Amino acid biosynthesis: New architectures in allosteric enzymes

Plant Physiology and Biochemistry

Volumn 46, Issue 3, 2008, Pages 325-339

  Curien, Gilles ^a   Biou, Valérie ^b   Mas Droux, Corine ^a   Robert Genthon, Mylène ^a   Ferrer, Jean Luc ^c   Dumas, Renaud ^a  

^a CNRS   (France)

^b LABORATOIRE D ENZYMOLOGIE ET BIOCHIMIE STRUCTURALES   (France)

^c INSTITUT DE BIOLOGIE STRUCTURALE   (France)

Author keywords

Acetohydroxyacid synthase; ACT domain; Allosteric control; Allostery; Amino acid; Aspartate kinase; Dihydrodipicolinate synthase; Enzyme; Homoserine dehydrogenase; Isopropylmalate synthase; Metabolism; Plant structural biology; S adenosylmethionine; Threonine deaminase; Threonine synthase

Indexed keywords

BACTERIA (MICROORGANISMS); FUNGI;

EID: 40849135894     PISSN: 09819428     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.plaphy.2007.12.006     Document Type: Review

References (91)

1. Aravind L., and Koonin E.V. Gleaning non-trivial structural, functional and evolutionary information about proteins by iterative database searches. J. Mol. Biol. 287 (1999) 1023-1040
2. Arevalo-Rodriguez M., Calderon I.L., and Holmberg S. Mutations that cause threonine sensitivity identify catalytic and regulatory regions of the aspartate kinase of Saccharomyces cerevisiae. Yeast 15 (1999) 1331-1345
3. Barak Z., Chipman D.M., and Gollop N. Physiological implications of the specificity of acetohydroxy acid synthase isozymes of enteric bacteria. J. Bacteriol 169 (1987) 3750-3756
4. Barber E.D., and Bright H.J. The rate of an allosteric process: inhibition of homoserine dehydrogenase I from E. coli by threonine. Proc. Natl. Acad. Sci. U.S.A. 60 (1968) 1363-1370
5. Blickling S., Beisel H.G., Bozic D., Knablein J., Laber B., and Huber R. Structure of dihydrodipicolinate synthase of Nicotiana sylvestris reveals novel quaternary structure. J. Mol. Biol. 274 (1997) 608-621
6. Blickling S., Renner C., Laber B., Pohlenz H.D., Holak T.A., and Huber R. Reaction mechanism of Escherichia coli dihydrodipicolinate synthase investigated by X-ray crystallography and NMR spectroscopy. Biochemistry 36 (1997) 24-33
7. Brush A., and Paulus H. The enzymic formation of O-acetylhomoserine in Bacillus subtilis and its regulation by methionine and S-adenosylmethionine. Biochem. Biophys. Res. Commun 45 (1971) 735-741
8. Calhoun D.H., Rimerman R.A., and Hatfield G.W. Threonine deaminase from Escherichia coli. I. Purification and properties. J. Biol. Chem. 248 (1973) 3511-3516
9. Chang A.K., and Duggleby R.G. Expression, purification and characterization of Arabidopsis thaliana acetohydroxyacid synthase. Biochem. J. 327 Pt 1 (1997) 161-169
10. Craciun A., Jacobs M., and Vauterin M. Arabidopsis loss-of-function mutant in the lysine pathway points out complex regulation mechanisms. FEBS Lett. 487 (2000) 234-238
11. Curien G., Dumas R., Ravanel S., and Douce R. Characterization of an Arabidopsis thaliana cDNA encoding an S-adenosylmethionine-sensitive threonine synthase. Threonine synthase from higher plants. FEBS Lett. 390 (1996) 85-90
12. Curien G., Job D., Douce R., and Dumas R. Allosteric activation of Arabidopsis threonine synthase by S-adenosylmethionine. Biochemistry 37 (1998) 13212-13221
