Skip to main content
Top
Published in: Malaria Journal 1/2018

Open Access 01-12-2018 | Research

Differential activity of methylene blue against erythrocytic and hepatic stages of Plasmodium

Authors: Henriette Bosson-Vanga, Jean-François Franetich, Valérie Soulard, Daniel Sossau, Maurel Tefit, Bocar Kane, Jean-Christophe Vaillant, Steffen Borrmann, Olaf Müller, Nathalie Dereuddre-Bosquet, Roger Le Grand, Olivier Silvie, Dominique Mazier

Published in: Malaria Journal | Issue 1/2018

Login to get access

Abstract

Background

In the context of malaria elimination/eradication, drugs that are effective against the different developmental stages of the parasite are highly desirable. The oldest synthetic anti-malarial drug, the thiazine dye methylene blue (MB), is known for its activity against Plasmodium blood stages, including gametocytes. The aim of the present study was to investigate a possible effect of MB against malaria parasite liver stages.

Methods

MB activity was investigated using both in vitro and in vivo models. In vitro assays consisted of testing MB activity on Plasmodium falciparum, Plasmodium cynomolgi and Plasmodium yoelii parasites in human, simian or murine primary hepatocytes, respectively. MB in vivo activity was evaluated using intravital imaging in BALB/c mice infected with a transgenic bioluminescent P. yoelii parasite line. The transmission-blocking activity of MB was also addressed using mosquitoes fed on MB-treated mice.

Results

MB shows no activity on Plasmodium liver stages, including hypnozoites, in vitro in primary hepatocytes. In BALB/c mice, MB has moderate effect on P. yoelii hepatic development but is highly effective against blood stage growth. MB is active against gametocytes and abrogates parasite transmission from mice to mosquitoes.

