Plant-like phosphofructokinase from Plasmodium falciparum belongs to a novel class of ATP-dependent enzymes

International Journal for Parasitology

Volumn 39, Issue 13, 2009, Pages 1441-1453

  Mony, Binny M ^a   Mehta, Monika ^a   Jarori, Gotam K ^a   Sharma, Shobhona ^a  

^a TATA INSTITUTE OF FUNDAMENTAL RESEARCH   (India)

Author keywords

Apicomplexa; Enzyme; Glycolysis; Phosphofructokinase; Plasmodium; Regulation

Indexed keywords

6 PHOSPHOFRUCTOKINASE; 6 PHOSPHOFRUCTOKINASE ALPHA SUBUNIT; 6 PHOSPHOFRUCTOKINASE BETA SUBUNIT; ADENOSINE TRIPHOSPHATE; CITRIC ACID; FRUCTOSE 2,6 BISPHOSPHATE; HISTIDINE; PHOSPHOENOLPYRUVATE; PHOSPHOTRANSFERASE; PYROPHOSPHATE; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG;

CATALYSIS; CHROMOSOME; COLIFORM BACTERIUM; ENZYME ACTIVITY; GENE; MALARIA; PARASITE; PROTEIN;

ADULT; ARTICLE; CATALYSIS; CHROMOSOME 11; CHROMOSOME 9; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME ANALYSIS; ESCHERICHIA COLI; GENETIC DATABASE; HUMAN; HUMAN CELL; MOLECULAR CLONING; MOLECULAR PHYLOGENY; MOLECULAR WEIGHT; NONHUMAN; NUCLEOTIDE SEQUENCE; PLANT; PLASMODIUM FALCIPARUM; PROTEIN DOMAIN; SEQUENCE ANALYSIS; SPECIES COMPARISON; STRUCTURAL HOMOLOGY;

ADENOSINE TRIPHOSPHATE; ANIMALS; GLYCOLYSIS; HUMANS; PHOSPHOFRUCTOKINASE-1; PHYLOGENY; PLANT PROTEINS; PLANTS; PLASMODIUM FALCIPARUM; PROTOZOAN PROTEINS;

APICOMPLEXA; ESCHERICHIA COLI; PLASMODIUM (APICOMPLEXA); PLASMODIUM FALCIPARUM; PROTOZOA;

EID: 69349090622     PISSN: 00207519     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ijpara.2009.05.011     Document Type: Article

References (62)

