Identification of lethal mutations in Escherichia coli genes encoding enzymes of the methylerythritol phosphate pathway

Biochemical and Biophysical Research Communications

Volumn 307, Issue 2, 2003, Pages 408-415

  Sauret Güeto, Susanna ^a   Ramos Valdivia, Ana ^b   Ibáñez, Ester ^a   Boronat, Albert ^a   Rodríguez Concepción, Manuel ^a  

^a UNIVERSITY OF BARCELONA   (Spain)

^b DEPARTAMENTO DE FÍSICA   (Mexico)

Author keywords

EMS; Escherichia coli; Isoprenoids; Methylerythritol; Mevalonate; Mutagenesis

Indexed keywords

ENZYME; ISOPRENOID; MESYLIC ACID ETHYL ESTER; METHYLERYTHRITOL PHOSPHATE; PHOSPHORUS DERIVATIVE; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; CATALYSIS; DRUG MANUFACTURE; ESCHERICHIA COLI; GENE FUNCTION; GENE IDENTIFICATION; GENE MUTATION; GENETIC CODE; LETHAL MUTANT; MUTAGENESIS; NONHUMAN; OPERON; POINT MUTATION; PRIORITY JOURNAL; PROTEIN FUNCTION; SCREENING; SYNTHESIS;

ANIMALIA; BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 0037675908     PISSN: 0006291X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-291X(03)01211-7     Document Type: Article

References (44)

