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MicroRNA-92a-CPEB3 axis protects neurons against inflammatory neurodegeneration

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MicroRNA-92a-CPEB3 axis protects neurons against inflammatory neurodegeneration. / Winkler, Iris; Engler, Jan Broder; Vieira, Vanessa; Bauer, Simone; Liu, Yi-Hsiang; Di Liberto, Giovanni; Grochowska, Katarzyna M; Wagner, Ingrid; Bier, Jasmina; Bal, Lukas C; Rothammer, Nicola; Meurs, Nina; Egervari, Kristof; Schattling, Benjamin; Salinas, Gabriela; Kreutz, Michael R; Huang, Yi-Shuian; Pless, Ole; Merkler, Doron; Friese, Manuel A.

In: SCI ADV, Vol. 9, No. 47, eadi6855, 24.11.2023.

Research output: SCORING: Contribution to journal › SCORING: Journal article › Research › peer-review

Harvard

Winkler, I, Engler, JB, Vieira, V, Bauer, S, Liu, Y-H, Di Liberto, G, Grochowska, KM, Wagner, I, Bier, J, Bal, LC, Rothammer, N, Meurs, N, Egervari, K, Schattling, B, Salinas, G, Kreutz, MR, Huang, Y-S, Pless, O, Merkler, D & Friese, MA 2023, 'MicroRNA-92a-CPEB3 axis protects neurons against inflammatory neurodegeneration', SCI ADV, vol. 9, no. 47, eadi6855. https://doi.org/10.1126/sciadv.adi6855

APA

Winkler, I., Engler, J. B., Vieira, V., Bauer, S., Liu, Y-H., Di Liberto, G., Grochowska, K. M., Wagner, I., Bier, J., Bal, L. C., Rothammer, N., Meurs, N., Egervari, K., Schattling, B., Salinas, G., Kreutz, M. R., Huang, Y-S., Pless, O., Merkler, D., & Friese, M. A. (2023). MicroRNA-92a-CPEB3 axis protects neurons against inflammatory neurodegeneration. SCI ADV, 9(47), [eadi6855]. https://doi.org/10.1126/sciadv.adi6855

Vancouver

Winkler I, Engler JB, Vieira V, Bauer S, Liu Y-H, Di Liberto G et al. MicroRNA-92a-CPEB3 axis protects neurons against inflammatory neurodegeneration. SCI ADV. 2023 Nov 24;9(47). eadi6855. https://doi.org/10.1126/sciadv.adi6855

Bibtex

@article{e73d0678c05f4da49653ad24eadae6ad,
title = "MicroRNA-92a-CPEB3 axis protects neurons against inflammatory neurodegeneration",
abstract = "Neuroinflammation causes neuronal injury in multiple sclerosis (MS) and other neurological diseases. MicroRNAs (miRNAs) are important modulators of neuronal stress responses, but knowledge about their contribution to neuronal protection or damage during inflammation is limited. Here, we constructed a regulatory miRNA-mRNA network of inflamed motor neurons by leveraging cell type-specific miRNA and mRNA sequencing of mice undergoing experimental autoimmune encephalomyelitis (EAE). We found robust induction of miR-92a in inflamed spinal cord neurons and identified cytoplasmic polyadenylation element-binding protein 3 (Cpeb3) as a key target of miR-92a-mediated posttranscriptional silencing. We detected CPEB3 repression in inflamed neurons in murine EAE and human MS. Moreover, both miR-92a delivery and Cpeb3 deletion protected neuronal cultures against excitotoxicity. Supporting a detrimental effect of Cpeb3 in vivo, neuron-specific deletion in conditional Cpeb3 knockout animals led to reduced inflammation-induced clinical disability in EAE. Together, we identified a neuroprotective miR-92a-Cpeb3 axis in neuroinflammation that might serve as potential treatment target to limit inflammation-induced neuronal damage.",
keywords = "Humans, Mice, Animals, MicroRNAs/genetics, Neuroinflammatory Diseases, Encephalomyelitis, Autoimmune, Experimental/genetics, Multiple Sclerosis, Inflammation/genetics, Neurons/metabolism, RNA, Messenger/metabolism, Mice, Inbred C57BL, RNA-Binding Proteins/genetics",
author = "Iris Winkler and Engler, {Jan Broder} and Vanessa Vieira and Simone Bauer and Yi-Hsiang Liu and {Di Liberto}, Giovanni and Grochowska, {Katarzyna M} and Ingrid Wagner and Jasmina Bier and Bal, {Lukas C} and Nicola Rothammer and Nina Meurs and Kristof Egervari and Benjamin Schattling and Gabriela Salinas and Kreutz, {Michael R} and Yi-Shuian Huang and Ole Pless and Doron Merkler and Friese, {Manuel A}",
year = "2023",
month = nov,
day = "24",
doi = "10.1126/sciadv.adi6855",
language = "English",
volume = "9",
journal = "SCI ADV",
issn = "2375-2548",
publisher = "American Association for the Advancement of Science",
number = "47",

