Discovery of a Plasmodium falciparum Glucose-6-phosphate Dehydrogenase 6-phosphogluconolactonase Inhibitor (R,Z)-N-((1-Ethylpyrrolidin-2-yl)methyl)-2- (2-fluorobenzylidene)-3-oxo-3,4-dihydro-2H-benzo[b][1,4]thiazine-6-carboxamide (ML276) that reduces parasite growth in vitro

Journal of Medicinal Chemistry

Volumn 55, Issue 16, 2012, Pages 7262-7272

  Preuss, Janina ^a,b,c   Malone, Patrick ^c   Peddibhotla, Satyamaheshwar ^c   Hedrick, Michael P ^c   Hershberger, Paul ^c   Gosalia, Palak ^c   Milewski, Monika ^c   Li, Yujie Linda ^c   Sugarman, Eliot ^c   Hood, Becky ^c   Suyama, Eigo ^c   Nguyen, Kevin ^c   Vasile, Stefan ^c   Sergienko, Eduard ^c   Mangravita Novo, Arianna ^c   Vicchiarelli, Michael ^c   McAnally, Danielle ^c   Smith, Layton H ^c   Roth, Gregory P ^c   Diwan, Jena ^c   Chung, Thomas D Y ^c   Jortzik, Esther ^b   Rahlfs, Stefan ^b   Becker, Katja ^b   Pinkerton, Anthony B ^c   Bode, Lars ^a   more..

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b JUSTUS LIEBIG UNIVERSITY   (Germany)

^c BURNHAM INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIPROTOZOAL AGENT; GLUCOSE 6 PHOSPHATE DEHYDROGENASE; GLUCOSE 6 PHOSPHATE DEHYDROGENASE 6 PHOSPHOGLUCONOLACTONASE; MICROBIAL ENZYME; ML 276; N [(1 ETHYLPYRROLIDIN 2 YL)METHYL] 2 (2 FLUOROBENZYLIDENE) 3 OXO 3,4 DIHYDRO 2H BENZO[B][1,4]THIAZINE 6 CARBOXAMIDE; UNCLASSIFIED DRUG;

ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; DRUG POTENCY; DRUG SOLUBILITY; DRUG STABILITY; DRUG STRUCTURE; ENZYME ACTIVITY; ENZYME INHIBITION; GROWTH INHIBITION; HIGH THROUGHPUT SCREENING; IN VITRO STUDY; NONHUMAN; PENTOSE PHOSPHATE CYCLE; PLASMODIUM FALCIPARUM;

ANTIMALARIALS; CARBOXYLIC ESTER HYDROLASES; DRUG STABILITY; GLUCOSEPHOSPHATE DEHYDROGENASE; HIGH-THROUGHPUT SCREENING ASSAYS; MULTIENZYME COMPLEXES; PARASITIC SENSITIVITY TESTS; PLASMODIUM FALCIPARUM; SMALL MOLECULE LIBRARIES; STEREOISOMERISM; STRUCTURE-ACTIVITY RELATIONSHIP; THIAZINES;

EID: 84866916330     PISSN: 00222623     EISSN: 15204804     Source Type: Journal    
DOI: 10.1021/jm300833h     Document Type: Article

References (42)

