Physical Exercise-Induced Myokines in Neurodegenerative Diseases
Abstract
:1. Introduction
2. Myokines and Neuronal Health
2.1. Apelin
2.2. BDNF
2.3. CTSB
2.4. CX3CL1
2.5. FGF2
2.6. FGF21
2.7. IGF-1
2.8. Irisin
2.9. LIF
3. Molecular Mechanisms Underlying Myokine Action in Neurodegenerative Diseases
3.1. Cell Survival
Myokine | ND | Function | Mechanism | Model | Reference |
---|---|---|---|---|---|
Apelin | AD | Decreased cell death | Aβ-induced autophagy ↓ Caspase-3 activity ↓ mTOR phosphorylation ↑ | Rats injected with Aβ25–35 and apelin-13 | [62] |
Decreased cell death | BDNF/TrkB signaling pathway ↑ | Rats injected with streptozotocin and apelin-13 | [64] | ||
Anti-inflammation | Astrocyte and microglia activation ↓ IL-1β and TNF-α expression ↓ | ||||
Decreased cell death | RIP1 and RIP3 expression ↓ | Rats injected with streptozotocin and apelin-13 | [67] | ||
Anti-inflammation | TNF-α expression ↓ | ||||
PD | Decreased cell death | ERK1/2 phosphorylation ↑ ER stress ↓ | SH-SY5Y cells treated with MPP+ and apelin-13 | [60] | |
Decreased cell death | PI3K signaling pathway ↑ Cytoplasmic cytochrome c ↓ Cleaved caspase-3 ↓ | SH-SY5Y cells treated with 6-OHDA and apelin-13 | [61] | ||
Increased α-synuclein clearance | PI3K/Akt/mTOR-autophagy signaling pathway ↑ | SH-SY5Y cells treated with MPP+ and apelin-36 | [65] | ||
Decreased cell death | IRE1α/XBP1/CHOP signaling pathway ↓ | Mice injected with MPTP and apelin-13 | [273] | ||
Increased α-synuclein clearance | Autophagy ↑ | ||||
Increased α-synuclein clearance | AMPK/mTOR/ULK1-autophagy pathway ↑ | SH-SY5Y cells treated with rotenone and apelin-13 | [66] | ||
Decreased cell death | ASK1/JNK signaling pathway ↓ | Mice injected with MPTP and apelin-36 | [274] | ||
Caspase-3 activity ↓ | |||||
Antioxidative stress | GSH and SOD ↑ | ||||
ALS | Pro-inflammation | Microglia activation ↑ | SOD1-G93A mice crossed with apelin−/− mice | [68] | |
BDNF | AD | Decreased Aβ production | BACE1 and PSEN1 ↓ | APPswe mice injected with TAT-BDNF peptide Rats injected with scopolamine and TAT-BDNF peptide | [275] |
Decreased tau phosphorylation | GSK3β activation ↓ | ||||
HD | Increased neurogenesis | TrkB phosphorylation ↑ | N171-82Q mice administered with 4′-DMA-7,8-DHF by oral gavage | [276] | |
CTSB | AD | Increased Aβ clearance | Proteolytic activity of CTSB itself | hAPPJ20 mice injected with Lenti-CTSB Primary cortical neurons from hAPPJ20 mice infected with Lenti-CTSB In vitro cleavage assay using Aβ1–42 and CTSB | [107] |
Increased Aβ clearance | Lamp1 expression ↑ | APP/PS1 mice injected with AAV-CTSB | [111] | ||
CX3CL1 | AD | Pro-inflammation | IL-6 and TNF-α expression ↑ | hAPPJ20 mice crossed with CX3CR1−/− mice | [127] |
Decreased tau phosphorylation | GSK3α/β activation ↓ | Tau P301L mice injected with AAV-CX3CL1 | [137] | ||
Anti-inflammation | Microglia activation ↓ | ||||
Pro-inflammation | NRF2/HO-1 signaling pathway ↓ | CX3CR1−/− mice injected with AAV-TAUP301L | [148] | ||
