The antioxidative effect of de novo generated vitamin B 6 in Plasmodium falciparum validated by protein interference

Biochemical Journal

Volumn 443, Issue 2, 2012, Pages 397-405

  Knöckel, Julia ^a,c   Müller, Ingrid B ^a   Butzloff, Sabine ^a   Bergmann, Bärbel ^a   Walter, Rolf D ^a   Wrenger, Carsten ^a,b  

^a BERNHARD NOCHT INSTITUTE FOR TROPICAL MEDICINE   (Germany)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

^c NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

Antioxidant; Malaria; Oxidative stress; Plasmodium falciparum; Singlet molecular oxygen; Vitamin B 6

Indexed keywords

ANTIOXIDANT; HEMOGLOBIN; OXYGEN; PYRIDOXAL 5 PHOSPHATE; REACTIVE OXYGEN METABOLITE;

ANTIOXIDANT ACTIVITY; ARTICLE; CONTROLLED STUDY; DETOXIFICATION; DIGESTION; ENZYME SYNTHESIS; FLUORESCENCE MICROSCOPY; GENETIC ANALYSIS; GENETIC TRANSCRIPTION; HUMAN; IN VIVO STUDY; NONHUMAN; NUCLEOTIDE SEQUENCE; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN METABOLISM; TRANSGENIC ORGANISM; VALIDATION PROCESS; WILD TYPE;

MOLECULAR SEQUENCE DATA; NITROGENOUS GROUP TRANSFERASES; OXIDATIVE STRESS; PERYLENE; PLASMODIUM FALCIPARUM; PROTOZOAN PROTEINS; UP-REGULATION; VITAMIN B 6;

PLASMODIUM FALCIPARUM;

EID: 84859464651     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20111542     Document Type: Article

References (50)

