Formation of catalytically active cross-species heterodimers of thymidylate synthase from Plasmodium falciparum and Plasmodium vivax

Molecular Biology Reports

Volumn 38, Issue 2, 2011, Pages 1029-1037

  Chanama, Manee ^c   Chanama, Suchart ^a   Shaw, Philip J ^b   Chitnumsub, Penchit ^b   Leartsakulpanich, Ubolsree ^b   Yuthavong, Yongyuth ^b  

^a CHULALONGKORN UNIVERSITY   (Thailand)

^b NATIONAL SCIENCE AND TECHNOLOGY DEVELOPMENT AGENCY   (Thailand)

^c NONE

Author keywords

Dihydrofolate reductase; Malaria; Plasmodium falciparum; Plasmodium vivax; Subunit complementation; Thymidylate synthase

Indexed keywords

HETERODIMER; THYMIDYLATE SYNTHASE;

ARTICLE; CATALYSIS; CONTROLLED STUDY; ENZYME KINETICS; ENZYME PURIFICATION; ESCHERICHIA COLI; MUTANT; NONHUMAN; PLASMID; PLASMODIUM FALCIPARUM; PLASMODIUM VIVAX; PROTEIN EXPRESSION;

ARGININE; CATALYSIS; CATALYTIC DOMAIN; CYSTEINE; DIMERIZATION; GENETIC COMPLEMENTATION TEST; HUMANS; KINETICS; MALARIA; MUTATION; PLASMIDS; PLASMODIUM FALCIPARUM; PLASMODIUM VIVAX; SPECIES SPECIFICITY; THYMIDYLATE SYNTHASE;

ESCHERICHIA COLI; PLASMODIUM FALCIPARUM; PLASMODIUM VIVAX;

EID: 79951578070     PISSN: 03014851     EISSN: 15734978     Source Type: Journal    
DOI: 10.1007/s11033-010-0199-7     Document Type: Article

References (42)

