Hydrogenosome metabolism is the key target for antiparasitic activity of resveratrol against trichomonas vaginalis

Antimicrobial Agents and Chemotherapy

Volumn 57, Issue 6, 2013, Pages 2476-2484

  Mallo, Natalia ^a   Lamas, Jesús ^a   Leiro, José M ^a  

^a UNIVERSITY OF SANTIAGO DE COMPOSTELA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIPARASITIC AGENT; CYTOSTATIC AGENT; HEAT SHOCK PROTEIN 70; IRON HYDROGENASE; PYRUVATE SYNTHASE; REACTIVE OXYGEN METABOLITE; RESVERATROL;

ANTIPARASITIC ACTIVITY; ARTICLE; DRUG ACTIVITY; DRUG CYTOTOXICITY; DRUG STRUCTURE; ENZYME ACTIVITY; FEMALE; GENE EXPRESSION; HUMAN; HYDROGENOSOME METABOLISM; IN VITRO STUDY; MEMBRANE POTENTIAL; METABOLISM; MINIMUM INHIBITORY CONCENTRATION; PARASITE CULTIVATION; PRIORITY JOURNAL; TRICHOMONAS VAGINALIS; TRICHOMONIASIS; TROPHOZOITE;

ANIMALS; ANTITRICHOMONAL AGENTS; FEMALE; HUMANS; HYDROGEN; HYDROGENASE; IRON-SULFUR PROTEINS; ORGANELLES; PARASITIC SENSITIVITY TESTS; PYRUVATE SYNTHASE; STILBENES; TRICHOMONAS VAGINALIS; TRICHOMONAS VAGINITIS; UP-REGULATION;

EID: 84877849291     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.00009-13     Document Type: Article

References (70)