1. Chappell J. Biochemistry and molecular biology of the isoprenoid biosynthetic pathway in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 46:1995;521-547.
2. McGarvey D.J., Croteau R. Terpenoid metabolism. Plant Cell. 7:1995;1015-1026.
3. Lichtenthaler H.K. The 1-deoxy-D-xylulose 5-phosphate pathway of isoprenoid biosynthesis in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50:1999;47-65.
4. Rohmer R. The discovery of a mevalonate-independent pathway for isoprenoid biosynthesis in bacteria, algae and higher plants. Nat. Prod. Rep. 16:1999;565-574.
5. Eisenreich W., Rohdich F., Bacher A. Deoxyxylulose phosphate pathway to terpenoids. Trends Plant Sci. 6:2001;78-84.
6. Rodríguez-Concepción M., Boronat A. Elucidation of the methylerythritol phosphate pathway for isoprenoid biosynthesis in bacteria and plastids. A metabolic milestone achieved through genomics. Plant Physiol. 130:2002;1079-1089.
7. Kuemmerle H.P., Murakawa T., Sakamoto H., Sato N., Konishi T., De Santis F. Fosmidomycin, a new phosphonic acid antibiotic. Part II: 1. Human pharmacokinetics. 2. Preliminary early phase IIa clinical studies. Int. J. Clin. Pharmacol. Ther. Toxicol. 23:1985;521-528.
8. Jomaa H., Wiesner J., Sanderbrand S., Altincicek B., Weidemeyer K., Hintz M., Türbachova I., Eberl M., Zeidler J., Lichtenthaler H.K., Soldati D., Beck E. Inhibitors of the nonmevalonate pathway of isoprenoid biosynthesis as antimalarial drugs. Science. 285:1999;1573-1576.
9. Missinou M.A., Borrmann S., Schindler A., Issifou S., Adegnika A.A., Matsiegui P.B., Binder R., Lell B., Wiesner J., Baranek T., Jomaa H., Kremsner P.G. Fosmidomycin for malaria. Lancet. 360:2002;1941-1942.
10. Sprenger G.A., Schorken U., Wiegert T., Grolle S., de Graaf A.A., Taylor S.V., Begley T.P., Bringer-Meyer S., Sahm H. Identification of a thiamine-dependent synthase in Escherichia coli required for the formation of the 1-deoxy-D-xylulose 5-phosphate precursor to isoprenoids, thiamine, and pyridoxol. Proc. Natl. Acad. Sci. USA. 94:1997;12857-12862.
11. Lois L.M., Campos N., Rosa Putra S., Danielsen K., Rohmer M., Boronat A. Cloning and characterization of a gene from Escherichia coli encoding a transketolase-like enzyme that catalyzes the synthesis of D-1-deoxyxylulose 5-phosphate, a common precursor for isoprenoid, thiamine, and pyridoxol biosynthesis. Proc. Natl. Acad. Sci. USA. 95:1998;2105-2110.
12. Takahashi S., Kuzuyama T., Watanabe H., Seto H. A 1-deoxy-D-xylulose 5-phosphate reductoisomerase catalyzing the formation of 2-C-methyl-D-erythritol 4-phosphate in an alternative nonmevalonate pathway for terpenoid biosynthesis. Proc. Natl. Acad. Sci. USA. 95:1998;9879-9884.
13. Rohdich F., Wungsintaweekul J., Fellermeier M., Sagner S., Herz S., Kis K., Eisenreich W., Bacher A., Zenk M.H. Cytidine 5'-triphosphate-dependent biosynthesis of isoprenoids: YgbP protein of Escherichia coli catalyzes the formation of 4-diphosphocytidyl-2-C- methylerythritol. Proc. Natl. Acad. Sci. USA. 96:1999;11758-11763.
14. Herz S., Wungsintaweekul J., Schuhr C.A., Hecht S., Lüttgen H., Sagner S., Fellermeier M., Eisenreich W., Zenk M.H., Bacher A., Rohdich F. Biosynthesis of terpenoids: YgbB protein converts 4-diphosphocytidyl-2C-methyl-D-erythritol 2-phosphate to 2C-methyl-D-erythritol 2,4-cyclodiphosphate. Proc. Natl. Acad. Sci. USA. 97:2000;2486-2490.
15. Lüttgen H., Rohdich F., Herz S., Wungsintaweekul J., Hecht S., Schuhr C.A., Fellermeier M., Sagner S., Zenk M.H., Bacher A., Eisenreich W. Biosynthesis of terpenoids: YchB protein of Escherichia coli phosphorylates the 2-hydroxy group of 4-diphosphocytidyl-2-C-methyl-D-erythritol. Proc. Natl. Acad. Sci. USA. 97:2000;1062-1067.
