Network-based assessment of the selectivity of metabolic drug targets in Plasmodium falciparum with respect to human liver metabolism

BMC Systems Biology

Volumn 6, Issue , 2012, Pages

  Bazzani, Susanna ^a   Hoppe, Andreas ^a   Holzhütter, Hermann Georg ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

Drug selectivity; Drug targets; Flux balance analysis; Genome scale networks; Human hepatocyte; Plasmodium falciparum; Reduced fitness

Indexed keywords

PLASMODIUM FALCIPARUM;

ANTIMALARIAL AGENT;

ANIMAL; ARTICLE; BIOLOGY; DRUG EFFECT; ENZYMOLOGY; HUMAN; LIVER; METABOLISM; METHODOLOGY; MOLECULARLY TARGETED THERAPY; MOUSE; PARASITOLOGY; PHYSIOLOGY; PLASMODIUM FALCIPARUM;

ANIMALS; ANTIMALARIALS; COMPUTATIONAL BIOLOGY; HUMANS; LIVER; METABOLIC NETWORKS AND PATHWAYS; MICE; MOLECULAR TARGETED THERAPY; PLASMODIUM FALCIPARUM;

MLCS; MLOWN;

EID: 84865535722     PISSN: None     EISSN: 17520509     Source Type: Journal    
DOI: 10.1186/1752-0509-6-118     Document Type: Article

References (60)

