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Redundant functions of the SLC5A transporters Rumpel, Bumpel, and Kumpel in ensheathing glial cells

Neuronal processing is energy demanding and relies on sugar metabolism. To nurture the Drosophila nervous system, the blood-brain barrier forming glial cells take up trehalose from the hemolymph and then distribute the metabolic products further to all neurons. This function is provided by glucose a...

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Autores principales: Yildirim, Kerem, Winkler, Bente, Pogodalla, Nicole, Mackensen, Steffi, Baldenius, Marie, Garcia, Luis, Naffin, Elke, Rodrigues, Silke, Klämbt, Christian
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Company of Biologists Ltd 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8790523/
https://www.ncbi.nlm.nih.gov/pubmed/34897385
http://dx.doi.org/10.1242/bio.059128
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author Yildirim, Kerem
Winkler, Bente
Pogodalla, Nicole
Mackensen, Steffi
Baldenius, Marie
Garcia, Luis
Naffin, Elke
Rodrigues, Silke
Klämbt, Christian
author_facet Yildirim, Kerem
Winkler, Bente
Pogodalla, Nicole
Mackensen, Steffi
Baldenius, Marie
Garcia, Luis
Naffin, Elke
Rodrigues, Silke
Klämbt, Christian
author_sort Yildirim, Kerem
collection PubMed
description Neuronal processing is energy demanding and relies on sugar metabolism. To nurture the Drosophila nervous system, the blood-brain barrier forming glial cells take up trehalose from the hemolymph and then distribute the metabolic products further to all neurons. This function is provided by glucose and lactate transporters of the solute carrier (SLC) 5A family. Here we identified three SLC5A genes that are specifically expressed in overlapping sets of CNS glial cells, rumpel, bumpel and kumpel. We generated mutants in all genes and all mutants are viable and fertile, lacking discernible phenotypes. Loss of rumpel causes subtle locomotor phenotypes and flies display increased daytime sleep. In addition, in bumpel kumpel double mutants, and to an even greater extent in rumpel bumpel kumpel triple mutants, oogenesis is disrupted at the onset of the vitollegenic phase. This indicates a partially redundant function between these genes. Rescue experiments exploring this effect indicate that oogenesis can be affected by CNS glial cells. Moreover, expression of heterologous mammalian SLC5A transporters, with known transport properties, suggest that Bumpel and/or Kumpel transport glucose or lactate. Overall, our results imply a redundancy in SLC5A nutrient sensing functions in Drosophila glial cells, affecting ovarian development and behavior.
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spelling pubmed-87905232022-01-26 Redundant functions of the SLC5A transporters Rumpel, Bumpel, and Kumpel in ensheathing glial cells Yildirim, Kerem Winkler, Bente Pogodalla, Nicole Mackensen, Steffi Baldenius, Marie Garcia, Luis Naffin, Elke Rodrigues, Silke Klämbt, Christian Biol Open Research Article Neuronal processing is energy demanding and relies on sugar metabolism. To nurture the Drosophila nervous system, the blood-brain barrier forming glial cells take up trehalose from the hemolymph and then distribute the metabolic products further to all neurons. This function is provided by glucose and lactate transporters of the solute carrier (SLC) 5A family. Here we identified three SLC5A genes that are specifically expressed in overlapping sets of CNS glial cells, rumpel, bumpel and kumpel. We generated mutants in all genes and all mutants are viable and fertile, lacking discernible phenotypes. Loss of rumpel causes subtle locomotor phenotypes and flies display increased daytime sleep. In addition, in bumpel kumpel double mutants, and to an even greater extent in rumpel bumpel kumpel triple mutants, oogenesis is disrupted at the onset of the vitollegenic phase. This indicates a partially redundant function between these genes. Rescue experiments exploring this effect indicate that oogenesis can be affected by CNS glial cells. Moreover, expression of heterologous mammalian SLC5A transporters, with known transport properties, suggest that Bumpel and/or Kumpel transport glucose or lactate. Overall, our results imply a redundancy in SLC5A nutrient sensing functions in Drosophila glial cells, affecting ovarian development and behavior. The Company of Biologists Ltd 2022-01-18 /pmc/articles/PMC8790523/ /pubmed/34897385 http://dx.doi.org/10.1242/bio.059128 Text en © 2022. Published by The Company of Biologists Ltd https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
spellingShingle Research Article
Yildirim, Kerem
Winkler, Bente
Pogodalla, Nicole
Mackensen, Steffi
Baldenius, Marie
Garcia, Luis
Naffin, Elke
Rodrigues, Silke
Klämbt, Christian
Redundant functions of the SLC5A transporters Rumpel, Bumpel, and Kumpel in ensheathing glial cells
title Redundant functions of the SLC5A transporters Rumpel, Bumpel, and Kumpel in ensheathing glial cells
title_full Redundant functions of the SLC5A transporters Rumpel, Bumpel, and Kumpel in ensheathing glial cells
title_fullStr Redundant functions of the SLC5A transporters Rumpel, Bumpel, and Kumpel in ensheathing glial cells
title_full_unstemmed Redundant functions of the SLC5A transporters Rumpel, Bumpel, and Kumpel in ensheathing glial cells
title_short Redundant functions of the SLC5A transporters Rumpel, Bumpel, and Kumpel in ensheathing glial cells
title_sort redundant functions of the slc5a transporters rumpel, bumpel, and kumpel in ensheathing glial cells
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8790523/
https://www.ncbi.nlm.nih.gov/pubmed/34897385
http://dx.doi.org/10.1242/bio.059128
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