A Genome-Scale Database and Reconstruction of Caenorhabditis elegans Metabolism

Cell Systems

Volumn 2, Issue 5, 2016, Pages 312-322

  Gebauer, Juliane ^a   Gentsch, Christoph ^a   Mansfeld, Johannes ^a,b   Schmeißer, Kathrin ^a   Waschina, Silvio ^a,c   Brandes, Susanne ^a,d   Klimmasch, Lukas ^a   Zamboni, Nicola ^b   Zarse, Kim ^a,b   Schuster, Stefan ^a   Ristow, Michael ^a,b   Schäuble, Sascha ^a   Kaleta, Christoph ^a,c  

^a FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

^b ETH ZURICH   (Switzerland)

^c UNIVERSITY OF KIEL   (Germany)

^d HANS KNÖLL INSTITUTE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; NICOTINAMIDE ADENINE DINUCLEOTIDE; QUINOLINIC ACID; REACTIVE OXYGEN METABOLITE; TRYPTOPHAN; CAENORHABDITIS ELEGANS PROTEIN;

ADAPTATION; AGING; AMINO ACID METABOLISM; ARTICLE; BIOSYNTHESIS; CAENORHABDITIS ELEGANS; DATA BASE; GENE EXPRESSION; GENOME; LIFESPAN; NONHUMAN; PRIORITY JOURNAL; ANIMAL; GENETIC DATABASE; HORMESIS; HUMAN; LONGEVITY; MOUSE;

ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; DATABASES, GENETIC; GENOME; HORMESIS; HUMANS; LONGEVITY; MICE; REACTIVE OXYGEN SPECIES;

EID: 84969793963     PISSN: 24054712     EISSN: 24054720     Source Type: Journal    
DOI: 10.1016/j.cels.2016.04.017     Document Type: Article

References (96)

