Plasmodium falciparum parasites are killed by a transition state analogue of purine nucleoside phosphorylase in a primate animal model

PLoS ONE

Volumn 6, Issue 11, 2011, Pages

  Cassera, María B ^a,g   Hazleton, Keith Z ^a   Merino, Emilio F ^a,g   Obaldia, Nicanor ^b   Ho, Meng Chiao ^a   Murkin, Andrew S ^a,f   DePinto, Richard ^c   Gutierrez, Jemy A ^a   Almo, Steven C ^a   Evans, Gary B ^d   Babu, Yarlagadda S ^e   Schramm, Vern L ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b Malaria Drug and Vaccine Evaluation Center   (Panama)

^c WATERS CORPORATION   (United States)

^d CALLAGHAN INNOVATION   (New Zealand)

^e BIOCRYST PHARMACEUTICALS INC   (United States)

^f UNIVERSITY AT BUFFALO   (United States)

^g VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BCX 4945; POLYAMINE; PURINE; PURINE NUCLEOSIDE PHOSPHORYLASE; PURINE NUCLEOSIDE PHOSPHORYLASE INHIBITOR; UNCLASSIFIED DRUG; 4' DEAZA 1' AZA 2' DEOXY 1' (9 METHYLENE)IMMUCILLIN G; 4'-DEAZA-1'-AZA-2'-DEOXY-1'-(9-METHYLENE)IMMUCILLIN G; ADENOSINE; ANTIMALARIAL AGENT; DRUG DERIVATIVE; PURINE DERIVATIVE; PYRROLIDINE DERIVATIVE;

ANIMAL EXPERIMENT; ANIMAL MODEL; AOTUS; AOTUS LEMURINUS; ARTICLE; BINDING AFFINITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; CRYSTAL STRUCTURE; DRUG BIOAVAILABILITY; DRUG BLOOD LEVEL; DRUG EFFECT; DRUG EFFICACY; DRUG MECHANISM; DRUG POTENCY; DRUG STRUCTURE; DRUG TARGETING; HUMAN; HUMAN CELL; MALARIA FALCIPARUM; METABOLITE; MOLECULAR STABILITY; NONHUMAN; PARASITE CLEARANCE; PLASMODIUM FALCIPARUM; POLYAMINE SYNTHESIS; TREATMENT DURATION; ANIMAL; BIOLOGICAL MODEL; CHEMISTRY; ERYTHROCYTE; METABOLISM; PARASITOLOGY; PATHOGENICITY; PRIMATE;

ANIMALIA; AOTUS (PRIMATE); PLASMODIUM FALCIPARUM; PRIMATES;

ADENOSINE; ANIMALS; ANTIMALARIALS; ERYTHROCYTES; HUMANS; MALARIA, FALCIPARUM; MODELS, BIOLOGICAL; PLASMODIUM FALCIPARUM; POLYAMINES; PRIMATES; PURINE-NUCLEOSIDE PHOSPHORYLASE; PURINES; PYRROLIDINES;

EID: 80855133585     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0026916     Document Type: Article

References (49)

