Sobremesa L-type Amino Acid Transporter Expressed in Glia Is Essential for Proper Timing of Development and Brain Growth

Overview

Journal Cell Rep

Publisher Cell Press

Specialties Biology
Cell Biology
Molecular Biology

Date 2018 Sep 21

PMID 30231999

Citations 13

Authors

Diego Galagovsky

Ana Depetris-Chauvin

Gerard Maniere

Flore Geillon

Martine Berthelot-Grosjean

Elodie Noirot

Georges Alves

Yael Grosjean

Affiliations

Soon will be listed here.

Abstract

In Drosophila, ecdysone hormone levels determine the timing of larval development. Its production is regulated by the stereotypical rise in prothoracicotropic hormone (PTTH) levels. Additionally, ecdysone levels can also be modulated by nutrition (specifically by amino acids) through their action on Drosophila insulin-like peptides (Dilps). Moreover, in glia, amino-acid-sensitive production of Dilps regulates brain development. In this work, we describe the function of an SLC7 amino acid transporter, Sobremesa (Sbm). Larvae with reduced Sbm levels in glia remain in third instar for an additional 24 hr. These larvae show reduced brain growth with increased body size but do not show reduction in insulin signaling or production. Interestingly, Sbm downregulation in glia leads to reduced Ecdysone production and a surprising delay in the rise of PTTH levels. Our work highlights Sbm as a modulator of both brain development and the timing of larval development via an amino-acid-sensitive and Dilp-independent function of glia.

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References

Miguel-Aliaga I . Nerveless and gutsy: intestinal nutrient sensing from invertebrates to humans. Semin Cell Dev Biol. 2012; 23(6):614-20. PMC: 3712190. DOI: 10.1016/j.semcdb.2012.01.002. View

Featherstone D . Glial solute carrier transporters in Drosophila and mice. Glia. 2011; 59(9):1351-63. DOI: 10.1002/glia.21085. View

Cheng L, Bailey A, Leevers S, Ragan T, Driscoll P, Gould A . Anaplastic lymphoma kinase spares organ growth during nutrient restriction in Drosophila. Cell. 2011; 146(3):435-47. DOI: 10.1016/j.cell.2011.06.040. View

Colombani J, Bianchini L, Layalle S, Pondeville E, Dauphin-Villemant C, Antoniewski C . Antagonistic actions of ecdysone and insulins determine final size in Drosophila. Science. 2005; 310(5748):667-70. DOI: 10.1126/science.1119432. View

Yamanaka N, Romero N, Martin F, Rewitz K, Sun M, OConnor M . Neuroendocrine control of Drosophila larval light preference. Science. 2013; 341(6150):1113-6. PMC: 3906047. DOI: 10.1126/science.1241210. View

Piyankarage S, Augustin H, Grosjean Y, Featherstone D, Shippy S . Hemolymph amino acid analysis of individual Drosophila larvae. Anal Chem. 2008; 80(4):1201-7. PMC: 2267754. DOI: 10.1021/ac701785z. View

Sepp K, Schulte J, Auld V . Peripheral glia direct axon guidance across the CNS/PNS transition zone. Dev Biol. 2002; 238(1):47-63. DOI: 10.1006/dbio.2001.0411. View

Okamoto N, Nishimura T . Signaling from Glia and Cholinergic Neurons Controls Nutrient-Dependent Production of an Insulin-like Peptide for Drosophila Body Growth. Dev Cell. 2015; 35(3):295-310. DOI: 10.1016/j.devcel.2015.10.003. View

Shim J, Mukherjee T, Banerjee U . Direct sensing of systemic and nutritional signals by haematopoietic progenitors in Drosophila. Nat Cell Biol. 2012; 14(4):394-400. PMC: 4342111. DOI: 10.1038/ncb2453. View

10.

Bjordal M, Arquier N, Kniazeff J, Pin J, Leopold P . Sensing of amino acids in a dopaminergic circuitry promotes rejection of an incomplete diet in Drosophila. Cell. 2014; 156(3):510-21. DOI: 10.1016/j.cell.2013.12.024. View

11.

Yuasa Y, Okabe M, Yoshikawa S, Tabuchi K, Xiong W, Hiromi Y . Drosophila homeodomain protein REPO controls glial differentiation by cooperating with ETS and BTB transcription factors. Development. 2003; 130(11):2419-28. DOI: 10.1242/dev.00468. View

12.

Tennessen J, Barry W, Cox J, Thummel C . Methods for studying metabolism in Drosophila. Methods. 2014; 68(1):105-15. PMC: 4048761. DOI: 10.1016/j.ymeth.2014.02.034. View

13.

Verrey F, Closs E, Wagner C, Palacin M, Endou H, Kanai Y . CATs and HATs: the SLC7 family of amino acid transporters. Pflugers Arch. 2004; 447(5):532-42. DOI: 10.1007/s00424-003-1086-z. View

14.

Augustin H, Grosjean Y, Chen K, Sheng Q, Featherstone D . Nonvesicular release of glutamate by glial xCT transporters suppresses glutamate receptor clustering in vivo. J Neurosci. 2007; 27(1):111-23. PMC: 2193629. DOI: 10.1523/JNEUROSCI.4770-06.2007. View

15.

Rewitz K, Yamanaka N, Gilbert L, OConnor M . The insect neuropeptide PTTH activates receptor tyrosine kinase torso to initiate metamorphosis. Science. 2009; 326(5958):1403-5. DOI: 10.1126/science.1176450. View

16.

Rajan A, Perrimon N . Drosophila cytokine unpaired 2 regulates physiological homeostasis by remotely controlling insulin secretion. Cell. 2012; 151(1):123-37. PMC: 3475207. DOI: 10.1016/j.cell.2012.08.019. View

17.

Nijhout H, Riddiford L, Mirth C, Shingleton A, Suzuki Y, Callier V . The developmental control of size in insects. Wiley Interdiscip Rev Dev Biol. 2014; 3(1):113-34. PMC: 4048863. DOI: 10.1002/wdev.124. View

18.

Mirth C, Truman J, Riddiford L . The role of the prothoracic gland in determining critical weight for metamorphosis in Drosophila melanogaster. Curr Biol. 2005; 15(20):1796-807. DOI: 10.1016/j.cub.2005.09.017. View

19.

Varghese J, Cohen S . microRNA miR-14 acts to modulate a positive autoregulatory loop controlling steroid hormone signaling in Drosophila. Genes Dev. 2007; 21(18):2277-82. PMC: 1973141. DOI: 10.1101/gad.439807. View

20.

Ngo K, Andrade I, Hartenstein V . Spatio-temporal pattern of neuronal differentiation in the Drosophila visual system: A user's guide to the dynamic morphology of the developing optic lobe. Dev Biol. 2017; 428(1):1-24. PMC: 5825191. DOI: 10.1016/j.ydbio.2017.05.008. View