A Boolean probabilistic model of metabolic adaptation to oxygen in relation to iron homeostasis and oxidative stress

BMC Systems Biology

Volumn 5, Issue , 2011, Pages

  Achcar, Fiona ^a   Camadro, Jean Michel ^a   Mestivier, Denis ^a  

^a INSTITUT JACQUES MONOD   (France)

Author keywords

[No Author keywords available]

Indexed keywords

IRON; OXYGEN;

AEROBIC METABOLISM; ARTICLE; BIOLOGICAL MODEL; COMPUTER SIMULATION; GENETICS; HOMEOSTASIS; METABOLISM; MOLECULAR EVOLUTION; MUTATION; OXIDATIVE STRESS; PHENOTYPE; SACCHAROMYCES CEREVISIAE; VALIDATION STUDY;

AEROBIOSIS; COMPUTER SIMULATION; EVOLUTION, MOLECULAR; HOMEOSTASIS; IRON; MODELS, BIOLOGICAL; MUTATION; OXIDATIVE STRESS; OXYGEN; PHENOTYPE; SACCHAROMYCES CEREVISIAE;

EID: 79953843449     PISSN: None     EISSN: 17520509     Source Type: Journal    
DOI: 10.1186/1752-0509-5-51     Document Type: Article

References (80)

