Hepatic src-1 activity orchestrates transcriptional circuitries of amino acid pathways with potential relevance for human metabolic pathogenesis

Molecular Endocrinology

Volumn 28, Issue 10, 2014, Pages 1707-1718

  Tannour Louet, Mounia ^a   York, Brian ^a   Ke, Tang ^a   Stashi, Erin ^a   Bouguerra, Hichem ^c,d   Zhou, Suoling ^a   Yu, Hui ^a   Wong, Lee Jun C ^a   Stevens, Robert D ^b   Xu, Jianming ^a   Newgard, Christopher B ^b   O’malley, Bert W ^a   Louet, Jean Francois ^a,d  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b DUKE UNIVERSITY MEDICAL CENTER   (United States)

^c UNIVERSITY OF TUNIS EL MANAR   (Tunisia)

^d CENTRE MÉDITERRANÉEN DE MÉDECINE MOLÉCULAIRE C3M   (France)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; STEROID RECEPTOR COACTIVATOR 1; TYROSINE; TYROSINE AMINOTRANSFERASE;

ADULT; AMINO ACID BLOOD LEVEL; AMINO ACID METABOLISM; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CATABOLISM; CISTRON; CLINICAL FEATURE; CONTROLLED STUDY; CORNEA DISEASE; ENZYME ACTIVITY; GENE DELETION; GENE EXPRESSION; GENETIC RISK; GENETIC VARIABILITY; HETEROZYGOTE; IDIOPATHIC DISEASE; LIVER; MALE; METABOLIC REGULATION; METABOLOMICS; MISSENSE MUTATION; MOUSE; NONHUMAN; NUCLEOTIDE BINDING SITE; QUANTITATIVE ANALYSIS; TRANSCRIPTION REGULATION; TYROSINEMIA; ANIMAL; DISEASE MODEL; DISORDERS OF AMINO ACID AND PROTEIN METABOLISM; GENETIC TRANSCRIPTION; GENETICS; KNOCKOUT MOUSE; METABOLISM;

AMINO ACID METABOLISM, INBORN ERRORS; AMINO ACIDS; ANIMALS; DISEASE MODELS, ANIMAL; LIVER; MICE; MICE, KNOCKOUT; NUCLEAR RECEPTOR COACTIVATOR 1; TRANSCRIPTION, GENETIC; TYROSINE TRANSAMINASE;

EID: 84907638046     PISSN: 08888809     EISSN: 19449917     Source Type: Journal    
DOI: 10.1210/me.2014-1083     Document Type: Article

References (52)

