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Evolutionary analysis of fructose 2,6-bisphosphate metabolism.

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Michels, Paulus [UCL] Rigden, Daniel J

Fructose 2,6-bisphosphate is a potent metabolic regulator in eukaryotic organisms; it affects the activity of key enzymes of the glycolytic and gluconeogenic pathways. The enzymes responsible for its synthesis and hydrolysis, 6-phosphofructo-2-kinase (PFK-2) and fructose-2,6-bisphosphatase (FBPase-2) are present in representatives of all major eukaryotic taxa. Results from a bioinformatics analysis of genome databases suggest that very early in evolution, in a common ancestor of all extant eukaryotes, distinct genes encoding PFK-2 and FBPase-2, or related enzymes with broader substrate specificity, fused resulting in a bifunctional enzyme both domains of which had, or later acquired, specificity for fructose 2,6-bisphosphate. Subsequently, in different phylogenetic lineages duplications of the gene of the bifunctional enzyme occurred, allowing the development of distinct isoenzymes for expression in different tissues, at specific developmental stages or under different nutritional conditions. Independently in different lineages of many unicellular eukaryotes one of the domains of the different PFK-2/FBPase-2 isoforms has undergone substitutions of critical catalytic residues, or deletions rendering some enzymes monofunctional. In a considerable number of other unicellular eukaryotes, mainly parasitic organisms, the enzyme seems to have been lost altogether. Besides the catalytic core, the PFK-2/FBPase-2 has often N- and C-terminal extensions which show little sequence conservation. The N-terminal extension in particular can vary considerably in length, and seems to have acquired motifs which, in a lineage-specific manner, may be responsible for regulation of catalytic activities, by phosphorylation or ligand binding, or for mediating protein-protein interactions.

Document type Article de périodique (Journal article) – Journal Article, Research Support, Non-U.S. Gov't, Review
Access type Accès restreint
Publication date 2006
Journal information "IUBMB life" - Vol. 58, no. 3, p. 133-41 (2006)
Peer reviewed yes
issn 1521-6543
Publication status Publié
Affiliation UCL - MD/BICL - Département de biochimie et de biologie cellulaire
MESH Subject Animals ; Energy Metabolism - genetics ; Evolution, Molecular ; Fructosediphosphates - metabolism ; Humans ; Phosphofructokinase-2 - genetics
Links
  1. Van Schaftingen, E. and Hue, L. and Hers, H. (1980) Fructose 2,6-bisphosphate, the probably structure of the glucose- and glucagon-sensitive stimulator of phosphofructokinase Biochem. J., 192, pp. 897 - 901.
  2. Van Schaftingen, E. and Hers, H. (1981) Inhibition of fructose-1,6-bisphosphatase by fructose 2,6-biphosphate Proc. Natl. Acad. Sci. USA, 78, pp. 2861 - 2863.
  3. Okar, D. and Manzano, A. and Navarro-Sabate, A. and Riera, L. and Bartrons, R. and Lange, A. (2001) PFK-2/FBPase-2: maker and breaker of the essential biofactor fructose-2,6-bisphosphate Trends Biochem. Sci., 26, pp. 30 - 35.
  4. Rider, M. and Bertrand, L. and Vertommen, D. and Michels, P. and Rousseau, G. and Hue, L. (2004) 6-phosphofructo-2-kinase/fructose-2,6-bisphosphatase: head-to-head with a bifunctional enzyme that controls glycolysis Biochem. J., 381, pp. 561 - 579.
  5. Nielsen, T. and Rung, J. and Villadsen, D. (2004) Fructose-2,6-bisphosphate: a traffic signal in plant metabolism Trends Plant Sci., 9, pp. 556 - 563.
  6. Opperdoes, F. and Borst, P. (1977) Localization of nine glycolytic enzymes in a microbody-like organelle in Trypanosoma brucei: the glycosome FEBS Lett., 80, pp. 360 - 364.
  7. Hannaert, V. and Bringaud, F. and Opperdoes, F. and Michels, P. (2003) Evolution of energy metabolism and its compartmentation in Kinetoplastida Kinetoplastid Biol. Dis., 2, pp. 11. http://www.kinetoplastids.com/content/2/1/11
  8. Van Schaftingen, E. and Opperdoes, F. and Hers, G. (1985) Stimulation of Trypanosoma brucei pyruvate kinase by fructose 2,6-bisphosphate Eur. J. Biochem., 153, pp. 403 - 406.
