Metabolic network topology reveals transcriptional regulatory signatures of type 2 diabetes

PLoS Computational Biology

Volumn 6, Issue 4, 2010, Pages

  Zelezniak, Aleksej ^a   Pers, Tune H ^a,b   Soares, Simão ^a,c   Patti, Mary Elizabeth ^d   Patil, Kiran Raosaheb ^a  

^a TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

^b The Capital Region   (Denmark)

^c UNIVERSITY OF MINHO   (Portugal)

^d JOSLIN DIABETES CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING SITES; BIOMOLECULES; INSULIN; METABOLISM; PHYSIOLOGY; TRANSCRIPTION; TRANSCRIPTION FACTORS;

INSULIN RESISTANCE; INSULIN SECRETION; METABOLIC GENES; METABOLIC NETWORK; MOLECULAR MECHANISM; NETWORK TOPOLOGY; PROMOTER REGION; TRANSCRIPTOMICS; TYPE 2 DIABETES MELLITUS; TYPE-2 DIABETES;

METABOLITES;

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; NICOTINAMIDE ADENINE DINUCLEOTIDE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR NRF1;

ALGORITHM; ARTICLE; BINDING SITE; CARBON METABOLISM; CLUSTER ANALYSIS; GENE REGULATORY NETWORK; LIPID METABOLISM; METABOLIC REGULATION; METABOLOMICS; NON INSULIN DEPENDENT DIABETES MELLITUS; OXIDATIVE PHOSPHORYLATION; PROMOTER REGION; SKELETAL MUSCLE; TRANSCRIPTION REGULATION; BIOLOGICAL MODEL; DNA MICROARRAY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC DATABASE; GENETIC TRANSCRIPTION; GENETICS; HUMAN; MALE; METABOLISM; METABOLOME; REGULATORY SEQUENCE;

ALGORITHMS; CLUSTER ANALYSIS; DATABASES, GENETIC; DIABETES MELLITUS, TYPE 2; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORKS; HUMANS; MALE; METABOLIC NETWORKS AND PATHWAYS; METABOLOME; MODELS, BIOLOGICAL; MUSCLE, SKELETAL; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; REGULATORY ELEMENTS, TRANSCRIPTIONAL; TRANSCRIPTION, GENETIC;

EID: 77952674482     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1000729     Document Type: Article

References (67)

