Massive excretion of calcium oxalate from late prepupal salivary glands of Drosophila melanogaster demonstrates active nephridial-like anion transport

Robert Farkaš, Ludmila Pečeňová, Lucia Mentelová, Milan Beňo, Denisa Beňová-Liszeková, Silvia Mahmoodová, Václav Tejnecký, Otakar Raška, Pavel Juda, Silvie Svidenská, Matúš Hornáček, Bruce A Chase, Ivan Raška

Research output: Contribution to journalArticle

3 Citations (Scopus)

Abstract

The Drosophila salivary glands (SGs) were well known for the puffing patterns of their polytene chromosomes and so became a tissue of choice to study sequential gene activation by the steroid hormone ecdysone. One well-documented function of these glands is to produce a secretory glue, which is released during pupariation to fix the freshly formed puparia to the substrate. Over the past two decades SGs have been used to address specific aspects of developmentally-regulated programmed cell death (PCD) as it was thought that they are doomed for histolysis and after pupariation are just awaiting their fate. More recently, however, we have shown that for the first 3–4 h after pupariation SGs undergo tremendous endocytosis and vacuolation followed by vacuole neutralization and membrane consolidation. Furthermore, from 8 to 10 h after puparium formation (APF) SGs display massive apocrine secretion of a diverse set of cellular proteins. Here, we show that during the period from 11 to 12 h APF, the prepupal glands are very active in calcium oxalate (CaOx) extrusion that resembles renal or nephridial excretory activity. We provide genetic evidence that Prestin, a Drosophila homologue of the mammalian electrogenic anion exchange carrier SLC26A5, is responsible for the instantaneous production of CaOx by the late prepupal SGs. Its positive regulation by the protein kinases encoded by fray and wnk lead to increased production of CaOx. The formation of CaOx appears to be dependent on the cooperation between Prestin and the vATPase complex as treatment with bafilomycin A1 or concanamycin A abolishes the production of detectable CaOx. These data demonstrate that prepupal SGs remain fully viable, physiologically active and engaged in various cellular activities at least until early pupal period, that is, until moments prior to the execution of PCD.

Original languageEnglish (US)
Pages (from-to)562-574
Number of pages13
JournalDevelopment Growth and Differentiation
Volume58
Issue number6
DOIs
StatePublished - Aug 1 2016

Fingerprint

Calcium Oxalate
Salivary Glands
Drosophila melanogaster
Anions
Drosophila
Cell Death
Polytene Chromosomes
Ecdysone
Endocytosis
Vacuoles
Adhesives
Protein Kinases
Transcriptional Activation
Steroids
Hormones
Kidney
Membranes
Proteins

Keywords

  • Drosophila
  • anion extrusion
  • calcium oxalate
  • fruitfly salivary glands
  • labial nephridia
  • prestin

ASJC Scopus subject areas

  • Developmental Biology
  • Cell Biology

Cite this

Massive excretion of calcium oxalate from late prepupal salivary glands of Drosophila melanogaster demonstrates active nephridial-like anion transport. / Farkaš, Robert; Pečeňová, Ludmila; Mentelová, Lucia; Beňo, Milan; Beňová-Liszeková, Denisa; Mahmoodová, Silvia; Tejnecký, Václav; Raška, Otakar; Juda, Pavel; Svidenská, Silvie; Hornáček, Matúš; Chase, Bruce A; Raška, Ivan.

In: Development Growth and Differentiation, Vol. 58, No. 6, 01.08.2016, p. 562-574.