Pro-oxidative stress | |||||
Increased neurogenesis | TGF-β/Smad2 signaling pathway ↑ | Tau P301S mice crossed with Tg-CX3CL1 mice | [277] | ||
Anti-inflammation | Microglia activation ↓ | APP/PS1 mice injected with MSCs carrying CX3CL1 | [141] | ||
PD | Anti-inflammation | Microglia activation ↓ | Rats injected with 6-OHDA and CX3CL1 | [135] | |
Anti-inflammation | Microglia activation ↓ | CX3CL1−/− mice injected with MPTP and CX3CL1 | [136] | ||
TNF-α and IL-1β expression ↓ | |||||
Pro-inflammation | Il-1β and IL-6 expression ↑ | CX3CR1−/− mice injected with AAV-α-SYN | [150] | ||
ALS | Pro-inflammation | Microglial activation ↑ IL-1β, iNOS, and TNF-α expression ↑ Arginase 1 and TGF-β expression ↓ NF-κB signaling pathway ↑ | SOD1-G93A mice crossed with CX3CR1−/− mice | [151] | |
Decreased SOD1 clearance | Autophagy ↓ | ||||
FGF2 | AD | Decreased cell death | Akt phosphorylation ↑ | CVEC treated with Aβ1–40 and FGF2 | [278] |
Decreased Aβ production | BACE1 expression ↓ | APP23 mice injected with FGF2 N2a cells transfected with APPswe and treated with FGF2 | [279] | ||
Anti-inflammation | iNOS expression ↓ Astrocyte activation ↓ | ||||
Decreased Aβ production | BACE1 expression ↓ | APPswe-HEK293 cells treated with GCM SH-SY5Y cells treated with FGF2 | [171] | ||
PD | Antioxidative stress | GSH ↑ | Primary rat embryonic mesencephalic cultures treated with 6-OHDA and FGF2 | [280] | |
Decreased cell death | MEK/ERK1/2 signaling pathway ↑ BAD phosphorylation ↑ AIF translocation ↓ PI3K/Akt signaling pathway ↑ | SH-SY5Y cells treated with rotenone and FGF2 Primary ventral mesencephalic cultures treated with rotenone and FGF2 | [281] | ||
Decreased cell death | Caspase-3 expression ↓ | Rats injected with 6-OHDA and PEGylated FGF2 | [282] | ||
Anti-inflammation | Astrocyte activation ↓ | PC12 cells treated with 6-OHDA and PEGylated FGF2 | |||
Decreased cell death | MEK/ERK1/2 signaling pathway ↑ PI3K/Akt signaling pathway ↑ ER stress ↓ | Rats injected with 6-OHDA and FGF2 Primary hippocampal neurons treated with 6-OHDA and FGF2 | [283] | ||
FGF21 | AD | Decreased cell death | Caspase-3 activity ↓ | SH-SY5Y cells treated with Aβ1–42 and FGF21 | [206] |
Anti-inflammation | HSP90/TLR4/NF-kB signaling pathway ↓ | ||||
Decreased cell death | Expression ratio of BCL2 to Bax (BCL2/Bax) ↑ Cleaved caspase-3 ↓ | Rats injected with Aβ25–35 and FGF21 SH-SY5Y cells treated with Aβ25–35 and FGF21 | [207] | ||
Decreased tau phosphorylation | PP2A phosphorylation ↓ | ||||
PD | Increased α-synuclein clearance | SIRT1-autophagy signaling pathway ↑ | Mice injected with MPTP and FGF21 SH-SY5Y cells treated with MPTP and FGF21 | [210] | |
Decreased cell death | Cleaved caspase-3 and JNK phosphorylation ↓ Expression ratio of BCL2 to Bax (BCL2/Bax) ↑ | Mice injected with MPTP and treated with FGF21 via intranasal routine SH-SY5Y cells treated with MPP+ and FGF21 Primary dopaminergic neurons treated with MPP+ and FGF21 | [211] | ||
