Drosophila as a Model for Diabetes and Diseases of Insulin Resistance

Current Topics in Developmental Biology

Volumn 121, Issue , 2017, Pages 397-419

  Graham, P ^a   Pick, L ^a  

^a NONE

Author keywords

Insulin signaling; Metabolic syndrome; Type 1 diabetes; Type 2 diabetes

Indexed keywords

ANIMAL; CARBOHYDRATE METABOLISM; DIABETES MELLITUS; DISEASE MODEL; DROSOPHILA; GENETICS; HUMAN; INSULIN RESISTANCE; OBESITY; PATHOLOGY; PHYSIOLOGY;

ANIMALS; CARBOHYDRATE METABOLISM; DIABETES MELLITUS; DISEASE MODELS, ANIMAL; DROSOPHILA; HUMANS; INSULIN RESISTANCE; OBESITY;

EID: 84998817203     PISSN: 00702153     EISSN: None     Source Type: Book Series    
DOI: 10.1016/bs.ctdb.2016.07.011     Document Type: Chapter

References (84)

1. Abou-Seif, M.A., Maier, V., Fuchs, J., Mezger, M., Pfeiffer, E.F., Bounias, M., Fluctuations of carbohydrates in haemolymph of honeybee (Apis mellifica) after fasting, feeding and stress. Hormone and Metabolic Research 25:1 (1993), 4–8.
2. Alberti, K.G., Zimmet, P., Shaw, J., IDF Epidemiology Task Force Consensus Group. The metabolic syndrome—A new worldwide definition. Lancet 366:9491 (2005), 1059–1062, 10.1016/S0140-6736(05)67402-8.
3. Alfa, R.W., Kim, S.K., Using Drosophila to discover mechanisms underlying type 2 diabetes. Disease Models & Mechanisms 9:4 (2016), 365–376, 10.1242/dmm.023887.
4. American Diabetes Association. Diagnosis and classification of diabetes mellitus. Diabetes Care 37:Suppl. 1 (2014), 581–590.
5. Arrese, E.L., Soulages, J.L., Insect fat body: Energy, metabolism, and regulation. Annual Review of Entomology 55 (2010), 207–225, 10.1146/annurev-ento-112408-085356.
6. Baker, K.D., Thummel, C.S., Diabetic larvae and obese flies-emerging studies of metabolism in Drosophila. Cell Metabolism 6:4 (2007), 257–266, 10.1016/j.cmet.2007.09.002.
7. Birse, R.T., Choi, J., Reardon, K., Rodriguez, J., Graham, S., Diop, S.,.. Oldham, S., High-fat-diet-induced obesity and heart dysfunction are regulated by the TOR pathway in Drosophila. Cell Metabolism 12:5 (2010), 533–544, 10.1016/j.cmet.2010.09.014.
8. Blatt, J., Roces, F., Haemolymph sugar levels in foraging honeybees (Apis mellifera carnica): Dependence on metabolic rate and in vivo measurement of maximal rates of trehalose synthesis. The Journal of Experimental Biology 204:Pt 15 (2001), 2709–2716.
9. Bodmer, R., Venkatesh, T.V., Heart development in Drosophila and vertebrates: Conservation of molecular mechanisms. Developmental Genetics 22:3 (1998), 181–186, 10.1002/(SICI)1520-6408(1998)22:3<181::AID-DVG1>3.0.CO;2-2.
10. Bonini, N.M., Fortini, M.E., Applications of the Drosophila retina to human disease modeling. Results and Problems in Cell Differentiation 37 (2002), 257–275.
11. Broughton, S.J., Piper, M.D., Ikeya, T., Bass, T.M., Jacobson, J., Driege, Y.,.. Partridge, L., Longer lifespan, altered metabolism, and stress resistance in Drosophila from ablation of cells making insulin-like ligands. Proceedings of the National Academy of Sciences of the United States of America 102:8 (2005), 3105–3110.
12. Candy, D.J., Becker, A., Wegener, G., Coordination and integration of metabolism and insect flight. Comparative Biochemistry and Physiology 117B (1997), 497–512.
13. Centers for Disease Control and Prevention (2016a). http://www.cdc.gov/diabetes.
14. Centers for Disease Control and Prevention (2016b). https://www.searchfordiabetes.org/dspHome.cfm. SEARCH.
15. Colombani, J., Raisin, S., Pantalacci, S., Radimerski, T., Montagne, J., Leopold, P., A nutrient sensor mechanism controls Drosophila growth. Cell 114:6 (2003), 739–749.
