Transcriptional and Chromatin Regulation during Fasting - The Genomic Era

Trends in Endocrinology and Metabolism

Volumn 26, Issue 12, 2015, Pages 699-710

  Goldstein, Ido ^a   Hager, Gordon L ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

Author keywords

Chromatin; Fasting; Gluconeogenesis; Ketogenesis; Transcription factors

Indexed keywords

ACETYL COENZYME A; CCAAT ENHANCER BINDING PROTEIN; CELL NUCLEUS RECEPTOR; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; FIBROBLAST GROWTH FACTOR 21; FORKHEAD TRANSCRIPTION FACTOR; GLUCOCORTICOID RECEPTOR; GLUCOSE; GLYCEROL; GLYCOGEN; HEPATOCYTE NUCLEAR FACTOR 4ALPHA; KETONE BODY; LIVER X RECEPTOR; MUSCLE PROTEIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; PROTEIN P53; STEROL REGULATORY ELEMENT BINDING PROTEIN; THYROID HORMONE RECEPTOR; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR FKHRL1; CHROMATIN;

BINDING SITE; CHROMATIN; DIET RESTRICTION; ENERGY METABOLISM; FATTY ACID OXIDATION; FOOD DEPRIVATION; GENE CONTROL; GLUCONEOGENESIS; GLUCOSE BLOOD LEVEL; GLYCOGENOLYSIS; HISTONE METHYLATION; HISTONE MODIFICATION; HORMONAL REGULATION; HUMAN; KETOGENESIS; LIVER CELL; METABOLIC REGULATION; NONHUMAN; NUTRIENT AVAILABILITY; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DEGRADATION; REVIEW; TRANSCRIPTION REGULATION; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENOMICS; METABOLISM;

CHROMATIN; FASTING; GENE EXPRESSION REGULATION; GENOMICS; HUMANS; TRANSCRIPTION, GENETIC;

EID: 84949570407     PISSN: 10432760     EISSN: 18793061     Source Type: Journal    
DOI: 10.1016/j.tem.2015.09.005     Document Type: Review

References (96)