1. Murray, C. J. L.; Rosenfeld, L. C.; Lim, S. S.; Andrews, K. G.; Foreman, K. J.; Haring, D.; Fullman, N; Naghavi, M.; Lozano, R; Lopez, A. D. Global malaria mortality between 1980 and 2010: a systematic analysis. Lancet 2012, 379, 413-431.
2. World Malaria Report 2008; World Health Organization: Geneva, 2008; http://whqlibdoc.who.int/publications/2008/9789241563697-eng.pdf.
3. Baron, J. M.; Higgins, J. M.; Dzik, W. H. A revised timeline for the origin of Plasmodium falciparum as a human pathogen. J. Mol. Evol. 2011, 73, 297-304.
4. Tanabe, K.; Mita, T.; Jombart, T.; Eriksson, A.; Horibe, S.; Palacpac, N; Ranford-Cartwright, L.; Sawai, H; Sakihama, N; Ohmae, H; Nakamura, M.; Ferreira, M. U.; Escalante, A A; Prugnolle, F.; Bjorkman, A.; Farnert, A; Kaneko, A.; Horii, T.; Manica, A; Kishino, H; Balloux, F. Plasmodium falciparum accompanied the human expansion out of Africa. Curr. Biol. 2010, 20, 1283-1289.
5. Rodrigues, T.; Moreira, R; Lopes, F. New hope in the fight against malaria? Future Med. Chem. 2011, 3, 1-3.
6. Hill, A. V. Vaccines against malaria. Philos. Trans. R Soc, B 2011, 366, 2806-2814.
7. Murambiwa, P.; Masola, B.; Govender, T.; Mukaratirwa, S.; Musabayane, C. T. Anti-malarial drug formulations and novel delivery systems: a review. Acta Trop. 2011, 118, 71-79.
8. Bousejra-El Garah, F.; Wong, M. H; Amewu, R K.; Muangnoicharoen, S.; Maggs, J. L.; Stigliani, J. L.; Park, B. K.; Chadwick, J.; Ward, S. A; O'Neill, P. M. Comparison of the reactivity of antimalarial 1, 2, 4, 5-tetraoxanes with 1, 2, 4-trioxolanes in the presence of ferrous iron salts, heme, and ferrous iron salts/phosphatidylcholine. J. Med. Chem. 2011, 54, 6443-6455.
9. Schlitzer, M. Antimalarial drugs-What is in use and what is in the pipeline. Arch. Pharm. 2008, 341, 149-163.
10. Murambiwa, P.; Masola, B.; Govender, T.; Mukaratirwa, S.; Musabayane, C. T. Anti-malarial drug formulations and novel delivery systems: A review. Acta Trop. 2011, 118, 71-79.
11. Trape, J. F. The public health impact of chloroquine resistance in Africa. Am. J. Trop. Med. Hyg. 2001, 64, 12-17.
12. Marks, F.; von Kalckreuth, V.; Kobbe, R; Adjei, S.; Adjei, O.; Horstmann, R D.; Meyer, C. G; May, J. Parasitological rebound effect and emergence of pyrimethamine resistance in Plasmodium falciparum after single-dose sulfadoxine-pyrimethamine. J. Infect. Dis. 2005, 192, 1962-1965.
13. Egan, T. J.; Kaschula, C. H. Strategies to reverse drug resistance in malaria. Curr. Opin. Infect. Dis. 2007, 20, 598-604.
14. Gottschall, J. L.; Elliot, W.; Lianos, E.; McFarland, J. G; Wolfmeyer, K.; Aster, R H. Quinine-induced immune thrombocyto penia associated with hemolytic uremic syndrome: a new clinical entity. Blood 1991, 77, 306-310.
15. Veinot, J. P.; Mai, K. T.; Zarychanski, R Chloroquine related cardiac toxicity. J. Rheumatol. 1998, 25, 1221 - 1225.
16. Guidelines for the Treatment of Malaria; World Health Organization: Geneva, 2010; http://whqlibdoc.who.int/publications/2010/9789241547925-eng.pdf.