1. K Mendis BJ Sina P Marchesini R Carter 2001 The neglected burden of Plasmodium vivax malaria Am J Trop Med Hyg 64 97 106 1:STN:280: DC%2BD3MzmsVOjuw%3D%3D 11425182 (Pubitemid 32552576)
2. B Sina 2002 Focus on Plasmodium vivax Trends Parasitol 18 287 289 10.1016/S1471-4922(02)02329-2 12379943 (Pubitemid 35257847)
3. RN Price E Tjitra CA Guerra S Yeung NJ White NM Anstey 2007 Vivax malaria: neglected and not benign Am J Trop Med Hyg 77 79 87 18165478
4. Y Yuthavong 2002 Basis for antifolate action and resistance in malaria Microbes Infect 4 175 182 1:CAS:528:DC%2BD38XhslWgur0%3D 10.1016/S1286-4579(01) 01525-8 11880049 (Pubitemid 34183491)
5. GH Hitching 1960 Pyrimethamine-use of an antimetabolite in the chemotherapy of malaria and other infections Clin Pharmacol Ther 1 570 589
6. PL Olliaro Y Yuthavong 1999 An overview of chemotherapeutic targets for antimalarial drug discovery Pharmacol Ther 81 91 110 1:CAS:528: DyaK1MXovVOnug%3D%3D 10.1016/S0163-7258(98)00036-9 10190581 (Pubitemid 29073558)
7. I Macreadie H Ginsburg W Sirawaraporn L Tilley 2000 Antimalarial drug development and new targets Parasitol Today 16 438 444 1:CAS:528: DC%2BD3cXmslKltLw%3D 10.1016/S0169-4758(00)01758-0 11006476
8. CW Carreras DV Santi 1995 The catalytic mechanism and structure of thymidylate synthase Annu Rev Biochem 64 721 762 1:CAS:528:DyaK2MXmsl2qtrg%3D 10.1146/annurev.bi.64.070195.003445 7574499
9. E Tjitra J Baker S Suprianto Q Cheng NM Anstey 2002 Therapeutic efficacies of artesunate-sulfadoxine-pyrimethamine and chloroquine-sulfadoxine- pyrimethamine in vivax malaria pilot studies: relationship to Plasmodium vivax dhfr mutations Antimicrob Agents Chemother 46 3947 3953 1:CAS:528: DC%2BD38XptVyntbg%3D 10.1128/AAC.46.12.3947-3953.2002 12435700 (Pubitemid 35403273)
10. PJ Houghton GS Germain BJ Hazelton JW Pennington JA Houghton 1989 Mutants of human colon adenocarcinoma, selected for thymidylate synthase deficiency Proc Natl Acad Sci USA 86 1377 1381 1:STN:280:DyaL1M7ksFantw%3D%3D 10.1073/pnas.86.4.1377 2537495 (Pubitemid 19061549)
11. HA Ingraham L Dickey M Goulian 1986 DNA fragmentation and cytotoxicity from increased cellular deoxyuridylate Biochemistry 25 3225 3230 1:CAS:528:DyaL28XitFyksro%3D 10.1021/bi00359a022 3524674 (Pubitemid 16056964)
12. A Yoshioka S Tanaka O Hiraoka Y Koyama Y Hirota D Ayusawa T Seno C Garrett Y Wataya 1987 Deoxyribonucleoside triphosphate imbalance. 5-Fluorodeoxyuridine-induced DNA double strand breaks in mouse FM3A cells and the mechanism of cell death J Biol Chem 262 8235 8241 1:CAS:528: DyaL2sXktlaktb4%3D 2954951
13. PK Rathod S Reshmi 1994 Susceptibility of Plasmodium falciparum to a combination of thymidine and ICI D1694, a quinazoline antifolate directed at thymidylate synthase Antimicrob Agents Chemother 38 476 480 1:CAS:528: DyaK2cXitFans7o%3D 8203840 (Pubitemid 24072234)
14. M Hekmat-Nejad PK Rathod 1996 Kinetics of Plasmodium falciparum thymidylate synthase: interactions with high-affinity metabolites of 5-fluoroorotate and D1694 Antimicrob Agents Chemother 40 1628 1632 1:CAS:528:DyaK28XktVaksL4%3D 8807052 (Pubitemid 26227347)
15. L Jiang PC Lee J White PK Rathod 2000 Potent and selective activity of a combination of thymidine and 1843U89, a folate-based thymidylate synthase inhibitor, against Plasmodium falciparum Antimicrob Agents Chemother 44 1047 1050 1:CAS:528:DC%2BD3cXitFOksrw%3D 10.1128/AAC.44.4.1047-1050.2000 10722510 (Pubitemid 30165289)
16. FW Muregi S Kano H Kino A Ishih 2009 Plasmodium berghei: efficacy of 5-fluoroorotate in combination with commonly used antimalarial drugs in a mouse model Exp Parasitol 121 376 380 1:CAS:528:DC%2BD1MXisFKrsbw%3D 10.1016/j.exppara.2009.01.009 19271282
