Stage specific gene expression and cellular localization of two isoforms of the serine hydroxymethyltransferase in the protozoan parasite Leishmania

Molecular and Biochemical Parasitology

Volumn 150, Issue 1, 2006, Pages 63-71

  Gagnon, Dominic ^a   Foucher, Aude ^a   Girard, Isabelle ^a   Ouellette, Marc ^a  

^a LAVAL UNIVERSITY   (Canada)

Author keywords

Drug target; Folate metabolism; Leishmania; Mitochondria

Indexed keywords

DIGITONIN; FOLIC ACID ANTAGONIST; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; GLYCINE; GLYCINE HYDROXYMETHYLTRANSFERASE; GREEN FLUORESCENT PROTEIN; HEAT SHOCK PROTEIN 60; HYBRID PROTEIN; ISOENZYME; METHOTREXATE; METHYLENETETRAHYDROFOLIC ACID; PROTOZOAL DNA; SERINE; TETRAHYDROFOLIC ACID; THIOSEMICARBAZIDE;

AMASTIGOTE; AMINO ACID SEQUENCE; ANTIBIOTIC RESISTANCE; ARTICLE; CELL FRACTIONATION; CELLULAR DISTRIBUTION; CYTOSOL; ENZYME MECHANISM; FLUORESCENCE MICROSCOPY; FOLATE METABOLISM; GENE EXPRESSION; LEISHMANIA; LEISHMANIA MAJOR; MITOCHONDRION; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMASTIGOTE; REAL TIME POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS; TRYPANOSOMA BRUCEI; TRYPANOSOMA CRUZI; WESTERN BLOTTING;

AMINO ACID SEQUENCE; ANIMALS; CHAPERONIN 60; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENOME, PROTOZOAN; GLYCINE HYDROXYMETHYLTRANSFERASE; GREEN FLUORESCENT PROTEINS; ISOENZYMES; LEISHMANIA MAJOR; MITOCHONDRIA; MOLECULAR SEQUENCE DATA; PROTOZOAN PROTEINS; SEQUENCE ALIGNMENT; TRANSFECTION;

KINETOPLASTIDA; LEISHMANIA MAJOR; PROTOZOA; TRYPANOSOMA BRUCEI; TRYPANOSOMA CRUZI;

EID: 33748464365     PISSN: 01666851     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molbiopara.2006.06.009     Document Type: Article

References (49)

