The systemic control of growth

Cold Spring Harbor Perspectives in Biology

Volumn 7, Issue 12, 2015, Pages

  Boulan, Laura ^a,b,c   Milán, Marco ^d   Léopold, Pierre ^a,b,c  

^a UNIVERSITÉ CÔTE D'AZUR   (France)

^b CNRS   (France)

^c INSERM   (France)

^d UNIVERSITY OF BARCELONA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

GROWTH HORMONE; INSULIN; SOMATOMEDIN;

ANATOMY AND HISTOLOGY; ANIMAL; BODY SIZE; DROSOPHILA; GENETICS; GROWTH; GROWTH, DEVELOPMENT AND AGING; METABOLISM; METAMORPHOSIS; NUTRITION; PHYSIOLOGY; SIGNAL TRANSDUCTION; SPECIES DIFFERENCE;

ANIMALS; BODY SIZE; DROSOPHILA; GROWTH; GROWTH HORMONE; INSULIN; METAMORPHOSIS, BIOLOGICAL; NUTRITIONAL PHYSIOLOGICAL PHENOMENA; SIGNAL TRANSDUCTION; SOMATOMEDINS; SPECIES SPECIFICITY;

EID: 84949238864     PISSN: None     EISSN: 19430264     Source Type: Journal    
DOI: 10.1101/cshperspect.a019117     Document Type: Article

References (175)

1. Adeghate E, Ponery AS, Wahab A. 2001. Effect of electrical field stimulation on insulin and glucagon secretion from the pancreas of normal and diabetic rats. Horm Metab Res 33: 281-289.
2. Alfa RW, Park S, Skelly KR, Poffenberger G, Jain N, Gu X, Kockel L, Wang J, Liu Y, Powers AC, et al. 2015. Suppression of insulin production and secretion by a decretin hormone. Cell Metab 21: 323-333.
3. Andersen DS, Colombani J, Leopold P. 2013. Coordination of organ growth: Principles and outstanding questions from the world of insects. Trends Cell Biol 23: 336-344.
4. Arquier N, Geminard C, Bourouis M, Jarretou G, Honegger B, Paix A, Leopold P. 2008. Drosophila ALS regulates growth and metabolism through functional interaction with insulin-like peptides. Cell Metab 7: 333-338.
5. Arsham AM, Neufeld TP. 2006. Thinking globally and acting locally with TOR. Curr Opin Cell Biol 18: 589-597.
6. Aspinwall CA, Lakey JR, Kennedy RT. 1999. Insulin-stimulated insulin secretion in single pancreatic b cells. J Biol Chem 274: 6360-6365.
7. Avruch J, Long X, Ortiz-Vega S, Rapley J, Papageorgiou A, Dai N. 2009. Amino acid regulation of TOR complex 1. Am J Physiol Endocrinol Metab 296: E592-E602.
8. Baehrecke EH. 2000. Steroid regulation ofprogrammed cell death during Drosophila development. Cell Death Differ 7: 1057-1062.
9. Bai H, Kang P, Tatar M. 2012. Drosophila insulin-like pep-tide-6 (dilp6) expression from fat body extends lifespan and represses secretion of Drosophila insulin-like pep-tide-2 from the brain. Aging Cell 11: 978-985.
10. Beadle GW, Tatum EL, Clancy C. 1938. Food level in relation to rate of development and eye pigmentation in Dro-sophila melanogaster. Biol Bull 75: 447-462.
11. Birse RT, Söderberg JAE, Luo J, Winther AME, Nässel DR. 2011. Regulation of insulin-producing cells in the adult Drosophila brain via the tachykinin peptide receptor DTKR. J Exp Biol 214: 4201-4208.
12. 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.
13. Böhni R, Riesgo-Escovar J, Oldham S, Brogiolo W, Stocker H, Andruss BF, Beckingham K, Hafen E. 1999. Autonomous control of cell and organ size by CHICO, a Dro-sophila homolog of vertebrate IRS1-4. Cell 97: 865-875.
14. Boulan L, Martín D, Milán M. 2013. bantam miRNA promotes systemic growth by connecting insulin signaling and ecdysone production. Curr Biol 23: 473-478.
15. 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.
16. Broughton S, Alic N, Slack C, Bass T, Ikeya T, Vinti G, Tom-masi AM, Driege Y, Hafen E, Partridge L. 2008. Reduction of DILP2 in Drosophila triages a metabolic phenotype from lifespan revealing redundancy and compensation among DILPs. PLoS ONE 3: e3721.
17. Browder MH, D'Amico LJ, Nijhout HF. 2001. The role of low levels of juvenile hormone esterase in the metamorphosis of Manduca sexta. J Insect Sci 1: 11.
