The human malaria parasite Plasmodium falciparum expresses an atypical N-terminally extended pyrophosphokinase with specificity for thiamine

References

Baker, L.J., Dorocke, J.A., Harris, R.A., and Timm, D.E. (2001). The crystal structure of yeast thiamin pyrophosphokinase. Structure9, 539–546.10.1016/S0969-2126(01)00615-3Search in Google Scholar

Begley, T.P., Downs, D.M., Ealick, S.E., McLafferty, F.W., Van Loon, A.P., Taylor, S., Campobasso, N., Chiu, H.J., Kinsland, C., Reddick, J.J., and Xi, J. (1999). Thiamin biosynthesis in prokaryotes. Arch. Microbiol.171, 293–300.10.1007/s002030050713Search in Google Scholar

Blaszczyk, J., Shi, G., Yan, H., and Ji, X. (2000). Catalytic center assembly of HPPK as revealed by the crystal structure of a ternary complex at 1.2 5 Å resolution. Structure8, 1049–1058.10.1016/S0969-2126(00)00502-5Search in Google Scholar

Bozdech, Z. and Ginsburg, H. (2005). Data mining of the transcriptome of Plasmodium falciparum: the pentose phosphate pathway and ancillary processes. Malar. J.4, 17.10.1186/1475-2875-4-17Search in Google Scholar PubMed PubMed Central

Fankhauser, H., Zurlinden, A., Schweingruber, A.M., Edenharter, E., and Schweingruber, M.E. (1995). Schizosaccharomyces pombe thiamine pyrophosphokinase is encoded by gene tnr3 and is a regulator of thiamine metabolism, phosphate metabolism, mating, and growth. J. Biol. Chem.270, 28457–28462.10.1074/jbc.270.47.28457Search in Google Scholar PubMed

Foth, B.J., Ralph, S.A., Tonkin, C.J., Struck, N.S., Fraunholz, M., Roos, D.S., Cowman, A.F., and McFadden, G.I. (2003). Dissecting apicoplast targeting in the malaria parasite Plasmodium falciparum. Science299, 705–708.10.1126/science.1078599Search in Google Scholar PubMed

Foth, B.J., Stimmler, L.M., Handman, E., Crabb, B.S., Hodder, A.N., and McFadden, G.I. (2005). The malaria parasite Plasmodium falciparum has only one pyruvate dehydrogenase complex, which is located in the apicoplast. Mol. Microbiol.55, 39–53.10.1111/j.1365-2958.2004.04407.xSearch in Google Scholar PubMed

Friedrich, W. (1988). Vitamins (Berlin, Germany: Walter de Gruyter).10.1515/9783110859188Search in Google Scholar

Gardner, M.J., Hall, N., Fung, E., White, O., Berriman, M., Hyman, R.W., Carlton, J.M., Pain, A., Nelson, K.E., Bowman, S., et al. (2002). Genome sequence of the human malaria parasite Plasmodium falciparum. Nature419, 498–511.10.1038/nature01097Search in Google Scholar PubMed PubMed Central

Gengenbacher, M., Fitzpatrick, T.B., Raschle, T., Flicker, K., Sinning, I., Müller, S., Macheroux, P., Tews, I., and Kappes, B. (2006). Vitamin B₆ biosynthesis by the malaria parasite Plasmodium falciparum: biochemical and structural insights. J. Biol. Chem.281, 3633–3641.10.1074/jbc.M508696200Search in Google Scholar PubMed

Günther, S., McMillan, P.J., Wallace, L.J., and Müller, S. (2005). Plasmodium falciparum possesses organelle-specific α-keto acid dehydrogenase complexes and lipoylation pathways. Biochem. Soc. Trans.33, 977–980.10.1042/BST0330977Search in Google Scholar

Haider, N., Eschbach, M.L., de Souza Dias, S., Gilberger, T.W., Walter, R.D., and Lüersen, K. (2005). The spermidine synthase of the malaria parasite Plasmodium falciparum: molecular and biochemical characterisation of the polyamine synthesis enzyme. Mol. Biochem. Parasitol.142, 224–236.10.1016/j.molbiopara.2005.04.004Search in Google Scholar

Higgins, D., Thompson, J., Gibson, T., Thompson, J.D., Higgins, D.G., and Gibson, T.J. (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res.22, 4673–4680.Search in Google Scholar

Hohmann, S. and Meacock, P.A. (1998). Thiamin metabolism and thiamin diphosphate-dependent enzymes in the yeast Saccharomyces cerevisiae: genetic regulation. Biochim. Biophys. Acta1385, 201–219.10.1016/S0167-4838(98)00069-7Search in Google Scholar

Kim, Y.S., Nosaka, K., Downs, D.M., Kwak, J.M., Park, D., Chung, I.K., and Nam, H.G. (1998). A Brassica cDNA clone encoding a bifunctional hydroxymethylpyrimidine kinase/thiamin-phosphate pyrophosphorylase involved in thiamin biosynthesis. Plant Mol. Biol.37, 955–666.Search in Google Scholar