1. Agbenyega T., Angus B.J., Bedu-Addo G., Baffoe-Bonnie B., Guyton T., Stacpoole P.W., and Krishna S. Glucose and lactate kinetics in children with severe malaria. J. Clin. Endocrinol. Metab. 85 (2000) 1569-1576
2. Alves A.M., Euverink G.J., Santos H., and Dijkhuizen L. Different physiological roles of ATP- and PP(i)-dependent phosphofructokinase isoenzymes in the methylotrophic actinomycete Amycolatopsis methanolica. J. Bacteriol. 183 (2001) 7231-7240
3. Aurrecoechea C., Brestelli J., Brunk B.P., Dommer J., Fischer S., Gajria B., Gao X., Gingle A., Grant G., Harb O.S., Heiges M., Innamorato F., Iodice J., Kissinger J.C., Kraemer E., Li W., Miller J.A., Nayak V., Pennington C., Pinney D.F., Roos D.S., Ross C., Stoeckert Jr. C.J., Treatman C., and Wang H. PlasmoDB: a functional genomic database for malaria parasites. Nucleic Acids Res. 37 (2009) D539-D543
4. Bapteste E., Moreira D., and Philippe H. Rampant horizontal gene transfer and phospho-donor change in the evolution of the phosphofructokinase. Gene 318 (2003) 185-191
5. Bär J., Golbik R., Hubner G., and Kopperschlager G. Denaturation of phosphofructokinase-1 from Saccharomyces cerevisiae by guanidinium chloride and reconstitution of the unfolded subunits to their catalytically active form. Biochemistry 39 (2000) 6960-6968
6. Beutler E. Red Cell Metabolism: A Manual of Biochemical Methods (1984), Grune & Stratton, Philadelphia 8-45
7. Bloxham D.P., and Lardy H.A. Phosphofructokinase. In: Boyer P.D. (Ed). The Enzymes vol. 8 (1973), Academic Press, New York, NY 239-278
8. Bruchhaus I., Jacobs T., Denart M., and Tannich E. Pyrophosphate-dependent phosphofructokinase of Entamoeba histolytica: molecular cloning, recombinant expression and inhibition by pyrophosphate analogues. Biochem. J. 316 (1996) 57-63
9. Buckwitz D., Jacobasch G., Gerth C., Holzhutter H.G., and Thamm R. A kinetic model of phosphofructokinase from Plasmodium berghei. Influence of ATP and fructose-6-phosphate. Mol. Biochem. Parasitol. 27 (1988) 225-232
10. 2(+)-complexed ATP. Biochem. J. 267 (1990) 353-357
11. Carlisle S.M., Blakeley S.D., Hemmingsen S.M., Trevanion S.J., Hiyoshi T., Kruger N.J., and Dennis D.T. Pyrophosphate-dependent phosphofructokinase: conservation of protein sequence between the alpha- and beta-subunits and with the ATP-dependent phosphofructokinase. J. Biol. Chem. 265 (1990) 18366-18371
12. Chan M., and Sim T.S. Functional analysis, overexpression, and kinetic characterization of pyruvate kinase from Plasmodium falciparum. Biochem. Biophys. Res. Commun. 326 (2005) 188-196
13. Chi A., and Kemp R.G. The primordial high energy compound: ATP or inorganic pyrophosphate?. J. Biol. Chem. 275 (2000) 35677-35679
14. Chi A.S., Deng Z., Albach R.A., and Kemp R.G. The two phosphofructokinase gene products of Entamoeba histolytica. J. Biol. Chem. 276 (2001) 19974-19981
15. Deng Z., Huang M., Singh K., Albach R.A., Latshaw S.P., Chang K.P., and Kemp R.G. Cloning and expression of the gene for the active PPi-dependent phosphofructokinase of Entamoeba histolytica. Biochem. J. 329 (1998) 659-664
16. Deng Z., Roberts D., Wang X., and Kemp R.G. Expression, characterization, and crystallization of the pyrophosphate-dependent phosphofructo-1-kinase of Borrelia burgdorferi. Arch. Biochem. Biophys. 371 (1999) 326-331
17. Denton H., Brown S.M., Roberts C.W., Alexander J., McDonald V., Thong K.W., and Coombs G.H. Comparison of the phosphofructokinase and pyruvate kinase activities of Cryptosporidium parvum, Eimeria tenella and Toxoplasma gondii. Mol. Biochem. Parasitol. 76 (1996) 23-29
18. Fleige T., Fischer K., Ferguson D.J., Gross U., and Bohne W. Carbohydrate metabolism in the Toxoplasma gondii apicoplast: localization of three glycolytic isoenzymes, the single pyruvate dehydrogenase complex, and a plastid phosphate translocator. Eukaryot. Cell 6 (2007) 984-996
19. Ginsburg H. Progress in in silico functional genomics: the malaria metabolic pathways database. Trends Parasitol. 22 (2006) 238-240