18. Bryk B, Hahn K, Cohen SM, Teleman AA. 2010. MAP4K3 regulates body size and metabolism in Drosophila. Dev Biol 344: 150-157.
19. Cáceres L, Necakov AS, Schwartz C, Kimber S, Roberts IJH, Krause HM. 2011. Nitric oxide coordinates metabolism, growth, and development via the nuclear receptor E75. Genes Dev 25: 1476-1485.
20. Caldwell PE, Walkiewicz M, Stern M. 2005. Ras activity in the Drosophila prothoracic gland regulates bodysize and developmental rate via ecdysone release. Curr Biol 15: 1785-1795.
21. Callier V, Nijhout HF. 2011. Control of body size byoxygen supply reveals size-dependent and size-independent mechanisms of molting and metamorphosis. Proc Natl Acad Sci 108: 14664-14669.
22. Callier V, Shingleton AW, Brent CS, Ghosh SM, Kim J, Harrison JF. 2013. The role of reduced oxygen in the developmental physiology of growth and metamorphosis initiation in Drosophila melanogaster. JExp Biol 216: 4334-4340.
23. Cheetham SW, Brand AH. 2013. Insulin finds its niche. Science 340: 817-818.
24. Chell JM, Brand AH. 2010. Nutrition-responsive glia control exit of neural stem cells from quiescence. Cell 143: 1161-1173.
25. Cheng LY, Bailey AP, Leevers SJ, Ragan TJ, Driscoll PC, Gould AP. 2011. Anaplastic lymphoma kinase spares organ growth during nutrient restriction in Drosophila. Cell 146: 435-447.
26. Colombani J, Raisin S, Pantalacci S, Radimerski T, Mon-tagne J, Léopold P. 2003. A nutrient sensor mechanism controls Drosophila growth. Cell 114: 739-749.
27. Colombani J, Bianchini L, Layalle S, Pondeville E, Dauphin-Villemant C, Antoniewski C, Carre C, Noselli S, Leopold P. 2005. Antagonistic actions of ecdysone and insulins determine final size in Drosophila. Science 310: 667-670.
28. Colombani J, Andersen DS, Leopold P. 2012. Secreted pep-tide Dilp8 coordinates Drosophila tissue growth with developmental timing. Science 336: 582-585.
29. Crocker A, Shahidullah M, Levitan IB, Sehgal A. 2010. Identification of a neural circuit that underlies the effects of octopamine on sleep:wake behavior. Neuron 65: 670-681.
30. Davidowitz G, D'Amico LJ, Nijhout HF. 2003. Critical weight in the development of insect body size. Evol Dev 5: 188-197.
31. D'Avino PP, Thummel CS. 2000. The ecdysone regulatory pathway controls wing morphogenesis and integrin expression during Drosophila metamorphosis. Dev Biol 220: 211-224.
32. Delanoue R, Slaidina M, Leopold P. 2010. The steroid hormone ecdysone controls systemic growth by repressing dMyc function in Drosophila fat cells. Dev Cell 18: 1012-1021.
33. Demontis F, Perrimon N. 2009. Integration ofinsulin recep-tor/Foxo signaling and dMyc activity during muscle growth regulates body size in Drosophila. Development 136: 983-993.
34. Demontis F, Patel VK, Swindell WR, Perrimon N. 2014. Intertissue control ofthe nucleolus via a myokine-depen-dent longevity pathway. Cell Rep 7: 1481-1494.
35. De Virgilio C, Loewith R. 2006. The TOR signalling network from yeast to man. IntJBiochem Cell Biol 38: 1476-1481.
36. Domene HM, Hwa V, Argente J, Wit JM, Wit JM, Camacho-Huabner C, Jasper HG, Pozo J, van Duyvenvoorde HA, Yakar S, et al. 2009. Human acid-labile subunit deficiency: Clinical, endocrine and metabolic consequences. HormRes 72: 129-141.
37. Dong J, Pan D. 2004. Tsc2 is not a critical target of Akt during normal Drosophila development. Genes Dev 18: 2479-2484.
38. Dong H, Kumar M, Zhang Y, Gyulkhandanyan A, Xiang YY, Ye B, Perrella J, Hyder A, Zhang N, Wheeler M, et al. 2006. g-Aminobutyric acid up- and downregulates insulin secretion from b cells in concert with changes in glucose concentration. Diabetologia 49: 697-705.
39. Drucker DJ, Philippe J, Mojsov S, Chick WL, Habener JF. 1987. Glucagon-like peptide I stimulates insulin gene expression and increases cyclic AMP levels in a rat islet cell line. Proc Natl Acad Sci 84: 3434-3438.
40. Duan C, Xu Q. 2005. Roles of insulin-like growth factor (IGF) binding proteins in regulating IGF actions. Gen Comp Endocrinol 142: 44-52.
