Integrative genomic analysis of CREB defines a critical role for transcription factor networks in mediating the fed/fasted switch in liver

BMC Genomics

Volumn 14, Issue 1, 2013, Pages

  Everett, Logan J ^a   Lay, John L ^a   Lukovac, Sabina ^a   Bernstein, Diana ^a   Steger, David J ^a   Lazar, Mitchell A ^a   Kaestner, Klaus H ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

CREB; Gene regulation; Hepatic fasting response; Integrative genomics; Transcription networks

Indexed keywords

CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; CYCLIC AMP RESPONSIVE ELEMENT MODULATOR; MESSENGER RNA; NUCLEAR RECEPTOR COACTIVATOR; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; TRANSCRIPTION FACTOR; TRANSCRIPTOME;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; CREB GENE; CRELD2 GENE; CREM GENE; DIET RESTRICTION; ENDOPLASMIC RETICULUM STRESS; GENE; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENE SWITCHING; GENE TARGETING; GENETIC ASSOCIATION; GENOME ANALYSIS; HIGH THROUGHPUT SEQUENCING; HSPA1A GENE; HSPA5 GENE; LIVER PARENCHYMA; MALE; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; NR3C1 GENE; NUCLEOTIDE SEQUENCE; NUTRIENT DYNAMICS; NUTRIENT UPTAKE; PCK1 GENE; PPARA GENE; PPARGC1A GENE; PROTEIN DNA BINDING; QUANTITATIVE ANALYSIS;

ANIMALS; BASE SEQUENCE; CHROMATIN IMMUNOPRECIPITATION; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; DNA; EATING; FASTING; GENE EXPRESSION REGULATION; GENOMICS; LIVER; MALE; MICE; MICE, INBRED C57BL; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; TRANSCRIPTION, GENETIC;

MAMMALIA; MUS;

EID: 84877811076     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-14-337     Document Type: Article

References (61)

