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Aging and disease    2020, Vol. 11 Issue (6) : 1537-1566     DOI: 10.14336/AD.2020.0225
Review Article |
Oxidative Stress at the Crossroads of Aging, Stroke and Depression
Anwen Shao1,*, Danfeng Lin2, Lingling Wang2, Sheng Tu3, Cameron Lenahan4,5, Jianmin Zhang1,6,7
1Department of Neurosurgery, Second Affiliated Hospital, School of Medicine, Zhejiang University, Zhejiang, China.
2Department of Surgical Oncology, Second Affiliated Hospital, School of Medicine, Zhejiang University, Zhejiang, China.
3State Key Laboratory for Diagnosis and Treatment of Infectious Diseases, Collaborative Innovation Center for Diagnosis and Treatment of Infectious Diseases, The First Affiliated Hospital, College of Medicine, Zhejiang University, Zhejiang, China.
4Burrell College of Osteopathic Medicine, Las Cruces, USA.
5Center for Neuroscience Research, School of Medicine, Loma Linda University, Loma Linda, CA, USA.
6Brain Research Institute, Zhejiang University, Zhejiang, China.
7Collaborative Innovation Center for Brain Science, Zhejiang University, Zhejiang, China.
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Epidemiologic studies have shown that in the aging society, a person dies from stroke every 3 minutes and 42 seconds, and vast numbers of people experience depression around the globe. The high prevalence and disability rates of stroke and depression introduce enormous challenges to public health. Accumulating evidence reveals that stroke is tightly associated with depression, and both diseases are linked to oxidative stress (OS). This review summarizes the mechanisms of OS and OS-mediated pathological processes, such as inflammation, apoptosis, and the microbial-gut-brain axis in stroke and depression. Pathological changes can lead to neuronal cell death, neurological deficits, and brain injury through DNA damage and the oxidation of lipids and proteins, which exacerbate the development of these two disorders. Additionally, aging accelerates the progression of stroke and depression by overactive OS and reduced antioxidant defenses. This review also discusses the efficacy and safety of several antioxidants and antidepressants in stroke and depression. Herein, we propose a crosstalk between OS, aging, stroke, and depression, and provide potential therapeutic strategies for the treatment of stroke and depression.

Keywords oxidative stress      stroke      subarachnoid hemorrhage      intracerebral hemorrhage      depression      mitochondrial dysfunction      antioxidant      aging     
Corresponding Authors: Shao Anwen   
About author:

These authors contributed equally to this work.

Just Accepted Date: 01 March 2020   Issue Date: 19 November 2020
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Shao Anwen
Lin Danfeng
Wang Lingling
Tu Sheng
Lenahan Cameron
Zhang Jianmin
Cite this article:   
Shao Anwen,Lin Danfeng,Wang Lingling, et al. Oxidative Stress at the Crossroads of Aging, Stroke and Depression[J]. Aging and disease, 2020, 11(6): 1537-1566.
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Figure 1.  Schematic model of the main source of ROS and redox reaction. ROS are generated mainly from enzymatic reactions in the cytoplasm, endoplasmic reticulum, mitochondria, and peroxisome [300]. Specifically, overproduced mitoROS can affect metabolic pathways, such as alteration of protein translation, oxidation of lipid and DNA, and impairment of ATP synthesis [301]. Moreover, assembled NOX (NOX1 and NOX2) complex transports an electron from cytosolic NADPH to oxygen to form superoxide on the extracellular side [13]. The NOX4 complex rapidly converts the superoxide to H2O2, which undergoes a Fenton reaction to produce hydroxyl radicals and ions, and to regulate many downstream effects [302]. However, these oxidative events are inhibited by antioxidants, such as SOD and CAT/GPx. Activation of Nrf2-ARE pathway increases antioxidants, such as HO-1, SOD1, and CAT to protect cells from FR accumulation [303].