1. M. Ashburner, C.A. Ball, J.A. Blake, D. Botstein, H. Butler, J.M. Cherry, A.P. Davis, K. Dolinski, S.S. Dwight, J.T. Eppig, et al. The Gene Ontology Consortium Gene ontology: tool for the unification of biology Nat. Genet. 25 2000 25 29
2. M. Baumgart, S. Priebe, M. Groth, N. Hartmann, U. Menzel, L. Pandolfini, P. Koch, M. Felder, M. Ristow, C. Englert, and et al. Longitudinal RNA-seq analysis of vertebrate aging identifies mitochondrial complex I as a small-molecule-sensitive modifier of lifespan Cell Syst. 2 2016 122 132
3. D.A. Benson, I. Karsch-Mizrachi, D.J. Lipman, J. Ostell, and E.W. Sayers GenBank Nucleic Acids Res. 39 2011 D32 D37
4. R.E. Beyer, B.A. Burnett, K.J. Cartwright, D.W. Edington, M.J. Falzon, K.R. Kreitman, T.W. Kuhn, B.J. Ramp, S.Y. Rhee, M.J. Rosenwasser, and et al. Tissue coenzyme Q (ubiquinone) and protein concentrations over the life span of the laboratory rat Mech. Ageing Dev. 32 1985 267 281
5. C. elegans Sequencing Consortium Genome sequence of the nematode C. elegans: a platform for investigating biology Science 282 1998 2012 2018
6. E.J. Calabrese, K.A. Bachmann, A.J. Bailer, P.M. Bolger, J. Borak, L. Cai, N. Cedergreen, M.G. Cherian, C.C. Chiueh, T.W. Clarkson, and et al. Biological stress response terminology: integrating the concepts of adaptive response and preconditioning stress within a hormetic dose-response framework Toxicol. Appl. Pharmacol. 222 2007 122 128
7. S.X. Cao, J.M. Dhahbi, P.L. Mote, and S.R. Spindler Genomic profiling of short- and long-term caloric restriction effects in the liver of aging mice Proc. Natl. Acad. Sci. USA 98 2001 10630 10635
8. R. Caspi, T. Altman, R. Billington, K. Dreher, H. Foerster, C.A. Fulcher, T.A. Holland, I.M. Keseler, A. Kothari, A. Kubo, and et al. The MetaCyc database of metabolic pathways and enzymes and the BioCyc collection of Pathway/Genome Databases Nucleic Acids Res. 42 2014 D459 D471
9. A.E. Civitarese, S. Carling, L.K. Heilbronn, M.H. Hulver, B. Ukropcova, W.A. Deutsch, S.R. Smith, E. Ravussin CALERIE Pennington Team Calorie restriction increases muscle mitochondrial biogenesis in healthy humans PLoS Med. 4 2007 e76
10. E. Culetto, and D.B. Sattelle A role for Caenorhabditis elegans in understanding the function and interactions of human disease genes Hum. Mol. Genet. 9 2000 869 877
11. S.P. Curran, and G. Ruvkun Lifespan regulation by evolutionarily conserved genes essential for viability PLoS Genet. 3 2007 e56
12. A.A. Da'dara, and R.D. Walter Molecular and biochemical characterization of S-adenosylmethionine decarboxylase from the free-living nematode Caenorhabditis elegans Biochem. J. 336 1998 545 550
13. J.M. Dale, L. Popescu, and P.D. Karp Machine learning methods for metabolic pathway prediction BMC Bioinformatics 11 2010 15
14. L.F. de Figueiredo, S. Schuster, C. Kaleta, and D.A. Fell Can sugars be produced from fatty acids? A test case for pathway analysis tools Bioinformatics 25 2009 152 158
15. N.C. Duarte, S.A. Becker, N. Jamshidi, I. Thiele, M.L. Mo, T.D. Vo, R. Srivas, and B.O. Palsson Global reconstruction of the human metabolic network based on genomic and bibliomic data Proc. Natl. Acad. Sci. USA 104 2007 1777 1782
16. C. Edwards, J. Canfield, N. Copes, A. Brito, M. Rehan, D. Lipps, J. Brunquell, S.D. Westerheide, and P.C. Bradshaw Mechanisms of amino acid-mediated lifespan extension in Caenorhabditis elegans BMC Genet. 16 2015 8
17. L. Ernster, and G. Dallner Biochemical, physiological and medical aspects of ubiquinone function Biochim. Biophys. Acta 1271 1995 195 204
18. A. Fire, S. Xu, M.K. Montgomery, S.A. Kostas, S.E. Driver, and C.C. Mello Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans Nature 391 1998 806 811
