13C metabolic flux analysis shows that resistin impairs the metabolic response to insulin in L6E9 myotubes

BMC Systems Biology

Volumn 8, Issue 1, 2014, Pages

  Guzmán, Shirley ^a   Marin, Silvia ^a   Miranda, Anibal ^a   Selivanov, Vitaly A ^a   Centelles, Josep J ^a   Harmancey, Romain ^b   Smih, Fatima ^b   Turkieh, Annie ^b   Durocher, Yves ^c   Zorzano, Antonio ^a,d   Rouet, Philippe ^b   Cascante, Marta ^a  

^a UNIVERSITY OF BARCELONA   (Spain)

^b Université de Toulouse   (France)

^c NATIONAL RESEARCH COUNCIL CANADA   (Canada)

^d INSTITUTE FOR RESEARCH IN BIOMEDICINE   (Spain)

Author keywords

Bioinformatics; Fluxomics; Glucose metabolism; Insulin resistance; Resistin; Tracer based metabolomics

Indexed keywords

CARBON; GLUCOSE; INSULIN; PHOSPHOENOLPYRUVATE CARBOXYKINASE (ATP); PYRUVATE DEHYDROGENASE; RESISTIN;

ANIMAL; BIOLOGY; COMPUTER PROGRAM; METABOLIC FLUX ANALYSIS; METABOLISM; PROCEDURES; RAT; SKELETAL MUSCLE;

ANIMALS; CARBON ISOTOPES; COMPUTATIONAL BIOLOGY; GLUCOSE; INSULIN; METABOLIC FLUX ANALYSIS; MUSCLE FIBERS, SKELETAL; PHOSPHOENOLPYRUVATE CARBOXYKINASE (ATP); PYRUVATE DEHYDROGENASE (LIPOAMIDE); RATS; RESISTIN; SOFTWARE;

EID: 84907260800     PISSN: None     EISSN: 17520509     Source Type: Journal    
DOI: 10.1186/s12918-014-0109-z     Document Type: Article

References (48)