1. Cahill G.F. Fuel metabolism in starvation. Annu. Rev. Nutr. 2006, 26:1-22.
2. Derks T.G., et al. Inhibition of mitochondrial fatty acid oxidation in vivo only slightly suppresses gluconeogenesis but enhances clearance of glucose in mice. Hepatology 2008, 47:1032-1042.
3. Newman J.C., Verdin E. Ketone bodies as signaling metabolites. Trends Endocrinol. Metab. 2014, 25:42-52.
4. Rizza R.A. Pathogenesis of fasting and postprandial hyperglycemia in type 2 diabetes: implications for therapy. Diabetes 2010, 59:2697-2707.
5. Saltiel A.R. New perspectives into the molecular pathogenesis and treatment of type 2 diabetes. Cell 2001, 104:517-529.
6. Teshigawara K., et al. Role of Kruppel-like factor 15 in PEPCK gene expression in the liver. Biochem. Biophys. Res. Commun. 2005, 327:920-926.
7. Unger R.H., Roth M.G. A new biology of diabetes revealed by leptin. Cell Metab. 2015, 21:15-20.
8. Altarejos J.Y., Montminy M. CREB and the CRTC co-activators: sensors for hormonal and metabolic signals. Nat. Rev. Mol. Cell Biol. 2011, 12:141-151.
9. Chalkiadaki A., Guarente L. Sirtuins mediate mammalian metabolic responses to nutrient availability. Nat. Rev. Endocrinol. 2012, 8:287-296.
10. Mihaylova M.M., Shaw R.J. Metabolic reprogramming by class I and II histone deacetylases. Trends Endocrinol. Metab. 2013, 24:48-57.
11. Kimball C.P., Murlin J.R. Aqueous extracts of pancreas: III. Some precipitation reactions of insulin. J. Biol. Chem. 1923, 58:337-346.
12. Ravnskjaer K., et al. Glucagon regulates gluconeogenesis through KAT2B- and WDR5-mediated epigenetic effects. J. Clin. Invest. 2013, 123:4318-4328.
13. Tsai W.W., et al. PRMT5 modulates the metabolic response to fasting signals. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:8870-8875.
14. Krones-Herzig A., et al. Signal-dependent control of gluconeogenic key enzyme genes through coactivator-associated arginine methyltransferase 1. J. Biol. Chem. 2006, 281:3025-3029.
15. Tikhanovich I., et al. Forkhead box class O transcription factors in liver function and disease. J. Gastroenterol. Hepatol. 2013, 28(Suppl. 1):125-131.
16. Haeusler R.A., et al. FoxOs function synergistically to promote glucose production. J. Biol. Chem. 2010, 285:35245-35248.
17. Zhang K., et al. Hepatic suppression of Foxo1 and Foxo3 causes hypoglycemia and hyperlipidemia in mice. Endocrinology 2012, 153:631-646.
18. Xiong X., et al. Deletion of hepatic FoxO1/3/4 genes in mice significantly impacts on glucose metabolism through downregulation of gluconeogenesis and upregulation of glycolysis. PLoS ONE 2013, 8:e74340.
19. Haeusler R.A., et al. Integrated control of hepatic lipogenesis versus glucose production requires FoxO transcription factors. Nat. Commun. 2014, 5:5190.
20. Kim D.H., et al. FoxO6 integrates insulin signaling with gluconeogenesis in the liver. Diabetes 2011, 60:2763-2774.
21. Calabuig-Navarro V., et al. FoxO6 depletion attenuates hepatic gluconeogenesis and protects against fat-induced glucose disorder in mice. J. Biol. Chem. 2015, 290:15581-15594.
22. Zhao J., et al. FoxO3 coordinately activates protein degradation by the autophagic/lysosomal and proteasomal pathways in atrophying muscle cells. Cell Metab. 2007, 6:472-483.
23. Shimazu T., et al. Suppression of oxidative stress by beta-hydroxybutyrate, an endogenous histone deacetylase inhibitor. Science 2013, 339:211-214.
24. Kaestner K.H. The FoxA factors in organogenesis and differentiation. Curr. Opin. Genet. Dev. 2010, 20:527-532.
25. Wolfrum C., et al. Foxa2 regulates lipid metabolism and ketogenesis in the liver during fasting and in diabetes. Nature 2004, 432:1027-1032.
26. Zhang L., et al. Foxa2 integrates the transcriptional response of the hepatocyte to fasting. Cell Metab. 2005, 2:141-148.