1. Altarejos JY, Montminy M. CREB and the CRTC co-activators: sensors for hormonal and metabolic signals. Nat Rev Mol Cell Biol 2011, 12:141-151. 10.1038/nrm3072, 21346730.
2. Montminy MR, Gonzalez GA, Yamamoto KK. Regulation of cAMP-inducible genes by CREB. Trends Neurosci 1990, 13:184-188. 10.1016/0166-2236(90)90045-C, 1693237.
3. Sakamoto K, Karelina K, Obrietan K. CREB: a multifaceted regulator of neuronal plasticity and protection. J Neurochem 2011, 116:1-9. 10.1111/j.1471-4159.2010.07080.x, 3575743, 21044077.
4. Wen AY, Sakamoto KM, Miller LS. The role of the transcription factor CREB in immune function. J Immunol 2010, 185:6413-6419. 10.4049/jimmunol.1001829, 21084670.
5. Koo S-H, Flechner L, Qi L, Zhang X, Screaton RA, Jeffries S, Hedrick S, Xu W, Boussouar F, Brindle P, Takemori H, Montminy M. The CREB coactivator TORC2 is a key regulator of fasting glucose metabolism. Nature 2005, 437:1109-1111. 10.1038/nature03967, 16148943.
6. Zhang X, Odom DT, Koo S-H, Conkright MD, Canettieri G, Best J, Chen H, Jenner R, Herbolsheimer E, Jacobsen E, Kadam S, Ecker JR, Emerson B, Hogenesch JB, Unterman T, Young RA, Montminy M. Genome-wide analysis of cAMP-response element binding protein occupancy, phosphorylation, and target gene activation in human tissues. Proc Natl Acad Sci USA 2005, 102:4459-4464. 10.1073/pnas.0501076102, 555478, 15753290.
7. Nichols M, Weih F, Schmid W, DeVack C, Kowenz-Leutz E, Luckow B, Boshart M, Schütz G. Phosphorylation of CREB affects its binding to high and low affinity sites: implications for cAMP induced gene transcription. EMBO J 1992, 11:3337-3346. 556868, 1354612.
8. Zhang L, Rubins NE, Ahima RS, Greenbaum LE, Kaestner KH. Foxa2 Integrates the transcriptional response of the hepatocyte to fasting. Cell Metab 2005, 2:141-148. 10.1016/j.cmet.2005.07.002, 16098831.
9. Erion DM, Ignatova ID, Yonemitsu S, Nagai Y, Chatterjee P, Weismann D, Hsiao JJ, Zhang D, Iwasaki T, Stark R, Flannery C, Kahn M, Carmean CM, Yu XX, Murray SF, Bhanot S, Monia BP, Cline GW, Samuel VT, Shulman GI. Prevention of hepatic steatosis and hepatic insulin resistance by knockdown of cAMP response element-binding protein. Cell Metab 2009, 10:499-506. 10.1016/j.cmet.2009.10.007, 2799933, 19945407.
10. Lin HV, Accili D. Hormonal regulation of hepatic glucose production in health and disease. Cell Metab 2011, 14:9-19. 10.1016/j.cmet.2011.06.003, 3131084, 21723500.
11. Meshkani R, Adeli K. Hepatic insulin resistance, metabolic syndrome and cardiovascular disease. Clin Biochem 2009, 42:1331-1346. 10.1016/j.clinbiochem.2009.05.018, 19501581.
12. Weickert MO, Pfeiffer AFH. Signalling mechanisms linking hepatic glucose and lipid metabolism. Diabetologia 2006, 49:1732-1741. 10.1007/s00125-006-0295-3, 16718463.
13. Herzig S, Long F, Jhala US, Hedrick S, Quinn R, Bauer A, Rudolph D, Schutz G, Yoon C, Puigserver P, Spiegelman B, Montminy M. CREB regulates hepatic gluconeogenesis through the coactivator PGC-1. Nature 2001, 413:179-183. 10.1038/35093131, 11557984.
14. Odom DT, Dowell RD, Jacobsen ES, Nekludova L, Rolfe PA, Danford TW, Gifford DK, Fraenkel E, Bell GI, Young RA. Core transcriptional regulatory circuitry in human hepatocytes. Mol Syst Biol 2006, 2:2006.0017. 1681491, 16738562.
15. Bedford DC, Kasper LH, Wang R, Chang Y, Green DR, Brindle PK. Disrupting the CH1 domain structure in the acetyltransferases CBP and p300 results in lean mice with increased metabolic control. Cell Metab 2011, 14:219-230. 10.1016/j.cmet.2011.06.010, 3163393, 21803292.
16. Le Lay J, Tuteja G, White P, Dhir R, Ahima R, Kaestner KH. CRTC2 (TORC2) Contributes to the transcriptional response to fasting in the liver but is not required for the maintenance of glucose homeostasis. Cell Metab 2009, 10:55-62. 10.1016/j.cmet.2009.06.006, 2748661, 19583954.