Anti-inflammation | Astrocyte and microglia activation ↓ IL-1β, IL-12, IFN-γ, and TNF-α expression ↓ | ||||
Enhanced mitochondrial function | AMPK/PGC-1α signaling pathway ↑ | ||||
ALS | Anti-inflammation | Serum TNF-α, MCP-1 level ↓ | SOD1-G93A mice injected with R1Mab1 | [213] | |
IGF-1 | AD | Decreased cell death | Akt phosphorylation ↑ | Rats infused with Aβ25–35 and IGF-1 via subcutaneous osmotic minipump | [237] |
Increased Aβ clearance | Aβ carrier-mediated transport ↑ | APP/PS2 mice injected with IGF-1 Choroid plexus epithelial cell culture system treated with Aβ1–40 and IGF-1 | [238] | ||
Anti-inflammation | Astrocyte activation ↓ | ||||
Decreased cell death | Mitochondrial membrane potential ↑ Cytoplasmic cytochrome c ↓ Cleaved caspase-3 ↓ Expression ratio of BCL-XL to Bax (BCL-XL/Bax) ↑ | SH-SY5Y cells treated with Aβ25–35 and IGF-1 | [284] | ||
Antioxidative stress | SOD and CAT activity ↑ PI3K/Akt/Nrf2/HO-1 signaling pathway ↑ | ||||
Decreased cell death | C-myb expression ↑ | SH-SY5Y cells treated with Aβ25–35 and IGF-1 | [285] | ||
Decreased tau phosphorylation | p25 protein production ↓ μ-Calpain expression ↓ | ||||
Decreased Aβ production | ADAM10 exprssion ↑ BACE1 expression ↓ | APP/PS1 mice injected with IGF-1 | [286] | ||
PD | Decreased cell death | PI3K/Akt signaling pathway ↑ | Rats injected with 6-OHDA and IGF-1 | [232] | |
Decreased cell death | Caspase-3 expression and activity ↓ PARP cleavage ↓ | PC12 cells treated with 6-OHDA and IGF-1 | [287] | ||
Antioxidative stress | NRF2/HO-1 signaling pathway ↑ | ||||
Decreased cell death | ERK1/2/CREB signaling pathway ↑ Akt/GSK3α/β/β-catenin signaling pathway ↑ | Rats injected with 6-OHDA and IGF-1 | [288] | ||
HD | Decreased cell death | PI3K/Akt signaling pathway ↑ Huntingtin phosphorylation ↑ | Primary striatal neurons transfected with mutant huntingtin and treated with IGF-1 SH-SY5Y cells treated with IGF-1 HEK293T cells transfected with mutant huntingtin | [289] | |
ALS | Decreased cell death | Akt/caspase-9/caspase-3 signaling pathway ↓ | SOD1-G93A mice injected with AAV-IGF-1 | [230] | |
Anti-inflammation | Astrocyte activation ↓ | ||||
Anti-inflammation | Astrocyte activation ↓ TNF-α expression ↓ | SOD1-G93A mice crossed with MLC/mIgf-1 transgenic mice | [233] | ||
Decreased cell death | Cleaved caspase-9 ↓ | SOD1-G93A mice injected with AAV-IGF-1 SOD1-G93A astrocyte-neuron coculture system treated with IGF-1 | [290] | ||
Anti-inflammation | Astrocyte and microglia activation ↓ NOS activity and peroxynitrite formation ↓ | ||||
Anti-inflammation | Macrophage invasion ↓ TNF-α expression ↓ | SOD1-G93A mice injected with AAV-IGF-1 | [291] | ||
Decreased cell death | JNK and p38 MAPK phosphorylation ↓ Bax expression ↓ BCL-2 expression ↑ Cleaved caspase-3 and cleaved caspase-9 ↓ | SOD1-G93A mice injected with AAV-IGF-1 | [292] | ||