1. Zimmet P, Alberti KG, Shaw J (2001) Global and societal implications of the diabetes epidemic. Nature 414: 782-787.
2. Simpson RW, Shaw JE, Zimmet PZ (2003) The prevention of type 2 diabetes- lifestyle change or pharmacotherapy? A challenge for the 21st century. Diabetes Res Clin Pract 59: 165-180.
3. Shulman GI (2000) Cellular mechanisms of insulin resistance. J Clin Invest 106: 171-176.
4. Pehling G, Tessari P, Gerich JE, Haymond MW, Service FJ, et al. (1984) Abnormal meal carbohydrate disposition in insulin-dependent diabetes. Relative contributions of endogenous glucose production and initial splanchnic uptake and effect of intensive insulin therapy. J Clin Invest 74: 985-991.
5. Muoio DM, Newgard CB (2008) Molecular and metabolic mechanisms of insulin resistance and [beta]-cell failure in type 2 diabetes. Nat Rev Mol Cell Biol 9: 193-205.
6. Saltiel AR, Kahn CR (2001) Insulin signalling and the regulation of glucose and lipid metabolism. Nature 414: 799-806.
7. Kelley DE, He J, Menshikova EV, Ritov VB (2002) Dysfunction of mitochondria in human skeletal muscle in type 2 diabetes. Diabetes 51: 2944-2950.
8. Mootha VK, Lindgren CM, Eriksson KF, Subramanian A, Sihag S, et al. (2003) PGC-1alpha-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat Genet 34: 267-273.
9. Patti ME, Butte AJ, Crunkhorn S, Cusi K, Berria R, et al. (2003) Coordinated reduction of genes of oxidative metabolism in humans with insulin resistance and diabetes: Potential role of PGC1 and NRF1. Proc Natl Acad Sci U S A 100: 8466-8471.
10. Boden G (1996) Fatty acids and insulin resistance. Diabetes Care 19: 394-395.
11. Ueki K, Kondo T, Tseng YH, Kahn CR (2004) Central role of suppressors of cytokine signaling proteins in hepatic steatosis, insulin resistance, and the metabolic syndrome in the mouse. Proc Natl Acad Sci U S A 101: 10422-10427.
12. Sreekumar R, Halvatsiotis P, Schimke JC, Nair KS (2002) Gene Expression Profile in Skeletal Muscle of Type 2 Diabetes and the Effect of Insulin Treatment. 51: 1913-1920.
13. Yang X, Pratley RE, Tokraks S, Bogardus C, Permana PA (2002) Microarray profiling of skeletal muscle tissues from equally obese, non-diabetic insulinsensitive and insulin-resistant Pima Indians. Diabetologia 45: 1584-1593.
14. Patil KR, Nielsen J (2005) Uncovering transcriptional regulation of metabolism by using metabolic network topology. Proc Natl Acad Sci U S A 102: 2685-2689.
15. Seggewiss J, Becker K, Kotte O, Eisenacher M, Yazdi MR, et al. (2006) Reporter metabolite analysis of transcriptional profiles of a Staphylococcus aureus strain with normal phenotype and its isogenic hemB mutant displaying the small-colony-variant phenotype. J Bacteriol 188: 7765-7777.
16. David H, Hofmann G, Oliveira AP, Jarmer H, Nielsen J (2006) Metabolic network driven analysis of genome-wide transcription data from Aspergillus nidulans. Genome Biol 7: R108.
17. Capel F, Klimcakova E, Viguerie N, Roussel B, Vitkova M, et al. (2009) Macrophages and adipocytes in human obesity: adipose tissue gene expression and insulin sensitivity during calorie restriction and weight stabilization. Diabetes 58: 1558-1567.
18. Baxter CJ, Redestig H, Schauer N, Repsilber D, Patil KR, et al. (2007) The metabolic response of heterotrophic Arabidopsis cells to oxidative stress. Plant Physiol 143: 312-325.
19. Duarte NC, Becker SA, Jamshidi N, Thiele I, Mo ML, et al. (2007) Global reconstruction of the human metabolic network based on genomic and bibliomic data. Proc Natl Acad Sci U S A 104: 1777-1782.
20. Ma H, Sorokin A, Mazein A, Selkov A, Selkov E, et al. (2007) The Edinburgh human metabolic network reconstruction and its functional analysis. Mol Syst Biol 3: 135.
21. Roden M (2005) Muscle triglycerides and mitochondrial function: possible mechanisms for the development of type 2 diabetes. Int J Obes (Lond) 29 Suppl 2: S111-115.
22. Savage DB, Petersen KF, Shulman GI (2007) Disordered lipid metabolism and the pathogenesis of insulin resistance. Physiol Rev 87: 507-520.