1. Millen KJ, Gleeson JG. Cerebellar development and disease. Curr Opin Neurobiol 2008, 18:12-9. 10.1016/j.conb.2008.05.010, 2474776, 18513948.
2. Orth M, Schapira AH. Mitochondria and degenerative disorders. Am J Med Genet 2001, 106:27-36. 10.1002/ajmg.1425, 11579422.
3. Schapira AH. Mitochondrial dysfunction in neurodegenerative diseases. Neurochem Res 2008, 33(12):2502-9. 10.1007/s11064-008-9855-x, 18998208.
4. Tabrizi SJ, Schapira AH. Secondary abnormalities of mitochondrial DNA associated with neurodegeneration. Biochem Soc Symp 1999, 66:99-110.
5. Xu JX. Radical metabolism is partner to energy metabolism in mitochondria. Ann N Y Acad Sci 2004, 1011:57-60. 10.1196/annals.1293.006, 15126283.
6. Murphy MP. How mitochondria produce reactive oxygen species. Biochem J 2009, 417:1-13. 10.1042/BJ20081386, 2605959, 19061483.
7. Evans MD, Dizdaroglu M, Cooke MS. Oxidative DNA damage and disease: induction, repair and significance. Mutat Res 2004, 567:1-61. 10.1016/j.mrrev.2003.11.001, 15341901.
8. Grimsrud PA, Xie H, Griffin TJ, Bernlohr DA. Oxidative stress and covalent modification of protein with bioactive aldehydes. J Biol Chem 2008, 283(32):21837-41. 10.1074/jbc.R700019200, 2494933, 18445586.
9. Niki E. Lipid peroxidation: physiological levels and dual biological effects. Free Radic Biol Med 2009, 47(5):469-84. 10.1016/j.freeradbiomed.2009.05.032, 19500666.
10. Kwong JQ, Beal MF, Manfredi G. The role of mitochondria in inherited neurodegenerative diseases. J Neurochem 2006, 97(6):1659-75. 10.1111/j.1471-4159.2006.03990.x, 16805775.
11. Ohta S, Ohsawa I. Dysfunction of mitochondria and oxidative stress in the pathogenesis of Alzheimer's disease: on defects in the cytochrome c oxidase complex and aldehyde detoxification. J Alzheimers Dis 2006, 9(2):155-66.
12. Valko M, Morris H, Cronin MT. Metals, toxicity and oxidative stress. Curr Med Chem 2005, 12(10):1161-208. 10.2174/0929867053764635, 15892631.
13. Heimpel H, Anselstetter V, Chrobak L, Denecke J, Einsiedler B, Gallmeier K, Griesshammer A, Marquardt T, Janka-Schaub G, Kron M, Kohne E. Congenital dyserythropoietic anemia type II: epidemiology, clinical appearance, and prognosis based on long-term observation. Blood 2003, 102(13):4576-81. 10.1182/blood-2003-02-0613, 12933587.
14. Lee PL, Beutler E. Regulation of hepcidin and iron-overload disease. Annu Rev Pathol 2009, 4:489-515. 10.1146/annurev.pathol.4.110807.092205, 19400694.
15. Nicolas G, Bennoun M, Porteu A, Mativet S, Beaumont C, Grandchamp B, Sirito M, Sawadogo M, Kahn A, Vaulont S. Severe iron deficiency anemia in transgenic mice expressing liver hepcidin. Proc Natl Acad Sci USA 2002, 99(7):4596-601. 10.1073/pnas.072632499, 123693, 11930010.
16. Calzone L, Gelay A, Zinovyev A, Radvanyi F, Barillot E. A comprehensive modular map of molecular interactions in RB/E2F pathway. Mol Syst Biol 2008, 4:173. 10.1038/msb.2008.7, 2290939, 18319725.
17. Kohn KW, Aladjem MI, Kim S, Weinstein JN, Pommier Y. Depicting combinatorial complexity with the molecular interaction map notation. Mol Syst Biol 2006, 2:51. 1681518, 17016517.
18. Gerard C, Goldbeter A. Temporal self-organization of the cyclin/Cdk network driving the mammalian cell cycle. Proc Natl Acad Sci USA 2009, 106(51):21643-8. 10.1073/pnas.0903827106, 2799800, 20007375.
19. Noble D. Biophysics and systems biology. Philos Transact A Math Phys Eng Sci 2010, 368(1914):1125-39. 10.1098/rsta.2009.0245, 20123750.
20. Tyson JJ, Albert R, Goldbeter A, Sible J. Biological switches and clocks. J R Soc Interface 2008, 5(Suppl 1):S1-8. 10.1098/rsif.2008.0179.focus, 2706456, 18522926.
21. Alvarez-Buylla ER, Chaos A, Aldana M, Benitez M, Cortes-Poza Y, Espinosa-Soto C, Hartasanchez DA, Lotto RB, Malkin D, Santos GJE, Padilla-Longoria P. Floral morphogenesis: stochastic explorations of a gene network epigenetic landscape. PLoS One 2008, 3(11):e3626. 10.1371/journal.pone.0003626, 2572848, 18978941.
22. Frazier JM, Chushak Y, Foy B. Stochastic simulation and analysis of biomolecular reaction networks. BMC Syst Biol 2009, 3:64. 10.1186/1752-0509-3-64, 2708125, 19534796.
23. Shmulevich I, Aitchison JD. Deterministic and stochastic models of genetic regulatory networks. Methods Enzymol 2009, 467:335-56. full_text, 19897099.
