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Neuron-specific knock-down of SMN1 causes neuron degeneration and death through an apoptotic mechanism

Spinal muscular atrophy is a devastating disease that is characterized by degeneration and death of a specific subclass of motor neurons in the anterior horn of the spinal cord. Although the gene responsible, survival motor neuron 1 (SMN1), was identified 20 years ago, it has proven difficult to inv...

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Autores principales: Gallotta, Ivan, Mazzarella, Nadia, Donato, Alessandra, Esposito, Alessandro, Chaplin, Justin C., Castro, Silvana, Zampi, Giuseppina, Battaglia, Giorgio S., Hilliard, Massimo A., Bazzicalupo, Paolo, Di Schiavi, Elia
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5181630/
https://www.ncbi.nlm.nih.gov/pubmed/27260405
http://dx.doi.org/10.1093/hmg/ddw119
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author Gallotta, Ivan
Mazzarella, Nadia
Donato, Alessandra
Esposito, Alessandro
Chaplin, Justin C.
Castro, Silvana
Zampi, Giuseppina
Battaglia, Giorgio S.
Hilliard, Massimo A.
Bazzicalupo, Paolo
Di Schiavi, Elia
author_facet Gallotta, Ivan
Mazzarella, Nadia
Donato, Alessandra
Esposito, Alessandro
Chaplin, Justin C.
Castro, Silvana
Zampi, Giuseppina
Battaglia, Giorgio S.
Hilliard, Massimo A.
Bazzicalupo, Paolo
Di Schiavi, Elia
author_sort Gallotta, Ivan
collection PubMed
description Spinal muscular atrophy is a devastating disease that is characterized by degeneration and death of a specific subclass of motor neurons in the anterior horn of the spinal cord. Although the gene responsible, survival motor neuron 1 (SMN1), was identified 20 years ago, it has proven difficult to investigate its effects in vivo. Consequently, a number of key questions regarding the molecular and cellular functions of this molecule have remained unanswered. We developed a Caenorhabditis elegans model of smn-1 loss-of-function using a neuron-specific RNA interference strategy to knock-down smn-1 selectively in a subclass of motor neurons. The transgenic animals presented a cell-autonomous, age-dependent degeneration of motor neurons detected as locomotory defects and the disappearance of presynaptic and cytoplasmic fluorescent markers in targeted neurons. This degeneration led to neuronal death as revealed by positive reactivity to genetic and chemical cell-death markers. We show that genes of the classical apoptosis pathway are involved in the smn-1-mediated neuronal death, and that this phenotype can be rescued by the expression of human SMN1, indicating a functional conservation between the two orthologs. Finally, we determined that Plastin3/plst-1 genetically interacts with smn-1 to prevent degeneration, and that treatment with valproic acid is able to rescue the degenerative phenotype. These results provide novel insights into the cellular and molecular mechanisms that lead to the loss of motor neurons when SMN1 function is reduced.
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spelling pubmed-51816302016-12-27 Neuron-specific knock-down of SMN1 causes neuron degeneration and death through an apoptotic mechanism Gallotta, Ivan Mazzarella, Nadia Donato, Alessandra Esposito, Alessandro Chaplin, Justin C. Castro, Silvana Zampi, Giuseppina Battaglia, Giorgio S. Hilliard, Massimo A. Bazzicalupo, Paolo Di Schiavi, Elia Hum Mol Genet Articles Spinal muscular atrophy is a devastating disease that is characterized by degeneration and death of a specific subclass of motor neurons in the anterior horn of the spinal cord. Although the gene responsible, survival motor neuron 1 (SMN1), was identified 20 years ago, it has proven difficult to investigate its effects in vivo. Consequently, a number of key questions regarding the molecular and cellular functions of this molecule have remained unanswered. We developed a Caenorhabditis elegans model of smn-1 loss-of-function using a neuron-specific RNA interference strategy to knock-down smn-1 selectively in a subclass of motor neurons. The transgenic animals presented a cell-autonomous, age-dependent degeneration of motor neurons detected as locomotory defects and the disappearance of presynaptic and cytoplasmic fluorescent markers in targeted neurons. This degeneration led to neuronal death as revealed by positive reactivity to genetic and chemical cell-death markers. We show that genes of the classical apoptosis pathway are involved in the smn-1-mediated neuronal death, and that this phenotype can be rescued by the expression of human SMN1, indicating a functional conservation between the two orthologs. Finally, we determined that Plastin3/plst-1 genetically interacts with smn-1 to prevent degeneration, and that treatment with valproic acid is able to rescue the degenerative phenotype. These results provide novel insights into the cellular and molecular mechanisms that lead to the loss of motor neurons when SMN1 function is reduced. Oxford University Press 2016-06-15 2016-06-03 /pmc/articles/PMC5181630/ /pubmed/27260405 http://dx.doi.org/10.1093/hmg/ddw119 Text en © The Author 2016. Published by Oxford University Press. http://creativecommons.org/licenses/by-nc/4.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com
spellingShingle Articles
Gallotta, Ivan
Mazzarella, Nadia
Donato, Alessandra
Esposito, Alessandro
Chaplin, Justin C.
Castro, Silvana
Zampi, Giuseppina
Battaglia, Giorgio S.
Hilliard, Massimo A.
Bazzicalupo, Paolo
Di Schiavi, Elia
Neuron-specific knock-down of SMN1 causes neuron degeneration and death through an apoptotic mechanism
title Neuron-specific knock-down of SMN1 causes neuron degeneration and death through an apoptotic mechanism
title_full Neuron-specific knock-down of SMN1 causes neuron degeneration and death through an apoptotic mechanism
title_fullStr Neuron-specific knock-down of SMN1 causes neuron degeneration and death through an apoptotic mechanism
title_full_unstemmed Neuron-specific knock-down of SMN1 causes neuron degeneration and death through an apoptotic mechanism
title_short Neuron-specific knock-down of SMN1 causes neuron degeneration and death through an apoptotic mechanism
title_sort neuron-specific knock-down of smn1 causes neuron degeneration and death through an apoptotic mechanism
topic Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5181630/
https://www.ncbi.nlm.nih.gov/pubmed/27260405
http://dx.doi.org/10.1093/hmg/ddw119
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