Interplay of RNA-Binding Proteins and microRNAs in Neurodegenerative Diseases
Abstract
:1. Introduction
2. RNA-Binding Proteins (RBPs)
2.1. RNA-Binding Motif Proteins (RBM)
2.2. Heterogeneous Nuclear Ribonucleoprotein (hnRNP)
2.3. Trans-Active Response DNA-Binding Protein of 43 kDa (TDP-43)
2.4. FET Proteins
2.5. Embryonic Lethal/Abnormal Visual System (ELAV)/Hu Family
2.6. CUG-BP, ELAV-Like Family (CELF) Proteins
2.7. Regulator of Calcineurin (RCAN)
2.8. Musashi (Msi)
2.9. Fragile X Mental Retardation Protein (FMRP)
2.10. T-Cell Restricted Intracellular Antigen (TIA) Proteins
2.11. Tristetraprolin (TTP)
2.12. Serine/Arginine-Rich Splicing Factor (SRSF)
2.13. Neuro-Oncological Ventral Antigen (NOVA)
2.14. Matrin3
2.15. Poly(A)-Binding Protein (PABP)
2.16. Scaffold Attachment Factor B (SAFB)
2.17. Sm Proteins—Components of Small Nuclear Ribonucleoprotein (snRNP)
2.18. Ribosomal Proteins
3. Involvement of RNA-Binding Proteins in Neuronal microRNA Biogenesis
4. Interplay between RNA-Binding Proteins and microRNAs in Neurodegenerative Disease
4.1. Amyotrophic Lateral Sclerosis (ALS) and Frontotemporal Dementia (FTD)
4.2. Alzheimer’s Disease
4.3. Parkinson’s Disease
4.4. Huntington’s Disease
4.5. Multiple System Atrophy (MSA)
5. Conclusions
Author Contributions
Funding
Conflicts of Interest
Abbreviations
ND | Neurodegenerative disease |
AD | Alzheimer’s disease |
PD | Parkinson’s disease |
HD | Huntington’s disease |
ALS | amyotrophic lateral sclerosis |
FTD | frontotemporal dementia |
MSA | multiple system atrophy |
RBP | RNA-binding protein |
miRNA | microRNA |
RNP | ribonucleoprotein |
RBD | RNA-binding domain |
RRM | RNA recognition motif |
ZF domain | zinc finger domain |
KH domain | heterogeneous nuclear ribonucleoprotein K homology domain |
dsRBD | double-stranded RNA-binding domain |
RBM | RNA-binding motif protein |
hnRNP | heterogeneous nuclear ribonucleoprotein |
hnRNA | heterogeneous nuclear RNA |
mRNA | messenger RNA |
AUF1 | AU-rich element /poly(U)-binding/degradation factor 1 |
PTBP1 | Polypyrimidine tract-binding protein 1 |
FUS | Fused in sarcoma |
TLS | Translated in liposarcoma |
TDP-43 | Trans-active response DNA-binding protein of 43 kDa |
HIV-1 | Human immunodeficiency virus type 1 |
TAR | trans-active response element |
EWS | Ewing sarcoma |
EWSR1 | Ewing sarcoma break point region 1 |
TAF15 | TATA-binding associated factor 15 |
FTLD | frontotemporal lobar degeneration |
ELAV | Embryonic lethal/abnormal visual system |
CELF | CUG triplet repeat RNA-binding protein, Embryonic lethal/abnormal visual system -like family |
RCAN | Regulator of calcineurin |
DSRC | Down syndrome critical region |
NFAT | nuclear factor of activated T cells |
Msi | Musashi |
FMRP | Fragile X mental retardation protein |
FXR | Fragile X-related protein |
TIA | T-cell restricted intracellular antigen |
TIAR | TIA1-related protein |
TTP | Tristetraprolin |
ZFP36 | Zinc finger protein 36 |
3’-UTR | 3’-untranslated region |
SRSF | Serine/arginine-rich splicing factor |
ESE | exonic splicing enhancer |
snRNP | small nuclear ribonucleoprotein |
NOVA | Neuro-oncological ventral antigen |
PABP | Poly(A)-binding protein |
SAFB | Scaffold attachment factor B |
S/MAR | scaffold or matrix attachment region DNA element |
SAP | Scaffold attachment factors -A/B, Acinus and Protein inhibitor of activated signal transducer and activator of transcription |