Conclusion

While confirming activity of MB against both sexual and asexual blood stages, the results indicate that MB has only little activity on the development of the hepatic stages of malaria parasites.
Literature
1.
go back to reference White NJ, Pukrittayakamee S, Hien TT, Faiz MA, Mokuolu OA, Dondorp AM. Malaria. Lancet. 2014;383:723–35.CrossRefPubMed White NJ, Pukrittayakamee S, Hien TT, Faiz MA, Mokuolu OA, Dondorp AM. Malaria. Lancet. 2014;383:723–35.CrossRefPubMed
2.
go back to reference WHO. World malaria report 2016. Geneva: World Health Organization; 2016. WHO. World malaria report 2016. Geneva: World Health Organization; 2016.
3.
go back to reference White NJ. Can new treatment developments combat resistance in malaria? Expert Opin Pharmacother. 2016;17:1303–7.CrossRefPubMed White NJ. Can new treatment developments combat resistance in malaria? Expert Opin Pharmacother. 2016;17:1303–7.CrossRefPubMed
5.
go back to reference Oliveira R, Miranda D, Magalhães J, Capela R, Perry MJ, O’Neill PM, et al. From hybrid compounds to targeted drug delivery in antimalarial therapy. Bioorg Med Chem. 2015;23:5120–30.CrossRefPubMed Oliveira R, Miranda D, Magalhães J, Capela R, Perry MJ, O’Neill PM, et al. From hybrid compounds to targeted drug delivery in antimalarial therapy. Bioorg Med Chem. 2015;23:5120–30.CrossRefPubMed
6.
go back to reference Burrows JN, van Huijsduijnen RH, Möhrle JJ, Oeuvray C, Wells TNC. Designing the next generation of medicines for malaria control and eradication. Malar J. 2013;12:187.CrossRefPubMedPubMedCentral Burrows JN, van Huijsduijnen RH, Möhrle JJ, Oeuvray C, Wells TNC. Designing the next generation of medicines for malaria control and eradication. Malar J. 2013;12:187.CrossRefPubMedPubMedCentral
7.
go back to reference Carmona-Fonseca J, Alvarez G, Maestre A. Methemoglobinemia and adverse events in Plasmodium vivax malaria patients associated with high doses of primaquine treatment. Am J Trop Med Hyg. 2009;80:188–93.PubMed Carmona-Fonseca J, Alvarez G, Maestre A. Methemoglobinemia and adverse events in Plasmodium vivax malaria patients associated with high doses of primaquine treatment. Am J Trop Med Hyg. 2009;80:188–93.PubMed
8.
go back to reference Potter BMJ, Xie LH, Vuong C, Zhang J, Zhang P, Duan D, et al. Differential CYP 2D6 metabolism alters primaquine pharmacokinetics. Antimicrob Agents Chemother. 2015;59:2380–7.CrossRefPubMedPubMedCentral Potter BMJ, Xie LH, Vuong C, Zhang J, Zhang P, Duan D, et al. Differential CYP 2D6 metabolism alters primaquine pharmacokinetics. Antimicrob Agents Chemother. 2015;59:2380–7.CrossRefPubMedPubMedCentral
9.
go back to reference Rajapakse S, Rodrigo C, Fernando SD. Tafenoquine for preventing relapse in people with Plasmodium vivax malaria. Cochrane Database Syst Rev. 2015;(4):CD010458. Rajapakse S, Rodrigo C, Fernando SD. Tafenoquine for preventing relapse in people with Plasmodium vivax malaria. Cochrane Database Syst Rev. 2015;(4):CD010458.
10.
go back to reference Ebstie YA, Abay SM, Tadesse WT, Ejigu DA. Tafenoquine and its potential in the treatment and relapse prevention of Plasmodium vivax malaria: the evidence to date. Drug Des Devel Ther. 2016;10:2387–99.CrossRefPubMedPubMedCentral Ebstie YA, Abay SM, Tadesse WT, Ejigu DA. Tafenoquine and its potential in the treatment and relapse prevention of Plasmodium vivax malaria: the evidence to date. Drug Des Devel Ther. 2016;10:2387–99.CrossRefPubMedPubMedCentral
11.
go back to reference Vennerstrom JL, Makler MT, Angerhofer CK, Williams JA. Antimalarial dyes revisited: xanthenes, azines, oxazines, and thiazines. Antimicrob Agents Chemother. 1995;39:2671–7.CrossRefPubMedPubMedCentral Vennerstrom JL, Makler MT, Angerhofer CK, Williams JA. Antimalarial dyes revisited: xanthenes, azines, oxazines, and thiazines. Antimicrob Agents Chemother. 1995;39:2671–7.CrossRefPubMedPubMedCentral
12.
