Syncrip/hnRNP Q influences synaptic transmission and regulates BMP signaling at the Drosophila neuromuscular synapse

Synaptic plasticity involves the modulation of synaptic connections in response to neuronal activity via multiple pathways. One mechanism modulates synaptic transmission by retrograde signals from the post-synapse that influence the probability of vesicle release in the pre-synapse. Despite its impo...

Full description

Bibliographic Details
Main Authors: James M. Halstead, Yong Qi Lin, Lita Durraine, Russell S. Hamilton, Graeme Ball, Greg G. Neely, Hugo J. Bellen, Ilan Davis
Format: Article
Language:English
Published: The Company of Biologists 2014-08-01
Series:Biology Open
Subjects:
Online Access:http://bio.biologists.org/content/3/9/839
_version_ 1818656727936008192
author James M. Halstead
Yong Qi Lin
Lita Durraine
Russell S. Hamilton
Graeme Ball
Greg G. Neely
Hugo J. Bellen
Ilan Davis
author_facet James M. Halstead
Yong Qi Lin
Lita Durraine
Russell S. Hamilton
Graeme Ball
Greg G. Neely
Hugo J. Bellen
Ilan Davis
author_sort James M. Halstead
collection DOAJ
description Synaptic plasticity involves the modulation of synaptic connections in response to neuronal activity via multiple pathways. One mechanism modulates synaptic transmission by retrograde signals from the post-synapse that influence the probability of vesicle release in the pre-synapse. Despite its importance, very few factors required for the expression of retrograde signals, and proper synaptic transmission, have been identified. Here, we identify the conserved RNA binding protein Syncrip as a new factor that modulates the efficiency of vesicle release from the motoneuron and is required for correct synapse structure. We show that syncrip is required genetically and its protein product is detected only in the muscle and not in the motoneuron itself. This unexpected non-autonomy is at least partly explained by the fact that Syncrip modulates retrograde BMP signals from the muscle back to the motoneuron. We show that Syncrip influences the levels of the Bone Morphogenic Protein ligand Glass Bottom Boat from the post-synapse and regulates the pre-synapse. Our results highlight the RNA-binding protein Syncrip as a novel regulator of synaptic output. Given its known role in regulating translation, we propose that Syncrip is important for maintaining a balance between the strength of presynaptic vesicle release and postsynaptic translation.
first_indexed 2024-12-17T03:30:11Z
format Article
id doaj.art-28aebf7f02234fd8a1701fb25d3ecd30
institution Directory Open Access Journal
issn 2046-6390
language English
last_indexed 2024-12-17T03:30:11Z
publishDate 2014-08-01
publisher The Company of Biologists
record_format Article
series Biology Open
spelling doaj.art-28aebf7f02234fd8a1701fb25d3ecd302022-12-21T22:05:17ZengThe Company of BiologistsBiology Open2046-63902014-08-013983984910.1242/bio.2014902720149027Syncrip/hnRNP Q influences synaptic transmission and regulates BMP signaling at the Drosophila neuromuscular synapseJames M. Halstead0Yong Qi Lin1Lita Durraine2Russell S. Hamilton3Graeme Ball4Greg G. Neely5Hugo J. Bellen6Ilan Davis7 Department of Biochemistry, South Parks Road, The University of Oxford, Oxford OX1 3QU, UK Howard Hughes Medical Institute, Department of Molecular and Human Genetics, Department of Neuroscience, Program in Developmental Biology, Neurological Research Institute at Baylor College of Medicine, Houston, TX 77030, USA Howard Hughes Medical Institute, Department of Molecular and Human Genetics, Department of Neuroscience, Program in Developmental Biology, Neurological Research Institute at Baylor College of Medicine, Houston, TX 77030, USA Department of Biochemistry, South Parks Road, The University of Oxford, Oxford OX1 3QU, UK Micron Imaging Facility, Department of Biochemistry, South Parks Road, The University of Oxford, Oxford OX1 3QU, UK Neuroscience Program, Garvan Institute of Medical Research, Darlinghurst, Sydney, NSW 2010, Australia Howard Hughes Medical