16. Altincicek B., Kollas A.K., Eberl M., Wiesner J., Sanderbrand S., Hintz M., Beck M., Jomaa H. LytB, a novel gene of the 2-C-methyl-D-erythritol 4-phosphate pathway of isoprenoid biosynthesis in Escherichia coli. FEBS Lett. 499:2001;37-40.
17. Altincicek B., Kollas A.K., Sanderbrand S., Wiesner J., Hintz M., Beck E., Jomaa H. GcpE is involved in the 2-C-methyl-D-erythritol 4-phosphate pathway of isoprenoid biosynthesis in Escherichia coli. J. Bacteriol. 183:2001;2411-2416.
18. Hecht S., Eisenreich W., Adam P., Amslinger S., Kis K., Bacher A., Arigoni D., Rohdich F. Studies on the nonmevalonate pathway to terpenes: the role of the GcpE (IspG) protein. Proc. Natl. Acad. Sci. USA. 26:2001;14837-14842.
19. Rohdich F., Hecht S., Gärtner K., Adam P., Krieger C., Amslinger S., Arigoni D., Bacher A., Eisenreich W. Studies on the nonmevalonate terpene biosynthetic pathway: metabolic role of IspH (LytB) protein. Proc. Natl. Acad. Sci. USA. 99:2002;1158-1163.
20. Rodríguez-Concepción M., Campos N., Lois L.M., Maldonado C., Hoeffler J.F., Grosdemange-Billiard C., Rohmer M., Boronat A. Genetic evidence of branching in the isoprenoid pathway for the production of isopentenyl diphosphate and dimethylallyl diphosphate in Escherichia coli. FEBS Lett. 473:2000;328-332.
21. Kemp L.E., Bond C.S., Hunter W.N. Crystallization and preliminary X-ray diffraction studies of recombinant Escherichia coli 4-diphosphocytidyl-2-C-methyl-D-erythritol synthetase. Acta Crystallogr. D. 57:2001;1189-1191.
22. Kemp L.E., Bond C.S., Hunter W.N. Structure of 2C-methyl-D-erythritol 2,4-cyclodiphosphate synthase: an essential enzyme for isoprenoid biosynthesis and target for antimicrobial drug development. Proc. Natl. Acad. Sci. USA. 99:2002;6591-6596.
23. Reuter K., Sanderbrand S., Jomaa H., Wiesner J., Steinbrecher I., Beck E., Hintz M., Klebe G., Stubbs M.T. Crystal structure of 1-deoxy-D-xylulose-5-phosphate reductoisomerase, a crucial enzyme in the non-mevalonate pathway of isoprenoid biosynthesis. J. Biol. Chem. 277:2002;5378-5384.
24. Richard S.B., Bowman M.E., Kwiatkowski W., Kang I., Chow C., Lillo A.M., Cane D.E., Noel J.P. Structure of 4-diphosphocytidyl-2-C-methylerythritol synthetase involved in mevalonate- independent isoprenoid biosynthesis. Nat. Struct. Biol. 8:2001;641-648.
25. Richard S.B., Ferrer J.L., Bowman M.E., Lillo A.M., Tetzlaff C.N., Cane D.E., Noel J.P. Structure and mechanism of 2-C-methyl-D-erythritol 2,4-cyclodiphosphate synthase. An enzyme in the mevalonate-independent isoprenoid biosynthetic pathway. J. Biol. Chem. 277:2002;8667-8672.
26. Steinbacher S., Kaiser J., Wungsintaweekul J., Hecht S., Eisenreich W., Gerhardt S., Bacher A., Rohdich F. Structure of 2-C-methyl-D-erythritol-2,4-cyclodiphosphate synthase involved in mevalonate-independent biosynthesis of isoprenoids. J. Mol. Biol. 316:2002;79-88.
27. Yajima S., Nonaka T., Kuzuyama T., Seto H., Ohsawa K. Crystal structure of 1-deoxy-D-xylulose 5-phosphate reductoisomerase complexed with cofactors: implications of a flexible loop movement upon substrate binding. J. Biochem. 131:2002;313-317.
28. Seemann M., Tse Sum Bui B., Wolff M., Tritsch D., Campos N., Boronat A., Marquet A., Rohmer M. Isoprenoid biosynthesis through the methylerythritol phosphate pathway: the (E)-4-hydroxy-3-methylbut-2-enyl diphosphate synthase (GcpE) is a [4Fe-4S] protein. Angew. Chem. Int. Ed. 41:2002;4337-4339.
29. Wolff M., Seemann M., Tse Sum Bui B., Frapart Y., Tritsch D., García-Estrabot A., Rodríguez-Concepción M., Boronat A., Marquet A., Rohmer M. Isoprenoid biosynthesis via the methylerythritol phosphate pathway: the (E)-4-hydroxy-3-methylbut-2-enyl diphosphate reductase (LytB/IspH) from Escherichia coli is a [4Fe-4S] protein. FEBS Lett. 541:2003;115-120.