13. Curien G., Laurencin M., Robert-Genthon M., and Dumas R. Allosteric monofunctional aspartate kinases from Arabidopsis. FEBS J 274 (2007) 164-176
14. Curien G., Ravanel S., and Dumas R. A kinetic model of the branch-point between the methionine and threonine biosynthesis pathways in Arabidopsis thaliana. Eur. J. Biochem. 270 (2003) 4615-4627
15. Curien G., Ravanel S., Robert M., and Dumas R. Identification of six novel Allosteric effectors of Arabidopsis thaliana Aspartate kinase-Homoserine dehydrogenase isoforms: Physiological context sets the specificity. J. Biol. Chem. 280 (2005) 41178-41183
16. Datko A.H., Giovanelli J., and Mudd S.H. Homocysteine biosynthesis in green plants. O-Phosphorylhomoserine as the physiological substrate for cystathionine gamma-synthase. J. Biol. Chem. 249 (1974) 1139-1155
17. Datta P. Purification and feedback control of threonine deaminase activity of Rhodopseudomonas spheroides. J. Biol. Chem. 241 (1966) 5836-5844
18. Datta P. Regulation of homoserine biosynthesis by L-cysteine, a terminal metabolite of a linked pathway. Proc. Natl. Acad. Sci. U.S.A. 58 (1967) 635-641
19. Datta P., and Gest H. Control of enzyme activity by concerted feedback inhibition. Proc. Natl. Acad. Sci. U.S.A. 52 (1964) 1004-1009
20. de Carvalho L.P.S., and Blanchard J.S. Kinetic and chemical mechanism of alpha-isopropylmalate synthase from Mycobacterium tuberculosis. Biochemistry 45 (2006) 8988-8999
21. de Kraker J.W., Luck K., Textor S., Tokuhisa J.G., and Gershenzon J. Two Arabidopsis genes (IPMS1 and IPMS2) encode isopropylmalate synthase, the branch-point step in the biosynthesis of leucine. Plant Physiol 143 (2007) 970-986
22. DeLaBarre B., Thompson P.R., Wright G.D., and Berghuis A.M. Crystal structures of homoserine dehydrogenase suggest a novel catalytic mechanism for oxidoreductases. Nat. Struct. Biol. 7 (2000) 238-244
23. Dereppe C., Bold G., Ghisalba O., Ebert E., and Schar H.P. Purification and characterization of dihydrodipicolinate synthase from pea. Plant Physiol 98 (1992) 813-821
24. Dobson R.C., Devenish S.R., Turner L.A., Clifford V.R., Pearce F.G., Jameson G.B., and Gerrard J.A. Role of arginine 138 in the catalysis and regulation of Escherichia coli dihydrodipicolinate synthase. Biochemistry 44 (2005) 13007-13013
25. Dobson R.C.J., Griffin M.D.W., Jameson G.B., and Gerrard J.A. The crystal structures of native and (S)-lysine-bound dihydrodipicolinate synthase from Escherichia coli with improved resolution show new features of biological significance. Acta Crystallogr. D 61 (2005) 1116-1124
26. Faehnle C.R., Liu X.Y., Pavlovsky A., and Viola R.E. The initial step in the archaeal aspartate biosynthetic pathway catalyzed by a monofunctional aspartokinase. Acta Crystallogr. F 62 (2006) 962-966
27. Frisch D.A., Gengenbach B.G., Tommey A.M., Sellner J.M., Somers D.A., and Myers D.E. Isolation and characterization of dihydrodipicolinate synthase from Maize. Plant Physiol. 96 (1991) 444-452
28. Gallagher D.T., Gilliland G.L., Xiao G., Zondlo J., Fisher K.E., Chinchilla D., and Eisenstein E. Structure and control of pyridoxal phosphate dependent allosteric threonine deaminase. Structure 6 (1998) 465-475