1. Adams SH. Emerging perspectives on essential amino Acid metabolism in obesity and the insulin-resistant state. Adv Nutr. 2011; 2(6):445-456.
2. Newgard CB. Interplay between lipids and branched-chain amino acids in development of insulin resistance. Cell Metab. 2012;15: 606-614.
3. Vander Heiden MG, Cantley LC, Thompson CB. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science. 2009;324(5930):1029-1033.
4. Eagle H. Nutrition needs of mammalian cells in tissue culture. Science. 1955;122(3168):501-514.
5. Wise DR, Thompson CB. Glutamine addiction: a new therapeutic target in cancer. Trends Biochem Sci. 2010;35(8):427-433.
6. Nicklin P, Bergman P, Zhang B, et al. Bidirectional transport of amino acids regulates mTOR and autophagy. Cell. 2009;136(3): 521-534.
7. Kroemer G, Pouyssegur J. Tumor cell metabolism: cancer’s Achilles’ heel. Cancer Cell. 2008;13(6):472-482.
8. Vander Heiden MG. Targeting cancer metabolism: a therapeutic window opens. Nat Rev Drug Discov. 2011;10(9):671-684.
9. Newgard CB, An J, Bain JR, et al. A branched-chain amino acidrelated metabolic signature that differentiates obese and lean humans and contributes to insulin resistance. Cell Metab. 2009;9(4): 311-326.
10. Wang TJ, Larson MG, Vasan RS, et al. Metabolite profiles and the risk of developing diabetes. Nat Med. 2011;17(4):448-453.
11. Grandison RC, Piper MD, Partridge L. Amino-acid imbalance explains extension of lifespan by dietary restriction in Drosophila. Nature. 2009;462(7276):1061-1064.
12. Spiegelman BM. Transcriptional control of mitochondrial energy metabolism through the PGC1 coactivators. Novartis Found Symp. 2007;287:60-63; discussion 63-69.
13. Feige JN, Auwerx J. Transcriptional coregulators in the control of energy homeostasis. Trends Cell Biol. 2007.
14. York B, O’Malley BW. Steroid receptor coactivator (SRC) family: masters of systems biology. J Biol Chem. 2010;285(50):38743-38750.
15. Xu J, Wu RC, O’Malley BW. Normal and cancer-related functions of the p160 steroid receptor co-activator (SRC) family. Nat Rev Cancer. 2009;9(9):615-630.
16. Louet JF, Chopra AR, Sagen JV, et al. The coactivator SRC-1 is an essential coordinator of hepatic glucose production. Cell Metab. 2010;12(6):606-618.
17. Louet JF, Coste A, Amazit L, et al. Oncogenic steroid receptor coactivator-3 is a key regulator of the white adipogenic program. Proc Natl Acad Sci USA. 2006;103(47):17868-17873.
18. Louet JF, O’Malley BW. Coregulators in adipogenesis: what could we learn from the SRC (p160) coactivator family? Cell Cycle. 2007; 6(20):2448-2452.
19. Picard F, Géhin M, Annicotte J, et al. SRC-1 and TIF2 control energy balance between white and brown adipose tissues. Cell. 2002;111(7):931-941.
20. York B, Reineke EL, Sagen JV, et al. Ablation of steroid receptor coactivator-3 resembles the human CACT metabolic myopathy. Cell Metab. 2012;15(5):752-763.
21. Chopra AR, Louet JF, Saha P, et al. Absence of the SRC-2 coactivator results in a glycogenopathy resembling Von Gierke’s disease. Science. 2008;322(5906):1395-1399.
22. Ferrara CT, Wang P, Neto EC, et al. Genetic networks of liver metabolism revealed by integration of metabolic and transcriptional profiling. PLoS Genet. 2008;4(3):e1000034.
23. Ronnebaum SM, Ilkayeva O, Burgess SC, et al. A pyruvate cycling pathway involving cytosolic NADP-dependent isocitrate dehydrogenase regulates glucose-stimulated insulin secretion. J Biol Chem. 2006;281(41):30593-30602.
24. An J, Muoio DM, Shiota M, et al. Hepatic expression of malonyl- CoA decarboxylase reverses muscle, liver and whole-animal insulin resistance. Nat Med. 2004;10(3):268-274.
25. McLean CY, Bristor D, Hiller M, et al. GREAT improves functional interpretation of cis-regulatory regions. Nat Biotechnol. 2010;28(5):495-501.
26. Bain JR, Stevens RD, Wenner BR, Ilkayeva O, Muoio DM, Newgard CB. Metabolomics applied to diabetes research: moving from information to knowledge. Diabetes. 2009;58(11):2429 -2443.
27. Newgard CB, Attie AD. Getting biological about the genetics of diabetes. Nat Med. 2010;16(4):388-391.
