Handling Uncertainty in Dynamic Models: The Pentose Phosphate Pathway in Trypanosoma brucei

PLoS Computational Biology

Volumn 9, Issue 12, 2013, Pages

  Kerkhoven, Eduard J ^a,b,i   Achcar, Fiona ^a,c   Alibu, Vincent P ^a   Burchmore, Richard J ^a   Gilbert, Ian H ^d   Trybiło, Maciej ^e   Driessen, Nicole N ^f,j   Gilbert, David ^e   Breitling, Rainer ^g   Bakker, Barbara M ^f,h   Barrett, Michael P ^a  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

^b CHALMERS UNIVERSITY OF TECHNOLOGY   (Sweden)

^c UNIVERSITY OF GRONINGEN   (Netherlands)

^d UNIVERSITY OF DUNDEE   (United Kingdom)

^e BRUNEL UNIVERSITY   (United Kingdom)

^f VU UNIVERSITY AMSTERDAM   (Netherlands)

^g UNIVERSITY OF MANCHESTER   (United Kingdom)

^h UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

ⁱ MAKERERE UNIVERSITY   (Uganda)

^j LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

more..

Author keywords

[No Author keywords available]

Indexed keywords

DYNAMICS; ENZYMES; UNCERTAINTY ANALYSIS;

CYTOSOLS; DYNAMICS MODELS; GLYCOSOME; PARASITE-; PENTOSE PHOSPHATE PATHWAY; POTENTIAL DRUG TARGETS; RIBOKINASE; TRYPANOSOMA BRUCEI; UNCERTAINTY; UNICELLULAR ORGANISMS;

DYNAMIC MODELS;

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; PROTOZOAL PROTEIN; RIBOKINASE; RIBOSE 5 PHOSPHATE; UNCLASSIFIED DRUG;

ARTICLE; CELL MEMBRANE PERMEABILITY; CHEMICAL BINDING; CONTROLLED STUDY; CYTOSOL; ENZYME MECHANISM; GLYCOSOME; INTRACELLULAR TRANSPORT; MATHEMATICAL COMPUTING; MATHEMATICAL MODEL; MICROBIAL METABOLISM; MOLECULAR DYNAMICS; NONHUMAN; PARASITE SURVIVAL; PENTOSE PHOSPHATE CYCLE; THEORETICAL STUDY; TRYPANOSOMA BRUCEI;

ANIMALS; GLUCOSE; GLYCOLYSIS; MODELS, BIOLOGICAL; PENTOSE PHOSPHATE PATHWAY; RNA INTERFERENCE; TRYPANOSOMA BRUCEI BRUCEI; UNCERTAINTY;

EID: 84892684614     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1003371     Document Type: Article

References (61)