19. M. Gallo, D. Park, and D.L. Riddle Increased longevity of some C. elegans mitochondrial mutants explained by activation of an alternative energy-producing pathway Mech. Ageing Dev. 132 2011 515 518
20. M. Ganter, T. Bernard, S. Moretti, J. Stelling, and M. Pagni MetaNetX.org: a website and repository for accessing, analysing and manipulating metabolic networks Bioinformatics 29 2013 815 816
21. J. Gebauer, S. Schuster, L.F. de Figueiredo, and C. Kaleta Detecting and investigating substrate cycles in a genome-scale human metabolic network FEBS J. 279 2012 3192 3202
22. F. Gomez, R. Saiki, R. Chin, C. Srinivasan, and C.F. Clarke Restoring de novo coenzyme Q biosynthesis in Caenorhabditis elegans coq-3 mutants yields profound rescue compared to exogenous coenzyme Q supplementation Gene 506 2012 106 116
23. T.I. Gossmann, M. Ziegler, P. Puntervoll, L.F. de Figueiredo, S. Schuster, and I. Heiland NAD(+) biosynthesis and salvage - a phylogenetic perspective FEBS J. 279 2012 3355 3363
24. M.L. Green, and P.D. Karp A Bayesian method for identifying missing enzymes in predicted metabolic pathway databases BMC Bioinformatics 5 2004 76
25. M. Hansen, A.-L. Hsu, A. Dillin, and C. Kenyon New genes tied to endocrine, metabolic, and dietary regulation of lifespan from a Caenorhabditis elegans genomic RNAi screen PLoS Genet. 1 2005 119 128
26. T.W. Harris, J. Baran, T. Bieri, A. Cabunoc, J. Chan, W.J. Chen, P. Davis, J. Done, C. Grove, K. Howe, and et al. WormBase 2014: new views of curated biology Nucleic Acids Res. 42 2014 D789 D793
27. A. Heinken, and I. Thiele Systems biology of host-microbe metabolomics Wiley Interdiscip. Rev. Syst. Biol. Med. 7 2015 195 219
28. L.A. Herndon, P.J. Schmeissner, J.M. Dudaronek, P.A. Brown, K.M. Listner, Y. Sakano, M.C. Paupard, D.H. Hall, and M. Driscoll Stochastic and genetic factors influence tissue-specific decline in ageing C. elegans Nature 419 2002 808 814
29. A.A. Hill, C.P. Hunter, B.T. Tsung, G. Tucker-Kellogg, and E.L. Brown Genomic analysis of gene expression in C. elegans Science 290 2000 809 812
30. P. Horton, K.-J. Park, T. Obayashi, N. Fujita, H. Harada, C.J. Adams-Collier, and K. Nakai WoLF PSORT: protein localization predictor Nucleic Acids Res. 35 2007 W585 W587
31. K. Houthoofd, B.P. Braeckman, I. Lenaerts, K. Brys, A. De Vreese, S. Van Eygen, and J.R. Vanfleteren Ageing is reversed, and metabolism is reset to young levels in recovering dauer larvae of C. elegans Exp. Gerontol. 37 2002 1015 1021
32. M. Hucka, A. Finney, H.M. Sauro, H. Bolouri, J.C. Doyle, H. Kitano, A.P. Arkin, B.J. Bornstein, D. Bray, A. Cornish-Bowden, et al. SBML Forum The systems biology markup language (SBML): a medium for representation and exchange of biochemical network models Bioinformatics 19 2003 524 531
33. A.J. Hulbert On the importance of fatty acid composition of membranes for aging J. Theor. Biol. 234 2005 277 288
34. Y.C. Jang, Y. Liu, C.R. Hayworth, A. Bhattacharya, M.S. Lustgarten, F.L. Muller, A. Chaudhuri, W. Qi, Y. Li, J.Y. Huang, and et al. Dietary restriction attenuates age-associated muscle atrophy by lowering oxidative stress in mice even in complete absence of CuZnSOD Aging Cell 11 2012 770 782
35. P.A. Jensen, and J.A. Papin Functional integration of a metabolic network model and expression data without arbitrary thresholding Bioinformatics 27 2011 541 547
36. T.E. Johnson, and G. McCaffrey Programmed aging or error catastrophe? An examination by two-dimensional polyacrylamide gel electrophoresis Mech. Ageing Dev. 30 1985 285 297
37. T.E. Johnson, D.H. Mitchell, S. Kline, R. Kemal, and J. Foy Arresting development arrests aging in the nematode Caenorhabditis elegans Mech. Ageing Dev. 28 1984 23 40