1. Lin Z, Will Y. Evaluation of Drugs with Specific Organ Toxicities in Organ Specific Cell Lines. Toxicol Sci 2012, 126(1):114-27. [http://view.ncbi.nlm.nih.gov/pubmed/22166485], 10.1093/toxsci/kfr339, 22166485.
2. Armstrong PB. Proteases and protease inhibitors: a balance of activities in host-pathogen interaction. Immunobiology 2006, 211(4):263-81. [http://view.ncbi.nlm.nih.gov/pubmed/16697919], 10.1016/j.imbio.2006.01.002, 16697919.
3. Singh VK, Ghosh I. Kinetic modeling of tricarboxylic acid cycle and glyoxylate bypass in Mycobacterium tuberculosis, and its application to assessment of drug targets. Theor Biol Med Model 2006, 3:27. [http://view.ncbi.nlm.nih.gov/pubmed/16887020], 10.1186/1742-4682-3-27, 1563452, 16887020.
4. Hornberg JJ, Bruggeman FJ, Bakker BM, Westerhoff HV. Metabolic control analysis to identify optimal drug targets. Prog Drug Res 2007, 64(171):173-89. [http://view.ncbi.nlm.nih.gov/pubmed/17195475].
5. Murabito E, Smallbone K, Swinton J, Westerhoff HV, Steuer R. A probabilistic approach to identify putative drug targets in biochemical networks. J R Soc Interface 2011, 8(59):880-95. [http://view.ncbi.nlm.nih.gov/pubmed/21123256], 10.1098/rsif.2010.0540, 3104352, 21123256.
6. Edwards JS, Palsson BO. Metabolic flux balance analysis and the in silico analysis of Escherichia coli K-12 gene deletions. BMC Bioinformatics 2000, 1:1. [http://view.ncbi.nlm.nih.gov/pubmed/11001586], 10.1186/1471-2105-1-1, 29061, 11001586.
7. Snitkin ES, Dudley AM, Janse DM, Wong K, Church GM, Segrè D. Model-driven analysis of experimentally determined growth phenotypes for 465 yeast gene deletion mutants under 16 different conditions. Genome Biol 2008, 9(9):R140. [http://view.ncbi.nlm.nih.gov/pubmed/18808699], 10.1186/gb-2008-9-9-r140, 2592718, 18808699.
8. Raman K, Rajagopalan P, Chandra N. Flux balance analysis of mycolic acid pathway: targets for anti-tubercular drugs. PLoS Comput Biol 2005, 1(5):e46. [http://view.ncbi.nlm.nih.gov/pubmed/16261191], 10.1371/journal.pcbi.0010046, 1246807, 16261191.
9. Lee DS, Burd H, Liu J, Almaas E, Wiest O, Barabási AL, Oltvai ZN, Kapatral V. Comparative genome-scale metabolic reconstruction and flux balance analysis of multiple Staphylococcus aureus genomes identify novel antimicrobial drug targets. J Bacteriol 2009, 191(12):4015-24. [http://view.ncbi.nlm.nih.gov/pubmed/19376871], 10.1128/JB.01743-08, 2698402, 19376871.
10. Mazumdar V, Snitkin ES, Amar S, Segrè D. Metabolic network model of a human oral pathogen. J Bacteriol 2009, 191:74-90. [http://view.ncbi.nlm.nih.gov/pubmed/18931137], 10.1128/JB.01123-08, 2612419, 18931137.
11. Oberhardt MA, Puchałka J. Genome-scale metabolic network analysis of the opportunistic pathogen Pseudomonas aeruginosa PAO1. J Bacteriol 2008, 190(8):2790-803. [http://view.ncbi.nlm.nih.gov/pubmed/18192387], 10.1128/JB.01583-07, 2293256, 18192387.
12. Fatumo S, Plaimas K, Adebiyi E, König R. Comparing metabolic network models based on genomic and automatically inferred enzyme information from Plasmodium and its human host to define drug targets in silico. Infect Genet Evol 2011, 11(4):708-15. [http://view.ncbi.nlm.nih.gov/pubmed/21515412], 10.1016/j.meegid.2011.04.013, 21515412.
13. Bordbar A, Lewis NE, Schellenberger J, Palsson BO, Jamshidi N. Insight into human alveolar macrophage and M. tuberculosis interactions via metabolic reconstructions. Mol Syst Biol 2010, 6:422. [http://view.ncbi.nlm.nih.gov/pubmed/20959820], 2990636, 20959820.