20. Goswami A., Singh S., Redkar V.D., and Sharma S. Characterization of P0, a ribosomal phosphoprotein of Plasmodium falciparum: antibody against amino-terminal domain inhibits parasite growth. J. Biol. Chem. 272 (1997) 12138-12143
21. Inoue H., Nojima H., and Okayama H. High efficiency transformation of Escherichia coli with plasmids. Gene 96 (1990) 23-28
22. Kemp R.G., and Gunasekera D. Evolution of the allosteric ligand sites of mammalian phosphofructo-1-kinase. Biochemistry 41 (2002) 9426-9430
23. Klinder A., Kirchberger J., Edelmann A., and Kopperschlager G. Assembly of phosphofructokinase-1 from Saccharomyces cerevisiae in extracts of single-deletion mutants. Yeast 14 (1998) 323-334
24. Knowles V.L., Greyson M.F., and Dennis D.T. Characterization of ATP-dependent fructose 6-phosphate 1-phosphotransferase isozymes from leaf and endosperm tissues of Ricinus communis. Plant Physiol. 92 (1990) 155-159
25. Kombrink E., Kruger N.J., and Beevers H. Kinetic properties of pyrophosphate: fructose-6-phosphate phosphotransferase from germinating castor bean endosperm. Plant Physiol. 74 (1984) 395-401
26. Lang-Unnasch N., and Murphy A.D. Metabolic changes of the malaria parasite during the transition from the human to the mosquito host. Annu. Rev. Microbiol. 52 (1998) 561-590
27. Layzer R.B. Phosphofructokinase from human erythrocytes. Methods Enzymol. 42 (1975) 110-115
28. López C., Chevalier N., Hannaert V., Rigden D.J., Michels P.A., and Ramirez J.L. Leishmania donovani phosphofructokinase: gene characterization, biochemical properties and structure-modeling studies. Eur. J. Biochem. 269 (2002) 3978-3989
29. Lovingshimer M.R., Siegele D., and Reinhart G.D. Construction of an inducible, pfkA and pfkB deficient strain of Escherichia coli for the expression and purification of phosphofructokinase from bacterial sources. Protein Expr. Purif. 46 (2006) 475-482
30. Marchler-Bauer A., Anderson J.B., Cherukuri P.F., DeWeese-Scott C., Geer L.Y., Gwadz M., He S., Hurwitz D.I., Jackson J.D., Ke Z., Lanczycki C.J., Liebert C.A., Liu C., Lu F., Marchler G.H., Mullokandov M., Shoemaker B.A., Simonyan V., Song J.S., Thiessen P.A., Yamashita R.A., Yin J.J., Zhang D., and Bryant S.H. CDD: a conserved domain database for protein classification. Nucleic Acids Res. 33 (2005) D192-D196
31. Massey T.H., and Deal Jr. W.C. Unusual, metabolite-dependent solubility properties of phosphofructokinase. J. Biol. Chem. 248 1 (1973) 56-62
32. Mather M.W., and Vaidya A.B. Mitochondria in malaria and related parasites: ancient, diverse and streamlined. J. Bioenerg. Biomembr. 40 (2008) 425-433
33. Mehta M., Sonawat H.M., and Sharma S. Malaria parasite-infected erythrocytes inhibit glucose utilization in uninfected red cells. FEBS Lett. 579 (2005) 6151-6158
34. Mertens E. ATP versus pyrophosphate: glycolysis revisited in parasitic protests. Parasitol. Today 9 (1993) 122-126
35. Michels P.A., Chevalier N., Opperdoes F.R., Rider M.H., and Rigden D.J. The glycosomal ATP-dependent phosphofructokinase of Trypanosoma brucei must have evolved from an ancestral pyrophosphate-dependent enzyme. Eur. J. Biochem. 250 (1997) 698-704
36. Müller M., Lee J.A., Gordon P., Gaasterland T., and Sensen C.W. Presence of prokaryotic and eukaryotic species in all subgroups of the PP(i)-dependent group II phosphofructokinase protein family. J. Bacteriol. 183 (2001) 6714-6716
37. Mustroph A., Sonnewald U., and Biemelt S. Characterisation of the ATP-dependent phosphofructokinase gene family from Arabidopsis thaliana. FEBS Lett. 581 (2007) 2401-2410
38. Nielsen T.H., Rung J.H., and Villadsen D. Fructose-2,6-bisphosphate: a traffic signal in plant metabolism. Trends Plant Sci. 9 (2004) 556-563
39. Oelshlegel Jr. F.J., Sander B.J., and Brewer G.J. Pyruvate kinase in malaria host-parasite interaction. Nature 255 (1975) 345-347
40. Pal-Bhowmick I., Vora H.K., and Jarori G.K. Sub-cellular localization and post-translational modifications of the Plasmodium yoelii enolase suggest moonlighting functions. Malar. J. 6 (2007) 45
41. Peng Z.Y., and Mansour T.E. Purification and properties of a pyrophosphate-dependent phosphofructokinase from Toxoplasma gondii. Mol. Biochem. Parasitol. 54 (1992) 223-230