27. Roesler W.J. The role of C/EBP in nutrient and hormonal regulation of gene expression. Annu. Rev. Nutr. 2001, 21:141-165.
28. Shen N., et al. The constitutive activation of Egr-1/C/EBPa mediates the development of type 2 diabetes mellitus by enhancing hepatic gluconeogenesis. Am. J. Pathol. 2015, 185:513-523.
29. Pan D., et al. The histone demethylase Jhdm1a regulates hepatic gluconeogenesis. PLoS Genet. 2012, 8:e1002761.
30. Louet J.F., et al. The coactivator SRC-1 is an essential coordinator of hepatic glucose production. Cell Metab. 2010, 12:606-618.
31. Goldstein I., Rotter V. Regulation of lipid metabolism by p53 - fighting two villains with one sword. Trends Endocrinol. Metab. 2012, 23:567-575.
32. Goldstein I., et al. p53 promotes the expression of gluconeogenesis-related genes and enhances hepatic glucose production. Cancer Metab. 2013, 1:9.
33. Wang S.J., et al. p53-Dependent regulation of metabolic function through transcriptional activation of pantothenate kinase-1 gene. Cell Cycle 2013, 12:753-761.
34. Goldstein I., et al. p53, a novel regulator of lipid metabolism pathways. J. Hepatol. 2012, 56:656-662.
35. Liu Y., et al. Ribosomal protein-Mdm2-p53 pathway coordinates nutrient stress with lipid metabolism by regulating MCD and promoting fatty acid oxidation. Proc. Natl. Acad. Sci. U.S.A. 2014, 111:E2414-E2422.
36. Zhang P., et al. Tumor suppressor p53 cooperates with SIRT6 to regulate gluconeogenesis by promoting FoxO1 nuclear exclusion. Proc. Natl. Acad. Sci. U.S.A. 2014, 111:10684-10689.
37. Yi J., Luo J. SIRT1 and p53, effect on cancer, senescence and beyond. Biochim. Biophys. Acta 2010, 1804:1684-1689.
38. Liu Y., et al. A fasting inducible switch modulates gluconeogenesis via activator/coactivator exchange. Nature 2008, 456:269-273.
39. Britton S.W., Silvette H. Some observations on the cortico-adrenal hormone. Science 1931, 73:373-374.
40. Patel R., et al. Minireview: new molecular mediators of glucocorticoid receptor activity in metabolic tissues. Mol. Endocrinol. 2014, 28:999-1011.
41. Opherk C., et al. Inactivation of the glucocorticoid receptor in hepatocytes leads to fasting hypoglycemia and ameliorates hyperglycemia in streptozotocin-induced diabetes mellitus. Mol. Endocrinol. 2004, 18:1346-1353.
42. Zinker B., et al. Liver-selective glucocorticoid receptor antagonism decreases glucose production and increases glucose disposal, ameliorating insulin resistance. Metab. Clin. Exp. 2007, 56:380-387.
43. Kersten S. Integrated physiology and systems biology of PPARalpha. Mol. Metab. 2014, 3:354-371.
44. Bernal-Mizrachi C., et al. Dexamethasone induction of hypertension and diabetes is PPAR-alpha dependent in LDL receptor-null mice. Nat. Med. 2003, 9:1069-1075.
45. Steineger H.H., et al. Dexamethasone and insulin demonstrate marked and opposite regulation of the steady-state mRNA level of the peroxisomal proliferator-activated receptor (PPAR) in hepatic cells. Hormonal modulation of fatty-acid-induced transcription. Eur. J. Biochem. 1994, 225:967-974.
46. Lee H.Y., et al. PPAR-alpha and glucocorticoid receptor synergize to promote erythroid progenitor self-renewal. Nature 2015, 522:474-477.
47. Anik A., et al. Maturity-onset diabetes of the young (MODY): an update. J. Pediatr. Endocrinol. Metab. 2015, 28:251-263.
48. Jitrapakdee S. Transcription factors and coactivators controlling nutrient and hormonal regulation of hepatic gluconeogenesis. Int. J. Biochem. Cell Biol. 2012, 44:33-45.
49. Rhee J., et al. Regulation of hepatic fasting response by PPARgamma coactivator-1alpha (PGC-1): requirement for hepatocyte nuclear factor 4alpha in gluconeogenesis. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:4012-4017.
