Cloning and functional characterization of an enzyme from Helicobacter pylori that catalyzes two steps of the methylerythritol phosphate pathway for isoprenoid biosynthesis

Biochimica et Biophysica Acta - General Subjects

Volumn 1800, Issue 9, 2010, Pages 919-928

  Pérez Gil, Jordi ^a   Bergua, María ^a   Boronat, Albert ^a   Imperial, Santiago ^a  

^a UNIVERSITY OF BARCELONA   (Spain)

Author keywords

2 C methyl d erythritol 2,4 cyclodiphosphatesynthase; 4 diphosphocytidyl 2 C methyl d erythritol synthase; Helicobacter pylori; Isoprenoid biosynthesis; Methylerythritol phosphate pathway

Indexed keywords

BACTERIAL ENZYME; ISOPRENOID; METHYLERYTHRITOL CYCLODIPHOSPHATE SYNTHASE; METHYLERYTHRITOL PHOSPHATE; UNCLASSIFIED DRUG; ANTIINFECTIVE AGENT; BACTERIAL PROTEIN; ENZYME INHIBITOR; ERYTHRITOL; LYASE; TERPENE;

AMINO ACID SEQUENCE; ARTICLE; BACTERIAL GENETICS; CATALYSIS; ENZYME ACTIVITY; ENZYME SYNTHESIS; ESCHERICHIA COLI; GENE LOCUS; GENETIC COMPLEMENTATION; HELICOBACTER PYLORI; IN VITRO STUDY; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN STRUCTURE; ANALOGS AND DERIVATIVES; ANTAGONISTS AND INHIBITORS; ANTIBIOTIC RESISTANCE; CHEMISTRY; DRUG DESIGN; DRUG EFFECTS; ENZYMOLOGY; GENETICS; HELICOBACTER INFECTIONS; METABOLISM;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; HELICOBACTER PYLORI;

ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; CLONING, MOLECULAR; DRUG DESIGN; DRUG RESISTANCE, BACTERIAL; ENZYME INHIBITORS; ERYTHRITOL; GENETIC COMPLEMENTATION TEST; HELICOBACTER INFECTIONS; HELICOBACTER PYLORI; PHOSPHORUS-OXYGEN LYASES; TERPENES;

EID: 77955280265     PISSN: 03044165     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbagen.2010.06.008     Document Type: Article

References (50)