23. Holland WL, Brozinick JT, Wang LP, Hawkins ED, Sargent KM, et al. (2007) Inhibition of ceramide synthesis ameliorates glucocorticoid-, saturated-fat-, and obesity-induced insulin resistance. Cell Metab 5: 167-179.
24. Chavez JA, Summers SA (2003) Characterizing the effects of saturated fatty acids on insulin signaling and ceramide and diacylglycerol accumulation in 3T3- L1 adipocytes and C2C12 myotubes. Arch Biochem Biophys 419: 101-109.
25. Salek RM, Maguire ML, Bentley E, Rubtsov DV, Hough T, et al. (2007) A metabolomic comparison of urinary changes in type 2 diabetes in mouse, rat, and human. Physiol Genomics 29: 99-108.
26. Newgard CB, An J, Bain JR, Muehlbauer MJ, Stevens RD, et al. (2009) A Branched-Chain Amino Acid-Related Metabolic Signature that Differentiates Obese and Lean Humans and Contributes to Insulin Resistance. Cell Metabolism 9: 311-326.
27. Fleischman A, Kron M, Systrom DM, Hrovat M, Grinspoon SK (2009) Mitochondrial Function and Insulin Resistance in Overweight and Normal- Weight Children. J Clin Endocrinol Metab.
28. Phielix E, Schrauwen-Hinderling VB, Mensink M, Lenaers E, Meex R, et al. (2008) Lower intrinsic ADP-stimulated mitochondrial respiration underlies in vivo mitochondrial dysfunction in muscle of male type 2 diabetic patients. Diabetes 57: 2943-2949.
29. Storey JD, Tibshirani R (2003) Statistical significance for genomewide studies. Proc Natl Acad Sci U S A 100: 9440-9445.
30. Bajaj M, Defronzo RA (2003) Metabolic and molecular basis of insulin resistance. J Nucl Cardiol 10: 311-323.
31. Itani SI, Ruderman NB, Schmieder F, Boden G (2002) Lipid-induced insulin resistance in human muscle is associated with changes in diacylglycerol, protein kinase C, and IkappaB-alpha. Diabetes 51: 2005-2011.
32. Patti ME, Corvera S, (2009) The Role of Mitochondria in the Pathogenesis of Type 2 Diabetes. Endo Reviews: In press.
33. Koves TR, Li P, An J, Akimoto T, Slentz D, et al. (2005) Peroxisome proliferator-activated receptor-gamma co-activator 1alpha-mediated metabolic remodeling of skeletal myocytes mimics exercise training and reverses lipidinduced mitochondrial inefficiency. J Biol Chem 280: 33588-33598.
34. Kersten S, Desvergne B, Wahli W (2000) Roles of PPARs in health and disease. Nature 405: 421-424.
35. Sen CK, Packer L (1996) Antioxidant and redox regulation of gene transcription. Faseb J 10: 709-720.
36. Scarpulla RC (2008) Nuclear control of respiratory chain expression by nuclear respiratory factors and PGC-1-related coactivator. Ann N Y Acad Sci 1147: 321-334.
37. Scarpulla RC (2006) Nuclear control of respiratory gene expression in mammalian cells. J Cell Biochem 97: 673-683.
38. Szendroedi J, Schmid AI, Chmelik M, Toth C, Brehm A, et al. (2007) Muscle mitochondrial ATP synthesis and glucose transport/phosphorylation in type 2 diabetes. PLoS Med 4: e154.
39. Petersen KF, Dufour S, Shulman GI (2005) Decreased insulin-stimulated ATP synthesis and phosphate transport in muscle of insulin-resistant offspring of type 2 diabetic parents. PLoS Med 2: e233.
40. Petersen KF, Befroy D, Dufour S, Dziura J, Ariyan C, et al. (2003) Mitochondrial dysfunction in the elderly: possible role in insulin resistance. Science 300: 1140-1142.
41. Ristow M, Zarse K, Oberbach A, Kloting N, Birringer M, et al. (2009) Antioxidants prevent health-promoting effects of physical exercise in humans. Proc Natl Acad Sci U S A 106: 8665-8670.
42. Brekasis D, Paget MS (2003) A novel sensor of NADH/NAD+ redox poise in Streptomyces coelicolor A3(2). Embo J 22: 4856-4865.
43. Zhang Q, Piston DW, Goodman RH (2002) Regulation of corepressor function by nuclear NADH. Science 295: 1895-1897.
44. Lin SJ, Defossez PA, Guarente L (2000) Requirement of NAD and SIR2 for lifespan extension by calorie restriction in Saccharomyces cerevisiae. Science 289: 2126-2128.
45. Anderson RM, Latorre-Esteves M, Neves AR, Lavu S, Medvedik O, et al. (2003) Yeast life-span extension by calorie restriction is independent of NAD fluctuation. Science 302: 2124-2126.
