Improving the description of metabolic networks: The TCA cycle as example

FASEB Journal

Volumn 26, Issue 9, 2012, Pages 3625-3636

  Stobbe, Miranda D ^a,d   Houten, Sander M ^a   Van Kampen, Antoine H C ^a,b,c,d   Wanders, Ronald J A ^a   Moerlan, Perry D ^a,d  

^a ACADEMIC MEDICAL CENTER   (Netherlands)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

^c UNIVERSITY OF AMSTERDAM   (Netherlands)

^d NETHERLANDS BIOINFORMATICS CENTRE   (Netherlands)

Author keywords

Community effort; Curation; Pathway database

Indexed keywords

ACONITATE HYDRATASE; CITRATE SYNTHASE; FUMARATE HYDRATASE; ISOCITRATE DEHYDROGENASE; MALATE DEHYDROGENASE; OXOGLUTARATE DEHYDROGENASE; SUCCINATE DEHYDROGENASE; SUCCINYL COENZYME A SYNTHETASE; TRICARBOXYLIC ACID;

DATA BASE; ENZYME ACTIVITY; GENE FUNCTION; HUMAN; METABOLISM; MITOCHONDRION; PRIORITY JOURNAL; PROFESSIONAL KNOWLEDGE; REVIEW;

CITRIC ACID CYCLE; HUMANS;

EID: 84865712588     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.11-203091     Document Type: Review

References (63)

