The Expression of miRNAs Involved in Long-Term Memory Formation in the CNS of the Mollusk <i>Helix lucorum</i>

Mollusks are unique animals with a relatively simple central nervous system (CNS) containing giant neurons with identified functions. With such simple CNS, mollusks yet display sufficiently complex behavior, thus ideal for various studies of behavioral processes, including long-term memory (LTM) for...

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Main Authors: Gennady V. Vasiliev, Vladimir Y. Ovchinnikov, Pavel D. Lisachev, Natalia P. Bondar, Larisa N. Grinkevich
Format: Article
Language:English
Published: MDPI AG 2022-12-01
Series:International Journal of Molecular Sciences
Subjects:
Online Access:https://www.mdpi.com/1422-0067/24/1/301
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author Gennady V. Vasiliev
Vladimir Y. Ovchinnikov
Pavel D. Lisachev
Natalia P. Bondar
Larisa N. Grinkevich
author_facet Gennady V. Vasiliev
Vladimir Y. Ovchinnikov
Pavel D. Lisachev
Natalia P. Bondar
Larisa N. Grinkevich
author_sort Gennady V. Vasiliev
collection DOAJ
description Mollusks are unique animals with a relatively simple central nervous system (CNS) containing giant neurons with identified functions. With such simple CNS, mollusks yet display sufficiently complex behavior, thus ideal for various studies of behavioral processes, including long-term memory (LTM) formation. For our research, we use the formation of the fear avoidance reflex in the terrestrial mollusk <i>Helix lucorum</i> as a learning model. We have shown previously that LTM formation in <i>Helix</i> requires epigenetic modifications of histones leading to both activation and inactivation of the specific genes. It is known that microRNAs (miRNAs) negatively regulate the expression of genes; however, the role of miRNAs in behavioral regulation has been poorly investigated. Currently, there is no miRNAs sequencing data being published on <i>Helix lucorum</i>, which makes it impossible to investigate the role of miRNAs in the memory formation of this mollusk. In this study, we have performed sequencing and comparative bioinformatics analysis of the miRNAs from the CNS of <i>Helix lucorum</i>. We have identified 95 different microRNAs, including microRNAs belonging to the MIR-9, MIR-10, MIR-22, MIR-124, MIR-137, and MIR-153 families, known to be involved in various CNS processes of vertebrates and other species, particularly, in the fear behavior and LTM. We have shown that in the CNS of <i>Helix lucorum</i> MIR-10 family (26 miRNAs) is the most representative one, including Hlu-Mir-10-S5-5p and Hlu-Mir-10-S9-5p as top hits. Moreover, we have shown the involvement of the MIR-10 family in LTM formation in <i>Helix</i>. The expression of 17 representatives of MIR-10 differentially changes during different periods of LTM consolidation in the CNS of <i>Helix</i>. In addition, using comparative analysis of microRNA expression upon learning in normal snails and snails with deficient learning abilities with dysfunction of the serotonergic system, we identified a number of microRNAs from several families, including MIR-10, which expression changes only in normal animals. The obtained data can be used for further fundamental and applied behavioral research.