24. Blinov ML, Faeder JR, Goldstein B, Hlavacek WS. A network model of early events in epidermal growth factor receptor signaling that accounts for combinatorial complexity. Biosystems 2006, 83(2-3):136-51. 10.1016/j.biosystems.2005.06.014, 16233948.
25. Faeder JR, Blinov ML, Hlavacek WS. Rule-based modeling of biochemical systems with BioNetGen. Methods Mol Biol 2009, 500:113-67. full_text, 19399430.
26. Davidich MI, Bornholdt S. Boolean network model predicts cell cycle sequence of fission yeast. PLoS One 2008, 3(2):e1672. 10.1371/journal.pone.0001672, 2243020, 18301750.
27. Mai Z, Liu H. Boolean network-based analysis of the apoptosis network: irreversible apoptosis and stable surviving. J Theor Biol 2009, 259(4):760-9. 10.1016/j.jtbi.2009.04.024, 19422837.
28. Mangla K, Dill DL, Horowitz MA. Timing robustness in the budding and fission yeast cell cycles. PloS One 2010, 5(2):e8906. [PMID: 20126540], 10.1371/journal.pone.0008906, 2813865, 20126540.
29. Schlatter R, Schmich K, Vizcarra IA, Scheurich P, Sauter T, Borner C, Ederer M, Merfort I, Sawodny O. ON/OFF and beyond-a boolean model of apoptosis. PLoS Comput Biol 2009, 5(12):e1000595. 10.1371/journal.pcbi.1000595, 2781112, 20011108.
30. Formanowicz D, Sackmann A, Formanowicz P, Blazewicz J. Petri net based model of the body iron homeostasis. J Biomed Inform 2007, 40(5):476-85. 10.1016/j.jbi.2006.12.001, 17258508.
31. Hawari AH, Hussein ZA. Simulation of a Petri net-based Model of the Terpenoid Biosynthetic Pathway. BMC Bioinformatics 2010, 11:83. 10.1186/1471-2105-11-83, 2838867, 20144236.
32. Li C, Nagasaki M, Ueno K, Miyano S. Simulation-based model checking approach to cell fate specification during Caenorhabditis elegans vulval development by hybrid functional Petri net with extension. BMC Syst Biol 2009, 3:42. 10.1186/1752-0509-3-42, 2691733, 19393101.
33. Semsey S, Andersson AMC, Krishna S, Jensen MH, Massé E, Sneppen K. Genetic regulation of fluxes: iron homeostasis of Escherichia coli. Nucleic Acids Research 2006, 34(17):4960-4967. 10.1093/nar/gkl627, 1635276, 16982641.
34. Sackmann A, Formanowicz D, Formanowicz P, Koch I, Blazewicz J. An analysis of the Petri net based model of the human body iron homeostasis process. Computational Biology and Chemistry 2007, 31:1-10. 10.1016/j.compbiolchem.2006.09.005, 17097351.
35. Sarria B, Dainty JR, Fox TE, Fairweather-Tait SJ. Estimation of iron absorption in humans using compartmental modelling. European Journal of Clinical Nutrition 2005, 59:142-144. 10.1038/sj.ejcn.1602030, 15252423., http://www.ncbi.nlm.nih.gov.gate1.inist.fr/pubmed/15252423
36. Jouhten P, Rintala E, Huuskonen A, Tamminen A, Toivari M, Wiebe M, Ruohonen L, Penttila 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.
37. Lill R, Muhlenhoff U. Iron-sulfur protein biogenesis in eukaryotes: components and mechanisms. Annu Rev Cell Dev Biol 2006, 22:457-86. 10.1146/annurev.cellbio.22.010305.104538, 16824008.
38. Rouault TA, Tong WH. Iron-sulphur cluster biogenesis and mitochondrial iron homeostasis. Nat Rev Mol Cell Biol 2005, 6(4):345-51. 10.1038/nrm1620, 15803140.
39. Chabrier-Rivier N, Chiaverini M, Danos V, Fages F, Schächter V. Modeling and querying biomolecular interaction networks. Theoretical Computer Science 2004, 325:25-44., http://www.sciencedirect.com/science/article/B6V1G-4C74FM9-1/2/978d950405c118e882fd1008fba7ab23
40. Urban-Grimal D, Labbe-Bois R. Genetic and biochemical characterization of mutants of Saccharomyces cerevisiae blocked in six different steps of heme biosynthesis. Mol Gen Genet 1981, 183:85-92. 10.1007/BF00270144, 7035824.
41. Liu XF, Elashvili I, Gralla EB, Valentine JS, Lapinskas P, Culotta VC. Yeast lacking superoxide dismutase. Isolation of genetic suppressors. J Biol Chem 1992, 267(26):18298-302.
42. Ogur M, Roshanmanesh A, Ogur S. Tricarboxylic Acid Cycle Mutants in Saccharomyces: Comparison of Independently Derived Mutants. Science 1965, 147:1590. 10.1126/science.147.3665.1590, 14260378.
43. Gollub EG, Liu KP, Dayan J, Adlersberg M, Sprinson DB. Yeast mutants deficient in heme biosynthesis and a heme mutant additionally blocked in cyclization of 2,3-oxidosqualene. J Biol Chem 1977, 252(9):2846-54.
