A novel N-terminal domain may dictate the glucose response of mondo proteins

PLoS ONE

Volumn 7, Issue 4, 2012, Pages

  McFerrin, Lisa G ^a   Atchley, William R ^a  

^a NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL NUCLEUS RECEPTOR; CYTOPLASM PROTEIN; GLUTAMINE; PROLINE; PROTEIN MONDOA; STEROL REGULATORY ELEMENT BINDING PROTEIN 1; UNCLASSIFIED DRUG; BASIC HELIX LOOP HELIX LEUCINE ZIPPER TRANSCRIPTION FACTOR; GLUCOSE;

ALPHA HELIX; AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; COMPLEX FORMATION; COMPUTER MODEL; COMPUTER PREDICTION; DIMERIZATION; GENETIC CONSERVATION; GLUCOSE METABOLISM; LIPOGENESIS; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN SECONDARY STRUCTURE; STRUCTURE ANALYSIS; ANIMAL; CAENORHABDITIS ELEGANS; DROSOPHILA; HUMAN; METABOLISM; MOLECULAR GENETICS; MOUSE; NUCLEOTIDE SEQUENCE; PHOSPHORYLATION; PROTEIN TERTIARY STRUCTURE; SEQUENCE HOMOLOGY; TRANSCRIPTION INITIATION;

EUKARYOTA; PROKARYOTA; VERTEBRATA;

AMINO ACID SEQUENCE; ANIMALS; BASIC HELIX-LOOP-HELIX LEUCINE ZIPPER TRANSCRIPTION FACTORS; CAENORHABDITIS ELEGANS; CONSERVED SEQUENCE; DROSOPHILA; GLUCOSE; GLUTAMINE; HUMANS; LIPOGENESIS; MICE; MOLECULAR SEQUENCE DATA; PHOSPHORYLATION; PROLINE; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; SEQUENCE HOMOLOGY, AMINO ACID; TRANSCRIPTIONAL ACTIVATION;

EID: 84859593599     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0034803     Document Type: Article

References (84)