14. Huthmacher C, Hoppe A, Bulik S, Holzhütter HG. Antimalarial drug targets in Plasmodium falciparum predicted by stage-specific metabolic network analysis. BMC Syst Biol 2010, 4:120. [http://view.ncbi.nlm.nih.gov/pubmed/20807400], 10.1186/1752-0509-4-120, 2941759, 20807400.
15. Folger O, Jerby L, Frezza C, Gottlieb E, Ruppin E, Shlomi T. Predicting selective drug targets in cancer through metabolic networks. Mol Syst Biol 2011, 7:501. [http://view.ncbi.nlm.nih.gov/pubmed/21694718], 3159974, 21694718.
16. Gille C, Bölling C, Hoppe A, Bulik S, Hoffmann S, Hübner K, Karlstädt A, Ganeshan R, König M, Rother K, Weidlich M, Behre J, Holzhütter HG. HepatoNet1: a comprehensive metabolic reconstruction of the human hepatocyte for the analysis of liver physiology. Mol Syst Biol 2010, 6:411. [http://view.ncbi.nlm.nih.gov/pubmed/20823849], 2964118, 20823849.
17. Nussenzweig RS, Long CA. Malaria vaccines: multiple targets. Science 1994, 265(5177):1381-3. [http://view.ncbi.nlm.nih.gov/pubmed/8073276], 10.1126/science.8073276, 8073276.
18. Fatumo S, Plaimas K, Mallm JP, Schramm G, Adebiyi E, Oswald M, Eils R, König R. Estimating novel potential drug targets of Plasmodium falciparum by analysing the metabolic network of knock-out strains in silico. Infect Genet Evol 2009, 9(3):351-8. [http://view.ncbi.nlm.nih.gov/pubmed/18313365], 10.1016/j.meegid.2008.01.007, 18313365.
19. Yeh I, Hanekamp T, Tsoka S, Karp PD, Altman RB. Computational analysis of Plasmodium falciparum metabolism: organizing genomic information to facilitate drug discovery. Genome Res 2004, 14(5):917-24. [http://view.ncbi.nlm.nih.gov/pubmed/15078855], 10.1101/gr.2050304, 479120, 15078855.
20. Holzhütter HG. The generalized flux-minimization method and its application to metabolic networks affected by enzyme deficiencies. Biosystems 2006, 83(2-3):98-107. [http://view.ncbi.nlm.nih.gov/pubmed/16229937], 10.1016/j.biosystems.2005.04.008, 16229937.
21. Tomoda H, Igarashi K, Cyong JC, Omura S. Evidence for an essential role of long chain acyl-CoA synthetase in animal cell proliferation. Inhibition of long chain acyl-CoA synthetase by triacsins caused inhibition of Raji cell proliferation. J Biol Chem 1991, 266(7):4214-9. [http://view.ncbi.nlm.nih.gov/pubmed/1999415].
22. Galvani E, Peters GJ, Giovannetti E. Thymidylate synthase inhibitors for non-small cell lung cancer. Expert Opin Investig Drugs 2011, 20(10):1343-56. [http://view.ncbi.nlm.nih.gov/pubmed/21905922], 10.1517/13543784.2011.617742, 21905922.
23. Wilson PM, Labonte MJ, Lenz HJD, Mack PC, Ladner RD. Inhibition of dUTPase induces synthetic lethality with thymidylate synthase-targeted therapies in non-small cell lung cancer. Mol Cancer Ther 2012, 11(3):616-28. [http://view.ncbi.nlm.nih.gov/pubmed/22172489], 10.1158/1535-7163.MCT-11-0781, 22172489.
24. Bello AM, Konforte D, Poduch E, Furlonger C, Wei L, Liu Y, Lewis M, Pai EF, Paige CJ, Kotra LP. Structure-activity relationships of orotidine-5'-monophosphate decarboxylase inhibitors as anticancer agents. J Med Chem 2009, 52(6):1648-58. [http://view.ncbi.nlm.nih.gov/pubmed/19260677], 10.1021/jm801224t, 19260677.
25. Ochiai T, Nishimura K, Noguchi H, Kitajima M, Tsukada A, Watanabe E, Nagaoka I, Futagawa S. Prognostic impact of orotate phosphoribosyl transferase among 5-fluorouracil metabolic enzymes in resectable colorectal cancers treated by oral 5-fluorouracil-based adjuvant chemotherapy. Int J Cancer 2006, 118(12):3084-8. [http://view.ncbi.nlm.nih.gov/pubmed/16425285], 10.1002/ijc.21779, 16425285.
