The Drosophila ortholog of TMEM18 regulates insulin and glucagon-like signaling

Journal of Endocrinology

Volumn 229, Issue 3, 2016, Pages 233-243

  Wiemerslage, Lyle ^a   Gohel, Priya A ^a   Maestri, Giulia ^a   Hilmarsson, Torfi G ^a   Mickael, Michel ^a   Fredriksson, Robert ^a   Williams, Michael J ^a   Schiöth, Helgi B ^a  

^a UPPSALA UNIVERSITY   (Sweden)

Author keywords

AKH; CG30051; Drosophila; Fly; Glucagon; Insulin; Obesity; SNP; TMEM18

Indexed keywords

GLUCAGON; INSULIN; SUGAR; TRIACYLGLYCEROL; DROSOPHILA PROTEIN; MEMBRANE PROTEIN; TMEM18 PROTEIN, HUMAN;

ADIPOCYTE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CLINICAL ASSESSMENT; DOWN REGULATION; DROSOPHILA MELANOGASTER; GENE; GENE EXPRESSION; GENE SILENCING; GLUCOSE BLOOD LEVEL; HOMEOSTATIC MODEL ASSESSMENT BETA; METABOLIC SYNDROME X; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OBESITY; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SINGLE NUCLEOTIDE POLYMORPHISM; TRANSMEMBRANE PROTEIN 18 GENE; ANIMAL; BIOLOGICAL MODEL; FAT PAD; GENETICS; HUMAN; LARVA; METABOLISM; SPECIES DIFFERENCE; TRANSGENIC ANIMAL;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FAT BODY; GENE KNOCKDOWN TECHNIQUES; GENES, INSECT; GLUCAGON; HUMANS; INSULIN; LARVA; MEMBRANE PROTEINS; MODELS, BIOLOGICAL; OBESITY; POLYMORPHISM, SINGLE NUCLEOTIDE; SIGNAL TRANSDUCTION; SPECIES SPECIFICITY;

EID: 84977640687     PISSN: 00220795     EISSN: 14796805     Source Type: Journal    
DOI: 10.1530/JOE-16-0040     Document Type: Article

References (47)

