Torso-like is a component of the hemolymph and regulates the insulin signaling pathway in Drosophila

Michelle A. Henstridge, Lucinda Aulsebrook, Takashi Koyama, Travis K. Johnson, James C. Whisstock, Tony Tiganis, Christen K. Mirth, Coral G. Warr

Research output: Contribution to journalArticleResearchpeer-review

Abstract

In Drosophila, key developmental transitions are governed by the steroid hormone ecdysone. A number of neuropeptide-activated signaling pathways control ecdysone production in response to environmental signals, including the insulin signaling pathway, which regulates ecdysone production in response to nutrition. Here, we find that the Membrane Attack Complex/Perforin-like protein Torso-like, best characterized for its role in activating the Torso receptor tyrosine kinase in early embryo patterning, also regulates the insulin signaling pathway in Drosophila. We previously reported that the small body size and developmental delay phenotypes of torso-like null mutants resemble those observed when insulin signaling is reduced. Here we report that, in addition to growth defects, torso-like mutants also display metabolic and nutritional plasticity phenotypes characteristic of mutants with impaired insulin signaling. We further find that in the absence of torso-like, the expression of insulin-like peptides is increased, as is their accumulation in insulin-producing cells. Finally, we show that Torso-like is a component of the hemolymph and that it is required in the prothoracic gland to control developmental timing and body size. Taken together, our data suggest that the secretion of Torso-like from the prothoracic gland influences the activity of insulin signaling throughout the body in Drosophila.

Original languageEnglish
Pages (from-to)1523-1533
Number of pages11
JournalGenetics
Volume208
Issue number4
DOIs
Publication statusPublished - 1 Apr 2018

Keywords

  • Body size
  • Developmental timing
  • Drosophila melanogaster
  • Insulin signaling
  • Torso-like

Cite this

@article{60d39d8692064cdb93a2d8614da6f201,
title = "Torso-like is a component of the hemolymph and regulates the insulin signaling pathway in Drosophila",
abstract = "In Drosophila, key developmental transitions are governed by the steroid hormone ecdysone. A number of neuropeptide-activated signaling pathways control ecdysone production in response to environmental signals, including the insulin signaling pathway, which regulates ecdysone production in response to nutrition. Here, we find that the Membrane Attack Complex/Perforin-like protein Torso-like, best characterized for its role in activating the Torso receptor tyrosine kinase in early embryo patterning, also regulates the insulin signaling pathway in Drosophila. We previously reported that the small body size and developmental delay phenotypes of torso-like null mutants resemble those observed when insulin signaling is reduced. Here we report that, in addition to growth defects, torso-like mutants also display metabolic and nutritional plasticity phenotypes characteristic of mutants with impaired insulin signaling. We further find that in the absence of torso-like, the expression of insulin-like peptides is increased, as is their accumulation in insulin-producing cells. Finally, we show that Torso-like is a component of the hemolymph and that it is required in the prothoracic gland to control developmental timing and body size. Taken together, our data suggest that the secretion of Torso-like from the prothoracic gland influences the activity of insulin signaling throughout the body in Drosophila.",
keywords = "Body size, Developmental timing, Drosophila melanogaster, Insulin signaling, Torso-like",
author = "Henstridge, {Michelle A.} and Lucinda Aulsebrook and Takashi Koyama and Johnson, {Travis K.} and Whisstock, {James C.} and Tony Tiganis and Mirth, {Christen K.} and Warr, {Coral G.}",
year = "2018",
month = "4",
day = "1",
doi = "10.1534/genetics.117.300601",
language = "English",
volume = "208",
pages = "1523--1533",
journal = "Genetics",
issn = "1943-2631",
publisher = "Genetics Society of America",
number = "4",

}

Torso-like is a component of the hemolymph and regulates the insulin signaling pathway in Drosophila. / Henstridge, Michelle A.; Aulsebrook, Lucinda; Koyama, Takashi; Johnson, Travis K.; Whisstock, James C.; Tiganis, Tony; Mirth, Christen K.; Warr, Coral G.

In: Genetics, Vol. 208, No. 4, 01.04.2018, p. 1523-1533.

Research output: Contribution to journalArticleResearchpeer-review

TY - JOUR

T1 - Torso-like is a component of the hemolymph and regulates the insulin signaling pathway in Drosophila

AU - Henstridge, Michelle A.

AU - Aulsebrook, Lucinda

AU - Koyama, Takashi

AU - Johnson, Travis K.

AU - Whisstock, James C.

AU - Tiganis, Tony

AU - Mirth, Christen K.

AU - Warr, Coral G.

PY - 2018/4/1

Y1 - 2018/4/1

N2 - In Drosophila, key developmental transitions are governed by the steroid hormone ecdysone. A number of neuropeptide-activated signaling pathways control ecdysone production in response to environmental signals, including the insulin signaling pathway, which regulates ecdysone production in response to nutrition. Here, we find that the Membrane Attack Complex/Perforin-like protein Torso-like, best characterized for its role in activating the Torso receptor tyrosine kinase in early embryo patterning, also regulates the insulin signaling pathway in Drosophila. We previously reported that the small body size and developmental delay phenotypes of torso-like null mutants resemble those observed when insulin signaling is reduced. Here we report that, in addition to growth defects, torso-like mutants also display metabolic and nutritional plasticity phenotypes characteristic of mutants with impaired insulin signaling. We further find that in the absence of torso-like, the expression of insulin-like peptides is increased, as is their accumulation in insulin-producing cells. Finally, we show that Torso-like is a component of the hemolymph and that it is required in the prothoracic gland to control developmental timing and body size. Taken together, our data suggest that the secretion of Torso-like from the prothoracic gland influences the activity of insulin signaling throughout the body in Drosophila.

AB - In Drosophila, key developmental transitions are governed by the steroid hormone ecdysone. A number of neuropeptide-activated signaling pathways control ecdysone production in response to environmental signals, including the insulin signaling pathway, which regulates ecdysone production in response to nutrition. Here, we find that the Membrane Attack Complex/Perforin-like protein Torso-like, best characterized for its role in activating the Torso receptor tyrosine kinase in early embryo patterning, also regulates the insulin signaling pathway in Drosophila. We previously reported that the small body size and developmental delay phenotypes of torso-like null mutants resemble those observed when insulin signaling is reduced. Here we report that, in addition to growth defects, torso-like mutants also display metabolic and nutritional plasticity phenotypes characteristic of mutants with impaired insulin signaling. We further find that in the absence of torso-like, the expression of insulin-like peptides is increased, as is their accumulation in insulin-producing cells. Finally, we show that Torso-like is a component of the hemolymph and that it is required in the prothoracic gland to control developmental timing and body size. Taken together, our data suggest that the secretion of Torso-like from the prothoracic gland influences the activity of insulin signaling throughout the body in Drosophila.

KW - Body size

KW - Developmental timing

KW - Drosophila melanogaster

KW - Insulin signaling

KW - Torso-like

UR - http://www.scopus.com/inward/record.url?scp=85044996284&partnerID=8YFLogxK

U2 - 10.1534/genetics.117.300601

DO - 10.1534/genetics.117.300601

M3 - Article

VL - 208

SP - 1523

EP - 1533

JO - Genetics

JF - Genetics

SN - 1943-2631

IS - 4

ER -