1. Barrett MP, Burchmore RJ, Stich A, Lazzari JO, Frasch AC, et al. (2003) The trypanosomiases. Lancet 362: 1469-1480 doi:10.1016/S0140-6736(03)14694-6.
2. Brun R, Blum J, Chappuis F, Burri C, (2010) Human African trypanosomiasis. Lancet 375: 148-159 doi:10.1016/S0140-6736(09)60829-1.
3. Barrett MP, Boykin DW, Brun R, Tidwell RR, (2007) Human African trypanosomiasis: pharmacological re-engagement with a neglected disease. Br J Pharmacol 152: 1155-1171 doi:10.1038/sj.bjp.0707354.
4. Bakker BM, Michels PAM, Opperdoes FR, Westerhoff HV, (1997) Glycolysis in bloodstream form Trypanosoma brucei can be understood in terms of the kinetics of the glycolytic enzymes. J Biol Chem 272: 3207-3215 doi:10.1074/jbc.272.6.3207.
5. Bakker BM, Michels PAM, Opperdoes FR, Westerhoff HV, (1999) What controls glycolysis in bloodstream form Trypanosoma brucei? J Biol Chem 274: 14551-14559 doi:10.1074/jbc.274.21.14551.
6. Helfert S, Estévez AM, Bakker B, Michels P, Clayton C, (2001) Roles of triosephosphate isomerase and aerobic metabolism in Trypanosoma brucei. Biochem J 357: 117-125.
7. Albert M-A, Haanstra JR, Hannaert V, Roy JV, Opperdoes FR, et al. (2005) Experimental and in silico analyses of glycolytic flux control in bloodstream form Trypanosoma brucei. J Biol Chem 280: 28306-28315 doi:10.1074/jbc.M502403200.
8. Achcar F, Kerkhoven EJ, (2012) The SilicoTryp Consortium (2012) Bakker BM, Barrett MP, et al. (2012) Dynamic modelling under uncertainty: the case of Trypanosoma brucei energy metabolism. PLoS Comput Biol 8: e1002352 doi:10.1371/journal.pcbi.1002352.
9. Haanstra JR, Kerkhoven EJ, van Tuijl A, Blits M, Wurst M, et al. (2011) A domino effect in drug action: from metabolic assault towards parasite differentiation. Mol Microbiol 79: 94-108 doi:10.1111/j.1365-2958.2010.07435.x.
10. Hanau S, Rippa M, Bertelli M, Dallocchio F, Barrett MP, (1996) 6-Phosphogluconate dehydrogenase from Trypanosoma brucei. Eur J Biochem 240: 592-599 doi:10.1111/j.1432-1033.1996.0592h.x.
11. Cordeiro AT, Thiemann OH, Michels PAM, (2009) Inhibition of Trypanosoma brucei glucose-6-phosphate dehydrogenase by human steroids and their effects on the viability of cultured parasites. Bioorg Med Chem 17: 2483-2489 doi:doi: DOI: 10.1016/j.bmc.2009.01.068.
12. Fairlamb AH, Henderson GB, Bacchi CJ, Cerami A, (1987) In vivo effects of difluoromethylornithine on trypanothione and polyamine levels in bloodstream forms of Trypanosoma brucei. Mol Biochem Parasitol 24: 185-191.
13. Allmann S, Morand P, Ebikeme C, Gales L, Biran M, et al. (2013) Cytosolic NADPH homeostasis in glucose-starved procyclic Trypanosoma brucei relies on malic enzyme and the pentose phosphate pathway fed by gluconeogenic flux. J Biol Chem 288: 18494-18505 doi:10.1074/jbc.M113.462978.
14. Barrett MP, Le Page RWF, (1993) A 6-phosphogluconate dehydrogenase gene from Trypanosoma brucei. Mol Biochem Parasitol 57: 89-99 doi:10.1016/0166-6851(93)90247-U.
15. Heise N, Opperdoes FR, (1999) Purification, localisation and characterisation of glucose-6-phosphate dehydrogenase of Trypanosoma brucei. Mol Biochem Parasitol 99: 21-32.
16. Duffieux F, Van Roy J, Michels PA, Opperdoes FR, (2000) Molecular characterization of the first two enzymes of the pentose-phosphate pathway of Trypanosoma brucei. Glucose-6-phosphate dehydrogenase and 6-phosphogluconolactonase. J Biol Chem 275: 27559-27565 doi:10.1074/jbc.M004266200.
17. Stoffel SA, Alibu VP, Hubert J, Ebikeme C, Portais J-C, et al. (2011) Transketolase in Trypanosoma brucei. Mol Biochem Parasitol 179: 1-7 doi:10.1016/j.molbiopara.2011.04.006.
18. Colasante C, Ellis M, Ruppert T, Voncken F, (2006) Comparative proteomics of glycosomes from bloodstream form and procyclic culture form Trypanosoma brucei brucei. Proteomics 6: 3275-3293 doi:10.1002/pmic.200500668.
19. Vertommen D, Van Roy J, Szikora J-P, Rider MH, Michels PAM, et al. (2008) Differential expression of glycosomal and mitochondrial proteins in the two major life-cycle stages of Trypanosoma brucei. Mol Biochem Parasitol 158: 189-201 doi:10.1016/j.molbiopara.2007.12.008.
