑TH-positive neurons ↓IL-1β, TNF-α and iNOS protein | Jung et al. 2014 [59] |
Silibinin (100, 200 mg/kg; i.g.) 7-day co-treatment | albino rats of Charles– Foster strain (male) | MPTP | ↑spatial memory and locomotor activity ↓mitochondrial complex-I and IV activity ↑mitochondrial complex-II and V activity ↑mitochondrial membrane potential ↓NO, MDA ↑SOD activity ↓caspase-3 and NFκB protein | Geed et al. 2014 [60] |
Genistein (10 mg/kg; i.p.) 3-day pre-treatment and 5-day-co-treatment | C57BL/6 mice (male) | MPTP | ↑TH-positive neurons ↑DA, DOPAC and HVA ↑TH and DAT mRNA ↓Bcl-2 mRNA | Liu et al. 2008 [61] |
Gastrodin (10, 30 and 60 mg/kg; p.o.) 15-day co-treatment | C57BL/6 mice (male) | MPTP | ↓bradykinesia and motor impairment ↑TH protein ↓GFAP protein ↑Bcl-2 protein ↓Bax and caspase-3 protein ↓PARP cleavage | Kumar et al. 2013 [62] |
Tanshinone I (5 and 10 mg/kg; i.g.) 7-day pre- and co-treatment | C57BL/6 mice (male) | MPTP | ↓Motor dysfunction ↑DA, DOPAC and HVA ↑TH-positive neurons ↓Iba1-positive activated microglia cells ↓TNF-α and IL-10 protein | Wang et al. 2015 [63] |
Ferulic acid (40 mg/kg; i.g.) 3-day pre-treatment and 4-day co-treatment | C57BL/6 mice (male) | MPTP | ↑motor balance and coordination ↓anxiety ↓degeneration of DAargic neurons ↓Bax/Bcl-2 ratio | Nagarajan et al. 2015 [64] |
Madecassoside (15, 30 and 60 mg/kg; i.g) 7-day pre-treatment and 14-day co-treatment | Wistar rats m (male) | MPTP | ↑limb coordination and limb placing ↑DA, DOPAC and HVA ↓MDA ↑GSH ↑Bcl-2/Bax ratio ↑BDNF protein | Xu et al. 2013 [65] |
Curcumin (50 mg/kg; i.p.) 3-times at time points 1, 3, and 7 h post first MPTP injection | ICR mice (male) | MPTP | ↑DA ↑density of DA neurons | Vajragupta et al. 2003 [66] |
Curcumin (80 mg/kg; i.p.) 7-day co-treatment | Swiss albino mice (male) | MPTP | ↑DA and DOPAC ↓MAO B activity | Rajeswari et al. 2008 [67] |
Curcumin (150 mg/kg; p.o.) 1-week pre-treatment | C57BL/6 mice (male) | MPTP | ↑motor performance (rotarod test) ↓steep reduction intotal ambulation time (open field test) ↑DA, DOPAC and HVA ↓GFAP over-expression ↓IL-6 and TNF-α protein ↓iNOS protein and NO content | Ojha et al. 2012 [68] |
Ginsenoside Rg1 (5, 10 and 20 mg/kg; i.p.) 3-day pre-treatment and 5-day co-treatment | C57-BL mice (male) | MPTP | ↑numbers of TH-positive and Nissl positive neurons in SN ↓TUNEL positive neurons in SN ↑GSH ↓MPTP-induced SOD activity ↓MPTP-induced phosphor—JNK and phospho-c-Jun level | Chen et al. 2005 [69] |
Piceid (100 and 200 mg/kg; p.o.) 7-day co-treatment and 7-day post-treatment | C57BL/6 mice (male) | MPTP | ↑locomotor activity ↑TH-positive neurons ↑SOD activity ↓MDA level ↑p-Akt expression ↓activated caspase 3 expression | Chen et al. 2015 [33] |
TF (10 mg/kg; i.g.) 35-day co-treatment | C57BL/6 mice (male) | MPTP/p | ↑Locomotor activity ↑TH- and DAT-positive neurons ↓caspase-3, 8, and 9 protein | Anandhan et al. 2012 [70] |
TF (10 mg/kg; i.g.) 3-day pre-treatment and 4-day co-treatment | C57BL/6 mice (male) | MPTP | ↑Locomotor activity ↑DAT-positive neurons ↓TBARS, ↑ GSH ↑SOD, CAT and GPx activity ↓MAO-B activity | Anandhan et al. 2012b [71] |