26. Pausch J, Rasenack J, Häussinger D, Gerok W. Hepatic carbamoyl phosphate metabolism. Role of cytosolic and mitochondrial carbamoyl phosphate in de novo pyrimidine synthesis. Eur J Biochem 1985, 150:189-94. [http://view.ncbi.nlm.nih.gov/pubmed/4018077], 10.1111/j.1432-1033.1985.tb09006.x, 4018077.
27. Brooke J, Szabados E, Lyons SD, Goodridge RJ, Harsanyi MC, Poiner A, Christopherson RI. Cytotoxic effects of dihydroorotase inhibitors upon human CCRF-CEM leukemia. Cancer Res 1990, 50(24):7793-8. [http://view.ncbi.nlm.nih.gov/pubmed/1979249].
28. Keil S, Müller M, Zoller G, Haschke G, Schroeter K, Glien M, Ruf S, Focken I, Herling AW, Schmoll D. Identification and synthesis of novel inhibitors of acetyl-CoA carboxylase with in vitro and in vivo efficacy on fat oxidation. J Med Chem 2010, 53(24):8679-87. [http://view.ncbi.nlm.nih.gov/pubmed/21082864], 10.1021/jm101179e, 21082864.
29. Chajès V, Cambot M, Moreau K, Lenoir GM, Joulin V. Acetyl-CoA carboxylase alpha is essential to breast cancer cell survival. Cancer Res 2006, 66(10):5287-94. [http://view.ncbi.nlm.nih.gov/pubmed/16707454], 10.1158/0008-5472.CAN-05-1489, 16707454.
30. Marrero M, Prough RA, Putnam RS, Bennett M, Milewich L. Inhibition of carbamoyl phosphate synthetase-I by dietary dehydroepiandrosterone. J Steroid Biochem Mol Biol 1991, 38(5):599-609. [http://view.ncbi.nlm.nih.gov/pubmed/1828177], 10.1016/0960-0760(91)90319-Z, 1828177.
31. Wydysh EA, Medghalchi SM, Vadlamudi A, Townsend CA. Design and synthesis of small molecule glycerol 3-phosphate acyltransferase inhibitors. J Med Chem 2009, 52(10):3317-27. [http://view.ncbi.nlm.nih.gov/pubmed/19388675], 10.1021/jm900251a, 3184552, 19388675.
32. Mashima T, Oh-hara T, Sato S, Mochizuki M, Sugimoto Y, Yamazaki K, Hamada J, Tada M, Moriuchi T, Ishikawa Y, Kato Y, Tomoda H, Yamori T, Tsuruo T. p53-defective tumors with a functional apoptosome-mediated pathway: a new therapeutic target. J Natl Cancer Inst 2005, 97(10):765-77. [http://view.ncbi.nlm.nih.gov/pubmed/15900046], 10.1093/jnci/dji133, 15900046.
33. Mitamura T, Palacpac NMQ. Lipid metabolism in Plasmodium falciparum-infected erythrocytes: possible new targets for malaria chemotherapy. Microbes Infect 2003, 5(6):545-52. [http://view.ncbi.nlm.nih.gov/pubmed/12758284], 10.1016/S1286-4579(03)00070-4, 12758284.
34. Labaied M, Dagan A, Dellinger M, Gèze M, Egée S, Thomas SL, Wang C, Gatt S, Grellier P. Anti-Plasmodium activity of ceramide analogs. Malar J 2004, 3:49. [http://view.ncbi.nlm.nih.gov/pubmed/15588325], 10.1186/1475-2875-3-49, 539285, 15588325.
35. Keppler DO, Schulz-Holstege C, Fauler J, Reiffen KA, Schneider F. Uridylate trapping, induction of UTP deficiency, and stimulation of pyrimidine synthesis de novo by D-galactosone. Biochem J 1982, 206:139-46. [http://view.ncbi.nlm.nih.gov/pubmed/7126188], 1158559, 7126188.
36. Kuhajda FP, Aja S, Tu Y, Han WF, Medghalchi SM, El M, Landree LE, Peterson JM, Daniels K, Wong K, Wydysh EA, Townsend CA, Ronnett GV. Pharmacological glycerol-3-phosphate acyltransferase inhibition decreases food intake and adiposity and increases insulin sensitivity in diet-induced obesity. Am J Physiol Regul Integr Comp Physiol 2011, 301:R116-30. [http://view.ncbi.nlm.nih.gov/pubmed/21490364], 10.1152/ajpregu.00147.2011, 3129873, 21490364.
