CREB in the Pond Snail Lymnaea stagnalis

Cloning, Gene Expression and Function in Identifiable Neurons of the Central Nervous System

Hisayo Sadamoto, Hanae Sato, Suguru Kobayashi, Jun Murakami, Hitoshi Aonuma, Hironori Ando, Yutaka Fujito, Kaoru Hamano, Masahiko Awaji, Ken Lukowiak, Akihisa Urano, Etsuro Ito

Research output: Contribution to journalArticle

61 Citations (Scopus)

Abstract

The pond snail Lymnaea stagnalis is an excellent model system in which to study the neuronal and molecular substrates of associative learning and its consolidation into long-term memory. Until now, the presence of cyclic AMP (cAMP)-responsive element binding protein (CREB), which is believed to be a necessary component in the process of a learned behavior that is consolidated into long-term memory, has only been assumed in Lymnaea neurons. We therefore cloned and analyzed the cDNA sequences of homologues of CREB1 and CREB2 and determined the presence of these mRNAs in identifiable neurons of the central nervous system (CNS) of L. stagnalis. The deduced amino acid sequence of Lymnaea CREB1 is homologous to transcriptional activators, mammalian CREB1 and Aplysia CREB1a, in the C-terminal DNA binding (bZIP) and phosphorylation domains, whereas the deduced amino acid sequence of Lymnaea CREB2 is homologous to transcriptional repressors, human CREB2, mouse activating transcription factor-4, and Aplysia CREB2 in the bZIP domain. In situ hybridization revealed that only a relatively few neurons showed strongly positive signals for Lymnaea CREB1 mRNA, whereas all the neurons in the CNS contained Lymnaea CREB2 mRNA. Using one of the neurons (the cerebral giant cell) containing Lymnaea CREB1 mRNA, we showed that the injection of a CRE oligonucleotide inhibited a cAMP-induced, long-lasting synaptic plasticity. We therefore conclude that CREBs are present in Lymnaea neurons and may function as necessary players in behavioral plasticity.

Original languageEnglish
Pages (from-to)455-466
Number of pages12
JournalJournal of Neurobiology
Volume58
Issue number4
DOIs
Publication statusPublished - 2004 Mar
Externally publishedYes

Fingerprint

Lymnaea
Organism Cloning
Carrier Proteins
Central Nervous System
Gene Expression
Neurons
Aplysia
Messenger RNA
Long-Term Memory
Cyclic AMP
Amino Acid Sequence
Activating Transcription Factor 4
Neuronal Plasticity
Snails
Giant Cells
Sequence Homology
Oligonucleotides
In Situ Hybridization
Complementary DNA
Phosphorylation

Keywords

  • Associative learning
  • Cerebral giant cell
  • Cyclic AMP
  • Facilitation
  • Long-term memory

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

CREB in the Pond Snail Lymnaea stagnalis : Cloning, Gene Expression and Function in Identifiable Neurons of the Central Nervous System. / Sadamoto, Hisayo; Sato, Hanae; Kobayashi, Suguru; Murakami, Jun; Aonuma, Hitoshi; Ando, Hironori; Fujito, Yutaka; Hamano, Kaoru; Awaji, Masahiko; Lukowiak, Ken; Urano, Akihisa; Ito, Etsuro.

In: Journal of Neurobiology, Vol. 58, No. 4, 03.2004, p. 455-466.

Research output: Contribution to journalArticle

Sadamoto, H, Sato, H, Kobayashi, S, Murakami, J, Aonuma, H, Ando, H, Fujito, Y, Hamano, K, Awaji, M, Lukowiak, K, Urano, A & Ito, E 2004, 'CREB in the Pond Snail Lymnaea stagnalis: Cloning, Gene Expression and Function in Identifiable Neurons of the Central Nervous System', Journal of Neurobiology, vol. 58, no. 4, pp. 455-466. https://doi.org/10.1002/neu.10296
Sadamoto, Hisayo ; Sato, Hanae ; Kobayashi, Suguru ; Murakami, Jun ; Aonuma, Hitoshi ; Ando, Hironori ; Fujito, Yutaka ; Hamano, Kaoru ; Awaji, Masahiko ; Lukowiak, Ken ; Urano, Akihisa ; Ito, Etsuro. / CREB in the Pond Snail Lymnaea stagnalis : Cloning, Gene Expression and Function in Identifiable Neurons of the Central Nervous System. In: Journal of Neurobiology. 2004 ; Vol. 58, No. 4. pp. 455-466.
@article{913e750fddc44774b644b8ece8e99d55,
title = "CREB in the Pond Snail Lymnaea stagnalis: Cloning, Gene Expression and Function in Identifiable Neurons of the Central Nervous System",
abstract = "The pond snail Lymnaea stagnalis is an excellent model system in which to study the neuronal and molecular substrates of associative learning and its consolidation into long-term memory. Until now, the presence of cyclic AMP (cAMP)-responsive element binding protein (CREB), which is believed to be a necessary component in the process of a learned behavior that is consolidated into long-term memory, has only been assumed in Lymnaea neurons. We therefore cloned and analyzed the cDNA sequences of homologues of CREB1 and CREB2 and determined the presence of these mRNAs in identifiable neurons of the central nervous system (CNS) of L. stagnalis. The deduced amino acid sequence of Lymnaea CREB1 is homologous to transcriptional activators, mammalian CREB1 and Aplysia CREB1a, in the C-terminal DNA binding (bZIP) and phosphorylation domains, whereas the deduced amino acid sequence of Lymnaea CREB2 is homologous to transcriptional repressors, human CREB2, mouse activating transcription factor-4, and Aplysia CREB2 in the bZIP domain. In situ hybridization revealed that only a relatively few neurons showed strongly positive signals for Lymnaea CREB1 mRNA, whereas all the neurons in the CNS contained Lymnaea CREB2 mRNA. Using one of the neurons (the cerebral giant cell) containing Lymnaea CREB1 mRNA, we showed that the injection of a CRE oligonucleotide inhibited a cAMP-induced, long-lasting synaptic plasticity. We therefore conclude that CREBs are present in Lymnaea neurons and may function as necessary players in behavioral plasticity.",
keywords = "Associative learning, Cerebral giant cell, Cyclic AMP, Facilitation, Long-term memory",
author = "Hisayo Sadamoto and Hanae Sato and Suguru Kobayashi and Jun Murakami and Hitoshi Aonuma and Hironori Ando and Yutaka Fujito and Kaoru Hamano and Masahiko Awaji and Ken Lukowiak and Akihisa Urano and Etsuro Ito",
year = "2004",
month = "3",
doi = "10.1002/neu.10296",
language = "English",
volume = "58",
pages = "455--466",
journal = "Developmental Neurobiology",
issn = "1932-8451",
publisher = "John Wiley and Sons Inc.",
number = "4",

