Low-density Lipoprotein Receptor-related Proteins in a Novel Mechanism of Axon Guidance and Peripheral Nerve Regeneration

The low-density lipoprotein receptor-related protein receptors 1 and 2 (LRP1 and LRP2) are emerging as important cell signaling mediators in modulating neuronal growth and repair. We examined whether LRP1 and LRP2 are able to mediate a specific aspect of neuronal growth: axon guidance. We sought to...

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Veröffentlicht in:The Journal of biological chemistry 2016-01, Vol.291 (3), p.1092-1102
Hauptverfasser: Landowski, Lila M., Pavez, Macarena, Brown, Lachlan S., Gasperini, Robert, Taylor, Bruce V., West, Adrian K., Foa, Lisa
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container_issue 3
container_start_page 1092
container_title The Journal of biological chemistry
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creator Landowski, Lila M.
Pavez, Macarena
Brown, Lachlan S.
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Taylor, Bruce V.
West, Adrian K.
Foa, Lisa
description The low-density lipoprotein receptor-related protein receptors 1 and 2 (LRP1 and LRP2) are emerging as important cell signaling mediators in modulating neuronal growth and repair. We examined whether LRP1 and LRP2 are able to mediate a specific aspect of neuronal growth: axon guidance. We sought to identify LRP1 and LRP2 ligands that could induce axonal chemoattraction, which might have therapeutic potential. Using embryonic sensory neurons (rat dorsal root ganglia) in a growth cone turning assay, we tested a range of LRP1 and LRP2 ligands for the ability to guide growth cone navigation. Three ligands were chemorepulsive: α-2-macroglobulin, tissue plasminogen activator, and metallothionein III. Conversely, only one LRP ligand, metallothionein II, was found to be chemoattractive. Chemoattraction toward a gradient of metallothionein II was calcium-dependent, required the expression of both LRP1 and LRP2, and likely involves further co-receptors such as the tropomyosin-related kinase A (TrkA) receptor. The potential for LRP-mediated chemoattraction to mediate axonal regeneration was examined in vivo in a model of chemical denervation in adult rats. In these in vivo studies, metallothionein II was shown to enhance epidermal nerve fiber regeneration so that it was complete within 7 days compared with 14 days in saline-treated animals. Our data demonstrate that both LRP1 and LRP2 are necessary for metallothionein II-mediated chemotactic signal transduction and that they may form part of a signaling complex. Furthermore, the data suggest that LRP-mediated chemoattraction represents a novel, non-classical signaling system that has therapeutic potential as a disease-modifying agent for the injured peripheral nervous system.
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In these in vivo studies, metallothionein II was shown to enhance epidermal nerve fiber regeneration so that it was complete within 7 days compared with 14 days in saline-treated animals. Our data demonstrate that both LRP1 and LRP2 are necessary for metallothionein II-mediated chemotactic signal transduction and that they may form part of a signaling complex. 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Pavez, Macarena ; Brown, Lachlan S. ; Gasperini, Robert ; Taylor, Bruce V. ; West, Adrian K. ; Foa, Lisa</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c542t-2be450d6acb44f831199f1b87b0434766edc7a7818d6caa4d738c0b65f4172123</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2016</creationdate><topic>Animals</topic><topic>axon</topic><topic>Axons - drug effects</topic><topic>Axons - physiology</topic><topic>Calcium Signaling - drug effects</topic><topic>cell signaling</topic><topic>Cells, Cultured</topic><topic>Chemotaxis - drug effects</topic><topic>Epidermis - drug effects</topic><topic>Epidermis - innervation</topic><topic>Ganglia, Spinal - cytology</topic><topic>Ganglia, Spinal - drug effects</topic><topic>Ganglia, Spinal - physiology</topic><topic>growth cone</topic><topic>Growth Cones - drug effects</topic><topic>Growth Cones - metabolism</topic><topic>Ligands</topic><topic>Low Density Lipoprotein Receptor-Related Protein-1 - agonists</topic><topic>Low Density Lipoprotein Receptor-Related Protein-1 - antagonists &amp; inhibitors</topic><topic>Low Density Lipoprotein Receptor-Related Protein-1 - genetics</topic><topic>Low