A conserved morphogenetic mechanism for epidermal ensheathment of nociceptive sensory neurites

Interactions between epithelial cells and neurons influence a range of sensory modalities including taste, touch, and smell. Vertebrate and invertebrate epidermal cells ensheath peripheral arbors of somatosensory neurons, including nociceptors, yet the developmental origins and functional roles of t...

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Published ineLife Vol. 8
Main Authors Jiang, Nan, Rasmussen, Jeffrey P, Clanton, Joshua A, Rosenberg, Marci F, Luedke, Kory P, Cronan, Mark R, Parker, Edward D, Kim, Hyeon-Jin, Vaughan, Joshua C, Sagasti, Alvaro, Parrish, Jay Z
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Published England eLife Science Publications, Ltd 11.03.2019
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Abstract Interactions between epithelial cells and neurons influence a range of sensory modalities including taste, touch, and smell. Vertebrate and invertebrate epidermal cells ensheath peripheral arbors of somatosensory neurons, including nociceptors, yet the developmental origins and functional roles of this ensheathment are largely unknown. Here, we describe an evolutionarily conserved morphogenetic mechanism for epidermal ensheathment of somatosensory neurites. We found that somatosensory neurons in and zebrafish induce formation of epidermal sheaths, which wrap neurites of different types of neurons to different extents. Neurites induce formation of plasma membrane phosphatidylinositol 4,5-bisphosphate microdomains at nascent sheaths, followed by a filamentous actin network, and recruitment of junctional proteins that likely form autotypic junctions to seal sheaths. Finally, blocking epidermal sheath formation destabilized dendrite branches and reduced nociceptive sensitivity in . Epidermal somatosensory neurite ensheathment is thus a deeply conserved cellular process that contributes to the morphogenesis and function of nociceptive sensory neurons.
AbstractList Interactions between epithelial cells and neurons influence a range of sensory modalities including taste, touch, and smell. Vertebrate and invertebrate epidermal cells ensheath peripheral arbors of somatosensory neurons, including nociceptors, yet the developmental origins and functional roles of this ensheathment are largely unknown. Here, we describe an evolutionarily conserved morphogenetic mechanism for epidermal ensheathment of somatosensory neurites. We found that somatosensory neurons in Drosophila and zebrafish induce formation of epidermal sheaths, which wrap neurites of different types of neurons to different extents. Neurites induce formation of plasma membrane phosphatidylinositol 4,5-bisphosphate microdomains at nascent sheaths, followed by a filamentous actin network, and recruitment of junctional proteins that likely form autotypic junctions to seal sheaths. Finally, blocking epidermal sheath formation destabilized dendrite branches and reduced nociceptive sensitivity in Drosophila. Epidermal somatosensory neurite ensheathment is thus a deeply conserved cellular process that contributes to the morphogenesis and function of nociceptive sensory neurons.
Interactions between epithelial cells and neurons influence a range of sensory modalities including taste, touch, and smell. Vertebrate and invertebrate epidermal cells ensheath peripheral arbors of somatosensory neurons, including nociceptors, yet the developmental origins and functional roles of this ensheathment are largely unknown. Here, we describe an evolutionarily conserved morphogenetic mechanism for epidermal ensheathment of somatosensory neurites. We found that somatosensory neurons in Drosophila and zebrafish induce formation of epidermal sheaths, which wrap neurites of different types of neurons to different extents. Neurites induce formation of plasma membrane phosphatidylinositol 4,5-bisphosphate microdomains at nascent sheaths, followed by a filamentous actin network, and recruitment of junctional proteins that likely form autotypic junctions to seal sheaths. Finally, blocking epidermal sheath formation destabilized dendrite branches and reduced nociceptive sensitivity in Drosophila . Epidermal somatosensory neurite ensheathment is thus a deeply conserved cellular process that contributes to the morphogenesis and function of nociceptive sensory neurons. Humans and other animals perceive and interact with the outside world through their sensory nervous system. Nerve cells, acting as the body’s ‘telegraph wires’, convey signals from sensory organs – like the eyes – to the brain, which then processes this information and tells the body how to respond. There are different kinds of sensory nerve cells that carry different types of information, but they all associate closely with the tissues and organs they connect to the brain. Human skin contains sensory nerve cells, which underpin our senses of touch and pain. There is a highly specialized, complex connection between some of these nerve cells and cells in the skin: the skin cells wrap tightly around the nerve cells’ free ends, forming sheath-like structures. This ‘ensheathment’ process happens in a wide range of animals, including those with a backbone, like fish and humans, and those without, like insects. Ensheathment is thought to be important for the skin’s nerve cells to work properly. Yet it remains unclear how or when these connections first appear. Jiang et al. therefore wanted to determine the developmental origins of ensheathment and to find out if these were also similar in animals with and without backbones. Experiments using fruit fly and zebrafish embryos revealed that nerve cells, not skin cells, were responsible for forming and maintaining the sheaths. In embryos where groups of sensory nerve cells were selectively killed – either using a laser or by making the cells produce a toxin – ensheathment did not occur. Further studies, using a variety of microscopy techniques, revealed that the molecular machinery required to stabilize the sheaths was similar in both fish and flies, and therefore likely to be conserved across different groups of animals. Removing sheaths in fly embryos led to nerve cells becoming unstable; the animals were also less sensitive to touch. This confirmed that ensheathment was indeed necessary for sensory nerve cells to work properly. By revealing how ensheathment first emerges, these findings shed new light on how the sensory nervous system develops and how its activity is controlled. In humans, skin cells ensheath the nerve cells responsible for sensing pain. A better understanding of how ensheathments first arise could therefore lead to new avenues for treating chronic pain and related conditions.