}

RIS

TY - JOUR

T1 - MicroRNA-92a-CPEB3 axis protects neurons against inflammatory neurodegeneration

AU - Winkler, Iris

AU - Engler, Jan Broder

AU - Vieira, Vanessa

AU - Bauer, Simone

AU - Liu, Yi-Hsiang

AU - Di Liberto, Giovanni

AU - Grochowska, Katarzyna M

AU - Wagner, Ingrid

AU - Bier, Jasmina

AU - Bal, Lukas C

AU - Rothammer, Nicola

AU - Meurs, Nina

AU - Egervari, Kristof

AU - Schattling, Benjamin

AU - Salinas, Gabriela

AU - Kreutz, Michael R

AU - Huang, Yi-Shuian

AU - Pless, Ole

AU - Merkler, Doron

AU - Friese, Manuel A

PY - 2023/11/24

Y1 - 2023/11/24

N2 - Neuroinflammation causes neuronal injury in multiple sclerosis (MS) and other neurological diseases. MicroRNAs (miRNAs) are important modulators of neuronal stress responses, but knowledge about their contribution to neuronal protection or damage during inflammation is limited. Here, we constructed a regulatory miRNA-mRNA network of inflamed motor neurons by leveraging cell type-specific miRNA and mRNA sequencing of mice undergoing experimental autoimmune encephalomyelitis (EAE). We found robust induction of miR-92a in inflamed spinal cord neurons and identified cytoplasmic polyadenylation element-binding protein 3 (Cpeb3) as a key target of miR-92a-mediated posttranscriptional silencing. We detected CPEB3 repression in inflamed neurons in murine EAE and human MS. Moreover, both miR-92a delivery and Cpeb3 deletion protected neuronal cultures against excitotoxicity. Supporting a detrimental effect of Cpeb3 in vivo, neuron-specific deletion in conditional Cpeb3 knockout animals led to reduced inflammation-induced clinical disability in EAE. Together, we identified a neuroprotective miR-92a-Cpeb3 axis in neuroinflammation that might serve as potential treatment target to limit inflammation-induced neuronal damage.

AB - Neuroinflammation causes neuronal injury in multiple sclerosis (MS) and other neurological diseases. MicroRNAs (miRNAs) are important modulators of neuronal stress responses, but knowledge about their contribution to neuronal protection or damage during inflammation is limited. Here, we constructed a regulatory miRNA-mRNA network of inflamed motor neurons by leveraging cell type-specific miRNA and mRNA sequencing of mice undergoing experimental autoimmune encephalomyelitis (EAE). We found robust induction of miR-92a in inflamed spinal cord neurons and identified cytoplasmic polyadenylation element-binding protein 3 (Cpeb3) as a key target of miR-92a-mediated posttranscriptional silencing. We detected CPEB3 repression in inflamed neurons in murine EAE and human MS. Moreover, both miR-92a delivery and Cpeb3 deletion protected neuronal cultures against excitotoxicity. Supporting a detrimental effect of Cpeb3 in vivo, neuron-specific deletion in conditional Cpeb3 knockout animals led to reduced inflammation-induced clinical disability in EAE. Together, we identified a neuroprotective miR-92a-Cpeb3 axis in neuroinflammation that might serve as potential treatment target to limit inflammation-induced neuronal damage.

KW - Humans

KW - Mice

KW - Animals

KW - MicroRNAs/genetics

KW - Neuroinflammatory Diseases

KW - Encephalomyelitis, Autoimmune, Experimental/genetics

KW - Multiple Sclerosis

KW - Inflammation/genetics

KW - Neurons/metabolism

KW - RNA, Messenger/metabolism

KW - Mice, Inbred C57BL

KW - RNA-Binding Proteins/genetics

U2 - 10.1126/sciadv.adi6855

DO - 10.1126/sciadv.adi6855

M3 - SCORING: Journal article

C2 - 38000031

VL - 9

JO - SCI ADV

JF - SCI ADV

SN - 2375-2548

IS - 47

M1 - eadi6855

ER -