Density Lipoprotein Receptor-Related Protein-1 - metabolism</topic><topic>Low Density Lipoprotein Receptor-Related Protein-2 - agonists</topic><topic>Low Density Lipoprotein Receptor-Related Protein-2 - antagonists &amp; inhibitors</topic><topic>Low Density Lipoprotein Receptor-Related Protein-2 - genetics</topic><topic>Low Density Lipoprotein Receptor-Related Protein-2 - metabolism</topic><topic>LRP1</topic><topic>LRP2</topic><topic>Male</topic><topic>metallothionein</topic><topic>Metallothionein - pharmacology</topic><topic>Metallothionein - therapeutic use</topic><topic>Nerve Regeneration - drug effects</topic><topic>Nerve Tissue Proteins - agonists</topic><topic>Nerve Tissue Proteins - antagonists &amp; inhibitors</topic><topic>Nerve Tissue Proteins - genetics</topic><topic>Nerve Tissue Proteins - metabolism</topic><topic>neurite outgrowth</topic><topic>Neurobiology</topic><topic>Neurogenesis - drug effects</topic><topic>Peripheral Nerves - cytology</topic><topic>Peripheral Nerves - drug effects</topic><topic>Peripheral Nerves - physiology</topic><topic>Peripheral Nervous System Diseases - drug therapy</topic><topic>Peripheral Nervous System Diseases - physiopathology</topic><topic>Rabbits</topic><topic>Rats, Sprague-Dawley</topic><topic>regeneration</topic><topic>RNA Interference</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Landowski, Lila M.</creatorcontrib><creatorcontrib>Pavez, Macarena</creatorcontrib><creatorcontrib>Brown, Lachlan S.</creatorcontrib><creatorcontrib>Gasperini, Robert</creatorcontrib><creatorcontrib>Taylor, Bruce V.</creatorcontrib><creatorcontrib>West, Adrian K.</creatorcontrib><creatorcontrib>Foa, Lisa</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Neurosciences Abstracts</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The Journal of biological chemistry</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Landowski, Lila M.</au><au>Pavez, Macarena</au><au>Brown, Lachlan S.</au><au>Gasperini, Robert</au><au>Taylor, Bruce V.</au><au>West, Adrian K.</au><au>Foa, Lisa</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Low-density Lipoprotein Receptor-related Proteins in a Novel Mechanism of Axon Guidance and Peripheral Nerve Regeneration</atitle><jtitle>The Journal of biological chemistry</jtitle><addtitle>J Biol Chem</addtitle><date>2016-01-15</date><risdate>2016</risdate><volume>291</volume><issue>3</issue><spage>1092</spage><epage>1102</epage><pages>1092-1102</pages><issn>0021-9258</issn><eissn>1083-351X</eissn><abstract>The low-density lipoprotein receptor-related protein receptors 1 and 2 (LRP1 and LRP2) are emerging as important cell signaling mediators in modulating neuronal growth and repair. 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subjects Animals
axon
Axons - drug effects
Axons - physiology
Calcium Signaling - drug effects
cell signaling
Cells, Cultured
Chemotaxis - drug effects
Epidermis - drug effects
Epidermis - innervation
Ganglia, Spinal - cytology
Ganglia, Spinal - drug effects
Ganglia, Spinal - physiology
growth cone
Growth Cones - drug effects
Growth Cones - metabolism
Ligands
Low Density Lipoprotein Receptor-Related Protein-1 - agonists
Low Density Lipoprotein Receptor-Related Protein-1 - antagonists & inhibitors
Low Density Lipoprotein Receptor-Related Protein-1 - genetics
Low Density Lipoprotein Receptor-Related Protein-1 - metabolism
Low Density Lipoprotein Receptor-Related Protein-2 - agonists
Low Density Lipoprotein Receptor-Related Protein-2 - antagonists & inhibitors
Low Density Lipoprotein Receptor-Related Protein-2 - genetics
Low Density Lipoprotein Receptor-Related Protein-2 - metabolism
LRP1
LRP2
Male
metallothionein
Metallothionein - pharmacology
Metallothionein - therapeutic use
Nerve Regeneration - drug effects
Nerve Tissue Proteins - agonists
Nerve Tissue Proteins - antagonists & inhibitors
Nerve Tissue Proteins - genetics
Nerve Tissue Proteins - metabolism
neurite outgrowth
Neurobiology
Neurogenesis - drug effects
Peripheral Nerves - cytology
Peripheral Nerves - drug effects
Peripheral Nerves - physiology
Peripheral Nervous System Diseases - drug therapy
Peripheral Nervous System Diseases - physiopathology
Rabbits
Rats, Sprague-Dawley
regeneration
RNA Interference
title Low-density Lipoprotein Receptor-related Proteins in a Novel Mechanism of Axon Guidance and Peripheral Nerve Regeneration
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