1. Luo W, Hu H, Chang R, Zhong J, Knabel M, et al. (2011) Pyruvate Kinase M2 Is a PHD3-Stimulated Coactivator for Hypoxia-Inducible Factor 1. Cell 145: 732-744.
2. Maddocks OD, Vousden KH, Metabolic regulation by p53. J Mol Med 89: 237-245.
3. Vander Heiden MG, Cantley LC, Thompson CB, (2009) Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 324: 1029-1033.
4. Postic C, Dentin R, Denechaud PD, Girard J, (2007) ChREBP, a transcriptional regulator of glucose and lipid metabolism. Annu Rev Nutr 27: 179-192.
5. Stoeckman AK, Ma L, Towle HC, (2004) Mlx is the functional heteromeric partner of the carbohydrate response element-binding protein in glucose regulation of lipogenic enzyme genes. J Biol Chem 279: 15662-15669.
6. Tabor DE, Kim JB, Spiegelman BM, Edwards PA, (1998) Transcriptional activation of the stearoyl-CoA desaturase 2 gene by sterol regulatory element-binding protein/adipocyte determination and differentiation factor 1. J Biol Chem 273: 22052-22058.
7. Magaña MM, Osborne TF, (1996) Two tandem binding sites for sterol regulatory element binding proteins are required for sterol regulation of fatty-acid synthase promoter. J Biol Chem 271: 32689-32694.
8. Rufo C, Teran-Garcia M, Nakamura MT, Koo SH, Towle HC, et al. (2001) Involvement of a unique carbohydrate-responsive factor in the glucose regulation of rat liver fatty-acid synthase gene transcription. J Biol Chem 276: 21969-21975.
9. Ma L, Robinson LN, Towle HC, (2006) ChREBP*Mlx is the principal mediator of glucose-induced gene expression in the liver. J Biol Chem 281: 28721-28730.
10. Sans C, Satterwhite D, Stoltzman C, Breen K, Ayer D, (2006) MondoA-Mlx Heterodimers Are Candidate Sensors of Cellular Energy Status: Mitochondrial Localization and Direct Regulation of Glycolysis. Molecular and Cellular Biology 26: 4863-4871.
11. Billin AN, Eilers AL, Coulter KL, Logan JS, Ayer DE, (2000) MondoA, a novel basic helix-loop-helix-leucine zipper transcriptional activator that constitutes a positive branch of a max-like network. Molecular and Cellular Biology 20: 8845-8854.
12. McFerrin LG, Atchley WR, Evolution of the Max and Mlx networks in animals. Genome Biol Evol 3: 915-937.
13. Yuan J, Tirabassi RS, Bush AB, Cole MD, (1998) The C. elegans MDL-1 and MXL-1 proteins can functionally substitute for vertebrate MAD and MAX. Oncogene 17: 1109-1118.
14. Ma L, Tsatsos NG, Towle HC, (2005) Direct role of ChREBP.Mlx in regulating hepatic glucose-responsive genes. J Biol Chem 280: 12019-12027.
15. Yamashita H, Takenoshita M, Sakurai M, Bruick RK, Henzel WJ, et al. (2001) A glucose-responsive transcription factor that regulates carbohydrate metabolism in the liver. Proc Natl Acad Sci USA 98: 9116-9121.
16. Eilers AL, Sundwall E, Lin M, Sullivan AA, Ayer DE, (2002) A novel heterodimerization domain, CRM1, and 14-3-3 control subcellular localization of the MondoA-Mlx heterocomplex. Molecular and Cellular Biology 22: 8514-8526.
17. Peterson C, Stoltzman C, Sighinolfi M, Han K, Ayer D, (2010) Glucose Controls Nuclear Accumulation, Promoter Binding, and Transcriptional Activity of the MondoA-Mlx Heterodimer. Molecular and Cellular Biology 30: 2887-2895.
18. Billin AN, Ayer DE, (2006) The Mlx network: evidence for a parallel Max-like transcriptional network that regulates energy metabolism. Curr Top Microbiol Immunol 302: 255-278.
19. Davies MN, O'Callaghan BL, Towle HC, (2008) Glucose activates ChREBP by increasing its rate of nuclear entry and relieving repression of its transcriptional activity. J Biol Chem 283: 24029-24038.
20. Stoltzman CA, Peterson CW, Breen KT, Muoio DM, Billin AN, et al. (2008) Glucose sensing by MondoA:Mlx complexes: a role for hexokinases and direct regulation of thioredoxin-interacting protein expression. Proc Natl Acad Sci USA 105: 6912-6917.
21. Li M, Chang B, Imamura M, Poungvarin N, Chan L, (2006) Glucose-dependent transcriptional regulation by an evolutionarily conserved glucose-sensing module. Diabetes 55: 1179-1189.