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spelling doaj.art-088bf943a7024816aff00131bda849292023-11-16T15:31:23ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672022-12-0124130110.3390/ijms24010301The Expression of miRNAs Involved in Long-Term Memory Formation in the CNS of the Mollusk <i>Helix lucorum</i>Gennady V. Vasiliev0Vladimir Y. Ovchinnikov1Pavel D. Lisachev2Natalia P. Bondar3Larisa N. Grinkevich4The Federal Research Center Institute of Cytology and Genetics, Siberian Branch, Russian Academy of Sciences, 10 Lavrentiev Avenue, Novosibirsk 630090, RussiaThe Federal Research Center Institute of Cytology and Genetics, Siberian Branch, Russian Academy of Sciences, 10 Lavrentiev Avenue, Novosibirsk 630090, RussiaFederal Research Center for Information and Computational Technologies, 6 Lavrentiev Avenue, Novosibirsk 630090, RussiaThe Federal Research Center Institute of Cytology and Genetics, Siberian Branch, Russian Academy of Sciences, 10 Lavrentiev Avenue, Novosibirsk 630090, RussiaThe Federal State Budget Scientific Institution Pavlov Institute of Physiology, Russian Academy of Sciences, 6 nab. Makarova, St. Petersburg 199034, RussiaMollusks are unique animals with a relatively simple central nervous system (CNS) containing giant neurons with identified functions. With such simple CNS, mollusks yet display sufficiently complex behavior, thus ideal for various studies of behavioral processes, including long-term memory (LTM) formation. For our research, we use the formation of the fear avoidance reflex in the terrestrial mollusk <i>Helix lucorum</i> as a learning model. We have shown previously that LTM formation in <i>Helix</i> requires epigenetic modifications of histones leading to both activation and inactivation of the specific genes. It is known that microRNAs (miRNAs) negatively regulate the expression of genes; however, the role of miRNAs in behavioral regulation has been poorly investigated. Currently, there is no miRNAs sequencing data being published on <i>Helix lucorum</i>, which makes it impossible to investigate the role of miRNAs in the memory formation of this mollusk. In this study, we have performed sequencing and comparative bioinformatics analysis of the miRNAs from the CNS of <i>Helix lucorum</i>. We have identified 95 different microRNAs, including microRNAs belonging to the MIR-9, MIR-10, MIR-22, MIR-124, MIR-137, and MIR-153 families, known to be involved in various CNS processes of vertebrates and other species, particularly, in the fear behavior and LTM. We have shown that in the CNS of <i>Helix lucorum</i> MIR-10 family (26 miRNAs) is the most representative one, including Hlu-Mir-10-S5-5p and Hlu-Mir-10-S9-5p as top hits. Moreover, we have shown the involvement of the MIR-10 family in LTM formation in <i>Helix</i>. The expression of 17 representatives of MIR-10 differentially changes during different periods of LTM consolidation in the CNS of <i>Helix</i>. In addition, using comparative analysis of microRNA expression upon learning in normal snails and snails with deficient learning abilities with dysfunction of the serotonergic system, we identified a number of microRNAs from several families, including MIR-10, which expression changes only in normal animals. The obtained data can be used for further fundamental and applied behavioral research.https://www.mdpi.com/1422-0067/24/1/301<i>Helix lucorum</i>CNSmicroRNAnext generation sequencinglong-term memoryMIR-10 family
spellingShingle Gennady V. Vasiliev
Vladimir Y. Ovchinnikov
Pavel D. Lisachev
Natalia P. Bondar
Larisa N. Grinkevich
The Expression of miRNAs Involved in Long-Term Memory Formation in the CNS of the Mollusk <i>Helix lucorum</i>
International Journal of Molecular Sciences
<i>Helix lucorum</i>
CNS
microRNA
next generation sequencing
long-term memory
MIR-10 family
title The Expression of miRNAs Involved in Long-Term Memory Formation in the CNS of the Mollusk <i>Helix lucorum</i>
title_full The Expression of miRNAs Involved in Long-Term Memory Formation in the CNS of the Mollusk <i>Helix lucorum</i>
title_fullStr The Expression of miRNAs Involved in Long-Term Memory Formation in the CNS of the Mollusk <i>Helix lucorum</i>
title_full_unstemmed The Expression of miRNAs Involved in Long-Term Memory Formation in the CNS of the Mollusk <i>Helix lucorum</i>
title_short The Expression of miRNAs Involved in Long-Term Memory Formation in the CNS of the Mollusk <i>Helix lucorum</i>
title_sort expression of mirnas involved in long term memory formation in the cns of the mollusk i helix lucorum i
topic <i>Helix lucorum</i>
CNS
microRNA
next generation sequencing
long-term memory
MIR-10 family
url https://www.mdpi.com/1422-0067/24/1/301
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