41. Duran A, Amanchy R, Linares JF, Joshi J, Abu-Baker S, Po-rollo A, Hansen M, Moscat J, Diaz-Meco MT. 2011. p62 is a key regulator ofnutrient sensing in the mTORC1 pathway. Mol Cell 44: 134-146.
42. Edgar BA. 2006. How flies get their size: Genetics meets physiology. Nat Rev Genet 7: 907-916.
43. Enell LE, Kapan N, Soaderberg JAE, Kahsai L, Naasse DR. 2010. Insulin signaling, lifespan and stress resistance are modulated by metabotropic GABA receptors on insulin producing cells in the brain of Drosophila. PLoS ONE 5: e15780.
44. Figueroa-Clarevega A, Bilder D. 2015. Malignant Drosophila tumors interrupt insulin signaling to induce cachexia-like wasting. Dev Cell 33: 47-55.
45. Francis VA, Zorzano A, Teleman AA. 2010. dDOR is an EcR coactivator that forms a feed-forward loop connecting insulin and ecdysone signaling. Curr Biol 20: 1799-808.
46. Fridell Y-WC, Hoh M, Kreneisz O, Hosier S, Chang C, Scantling D, Mulkey DK, Helfand SL. 2009. Increased uncoupling protein (UCP) activity in Drosophila insulin-producing neurons attenuates insulin signaling and extends lifespan. Aging (Albany NY) 1: 699-713.
47. Garelli A, Gontijo AM, Miguela V, Caparros E, Dominguez M. 2012. Imaginal discs secrete insulin-like peptide 8 to mediate plasticityofgrowth and maturation. Science 336: 579-582.
48. Garofalo RS. 2002. Genetic analysis of insulin signaling in Drosophila. Trends Endocrinol Metab 13: 156-162.
49. Géminard C, Rulifson EJ, Léopold P. 2009. Remote control of insulin secretion by fat cells in Drosophila. Cell Metab 10: 199-207.
50. Gibbens YY, Warren JT, Gilbert LI, O'Connor MB. 2011. Neuroendocrine regulation of Drosophila metamorphosis requires TGF-b/activin signaling. Development 138: 2693-2703.
51. Gilbert LI. 2004. Halloween genes encode P450 enzymes that mediate steroid hormone biosynthesis in Drosophila melanogaster. Mol Cell Endocrinol 215: 1-10.
52. Goberdhan DCI, Paricio N, Goodman EC, Mlodzik M, Wilson C. 1999. Drosophila tumor suppressor PTENcontrols cell size and number by antagonizing the Chico/PI3-ki-nase signaling pathway. Genes Dev 13: 3244-3258.
53. Grewal SS, Li L, Orian A, Eisenman RN, Edgar BA. 2005. Myc-dependent regulation of ribosomal RNA synthesis during Drosophila development. Nat Cell Biol 7: 295-302.
54. Grönke S, Clarke D-F, Broughton S, Andrews TD, Partridge L. 2010. Molecular evolution and functional characterization of Drosophila insulin-like peptides. PLoS Genet 6: e1000857.
55. Guertin DA, Guntur KVP, Bell GW, Thoreen CC, Sabatini DM. 2006. Functional genomics identifies TOR-regulated genes that control growth and division. Curr Biol 16: 958-970.
56. Guittard E, Blais C, Maria A, Parvy J-P, Pasricha S, Lumb C, Lafont R, Daborn PJ, Dauphin-Villemant C. 2011. CYP18A1, a key enzyme of Drosophila steroid hormone inactivation, is essential for metamorphosis. Dev Biol 349: 35-45.
57. Halme A, Cheng M, Hariharan IK. 2010. Retinoids regulate a developmental checkpoint for tissue regeneration in Drosophila. Curr Biol 20: 458-463.
58. Hardie DG. 2007. AMP-activated/SNF1 protein kinases: Conserved guardians of cellular energy. Nat Rev Mol Cell Biol 8: 774-785.
59. Holz MK, Ballif BA, Gygi SP, Blenis J. 2005. mTOR and S6K1 mediate assembly of the translation preinitiation complex through dynamic protein interchange and ordered phosphorylation events. Cell 123: 569-580.
60. Honegger B, Galic M, Koahler K, Wittwer F, Brogiolo W, Hafen E, Stocker H. 2008. Imp-L2, a putative homolog of vertebrate IGF-binding protein 7, counteracts insulin signaling in Drosophila and is essential for starvation resistance. J Biol 7: 10.
61. Huang X, Suyama K, Buchanan J, Zhu AJ, Scott MP. 2005. A Drosophila model of the Niemann-Pick type C lysosome storage disease: dnpc1a is required for molting and sterol homeostasis. Development 132: 5115-5124.
62. Huang X, Warren JT, Buchanan J, Gilbert LI, Scott MP. 2007. Drosophila Niemann-Pick type C-2 genes control sterol homeostasis and steroid biosynthesis: A model ofhuman neurodegenerative disease. Development 134: 3733-3742.
