The bacterial redox signaller pyocyanin as an antiplasmodial agent: comparisons with its thioanalog methylene blue

References

• Dietrich LE, Teal TK, Price-Whelan A, Newman DK. Redox-active antibiotics control gene expression and community behavior in divergent bacteria. Science 2008;321:1203–6.
   PubMed Web of Science ®Google Scholar
• Gibson J, Sood A, Hogan DA. Pseudomonas aeruginosa–Candida albicans interactions: localization and fungal toxicity of a phenazine derivative. Appl Environ Microbiol 2009;75:504–13.
   PubMed Web of Science ®Google Scholar
• Lau GW, Hassett DJ, Ran H, Kong F. The role of pyocyanin in Pseudomonas aeruginosa infection. Trends Mol Med 2004;10:599–606.
   PubMed Web of Science ®Google Scholar
• Mentel M, Ahuja EG, Mavrodi DV, Breinbauer R, Thomashow LS, Blankenfeldt W. Of two make one: the biosynthesis of phenazines. Chembiochem 2009;10:2295–304.
   PubMed Web of Science ®Google Scholar
• Wilson R, Sykes DA, Watson D, Rutman A, Taylor GW, Cole PJ. Measurement of Pseudomonas aeruginosa phenazine pigments in sputum and assessment of their contribution to sputum sol toxicity for respiratory epithelium. Infect Immun 1988;56:2515–7.
   PubMed Web of Science ®Google Scholar
• O'Malley YQ, Reszka KJ, Spitz DR, Denning GM, Britigan BE. Pseudomonas aeruginosa pyocyanin directly oxidizes glutathione and decreases its levels in airway epithelial cells. Am J Physiol Lung Cell Mol Physiol 2004;287:L94–103.
   PubMed Web of Science ®Google Scholar
• Muller M. Pyocyanin induces oxidative stress in human endothelial cells and modulates the glutathione redox cycle. Free Radic Biol Med 2002;33:1527–33.
   PubMed Web of Science ®Google Scholar
• Ran H, Hassett DJ, Lau GW. Human targets of Pseudomonas aeruginosa pyocyanin. Proc Natl Acad Sci USA 2003;100:14315–20.
   PubMed Web of Science ®Google Scholar
• Cheluvappa R, Shimmon R, Dawson M, Hilmer SN, Le Couteur DG. Reactions of Pseudomonas aeruginosa pyocyanin with reduced glutathione. Acta Biochim Pol 2008;55:571–80.
   PubMed Web of Science ®Google Scholar
• Mahajan-Miklos S, Tan MW, Rahme LG, Ausubel FM. Molecular mechanisms of bacterial virulence elucidated using a Pseudomonas aeruginosa-Caenorhabditis elegans pathogenesis model. Cell 1999;96:47–56.
   PubMed Web of Science ®Google Scholar
• Baron SS, Rowe JJ. Antibiotic action of pyocyanin. Antimicrob Agents Chemother 1981;20:814–20.
   PubMed Web of Science ®Google Scholar
• Lau GW, Goumnerov BC, Walendziewicz CL, Hewitson J, Xiao W, Mahajan-Miklos S, et al. The Drosophila melanogaster toll pathway participates in resistance to infection by the gram-negative human pathogen Pseudomonas aeruginosa. Infect Immun 2003;71:4059–66.
   PubMed Web of Science ®Google Scholar
• Rahme LG, Ausubel FM, Cao H, Drenkard E, Goumnerov BC, Lau GW, et al. Plants and animals share functionally common bacterial virulence factors. P Natl Acad Sci USA 2000;97:8815–21.
   PubMed Web of Science ®Google Scholar
• Cao H, Baldini RL, Rahme LG. Common mechanisms for pathogens of plants and animals. Annu Rev Phytopathol 2001;39:259–84.
   PubMed Web of Science ®Google Scholar
• Liu GY, Nizet V. Color me bad: microbial pigments as virulence factors. Trends Microbiol 2009;17:406–13.
   PubMed Web of Science ®Google Scholar
• Guttmann P, Ehrlich P. Über die Wirkung des Methylenblau bei Malaria. Berlin Klin Woch 1891;28:953–6.
   Google Scholar
• Akoachere M, Buchholz K, Fischer E, Burhenne J, Haefeli WE, Schimer RH, et al. In vitro assessment of methylene blue on chloroquine-sensitive and -resistant Plasmodium falciparum strains reveals synergistic action with artemisinins. Antimicrob Agents Chemother 2005;49:4592–7.