1. Miller M, Liao Y, Gomez AM, Gaydos CA, D'Mellow D. 2008. Factors associated with the prevalence and incidence of Trichomonas vaginalis infection among African American women in New York City who use drugs. J. Infect. Dis. 197:503-509.
2. Anderson MR, Klink K, Cohrssen A. 2004. Evaluation of vaginal complaints. JAMA 291:1368-1379.
3. Azimi H, Fallah-Tafti M, Karimi-Darmiyan M, Abdollahi M. 2011. A comprehensive review of vaginitis phytotherapy. Pak. J. Biol. Sci. 14:960-966.
4. Harp DF, Chowdhury I. 2011. Trichomoniasis: Evaluation to execution. Eur. J. Obstet. Gynecol. Reprod. Biol. 157:3-9.
5. Kirkcaldy RD, Augostini P, Asbel LE, Bernstein KT, Kerani RP, Mettenbrink CJ, Pathela P, Schwebke JR, Secor WE, Workowski KA, Davis D, Braxton J, Weinstock HS. 2012. Trichomonas vaginalis antimicrobial drug resistance in 6 US cities, STD Surveillance Network, 2009-2010. Emerg. Infect. Dis. 18:939-943.
6. Cudmore SL, Delgaty KL, Hayward-McClelland SF, Petrin DP, Garber GE. 2004. Treatment of infections caused by metronidazole-resistance Trichomonas vaginalis. Clin. Microbiol. Rev. 17:783-793.
7. Das S, Huengsberg M, Shahmanesh M. 2005. Treatment failure of vaginal trichomoniasis in clinical practice. Int. J. STD AIDS 16:284-286.
8. Löfmark S, Edlund C, Nord CE. 2010. Metronidazole is still the drug of choice for treatment of anaerobic infections. Clin. Infect. Dis. 50(Suppl 1):S16-S23.
9. Muzny C, Barnes A, Mena L. 2012. Symptomatic Trichomonas vaginalis infection in the setting of severe nitroimidazole allergy: Successful treatment with boric acid. Sex. Health 9:389-391.
10. Borris RP. 1996. Natural products research: Perspectives from a major pharmaceutical company. J. Ethnopharmacol. 51:29-38.
11. Butler MS. 2004. The role of natural products in drug discovery. J. Nat. Prod. 67:2141-2153.
12. Koehn FE, Carter GT. 2005. Rediscovering natural products as a source of new drugs. Discov. Med. 5:159-164.
13. Chang X, Heene E, Qiao F, Nick P. 2011. The phytoalexin resveratrol regulates the initiation of hypersensitive cell death in Vitis cell. PLoS One 6:e26405. doi:10.1371/journal.pone.0026405.
14. Siemann EH, Creasy LL. 1992. Concentration of the phytoalexin resveratrol in wine. Am. J. Enol. Vitic. 43:49-52.
15. Jeandet P, Douillet-Breuil AC, Bessis R, Debord S, Sbaghi M, Adrian M. 2002. Phytoalexins from the Vitaceae: Biosynthesis, phytoalexin gene expression in transgenic plants, antifungal activity, and metabolism. J. Agric. Food Chem. 50:2731-2741.
16. Chan MM. 2002. Antimicrobial effect of resveratrol on dermatophytes and bacterial pathogens of the skin. Biochem. Pharmacol. 63:99-104.
17. Jung HJ, Hwang IA, Sung WS, Kang H, Kang BS, Seu YB, Lee DG. 2005. Fungicidal effect of resveratrol on human infectious fungi. Arch. Pharm. Res. 28:557-560.
18. Leiro J, Arranz JA, Parama A, Alvarez MF, Sanmartin ML. 2004. In vitro effects of the polyphenols resveratrol, mangiferin and (?)-epigallocatechin-3- gallate on the scuticociliate fish pathogen Philasterides dicentrarchi. Dis. Aquat. Organ. 59:171-174.
19. Leiro J, Cano E, Ubeira FM, Orallo F, Sanmartin ML. 2004. In vitro effects of resveratrol on the viability and infectivity of the microsporidian Encephalitozoon cuniculi. Antimicrob. Agents Chemother. 48:2497-2501.
20. Docherty JJ, Fu MM, Stiffler BS, Limperos RJ, Pokabla CM, DeLucia AL. 1999. Resveratrol inhibition of herpes simplex virus replication. Antiviral Res. 43:145-155.
21. Kedzierski L, Curtis JM, Kaminska M, Jodynis-Liebert J, Murias M. 2007. In vitro antileishmanial activity of resveratrol and its hydroxylated analogues against Leishmania major promastigotes and amastigotes. Parasitol. Res. 102:91-97.