30. Campos N., Rodríguez-Concepción M., Sauret-Güeto S., Gallego F., Lois L.M., Boronat A. Escherichia coli engineered to synthesize isopentenyl diphosphate and dimethylallyl diphosphate from mevalonate: a novel system for genetic analysis of the 2-C-methyl-D-erythritol 4-phosphate pathway. Biochem. J. 353:2001;59-67.
31. Sambrook R., Fritsch E., Maniatis T. Molecular Cloning: A Laboratory Manual. Cold Spring Harbor. 1989;Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
32. Querol J., Rodríguez-Concepción M., Boronat A., Imperial S. Essential role of residue H49 for activity of Escherichia coli 1-deoxy-D-xylulose 5-phosphate synthase, the enzyme catalyzing the first step of the 2-C-methyl-D-erythritol 4-phosphate pathway for isoprenoid biosynthesis. Biochem. Biophys. Res. Commun. 289:2001;155-160.
33. Hoeffler J.F., Tritsch D., Grosdemange-Billiard C., Rohmer M. Isoprenoid biosynthesis via the methylerythritol phosphate pathway. Mechanistic investigations of the 1-deoxy-D-xylulose 5-phosphate reductoisomerase. Eur. J. Biochem. 269:2002;4446-4457.
34. Seemann M., Campos N., Rodríguez-Concepción M., Ibáñez E., Duvold T., Tritsch D., Boronat A., Rohmer M. Isoprenoid biosynthesis in Escherichia coli via the methylerythritol phosphate pathway: enzymatic conversion of methylerythritol cyclodiphosphate into a phosphorylated derivative of (E)-2-methylbut-2-ene-1,4-diol. Tetrahedron Lett. 43:2002;1413-1415.
35. Querol J., Campos N., Imperial S., Boronat A., Rodríguez-Concepción M. Functional analysis of the Arabidopsis thaliana GCPE protein involved in plastid isoprenoid biosynthesis. FEBS Lett. 514:2002;343-346.
36. Pienkowska M., Glickman B.W., Ferreira A., Anderson M., Zielenska M. Large-scale mutational analysis of EMS-induced mutation in the lacI gene of Escherichia coli. Mutat. Res. 288:1993;123-131.
37. Vidal A., Abril N., Pueyo C. DNA repair by Ogt alkyltransferase influences EMS mutational specificity. Carcinogenesis. 16:1995;817-821.
38. Schneider G., Lindqvist Y. Crystallography and mutagenesis of transketolase: mechanistic implications for enzymatic thiamine catalysis. Biochim. Biophys. Acta. 1385:1998;387-398.
39. Walter M.H., Hans J., Strack D. Two distantly related genes encoding 1-deoxy-D-xylulose 5-phosphate synthases: differential regulation in shoots and apocarotenoid-accumulating mycorrhizal roots. Plant J. 31:2002;243-254.
40. Wolff M., Seemann M., Grosdmange-Billiard C., Tritsch D., Campos N., Rodríguez-Concepción M., Boronat A., Rohmer M. Isoprenoid biosynthesis via the methylerythritol phosphate pathway. (E)-4-Hydroxy-3-methyl but-2-enyl diphosphate: chemical synthesis and formation from methylerythritol cyclodiphosphate by a cell-free system from Escherichia coli. Tetrahedron Lett. 43:2002;2555-2559.
41. Hintz M., Reichenberg A., Altincicek B., Bahr U., Gschwind R.M., Kollas A.K., Beck E., Wiesner J., Eberl M., Jomaa H. Identification of (E)-4-hydroxy-3-methyl-but-2-enyl pyrophosphate as a major activator for human. γδ T cells in Escherichia coli FEBS Lett. 509:2001;317-322.
42. Eberl M., Altincicek B., Kollas A.K., Sanderbrand S., Bahr U., Reichenberg A., Beck E., Foster D., Wiesner J., Hintz M., Jomaa H. Accumulation of a potent gammadelta T-cell stimulator after deletion of the lytB gene in Escherichia coli. Immunology. 106:2002;200-211.
43. Krall L., Raschke M., Zenk M., Baron C. The Tzs protein from Agrobacterium tumefaciens C58 produces zeatin riboside 5'-phosphate from 4-hydroxy-3-methyl-2-(E)-butenyl diphosphate and AMP. FEBS Lett. 527:2002;315-318.
44. Rodríguez-Concepción M., Ahumada I., Diez-Juez E., Sauret-Güeto S., Lois L.M., Gallego F., Carretero-Paulet L., Campos N., Boronat A. 1-Deoxy-D-xylulose 5-phosphate reductoisomerase and plastid isoprenoid biosynthesis during tomato fruit ripening. Plant J. 27:2001;213-222.