38. T. Jonassen, and C.F. Clarke Isolation and functional expression of human COQ3, a gene encoding a methyltransferase required for ubiquinone biosynthesis J. Biol. Chem. 275 2000 12381 12387
39. T. Jonassen, B.N. Marbois, K.F. Faull, C.F. Clarke, and P.L. Larsen Development and fertility in Caenorhabditis elegans clk-1 mutants depend upon transport of dietary coenzyme Q8 to mitochondria J. Biol. Chem. 277 2002 45020 45027
40. M. Jové, A. Naudí, O. Ramírez-Núñez, M. Portero-Otín, C. Selman, D.J. Withers, and R. Pamplona Caloric restriction reveals a metabolomic and lipidomic signature in liver of male mice Aging Cell 13 2014 828 837
41. th German Conference on Bioinformatics (GCB), I. Grosse, S. Neumann, S. Posch, F. Schreiber, and P. Stadler, eds. (Gesellschaft f. Informatik e.V.), pp. 180-190.
42. T. Kaletta, and M.O. Hengartner Finding function in novel targets: C. elegans as a model organism Nat. Rev. Drug Discov. 5 2006 387 398
43. M. Kanehisa, and S. Goto KEGG: kyoto encyclopedia of genes and genomes Nucleic Acids Res. 28 2000 27 30
44. P.D. Karp, S.M. Paley, M. Krummenacker, M. Latendresse, J.M. Dale, T.J. Lee, P. Kaipa, F. Gilham, A. Spaulding, L. Popescu, and et al. Pathway Tools version 13.0: integrated software for pathway/genome informatics and systems biology Brief. Bioinform. 11 2010 40 79
45. T. Kayo, D.B. Allison, R. Weindruch, and T.A. Prolla Influences of aging and caloric restriction on the transcriptional profile of skeletal muscle from rhesus monkeys Proc. Natl. Acad. Sci. USA 98 2001 5093 5098
46. I.M. Keseler, A. Mackie, M. Peralta-Gil, A. Santos-Zavaleta, S. Gama-Castro, C. Bonavides-Martínez, C. Fulcher, A.M. Huerta, A. Kothari, M. Krummenacker, and et al. EcoCyc: fusing model organism databases with systems biology Nucleic Acids Res. 41 2013 D605 D612
47. J. Kimble, and D. Hirsh The postembryonic cell lineages of the hermaphrodite and male gonads in Caenorhabditis elegans Dev. Biol. 70 1979 396 417
48. M.R. Klass A method for the isolation of longevity mutants in the nematode Caenorhabditis elegans and initial results Mech. Ageing Dev. 22 1983 279 286
49. B. Lakowski, and S. Hekimi Determination of life-span in Caenorhabditis elegans by four clock genes Science 272 1996 1010 1013
50. B. Lakowski, and S. Hekimi The genetics of caloric restriction in Caenorhabditis elegans Proc. Natl. Acad. Sci. USA 95 1998 13091 13096
51. S.K. Langer Kultivierung von Caenorhabditis elegans über Flüssigmedium zur Untersuchung des molekularen Folsäuremetabolismus 2009 Universität Wien
52. P.L. Larsen, and C.F. Clarke Extension of life-span in Caenorhabditis elegans by a diet lacking coenzyme Q Science 295 2002 120 123
53. C.-K. Lee, D.B. Allison, J. Brand, R. Weindruch, and T.A. Prolla Transcriptional profiles associated with aging and middle age-onset caloric restriction in mouse hearts Proc. Natl. Acad. Sci. USA 99 2002 14988 14993
54. F. Liu, J.D. Thatcher, J.M. Barral, and H.F. Epstein Bifunctional glyoxylate cycle protein of Caenorhabditis elegans: a developmentally regulated protein of intestine and muscle Dev. Biol. 169 1995 399 414
55. K. Lüersen, M.-L. Eschbach, E. Liebau, and R.D. Walter Functional GATA- and initiator-like-elements exhibit a similar arrangement in the promoters of Caenorhabditis elegans polyamine synthesis enzymes Biol. Chem. 385 2004 711 721
56. M. Macrae, and P. Coffino Complementation of a polyamine-deficient Escherichia coli mutant by expression of mouse ornithine decarboxylase Mol. Cell. Biol. 7 1987 564 567
57. M. MacRae, D.L. Kramer, and P. Coffino Developmental effect of polyamine depletion in Caenorhabditis elegans Biochem. J. 333 1998 309 315