44. Tamura S, Yoshimura E. Promotion of Zn(2+) uptake by Al (3+) in a Saccharomyces Cerevisiae mutant that lacks the ZRT1 gene encoding a high-affinity Zn transporter. Biological Trace Element Research 2008, 124(3):262-268. 10.1007/s12011-008-8145-4, 18463798.
45. Auchère F, Santos R, Planamente S, Lesuisse E, Camadro J. Glutathione-dependent redox status of frataxin-deficient cells in a yeast model of Friedreich's ataxia. Human Molecular Genetics 2008, 17(18):2790-2802. [PMID: 18562474]., http://www.ncbi.nlm.nih.gov.gate1.inist.fr/pubmed/18562474
46. Kastaniotis AJ, Zitomer RS. Rox1 mediated repression. Oxygen dependent repression in yeast. Adv Exp Med Biol 2000, 475:185-95. full_text, 10849660.
47. Zitomer RS, Lowry CV. Regulation of gene expression by oxygen in Saccharomyces cerevisiae. Microbiol Rev 1992, 56:1-11. 372851, 1579104.
48. Lutstorf U, Megnet R. Multiple forms of alcohol dehydrogenase in Saccharomyces cerevisiae. I. Physiological control of ADH-2 and properties of ADH-2 and ADH-4. Arch Biochem Biophys 1968, 126(3):933-44. 10.1016/0003-9861(68)90487-6, 5686604.
49. Achcar F, Camadro J, Mestivier D. AutoClass@IJM: a powerful tool for Bayesian classification of heterogeneous data in biology. Nucleic Acids Research 2009, (37 Web Server):W63-67. 10.1093/nar/gkp430, 2703914, 19474346.
50. Babcock M, de Silva D, Oaks R, Davis-Kaplan S, Jiralerspong S, Montermini L, Pandolfo M, Kaplan J. Regulation of mitochondrial iron accumulation by Yfh1p, a putative homolog of frataxin. Science 1997, 276(5319):1709-12. 10.1126/science.276.5319.1709, 9180083.
51. Foury F, Talibi D. Mitochondrial control of iron homeostasis. A genome wide analysis of gene expression in a yeast frataxin-deficient strain. J Biol Chem 2001, 276(11):7762-8. 10.1074/jbc.M005804200, 11112771.
52. Measday V, Baetz K, Guzzo J, Yuen K, Kwok T, Sheikh B, Ding H, Ueta R, Hoac T, Cheng B, Pot I, Tong A, Yamaguchi-Iwai Y, Boone C, Hieter P, Andrews B. Systematic yeast synthetic lethal and synthetic dosage lethal screens identify genes required for chromosome segregation. Proc Natl Acad Sci USA 2005, 102(39):13956-61. 10.1073/pnas.0503504102, 1236538, 16172405.
53. Thomas D, Jacquemin I, Surdin-Kerjan Y. MET4, a leucine zipper protein, and centromere-binding factor 1 are both required for transcriptional activation of sulfur metabolism in Saccharomyces cerevisiae. Mol Cell Biol 1992, 12(4):1719-27. 369615, 1549123.
54. Lesuisse E, Santos R, Matzanke BF, Knight SAB, Camadro J, Dancis A. Iron use for haeme synthesis is under control of the yeast frataxin homologue (Yfh1). Human Molecular Genetics 2003, 12(8):879-889. 10.1093/hmg/ddg096, 12668611.
55. Miao R, Kim H, Koppolu UMK, Ellis EA, Scott RA, Lindahl PA. Biophysical characterization of the iron in mitochondria from Atm1p-depleted Saccharomyces cerevisiae. Biochemistry 2009, 48(40):9556-9568. 10.1021/bi901110n, 2758324, 19761223.
56. Miao R, Martinho M, Morales JG, Kim H, Ellis EA, Lill R, Hendrich MP, Münck E, Lindahl PA. EPR and Mössbauer spectroscopy of intact mitochondria isolated from Yah1p-depleted Saccharomyces cerevisiae. Biochemistry 2008, 47(37):9888-9899. 10.1021/bi801047q, 18717590.
57. Lide DR. Solubility Product Constants. CRC Handbook of Chemistry and Physics 2009, CRC Press, 90., http://www.hbcpnetbase.com
58. Ligeti E, Fonyó A. Mitochondrial phosphate carrier. Functional role of its SH groups and interrelations within the carrier unit. European Journal of Biochemistry/FEBS 1987, 167:167-173. 10.1111/j.1432-1033.1987.tb13319.x, 3622508.
59. Madeo F, Fröhlich E, Ligr M, Grey M, Sigrist SJ, Wolf DH, Fröhlich KU. Oxygen stress: a regulator of apoptosis in yeast. The Journal of Cell Biology 1999, 145(4):757-767. 10.1083/jcb.145.4.757, 2133192, 10330404.
60. Sipos K, Lange H, Fekete Z, Ullmann P, Lill R, Kispal G. Maturation of cytosolic iron-sulfur proteins requires glutathione. The Journal of Biological Chemistry 2002, 277(30):26944-26949. 10.1074/jbc.M200677200, 12011041.
61. Kohn KW, Aladjem MI, Weinstein JN, Pommier Y. Molecular interaction maps of bioregulatory networks: a general rubric for systems biology. Mol Biol Cell 2006, 17:1-13. 10.1091/mbc.E05-09-0824, 1345641, 16267266.