17. Dondorp, A. M.; Nosten, F.; Yi, P.; Das, D.; Phyo, A P.; Tarning, J.; Lwin, K. M.; Ariey, F.; Hanpithakpong, W.; Lee, S. J.; Ringwald, P.; Silamut, K.; Imwong, M.; Chotivanich, K.; Lim, P.; Herdman, T.; An, S. S.; Yeung, S.; Singhasivanon, P.; Day, N. P.; Lindegardh, N.; Socheat, D.; White, N. J. Artemisinin resistance in Plasmodium falciparum malaria. N. Engl. J. Med. 2009, 361, 455-467.
18. Noedl, H.; Se, Y.; Sriwichai, S.; Schaecher, K.; Teja-Isavadharm, P.; Smith, B.; Rutvisuttinunt, W.; Bethell, D.; Surasri, S.; Fukuda, M. M.; Socheat, D.; Chan Thap, L. Artemisinin resistance in Cambodia: a clinical trial designed to address an emerging problem in Southeast Asia. Clin. Infect. Dis. 2010, 51, e82-e89.
19. Carrara, V. I.; Zwang, J.; Ashley, E. A.; Price, R. N.; Stepniewska, K.; Barends, M.; Brockman, A.; Anderson, T.; McGready, R.; Phaiphun, L.; Proux, S.; van Vugt, M.; Hutagalung, R.; Lwin, K. M.; Phyo, A. P.; Preechapornkul, P.; Imwong, M.; Pukrittayakamee, S.; Singhasivanon, P.; White, N. J.; Nosten, F. Changes in the treatment responses to artesunate-mefloquine on the northwestern border of Thailand during 13 years of continuous deployment. PLoS One 2009, 4, e4551.
20. Jortzik, E.; Mailu, B. M.; Preuss, J.; Fischer, M.; Bode, L.; Rahlfs, S.; Becker, K. Glucose-6-phosphate dehydrogenase-6-phosphogluco-nolactonase: a unique bifunctional enzyme from Plasmodium falciparum. Biochem. J. 2011, 436, 641-650.
21. Nkhoma, E. T.; Poole, C.; Vannappagari, V.; Hall, S. A.; Beutler, E. The global prevalence of glucose-6-phosphate dehydrogenase deficiency: a systematic review and meta-analysis. Blood Cells Mol. Dis. 2009, 42, 267-278.
22. Luzzatto, L. Glucose 6-phosphate dehydrogenase deficiency: from genotype to phenotype. Haematologica 2006, 91, 1303-1306.
23. Cappadoro, M.; Giribaldi, G.; O'Brien, E.; Turrini, F.; Mannu, F.; Ulliers, D.; Simula, G.; Luzzatto, L.; Arese, P. Early phagocytosis of glucose-6-phosphate dehydrogenase (G6PD)-deficient erythrocytes parasitized by Plasmodium falciparum may explain malaria protection in G6PD deficiency. Blood 1998, 92, 2527-2534.
24. Ruwende, C.; Khoo, S. C.; Snow, R. W.; Yates, S. N.; Kwiatkowski, D.; Gupta, S.; Warn, P.; Allsopp, C. E.; Gilbert, S. C.; Peschu, N.; et al. Natural selection of hemi- and heterozygotes for G6PD deficiency in Africa by resistance to severe malaria. Nature 1995, 376, 246-249.
25. Atamna, H.; Pascarmona, G.; Ginsburg, H. Hexose-mono-phosphate shunt activity in intact Plasmodium falciparum-infected erythrocytes and in free parasites. Mol. Biochem. Parasitol. 1994, 67, 79-89.
26. Preuss, J.; Jortzik, E.; Becker, K. Glucose-6-phosphate metabolism in Plasmodium falciparum. IUBMB Life 2012, 64, 603-611.
27. Becker, K.; Koncarevic, S.; Hunt, N. H.: Oxidative stress and antioxidant defense in malarial parasites. In Molecular Approaches to Malaria; Sherman, I. W., Ed.; American Society of Microbiology Press.: Washington DC, 2005; pp 365-383.
28. Crooke, A.; Diez, A.; Mason, P. J.; Bautista, J. M. Transient silencing of Plasmodium falciparum bifunctional glucose-6-phosphate dehydrogenase- 6-phosphogluconolactonase. FEBS J. 2006, 273, 1537-1546.
