Proteomic and network analysis characterize stage-specific metabolism in Trypanosoma cruzi

BMC Systems Biology

Volumn 3, Issue , 2009, Pages

  Roberts, Seth B ^a   Robichaux, Jennifer L ^b   Chavali, Arvind K ^b   Manque, Patricio A ^a   Lee, Vladimir ^a   Lara, Ana M ^a   Papin, Jason A ^b   Buck, Gregory A ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

^b University of Virginia   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HEXAPODA; KINETOPLASTIDA; TRYPANOSOMA CRUZI; TRYPANOSOMA CRUZI STRAIN CL BRENER;

AMINO ACID;

ANIMAL; ARTICLE; BIOLOGICAL MODEL; CARBOHYDRATE METABOLISM; ENERGY METABOLISM; GROWTH, DEVELOPMENT AND AGING; HOST PARASITE INTERACTION; INSECT; LIFE CYCLE; METABOLISM; PARASITOLOGY; PHYSIOLOGY; PROTEOMICS; REPRODUCIBILITY; TRYPANOSOMA CRUZI;

AMINO ACIDS; ANIMALS; CARBOHYDRATE METABOLISM; ENERGY METABOLISM; HOST-PARASITE INTERACTIONS; INSECTS; LIFE CYCLE STAGES; MODELS, BIOLOGICAL; PROTEOMICS; REPRODUCIBILITY OF RESULTS; TRYPANOSOMA CRUZI;

EID: 67649908740     PISSN: None     EISSN: 17520509     Source Type: Journal    
DOI: 10.1186/1752-0509-3-52     Document Type: Article

References (73)