1. Sorensen TI. The changing lifestyle in the world. Body weight and what else?. Diabetes Care 2000, 23(Suppl 2):B1-B4. 10860183.
2. Lavie CJ, Milani RV, Ventura HO. Obesity and cardiovascular disease: risk factor, paradox, and impact of weight loss. J Am Coll Cardiol 2009, 53:1925-1932. 10.1016/j.jacc.2008.12.068, 19460605.
3. Wijnhoven TM, van Raaij JM, Spinelli A, Rito AI, Hovengen R, Kunesova M, Starc G, Rutter H, Sjoberg A, Petrauskiene A, O'Dwyer U, Petrova S, Farrugia SV, Wauters M, Yngve A, Rubana IM, Breda J. WHO European Childhood Obesity Surveillance Initiative 2008: weight, height and body mass index in 6-9-year-old children. Pediatr Obes 2013, 8:79-97. 10.1111/j.2047-6310.2012.00090.x, 23001989.
4. Poyrazoglu S, Bas F, Darendeliler F. Metabolic syndrome in young people. Curr Opin Endocrinol Diabetes Obes 2014, 21:56-63. 10.1097/01.med.0000436414.90240.2c, 24247648.
5. Chen L, Magliano DJ, Zimmet PZ. The worldwide epidemiology of type 2 diabetes mellitus-present and future perspectives. Nat Rev Endocrinol 2012, 8:228-236. 10.1038/nrendo.2011.183.
6. Gauthier MS, Ruderman NB. Adipose tissue inflammation and insulin resistance: all obese humans are not created equal. Biochem J 2010, 430:e1-e4. 10.1042/BJ20101062, 20704568.
7. Lolmede K, Duffaut C, Zakaroff-Girard A, Bouloumie A. Immune cells in adipose tissue: key players in metabolic disorders. Diabetes Metabol 2011, 37:283-290. 10.1016/j.diabet.2011.03.002.
8. Donath MY, Shoelson SE. Type 2 diabetes as an inflammatory disease. Nat Rev Immunol 2011, 11:98-107. 10.1038/nri2925, 21233852.
9. Samaras K, Botelho NK, Chisholm DJ, Lord RV. Subcutaneous and visceral adipose tissue gene expression of serum adipokines that predict type 2 diabetes. Obesity 2010, 18:884-889. 10.1038/oby.2009.443, 20019678.
10. Cao H. Adipocytokines in obesity and metabolic disease. J Endocrinol 2014, 220:T47-T59. 10.1530/JOE-13-0339, 24403378.
11. Coelho M, Oliveira T, Fernandes R. Biochemistry of adipose tissue: an endocrine organ. Arch Med Sci 2013, 9:191-200. 10.5114/aoms.2013.33181, 23671428.
12. Holcomb IN, Kabakoff RC, Chan B, Baker TW, Gurney A, Henzel W, Nelson C, Lowman HB, Wright BD, Skelton NJ, Frantz GD, Tumas DB, Peale FV, Shelton DL, Hébert CC. FIZZ1, a novel cysteine-rich secreted protein associated with pulmonary inflammation, defines a new gene family. EMBO J 2000, 19:4046-4055. 10.1093/emboj/19.15.4046, 10921885.
13. Steppan CM, Bailey ST, Bhat S, Brown EJ, Banerjee RR, Wright CM, Patel HR, Ahima RS, Lazar MA. The hormone resistin links obesity to diabetes. Nature 2001, 409:307-312. 10.1038/35053000, 11201732.
14. Lazar MA. Resistin- and obesity-associated metabolic diseases. Horm Metab Res 2007, 39:710-716. 10.1055/s-2007-985897, 17952831.
15. Schwartz DR, Lazar MA. Human resistin: found in translation from mouse to man. Trends Endocrinol Metab 2011, 22:259-265. 21497511.
16. Qatanani M, Szwergold NR, Greaves DR, Ahima RS, Lazar MA. Macrophage-derived human resistin exacerbates adipose tissue inflammation and insulin resistance in mice. J Clin Invest 2009, 119:531-539. 10.1172/JCI37273, 19188682.
17. Park HK, Ahima RS. Resistin in rodents and humans. Diabetes Metab J 2013, 37:404-414. 10.4093/dmj.2013.37.6.404, 24404511.
18. DeFronzo RA. Lilly lecture 1987. The triumvirate: beta-cell, muscle, liver. A collusion responsible for NIDDM. Diabetes 1988, 37:667-687. 10.2337/diab.37.6.667, 3289989.
19. Fan HQ, Gu N, Liu F, Fei L, Pan XQ, Guo M, Chen RH, Guo XR. Prolonged exposure to resistin inhibits glucose uptake in rat skeletal muscles. Acta Pharmacol Sin 2007, 28:410-416. 10.1111/j.1745-7254.2007.00523.x, 17303005.
20. Jorgensen SB, Honeyman J, Oakhill JS, Fazakerley D, Stockli J, Kemp BE, Steinberg GR. Oligomeric resistin impairs insulin and AICAR-stimulated glucose uptake in mouse skeletal muscle by inhibiting GLUT4 translocation. Am J Physiol Endocrinol Metab 2009, 297:E57-E66. 10.1152/ajpendo.90744.2008, 19435854.
21. Moon B, Kwan JJ, Duddy N, Sweeney G, Begum N. Resistin inhibits glucose uptake in L6 cells independently of changes in insulin signaling and GLUT4 translocation. Am J Physiol Endocrinol Metab 2003, 285:E106-E115. 12618360.
22. Palanivel R, Maida A, Liu Y, Sweeney G. Regulation of insulin signalling, glucose uptake and metabolism in rat skeletal muscle cells upon prolonged exposure to resistin. Diabetologia 2006, 49:183-190. 10.1007/s00125-005-0060-z, 16341686.
23. Palanivel R, Sweeney G. Regulation of fatty acid uptake and metabolism in L6 skeletal muscle cells by resistin. FEBS Lett 2005, 579:5049-5054. 10.1016/j.febslet.2005.08.011, 16137686.
24. Satoh H, Nguyen MT, Miles PD, Imamura T, Usui I, Olefsky JM. Adenovirus-mediated chronic “ hyper-resistinemia“ leads to in vivo insulin resistance in normal rats. J Clin Invest 2004, 114:224-231. 10.1172/JCI20785, 15254589.
25. Dettmer K, Hammock BD. Metabolomics-a new exciting field within the “ omics“ sciences. Environ Health Perspect 2004, 112:A396-A397. 15159211.
26. Selivanov VA, Marin S, Lee PW, Cascante M. Software for dynamic analysis of tracer-based metabolomic data: estimation of metabolic fluxes and their statistical analysis. Bioinformatics 2006, 22:2806-2812. 10.1093/bioinformatics/btl484, 17000750.