1. DeBerardinis, R., and Thompson, C. (2012) Cellular metabolism and disease: what do metabolic outliers teach us? Cell 148, 1132-1144
2. Hanahan, D., and Weinberg, R. A. (2011) Hallmarks of cancer: the next generation. Cell 144, 646-674
3. Kanehisa, M., Goto, S., Sato, Y., Furumichi, M., and Tanabe, M. (2012) KEGG for integration and interpretation of large-scale molecular data sets. Nucleic Acids Res. 40, D109-D114
4. Karp, P. D., and Caspi, R. (2011) A survey of metabolic databases emphasizing the MetaCyc family. Arch. Toxicol. 85, 1015-1033
5. Oberhardt, M. A., Palsson, B. Ø., and Papin, J. A. (2009) Applications of genome-scale metabolic reconstructions. Mol.Syst. Biol. 5, 320
6. Rey, G., Cesbron, F., Rougemont, J., Reinke, H., Brunner, M., and Naef, F. (2011) Genome-wide and phase-specific DNA-binding rhythms of BMAL1 control circadian output functions in mouse liver. PLoS Biol. 9, e1000595
7. Radrich, K., Tsuruoka, Y., Dobson, P., Gevorgyan, A., Swainston, N., Baart, G., and Schwartz, J. M. (2010) Integration of metabolic databases for the reconstruction of genome-scale metabolic networks. BMC Syst. Biol. 4, 114
8. Herrgård, M. J., Swainston, N., Dobson, P., Dunn, W. B., Arga, K. Y., Arvas, M., Blüthgen, N., Borger, S., Costenoble, R., Heinemann, M., Hucka, M., Le Novère, N., Li, P., Liebermeister, W., Mo, M. L., Oliveira, A. P., Petranovic, D., Pettifer, S., Simeonidis, E., Smallbone, K., Spasie, I., Weichart, D., Brent, R., Broomhead, D. S., Westerhoff, H. V., Kürdar, B., Penttilä, M., Klipp, E., Palsson, B. Ø., Sauer, U., Oliver, S. G., Mendes, P., Nielsen, J., and Kell, D. B. (2008) A consensus yeast metabolic network reconstruction obtained from a community approach to systems biology. Nat. Biotechnol. 26, 1155-1160
9. Stobbe, M. D., Houten, S. M., Jansen, G. A., van Kampen, A. H. C., and Moerland, P. D. (2011) Critical assessment of human metabolic pathway databases: a stepping stone for future integration. BMC Syst. Biol. 5, 165
10. Duarte, N. C., Becker, S. A., Jamshidi, N., Thiele, I., Mo, M. L., Vo, T. D., Srivas, R., and Palsson, B. Ø. (2007) Global reconstruction of the human metabolic network based on genomic and bibliomic data. Proc. Natl. Acad. Sci. U. S. A. 104, 1777-1782
11. Croft, D., O'Kelly, G., Wu, G., Haw, R., Gillespie, M., Matthews, L., Caudy, M., Garapati, P., Gopinath, G., Jassal, B., Jupe, S., Kalatskaya, I., Mahajan, S., May, B., Ndegwa, N., Schmidt, E., Shamovsky, V., Yung, C., Birney, E., Hermjakob, H., D'Eustachio, P., and Stein, L. (2011) Reactome: a database of reactions, pathways and biological processes. Nucleic Acids Res.39, D691-D697
12. Krebs, H. A., and Johnson, W. A. (1937) The role of citric acid in intermediate metabolism in animal tissues. Enzymologia 4, 148-156
13. Porcelli, A. M., Ghelli, A., Zanna, C., Pinton, P., Rizzuto, R., and Rugolo, M. (2005) pH difference across the outer mitochondrial membrane measured with a green fluorescent protein mutant. Biochem. Biophys. Res. Commun. 326, 799-804
14. Llopis, J., McCaffery, J. M., Miyawaki, A., Farquhar, M. G., and Tsien, R. Y. (1998) Measurement of cytosolic, mitochondrial, and Golgi pH in single living cells with green fluorescent proteins. Proc. Natl. Acad. Sci. U. S. A. 95, 6803-6808
15. Hoek, J. B., Nicholls, D. G., Williamson, J. R. (1980) Determination of the mitochondrial protonmotive force in isolated hepatocytes. J. Biol. Chem. 255, 1458-1464
16. Greksak, M., Lopes-Cardozo, M., and van den Bergh, S. G. (1982) Citrate synthesis in intact rat-liver mitochondria is irreversible. Eur. J. Biochem. 122, 423-427
17. Hoppe, A., Hoffmann, S., and Holzhütter, H.-G. (2007) Including metabolite concentrations into flux balance analysis: thermodynamic realizability as a constraint on flux distributions in metabolic networks. BMC Syst. Biol. 1, 23
18. Krebs, H. A., and Holzach, O. (1952) The conversion of citrate into cis-aconitate and isocitrate in the presence of aconitase. Biochem. J. 52, 527-528
19. Lawson, A. M., Chalmers, R. A., and Watts, R. W. E. (1976) Urinary organic acids in man. I. Normal patterns. Clin. Chem. 22, 1283-1287
20. Gabriel, J. L., Zervos, P. R., and Plaut, G. W. E. (1986) Activity of purified NAD-specific isocitrate dehydrogenase at modulator and substrate concentrations approximating conditions in mitochondria. Metabolism 35, 661-667
21. Hoek, J. B., and Rydström, J. (1988) Physiological roles of nicotinamide nucleotide transhydrogenase. Biochem. J. 254, 1-10