   PubMed Web of Science ®Google Scholar
• Blumenstiel K, Schoneck R, Yardley V, Croft SL, Krauth-Siegel RL. Nitrofuran drugs as common subversive substrates of Trypanosoma cruzi lipoamide dehydrogenase and trypanothione reductase. Biochem Pharmacol 1999;58:1791–9.
   PubMed Web of Science ®Google Scholar
• Buchholz K, Schirmer RH, Eubel JK, Akoachere MB, Dandekar T, Becker K, et al. Interactions of methylene blue with human disulfide reductases and their orthologues from Plasmodium falciparum. Antimicrob Agents Chemother 2008;52:183–91.
   PubMed Web of Science ®Google Scholar
• Meissner P, Adler H, Kasozi D, Fritz-Wolf K, Schirmer RH. The reducing milieu of parasitized cells as a target of antimalarial agents: methylene blue as an ethical drug. In: , Becker K. (ed.) Apicomplexan parasites – molecular approaches toward targeted drug development. Drug discovery in infectious diseases (vol. 2). Weinheim: Wiley-VCH; 2011. p. 115–36.
   Google Scholar
• Massey V. The identity of diaphorase and lipoyl dehydrogenase. Biochim Biophys Acta 1960;15:314–22.
   Google Scholar
• Schirmer H. Essay on the medical history of methylene blue [posted 2009 Jul 30]. Available from: http://www.alzforum.org/new/Schirmer.asp.
   Google Scholar
• Campbell ZT, Baldwin TO. Fre is the major flavin reductase supporting bioluminescence from Vibrio harveyi luciferase in Escherichia coli. J Biol Chem 2009;284:8322–8.
   PubMed Web of Science ®Google Scholar
• Baron SS, Terranova G, Rowe JJ. Molecular mechanism of the antimicrobial action of pyocyanin. Curr Microbiol 1989;18:223–30.
   Web of Science ®Google Scholar
• Schirmer RH, Adler H, Zappe HA, Gromer S, Becker K, Coulibaly B, et al. Disulfide reductases as drug targets: methylene blue combination therapies for falciparum malaria in African children. Zaragoza: Prensas Universitarias de Zaragoza; 2008. See http://bzh.db-engine.de/default.asp?lfn=2387.
   Google Scholar
• Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, et al. USCF Chimera – a visualization system for exploratory research and analysis. J Comput Chem 2004;25:1605–12.
   PubMed Web of Science ®Google Scholar
• Färber PM, Arscott LD, Williams CH, Becker K, Schirmer RH. Recombinant Plasmodium falciparum glutathione reductase is inhibited by the antimalarial dye methylene blue. FEBS Lett 1998;422:311–4.
   PubMed Web of Science ®Google Scholar
• Krauth-Siegel RL, Bauer H, Schirmer RH. Dithiol proteins as guardians of the intracellular redox milieu in parasites: old and new drug targets in trypanosomes and malaria-causing plasmodia. Angew Chem Int Ed Engl 2005;44:690–715.
   PubMed Web of Science ®Google Scholar
• Cornish-Bowden A. A simple graphical method for determining the inhibition constants of mixed, uncompetitive and non-competitive inhibitors. Biochem J 1974;137:143–4.
   PubMed Web of Science ®Google Scholar
• Berkholz DS, Faber HR, Savvides SN, Karplus PA. Catalytic cycle of human glutathione reductase near 1 A resolution. J Mol Biol 2008;382:371–84.
   PubMed Web of Science ®Google Scholar
• Savvides SN, Karplus PA. Kinetics and crystallographic analysis of human glutathione reductase in complex with a xanthene inhibitor. J Biol Chem 1996;271:8101–7.
   PubMed Web of Science ®Google Scholar
• Biot C, Bauer H, Schirmer RH, Davioud-Charvet E. 5-substituted tetrazoles as bioisosteres of carboxylic acids. Bioisosterism and mechanistic studies on glutathione reductase inhibitors as antimalarials. J Med Chem 2004;47:5972–83.
   PubMed Web of Science ®Google Scholar
• Vennerstrom JL, Makler MT, Angerhofer CK, Williams JA. Antimalarial dyes revisited: xanthenes, azines, oxazines, and thiazines. Antimicrob Agents Chemother 1995;39:2671–7.