29. Garrido-Franco M., Ehlert S., Messerschmidt A., Marinkovic S., Huber R., Laber B., Bourenkov G.P., and Clausen T. Structure and function of threonine synthase from yeast. J. Biol. Chem. 277 (2002) 12396-12405
30. Gil-Ortiz F., Ramon-Maiques S., Fita I., and Rubio V. The course of phosphorus in the reaction of N-acetyl-L-glutamate kinase, determined from the structures of crystalline complexes, including a complex with an AlF(4)(-) transition state mimic. J. Mol. Biol. 331 (2003) 231-244
31. Grant G.A. The ACT domain: a small molecule binding domain and its role as a common regulatory element. J. Biol. Chem. 281 (2006) 33825-33829
32. Graves L.M., and Switzer R.L. Aspartokinase III, a new isozyme in Bacillus subtilis 168. J. Bacteriol. 172 (1990) 218-223
33. Hagelstein P., and Schultz G. Leucine synthesis in spinach chloroplasts: partial characterization of 2-isopropylmalate synthase. Biol. Chem. Hoppe-Seyler 374 (1993) 1105-1108
34. Halling S.M., and Stahly D.P. Dihydrodipicolinic acid synthase of Bacillus licheniformis. Quaternary structure, kinetics, and stability in the presence of sodium chloride and substrates. Biochim. Biophys. Acta 452 (1976) 580-596
35. Hill C.M., Pang S.S., and Duggleby R.G. Purification of Escherichia coli acetohydroxyacid synthase isoenzyme II and reconstitution of active enzyme from its individual pure subunits. Biochem. J. 327 Pt 3 (1997) 891-898
36. Kalinowski J., Cremer J., Bachmann B., Eggeling L., Sahm H., and Puhler A. Genetic and Biochemical-Analysis of the Aspartokinase from Corynebacterium glutamicum. Mol. Microbiol. 5 (1991) 1197-1204
37. Kaplun A., Vyazmensky M., Zherdev Y., Belenky I., Slutzker A., Mendel S., Barak Z., Chipman D.M., and Shaanan B. Structure of the regulatory subunit of acetohydroxyacid synthase isozyme III from Escherichia coli. J. Mol. Biol. 357 (2006) 951-963
38. Karsten W.E. Dihydrodipicolinate synthase from Escherichia coli: pH dependent changes in the kinetic mechanism and kinetic mechanism of allosteric inhibition by L-lysine. Biochemistry 36 (1997) 1730-1739
39. Kerr D.S., and Flavin M. The regulation of methionine synthesis and the nature of cystathionine gamma-synthase in Neurospora. J. Biol. Chem. 245 (1970) 1842-1855
40. Kobashi N., Nishiyama M., and Tanokura M. Aspartate kinase-independent lysine synthesis in an extremely thermophilic bacterium, Thermus thermophilus: Lysine is synthesized via alpha-aminoadipic acid not via diaminopimelic acid. J. Bacteriol. 181 (1999) 1713-1718
41. Kohlhaw G., Leary T.R., and Umbarger H.E. Alpha-isopropylmalate synthase from Salmonella typhimurium. Purification and properties. J. Biol. Chem. 244 (1969) 2218-2225
42. Koon N., Squire C.J., and Baker E.N. Crystal structure of LeuA from Mycobacterium tuberculosis, a key enzyme in leucine biosynthesis. Proc. Natl. Acad. Sci. U.S.A. 101 (2004) 8295-8300
43. Kotaka M., Ren J., Lockyer M., Hawkins A.R., and Stammers D.K. Structures of R- and T-state Escherichia coli aspartokinase III: Mechanisms of the allosteric transition and inhibition by lysine. J. Biol. Chem. (2006)
44. Kumpaisal R., Hashimoto T., and Yamada Y. Purification and characterization of dihydrodipicolinate synthase from wheat suspension cultures. Plant Physiol. 85 (1987) 145-151