Research output: Contribution to journalArticle

Farkaš, R, Pečeňová, L, Mentelová, L, Beňo, M, Beňová-Liszeková, D, Mahmoodová, S, Tejnecký, V, Raška, O, Juda, P, Svidenská, S, Hornáček, M, Chase, BA & Raška, I 2016, 'Massive excretion of calcium oxalate from late prepupal salivary glands of Drosophila melanogaster demonstrates active nephridial-like anion transport', Development Growth and Differentiation, vol. 58, no. 6, pp. 562-574. https://doi.org/10.1111/dgd.12300
Farkaš, Robert ; Pečeňová, Ludmila ; Mentelová, Lucia ; Beňo, Milan ; Beňová-Liszeková, Denisa ; Mahmoodová, Silvia ; Tejnecký, Václav ; Raška, Otakar ; Juda, Pavel ; Svidenská, Silvie ; Hornáček, Matúš ; Chase, Bruce A ; Raška, Ivan. / Massive excretion of calcium oxalate from late prepupal salivary glands of Drosophila melanogaster demonstrates active nephridial-like anion transport. In: Development Growth and Differentiation. 2016 ; Vol. 58, No. 6. pp. 562-574.
@article{16fd826d4992450bb515413dfa007482,
title = "Massive excretion of calcium oxalate from late prepupal salivary glands of Drosophila melanogaster demonstrates active nephridial-like anion transport",
abstract = "The Drosophila salivary glands (SGs) were well known for the puffing patterns of their polytene chromosomes and so became a tissue of choice to study sequential gene activation by the steroid hormone ecdysone. One well-documented function of these glands is to produce a secretory glue, which is released during pupariation to fix the freshly formed puparia to the substrate. Over the past two decades SGs have been used to address specific aspects of developmentally-regulated programmed cell death (PCD) as it was thought that they are doomed for histolysis and after pupariation are just awaiting their fate. More recently, however, we have shown that for the first 3–4 h after pupariation SGs undergo tremendous endocytosis and vacuolation followed by vacuole neutralization and membrane consolidation. Furthermore, from 8 to 10 h after puparium formation (APF) SGs display massive apocrine secretion of a diverse set of cellular proteins. Here, we show that during the period from 11 to 12 h APF, the prepupal glands are very active in calcium oxalate (CaOx) extrusion that resembles renal or nephridial excretory activity. We provide genetic evidence that Prestin, a Drosophila homologue of the mammalian electrogenic anion exchange carrier SLC26A5, is responsible for the instantaneous production of CaOx by the late prepupal SGs. Its positive regulation by the protein kinases encoded by fray and wnk lead to increased production of CaOx. The formation of CaOx appears to be dependent on the cooperation between Prestin and the vATPase complex as treatment with bafilomycin A1 or concanamycin A abolishes the production of detectable CaOx. These data demonstrate that prepupal SGs remain fully viable, physiologically active and engaged in various cellular activities at least until early pupal period, that is, until moments prior to the execution of PCD.",
keywords = "Drosophila, anion extrusion, calcium oxalate, fruitfly salivary glands, labial nephridia, prestin",
author = "Robert Farkaš and Ludmila Pečeňov{\'a} and Lucia Mentelov{\'a} and Milan Beňo and Denisa Beňov{\'a}-Liszekov{\'a} and Silvia Mahmoodov{\'a} and V{\'a}clav Tejneck{\'y} and Otakar Raška and Pavel Juda and Silvie Svidensk{\'a} and Mat{\'u}š Horn{\'a}ček and Chase, {Bruce A} and Ivan Raška",
year = "2016",
month = "8",
day = "1",
doi = "10.1111/dgd.12300",
language = "English (US)",
volume = "58",
pages = "562--574",
journal = "Development Growth and Differentiation",
issn = "0012-1592",
publisher = "Wiley-Blackwell",
number = "6",

}

TY - JOUR

T1 - Massive excretion of calcium oxalate from late prepupal salivary glands of Drosophila melanogaster demonstrates active nephridial-like anion transport