   PubMed Web of Science ®Google Scholar
• Sturm N, Hu Y, Zimmermann H, Fritz-Wolf K, Wittlin S, Rahlfs S, et al. Compounds structurally related to ellagic acid show improved antiplasmodial activity. Antimicrob Agents Chemother 2009;53:622–30.
   PubMed Web of Science ®Google Scholar
• Peters W. Chemotherapy and drug resistance in malaria, vol. 1. London: Academic Press; 1987. p. 542.
   Google Scholar
• Mendis K, Rietveld A, Warsame M, Bosman A, Greenwood B, Wernsdorfer WH. From malaria control to eradication: The WHO perspective. Trop Med Int Health 2009;14:802–9.
   PubMed Web of Science ®Google Scholar
• Coulibaly B, Zoungrana A, Mockenhaupt FP, Schirmer RH, Klose C, Mansmann U, et al. Strong gametocytocidal effect of methylene blue-based combination therapy against falciparum malaria: a randomised controlled trial. PLoS One 2009;4:e5318.
   PubMed Web of Science ®Google Scholar
• White NJ. The role of anti-malarial drugs in eliminating malaria. Malar J 2008;7(Suppl 1):S8.
   PubMed Web of Science ®Google Scholar
• Mavrodi DV, Bonsall RF, Delaney SM, Soule MJ, Phillips G, Thomashow LS. Functional analysis of genes for biosynthesis of pyocyanin and phenazine-1-carboxamide from Pseudomonas aeruginosa PAO1. J Bacteriol 2001;183:6454–65.
   PubMed Web of Science ®Google Scholar
• Gallagher LA, McKnight SL, Kuznetsova MS, Pesci EC, Manoil C. Functions required for extracellular quinolone signaling by Pseudomonas aeruginosa. J Bacteriol 2002;184:6472–80.
   PubMed Web of Science ®Google Scholar
• Winstanley C, Fothergill JL. The role of quorum sensing in chronic cystic fibrosis Pseudomonas aeruginosa infections. FEMS Microbiol Lett 2009;290:1–9.
   PubMed Web of Science ®Google Scholar
• Fuqua C, Parsek MR, Greenberg EP. Regulation of gene expression by cell-to-cell communication: acyl-homoserine lactone quorum sensing. Annu Rev Genet 2001;35:439–68.
   PubMed Web of Science ®Google Scholar
• Price-Whelan A, Dietrich LE, Newman DK. Pyocyanin alters redox homeostasis and carbon flux through central metabolic pathways in Pseudomonas aeruginosa PA14. J Bacteriol 2007;189:6372–81.
   PubMed Web of Science ®Google Scholar
• Kantz A, Chin F, Nallamothu N, Nguyen T, Gassner GT. Mechanism of flavin transfer and oxygen activation by the two-component flavoenzyme styrene monooxygenase. Arch Biochem Biophys 2005;442:102–16.
   PubMed Web of Science ®Google Scholar
• McMillan PJ, Stimmler LM, Foth BJ, McFadden GI, Müller S. The human malaria parasite Plasmodium falciparum possesses two distinct dihydrolipoamide dehydrogenases. Mol Microbiol 2005;55:27–38.
   PubMed Web of Science ®Google Scholar
• Smalley ME. Plasmodium falciparum gametocytes: The effect of chloroquine on their development. Trans R Soc Trop Med Hyg 1977;71:526–9.
   PubMed Web of Science ®Google Scholar
• Lasonder E, Ishihama Y, Andersen JS, Vermunt AM, Pain A, Sauerwein RW, et al. Analysis of the Plasmodium falciparum proteome by high-accuracy mass spectrometry. Nature 2002;419:537–42.
   PubMed Web of Science ®Google Scholar
• Le Roch KG, Zhou Y, Blair PL, Grainger M, Moch JK, et al. Discovery of gene function by expression profiling of the malaria parasite life cycle. Science 2003;301:1503–8.
   PubMed Web of Science ®Google Scholar
• Shah S. The fever, how malaria has ruled humankind for 500,000 years. New York: Farrar, Straus and Giroux; 2010.