42. Ramirez-Flandes S., and Ulloa O. Bosque: integrated phylogenetic analysis software. Bioinformatics 24 (2008) 2539-2541
43. Reeves R.E., South D.J., Blytt H.J., and Warren L.G. Pyrophosphate: d-fructose 6-phosphate 1-phosphotransferase: a new enzyme with the glycolytic function of 6-phosphofructokinase. J. Biol. Chem. 249 (1974) 7737-7741
44. Roth Jr. E.F., Raventos-Suarez C., Perkins M., and Nagel R.L. Glutathione stability and oxidative stress in P. falciparum infection in vitro: responses of normal and G6PD deficient cells. Biochem. Biophys. Res. Commun. 109 (1982) 355-362
45. Roth Jr. E.F., Calvin M.C., Max-Audit I., Rosa J., and Rosa R. The enzymes of the glycolytic pathway in erythrocytes infected with Plasmodium falciparum malaria parasites. Blood 72 (1988) 1922-1925
46. Sander B.J., Lowery M.S., and Kruckeberg W.C. Plasmodium berghei acid-insensitive phosphofructokinase in infected mouse erythrocytes. Exp. Parasitol. 53 (1982) 11-16
47. Schichtherle M., and Wahlgren M. Small-scale genomic DNA isolation from Plasmodium falciparum. In: Moll K., Ljungström I., Perlmann H., Scherf A., and Wahlgren M. (Eds). Methods in Malaria Research (2008), MR4/ATCC, Manassas 199-200
48. Shirakihara Y., and Evans P.R. Crystal structure of the complex of phosphofructokinase from Escherichia coli with its reaction products. J. Mol. Biol. 204 (1988) 973-994
49. Singh S., Sehgal A., Waghmare S., Chakraborty T., Goswami A., and Sharma S. Surface expression of the conserved ribosomal protein P0 on parasite and other cells. Mol. Biochem. Parasitol. 119 (2002) 121-124
50. Suzuki J., Mutton M.A., Ferro M.I., Lemos M.V., Pizauro J.M., Mutton M.J., and Di Mauro S.M. Putative pyrophosphate phosphofructose 1-kinase genes identified in sugar cane may be getting energy from pyrophosphate. Genet. Mol. Res. 2 (2003) 376-382
51. Todd J.F., Blakeley S.D., and Dennis D.T. Structure of the genes encoding the alpha- and beta-subunits of castor pyrophosphate-dependent phosphofructokinase. Gene 152 (1995) 181-186
52. Turner W.L., and Plaxton W.C. Purification and characterization of pyrophosphate- and ATP-dependent phosphofructokinases from banana fruit. Planta 217 (2003) 113-121
53. Uyeda K. Phosphofructokinases. Adv. Enzymol. 48 (1979) 193-244
54. Van Praag E. Use of 3-D computer modelling and kinetic studies to analyse grapefruit pyrophosphate-dependent phosphofructokinase. Int. J. Biol. Macromol. 21 (1997) 307-317
55. Van Schaftingen E., Lederer B., Bartrons R., and Hers H.G. A kinetic study of pyrophosphate: fructose-6-phosphate phosphotransferase from potato tubers. Application to a microassay of fructose 2,6-bisphosphate. Eur. J. Biochem. 129 (1982) 191-195
56. Winkler C., Delvos B., Martin W., and Henze K. Purification, microsequencing and cloning of spinach ATP-dependent phosphofructokinase link sequence and function for the plant enzyme. FEBS J. 274 (2007) 429-438
57. World Health Organization, 2008. World Malaria Report 2008. WHO, Geneva.
58. Wong J.H., Kiss F., Wu M.X., and Buchanan B.B. Pyrophosphate fructose-6-p 1-phosphotransferase from tomato fruit: evidence for change during ripening. Plant Physiol. 94 (1990) 499-506
59. Yan T.F., and Tao M. Multiple forms of pyrophosphate: d-fructose-6-phosphate 1-phosphotransferase from wheat seedlings. Regulation by fructose 2,6-bisphosphate. J. Biol. Chem. 259 (1984) 5087-5092
60. Yanai I., Wolf Y.I., and Koonin E.V. Evolution of gene fusions: horizontal transfer versus independent events. Genome Biol. 3 (2002) research0024
61. Zhao Y., Pokutta S., Maurer P., Lindt M., Franklin R.M., and Kappes B. Calcium-binding properties of a calcium-dependent protein kinase from Plasmodium falciparum and the significance of individual calcium-binding sites for kinase activation. Biochemistry 33 (1994) 3714-3721
62. Zhu X., Byrnes M., Nelson J.W., and Chang S.H. Role of glycine 212 in the allosteric behavior of phosphofructokinase from Bacillus stearothermophillus. Biochemistry 34 (1995) 2560-2565