17. Cha-Molstad H, Keller DM, Yochum GS, Impey S, Goodman RH. Cell-type-specific binding of the transcription factor CREB to the cAMP-response element. Proc Natl Acad Sci USA 2004, 101:13572-13577. 10.1073/pnas.0405587101, 518796, 15342915.
18. Conkright MD, Guzmán E, Flechner L, Su AI, Hogenesch JB, Montminy M. Genome-wide analysis of CREB target genes reveals a core promoter requirement for cAMP responsiveness. Mol Cell 2003, 11:1101-1108. 10.1016/S1097-2765(03)00134-5, 12718894.
19. Lin B, Morris DW, Chou JY. The role of HNF1alpha, HNF3gamma, and cyclic AMP in glucose-6-phosphatase gene activation. Biochemistry 1997, 36:14096-14106. 10.1021/bi9703249, 9369482.
20. Park EA, Gurney AL, Nizielski SE, Hakimi P, Cao Z, Moorman A, Hanson RW. Relative roles of CCAAT/enhancer-binding protein beta and cAMP regulatory element-binding protein in controlling transcription of the gene for phosphoenolpyruvate carboxykinase (GTP). J Biol Chem 1993, 268:613-619.
21. Quinn PG, Wong TW, Magnuson MA, Shabb JB, Granner DK. Identification of basal and cyclic AMP regulatory elements in the promoter of the phosphoenolpyruvate carboxykinase gene. Mol Cell Biol 1988, 8:3467-3475. 363584, 2850495.
22. Celniker SE, Dillon LAL, Gerstein MB, Gunsalus KC, Henikoff S, Karpen GH, Kellis M, Lai EC, Lieb JD, MacAlpine DM, Micklem G, Piano F, Snyder M, Stein L, White KP, Waterston RH. Unlocking the secrets of the genome. Nature 2009, 459:927-930. 10.1038/459927a, 2843545, 19536255.
23. Myers RM, Stamatoyannopoulos J, Snyder M, Dunham I, Hardison RC, Bernstein BE, Gingeras TR, Kent WJ, Birney E, Wold B, Crawford GE. A user's guide to the encyclopedia of DNA elements (ENCODE). PLoS Biol 2011, 9:e1001046. 10.1371/journal.pbio.1001046, 3079585, 21526222.
24. Heinz S, Benner C, Spann N, Bertolino E, Lin YC, Laslo P, Cheng JX, Murre C, Singh H, Glass CK. Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol Cell 2010, 38:576-589. 10.1016/j.molcel.2010.05.004, 2898526, 20513432.
25. Tuteja G, White P, Schug J, Kaestner KH. Extracting transcription factor targets from ChIP-Seq data. Nucleic Acids Res 2009, 37:e113. 10.1093/nar/gkp536, 2761252, 19553195.
26. Zhang Y, Liu T, Meyer CA, Eeckhoute J, Johnson DS, Bernstein BE, Nusbaum C, Myers RM, Brown M, Li W, Liu XS. Model-based analysis of ChIP-Seq (MACS). Genome Biol 2008, 9:R137. 10.1186/gb-2008-9-9-r137, 2592715, 18798982.
27. Cho H, Zhao X, Hatori M, Yu RT, Barish GD, Lam MT, Chong LW, Ditacchio L, Atkins AR, Glass CK, Liddle C, Auwerx J, Downes M, Panda S, Evans RM. Regulation of circadian behaviour and metabolism by REV-ERB-α and REV-ERB-β. Nature 2012, 485:123-127. 10.1038/nature11048, 3367514, 22460952.
28. Feng D, Liu T, Sun Z, Bugge A, Mullican SE, Alenghat T, Liu XS, Lazar MA. A circadian rhythm orchestrated by histone deacetylase 3 controls hepatic lipid metabolism. Science 2011, 331:1315-1319. 10.1126/science.1198125, 3389392, 21393543.
29. Hurtado A, Holmes KA, Ross-Innes CS, Schmidt D, Carroll JS. FOXA1 Is a key determinant of estrogen receptor function and endocrine response. Nature Genet 2011, 43:27-33. 10.1038/ng.730, 3024537, 21151129.
30. Robinson MD, McCarthy DJ, Smyth GK, Edge R. A bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 2010, 26:139-140. 10.1093/bioinformatics/btp616, 2796818, 19910308.
31. Impey S, Mccorkle SR, Cha-molstad H, Dwyer JM, Yochum GS, Boss JM, Mcweeney S, Dunn JJ, Mandel G, Goodman RH, York N. Defining the CREB regulon/: a genome-wide analysis of transcription factor regulatory regions emory school of medicine. Cell 2004, 119:1041-1054.
32. Martianov I, Choukrallah MA, Krebs A, Ye T, Legras S, Rijkers E, Van Ijcken W, Jost B, Sassone-Corsi P, Davidson I. Cell-specific occupancy of an extended repertoire of CREM and CREB binding loci in male germ cells. BMC Genomics 2010, 11:530. 10.1186/1471-2164-11-530, 3091680, 20920259.