45. Laber B., Gomis-Ruth F.X., Romao M.J., and Huber R. Escherichia coli dihydrodipicolinate synthase. Identification of the active site and crystallization. Biochem. J. 288 (1992) 691-695
46. Laber B., Maurer W., Hanke C., Grafe S., Ehlert S., Messerschmidt A., and Clausen T. Characterization of recombinant Arabidopsis thaliana threonine synthase. Eur. J. Biochem. 263 (1999) 212-221
47. Lee L.W., Ravel J.M., and Shive W. Multimetabolite control of a biosynthetic pathway by sequential metabolites. J. Biol. Chem. 241 (1966) 5479-5480
48. Lee Y.T., and Duggleby R.G. Identification of the regulatory subunit of Arabidopsis thaliana acetohydroxyacid synthase and reconstitution with its catalytic subunit. Biochemistry 40 (2001) 6836-6844
49. Lee Y.T., and Duggleby R.G. Regulatory interactions in Arabidopsis thaliana acetohydroxyacid synthase. FEBS Lett. 512 (2002) 180-184
50. Loizeau K., Gambonnet B., Zhang G.-F., Curien G., Jabrin S., Van Der Straeten D., Lambert W.E., Rébeillé F., and Ravanel S. Regulation of One-carbon metabolism in Arabidopsis: The N-terminal regulatory domain of cystathionine gamma-synthase is cleaved in response to folate starvation. Plant Physiol. 145 (2007) 491-503
51. Marco-Marin C., Ramon-Maiques S., Tavarez S., and Rubio V. Site-directed mutagenesis of Escherichia coli acetylglutamate kinase and aspartokinase III probes the catalytic and substrate-binding mechanisms of these amino acid kinase family enzymes and allows three-dimensional modelling of aspartokinase. J. Mol. Biol. 334 (2003) 459-476
52. Mas-Droux C., Biou V., and Dumas R. Allosteric threonine synthase. Reorganization of the pyridoxal phosphate site upon asymmetric activation through S-adenosylmethionine binding to a novel site. J. Biol. Chem. 281 (2006) 5188-5196
53. Mas-Droux C., Curien G., Robert-Genthon M., Laurencin M., Ferrer J.L., and Dumas R. A novel organization of ACT domains in allosteric enzymes revealed by the crystal structure of Arabidopsis Aspartate kinase. Plant Cell 18 (2006) 1681-1692
54. McCourt J.A., and Duggleby R.G. Acetohydroxyacid synthase and its role in the biosynthetic pathway for branched-chain amino acids. Amino Acids 31 (2006) 173-210
55. McCourt J.A., and Duggleby R.G. How an enzyme answers multiple-choice questions. Trends Biochem. Sci. 30 (2005) 222-225
56. Mirwaldt C., Korndorfer I., and Huber R. The crystal structure of dihydrodipicolinate synthase from Escherichia coli at 2.5 A resolution. J. Mol. Biol. 246 (1995) 227-239
57. Mirza I.A., Nazi I., Korczynska M., Wright G.D., and Berghuis A.M. Crystal structure of homoserine transacetylase from Haemophilus influenzae reveals a new family of alpha/beta-hydrolases. Biochemistry 44 (2005) 15768-15773
58. Miyajima R., and Shiio I. Regulation of aspartate family amino acid biosynthesis in Brevibacterium flavum. VII. Properties of homoserine O-transacetylase. J. Biochem. 73 (1973) 1061-1068
59. Monod J., Changeux J.P., and Jacob M. Allosteric protein and cellular control. J. Mol. Biol. 6 (1963) 306-329
60. Nagai S., and Kerr D. Homoserine transacetylase (Neurospora). Methods Enzymol. vol. XVIIB (1971) 442-445
61. Omi R., Goto M., Miyahara I., Mizuguchi H., Hayashi H., Kagamiyama H., and Hirotsu K. Crystal structures of threonine synthase from Thermus thermophilus HB8: conformational change, substrate recognition, and mechanism. J. Biol. Chem. 278 (2003) 46035-46045
