The transcription factor Cabut coordinates energy metabolism and the circadian clock in response to sugar sensing

EMBO Journal

Volumn 34, Issue 11, 2015, Pages 1538-1553

  Bartok, Osnat ^a   Teesalu, Mari ^b,c   Ashwall Fluss, Reut ^a   Pandey, Varun ^a   Hanan, Mor ^a   Rovenko, Bohdana M ^b,c   Poukkula, Minna ^c   Havula, Essi ^b,c   Moussaieff, Arieh ^a   Vodala, Sadanand ^d   Nahmias, Yaakov ^a   Kadener, Sebastian ^a   Hietakangas, Ville ^b,c  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^b UNIVERSITY OF HELSINKI   (Finland)

^c UNIVERSITY OF HELSINKI   (Finland)

^d BRANDEIS UNIVERSITY   (United States)

Author keywords

cabut; circadian; metabolism; nutrient sensing; transcription

Indexed keywords

GLUCOSE; GLYCEROL; INSECT PROTEIN; PHOSPHOENOLPYRUVATE CARBOXYKINASE (GTP); TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR CABUT; UNCLASSIFIED DRUG; CABUT PROTEIN, DROSOPHILA; DROSOPHILA PROTEIN; PHOSPHOENOLPYRUVATE CARBOXYKINASE (ATP); TRANSCRIPTOME;

ADULT; ARTICLE; CARBON METABOLISM; CIRCADIAN RHYTHM; DEFENSE MECHANISM; DEREGULATION; DROSOPHILA; ENERGY METABOLISM; FEMALE; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GLUCOSE HOMEOSTASIS; GLUCOSE METABOLISM; LOCOMOTION; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DIET; PROTEIN INTAKE; SUGAR INTAKE; TRANSCRIPTION INITIATION SITE; TRANSCRIPTION REGULATION; UPREGULATION; ANIMAL; DROSOPHILA MELANOGASTER; FEEDING BEHAVIOR; GENETICS; METABOLISM; PHYSIOLOGY;

ANIMALIA;

ANIMALS; CIRCADIAN CLOCKS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; ENERGY METABOLISM; FEEDING BEHAVIOR; GLUCOSE; GLYCEROL; PHOSPHOENOLPYRUVATE CARBOXYKINASE (ATP); TRANSCRIPTION FACTORS; TRANSCRIPTOME;

EID: 84937191093     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.15252/embj.201591385     Document Type: Article

References (57)