46. Rutter J, Reick M, Wu LC, McKnight SL (2001) Regulation of clock and NPAS2 DNA binding by the redox state of NAD cofactors. Science 293: 510-514.
47. Agarwal AK, Auchus RJ (2005) Minireview: cellular redox state regulates hydroxysteroid dehydrogenase activity and intracellular hormone potency. Endocrinology 146: 2531-2538.
48. Rodgers JT, Lerin C, Haas W, Gygi SP, Spiegelman BM, et al. (2005) Nutrient control of glucose homeostasis through a complex of PGC-1alpha and SIRT1. Nature 434: 113-118.
49. Cimini D, Patil KR, Schiraldi C, Nielsen J (2009) Global transcriptional response of Saccharomyces cerevisiae to the deletion of SDH3. BMC Syst Biol 3: 17.
50. Raghevendran V, Patil KR, Olsson L, Nielsen J (2006) Hap4 is not essential for activation of respiration at low specific growth rates in Saccharomyces cerevisiae. J Biol Chem 281: 12308-12314.
51. Schuurmans JM, Rossell SL, van Tuijl A, Bakker BM, Hellingwerf KJ, et al. (2008) Effect of hxk2 deletion and HAP4 overexpression on fermentative capacity in Saccharomyces cerevisiae. FEMS Yeast Res 8: 195-203.
52. He J, Watkins S, Kelley DE (2001) Skeletal muscle lipid content and oxidative enzyme activity in relation to muscle fiber type in type 2 diabetes and obesity. Diabetes 50: 817-823.
53. Daran-Lapujade P, Rossell S, van Gulik WM, Luttik MA, de Groot MJ, et al. (2007) The fluxes through glycolytic enzymes in Saccharomyces cerevisiae are predominantly regulated at posttranscriptional levels. Proc Natl Acad Sci U S A 104: 15753-15758.
54. Bruning T, Vamvakas S, Makropoulos V, Birner G (1998) Acute intoxication with trichloroethene: clinical symptoms, toxicokinetics, metabolism, and development of biochemical parameters for renal damage. Toxicol Sci 41: 157-165.
55. Laughter AR, Dunn CS, Swanson CL, Howroyd P, Cattley RC, et al. (2004) Role of the peroxisome proliferator-activated receptor alpha (PPARalpha) in responses to trichloroethylene and metabolites, trichloroacetate and dichloroacetate in mouse liver. Toxicology 203: 83-98.
56. Ramirez de Molina A, Gallego-Ortega D, Sarmentero J, Banez-Coronel M, Martin-Cantalejo Y, et al. (2005) Choline kinase is a novel oncogene that potentiates RhoA-induced carcinogenesis. Cancer Res 65: 5647-5653.
57. Banez-Coronel M, de Molina AR, Rodriguez-Gonzalez A, Sarmentero J, Ramos MA, et al. (2008) Choline kinase alpha depletion selectively kills tumoral cells. Curr Cancer Drug Targets 8: 709-719.
58. Oliveira AP, Patil KR, Nielsen J (2008) Architecture of transcriptional regulatory circuits is knitted over the topology of bio-molecular interaction networks. BMC Syst Biol 2: 17.
59. Cakir T, Patil KR, Onsan Z, Ulgen KO, Kirdar B, et al. (2006) Integration of metabolome data with metabolic networks reveals reporter reactions. Mol Syst Biol 2: 50.
60. Kummel A, Panke S, Heinemann M (2006) Putative regulatory sites unraveled by network-embedded thermodynamic analysis of metabolome data. Mol Syst Biol 2: 2006 0034.
61. Henry CS, Broadbelt LJ, Hatzimanikatis V (2007) Thermodynamics-based metabolic flux analysis. Biophys J 92: 1792-1805.
62. Ma H, Goryanin I (2008) Human metabolic network reconstruction and its impact on drug discovery and development. Drug Discov Today 13: 402-408.
63. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, et al. (2003) Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4: 249-264.
64. Gautier L, Cope L, Bolstad BM, Irizarry RA (2004) affy-analysis of Affymetrix GeneChip data at the probe level. Bioinformatics 20: 307-315.
65. Smyth GK (2004) Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3: Article3.
66. Matys V, Fricke E, Geffers R, Gossling E, Haubrock M, et al. (2003) TRANSFAC: transcriptional regulation, from patterns to profiles. Nucleic Acids Res 31: 374-378.
67. Marstrand TT, Frellsen J, Moltke I, Thiim M, Valen E, et al. (2008) Asap: a framework for over-representation statistics for transcription factor binding sites. PLoS ONE 3: e1623.