Inhibition of p-aminobenzoate and folate syntheses in plants and apicomplexan parasites by natural product rubreserine

Journal of Biological Chemistry

Volumn 287, Issue 26, 2012, Pages 22367-22376

  Camara, Djeneb ^a   Bisanz, Cordelia ^b   Barette, Caroline ^c   Van Daele, Jeroen ^d   Human, Esmare ^e   Barnard, Bernice ^e   Van Der Straeten, Dominique ^d   Stove, Christophe P ^d   Lambert, Willy E ^d   Douce, Roland ^a   Maréchal, Eric ^a   Birkholtz, Lyn Marie ^e   Cesbron Delauw, Marie France ^b   Dumas, Renaud ^a   Rébeillé, Fabrice ^a  

^a Laboratoire de Physiologie Cellulaire Vegetale Grenoble   (France)

^b CNRS   (France)

^c CEA GRENOBLE   (France)

^d GHENT UNIVERSITY   (Belgium)

^e UNIVERSITY OF PRETORIA   (South Africa)

Author keywords

[No Author keywords available]

Indexed keywords

APICOMPLEXAN PARASITES; ARABIDOPSIS; ARABIDOPSIS THALIANA; AUTOMATED SCREENING; BIFUNCTIONAL; BIFUNCTIONAL ENZYMES; CENTRAL COMPONENT; COFACTORS; DRUG TARGETS; EUKARYOTIC CELLS; EUKARYOTIC ORGANISMS; FOLATE CONTENT; GROWTH INHIBITION; HUMAN FIBROBLAST; INHIBITOR CONCENTRATION; NATURAL PRODUCTS; PLASMODIUM FALCIPARUM; SYNTHASES; TOXOPLASMA GONDII;

AMIDES; AMINO ACIDS; AUTOMATION; BIOSYNTHESIS; CELL CULTURE; SULFUR COMPOUNDS;

BIOCHEMISTRY;

4 AMINOBENZOIC ACID; FOLIC ACID; FOLIC ACID ANTAGONIST; FOLINIC ACID; GLUTAMINE AMIDOTRANSFERASE AMINODEOXYCHORISMATE SYNTHASE; RUBRESERINE; SULFONAMIDE; SYNTHETASE; UNCLASSIFIED DRUG;

APICOMPLEXA; ARABIDOPSIS; ARTICLE; BIOSYNTHESIS; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG MECHANISM; ENZYME INHIBITION; GROWTH INHIBITION; GROWTH RATE; HUMAN; HUMAN CELL; IC 50; NONHUMAN; PARASITE CONTROL; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; TOXOPLASMA GONDII;

4-AMINOBENZOIC ACID; ANIMALS; ANTIPARASITIC AGENTS; APICOMPLEXA; ARABIDOPSIS; DOSE-RESPONSE RELATIONSHIP, DRUG; ESCHERICHIA COLI; FOLIC ACID; INHIBITORY CONCENTRATION 50; KINETICS; MODELS, CHEMICAL; PHYSOSTIGMINE; PHYTOTHERAPY; PLANT EXTRACTS; PLASMODIUM FALCIPARUM; RECOMBINANT PROTEINS; TOXOPLASMA;

EID: 84862705768     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.365833     Document Type: Article

References (58)