1. Abruzzi KC, Rodriguez J, Menet JS, Desrochers J, Zadina A, Luo W, Tkachev S, Rosbash M, (2011) Drosophila CLOCK target gene characterization: implications for circadian tissue-specific gene expression. Genes Dev 25: 2374-2386
2. Ballard FJ, Hanson RW, Leveille GA, (1967) Phosphoenolpyruvate carboxykinase and the synthesis of glyceride-glycerol from pyruvate in adipose tissue. J Biol Chem 242: 2746-2750
3. Bass J, (2012) Circadian topology of metabolism. Nature 491: 348-356
4. Becker A, Schlöder P, Steele JE, Wegener G, (1996) The regulation of trehalose metabolism in insects. Experientia 52: 433-439
5. Belacortu Y, Weiss R, Kadener S, Paricio N, (2012) Transcriptional activity and nuclear localization of Cabut, the Drosophila ortholog of vertebrate TGF-β-inducible early-response gene (TIEG) proteins. PLoS ONE 7: e32004
6. Benhamed F, Denechaud PD, Lemoine M, Robichon C, Moldes M, Bertrand-Michel J, Ratziu V, Serfaty L, Housset C, Capeau J, Girard J, Guillou H, Postic C, (2012) The lipogenic transcription factor ChREBP dissociates hepatic steatosis from insulin resistance in mice and humans. J Clin Invest 122: 2176-2194
7. Brown JL, Grau DJ, DeVido SK, Kassis JA, (2005) An Sp1/KLF binding site is important for the activity of a Polycomb group response element from the Drosophila engrailed gene. Nucleic Acids Res 33: 5181-5189
8. Chang TJ, Lee WJ, Chang HM, Lee KC, Chuang LM, (2008) Expression of subcutaneous adipose tissue phosphoenolpyruvate carboxykinase correlates with body mass index in nondiabetic women. Metabolism 57: 367-372
9. Chen JL, Peacock E, Samady W, Turner SM, Neese RA, Hellerstein MK, Murphy EJ, (2005) Physiologic and pharmacologic factors influencing glyceroneogenic contribution to triacylglyceride glycerol measured by mass isotopomer distribution analysis. J Biol Chem 280: 25396-25402
10. Dibner C, Schibler U, (2015). Circadian timing of metabolism in animal models and humans. J Intern Med 277: 513-527
11. Dietzl G, Chen D, Schnorrer F, Su KC, Barinova Y, Fellner M, Gasser B, Kinsey K, Oppel S, Scheiblauer S, Couto A, Marra V, Keleman K, Dickson BJ, (2007) A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature 448: 151-156
12. Eissing L, Scherer T, Tödter K, Knippschild U, Greve JW, Buurman WA, Pinnschmidt HO, Rensen SS, Wolf AM, Bartelt A, Heeren J, Buettner C, Scheja L, (2013) De novo lipogenesis in human fat and liver is linked to ChREBP-β and metabolic health. Nat Commun 4: 1528
13. Engreitz JM, Pandya-Jones A, McDonel P, Shishkin A, Sirokman K, Surka C, Kadri S, Xing J, Goren A, Lander ES, Plath K, Guttman M, (2013) The Xist lncRNA exploits three-dimensional genome architecture to spread across the X chromosome. Science 341: 1237973
14. Filhoulaud G, Guilmeau S, Dentin R, Girard J, Postic C, (2013) Novel insights into ChREBP regulation and function. Trends Endocrinol Metab 24: 257-268
15. Franckhauser S, Muñoz S, Pujol A, Casellas A, Riu E, Otaegui P, Su B, Bosch F, (2002) Increased fatty acid re-esterification by PEPCK overexpression in adipose tissue leads to obesity without insulin resistance. Diabetes 51: 624-630
16. Grönke S, Mildner A, Fellert S, Tennagels N, Petry S, Müller G, Jäckle H, Kühnlein RP, (2005) Brummer lipase is an evolutionary conserved fat storage regulator in Drosophila. Cell Metab 1: 323-330
17. Guillaumond F, Gréchez-Cassiau A, Subramaniam M, Brangolo S, Peteri-Brünback B, Staels B, Fiévet C, Spelsberg TC, Delaunay F, Teboul M, (2010) Kruppel-like factor KLF10 is a link between the circadian clock and metabolism in liver. Mol Cell Biol 30: 3059-3070
18. Gutierrez-Aguilar R, Benmezroua Y, Balkau B, Marre M, Helbecque N, Charpentier G, Polychronakos C, Sladek R, Froguel P, Neve B, (2007) Minor contribution of SMAD7 and KLF10 variants to genetic susceptibility of type 2 diabetes. Diabetes Metab 33: 372-378