37. Santiago TC, Zufferey R, Mehra RS, Coleman RA, Mamoun CB. The Plasmodium falciparum PfGatp is an endoplasmic reticulum membrane protein important for the initial step of malarial glycerolipid synthesis. J Biol Chem 2004, 279(10):9222-32. [http://view.ncbi.nlm.nih.gov/pubmed/14668349], 10.1074/jbc.M310502200, 14668349.
38. Palacpac NMQ, Hiramine Y, Mi-ichi F, Torii M, Kita K, Hiramatsu R, Horii T, Mitamura T. Developmental-stage-specific triacylglycerol biosynthesis, degradation and trafficking as lipid bodies in Plasmodium falciparum-infected erythrocytes. J Cell Sci 2004, 117(Pt 8):1469-80. [http://view.ncbi.nlm.nih.gov/pubmed/15020675].
39. Velanker SS, Ray SS, Gokhale RS, Suma S, Balaram H, Balaram P, Murthy MR. Triosephosphate isomerase from Plasmodium falciparum: the crystal structure provides insights into antimalarial drug design. Structure 1997, 5(6):751-61. [http://view.ncbi.nlm.nih.gov/pubmed/9261072], 10.1016/S0969-2126(97)00230-X, 9261072.
40. Hübscher G, Mayer RJ, Hansen HJ. Glycolytic enzymes as a multi-enzyme system. J Bioenerg 1971, 2(2):115-8. [http://view.ncbi.nlm.nih.gov/pubmed/4257578], 10.1007/BF01648926, 4257578.
41. Srinivasan P, Beatty WL, Diouf A, Herrera R, Ambroggio X, Moch JK, Tyler JS, Narum DL, Pierce SK, Boothroyd JC, Haynes JD, Miller LH. Binding of Plasmodium merozoite proteins RON2 and AMA1 triggers commitment to invasion. Proc Natl Acad Sci U S A 2011, 108(32):13275-80. [http://view.ncbi.nlm.nih.gov/pubmed/21788485], 10.1073/pnas.1110303108, 3156155, 21788485.
42. van S, Priebe W, Saliba KJ. The inhibitory effect of 2-halo derivatives of D-glucose on glycolysis and on the proliferation of the human malaria parasite Plasmodium falciparum. J Pharmacol Exp Ther 2008, 327(2):511-7. [http://view.ncbi.nlm.nih.gov/pubmed/18713952], 10.1124/jpet.108.141929, 18713952.
43. Santos de Macedo C, Gerold P, Jung N, Azzouz N, Kimmel J, Schwarz RT. Inhibition of glycosyl-phosphatidylinositol biosynthesis in Plasmodium falciparum by C-2 substituted mannose analogues. Eur J Biochem 2001, 268(23):6221-8. [http://view.ncbi.nlm.nih.gov/pubmed/11733018], 10.1046/j.0014-2956.2001.02571.x, 11733018.
44. van B, Olszewski KL, Wilinski D, Llinás M, Louw AI, Birkholtz LM. Co-inhibition of Plasmodium falciparum S-adenosylmethionine decarboxylase/ornithine decarboxylase reveals perturbation-specific compensatory mechanisms by transcriptome, proteome, and metabolome analyses. J Biol Chem 2009, 284(7):4635-46. [http://view.ncbi.nlm.nih.gov/pubmed/19073607].
45. Zini M, Passariello CL, Gottardi D, Cetrullo S, Flamigni F, Pignatti C, Minarini A, Tumiatti V, Milelli A, Melchiorre C, Stefanelli C. Cytotoxicity of methoctramine and methoctramine-related polyamines. Chem Biol Interact 2009, 181(3):409-16. [http://view.ncbi.nlm.nih.gov/pubmed/19576191], 10.1016/j.cbi.2009.06.015, 19576191.
46. Déchamps S, Wengelnik K, Cerdan R, Vial HJ, Berry-Sterkers L. The Kennedy phospholipid biosynthesis pathways are refractory to genetic disruption in Plasmodium berghei and therefore appear essential in blood stages. Mol Biochem Parasitol 2010, 173(2):69-80. [http://view.ncbi.nlm.nih.gov/pubmed/20478340], 10.1016/j.molbiopara.2010.05.006, 20478340.
47. Saleh A, Friesen J, Baumeister S, Gross U, Bohne W. Growth inhibition of Toxoplasma gondii and Plasmodium falciparum by nanomolar concentrations of 1-hydroxy-2-dodecyl-4(1H)quinolone, a high-affinity inhibitor of alternative (type II) NADH dehydrogenases. Antimicrob Agents Chemother 2007, 51(4):1217-22. [http://view.ncbi.nlm.nih.gov/pubmed/17242151], 10.1128/AAC.00895-06, 1855512, 17242151.