29. Baum, J.; Papenfuss, A. T.; Mair, G. R.; Janse, C. J.; Vlachou, D.; Waters, A. P.; Cowman, A. F.; Crabb, B. S.; de Koning-Ward, T. F. Molecular genetics and comparative genomics reveal RNAi is not functional in malaria parasites. Nucleic Acids Res. 2009, 37, 3788-3798.
30. Lopez-Barragan, M. J.; Lemieux, J.; Quinones, M.; Williamson, K. C.; Molina-Cruz, A.; Cui, K.; Barillas-Mury, C.; Zhao, K.; Su, X. Z. Directional gene expression and antisense transcripts in sexual and asexual stages of Plasmodium falciparum. BMC Genomics 2011, 12, 587.
31. Clarke, J. L.; Scopes, D. A.; Sodeinde, O.; Mason, P. J. Glucose-6-phosphate dehydrogenase-6-phosphogluconolactonase. A novel bifunctional enzyme in malaria parasites. Eur. J. Biochem. 2001, 268, 2013-2019.
32. Clarke, J. L.; Sodeinde, O.; Mason, P. J. A unique insertion in Plasmodium berghei glucose-6-phosphate dehydrogenase-6-phospho-gluconolactonase: evolutionary and functional studies. Mol. Biochem. Parasitol. 2003, 127, 1-8.
33. ML276 has been declared a probe via the Molecular Libraries Probe Production Centers Network (MLPCN) and is available through the network, see: http://mli.nih.gov/mli/.
34. Preuss, J.; Hedrick, M.; Sergienko, E.; Pinkerton, A.; Mangravita-Novo, A.; Smith, L.; Marx, C.; Fischer, E.; Jortzik, E.; Rahlfs, S.; Becker, K.; Bode, L. High-throughput screening for small- molecule inhibitors of Plasmodium falciparum glucose-6-phosphate dehydrogenase 6-phosphogluconolactonase. J. Biomol. Screening 2012, 17, 738-751.
35. Trifilenkov, A. S.; Kobak, V. V.; Salina, M. A.; Kusovkova, J. A.; Ilyin, A. P.; Khvat, A. V.; Tkachenko, S. E.; Ivachtchenko, A. V. Liquid phase parallel synthesis of combinatorial libraries of substituted 6-carbamoyl-3, 4-dihydro-2H-benzo[1, 4]thiazines. J. Comb. Chem. 2006, 8, 469-479.
36. Worley, J. W.; Ratts, K. W.; Cammack, K. L. 2- Dialkylphosphonyl- and 2-Alkylidene-3, 4-dihydro-3-oxo-2H-1, 4-ben-zothiazines. J. Org. Chem. 1975, 40, 1731-1734.
37. Ploemen, J. H.; Van Schanke, A.; Van Ommen, B.; Van Bladeren, P. J. Reversible conjugation of ethacrynic acid with glutathione and human glutathione S-transferase P1-1. Cancer Res. 1994, 54, 915-919.
38. Koncarevic, S.; Rohrbach, P.; Deponte, M.; Krohne, G.; Prieto, J. H.; Yates, J., III; Rahlfs, S.; Becker, K. The malarial parasite Plasmodium falciparum imports the human protein peroxiredoxin 2 for peroxide detoxification. Proc. Natl. Acad. Sci. U.S.A. 2009, 106, 13323-13328.
39. Desjardins, R. E.; Canfield, C. J.; Haynes, J. D.; Chulay, J. D. Quantitative assessment of antimalarial activity in vitro by a semiautomated microdilution technique. Antimicrob. Agents Chemother. 1979, 16, 710-718.
40. Fivelman, Q. L.; Adagu, I. S.; Warhurst, D. C. Modified fixed-ratio isobologram method for studying in vitro interactions between atovaquone and proguanil or dihydroartemisinin against drug-resistant strains of Plasmodium falciparum. Antimicrob. Agents Chemother. 2004, 48, 4097-4102.
41. Cornish-Bowden, A.: Introduction to enzyme kinetics. In Fundamentals of Enzyme Kinetics, 3rd ed.; Cornish-Bowden, A., Ed.; Portland Press: London, 2004.
42. Cornish-Bowden, A.: Reversible inhibition and activation. In Fundamentals of Enzyme Kinetics, 3rd ed.; Cornish-Bowden, A., Ed.; Portland Press: London, 2004.