Compartmentation of glycogen metabolism revealed from 13C isotopologue distributions

BMC Systems Biology

Volumn 5, Issue , 2011, Pages

  Marin de Mas, Igor ^a   Selivanov, Vitaly A ^a,b   Marin, Silvia ^a   Roca, Josep ^a   Orešič, Matej ^c   Agius, Loranne ^d   Cascante, Marta ^a  

^a UNIVERSITY OF BARCELONA   (Spain)

^b MOSCOW STATE UNIVERSITY   (Russian Federation)

^c UNIVERSITY OF HELSINKI   (Finland)

^d NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 80054972207     PISSN: None     EISSN: 17520509     Source Type: Journal    
DOI: 10.1186/1752-0509-5-175     Document Type: Article

References (55)

1. Irving CS, Wong WW, Shulman RJ, Smith EO, Klein PD. [13C]bicarbonate kinetics in humans: intra- vs interindividual variations. Am J Physiol 1983, 245:R190-202.
2. Chance EM, Seeholzer SH, Kobayashi K, Williamson JR. Mathematical analysis of isotope labeling in the citric acid cycle with applications to 13C NMR studies in perfused rat hearts. J Biol Chem 1983, 258:13785-94.
3. Fan TWM, Lane AN, Higashi RM, Farag MA, Gao H, Bousamra M, Miller DM. Altered regulation of metabolic pathways in human lung cancer discerned by (13)C stable isotope-resolved metabolomics (SIRM). Mol Cancer 2009, 8:41. 10.1186/1476-4598-8-41, 2717907, 19558692.
4. Amaral AI, Teixeira AP, Martens S, Bernal V, Sousa MF, Alves PM. Metabolic alterations induced by ischemia in primary cultures of astrocytes: merging 13C NMR spectroscopy and metabolic flux analysis. J Neurochem 2010, 113:735-748. 10.1111/j.1471-4159.2010.06636.x, 20141568.
5. Selivanov VA, Vizán 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. 10.1186/1752-0509-4-135, 2984393, 20925932.
6. Jouhten P, Pitkänen E, Pakula T, Saloheimo M, Penttilä M, Maaheimo H. 13C-metabolic flux ratio and novel carbon path analyses confirmed that Trichoderma reesei uses primarily the respirative pathway also on the preferred carbon source glucose. BMC Syst Biol 2009, 3:104. 10.1186/1752-0509-3-104, 2776023, 19874611.
7. Jouhten P, Rintala E, Huuskonen A, Tamminen A, Toivari M, Wiebe M, Ruohonen L, Penttilä M, Maaheimo H. Oxygen dependence of metabolic fluxes and energy generation of Saccharomyces cerevisiae CEN.PK113-1A. BMC Syst Biol 2008, 2:60. 10.1186/1752-0509-2-60, 2507709, 18613954.
8. Aboka FO, Heijnen JJ, van Winden WA. Dynamic 13C-tracer study of storage carbohydrate pools in aerobic glucose-limited Saccharomyces cerevisiae confirms a rapid steady-state turnover and fast mobilization during a modest stepup in the glucose uptake rate. FEMS Yeast Res 2009, 9:191-201. 10.1111/j.1567-1364.2008.00465.x, 19220865.
9. Fendt SM, Sauer U. Transcriptional regulation of respiration in yeast metabolizing differently repressive carbon substrates. BMC Syst Biol 2010, 4:12. 10.1186/1752-0509-4-12, 2847992, 20167065.
10. Wiechert W. 13C metabolic flux analysis. Metab Eng 2001, 3:195-206. 10.1006/mben.2001.0187, 11461141.
11. 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.
12. Selivanov VA, Meshalkina LE, Solovjeva ON, Kuchel PW, Ramos-Montoya A, Kochetov GA, Lee PWN, 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.
13. Schaub J, Mauch K, Reuss M. Metabolic flux analysis in Escherichia coli by integrating isotopic dynamic and isotopic stationary 13C labeling data. Biotechnol Bioeng 2008, (99):1170-85.
14. Wahl SA, Nöh K, Wiechert W. 13C labeling experiments at metabolic nonstationary conditions: an exploratory study. BMC Bioinformatics 2008, 9:152. 10.1186/1471-2105-9-152, 2373788, 18366666.
15. Selivanov VA, Votyakova TV, Pivtoraiko VN, Zeak J, Sukhomlin T, Trucco M, Roca J, Cascante M. Reactive oxygen species production by forward and reverse electron fluxes in the mitochondrial respiratory chain. PLoS Comput Biol 2011, 7:e1001115. 10.1371/journal.pcbi.1001115, 3068929, 21483483.
16. Zamboni N, Sauer U. Novel biological insights through metabolomics and 13C-flux analysis. Curr Opin Microbiol 2009, 12:553-558. 10.1016/j.mib.2009.08.003, 19744879.