1. Almen MS, Jacobsson JA, Shaik JH, Olszewski PK, Cedernaes J, Alsio J, Sreedharan S, Levine AS, Fredriksson R, Marcus C, et al. 2010 The obesity gene, TMEM18, is of ancient origin, found in majority of neuronal cells in all major brain regions and associated with obesity in severely obese children. BMC Medical Genetics 11 58.
2. Altschul SF, Gish W, Miller W, Myers EW & Lipman DJ 1990 Basic local alignment search tool. Journal of Molecular Biology 215 403-410. (doi:10.1016/S0022-2836(05)80360-2)
3. Barness LA, Opitz JM & Gilbert-Barness E 2007 Obesity: genetic, molecular, and environmental aspects. American Journal of Medical Genetics A 143A 3016-3034. (doi:10.1002/ajmg.a.32035)
4. Bharucha KN, Tarr P & Zipursky SL 2008 A glucagon-like endocrine pathway in Drosophila modulates both lipid and carbohydrate homeostasis. Journal of Experimental Biology 211 3103-3110. (doi:10.1242/jeb.016451)
5. Boyle AP, Hong EL, Hariharan M, Cheng Y, Schaub MA, Kasowski M, Karczewski KJ, Park J, Hitz BC, Weng S, et al. 2012 Annotation of functional variation in personal genomes using RegulomeDB. Genome Research 22 1790-1797. (doi:10.1101/gr.137323.112)
6. Braco JT, Gillespie EL, Alberto GE, Brenman JE & Johnson EC 2012 Energy-dependent modulation of glucagon-like signaling in Drosophila via the AMP-activated protein kinase. Genetics 192 457-466. (doi:10.1534/genetics.112.143610)
7. Brand AH & Perrimon N 1993 Targeted gene-expression as a means of altering cell fates and generating dominant phenotypes. Development 118 401-415.
8. Britton JS, Lockwood WK, Li L, Cohen SM & Edgar BA 2002 Drosophila's insulin/PI3-kinase pathway coordinates cellular metabolism with nutritional conditions. Developmental Cell 2 239-249. (doi:10.1016/S1534-5807(02)00117-X)
9. Broughton SJ, Piper MD, Ikeya T, Bass TM, Jacobson J, Driege Y, Martinez P, Hafen E, Withers DJ, Leevers SJ, et al. 2005 Longer lifespan, altered metabolism, and stress resistance in Drosophila from ablation of cells making insulin-like ligands. PNAS 102 3105-3110. (doi:10.1073/pnas.0405775102)
10. Buch S, Melcher C, Bauer M, Katzenberger J & Pankratz MJ 2008 Opposing effects of dietary protein and sugar regulate a transcriptional target of Drosophila insulin-like peptide signaling. Cell Metabolism 7 321-332. (doi:10.1016/j.cmet.2008.02.012)
11. Calle EE, Rodriguez C, Walker-Thurmond K & Thun MJ 2003 Overweight, obesity, and mortality from cancer in a prospectively studied cohort of U.S. adults. New England Journal of Medicine 348 1625-1638.
12. Cao J, Ni J, Ma W, Shiu V, Milla LA, Park S, Spletter ML, Tang S, Zhang J, Wei X, et al. 2014 Insight into insulin secretion from transcriptome and genetic analysis of insulin-producing cells of Drosophila. Genetics 197 175-192. (doi:10.1534/genetics.113.160663)
13. Chatterjee D, Katewa SD, Qi Y, Jackson SA, Kapahi P & Jasper H 2014 Control of metabolic adaptation to fasting by dILP6-induced insulin signaling in Drosophila oenocytes. PNAS 111 17959-17964. (doi:10.1073/pnas.1409241111)
14. Deveci M, Catalyurek UV & Toland AE 2014 mrSNP: software to detect SNP effects on microRNA binding. BMC Bioinformatics 15 73. (doi:10.1186/1471-2105-15-73)
15. Dupuis J, Langenberg C, Prokopenko I, Saxena R, Soranzo N, Jackson AU, Wheeler E, Glazer NL, Bouatia-Naji N, Gloyn AL et al. 2010 New genetic loci implicated in fasting glucose homeostasis and their impact on type 2 diabetes risk. Nature Genetics 42 105-116.
16. Haslam DW & James WP 2005 Obesity. Lancet 366 1197-1209. (doi:10.1016/S0140-6736(05)67483-1)
17. 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. Current Biology 12 1293-1300. (doi:10.1016/S0960-9822(02)01043-6)
18. Ja WW, Carvalho GB, Mak EM, de la Rosa NN, Fang AY, Liong JC, Brummel T & Benzer S 2007 Prandiology of Drosophila and the CAFE assay. PNAS 104 8253-8256. (doi:10.1073/pnas.0702726104)
19. Jurvansuu JM & Goldman A 2011 Obesity risk gene TMEM18 encodes a sequence-specific DNA-binding protein. PLoS ONE 6 e25317.
20. Jurvansuu J, Zhao Y, Leung DS, Boulaire J, Yu YH, Ahmed S & Wang S 2008 Transmembrane protein 18 enhances the tropism of neural stem cells for glioma cells. Cancer Research 68 4614-4622. (doi:10.1158/0008-5472.CAN-07-5291)
21. Kalnina I, Zaharenko L, Vaivade I, Rovite V, Nikitina-Zake L, Peculis R, Fridmanis D, Geldnere K, Jacobsson JA, Almen MS, et al. 2013 Polymorphisms in FTO and near TMEM18 associate with type 2 diabetes and predispose to younger age at diagnosis of diabetes. Gene 527 462-468. (doi:10.1016/j.gene.2013.06.079)
22. Kannan K & Fridell YW 2013 Functional implications of Drosophila insulin-like peptides in metabolism, aging, and dietary restriction. Frontiers in Physiology 4 288.
23. Kim SK & Rulifson EJ 2004 Conserved mechanisms of glucose sensing and regulation by Drosophila corpora cardiaca cells. Nature 431 316-320. (doi:10.1038/nature02897)
24. Lee G & Park JH 2004 Hemolymph sugar homeostasis and starvationinduced hyperactivity affected by genetic manipulations of the adipokinetic hormone-encoding gene in Drosophila melanogaster. Genetics 167 311-323. (doi:10.1534/genetics.167.1.311)
