Growth regulation by amino acid transporters in Drosophila larvae.
Glia
Insulin producing cells
LAT1
Molecular signal
Neuron
Physiology
Journal
Cellular and molecular life sciences : CMLS
ISSN: 1420-9071
Titre abrégé: Cell Mol Life Sci
Pays: Switzerland
ID NLM: 9705402
Informations de publication
Date de publication:
Nov 2020
Nov 2020
Historique:
received:
23
09
2019
accepted:
20
04
2020
revised:
27
03
2020
pubmed:
3
5
2020
medline:
4
11
2020
entrez:
3
5
2020
Statut:
ppublish
Résumé
Drosophila larvae need to adapt their metabolism to reach a critical body size to pupate. This process needs food resources and has to be tightly adjusted to control metamorphosis timing and adult size. Nutrients such as amino acids either directly present in the food or obtained via protein digestion play key regulatory roles in controlling metabolism and growth. Amino acids act especially on two organs, the fat body and the brain, to control larval growth, body size developmental timing and pupariation. The expression of specific amino acid transporters in fat body cells, and in the brain through specific neurons and glial cells is essential to activate downstream molecular signaling pathways in response to amino acid levels. In this review, we highlight some of these specific networks dependent on amino acid diet to control DILP levels, and by consequence larval metabolism and growth.
Identifiants
pubmed: 32358623
doi: 10.1007/s00018-020-03535-6
pii: 10.1007/s00018-020-03535-6
pmc: PMC7588360
doi:
Substances chimiques
Amino Acid Transport Systems
0
Amino Acids
0
Drosophila Proteins
0
Hormones
0
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
4289-4297Subventions
Organisme : European Funding for Regional Economical Development
ID : FEDER
Organisme : Conseil régional de Bourgogne-Franche-Comté
ID : PARI
Organisme : European Research Council
ID : 311403
Pays : International
Références
Carvalho MJA, Mirth CK (2015) Coordinating morphology with behavior during development: an integrative approach from a fly perspective. Front Ecol Evol 3:5. https://doi.org/10.3389/fevo.2015.00005
doi: 10.3389/fevo.2015.00005
Mattila J, Hietakangas V (2017) Regulation of carbohydrate energy metabolism in Drosophila melanogaster. Genetics 207(4):1231–1253. https://doi.org/10.1534/genetics.117.199885
doi: 10.1534/genetics.117.199885
Heier C, Kühnlein RP (2018) Triacylglycerol metabolism in Drosophila melanogaster. Genetics 210(4):1163–1184. https://doi.org/10.1534/genetics.118.301583
doi: 10.1534/genetics.118.301583
Lemaitre B, Miguel-Aliaga I (2013) The digestive tract of Drosophila melanogaster. Annu Rev Genet 47:377–404. https://doi.org/10.1146/annurev-genet-111212-133343
doi: 10.1146/annurev-genet-111212-133343
Boudko DY (2012) Molecular basis of essential amino acid transport from studies of insect nutrient amino acid transporters of the SLC6 family (NAT-SLC6). J Insect Physiol 58(4):433–449. https://doi.org/10.1016/j.jinsphys.2011.12.018
doi: 10.1016/j.jinsphys.2011.12.018
Tennessen JM, Thummel CS (2011) Coordinating growth and maturation—insights from Drosophila. Curr Biol 21(18):R750–R757. https://doi.org/10.1016/j.cub.2011.06.033
doi: 10.1016/j.cub.2011.06.033
Nässel DR, Liu Y, Luo J (2015) Insulin/IGF signaling and its regulation in Drosophila. Gen Comp Endocrinol 221:255–266. https://doi.org/10.1016/j.ygcen.2014.11.021
doi: 10.1016/j.ygcen.2014.11.021
Delanoue R, Romero NM (2020) Growth and maturation in development: a fly's perspective. Int J Mol Sci 21(4):piiE1260. https://doi.org/10.3390/ijms21041260
doi: 10.3390/ijms21041260
Zeng J, Huynh N, Phelps B, King-Jones K (2020) Snail synchronizes endocycling in a TOR-dependent manner to coordinate entry and escape from endoreplication pausing during the Drosophila critical weight checkpoint. PLoS Biol 18(2):e3000609. https://doi.org/10.1371/journal.pbio.3000609