16. Crivat, G., Lizunov, V.A., Li, C.R., Stenkula, K.G., Zimmerberg, J., Cushman, S.W., Pick, L., Insulin stimulates translocation of human GLUT4 to the membrane in fat bodies of transgenic Drosophila melanogaster. PloS One, 8(11), 2013, e77953, 10.1371/journal.pone.0077953.
17. Cushman, S.W., Goodyear, L.J., Pilch, P.F., Ralston, E., Galbo, H., Ploug, T.,.. Klip, A., Molecular mechanisms involved in GLUT4 translocation in muscle during insulin and contraction stimulation. Advances in Experimental Medicine and Biology 441 (1998), 63–71.
18. Das, R., Dobens, L.L., Conservation of gene and tissue networks regulating insulin signalling in flies and vertebrates. Biochemical Society Transactions 43:5 (2015), 1057–1062, 10.1042/BST20150078.
19. Dawson, K., Aviles-Hernandez, A., Cushman, S.W., Malide, D., Insulin-regulated trafficking of dual-labeled glucose transporter 4 in primary rat adipose cells. Biochemical and Biophysical Research Communications 287:2 (2001), 445–454, 10.1006/bbrc.2001.5620.
20. Diop, S.B., Bodmer, R., Gaining insights into diabetic cardiomyopathy from Drosophila. Trends in Endocrinology and Metabolism 26:11 (2015), 618–627, 10.1016/j.tem.2015.09.009.
21. Duve, H., Thorpe, A., Lazarus, N.R., Isolation of material displaying insulin-like immunological biological activity from the brain of the blowfly Calliphora vomitoria. The Biochemical Journal 184:2 (1979), 221–227.
22. Duvillie, B., Cordonnier, N., Deltour, L., Dandoy-Dron, F., Itier, J.M., Monthioux, E.,.. Bucchini, D., Phenotypic alterations in insulin-deficient mutant mice. Proceedings of the National Academy of Sciences of the United States of America 94:10 (1997), 5137–5140.
23. Fernandez-Almonacid, R., Rosen, O.M., Structure and ligand specificity of the Drosophila melanogaster insulin receptor. Molecular and Cellular Biology 7 (1987), 2718–2727.
24. Fridell, Y.W., Hoh, M., Kreneisz, O., Hosier, S., Chang, C., Scantling, D.,.. Helfand, S.L., Increased uncoupling protein (UCP) activity in Drosophila insulin-producing neurons attenuates insulin signaling and extends lifespan. Aging (Albany NY) 1:8 (2009), 699–713.
25. Ganetzky, B., Genetic analysis of ion channel dysfunction in Drosophila. Kidney International 57:3 (2000), 766–771, 10.1046/j.1523-1755.2000.00913.x.
26. Garofalo, R.S., Genetic analysis of insulin signaling in Drosophila. Trends in Endocrinology and Metabolism 13:4 (2002), 156–162.
27. Gibson, G., Reed, L.K., Cryptic genetic variation. Current Biology 18:21 (2008), R989–R990, 10.1016/j.cub.2008.08.011.
28. Goberdhan, D.C., Wilson, C., The functions of insulin signaling: Size isn't everything, even in Drosophila. Differentiation 71:7 (2003), 375–397.
29. Gronke, S., Clarke, D.F., Broughton, S., Andrews, T.D., Partridge, L., Molecular evolution and functional characterization of Drosophila insulin-like peptides. PLoS Genetics, 6(2), 2010, e1000857, 10.1371/journal.pgen.1000857.
30. Haselton, A., Sharmin, E., Schrader, J., Sah, M., Poon, P., Fridell, Y.W., Partial ablation of adult Drosophila insulin-producing neurons modulates glucose homeostasis and extends life span without insulin resistance. Cell Cycle 9:15 (2010), 3063–3071, 10.4161/cc.9.15.12458.
31. He, B.Z., Ludwig, M.Z., Dickerson, D.A., Barse, L., Arun, B., Vilhjalmsson, B.J.,.. Kreitman, M., Effect of genetic variation in a Drosophila model of diabetes-associated misfolded human proinsulin. Genetics 196:2 (2014), 557–567, 10.1534/genetics.113.157800.
32. Huang, S., Czech, M.P., The GLUT4 glucose transporter. Cell Metabolism 5:4 (2007), 237–252, 10.1016/j.cmet.2007.03.006.
