Modeling obesity and its associated disorders in Drosophila

Physiology

Volumn 28, Issue 2, 2013, Pages 117-124

  Trinh, Irene ^a   Boulianne, Gabrielle L ^a  

^a HOSPITAL FOR SICK CHILDREN   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL; DISEASE PREDISPOSITION; DROSOPHILA; ENVIRONMENT; GENETIC PREDISPOSITION; GENETICS; GENOTYPE ENVIRONMENT INTERACTION; HUMAN; OBESITY; PATHOPHYSIOLOGY; PHYSIOLOGY; REVIEW;

ANIMALS; DISEASE SUSCEPTIBILITY; DROSOPHILA; ENVIRONMENT; GENE-ENVIRONMENT INTERACTION; GENETIC PREDISPOSITION TO DISEASE; HUMANS; OBESITY;

EID: 84874586591     PISSN: 15489213     EISSN: 15489221     Source Type: Journal    
DOI: 10.1152/physiol.00025.2012     Document Type: Review

References (75)

1. Al-Anzi B, Sapin V, Waters C, Zinn K, Wyman RJ, Benzer S. Obesity-blocking neurons in Drosophila. Neuron 63: 329-341, 2009.
2. Ayroles JF, Carbone MA, Stone EA, Jordan KW, Lyman RF, Magwire MM, Rollmann SM, Duncan LH, Lawrence F, Anholt RR, Mackay TF. Systems genetics of complex traits in Drosophila melanogaster. Nat Genet 41: 299-307, 2009.
3. Baker KD, Thummel CS. Diabetic larvae and obese flies-emerging studies of metabolism in Drosophila. Cell Metab 6: 257-266, 2007.
4. Bharucha KN. The epicurean fly: using Drosophila melanogaster to study metabolism. Pediatr Res 65: 132-137, 2009.
5. Birse RT, Choi J, Reardon K, Rodriguez J, Graham S, Diop S, Ocorr K, Bodmer R, Oldham S. High-fat-diet-induced obesity and heart dysfunction are regulated by the TOR pathway in Drosophila. Cell Metab 12: 533-544, 2010.
6. Birse RT, Soderberg JA, Luo J, Winther AM, Nassel DR. Regulation of insulin-producing cells in the adult Drosophila brain via the tachykinin peptide receptor DTKR. J Exp Biol 214: 4201-4208, 2011.
7. Bogardus C. Missing heritability and GWAS utility. Obesity (Silver Spring) 17: 209-210, 2009.
8. Bouchard C. Current understanding of the etiology of obesity: genetic and nongenetic factors. Am J Clin Nutr 53: 1561S-1565S, 1991.
9. Britton JS, Edgar BA. Environmental control of the cell cycle in Drosophila: nutrition activates mitotic and endoreplicative cells by distinct mechanisms. Development 125: 2149-2158, 1998.
10. Broughton SJ, Piper MD, Ikeya T, Bass TM, Jacobson J, Driege Y, Martinez P, Hafen E, Withers DJ, Leevers SJ, Partridge L. Longer lifespan, altered metabolism, and stress resistance in Drosophila from ablation of cells making insulin-like ligands. Proc Natl Acad Sci USA 102: 3105-3110, 2005.
11. Buch S, Melcher C, Bauer M, Katzenberger J, Pankratz MJ. Opposing effects of dietary protein and sugar regulate a transcriptional target of Drosophila insulin-like peptide signaling. Cell Metab 7: 321-332, 2008.
12. Canavoso LE, Jouni ZE, Karnas KJ, Pennington JE, Wells MA. Fat metabolism in insects. Annu Rev Nutr 21: 23-46, 2001.
13. Cao C, Brown MR. Localization of an insulin-like peptide in brains of two flies. Cell Tissue Res 304: 317-321, 2001.
14. Carmelli D, Cardon LR, Fabsitz R. Clustering of hypertension, diabetes, and obesity in adult male twins: same genes or same environments? Am J Hum Genet 55: 566-573, 1994.
15. Chow WH, Gridley G, Fraumeni JF Jr, Jarvholm B. Obesity, hypertension, and the risk of kidney cancer in men. N Engl J Med 343: 1305-1311, 2000.