33. Boden G, Song W, Duan X, Cheung P, Kresge K, Barrero C, Merali S. Infusion of glucose and lipids at physiological rates causes acute endoplasmic reticulum stress in rat liver. Obesity 2011, 19:1366-1373. 10.1038/oby.2011.71, 21475143.
34. Yang L, Xue Z, He Y, Sun S, Chen H, Qi L. A phos-tag-based approach reveals the extent of physiological endoplasmic reticulum stress. PLoS One 2010, 5:e11621. 10.1371/journal.pone.0011621, 2905412, 20661282.
35. Ravnskjaer K, Kester H, Liu Y, Zhang X, Lee D, Yates JR, Montminy M. Cooperative interactions between CBP and TORC2 confer selectivity to CREB target gene expression. EMBO J 2007, 26:2880-2889. 10.1038/sj.emboj.7601715, 1894761, 17476304.
36. Nitsch D, Boshart M, Schütz G. Activation of the tyrosine aminotransferase gene is dependent on synergy between liver-specific and hormone-responsive elements. Proc Natl Acad Sci USA 1993, 90:5479-5483. 10.1073/pnas.90.12.5479, 46744, 8100067.
37. Christoffels VM, Grange T, Kaestner KH, Cole TJ, Darlington GJ, Croniger CM, Lamers WH. Glucocorticoid receptor, C/EBP, HNF3, and protein kinase a coordinately activate the glucocorticoid response unit of the carbamoylphosphate synthetase I gene. Mol Cell Biol 1998, 18:6305-6315. 109217, 9774647.
38. Soccio RE, Tuteja G, Everett LJ, Li Z, Lazar MA, Kaestner KH. Species-specific strategies underlying conserved functions of metabolic transcription factors. Mol Endocrinol 2011, 25:694-706. 10.1210/me.2010-0454, 3386547, 21292830.
39. Boergesen M, Pedersen T, Gross B, Van Heeringen SJ, Hagenbeek D, Bindesbøll C, Caron S, Lalloyer F, Steffensen KR, Nebb HI, Gustafsson J-T, Stunnenberg HG, Staels B, Mandrup S. Genome-wide profiling of liver X receptor, retinoid X receptor, and peroxisome proliferator-activated receptor α in mouse liver reveals extensive sharing of binding sites. Mol Cell Biol 2012, 32:852-867. 10.1128/MCB.06175-11, 3272984, 22158963.
40. Croniger CM, Millward C, Yang J, Kawai Y, Arinze IJ, Liu S, Harada-Shiba M, Chakravarty K, Friedman JE, Poli V, Hanson RW. Mice with a deletion in the gene for CCAAT/enhancer-binding protein beta have an attenuated response to cAMP and impaired carbohydrate metabolism. J Biol Chem 2001, 276:629-638.
41. Friedman JR, Kaestner KH. The foxa family of transcription factors in development and metabolism. Cell Mol Life Sci 2006, 63:2317-2328. 10.1007/s00018-006-6095-6, 16909212.
42. Le Phuc P, Friedman JR, Schug J, Brestelli JE, Parker JB, Bochkis IM, Kaestner KH. Glucocorticoid receptor-dependent gene regulatory networks. PLoS Genet 2005, 1:e16. 10.1371/journal.pgen.0010016, 1186734, 16110340.
43. Kataoka K. Multiple mechanisms and functions of maf transcription factors in the regulation of tissue-specific genes. J Biochem 2007, 141:775-781. 10.1093/jb/mvm105, 17569705.
44. Servillo G, Della Fazia MA, Sassone-Corsi P. Coupling cAMP signaling to transcription in the liver: pivotal role of CREB and CREM. Exp Cell Res 2002, 275:143-154. 10.1006/excr.2002.5491, 11969286.
45. Zhou XY, Shibusawa N, Naik K, Porras D, Temple K, Ou H, Kaihara K, Roe MW, Brady MJ, Wondisford FE. Insulin regulation of hepatic gluconeogenesis through phosphorylation of CREB-binding protein. Nat Med 2004, 10:633-637. 10.1038/nm1050, 15146178.
46. Schmidt D, Wilson MD, Ballester B, Schwalie PC, Brown GD, Marshall A, Kutter C, Watt S, Martinez-Jimenez CP, Mackay S, Talianidis I, Flicek P, Odom DT. Five-vertebrate ChIP-seq reveals the evolutionary dynamics of transcription factor binding. Science 2010, 328:1036-1040. 10.1126/science.1186176, 3008766, 20378774.
47. Seo HY, Kim MK, Min AK, Kim HS, Ryu SY, Kim NK, Lee KM, Kim HJ, Choi HS, Lee KU, Park KG, Lee IK. Endoplasmic reticulum stress-induced activation of activating transcription factor 6 decreases cAMP-stimulated hepatic gluconeogenesis via inhibition of CREB. Endocrinology 2010, 151:561-568. 10.1210/en.2009-0641, 20022930.