go back to reference Synthetic Schulemann W, Preparations Anti-Malarial. Proc R Soc Med. 1932;25:897–905. Synthetic Schulemann W, Preparations Anti-Malarial. Proc R Soc Med. 1932;25:897–905.
13.
go back to reference Guttmann P, Ehrlich P. Ueber die Wirkung des Methylenblau bei Malaria. Berlin Klin. Wochenschr. 1960;28:953–6. Guttmann P, Ehrlich P. Ueber die Wirkung des Methylenblau bei Malaria. Berlin Klin. Wochenschr. 1960;28:953–6.
14.
go back to reference Schirmer RH, Adler H, Pickhardt M, Mandelkow E. Lest we forget you—methylene blue. Neurobiol Aging. 2011;32:e7–16.CrossRef Schirmer RH, Adler H, Pickhardt M, Mandelkow E. Lest we forget you—methylene blue. Neurobiol Aging. 2011;32:e7–16.CrossRef
15.
go back to reference Schirmer RH, Coulibaly B, Stich A, Scheiwein M, Merkle H, Eubel J, et al. Methylene blue as an antimalarial agent. Redox Rep Commun Free Radic Res. 2003;8:272–5.CrossRef Schirmer RH, Coulibaly B, Stich A, Scheiwein M, Merkle H, Eubel J, et al. Methylene blue as an antimalarial agent. Redox Rep Commun Free Radic Res. 2003;8:272–5.CrossRef
16.
go back to reference Pascual A, Henry M, Briolant S, Charras S, Baret E, Amalvict R, et al. In vitro activity of Proveblue (methylene blue) on Plasmodium falciparum strains resistant to standard antimalarial drugs. Antimicrob Agents Chemother. 2011;55:2472–4.CrossRefPubMedPubMedCentral Pascual A, Henry M, Briolant S, Charras S, Baret E, Amalvict R, et al. In vitro activity of Proveblue (methylene blue) on Plasmodium falciparum strains resistant to standard antimalarial drugs. Antimicrob Agents Chemother. 2011;55:2472–4.CrossRefPubMedPubMedCentral
17.
go back to reference Meissner PE, Mandi G, Witte S, Coulibaly B, Mansmann U, Rengelshausen J, et al. Safety of the methylene blue plus chloroquine combination in the treatment of uncomplicated falciparum malaria in young children of Burkina Faso. Malar J. 2005;4:45.CrossRefPubMedPubMedCentral Meissner PE, Mandi G, Witte S, Coulibaly B, Mansmann U, Rengelshausen J, et al. Safety of the methylene blue plus chloroquine combination in the treatment of uncomplicated falciparum malaria in young children of Burkina Faso. Malar J. 2005;4:45.CrossRefPubMedPubMedCentral
18.
go back to reference Coulibaly B, Pritsch M, Bountogo M, Meissner PE, Nebié E, Klose C, et al. Efficacy and safety of triple combination therapy with artesunate-amodiaquine-methylene blue for falciparum malaria in children: a randomized controlled trial in Burkina Faso. J Infect Dis. 2015;211:689–97.CrossRefPubMed Coulibaly B, Pritsch M, Bountogo M, Meissner PE, Nebié E, Klose C, et al. Efficacy and safety of triple combination therapy with artesunate-amodiaquine-methylene blue for falciparum malaria in children: a randomized controlled trial in Burkina Faso. J Infect Dis. 2015;211:689–97.CrossRefPubMed
19.
go back to reference Müller O, Mockenhaupt FP, Marks B, Meissner P, Coulibaly B, Kuhnert R, et al. Haemolysis risk in methylene blue treatment of G6PD-sufficient and G6PD-deficient West-African children with uncomplicated falciparum malaria: a synopsis of four RCTs. Pharmacoepidemiol Drug Saf. 2013;22:376–85.CrossRefPubMed Müller O, Mockenhaupt FP, Marks B, Meissner P, Coulibaly B, Kuhnert R, et al. Haemolysis risk in methylene blue treatment of G6PD-sufficient and G6PD-deficient West-African children with uncomplicated falciparum malaria: a synopsis of four RCTs. Pharmacoepidemiol Drug Saf. 2013;22:376–85.CrossRefPubMed
20.
go back to reference Manzoni G, Briquet S, Risco-Castillo V, Gaultier C, Topçu S, Ivănescu ML, et al. A rapid and robust selection procedure for generating drug-selectable marker-free recombinant malaria parasites. Sci Rep. 2014;4:4760.CrossRefPubMedPubMedCentral Manzoni G, Briquet S, Risco-Castillo V, Gaultier C, Topçu S, Ivănescu ML, et al. A rapid and robust selection procedure for generating drug-selectable marker-free recombinant malaria parasites. Sci Rep. 2014;4:4760.CrossRefPubMedPubMedCentral