27. DeFronzo RA. Insulin resistance: a multifaceted syndrome responsible for NIDDM, obesity, hypertension, dyslipidaemia and atherosclerosis. Neth J Med 1997, 50:191-197. 10.1016/S0300-2977(97)00012-0, 9175399.
28. Constantin-Teodosiu D. Regulation of muscle pyruvate dehydrogenase complex in insulin resistance: effects of exercise and dichloroacetate. Diabetes Metab J 2013, 37:301-314. 10.4093/dmj.2013.37.5.301, 24199158.
29. Huang B, Wu P, Bowker-Kinley MM, Harris RA. Regulation of pyruvate dehydrogenase kinase expression by peroxisome proliferator-activated receptor-alpha ligands, glucocorticoids, and insulin. Diabetes 2002, 51:276-283. 10.2337/diabetes.51.2.276, 11812733.
30. Crabtree B, Newsholme EA. The activities of phosphorylase, hexokinase, phosphofructokinase, lactate dehydrogenase and the glycerol 3-phosphate dehydrogenases in muscles from vertebrates and invertebrates. Biochem J 1972, 126:49-58. 4342385.
31. Hakimi P, Yang J, Casadesus G, Massillon D, Tolentino-Silva F, Nye CK, Cabrera ME, Hagen DR, Utter CB, Baghdy Y, Johnson DH, Wilson DL, Kirwan JP, Kalhan SC, Hanson RW. Overexpression of the cytosolic form of phosphoenolpyruvate carboxykinase (GTP) in skeletal muscle repatterns energy metabolism in the mouse. J Biol Chem 2007, 282:32844-32855. 10.1074/jbc.M706127200, 17716967.
32. Minet AD, Gaster M. Pyruvate carboxylase is expressed in human skeletal muscle. Biochem Biophys Res Commun 2010, 402:196-197. 10.1016/j.bbrc.2010.08.102, 20807508.
33. Selivanov VA, Meshalkina LE, Solovjeva ON, Kuchel PW, Ramos-Montoya A, Kochetov GA, Lee PW, Cascante M. Rapid simulation and analysis of isotopomer distributions using constraints based on enzyme mechanisms: an example from HT29 cancer cells. Bioinformatics 2005, 21:3558-3564. 10.1093/bioinformatics/bti573, 16002431.
34. Selivanov VA, Puigjaner J, Sillero A, Centelles JJ, Ramos-Montoya A, Lee PW, Cascante M. An optimized algorithm for flux estimation from isotopomer distribution in glucose metabolites. Bioinformatics 2004, 20:3387-3397. 10.1093/bioinformatics/bth412, 15256408.
35. Selivanov VA, Vizan P, Mollinedo F, Fan TW, Lee PW, Cascante M: Edelfosine-induced metabolic changes in cancer cells that precede the overproduction of reactive oxygen species and apoptosis. BMC Syst Biol 2010, 4:135.
36. de Mas IM, Selivanov VA, Marin S, Roca J, Oresic M, Agius L, Cascante M: Compartmentation of glycogen metabolism revealed from 13C isotopologue distributions. BMC Syst Biol 2011, 5:175.
37. Rosen ED, Spiegelman BM. Adipocytes as regulators of energy balance and glucose homeostasis. Nature 2006, 444:847-853. 10.1038/nature05483, 17167472.
38. Suarez E, Bach D, Cadefau J, Palacin M, Zorzano A, Guma A. A novel role of neuregulin in skeletal muscle. Neuregulin stimulates glucose uptake, glucose transporter translocation, and transporter expression in muscle cells. J Biol Chem 2001, 276:18257-18264. 10.1074/jbc.M008100200, 11278386.
39. van Winden W, Verheijen P, Heijnen S. Possible pitfalls of flux calculations based on (13)C-labeling. Metab Eng 2001, 3:151-162. 10.1006/mben.2000.0174, 11289791.
40. Lee FN, Zhang L, Zheng D, Choi WS, Youn JH. Insulin suppresses PDK-4 expression in skeletal muscle independently of plasma FFA. Am J Physiol Endocrinol Metab 2004, 287:E69-E74. 10.1152/ajpendo.00461.2003, 15026305.
41. Quinn PG, Yeagley D. Insulin regulation of PEPCK gene expression: a model for rapid and reversible modulation. Curr Drug Targets Immune Endocr Metabol Disord 2005, 5:423-437. 10.2174/156800805774912962, 16375695.
42. Cifani C, Durocher Y, Pathak A, Penicaud L, Smih F, Massi M, Rouet P, Polidori C. Possible common central pathway for resistin and insulin in regulating food intake. Acta Physiol 2009, 196:395-400. 10.1111/j.1748-1716.2008.01949.x.
43. Marin S, Lee WN, Bassilian S, Lim S, Boros LG, Centelles JJ, FernAndez-Novell JM, Guinovart JJ, Cascante M. Dynamic profiling of the glucose metabolic network in fasted rat hepatocytes using [1,2-13C2]glucose. Biochem J 2004, 381:287-294. 10.1042/BJ20031737, 15032751.
44. Vizan P, Sanchez-Tena S, Alcarraz-Vizan G, Soler M, Messeguer R, Pujol MD, Lee WN, Cascante M. Characterization of the metabolic changes underlying growth factor angiogenic activation: identification of new potential therapeutic targets. Carcinogenesis 2009, 30:946-952. 10.1093/carcin/bgp083, 19369582.
45. Lee WN, Byerley LO, Bergner EA, Edmond J. Mass isotopomer analysis: theoretical and practical considerations. Biol Mass Spectrom 1991, 20:451-458. 10.1002/bms.1200200804, 1768701.
46. Harmancey R, Senard JM, Rouet P, Pathak A, Smih F. Adrenomedullin inhibits adipogenesis under transcriptional control of insulin. Diabetes 2007, 56:553-563. 10.2337/db06-0857, 17327422.
47. Schmittgen TD, Zakrajsek BA. Effect of experimental treatment on housekeeping gene expression: validation by real-time, quantitative RT-PCR. J Biochem Biophys Methods 2000, 46:69-81. 10.1016/S0165-022X(00)00129-9, 11086195.
48. Aerts JL, Gonzales MI, Topalian SL. Selection of appropriate control genes to assess expression of tumor antigens using real-time RT-PCR. BioTechniques 2004, 36:84-86. 88, 90-81, 14740490.