22. Wise, D. R., Ward, P. S., Shay, J. E. S., Cross, J. R., Gruber, J. J., Sachdeva, U. M., Platt, J. M., DeMatteo, R. G., Simon, M. C., and Thompson, C. B. (2011) Hypoxia promotes isocitrate dehydro-genase-dependent carboxylation of α-ketoglutarate to citrate tosupport cell growth and viability. Proc. Natl. Acad. Sci. U. S. A.108, 19611-19616
23. Mullen, A. R., Wheaton, W. W., Jin, E. S., Chen, P. H., Sullivan, L. B., Cheng, T., Yang, Y., Linehan, W. M., Chandel, N. S., and DeBerardinis, R. J. (2012) Reductive carboxylation supports growth in tumour cells with defective mitochondria. Nature 481, 385-388
24. Sazanov, L. A., and Jackson, J. B. (1994) Proton-translocating transhydrogenase and NAD- and NADP-linked isocitrate dehydrogenases operate in a substrate cycle which contributes to fine regulation of the tricarboxylic acid cycle activity in mitochondria. FEBS Lett. 344, 109-116
25. Des Rosiers, C., Fernandez, C. A., David, F., and Brunengraber, H. (1994) Reversibility of the mitochondrial isocitrate dehydrogenase reaction in the perfused rat liver. Evidence from isotopomer analysis of citric acid cycle intermediates. J. Biol. Chem.269, 27179-27182
26. Comte, B., Vincent, G., Bouchard, B., Benderdour, M., and Des Rosiers, C. (2002) Reverse flux through cardiac NADP+-isocitrate dehydrogenase under normoxia and ischemia. Am. J.Physiol. Heart Circ. Physiol. 283, H1505-H1514
27. Hartong, D. T., Dange, M., McGee, T. L., Berson, E. L., Dryja, T. P., and Colman, R. F. (2008) Insights from retinitis pigmentosa into the roles of isocitrate dehydrogenases in the Krebs cycle. Nat. Genet. 40, 1230-1234
28. Ceccarelli, C., Grodsky, N. B., Ariyaratne, N., Colman, R. F., and Bahnson, B. J. (2002) Crystal structure of porcine mitochondrial NADP+-dependent isocitrate dehydrogenase complexed with Mn2+ and isocitrate. J. Biol. Chem. 277, 43454-43462
29. Siebert, G., Carsiotis, M., and Plaut, G. W. E. (1957) The enzymatic properties of isocitric dehydrogenase. J. Biol. Chem.226, 977-991
30. Ramakrishna, M., and Krishnaswamy, P. R. (1966) Formation of enzyme bound carbon dioxide in the reductive carboxylation of alpha-ketoglutarate by isocitrate dehydrogenase. Biochem. Biophys.Res. Commun. 25, 378-382
31. Plaut, G. W. E., and Sung, S. C. (1954) Diphosphopyridine nucleotide isocitric dehydrogenase from animal tissues. J. Biol.Chem. 207, 305-314
32. Sheu, K.-F. R., and Blass, J. P. (1999) The α- ketoglutaratedehydrogenase complex. Ann. N. Y. Acad. Sci. 893, 61-78
33. Liu, T. C., Kim, H., Arizmendi, C., Kitano, A., and Patel, M. S. (1993) Identification of two missense mutations in a dihydrolipoamide dehydrogenase-deficient patient. Proc. Natl. Acad. Sci.U. S. A. 90, 5186-5190
34. Bunik, V. I., and Degtyarev, D. (2008) Structure-function relationships in the 2-oxo acid dehydrogenase family: substrate-specific signatures and functional predictions for the 2-oxoglutarate dehydrogenase-like proteins. Proteins 71, 874-890
35. McCartney, R. G., Rice, J. E., Sanderson, S. J., Bunik, V., Lindsay, H., and Lindsay, J. G. (1998) Subunit interactions in the mammalian α-ketoglutarate dehydrogenase complex. Evidencefor direct association of the alpha-ketoglutarate dehydrogenase and dihydrolipoamide dehydrogenase components. J. Biol.Chem. 273, 24158-24164
36. Aral, B., Benelli, C., Ait-Ghezala, G., Amessou, M., Fouque, F., Maunoury, C., Créau, N., Kamoun, P., and Marsac, C. (1997) Mutations in PDX1, the human lipoyl-containing component X of the pyruvate dehydrogenase-complex gene on chromosome 11p1, in congenital lactic acidosis. Am. J. Hum. Genet. 61, 1318-1326
37. Johnson, J. D., Muhonen, W. W., and Lambeth, D. O. (1998) Characterization of the ATP- and GTP-specific succinyl-CoA synthetases in pigeon. J. Biol. Chem. 273, 27573-27579
38. Bierau, J., Lindhout, M., and Bakker, J. A. (2007) Pharmacogenetic significance of inosine triphosphatase. Pharmacogenomics 8, 1221-1228
39. Lambeth, D. O., Tews, K. N., Adkins, S., Frohlich, D., and Milavetz, B. I. (2004) Expression of two succinyl-CoA synthetases with different nucleotide specificities in mammalian tissues. J.Biol. Chem. 279, 36621-36624
40. Ostergaard, E., Christensen, E., Kristensen, E., Mogensen, B., Duno, M., Shoubridge, E. A., and Wibrand, F. (2007) Deficiency of the α subunit of succinate-coenzyme A ligase causes fatal infantile lactic acidosis with mitochondrial DNA depletion. Am.J. Hum. Genet. 81, 383-387
41. Mewies, M., McIntire, W. S., and Scrutton, N. S. (1998) Covalent attachment of flavin adenine dinucleotide (FAD) and flavin mononucleotide (FMN) to enzymes: the current state of affairs. Protein Sci. 7, 7-21