21.
go back to reference Silvie O, Rubinstein E, Franetich J-F, Prenant M, Belnoue E, Rénia L, et al. Hepatocyte CD81 is required for Plasmodium falciparum and Plasmodium yoelii sporozoite infectivity. Nat Med. 2003;9:93–6.CrossRefPubMed Silvie O, Rubinstein E, Franetich J-F, Prenant M, Belnoue E, Rénia L, et al. Hepatocyte CD81 is required for Plasmodium falciparum and Plasmodium yoelii sporozoite infectivity. Nat Med. 2003;9:93–6.CrossRefPubMed
22.
go back to reference Dembele L, Gego A, Zeeman A-M, Franetich J-F, Silvie O, Rametti A, et al. Towards an in vitro model of plasmodium hypnozoites suitable for drug discovery. PLoS ONE. 2011;6:e18162.CrossRefPubMedPubMedCentral Dembele L, Gego A, Zeeman A-M, Franetich J-F, Silvie O, Rametti A, et al. Towards an in vitro model of plasmodium hypnozoites suitable for drug discovery. PLoS ONE. 2011;6:e18162.CrossRefPubMedPubMedCentral
23.
go back to reference Rénia L, Mattei D, Goma J, Pied S, Dubois P, Miltgen F, et al. A malaria heat-shock-like determinant expressed on the infected hepatocyte surface is the target of antibody-dependent cell-mediated cytotoxic mechanisms by nonparenchymal liver cells. Eur J Immunol. 1990;20:1445–9.CrossRefPubMed Rénia L, Mattei D, Goma J, Pied S, Dubois P, Miltgen F, et al. A malaria heat-shock-like determinant expressed on the infected hepatocyte surface is the target of antibody-dependent cell-mediated cytotoxic mechanisms by nonparenchymal liver cells. Eur J Immunol. 1990;20:1445–9.CrossRefPubMed
24.
go back to reference Le Nagard H, Vincent C, Mentré F, Le Bras J. Online analysis of in vitro resistance to antimalarial drugs through nonlinear regression. Comput Methods Programs Biomed. 2011;104:10–8.CrossRefPubMed Le Nagard H, Vincent C, Mentré F, Le Bras J. Online analysis of in vitro resistance to antimalarial drugs through nonlinear regression. Comput Methods Programs Biomed. 2011;104:10–8.CrossRefPubMed
25.
go back to reference Mwakingwe A, Ting L-M, Hochman S, Chen J, Sinnis P, Kim K. Noninvasive real-time monitoring of liver-stage development of bioluminescent Plasmodium parasites. J Infect Dis. 2009;200:1470–8.CrossRefPubMed Mwakingwe A, Ting L-M, Hochman S, Chen J, Sinnis P, Kim K. Noninvasive real-time monitoring of liver-stage development of bioluminescent Plasmodium parasites. J Infect Dis. 2009;200:1470–8.CrossRefPubMed
26.
go back to reference Matos J, da Cruz FP, Cabrita É, Gut J, Nogueira F, do Rosário VE, et al. Novel potent metallocenes against liver stage malaria. Antimicrob Agents Chemother. 2012;56:1564–70.CrossRefPubMedPubMedCentral Matos J, da Cruz FP, Cabrita É, Gut J, Nogueira F, do Rosário VE, et al. Novel potent metallocenes against liver stage malaria. Antimicrob Agents Chemother. 2012;56:1564–70.CrossRefPubMedPubMedCentral
27.
go back to reference Delves M, Plouffe D, Scheurer C, Meister S, Wittlin S, Winzeler EA, et al. The activities of current antimalarial drugs on the life cycle stages of Plasmodium: a comparative study with human and rodent parasites. PLoS Med. 2012;9:e1001169.CrossRefPubMedPubMedCentral Delves M, Plouffe D, Scheurer C, Meister S, Wittlin S, Winzeler EA, et al. The activities of current antimalarial drugs on the life cycle stages of Plasmodium: a comparative study with human and rodent parasites. PLoS Med. 2012;9:e1001169.CrossRefPubMedPubMedCentral
28.
go back to reference Garavito G, Bertani S, Rincon J, Maurel S, Monje MC, Landau I, et al. Blood schizontocidal activity of methylene blue in combination with antimalarials against Plasmodium falciparum. Parasite. 2007;14:135–40.CrossRefPubMed Garavito G, Bertani S, Rincon J, Maurel S, Monje MC, Landau I, et al. Blood schizontocidal activity of methylene blue in combination with antimalarials against Plasmodium falciparum. Parasite. 2007;14:135–40.CrossRefPubMed