63. Huang X, Warren JT, Gilbert LI. 2008. New players in the regulation of ecdysone biosynthesis. J Genet Genomics 35: 1-10.
64. Hyun S, Lee JH, Jin H, Nam J, Namkoong B, Lee G, Chung J, Kim VN. 2009. Conserved microRNA miR-8/miR-200 and its target USH/FOG2 control growth by regulating PI3K. Cell 139: 1096-1108.
65. 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.
66. Inoki K, Li Y, Zhu T, Wu J, Guan K-L. 2002. TSC2 is phos- phorylated and inhibited by Akt and suppresses mTOR signalling. Nat Cell Biol 4: 648-657.
67. Inoki K, Li Y, Xu T, Guan K-L. 2003a. Rheb GTPase is a direct target of TSC2 GAP activity and regulates mTOR signaling. Genes Dev 17: 1829-1834.
68. Inoki K, Zhu T, Guan K-L. 2003b. TSC2 mediates cellular energy response to control cell growth and survival. Cell 115: 577-590.
69. Jin H, Kim V, Hyun S. 2012. Conserved microRNA miR-8 controls body size in response to steroid signaling in Drosophila. Genes Dev 26: 1427-1432.
70. Johnston DM, Sedkov Y, Petruk S, Riley KM, Fujioka M, Jaynes JB, Mazo A. 2011. Ecdysone- and NO-mediated gene regulation bycompeting EcR/Usp and E75Anucle-ar receptors during Drosophila development. Mol Cell 44: 51-61.
71. Kalaany NY, Sabatini DM. 2009. Tumours with PI3K activation are resistant to dietary restriction. Nature 458: 725-731.
72. Kaplan DD, Zimmermann G, Suyama K, Meyer T, Scott MP. 2008. A nucleostemin family GTPase, NS3, acts in sero-tonergic neurons to regulate insulin signaling and control body size. Genes Dev 22: 1877-1893.
73. Kawakami A, Kataoka H, Oka T, Mizoguchi A, Kimura-Kawakami M, Adachi T, Iwami M, Nagasawa H, Suzuki A, Ishizaki H. 1990. Molecular cloning of the Bombyx mori prothoracicotropic hormone. Science 247: 1333-1335.
74. Killip LE, Grewal SS. 2012. DREF is required for cell and organismal growth in Drosophila and functions downstream of the nutrition/TOR pathway. Dev Biol 371: 191-202.
75. Kim SK, Rulifson EJ. 2004. Conserved mechanisms of glucose sensing and regulation by Drosophila corpora cardi- aca cells. Nature 431: 316-320.
76. Kim E, Goraksha-Hicks P, Li L, Neufeld TP, Guan K-L. 2008. Regulation of TORC1 by Rag GTPases in nutrient response. Nat Cell Biol 10: 935-945.
77. Kim Y-M, Stone M, Hwang TH, Kim Y-G, Dunlevy JR, Griffin TJ, Kim D-H. 2012. SH3BP4 is a negative regulator of amino acid-Rag GTPase-mTORC1 signaling. Mol Cell 46: 1-14.
78. King-Jones K, Thummel CS. 2005. Nuclear receptors—A perspective from Drosophila. Nat Rev Genet 6: 311-323.
79. Kréneisz O, Chen X, Fridell Y-WC, Mulkey DK. 2010. Glucose increases activity and Ca2+ in insulin-producing cells of adult Drosophila. Neuroreport 21: 1116-1120.
80. Kwon Y, Song W, Droujinine IA, Hu Y, Asara JM, Perrimon N. 2015. Systemic organ wasting induced by localized expression of the secreted insulin/IGF antagonist lmpL2. Dev Cell 33: 36-46.
81. Layalle S, Arquier N, Leopold P. 2008. The TOR pathway couples nutrition and developmental timing in Dro-sophila. Dev Cell 15: 568 -577
82. Lee CY, Baehrecke EH. 2001. Steroid regulation ofautopha-gic programmed cell death during development. Development 128: 1443-1455.
83. Lee KS, Kwon OY, Lee JH, Kwon K, Min KJ, Jung SA, Kim AK, You KH, Tatar M, Yu K. 2008. Drosophila short neu- ropeptide F signalling regulates growth byERK-mediated insulin signalling. Nat Cell Biol 10: 468-475.
84. Leevers SJ, Weinkove D, MacDougall LK, Hafen E, Water-field MD. 1996. The Drosophila phosphoinositide-3-ki-nase Dp110 promotes cell growth. EMBO J 15: 6584-6594.