  9. Van Schaftingen, E. and Opperdoes, F. and Hers, H. (1987) Effects of various metabolic conditions and of the trivalent arsenical melarsen oxide on the intracellular levels of fructose 2,6-bisphosphate and of glycolytic intermediates in Trypanosoma brucei Eur. J. Biochem., 166, pp. 653 - 661.
  10. Pilkis, S. and Chrisman, T. and Burgress, B. and McGrane, M. and Colosia, A. and Pilkis, J. and Claus, T. and El-Maghrabi, M. (1983) Rat hepatic 6-phosphofructo-2-kinase/fructose-2,6-bisphosphatase: a unique bifunctional enzyme Adv. Enzyme Regul., 21, pp. 147 - 173.
  11. Hasemann, C. and Istvan, E. and Uyeda, K. and Deisenhofer, J. (1996) The crystal structure of the bifunctional enzyme 6-phosphofructo-2-kinase/fructose-2,6-bisphosphatase reveals distinct domain homologies Structure, 4, pp. 1017 - 1029.
  12. Bertrand, L. and Vertommen, D. and Depiereux, E. and Hue, L. and Rider, M. and Feytmans, E. (1997) Modelling the 2-kinase domain of 6-phosphofructo-2-kinase/fructose-2,6-bisphosphatase on adenylate kinase Biochem. J., 321, pp. 615 - 621.
  13. Bazan, J. and Fletterick, R. and Pilkis, S. (1989) Evolution of a bifunctional enzyme: 6-phosphofructo-2-kinase/fructose-2,6-bisphosphatase Proc. Natl. Acad. Sci. USA, 86, pp. 9642 - 9646.
  14. Kretschmer, M. and Fraenkel, D. (1991) Yeast 6-phosphofructo-2-kinase: sequence and mutant Biochemistry, 30, pp. 10663 - 10672.
  15. Paravicini, G. and Kretschmer, M. (1992) The yeast FBP26 gene codes for a fructose-2,6-bisphosphatase Biochemistry, 31, pp. 7126 - 7133.
  16. Boles, E. and Gohlmann, H. and Zimmermann, F. (1996) Cloning of a second gene encoding 6-phosphofructo-2-kinase in yeast, and characterization of mutant strains without fructose 2,6-bisphosphate Mol. Microbiol., 20, pp. 65 - 76.
  17. Chevalier, N. and Bertrand, L. and Rider, M. and Opperdoes, F. and Rigden, D. and Michels, P. (2005) 6-Phosphofructo-2-kinase and fructose-2,6-bisphosphatase in Trypanosomatidae. Molecular characterization, database searches, modelling studies and evolutionary analysis FEBS J., 272, pp. 3542 - 3560.
  18. Van Schaftingen, E. and Mertens, E. and Opperdoes, F.(1990) Fructose 2,6-bisphosphate in primitive systems. In Fructose 2,6-bisphosphate. ( pp. 229 - 244 ). Boca Raton : CRC Press.
  19. Marcus, F. and Edelstein, I. and Rittenhouse, J. (1984) Inhibition of Escherichia coli fructose-1,6-bisphosphatase by fructose 2,6-bisphosphate Biochem. Biophys. Res. Commun., 119, pp. 1103 - 1108.
  20. Rittmann, D. and Schaffer, S. and Wendisch, V. and Sahm, H. (2003) Fructose-1,6-bisphosphatase from Corynebacterium glutamicum: expression and deletion of the fbp gene and biochemical characterization of the enzyme Arch. Microbiol., 180, pp. 285 - 292.
  21. Mizuguchi, H. and Cook, P. and Tai, C. and Hasemann, C. and Uyeda, K. (1999) Reaction mechanism of fructose-2,6-bisphosphatase. A mutation of nucleophilic catalyst, histidine 256, induces an alteration in the reaction pathway J. Biol. Chem., 274, pp. 2166 - 2175.
  22. Bertrand, L. and Deprez, J. and Vertommen, D. and Di Pietro, A. and Hue, L. and Rider, M. (1997) Site-directed mutagenesis of Lys-174, Asp-179 and Asp-191 in the 2-kinase domain of 6-phosphofructo-2-kinase/fructose-2,6-bisphosphatase Biochem. J., 321, pp. 623 - 627.
