Two Drosophila model neurons can regenerate axons from the stump or from a converted dendrite, with feedback between the two sites

Abstract Background After axon severing, neurons recover function by reinitiating axon outgrowth. New outgrowth often originates from the remaining axon stump. However, in many mammalian neurons, new axons initiate from a dendritic site when the axon is injured close to the cell body. Methods Drosop...

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Main Authors: Kavitha S. Rao, Melissa M. Rolls
Format: Article
Language:English
Published: BMC 2017-08-01
Series:Neural Development
Subjects:
Online Access:http://link.springer.com/article/10.1186/s13064-017-0092-3
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spelling doaj-41f51681e5744017876c9cd1d3bcbfec2020-11-24T21:18:33ZengBMCNeural Development1749-81042017-08-0112111110.1186/s13064-017-0092-3Two Drosophila model neurons can regenerate axons from the stump or from a converted dendrite, with feedback between the two sitesKavitha S. Rao0Melissa M. Rolls1Department of Biochemistry and Molecular Biology, The Pennsylvania State UniversityDepartment of Biochemistry and Molecular Biology, The Pennsylvania State UniversityAbstract Background After axon severing, neurons recover function by reinitiating axon outgrowth. New outgrowth often originates from the remaining axon stump. However, in many mammalian neurons, new axons initiate from a dendritic site when the axon is injured close to the cell body. Methods Drosophila sensory neurons are ideal for studying neuronal injury responses because they can be injured reproducibly in a variety of genetic backgrounds. In Drosophila, it has been shown that a complex sensory neuron, ddaC, can regenerate an axon from a stump, and a simple sensory neuron, ddaE, can regenerate an axon from a dendrite. To provide a more complete picture of axon regeneration in these cell types, we performed additional injury types. Results We found that ddaE neurons can initiate regeneration from an axon stump when a stump remains. We also showed that ddaC neurons regenerate from the dendrite when the axon is severed close to the cell body. We next demonstrated if a stump remains, new axons can originate from this site and a dendrite at the same time. Because cutting the axon close to the cell body results in growth of the new axon from a dendrite, and cutting further out may not, we asked whether the initial response in the cell body was similar after both types of injury. A transcriptional reporter for axon injury signaling, puc-GFP, increased with similar timing and levels after proximal and distal axotomy. However, changes in dendritic microtubule polarity differed in response to the two types of injury, and were influenced by the presence of a scar at the distal axotomy site. Conclusions We conclude that both ddaE and ddaC can regenerate axons either from the stump or a dendrite, and that there is some feedback between the two sites that modulates dendritic microtubule polarity.http://link.springer.com/article/10.1186/s13064-017-0092-3Axon regenerationMicrotubule polarityLaser surgery
collection DOAJ
language English
format Article
sources DOAJ
author Kavitha S. Rao
Melissa M. Rolls
spellingShingle Kavitha S. Rao
Melissa M. Rolls
Two Drosophila model neurons can regenerate axons from the stump or from a converted dendrite, with feedback between the two sites
Neural Development
Axon regeneration
Microtubule polarity
Laser surgery
author_facet Kavitha S. Rao
Melissa M. Rolls
author_sort Kavitha S. Rao
title Two Drosophila model neurons can regenerate axons from the stump or from a converted dendrite, with feedback between the two sites
title_short Two Drosophila model neurons can regenerate axons from the stump or from a converted dendrite, with feedback between the two sites
title_full Two Drosophila model neurons can regenerate axons from the stump or from a converted dendrite, with feedback between the two sites
title_fullStr Two Drosophila model neurons can regenerate axons from the stump or from a converted dendrite, with feedback between the two sites
title_full_unstemmed Two Drosophila model neurons can regenerate axons from the stump or from a converted dendrite, with feedback between the two sites
title_sort two drosophila model neurons can regenerate axons from the stump or from a converted dendrite, with feedback between the two sites
publisher BMC
series Neural Development
issn 1749-8104
publishDate 2017-08-01
description Abstract Background After axon severing, neurons recover function by reinitiating axon outgrowth. New outgrowth often originates from the remaining axon stump. However, in many mammalian neurons, new axons initiate from a dendritic site when the axon is injured close to the cell body. Methods Drosophila sensory neurons are ideal for studying neuronal injury responses because they can be injured reproducibly in a variety of genetic backgrounds. In Drosophila, it has been shown that a complex sensory neuron, ddaC, can regenerate an axon from a stump, and a simple sensory neuron, ddaE, can regenerate an axon from a dendrite. To provide a more complete picture of axon regeneration in these cell types, we performed additional injury types. Results We found that ddaE neurons can initiate regeneration from an axon stump when a stump remains. We also showed that ddaC neurons regenerate from the dendrite when the axon is severed close to the cell body. We next demonstrated if a stump remains, new axons can originate from this site and a dendrite at the same time. Because cutting the axon close to the cell body results in growth of the new axon from a dendrite, and cutting further out may not, we asked whether the initial response in the cell body was similar after both types of injury. A transcriptional reporter for axon injury signaling, puc-GFP, increased with similar timing and levels after proximal and distal axotomy. However, changes in dendritic microtubule polarity differed in response to the two types of injury, and were influenced by the presence of a scar at the distal axotomy site. Conclusions We conclude that both ddaE and ddaC can regenerate axons either from the stump or a dendrite, and that there is some feedback between the two sites that modulates dendritic microtubule polarity.
topic Axon regeneration
Microtubule polarity
Laser surgery
url http://link.springer.com/article/10.1186/s13064-017-0092-3
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