1. Sun X Lu Z The response of the metabolic network of the red blood cell to pyruvate kinase deficiency Conf Proc IEEE Eng Med Biol Soc 2005, 1:913-916 17282332
2. Ishii N Robert M Nakayama Y Kanai A Tomita M Toward large-scale modeling of the microbial cell for computer simulation J Biotechnol 2004, 113(1-3):281-294 10.1016/j.jbiotec.2004.04.038 15380661
3. Reed JL Vo TD Schilling CH Palsson BO An expanded genome-scale model of Escherichia coli K-12 (iJR904 GSM/GPR) Genome Biol 2003, 4(9):R54 193654 12952533 10.1186/gb-2003-4-9-r54
4. Duarte NC Herrgard MJ Palsson BO Reconstruction and validation of Saccharomyces cerevisiae iND750, a fully compartmentalized genome-scale metabolic model Genome Res 2004, 14(7):1298-1309 442145 15197165 10.1101/ gr.2250904
5. Papin JA Hunter T Palsson BO Subramaniam S Reconstruction of cellular signalling networks and analysis of their properties Nat Rev Mol Cell Biol 2005, 6(2):99-111 10.1038/nrm1570 15654321
6. Joyce AR Palsson BO Toward whole cell modeling and simulation: comprehensive functional genomics through the constraint-based approach Prog Drug Res 2007, 64:265, 267 -309 17195479
7. Lee JM Gianchandani EP Papin JA Flux balance analysis in the era of metabolomics Brief Bioinform 2006, 7(2):140-150 10.1093/bib/bbl007 16772264
8. Reed JL Famili I Thiele I Palsson BO Towards multidimensional genome annotation Nat Rev Genet 2006, 7(2):130-141 10.1038/nrg1769 16418748
9. Price ND Papin JA Schilling CH Palsson BO Genome-scale microbial in silico models: The constraints-based approach Trends Biotechnol 2003, 21(4):162-169 10.1016/S0167-7799(03)00030-1 12679064
10. Price ND Reed JL Palsson BO Genome-scale models of microbial cells: evaluating the consequences of constraints Nat Rev Microbiol 2004, 2(11):886-897 10.1038/nrmicro1023 15494745
11. Duarte NC Becker SA Jamshidi N Thiele I Mo ML Vo TD Srivas R Palsson BO Global reconstruction of the human metabolic network based on genomic and bibliomic data Proc Natl Acad Sci USA 2007, 104(6):1777-1782 1794290 17267599 10.1073/pnas.0610772104
12. Feist AM Scholten JC Palsson BO Brockman FJ Ideker T Modeling methanogenesis with a genome-scale metabolic reconstruction of Methanosarcina barkeri Mol Syst Biol 2006, 2:2006.0004 1681478 16738551 10.1038/msb4100046
13. Thiele I Vo TD Price ND Palsson BO Expanded metabolic reconstruction of Helicobacter pylori (iIT341 GSM/GPR): An in silico genome-scale characterization of single- and double-deletion mutants J Bacteriol 2005, 187(16):5818-5830 1196094 16077130 10.1128/JB.187.16.5818-5830.2005
14. Edwards JS Palsson BO Systems properties of the Haemophilus influenzae Rd metabolic genotype J Biol Chem 1999, 274(25):17410-17416 10.1074/ jbc.274.25.17410 10364169
15. De Souza W Basic cell biology of Trypanosoma cruzi Curr Pharm Des 2002, 8(4):269-285 10.2174/1381612023396276 11860366
16. Opperdoes FR Compartmentation of carbohydrate metabolism in trypanosomes Annu Rev Microbiol 1987, 41:127-151 10.1146/annurev.mi.41.100187.001015 3120638
17. Opperdoes FR Borst P Localization of nine glycolytic enzymes in a microbody-like organelle in Trypanosoma brucei: The glycosome FEBS Lett 1977, 80(2):360-364 10.1016/0014-5793(77)80476-6 142663
18. Docampo R de Souza W Miranda K Rohloff P Moreno SN Acidocalcisomes - conserved from bacteria to man Nat Rev Microbiol 2005, 3(3):251-261 10.1038/nrmicro1097 15738951
19. Cunha-e-Silva N Sant'Anna C Pereira MG Porto-Carreiro I Jeovanio AL de Souza W Reservosomes: Multipurpose organelles? Parasitol Res 2006, 99(4):325-327 10.1007/s00436-006-0190-3 16794853
20. Estevez AM Simpson L Uridine insertion/deletion RNA editing in trypanosome mitochondria - a review Gene 1999, 240(2):247-260 10.1016/ S0378-1119(99)00437-0 10580144
21. Gao G Nara T Nakajima-Shimada J Aoki T Novel organization and sequences of five genes encoding all six enzymes for de novo pyrimidine biosynthesis in Trypanosoma cruzi J Mol Biol 1999, 285(1):149-161 10.1006/jmbi.1998.2293 9878395