  23. Kim, S. and Manes, N. and El-Maghrabi, M. and Lee, Y. (2006) Crystal structure of the hypoxia-inducible form of 6-phosphofructo-2-kinase/fructose-2,6-bisphosphatase (PFKFB3): a possible new target for cancer therapy J. Biol. Chem., 281, pp. 2939 - 2944.
  24. Koonin, E. and Makarova, K. and Aravind, L. (2001) Horizontal gene transfer in prokaryotes: quantification and classification Annu. Rev. Microbiol., 55, pp. 709 - 742.
  25. Calteau, A. and Gouy, M. and Perriere, G. (2005) Horizontal transfer of two operons coding for hydrogenases between bacteria and archaea J. Mol. Evol., 60, pp. 557 - 565.
  26. Poorman, R. and Randolph, A. and Kemp, R. and Heinrikson, R. (1984) Evolution of phosphofructokinase – gene duplication and creation of new effector sites Nature, 309, pp. 467 - 469.
  27. Fothergill-Gilmore, L. and Michels, P. (1993) Evolution of glycolysis Prog. Biophys. Mol. Biol., 59, pp. 105 - 235.
  28. Li, Y. and Rivera, D. and Ru, W. and Gunasekera, D. and Kemp, R. (1999) Identification of allosteric sites in rabbit phosphofructo-1-kinase Biochemistry, 38, pp. 16407 - 16412.
  29. Meyer, A. and Schartl, M. (1999) Gene and genome duplications in vertebrates: the one-to-four (-to-eight in fish) rule and the evolution of novel gene functions Curr. Opin. Cell Biol., 11, pp. 699 - 704.
  30. Sedgwick, S. and Smerdon, S. (1999) The ankyrin repeat: a diversity of interactions on a common structural framework Trends Biochem. Sci., 24, pp. 311 - 316.
  31. Lee, Y. and Li, Y. and Uyeda, K. and Hasemann, C. (2003) Tissue-specific structure/function differentiation of the liver isoform of 6-phosphofructo-2-kinase/fructose-2,6-bisphosphatase J. Biol. Chem., 278, pp. 523 - 530.
  32. Rigden, D. and Bagyan, I. and Lamani, E. and Setlow, P. and Jedrzejas, M. (2001) A cofactor-dependent phosphoglycerate mutase homolog from Bacillus stearothermophilus is actually a broad specificity phosphatase Protein Sci., 10, pp. 1835 - 1846.
  33. Tauler, A. and Lange, A. and El-Maghrabi, M. and Pilkis, S. (1989) Expression of rat liver 6-phosphofructo-2-kinase/fructose-2,6-bisphosphatase and its kinase domain in Escherichia coli Proc. Natl. Acad. Sci. USA, 86, pp. 7316 - 7320.
  34. Liang, J. and Huang, S. and Zhang, Y. and Ke, H. and Lipscomb, W. (1992) Crystal structure of the neutral form of fructose 1,6-bisphosphatase complexed with regulatory inhibitor fructose 2,6-bisphosphate at 2.6-Å resolution Proc. Natl. Acad. Sci. USA, 89, pp. 2404 - 2408.
  35. Xue, Y. and Huang, S. and Liang, J. and Zhang, Y. and Lipscomb, W. (1994) Crystal structure of fructose-1,6-bisphosphatase complexed with fructose 2,6-bisphosphate, AMP, and Zn2+ at 2.0-Å resolution: aspects of synergism between inhibitors Proc. Natl. Acad. Sci. USA, 91, pp. 12482 - 12486.
  36. Kraft, L. and Sprenger, G. and Lindqvist, Y. (2002) Conformational changes during the catalytic cycle of gluconate kinase as revealed by X-ray crystallography J. Mol. Biol., 318, pp. 1057 - 1069.
  37. Rigden, D. and Littlejohn, J. and Henderson, K. and Jedrzejas, M. (2003) Structures of phosphate and trivanadate complexes of Bacillus stearothermophilus phosphatase PhoE: structural and functional analysis in the cofactor-dependent phosphoglycerate mutase superfamily J. Mol. Biol., 325, pp. 411 - 420.
Bibliographic reference Michels, Paulus ; Rigden, Daniel J. Evolutionary analysis of fructose 2,6-bisphosphate metabolism.. In: IUBMB life, Vol. 58, no. 3, p. 133-41 (2006)
Permanent URL http://hdl.handle.net/2078.1/10614