29.
go back to reference Dormoi J, Pascual A, Briolant S, Amalvict R, Charras S, Baret E, et al. Proveblue (methylene blue) as an antimalarial agent: in vitro synergy with dihydroartemisinin and atorvastatin. Antimicrob Agents Chemother. 2012;56:3467–9.CrossRefPubMedPubMedCentral Dormoi J, Pascual A, Briolant S, Amalvict R, Charras S, Baret E, et al. Proveblue (methylene blue) as an antimalarial agent: in vitro synergy with dihydroartemisinin and atorvastatin. Antimicrob Agents Chemother. 2012;56:3467–9.CrossRefPubMedPubMedCentral
30.
go back to reference Fall B, Camara C, Fall M, Nakoulima A, Dionne P, Diatta B, et al. Plasmodium falciparum susceptibility to standard and potential anti-malarial drugs in Dakar, Senegal, during the 2013–2014 malaria season. Malar J. 2015;14:60.CrossRefPubMedPubMedCentral Fall B, Camara C, Fall M, Nakoulima A, Dionne P, Diatta B, et al. Plasmodium falciparum susceptibility to standard and potential anti-malarial drugs in Dakar, Senegal, during the 2013–2014 malaria season. Malar J. 2015;14:60.CrossRefPubMedPubMedCentral
31.
go back to reference Dormoi J, Briolant S, Desgrouas C, Pradines B. Efficacy of proveblue (methylene blue) in an experimental cerebral malaria murine model. Antimicrob Agents Chemother. 2013;57:3412–4.CrossRefPubMedPubMedCentral Dormoi J, Briolant S, Desgrouas C, Pradines B. Efficacy of proveblue (methylene blue) in an experimental cerebral malaria murine model. Antimicrob Agents Chemother. 2013;57:3412–4.CrossRefPubMedPubMedCentral
32.
go back to reference Dormoi J, Pradines B. Dose responses of proveblue methylene blue in an experimental murine cerebral malaria model. Antimicrob Agents Chemother. 2013;57:4080–1.CrossRefPubMedPubMedCentral Dormoi J, Pradines B. Dose responses of proveblue methylene blue in an experimental murine cerebral malaria model. Antimicrob Agents Chemother. 2013;57:4080–1.CrossRefPubMedPubMedCentral
33.
go back to reference Dormoi J, Briolant S, Desgrouas C, Pradines B. Impact of methylene blue and atorvastatin combination therapy on the apparition of cerebral malaria in a murine model. Malar J. 2013;12:127.CrossRefPubMedPubMedCentral Dormoi J, Briolant S, Desgrouas C, Pradines B. Impact of methylene blue and atorvastatin combination therapy on the apparition of cerebral malaria in a murine model. Malar J. 2013;12:127.CrossRefPubMedPubMedCentral
34.
go back to reference Mandi G, Witte S, Meissner P, Coulibaly B, Mansmann U, Rengelshausen J, et al. Safety of the combination of chloroquine and methylene blue in healthy adult men with G6PD deficiency from rural Burkina Faso. Trop Med Int Health. 2005;10:32–8.CrossRefPubMed Mandi G, Witte S, Meissner P, Coulibaly B, Mansmann U, Rengelshausen J, et al. Safety of the combination of chloroquine and methylene blue in healthy adult men with G6PD deficiency from rural Burkina Faso. Trop Med Int Health. 2005;10:32–8.CrossRefPubMed
35.
go back to reference Meissner PE, Mandi G, Coulibaly B, Witte S, Tapsoba T, Mansmann U, et al. Methylene blue for malaria in Africa: results from a dose-finding study in combination with chloroquine. Malar J. 2006;5:84.CrossRefPubMedPubMedCentral Meissner PE, Mandi G, Coulibaly B, Witte S, Tapsoba T, Mansmann U, et al. Methylene blue for malaria in Africa: results from a dose-finding study in combination with chloroquine. Malar J. 2006;5:84.CrossRefPubMedPubMedCentral
36.
go back to reference Zoungrana A, Coulibaly B, Sié A, Walter-Sack I, Mockenhaupt FP, Kouyaté 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.CrossRefPubMedPubMedCentral Zoungrana A, Coulibaly B, Sié A, Walter-Sack I, Mockenhaupt FP, Kouyaté 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.CrossRefPubMedPubMedCentral
37.