17. J Yuvaniyama P Chitnumsub S Kamchonwongpaisan J Vanichtanankul W Sirawaraporn P Taylor MD Walkinshaw Y Yuthavong 2003 Insights into antifolate resistance from malarial DHFR-TS structures Nat Struct Biol 10 357 365 1:CAS:528:DC%2BD3sXjtFKns74%3D 10.1038/nsb921 12704428 (Pubitemid 36523270)
18. LW Hardy JS Finer-Moore WR Montfort MO Jones DV Santi RM Stroud 1987 Atomic structure of thymidylate synthase: target for rational drug design Science 235 448 455 1:CAS:528:DyaL2sXhsFais70%3D 10.1126/science.3099389 3099389 (Pubitemid 17009578)
19. WR Montfort KM Perry EB Fauman JS Finer-Moore GF Maley L Hardy F Maley RM Stroud 1990 Structure, multiple site binding, and segmental accommodation in thymidylate synthase on binding dUMP and an anti-folate Biochemistry 29 6964 6977 1:CAS:528:DyaK3cXksFCqtbY%3D 10.1021/bi00482a004 2223754 (Pubitemid 20241141)
20. CA Schiffer IJ Clifton VJ Davisson DV Santi RM Stroud 1995 Crystal structure of human thymidylate synthase: a structural mechanism for guiding substrates into the active site Biochemistry 34 16279 16287 1:CAS:528: DyaK2MXpsFyrtbs%3D 10.1021/bi00050a007 8845352 (Pubitemid 26006470)
21. JS Finer-Moore WR Montfort RM Stroud 1990 Pairwise specificity and sequential binding in enzyme catalysis: thymidylate synthase Biochemistry 29 6977 6986 1:CAS:528:DyaK3cXksFCqtr8%3D 10.1021/bi00482a005 2223755 (Pubitemid 20241142)
22. KM Perry EB Fauman JS Finer-Moore WR Montfort GF Maley F Maley RM Stroud 1990 Plastic adaptation toward mutations in proteins: structural comparison of thymidylate synthases Proteins 8 315 333 1:CAS:528:DyaK3MXhsF2ktbs%3D 10.1002/prot.340080406 2128651
23. P Bawankar PJ Shaw R Sardana PH Babar S Patankar 2010 5′ and 3′ end modifications of spliceosomal RNAs in Plasmodium falciparum Mol Biol Rep 37 2125 2133 1:CAS:528:DC%2BC3cXis1Wls7o%3D 10.1007/s11033-009-9682-4 19669595
24. U Leartsakulpanich M Imwong S Pukrittayakamee NJ White G Snounou W Sirawaraporn Y Yuthavong 2002 Molecular characterization of dihydrofolate reductase in relation to antifolate resistance in Plasmodium vivax Mol Biochem Parasitol 119 63 73 1:CAS:528:DC%2BD38XitFyl 10.1016/S0166-6851(01)00402-9 11755187 (Pubitemid 34038026)
25. JH McKie 1994 Homology modelling of the dihydrofolate reductase-thymidylate synthase bifunctional enzyme of Leishmania major, a potential target for rational drug design in leishmaniasis Drug Des Discov 11 269 288 1:CAS:528:DyaK2MXjtFKhsA%3D%3D 7727680 (Pubitemid 24216200)
26. P Reche R Arrebola A Olmo DV Santi D Gonzalez-Pacanowska LM Ruiz-Perez 1994 Cloning and expression of the dihydrofolate reductase-thymidylate synthase gene from Trypanosoma cruzi Mol Biochem Parasitol 65 247 258 1:CAS:528:DyaK2cXlslWlsLo%3D 10.1016/0166-6851(94)90076-0 7969266 (Pubitemid 24229070)
27. M Trujillo RG Donald DS Roos PJ Greene DV Santi 1996 Heterologous expression and characterization of the bifunctional dihydrofolate reductase-thymidylate synthase enzyme of Toxoplasma gondii Biochemistry 35 6366 6374 1:CAS:528:DyaK28Xis1arsrk%3D 10.1021/bi952923q 8639582 (Pubitemid 26164070)
28. RH O'Neil RH Lilien BR Donald RM Stroud AC Anderson 2003 The crystal structure of dihydrofolate reductase-thymidylate synthase from Cryptosporidium hominis reveals a novel architecture for the bifunctional enzyme J Eukaryot Microbiol 50 Suppl 555 556 10.1111/j.1550-7408.2003.tb00627.x 14736160 (Pubitemid 38043014)