28. Chopra AR, Kommagani R, Saha P, et al. Cellular energy depletion resets whole-body energy by promoting coactivator-mediated dietary fuel absorption. Cell Metab. 2011;13(1):35-43.
29. Desvergne B, Michalik L, Wahli W. Transcriptional regulation of metabolism. Physiol Rev. 2006;86(2):465-514.
30. Cole TJ, Blendy JA, Monaghan AP, et al. Targeted disruption of the glucocorticoid receptor gene blocks adrenergic chromaffin cell development and severely retards lung maturation. Genes Dev. 1995; 9(13):1608-1621.
31. Scott CR. The genetic tyrosinemias. Am J Med Genet C Semin Med Genet. 2006;142C(2):121-126.
32. Nitsch D, Schütz G. The distal enhancer implicated in the developmental regulation of the tyrosine aminotransferase gene is bound by liver-specific and ubiquitous factors. Mol Cell Biol. 1993;13(8): 4494-4504.
33. 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(12):5479-5483.
34. Nitsch D, Boshart M, Schütz G. Extinction of tyrosine aminotransferase gene activity in somatic cell hybrids involves modification and loss of several essential transcriptional activators. Genes Dev. 1993;7(2):308-319.
35. Handschin C, Spiegelman BM. Peroxisome proliferator-activated receptor coactivator γ coactivators, energy homeostasis, and metabolism. Endocr Rev. 2006;27(7):728-735.
36. Zieske JD. Corneal development associated with eyelid opening. Int J Dev Biol. 2004;48(8-9):903-911.
37. Mehere P, Han Q, Lemkul JA, Vavricka CJ, Robinson H, Bevan DR, Li J. Tyrosine aminotransferase: biochemical and structural properties and molecular dynamics simulations. Protein Cell. 2010; 1(11):1023-1032.
38. Hartmaier RJ, Richter AS, Gillihan RM, et al. A SNP in steroid receptor coactivator-1 disrupts a GSK3γ phosphorylation site and is associated with altered tamoxifen response in bone. Mol Endocrinol. 2012;26(2):220-227.
39. O’Malley BW. Molecular biology. Little molecules with big goals. Science. 2006;313(5794):1749-1750.
40. Rosenfeld MG, Lunyak VV, Glass CK. Sensors and signals: a coactivator/ corepressor/epigenetic code for integrating signal-dependent programs of transcriptional response. Genes Dev. 2006; 20(11):1405-1428.
41. Lonard DM, O’malley BW. Nuclear receptor coregulators: judges, juries, and executioners of cellular regulation. Mol Cell. 2007; 27(5):691-700.
42. O’Malley BW. Masters of the genome. Nat Rev Mol Cell Biol. 2010;11(5):311.
43. York B, Yu C, Sagen JV, et al. Reprogramming the posttranslational code of SRC-3 confers a switch in mammalian systems biology. Proc Natl Acad Sci USA. 2010;107(24):11122-11127.
44. Hayhurst GP, Lee YH, Lambert G, Ward JM, Gonzalez FJ. Hepatocyte nuclear factor 4α (nuclear receptor 2A1) is essential for maintenance of hepatic gene expression and lipid homeostasis. Mol Cell Biol. 2001;21(4):1393-1403.
45. Fu L, Dong SS, Xie YW, et al. Down-regulation of tyrosine aminotransferase at a frequently deleted region 16q22 contributes to the pathogenesis of hepatocellular carcinoma. Hepatology. 2010; 51(5):1624-1634.
46. Ferguson AA, Roy S, Kormanik KN, et al. TATN-1 mutations reveal a novel role for tyrosine as a metabolic signal that influences developmental decisions and longevity in Caenorhabditis elegans. PLoS Genet. 2013;9(12):e1004020.
47. Xu J, Li Q. Review of the in vivo functions of the p160 steroid receptor coactivator family. Mol Endocrinol. 2003;17(9):1681-1692.
48. Wu RC, Feng Q, Lonard DM, O’Malley BW. SRC-3 coactivator functional lifetime is regulated by a phospho-dependent ubiquitin time clock. Cell. 2007;129(6):1125-1140.
49. Lonard DM, Lanz RB, O’Malley BW. Nuclear receptor coregulators and human disease. Endocr Rev. 2007;28(5):575-587.
50. Stashi E, York B, O’Malley BW. Steroid receptor coactivators: servants and masters for control of systems metabolism. Trends Endocrinol Metab. 2014;25(7):337-347.
51. Jungas RL, Halperin ML, Brosnan JT. Quantitative analysis of amino acid oxidation and related gluconeogenesis in humans. Physiol Rev. 1992;72(2):419-448.
52. Stashi E, Lanz RB, Mao J, et al. SRC-2 is an essential coactivator for orchestrating metabolism and circadian rhythm. Cell Rep. 2014; 6(4):633-645.