Kinetics and product analysis of the reaction catalysed by recombinant homoaconitase from Thermus thermophilus

Biochemical Journal

Volumn 396, Issue 3, 2006, Pages 479-485

  Jia, Yunhua ^a   Tomita, Takeo ^b   Yamauchi, Kazuma ^b   Nishiyama, Makoto ^b   Palmer, David R J ^a  

^a UNIVERSITY OF SASKATCHEWAN   (Canada)

^b UNIVERSITY OF TOKYO   (Japan)

Author keywords

aminoadipate pathway; cis homoaconitate; Homoaconitase (HACN); Homocitrate; Homoisocitrate; Thermus thermophilus

Indexed keywords

BACTERIA; BIOSYNTHESIS; CATALYSIS; CHEMICAL REACTIONS; DEHYDRATION; ENZYME INHIBITION; ESCHERICHIA COLI; FEEDBACK; FUNGI; HYDRATION; SUBSTRATES;

AMINOADIPATE PATHWAY; CIS-HOMOACONITATE; HOMOACONITASE (HACN); HOMOCITRATE; HOMOISOCITRATE; THERMUS THERMOPHILUS;

ENZYMES;

ACONITATE HYDRATASE; ACONITIC ACID; BACTERIAL ENZYME; CITRIC ACID; HOMOACONITASE; LYSINE; UNCLASSIFIED DRUG; HOMOACONITATE HYDRATASE; HOMOCITRIC ACID; HYDROLYASE; IRON SULFUR PROTEIN; RECOMBINANT PROTEIN; TRICARBOXYLIC ACID;

ARTICLE; CATALYSIS; CITRIC ACID CYCLE; ENZYME ACTIVITY; ESCHERICHIA COLI; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HYDRATION; KINETICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN STRUCTURE; THERMUS THERMOPHILUS; ANIMAL; DRUG ANTAGONISM; ENZYMOLOGY; HEART MUSCLE; METABOLISM; SWINE;

ESCHERICHIA COLI; FUNGI; THERMUS THERMOPHILUS;

ACONITATE HYDRATASE; ANIMALS; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; ESCHERICHIA COLI; HYDRO-LYASES; IRON-SULFUR PROTEINS; KINETICS; LYSINE; MYOCARDIUM; RECOMBINANT PROTEINS; SWINE; THERMUS THERMOPHILUS; TRICARBOXYLIC ACIDS;

EID: 33744992283     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20051711     Document Type: Article

References (44)