16. Cognigni P, Bailey AP, Miguel-Aliaga I. Enteric neurons and systemic signals couple nutritional and reproductive status with intestinal homeostasis. Cell Metab 13: 92-104, 2011.
17. Colombani J, Raisin S, Pantalacci S, Radimerski T, Montagne J, Leopold P. A nutrient sensor mechanism controls Drosophila growth. Cell 114: 739-749, 2003.
18. Dantuma NP, Potters M, De Winther MP, Tensen CP, Kooiman FP, Bogerd J, Van der Horst DJ. An insect homolog of the vertebrate very low density lipoprotein receptor mediates endocytosis of lipophorins. J Lipid Res 40: 973-978, 1999.
19. Day FR, Loos RJ. Developments in obesity genetics in the era of genome-wide association studies. J Nutrigenet Nutrigenomics 4: 222-238, 2011.
20. Eckel RH, Grundy SM, Zimmet PZ. The metabolic syndrome. Lancet 365: 1415-1428, 2005.
21. Farooqi IS, O'Rahilly S. Monogenic human obesity syndromes. Recent Prog Horm Res 59: 409-424, 2004.
22. Farooqi IS, O'Rahilly S. Monogenic obesity in humans. Annu Rev Med 56: 443-458, 2005.
23. Frayling TM, Timpson NJ, Weedon MN, Zeggini E, Freathy RM, Lindgren CM, Perry JR, Elliott KS, Lango H, Rayner NW, Shields B, Harries LW, Barrett JC, Ellard S, Groves CJ, Knight B, Patch AM, Ness AR, Ebrahim S, Lawlor DA, Ring SM, Ben-Shlomo Y, Jarvelin MR, Sovio U, Bennett AJ, Melzer D, Ferrucci L, Loos RJ, Barroso I, Wareham NJ, Karpe F, Owen KR, Cardon LR, Walker M, Hitman GA, Palmer CN, Doney AS, Morris AD, Smith GD, Hattersley AT, McCarthy MI. A common variant in the FTO gene is associated with body mass index and predisposes to childhood and adult obesity. Science 316: 889-894, 2007.
24. Geminard C, Rulifson EJ, Leopold P. Remote control of insulin secretion by fat cells in Drosophila. Cell Metab 10: 199-207, 2009.
25. Gibbons GF, Islam K, Pease RJ. Mobilisation of triacylglycerol stores. Biochim Biophys Acta 1483: 37-57, 2000.
26. Gutierrez E, Wiggins D, Fielding B, Gould AP. Specialized hepatocyte-like cells regulate Drosophila lipid metabolism. Nature 445: 275-280, 2007.
27. Haselton AT, Fridell YW. Adult Drosophila melanogaster as a model for the study of glucose homeostasis. Aging (Milano) 2: 523-526, 2010.
28. Hong SH, Lee KS, Kwak SJ, Kim AK, Bai H, Jung MS, Kwon OY, Song WJ, Tatar M, Yu K. Minibrain/Dyrk1a regulates food intake through the Sir2-FOXO-sNPF/NPY pathway in Drosophila and mammals. PLoS Genet 8: e1002857, 2012.
29. Horvath TL, Diano S. The floating blueprint of hypothalamic feeding circuits. Nat Rev Neurosci 5: 662-667, 2004.
30. Ichihara S, Yamada Y. Genetic factors for human obesity. Cell Mol Life Sci 65: 1086-1098, 2008.
31. Kapan N, Lushchak OV, Luo J, Nassel DR. Identified peptidergic neurons in the Drosophilabrain regulate insulin-producing cells, stress responses and metabolism by coexpressed short neuropeptide F and corazonin. Cell Mol Life Sci. In press.
32. Kenchaiah S, Evans JC, Levy D, Wilson PW, Benjamin EJ, Larson MG, Kannel WB, Vasan RS. Obesity and the risk of heart failure. N Engl J Med 347: 305-313, 2002.
33. Kleinridders A, Konner AC, Bruning JC. CNS-targets in control of energy and glucose homeostasis. Curr Opin Pharmacol 9: 794-804, 2009.