1. Rébeillé, F., Ravanel, S., Jabrin, S., Douce, R., Storozhenko, S., and Van Der Straeten, D. (2006) Folates in plants. Biosynthesis, distribution, and enhancement. Physiol. Plant. 126, 330-342
2. Blancquaert, D., Storozhenko, S., Loizeau, K., De Steur, H., De Brouwer, V., Viaene, J., Ravanel, S., Rébeillé, F., Lambert, W., and Van Der Straeten, D. (2010) Folates and folic acid. From fundamental research toward sustainable health. Crit. Rev. Plant Sci. 29, 14-35
3. Ravanel, S., Douce, R., and Rébeillé, F. (2011) in Advances in Botanical Research (Rébeillé, F., and Douce, R., eds) Vol. 59, pp. 67-106, Elsevier, Amsterdam, The Netherlands
4. Storozhenko, S., De Brouwer, V., Volckaert, M., Navarrete, O., Blancquaert, D., Zhang, G. F., Lambert, W., and Van Der Straeten, D. (2007) Folate fortification of rice by metabolic engineering. Nat. Biotechnol. 25, 1277-1279
5. Díaz de la Garza, R. I., Gregory, J. F., 3rd, and Hanson, A. D. (2007) Folate biofortification of tomato fruit. Proc. Natl. Acad. Sci. U.S.A. 104, 4218-4222
6. Rébeillé, F., Alban, C., Bourguignon, J., Ravanel, S., and Douce, R. (2007) The role of plant mitochondria in the biosynthesis of coenzymes. Photosynth. Res. 92, 149-162
7. Bertino, J. R. (2009) Cancer research. From folate antagonism to molecular targets. Best Pract. Res. Clin. Haematol. 22, 577-582
8. Nzila, A. (2006) Inhibitors of de novo folate enzymes in Plasmodium falciparum. Drug Discov. Today 11, 939-944
9. Wang, P., Wang, Q., Aspinall, T. V., Sims, P. F., and Hyde, J. E. (2004) Transfection studies to explore essential folate metabolism and antifolate drug synergy in the human malaria parasite Plasmodium falciparum. Mol. Microbiol. 51, 1425-1438
10. Wang, P., Wang, Q., Yang, Y., Coward, J. K., Nzila, A., Sims, P. F., and Hyde, J. E. (2010) Characterization of the bifunctional dihydrofolate synthase- folylpolyglutamate synthase from Plasmodium falciparum; a potential novel target for antimalarial antifolate inhibition. Mol. Biochem. Parasitol. 172, 41-51
11. Nzila, A., Ward, S. A., Marsh, K., Sims, P. F., and Hyde, J. E. (2005) Comparative folate metabolism in humans and malaria parasites (part II). Activities as yet untargeted or specific to Plasmodium. Trends Parasitol. 21, 334-339
12. Rattanachuen, W., Jönsson, M., Swedberg, G., and Sirawaraporn, W. (2009) Probing the roles of nonhomologous insertions in the N-terminal domain of Plasmodium falciparum hydroxymethylpterin pyrophosphokinase- dihydropteroate synthase. Mol. Biochem. Parasitol. 168, 135-142
13. Hyde, J. E. (2005) Exploring the folate pathway in Plasmodium falciparum. Acta Trop. 94, 191-206
14. Salcedo-Sora, J. E., Ochong, E., Beveridge, S., Johnson, D., Nzila, A., Biagini, G. A., Stocks, P. A., O'Neill, P. M., Krishna, S., Bray, P. G., and Ward, S. A. (2011) The molecular basis of folate salvage in Plasmodium falciparum. Characterization of two folate transporters. J. Biol. Chem. 286, 44659-44668
15. Siehl, D. (1999) in Plant Amino Acids (Singh, B. K., ed) pp. 171-204, Marcel Dekker, Inc., New York
16. Roux, B., and Walsh, C. T. (1992) p-Aminobenzoate synthesis in Escherichia coli. Kinetic and mechanistic characterization of the amidotransferase PabA. Biochemistry 31, 6904-6910
17. Basset, G. J., Quinlivan, E. P., Ravanel, S., Rébeillé, F., Nichols, B. P., Shinozaki, K., Seki, M., Adams-Phillips, L. C., Giovannoni, J. J., Gregory, J. F., 3rd, and Hanson, A. D. (2004) Folate synthesis in plants. The p-aminobenzoate branch is initiated by a bifunctional PabA-PabB protein that is targeted to plastids. Proc. Natl. Acad. Sci. U.S.A. 101, 1496-1501
18. Zalkin, H. (1993) The amidotransferases. Adv. Enzymol. Relat. Areas Mol. Biol. 66, 203-309
19. Camara, D., Richefeu-Contesto, C., Gambonnet, B., Dumas, R., and Rébeillé, F. (2011) The synthesis of pABA. Coupling between the glutamine amidotransferase and aminodeoxychorismate synthase domains of the bifunctional aminodeoxychorismate synthase from Arabidopsis thaliana. Arch. Biochem. Biophys. 505, 83-90
20. Ziebart, K. T., and Toney, M. D. (2010) Nucleophile specificity in anthranilate synthase, aminodeoxychorismate synthase, isochorismate synthase, and salicylate synthase. Biochemistry 49, 2851-2859