1. Percudani, R. and Peracchi, A. (2003) A genomic overview of pyridoxal-phosphate-dependent enzymes. EMBO Rep. 4, 850-854
2. Amadasi, A., Bertoldi, M., Contestabile, R., Bettati, S., Cellini, B., di Salvo, M. L., Borri-Voltattorni, C., Bossa, F. and Mozzarelli, A. (2007) Pyridoxal 5′-phosphate enzymes astargets for therapeutic agents. Curr. Med. Chem. 14, 1291-1324
3. Ehrenshaft, M., Bilski, P., Li, M. Y., Chignell, C. F. and Daub, M. E. (1999) A highly conserved sequence is a novel gene involved in de novo vitamin B6 biosynthesis. Proc. Natl. Acad. Sci. U.S.A. 96, 9374-9378 (Pubitemid 29374762)
4. Knöckel, J., Müller, I. B., Bergmann, B., Walter, R. D. and Wrenger, C. (2007) The apicomplexan parasite Toxoplasma gondii generates pyridoxal phosphate de novo. Mol. Biochem. Parasitol. 152, 108-111 (Pubitemid 46107705)
5. 6 biosynthesis in higher plants. Proc. Natl. Acad. Sci. U.S.A. 102, 13687-13692
6. 6 biosynthesis pathway in the human malaria parasite Plasmodium falciparum. J. Biol. Chem. 280, 5242-5248
7. 6biosynthesis isessential for survival and virulence of Mycobacterium tuberculosis. Mol. Microbiol. 78, 980-988
8. Müller, I. B., Knöckel, J., Groves, M. R., Jordanova, R., Ealick, S. E., Walter, R. D. and Wrenger, C. (2008) The assembly of the plasmodial PLP synthase complex follows a defined course. PLoS ONE 3, e1815
9. Zein, F., Zhang, Y., Kang, Y. N., Burns, K., Begley, T. P. and Ealick, S. E. (2006) Structural insights into the mechanism of the PLP synthase holoenzyme from Thermotoga maritima . Biochemistry 45, 14609-14620 (Pubitemid 44906977)
10. Stocker, P., Lesgards, J. F., Vidal, N., Chalier, F. and Prost, M. (2003) ESR study of a biological assay on whole blood: antioxidant efficiency of various vitamins. Biochim. Biophys. Acta 1621, 1-8 (Pubitemid 36349691)
11. Ehrenshaft, M., Chung, K. R., Jenns, A. E. and Daub, M. E. (1999) Functional characterization of SOR1, a gene required for resistance to photosensitizing toxins in the fungus Cercospora nicotianae. Curr. Genet. 34, 478-485 (Pubitemid 29057386)
12. Matxain, J. M., Ristilä, M., Strid, A. and Eriksson, L. A. (2006) Theoretical study of the antioxidant properties of pyridoxine. J. Phys. Chem. A 110, 13068-13072 (Pubitemid 46065638)
13. Ohta, B. K. and Foote, C. S. (2002) Characterization of endoperoxide and hydroperoxide intermediates in the reaction of pyridoxine with singlet oxygen. J. Am. Chem. Soc. 124, 12064-12065 (Pubitemid 35154852)
14. + -dependent isocitrate dehydrogenase. Mol. Cell. Biochem. 302, 27-34
15. Guzik, T. J., Korbut, R. and Adamek-Guzik, T. (2003) Nitric oxide and superoxide in inflammation and immune regulation. J. Physiol. Pharmacol. 54, 469-487 (Pubitemid 38029745)
16. Becker, K., Rahlfs, S., Nickel, C. and Schirmer, R. H. (2003) Glutathione: functions and metabolism in the malarial parasite Plasmodium falciparum. Biol. Chem. 384, 551-566 (Pubitemid 36609171)
17. Lew, V. L., Macdonald, L., Ginsburg, H., Krugliak, M. and Tiffert, T. (2004) Excess haemoglobin digestion by malaria parasites: a strategy to prevent premature host cell lysis. Blood Cells Mol. Dis. 32, 353-359 (Pubitemid 38581853)
18. Papalexis, V., Siomos, M. A., Campanale, N., Guo, X., Kocak, G., Foley, M. and Tilley, L. (2001) Histidine-rich protein 2of the malaria parasite, Plasmodium falciparum, is involved in detoxification of the by-products of haemoglobin degradation. Mol. Biochem. Parasitol. 115, 77-86 (Pubitemid 32493855)
19. Khan, A. U. and Kasha, M. (1994) Singlet molecular oxygen in the Haber-Weiss reaction. Proc. Natl. Acad. Sci. U.S.A. 91, 12365-12367
20. Naqui, A., Chance, B. and Cadenas, E. (1986) Reactive oxygen intermediates inbiochemistry. Annu. Rev. Biochem. 55, 137-166
21. Müller, S. (2004) Redox and antioxidant systems of the malaria parasite Plasmodium falciparum. Mol. Microbiol. 53, 1291-1305
22. Wang, X. and Quinn, P. J. (1999) Vitamin Eand its function in membranes. Prog. Lipid Res. 38, 309-336 (Pubitemid 29408248)
23. Daub, M. E., Herrero, S. and Chung, K. R. (2005) Photoactivated perylenequinone toxins infungal pathogenesis of plants. FEMS Microbiol. Lett. 252, 197-206 (Pubitemid 41531644)
24. Price, M., Reiners, J. J., Santiago, A. M. and Kessel, D. (2009) Monitoring singlet oxygen and hydroxyl radical formation with fluorescent probes during photodynamic therapy. Photochem. Photobiol. 85, 1177-1181
25. Trager, W. and Jensen, J. B. (1976) Human malaria parasites incontinuous culture. Science 193, 673-675