1. Herwaldt B.L. Leishmaniasis. Lancet 354 (1999) 1191-1199
2. Murray H.W., Berman J., Davies C.R., and Saravia N.G. Advances in leishmaniasis. Lancet 366 (2005) 1561-1577
3. Croft S.L., Sundar S., and Fairlamb A.H. Drug resistance in leishmaniasis. Clin Microbiol Rev 19 (2006) 111-126
4. Nzila A., Ward S.A., Marsh K., Sims P.F., and Hyde J.E. Comparative folate metabolism in humans and malaria parasites (Part I): pointers for malaria treatment from cancer chemotherapy. Trends Parasitol 21 (2005) 292-298
5. Cronstein B.N. Low-dose methotrexate: a mainstay in the treatment of rheumatoid arthritis. Pharmacol Rev 57 (2005) 163-172
6. Nare B., Luba J., Hardy L.W., and Beverley S. New approaches to Leishmania chemotherapy: pteridine reductase 1 (PTR1) as a target and modulator of antifolate sensitivity [In Process Citation]. Parasitology 114 Suppl (1997) S101-S110
7. Ouellette M., Drummelsmith J., El Fadili A., Kundig C., Richard D., and Roy G. Pterin transport and metabolism in Leishmania and related trypanosomatid parasites. Int J Parasitol 32 (2002) 385-398
8. Richard D., Kundig C., and Ouellette M. A new type of high affinity folic acid transporter in the protozoan parasite Leishmania and deletion of its gene in methotrexate-resistant cells. J Biol Chem 277 (2002) 29460-29467
9. Richard D., Leprohon P., Drummelsmith J., and Ouellette M. Growth phase regulation of the main folate transporter of Leishmania infantum and its role in methotrexate resistance. J Biol Chem 279 (2004) 54494-54501
10. Cunningham M.L., and Beverley S.M. Pteridine salvage throughout the Leishmania infectious cycle: implications for antifolate chemotherapy. Mol Biochem Parasitol 113 (2001) 199-213
11. Beverley S.M., Ellenberger T.E., and Cordingley J.S. Primary structure of the gene encoding the bifunctional dihydrofolate reductase-thymidylate synthase of Leishmania major. Proc Natl Acad Sci USA 83 (1986) 2584-2588
12. Grumont R., Washtien W.L., Caput D., and Santi D.V. Bifunctional thymidylate synthase-dihydrofolate reductase from Leishmania tropica: sequence homology with the corresponding monofunctional proteins. Proc Natl Acad Sci USA 83 (1986) 5387-5391
13. El Fadili A., Kundig C., and Ouellette M. Characterization of the folylpolyglutamate synthetase gene and polyglutamylation of folates in the protozoan parasite Leishmania. Mol Biochem Parasitol 124 (2002) 63-71
14. El Fadili A., Richard D., Kundig C., and Ouellette M. Effect of polyglutamylation of methotrexate on its accumulation and the development of resistance in the protozoan parasite Leishmania. Biochem Pharmacol 66 (2003) 999-1008
15. Ivens A.C., Peacock C.S., Worthey E.A., Murphy L., Aggarwal G., Berriman M., et al. The genome of the kinetoplastid parasite, Leishmania major. Science 309 (2005) 436-442
16. Schirch V., and Szebenyi D.M. Serine hydroxymethyltransferase revisited. Curr Opin Chem Biol 9 (2005) 482-487
17. Salcedo E., Sims P.F., and Hyde J.E. A glycine-cleavage complex as part of the folate one-carbon metabolism of Plasmodium falciparum. Trends Parasitol 21 (2005) 406-411
18. Capelluto D.G., Hellman U., Cazzulo J.J., and Cannata J.J. Purification and partial characterization of three isoforms of serine hydroxymethyltransferase from Crithidia fasciculata. Mol Biochem Parasitol 98 (1999) 187-201
19. Capelluto D.G., Hellman U., Cazzulo J.J., and Cannata J.J. Purification and some properties of serine hydroxymethyltransferase from Trypanosoma cruzi. Eur J Biochem 267 (2000) 712-719
20. Scott D.A., Coombs G.H., and Sanderson B.E. Folate utilisation by Leishmania species and the identification of intracellular derivatives and folate-metabolising enzymes. Mol Biochem Parasitol 23 (1987) 139-149
21. Ouellette M., Fase-Fowler F., and Borst P. The amplified H circle of methotrexate-resistant leishmania tarentolae contains a novel P-glycoprotein gene. EMBO J 9 (1990) 1027-1033
22. Papadopoulou B., Roy G., and Ouellette M. A novel antifolate resistance gene on the amplified H circle of Leishmania. EMBO J 11 (1992) 3601-3608
23. Claros M.G., and Vincens P. Computational method to predict mitochondrially imported proteins and their targeting sequences. Eur J Biochem 241 (1996) 779-786
24. Papadopoulou B., Roy G., Mourad W., Leblanc E., and Ouellette M. Changes in folate and pterin metabolism after disruption of the Leishmania H locus short chain dehydrogenase gene. J Biol Chem 269 (1994) 7310-7315
25. Foucher A., Papadopoulou B., and Ouellette M. Prefractionation by digitonin extraction increased representation of the cytosolic and intracellular proteome of Leishmania infantum. J Proteome Res 5 (2006) 1741-1750