34. Kopelman PG. Obesity as a medical problem. Nature 404: 635-643, 2000.
35. Kuhnlein RP. The contribution of the Drosophila model to lipid droplet research. Prog Lipid Res 50: 348-356, 2011.
36. Kuhnlein RP. Energy homeostasis regulation in Drosophila: a lipocentric perspective. Results Probl Cell Differ 52: 159-173, 2010.
37. Kuhnlein RP. Thematic review series: Lipid drop-let synthesis and metabolism: from yeast to man. Lipid droplet-based storage fat metabolism in Drosophila. J Lipid Res 53: 1430-1436, 2012.
38. Lee CH, Olson P, Evans RM. Minireview: Lipid metabolism, metabolic diseases, and peroxisome proliferator-activated receptors. Endocrinology 144: 2201-2207, 2003.
39. Lee KS, Kwon OY, Lee JH, Kwon K, Min KJ, Jung SA, Kim AK, You KH, Tatar M, Yu K. Drosophila short neuropeptide F signalling regulates growth by ERK-mediated insulin signalling. Nat Cell Biol 10: 468-475, 2008.
40. Lee KT, Byun MJ, Kang KS, Park EW, Lee SH, Cho S, Kim H, Kim KW, Lee T, Park JE, Park W, Shin D, Park HS, Jeon JT, Choi BH, Jang GW, Choi SH, Kim DW, Lim D, Park MR, Ott J, Schook LB, Kim TH. Neuronal genes for subcutaneous fat thickness in human and pig are identified by local genomic sequencing and combined SNP association study. PLos One 6: e16356, 2011.
41. Li S, Loos RJ. Progress in the genetics of common obesity: size matters. Curr Opin Lipidol 19: 113-121, 2008.
42. Lim HY, Wang W, Wessells RJ, Ocorr K, Bodmer R. Phospholipid homeostasis regulates lipid metabolism and cardiac function through SREBP signaling in Drosophila. Genes Dev 25: 189-200, 2011.
43. Luo J, Becnel J, Nichols CD, Nassel DR. Insulin-producing cells in the brain of adult Drosophila are regulated by the serotonin 5-HT1A receptor. Cell Mol Life Sci 69: 471-484, 2012.
44. Mackay TF, Richards S, Stone EA, Barbadilla A, Ayroles JF, Zhu D, Casillas S, Han Y, Magwire MM, Cridland JM, Richardson MF, Anholt RR, Barron M, Bess C, Blankenburg KP, Carbone MA, Castellano D, Chaboub L, Duncan L, Harris Z, Javaid M, Jayaseelan JC, Jhangiani SN, Jordan KW, Lara F, Lawrence F, Lee SL, Librado P, Linheiro RS, Lyman RF, Mackey AJ, Munidasa M, Muzny DM, Nazareth L, Newsham I, Perales L, Pu LL, Qu C, Ramia M, Reid JG, Rollmann SM, Rozas J, Saada N, Turlapati L, Worley KC, Wu YQ, Yamamoto A, Zhu Y, Bergman CM, Thornton KR, Mittelman D, Gibbs RA. The Drosophila melanogaster Genetic Reference Panel. Nature 482: 173-178, 2012.
45. Matthews KA, Kaufman TC, Gelbart WM. Research resources for Drosophila: the expanding universe. Nat Rev Genet 6: 179-193, 2005.
46. Melcher C, Bader R, Pankratz MJ. Amino acids, taste circuits, and feeding behavior in Drosophila: towards understanding the psychology of feeding in flies and man. J Endocrinol 192: 467-472, 2007.
47. Melcher C, Pankratz MJ. Candidate gustatory interneurons modulating feeding behavior in the Drosophila brain. PLoS Biol 3: e305, 2005.
48. Murphy DJ. The dynamic roles of intracellular lipid droplets: from archaea to mammals. Protoplasma 249: 541-585, 2011.
49. Musselman LP, Fink JL, Narzinski K, Ramachandran PV, Hathiramani SS, Cagan RL, Baranski TJ. A high-sugar diet produces obesity and insulin resistance in wild-type Drosophila. Dis Model Mech 4: 842-849, 2011.