20. Opperdoes FR, Szikora J-P, (2006) In silico prediction of the glycosomal enzymes of Leishmania major and trypanosomes. Mol Biochem Parasitol 147: 193-206 doi:10.1016/j.molbiopara.2006.02.010.
21. Visser N, Opperdoes FR, (1980) Glycolysis in Trypanosoma brucei. Eur J Biochem 103: 623-632.
22. Turnock DC, Ferguson MAJ, (2007) Sugar Nucleotide Pools of Trypanosoma brucei, Trypanosoma cruzi, and Leishmania major. Eukaryotic Cell 6: 1450-1463 doi:10.1128/EC.00175-07.
23. Cronin CN, Nolan DP, Paul Voorheis H, (1989) The enzymes of the classical pentose phosphate pathway display differential activities in procyclic and bloodstream forms of Trypanosoma brucei. FEBS Letters 244: 26-30 doi:10.1016/0014-5793(89)81154-8.
24. Tewari YB, Steckler DK, Goldberg RN, Gitomer WL, (1988) Thermodynamics of hydrolysis of sugar phosphates. J Biol Chem 263: 3670-3675.
25. Krakow JL, Wang CC, (1990) Purification and characterization of glycerol kinase from Trypanosoma brucei. Mol Biochem Parasitol 43: 17-25.
26. Voncken F, Gao F, Wadforth C, Harley M, Colasante C, (2013) The Phosphoarginine Energy-Buffering System of Trypanosoma brucei Involves Multiple Arginine Kinase Isoforms with Different Subcellular Locations. PLoS ONE 8: e65908 doi:10.1371/journal.pone.0065908.
27. Van Roermund CW, Drissen R, van Den Berg M, Ijlst L, Hettema EH, et al. (2001) Identification of a peroxisomal ATP carrier required for medium-chain fatty acid beta-oxidation and normal peroxisome proliferation in Saccharomyces cerevisiae. Mol Cell Biol 21: 4321-4329 doi:10.1128/MCB.21.13.4321-4329.2001.
28. Teusink B, Walsh MC, van Dam K, Westerhoff HV, (1998) The danger of metabolic pathways with turbo design. Trends Biochem Sci 23: 162-169 doi:10.1016/S0968-0004(98)01205-5.
29. Blangy D, Buc H, Monod J, (1968) Kinetics of the allosteric interactions of phosphofructokinase from Escherichia coli. J Mol Biol 31: 13-35 doi:10.1016/0022-2836(68)90051-X.
30. Bakker BM, Mensonides FI, Teusink B, van Hoek P, Michels PA, et al. (2000) Compartmentation protects trypanosomes from the dangerous design of glycolysis. Proc Natl Acad Sci USA 97: 2087-2092 doi:10.1073/pnas.030539197.
31. Haanstra JR, Tuijl A van, Kessler P, Reijnders W, Michels PAM, et al. (2008) Compartmentation prevents a lethal turbo-explosion of glycolysis in trypanosomes. Proc Natl Acad Sci USA 105: 17718-17723 doi:10.1073/pnas.0806664105.
32. Furuya T, Kessler P, Jardim A, Schnaufer A, Crudder C, et al. (2002) Glucose is toxic to glycosome-deficient trypanosomes. Proc Natl Acad Sci USA 99: 14177-14182 doi:10.1073/pnas.222454899.
33. Kessler PS, Parsons M, (2005) Probing the role of compartmentation of glycolysis in procyclic form Trypanosoma brucei RNA interference studies of PEX14, hexokinase and phosphofructokinase. J Biol Chem 280: 9030-9036 doi:10.1074/jbc.M412033200.
34. Gualdron-López M, Vapola MH, Miinalainen IJ, Hiltunen JK, Michels PAM, et al. (2012) Channel-forming activities in the glycosomal fraction from the bloodstream form of Trypanosoma brucei. PLoS ONE 7: e34530 doi:10.1371/journal.pone.0034530.
35. Maugeri DA, Cazzulo JJ, (2004) The pentose phosphate pathway in Trypanosoma cruzi. FEMS Microbiol Lett 234: 117-123 doi:10.1016/j.femsle.2004.03.018.
36. Grant PT, Fulton JD, (1957) The catabolism of glucose by strains of Trypanosoma rhodesiense. Biochem J 66: 242-250.
37. Haanstra JR, van Tuijl A, van Dam J, van Winden W, Tielens AGM, et al. (2012) Proliferating bloodstream-form Trypanosoma brucei use a negligible part of consumed glucose for anabolic processes. Int J Parasitol 42: 667-673 doi:10.1016/j.ijpara.2012.04.009.
38. LePage RW, Barrett MP, (1990) Cloning of the 6-phosphogluconate dehydrogenase gene from Trypanosoma brucei by complementation in Escherichia coli. Biochem Soc Trans 18: 724-727.
39. Bewley GC, Lucchesi JC, (1975) Lethal effects of low and "null" activity alleles of 6-phosphogluconate dehydrogenase in Drosophila melanogaster. Genetics 79: 451-457.
40. Hughes MB, Lucchesi JC, (1977) Genetic rescue of a lethal "null" activity allele of 6-phosphogluconate dehydrogenase in Drosophila melanogaster. Science 196: 1114-1115 doi:10.1126/science.404711.
