Prenatal Deletion of the RNA-Binding Protein HuD Disrupts Postnatal Cortical Circuit Maturation and Behavior

DeBoer, Erik M.; Azevedo, Ricardo; Vega, Taylor A.; Brodkin, Jesse; Akamatsu, Wado; Okano, Hideyuki; Wagner, George C.; Rasin, Mladen-Roko

doi:10.1523/jneurosci.3703-13.2014

Cited by 72Neurogenesis and neuroplasticity mechanismsGenetics and Neurodevelopmental DisordersRNA Research and Splicing

Prenatal Deletion of the RNA-Binding Protein HuD Disrupts Postnatal Cortical Circuit Maturation and Behavior

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DeBoer, Erik M., Azevedo, Ricardo, Vega, Taylor A., Brodkin, Jesse, Akamatsu, Wado, Okano, Hideyuki, Wagner, George C., Rasin, Mladen-Roko·2014·The Journal of Neuroscience

DOI 10.1523/jneurosci.3703-13.2014PMC PMC3942583

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Abstract

The proper functions of cortical circuits are dependent upon both appropriate neuronal subtype specification and their maturation to receive appropriate signaling. These events establish a balanced circuit that is important for learning, memory, emotion, and complex motor behaviors. Recent research points to mRNA metabolism as a key regulator of this development and maturation process. Hu antigen D (HuD), an RNA-binding protein, has been implicated in the establishment of neuronal identity and neurite outgrowth in vitro. Therefore, we investigated the role of HuD loss of function on neuron specification and dendritogenesis in vivo using a mouse model. We found that loss of HuD early in development results in a defective early dendritic overgrowth phase and pervasive deficits in neuron specification in the lower neocortical layers and defects in dendritogenesis in the CA3 region of the hippocampus. Subsequent behavioral analysis revealed a deficit in performance of a hippocampus-dependent task: the Morris water maze. Further,HuD knock-out (KO) mice exhibited lower levels of anxiety than their wild-type counterparts and were overall less active. Last, we found that HuD KO mice are more susceptible to auditory-induced seizures, often resulting in death. Our findings suggest that HuD is necessary for the establishment of neocortical and hippocampal circuitry and is critical for their function.

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ELAVL4 expression decreases self-renewal of neural progenitor cells and promotes deep-layer glutamatergic neuronal differentiation.
“ELAVL4 expression decreases self-renewal of neural progenitor cells and promotes deep-layer glutamatergic neuronal differentiation (Akamatsu et al., 2005; DeBoer et al., 2014; Popovitchenko et al., 2020).”
From ELAVL4, splicing, and glutamatergic dysfunction precede neuron loss in MAPT mutation cerebral organoids (2021) · cites this paper as DeBoer et al., 2014
The Results section, “HuD is critical for the balanced expression of Tle4 in lower layer neocortical neurons” (page unavailable), reports fewer Tle4-positive lower-layer neurons after HuD deletion and suggests a role in their specification and/or maintenance. That supports a connection to deep-layer neuronal identity, but does not establish that ELAVL4 expression promotes differentiation specifically. Our copy does not report that ELAVL4 decreases neural progenitor self-renewal. (LLM, conf=0.86)
Experimental — accuracy not yet measured
ELAVL4 is selectively expressed in neuronal populations vulnerable to cell death in tau-V337M organoids.
“ELAVL4 is selectively expressed in neuronal populations vulnerable to cell death in tau-V337M organoids, consistent with its reported expression in the brain (Bronicki and Jasmin, 2013; DeBoer et al., 2014).”
From ELAVL4, splicing, and glutamatergic dysfunction precede neuron loss in MAPT mutation cerebral organoids (2021) · cites this paper as DeBoer et al., 2014
Depletion of nElavl in the brain leads to multiple neurological defects.
“Depletion of nElavl in the brain leads to multiple neurological defects124,125.”
From The neurogenetics of alternative splicing (2016) · cites this paper as [125]

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Authors: DeBoer, E. M., Azevedo, R., Vega, T. A., Brodkin, J., Akamatsu, W., Okano, H., Wagner, G. C., & Rasin, M.-R.
Affiliations: Rutgers, The State University of New Jersey (US)
University of California, Berkeley (US)
Keio University (JP)
ORCID: Vega, Taylor A.
Brodkin, Jesse
Akamatsu, Wado
Okano, Hideyuki
Wagner, George C.
Venue: The Journal of Neuroscience
Publisher: Society for Neuroscience
Published: 2014-03-05
Volume: 34
Issue: 10
Pages: 3674-3686
ISSN: 0270-6474 (ISSN-L)
1529-2401
DOI: 10.1523/jneurosci.3703-13.2014
PMC: PMC3942583
OpenAlex: W1990508004
Cited by: 72
References: 69
Citations by year: 2026: 2 · 2025: 5 · 2024: 4 · 2023: 8 · 2022: 5 · 2021: 13 · 2020: 7 · 2019: 4 · 2018: 4 · 2017: 5 · 2016: 6 · 2015: 7 · 2014: 2
FWCI: 2.32
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: cc-by-nc-sa
creativecommons.org/licenses/by-nc-sa/4.0/ (vor, 184 d)
Locations: Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: National Institutes of Health (NS064303)
National Institute of Neurological Disorders and Stroke (NS075367, R00NS064303, NS064303, K99NS064303, R01NS075367)
Topics: Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Research and Splicing
Keywords: HUD, RNA-binding proteins, dendritogenesis, neuronal specification, hippocampal CA3, mRNA metabolism, Morris water maze, anxiety, knockout mice
MeSH terms: ELAV-Like Protein 4, Animals, Animals, Newborn, Female, Hippocampus, Male, Nerve Net, Seizures, RNA-Binding Proteins, Gene Deletion, Mice, Knockout, Maze Learning, Neocortex, Mice, ELAV Proteins

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Prenatal Deletion of the RNA-Binding Protein HuD Disrupts Postnatal Cortical Circuit Maturation and Behavior

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