19. Hanson RW, Reshef L, (2003) Glyceroneogenesis revisited. Biochimie 85: 1199-1205
20. Hardin PE, (2011) Molecular genetic analysis of circadian timekeeping in Drosophila. Adv Genet 74: 141-173
21. Havula E, Hietakangas V, (2012) Glucose sensing by ChREBP/MondoA-Mlx transcription factors. Semin Cell Dev Biol 23: 640-647
22. Havula E, Teesalu M, Hyötyläinen T, Seppälä H, Hasygar K, Auvinen P, Orešič M, Sandmann T, Hietakangas V, (2013) Mondo/ChREBP-Mlx-regulated transcriptional network is essential for dietary sugar tolerance in Drosophila. PLoS Genet 9: e1003438
23. Hietakangas V, Cohen SM, (2009) Regulation of tissue growth through nutrient sensing. Annu Rev Genet 43: 389-410
24. Huang DW, Sherman BT, Lempicki RA, (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4: 44-57
25. Hughes ME, Hogenesch JB, Kornacker K, (2010) JTK-CYCLE: an efficient nonparametric algorithm for detecting rhythmic components in genome-scale data sets. J Biol Rhythms 25: 372-380
26. Iizuka K, Takeda J, Horikawa Y, (2011) Krüppel-like factor-10 is directly regulated by carbohydrate response element-binding protein in rat primary hepatocytes. Biochem Biophys Res Commun 412: 638-643
27. Ishii S, Iizuka K, Miller BC, Uyeda K, (2004) Carbohydrate response element binding protein directly promotes lipogenic enzyme gene transcription. Proc Natl Acad Sci USA 101: 15597-15602
28. Jeong YS, Kim D, Lee YS, Kim HJ, Han JY, Im SS, Chong HK, Kwon JK, Cho YH, Kim WK, Osborne TF, Horton JD, Jun HS, Ahn YH, Ahn SM, Cha JY, (2011) Integrated expression profiling and genome-wide analysis of ChREBP targets reveals the dual role for ChREBP in glucose-regulated gene expression. PLoS ONE 6: e22544
29. Jin ES, Sherry AD, Malloy CR, (2013) Metabolism of glycerol, glucose, and lactate in the citric acid cycle prior to incorporation into hepatic acylglycerols. J Biol Chem 288: 14488-14496
30. Kadener S, Stoleru D, McDonald M, Nawathean P, Rosbash M, (2007) Clockwork Orange is a transcriptional repressor and a new Drosophila circadian pacemaker component. Genes Dev 21: 1675-1686
31. Kalhan SC, Mahajan S, Burkett E, Reshef L, Hanson RW, (2001) Glyceroneogenesis and the source of glycerol for hepatic triacylglycerol synthesis in humans. J Biol Chem 276: 12928-12931
32. Kooner JS, Chambers JC, Aguilar-Salinas CA, Hinds DA, Hyde CL, Warnes GR, Gõmez Pérez FJ, Frazer KA, Elliott P, Scott J, Milos PM, Cox D, Thompson JF, (2008) Genome-wide scan identifies variation in MLXIPL associated with plasma triglycerides. Nat Genet 40: 149-151
33. Levine JD, Funes P, Dowse HB, Hall JC, (2002) Signal analysis of behavioral and molecular cycles. BMC Neurosci 3: 1
34. Mahendran Y, Cederberg H, Vangipurapu J, Kangas AJ, Soininen P, Kuusisto J, Uusitupa M, Ala-Korpela M, Laakso M, (2013) Glycerol and fatty acids in serum predict the development of hyperglycemia and type 2 diabetes in Finnish men. Diabetes Care 36: 3732-3738
35. Masri S, Sassone-Corsi P, (2014). Sirtuins and the circadian clock: bridging chromatin and metabolism. Sci Signal 7, re6
36. Mattson MP, Allison DB, Fontana L, Harvie M, Longo VD, Malaisse WJ, Mosley M, Notterpek L, Ravussin E, Scheer FAJL, Seyfried TN, Varady KA, Panda S, (2014) Meal frequency and timing in health and disease. Proc Natl Acad Sci USA 111: 16647-16653
37. Muñoz-Descalzo S, Terol J, Paricio N, (2005) Cabut, a C2H2 zinc finger transcription factor, is required during Drosophila dorsal closure downstream of JNK signaling. Dev Biol 287: 168-179
38. Nye CK, Hanson RW, Kalhan SC, (2008) Glyceroneogenesis is the dominant pathway for triglyceride glycerol synthesis in vivo in the rat. J Biol Chem 283: 27565-27574