Interactions between epithelial cells and neurons influence a range of sensory modalities including taste, touch, and smell. Vertebrate and invertebrate epidermal cells ensheath peripheral arbors of somatosensory neurons, including nociceptors, yet the developmental origins and functional roles of this ensheathment are largely unknown. Here, we describe an evolutionarily conserved morphogenetic mechanism for epidermal ensheathment of somatosensory neurites. We found that somatosensory neurons in Drosophila and zebrafish induce formation of epidermal sheaths, which wrap neurites of different types of neurons to different extents. Neurites induce formation of plasma membrane phosphatidylinositol 4,5-bisphosphate microdomains at nascent sheaths, followed by a filamentous actin network, and recruitment of junctional proteins that likely form autotypic junctions to seal sheaths. Finally, blocking epidermal sheath formation destabilized dendrite branches and reduced nociceptive sensitivity in Drosophila. Epidermal somatosensory neurite ensheathment is thus a deeply conserved cellular process that contributes to the morphogenesis and function of nociceptive sensory neurons. eLife digest Humans and other animals perceive and interact with the outside world through their sensory nervous system. Nerve cells, acting as the body's 'telegraph wires', convey signals from sensory organs -- like the eyes -- to the brain, which then processes this information and tells the body how to respond. There are different kinds of sensory nerve cells that carry different types of information, but they all associate closely with the tissues and organs they connect to the brain. Human skin contains sensory nerve cells, which underpin our senses of touch and pain. There is a highly specialized, complex connection between some of these nerve cells and cells in the skin: the skin cells wrap tightly around the nerve cells' free ends, forming sheath-like structures. This 'ensheathment' process happens in a wide range of animals, including those with a backbone, like fish and humans, and those without, like insects. Ensheathment is thought to be important for the skin's nerve cells to work properly. Yet it remains unclear how or when these connections first appear. Jiang et al. therefore wanted to determine the developmental origins of ensheathment and to find out if these were also similar in animals with and without backbones. Experiments using fruit fly and zebrafish embryos revealed that nerve cells, not skin cells, were responsible for forming and maintaining the sheaths. In embryos where groups of sensory nerve cells were selectively killed -- either using a laser or by making the cells produce a toxin -- ensheathment did not occur. Further studies, using a variety of microscopy techniques, revealed that the molecular machinery required to stabilize the sheaths was similar in both fish and flies, and therefore likely to be conserved across different groups of animals. Removing sheaths in fly embryos led to nerve cells becoming unstable; the animals were also less sensitive to touch. This confirmed that ensheathment was indeed necessary for sensory nerve cells to work properly. By revealing how ensheathment first emerges, these findings shed new light on how the sensory nervous system develops and how its activity is controlled. In humans, skin cells ensheath the nerve cells responsible for sensing pain. A better understanding of how ensheathments first arise could therefore lead to new avenues for treating chronic pain and related conditions.
Interactions between epithelial cells and neurons influence a range of sensory modalities including taste, touch, and smell. Vertebrate and invertebrate epidermal cells ensheath peripheral arbors of somatosensory neurons, including nociceptors, yet the developmental origins and functional roles of this ensheathment are largely unknown. Here, we describe an evolutionarily conserved morphogenetic mechanism for epidermal ensheathment of somatosensory neurites. We found that somatosensory neurons in and zebrafish induce formation of epidermal sheaths, which wrap neurites of different types of neurons to different extents. Neurites induce formation of plasma membrane phosphatidylinositol 4,5-bisphosphate microdomains at nascent sheaths, followed by a filamentous actin network, and recruitment of junctional proteins that likely form autotypic junctions to seal sheaths. Finally, blocking epidermal sheath formation destabilized dendrite branches and reduced nociceptive sensitivity in . Epidermal somatosensory neurite ensheathment is thus a deeply conserved cellular process that contributes to the morphogenesis and function of nociceptive sensory neurons.