Institute, Department of Molecular and Human Genetics, Department of Neuroscience, Program in Developmental Biology, Neurological Research Institute at Baylor College of Medicine, Houston, TX 77030, USA Department of Biochemistry, South Parks Road, The University of Oxford, Oxford OX1 3QU, UK Synaptic plasticity involves the modulation of synaptic connections in response to neuronal activity via multiple pathways. One mechanism modulates synaptic transmission by retrograde signals from the post-synapse that influence the probability of vesicle release in the pre-synapse. Despite its importance, very few factors required for the expression of retrograde signals, and proper synaptic transmission, have been identified. Here, we identify the conserved RNA binding protein Syncrip as a new factor that modulates the efficiency of vesicle release from the motoneuron and is required for correct synapse structure. We show that syncrip is required genetically and its protein product is detected only in the muscle and not in the motoneuron itself. This unexpected non-autonomy is at least partly explained by the fact that Syncrip modulates retrograde BMP signals from the muscle back to the motoneuron. We show that Syncrip influences the levels of the Bone Morphogenic Protein ligand Glass Bottom Boat from the post-synapse and regulates the pre-synapse. Our results highlight the RNA-binding protein Syncrip as a novel regulator of synaptic output. Given its known role in regulating translation, we propose that Syncrip is important for maintaining a balance between the strength of presynaptic vesicle release and postsynaptic translation.http://bio.biologists.org/content/3/9/839SyncripDrosophilaLocalized translationSynaptic transmissionmRNA localization neuromuscular junction
spellingShingle James M. Halstead
Yong Qi Lin
Lita Durraine
Russell S. Hamilton
Graeme Ball
Greg G. Neely
Hugo J. Bellen
Ilan Davis
Syncrip/hnRNP Q influences synaptic transmission and regulates BMP signaling at the Drosophila neuromuscular synapse
Biology Open
Syncrip
Drosophila
Localized translation
Synaptic transmission
mRNA localization neuromuscular junction
title Syncrip/hnRNP Q influences synaptic transmission and regulates BMP signaling at the Drosophila neuromuscular synapse
title_full Syncrip/hnRNP Q influences synaptic transmission and regulates BMP signaling at the Drosophila neuromuscular synapse
title_fullStr Syncrip/hnRNP Q influences synaptic transmission and regulates BMP signaling at the Drosophila neuromuscular synapse
title_full_unstemmed Syncrip/hnRNP Q influences synaptic transmission and regulates BMP signaling at the Drosophila neuromuscular synapse
title_short Syncrip/hnRNP Q influences synaptic transmission and regulates BMP signaling at the Drosophila neuromuscular synapse
title_sort syncrip hnrnp q influences synaptic transmission and regulates bmp signaling at the drosophila neuromuscular synapse
topic Syncrip
Drosophila
Localized translation
Synaptic transmission
mRNA localization neuromuscular junction
url http://bio.biologists.org/content/3/9/839
work_keys_str_mv AT jamesmhalstead syncriphnrnpqinfluencessynaptictransmissionandregulatesbmpsignalingatthedrosophilaneuromuscularsynapse
AT yongqilin syncriphnrnpqinfluencessynaptictransmissionandregulatesbmpsignalingatthedrosophilaneuromuscularsynapse
AT litadurraine syncriphnrnpqinfluencessynaptictransmissionandregulatesbmpsignalingatthedrosophilaneuromuscularsynapse
AT russellshamilton syncriphnrnpqinfluencessynaptictransmissionandregulatesbmpsignalingatthedrosophilaneuromuscularsynapse
AT graemeball syncriphnrnpqinfluencessynaptictransmissionandregulatesbmpsignalingatthedrosophilaneuromuscularsynapse
AT greggneely syncriphnrnpqinfluencessynaptictransmissionandregulatesbmpsignalingatthedrosophilaneuromuscularsynapse
AT hugojbellen syncriphnrnpqinfluencessynaptictransmissionandregulatesbmpsignalingatthedrosophilaneuromuscularsynapse
AT ilandavis syncriphnrnpqinfluencessynaptictransmissionandregulatesbmpsignalingatthedrosophilaneuromuscularsynapse