Anti-inflammation | Astrocyte and microglia activation ↓ | ||||
Irisin | AD | Anti-inflammation | IL-1β and IL-6 level ↓ Akt/IκBα/NF-κB/COX-2 signaling pathway ↓ | Primary hippocampal astrocytes treated with Aβ25–35 and irisin | [293] |
LIF | AD | Decreased cell death | Aβ-induced autophagy ↓ | HT-22 mouse hippocampal cells treated with Aβ1–42 and LIF | [268] |
3.2. Neurogenesis
3.3. Neuroinflammation
3.4. Proteostasis
3.5. Mitochondrial Function and Oxidative Damage
3.6. Aβ Production and Tau Phosphorylation
4. Conclusions and Perspectives
Author Contributions
Funding
Conflicts of Interest
Abbreviations
α-SYN | Alpha-synuclein |
Aβ | Amyloid beta |
AD | Alzheimer’s disease |
AIF | Apoptosis-inducing factor |
ALS | Amyotrophic lateral sclerosis |
AMPK | AMP-activated protein kinase |
APP | Amyloid beta precursor protein |
ASK1 | Apoptosis signal-regulating kinase 1 |
BACE1 | Beta-site APP cleaving enzyme 1 |
BAD | BCL2-associated agonist of cell death |
BAX | BCL2-associated X protein |
BCL2 | B-cell lymphoma 2 |
BCL-XL | B-cell lymphoma-extra large |
BDNF | Brain-derived neurotrophic factor |
CAT | Catalase |
CHOP | C/EBP homologous protein |
c-myb | Cellular myeloblastosis |
COX-2 | Cyclooxygenase 2 |
CREB | cAMP responsive element binding protein |
CTSB | Cathepsin B |
CVEC | Post-capillary venular endothelial cell |
CX3CL1 | C-X3-C motif chemokine ligand 1 |
CX3CR1 | C-X3-C motif chemokine receptor 1 |
ER | Endoplasmic reticulum |
ERK | Extracellular signal-regulated kinase |
FGF2 | Fibroblast growth factor 2 |
FGF21 | Fibroblast growth factor 21 |
4′-DMA-7,8-DHF | 4′-Dimethylamino-7,8- dihydroxyflavone |
GCM | Glioma cell-conditioned medium |
GSH | Glutathione |
GSK3 | Glycogen synthase kinase 3 |
HD | Huntington’s disease |
HO-1 | Heme oxygenase 1 |
HSP90 | Heat shock protein 90 |
IFN-γ | Interferon gamma |
IGF-1 | Insulin-like growth factor 1 |
IκBα | Nuclear factor of kappa light polypeptide gene enhancer in B-cells inhibitor, alpha |
IL-1β | Interleukin 1 beta |
IL-6 | Interleukin 6 |
IL-12 | Interleukin 12 |
iNOS | Inducible nitric oxide synthase |
IRE1α | Inositol-requiring enzyme 1 alpha |
JNK | c-Jun N-terminal kinase |
Lamp1 | Lysosomal-associated membrane protein 1 |
LIF | Leukemia inhibitory factor |
MAPK | Mitogen-activated protein kinase |
MCP-1 | Monocyte chemo-attractant protein 1 |
MEK | Mitogen-activated protein kinase kinase |
MPP+ | 1-Methyl-4-phenylpyridinium |
MPTP | 1-Methyl-4-phenyl-1,2,3,6-tetrahydropyridine |
MSC | Mesenchymal stem cell |
mTOR | Mechanistic target of rapamycin |
NF-κB | Nuclear factor kappa B |
NOS | Nitric oxide synthase |
NRF2 | Nuclear factor erythroid 2-related factor 2 |
PARP | Poly (ADP-ribose) polymerase |
PD | Parkinson’s disease |
PGC-1α | Peroxisome proliferator-activated receptor gamma coactivator 1-alpha |
PI3K | Phosphoinositide 3-kinase |
PP2A | Protein phosphatase 2 |
PSEN1 | Presenilin 1 |
RIP1 | Receptor-interacting protein kinase 1 |