33. Ikeya, T., Galic, M., Belawat, P., Nairz, K., Hafen, E., Nutrient-dependent expression of insulin-like peptides from neuroendocrine cells in the CNS contributes to growth regulation in Drosophila. Current Biology 12:15 (2002), 1293–1300.
34. Joost, H.G., Thorens, B., The extended GLUT-family of sugar/polyol transport facilitators: Nomenclature, sequence characteristics, and potential function of its novel members (review). Molecular Membrane Biology 18:4 (2001), 247–256.
35. Kahn, B.B., Cushman, S.W., Cell biology of insulin's stimulatory action on glucose transport and its perturbation in altered metabolic states. The Annals of the New York Academy of Sciences 488 (1986), 356–369.
36. Kahn, R.C., King, G.L., Moses, A.C., Weir, G.C., Jacobson, A.M., Smith, R.J., Joslin's diabetes mellitus. 14th ed., 2005, Lippincott Williams & Wilkins, Boston, MA.
37. Kannan, K., Fridell, Y.W., Functional implications of Drosophila insulin-like peptides in metabolism, aging, and dietary restriction. Frontiers in Physiology, 4, 2013, 288, 10.3389/fphys.2013.00288.
38. Kim, S.K., Rulifson, E.J., Conserved mechanisms of glucose sensing and regulation by Drosophila corpora cardiaca cells. Nature 431:7006 (2004), 316–320.
39. 2 + in insulin-producing cells of adult Drosophila. Neuroreport 21:17 (2010), 1116–1120, 10.1097/WNR.0b013e3283409200.
40. Lasko, P., Diabetic flies? Using Drosophila melanogaster to understand the causes of monogenic and genetically complex diseases. Clinical Genetics 62:5 (2002), 358–367.
41. Lebreton, S., Witzgall, P., Olsson, M., Becher, P.G., Dietary glucose regulates yeast consumption in adult Drosophila males. Frontiers in Physiology, 5, 2014, 504, 10.3389/fphys.2014.00504.
42. Lee, G., Park, J.H., Hemolymph sugar homeostasis and starvation-induced hyperactivity affected by genetic manipulations of the adipokinetic hormone-encoding gene in Drosophila melanogaster. Genetics 167:1 (2004), 311–323.
43. LeRoith, D., Lesniak, M.A., Roth, J., Insulin in insects and annelids. Diabetes 30:1 (1981), 70–76.
44. Lizunov, V.A., Matsumoto, H., Zimmerberg, J., Cushman, S.W., Frolov, V.A., Insulin stimulates the halting, tethering, and fusion of mobile GLUT4 vesicles in rat adipose cells. The Journal of Cell Biology 169:3 (2005), 481–489.
45. Lizunov, V.A., Stenkula, K.G., Lisinski, I., Gavrilova, O., Yver, D.R., Chadt, A., Cushman, S.W. Insulin stimulates fusion, but not tethering, of GLUT4 vesicles in skeletal muscle of HA-GLUT4-GFP transgenic mice. American Journal of Physiology. Endocrinology and Metabolism 302:8 (2012), E950–E960, 10.1152/ajpendo.00466.2011.
46. Maurizio, A., Studies on the sugar spectrum of the hemolymph of the honeybee (Apis mellifica L.). I. The blood sugar spectrum of adult bees. Journal of Insect Physiology 11:6 (1965), 745–763.
47. Mueckler, M., Thorens, B., The SLC2 (GLUT) family of membrane transporters. Molecular Aspects of Medicine 34:2-3 (2013), 121–138, 10.1016/j.mam.2012.07.001.
48. Murphy, T.A., Wyatt, G.R., The enzymes of glycogen and trehalose synthesis in silk moth fat body. The Journal of Biological Chemistry 240 (1965), 1500–1508.
49. Musselman, L.P., Fink, J.L., Narzinski, K., Ramachandran, P.V., Hathiramani, S.S., Cagan, R.L., Baranski, T.J., A high-sugar diet produces obesity and insulin resistance in wild-type Drosophila. Disease Models & Mechanisms 4:6 (2011), 842–849, 10.1242/dmm.007948.
50. Musselman, L.P., Fink, J.L., Ramachandran, P.V., Patterson, B.W., Okunade, A.L., Maier, E.,.. Baranski, T.J., Role of fat body lipogenesis in protection against the effects of caloric overload in Drosophila. The Journal of Biological Chemistry 288:12 (2013), 8028–8042, 10.1074/jbc.M112.371047.