go back to reference Bountogo M, Zoungrana A, Coulibaly B, Klose C, Mansmann U, Mockenhaupt FP, et al. Efficacy of methylene blue monotherapy in semi-immune adults with uncomplicated falciparum malaria: a controlled trial in Burkina Faso. Trop Med Int Health. 2010;15:713–7.CrossRefPubMed Bountogo M, Zoungrana A, Coulibaly B, Klose C, Mansmann U, Mockenhaupt FP, et al. Efficacy of methylene blue monotherapy in semi-immune adults with uncomplicated falciparum malaria: a controlled trial in Burkina Faso. Trop Med Int Health. 2010;15:713–7.CrossRefPubMed
38.
go back to reference Adjalley SH, Johnston GL, Li T, Eastman RT, Ekland EH, Eappen AG, et al. Quantitative assessment of Plasmodium falciparum sexual development reveals potent transmission-blocking activity by methylene blue. Proc Natl Acad Sci USA. 2011;108:E1214–23.CrossRefPubMedPubMedCentral Adjalley SH, Johnston GL, Li T, Eastman RT, Ekland EH, Eappen AG, et al. Quantitative assessment of Plasmodium falciparum sexual development reveals potent transmission-blocking activity by methylene blue. Proc Natl Acad Sci USA. 2011;108:E1214–23.CrossRefPubMedPubMedCentral
39.
go back to reference 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.CrossRefPubMedPubMedCentral 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.CrossRefPubMedPubMedCentral
40.
go back to reference Schmidt LH. Compatibility of relapse patterns of Plasmodium cynomolgi infections in rhesus monkeys with continuous cyclical development and hypnozoite concepts of relapse. Am J Trop Med Hyg. 1986;35:1077–99.CrossRefPubMed Schmidt LH. Compatibility of relapse patterns of Plasmodium cynomolgi infections in rhesus monkeys with continuous cyclical development and hypnozoite concepts of relapse. Am J Trop Med Hyg. 1986;35:1077–99.CrossRefPubMed
41.
go back to reference Deye GA, Gettayacamin M, Hansukjariya P, Im-erbsin R, Sattabongkot J, Rothstein Y, et al. Use of a rhesus Plasmodium cynomolgi model to screen for anti-hypnozoite activity of pharmaceutical substances. Am J Trop Med Hyg. 2012;86:931–5.CrossRefPubMedPubMedCentral Deye GA, Gettayacamin M, Hansukjariya P, Im-erbsin R, Sattabongkot J, Rothstein Y, et al. Use of a rhesus Plasmodium cynomolgi model to screen for anti-hypnozoite activity of pharmaceutical substances. Am J Trop Med Hyg. 2012;86:931–5.CrossRefPubMedPubMedCentral
42.
go back to reference Putrianti ED, Silvie O, Kordes M, Borrmann S, Matuschewski K. Vaccine-like immunity against malaria by repeated causal-prophylactic treatment of liver-stage Plasmodium parasites. J Infect Dis. 2009;199:899–903.CrossRefPubMed Putrianti ED, Silvie O, Kordes M, Borrmann S, Matuschewski K. Vaccine-like immunity against malaria by repeated causal-prophylactic treatment of liver-stage Plasmodium parasites. J Infect Dis. 2009;199:899–903.CrossRefPubMed
43.
go back to reference Friesen J, Silvie O, Putrianti ED, Hafalla JCR, Matuschewski K, Borrmann S. Natural immunization against malaria: causal prophylaxis with antibiotics. Sci Transl Med. 2010;2:40ra49.CrossRefPubMed Friesen J, Silvie O, Putrianti ED, Hafalla JCR, Matuschewski K, Borrmann S. Natural immunization against malaria: causal prophylaxis with antibiotics. Sci Transl Med. 2010;2:40ra49.CrossRefPubMed
45.
go back to reference Annoura T, Chevalley S, Janse CJ, Franke-Fayard B, Khan SM. Quantitative analysis of Plasmodium berghei liver stages by bioluminescence imaging. Methods Mol Biol. 2013;923:429–43.CrossRefPubMed Annoura T, Chevalley S, Janse CJ, Franke-Fayard B, Khan SM. Quantitative analysis of Plasmodium berghei liver stages by bioluminescence imaging. Methods Mol Biol. 2013;923:429–43.CrossRefPubMed
46.
go back to reference Miller JL, Murray S, Vaughan AM, Harupa A, Sack B, Baldwin M, et al. Quantitative bioluminescent imaging of pre-erythrocytic malaria parasite infection using luciferase-expressing Plasmodium yoelii. PLoS ONE. 2013;8:e60820.CrossRefPubMedPubMedCentral Miller JL, Murray S, Vaughan AM, Harupa A, Sack B, Baldwin M, et al. Quantitative bioluminescent imaging of pre-erythrocytic malaria parasite infection using luciferase-expressing Plasmodium yoelii. PLoS ONE. 2013;8:e60820.CrossRefPubMedPubMedCentral
