ciRS-7 and miR-7 regulate ischemia-induced neuronal death via glutamatergic signaling

Flavia Scoyni; Valeriia Sitnikova; Luca Giudice; Paula Korhonen; Davide M. Trevisan; Ana Hernandez de Sande; Mireia Gomez-Budia; Raisa Giniatullina; Irene F. Ugidos; Hiramani Dhungana; Cristiana Pistono; Nea Korvenlaita; Nelli Noora Välimäki; Salla M. Kangas; Anniina E. Hiltunen; Emma Gribchenko; Minna U. Kaikkonen-Määttä; Jari Koistinaho; Seppo Ylä-Herttuala; Reetta Hinttala; Morten T. Venø; Junyi Su; Markus Stoffel; Anne Schaefer; Nikolaus Rajewsky; Jørgen Kjems; Mary P. LaPierre; Monika Piwecka; Jukka Jolkkonen; Rashid Giniatullin; Thomas B. Hansen; Tarja Malm

doi:10.1016/j.celrep.2024.113862

ciRS-7 and miR-7 regulate ischemia-induced neuronal death via glutamatergic signaling

Flavia Scoyni^*, Valeriia Sitnikova, Luca Giudice, Paula Korhonen, Davide M. Trevisan, Ana Hernandez de Sande, Mireia Gomez-Budia, Raisa Giniatullina, Irene F. Ugidos, Hiramani Dhungana, Cristiana Pistono, Nea Korvenlaita, Nelli Noora Välimäki, Salla M. Kangas, Anniina E. Hiltunen, Emma Gribchenko, Minna U. Kaikkonen-Määttä, Jari Koistinaho, Seppo Ylä-Herttuala, Reetta HinttalaMorten T. Venø, Junyi Su, Markus Stoffel, Anne Schaefer, Nikolaus Rajewsky, Jørgen Kjems, Mary P. LaPierre, Monika Piwecka, Jukka Jolkkonen, Rashid Giniatullin, Thomas B. Hansen, Tarja Malm^*

^*Corresponding author af dette arbejde

Publikation: Bidrag til tidsskrift/Konferencebidrag i tidsskrift /Bidrag til avis › Tidsskriftartikel › Forskning › peer review

3 Citationer (Scopus)

Abstract

Brain functionality relies on finely tuned regulation of gene expression by networks of non-coding RNAs (ncRNAs) such as the one composed by the circular RNA ciRS-7 (also known as CDR1as), the microRNA miR-7, and the long ncRNA Cyrano. We describe ischemia-induced alterations in the ncRNA network both in vitro and in vivo and in transgenic mice lacking ciRS-7 or miR-7. Our data show that cortical neurons downregulate ciRS-7 and Cyrano and upregulate miR-7 expression during ischemia. Mice lacking ciRS-7 exhibit reduced lesion size and motor impairment, while the absence of miR-7 alone results in increased ischemia-induced neuronal death. Moreover, miR-7 levels in pyramidal excitatory neurons regulate neurite morphology and glutamatergic signaling, suggesting a potential molecular link to the in vivo phenotype. Our data reveal the role of ciRS-7 and miR-7 in modulating ischemic stroke outcome, shedding light on the pathophysiological function of intracellular ncRNA networks in the brain.

Originalsprog	Engelsk
Artikelnummer	113862
Tidsskrift	Cell Reports
Vol/bind	43
Nummer	3
Antal sider	24
ISSN	2211-1247
DOI	https://doi.org/10.1016/j.celrep.2024.113862
Status	Udgivet - mar. 2024

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10.1016/j.celrep.2024.113862Licens: CC BY

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Scoyni, F., Sitnikova, V., Giudice, L., Korhonen, P., Trevisan, D. M., Hernandez de Sande, A., Gomez-Budia, M., Giniatullina, R., Ugidos, I. F., Dhungana, H., Pistono, C., Korvenlaita, N., Välimäki, N. N., Kangas, S. M., Hiltunen, A. E., Gribchenko, E., Kaikkonen-Määttä, M. U., Koistinaho, J., Ylä-Herttuala, S., ... Malm, T. (2024). ciRS-7 and miR-7 regulate ischemia-induced neuronal death via glutamatergic signaling. Cell Reports, 43(3), Artikel 113862. https://doi.org/10.1016/j.celrep.2024.113862