51. Na, J., Musselman, L.P., Pendse, J., Baranski, T.J., Bodmer, R., Ocorr, K., Cagan, R., A Drosophila model of high sugar diet-induced cardiomyopathy. PLoS Genetics, 9(1), 2013, e1003175, 10.1371/journal.pgen.1003175.
52. Nassel, D.R., Broeck, J.V., Insulin/IGF signaling in Drosophila and other insects: Factors that regulate production, release and post-release action of the insulin-like peptides. Cellular and Molecular Life Sciences 73:2 (2015), 271–290, 10.1007/s00018-015-2063-3.
53. Nation, J.L., Insect physiology and biochemistry. 2002, CRC Press LLC, Boca Raton.
54. Nishida, Y., Hata, M., Nishizuka, Y., Rutter, W.J., Ebina, Y., Cloning of a Drosophila cDNA encoding a polypeptide similar to the human insulin receptor precursor. Biochemical and Biophysical Research Communications 141 (1986), 474–481.
55. O'Connor, K.J., Baxter, D., The demonstration of insulin-like material in the honey bee, Apis mellifera. Comparative Biochemistry and Physiology 81B (1985), 755–760.
56. Oldham, S., Obesity and nutrient sensing TOR pathway in flies and vertebrates: Functional conservation of genetic mechanisms. Trends in Endocrinology and Metabolism 22:2 (2011), 45–52, 10.1016/j.tem.2010.11.002.
57. Owusu-Ansah, E., Perrimon, N., Modeling metabolic homeostasis and nutrient sensing in Drosophila: Implications for aging and metabolic diseases. Disease Models & Mechanisms 7:3 (2014), 343–350, 10.1242/dmm.012989.
58. Padmanabha, D., Baker, K.D., Drosophila gains traction as a repurposed tool to investigate metabolism. Trends in Endocrinology and Metabolism 25:10 (2014), 518–527, 10.1016/j.tem.2014.03.011.
59. Park, S., Alfa, R.W., Topper, S.M., Kim, G.E., Kockel, L., Kim, S.K., A genetic strategy to measure circulating Drosophila insulin reveals genes regulating insulin production and secretion. PLoS Genetics, 10(8), 2014, e1004555, 10.1371/journal.pgen.1004555.
60. Pasco, M.Y., Leopold, P., High sugar-induced insulin resistance in Drosophila relies on the lipocalin Neural Lazarillo. PloS One, 7(5), 2012, e36583, 10.1371/journal.pone.0036583.
61. Pendse, J., Ramachandran, P.V., Na, J., Narisu, N., Fink, J.L., Cagan, R.L.,.. Baranski, T.J., A Drosophila functional evaluation of candidates from human genome-wide association studies of type 2 diabetes and related metabolic traits identifies tissue-specific roles for dHHEX. BMC Genomics, 14, 2013, 136, 10.1186/1471-2164-14-136.
62. Petruzzelli, L., Herrera, R., Arenas-Garcia, R., Fernandez, R., Birnbaum, M.J., Rosen, O.M., Isolation of a Drosophila genomic sequence homologous to the kinase domain of the human insulin receptor and detection of the phosphorylated Drosophila receptor with an anti-peptide antibody. Proceedings of the National Academy of Sciences of the United States of America 83 (1986), 4710–4714.
63. Petruzzelli, L., Herrera, R., Garcia-Arenas, R., Rosen, O.M., Acquisition of insulin-dependent protein tyrosine kinase activity during Drosophila embryogenesis. The Journal of Biological Chemistry 260 (1986), 16072–16075.
64. Reed, L.K., Lee, K., Zhang, Z., Rashid, L., Poe, A., Hsieh, B.,.. Gibson, G., Systems genomics of metabolic phenotypes in wild-type Drosophila melanogaster. Genetics 197:2 (2014), 781–793, 10.1534/genetics.114.163857.
65. Reed, L.K., Williams, S., Springston, M., Brown, J., Freeman, K., DesRoches, C.E.,.. Gibson, G., Genotype-by-diet interactions drive metabolic phenotype variation in Drosophila melanogaster. Genetics 185:3 (2010), 1009–1019, 10.1534/genetics.109.113571.
66. Rovenko, B.M., Perkhulyn, N.V., Gospodaryov, D.V., Sanz, A., Lushchak, O.V., Lushchak, V.I., High consumption of fructose rather than glucose promotes a diet-induced obese phenotype in Drosophila melanogaster. Comparative Biochemistry and Physiology. Part A, Molecular & Integrative Physiology 180 (2015), 75–85, 10.1016/j.cbpa.2014.11.008.