39. Oh KJ, Han HS, Kim MJ, Koo SH, (2013) CREB and FoxO1: two transcription factors for the regulation of hepatic gluconeogenesis. BMB Rep 46: 567-574
40. Olswang Y, Cohen H, Papo O, Cassuto H, Croniger CM, Hakimi P, Tilghman SM, Hanson RW, Reshef L, (2002) A mutation in the peroxisome proliferator-activated receptor gamma-binding site in the gene for the cytosolic form of phosphoenolpyruvate carboxykinase reduces adipose tissue size and fat content in mice. Proc Natl Acad Sci USA 99: 625-630
41. Partch CL, Green CB, Takahashi JS, (2014) Molecular architecture of the mammalian circadian clock. Trends Cell Biol 24: 90-99
42. Peek CB, Ramsey KM, Marcheva B, Bass J, (2012) Nutrient sensing and the circadian clock. Trends Endocrinol Metab 23: 312-318
43. Qi Q, Chu AY, Kang JH, Jensen MK, Curhan GC, Pasquale LR, Ridker PM, Hunter DJ, Willett WC, Rimm EB, Chasman DI, Hu FB, Qi L, (2012) Sugar-sweetened beverages and genetic risk of obesity. N Engl J Med 367: 1387-1396
44. Sassu ED, McDermott JE, Keys BJ, Esmaeili M, Keene AC, Birnbaum MJ, DiAngelo JR, (2012) Mio/dChREBP coordinately increases fat mass by regulating lipid synthesis and feeding behavior in Drosophila. Biochem Biophys Res Commun 426: 43-48
45. Spittau B, Krieglstein K, (2012) Klf10 and Klf11 as mediators of TGF-beta superfamily signaling. Cell Tissue Res 347: 65-72
46. Spittau B, Wang Z, Boinska D, Krieglstein K, (2007) Functional domains of the TGF-beta-inducible transcription factor Tieg3 and detection of two putative nuclear localization signals within the zinc finger DNA-binding domain. J Cell Biochem 101: 712-722
47. Stanhope KL, Schwarz JM, Havel PJ, (2013) Adverse metabolic effects of dietary fructose: results from the recent epidemiological, clinical, and mechanistic studies. Curr Opin Lipidol 24: 198-206
48. Stark R, Guebre-Egziabher F, Zhao X, Feriod C, Dong J, Alves TC, Ioja S, Pongratz RL, Bhanot S, Roden M, Cline GW, Shulman GI, Kibbey RG, (2014) A role for mitochondrial phosphoenolpyruvate carboxykinase (PEPCK-M) in the regulation of hepatic gluconeogenesis. J Biol Chem 289: 7257-7263
49. Subramaniam M, Hawse JR, Bruinsma ES, Grygo SB, Cicek M, Oursler MJ, Spelsberg TC, (2010) TGFbeta inducible early gene- 1 directly binds to, and represses, the OPG promoter in osteoblasts. Biochem Biophys Res Commun 392: 72-76
50. Tennessen JM, Barry WE, Cox J, Thummel CS, (2014). Methods for studying metabolism in Drosophila. Methods San Diego Calif 68: 105-115
51. Wang B, Moya N, Niessen S, Hoover H, Mihaylova MM, Shaw RJ, Yates JR 3rd, Fischer WH, Thomas JB, Montminy M, (2011) A hormone-dependent module regulating energy balance. Cell 145: 596-606
52. Weiss R, Bartok O, Mezan S, Malka Y, Kadener S, (2014) Synergistic interactions between the molecular and neuronal circadian networks drive robust behavioral circadian rhythms in Drosophila melanogaster. PLoS Genet 10: e1004252
53. Xu K, DiAngelo JR, Hughes ME, Hogenesch JB, Sehgal A, (2011) The circadian clock interacts with metabolic physiology to influence reproductive fitness. Cell Metab 13: 639-654
54. Xu K, Zheng X, Sehgal A, (2008) Regulation of feeding and metabolism by neuronal and peripheral clocks in Drosophila. Cell Metab 8: 289-300
55. Zhang H, Chen Q, Yang M, Zhu B, Cui Y, Xue Y, Gong N, Cui A, Wang M, Shen L, Zhang S, Fang F, Chang Y, (2013) Mouse KLF11 regulates hepatic lipid metabolism. J Hepatol 58: 763-770
56. Zhang W, Thompson BJ, Hietakangas V, Cohen SM, (2011) MAPK/ERK signaling regulates insulin sensitivity to control glucose metabolism in Drosophila. PLoS Genet 7: e1002429
57. Zhao J, Kilman VL, Keegan KP, Peng Y, Emery P, Rosbash M, Allada R, (2003) Drosophila clock can generate ectopic circadian clocks. Cell 113: 755-766