MSP | multisystem proteinopathy |
pri-miRNA | primary microRNA |
pre-miRNA | microRNA precursor |
RISC | RNA-induced silencing complex |
miR-NID1 | Neurexin-1 intron-derived microRNA |
RALY | RNA-binding protein-associated with lethal yellow mutation |
PRMT1 | Protein arginine N-methyltransferase 1 |
VEGF | Vascular endothelial growth factor |
A | Amyloid |
MECP2 | Methyl CpG-binding protein 2 |
APP | Amyloid precursor protein |
mGluR5 | metabolic Glutamate receptor 5 |
MAP1B | Microtubule-associated protein 1V |
Calm1 | Calmodulin 1 |
circSnx5 | Circular RNA-sorting nexin 5 |
SOCS1 | Suppressor of cytokine signaling 1 |
HTT | huntingtin |
SREK1 | Splicing regulatory glutamic acid and lysine rich protein 1 |
TUNA | T-cell leukemia/lymphoma protein 1 upstream neuron-associated |
EAAC1 | Excitatory amino acid carrier 1 |
GTRAP3-18 | Glutamate transport associated protein 3-18 |
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RBP | Domain [22] | Binding Motif [23,24] | |
---|---|---|---|
RBM | more than one RRM ZF domain (RBM4, 4B, 5, 10, 20, 22, 26, 27) | GCGC(G) | RBM4, 4B, 8A |
GAAGG | RBM5 | ||
AUCCA | RBM6 | ||
GUGUG | RBM24, 38 | ||
GUAG | RBM28 | ||
UACA/UU | RBM41 | ||
AACUA | RBM42 | ||
GACGAC | RBM45 | ||
AUC/GA | RBM46, 47 | ||
AUAUA | RBMS1, S2, S3 | ||
CCA/C | RBMX | ||
CU/ACAA | RBMXL1, XL2, XL3, Y1A1, Y1B, Y1D, Y1E, Y1F, Y1J | ||
hnRNP | one to three RRMs (except hnRNP E, F, H, K, U) three qRRMs (hnRNP F, H)three KH domains (hnRNP E, K)acidic-rich domain (hnRNP C, Q, R, U) | UAGGG | hnRNP A1, A1L2, A2B1, A3 |
UUUUU | hnRNP C, CL1 | ||
GGGAGG | hnRNP F, H1, H2 | ||
CCAA/UC/ACC | hnRNP K | ||
ACAC | hnRNP L | ||
ACANACA | hnRNP LL | ||
UAAU/AU/A | hnRNP DL | ||
TDP-43 | two RRMs, G-rich region | GAAUG | |
FET proteins | RRM, three RGG boxes, SYGQ-rich region, ZF domain | poly(G) | |
ELAV/Hu family | three RRMs, hinge region | poly(U) | |
CELF | three RRMs, hinge region | GUGU | |
RCAN | RRM, LxxP motif, PxIxIT-like motif, TxxP motif | n.d. | |
Msi | two RRMs | UAG | |
FMRP | two KH domains, RGG box | GAC | |
TIA | three RRMS, Q-rich domain | poly(U) | |
TTP | two ZF domains, | AU-rich | |
SRSF | one or two RRMs, RS domain | GGAGGA/G | SRSF 1, 2, 4, 6, 9 |
(A)GCAG(C) | SRSF 2, 4, 5, 8, 10 | ||
GA/GUCAACCNGGCGACA/CG | SRSF 4, 6 | ||
NOVA | three KH domains | U/CCAU/C | |
Matrin3 | two RRMs, two ZF domains | AUCUU | |
PABP | one or four RRMs | poly(A) | |
SAFB | SAP domain, RRM, RG/RGG domain | AG-rich |
Associated RBPs | Related miRNAs | Target Gene(s) | Relation between RBPs and miRNAs | miRNA Abnormalities in Diseases |
---|---|---|---|---|
TDP-43 | miR-181c-5p | TDP-43 | forms a negative feedback loop in miRNA processing [124] | is reduced in the spinal cord of ALS patients [125] |
miR-27b-3p | ||||
miR-8485 | NRXN1 | forms an miRISC complex to decrease genes related to synaptic formation [126] | n.d. | |
FUS/TDP-43 | miR-183/96/182 | PP1 | regulates miRNA biogenesis, which is related to memory formation [129] | is reduced in the frontal cortex of ALS patients [129] |
TAF15 | miR-17-92 | CDKN1A/p21 | regulates miRNA biogenesis to decrease genes related to cell proliferation [132] | is reduced in an SOD1G93A mouse model [133] |
hnRNP A1 | miR-590-3p | n.d. | is cooperatively regulated in neuronal maintenance ? [135] | is increased in the blood cells of FTD patients [135] |