29. W Sirawaraporn P Prapunwattana R Sirawaraporn Y Yuthavong DV Santi 1993 The dihydrofolate reductase domain of Plasmodium falciparum thymidylate synthase-dihydrofolate reductase. Gene synthesis, expression, and anti-folate-resistant mutants J Biol Chem 268 21637 21644 1:CAS:528:DyaK2cXjsVeg 8408015 (Pubitemid 23320657)
30. S Shallom K Zhang L Jiang PK Rathod 1999 Essential protein-protein interactions between Plasmodium falciparum thymidylate synthase and dihydrofolate reductase domains J Biol Chem 274 37781 37786 1:CAS:528: DC%2BD3cXkt1GgtQ%3D%3D 10.1074/jbc.274.53.37781 10608839 (Pubitemid 30026840)
31. J Wattanarangsan S Chusacultanachai J Yuvaniyama S Kamchonwongpaisan Y Yuthavong 2003 Effect of N-terminal truncation of Plasmodium falciparum dihydrofolate reductase on dihydrofolate reductase and thymidylate synthase activity Mol Biochem Parasitol 126 97 102 1:CAS:528:DC%2BD3sXmsFSltA%3D%3D 10.1016/S0166-6851(02)00240-2 12554089 (Pubitemid 36120609)
32. M Pookanjanatavip Y Yuthavong PJ Greene DV Santi 1992 Subunit complementation of thymidylate synthase Biochemistry 31 10303 10309 1:CAS:528:DyaK38XmtVOrurY%3D 10.1021/bi00157a018 1420149
33. M Chanama P Chitnumsub Y Yuthavong 2005 Subunit complementation of thymidylate synthase in Plasmodium falciparum bifunctional dihydrofolate reductase-thymidylate synthase Mol Biochem Parasitol 139 83 90 1:CAS:528:DC%2BD2cXhtVyqsL7L 10.1016/j.molbiopara.2004.09.010 15610822 (Pubitemid 40029599)
34. P Chitnumsub J Yuvaniyama J Vanichtanankul S Kamchonwongpaisan MD Walkinshaw Y Yuthavong 2004 Characterization, crystallization and preliminary X-ray analysis of bifunctional dihydrofolate reductase-thymidylate synthase from Plasmodium falciparum Acta Crystallogr D 60 780 783 10.1107/S0907444904001544 15039585 (Pubitemid 41184847)
35. MM Bradford 1976 A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Anal Biochem 72 248 254 1:CAS:528:DyaE28XksVehtrY%3D 10.1016/0003-2697(76)90527- 3 942051
36. TD Meek EP Garvey DV Santi 1985 Purification and characterization of the bifunctional thymidylate synthetase-dihydrofolate reductase from methotrexate-resistant Leishmania tropica Biochemistry 24 678 686 1:CAS:528:DyaL2MXptFyjtA%3D%3D 10.1021/bi00324a021 3922404 (Pubitemid 15142252)
37. Segel IH (1975) Enzyme kinetics: behavior and analysis of rapid equilibrium and steady-state enzyme systems. Wiley-Interscience, New York
38. DV Santi CS McHenry 1972 5-Fluoro-2′-deoxyuridylate: covalent complex with thymidylate synthetase Proc Natl Acad Sci USA 69 1855 1857 1:CAS:528:DyaE38XkvVCqtr0%3D 10.1073/pnas.69.7.1855 4505665
39. DA Matthews K Appelt SJ Oatley 1989 Stacked beta-bulges in thymidylate synthase account for a novel right-handed rotation between opposing beta-sheets J Mol Biol 205 449 454 1:CAS:528:DyaL1MXhs12hs7Y%3D 10.1016/0022-2836(89)90354-9 2648002 (Pubitemid 19060196)
40. T Dasgupta KS Anderson 2008 Probing the role of parasite-specific, distant structural regions on communication and catalysis in the bifunctional thymidylate synthase-dihydrofolate reductase from Plasmodium falciparum Biochemistry 47 1336 1345 1:CAS:528:DC%2BD1cXlsl2isg%3D%3D 10.1021/bi701624u 18189414 (Pubitemid 351198710)
41. RH O'Neil RH Lilien BR Donald RM Stroud AC Anderson 2003 Phylogenetic classification of protozoa based on the structure of the linker domain in the bifunctional enzyme, dihydrofolate reductase-thymidylate synthase J Biol Chem 278 52980 52987 10.1074/jbc.M310328200 14555647 (Pubitemid 38035900)
42. O Senkovich N Schormann D Chattopadhyay 2009 Structures of dihydrofolate reductase-thymidylate synthase of Trypanosoma cruzi in the folate-free state and in complex with two antifolate drugs, trimetrexate and methotrexate Acta Crystallogr D 65 704 716 10.1107/S090744490901230X 19564691