@article{ed74b3ab68d949e894fcf94388d98044,

title = "ciRS-7 and miR-7 regulate ischemia-induced neuronal death via glutamatergic signaling",

abstract = "Brain functionality relies on finely tuned regulation of gene expression by networks of non-coding RNAs (ncRNAs) such as the one composed by the circular RNA ciRS-7 (also known as CDR1as), the microRNA miR-7, and the long ncRNA Cyrano. We describe ischemia-induced alterations in the ncRNA network both in vitro and in vivo and in transgenic mice lacking ciRS-7 or miR-7. Our data show that cortical neurons downregulate ciRS-7 and Cyrano and upregulate miR-7 expression during ischemia. Mice lacking ciRS-7 exhibit reduced lesion size and motor impairment, while the absence of miR-7 alone results in increased ischemia-induced neuronal death. Moreover, miR-7 levels in pyramidal excitatory neurons regulate neurite morphology and glutamatergic signaling, suggesting a potential molecular link to the in vivo phenotype. Our data reveal the role of ciRS-7 and miR-7 in modulating ischemic stroke outcome, shedding light on the pathophysiological function of intracellular ncRNA networks in the brain.",

keywords = "cell death, circularRNAs, CP: Neuroscience, excitotoxicity, glutamate, ischemic stroke, microRNAs, molecular networks, non-coding RNAs, post-transcriptional regulation",

author = "Flavia Scoyni and Valeriia Sitnikova and Luca Giudice and Paula Korhonen and Trevisan, {Davide M.} and {Hernandez de Sande}, Ana and Mireia Gomez-Budia and Raisa Giniatullina and Ugidos, {Irene F.} and Hiramani Dhungana and Cristiana Pistono and Nea Korvenlaita and V{\"a}lim{\"a}ki, {Nelli Noora} and Kangas, {Salla M.} and Hiltunen, {Anniina E.} and Emma Gribchenko and Kaikkonen-M{\"a}{\"a}tt{\"a}, {Minna U.} and Jari Koistinaho and Seppo Yl{\"a}-Herttuala and Reetta Hinttala and Ven{\o}, {Morten T.} and Junyi Su and Markus Stoffel and Anne Schaefer and Nikolaus Rajewsky and J{\o}rgen Kjems and LaPierre, {Mary P.} and Monika Piwecka and Jukka Jolkkonen and Rashid Giniatullin and Hansen, {Thomas B.} and Tarja Malm",

year = "2024",

month = mar,

doi = "10.1016/j.celrep.2024.113862",

language = "English",

volume = "43",

journal = "Cell Reports",

issn = "2211-1247",

publisher = "Cell Press",

number = "3",

}

Scoyni, F, Sitnikova, V, Giudice, L, Korhonen, P, Trevisan, DM, Hernandez de Sande, A, Gomez-Budia, M, Giniatullina, R, Ugidos, IF, Dhungana, H, Pistono, C, Korvenlaita, N, Välimäki, NN, Kangas, SM, Hiltunen, AE, Gribchenko, E, Kaikkonen-Määttä, MU, Koistinaho, J, Ylä-Herttuala, S, Hinttala, R, Venø, MT, Su, J, Stoffel, M, Schaefer, A, Rajewsky, N, Kjems, J, LaPierre, MP, Piwecka, M, Jolkkonen, J, Giniatullin, R, Hansen, TB & Malm, T 2024, 'ciRS-7 and miR-7 regulate ischemia-induced neuronal death via glutamatergic signaling', Cell Reports, bind 43, nr. 3, 113862. https://doi.org/10.1016/j.celrep.2024.113862

TY - JOUR

T1 - ciRS-7 and miR-7 regulate ischemia-induced neuronal death via glutamatergic signaling

AU - Scoyni, Flavia

AU - Sitnikova, Valeriia

AU - Giudice, Luca

AU - Korhonen, Paula

AU - Trevisan, Davide M.