25. Manning AK, Hivert MF, Scott RA, Grimsby JL, Bouatia-Naji N, Chen H, Rybin D, Liu CT, Bielak LF, Prokopenko I, et al. 2012 A genome-wide approach accounting for body mass index identifies genetic variants influencing fasting glycemic traits and insulin resistance. Nature Genetics 44 659-669.
26. Matsuda H, Yamada T, Yoshida M & Nishimura T 2015 Flies without trehalose. Journal of Biological Chemistry 290 1244-1255. (doi:10.1074/jbc.M114.619411)
27. Nassel DR, Kubrak OI, Liu Y, Luo J & Lushchak OV 2013 Factors that regulate insulin producing cells and their output in Drosophila. Frontiers in Physiology 4 252.
28. Rask-Andersen M, Jacobsson JA, Moschonis G, Chavan RA, Sikder MA, Allzen E, Alsio J, Chrousos GP, Manios Y, Fredriksson R, et al. 2012 Association of TMEM18 variants with BMI and waist circumference in children and correlation of mRNA expression in the PFC with body weight in rats. European Journal of Human Genetics 20 192-197. (doi:10.1038/ejhg.2011.176)
29. Robinson SW, Herzyk P, Dow JAT & Leader DP 2013 FlyAtlas: database of gene expression in the tissues of Drosophila melanogaster. Nucleic Acids Research 41 D744-D750.
30. Rohde K, Keller M, Klos M, Schleinitz D, Dietrich A, Schon MR, Gartner D, Lohmann T, Dressler M, Stumvoll M, et al. 2014 Adipose tissue depot specific promoter methylation of TMEM18. Journal of Molecular Medicine 92 881-888. (doi:10.1007/s00109-014-1154-1)
31. Rosenbloom KR, Dreszer TR, Long JC, Malladi VS, Sloan CA, Raney BJ, Cline MS, Karolchik D, Barber GP, Clawson H, et al. 2012 ENCODE whole-genome data in the UCSC Genome Browser: update 2012. Nucleic Acids Research 40 D912-D917.
32. Rosenbloom KR, Sloan CA, Malladi VS, Dreszer TR, Learned K, Kirkup VM, Wong MC, Maddren M, Fang R, Heitner SG, et al. 2013 ENCODE data in the UCSC Genome Browser: year 5 update. Nucleic Acids Research 41 D56-D63.
33. Rulifson EJ, Kim SK & Nusse R 2002 Ablation of insulin-producing neurons in flies: growth and diabetic phenotypes. Science 296 1118-1120. (doi:10.1126/science.1070058)
34. Slack C, Werz C, Wieser D, Alic N, Foley A, Stocker H, Withers DJ, Thornton JM, Hafen E & Partridge L 2010 Regulation of lifespan, metabolism, and stress responses by the Drosophila SH2B protein, Lnk. PLoS Genetics 6 e1000881.
35. Soranzo N, Sanna S, Wheeler E, Gieger C, Radke D, Dupuis J, Bouatia-Naji N, Langenberg C, Prokopenko I, Stolerman E, et al. 2010 Common variants at 10 genomic loci influence hemoglobin A(1)(C) levels via glycemic and nonglycemic pathways. Diabetes 59 3229-3239.
36. Speliotes EK, Willer CJ, Berndt SI, Monda KL, Thorleifsson G, Jackson AU, Lango Allen H, Lindgren CM, Luan J, Magi R, et al. 2010 Association analyses of 249,796 individuals reveal 18 new loci associated with body mass index. Nature Genetics 42 937-948.
37. Tennessen JM, Baker KD, Lam G, Evans J & Thummel CS 2011 The Drosophila estrogen-related receptor directs a metabolic switch that supports developmental growth. Cell Metabolism 13 139-148. (doi:10.1016/j.cmet.2011.01.005)
38. Teslovich TM, Musunuru K, Smith AV, Edmondson AC, Stylianou IM, Koseki M, Pirruccello JP, Ripatti S, Chasman DI, Willer CJ, et al. 2010 Biological, clinical and population relevance of 95 loci for blood lipids. Nature 466 707-713.
39. Thorleifsson G, Walters GB, Gudbjartsson DF, Steinthorsdottir V, Sulem P, Helgadottir A, Styrkarsdottir U, Gretarsdottir S, Thorlacius S, Jonsdottir I, et al. 2009 Genome-wide association yields new sequence variants at seven loci that associate with measures of obesity. Nature Genetics 41 18-24. (doi:10.1038/ng.274)
40. Uhlen M, Oksvold P, Fagerberg L, Lundberg E, Jonasson K, Forsberg M, Zwahlen M, Kampf C, Wester K, Hober S, et al. 2010 Towards a knowledge-based Human Protein Atlas. Nature Biotechnology 28 1248-1250. (doi:10.1038/nbt1210-1248)
41. Uhlén M, Fagerberg L, Hallström BM, Lindskog C, Oksvold P, Mardinoglu A, Sivertsson Å, Kampf C, Sjöstedt E, Asplund A, et al. 2015 Tissue-based map of the human proteome. Science 347 1260419.
42. Wang S, Tulina N, Carlin DL & Rulifson EJ 2007 The origin of islet-like cells in Drosophila identifies parallels to the vertebrate endocrine axis. PNAS 104 19873-19878. (doi:10.1073/pnas.0707465104)
43. Willer CJ, Speliotes EK, Loos RJ, Li S, Lindgren CM, Heid IM, Berndt SI, Elliott AL, Jackson AU, Lamina C, et al. 2009 Six new loci associated with body mass index highlight a neuronal influence on body weight regulation. Nature Genetics 41 25-34.
44. Williams MJ, Almen MS, Fredriksson R & Schioth HB 2012 What model organisms and interactomics can reveal about the genetics of human obesity. Cellular and Molecular Life Sciences 69 3819-3834. (doi:10.1007/s00018-012-1022-5)
45. Williams MJ, Goergen P, Rajendran J, Klockars A, Kasagiannis A, Fredriksson R & Schioth HB 2014a Regulation of aggression by obesity-linked genes TfAP-2 and Twz through octopamine signaling in Drosophila. Genetics 196 349-362.
46. Williams MJ, Wang Y, Klockars A, Monica Lind P, Fredriksson R & Schioth HB 2014b Exposure to bisphenol A affects lipid metabolism in Drosophila melanogaster. Basic & Clinical Pharmacology & Toxicology 114 414-420.
47. Winter D, Vinegar B, Nahal H, Ammar R, Wilson GV & Provart NJ 2007 An "Electronic Fluorescent Pictograph" browser for exploring and analyzing large-scale biological data sets. PLoS ONE 2 e718.