48. Mita T, Tanabe K, Kita K. Spread and evolution of Plasmodium falciparum drug resistance. Parasitol Int 2009, 58(3):201-9. [http://view.ncbi.nlm.nih.gov/pubmed/19393762], 10.1016/j.parint.2009.04.004, 19393762.
49. Tang W. Drug metabolite profiling and elucidation of drug-induced hepatotoxicity. Expert Opin Drug Metab Toxicol 2007, 3(3):407-20. [http://view.ncbi.nlm.nih.gov/pubmed/17539747], 10.1517/17425255.3.3.407, 17539747.
50. Feist AM, Palsson BO. The biomass objective function. Curr Opin Microbiol 2010, 13(3):344-9. [http://view.ncbi.nlm.nih.gov/pubmed/20430689], 10.1016/j.mib.2010.03.003, 2912156, 20430689.
51. Kolev NG, Tschudi C, Ullu E. RNA interference in protozoan parasites: achievements and challenges. Eukaryot Cell 2011, 10(9):1156-63. [http://view.ncbi.nlm.nih.gov/pubmed/21764910], 10.1128/EC.05114-11, 3187059, 21764910.
52. Bello AM, Poduch E, Liu Y, Wei L, Crandall I, Wang X, Dyanand C, Kain KC, Pai EF, Kotra LP. Structure-activity relationships of C6-uridine derivatives targeting plasmodia orotidine monophosphate decarboxylase. J Med Chem 2008, 51(3):439-48. [http://view.ncbi.nlm.nih.gov/pubmed/18189347], 10.1021/jm7010673, 18189347.
53. Bello AM, Poduch E, Fujihashi M, Amani M, Li Y, Crandall I, Hui R, Lee PI, Kain KC, Pai EF, Kotra LP. A potent, covalent inhibitor of orotidine 5'-monophosphate decarboxylase with antimalarial activity. J Med Chem 2007, 50(5):915-21. [http://view.ncbi.nlm.nih.gov/pubmed/17290979], 10.1021/jm060827p, 17290979.
54. Chait R, Craney A, Kishony R. Antibiotic interactions that select against resistance. Nature 2007, 446(7136):668-71. [http://view.ncbi.nlm.nih.gov/pubmed/17410176], 10.1038/nature05685, 17410176.
55. Olszewski KL, Morrisey JM, Wilinski D, Burns JM, Vaidya AB, Rabinowitz JD, Llins M. Host-parasite interactions revealed by Plasmodium falciparum metabolomics. Cell Host Microbe 2009, 5(2):191-9. [http://view.ncbi.nlm.nih.gov/pubmed/19218089], 10.1016/j.chom.2009.01.004, 2737466, 19218089.
56. Azzarello J, Fung KM, Lin HK. Tissue distribution of human AKR1C3 and rat homolog in the adult genitourinary system. J Histochem Cytochem 2008, 56(9):853-61. [http://view.ncbi.nlm.nih.gov/pubmed/18574251], 10.1369/jhc.2008.951384, 2516960, 18574251.
57. Kanehisa M, Goto S. KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res 2000, 28:27-30. [http://view.ncbi.nlm.nih.gov/pubmed/10592173], 10.1093/nar/28.1.27, 102409, 10592173.
58. Scheer M, Grote A, Chang A, Schomburg I, Munaretto C, Rother M, Söhngen C, Stelzer M, Thiele J, Schomburg D. BRENDA, the enzyme information system in 2011. Nucleic Acids Res 2011, 39(Database issue):D670-6. [http://view.ncbi.nlm.nih.gov/pubmed/21062828], 3013686, 21062828.
59. Castro J, Cortés JP, Guzmán M. Properties of the mitochondrial membrane and carnitine palmitoyltransferase in the periportal and the perivenous zone of the liver. Effects of chronic ethanol feeding. Biochem Pharmacol 1991, 41(12):1987-95. [http://view.ncbi.nlm.nih.gov/pubmed/2039548], 10.1016/0006-2952(91)90140-Z, 2039548.
60. Holzhütter HG. The principle of flux minimization and its application to estimate stationary fluxes in metabolic networks. Eur J Biochem 2004, 271(14):2905-22. [http://view.ncbi.nlm.nih.gov/pubmed/15233787], 10.1111/j.1432-1033.2004.04213.x, 15233787.