hnRNP H | miR-663a | CDK4, CDK6 | is cooperatively regulated in cellular senescence by targeting genes related to the cell cycle [137] | is increased in the blood cells of ALS patients [138] |
RALY | miR-483 | ATP5I, ATP5G1, ATP5G3, CYC1 | regulates miRNA biogenesis to decrease genes related to mitochondrial metabolism [140] | n.d. |
miR-676 | ||||
miR-877 | ||||
RBM17 | miR-150-5p | VEGF-A | is cooperatively regulated in genes related to growth factors [143] | is reduced in the CSF of ALS patients [145] |
HuD | miR-125a-5p | CAMSAP3 | cooperatively regulates circRNA in aging by targeting genes related to neuronal polarization [148] | is reduced in aging mice [147] |
Matrin-3 | miR-138-5p | n.d. | inhibits miRNA biogenesis in the regulation of neuronal development [152] | n.d. |
Associated RBPs | Related miRNAs | Target Gene(s) | Relation between RBPs and miRNAs | miRNA Abnormalities in Diseases |
---|---|---|---|---|
hnRNP K | miR-7 | ISNR, IRS-2, IDE | intronic miRNA and its host genes, regulating genes involved in the insulin signaling in neuronal cells [156] | is elevated in the brain of AD patients [156] |
Msi2 | miR-7 | n.d. | regulates miRNA biogenesis, which is related to neuronal differentiation [107] | is elevated in the brain of AD patients [156] |
RBM8A | miR-29a | RBM8A | competitively regulates cell proliferation and differentiation [160] | is decreased in the brain and blood cells of AD patients [161] |
RBM45 | miR-4454 | INSR, GLUT4 | competitively regulates insulin response [163] | n.d. |
TIA1/HuC | miR-200a | MECP2 | promotes or inhibits the action for miRNA recruitment on genes critical for neuronal maturation [165] | is altered in an AD model and in AD patients [166,167] |
miR-302c | n.d. | |||
CELF1 | miR-574-5p | mPGES-1 | competitively regulates genes related to inflammation and proliferation [169] | is increased in the cortex of APP KO mice [171] |
miR-206 | MyoD | competitively regulates genes related to differentiation [170] | is increased in the brain of an AD mouse model [172] | |
miR-222 | CDK4 | cooperatively regulates cellular senescence by targeting genes related to the cell cycle [174] | is decreased in the serum of AD patients [173] | |
miR-122 | BCKDK, ALDOA, NDRG3, CCNG1, CAT1 | enhances destabilization of miRNA in the regulation of energy metabolism, stress response and cell cycle [176] | is increased in the brain of AD patients [175] | |
FMRP | miR-128-3p | mGluR5 | competitively regulates astroglial development by targeting glutamate receptor genes [179] | is increased in monocytes of AD patients [178] |
miR-181d | MAP1B, Calm1 | cooperatively regulates axon elongation by targeting genes crucial for calcium signaling [180] | is altered in an AD model and in AD patients [181] | |
miR-125b | NR2A | cooperatively regulates synaptic strength by targeting an NMDA receptor subunit gene [182] | is increased in the CSF of AD patients [183] | |
miR-132 | p250GAP? | cooperatively regulates synaptic strength possibly by targeting genes related to Rho family GTPase [182] | is decreased in the exosome of AD patients [184] | |
hnRNP C | miR-544 | SOCS1 | competitively regulates circRNA in inflammation by targeting genes related to cytokine signaling [185] | is increased in high LOAD risk SNPs [186] |
RCAN1 | miR-324-5p | n.d. | inhibits RBP expression [188] | n.d. |
miR-4738-3p | ||||
EWS | miR-29b | Col4a1, CTGF | negatively regulates miRNA biogenesis in cell senescence by targeting genes related to differentiation [190] | is decreased in the serum of AD patients [192] |