47.
go back to reference Garavito G. Etude pharmacologique expérimentale de l'activité antipaludique d’un composé de synthèse: le chlorure de methyl-thioninium. PhD Thesis, Université Toulouse III/Paul Sabatier École Doctorale BSB, IOP Publishing Physics, Toulouse, 2007; pp 155. Garavito G. Etude pharmacologique expérimentale de l'activité antipaludique d’un composé de synthèse: le chlorure de methyl-thioninium. PhD Thesis, Université Toulouse III/Paul Sabatier École Doctorale BSB, IOP Publishing Physics, Toulouse, 2007; pp 155.
48.
go back to reference Sparr C, Purkayastha N, Kolesinska B, Gengenbacher M, Amulic B, Matuschewski K, et al. Improved efficacy of fosmidomycin against Plasmodium and Mycobacterium species by combination with the cell-penetrating peptide octaarginine. Antimicrob Agents Chemother. 2013;57:4689–98.CrossRefPubMedPubMedCentral Sparr C, Purkayastha N, Kolesinska B, Gengenbacher M, Amulic B, Matuschewski K, et al. Improved efficacy of fosmidomycin against Plasmodium and Mycobacterium species by combination with the cell-penetrating peptide octaarginine. Antimicrob Agents Chemother. 2013;57:4689–98.CrossRefPubMedPubMedCentral
49.
go back to reference Baumeister S, Wiesner J, Reichenberg A, Hintz M, Bietz S, Harb OS, et al. Fosmidomycin uptake into Plasmodium and Babesia-infected erythrocytes is facilitated by parasite-induced new permeability pathways. PLoS ONE. 2011;6:e19334.CrossRefPubMedPubMedCentral Baumeister S, Wiesner J, Reichenberg A, Hintz M, Bietz S, Harb OS, et al. Fosmidomycin uptake into Plasmodium and Babesia-infected erythrocytes is facilitated by parasite-induced new permeability pathways. PLoS ONE. 2011;6:e19334.CrossRefPubMedPubMedCentral
50.
go back to reference Nair SC, Brooks CF, Goodman CD, Sturm A, Strurm A, McFadden GI, et al. Apicoplast isoprenoid precursor synthesis and the molecular basis of fosmidomycin resistance in Toxoplasma gondii. J Exp Med. 2011;208:1547–59.CrossRefPubMedPubMedCentral Nair SC, Brooks CF, Goodman CD, Sturm A, Strurm A, McFadden GI, et al. Apicoplast isoprenoid precursor synthesis and the molecular basis of fosmidomycin resistance in Toxoplasma gondii. J Exp Med. 2011;208:1547–59.CrossRefPubMedPubMedCentral
51.
go back to reference Arfeen M, Patel DS, Abbat S, Taxak N, Bharatam PV. Importance of cytochromes in cyclization reactions: quantum chemical study on a model reaction of proguanil to cycloguanil. J Comput Chem. 2014;35:2047–55.CrossRefPubMed Arfeen M, Patel DS, Abbat S, Taxak N, Bharatam PV. Importance of cytochromes in cyclization reactions: quantum chemical study on a model reaction of proguanil to cycloguanil. J Comput Chem. 2014;35:2047–55.CrossRefPubMed
52.
go back to reference Carraz M, Jossang A, Franetich J-F, Siau A, Ciceron L, Hannoun L, et al. A plant-derived morphinan as a novel lead compound active against malaria liver stages. PLoS Med. 2006;3:e513.CrossRefPubMedPubMedCentral Carraz M, Jossang A, Franetich J-F, Siau A, Ciceron L, Hannoun L, et al. A plant-derived morphinan as a novel lead compound active against malaria liver stages. PLoS Med. 2006;3:e513.CrossRefPubMedPubMedCentral
Metadata
Title
Differential activity of methylene blue against erythrocytic and hepatic stages of Plasmodium
Authors
Henriette Bosson-Vanga
Jean-François Franetich
Valérie Soulard
Daniel Sossau
Maurel Tefit
Bocar Kane
Jean-Christophe Vaillant
Steffen Borrmann
Olaf Müller
Nathalie Dereuddre-Bosquet
Roger Le Grand
Olivier Silvie
Dominique Mazier
Publication date
01-12-2018
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2018
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/s12936-018-2300-y

Other articles of this Issue 1/2018

Malaria Journal 1/2018 Go to the issue
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.