22. Son IH, Chung IM, Lee SJ, Moon HI. 2007. Antiplasmodial activity of novel stilbene derivatives isolated from Parthenocissus tricuspidata from South Korea. Parasitol. Res. 101:237-241.
23. Nakata R, Takahashi S, Inoue H. 2012. Recent advances in the study on resveratrol. Biol. Pharm. Bull. 35:273-279.
24. Embley TM, van der Giezen M, Horner DS, Dyal PL, Foster P. 2003. Mitochondria and hydrogenosomes are two forms of the same fundamental organelle. Philos. Trans. R. Soc. Lond. B Biol. Sci. 358:191-203.
25. Kulda J. 1999. Trichomonads, hydrogenosomes and drug resistance. Int. J. Parasitol. 29:199-212.
26. Benchimol M. 2008. The hydrogenosome as a drug target. Curr. Pharm. Des. 14:872-881.
27. Diamond LS. 1957. The establishment of various trichomonads of animals and man in axenic cultures. J. Parasitol. 43:488-490.
28. Vilela RC, Benchimol M. 2012. Trichomonas vaginalis and Tritrichomonas foetus: Interaction with fibroblasts and muscle cells-new insights into parasite-mediated host cell cytotoxicity. Mem. Inst. Oswaldo Cruz 107: 720-727.
29. Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2?CT method. Methods 25: 402-408.
30. Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, Kubista M, Mueller R, Nolan T, Pfaffl MW, Shipley GL, Vandesompele J, Wittwer CT. 2009. The MIQE guidelines: Minimum information for publication of quantitative real-time PCR experiments. Clin. Chem. 55:611-622.
31. Laemmli EK. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
32. Paramá A, Iglesias R, Álvarez MF, Leiro J, Ubeira FM, Sanmartín ML. 2004. Cysteine proteinase activities in the fish pathogen Philasterides dicentrarchi (Ciliophora: Scuticociliatida). Parasitology 128:541-548.
33. Paramá A, Castro R, Lamas J, Sanmartín ML, Santamarina MT, Leiro J. 2007. Scuticociliate proteinases may modulate turbot immune response by inducing apoptosis in pronephric leucocytes. Int. J. Parasitol. 37:87-95.
34. Álvarez E, Campos-Toimil M, Justiniano-Basaran H, Lugnier C, Orallo F. 2006. Study of the mechanisms involved in the vasorelaxation induced by (?)-epigallocatechin-3-gallate in rat aorta. Br. J. Pharmacol. 147:269-280.
35. Dunne RL, Dunn LA, Upcroft P, O'Donoghue PJ, Upcroft JA. 2003. Drug resistance in sexually transmitted protozoan Trichomonas vaginalis. Cell Res. 13:239-249.
36. Bachmann LH, Hobbs MM, Seña AC, Sobel JD, Schwebke JR, Krieger JN, McClelland RS, Workowski KA. 2011. Trichomonas vaginalis genital infections: Progress and challenges. Clin. Infect. Dis. 53(Suppl 3):S160-S172.
37. Secor WE. 2012. Trichomonas vaginalis: Treatment questions and challenges. Expert. Rev. Anti Infect. Ther. 10:107-109.
38. Scott E, Steward WP, Gescher AJ, Brown K. 2012. Resveratrol in human cancer chemoprevention-choosing the 'right' dose. Mol. Nutr. Food Res. 56:7-13.
39. Calzada F, Yépez-Mulia L, Tapia-Contreras A. 2007. Effect of Mexican medicinal plant used to treat trichomoniasis on Trichomonas vaginalis trophozoites. J. Ethnopharmacol. 113:248-251.
40. Arthan D, Sithiprom S, Thima K, Limmatvatirat C, Chavalitshewinkoon- Petmitr P, Svasti J. 2008. Inhibitory effects of Thai plants betaglycosides on Trichomonas vaginalis. Parasitol. Res. 103:443-448.
41. Cantillo-Ciau Z, Moo-Puc R, Quijano L, Freile-Pelegrín Y. 2010. The tropical brown alga Lobophora variegata: A source of antiprotozoal compounds. Mar. Drugs 8:1292-1304.
42. Frasson AP, dos Santos O, Duarte M, da Silva Trentin D, Giordani RB, da Silva AG, da Silva MV, Tasca T, Macedo AJ. 2012. First report of anti-Trichomonas vaginalis activity of the medicinal plant Polygala decumbens from the Brazilian semi-arid region, Caatinga. Parasitol. Res. 110:2581-2587.
43. Moraes ME, Cunha GH, Bezerra MM, Fechine FV, Pontes AV, Andrade WS, Frota Bezerra FA, Moraes MO, Cavalcanti PP. 2012. Efficacy of the Mentha crispa in the treatment of women with Trichomonas vaginalis infection. Arch. Gynecol. Obstet. 286:125-130.