1. Hyde JE, (2007) Targeting purine and pyrimidine metabolism in human apicomplexan parasites. Curr Drug Targets 8: 31-47.
2. Ting LM, Shi W, Lewandowicz A, Singh V, Mwakingwe A, et al. (2005) Targeting a novel Plasmodium falciparum purine recycling pathway with specific immucillins. J Biol Chem 280: 9547-9554.
3. Downie MJ, Saliba KJ, Howitt SM, Broer S, Kirk K, (2006) Transport of nucleosides across the Plasmodium falciparum parasite plasma membrane has characteristics of PfENT1. Mol Microbiol 60: 738-748.
4. El Bissati K, Zufferey R, Witola WH, Carter NS, Ullman B, et al. (2006) The plasma membrane permease PfNT1 is essential for purine salvage in the human malaria parasite Plasmodium falciparum. Proc Natl Acad Sci U S A 103: 9286-9291.
5. Haider N, Eschbach ML, Dias Sde S, Gilberger TW, Walter RD, et al. (2005) The spermidine synthase of the malaria parasite Plasmodium falciparum: molecular and biochemical characterisation of the polyamine synthesis enzyme. Mol Biochem Parasitol 142: 224-236.
6. Pascale RM, Simile MM, De Miglio MR, Feo F, (2002) Chemoprevention of hepatocarcinogenesis: S-adenosyl-L-methionine. Alcohol 27: 193-198.
7. Pegg AE, (1988) Polyamine metabolism and its importance in neoplastic growth and a target for chemotherapy. Cancer Res 48: 759-774.
8. Teng R, Junankar PR, Bubb WA, Rae C, Mercier P, et al. (2008) Metabolite profiling of the intraerythrocytic malaria parasite Plasmodium falciparum by (1)H NMR spectroscopy. NMR in Biomedicine 22: 292-302.
9. Clark K, Niemand J, Reeksting S, Smit S, van Brummelen AC, et al. (2010) Functional consequences of perturbing polyamine metabolism in the malaria parasite, Plasmodium falciparum. Amino Acids 38: 633-644.
10. Cassera MB, Hazleton KZ, Riegelhaupt PM, Merino EF, Luo M, et al. (2008) Erythrocytic adenosine monophosphate as an alternative purine source in Plasmodium falciparum. J Biol Chem 283: 32889-32899.
11. Kicska GA, Tyler PC, Evans GB, Furneaux RH, Schramm VL, et al. (2002) Purine-less death in Plasmodium falciparum induced by immucillin-H, a transition state analogue of purine nucleoside phosphorylase. J Biol Chem 277: 3226-3231.
12. Madrid DC, Ting LM, Waller KL, Schramm VL, Kim K, (2008) Plasmodium falciparum purine nucleoside phosphorylase is critical for viability of malaria parasites. J Biol Chem 283: 35899-35907.
13. Ting LM, Gissot M, Coppi A, Sinnis P, Kim K, (2008) Attenuated Plasmodium yoelii lacking purine nucleoside phosphorylase confer protective immunity. Nature Medicine 14: 954-958.
14. Bungener W, Nielsen G, (1968) Nucleic acid metabolism in experimental malaria. 2. Incorporation of adenosine and hypoxanthine into the nucleic acids of malaria parasites Plasmodium berghei and Plasmodium vinckei. Zeitschrift fur Tropenmedizin und Parasitologie 19: 185-197.
15. Bzowska A, Kulikowska E, Shugar D, (2000) Purine nucleoside phosphorylases: properties, functions, and clinical aspects. Pharmacol Ther 88: 349-425.
16. Taylor Ringia EA, Schramm VL, (2005) Transition states and inhibitors of the purine nucleoside phosphorylase family. Curr Top Med Chem 5: 1237-1258.
17. Bantia S, Parker C, Upshaw R, Cunningham A, Kotian P, et al. (2010) Potent orally bioavailable purine nucleoside phosphorylase inhibitor BCX-4208 induces apoptosis in B- and T-lymphocytes-a novel treatment approach for autoimmune diseases, organ transplantation and hematologic malignancies. Int Immunopharmacol 10: 784-790.
18. Lewandowicz A, Schramm VL, (2004) Transition state analysis for human and Plasmodium falciparum purine nucleoside phosphorylases. Biochemistry 43: 1458-1468.
19. Traut TW, (1994) Physiological concentrations of purines and pyrimidines. Molecular and Cellular Biochemistry 140: 1-22.
20. Quashie NB, de Koning HP, Ranford-Cartwright LC, (2006) An improved and highly sensitive microfluorimetric method for assessing susceptibility of Plasmodium falciparum to antimalarial drugs in vitro. Malar J 5: 95.
21. Griffith DA, Jarvis SM, (1996) Nucleoside and nucleobase transport systems of mammalian cells. Biochim Biophys Acta 1286: 153-181.
22. Bitonti AJ, Dumont JA, Bush TL, Edwards ML, Stemerick DM, et al. (1989) Bis(benzyl)polyamine analogs inhibit the growth of chloroquine-resistant human malaria parasites (Plasmodium falciparum) in vitro and in combination with alpha-difluoromethylornithine cure murine malaria. Proc Natl Acad Sci U S A 86: 651-655.
23. Taylor DW, Siddiqui WA, (1979) Susceptibility of owl monkeys to Plasmodium falciparum infection in relation to location of origin, phenotype, and karyotype. J Parasitol 65: 267-271.
24. Lewandowicz A, Tyler PC, Evans GB, Furneaux RH, Schramm VL, (2003) Achieving the ultimate physiological goal in transition state analogue inhibitors for purine nucleoside phosphorylase. J Biol Chem 278: 31465-31468.