50. Pasco MY, Leopold P. High sugar-induced insulin resistance in Drosophila relies on the lipocalin Neural Lazarillo. PLos One 7: e36583, 2012.
51. Pennington JE, Nussenzveig RH, Van Heusden MC. Lipid transfer from insect fat body to lipophorin: comparison between a mosquito triacylglycerol-rich lipophorin and a sphinx moth diacylglycerol-rich lipophorin. J Lipid Res 37: 1144-1152, 1996.
52. Perusse L, Rankinen T, Zuberi A, Chagnon YC, Weisnagel SJ, Argyropoulos G, Walts B, Snyder EE, Bouchard C. The human obesity gene map: the 2004 update. Obes Res 13: 381-490, 2005.
53. Pospisilik JA, Schramek D, Schnidar H, Cronin SJ, Nehme NT, Zhang X, Knauf C, Cani PD, Aumayr K, Todoric J, Bayer M, Haschemi A, Puviindran V, Tar K, Orthofer M, Neely GG, Dietzl G, Manoukian A, Funovics M, Prager G, Wagner O, Ferrandon D, Aberger F, Hui CC, Esterbauer H, Penninger JM. Drosophila genome-wide obesity screen reveals hedgehog as a determinant of brown versus white adipose cell fate. Cell 140: 148-160, 2010.
54. Rajan A, Perrimon N. Drosophila cytokine unpaired 2 regulates physiological homeostasis by remotely controlling insulin secretion. Cell 151: 123-137, 2012.
55. Rankinen T, Zuberi A, Chagnon YC, Weisnagel SJ, Argyropoulos G, Walts B, Perusse L, Bouchard C. The human obesity gene map: the 2005 update. Obesity (Silver Spring) 14: 529-644, 2006.
56. Reiter LT, Potocki L, Chien S, Gribskov M, Bier E. A systematic analysis of human disease-associated gene sequences in Drosophila melanogaster. Genome Res 11: 1114-1125, 2001.
57. Ribeiro C, Dickson BJ. Sex peptide receptor and neuronal TOR/S6K signaling modulate nutrient balancing in Drosophila. Curr Biol 20: 1000-1005, 2010.
58. Rulifson EJ, Kim SK, Nusse R. Ablation of insulin-producing neurons in flies: growth and diabetic phenotypes. Science 296: 1118-1120, 2002.
59. Sanchez-Lasheras C, Konner AC, Bruning JC. Integrative neurobiology of energy homeostasis-neurocircuits, signals and mediators. Front Neuroendocrinol 31: 4-15, 2010.
60. Schultz JR, Tu H, Luk A, Repa JJ, Medina JC, Li L, Schwendner S, Wang S, Thoolen M, Mangelsdorf DJ, Lustig KD, Shan B. Role of LXRs in control of lipogenesis. Genes Dev 14: 2831-2838, 2000.
61. Scuteri A, Sanna S, Chen WM, Uda M, Albai G, Strait J, Najjar S, Nagaraja R, Orru M, Usala G, Dei M, Lai S, Maschio A, Busonero F, Mulas A, Ehret GB, Fink AA, Weder AB, Cooper RS, Galan P, Chakravarti A, Schlessinger D, Cao A, Lakatta E, Abecasis GR. Genome-wide association scan shows genetic variants in the FTO gene are associated with obesity-related traits. PLoS Genet 3: e115, 2007.
62. Seeley RJ, Woods SC. Monitoring of stored and available fuel by the CNS: implications for obesity. Nat Rev Neurosci 4: 901-909, 2003.
63. Sieber MH, Thummel CS. The DHR96 nuclear receptor controls triacylglycerol homeostasis in Drosophila. Cell Metab 10: 481-490, 2009.
64. Soderberg JA, Carlsson MA, Nassel DR. Insulin-producing cells in the drosophila brain also express satiety-inducing cholecystokinin-like peptide, drosulfakinin. Front Endocrinol (Lausanne) 3: 109, 2012.