22. Benabdellah K Gonzalez-Rey E Gonzalez A Alternative trans-splicing of the Trypanosoma cruzi LYT1 gene transcript results in compartmental and functional switch for the encoded protein Mol Microbiol 2007, 65(6):1559-1567 10.1111/j.1365-2958.2007.05892.x 17824931
23. Jamison DT World Bank, Disease Control Priorities Project Disease control priorities in developing countries New York; Washington, DC: Oxford University Press; World Bank 2 2006
24. Prata A Clinical and epidemiological aspects of Chagas disease Lancet Infect Dis 2001, 1(2):92-100 10.1016/S1473-3099(01)00065-2 11871482
25. Bern C Montgomery SP Herwaldt BL Rassi A Jr Marin-Neto JA Dantas RO Maguire JH Acquatella H Morillo C Kirchhoff LV Gilman RH Reyes PA Salvatella R Moore AC Evaluation and treatment of chagas disease in the United States: A systematic review JAMA 2007, 298(18):2171-2181 10.1001/ jama.298.18.2171 18000201
26. de Andrade AL Zicker F de Oliveira RM Almeida Silva S Luquetti A Travassos LR Almeida IC de Andrade SS de Andrade JG Martelli CM Randomised trial of efficacy of benznidazole in treatment of early Trypanosoma cruzi infection Lancet 1996, 348(9039):1407-1413 10.1016/ S0140-6736(96)04128-1 8937280
27. Sosa Estani S Segura EL Ruiz AM Velazquez E Porcel BM Yampotis C Efficacy of chemotherapy with benznidazole in children in the indeterminate phase of Chagas' disease Am J Trop Med Hyg 1998, 59(4):526-529 9790423
28. Guimaraes AC Otto TD Alves-Ferreira M Miranda AB Degrave WM In silico reconstruction of the amino acid metabolic pathways of Trypanosoma cruzi Genet Mol Res 2008, 7(3):872-882 18949706
29. Opperdoes FR Szikora JP In silico prediction of the glycosomal enzymes of Leishmania major and trypanosomes Mol Biochem Parasitol 2006, 147(2):193-206 10.1016/j.molbiopara.2006.02.010 16546274
30. Bringaud F Riviere L Coustou V Energy metabolism of trypanosomatids: adaptation to available carbon sources Mol Biochem Parasitol 2006, 149(1):1-9 10.1016/j.molbiopara.2006.03.017 16682088
31. Sanchez-Moreno M Fernandez-Becerra MC Castilla-Calvente JJ Osuna A Metabolic studies by 1H NMR of different forms of Trypanosoma cruzi as obtained by 'in vitro' culture FEMS Microbiol Lett 1995, 133(1-2):119-125 10.1111/j.1574-6968.1995.tb07871.x 8566696
32. Tielens AG Van Hellemond JJ Differences in energy metabolism between trypanosomatidae Parasitol Today 1998, 14(7):265-272 10.1016/ S0169-4758(98)01263-0 17040781
33. Frydman B de los Santos C Cannata JJ Cazzulo JJ Carbon-13 nuclear magnetic resonance analysis of [1-13C]glucose metabolism in Trypanosoma cruzi. Evidence of the presence of two alanine pools and of two CO2 fixation reactions Eur J Biochem 1990, 192(2):363-368 10.1111/ j.1432-1033.1990.tb19235.x 2120054
34. Cazzulo JJ Franke de Cazzulo BM Engel JC Cannata JJ End products and enzyme levels of aerobic glucose fermentation in trypanosomatids Mol Biochem Parasitol 1985, 16(3):329-343 10.1016/0166-6851(85)90074-X 3903497
35. Cross GA Klein RA Linstead DJ Utilization of amino acids by Trypanosoma brucei in culture: L-threonine as a precursor for acetate Parasitology 1975, 71(2):311-326 10.1017/S0031182000046758 1187188
36. Mahadevan R Schilling CH The effects of alternate optimal solutions in constraint-based genome-scale metabolic models Metab Eng 2003, 5(4):264-276 10.1016/j.ymben.2003.09.002 14642354
37. Azema L Lherbet C Baudoin C Blonski C Cell permeation of a Trypanosoma brucei aldolase inhibitor: Evaluation of different enzyme-labile phosphate protecting groups Bioorg Med Chem Lett 2006, 16(13):3440-3443 10.1016/j.bmcl.2006.04.010 16632348
38. Dardonville C Rinaldi E Hanau S Barrett MP Brun R Gilbert IH Synthesis and biological evaluation of substrate-based inhibitors of 6-phosphogluconate dehydrogenase as potential drugs against African trypanosomiasis Bioorg Med Chem 2003, 11(14):3205-3214 10.1016/ S0968-0896(03)00191-3 12818683