22. Li M, Chen W, Poungvarin N, Imamura M, Chan L, (2008) Glucose-Mediated Transactivation of Carbohydrate Response Element-Binding Protein Requires Cooperative Actions from Mondo Conserved Regions and Essential Trans-Acting Factor 14-3-3. Mol Endocrinol 22: 1658-1672.
23. Davies M, O'callaghan B, Towle H, (2010) Activation and Repression of Glucose-stimulated ChREBP Requires the Concerted Action of Multiple Domains within the MondoA Conserved Region AJP Endocrinology and Metabolism.
24. Cairo S, Merla G, Urbinati F, Ballabio A, Reymond A, (2001) WBSCR14, a gene mapping to the Williams-Beuren syndrome deleted region, is a new member of the Mlx transcription factor network. Human Molecular Genetics 10: 617-627.
25. Kawaguchi T, Takenoshita M, Kabashima T, Uyeda K, (2001) Glucose and cAMP regulate the L-type pyruvate kinase gene by phosphorylation/dephosphorylation of the carbohydrate response element binding protein. Proc Natl Acad Sci USA 98: 13710-13715.
26. Merla G, Howald C, Antonarakis SE, Reymond A, (2004) The subcellular localization of the ChoRE-binding protein, encoded by the Williams-Beuren syndrome critical region gene 14, is regulated by 14-3-3. Human Molecular Genetics 13: 1505-1514.
27. Tsatsos NG, Davies MN, O'Callaghan BL, Towle HC, (2008) Identification and function of phosphorylation in the glucose-regulated transcription factor ChREBP. Biochem J 411: 261-270.
28. Fukasawa M, Ge Q, Wynn R, Ishii S, Uyeda K, (2010) Coordinate regulation/localization of the carbohydrate responsive binding protein (ChREBP) by two nuclear export signal sites: Discovery of a new leucine-rich nuclear export signal site. Biochem Biophys Res Commun 391: 1166-1169.
29. Sakiyama H, Wynn RM, Lee WR, Fukasawa M, Mizuguchi H, et al. (2008) Regulation of nuclear import/export of carbohydrate response element-binding protein (ChREBP): interaction of an alpha-helix of ChREBP with the 14-3-3 proteins and regulation by phosphorylation. J Biol Chem 283: 24899-24908.
30. Kabashima T, Kawaguchi T, Wadzinski BE, Uyeda K, (2003) Xylulose 5-phosphate mediates glucose-induced lipogenesis by xylulose 5-phosphate-activated protein phosphatase in rat liver. Proc Natl Acad Sci USA 100: 5107-5112.
31. Li M, Chen W, Harmancey R, Nuotio-Antar A, Imamura M, et al. (2010) Glucose-6-phosphate mediates activation of the carbohydrate responsive binding protein (ChREBP). Biochem Biophys Res Commun pp. 6.
32. Matés JM, Segura JA, Campos-Sandoval JA, Lobo C, Alonso L, et al. (2009) Glutamine homeostasis and mitochondrial dynamics. Int J Biochem Cell Biol 41: 2051-2061.
33. Tong X, Zhao F, Mancuso A, Gruber JJ, Thompson CB, (2009) The glucose-responsive transcription factor ChREBP contributes to glucose-dependent anabolic synthesis and cell proliferation. Proc Natl Acad Sci USA 106: 21660-21665.
34. Capra JA, Singh M, (2007) Predicting functionally important residues from sequence conservation. Bioinformatics 23: 1875-1882.
35. Nolte RT, Wisely GB, Westin S, Cobb JE, Lambert MH, et al. (1998) Ligand binding and co-activator assembly of the peroxisome proliferator-activated receptor-gamma. Nature 395: 137-143.
36. Odom DT, Zizlsperger N, Gordon DB, Bell GW, Rinaldi NJ, et al. (2004) Control of pancreas and liver gene expression by HNF transcription factors. Science 303: 1378-1381.
37. Xu J, Christian B, Jump DB, (2006) Regulation of rat hepatic L-pyruvate kinase promoter composition and activity by glucose, n-3 polyunsaturated fatty acids, and peroxisome proliferator-activated receptor-alpha agonist. J Biol Chem 281: 18351-18362.
38. Zhang P, Metukuri M, Bindom S, Prochownik E, O'doherty R, et al. (2010) c-Myc Is Required for the ChREBP-Dependent Activation of Glucose-Responsive Genes. Mol Endocrinol pp. 13.
39. Burke SJ, Collier JJ, Scott DK, (2009) cAMP opposes the glucose-mediated induction of the L-PK gene by preventing the recruitment of a complex containing ChREBP, HNF4alpha, and CBP. FASEB J 23: 2855-2865.