1. Weidner, G., Steffan, B. and Brakhage, A. A. (1997) The Aspergillus nidulans lysF gene encodes homoaconitase, an enzyme involved in the fungus-specific lysine biosynthesis pathway. Mol. Gen. Genet. 255, 237-247
2. Zabriskie, T. M. and Jackson, M. D. (2000) Lysine biosynthesis and metabolism in fungi. Natural Products Rep. 17, 85-97
3. Bhattacharjee, J. K. (1985) α-Aminoadipate pathway for the biosynthesis of lysine in lower eukaryotes. Crit. Rev. Microbiol. 12, 131-151
4. Born, T. L. and Blanchard, J. S. (1999) Structure/function studies on enzymes in the diaminopimelate pathway of bacterial cell wall biosynthesis. Curr. Opin. Chem. Biol. 3, 607-313
5. 13C-NMR study of acetate assimilation in Thermoproteus neutrophilus. Eur. J. Biochem. 186, 695-700
6. Kawarabayasi, Y., Hino, Y., Horikawa, H., Jin-no, K., Takahashi, M., Sekine, M., Baba, S., Ankai, A., Kosugi, H., Hosoyama, A. et al. (2001) Complete genome sequence of an aerobic thermoacidophilic crenarchaeon, Sulfolobus tokodaii strain 7. DNA Research 8, 123-140
7. She, Q., Singh, R. K., Confalonieri, F., Zivanovic, Y., Allard, G., Awayez, M. J., Chan-Weiher, C. C., Clausen, I. G., Curtis, B. A., De Moors, A. et al. (2001) The complete genome of the crenarchaeon Sulfolobus solfataricus P2. Proc. Natl. Acad. Sci. U.S.A. 98, 7835-7840
8. Kawarabayasi, Y., Hino, Y., Horikawa, H., Yamazaki, S., Haikawa, Y., Jin-no, K., Takahashi, M., Sekine, M., Baba, S., Ankai, A. et al. (1999) Complete genome sequence of an aerobic hyper-thermophilic crenarchaeon, Aeropyrum pernix K1. DNA Res. 6, 145-152
9. Cohen, G. N., Barbe, V., Flament, D., Galperin, M., Heiling, R., Lecompte, O., Poch, O., Prieur, D., Querellou, J., Ripp, R. et al. (2003) An integrated analysis of the genome of the hyperthermophilic archaeon Pyrococcus abyssi. Mol. Microbiol. 47, 1496-1512
10. Kawarabayasi, Y., Sawada, M., Horikawa, H., Haikawa, Y., Hino, Y., Yamamoto, S., Sekine, M., Baba, S., Kosugi, H., Hosoyama, A. et al. (1998) Complete sequence and gene organization of the genome of a hyperthermophilic archaeabacterium, Pyrococcus horikoshii OT3. DNA Res. 5, 55-76
11. Kosuge, T. and Hosbino, T. (1998) Lysine is synthesized through the α-aminoadipate pathway in Thermus thermophilus. FEMS Microbiol Lett. 169, 361-367
12. Kobashi, N., Nishiyama, M. and Tanokura, M. (1999) Aspartate kinase-independent lysine synthesis in an extremely thermophilic bacterium, Thermus thermophilus: lysine is synthesized via α-aminoadipic acid not via diaminopimelic acid. J. Bacteriol. 181, 1713-1718
13. Nishida, H., Nishiyama, M., Kobashi, N., Kosuge, T., Hoshino, T. and Yamane, H. (1999) A prokaryotic gene cluster involved in synthesis of lysine through the amino adipate pathway: a key to the evolution of amino acid biosynthesis. Genome Res. 9, 1175-1183
14. Miyazaki, J., Kobashi, N., Nishiyama, M. and Yamane, H. (2001) Functional and evolutionary relationship between arginine biosynthesis and prokaryotic lysine biosynthesis through α-aminoadipate. J. Bacteriol. 183, 5067-5073
15. Miyazaki, J., Kobashi, N., Fuji, T., Nishiyama, M. and Yamane, H. (2002) Characterization of a lysK gene as an argE homolog in Thermus thermophilus HB27. FEBS Lett. 512, 269-274
16. Sakai, H., Vassylyeva, M. N., Matsuura, T., Sekine, S., Gotoh, K., Nishiyama, M., Terada, T., Shirouzu, M., Kuramitsu, S., Vassylyev, D. G. and Yokoyama, S. (2003) Crystal structure of a lysine biosynthesis enzyme, LysX, from Thermus thermophilus HB8. J. Mol. Biol. 332, 729-740
17. Velasco, A. M., Leguina, J. I. and Lazcano, A. (2002) Molecular evolution of the lysine biosynthetic pathways. J. Mol. Evol. 50, 445-459
18. Hutton, C. A., Southwood, T. J. and Turner, J. J. (2003) Inhibitors of lysine biosynthesis as antibacterial agents. Mini Rev. Med. Chem. 3, 115-127
19. Suvama, K., Scab, L., Bhattacharjee, V. and Bhattacharjee, J. K. (1998) Molecular analysis of the LYS2 gene of Candida albicans: homology to peptide antibiotic synthetases and the regulation of the α-aminoadipate reductase. Curr. Genet. 33, 268-275
20. Palmer, D. R. J., Balogh, H., Ma, G., Zhou, X. and Kaminskyj, S. G. W. (2004) Synthesis and antifungal properties of compounds which target the α-aminoadipate pathway. Pharmazie 59, 93-98
21. Wulandari, A. P., Miyazaki, J., Kobashi, N., Nishiyama, M., Hoshino, T. and Yamane, H. (2002) Characterization of bacterial homocitrate synthase involved in lysine biosynthesis. FEBS Lett. 522, 35-40
22. Andi, B., West, A. H. and Cook, P. F. (2004) Kinetic mechanism of histidine-tagged homocitrate synthase from Saccharomyces cerevisiae. Biochemistry 43, 11790-11795