58. J. Mansfeld, N. Urban, S. Priebe, M. Groth, C. Frahm, N. Hartmann, J. Gebauer, M. Ravichandran, A. Dommaschk, S. Schmeisser, and et al. Branched-chain amino acid catabolism is a conserved regulator of physiological ageing Nat. Commun. 6 2015 10043
59. A. Mardinoglu, R. Agren, C. Kampf, A. Asplund, M. Uhlen, and J. Nielsen Genome-scale metabolic modelling of hepatocytes reveals serine deficiency in patients with non-alcoholic fatty liver disease Nat. Commun. 5 2014 3083
60. A. Meinitzer, A. Tomaschitz, S. Pilz, M. Truber, G. Zechner, M. Gaksch, B. Prietl, G. Treiber, M. Schwarz, and A. Baranyi Development of a liquid chromatography-mass spectrometry method for the determination of the neurotoxic quinolinic acid in human serum Clin. Chim. Acta 436 2014 268 272
61. H. Miyadera, H. Amino, A. Hiraishi, H. Taka, K. Murayama, H. Miyoshi, K. Sakamoto, N. Ishii, S. Hekimi, and K. Kita Altered quinone biosynthesis in the long-lived clk-1 mutants of Caenorhabditis elegans J. Biol. Chem. 276 2001 7713 7716
62. H. Miyadera, K. Kano, H. Miyoshi, N. Ishii, S. Hekimi, and K. Kita Quinones in long-lived clk-1 mutants of Caenorhabditis elegans FEBS Lett. 512 2002 33 37
63. I. Montoliu, M. Scherer, F. Beguelin, L. DaSilva, D. Mari, S. Salvioli, F.P. Martin, M. Capri, L. Bucci, R. Ostan, and et al. Serum profiling of healthy aging identifies phospho- and sphingolipid species as markers of human longevity Aging (Albany, N.Y.) 6 2014 9 25
64. F.C. Neidhardt, J.L. Ingraham, and M. Schaechter Physiology of the Bacterial Cell: A Molecular Approach 1990 Sinauer Associates
65. M.A. Oberhardt, B.O. Palsson, and J.A. Papin Applications of genome-scale metabolic reconstructions Mol. Syst. Biol. 5 2009 320
66. J. Odo, M. Inoguchi, and A. Hirai Fluorometric determination of quinolinic acid using the catalytic activity of horseradish peroxidase J. Health Sci. 55 2009 242 248
67. J.D. Orth, T.M. Conrad, J. Na, J.A. Lerman, H. Nam, A.M. Feist, and B.O. Palsson A comprehensive genome-scale reconstruction of Escherichia coli metabolism - 2011 Mol. Syst. Biol. 7 2011 535
68. R. Pamplona, G. Barja, and M. Portero-Otín Membrane fatty acid unsaturation, protection against oxidative stress, and maximum life span: a homeoviscous-longevity adaptation? Ann. N Y Acad. Sci. 959 2002 475 490
69. S. Priebe, U. Menzel, K. Zarse, M. Groth, M. Platzer, M. Ristow, and R. Guthke Extension of life span by impaired glucose metabolism in Caenorhabditis elegans is accompanied by structural rearrangements of the transcriptomic network PLoS ONE 8 2013 e77776
70. R Core Team R: A Language and Environment for Statistical Computing 2015 R Foundation for Statistical Computing Vienna, Austria
71. E.A. Rath, and S.W. Thenen Influence of age and genetic background on in vivo fatty acid synthesis in obese (ob/ob) mice Biochim. Biophys. Acta 618 1980 18 27
72. M. Ristow, and K. Zarse How increased oxidative stress promotes longevity and metabolic health: The concept of mitochondrial hormesis (mitohormesis) Exp. Gerontol. 45 2010 410 418
73. A. Rongvaux, F. Andris, F. Van Gool, and O. Leo Reconstructing eukaryotic NAD metabolism BioEssays 25 2003 683 690
74. M. Rothstein Nematode biochemistry III. Exrection products Comp. Biochem. Physiol. 9 1963 51 59
75. S. Sahoo, M.K. Aurich, J.J. Jonsson, and I. Thiele Membrane transporters in a human genome-scale metabolic knowledgebase and their implications for disease Front. Physiol. 5 2014 91
76. J. Schellenberger, J.O. Park, T.M. Conrad, and B.O. Palsson BiGG: a Biochemical Genetic and Genomic knowledgebase of large scale metabolic reconstructions BMC Bioinformatics 11 2010 213