1. Chappell J. The genetics and molecular genetics of terpene and sterol origami. Curr. Opin. Plant Biol. 2002, 5:151-157.
2. Sacchettini J.C., Poulter C.D. Creating isoprenoid diversity. Science 1997, 277:1788-1789.
3. Rohmer M., Knani M., Simonin P., Sutter B., Sahm H. Isoprenoid biosynthesis in bacteria: a novel pathway for the early steps leading to isopentenyl diphosphate. Biochem. J. 1993, 295:517-524.
4. Schwender J., Seemann M., Lichtenthaler H.K., Rohmer M. Biosynthesis of isoprenoids (carotenoids, sterols, prenyl side-chains of chlorophylls and plastoquinone) via a novel pyruvate/ glyceraldehyde 3-phosphate non-mevalonate pathway in the green alga Scenedesmus obliquus. Biochem. J. 1996, 316:73-80.
5. Arigoni D., Sagner S., Latzel C., Eisenreich W., Bacher A., Zenk M.H. Terpenoid biosynthesis from 1-deoxy-d-xylulose in higher plants by intramolecular skeletal rearrangement. Proc. Natl Acad. Sci. USA 1997, 94:10600-10605.
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. 2002, 130:1079-1089.
7. Sprenger G.A., Schörken U., Wiegert T., Grolle S., De Graaf A.A., Taylor S.V., Begley T.P., Bringer-Meyer S., Sahm H. Identification of a thiamin-dependent synthase in Escherichia coli required for the formation of the 1-deoxy-d-xylulose 5-phosphate precursor to isoprenoids, thiamin, and pyridoxol. Proc. Natl Acad. Sci. USA 1997, 94:12857-12862.
8. Lois L.M., Campos N., Putra S.R., 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, thiamin, and pyridoxol biosynthesis. Proc. Natl Acad. Sci. USA 1998, 95:2105-2110.
9. Xiang S., Usunow G., Lange G., Busch M., Tong L. Crystal structure of 1-deoxy-d-xylulose 5-phosphate synthase, a crucial enzyme for isoprenoids biosynthesis. J. Biol. Chem. 2007, 282:2676-2682.
10. Kuzuyama T., Takahashi S., Watanabe H., Seto H. Direct formation of 2-C-methyl-d-erythritol 4-phosphate from 1-deoxy-d-xylulose 5-phosphate by 1-deoxy-d-xylulose 5-phosphate reductoisomerase, a new enzyme in the non-mevalonate pathway to isopentenyl diphosphate. Tetrahedron Lett. 1998, 39:4509-4512.
11. 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 1998, 95:9879-9884.
12. Proteau P.J. 1-Deoxy-d-xylulose 5-phosphate reductoisomerase: an overview. Bioorg. Chem. 2004, 32:483-493.
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 1999, 96:11758-11763.
14. 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. 2001, 8:641-648.
15. Richard S.B., Lillo A.M., Tetzlaff C.N., Bowman M.E., Noel J.P., Cane D.E. Kinetic analysis of Escherichia coli 2-C-methyl-d-erythritol-4-phosphate cytidyltransferase, wild type and mutants, reveals roles of active site amino acids. Biochemistry 2004, 43:12189-12197.
16. 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-methylerythritol. Proc. Natl Acad. Sci. USA 2000, 97:1062-1067.
17. Miallau L., Alphey M.S., Kemp L.E., Leonard G.A., McSweeney S.M., Hecht S., Bacher A., Eisenreich W., Rohdich F., Hunter W.N. Biosynthesis of isoprenoids: crystal structure of 4-diphosphocytidyl-2C-methyl-d-erythritol kinase. Proc. Natl Acad. Sci. USA 2003, 100:9173-9178.
18. 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 1999, 97:2486-2490.
19. Rodríguez-Concepcion 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. 2000, 473:328-332.
20. Kollas A.K., Duin E.C., Eberl M., Altincicek B., Hintz M., Reichenberg A., Henschker D., Henne A., Steinbrecher I., Ostrovsky D.N., Hedderich R., Beck E., Jomaa H., Wiesner J. Functional characterization of GcpE, an essential enzyme of the non-mevalonate pathway of isoprenoid biosynthesis. FEBS Lett. 2002, 532:432-436.
21. Rohdich F., Zepeck F., Adam P., Hecht S., Kaiser J., Laupitz R., Gräwert T., Amslinger S., Eisenreich W., Bacher A., Arigoni D. The deoxyxylulose phosphate pathway of isoprenoid biosynthesis: studies on the mechanisms of the reactions catalyzed by IspG and IspH protein. Proc. Natl Acad. Sci. USA 2003, 100:1586-1591.
22. Rohdich F., Bacher A., Eisenreich W. Perspectives in anti-infective drug design. The late steps in the biosynthesis of the universal terpenoid precursors, isopentenyl diphosphate and dimethylallyl diphosphate. Bioorg. Chem. 2004, 32:292-308.
23. Rekittke I., Wiesner J., Röhrich R., Demmer U., Warkentin E., Xu W., Troschke K., Hintz M., No J.H., Duin E.C., Oldfield E., Jomaa H., Ermler U. Structure of (E)-4-Hydroxy-3-methyl-but-2-enyl diphosphate reductase, the terminal enzyme of the non-mevalonate pathway. J. Am. Chem. Soc. 2008, 130:17206-17207.
24. Testa C.A., Brown M.J. The methylerythritol phosphate pathway and its significance as a novel drug target. Curr. Pharm. Biotechnol. 2003, 4:248-259.
25. Jomaa H., Wiesner J., Sanderbrand S., Altincicek B., Weidemeyer C., Hintz M., Turbachova I., Eberl M., Zeidler J., Lichtenthaler H.K., Soldati D., Beck E. Inhibitors of the nonmevalonate pathway of isoprenoid biosynthesis as antimalarial drugs. Science 1999, 285:1573-1576.
26. Rodriguez-Concepcion M. The MEP pathway: a new target for the development of herbicides, antibiotics and antimalarial drugs. Curr. Pharm. Des. 2004, 10:2391-2400.
27. Eoh H., Brennan P.J., Crick D.C. The Mycobacterium tuberculosis MEP (2C-methyl-d-erythritol 4-phosphate) pathway as a new drug target. Tuberculosis 2009, 89:1-11.