50. Dankel S.N., et al. cAMP-mediated regulation of HNF-4alpha depends on the level of coactivator PGC-1alpha. Biochim. Biophys. Acta 2010, 1803:1013-1019.
51. Mullur R., et al. Thyroid hormone regulation of metabolism. Physiol. Rev. 2014, 94:355-382.
52. Zhang Y., et al. Peroxisomal proliferator-activated receptor-gamma coactivator-1 alpha (PGC-1 alpha) enhances the thyroid hormone induction of carnitine palmitoyltransferase I (CPT-I alpha). J. Biol. Chem. 2004, 279:53963-53971.
53. Singh S.P., Snyder A.K. Effect of thyrotoxicosis on gluconeogenesis from alanine in the perfused rat liver. Endocrinology 1978, 102:182-187.
54. Jackson-Hayes L., et al. A thyroid hormone response unit formed between the promoter and first intron of the carnitine palmitoyltransferase-Ialpha gene mediates the liver-specific induction by thyroid hormone. J. Biol. Chem. 2003, 278:7964-7972.
55. Lee J.M., et al. Nutrient-sensing nuclear receptors coordinate autophagy. Nature 2014, 516:112-115.
56. Sinha R.A., et al. Thyroid hormone stimulates hepatic lipid catabolism via activation of autophagy. J. Clin. Invest. 2012, 122:2428-2438.
57. Shlyueva D., et al. Transcriptional enhancers: from properties to genome-wide predictions. Nat. Rev. Genet. 2014, 15:272-286.
58. Zhou V.W., et al. Charting histone modifications and the functional organization of mammalian genomes. Nat. Rev. Genet. 2011, 12:7-18.
59. Phuc Le P., et al. Glucocorticoid receptor-dependent gene regulatory networks. PLoS Genet. 2005, 1:e16.
60. Grontved L., et al. C/EBP maintains chromatin accessibility in liver and facilitates glucocorticoid receptor recruitment to steroid response elements. EMBO J. 2013, 32:1568-1583.
61. Everett L.J., et al. Integrative genomic analysis of CREB defines a critical role for transcription factor networks in mediating the fed/fasted switch in liver. BMC Genomics 2013, 14:337.
62. Zhang X., et al. Genome-wide analysis of cAMP-response element binding protein occupancy, phosphorylation, and target gene activation in human tissues, Proc. Natl. Acad. Sci. U.S.A. 2005, 102:4459-4464.
63. Ramadoss P., et al. Novel mechanism of positive versus negative regulation by thyroid hormone receptor beta1 (TRbeta1) identified by genome-wide profiling of binding sites in mouse liver. J. Biol. Chem. 2014, 289:1313-1328.
64. Grontved L., et al. Transcriptional activation by the thyroid hormone receptor through ligand-dependent receptor recruitment and chromatin remodelling. Nat. Commun. 2015, 6:7048.
65. Patel R., et al. LXRbeta is required for glucocorticoid-induced hyperglycemia and hepatosteatosis in mice. J. Clin. Invest. 2011, 121:431-441.
66. van der Meer D.L., et al. Profiling of promoter occupancy by PPARalpha in human hepatoma cells via ChIP-chip analysis. Nucleic Acids Res. 2010, 38:2839-2850.
67. Boergesen M., et al. Genome-wide profiling of liver X receptor, retinoid X receptor, and peroxisome proliferator-activated receptor alpha in mouse liver reveals extensive sharing of binding sites. Mol. Cell. Biol. 2012, 32:852-867.
68. McMullen P.D., et al. A map of the PPARalpha transcription regulatory network for primary human hepatocytes. Chem. Biol. Interact. 2014, 209:14-24.
69. Calkin A.C., Tontonoz P. Transcriptional integration of metabolism by the nuclear sterol-activated receptors LXR and FXR. Nat. Rev. Mol. Cell Biol. 2012, 13:213-224.
70. Shin D.J., et al. Genome-wide analysis of FoxO1 binding in hepatic chromatin: potential involvement of FoxO1 in linking retinoid signaling to hepatic gluconeogenesis. Nucleic Acids Res. 2012, 40:11499-11509.
71. Li Z., et al. Foxa1 and Foxa2 are essential for sexual dimorphism in liver cancer. Cell 2012, 148:72-83.