65. Stein CJ, Colditz GA. The epidemic of obesity. J Clin Endocrinol Metab 89: 2522-2525, 2004.
66. Teleman AA. Molecular mechanisms of metabolic regulation by insulin in Drosophila. Biochem J 425: 13-26, 2010.
67. Thorleifsson G, Walters GB, Gudbjartsson DF, Steinthorsdottir V, Sulem P, Helgadottir A, Styrkarsdottir U, Gretarsdottir S, Thorlacius S, Jonsdottir I, Jonsdottir T, Olafsdottir EJ, Olafsdottir GH, Jonsson T, Jonsson F, Borch-Johnsen K, Hansen T, Andersen G, Jorgensen T, Lauritzen T, Aben KK, Verbeek AL, Roeleveld N, Kampman E, Yanek LR, Becker LC, Tryggvadottir L, Rafnar T, Becker DM, Gulcher J, Kiemeney LA, Pedersen O, Kong A, Thorsteinsdottir U, Stefansson K. Genome-wide association yields new sequence variants at seven loci that associate with measures of obesity. Nat Genet 41: 18-24, 2009.
68. Thorne N, Amrein H. Atypical expression of Drosophila gustatory receptor genes in sensory and central neurons. J Comp Neurol 506: 548-568, 2008.
69. Wajchenberg BL. Subcutaneous and visceral adipose tissue: their relation to the metabolic syndrome. Endocr Rev 21: 697-738, 2000.
70. Wang MC, Bohmann D, Jasper H. JNK extends life span and limits growth by antagonizing cellular and organism-wide responses to insulin signaling. Cell 121: 115-125, 2005.
71. Weiss R, Dziura J, Burgert TS, Tamborlane WV, Taksali SE, Yeckel CW, Allen K, Lopes M, Savoye M, Morrison J, Sherwin RS, Caprio S. Obesity and the metabolic syndrome in children and adolescents. N Engl J Med 350: 2362-2374, 2004.
72. WHO. Obesity and Overweight: World Health Organization, 2006. World Health Organization, 2006.
73. Willer CJ, Speliotes EK, Loos RJ, Li S, Lindgren CM, Heid IM, Berndt SI, Elliott AL, Jackson AU, Lamina C, Lettre G, Lim N, Lyon HN, McCarroll SA, Papadakis K, Qi L, Randall JC, Roccasecca RM, Sanna S, Scheet P, Weedon MN, Wheeler E, Zhao JH, Jacobs LC, Prokopenko I, Soranzo N, Tanaka T, Timpson NJ, Almgren P, Bennett A, Bergman RN, Bingham SA, Bonnycastle LL, Brown M, Burtt NP, Chines P, Coin L, Collins FS, Connell JM, Cooper C, Smith GD, Dennison EM, Deodhar P, Elliott P, Erdos MR, Estrada K, Evans DM, Gianniny L, Gieger C, Gillson CJ, Guiducci C, Hackett R, Hadley D, Hall AS, Havulinna AS, Hebebrand J, Hofman A, Isomaa B, Jacobs KB, Johnson T, Jousilahti P, Jovanovic Z, Khaw KT, Kraft P, Kuokkanen M, Kuusisto J, Laitinen J, Lakatta EG, Luan J, Luben RN, Mangino M, McArdle WL, Meitinger T, Mulas A, Munroe PB, Narisu N, Ness AR, Northstone K, O'Rahilly S, Purmann C, Rees MG, Ridderstrale M, Ring SM, Rivadeneira F, Ruokonen A, Sandhu MS, Saramies J, Scott LJ, Scuteri A, Silander K, Sims MA, Song K, Stephens J, Stevens S, Stringham HM, Tung YC, Valle TT, Van Duijn CM, Vimaleswaran KS, Vollenweider P, et al. Six new loci associatedwith body mass index highlight a neuronal influence on body weight regulation. Nat Genet 41: 25-34, 2009.
74. Wu Q, Zhang Y, Xu J, Shen P. Regulation of hunger-driven behaviors by neural ribosomal S6 kinase in Drosophila. Proc Natl Acad Sci USA 102: 13289-13294, 2005.
75. Yu Y, Sun Y, He S, Yan C, Rui L, Li W, Liu Y. Neuronal Cbl controls biosynthesis of insulin-like peptides in Drosophila melanogaster. Mol Cell Biol 32: 3610-3623, 2012.