25. Huser HJ, (1970) Atlas of Comparative Primate Hematology New York Academic Press.
26. Farthing D, Sica D, Gehr T, Wilson B, Fakhry I, et al. (2007) An HPLC method for determination of inosine and hypoxanthine in human plasma from healthy volunteers and patients presenting with potential acute cardiac ischemia. J Chromatogr B Analyt Technol Biomed Life Sci 854: 158-164.
27. Schreiber G, Tiemeyer W, Flurer C, Zucker H, (1986) Purine metabolites in serum of higher primates, including man. International Journal of Primatology 7: 521-531.
28. Mao C, Cook WJ, Zhou M, Koszalka GW, Krenitsky TA, et al. (1997) The crystal structure of Escherichia coli purine nucleoside phosphorylase: a comparison with the human enzyme reveals a conserved topology. Structure 5: 1373-1383.
29. Shi W, Ting LM, Kicska GA, Lewandowicz A, Tyler PC, et al. (2004) Plasmodium falciparum purine nucleoside phosphorylase: crystal structures, immucillin inhibitors, and dual catalytic function. J Biol Chem 279: 18103-18106.
30. Ho MC, Shi W, Rinaldo-Matthis A, Tyler PC, Evans GB, et al. (2010) Four generations of transition-state analogues for human purine nucleoside phosphorylase. Proc Natl Acad Sci U S A 107: 4805-4812.
31. Deng H, Lewandowicz A, Schramm VL, Callender R, (2004) Activating the phosphate nucleophile at the catalytic site of purine nucleoside phosphorylase: a vibrational spectroscopic study. J Am Chem Soc 126: 9516-9517.
32. Balakrishnan K, Verma D, O'Brien S, Kilpatrick JM, Chen Y, et al. (2010) Phase 2 and pharmacodynamic study of oral forodesine in patients with advanced, fludarabine-treated chronic lymphocytic leukemia. Blood 116: 886-892.
33. ClinicalTrial.gov, Identifier: NCT00985127 (2010) Study to evaluate the urate-lowering activity and safety of oral BCX4208 administered in subjects with gout.
34. Pukrittayakamee S, Looareesuwan S, Keeratithakul D, Davis TM, Teja-Isavadharm P, et al. (1997) A study of the factors affecting the metabolic clearance of quinine in malaria. European Journal of Clinical Pharmacology 52: 487-493.
35. Eastman RT, Fidock DA, (2009) Artemisinin-based combination therapies: a vital tool in efforts to eliminate malaria. Nat Rev Microbiol 7: 864-874.
36. Golenser J, Waknine JH, Krugliak M, Hunt NH, Grau GE, (2006) Current perspectives on the mechanism of action of artemisinins. Int J Parasitol 36: 1427-1441.
37. Titulaer HAC, Zuidema J, Lugt CB, (1991) Formulation and pharmacokinetics of artemisinin and its derivatives. International Journal of Pharmaceutics 69: 83-92.
38. Basu I, Cordovano G, Das I, Belbin TJ, Guha C, et al. (2007) A transition state analogue of 5′-methylthioadenosine phosphorylase induces apoptosis in head and neck cancers. J Biol Chem 282: 21477-21486.
39. Obaldia N 3rd, (1991) Detection of Klebsiella pneumoniae antibodies in Aotus l. lemurinus (Panamanian owl monkey) using an enzyme linked immunosorbent assay (ELISA) test. Laboratory Animals 25: 133-141.
40. Zhang Y, Huo M, Zhou J, Xie S, (2010) PKSolver: An add-in program for pharmacokinetic and pharmacodynamic data analysis in Microsoft Excel. Computer Methods and Programs in Biomedicine 99: 306-314.
41. Earle WC, Perez M, (1932) Enumeration of parasites in the blood of malarial patients. Journal of Laboratory and Clinical Medicine 17: 1124-1130.
42. Lambert JD, Temmink JH, Marquis J, Parkhurst RM, Lugt CB, et al. (1991) Endod: safety evaluation of a plant molluscicide. Regulatory Toxicology and Pharmacology 14: 189-201.
43. Edwards AA, Mason JM, Clinch K, Tyler PC, Evans GB, et al. (2009) Altered enthalpy-entropy compensation in picomolar transition state analogues of human purine nucleoside phosphorylase. Biochemistry 48: 5226-5238.
44. (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallographica Section D: Biological Crystallography 50: 760-763.
45. Emsley P, Cowtan K, (2004) Coot: model-building tools for molecular graphics. Acta Crystallographica Section D: Biological Crystallography 60: 2126-2132.
46. Potterton E, Briggs P, Turkenburg M, Dodson E, (2003) A graphical user interface to the CCP4 program suite. Acta Crystallographica Section D: Biological Crystallography 59: 1131-1137.
47. Sajiki H, Esaki H, Aoki F, Maegawa T, Hirota K, (2005) Palladium-Catalyzed Base-Selective H-D Exchange Reaction of Nucleosides in Deuterium Oxide. Synlett 9: 1385-1388.
48. Evans GB, Furneaux RH, Tyler PC, Schramm VL, (2003) Synthesis of a transition state analogue inhibitor of purine nucleoside phosphorylase via the Mannich reaction. Org Lett 5: 3639-3640.
49. Evans GB, Furneaux RH, Lewandowicz A, Schramm VL, Tyler PC, (2003) Synthesis of second-generation transition state analogues of human purine nucleoside phosphorylase. J Med Chem 46: 5271-5276.