AU - Hernandez de Sande, Ana

AU - Gomez-Budia, Mireia

AU - Giniatullina, Raisa

AU - Ugidos, Irene F.

AU - Dhungana, Hiramani

AU - Pistono, Cristiana

AU - Korvenlaita, Nea

AU - Välimäki, Nelli Noora

AU - Kangas, Salla M.

AU - Hiltunen, Anniina E.

AU - Gribchenko, Emma

AU - Kaikkonen-Määttä, Minna U.

AU - Koistinaho, Jari

AU - Ylä-Herttuala, Seppo

AU - Hinttala, Reetta

AU - Venø, Morten T.

AU - Su, Junyi

AU - Stoffel, Markus

AU - Schaefer, Anne

AU - Rajewsky, Nikolaus

AU - Kjems, Jørgen

AU - LaPierre, Mary P.

AU - Piwecka, Monika

AU - Jolkkonen, Jukka

AU - Giniatullin, Rashid

AU - Hansen, Thomas B.

AU - Malm, Tarja

PY - 2024/3

Y1 - 2024/3

N2 - Brain functionality relies on finely tuned regulation of gene expression by networks of non-coding RNAs (ncRNAs) such as the one composed by the circular RNA ciRS-7 (also known as CDR1as), the microRNA miR-7, and the long ncRNA Cyrano. We describe ischemia-induced alterations in the ncRNA network both in vitro and in vivo and in transgenic mice lacking ciRS-7 or miR-7. Our data show that cortical neurons downregulate ciRS-7 and Cyrano and upregulate miR-7 expression during ischemia. Mice lacking ciRS-7 exhibit reduced lesion size and motor impairment, while the absence of miR-7 alone results in increased ischemia-induced neuronal death. Moreover, miR-7 levels in pyramidal excitatory neurons regulate neurite morphology and glutamatergic signaling, suggesting a potential molecular link to the in vivo phenotype. Our data reveal the role of ciRS-7 and miR-7 in modulating ischemic stroke outcome, shedding light on the pathophysiological function of intracellular ncRNA networks in the brain.

AB - Brain functionality relies on finely tuned regulation of gene expression by networks of non-coding RNAs (ncRNAs) such as the one composed by the circular RNA ciRS-7 (also known as CDR1as), the microRNA miR-7, and the long ncRNA Cyrano. We describe ischemia-induced alterations in the ncRNA network both in vitro and in vivo and in transgenic mice lacking ciRS-7 or miR-7. Our data show that cortical neurons downregulate ciRS-7 and Cyrano and upregulate miR-7 expression during ischemia. Mice lacking ciRS-7 exhibit reduced lesion size and motor impairment, while the absence of miR-7 alone results in increased ischemia-induced neuronal death. Moreover, miR-7 levels in pyramidal excitatory neurons regulate neurite morphology and glutamatergic signaling, suggesting a potential molecular link to the in vivo phenotype. Our data reveal the role of ciRS-7 and miR-7 in modulating ischemic stroke outcome, shedding light on the pathophysiological function of intracellular ncRNA networks in the brain.

KW - cell death

KW - circularRNAs

KW - CP: Neuroscience

KW - excitotoxicity

KW - glutamate

KW - ischemic stroke

KW - microRNAs

KW - molecular networks

KW - non-coding RNAs

KW - post-transcriptional regulation

UR - http://www.scopus.com/inward/record.url?scp=85186691495&partnerID=8YFLogxK

U2 - 10.1016/j.celrep.2024.113862

DO - 10.1016/j.celrep.2024.113862

M3 - Journal article

C2 - 38446664

AN - SCOPUS:85186691495

SN - 2211-1247

VL - 43

JO - Cell Reports

JF - Cell Reports

IS - 3

M1 - 113862

ER -

ciRS-7 and miR-7 regulate ischemia-induced neuronal death via glutamatergic signaling

Abstract

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