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Drosophila carboxypeptidase D (SILVER) is a key enzyme in neuropeptide processing required to maintain locomotor activity levels and survival rate

View ORCID ProfileDennis Pauls, View ORCID ProfileYasin Hamarat, Luisa Trufasu, Tim M. Schendzielorz, Gertrud Gramlich, Jörg Kahnt, View ORCID ProfileJens T. Vanselow, Andreas Schlosser, View ORCID ProfileChristian Wegener
doi: https://doi.org/10.1101/551853
Dennis Pauls
1Neurobiology and Genetics, Theodor-Boveri-Institute, Biocenter, University of Würzburg, Am Hubland, D-97074 Würzburg, Germany
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Yasin Hamarat
1Neurobiology and Genetics, Theodor-Boveri-Institute, Biocenter, University of Würzburg, Am Hubland, D-97074 Würzburg, Germany
2Kaunas University of Technology, “Santaka” Valley I Health Telematics Science Institute Baršauskas str. 59, LT-51423, Kaunas, Lithuania
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Luisa Trufasu
1Neurobiology and Genetics, Theodor-Boveri-Institute, Biocenter, University of Würzburg, Am Hubland, D-97074 Würzburg, Germany
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Tim M. Schendzielorz
1Neurobiology and Genetics, Theodor-Boveri-Institute, Biocenter, University of Würzburg, Am Hubland, D-97074 Würzburg, Germany
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Gertrud Gramlich
1Neurobiology and Genetics, Theodor-Boveri-Institute, Biocenter, University of Würzburg, Am Hubland, D-97074 Würzburg, Germany
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Jörg Kahnt
3Max-Planck-Institute of Terrestrial Microbiology, Karl-von-Frisch-Str. 10, D-35043 Marburg, Germany
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Jens T. Vanselow
4Rudolf Virchow Center for Experimental Biomedicine, University of Würzburg, D-97080 Würzburg, Germany
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Andreas Schlosser
4Rudolf Virchow Center for Experimental Biomedicine, University of Würzburg, D-97080 Würzburg, Germany
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Christian Wegener
1Neurobiology and Genetics, Theodor-Boveri-Institute, Biocenter, University of Würzburg, Am Hubland, D-97074 Würzburg, Germany
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  • ORCID record for Christian Wegener
  • For correspondence: christian.wegener@biozentrum.uni-wuerzburg.de
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Abstract

Neuropeptides are processed from larger preproproteins by a dedicated set of enzymes. The molecular and biochemical mechanisms underlying preproprotein processing and the functional importance of processing enzymes are well characterised in mammals, but little studied outside this group. In contrast to mammals, Drosophila lacks a gene for carboxypeptidase E (CPE), a key enzyme for mammalian peptide processing.

By combining peptidomics and neurogenetics, we addressed the role of Drosophila carboxypeptidase D (dCPD) in global neuropeptide processing and selected peptide-regulated behaviours. We found that a deficiency in dCPD results in C-terminally extended peptides across the peptidome, suggesting that dCPD took over CPE function in the fruit fly. dCPD is widely expressed throughout the nervous system, including peptidergic neurons in the mushroom body and neuroendocrine cells expressing adipokinetic hormone. Conditional hypomorphic mutation in the dCPD-encoding gene silver in the larva causes lethality, and leads to deficits in adult starvation-induced hyperactivity and appetitive gustatory preference, as well as to reduced survival rate and activity levels. A phylogenomic analysis suggests that loss of CPE is not a common insect feature, but specifically occured in Hymenoptera and Diptera. Our results show that dCPD is a key enzyme for neuropeptide processing in Drosophila, and is required for proper peptide-regulated behaviour. dCPD thus appears as a suitable target to genetically shut down total neuropeptide production in peptidergic neurons. Our results raise the question why Drosophila and other Diptera and Hymenoptera –unlike other insects-have obviously lost the gene for CPE but kept a gene encoding CPD.

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Posted February 15, 2019.
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Drosophila carboxypeptidase D (SILVER) is a key enzyme in neuropeptide processing required to maintain locomotor activity levels and survival rate
Dennis Pauls, Yasin Hamarat, Luisa Trufasu, Tim M. Schendzielorz, Gertrud Gramlich, Jörg Kahnt, Jens T. Vanselow, Andreas Schlosser, Christian Wegener
bioRxiv 551853; doi: https://doi.org/10.1101/551853
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Drosophila carboxypeptidase D (SILVER) is a key enzyme in neuropeptide processing required to maintain locomotor activity levels and survival rate
Dennis Pauls, Yasin Hamarat, Luisa Trufasu, Tim M. Schendzielorz, Gertrud Gramlich, Jörg Kahnt, Jens T. Vanselow, Andreas Schlosser, Christian Wegener
bioRxiv 551853; doi: https://doi.org/10.1101/551853

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