AU - Farkaš, Robert

AU - Pečeňová, Ludmila

AU - Mentelová, Lucia

AU - Beňo, Milan

AU - Beňová-Liszeková, Denisa

AU - Mahmoodová, Silvia

AU - Tejnecký, Václav

AU - Raška, Otakar

AU - Juda, Pavel

AU - Svidenská, Silvie

AU - Hornáček, Matúš

AU - Chase, Bruce A

AU - Raška, Ivan

PY - 2016/8/1

Y1 - 2016/8/1

N2 - The Drosophila salivary glands (SGs) were well known for the puffing patterns of their polytene chromosomes and so became a tissue of choice to study sequential gene activation by the steroid hormone ecdysone. One well-documented function of these glands is to produce a secretory glue, which is released during pupariation to fix the freshly formed puparia to the substrate. Over the past two decades SGs have been used to address specific aspects of developmentally-regulated programmed cell death (PCD) as it was thought that they are doomed for histolysis and after pupariation are just awaiting their fate. More recently, however, we have shown that for the first 3–4 h after pupariation SGs undergo tremendous endocytosis and vacuolation followed by vacuole neutralization and membrane consolidation. Furthermore, from 8 to 10 h after puparium formation (APF) SGs display massive apocrine secretion of a diverse set of cellular proteins. Here, we show that during the period from 11 to 12 h APF, the prepupal glands are very active in calcium oxalate (CaOx) extrusion that resembles renal or nephridial excretory activity. We provide genetic evidence that Prestin, a Drosophila homologue of the mammalian electrogenic anion exchange carrier SLC26A5, is responsible for the instantaneous production of CaOx by the late prepupal SGs. Its positive regulation by the protein kinases encoded by fray and wnk lead to increased production of CaOx. The formation of CaOx appears to be dependent on the cooperation between Prestin and the vATPase complex as treatment with bafilomycin A1 or concanamycin A abolishes the production of detectable CaOx. These data demonstrate that prepupal SGs remain fully viable, physiologically active and engaged in various cellular activities at least until early pupal period, that is, until moments prior to the execution of PCD.

AB - The Drosophila salivary glands (SGs) were well known for the puffing patterns of their polytene chromosomes and so became a tissue of choice to study sequential gene activation by the steroid hormone ecdysone. One well-documented function of these glands is to produce a secretory glue, which is released during pupariation to fix the freshly formed puparia to the substrate. Over the past two decades SGs have been used to address specific aspects of developmentally-regulated programmed cell death (PCD) as it was thought that they are doomed for histolysis and after pupariation are just awaiting their fate. More recently, however, we have shown that for the first 3–4 h after pupariation SGs undergo tremendous endocytosis and vacuolation followed by vacuole neutralization and membrane consolidation. Furthermore, from 8 to 10 h after puparium formation (APF) SGs display massive apocrine secretion of a diverse set of cellular proteins. Here, we show that during the period from 11 to 12 h APF, the prepupal glands are very active in calcium oxalate (CaOx) extrusion that resembles renal or nephridial excretory activity. We provide genetic evidence that Prestin, a Drosophila homologue of the mammalian electrogenic anion exchange carrier SLC26A5, is responsible for the instantaneous production of CaOx by the late prepupal SGs. Its positive regulation by the protein kinases encoded by fray and wnk lead to increased production of CaOx. The formation of CaOx appears to be dependent on the cooperation between Prestin and the vATPase complex as treatment with bafilomycin A1 or concanamycin A abolishes the production of detectable CaOx. These data demonstrate that prepupal SGs remain fully viable, physiologically active and engaged in various cellular activities at least until early pupal period, that is, until moments prior to the execution of PCD.

KW - Drosophila

KW - anion extrusion

KW - calcium oxalate

KW - fruitfly salivary glands

KW - labial nephridia

KW - prestin

UR - http://www.scopus.com/inward/record.url?scp=84978136449&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84978136449&partnerID=8YFLogxK

U2 - 10.1111/dgd.12300

DO - 10.1111/dgd.12300

M3 - Article

VL - 58

SP - 562

EP - 574

JO - Development Growth and Differentiation

JF - Development Growth and Differentiation

SN - 0012-1592

IS - 6

ER -