40. Schleiff E, (2000) Signals and receptors-the translocation machinery on the mitochondrial surface. J Bioenerg Biomembr 32: 55-66.
41. Chacinska A, Koehler CM, Milenkovic D, Lithgow T, Pfanner N, (2009) Importing mitochondrial proteins: machineries and mechanisms. Cell 138: 628-644.
42. Emanuelsson O, Brunak S, von Heijne G, Nielsen H, (2007) Locating proteins in the cell using TargetP, SignalP and related tools. Nat Protoc 2: 953-971.
43. Tsatsos NG, Towle HC, (2006) Glucose activation of ChREBP in hepatocytes occurs via a two-step mechanism. Biochem Biophys Res Commun 340: 449-456.
44. Pickett C, Breen K, Ayer D, (2007) A C. elegans Myc-like network cooperates with semaphorin and Wnt signaling pathways to control cell migration. Developmental Biology 310: 226-239.
45. de Luis O, Valero MC, Jurado LA, (2000) WBSCR14, a putative transcription factor gene deleted in Williams-Beuren syndrome: complete characterisation of the human gene and the mouse ortholog. Eur J Hum Genet 8: 215-222.
46. Rohl CA, Strauss CE, Misura KM, Baker D, (2004) Protein structure prediction using Rosetta. Meth Enzymol 383: 66-93.
47. Ashkenazy H, Erez E, Martz E, Pupko T, Ben-Tal N, (2010) ConSurf 2010: calculating evolutionary conservation in sequence and structure of proteins and nucleic acids. Nucleic Acids Res 38: W529-W533.
48. Kay BK, Williamson MP, Sudol M, (2000) The importance of being proline: the interaction of proline-rich motifs in signaling proteins with their cognate domains. FASEB J 14: 231-241.
49. Guo L, Han A, Bates DL, Cao J, Chen L, (2007) Crystal structure of a conserved N-terminal domain of histone deacetylase 4 reveals functional insights into glutamine-rich domains. Proc Natl Acad Sci USA 104: 4297-4302.
50. Piskacek S, Gregor M, Nemethova M, Grabner M, Kovarik P, et al. (2007) Nine-amino-acid transactivation domain: establishment and prediction utilities. Genomics 89: 756-768.
51. Dong X, Biswas A, Süel KE, Jackson LK, Martinez R, et al. (2009) Structural basis for leucine-rich nuclear export signal recognition by CRM1. Nature 458: 1136-1141.
52. Ryan JF, Burton PM, Mazza ME, Kwong GK, Mullikin JC, et al. (2006) The cnidarian-bilaterian ancestor possessed at least 56 homeoboxes: evidence from the starlet sea anemone, Nematostella vectensis. Genome Biol 7: R64.
53. Ottmann C, Yasmin L, Weyand M, Veesenmeyer JL, Diaz MH, et al. (2007) Phosphorylation-independent interaction between 14-3-3 and exoenzyme S: from structure to pathogenesis. EMBO J 26: 902-913.
54. Gould CM, Diella F, Via A, Puntervoll P, Gemünd C, et al. (2010) ELM: the status of the 2010 eukaryotic linear motif resource. Nucleic Acids Research 38: D167-180.
55. Sharrocks AD, Yang SH, Galanis A, (2000) Docking domains and substrate-specificity determination for MAP kinases. Trends in Biochemical Sciences 25: 448-453.
56. Tanoue T, Maeda R, Adachi M, Nishida E, (2001) Identification of a docking groove on ERK and p38 MAP kinases that regulates the specificity of docking interactions. EMBO J 20: 466-479.
57. Raman M, Chen W, Cobb MH, (2007) Differential regulation and properties of MAPKs. Oncogene 26: 3100-3112.
58. Sakiyama H, Fujiwara N, Noguchi T, Eguchi H, Yoshihara D, et al. (2010) The role of O-linked GlcNAc modification on the glucose response of ChREBP. Biochem Biophys Res Commun pp. 6.
59. Escriva H, Langlois MC, Mendonça RL, Pierce R, Laudet V, (1998) Evolution and diversification of the nuclear receptor superfamily. Ann N Y Acad Sci 839: 143-146.
60. Poupeau A, Postic C, Cross-regulation of hepatic glucose metabolism via ChREBP and Nuclear Receptors. Biochim Biophys Acta.
61. Crooks GE, Hon G, Chandonia JM, Brenner SE, (2004) WebLogo: a sequence logo generator. Genome Research 14: 1188-1190.
62. Shannon CE, (1951) Prediction and entropy of printed English. The Bell System Technical Journal 30: 50-64.
63. Atchley WR, Terhalle W, Dress A, (1999) Positional dependence, cliques, and predictive motifs in the bHLH protein domain. J Mol Evol 48: 501-516.
