The Insulin-Regulated CREB Coactivator TORC Promotes Stress Resistance in Drosophila

Cell Metabolism

Volumn 7, Issue 5, 2008, Pages 434-444

  Wang, Biao ^a   Goode, Jason ^a   Best, Jennifer ^a   Meltzer, Jodi ^b   Schilman, Pablo E ^c   Chen, Jian ^b   Garza, Dan ^b   Thomas, John B ^a   Montminy, Marc ^a  

^a SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^b NOVARTIS INSTITUTES FOR BIOMEDICAL RESEARCH   (United States)

^c UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

HUMDISEASE; SIGNALING

Indexed keywords

CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; DROSOPHILA PROTEIN; GLYCOGEN; INSULIN; LIPID; MUTANT PROTEIN; PROTEIN SERINE THREONINE KINASE; SALT INDUCIBLE KINASE 2; TRANSDUCER OF REGULATED CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN ACTIVITY 2;

ANIMAL CELL; ARTICLE; BRAIN; CELL STRAIN HEK293; CONTROLLED STUDY; DROSOPHILA; ENERGY BALANCE; GENE TARGETING; HUMAN; HUMAN CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; REFEEDING; SIGNAL TRANSDUCTION; STARVATION;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BLOTTING, WESTERN; BRAIN; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FEMALE; GLYCOGEN; HYPOGLYCEMIC AGENTS; INSULIN; LIPIDS; MALE; NEURONS; OXIDATIVE STRESS; PEPTIDE FRAGMENTS; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; STARVATION; TRANSCRIPTION FACTORS;

MAMMALIA;

EID: 42649140573     PISSN: 15504131     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cmet.2008.02.010     Document Type: Article

References (41)