TF (10 mg/kg; i.g.) 35-day co-treatment | C57BL/6 mice (male) | MPTP/p | ↓Akinesia, catalepsy ↓IL-1β, TNF-α, IL-6 as well as MPTP-induced IL-4 and IL-10 ↓GFAP and COX-2 protein ↑Bcl-2 protein ↓Bax protein | Anandhan et al. 2013 [72] |
Apigenin (5, 10 and 20 mg/kg; p.o.), luteolin (10 and 20 mg/kg; p.o.) 5-day pre-treatment and 21-day co-treatment | Swiss-albino mice (male) | MPTP/p | ↑Locomotor activity ↑TH-positive neurons ↓MDA, ↑GSH ↑SOD and CAT activity ↓GFAP and TNF-α protein ↑BDNF protein ↓MAO-B activity | Patil et al. 2014 [73] |
SA (20 mg/kg; i.g.) 35-day co-treatment | C57BL/6 mice (male) | MPTP/p | ↓impairment of motor coordination ↑TH- and DAT-positive neurons ↑TH, DAT and VMAT2 protein ↑DA, DOPAC and HVA ↓TBARS, ↑ GSH ↑SOD, CAT and GPx activity ↓IL-1β, TNF-α protein ↓COX-2 protein | Rekha et al. 2014 [74] |
Quercetin (25, 50, 75 mg/kg; i.p.) 4-day post-treatment | Sprague Dawley rats (male) | ROT | ↑rotational behavior ↑TH-positive neurons ↓TUNEL positive neurons ↑DA ↑complex-I activity ↑GSH, GSSG ↓ROT-induced activity of SOD and CAT | Karuppagounder et al. 2013 [75] |
CUR (20 mg/kg; i.g.) 50-day co-treatment | Lewis rats (male) | ROT | ↓postural impairment ↑motor coordination ↑TH activity ↓MDA, ↑ GSH ↑HO-1 and NQO1 protein ↑Akt/Nrf2 phosphorylation (activation) | Cui et al. 2016 [76] |
Piceid (80 mg/kg; i.g.) 5-week co-treatment | Sprague Dawley rats (male) | ROT | ↓postural impairment ↑motor coordination ↑TH-positive neurons ↑ATP ↑Trx, GSH ↑SOD activity | Chen et al. 2015 [33] |
FA (80 mg/kg; i.g.) 4-week co-treatment | Wistar rats (male) | ROT | ↑TH-positive neurons ↑SOD and CAT activity ↓MDA, ↑ GSH ↓GFAP and Iba1 protein ↓IL-1β, TNF-α, IL-6 protein ↓COX-2 and iNOS protein | Ojha et al. 2015 [77] |
Sesamol (15 mg/kg; p.o.) naringenin(10 mg/kg; p.o.) 10-day post-treatment | Wistar rats (male) | ROT | ↑motor coordination ↑body weight ↓degenerated neurons ↑TH and ubiquitin expression ↑parkin, CHIP, and DJ1 expression ↓caspase-9 and 3 protein ↑Hsp70 and Hsp90 protein | Sonia Angeline et al. 2013 [78] |
EGCG (10 mg/kg; i.p.) 24 h before LPS and continues for 7 days | Sprague Dawley rats (male) | LPS | ↑TH-positive neurons ↑DA ↓TNF-α and nitrite | AL-amri et al. 2013 [79] |
CUR (50 mg/kg; i.p.) 10-day treatment beginning 5 days prior to Hcy | Lewis rats (male) | Hcy | ↑Locomotor Activity ↑Nissl-stained neurons ↑Bcl-2 protein and ↓ Bax protein ↓Bax/Bcl-2 | Mansouri et al. 2012 [80] |
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Kujawska, M.; Jodynis-Liebert, J. Polyphenols in Parkinson’s Disease: A Systematic Review of In Vivo Studies. Nutrients 2018, 10, 642. https://doi.org/10.3390/nu10050642
Kujawska M, Jodynis-Liebert J. Polyphenols in Parkinson’s Disease: A Systematic Review of In Vivo Studies. Nutrients. 2018; 10(5):642. https://doi.org/10.3390/nu10050642
Chicago/Turabian StyleKujawska, Małgorzata, and Jadwiga Jodynis-Liebert. 2018. "Polyphenols in Parkinson’s Disease: A Systematic Review of In Vivo Studies" Nutrients 10, no. 5: 642. https://doi.org/10.3390/nu10050642
APA StyleKujawska, M., & Jodynis-Liebert, J. (2018). Polyphenols in Parkinson’s Disease: A Systematic Review of In Vivo Studies. Nutrients, 10(5), 642. https://doi.org/10.3390/nu10050642