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Increase of the RNA-binding protein HuD and posttranscriptional up-regulation of the GAP-43 gene during spatial memory

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Pascale, Alessia, Gusev, Pavel A., Amadio, Marialaura, Dottorini, Tania, Govoni, Stefano, Alkon, Daniel L., Quattrone, Alessandro·2004·Proceedings of the National Academy of Sciences
DOI 10.1073/pnas.0307674100PMC PMC337033
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Abstract

Neuronal ELAV-like proteins (HuB, HuC, and HuD) are highly conserved RNA-binding proteins able to selectively associate with the 3′ UTR of a subset of target mRNAs and increase their cytoplasmic stability and rate of translation. We previously demonstrated the involvement of these proteins in learning, reporting that they undergo a sustained up-regulation in the hippocampus of mice trained in a spatial discrimination task. Here, we extend this finding, showing that a similar up-regulation occurs in the hippocampus of rats trained in another spatial learning paradigm, the Morris water maze. HuD, a strictly neuron-specific ELAV-like protein, is shown to increase after learning, with a preferential binding to the cytoskeletal fraction. HuD up-regulation is associated with an enhancement of GAP-43 mRNA and protein levels, with an apparently increased HuD colocalization with the GAP-43 mRNA and an increased association of neuronal ELAV-like proteins with the GAP-43 mRNA. These learning-dependent biochemical events appear to be spatiotemporally controlled, because they do not occur in another brain region involved in learning, the retrosplenial cortex, and at the level of protein expression they show extinction 1 month after training despite memory retention. By contrast, HuD mRNA levels still remain increased after 1 month in the CA1 region. This persistence may have implications for long-term memory recall.

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  • Expression of nELAV proteins and GAP-43 mRNA increased in the cytoskeletal and membrane fractions of murine hippocampal neurons following spatial discrimination tasks.

    “The first studies to link HuD to learning and memory demonstrated that expression of nELAV proteins and GAP-43 mRNA increased in the cytoskeletal and membrane fractions of murine hippocampal neurons following spatial discrimination tasks (Quattrone et al. 2001; Pascale et al. 2004).”

    From Emerging complexity of the HuD/ELAVl4 gene; implications for neuronal development, function, and dysfunction (2013) · cites this paper as Pascale et al. 2004

    The Discussion reports earlier up-regulation of neuronal ELAV proteins after a mouse spatial task, while this paper's Results examine rats trained in the Morris water maze. The Results show increased ELAV-like proteins chiefly in the cytoskeletal fraction and increased GAP-43 mRNA in the hippocampus. The membrane and cytoskeletal fraction increases reported for GAP-43 concern its protein, not its mRNA; the ELAV-like protein increase had no membrane contribution. (LLM, conf=0.89)

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Cited by

Sorted by citations

Authors
Pascale, A., Gusev, P. A., Amadio, M., Dottorini, T., Govoni, S., Alkon, D. L., & Quattrone, A.
Affiliations
West Virginia University (US)
ORCID
Venue
Proceedings of the National Academy of Sciences
Publisher
National Academy of Sciences
Published
2004-01-26
Volume
101
Issue
5
Pages
1217-1222
ISSN
  • 0027-8424 (ISSN-L)
  • 1091-6490
DOI
10.1073/pnas.0307674100
PMC
PMC337033
OpenAlex
W2081228528
Cited by
174
References
3
Citations by year
2026: 5 · 2025: 5 · 2024: 3 · 2023: 5 · 2022: 9 · 2021: 7 · 2020: 7 · 2019: 2 · 2018: 4 · 2017: 6 · 2016: 6 · 2015: 10 · 2014: 12 · 2013: 11 · 2012: 9
FWCI
6.39
Type
journal article
Language
en
Open access
Locations
  • Proceedings of the National Academy of Sciences (publishedVersion)
  • Europe PMC (PubMed Central) (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
  • Iris (University of Trento) (submittedVersion)
Funders
University of Connecticut
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Research and Splicing
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Keywords
HUD, ELAV-like proteins, RNA-binding proteins, GAP-43, spatial memory, post-transcriptional regulation, hippocampus, CA1, 3' untranslated region, mRNA stability, cytoskeletal association, long-term memory, retrosplenial cortex
MeSH terms
Animals, Gene Expression Regulation, Hippocampus, Male, Memory, Nerve Tissue Proteins, Spatial Behavior, Transcription, Genetic, Up-Regulation, RNA-Binding Proteins, Rats, Wistar, GAP-43 Protein, Rats, ELAV Proteins

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