1. Ahn S., Olive M., Aggarwal S., Krylov D., Ginty D., and Vinson C. A dominant negative inhibitor of CREB reveals that it is a general mediator stimulus-dependent transcription of c-fos. Mol. Cell. Biol. 18 (1998) 967-977
2. Belvin M.P., Zhou H., and Yin J.C. The Drosophila dCREB2 gene affects the circadian clock. Neuron 22 (1999) 777-787
3. Bittinger M.A., McWhinnie E., Meltzer J., Iourgenko V., Latario B., Liu X., Chen C.H., Song C., Garza D., and Labow M. Activation of cAMP response element-mediated gene expression by regulated nuclear transport of TORC proteins. Curr. Biol. 14 (2004) 2156-2161
4. Bohni R., Riesgo-Escovar J., Oldham S., Brogiolo W., Stocker H., Andruss B.F., Beckingham K., and Hafen E. Autonomous control of cell and organ size by CHICO, a Drosophila homolog of vertebrate IRS1-4. Cell 97 (1999) 865-875
5. Brand A.H., and Perrimon N. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118 (1993) 401-415
6. Broughton S.J., Piper M.D., Ikeya T., Bass T.M., Jacobson J., Driege Y., Martinez P., Hafen E., Withers D.J., Leevers S.J., and 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 (2005) 3105-3110
7. Chen L., Rio D.C., Haddad G.G., and Ma E. Regulatory role of dADAR in ROS metabolism in Drosophila CNS. Brain Res. Mol. Brain Res. 131 (2004) 93-100
8. Clancy D.J., Gems D., Harshman L.G., Oldham S., Stocker H., Hafen E., Leevers S.J., and Partridge L. Extension of life-span by loss of CHICO, a Drosophila insulin receptor substrate protein. Science 292 (2001) 104-106
9. Dentin R., Liu Y., Koo S.H., Hedrick S., Vargas T., Heredia J., Yates III J., and Montminy M. Insulin modulates gluconeogenesis by inhibition of the coactivator TORC2. Nature 449 (2007) 366-369
10. Djawdan M., Chippindale A.K., Rose M.R., and Bradley T.J. Metabolic reserves and evolved stress resistance in Drosophila melanogaster. Physiol. Zool. 71 (1998) 584-594
11. Fridell Y.W., Sanchez-Blanco A., Silvia B.A., and Helfand S.L. Targeted expression of the human uncoupling protein 2 (hUCP2) to adult neurons extends life span in the fly. Cell Metab. 1 (2005) 145-152
12. Gershman B., Puig O., Hang L., Peitzsch R.M., Tatar M., and Garofalo R.S. High-resolution dynamics of the transcriptional response to nutrition in Drosophila: a key role for dFOXO. Physiol. Genomics 29 (2007) 24-34
13. Giannakou M.E., and Partridge L. Role of insulin-like signalling in Drosophila lifespan. Trends Biochem. Sci. 32 (2007) 180-188
14. Hendricks J.C., Williams J.A., Panckeri K., Kirk D., Tello M., Yin J.C., and Sehgal A. A non-circadian role for cAMP signaling and CREB activity in Drosophila rest homeostasis. Nat. Neurosci. 4 (2001) 1108-1115
15. Iijima-Ando K., and Yin J.C. Transgenic cAMP response element reporter flies for monitoring circadian rhythms. Methods Enzymol. 393 (2005) 302-315
16. Ja W.W., Carvalho G.B., Mak E.M., de la Rosa N.N., Fang A.Y., Liong J.C., Brummel T., and Benzer S. Prandiology of Drosophila and the CAFE assay. Proc. Natl. Acad. Sci. USA 104 (2007) 8253-8256
17. Junger M.A., Rintelen F., Stocker H., Wasserman J.D., Vegh M., Radimerski T., Greenberg M.E., and Hafen E. The Drosophila forkhead transcription factor FOXO mediates the reduction in cell number associated with reduced insulin signaling. J. Biol. 2 (2003) 20
18. Kim S.K., and Rulifson E.J. Conserved mechanisms of glucose sensing and regulation by Drosophila corpora cardiaca cells. Nature 431 (2004) 316-320
19. Koo S.H., Flechner L., Qi L., Zhang X., Screaton R.A., Jeffries S., Hedrick S., Xu W., Boussouar F., Brindle P., et al. The CREB coactivator TORC2 is a key regulator of fasting glucose metabolism. Nature 437 (2005) 1109-1111
20. Kramer J.M., Davidge J.T., Lockyer J.M., and Staveley B.E. Expression of Drosophila FOXO regulates growth and can phenocopy starvation. BMC Dev. Biol. 3 (2003) 5
21. Lee G., and 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 (2004) 311-323
22. Lighton J.R. Measurements on insects. In: Payne P.A. (Ed). Concise Encyclopedia on Biological and Biomedical Measurement Systems (1991), Pergamon Press, Oxford 201-208
23. Lighton J.R., and Turner R.J. Thermolimit respirometry: an objective assessment of critical thermal maxima in two sympatric desert harvester ants, Pogonomyrmex rugosus and P. californicus. J. Exp. Biol. 207 (2004) 1903-1913
24. Matsumoto M., Pocai A., Rossetti L., Depinho R.A., and Accili D. Impaired regulation of hepatic glucose production in mice lacking the forkhead transcription factor foxo1 in liver. Cell Metab. 6 (2007) 208-216
25. Mockett R.J., Bayne A.C., Kwong L.K., Orr W.C., and Sohal R.S. Ectopic expression of catalase in Drosophila mitochondria increases stress resistance but not longevity. Free Radic. Biol. Med. 34 (2003) 207-217
26. Okamoto M., Takemori H., and Katoh Y. Salt-inducible kinase in steroidogenesis and adipogenesis. Trends Endocrinol. Metab. 15 (2004) 21-26
27. Perazzona B., Isabel G., Preat T., and Davis R.L. The role of cAMP response element-binding protein in Drosophila long-term memory. J. Neurosci. 24 (2004) 8823-8828
28. Puig O., Marr M.T., Ruhf M.L., and Tjian R. Control of cell number by Drosophila FOXO: downstream and feedback regulation of the insulin receptor pathway. Genes Dev. 17 (2003) 2006-2020
29. Ravnskjaer K., Kester H., Liu Y., Zhang X., Lee D., Yates III J.R., and Montminy M. Cooperative interactions between CBP and TORC2 confer selectivity to CREB target gene expression. EMBO J. 26 (2007) 2880-2889
30. Robertson H.M., Preston C.R., Phillis R.W., Johnson-Schlitz D.M., Benz W.K., and Engels W.R. A stable genomic source of P element transposase in Drosophila melanogaster. Genetics 118 (1988) 461-470
31. Rulifson E.J., Kim S.K., and Nusse R. Ablation of insulin-producing neurons in flies: growth and diabetic phenotypes. Science 296 (2002) 1118-1120
32. Sakai T., Tamura T., Kitamoto T., and Kidokoro Y. A clock gene, period, plays a key role in long-term memory formation in Drosophila. Proc. Natl. Acad. Sci. USA 101 (2004) 16058-16063
33. Screaton R.A., Conkright M.D., Katoh Y., Best J.L., Canettieri G., Jeffries S., Guzman E., Niessen S., Yates III J.R., Takemori H., et al. The CREB coactivator TORC2 functions as a calcium- and cAMP-sensitive coincidence detector. Cell 119 (2004) 61-74
34. Spiegelman B.M., and Heinrich R. Biological control through regulated transcriptional coactivators. Cell 119 (2004) 157-167
35. Sullivan K.M., and Rubin G.M. The Ca(2+)-calmodulin-activated protein phosphatase calcineurin negatively regulates EGF receptor signaling in Drosophila development. Genetics 161 (2002) 183-193
36. Svensson M.J., and Larsson J. Thioredoxin-2 affects lifespan and oxidative stress in Drosophila. Hereditas 144 (2007) 25-32
37. Takemori H., Kanematsu M., Kajimura J., Hatano O., Katoh Y., Lin X.Z., Min L., Yamazaki T., Doi J., and Okamoto M. Dephosphorylation of TORC initiates expression of the StAR gene. Mol. Cell. Endocrinol. 265-266 (2007) 196-204
38. Van Handel E. Rapid determination of glycogen and sugars in mosquitoes. J. Am. Mosq. Control Assoc. 1 (1985) 299-301
39. Van Handel E. Rapid determination of total lipids in mosquitoes. J. Am. Mosq. Control Assoc. 1 (1985) 302-304
40. Wu Z., Huang X., Feng Y., Handschin C., Gullicksen P.S., Bare O., Labow M., Spiegelman B., and Stevenson S.C. Transducer of regulated CREB-binding proteins (TORCs) induce PGC-1alpha transcription and mitochondrial biogenesis in muscle cells. Proc. Natl. Acad. Sci. USA 103 (2006) 14379-14384
41. Zinke I., Schutz C.S., Katzenberger J.D., Bauer M., and Pankratz M.J. Nutrient control of gene expression in Drosophila: microarray analysis of starvation and sugar-dependent response. EMBO J. 21 (2002) 6162-6173