17. 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.
18. Cornish-Bowden A, Cardenas ML. Channeling can affect concentrations of metabolic intermediates at constant net flux - artifact or reality. Eur J Biochem 1993, 213:87-92. 10.1111/j.1432-1033.1993.tb17737.x, 8477736.
19. Mendes P, Kell DB, Westerhoff HV. Channelling can decrease pool size. Eur J Biochem 1992, 204:257-266. 10.1111/j.1432-1033.1992.tb16632.x, 1740137.
20. Atkinson D. Conservation of solvent capacity. Cellular Energy Metabolism and its Regulation. Academic Press NY 1977, 13-31.
21. Meyer FM, Gerwig J, Hammer E, Herzberg C, Commichau FM, Völker U, Stülke J. Physical interactions between tricarboxylic acid cycle enzymes in Bacillus subtilis: evidence for a metabolon. Metab Eng 2011, 13:18-27. 10.1016/j.ymben.2010.10.001, 20933603.
22. Hardin CD, Finder DR. Glycolytic flux in permeabilized freshly isolated vascular smooth muscle cells. Am J Physiol 1998, 274:C88-C96.
23. Shearer G, Lee JC, Koo J, Kohl DH. Quantitative estimation of channeling from early glycolytic intermediates to CO in intact Escherichia coli. FEBS J 2005, 272:3260-3269. 10.1111/j.1742-4658.2005.04712.x, 15978033.
24. Cascante M, Centelles JJ, Agius L. Use of alpha-toxin from Staphylococcus aureus to test for channelling of intermediates of glycolysis between glucokinase and aldolase in hepatocytes. Biochem J 2000, 352:899-905. 10.1042/0264-6021:3520899, 1221532, 11104701.
25. Huang X, Holden HM, Raushel FM. Channeling of substrates and intermediates in enzyme-catalyzed reactions. Annual Review of Biochemistry 2001, 70:149-180. 10.1146/annurev.biochem.70.1.149, 11395405.
26. Kleijn RJ, van Winden WA, van Gulik WM, Heijnen JJ. Revisiting the 13C-label distribution of the non-oxidative branch of the pentose phosphate pathway based upon kinetic and genetic evidence. FEBS J 2005, 272:4970-4982. 10.1111/j.1742-4658.2005.04907.x, 16176270.
27. Zamboni N. 13C metabolic flux analysis in complex systems. Curr Opin Biotechnol 2011, 22:103-108. 10.1016/j.copbio.2010.08.009, 20833526.
28. Marin S, Lee WP, 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, 1133787, 15032751.
29. Press WH, Flannery BP, Teukolsky SA, Vetterling WT. Numerical Recipes in C: The Art of Scientific Computing. Cambridge University Press NY 2002,
30. Flanigan I, Collins JG, Arora KK, MacLeod JK, Williams JF. Exchange reactions catalyzed by group-transferring enzymes oppose the quantitation and the unravelling of the identify of the pentose pathway. Eur J Biochem 1993, 213:477-485. 10.1111/j.1432-1033.1993.tb17784.x, 8477719.
31. Rose IA, Warms JV, Kuo DJ. Concentration and partitioning of intermediates in the fructose bisphosphate aldolase reaction Comparison of the muscle and liver enzymes. J Biol Chem 1987, 262:692-701.
32. Nikerel IE, van Winden WA, Verheijen PJ, Heijnen JJ. Model reduction and a priori kinetic parameter identifiability analysis using metabolome time series for metabolic reaction networks with linlog kinetics. Metab Eng 2009, (11):20-30.
33. Xiong W, Liu L, Wu C, Yang C, Wu Q. 13C-tracer and gas chromatography-mass spectrometry analyses reveal metabolic flux distribution in the oleaginous microalga Chlorella protothecoides. Plant Physiol 2010, 154:1001-11. 10.1104/pp.110.158956, 2948989, 20720172.
34. Tang Y, Pingitore F, Mukhopadhyay A, Phan R, Hazen TC, Keasling JD. Pathway confirmation and flux analysis of central metabolic pathways in Desulfovibrio vulgaris hildenborough using gas chromatography-mass spectrometry and Fourier transform-ion cyclotron resonance mass spectrometry. J Bacteriol 2007, 189:940-9. 10.1128/JB.00948-06, 1797301, 17114264.
35. Richardson AD, Yang C, Osterman A, Smith JW. Central carbon metabolism in the progression of mammary carcinoma. Breast Cancer Res Treat 2008, 110:297-307. 10.1007/s10549-007-9732-3, 2440942, 17879159.