doi: 10.1371/journal.pbio.3000609
Holtof M, Lenaerts C, Cullen D, Vanden BJ (2019) Extracellular nutrient digestion and absorption in the insect gut. Cell Tissue Res 377(3):397–414. https://doi.org/10.1007/s00441-019-03031-9
doi: 10.1007/s00441-019-03031-9
Droujinine IA, Perrimon N (2016) Interorgan communication pathways in physiology: focus on Drosophila. Annu Rev Genet 23(50):539–570. https://doi.org/10.1146/annurev-genet-121415-122024
doi: 10.1146/annurev-genet-121415-122024
Nässel DR, Vanden Broeck J (2016) Insulin/IGF signaling in Drosophila and other insects: factors that regulate production, release and post-release action of the insulin-like peptides. Cell Mol Life Sci 73(2):271–290. https://doi.org/10.1007/s00018-015-2063-3
doi: 10.1007/s00018-015-2063-3
Chen C, Jack J, Garofalo RS (1996) The Drosophila insulin receptor is required for normal growth. Endocrinology 137:846–856. https://doi.org/10.1210/endo.137.3.8603594
doi: 10.1210/endo.137.3.8603594
Brogiolo W, Stocker H, Ikeya T, Rintelen F, Fernandez R, Hafen E (2001) An evolutionarily conserved function of the Drosophila insulin receptor and insulin-like peptides in growth control. Curr Biol 11:213–221. https://doi.org/10.1016/S0960-9822(01)00068-9
doi: 10.1016/S0960-9822(01)00068-9
Colombani J, Andersen DS, Léopold P (2012) Secreted peptide Dilp8 coordinates Drosophila tissue growth with developmental timing. Science 336:582–585. https://doi.org/10.1126/science.1216689
doi: 10.1126/science.1216689
Garelli A, Gontijo AM, Miguela V, Caparros E, Dominguez M (2012) Imaginal discs secrete insulin-like peptide 8 to mediate plasticity of growth and maturation. Science 336(6081):579–582. https://doi.org/10.1126/science.1216735
doi: 10.1126/science.1216735
Garelli A, Heredia F, Casimiro AP, Macedo A, Nunes C, Garcez M, Dias ARM, Volonte YA, Uhlmann T, Caparros E, Koyama T, Gontijo AM (2015) Dilp8 requires the neuronal relaxin receptor Lgr3 to couple growth to developmental timing. Nat Commun 29(6):8732. https://doi.org/10.1038/ncomms9732
doi: 10.1038/ncomms9732
Wang S, Tulina N, Carlin DL, Rulifson EJ (2007) The origin of islet-like cells in Drosophila identifies parallels to the vertebrate endocrine axis. Proc Natl Acad Sci USA 104:19873–19878. https://doi.org/10.1073/pnas.0707465104
doi: 10.1073/pnas.0707465104
Clements J, Hens K, Francis C, Schellens A, Callaerts (2008) Conserved role for the Drosophila Pax6 homolog eyeless in differentiation and function of insulin-producing neurons. Proc Natl Acad Sci USA 105:16183–16188. https://doi.org/10.1073/pnas.0708330105
doi: 10.1073/pnas.0708330105
Ikeya T, Galic M, Belawat P, Nairz K, Hafen E (2002) Nutrient-dependent expression of insulin-like peptides from neuroendocrine cells in the CNS contributes to growth regulation in Drosophila. Curr Biol 12:1293–1300. https://doi.org/10.1016/S0960-9822(02)01043-6
doi: 10.1016/S0960-9822(02)01043-6
Rulifson EJ, Kim SK, Nusse R (2002) Ablation of insulin-producing neurons in flies: growth and diabetic phenotypes. Science 296:1118–1120. https://doi.org/10.1126/science.1070058
doi: 10.1126/science.1070058
Okamoto N, Yamanaka N, Yagi Y, Nishida Y, Kataoka H, O'Connor MB, Mizoguchi A (2009) A fat body-derived IGF-like peptide regulates postfeeding growth in Drosophila. Dev Cell 17:885–891. https://doi.org/10.1016/j.devcel.2009.10.008
doi: 10.1016/j.devcel.2009.10.008
Slaidina M, Delanoue R, Gronke S, Partridge L, Léopold P (2009) A Drosophila insulin-like peptide promotes growth during nonfeeding states. Dev Cell 17:874–884. https://doi.org/10.1016/j.devcel.2009.10.009
doi: 10.1016/j.devcel.2009.10.009
Chell JM, Brand AH (2010) Nutrition-responsive glia control exit of neural stem cells from quiescence. Cell 143:1161–1173. https://doi.org/10.1016/j.cell.2010.12.007
doi: 10.1016/j.cell.2010.12.007