77. J. Schellenberger, R. Que, R.M.T. Fleming, I. Thiele, J.D. Orth, A.M. Feist, D.C. Zielinski, A. Bordbar, N.E. Lewis, S. Rahmanian, and et al. Quantitative prediction of cellular metabolism with constraint-based models: the COBRA Toolbox v2.0 Nat. Protoc. 6 2011 1290 1307
78. K. Schmeisser, J. Mansfeld, D. Kuhlow, S. Weimer, S. Priebe, I. Heiland, M. Birringer, M. Groth, A. Segref, Y. Kanfi, and et al. Role of sirtuins in lifespan regulation is linked to methylation of nicotinamide Nat. Chem. Biol. 9 2013 693 700
79. S. Schmeisser, S. Priebe, M. Groth, S. Monajembashi, P. Hemmerich, R. Guthke, M. Platzer, and M. Ristow Neuronal ROS signaling rather than AMPK/sirtuin-mediated energy sensing links dietary restriction to lifespan extension Mol. Metab. 2 2013 92 102
80. T.J. Schulz, K. Zarse, A. Voigt, N. Urban, M. Birringer, and M. Ristow Glucose restriction extends Caenorhabditis elegans life span by inducing mitochondrial respiration and increasing oxidative stress Cell Metab. 6 2007 280 293
81. S. Schuster, T. Dandekar, and D.A. Fell Detection of elementary flux modes in biochemical networks: a promising tool for pathway analysis and metabolic engineering Trends Biotechnol. 17 1999 53 60
82. D.D. Shaye, and I. Greenwald OrthoList: a compendium of C. elegans genes with human orthologs PLoS ONE 6 2011 e20085
83. T. Shlomi, M.N. Cabili, M.J. Herrgård, B.O. Palsson, and E. Ruppin Network-based prediction of human tissue-specific metabolism Nat. Biotechnol. 26 2008 1003 1010
84. D.E. Shore, C.E. Carr, and G. Ruvkun Induction of cytoprotective pathways is central to the extension of lifespan conferred by multiple longevity pathways PLoS Genet. 8 2012 e1002792
85. A. Sols, and R.K. Crane Substrate specificity of brain hexokinase J. Biol. Chem. 210 1954 581 595
86. T.W. Stone Neuropharmacology of quinolinic and kynurenic acids Pharmacol. Rev. 45 1993 309 379
87. J.E. Sulston, E. Schierenberg, J.G. White, and J.N. Thomson The embryonic cell lineage of the nematode Caenorhabditis elegans Dev. Biol. 100 1983 64 119
88. N.J. Szewczyk, E. Kozak, and C.A. Conley Chemically defined medium and Caenorhabditis elegans BMC Biotechnol. 3 2003 19
89. I. Thiele, and B.O. Palsson A protocol for generating a high-quality genome-scale metabolic reconstruction Nat. Protoc. 5 2010 93 121
90. I. Thiele, N. Swainston, R.M.T. Fleming, A. Hoppe, S. Sahoo, M.K. Aurich, H. Haraldsdottir, M.L. Mo, O. Rolfsson, M.D. Stobbe, and et al. A community-driven global reconstruction of human metabolism Nat. Biotechnol. 31 2013 419 425
91. A.T. van der Goot, W. Zhu, R.P. Vázquez-Manrique, R.I. Seinstra, K. Dettmer, H. Michels, F. Farina, J. Krijnen, R. Melki, R.C. Buijsman, and et al. Delaying aging and the aging-associated decline in protein homeostasis by inhibition of tryptophan degradation Proc. Natl. Acad. Sci. USA 109 2012 14912 14917
92. J.R. Vanfleteren, and A. De Vreese Rate of aerobic metabolism and superoxide production rate potential in the nematode Caenorhabditis elegans J. Exp. Zool. 274 1996 93 100
93. J. Wang, and S.K. Kim Global analysis of dauer gene expression in Caenorhabditis elegans Development 130 2003 1621 1634
94. K. Yizhak, S.E. Le Dévédec, V.M. Rogkoti, F. Baenke, V.C. de Boer, C. Frezza, A. Schulze, B. van de Water, and E. Ruppin A computational study of the Warburg effect identifies metabolic targets inhibiting cancer migration Mol. Syst. Biol. 10 2014 744
95. K. Zarse, S. Schmeisser, M. Groth, S. Priebe, G. Beuster, D. Kuhlow, R. Guthke, M. Platzer, C.R. Kahn, and M. Ristow Impaired insulin/IGF1 signaling extends life span by promoting mitochondrial L-proline catabolism to induce a transient ROS signal Cell Metab. 15 2012 451 465
96. H. Zur, E. Ruppin, and T. Shlomi iMAT: an integrative metabolic analysis tool Bioinformatics 26 2010 3140 3142