Figure 2.  Pathogenesis and correlation between stroke and depression. There are different mechanisms in ischemic stroke [16], ICH [17], SAH [304], and depression [10]. Stroke and depression are associated with oxidative stress. Due to overactive OS activity and impaired anti-OS defenses, 16-30% of ischemic stroke survivors [31, 32], 25% of ICH [33] patients, and 50% of SAH [34] patients may develop depression later, but the age groups vary among studies. Conversely, depression increases the risk of stroke by 33% in patients who experience stressful life events [37].
Figure 3.  Mechanism of oxidative stress in ischemic stroke.
Figure 4.  Schematic model of oxidative mechanisms in ICH and SAH, especially associated with hemoglobin (Hb). During the hemoglobin-heme-iron axis, Hb is released into the extracellular space and is accompanied by an abundance of superoxide generated from the non-enzymatic oxidation of Hb [46]. This oxidation of Hb produces methemoglobin, which releases heme to stimulate lipid peroxidation and other oxidative actions around the hematoma in brain tissue. Meanwhile, iron released from Hb degradation is used in the Fenton reaction to transform H2O2 into the hydroxyl radical, leading to increased oxidative damage [47].
Figure 5.  Mechanisms of oxidative stress and OS-mediated cell death pathway in depression.
Figure 6.  Proposed crosslink and interplay among aging, oxidative stress, stroke and depression.
StrokeAntioxidantsAnti-OS activityMechanism of anti-OS activity and others
Ischemic strokefucoxanthinanti-OSinhibit OS via Nrf2/HO-1 signaling pathway
Sirtuin 6
Korean Red Ginseng
11-Keto-β-boswellic acid
S-allyl cysteine
monomethyl fumarate
ursolic acidupregulate Nrf2 pathway and expression levels of BDNF
HP-1cAMPK-Nrf2 pathway activation, without any toxicity after penetrating the brain
andrographolideup-regulate Nrf2/HO-1 expression via regulation of p38 MAPK
2,2,6,6-tetramethyl-1-piperidinoxylinhibit p38 MAPK and p53 cascades
3H-1,2-Dithiole-3-thionesuppress microglia activation; inhibit CNS peripheral cell infiltration
3-n-butylphthalideanti-OS; attenuate mitochondrial dysfunctioninhibit OS; activate Nrf2/HO-1/AMPK pathway; improve MMP and complexes I-IV
melatoninactivate SIRT1 signaling
progesteronesuppress mtROS production and block MPTP
5-methoxyindole-2-carboxylic acidincrease antioxidative capacity via the Nrf2 signaling pathway; reduce OS
SkQR1protect mitochondria
GKanti-OS; protect blood vesselsfaciliate angiogenesis through HIF-1α/VEGF and JAK2/STAT3 pathway
leonurineupregulate VEGF expression by Nrf-2 pathway
astragaloside IVanti-OS; protect BBBNrf2 signaling pathway
Tao Hong Si Wu Decoctionanti-OS
schizandrin Aanti-OS; anti-inflammationAMPK/Nrf2 pathway
tryptanthrindecrease pro-inflammatory cytokines in BV2 microglia cells via Nrf2/HO-1 signaling and NF-κB
3, 14, 19-triacetyl andrographolideinhibit TLR4/NF-κB; upregulate Nrf2/ARE
quercetinsuppress LPS-induced oxidant production and expression of adhesion molecules
apelin 13affect AMPK/GSK-3β pathway activated by AR/Gα/PLC/IP3/CaMKK signaling;
diosgeninsuppress TLR4/MyD88/NF-kB-induced inflammation
irisinregulate ROS-NLRP3 inflammation
TPENinhibit OS and inflammation
N-acetyl lysyltyrosylcysteine amide
Tanshinone IIA
berberinereduce the infarct volume and brain edema; improve motor function;
melilotus officinalisreduce cerebral thrombosis and inflammatory mediators
DHCprotect BBB; inhibit inflammation by affecting ROS, NOX2, NOX4, NF-ĸB, and NO
resveratrolmodulate intestinal flora-mediated Th17/Tregs and Th1/Th2 polarity shift