Sousa-Nunes R, Yee LL, Gould AP (2011) Fat cells reactivate quiescent neuroblasts via TOR and glial insulin relays in Drosophila. Nature 471:508–512. https://doi.org/10.1038/nature09867
doi: 10.1038/nature09867
Arrese EL, Soulages JL (2010) Insect fat body: energy, metabolism and regulation. Annu Rev Entomol 55:207–225. https://doi.org/10.1146/annurev-ento-112408-085356
doi: 10.1146/annurev-ento-112408-085356
Carvalho M, Sampaio JL, Palm W, Brankatschk M, Eaton S, Shevchenko A (2012) Effects of diet and development on the Drosophila lipidome. Mol Syst Biol 8:600. https://doi.org/10.1038/msb.2012.29
doi: 10.1038/msb.2012.29
Colombani J, Raisin S, Pantalacci S, Radimerski T, Montagne J, Léopold P (2003) A nutrient sensor mechanism controls Drosophila growth. Cell 114:739–749. https://doi.org/10.1016/S0092-8674(03)00713-X
doi: 10.1016/S0092-8674(03)00713-X
Augustin H, Grosjean Y, Chen K, Sheng Q, Featherstone DE (2007) Nonvesicular release of glutamate by glial xCT transporters suppresses glutamate receptor clustering in vivo. J Neurosci 27:111–123. https://doi.org/10.1523/JNEUROSCI.4770-06.2007
doi: 10.1523/JNEUROSCI.4770-06.2007
Grosjean Y, Grillet M, Augustin H, Ferveur JF, Featherstone DE (2008) A glial amino-acid transporter controls synapse strength and courtship in Drosophila. Nat Neurosci 11:54–61. https://doi.org/10.1038/nn2019
doi: 10.1038/nn2019
Manière G, Ziegler AB, Geillon F, Featherstone DE, Grosjean Y (2016) Direct sensing of nutrients via a LAT1-like transporter in Drosophila insulin-producing cells. Cell Rep 17:137–148. https://doi.org/10.1016/j.celrep.2016.08.093
doi: 10.1016/j.celrep.2016.08.093
Manière G, Grosjean Y (2017) Drosophila and humans share similar mechanisms of insulin secretion. Med Sci (Paris) 33:140–141. https://doi.org/10.1051/medsci/20173302008
doi: 10.1051/medsci/20173302008
Martin JF, Hesperger E, Simcox A, Shearn A (2000) Minidiscs encodes a putative amino acid transporter subunit required non-autonomously for imaginal cell proliferation. Mech Dev 92:155–167. https://doi.org/10.1016/S0925-4773(99)00338-X
doi: 10.1016/S0925-4773(99)00338-X
Nowak K, Seisenbacher G, Hafen E, Stocker H (2013) Nutrient restriction enhances the proliferative potential of cells lacking the tumor suppressor PTEN in mitotic tissues. Elife 2:e00380. https://doi.org/10.7554/eLife.00380
doi: 10.7554/eLife.00380
Géminard C, Rulifson EJ, Léopold P (2009) Remote control of insulin secretion by fat cells in Drosophila. Cell Metab 10:199–207. https://doi.org/10.1016/j.cmet.2009.08.002
doi: 10.1016/j.cmet.2009.08.002
Koyama T, Mirth CK (2016) Growth-blocking peptides as nutrition-sensitive signals for insulin secretion and body size regulation. PLoS Biol 14:e1002392. https://doi.org/10.1371/journal.pbio.1002392
doi: 10.1371/journal.pbio.1002392
Agrawal N, Delanoue R, Mauri A, Basco D, Pasco M, Thorens B, Léopold P (2016) The Drosophila TNF eiger is an adipokine that acts on insulin-producing cells to mediate nutrient response. Cell Metab 23:675–684. https://doi.org/10.1016/j.cmet.2016.03.003
doi: 10.1016/j.cmet.2016.03.003
Delanoue R, Meschi E, Agrawal N, Mauri A, Tsatskis Y, McNeill H, Léopold P (2016) Drosophila insulin release is triggered by adipose Stunted ligand to brain Methuselah receptor. Science 353:1553–1556. https://doi.org/10.1126/science.aaf8430
doi: 10.1126/science.aaf8430
Meschi E, Léopold P, Delanoue R (2019) An EGF-responsive neural circuit couples insulin secretion with nutrition in Drosophila. Dev Cell 48:76–86. https://doi.org/10.1016/j.devcel.2018.11.029
doi: 10.1016/j.devcel.2018.11.029
Bjordal M, Arquier N, Kniazeff J, Pin JP, Léopold P (2014) Sensing of amino acids in a dopaminergic circuitry promotes rejection of an incomplete diet in Drosophila. Cell 156:510–521. https://doi.org/10.1016/j.cell.2013.12.024
doi: 10.1016/j.cell.2013.12.024
