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Interaction of survival of motor neuron (SMN) and HuD proteins with mRNA cpg15 rescues motor neuron axonal deficits
Open accessAbstract
Spinal muscular atrophy (SMA), caused by the deletion of the SMN1 gene, is the leading genetic cause of infant mortality. SMN protein is present at high levels in both axons and growth cones, and loss of its function disrupts axonal extension and pathfinding. SMN is known to associate with the RNA-binding protein hnRNP-R, and together they are responsible for the transport and/or local translation of β-actin mRNA in the growth cones of motor neurons. However, the full complement of SMN-interacting proteins in neurons remains unknown. Here we used mass spectrometry to identify HuD as a novel neuronal SMN-interacting partner. HuD is a neuron-specific RNA-binding protein that interacts with mRNAs, including candidate plasticity-related gene 15 (cpg15). We show that SMN and HuD form a complex in spinal motor axons, and that both interact with cpg15 mRNA in neurons. CPG15 is highly expressed in the developing ventral spinal cord and can promote motor axon branching and neuromuscular synapse formation, suggesting a crucial role in the development of motor axons and neuromuscular junctions. Cpg15 mRNA previously has been shown to localize into axonal processes. Here we show that SMN deficiency reduces cpg15 mRNA levels in neurons, and, more importantly, cpg15 overexpression partially rescues the SMN-deficiency phenotype in zebrafish. Our results provide insight into the function of SMN protein in axons and also identify potential targets for the study of mechanisms that lead to the SMA pathology and related neuromuscular diseases.
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“Importantly, overexpression of HuD or of one of its target mRNAs (cpg-15) was found to partially rescue SMA-like defects related to cell morphology and recruitment of specific mRNAs into RNA granules (Hubers et al. 2010; Akten et al. 2011).”
From Emerging complexity of the HuD/ELAVl4 gene; implications for neuronal development, function, and dysfunction (2013) · cites this paper as Akten et al. 2011
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“A series of cell imaging and biochemical experiments in three independent studies demonstrated that HuD interacts with SMN protein in axonal compartments of neurons (Hubers et al. 2010; Akten et al. 2011; Fallini et al. 2011).”
From Emerging complexity of the HuD/ELAVl4 gene; implications for neuronal development, function, and dysfunction (2013) · cites this paper as Akten et al. 2011
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Thelen, M. P., Wirth, B., & Kye, M. J. (2020) · Figshare · doi:10.6084/m9.figshare.13481043
Self-citationThelen, M. P., Wirth, B., & Kye, M. J. (2020) · Figshare · doi:10.6084/m9.figshare.13481037
Self-citationNon–Cell-Autonomous Mechanisms and Systemic Interactions in Spinal Muscular Atrophy
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Dodré, M. (2014) · theses.fr (ABES) · doi:10.70675/b97d6973z95aaz4364z8030z3b86fc1d910d
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Metadata
- Authors
- Akten, B., Kye, M. J., Hao, L. T., Wertz, M. H., Singh, S., Nie, D., Huang, J., Merianda, T. T., Twiss, J. L., Beattie, C. E., Steen, J. A. J., & Sahin, M.
- Affiliations
- Boston Children's Hospital (US)
- The Ohio State University (US)
- Drexel University (US)
- The F.M. Kirby Neurobiology Center, Department of Neurology, Children's Hospital Boston, Harvard Medical School, Boston, MA 02115;
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2011-06-07
- Volume
- 108
- Issue
- 25
- Pages
- 10337-10342
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC3121858
- OpenAlex
- W2013174632
- Cited by
- 203
- References
- 36
- Citations by year
- 2026: 7 · 2025: 4 · 2024: 4 · 2023: 11 · 2022: 12 · 2021: 15 · 2020: 18 · 2019: 8 · 2018: 13 · 2017: 21 · 2016: 18 · 2015: 13 · 2014: 21 · 2013: 22 · 2012: 12
- FWCI
- 9.58
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Spinal Muscular Atrophy Foundation
- Hearst Foundations
- Harvard NeuroDiscovery Center
- National Institutes of Health
- National Institute of Neurological Disorders and Stroke (NS050414, R01 NS66973, NS 041596, R01NS050414, R01NS066973, R56NS050414, R01NS041596)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (P30HD018655, P30HD-18655)
- Topics
- Health Sciences › Medicine › Genetics (clinical) › Neurogenetic and Muscular Disorders Research
- Health Sciences › Medicine › Clinical Neurology › Amyotrophic Lateral Sclerosis Research
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Hereditary Neurological Disorders
- Keywords
- spinal muscular atrophy, SMN protein, HUD, RNA-binding proteins, motor neuron axons, axon branching, neuromuscular synapse formation
- MeSH terms
- ELAV-Like Protein 4, Animals, Axons, Cells, Cultured, Embryo, Mammalian, Humans, Motor Neurons, Nerve Tissue Proteins, Neuropeptides, Recombinant Fusion Proteins, RNA, Messenger, Zebrafish, Animals, Genetically Modified, Mice, ELAV Proteins, Survival of Motor Neuron 1 Protein, GPI-Linked Proteins
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