Interactions between epithelial cells and neurons influence a range of sensory modalities including taste, touch, and smell. Vertebrate and invertebrate epidermal cells ensheath peripheral arbors of somatosensory neurons, including nociceptors, yet the developmental origins and functional roles of this ensheathment are largely unknown. Here, we describe an evolutionarily conserved morphogenetic mechanism for epidermal ensheathment of somatosensory neurites. We found that somatosensory neurons in Drosophila and zebrafish induce formation of epidermal sheaths, which wrap neurites of different types of neurons to different extents. Neurites induce formation of plasma membrane phosphatidylinositol 4,5-bisphosphate microdomains at nascent sheaths, followed by a filamentous actin network, and recruitment of junctional proteins that likely form autotypic junctions to seal sheaths. Finally, blocking epidermal sheath formation destabilized dendrite branches and reduced nociceptive sensitivity in Drosophila. Epidermal somatosensory neurite ensheathment is thus a deeply conserved cellular process that contributes to the morphogenesis and function of nociceptive sensory neurons. Humans and other animals perceive and interact with the outside world through their sensory nervous system. Nerve cells, acting as the body’s ‘telegraph wires’, convey signals from sensory organs – like the eyes – to the brain, which then processes this information and tells the body how to respond. There are different kinds of sensory nerve cells that carry different types of information, but they all associate closely with the tissues and organs they connect to the brain. Human skin contains sensory nerve cells, which underpin our senses of touch and pain. There is a highly specialized, complex connection between some of these nerve cells and cells in the skin: the skin cells wrap tightly around the nerve cells’ free ends, forming sheath-like structures. This ‘ensheathment’ process happens in a wide range of animals, including those with a backbone, like fish and humans, and those without, like insects. Ensheathment is thought to be important for the skin’s nerve cells to work properly. Yet it remains unclear how or when these connections first appear. Jiang et al. therefore wanted to determine the developmental origins of ensheathment and to find out if these were also similar in animals with and without backbones. Experiments using fruit fly and zebrafish embryos revealed that nerve cells, not skin cells, were responsible for forming and maintaining the sheaths. In embryos where groups of sensory nerve cells were selectively killed – either using a laser or by making the cells produce a toxin – ensheathment did not occur. Further studies, using a variety of microscopy techniques, revealed that the molecular machinery required to stabilize the sheaths was similar in both fish and flies, and therefore likely to be conserved across different groups of animals. Removing sheaths in fly embryos led to nerve cells becoming unstable; the animals were also less sensitive to touch. This confirmed that ensheathment was indeed necessary for sensory nerve cells to work properly. By revealing how ensheathment first emerges, these findings shed new light on how the sensory nervous system develops and how its activity is controlled. In humans, skin cells ensheath the nerve cells responsible for sensing pain. A better understanding of how ensheathments first arise could therefore lead to new avenues for treating chronic pain and related conditions.
Audience Academic
Author Luedke, Kory P
Rasmussen, Jeffrey P
Parker, Edward D
Rosenberg, Marci F
Jiang, Nan
Clanton, Joshua A
Cronan, Mark R
Parrish, Jay Z
Vaughan, Joshua C
Kim, Hyeon-Jin
Sagasti, Alvaro
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/30855229$$D View this record in MEDLINE/PubMed
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Fri Oct 25 08:33:46 EDT 2024
Sat Nov 09 14:38:28 EST 2024
Tue Nov 19 20:36:40 EST 2024
Tue Nov 12 23:29:34 EST 2024
Thu Aug 01 19:11:50 EDT 2024
Fri Dec 06 04:06:39 EST 2024
Wed Oct 16 00:47:02 EDT 2024
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Keywords Drosophila
neuroscience
nociception
ensheathment
zebrafish
D. melanogaster
epidermis
somatosensory neuron
Language English
License 2019, Jiang et al.
http://creativecommons.org/licenses/by/4.0
This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.
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content type line 23
Department of Biology, University of Washington, Seattle, United States.
ORCID 0000-0002-6550-8935
0000-0002-6823-0692
0000-0002-0656-9148
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Snippet Interactions between epithelial cells and neurons influence a range of sensory modalities including taste, touch, and smell. Vertebrate and invertebrate...
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SourceType Open Website
Open Access Repository
Aggregation Database
Index Database
SubjectTerms Actin
Animals
Axonogenesis
Cell membranes
Chronic pain
Drosophila
ensheathment
Epidermal Cells - cytology
Epidermal Cells - physiology
epidermis
Epidermis - anatomy & histology
Epidermis - growth & development
Epithelial cells
Fruit flies (Tephritidae)
Insects
Invertebrates
Machinery
Microscopy
Morphogenesis
Muscle proteins
Neural circuitry
Neurons
Neuroscience
nociception
Nociceptors
Nociceptors - cytology
Nociceptors - physiology
Observations
Olfaction
Pain management
Pain perception
Phosphatidylinositol 4,5-diphosphate
Phospholipids
Physiological aspects
Proteins
Sensory neurons
Sheaths
Skin
somatosensory neuron
Zebrafish
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Title A conserved morphogenetic mechanism for epidermal ensheathment of nociceptive sensory neurites
URI https://www.ncbi.nlm.nih.gov/pubmed/30855229
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Volume 8
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