39. Aronov AM Suresh S Buckner FS Van Voorhis WC Verlinde CL Opperdoes FR Hol WG Gelb MH Structure-based design of submicromolar, biologically active inhibitors of trypanosomatid glyceraldehyde-3-phosphate dehydrogenase Proc Natl Acad Sci USA 1999, 96(8):4273-4278 16322 10200252 10.1073/pnas.96.8.4273
40. Sanz-Rodriguez CE Concepcion JL Pekerar S Oldfield E Urbina JA Bisphosphonates as inhibitors of Trypanosoma cruzi hexokinase: Kinetic and metabolic studies J Biol Chem 2007, 282(17):12377-12387 10.1074/ jbc.M607286200 17329254
41. Cortes-Figueroa AA Perez-Torres A Salaiza N Cabrera N Escalona-Montano A Rondan A Aguirre-Garcia M Gomez-Puyou A Perez-Montfort R Becker I A monoclonal antibody that inhibits Trypanosoma cruzi growth in vitro and its reaction with intracellular triosephosphate isomerase Parasitol Res 2008, 102(4):635-643 10.1007/s00436-007-0803-5 18046577
42. Rubbo H Denicola A Radi R Peroxynitrite inactivates thiol-containing enzymes of Trypanosoma cruzi energetic metabolism and inhibits cell respiration Arch Biochem Biophys 1994, 308(1):96-102 10.1006/ abbi.1994.1014 8311481
43. Albert MA Haanstra JR Hannaert V Van Roy J Opperdoes FR Bakker BM Michels PA Experimental and in silico analyses of glycolytic flux control in bloodstream form Trypanosoma brucei J Biol Chem 2005, 280(31):28306-28315 10.1074/jbc.M502403200 15955817
44. Coustou V Biran M Breton M Guegan F Riviere L Plazolles N Nolan D Barrett MP Franconi JM Bringaud F Glucose-induced remodeling of intermediary and energy metabolism in procyclic Trypanosoma brucei J Biol Chem 2008, 283(24):16342-16354 10.1074/jbc.M709592200 18430732
45. Bochud-Allemann N Schneider A Mitochondrial substrate level phosphorylation is essential for growth of procyclic Trypanosoma brucei J Biol Chem 2002, 277(36):32849-32854 10.1074/jbc.M205776200 12095995
46. Hwang HY Ullman B Genetic analysis of purine metabolism in Leishmania donovani J Biol Chem 1997, 272(31):19488-19496 10.1074/jbc.272.31.19488 9235951
47. Subramaniam C Veazey P Redmond S Hayes-Sinclair J Chambers E Carrington M Gull K Matthews K Horn D Field MC Chromosome-wide analysis of gene function by RNA interference in the african trypanosome Eukaryot Cell 2006, 5(9):1539-1549 1563588 16963636 10.1128/EC.00141-06
48. Besteiro S Biran M Biteau N Coustou V Baltz T Canioni P Bringaud F Succinate secreted by Trypanosoma brucei is produced by a novel and unique glycosomal enzyme, NADH-dependent fumarate reductase J Biol Chem 2002, 277(41):38001-38012 10.1074/jbc.M201759200 12138089
49. Fast B Kremp K Boshart M Steverding D Iron-dependent regulation of transferrin receptor expression in Trypanosoma brucei Biochem J 1999, 342(Pt 3):691-696 1220511 10477281 10.1042/0264-6021:3420691
50. Riviere L van Weelden SW Glass P Vegh P Coustou V Biran M van Hellemond JJ Bringaud F Tielens AG Boshart M Acetyl: succinate CoA-transferase in procyclic Trypanosoma brucei. Gene identification and role in carbohydrate metabolism J Biol Chem 2004, 279(44):45337-45346 10.1074/ jbc.M407513200 15326192
51. Coustou V Besteiro S Biran M Diolez P Bouchaud V Voisin P Michels PA Canioni P Baltz T Bringaud F ATP generation in the Trypanosoma brucei procyclic form: Cytosolic substrate level is essential, but not oxidative phosphorylation J Biol Chem 2003, 278(49):49625-49635 10.1074/ jbc.M307872200 14506274
52. Maugeri DA Cazzulo JJ The pentose phosphate pathway in Trypanosoma cruzi FEMS Microbiol Lett 2004, 234(1):117-123 10.1111/ j.1574-6968.2004.tb09522.x 15109729
53. Cannata JJ Cazzulo JJ The aerobic fermentation of glucose by Trypanosoma cruzi Comp Biochem Physiol B 1984, 79(3):297-308 10.1016/ 0305-0491(84)90380-8 6391799
54. Shlomi T Cabili MN Herrgard MJ Palsson BO Ruppin E Network-based prediction of human tissue-specific metabolism Nat Biotechnol 2008, 26(9):1003-1010 10.1038/nbt.1487 18711341
55. Chavali AK Whittemore JD Eddy JA Williams KT Papin JA Systems analysis of metabolism in the pathogenic trypanosomatid Leishmania major Mol Syst Biol 2008, 4:177 2290936 18364711 10.1038/msb.2008.15