62. Paris S., Viemon C., Curien G., and Dumas R. Mechanism of control of Arabidopsis thaliana aspartate kinase-homoserine dehydrogenase by threonine. J. Biol. Chem. 278 (2003) 5361-5366
63. Parsot C., and Cohen G.N. Cloning and nucleotide sequence of the Bacillus subtilis hom gene coding for homoserine dehydrogenase. Structural and evolutionary relationships with Escherichia coli aspartokinases-homoserine dehydrogenases I and II. J. Biol. Chem. 263 (1988) 14654-14660
64. Patte J.C., and Cohen G.N. Intéractions coopératives effecteur-effecteur chez deux enzymes allostériques inhibées de manière non compétitive. C.R. Acad. Sci. 259 (1964) 1255-1258
65. Patte J.C., Le Bras G., Loviny T., and Cohen G.N. Rétro-inhibition et répression de l'homosérine déshydrogénase d'Escherichia coli. Biochim. Biophys. Acta 67 (1963) 16-30
66. Patte J.C., Le Bras G., and Cohen G.N. Regulation by methionine of the synthesis of a third aspartokinase and of a second homoserine dehydrogenase in Escherichia coli K 12. Biochim. Biophys. Acta 136 (1967) 245-247
67. Powell J.F. Isolation of dipicolinic acid (pyridine-2:6-dicarboxylic acid) from spores of Bacillus megatherium. Biochem. J. 54 (1953) 210-211
68. Ramon-Maiques S., Marina A., Gil-Ortiz F., Fita I., and Rubio V. Structure of acetylglutamate kinase, a key enzyme for arginine biosynthesis and a prototype for the amino acid kinase enzyme family, during catalysis. Structure 10 (2002) 329-342
69. Ramon-Maiques S., Marina A., Uriarte M., Fita I., and Rubio V. The 1.5 A resolution crystal structure of the carbamate kinase-like carbamoyl phosphate synthetase from the hyperthermophilic Archaeon Pyrococcus furiosus, bound to ADP, confirms that this thermostable enzyme is a carbamate kinase, and provides insight into substrate binding and stability in carbamate kinases. J. Mol. Biol. 299 (2000) 463-476
70. Richaud C., Mazat J.P., Felenbok B., and Patte J.C. The role of lysine and leucine binding on the catalytical and structural properties of aspartokinase III of Escherichia coli K 12. Eur. J. Biochem. 48 (1974) 147-156
71. Robichon-Szulmajster H., and Cherest H. Regulation of homoserine O-transacetylase, first step in methionine biosynthesis in Saccharomyces cerevisiae. Biochem. Biophys. Res. Commun. 28 (1967) 256-262
72. Rosner A., and Paulus H. Regulation of aspartokinase in Bacillus subtilis. The separation and properties of two isofunctional enzymes. J. Biol. Chem. 246 (1971) 2965-2971
73. Schuller D.J., Grant G.A., and Banaszak L.J. The allosteric ligand site in the Vmax-type cooperative enzyme phosphoglycerate dehydrogenase. Nat. Struct. Biol. 2 (1995) 69-76
74. Selhub J., Savin M.A., Sakami W., and Flavin M. Synchronization of converging metabolic pathways: activation of the Cystathionine gamma-synthase of Neurospora crassa by methyltetrahydrofolate. Proc. Natl. Acad. Sci. U.S.A. 68 (1971) 312-314
75. Sharma R.J., and Mazumder R. Purification, properties, and feedback control of L-threonine dehydratase from spinach. J. Biol. Chem. 245 (1970) 3008-3014
76. Shiio I., and Miyajima R. Concerted inhibition and its reversal by end products of aspartate kinase in Brevibacterium flavum. J. Biochem 65 (1969) 849-859