67. Rulifson, E.J., Kim, S.K., Nusse, R., Ablation of insulin-producing neurons in flies: Growth and diabetic phenotypes. Science 296:5570 (2002), 1118–1120.
68. Rutter, G.A., Pullen, T.J., Hodson, D.J., Martinez-Sanchez, A., Pancreatic beta-cell identity, glucose sensing and the control of insulin secretion. The Biochemical Journal 466:2 (2015), 203–218, 10.1042/BJ20141384.
69. Szendroedi, J., Roden, M., Ectopic lipids and organ function. Current Opinion in Lipidology 20:1 (2009), 50–56.
70. Tager, H.S., Markese, J., Kramer, K.J., Speirs, R.D., Childs, C.N., Glucagon-like and insulin-like hormones of the insect neurosecretory system. The Biochemical Journal 156:3 (1976), 515–520.
71. Taguchi, A., White, M.F., Insulin-like signaling, nutrient homeostasis, and life span. Annual Review of Physiology 70 (2008), 191–212.
72. Tatar, M., The neuroendocrine regulation of Drosophila aging. Experimental Gerontology 39:11-12 (2004), 1745–1750.
73. Teleman, A.A., Molecular mechanisms of metabolic regulation by insulin in Drosophila. The Biochemical Journal 425:1 (2010), 13–26, 10.1042/BJ20091181.
74. Thompson, S.N., Blood sugar formation from dietary carbohydrate is facilitated by the pentose phosphate pathway in an insect Manduca sexta Linnaeus. Biochimica et Biophysica Acta 1472:3 (1999), 565–575.
75. Thompson, S.N., Borchardt, D.B., Wang, L.W., Dietary nutrient levels regulate protein and carbohydrate intake, gluconeogenic/glycolytic flux and blood trehalose level in the insect Manduca sexta L. Journal of Comparative Physiology. B 173:2 (2003), 149–163.
76. Thompson, S.N., Redak, R.A., Interactions of dietary protein and carbohydrate determine blood sugar level and regulate nutrient selection in the insect Manduca sexta L. Biochimica et Biophysica Acta 1523:1 (2000), 91–102.
77. Ugrankar, R., Berglund, E., Akdemir, F., Tran, C., Kim, M.S., Noh, J.,.. Graff, J.M., Drosophila glucome screening identifies Ck1alpha as a regulator of mammalian glucose metabolism. Nature Communications, 6, 2015, 7102, 10.1038/ncomms8102.
78. van Herpen, N.A., Schrauwen-Hinderling, V.B., Lipid accumulation in non-adipose tissue and lipotoxicity. Physiology and Behavior 94:2 (2008), 231–241, 10.1016/j.physbeh.2007.11.049.
79. Wessells, R.J., Fitzgerald, E., Cypser, J.R., Tatar, M., Bodmer, R., Insulin regulation of heart function in aging fruit flies. Nature Genetics 36:12 (2004), 1275–1281.
80. Williams, S., Dew-Budd, K., Davis, K., Anderson, J., Bishop, R., Freeman, K.,.. Reed, L.K., Metabolomic and gene expression profiles exhibit modular genetic and dietary structure linking metabolic syndrome phenotypes in Drosophila. G3 (Bethesda, Md.) 5:12 (2015), 2817–2829, 10.1534/g3.115.023564.
81. Wu, Q., Brown, M.R., Signaling and function of insulin-like peptides in insects. Annual Review of Entomology 51 (2006), 1–24.
82. Wyatt, G.R., Kale, G.F., The chemistry of insect hemolymph. II. Trehalose and other carbohydrates. The Journal of General Physiology 40:6 (1957), 833–847.
83. Yang, Y., Chang, B.H., Chan, L., Sustained expression of the transcription factor GLIS3 is required for normal beta cell function in adults. EMBO Molecular Medicine 5:1 (2013), 92–104, 10.1002/emmm.201201398.
84. Zhang, H., Liu, J., Li, C.R., Momen, B., Kohanski, R.A., Pick, L., Deletion of Drosophila insulin-like peptides causes growth defects and metabolic abnormalities. Proceedings of the National Academy of Sciences of the United States of America 106:46 (2009), 19617–19622.