RIP3 | Receptor-interacting protein kinase 3 |
SIRT1 | Sirtuin 1 |
6-OHDA | 6-hydroxydopamine |
Smad2 | Mothers against decapentaplegic homolog 1 |
SOD | Superoxide dismutase |
TAT | Transactivator of transcription |
TGF-β | Transforming growth factor beta |
TLR4 | Toll-like receptor 4 |
TNF-α | Tumor necrosis factor alpha |
TrkB | Tropomyosin receptor kinase B |
ULK1 | Unc-51 like autophagy activating kinase 1 |
XBP1 | X-box binding protein 1 |
Notes
APP/PS1 mice | APP/PS1 mice overexpress human APP with Swedish mutation (K670N and M671L) and presenilin 1, bearing an L166P mutation in neurons driven by thymocyte differentiation antigen 1 (Thy-1) promoter [343]. |
APP/PS2 mice | APP/PS2 mice overexpress human APP with the Swedish mutation and presenilin 2, bearing an N141I mutation driven by the Thy-1 promoter and prion protein (Prnp) promoter, respectively [344,345]. |
APPswe mice | APPswe mice overexpress human APP with the Swedish mutation driven by the Prnp promoter [346]. |
APP23 mice | APP23 mice overexpress human APP with the Swedish mutation in neurons driven by the Thy-1 promoter [347]. |
hAPPJ20 mice | hAPPJ20 mice overexpress human APP with the Swedish mutation and Indiana mutation (V717F) in neurons driven by platelet-derived growth factor (PDGF)-β promoter [348]. |
MLC/mIGF-1 | MLC/mIGF-1 mice express rat mIGF-1, an isoform of IGF-1, cDNA driven by skeletal muscle-specific regulatory elements from the rat myosin light chain (MLC)-1/3 locus [349]. |
N171-82Q mice | N171-82Q mice express an N-terminally truncated huntingtin cDNA that contains 82 glutamines and encompasses the first 171 amino acids of huntingtin (N171-82Q) driven by the Prnp promoter [350]. |
PS19 mice | PS19 mice overexpress human tau with a mutation (P301S) driven by the Prnp promoter [351] |
R1Mab1 | R1Mab1 is an IgG humanized monoclonal antibody with agonistic activity on the fibroblast growth factor receptor 1 (FGFR1) [213]. |
SOD-G93A mice | SOD-G93A mice overexpress human SOD1 with a mutation (G93A) and develop adult-onset motor neuron loss [352]. |
Tau P301L mice | Tau P301L mice overexpress human tau with a mutation (P301L) in neurons driven by the Thy-1 promoter [353]. |
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Lee, B.; Shin, M.; Park, Y.; Won, S.-Y.; Cho, K.S. Physical Exercise-Induced Myokines in Neurodegenerative Diseases. Int. J. Mol. Sci. 2021, 22, 5795. https://doi.org/10.3390/ijms22115795
Lee B, Shin M, Park Y, Won S-Y, Cho KS. Physical Exercise-Induced Myokines in Neurodegenerative Diseases. International Journal of Molecular Sciences. 2021; 22(11):5795. https://doi.org/10.3390/ijms22115795
Chicago/Turabian StyleLee, Banseok, Myeongcheol Shin, Youngjae Park, So-Yoon Won, and Kyoung Sang Cho. 2021. "Physical Exercise-Induced Myokines in Neurodegenerative Diseases" International Journal of Molecular Sciences 22, no. 11: 5795. https://doi.org/10.3390/ijms22115795