85. Loewith R, Jacinto E, Wullschleger S, Lorberg A, Crespo JL, Bonenfant D, Oppliger W, Jenoe P, Hall MN. 2002. Two TOR complexes, only one of which is rapamycin sensitive, have distinct roles in cell growth control. Mol Cell 10: 457-468.
86. Luo J, Becnel J, Nichols CD, Nassel DR. 2012. Insulin-producing cells in the brain ofadult Drosophila are regulated by the serotonin 5-HT1A receptor. Cell Mol Life Sci 69: 471-484.
87. Luo J, Lushchak OV, Goergen P, Williams MJ, Naassel DR. 2014. Drosophila insulin-producing cells are differentially modulated by serotonin and octopamine receptors and affect social behavior. PLoS ONE 9: e99732.
88. Marshall L, Rideout EJ, Grewal SS. 2012. Nutrient/TOR-dependent regulation of RNA polymerase III controls tissue and organismal growth in Drosophila. EMBO J 31: 1916-1930.
89. 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 Dro-sophila. Dev Cell 13: 857-871.
90. McBride A, Ghilagaber S, Nikolaev A, Hardie DG. 2009. The glycogen-binding domain on the AMPK b subunit allows the kinase to act as a glycogen sensor. Cell Metab 9: 23-34.
91. McIntyre N, Holdsworth C, Turner D. 1964. New interpretation of oral glucose tolerance. Lancet 4: 20-21.
92. Miguel-Aliaga I. 2012. Nerveless and gutsy: Intestinal nutrient sensing from invertebrates to humans. Semin Cell Dev Biol 23: 614-620.
93. Miron M, Verdu J, Lachance PE, Birnbaum MJ, Lasko PF, Sonenberg N. 2001. The translational inhibitor 4E-BP is an effector of PI3K/Akt signalling and cell growth in Drosophila. Nat Cell Biol 3: 596-601.
94. Mirth CK, Riddiford LM. 2007. Size assessment and growth control: How adult size is determined in insects. Bioessays 29: 344-355.
95. Mirth CK, Shingleton AW. 2012. Integrating bodyand organ size in Drosophila: Recent advances and outstanding problems. Front Endocrinol (Lausanne) 3: 1-13.
96. Mirth C, Truman JW, Riddiford LM. 2005. The role of the prothoracic gland in determining critical weight for metamorphosis in Drosophila melanogaster. Curr Biol 15: 1796-1807.
97. Miyamoto T, Slone J, Song X, Amrein H. 2012. A fructose receptor functions as a nutrient sensor in the Drosophila brain. Cell 151: 1113-1125.
98. Nakae J, Kido Y, Accili D. 2001. Distinct and overlapping functions of insulin and IGF-I receptors. Endocr Rev 22: 818-835.
99. Nijhout HF, Grunert LW. 2002. Bombyxin is a growth factor for wing imaginal disks in Lepidoptera. Proc Natl Acad Sci 99: 15446-15450.
100. Nijhout H, Davidowitz G, Roff D. 2006. Aquantitative analysis ofthe mechanism that controls bodysize in Manduca sexta. J Biol 5: 16.
101. 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 Dro- sophila. Dev Cell 17: 885-891.
102. Okamoto N, Nakamori R, Murai T, Yamauchi Y, Masuda A, Nishimura T. 2013. A secreted decoy of InR antagonizes insulin/IGF signaling to restrict body growth in Dro- sophila. Genes Dev 27: 87-97.
103. Ou Q, Magico A, King-Jones K. 2011. Nuclear receptor DHR4 controls the timing of steroid hormone pulses during Drosophila development. PLoS Biol 9: e1001160.
104. Pallares-Cartes C, Cakan-Akdogan G, Teleman Aa. 2012. Tissue-specific coupling between insulin/IGF and TORC1 signaling via PRAS40 in Drosophila. Dev Cell 22: 172-182.
105. Parisi F, Riccardo S, Zola S, Lora C, Grifoni D, Brown LM, Bellosta P. 2013. dMyc expression in the fat body affects DILP2 release and increases the expression of the fat de-saturase Desat1 resulting in organismal growth. Dev Biol 379: 64-75.
106. Park S, Alfa RW, Topper SM, Kim GES, Kockel L, Kim SK. 2014. Ageneticstrategyto measure circulatingDrosophila insulin reveals genes regulating insulin production and secretion. PLoS Genet 10: e1004555.
107. Parker NF, Shingleton AW. 2011. The coordination ofgrowth among Drosophila organs in response to localized growth-perturbation. Dev Biol 357: 318-325.
108. Pedersen BK, Febbraio MA. 2012. Muscles, exercise and obesity: Skeletal muscle as a secretory organ. Nat Rev Endocrinol 8: 457-465.