21. Kerbarh, O., Bulloch, E. M., Payne, R. J., Sahr, T., Ré beillé, F., and Abell, C. (2005) Mechanistic and inhibition studies of chorismate-utilizing enzymes. Biochem. Soc. Trans. 33, 763-766
22. Bulloch, E. M., Jones, M. A., Parker, E. J., Osborne, A. P., Stephens, E., Davies, G. M., Coggins, J. R., and Abell, C. (2004) Identification of 4-amino- 4-deoxychorismate synthase as the molecular target for the antimicrobial action of (6S)-6-fluoroshikimate. J. Am. Chem. Soc. 126, 9912-9913
23. Kozlowski, M. C., Tom, N. J., Seto, C. T., Sefler, A. M., and Bartlett, P. A. (1995) Chorismate-utilizing enzymes isochorismate synthase, anthranilate synthase, and p-aminobenzoate synthase. Mechanistic insight through inhibitor design. J. Am. Chem. Soc. 117, 2128-2140
24. Payne, R. J., Bulloch, E. M., Toscano, M. M., Jones, M. A., Kerbarh, O., and Abell, C. (2009) Synthesis and evaluation of 2,5-dihydrochorismate analogues as inhibitors of the chorismate-utilizing enzymes. Org. Biomol. Chem. 7, 2421-2429
25. Payne, R. J., Bulloch, E. M., Kerbarh, O., and Abell, C. (2010) Inhibition of chorismate-utilizing enzymes by 2-amino-4-carboxypyridine and 4-carboxypyridone and 5-carboxypyridone analogues. Org. Biomol. Chem. 8, 3534-3542
26. Ziebart, K. T., Dixon, S. M., Avila, B., El-Badri, M. H., Guggenheim, K. G., Kurth, M. J., and Toney, M. D. (2010) Targeting multiple chorismateutilizing enzymes with a single inhibitor. Validation of a three-stage design. J. Med. Chem. 53, 3718-3729
27. Dixon, S., Ziebart, K. T., He, Z., Jeddeloh, M., Yoo, C. L., Wang, X., Lehman, A., Lam, K. S., Toney, M. D., and Kurth, M. J. (2006) Aminodeoxychorismate synthase inhibitors from one-bead one-compound combinatorial libraries. "Staged" inhibitor design. J. Med. Chem. 49, 7413-7426
28. Riedlinger, J., Reicke, A., Zähner, H., Krismer, B., Bull, A. T., Maldonado, L. A., Ward, A. C., Goodfellow, M., Bister, B., Bischoff, D., Süssmuth, R. D., and Fiedler, H. P. (2004) Abyssomicins, inhibitors of the para-aminobenzoic acid pathway produced by the marine Verrucosispora strain AB-18- 032. J. Antibiot. 57, 271-279
29. Keller, S., Schadt, H. S., Ortel, I., and Süssmuth, R. D. (2007) Action of atrop-abyssomicin C as an inhibitor of 4-amino-4-deoxychorismate synthase PabB. Angew. Chem. Int. Ed. Engl. 46, 8284-8286
30. Loizeau, K., De Brouwer, V., Gambonnet, B., Yu, A., Renou, J. P., Van Der Straeten, D., Lambert, W. E., Rébeillé, F., and Ravanel, S. (2008)Agenomewide and metabolic analysis determined the adaptive response of Arabidopsis cells to folate depletion induced by methotrexate. Plant Physiol. 148, 2083-2095
31. Bisanz, C., Bastien, O., Grando, D., Jouhet, J., Maréchal, E., and Cesbron- Delauw, M. F. (2006) Toxoplasma gondii acyl-lipid metabolism. De novo synthesis from apicoplast-generated fatty acids versus scavenging of host cell precursors. Biochem. J. 394, 197-205
32. Allen, R. J., and Kirk, K. (2010) Plasmodium falciparum culture. The benefits of shaking. Mol. Biochem. Parasitol. 169, 63-65
33. Bennett, T. N., Paguio, M., Gligorijevic, B., Seudieu, C., Kosar, A. D., Davidson, E., and Roepe, P. D. (2004) Novel, rapid, and inexpensive cell-based quantification of antimalarial drug efficacy. Antimicrob. Agents Chemother. 48, 1807-1810
34. Smilkstein, M., Sriwilaijaroen, N., Kelly, J. X., Wilairat, P., and Riscoe, M. (2004) Simple and inexpensive fluorescence-based technique for highthroughput antimalarial drug screening. Antimicrob. Agents Chemother. 48, 1803-1806
35. Zhang, J. H., Chung, T. D., and Oldenburg, K. R. (1999)Asimple statistical parameter for use in evaluation and validation of high throughput screening assays. J. Biomol. Screen. 4, 67-73
36. Zhang, G. F., Mortier, K. A., Storozhenko, S., Van De Steene, J., Van Der Straeten, D., and Lambert, W. E. (2005) Free and total para-aminobenzoic acid analysis in plants with high performance liquid chromatography/ tandem mass spectrometry. Rapid Commun. Mass Spectrom. 19, 963-969
37. De Brouwer, V., Zhang, G. F., Storozhenko, S., Straeten, D. V., and Lambert, W. E. (2007) pH stability of individual folates during critical sample preparation steps in prevision of the analysis of plant folates. Phytochem. Anal. 18, 496-508
