Temporal groups of lineage-related neurons have different neuropeptidergic fates and related functions in the Drosophila melanogaster CNS

Abstract

The central nervous system (CNS) of Drosophila is comprised of the brain and the ventral nerve cord (VNC), which are the homologous structures of the vertebrate brain and the spinal cord, respectively. Neurons of the CNS arise from neural stem cells called neuroblasts (NBs). Each neuroblast gives rise to a specific repertory of cell types whose fate is unknown in most lineages. A combination of spatial and temporal genetic cues defines the fate of each neuron. We studied the origin and specification of a group of peptidergic neurons present in several abdominal segments of the larval VNC that are characterized by the expression of the neuropeptide GPB5, the GPB5-expressing neurons (GPB5-ENs). Our data reveal that the progenitor NB that generates the GPB5-ENs also generates the abdominal leucokinergic neurons (ABLKs) in two different temporal windows. We also show that these two set of neurons share the same axonal projections in larvae and in adults and, as previously suggested, may both function in hydrosaline regulation. Our genetic analysis of potential specification determinants reveals that Klumpfuss (klu) and huckebein (hkb) are involved in the specification of the GPB5 cell fate. Additionally, we show that GPB5-ENs have a role in starvation resistance and longevity; however, their role in desiccation and ionic stress resistance is not as clear. We hypothesize that the neurons arising from the same neuroblast lineage are both architecturally similar and functionally related.

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Acknowledgements

We are grateful to JA Veenstra for providing the GPB5-Gal4 and UAS-GPB5RNAi flies and Beatriz Fraile for her technical help in the laboratory. We thank the Bloomington Stock Center for providing fly stocks and the Confocal Microscopy Service of the CBM-SO for technical imaging assistance. We appreciate Melinda Modrell’s assistance with the English language.

Funding

This work was supported by a Spanish Ministerio de Ciencia e Innovación (grant number BFU2014-53761 (to F.J.D-B.)) and by institutional grants from the Fundación Ramón Areces and Banco de Santander to the CBM-SO.

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All authors had full access to all of the data in the study and take responsibility for the accuracy of the data analysis. Study concept and design: FJDB and PH. Acquisition of data: LDP, LMP and PH. Analysis and interpretation of data: LDP, LMP, FJDB and PH. Drafting of manuscript: PH. Obtained funding: FJDB. Study supervision: FJDB and PH.

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Correspondence to Pilar Herrero.

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This article does not contain any studies with human participants performed by any of the authors.

All procedures performed in this study involving animals were in accordance with the ethical standards of the institution at which the studies were conducted (Consejo Superior de Investigaciones Cientificas/Spanish National Research Council). The only animal used by the authors is insects (Drosophila melanogaster). The use of insects as an experimental system does not require ethical approval.

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Díaz-de-la-Peña, L., Maestro-Paramio, L., Díaz-Benjumea, F.J. et al. Temporal groups of lineage-related neurons have different neuropeptidergic fates and related functions in the Drosophila melanogaster CNS. Cell Tissue Res 381, 381–396 (2020). https://doi.org/10.1007/s00441-020-03231-8

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Keywords

  • GPB5 glycopeptidergic neurons
  • Drosophila
  • Neuroblast lineage origin
  • Longevity
  • Starvation resistance effects