109. Petryk A, Warren JT, Marques G, Jarcho MP, Gilbert LI, Kahler J, Parvy J-P, Li Y, Dauphin-Villemant C, O'Connor MB. 2003. Shade is the Drosophila P450 enzyme that mediates the hydroxylation of ecdysone to the steroid insect molting hormone 20-hydroxyecdysone. Proc Natl Acad Sci 100: 13773-13778.
110. Potter CJ, Huang H, Xu T. 2001. Drosophila Tsc1 functions with Tsc2 to antagonize insulin signaling in regulating cell growth, cell proliferation, and organ size. Cell 105: 357-368.
111. Potter CJ, Pedraza LG, Xu T. 2002. Akt regulates growth by directly phosphorylating Tsc2. Nat Cell Biol 4: 658-665
112. Rajan A, Perrimon N. 2012. Drosophila cytokine unpaired 2 regulates physiological homeostasis by remotely controlling insulin secretion. Cell 151: 123-137.
113. Reinking J, Lam MMS, Pardee K, Sampson HM, Liu S, Yang P, Williams S, White W, Lajoie G, Edwards A, et al. 2005. The Drosophila nuclear receptor e75 contains heme and is gas responsive. Cell 122: 195-207.
114. Rewitz KF, Yamanaka N, Gilbert LI, O'Connor MB. 2009. The insect neuropeptide PTTH activates receptor tyro-sine kinase torso to initiate metamorphosis. Science 326: 1403-1405.
115. Rewitz KF, Yamanaka N, O'Connor MB. 2010. Steroid hormone inactivation is required during the juvenile-adult transition in Drosophila. Dev Cell 19: 895-902.
116. Ribeiro C, Dickson BJ. 2010. Sex peptide receptor and neu-ronal TOR/S6K signaling modulate nutrient balancing in Drosophila. Curr Biol 20: 1000-1005.
117. Riddiford LM. 1993. Hormone receptors and the regulation of insect metamorphosis. Receptor 3: 203-209.
118. Riddiford LM, Truman JW, Mirth CK, Shen Y-C. 2010. A role for juvenile hormone in the prepupal development of Drosophila melanogaster. Development 137: 1117-1126.
119. Rideout EJ, Marshall L, Grewal SS. 2012. Drosophila RNA polymerase III repressor Maf1 controls body size and developmental timing by modulating tRNAiMet synthesis and systemic insulin signaling. Proc Natl Acad Sci 109: 1139-1144.
120. Rodenfels J, Lavrynenko O, Ayciriex S, Sampaio JL, Car-valho M, Shevchenko A, Eaton S. 2014. Production of systemically circulating Hedgehog by the intestine couples nutrition to growth and development. Genes Dev 28: 2636-2651.
121. Rulifson EJ, Kim SK, Nusse R. 2002. Ablation of insulin- producing neurons in flies: Growth and diabetic pheno- types. Science 296: 1118-1120.
122. Russell M. 1974. Pattern formation in the imaginal discs ofa temperature sensitive cell-lethal mutant of Drosophila melanogaster. Dev Biol 40: 24-39.
123. Rusten TE, Lindmo K, Juhisz G, Sass M, Seglen PO, Brech A, Stenmark H. 2004. Programmed autophagy in the Dro-sophila fat body is induced by ecdysone through regulation of the PI3K pathway. Dev Cell 7: 179-192.
124. Saha AK, Chaudhuri AB, Moorthy SM, Roy S. 2009. Studies on determination of larval critical weight in silkworm, Bombyx mori L.—An index of quality. IntJ Ind Entomol 19: 243-248.
125. Sancak Y, Thoreen CC, Peterson TR, Lindquist RA, Kang SA, Spooner E, Carr Sa, Sabatini DM. 2007. PRAS40 is an insulin-regulated inhibitor of the mTORC1 protein ki-nase. Mol Cell 25: 903-915.
126. Sancak Y, Peterson TR, Shaul YD, Lindquist RA, Thoreen CC, Bar-Peled L, Sabatini DM. 2008. The Rag GTPases bind raptor and mediate amino acid signaling to mTORC1. Science 320: 1496-1501.
127. Sancak Y, Bar-Peled L, Zoncu R, Markhard AL, Nada S, Sabatini DM. 2010. Ragulator-Rag complex targets mTORC1 to the lysosomal surface and is necessary for its activation by amino acids. Cell 141: 290-303.
128. Saucedo LJ, Gao X, Chiarelli DA, Li L, Pan D, Edgar BA. 2003. Rheb promotes cell growth as a component of the insulin/TOR signalling network. Nat Cell Biol 5: 566-571.
129. Schleich S, Teleman Aa. 2009. Akt phosphorylates both Tsc1 and Tsc2 in Drosophila, but neither phosphorylation is required for normal animal growth. PLoS ONE 4: e6305.
130. Schubiger M, Truman JW. 2000. The RXR ortholog USP suppresses early metamorphic processes in Drosophila in the absence of ecdysteroids. Development 127: 1151-1159.