EPO-cyclosporinesuppress the innate immune response to OS, inflammation and MAPK family signaling
rheinanti-OS; anti-apoptosisinhibit OS and apoptosis
deuterohemin His peptide-6
radix scrophulariae
clostridium butyricum
adiponectinattenuate mitochondrial vulnerability through the JAK2/STAT3 pathway
YiQiFuMaireduce PKCδ/Drp1-mediated mitochondrial fission
withania somniferainhibit PARP1-AIF-Mediated caspase-independent apoptosis
SMXZFsuppress H2O2-induced neuronal apoptosis through caspase-3/ROCK1/MLC pathway
diallyl trisufidesuppress OGD-induced apoptosis via the PI3K/Akt-mediated Nrf2/HO-1 signaling pathway
plumbaginanti-OS; anti-inflammation; anti-apoptosisinhibit OS, inflammation and apoptosis
hollow prussian blue nanozymes
Sirt3promote autophagyregulate the AMPK-mTOR pathway; decrease H2O2; increase ATP generation
β-arrestin-1interact two major components of the BECN1 autophagic core complex
vitexinanti-autophagyinhibit autophagy through the mTOR/Ulk1 pathway
silibininsuppress the mitochondrial and autophagic cell death pathways
3-methyladenineinhibit expression of LC3 and Beclin-1
astragalosidesblock OGD-R-induced apoptosis and autophagy by inhibiting OS and ER stress
isoquercetinanti-OS; anti-inflammation; anti-apoptosis; anti-autophagyinfluence TLR4, NF-κB and caspase-1; ERK1/2, JNK1/2, and MAPK; TNF-α, IL-1β and IL-6; NOX4/ROS/NF-κB signaling pathway; CREB, Bax, Bcl-2, and caspase-3
ECGGaffect PI3K/AKT/eNOS and NRF2/HO-1 signaling pathway; promote neovascularization and cell proliferation
ICHgreen teaanti-OSreduce EBI
mammalian sterile 20-like kinase-1
melatoninreduce DNA damage and MPTP opening
dexmedetomidineinhibit PGC-1α pathway inactivation and mtROS
oleuropeinalleviate brain edema; preserve the BBB
isoliquiritigeninanti-OS; anti-inflammationROS/NF-κB, NLRP3 inflammasome pathway and Nrf2-mediated activities
Sirt3suppress NLRP3 and IL-1β levels
Sodium Benzoateanti-OS; anti-apoptosisregulate DJ-1/Akt/IKK/NFκB pathway to inhibit neuronal apoptosis and mtROS
carnosinedecrease brain edema, BBB disruption, OS and neuronal apoptosis
metforminanti-OS; anti-inflammation; anti-apoptosis;inhibit OS, apoptosis and neuroinflammation
hydrogen gas
protocatechuic acid
hypoxia-inducible factor prolyl hydroxylase domain (HIF-PHD) metalloenzymesabolish ATF4-dependent neuronal death
SAHdimethyl formamideanti-OSimprove EBI and cognitive dysfunction via the Keap1-Nrf2-ARE system
telmisartananti-OS; inhibit cerebral vasospasmdecrease TXNIP expression
nebivololincrease GSH-Px activity
curcuminreduce TNF-α
curcumin nanoparticlesanti-OS; anti-inflammationkeep BBB integrity; activate glutamate transporter-1; inhibit inflammation and OS
UAsuppress the TLR4-mediated inflammatory pathway
pterostilbeneinhibit NLRP3 inflammasome and Nox2-related OS
apigeninanti-OS; anti-apoptosisinhibit EBI through the dual effects of anti-oxidation and anti-apoptosis
docosahexaenoic acid
sodium hydrosulfide
AVE 0991decreases OS and neuronal apoptosis through Mas/PKA/p-CREB/UCP-2 pathway
allicinextenuate brain edema and BBB dysfunction;
mangiferinanti-OS; anti-inflammation;
regulate the mitochondrial apoptosis pathway, NLRP3 and NF-κB.
memantineinhibit inflammation-mediated BBB breakdown and ER stress-based apoptosis
Salvianolic acid Bactivate Nrf2 signaling pathway
Salvianolic acid Aassociate with Nrf2 signaling, the phosphorylation of ERK and P38 MAPK signaling
mitoquinonepromote autophagyactivate mitophagy via Keap1/Nrf2/PHB2 (prohibitin 2) pathway
melatoninpromote autophagystimulate autophagy to inhibit apoptotic death of neural cells
Table 1  Antioxidants in Stroke.