Kumar, S., Tamura, K., and Nei, M. (2004). MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Briefings Bioinformatics5, 150–163.10.1093/bib/5.2.150Search in Google Scholar

Kyes, S., Pinches, R., and Newbold, C. (2000). A simple RNA analysis method shows var and rif multigene family expression patterns in Plasmodium falciparum. Mol. Biochem. Parasitol.105, 311–315.10.1016/S0166-6851(99)00193-0Search in Google Scholar

Lakaye, B., Wirtzfeld, B., Wins, P., Grisar, T., and Bettendorff, L. (2004). Thiamine triphosphate, a new signal required for optimal growth of Escherichia coli during amino acid starvation. J. Biol. Chem.279, 17142–17147.10.1074/jbc.M313569200Search in Google Scholar PubMed

Lambros, C. and Vanderberg, J.P. (1979). Synchronization of Plasmodium falciparum erythrocytic stages in culture. J. Parasitol.65, 418–420.10.2307/3280287Search in Google Scholar

Liu, J.Y., Timm, D.E., and Hurley, T.D. (2006) Pyrithiamin as a substrate for thiamine pyrophosphokinase. J. Biol. Chem.281, 6601–6607.10.1074/jbc.M510951200Search in Google Scholar PubMed

Morett, E., Korbel, J.O., Rajan, E., Saab-Rincon, G., Olvera, L., Olvera, M., Schmidt, S., Snel, B., and Bork, P. (2003). Systematic discovery of analogous enzymes in thiamin biosynthesis. Nat. Biotechnol.21, 790–795.10.1038/nbt834Search in Google Scholar PubMed

Marobbio, C.M., Vozza, A., Harding, M., Bisaccia, F., Palmieri, F., and Walker, J.E. (2002). Identification and reconstitution of the yeast mitochondrial transporter for thiamine pyrophosphate. EMBO J.21, 5653–5661.10.1093/emboj/cdf583Search in Google Scholar PubMed PubMed Central

McMillan, P.J., Stimmler, L.M., Foth, B.J., McFadden, G.I., and Müller, S. (2005). The human malaria parasite Plasmodium falciparum possesses two distinct dihydrolipoamide dehydrogenases. Mol. Microbiol.55, 27–38.10.1111/j.1365-2958.2004.04398.xSearch in Google Scholar

Melnick, J., Lis, E., Park, J.H., Kinsland, C., Mori, H., Baba, T., Perkins, J., Schyns, G., Vassieva, O., Osterman, A., and Begley, T.P. (2004). Identification of the two missing bacterial genes involved in thiamine salvage: thiamine pyrophosphokinase and thiamine kinase. J. Bacteriol.186, 3660–3662.10.1128/JB.186.11.3660-3662.2004Search in Google Scholar

Müller, I.B., Walter, R.D., and Wrenger, C. (2005). Structural metal dependency of the arginase from the human malaria parasite Plasmodium falciparum. Biol. Chem.386, 117–126.10.1515/BC.2005.015Search in Google Scholar

Nosaka, K., Kaneko, Y., Nishimura, H., and Iwashima, A. (1993). Isolation and characterization of a thiamin pyrophosphokinase gene, THI80, from Saccharomyces cerevisiae. J. Biol. Chem.268, 17440–17447.10.1016/S0021-9258(19)85354-1Search in Google Scholar

Nosaka, K., Onozuka, M., Nishino, H., Nishimura, H., Kawasaki, Y., and Ueyama, H. (1999). Molecular cloning and expression of a mouse thiamin pyrophosphokinase cDNA. J. Biol. Chem.274, 34129–34133.10.1074/jbc.274.48.34129Search in Google Scholar

Nosaka, K., Onozuka, M., Kakazu, N., Hibi, S., Nishimura, H., Nishino, H., and Abe, T. (2001). Isolation and characterization of a human thiamine pyrophosphokinase cDNA. Biochim. Biophys. Acta1517, 293–297.10.1016/S0167-4781(00)00247-5Search in Google Scholar

Peterson, J.W., Gubler, C.J., and Kuby, S.A. (1975). Partial purification and properties of thiamine pyrophosphokinase from pig brain. Biochim. Biophys. Acta397, 377–394.10.1016/0005-2744(75)90127-8Search in Google Scholar

Pohl, M., Sprenger, G.A., and Müller, M. (2004). A new perspective on thiamine catalysis. Curr. Opin. Biotechnol.15, 335–342.10.1016/j.copbio.2004.06.002Search in Google Scholar PubMed