131. Schubiger M, Carre C, Antoniewski C, Truman JW. 2005. Ligand-dependent de-repression via EcR/USP acts as a gate to coordinate the differentiation of sensory neurons in the Drosophila wing. Development 132: 5239-5248.
132. Scott RC, Schuldiner O, Neufeld TP. 2004. Role and regulation of starvation-induced autophagy in the Drosophila fat body. Dev Cell 7: 167-178.
133. Sehnal F, Bryant PJ. 1993. Delayed pupariation in Drosophila imaginal disc overgrowth mutants is associated with reduced ecdysteroid titer. J Insect Physiol 39: 1051-1059.
134. Shin SC, Kim S-H, You H, Kim B, Kim AC, Lee K-A, Yoon J-H, Ryu J-H, Lee W-J. 2011. Drosophila microbiome modulates host developmental and metabolic homeostasis via insulin signaling. Science 334: 670-674.
135. Shingleton AW, Das J, Vinicius L, Stern DL. 2005. The temporal requirements for insulin signaling during development in Drosophila. PLoS Biol 3: e289.
136. Simpson P, Schneiderman HA. 1975. Isolation of temperature sensitive mutations blocking clone development in Drosophila melanogaster, and the effects of a temperature sensitive cell lethal mutation on pattern formation in imaginal discs. Wilhelm Roux's Arch 178: 247-275.
137. Simpson P, Berreur P, Berreur-Bonnenfant J. 1980. The initiation of pupariation in Drosophila: Dependence on growth of the imaginal discs. J Embryol Exp Morphol 57: 155-165.
138. Slaidina M, Delanoue R, Gronke S, Partridge L, Léopold P. 2009. A Drosophila insulin-like peptide promotes growth during nonfeeding states. Dev Cell 17: 874-84.
139. Song Q, Gilbert LI. 1994. S6 phosphorylation results from prothoracicotropic hormone stimulation of insect pro-thoracic glands: A role for S6 kinase. Dev Genet 15: 332-338.
140. Song Q, Gilbert LI. 1997. Molecular cloning, developmental expression, and phosphorylation ofribosomal protein S6 in the endocrine gland responsible for insect molting. J Biol Chem 272: 4429-4435.
141. Sonoda N, Imamura T, Yoshizaki T, Babendure JL, Lu J-C, Olefsky JM. 2008. b-Arrestin-1 mediates glucagon-like peptide-1 signaling to insulin secretion in cultured pancreatic b cells. Proc Natl Acad Sci 105: 6614-6619.
142. 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.
143. Spéder P, Brand AH. 2014. Gap junction proteins in the blood-brain barrier control nutrient-dependent reactivation ofDrosophila neural stem cells. Dev Cell 30: 309-321.
144. Stieper BC, Kupershtok M, Driscoll MV, Shingleton AW. 2008. Imaginal discs regulate developmental timing in Drosophila melanogaster. Dev Biol 321: 18-26.
145. Stocker H, Radimerski T, Schindelholz B, Wittwer F, Belawat P, Daram P, Breuer S, Thomas G, Hafen E. 2003. Rheb is an essential regulator of S6K in controlling cell growth in Drosophila. Nat Cell Biol 5: 559-565.
146. Storelli G, Defaye A, Erkosar B, Hols P, Royet J, Leulier F. 2011. Lactobacillus plantarum promotes Drosophila systemic growth by modulating hormonal signals through TOR-dependent nutrient sensing. Cell Metab 14: 403-414.
147. Talamillo A, Sánchez J, Cantera R, Pérez C, Martín D, Ca-minero E, Barrio R. 2008. Smt3 is required for Drosophila melanogaster metamorphosis. Development 135: 1659-1668.
148. Talamillo A, Herboso L, Pirone L, Perez C, Gonzalez M, Sanchez J, Mayor U, Lopitz-Otsoa F, Rodriguez MS, Sutherland JD, et al. 2013. Scavenger receptors mediate the role of SUMO and Ftz-f1 in Drosophila steroidogenesis. PLoS Genet 9: e1003473.
149. Talbot WS, Swyryd EA, Hogness DS. 1993. Drosophila tissues with different metamorphic responses to ecdysone express different ecdysone receptor isoforms. Cell 73: 1323-1337.
150. Tang HY, Smith-Caldas MSB, Driscoll MV, Salhadar S, Shin-gleton AW. 2011. FOXO regulates organ-specific pheno-typic plasticity in Drosophila. PLoS Genet 7: e1002373.
151. Tapon N, Ito N, Dickson BJ, Treisman JE, Hariharan IK. 2001. The Drosophila tuberous sclerosis complex gene homologs restrict cell growth and cell proliferation. Cell 105: 345-355.