miR-18b | is increased in serum of AD patients [192] | |||
miR-351 | UVRAG | negatively regulates miRNA biogenesis in autophagy by targeting genes related to the autolysosomal pathway [190] | is increased in the hippocampus of an AD mouse model [193] | |
miR-125a | is increased in AD cellular model [194] | |||
PABP | miR-2 | n.d. | facilitates miRISC onto the 3’-UTR of targeting gene [114] | n.d. |
Associated RBPs | Related miRNAs | Target Gene(s) | Relation between RBPs and miRNAs | miRNA Abnormalities in Diseases |
---|---|---|---|---|
DJ-1 | miR-221 | n.d. | positively regulates miRNA expression in neurite outgrowth and neuronal differentiation [204] | is decreased in serum of PD patients [205] |
miR-155 | SOCS1 | negatively regulates miRNA expression in inflammation by targeting genes related to cytokine signaling [206] | is increased in SNpc of a PD mouse model [207] | |
HuD | miR-30a-3p | p27 | competitively regulates proliferation by targeting gene related to cell cycle [209] | is increased in the serum of PD patients [210] |
TTP | miR-9 | Tubb3, HuB, HuC, HuR, NOVA1 | inhibits RBP regulating neuronal differentiation and targeting neuronal markers [212] | is increased in PD patients and a mouse model of PD [210,213] |
Disease | Associated RBPs | Related miRNAs | Target Gene(s) | Relation between RBPs and miRNAs | miRNA Abnormalities in Diseases |
---|---|---|---|---|---|
HD | SRSF6 | miR-193a-5p | OGDHL, ECM1 | forms a negative feedback loop in cancer cell migration and invasion by regulating alternative splicing [217] | is decreased in the blood of Autism patients [218] |
PTBP1 | miR-195-5p | ETV1 | competitively regulates circRNA in BTB permeability by targeting genes related to tight junction [220] | is decreased in the brain and CSF of AD patients [222] | |
miR-186-5p | Occludin | competitively regulates circRNA in BTB permeability by targeting genes related to tight junction [221] | is decreased in the brain of aged mouse [224] | ||
hnRNP K | miR-107 | Bcl2l2 | promotes miRNA activation via circRNA in neuronal apoptosis by targeting apoptotic regulating genes [225] | is decreased in the brain of AD patients [226] | |
HuR | miR-7 | n.d. | regulates miRNA biogenesis, which is related to neuronal differentiation [107] | is elevated in the brain of AD patient [156] | |
SAFB1 | miR-19a | n.d. | regulates miRNA biogenesis [229] | is decreased in a cellular model of HD [230] | |
MSA | NOVA1 | miR-96-5p | GTRAP3-18 | inhibits RBPs regulating neuroprotection and targeting neurotoxic genes [231] | is decreased in the frontal cortex of MSA patients [232] |
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Kinoshita, C.; Kubota, N.; Aoyama, K. Interplay of RNA-Binding Proteins and microRNAs in Neurodegenerative Diseases. Int. J. Mol. Sci. 2021, 22, 5292. https://doi.org/10.3390/ijms22105292
Kinoshita C, Kubota N, Aoyama K. Interplay of RNA-Binding Proteins and microRNAs in Neurodegenerative Diseases. International Journal of Molecular Sciences. 2021; 22(10):5292. https://doi.org/10.3390/ijms22105292
Chicago/Turabian StyleKinoshita, Chisato, Noriko Kubota, and Koji Aoyama. 2021. "Interplay of RNA-Binding Proteins and microRNAs in Neurodegenerative Diseases" International Journal of Molecular Sciences 22, no. 10: 5292. https://doi.org/10.3390/ijms22105292