26. Truscott K.N., Brandner K., and Pfanner N. Mechanisms of protein import into mitochondria. Curr Biol 13 (2003) R326-R337
27. El-Sayed N.M., Myler P.J., Blandin G., Berriman M., Crabtree J., Aggarwal G., et al. Comparative genomics of trypanosomatid parasitic protozoa. Science 309 (2005) 404-409
28. Schluter A., Wiesgigl M., Hoyer C., Fleischer S., Klaholz L., Schmetz C., and Clos J. Expression and subcellular localization of cpn60 protein family members in Leishmania donovani. Biochim Biophys Acta 1491 (2000) 65-74
29. Rey-Ladino J.A., Joshi P.B., Singh B., Gupta R., and Reiner N.E. Leishmania major: molecular cloning, sequencing, and expression of the heat shock protein 60 gene reveals unique carboxy terminal peptide sequences. Exp Parasitol 85 (1997) 249-263
30. Ellenberger T.E., and Beverley S.M. Biochemistry and regulation of folate and methotrexate transport in Leishmania major. J Biol Chem 262 (1987) 10053-10058
31. Brun R., and Schonenberger. Cultivation and in vitro cloning or procyclic culture forms of Trypanosoma brucei in a semi-defined medium. Short communication. Acta Trop 36 (1979) 289-292
32. Chowdhury S.F., Di Lucrezia R., Guerrero R.H., Brun R., Goodman J., Ruiz-Perez L.M., Pacanowska D.G., and Gilbert I.H. Novel inhibitors of leishmanial dihydrofolate reductase. Bioorg Med Chem Lett 11 (2001) 977-980
33. Pez D., Leal I., Zuccotto F., Boussard C., Brun R., Croft S.L., Yardley V., Ruiz Perez L.M., Gonzalez Pacanowska D., and Gilbert I.H. 2,4-Diaminopyrimidines as inhibitors of leishmanial and trypanosomal dihydrofolate reductase. Bioorg Med Chem 11 (2003) 4693-4711
34. Acharya J.K., and Rao N.A. A novel intermediate in the interaction of thiosemicarbazide with sheep liver serine hydroxymethyltransferase. J Biol Chem 267 (1992) 19066-19071
35. Baskaran N., Prakash V., Savithri H.S., Radhakrishnan A.N., and Appaji Rao N. Mode of interaction of aminooxy compounds with sheep liver serine hydroxymethyltransferase. Biochemistry 28 (1989) 9613-9617
36. Heise N., and Opperdoes F.R. Localisation of a 3-hydroxy-3-methylglutaryl-coenzyme A reductase in the mitochondrial matrix of Trypanosoma brucei procyclics. Z Naturforsch [C] 55 (2000) 473-477
37. Pena-Diaz J., Montalvetti A., Flores C.L., Constan A., Hurtado-Guerrero R., De Souza W., Gancedo C., Ruiz-Perez L.M., and Gonzalez-Pacanowska D. Mitochondrial localization of the mevalonate pathway enzyme 3-hydroxy-3-methyl-glutaryl-CoA reductase in the Trypanosomatidae. Mol Biol Cell 15 (2004) 1356-1363
38. Appling D.R. Compartmentation of folate-mediated one-carbon metabolism in eukaryotes. FASEB J 5 (1991) 2645-2651
39. McNeil J.B., Bognar A.L., and Pearlman R.E. In vivo analysis of folate coenzymes and their compartmentation in Saccharomyces cerevisiae. Genetics 142 (1996) 371-381
40. Piper M.D., Hong S.P., Ball G.E., and Dawes I.W. Regulation of the balance of one-carbon metabolism in Saccharomyces cerevisiae. J Biol Chem 275 (2000) 30987-30995
41. Berriman M., Ghedin E., Hertz-Fowler C., Blandin G., Renauld H., Bartholomeu D.C., et al. The genome of the African trypanosome Trypanosoma brucei. Science 309 (2005) 416-422
42. Nirmalan N., Wang P., Sims P.F., and Hyde J.E. Transcriptional analysis of genes encoding enzymes of the folate pathway in the human malaria parasite Plasmodium falciparum. Mol Microbiol 46 (2002) 179-190
43. Liu X., Reig B., Nasrallah I.M., and Stover P.J. Human cytoplasmic serine hydroxymethyltransferase is an mRNA binding protein. Biochemistry 39 (2000) 11523-11531
44. Gelling C.L., Piper M.D., Hong S.P., Kornfeld G.D., and Dawes I.W. Identification of a novel one-carbon metabolism regulon in Saccharomyces cerevisiae. J Biol Chem 279 (2004) 7072-7081
45. Subramanian M., Qiao W.B., Khanam N., Wilkins O., Der S.D., Lalich J.D., and Bognar A.L. Transcriptional regulation of the one-carbon metabolism regulon in Saccharomyces cerevisiae by Bas1p. Mol Microbiol 57 (2005) 53-69
46. Stover P.J., Chen L.H., Suh J.R., Stover D.M., Keyomarsi K., and Shane B. Molecular cloning, characterization, and regulation of the human mitochondrial serine hydroxymethyltransferase gene. J Biol Chem 272 (1997) 1842-1848
47. Jenkins W.T., and D'Ari L. Glutamic-aspartic transaminase. XI. Reactivity toward thiosemicarbazide. Biochemistry 5 (1966) 2900-2905
48. Christen P., and Mehta P.K. From cofactor to enzymes. The molecular evolution of pyridoxal-5′-phosphate-dependent enzymes. Chem Rec 1 (2001) 436-447
49. Alfadhli S., and Rathod P.K. Gene organization of a Plasmodium falciparum serine hydroxymethyltransferase and its functional expression in Escherichia coli. Mol Biochem Parasitol 110 (2000) 283-291