36. Rich TC, Fagan KA, Nakata H, Schaack J, Cooper DM, Karpen JW. Cyclic nucleotide-gated channels colocalize with adenylyl cyclase in regions of restricted cAMP diffusion. J Gen Physiol 2000, 116:147-161. 10.1085/jgp.116.2.147, 2229499, 10919863.
37. Karpen JWT, Rich C. The fourth dimension in cellular signaling. Science 2001, 293:2204-2205. 10.1126/science.293.5538.2204, 11569497.
38. Meléndez-Hevia E, Guinovart JJ, Cascante M. The role of channelling in glycogen metabolism. In: Chanelling in intermediary metabolism. Portland Press London 1997, 269-291.
39. Selivanov VA, Alekseev AE, Hodgson DM, Dzeja PP, Terzic A. Nucleotide-gated KATP channels integrated with creatine and adenylate kinases: amplification, tuning and sensing of energetic signals in the compartmentalized cellular environment. Mol Cell Biochem 2004, 256-257:243-256. 2760266, 14977185.
40. Abraham MR, Selivanov VA, Hodgson DM, Pucar D, Zingman LV, Wieringa B, Dzeja PP, Alekseev AE, Terzic A. Coupling of cell energetics with membrane metabolic sensing. Integrative signaling through creatine kinase phosphotransfer disrupted by M-CK gene knock-out. J Biol Chem 2002, 277:24427-24434. 10.1074/jbc.M201777200, 11967264.
41. Selivanov VA, Krause S, Roca J, Cascante M. Modeling of spatial metabolite distributions in the cardiac sarcomere. Biophys J 2007, 92:3492-2500. 10.1529/biophysj.106.101352, 1853159, 17325002.
42. Brown KS, Sethna JP. Statistical mechanical approaches to models with many poorly known parameters. Phys Rev 2003, E 68.
43. Battogtokh D, Asch DK, Case ME, Arnold J, Schuttler B. An ensemble method for identifying regulatory circuits with special reference to the qa gene cluster of Neurospora crassa. Proc Natl Acad Sci USA 2002, 99:16904-16909. 10.1073/pnas.262658899, 139242, 12477937.
44. Gutenkunst RN, Waterfall JJ, Casey FP, Brown KS, Myers CR, Sethna JP. Universally sloppy parameter senitivities in systems biology models. PloS Comput Biol 2007, 3:1871-1878. 2000971, 17922568.
45. Gomez-Cabrero D, Compte A, Tegner J. Workflow for generating competing hypothesis from models with parameter uncertainty. Interface Focus 2011,
46. Fritzson PA. Principles of Object-Oriented Modeling and Simulation with Modelica. IEEE Press NY 2004, 21.
47. Fernández-Novell JM, Ariño J, Guinovart JJ. Effects of glucose on the activation and translocation of glycogen synthase in diabetic rat hepatocytes. Eur J Biochem 1994, 226:665-67188. 10.1111/j.1432-1033.1994.tb20094.x, 8001583.
48. Chan TM, Exton JH. A rapid method for the determination of glycogen content and radioactivity in small quantities of tissue or isolated hepatocytes. Anal Biochem 1976, 71:96-105. 10.1016/0003-2697(76)90014-2, 1275237.
49. Kunst A, Draeger B, Ziegenhorn J. D-Glucose; UV-methods with Hexolinase and Glucose-6-phosphate Dehydrogenase. In Methods of enzymatic analysis 1984, 6:163-172.
50. Passoneau JV, Lowry OH. Enzymatic analysis: a practical guide. The Humana Press Inc 1993,
51. Tserng KY, Gilfillan CA, Kalhan SC. Determination of carbon-13 labeled lactate in blood by gas chromatography/mass spectrometry. Anal Chem 1984, 56:517-523. 10.1021/ac00267a049, 6711822.
52. Katz J, Lee WN, Wals PA, Bergner EA. Studies of glycogen synthesis and the Krebs cycle by mass isotopomer analysis with [U-13C]glucose in rats. J Biol Chem 1989, 264:12994-13004.
53. Kurland IJ, Alcivar A, Bassilian S, Lee WNP. Loss of [13C]glycerol carbon via the pentose cycle. Implications for gluconeogenesis measurement by mass isotoper distribution analysis. J Biol Chem 2000, 275:36787-36793. 10.1074/jbc.M004739200, 10960476.
54. Lee WP, Edmond J, Bassilian S, Morrow J. Mass isotopomer study of glutamine oxidation and synthesis in primary culture of astrocytes. Develop Neurosci 1996, 18:469-477.
55. Lee W-NP, 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.