Cheng Q, Beltran VD, Chan SM, Brown JR, Bevington A, Herbert TP (2016) System-L amino acid transporters play a key role in pancreatic β-cell signalling and function. J Mol Endocrinol 56:175–187. https://doi.org/10.1530/JME-15-0212
doi: 10.1530/JME-15-0212
Ziegler AB, Manière G, Grosjean Y (2018) JhI-21 plays a role in Drosophila insulin-like peptide release from larval IPCs via leucine transport. Sci Rep 8:1908. https://doi.org/10.1038/s41598-018-20394-1
doi: 10.1038/s41598-018-20394-1
Okamoto N, Nishimura T (2015) Signaling from glia and cholinergic neurons controls nutrient-dependent production of an insulin-like peptide for Drosophila body growth. Dev Cell 35:295–310. https://doi.org/10.1016/j.devcel.2015.10.003
doi: 10.1016/j.devcel.2015.10.003
Ou O, King-Jones K (2013) What goes up must come down: transcription factors have their say in making ecdysone pulses. Curr Topics Dev Biol 103:35–71. https://doi.org/10.1016/B978-0-12-385979-2.00002-2
doi: 10.1016/B978-0-12-385979-2.00002-2
Colombani J, Bianchini L, Layalle S, Pondeville E, Dauphin-Villemant C, Antoniewski C, Carré C, Noselli S, Léopold P (2005) Antagonistic actions of ecdysone and insulins determine final size in Drosophila. Science 310:667–670. https://doi.org/10.1126/science.1119432
doi: 10.1126/science.1119432
Galagovsky D, Depetris-Chauvin A, Manière G, Geillon F, Berthelot-Grosjean M, Noirot E, Alves G, Grosjean Y (2018) Sobremesa L-type amino acid transporter expressed in glia is essential for proper timing of development and brain growth. Cell Rep 24:3156–3166. https://doi.org/10.1016/j.celrep.2018.08.067
doi: 10.1016/j.celrep.2018.08.067
McBrayer Z, Ono H, Shimell M, Parvy JP, Beckstead RB, Warren JT, Thummel CS, Dauphin-Villemant C, Gilbert LI, O'Connor MB (2007) Prothoracicotropic hormone regulates developmental timing and body size in Drosophila. Dev Cell 13(6):857–871. https://doi.org/10.1016/j.devcel.2007.11.003
doi: 10.1016/j.devcel.2007.11.003
Homem CC, Knoblich JA (2012) Drosophila neuroblasts: a model for stem cell biology. Development 139(23):4297–4310. https://doi.org/10.1242/dev.080515
doi: 10.1242/dev.080515
Britton JS, Edgar BA (1998) Environmental control of the cell cycle in Drosophila : nutrition activates mitotic and endoreplicative cells by distinct mechanisms. Development 125:2149–2158
Stefana MI, Driscoll PC, Obata F, Pengelly AR, Newell CL, MacRae JI, Gould AP (2017) Developmental diet regulates Drosophila lifespan via lipid autotoxins. Nat Commun 8(1):1384. https://doi.org/10.1038/s41467-017-01740-9
doi: 10.1038/s41467-017-01740-9
Jayakumar S, Richhariya S, Reddy OV, Texada MJ, Hasan G (2016) Drosophila larval to pupal switch under nutrient stress requires IP
doi: 10.7554/eLife.17495
Jayakumar S, Richhariya S, Deb BK, Hasan G (2018) A multicomponent neuronal response encodes the larval decision to pupariate upon amino acid starvation. J Neurosci 38(47):10202–10219. https://doi.org/10.1523/JNEUROSCI.1163-18
doi: 10.1523/JNEUROSCI.1163-18
Ki Y, Lim C (2019) Sleep-promoting effects of threonine link amino acid metabolism in Drosophila neuron to GABAergic control of sleep drive. Elife 8:e40593. https://doi.org/10.7554/eLife.40593
doi: 10.7554/eLife.40593
Yang Z, Huang R, Fu X, Wang G, Qi W, Mao D, Shi Z, Shen WL, Wang L (2018) A post-ingestive amino acid sensor promotes food consumption in Drosophila. Cell Res 28(10):1013–1025. https://doi.org/10.1038/s41422-018-0084-9
doi: 10.1038/s41422-018-0084-9
Lin KY, Hsu HJ (2020) Regulation of adult female germline stem cells by nutrient-responsive signaling. Curr Opin Insect Sci 37:16–22. https://doi.org/10.1016/j.cois.2019.10.005
doi: 10.1016/j.cois.2019.10.005
Park JH, Chen J, Jang S, Ahn TJ, Choi MS, Kwon JY (2016) A subset of enteroendocrine cells is activated by amino acids in the Drosophila midgut. FEBS lett 590:493–500. https://doi.org/10.1002/1873-3468.12073
doi: 10.1002/1873-3468.12073