62. Hower V, Mendes P, Torti FM, Laubenbacher R, Akman S, Shulaev V, Torti SV. A general map of iron metabolism and tissue-speci c subnetworks. Mol Biosyst 2009, 5(5):422-43. 10.1039/b816714c, 2680238, 19381358.
63. Hlavacek WS. How to deal with large models?. Molecular Systems Biology 2009, 5:240. 10.1038/msb.2008.80, 2644176, 19156132.
64. Alves R, Herrero E, Sorribas A. Predictive reconstruction of the mitochondrial iron-sulfur cluster assembly metabolism. II. Role of glutaredoxin Grx5. Proteins 2004, 57(3):481-492. 10.1002/prot.20228, 15382238.
65. Alves R, Herrero E, Sorribas A. Predictive reconstruction of the mitochondrial iron-sulfur cluster assembly metabolism: I. The role of the protein pair ferredoxin-ferredoxin reductase (Yah1-Arh1). Proteins 2004, 56(2):354-366. 10.1002/prot.20110, 15211518.
66. Qi Z, Miller GW, Voit EO. Computational Systems Analysis of Dopamine Metabolism. PLoS ONE 2008, 3(6):e2444.. 10.1371/journal.pone.0002444, 2435046, 18568086.
67. Zhou L, Cortassa S, Wei A, Aon MA, Winslow RL, O'Rourke B. Modeling Cardiac Action Potential Shortening Driven by Oxidative Stress-Induced Mitochondrial Oscillations in Guinea Pig Cardiomyocytes. Biophysical Journal 2009, 97(7):1843-1852. 10.1016/j.bpj.2009.07.029, 2756351, 19804714.
68. Caspi R, Foerster H, Fulcher CA, Hopkinson R, Ingraham J, Kaipa P, Krummenacker M, Paley S, Pick J, Rhee SY, Tissier C, Zhang P, Karp PD. MetaCyc: a multiorganism database of metabolic pathways and enzymes. Nucleic Acids Research 2006, (34 Database):D511-516. 10.1093/nar/gkj128, 1347490, 16381923.
69. Ghaemmaghami S, Huh W, Bower K, Howson RW, Belle A, Dephoure N, O'Shea EK, Weissman JS. Global analysis of protein expression in yeast. Nature 2003, 425(6959):737-741. 10.1038/nature02046, 14562106.
70. Mnaimneh S, Davierwala AP, Haynes J, Moffat J, Peng WT, Zhang W, Yang X, Pootoolal J, Chua G, Lopez A, Trochesset M, Morse D, Krogan NJ, Hiley SL, Li Z, Morris Q, Grigull J, Mitsakakis N, Roberts CJ, Greenblatt JF, Boone C, Kaiser CA, Andrews BJ, Hughes TR. Exploration of essential gene functions via titratable promoter alleles. Cell 2004, 118:31-44. 10.1016/j.cell.2004.06.013, 15242642.
71. Ultsch A. Improving the identification of differentially expressed genes in cDNA microarray experiments. Classification - the Ubiquitous Challenge 2005, 378-385., http://[http://apps.isiknowledge.com.gate1.inist.fr/ full record.do?product=WOS&search m ode=GeneralSearch&qid=1&SID=U2pB75G 28PK3AI@kBaf&page=1&doc=1]
72. Boyle EI, Weng S, Gollub J, Jin H, Botstein D, Cherry JM, Sherlock G. GO::TermFinder - open source software for accessing Gene Ontology information and finding significantly enriched Gene Ontology terms associated with a list of genes. Bioinformatics 2004, 20(18):3710-3715. 10.1093/bioinformatics/bth456, 3037731, 15297299.
73. Chen OS, Crisp RJ, Valachovic M, Bard M, Winge DR, Kaplan J. Transcription of the yeast iron regulon does not respond directly to iron but rather to iron-sulfur cluster biosynthesis. The Journal of Biological Chemistry 2004, 279(28):29513-8. 10.1074/jbc.M403209200, 15123701.
74. Dix DR, Bridgham JT, Broderius MA, Byersdorfer CA, Eide DJ. The FET4 gene encodes the low affinity Fe(II) transport protein of Saccharomyces cerevisiae. The Journal of Biological Chemistry 1994, 269(42):26092-26099.
75. Lin SS, Manchester JK, Gordon JI. Enhanced gluconeogenesis and increased energy storage as hallmarks of aging in Saccharomyces cerevisiae. The Journal of Biological Chemistry 2001, 276(38):36000-7. 10.1074/jbc.M103509200, 11461906.
76. Minard KI, McAlister-Henn L. Sources of NADPH in yeast vary with carbon source. The Journal of Biological Chemistry 2005, 280(48):39890-39896. 10.1074/jbc.M509461200, 16179340.
77. Voet D, Voet JG. Regulation of the Citric Acid Cycle. In Biochemistry 1995, 557-559. Wiley, 2.
78. Hinkle PC, McCarty RE. How cells make ATP. Scientific American 1978, 238(3):104-117. 10.1038/scientificamerican0378-104, 635521.
79. Auchère F, Rusnak F. What is the ultimate fate of superoxide anion in vivo?. Journal of Biological Inorganic Chemistry: JBIC: A Publication of the Society of Biological Inorganic Chemistry 2002, 7(6):664-7.
80. Aebi H. Catalase in vitro. Methods Enzymol 1984, 105:121-6. full_text, 6727660.