}

TY - JOUR

T1 - CREB in the Pond Snail Lymnaea stagnalis

T2 - Cloning, Gene Expression and Function in Identifiable Neurons of the Central Nervous System

AU - Sadamoto, Hisayo

AU - Sato, Hanae

AU - Kobayashi, Suguru

AU - Murakami, Jun

AU - Aonuma, Hitoshi

AU - Ando, Hironori

AU - Fujito, Yutaka

AU - Hamano, Kaoru

AU - Awaji, Masahiko

AU - Lukowiak, Ken

AU - Urano, Akihisa

AU - Ito, Etsuro

PY - 2004/3

Y1 - 2004/3

N2 - The pond snail Lymnaea stagnalis is an excellent model system in which to study the neuronal and molecular substrates of associative learning and its consolidation into long-term memory. Until now, the presence of cyclic AMP (cAMP)-responsive element binding protein (CREB), which is believed to be a necessary component in the process of a learned behavior that is consolidated into long-term memory, has only been assumed in Lymnaea neurons. We therefore cloned and analyzed the cDNA sequences of homologues of CREB1 and CREB2 and determined the presence of these mRNAs in identifiable neurons of the central nervous system (CNS) of L. stagnalis. The deduced amino acid sequence of Lymnaea CREB1 is homologous to transcriptional activators, mammalian CREB1 and Aplysia CREB1a, in the C-terminal DNA binding (bZIP) and phosphorylation domains, whereas the deduced amino acid sequence of Lymnaea CREB2 is homologous to transcriptional repressors, human CREB2, mouse activating transcription factor-4, and Aplysia CREB2 in the bZIP domain. In situ hybridization revealed that only a relatively few neurons showed strongly positive signals for Lymnaea CREB1 mRNA, whereas all the neurons in the CNS contained Lymnaea CREB2 mRNA. Using one of the neurons (the cerebral giant cell) containing Lymnaea CREB1 mRNA, we showed that the injection of a CRE oligonucleotide inhibited a cAMP-induced, long-lasting synaptic plasticity. We therefore conclude that CREBs are present in Lymnaea neurons and may function as necessary players in behavioral plasticity.

AB - The pond snail Lymnaea stagnalis is an excellent model system in which to study the neuronal and molecular substrates of associative learning and its consolidation into long-term memory. Until now, the presence of cyclic AMP (cAMP)-responsive element binding protein (CREB), which is believed to be a necessary component in the process of a learned behavior that is consolidated into long-term memory, has only been assumed in Lymnaea neurons. We therefore cloned and analyzed the cDNA sequences of homologues of CREB1 and CREB2 and determined the presence of these mRNAs in identifiable neurons of the central nervous system (CNS) of L. stagnalis. The deduced amino acid sequence of Lymnaea CREB1 is homologous to transcriptional activators, mammalian CREB1 and Aplysia CREB1a, in the C-terminal DNA binding (bZIP) and phosphorylation domains, whereas the deduced amino acid sequence of Lymnaea CREB2 is homologous to transcriptional repressors, human CREB2, mouse activating transcription factor-4, and Aplysia CREB2 in the bZIP domain. In situ hybridization revealed that only a relatively few neurons showed strongly positive signals for Lymnaea CREB1 mRNA, whereas all the neurons in the CNS contained Lymnaea CREB2 mRNA. Using one of the neurons (the cerebral giant cell) containing Lymnaea CREB1 mRNA, we showed that the injection of a CRE oligonucleotide inhibited a cAMP-induced, long-lasting synaptic plasticity. We therefore conclude that CREBs are present in Lymnaea neurons and may function as necessary players in behavioral plasticity.

KW - Associative learning

KW - Cerebral giant cell

KW - Cyclic AMP

KW - Facilitation

KW - Long-term memory

UR - http://www.scopus.com/inward/record.url?scp=10744230108&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=10744230108&partnerID=8YFLogxK

U2 - 10.1002/neu.10296

DO - 10.1002/neu.10296

M3 - Article

VL - 58

SP - 455

EP - 466

JO - Developmental Neurobiology

JF - Developmental Neurobiology

SN - 1932-8451

IS - 4

ER -