77. Soper T.S., Doellgast J., and Kohlhaw G.B. Mechanism of feedback inhibition by leucine. Purification and properties of a feedback-resistant alpha-isopropylmalate synthase. Arch. Biochem. Biophys. 173 (1976) 362-374
78. Teng-Leary E., and Kohlhaw G.B. Binding of alpha-ketoisovalerate to alpha-isopropylmalate synthase. Half-of-the-sites and all-of-the-sites availability. Biochim. Biophys. Acta 410 (1975) 210-219
79. Thomazeau K., Curien G., Dumas R., and Biou V. Crystal structure of threonine synthase from Arabidopsis thaliana. Protein Sci. 10 (2001) 638-648
80. Umbarger H.E. Evidence for a negative-feedback mechanism in the biosynthesis of isoleucine. Science 123 (1956) 848
81. Vauterin M., Frankard V., and Jacobs M. Functional rescue of a bacterial dapA auxotroph with a plant cDNA library selects for mutant clones encoding a feedback-insensitive dihydrodipicolinate synthase. Plant J. 21 (2000) 239-248
82. Vauterin M., and Jacobs M. Isolation of a poplar and an Arabidopsis thaliana dihydrodipicolinate synthase cDNA clone. Plant Mol. Biol. 25 (1994) 545-550
83. Vyazmensky M., Sella C., Barak Z., and Chipman D.M. Isolation and characterization of subunits of acetohydroxy acid synthase isozyme III and reconstitution of the holoenzyme. Biochemistry 35 (1996) 10339-10346
84. Weinstock O., Sella C., Chipman D.M., and Barak Z. Properties of subcloned subunits of bacterial acetohydroxy acid synthases. J. Bacteriol. 174 (1992) 5560-5566
85. Wessel P.M., Graciet E., Douce R., and Dumas R. Evidence for two distinct effector-binding sites in threonine deaminase by site-directed mutagenesis, kinetic, and binding experiments. Biochemistry 39 (2000) 15136-15143
86. Wyman A., and Paulus H. Purification and properties of homoserine transacetylase from Bacillus polymyxa. J. Biol. Chem. 250 (1975) 3897-3903
87. Yamagata S. Partial purification and some properties of homoserine O-acetyltransferase of a methionine auxotroph of Saccharomyces cerevisiae. J. Bacteriol. 169 (1987) 3458-3463
88. Yamakura F., Ikeda Y., Kimura K., and Sasakawa T. Partial purification and some properties of pyruvate-aspartic semialdehyde condensing enzyme from sporulating Bacillus subtilis. J. Biochem. 76 (1974) 611-621
89. Yoshida A., Tomita T., Kurihara T., Fushinobu S., Kuzuyama T., and Nishiyama M. Structural Insight into concerted inhibition of alpha 2 beta 2-type aspartate kinase from Corynebacterium glutamicum. J. Mol. Biol. 368 (2007) 521-536
90. Zabriskie T.M., and Jackson M.D. Lysine biosynthesis and metabolism in fungi. Natural Product Reports 17 (2000) 85-97
91. Zubieta C., Krishna S.S., McMullan D., Miller M.D., Abdubek P., Agarwalla S., Ambing E., Astakhova T., Axelrod H.L., Carlton D., Chiu H.J., Clayton T., Deller M., DiDonato M., Duan L., Elsliger M.A., Grzechnik S.K., Hale J., Hampton E., Han G.W., Haugen J., Jaroszewski L., Jin K.K., Klock H.E., Knuth M.W., Koesema E., Kumar A., Marciano D., Morse A.T., Nigoghossian E., Oommachen S., Reyes R., Rife C.L., van den Bedem H., Weekes D., White A., Xu Q., Hodgson K.O., Wooley J., Deacon A.M., Godzik A., Lesley S.A., and Wilson I.A. Crystal structure of homoserine O-succinyltransferase from Bacillus cereus at 2.4 A resolution. Proteins 68 (2007) 999-1005