72. Johnson M.E., et al. Genome-wide analyses of ChIP-Seq derived FOXA2 DNA occupancy in liver points to genetic networks underpinning multiple complex traits. J. Clin. Endocrinol. Metab. 2014, 99:E1580-E1585.
73. Schmidt D., et al. Five-vertebrate ChIP-seq reveals the evolutionary dynamics of transcription factor binding. Science 2010, 328:1036-1040.
74. Voss T.C., et al. Dynamic exchange at regulatory elements during chromatin remodeling underlies assisted loading mechanism. Cell 2011, 146:544-554.
75. Pei L., et al. NR4A orphan nuclear receptors are transcriptional regulators of hepatic glucose metabolism. Nat. Med. 2006, 12:1048-1055.
76. Min A.K., et al. Orphan nuclear receptor Nur77 mediates fasting-induced hepatic fibroblast growth factor 21 expression. Endocrinology 2014, 155:2924-2931.
77. Seok S., et al. Transcriptional regulation of autophagy by an FXR-CREB axis. Nature 2014, 516:108-111.
78. Settembre C., et al. TFEB controls cellular lipid metabolism through a starvation-induced autoregulatory loop. Nat. Cell Biol. 2013, 15:647-658.
79. Longuet C., et al. The glucagon receptor is required for the adaptive metabolic response to fasting. Cell Metab. 2008, 8:359-371.
80. Lu Y., et al. Yin Yang 1 promotes hepatic gluconeogenesis through upregulation of glucocorticoid receptor. Diabetes 2013, 62:1064-1073.
81. Takashima M., et al. Role of KLF15 in regulation of hepatic gluconeogenesis and metformin action. Diabetes 2010, 59:1608-1615.
82. Gray S., et al. Regulation of gluconeogenesis by Kruppel-like factor 15. Cell Metab. 2007, 5:305-312.
83. Chen S., et al. Control of hepatic gluconeogenesis by the promyelocytic leukemia zinc finger protein. Mol. Endocrinol. 2014, 28:1987-1998.
84. Danno H., et al. The liver-enriched transcription factor CREBH is nutritionally regulated and activated by fatty acids and PPARalpha. Biochem. Biophys. Res. Commun. 2010, 391:1222-1227.
85. Lee M.W., et al. Regulation of hepatic gluconeogenesis by an ER-bound transcription factor, CREBH. Cell Metab. 2010, 11:331-339.
86. Bae K.H., et al. Alpha lipoic acid induces hepatic fibroblast growth factor 21 expression via up-regulation of CREBH. Biochem. Biophys. Res. Commun. 2014, 455:212-217.
87. Kim H., et al. Liver-enriched transcription factor CREBH interacts with peroxisome proliferator-activated receptor alpha to regulate metabolic hormone FGF21. Endocrinology 2014, 155:769-782.
88. Nakagawa Y., et al. Hepatic CREB3L3 controls whole-body energy homeostasis and improves obesity and diabetes. Endocrinology 2014, 155:4706-4719.
89. Badman M.K., et al. Hepatic fibroblast growth factor 21 is regulated by PPARalpha and is a key mediator of hepatic lipid metabolism in ketotic states. Cell Metab. 2007, 5:426-437.
90. Inagaki T., et al. Endocrine regulation of the fasting response by PPARalpha-mediated induction of fibroblast growth factor 21. Cell Metab. 2007, 5:415-425.
91. Patel R., et al. Glucocorticoids regulate the metabolic hormone FGF21 in a feed-forward loop. Mol. Endocrinol. 2015, 29:213-223.
92. Cheng X., et al. Fibroblast growth factor (Fgf) 21 is a novel target gene of the aryl hydrocarbon receptor (AhR). Toxicol. Appl. Pharmacol. 2014, 278:65-71.
93. De Sousa-Coelho A.L., et al. Activating transcription factor 4-dependent induction of FGF21 during amino acid deprivation. Biochem. J. 2012, 443:165-171.
94. Wang Y., et al. Regulation of FGF21 expression and secretion by retinoic acid receptor-related orphan receptor alpha. J. Biol. Chem. 2010, 285:15668-15673.
95. Cyphert H.A., et al. Activation of the farnesoid X receptor induces hepatic expression and secretion of fibroblast growth factor 21. J. Biol. Chem. 2012, 287:25123-25138.
96. Li H., et al. Sodium butyrate stimulates expression of fibroblast growth factor 21 in liver by inhibition of histone deacetylase 3. Diabetes 2012, 61:797-806.