41. Lobo Z, Maitra PK, (1982) Pentose phosphate pathway mutants of yeast. Mol Gen Genet 185: 367-368 doi:10.1007/BF00330815.
42. Sukhatme VP, Chan B, (2012) Glycolytic cancer cells lacking 6-phosphogluconate dehydrogenase metabolize glucose to induce senescence. FEBS Letters 586: 2389-2395 doi:10.1016/j.febslet.2012.05.052.
43. Marchand M, Kooystra U, Wierenga RK, Lambeir AM, Van Beeumen J, et al. (1989) Glucosephosphate isomerase from Trypanosoma brucei. Cloning and characterization of the gene and analysis of the enzyme. Eur J Biochem 184: 455-464.
44. Goldberg RN, Tewari YB, (1995) Thermodynamics of Enzyme-Catalyzed Reactions: Part 5. Isomerases and Ligases. J Phys Chem Ref Data 24: 1765-1801.
45. Ryley J, (1962) Studies on the metabolism of the protozoa. 9. Comparative metabolism of blood-stream and culture forms of Trypanosoma rhodesiense. Biochem J 85: 211-223.
46. Achcar F, Barrett MP, Breitling R, (2013) Explicit consideration of topological and parameter uncertainty gives new insights into a well-established model of glycolysis. FEBS Journal doi: 10.1111/febs.12436.
47. Cronin CN, Tipton KF, (1987) Kinetic studies on the reaction catalysed by phosphofructokinase from Trypanosoma brucei. Biochem J 245: 13-18.
48. Miclet E, Stoven V, Michels PA, Opperdoes FR, Lallemand JY, et al. (2001) NMR spectroscopic analysis of the first two steps of the pentose-phosphate pathway elucidates the role of 6-phosphogluconolactonase. J Biol Chem 276: 34840-34846 doi:10.1074/jbc.M105174200.
49. Olivier BG, Rohwer JM, Hofmeyr J-HS, (2005) Modelling cellular systems with PySCeS. Bioinformatics 21: 560-561 doi:10.1093/bioinformatics/bti046.
50. Hoops S, Sahle S, Gauges R, Lee C, Pahle J, et al. (2006) COPASI-a COmplex PAthway SImulator. Bioinformatics 22: 3067-3074 doi:10.1093/bioinformatics/btl485.
51. Anderson A, Cooper RA, (1969) The significance of ribokinase for ribose utilization by Escherichia coli. Biochim Biophys Acta 177: 163-165.
52. Hirumi H, Hirumi K, (1989) Continuous cultivation of Trypanosoma brucei blood stream forms in a medium containing a low concentration of serum protein without feeder cell layers. J Parasitol 75: 985-989.
53. Ward CP, Wong PE, Burchmore RJ, de Koning HP, Barrett MP, (2011) Trypanocidal furamidine analogues: influence of pyridine nitrogens on trypanocidal activity, transport kinetics, and resistance patterns. Antimicrob Agents Chemother 55: 2352-2361 doi:10.1128/AAC.01551-10.
54. Alsford S, Horn D, (2008) Single-locus targeting constructs for reliable regulated RNAi and transgene expression in Trypanosoma brucei. Mol Biochem Parasitol 161: 76-79 doi:10.1016/j.molbiopara.2008.05.006.
55. Alibu VP, Storm L, Haile S, Clayton C, Horn D, (2005) A doubly inducible system for RNA interference and rapid RNAi plasmid construction in Trypanosoma brucei. Mol Biochem Parasitol 139: 75-82 doi:10.1016/j.molbiopara.2004.10.002.
56. Cross M, Kieft R, Sabatini R, Dirks-Mulder A, Chaves I, et al. (2002) J-binding protein increases the level and retention of the unusual base J in trypanosome DNA. Mol Microbiol 46: 37-47 doi:10.1046/j.1365-2958.2002.03144.x.
57. Burkard G, Fragoso CM, Roditi I, (2007) Highly efficient stable transformation of bloodstream forms of Trypanosoma brucei. Mol Biochem Parasitol 153: 220-223 doi:10.1016/j.molbiopara.2007.02.008.
58. Schumann Burkard G, Jutzi P, Roditi I, (2011) Genome-wide RNAi screens in bloodstream form trypanosomes identify drug transporters. Mol Biochem Parasitol 175: 91-94 doi:10.1016/j.molbiopara.2010.09.002.
59. Hauser R, Pypaert M, Hausler T, Horn EK, Schneider A, (1996) In vitro import of proteins into mitochondria of Trypanosoma brucei and Leishmania tarentolae. J Cell Sci 109: 517-523.
60. Pfeiffer T, Sánchez-Valdenebro I, Nuño JC, Montero F, Schuster S, (1999) METATOOL: for studying metabolic networks. Bioinformatics 15: 251-257 doi:10.1093/bioinformatics/15.3.251.
61. Gualdrón-López M, Brennand A, Hannaert V, Quiñones W, Cáceres AJ, et al. (2012) When, how and why glycolysis became compartmentalised in the Kinetoplastea. A new look at an ancient organelle. Int J Parasitol 42: 1-20 doi:10.1016/j.ijpara.2011.10.007.