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The RNA-binding Protein HuD Is Required for GAP-43 mRNA Stability, GAP-43 Gene Expression, and PKC-dependent Neurite Outgrowth in PC12 Cells

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Mobarak, Charlotte D., Anderson, Kim D., Morin, Melissa, Beckel-Mitchener, Andrea, Rogers, Sherry L., Furneaux, Henry, King, Peter, Perrone-Bizzozero, Nora I.·2000·Molecular Biology of the Cell
DOI 10.1091/mbc.11.9.3191PMC PMC14985
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Abstract

The RNA-binding protein HuD binds to a regulatory element in the 3′ untranslated region (3′ UTR) of the GAP-43 mRNA. To investigate the functional significance of this interaction, we generated PC12 cell lines in which HuD levels were controlled by transfection with either antisense (pDuH) or sense (pcHuD) constructs. pDuH-transfected cells contained reduced amounts of GAP-43 protein and mRNA, and these levels remained low even after nerve growth factor (NGF) stimulation, a treatment that is normally associated with protein kinase C (PKC)-dependent stabilization of the GAP-43 mRNA and neuronal differentiation. Analysis of GAP-43 mRNA stability demonstrated that the mRNA had a shorter half-life in these cells. In agreement with their deficient GAP-43 expression, pDuH cells failed to grow neurites in the presence of NGF or phorbol esters. These cells, however, exhibited normal neurite outgrowth when exposed to dibutyryl-cAMP, an agent that induces outgrowth independently from GAP-43. We observed opposite effects in pcHuD-transfected cells. The GAP-43 mRNA was stabilized in these cells, leading to an increase in the levels of the GAP-43 mRNA and protein. pcHuD cells were also found to grow short spontaneous neurites, a process that required the presence of GAP-43. In conclusion, our results suggest that HuD plays a critical role in PKC-mediated neurite outgrowth in PC12 cells and that this protein does so primarily by promoting the stabilization of the GAP-43 mRNA.

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  • Currently, there are only three known pathways that regulate the abundance or function of HuD: protein kinase C (PKC), coactivator-associated arginine methyltransferase 1 (CARM1), and protein kinase B (PKB/AKT).

    “Currently, there are only three known pathways that regulate the abundance or function of HuD: protein kinase C (PKC) (Mobarak et al. 2000; Pascale et al. 2005; Lim and Alkon 2012); coactivator-associated arginine methyltransferase 1 (CARM1) (Fujiwara et al. 2006; Hubers et al. 2010); and protein kinase B (PKB/AKT) (Fujiwara et al. 2011a).”

    From Emerging complexity of the HuD/ELAVl4 gene; implications for neuronal development, function, and dysfunction (2013) · cites this paper as Mobarak et al. 2000

    The Mobarak et al. citation is attached to the PKC pathway, not to CARM1 or PKB/AKT. The Discussion says PKC likely controls HuD function, but presents this as an inference rather than an established regulatory pathway; its experiments establish HuD’s role in PKC-dependent neurite outgrowth in PC12 cells. (LLM, conf=0.83)

    Experimental — accuracy not yet measured

  • HuD has an essential role in terminal differentiation, namely dendritic and axonal outgrowth.

    “Studies in which HuD levels were down-regulated or over-expressed in cultured cells have revealed an essential role for HuD in terminal differentiation, namely dendritic and axonal outgrowth (Wakamatsu and Weston 1997; Aranda-Abreu et al. 1999; Mobarak et al. 2000; Anderson et al. 2001; Hubers et al. 2010).”

    From Emerging complexity of the HuD/ELAVl4 gene; implications for neuronal development, function, and dysfunction (2013) · cites this paper as Mobarak et al. 2000

    The Results and Discussion show that reducing HuD impairs NGF- and PKC-dependent neurite outgrowth in PC12 cells, while overexpressing HuD promotes process outgrowth. But the study examines early, immature neurites rather than establishing an essential role in terminal differentiation or specifically in both dendritic and axonal outgrowth; cAMP-dependent outgrowth remains intact. Page numbers are not available in our copy. (LLM, conf=0.88)

    Experimental — accuracy not yet measured

  • Overexpression or down-regulation of HuD results in increased or decreased, respectively, GAP-43 mRNA levels and/or stability in cultured cells and the mouse nervous system.

    “Multiple studies have shown that overexpression or down-regulation of HuD results in increased or decreased, respectively, GAP-43 mRNA levels and/or stability in cultured cells and the mouse nervous system (Anderson et al. 2000, 2001; Mobarak et al. 2000; Bolognani et al. 2006, 2007a).”

    From Emerging complexity of the HuD/ELAVl4 gene; implications for neuronal development, function, and dysfunction (2013) · cites this paper as Mobarak et al. 2000

  • HuD is a focal downstream target of the neurite-extending pathway activated by NGF or phorbol ester, since HuD knockdown prevents neurite outgrowth in PC12 cells.

    “Importantly, HuD is a focal downstream target of this neurite-extending pathway since nerve growth factor (NGF) or phorbol ester treatment of PC12 cells following HuD knockdown prevents neurite outgrowth (Mobarak et al. 2000).”

    From Emerging complexity of the HuD/ELAVl4 gene; implications for neuronal development, function, and dysfunction (2013) · cites this paper as Mobarak et al. 2000

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Cited by

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Authors
Mobarak, C. D., Anderson, K. D., Morin, M., Beckel-Mitchener, A., Rogers, S. L., Furneaux, H., King, P., & Perrone-Bizzozero, N. I.
Affiliations
  • Departments of Neurosciences and
  • University of New Mexico (US)
  • Memorial Sloan Kettering Cancer Center (US)
  • University of Alabama at Birmingham (US)
ORCID
Venue
Molecular Biology of the Cell
Publisher
American Society for Cell Biology (ASCB)
Published
2000-09
Volume
11
Issue
9
Pages
3191-3203
ISSN
  • 1059-1524 (ISSN-L)
  • 1939-4586
DOI
10.1091/mbc.11.9.3191
PMC
PMC14985
OpenAlex
W2161629430
Cited by
133
References
3
Citations by year
2026: 1 · 2025: 2 · 2024: 1 · 2023: 1 · 2022: 2 · 2021: 5 · 2020: 2 · 2019: 3 · 2018: 2 · 2017: 5 · 2016: 4 · 2015: 7 · 2014: 5 · 2013: 11 · 2012: 4
FWCI
2.17
Type
journal article
Language
en
Open access
Locations
  • Molecular Biology of the Cell (publishedVersion)
  • Europe PMC (PubMed Central) (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
Funders
  • National Institutes of Health (5s06gm052576-04)
  • School of Medicine, University of New Mexico
  • National Institute of General Medical Sciences (GM 52576)
  • National Institute of Neurological Disorders and Stroke (NS 30255, R01NS030255)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Research and Splicing
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Axon Guidance and Neuronal Signaling
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Nerve injury and regeneration
Keywords
HUD, RNA-binding proteins, GAP-43, mRNA stability, 3' untranslated region, protein kinase C, neurite outgrowth, nerve growth factor, PC12 cells, neuronal differentiation, cAMP signaling
MeSH terms
Animals, Bucladesine, Gene Expression Regulation, Nerve Tissue Proteins, Protein Kinase C, Recombinant Proteins, RNA, Messenger, Tetradecanoylphorbol Acetate, Transcription, Genetic, Transfection, Neurites, RNA-Binding Proteins, PC12 Cells, GAP-43 Protein, Reverse Transcriptase Polymerase Chain Reaction, Nerve Growth Factor, Rats, ELAV Proteins

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