42. Fernandez, C. A., and Des Rosiers, C. (1995) Modeling of liver citric acid cycle and gluconeogenesis based on 13C mass isotopomer distribution analysis of intermediates. J. Biol. Chem. 270, 10037-10042
43. Des Rosiers, C., Donato, L. D., Comte, B., Laplante, A., Marcoux, C., David, F., Fernandez, C. A., and Brunengraber, H. (1995) Isotopomer analysis of citric acid cycle and gluconeogenesis in rat liver. Reversibility of isocitrate dehydrogenase and involvement of ATP-citrate lyase in gluconeogenesis. J. Biol.Chem. 270, 10027-10036
44. Romero, P., Wagg, J., Green, M. L., Kaiser, D., Krummenacker, M., and Karp, P. D. (2004) Computational prediction of human metabolic pathways from the complete human genome. Genome Biol. 6, R2
45. Berg, J. M., Tymocsko, J. L., and Stryer, L. (2012) Biochemistry,W.H. Freeman, New York
46. Pico, A. R., Kelder, T., van Iersel, M. P., Hanspers, K., Conklin, B. R., and Evelo, C. (2008) WikiPathways: pathway editing for the people. PLoS Biol. 6, e184
47. Antonov, A. V., Dietmann, S., and Mewes, H. W. (2008) KEGG spider: interpretation of genomics data in the context of the global gene metabolic network. Genome Biol. 9, R179
48. Jerby, L., Shlomi, T., and Ruppin, E. (2010) Computational reconstruction of tissue-specific metabolic models: application to human liver metabolism. Mol. Syst. Biol. 6, 401
49. Morgat, A., Coissac, E., Coudert, E., Axelsen, K. B., Keller, G., Bairoch, A., Bridge, A., Bougueleret, L., Xenarios, I., and Viari, A. (2012) UniPathway: a resource for the exploration and annotation of metabolic pathways. Nucleic Acids Res. 40, D761-D769
50. Thiele, I., Hyduke, D. R., Steeb, B., Fankam, G., Allen, D. K., Bazzani, S., Charusanti, P., Chen, F. C., Fleming, R. M., Hsiung, C. A., De Keersmaecker, S. C., Liao, Y. C., Marchal, K., Mo, M. L., Özdemir, E., Raghunathan, A., Reed, J. L., Shin, S. I., Sigurbjörnsdóttir, S., Steinmann, J., Sudarsan, S., Swainston, N., Thijs, I. M., Zengler, K., Palsson, B. Ø., Adkins, J., and Bumann, D. (2011) A community effort towards a knowledge-base and mathematical model of the human pathogen Salmonella typhimurium LT2. BMC Syst. Biol. 5, 8
51. Chindelevitch, L., Stanley, S., Hung, D., Regev, A., and Berger, B. (2012) MetaMerge: scaling up genome-scale metabolic reconstructions, with application to mycobacterium tuberculosis. Genome Biol. 13, R6
52. Rolfsson, O., Palsson, B. Ø., and Thiele, I. (2011) The human metabolic reconstruction Recon 1 directs hypotheses of novel human metabolic functions. BMC Syst. Biol. 5, 155
53. Ashburner, M., Ball, C. A., Blake, J. A., Botstein, D., Butler, H., Cherry, J. M., Davis, A. P., Dolinski, K., Dwight, S. S., Eppig, J. T., Harris, M. A., Hill, D. P., Issel-Tarver, L., Kasarskis, A., Lewis, S., Matese, J. C., Richardson, J. E., Ringwald, M., Rubin, G. M., and Sherlock, G. (2000) Gene Ontology: tool for the unification of biology. Nat. Genet. 25, 25-29
54. Szklarczyk, D., Franceschini, A., Kuhn, M., Simonovic, M., Roth, A., Minguez, P., Doerks, T., Stark, M., Muller, J., Bork, P., Jensen, L. J., and von Mering, C. (2011) The STRING database in 2011: functional interaction networks of proteins, globally integrated and scored. Nucleic Acids Res. 39, D561-D568
55. Lee, D. S., Park, J., Kay, K. A., Christakis, N. A., Oltvai, Z. N., and Barabási, A. L. (2008) The implications of human metabolic network topology for disease comorbidity. Proc. Natl. Acad. Sci.U. S. A. 105, 9880-9885
56. Zelezniak, A., Pers, T. H., Soares, S., Patti, M. E., and Patil, K. R. (2010) Metabolic network topology reveals transcriptional regulatory signatures of type 2 diabetes. PLoS Comput. Biol. 6, e1000729
57. Thiele, I., and Palsson, B. Ø. (2010) Reconstruction annotation jamborees: a community approach to systems biology. Mol. Syst.Biol. 6, 361
58. Mo, M. L., and Palsson, B. Ø. (2009) Understanding human metabolic physiology: a genome-to-systems approach. Trends Biotechnol. 27, 37-44
59. Houtkooper, R. H., Cantó, C., Wanders, R. J., and Auwerx, J. (2010) The secret life of NAD+: an old metabolite controlling new metabolic signaling pathways. Endocr. Rev. 31, 194-223
60. Jensen, L. J., and Bork, P. (2010) Ontologies in quantitative biology: a basis for comparison, integration, and discovery. PLoSBiol. 8, e1000374
61. Groth, P., Gibson, A., and Velterop, J. (2010) The anatomy of a nanopublication. Info. Serv. Use 30, 51-56
62. Kitano, H., Ghosh, S., and Matsuoka, Y. (2011) Social engineering for virtual "big science " in systems biology. Nat. Chem. Biol.7, 323-326
63. Hao, T., Ma, H. W., Zhao, X. M., and Goryanin, I. (2010) Compartmentalization of the edinburgh human metabolic network. BMC Bioinfor. 11, 393