64. Landau M, Mayrose I, Rosenberg Y, Glaser F, Martz E, et al. (2005) ConSurf 2005: the projection of evolutionary conservation scores of residues on protein structures. Nucleic Acids Research 33: W299-W302.
65. Gattiker A, Gasteiger E, Bairoch A, (2002) ScanProsite: a reference implementation of a PROSITE scanning tool. Appl Bioinformatics 1: 107-108.
66. Aleshin AE, Kirby C, Liu X, Bourenkov GP, Bartunik HD, et al. (2000) Crystal structures of mutant monomeric hexokinase I reveal multiple ADP binding sites and conformational changes relevant to allosteric regulation. J Mol Biol 296: 1001-1015.
67. Kamata K, Mitsuya M, Nishimura T, Eiki J, Nagata Y, (2004) Structural basis for allosteric regulation of the monomeric allosteric enzyme human glucokinase. Structure 12: 429-438.
68. Mulichak AM, Wilson JE, Padmanabhan K, Garavito RM, (1998) The structure of mammalian hexokinase-1. Nat Struct Biol 5: 555-560.
69. Regni C, Shackelford GS, Beamer LJ, (2006) Complexes of the enzyme phosphomannomutase/phosphoglucomutase with a slow substrate and an inhibitor. Acta Crystallogr Sect F Struct Biol Cryst Commun 62: 722-726.
70. Zhang G, Dai J, Wang L, Dunaway-Mariano D, Tremblay LW, et al. (2005) Catalytic cycling in beta-phosphoglucomutase: a kinetic and structural analysis. Biochemistry 44: 9404-9416.
71. Graham Solomons JT, Zimmerly EM, Burns S, Krishnamurthy N, Swan MK, et al. (2004) The crystal structure of mouse phosphoglucose isomerase at 1.6A resolution and its complex with glucose 6-phosphate reveals the catalytic mechanism of sugar ring opening. Journal of Molecular Biology 342: 847-860.
72. Cosgrove MS, Gover S, Naylor CE, Vandeputte-Rutten L, Adams MJ, et al. (2000) An examination of the role of asp-177 in the His-Asp catalytic dyad of Leuconostoc mesenteroides glucose 6-phosphate dehydrogenase: X-ray structure and pH dependence of kinetic parameters of the D177N mutant enzyme. Biochemistry 39: 15002-15011.
73. Kotaka M, Gover S, Vandeputte-Rutten L, Au SW, Lam VM, et al. (2005) Structural studies of glucose-6-phosphate and NADP+ binding to human glucose-6-phosphate dehydrogenase. Acta Crystallogr D Biol Crystallogr 61: 495-504.
74. Teplyakov A, Obmolova G, Badet-Denisot MA, Badet B, (1999) The mechanism of sugar phosphate isomerization by glucosamine 6-phosphate synthase. Protein Sci 8: 596-602.
75. Teplyakov A, Obmolova G, Badet B, Badet-Denisot MA, (2001) Channeling of ammonia in glucosamine-6-phosphate synthase. Journal of Molecular Biology 313: 1093-1102.
76. Nakaishi Y, Bando M, Shimizu H, Watanabe K, Goto F, et al. (2009) Structural analysis of human glutamine:fructose-6-phosphate amidotransferase, a key regulator in type 2 diabetes. FEBS Lett 583: 163-167.
77. Combet C, Blanchet C, Geourjon C, Deléage G, (2000) NPS@: network protein sequence analysis. Trends Biochem Sci 25: 147-150.
78. Porollo A, Meller J, (2007) Versatile annotation and publication quality visualization of protein complexes using POLYVIEW-3D. BMC Bioinformatics 8: 316.
79. Ginalski K, Elofsson A, Fischer D, Rychlewski L, (2003) 3D-Jury: a simple approach to improve protein structure predictions. Bioinformatics 19: 1015-1018.
80. DiMaio F, Terwilliger TC, Read RJ, Wlodawer A, Oberdorfer G, et al. Improved molecular replacement by density- and energy-guided protein structure optimization. Nature 473: 540-543.
81. Malmström L, Riffle M, Strauss CE, Chivian D, Davis TN, et al. (2007) Superfamily assignments for the yeast proteome through integration of structure prediction with the gene ontology. PLoS Biol 5: e76.
82. Riffle M, Malmström L, Davis TN, (2005) The Yeast Resource Center Public Data Repository. Nucleic Acids Res 33: D378-382.
83. Eswar N, Webb B, Marti-Renom MA, Madhusudhan MS, Eramian D, et al. (2006) Comparative protein structure modeling using Modeller. Curr Protoc Bioinformatics Chapter 5: Unit 5.6.
84. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, et al. (2004) UCSF Chimera-a visualization system for exploratory research and analysis. J Comput Chem 25: 1605-1612.