   Google Scholar
• Zoungrana A, Coulibaly B, Sie A, Walter-Sack I, Mockenhaupt FP, Kouyate B, et al. Safety and efficacy of methylene blue combined with artesunate or amodiaquine for uncomplicated falciparum malaria: a randomized controlled trial from Burkina Faso. PLoS One 2008;3:e1630.
   PubMed Web of Science ®Google Scholar
• Reszka KJ, Denning GM, Britigan BE. Photosensitized oxidation and inactivation of pyocyanin, a virulence factor of Pseudomonas aeruginosa. Photochem Photobiol 2006;82:466–73.
   PubMed Web of Science ®Google Scholar
• Nordhoff A, Bucheler US, Werner D, Schirmer RH. Folding of the four domains and dimerization are impaired by the Gly446 → Glu exchange in human glutathione reductase. Implications for the design of antiparasitic drugs. Biochemistry 1993;32:4060–6.
   PubMed Web of Science ®Google Scholar
• Keese MA, Saffrich R, Dandekar T, Becker K, Schirmer RH. Microinjected glutathione reductase crystals as indicators of the redox status in living cells. FEBS Lett 1999;447:135–8.
   PubMed Web of Science ®Google Scholar
• Kabsch W. Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants. J Appl Crystallogr 1993;26:795–800.
   Web of Science ®Google Scholar
• Adams PD, Grosse-Kunstleve RW, Hung LW, Ioerger TR, McCoy AJ, Moriarty NW, et al. PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr D Biol Crystallogr 2002;58:1948–54.
   PubMed Web of Science ®Google Scholar
• Jones TA, Zou JY, Cowan SW, Kjeldgaard M. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr 1991;A47(Pt 2):110–9.
   Google Scholar
• Laskowski RA, MacArthur MW, Moss DS, Thornton JM. PROCHECK: a program to check the stereochemical quality of protein structures. J Appl Crystallogr 1993;26:283–91.
   Web of Science ®Google Scholar
• Trager W, Jensen JB. Human malaria parasites in continuous culture. Science 1976;193:673–5.
   PubMed Web of Science ®Google Scholar
• Lambros C, Vanderberg JP. Synchronization of Plasmodium falciparum erythrocytic stages in culture. J Parasitol 1979;65:418–20.
   PubMed Web of Science ®Google Scholar
• Desjardins RE, Canfield CJ, Haynes JD, Chulay JD. Quantitative assessment of antimalarial activity in vitro by a semiautomated microdilution technique. Antimicrob Agents Chemother 1979;16:710–8.
   PubMed Web of Science ®Google Scholar
• Fivelman QL, Adagu IS, Warhurst DC. Modified fixed-ratio isobologram method for studying in vitro interactions between atovaquone and proguanil or dihydroartemisinin against drug-resistant strains of Plasmodium falciparum. Antimicrob Agents Chemother 2004;48:4097–102.
   PubMed Web of Science ®Google Scholar
• Maerki S, Brun R, Charman SA, Dorn A, Matile H, Wittlin S. In vitro assessment of the pharmacodynamic properties and the partitioning of OZ277/RBx-11160 in cultures of Plasmodium falciparum. J Antimicrob Chemother 2006;58:52–8.
   PubMed Web of Science ®Google Scholar
• Ifediba T, Vanderberg JP. Complete in vitro maturation of Plasmodium falciparum gametocytes. Nature 1981;294:364–6.
   PubMed Web of Science ®Google Scholar
• Ponnudurai T, Lensen AH, Meis JF, Meuwissen JH. Synchronization of Plasmodium falciparum gametocytes using an automated suspension culture system. Parasitol 1986;93(Pt 2):263–74.
   PubMedGoogle Scholar
• Saul A, Graves P, Edser L. Refractoriness of erythrocytes infected with Plasmodium falciparum gametocytes to lysis by sorbitol. Int J Parasitol 1990;20:1095–7.
   PubMed Web of Science ®Google Scholar
• Ribaut C, Berry A, Chevalley S, Reybier K, Morlais I, Parzy D, et al. Concentration and purification by magnetic separation of the erythrocytic stages of all human Plasmodium species. Malar J 2008;7:45.
   PubMed Web of Science ®Google Scholar
• Chutmongkonkul M, Maier WA, Seitz HM. A new model for testing gametocytocidal effects of some antimalarial drugs on Plasmodium falciparum in vitro. Ann Trop Med Parasitol 1992;86:207–15.
   PubMed Web of Science ®Google Scholar