23. Strassman, M. and Ceci, L. N. (1966) Enzymatic formation of cis-homoaconitic acid, an intermediate in lysine biosynthesis in yeast. J. Biol. Chem. 241, 5401-5407
24. Bhattacharjee, J. K., Tucci, A. F. and Strassman, M. (1968) Accumulation of α-ketoglutarate in yeast mutants requiring lysine. Arch. Biochim. Biophys. 123, 235-239
25. Hall, L. T., Sanchez, R. J., Holloway, S. P., Zhu, H., Stine, J. E., Lyons, T. J., Demeler, B., Schirf, V., Hansen, J. C., Nersissian, A. M. et al. (2000) X-ray crystallographic and analytical ultracentrifugation analyses of truncated and full-length yeast copper chaperones for SOD (LYS7): a dimer-dimer model of LYS7-SOD association and copper delivery. Biochemistry 39, 3611-3623
26. Wallace, M. A., Liou, L. L., Martins, J., Clement, M. H., Bailey, S., Longo, V. D., Valentine, J. S. and Gralla, E. B. (2004) Superoxide inhibits 4Fe-4S cluster enzymes involved in amino acid biosynthesis. Cross-compartment protection by CuZn-superoxide dismutase. J. Biol. Chem. 279, 32055-32062
27. Irvin, S. D. and Bhattacharjee, J. K. (1998) A unique fungal lysine biosynthesis enzyme shares a common ancestor with tricarboxylic acid cycle and leucine biosynthetic enzymes found in diverse organisms. J. Mol. Evol. 46, 401-408
28. Beinert, H., Kennedy, M. C. and Stout, C. D. (1996) Aconitase as iron-sulfur protein, enzyme, and iron-regulatory protein. Chem. Rev. 96, 2335-2373
29. Lombo, T., Takaya, N., Miyazaki, J., Gotoh, K., Nishiyama, M., Kosuge, T., Nakamura, A. and Hoshino, T. (2004) Functional analysis of the small subunit of the putative homoaconitase from Pyrococcus horikoshii in the Thermus lysine biosynthetic pathway. FEMS Microbiol. Lett. 233, 315-324
30. Gerlt, J. A. and Babbitt, P. C. (2001) Divergent evolution of enzymatic function: mechanistically diverse superfamilies and functionally distinct suprafamilies. Annu. Rev. Biochem. 70, 209-246
31. The Kyoto Encyclopedia of Genes and Genomes (http://www.genome.ad.jp/ kegg/) states clearly that homoaconitase catalyses both steps. The ExPASy enzyme nomenclature database (http://www.expasy.org/enzyme/) suggests that the enzyme catalyses the first step only. BRENDA (http://www.brenda.uni-koeln.de/) indicates that the enzyme catalyses only the second step
32. Brock, M., Maerker, C., Schutz, A., Volker, U. and Buckel, W. (2002) Oxidation of propionate to pyruvate in Escherichia coli. Involvement of methylcitrate dehydratase and aconitase. Eur. J. Biochem. 269, 6184-6194
33. Howell, D. M., Harich, K., Xu, H. and White, R. H. (1998) A-keto acid chain elongation reactions involved in the biosynthesis of coenzyme B (7-mercaptoheptanoyl threonine phosphate) in methanogenic Archaea. Biochemistry 37, 10108-10117
34. Massoudi, H. H., Cantacuzene, D., Wakselman, C. and Delatour, C. B. (1983) Synthesis of cis-isomer and trans-isomer of homaconitic and fluorohomoaconitic acid. Synthesis 1983, 1010-1012
35. Ma, G. and Palmer, D. R. J. (2000) Improved asymmetric syntheses of (R)-(-)-homocitrate and (2R,3S)-(-)-homoisocitrate, intermediates in the α-aminoadipate pathway of fungi. Tetrahedron Lett. 41, 9209-9212
36. Jia, Y., Palmer, D. R. J. and Quail, W. J. (2005) The mono-(S)-α-methylbenzylammonium salt of (R)-homocitric lactone, Acta Cryst. E in the press
37. Miyazaki, J., Kobashi, N., Nishiyama, M. and Yamane, H. (2003) Characterization of homoisocitrate dehydrogenase involved in lysine biosynthesis of an extremely thermophilic bacterium, Thermus thermophilus HB27, and evolutionary implication of β-decarboxylating dehydrogenase. J. Biol. Chem. 278, 1864-1871
38. Sambrook, J., Fritsch, E. F. and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
39. Uhrigshardt, H., Walden, M., John, H. and Anemuller, S. (2001) Purification and characterization of the first archaeal aconitase from the thermoacidophilic Sulfolobus acidocaldarius. Eur. J. Biochem. 268, 1760-1771
40. Cornish-Bowden, A. (1995) Analysis of Enzyme Kinetic Data, Oxford University Press, New York
41. Cawthray, G. R. (2003) An improved reversed-phase liquid chromatographic method for the analysis of low-molecular mass organic acids in plant root exudates. J. Chromatogr. A 1011, 233-240
42. Morrison, J. F. (1954) The activation of aconitase by ferrous ions and reducing agents. Biochem. J. 56, 685-692
43. 2- of aconitase during cluster interconversions and removal. A convenient preparation of apoenzyme. J. Biol. Chem. 263, 8194-8198
44. Miyazaki, K. (2005) Bifunctional isocitrate-homoisocitrate dehydrogenase: a missing link in the evolution of β-decarboxylating dehydrogenase. Biochem. Biophys. Res. Commun. 331, 341-346