56. Joyce AR Reed JL White A Edwards R Osterman A Baba T Mori H Lesely SA Palsson BO Agarwalla S Experimental and computational assessment of conditionally essential genes in Escherichia coli J Bacteriol 2006, 188(23):8259-8271 1698209 17012394 10.1128/JB.00740-06
57. Feist AM Henry CS Reed JL Krummenacker M Joyce AR Karp PD Broadbelt LJ Hatzimanikatis V Palsson BO A genome-scale metabolic reconstruction for Escherichia coli K-12 MG1655 that accounts for 1260 ORFs and thermodynamic information Mol Syst Biol 2007, 3:121 1911197 17593909 10.1038/msb4100155
58. Forster J Famili I Fu P Palsson BO Nielsen J Genome-scale reconstruction of the Saccharomyces cerevisiae metabolic network Genome Res 2003, 13(2):244-253 420374 12566402 10.1101/gr.234503
59. Duarte NC Herrgard MJ Palsson BO Reconstruction and validation of Saccharomyces cerevisiae iND750, a fully compartmentalized genome-scale metabolic model Genome Res 2004, 14(7):1298-1309 442145 15197165 10.1101/ gr.2250904
60. Herrgard MJ Lee BS Portnoy V Palsson BO Integrated analysis of regulatory and metabolic networks reveals novel regulatory mechanisms in Saccharomyces cerevisiae Genome Res 2006, 16(5):627-635 1457053 16606697 10.1101/gr.4083206
61. Becker SA Palsson BO Context-specific metabolic networks are consistent with experiments PLoS Comput Biol 2008, 4(5):e1000082 2366062 18483554 10.1371/journal.pcbi.1000082
62. UniProt Consortium The Universal Protein Resource (UniProt) Nucleic Acids Res 2007 35 Database D193-7 1669721 17142230 10.1093/nar/gkl929
63. Kanehisa M Araki M Goto S Hattori M Hirakawa M Itoh M Katayama T Kawashima S Okuda S Tokimatsu T Yamanishi Y KEGG for linking genomes to life and the environment Nucleic Acids Res 2008, 36 Database D480-4 2238879 18077471
64. Hertz-Fowler C Peacock CS Wood V Aslett M Kerhornou A Mooney P Tivey A Berriman M Hall N Rutherford K Parkhill J Ivens AC Rajandream MA Barrell B GeneDB: A resource for prokaryotic and eukaryotic organisms Nucleic Acids Res 2004 32 Database D339-43 308742 14681429 10.1093/nar/gkh007
65. Tetaud E Bringaud F Chabas S Barrett MP Baltz T Characterization of glucose transport and cloning of a hexose transporter gene in Trypanosoma cruzi Proc Natl Acad Sci USA 1994, 91(17):8278-8282 44589 8058795 10.1073/pnas.91.17.8278
66. Franco da Silveira J Colli W Chemical composition of the plasma membrane from epimastigote forms of Trypanosoma cruzi Biochim Biophys Acta 1981, 644(2):341-350 10.1016/0005-2736(81)90392-8 7020760
67. Silber AM Rojas RL Urias U Colli W Alves MJ Biochemical characterization of the glutamate transport in Trypanosoma cruzi Int J Parasitol 2006, 36(2):157-163 10.1016/j.ijpara.2005.10.006 16373069
68. Silber AM Tonelli RR Martinelli M Colli W Alves MJ Active transport of L-proline in Trypanosoma cruzi J Eukaryot Microbiol 2002, 49(6):441-446 10.1111/j.1550-7408.2002.tb00225.x 12503677
69. Canepa GE Bouvier LA Urias U Miranda MR Colli W Alves MJ Pereira CA Aspartate transport and metabolism in the protozoan parasite Trypanosoma cruzi FEMS Microbiol Lett 2005, 247(1):65-71 10.1016/ j.femsle.2005.04.029 15927749
70. Gianchandani EP Oberhardt MA Burgard AP Maranas CD Papin JA Predicting biological system objectives de novo from internal state measurements BMC Bioinformatics 2008, 9:43 2258290 18218092 10.1186/1471-2105-9-43
71. Dauner M Bailey JE Sauer U Metabolic flux analysis with a comprehensive isotopomer model in Bacillus subtilis Biotechnol Bioeng 2001, 76(2):144-156 10.1002/bit.1154 11505384
72. Varma A Palsson BO Metabolic capabilities of Escherichia coli J Theor Biol 1993, 165(4):503 -522 10.1006/jtbi.1993.1203
73. Xu P Alves JM Kitten T Brown A Chen Z Ozaki LS Manque P Ge X Serrano MG Puiu D Hendricks S Wang Y Chaplin MD Akan D Paik S Peterson DL Macrina FL Buck GA Genome of the opportunistic pathogen Streptococcus sanguinis J Bacteriol 2007, 189(8):3166-3175 1855836 17277061 10.1128/JB.01808-06