152. Tee AR, Manning BD, Roux PP, Cantley LC, Blenis J. 2003. Tuberous sclerosis complex gene products, Tuberin and Hamartin, control mTOR signaling by acting as a GTPase-activating protein complex toward Rheb. Curr Biol 13: 1259-1268.
153. Teleman AA, Chen YW, Cohen SM. 2005. 4E-BP functions as a metabolic brake used under stress conditions but not during normal growth. Genes Dev 19: 1844-1848.
154. Teleman AA, Hietakangas V, Sayadian AC, Cohen SM. 2008. Nutritional control of protein biosynthetic capacity by insulin via Myc in Drosophila. Cell Metab 7: 21-32.
155. Thomas HE, Stunnenberg HG, Stewart AF. 1993. Heterodi-merization of the Drosophila ecdysone receptor with ret-inoid X receptor and ultraspiracle. Nature 362: 471-475.
156. Toshima N, Tanimura T. 2012. Taste preference for amino acids is dependent on internal nutritional state in Drosophila melanogaster. J Exp Biol 215: 2827-2832.
157. Vander Haar E, Lee S-I, Bandhakavi S, Griffin TJ, Kim D-H. 2007. Insulin signalling to mTOR mediated by the Akt/ PKB substrate PRAS40. Nat Cell Biol 9: 316-323.
158. Vargas MA, Luo N, Yamaguchi A, Kapahi P. 2010. A role for S6 kinase and serotonin in postmating dietary switch and balance of nutrients in D. melanogaster. Curr Biol 20: 1113-1125.
159. Varghese J, Lim SF, Cohen SM. 2010. Drosophila miR-14 regulates insulin production and metabolism through its target, sugarbabe. Genes Dev 24: 2748-2753.
160. Wang X, Li W, Williams M, Terada N, Alessi DR, Proud CG. 2001. Regulation of elongation factor 2 kinase by p90(RSK1) and p70 S6 kinase. Eur Mol Biol Organ J 20: 4370-4379.
161. 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 104: 19873-19878.
162. Warren JT, Yerushalmi Y, Shimell MJ, O'Connor MB, Restifo LL, Gilbert LI. 2006. Discrete pulses ofmolting hormone, 20-hydroxyecdysone, during late larval development of Drosophila melanogaster: Correlations with changes in gene activity. Dev Dyn 235: 315-326.
163. Wingrove JA, O'Farrell PH. 1999. Nitric oxide contributes to behavioral, cellular, and developmental responses to low oxygen in Drosophila. Cell 98: 105-114.
164. Wollam J, Antebi A. 2011. Sterol regulation of metabolism, homeostasis, and development. Annu Rev Biochem 80: 885-916.
165. Wu Q, Brown MR. 2006. Signaling and function of insulinlike peptides in insects. Annu Rev Entomol 51: 1-24.
166. Wullschleger S, Loewith R, Hall MN. 2006. TOR signaling in growth and metabolism. Cell 124: 471-484.
167. Xiang Y, Liu Z, Huang X. 2010. br regulates the expression of the ecdysone biosynthesis gene npcl. Dev Biol 344: 800-808.
168. Yamaguchi T, Fernandez R, Roth RA. 1995. Comparison of the signaling abilities ofthe Drosophila and human insulin receptors in mammalian cells. Biochemistry 34: 4962-4968.
169. Yamanaka N, Rewitz KF, O'Connor MB. 2013. Ecdysone control of developmental transitions: Lessons from Dro-sophila research. Annu Rev Entomol 58: 497-516.
170. Yao TP, Forman BM, Jiang Z, Cherbas L, Chen JD, McKeown M, Cherbas P, Evans RM. 1993. Functional ecdysone receptor is the product of EcR and Ultraspiracle genes. Nature 366: 476-479.
171. Young S-C, Yeh W-L, Gu S-H. 2012. Transcriptional regulation of the PTTH receptor in prothoracic glands of the silkworm, Bombyx mori. J Insect Physiol 58: 102-109.
172. Zhang H, Stallock JP, Ng JC, Reinhard C, Neufeld TP. 2000. Regulation of cellular growth by the Drosophila target of rapamycin dTOR. Genes Dev 14: 2712-2724.
173. Zhang Y, Gao X, Saucedo LJ, Ru B, Edgar BA, Pan D. 2003. Rheb is a direct target of the tuberous sclerosis tumour suppressor proteins. Nat Cell Biol 5: 578-581.
174. Zhang H, Liu J, Li CR, Momen B, Kohanski RA, Pick L. 2009. Deletion ofDrosophila insulin-like peptides causes growth defects and metabolic abnormalities. Proc Natl Acad Sci 106: 19617-19622.
175. Zhou X, Zhou B, Truman JW, Riddiford LM. 2004. Over- expression of broad: A new insight into its role in the Drosophila prothoracic gland cells. J Exp Biol 207: 1151-1161.