AntioxidantsAnti-OS activityMechanism of anti-OS activity and others
Depressionbay 60-7550anti-OSdownregulate gp91phox; activate the cAMP/cGMP-pVASP-CREB-BDNF signaling pathway
p-chloro-diphenyl diselenidemodulate glutamate neurotransmission
homocysteineinhibit ROS by activating NMDA receptors
vitamin Dsuppress OS
2,3,5,4'-tetrahydroxystilbene-2-O-β-D-glucopyranosideanti-OS; anti-inflammationreduce proinflammatory factors; restore the diminished Akt signaling pathway; faciliate astrocyte proliferation and neurogenesis
vorinostatmodulate NF-κB p65, COX-2 and phosphorylated JNK levels
melatonininhibit OS and inflammation
selenium-containing compounds
ketamineincrease glutamate release; affect energy metabolism
mitochondrial uncoupling protein 2anti-OS; anti-inflammation; anti-apoptosisdownregulate the activation of NLRP3 inflammasome; suppress the ROS-TXNIP-NLRP3 pathway in astrocytes
dl-3-n-butylphthalideinhibit OS, inflammatory responses and apoptosis
25-methoxyhispidol A
allicinreduce neuroinflammation, OS, iron overaccumulation; inhibit neuronal apoptosis in the hippocampus
AVLEsuppress the apoptosis of hippocampus cells via regulation of Bcl-2/Bax pathways
Table 2  Antioxidants in Depression.
Co-antioxidants in stroke and depression from experiments
Ischemic strokeICHSAH
Clinical trials and outcomes in strokeClinical trials and outcomes in depression
flavonoidmeta-analysishigh flavonoid reduces risk of strokeRCThigher flavonoid links to lower depression risk especially among women
UARCT and URICOICTUSUA is safe; UA enhances outcomes of strokecohort studies and meta-analysisUA are associated with low risk of depression hospitalization and lower MDA levels
melatoninRCTearly melatonin usage ameliorates the brain injury of asphyxial newbornsRCTbuspirone-melatonin therapy benefits cognitive function
Reviewmelatonin does not affect mood disorders
Table 3  Co-antioxidants in stroke and depression from experiments.
Antioxidants in PSDClinical trialsOutcomes
fluoxetineFOCUSnot support routine use of fluoxetine in preventing PSD or promoting function recovery
fluoxetine/paroxetinemeta-analysis of 12 trialsfluoxetine is the worst choice for PSD treatment; paroxetine is the best drug in terms of efficacy and acceptability
meta-analysis of 20 RCTscitalopram has similar efficacy and safety as other SSRIs but acts faster than them
fluoxetineFLAMEexhibit a positive connection between motor recovery
escitalopramCochrane reviewescitalopram is the best tolerated SSRI, followed by sertraline and paroxetine for PSD
escitalopramRCTnot take effects on depressive symptoms; diarrhea is more likely to occur
escitalopramRCTeffective at decreasing the incidence of depression in nondepressed patients
CitalopramRCTsafe for patients with acute ischemic stroke
CitalopramRCTdifferent effects in different stages of PSD
citalopramRCTSSRI treatment is well tolerated and beneficial in PSD
SSRIregistry-based score-matched follow-up studypre-stroke SSRI use increases risk of the hemorrhagic stroke; no increased stroke severity and mortality ischemic stroke
milnacipranRCTmilnacipran prevents post-stroke depression; safe to use without serious adverse events
Table 4  Antidepressants in PSD treatment.
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