38. De Brouwer, V., Storozhenko, S., Stove, C. P., Van Daele, J., Van der Straeten, D., and Lambert, W. E. (2010) Ultra-performance liquid chromatography- tandem mass spectrometry (UPLC-MS/MS) for the sensitive determination of folates in rice. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 878, 509-513
39. Sahr, T., Ravanel, S., Basset, G., Nichols, B. P., Hanson, A. D., and Rébeillé, F. (2006) Folate synthesis in plants. Purification, kinetic properties, and inhibition of aminodeoxychorismate synthase. Biochem. J. 396, 157-162
40. Poobrasert, O., Chai, H., Pezzuto, J. M., and Cordell, G. A. (1996) Cytotoxic degradation product of physostigmine. J. Nat. Prod. 59, 1087-1089
41. Yang, S. T., Wilken, L. O., and Clark, C. R. (1987) Liquid chromatographic determination of the pH-dependent degradation of eseroline. Hydrolysis product of physostigmine. J. Pharm. Biomed. Anal. 5, 383-393
42. Robinson, B. (1965) Structure of rubreserine. A decomposition product of physostigmine. J. Pharm. Pharmacol. 17, 89-91
43. Segel, I. H. (1975) Enzyme Kinetics, John Wiley & Sons, Inc., New York
44. Quinlivan, E. P., Roje, S., Basset, G., Shachar-Hill, Y., Gregory, J. F., 3rd, and Hanson, A. D. (2003) The folate precursor p-aminobenzoate is reversibly converted to its glucose ester in the plant cytosol. J. Biol. Chem. 278, 20731-20737
45. Eudes, A., Bozzo, G. G., Waller, J. C., Naponelli, V., Lim, E. K., Bowles, D. J., Gregory, J. F., 3rd, and Hanson, A. D. (2008) Metabolism of the folate precursor p-aminobenzoate in plants. Glucose ester formation and vacuolar storage. J. Biol. Chem. 283, 15451-15459
46. Orsomando, G., Bozzo, G. G., de la Garza, R. D., Basset, G. J., Quinlivan, E. P., Naponelli, V., Rébeillé, F., Ravanel, S., Gregory, J. F., 3rd, and Hanson, A. D. (2006) Evidence for folate-salvage reactions in plants. Plant J. 46, 426-435
47. Mosmann, T. (1983) Rapid colorimetric assay for cellular growth and survival. Application to proliferation and cytotoxicity assays. J. Immunol. Methods 65, 55-63
48. Massière, F., and Badet-Denisot, M. A. (1998) The mechanism of glutamine- dependent amidotransferases. Cell. Mol. Life Sci. 54, 205-222
49. Zhang, X. H., Brotherton, J. E., Widholm, J. M., and Portis, A. R. (2001) Targeting a nuclear anthranilate synthase α-subunit gene to the tobacco plastid genome results in enhanced tryptophan biosynthesis. Return of a gene to its pre-endosymbiotic origin. Plant Physiol. 127, 131-141
50. Nakamura, J., Straub, K., Wu, J., and Lou, L. (1995) The glutamine hydrolysis function of human GMP synthetase. Identification of an essential active-site cysteine. J. Biol. Chem. 270, 23450-23455
51. Sibley, L. D., Messina, M., and Niesman, I. R. (1994) Stable DNA transformation in the obligate intracellular parasite Toxoplasma gondii by complementation of tryptophan auxotrophy. Proc. Natl. Acad. Sci. U.S.A. 91, 5508-5512
52. Roberts, C. W., Roberts, F., Lyons, R. E., Kirisits, M. J., Mui, E. J., Finnerty, J., Johnson, J. J., Ferguson, D. J., Coggins, J. R., Krell, T., Coombs, G. H., Milhous, W. K., Kyle, D. E., Tzipori, S., Barnwell, J., Dame, J. B., Carlton, J., and McLeod, R. (2002) The shikimate pathway and its branches in apicomplexan parasites. J. Infect. Dis. 185, S25-S36
53. Bhat, J. Y., Shastri, B. G., and Balaram, H. (2008) Kinetic and biochemical characterization of Plasmodium falciparum GMP synthetase. Biochem. J. 409, 263-273
54. Schröder, M., Giermann, N., and Zrenner, R. (2005) Functional analysis of the pyrimidine de novo synthesis pathway in solanaceous species. Plant Physiol. 138, 1926-1938
55. Fox, B. A., and Bzik, D. J. (2002) De novo pyrimidine biosynthesis is required for virulence of Toxoplasma gondii. Nature 415, 926-929
56. Ellis, S., Krayer, O., and Plachte, F. L. (1943) Studies on physostigmine and related substances. III. Breakdown products of physostigmine; their inhibitory effect on cholinesterase and their pharmacological action. Pharmacol. Exp. Ther. 79, 309-319
57. Kaur, K., Jain, M., Kaur, T., and Jain, R. (2009) Antimalarials from nature. Bioorg. Med. Chem. 17, 3229-3256
58. Meneceur, P., Bouldouyre, M. A., Aubert, D., Villena, I., Menotti, J., Sauvage, V., Garin, J. F., and Derouin, F. (2008) In vitro susceptibility of various genotypic strains of Toxoplasma gondii to pyrimethamine, sulfadiazine, and atovaquone. Antimicrob. Agents Chemother. 52, 1269-1277