48. Wang Y, Vera L, Fischer WH, Montminy M. The CREB coactivator CRTC2 links hepatic ER stress and fasting gluconeogenesis. Nature 2009, 460:534-537. 2730924, 19543265.
49. Ozcan U, Cao Q, Yilmaz E, Lee AH, Iwakoshi NN, Ozdelen E, Tuncman G, Görgün C, Glimcher LH, Hotamisligil GS. Endoplasmic reticulum stress links obesity, insulin action, and type 2 diabetes. Science 2004, 306:457-461. 10.1126/science.1103160, 15486293.
50. Wagner M, Moore DD. Endoplasmic reticulum stress and glucose homeostasis. Curr Opin Clin Nutr Metab Care 2011, 14:367-373. 10.1097/MCO.0b013e32834778d4, 21543975.
51. Smyth GK, Michaud J, Scott HS. Use of within-array replicate spots for assessing differential expression in microarray experiments. Bioinformatics 2005, 21:2067-2075. 10.1093/bioinformatics/bti270, 15657102.
52. Tusher VG, Tibshirani R, Chu G. Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci USA 2001, 98:5116-5121. 10.1073/pnas.091062498, 33173, 11309499.
53. Tuteja G, Jensen ST, White P, Kaestner KH. Cis-regulatory modules in the mammalian liver: composition depends on strength of Foxa2 consensus site. Nucleic Acids Res 2008, 36:4149-4157. 10.1093/nar/gkn366, 2475634, 18556755.
54. Salmon-Divon M, Dvinge H, Tammoja K, Bertone P. PeakAnalyzer: genome-wide annotation of chromatin binding and modification loci. BMC Bioinformatics 2010, 11:415. 10.1186/1471-2105-11-415, 2923140, 20691053.
55. Liu T, Ortiz JA, Taing L, Meyer CA, Lee B, Zhang Y, Shin H, Wong SS, Ma J, Lei Y, Pape UJ, Poidinger M, Chen Y, Yeung K, Brown M, Turpaz Y, Liu XS. Cistrome: an integrative platform for transcriptional regulation studies. Genome Biol 2011, 12:R83. 10.1186/gb-2011-12-8-r83, 3245621, 21859476.
56. Ji H, Jiang H, Ma W, Johnson DS, Myers RM, Wong WH. An integrated software system for analyzing ChIP-chip and ChIP-seq data. Nat Biotechnol 2008, 26:1293-1300. 10.1038/nbt.1505, 2596672, 18978777.
57. Bryne JC, Valen E, Tang MHE, Marstrand T, Winther O, Da Piedade I, Krogh A, Lenhard B, Sandelin A. JASPAR, the open access database of transcription factor-binding profiles: new content and tools in the 2008 update. Nucleic Acids Res 2008, 36:D102-D106. 10.1093/nar/gkn449, 2238834, 18006571.
58. Bucher P. Weight matrix descriptions of four eukaryotic RNA polymerase II promoter elements derived from 502 unrelated promoter sequences. J Mol Biol 1990, 212:563-578. 10.1016/0022-2836(90)90223-9, 2329577.
59. Carninci P, Sandelin A, Lenhard B, Katayama S, Shimokawa K, Ponjavic J, Semple CAM, Taylor MS, Engström PG, Frith MC, Forrest ARR, Alkema WB, Tan SL, Plessy C, Kodzius R, Ravasi T, Kasukawa T, Fukuda S, Kanamori-Katayama M, Kitazume Y, Kawaji H, Kai C, Nakamura M, Konno H, Nakano K, Mottagui-Tabar S, Arner P, Chesi A, Gustincich S, Persichetti F. Genome-wide analysis of mammalian promoter architecture and evolution. Nature Genet 2006, 38:626-635. 10.1038/ng1789, 16645617.
60. Suzuki Y, Tsunoda T, Sese J, Taira H, Mizushima-Sugano J, Hata H, Ota T, Isogai T, Tanaka T, Nakamura Y, Suyama A, Sakaki Y, Morishita S, Okubo K, Sugano S. Identification and characterization of the potential promoter regions of 1031 kinds of human genes. Genome Res 2001, 11:677-684. 10.1101/gr.GR-1640R, 311086, 11337467.
61. Fujita PA, Rhead B, Zweig AS, Hinrichs AS, Karolchik D, Cline MS, Goldman M, Barber GP, Clawson H, Coelho A, Diekhans M, Dreszer TR, Giardine BM, Harte RA, Hillman-Jackson J, Hsu F, Kirkup V, Kuhn RM, Learned K, Li CH, Meyer LR, Pohl A, Raney BJ, Rosenbloom KR, Smith KE, Haussler D, Kent WJ. The UCSC genome browser database: update 2011. Nucleic Acids Res 2011, 39:D876-D882. 10.1093/nar/gkq963, 3242726, 20959295.