26. Das Gupta, R., Krause-Ihle, T., Bergmann, B., Müller, I. B., Khomutov, A. R., Müller, S., Walter, R. D. and Luersen, K. (2005) 3-Aminooxy-1-aminopropane and derivatives have an antiproliferative effect on cultured Plasmodium falciparum by decreasing intracellular polyamine concentrations. Antimicrob. Agents Chemother. 49, 2857-2864 (Pubitemid 40917603)
27. Crabb, B. S., Rug, M., Gilberger, T. W., Thompson, J. K., Triglia, T., Maier, A. G. and Cowman, A. F. (2004) Transfection of the human malaria parasite Plasmodium falciparum. Methods Mol. Biol. 270, 263-276
28. Knöckel, J., Bergmann, B., Müller, I. B., Rathaur, S., Walter, R. D. and Wrenger, C. (2008) Filling the gap of intracellular dephosphorylation in the Plasmodium falciparum vitamin B1 biosynthesis. Mol. Biochem. Parasitol. 157, 241-243
29. Müller, I. B., Knockel, J., Eschbach, M. L., Bergmann, B., Walter, R. D. and Wrenger, C. (2010) Secretion of an acid phosphatase provides a possible mechanism to acquire host nutrients by Plasmodium falciparum. Cell. Microbiol. 12, 677-691
30. Müller, I. B., Wu, F., Bergmann, B., Knockel, J., Walter, R. D., Gehring, H. and Wrenger, C. (2009) Poisoning pyridoxal 5-phosphate-dependent enzymes: a new strategy to target the malaria parasite Plasmodium falciparum. PLoS ONE 4, e4406
31. Saliba, K. J., Horner, H. A. and Kirk, K. (1998) Transport and metabolism of the essential vitamin pantothenic acid in human erythrocytes infected with the malaria parasite Plasmodium falciparum. J. Biol. Chem. 273, 10190-10195 (Pubitemid 28227619)
32. Eschbach, M. L., Müller, I. B., Gilberger, T. W., Walter, R. D. and Wrenger, C. (2006) The human malaria parasite Plasmodium falciparum expresses an atypical N-terminally extended pyrophosphokinase with specificity for thiamine. Biol. Chem. 387, 1583-1591 (Pubitemid 44837583)
33. Daub, M. E., Jenns, A. E. and Ehrenshaft, M. (1995) Fungal resistance tophotosensitizers that generate singlet oxygen. ACS Symp. Ser. 616, 201-216
34. Dobrowolski, D. C. and Foote, C. S. (1983) Cercosporin, asinglet oxygen generator. Angew. Chem. Int. Ed. Engl. 22, 720-721
35. Daub, M. E. and Hangarter, R. P. (1983) Light-induced production of singlet oxygen and superoxide by the fungal toxin, cercosporin. Plant Physiol. 73, 855-857
36. Daub, M. E. (1982) Peroxidation of tobacco membrane lipids by the photosensitizing toxin, cercosporin. Plant Physiol. 69, 1361-1364
37. Hughes, K. W., Negrotto, D., Daub, M. E. and Meeusen, R. L. (1984) Free-radical stress response inparaquat-sensitive and resistant tobacco plants. Environ. Exp. Bot. 24, 151-157
38. Setsukinai, K., Urano, Y., Kakinuma, K., Majima, H. J. and Nagano, T. (2003) Development of novel fluorescence probes that can reliably detect reactive oxygen species and distinguish specific species. J. Biol. Chem. 278, 3170-3175 (Pubitemid 36801227)
39. 2. Chemistry 13, 4636-4642
40. Egan, T. J. (2002) Physico-chemical aspects of hemozoin (malaria pigment) structure and formation. J. Inorg. Biochem. 91, 19-26
41. Goldberg, D. E. (1992) Plasmodial hemoglobin degradation: anordered pathway in a specialized organelle. Infect. Agents Dis. 1, 207-211
42. Becker, K., Tilley, L., Vennerstrom, J. L., Roberts, D., Rogerson, S. and Ginsburg, H. (2004) Oxidative stress inmalaria parasite-infected erythrocytes: host-parasite interactions. Int. J. Parasitol. 34, 163-189 (Pubitemid 38229822)
43. Di Mascio, P., Devasagayam, T. P., Kaiser, S. and Sies, H. (1990) Carotenoids, tocopherols and thiols as biological singlet molecular oxygen quenchers. Biochem. Soc. Trans. 18, 1054-1056
44. Bozdech, Z., Llinas, M., Pulliam, B. L., Wong, E. D., Zhu, J. and DeRisi, J. L. (2003) The transcriptome of the intraerythrocytic developmental cycle of Plasmodium falciparum. PLoS Biol. 1, e5
45. 6 biosynthesis in tobacco and fungi uncovers limitations to up-regulation of the pathway. Plant Sci. 172, 609-620
46. Graham, C. M., Ehrenshaft, M., Hausner, G. and Reid, D. M. (2004) A highly conserved gene for vitamin B biosynthesis may have consequences for stress and hormone responses in plants. Physiol. Plant. 121, 8-14
47. 6 biosynthesis that is up-regulated by oxidative stress in the arbuscular mycorrhizal fungus Glomus intraradices. New Phytol. 184, 682-693
48. 6 deficient plants display increased sensitivity to high light and photo-oxidative stress. BMC Plant Biol. 9, 130
49. 6 biosynthesis by the malaria parasite Plasmodium falciparum: biochemical and structural insights. J. Biol. Chem. 281, 3633-3641
50. Barillas-Mury, C. and Kumar, S. (2005) Plasmodium-mosquito interactions: atale of dangerous liaisons. Cell. Microbiol. 7, 1539-1545 (Pubitemid 41511911)