28. Hahn F.M., Eubanks L.M., Testa C.A., Blagg B.S., Baker J.A., Poulter C.D. 1-Deoxy-d-xylulose 5-phosphate synthase, the gene product of open reading frame (ORF) 2816 and ORF 2895 in Rhodobacter capsulatus. J. Bacteriol. 2001, 183:1-11.
29. Cane D.E., Chow C., Lillo A., Kang I. Molecular cloning, expression and characterization of the first three genes in the mevalonate-independent isoprenoid pathway in Streptomyces coelicolor. Bioorg. Med. Chem. 2001, 9:1467-1477.
30. Gabrielsen M., Rohdich F., Eisenreich W., Gräwert T., Hecht S., Bacher A., Hunter W.N. Biosynthesis of isoprenoids: a bifunctional IspDF enzyme from Campylobacter jejuni. Eur. J. Biochem. 2004, 271:3028-3035.
31. Testa C.A., Lherbet C., Pojer F., Noel J.P., Poulter C.D. Cloning and expression of IspDF from Mesorhizobium loti. Characterization of a bifunctional protein that catalyzes non-consecutive steps in the methylerythritol phosphate pathway. Biochim. Biophys. Acta 2006, 1764:85-96.
32. Lherbet C., Pojer F., Richard S.B., Noel J.P., Poulter C.D. Absence of substrate channeling between active sites in the Agrobacterium tumefaciens IspDF and IspE enzymes of the methyl erythritol phosphate pathway. Biochemistry 2006, 45:3548-3553.
33. Vaira U., Gatta L., Ricci C., D'Anna L., Iglioli M.M. Helicobacter pylori: diseases, tests and treatment. Dig. Liver Dis. 2001, 33:788-794.
34. Bernal C., Palacin C., Boronat A., Imperial S. A colorimetric assay for the determination of 4-diphosphocytidyl-2-C-methyl-d-erythritol synthase activity. Anal. Biochem. 2005, 337:55-61.
35. Bernal C., Mendez E., Terencio J. A Boronat, S Imperial, A spectrophotometric assay for the determination of 4-diphosphocytidyl-2-C-methyl-d-erythritol kinase activity. Anal. Biochem. 2005, 340:245-251.
36. Sauret-Gueto S., Ramos-Valdivia A., Ibañez E., Boronat A., Rodriguez-Concepcion M. Identification of lethal mutations in Escherichia coli genes encoding enzymes of the methylerythritol phosphate pathway. Biochem. Biophys. Res. Commun. 2003, 307:408-415.
37. Sambrook J., Fritsch E.F., Maniatis T. Molecular cloning a laboratory manual 1989, Cold Spring Harbor, Cold Spring Harbor Laboratory. 2nd ed.
38. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72:248-254.
39. Campos N., Rodriguez-Concepcion M., Sauret-Gueto S., Gallego F., Lois L.M., Boronat A. Escherichia coli engineered to synthesize isopentenyl diphosphate and dimethylallyl diphosphate from mevalonate: a novel system for the genetic analysis of the 2-C-methyl-d-erythritol 4-phosphate pathway for isoprenoid biosynthesis. Biochem. J. 2001, 353:59-67.
40. Suerbaum S., Michetti P. Helicobacter pylori infection. N Engl J. Med. 2002, 347:1175-1186.
41. Tomb J.F., White O., Kerlavage A.R., Clayton R.A., Sutton G.G., Fleischmann R.D., Ketchum K.A., Klenk H.P., Gill S., Dougherty B.A., Nelson K., Quackenbush J., Zhou L., Kirkness E.F., Peterson S., Loftus B., Richardson D., Dodson R., Khalak H.G., Glodek A., McKenney K., Fitzegerald L.M., Lee N., Adams M.D., Hickey E.K., Berg D.E., Gocayne J.D., Utterback T.R., Peterson J.D., Kelley J.M., Cotton M.D., Weidman J.M., Fujii C., Bowman C., Watthey L., Wallin E., Hayes W.S., Borodovsky M., Karp P.D., Smith H.O., Fraser C.M., Venter J.C. The complete genome sequence of the gastric pathogen Helicobacter pylori. Nature 1997, 388:539-547.
42. Lee A. The Helicobacter pylori genome. New insights into pathogenesis and therapeutics. N Engl J. Med. 1998, 338:832-833.
43. Gabrielsen M., Bond C.S., Hallyburton I., Hecht S., Bacher A., Eisenreich W., Rohdich F., Hunter W.N. Hexameric assembly of the bifunctional methylerythritol 2, 4-cyclodiphosphate synthase and protein-protein associations in the deoxy-xylulose-dependent pathway of isoprenoid precursor biosynthesis. J. Biol. Chem. 2004, 279:52753-52761.
44. Obiol-Pardo C., Granadino-Roldán J.M., Rubio-Martinez J. Protein-protein recognition as a first step towards the inhibition of XIAP and survivin anti-apoptotic proteins. J. Mol. Recognit. 2008, 21:190-204.
45. Giménez-Oya V., Villacañas O., Fernàndez-Busquets X., Rubio-Martinez J., Imperial S. Mimicking direct protein-protein and solvent-mediated interactions in the CDP-methylerythritol kinase homodimer: a pharmacophore-directed virtual screening approach. J. Mol. Model. 2009, 15:997-1007.
46. Sauret-Gueto S., Urós E., Ibanez E., Boronat A., Rodriguez-Concepcion M. A mutant pyruvate dehydrogenase E1 subunit allows survival of Escherichia coli strains defective in 1-deoxy-d-xylulose 5-phosphate synthase. FEBS Lett. 2006, 580:736-740.
47. Campo S.M., Zullo A., Hassan C., Moroni S. Antibiotic treatment strategies for Helicobacter pylori infection. Recent Pat Anti-Infect. Drug Discov. 2007, 2:11-17.
48. Lazarou J., Pomeranz B.H., Corey P.N. Incidence of adverse drug reactions in hospitalized patients: a meta-analysis of prospective studies. JAMA 1998, 279:1200-1205.
49. El-Omar E.M. What is the optimal therapy for the eradication of Helicobacter pylori?. Nat. Clin. Pract. Gastroenterol. Hepatol. 2006, 3:126-127.
50. Dore M.P., Maragkoudakis E., Pironti A., Tadeu V., Tedde R., Realdi G., Delitala G. Twice-a-day quadruple therapy for eradication of Helicobacter pylori in the elderly. Helicobacter 2006, 11:52-55.