Ralph, S.A., van Dooren, G.G., Waller, R.F., Crawford, M.J., Fraunholz, M.J., Foth, B.J., Tonkin, C.J., Roos, D.S., and McFadden, G.I. (2004). Tropical infectious diseases: metabolic maps and functions of the Plasmodium falciparum apicoplast. Nat. Rev. Microbiol.2, 203–216.10.1038/nrmicro843Search in Google Scholar PubMed

Rodionov, D.A., Vitreschak, A.G., Mironov, A.A., and Gelfand, M.S. (2002). Comparative genomics of thiamin biosynthesis in procaryotes. New genes and regulatory mechanisms. J. Biol. Chem.277, 48949–48959.10.1074/jbc.M208965200Search in Google Scholar PubMed

Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual, 2nd ed. (Cold Spring Harbor, NY, USA: Cold Spring Harbor Laboratory).Search in Google Scholar

Schopfer, W.H. (1949). Plants and Vitamins (Waltham, MA, USA: Chronica Botanica).Search in Google Scholar

Shioda, T., Egi, Y., Yamada, K., and Kawasaki, T. (1991). Properties of thiamin triphosphate-synthesizing activity of chicken cytosolic adenylate kinase and the effect of adenine nucleotides. Biochim. Biophys. Acta1115, 30–35.10.1016/0304-4165(91)90007-4Search in Google Scholar

Struck, N.S., de Souza Dias, S., Langer, C., Marti, M., Pearce, J.A., Cowman, A.F., and Gilberger, T.W. (2005). Re-defining the Golgi complex in Plasmodium falciparum using the novel Golgi marker PfGRASP. J. Cell. Sci.118, 5603–5613.10.1242/jcs.02673Search in Google Scholar PubMed

Tonkin, C.J., van Dooren, G.G., Spurck, T.P., Struck, N.S., Good, R.T., Handman, E., Cowman, A.F., and McFadden, G.I. (2004). Localization of organellar proteins in Plasmodium falciparum using a novel set of transfection vectors and a new immunofluorescence fixation method. Mol. Biochem. Parasitol.137, 13–21.10.1016/j.molbiopara.2004.05.009Search in Google Scholar PubMed

Trager, W. and Jensen, J.B. (1976). Human malaria parasites in continuous culture. Science193, 673–675.10.1126/science.781840Search in Google Scholar PubMed

Umlas, J. and Fallon, J.N. (1971). New thick-film technique for malaria diagnosis. Use of saponin stromatolytic solution for lysis. Am. J. Trop. Med. Hyg.20, 527–529.10.4269/ajtmh.1971.20.527Search in Google Scholar PubMed

Voskoboyev, A.I. and Ostrovsky, Y.M. (1982). Thiamin pyrophosphokinase: structure, properties, and role in thiamin metabolism. Ann. NY Acad. Sci.378, 161–176.10.1111/j.1749-6632.1982.tb31195.xSearch in Google Scholar PubMed

Wakabayashi, Y. (1978). Purification of thiamine pyrophosphokinase from pig brain. Vitamins52, 223–228.Search in Google Scholar

Wightman, R. and Meacock, P.A. (2003). The THI5 gene family of Saccharomyces cerevisiae: distribution of homologues among the hemiascomycetes and functional redundancy in the aerobic biosynthesis of thiamin from pyridoxine. Microbiology149, 1447–1460.10.1099/mic.0.26194-0Search in Google Scholar PubMed

Wrenger, C. and Müller, S. (2004). The human malaria parasite Plasmodium falciparum has distinct organelle-specific lipoylation pathways. Mol. Microbiol.53, 103–113.10.1111/j.1365-2958.2004.04112.xSearch in Google Scholar PubMed

Wrenger, C., Eschbach, M.L., Müller, I.B., Warnecke, D., and Walter, R.D. (2005). Analysis of the vitamin B₆ biosynthesis pathway in the human malaria parasite Plasmodium falciparum. J. Biol. Chem.280, 5242–5248.10.1074/jbc.M412475200Search in Google Scholar PubMed

Wrenger, C., Eschbach, M.L., Müller, I.B., Laun, N.P., Begley, T.P., and Walter, R.D. (2006). Vitamin B₁de novo synthesis in the human malaria parasite Plasmodium falciparum depends on external provision of 4-amino-5-hydroxymethyl-2-methylpyrimidine. Biol. Chem.387, 41–51.Search in Google Scholar

Zeidler, J., Sayer, B.G., and Spenser, I.D. (2003). Biosynthesis of vitamin B1 in yeast. Derivation of the pyrimidine unit from pyridoxine and histidine. Intermediacy of urocanic acid. J. Am. Chem. Soc.125, 13094–13105.Search in Google Scholar

Zurlinden, A. and Schweingruber, M.E. (1994). Cloning, nucleotide sequence, and regulation of Schizosaccharomyces pombe thi4, a thiamine biosynthetic gene. J. Bacteriol.176, 6631–6635.10.1128/jb.176.21.6631-6635.1994Search in Google Scholar PubMed PubMed Central