44. Crozet MD, Botta C, Gasquet M, Curti C, Rémusat V, Hutter S, Chapelle O, Azas N, De Méo M, Vanelle P. 2009. Lowering of 5-nitroimidazole's mutagenicity: Towards optimal antiparasitic pharmacophore. Eur. J. Med. Chem. 44:653-659.
45. Benchimol M. 1999. The hydrogenosome. Acta Microsc. 8:1-22.
46. Lindmark DG, Müller M. 1973. Hydrogenosome, a cytoplasmic organelle of the anaerobic flagellate Tritrichomonas foetus, and its role in pyruvate metabolism. J. Biol. Chem. 248:7724-7728.
47. Embley TM, Horner DA, Hirt RP. 1997. Anaerobic eukaryotic evolution: Hydrogenosomes as biochemically modified mitochondria. Trends Ecol. Evol. 12:437-441.
48. Williams KP, Leadlay PF, Lowe PN. 1990. Inhibition of pyruvate: Ferredoxin oxidoreductase from Trichomonas vaginalis by pyruvate and its analogues. Comparison with the pyruvate decarboxylase component of the pyruvate dehydrogenase complex. Biochem. J. 268:69-75.
49. Page-Sharp MC, Behm CA, Smith GD. 1996. Tritrichomonas foetus and Trichomonas vaginalis: The pattern of inactivation of hydrogenase activity by oxygen and activities of catalase and ascorbate peroxidase. Microbiology 142:207-211.
50. Frey M. 2002. Hydrogenases: Hydrogen-activating enzymes. Chem. Biochem. 3:153-160.
51. Payne MJ, Chapman A, Cammarck R. 1993. Evidence for an [Fe]-type hydrogenase in the parasitic protozoan Trichomonas vaginalis. FEBS Lett. 317:101-104.
52. Müller M. 1993. The hydrogenosome. J. Gen. Microbiol. 139:2879-2889.
53. Bui ET, Johnson PJ. 1996. Identification and characterization of [Fe]-hydrogenases in the hydrogenosome of Trichomonas vaginalis. Mol. Biochem. Parasitol. 76:305-310.
54. Horner DS, Foster PG, Embley TM. 2000. Iron hydrogenases and the evolution of anaerobic eukaryotes. Mol. Biol. Evol. 17:1695-1709.
55. Ueno Y, Kurano N, Miyachi S. 1999. Purification and characterization of hydrogenase from the marine green alga, Chlorococcum littorale. FEBS Lett. 443:144-148.
56. Hrdý I, Cammack R, Stopka P, Kulda J, Tachezy J. 2005. Alternative pathway of metronidazole activation in Trichomonas vaginalis hydrogenosomes. Antimicrob. Agents Chemother. 49:5033-5036.
57. Lloyd D, Kristensen B. 1985. Metronidazole inhibition of hydrogen production in vivo in drug-sensitive and-resistant strains of Trichomonas vaginalis. J. Gen. Microbiol. 131:137-140.
58. Karlsson J, Emgard M, Brundin P, Burkitt MJ. 2000. Trans-resveratrol protects embryonic mesencephalic cells from tert-butyl hydroperoxide: Electron paramagnetic resonance spin trapping evidence for a radical scavenging mechanism. J. Neurochem. 75:141-150.
59. Kim Y-S, Song H-O, Choi I-H, Park S-J, Ryu J-S. 2006. Hydrogenosomal activity of Trichomonas vaginalis cultivated under different iron conditions. Korean J. Parasitol. 44:373-378.
60. Kim M, Song E. 2010. Iron transport by proteoliposomes containing mitochondrial F(1) F(0) ATP synthase isolated from rat heart. Biochimie 92:333-342.
61. Agnello M, Morici G, Rinaldi AM. 2008. A method for measuring mitochondrial mass and activity. Cytotechnology 56:145-149.
62. Emelyanov VV, Goldberg AV. 2011. Fermentation enzymes of Giardia intestinalis, pyruvate:ferredoxin oxidoreductase and hydrogenase do not localize to its mitosomes. Microbiology 157:1602-1611.
63. Lamas J, Morais P, Arranz JA, Sanmartín ML, Orallo F, Leiro J. 2009. Resveratrol promotes an inhibitory effect on the turbot scuticociliate parasite Philasterides dicentrarchi by mechanisms related to cellular detoxification. Vet. Parasitol. 161:307-315.
64. Solans A, Zambrano A, Rodríguez M, Barrientos A. 2006. Cytotoxicity of a mutant huntingtin fragment in yeast involves early alterations in mitochondrial OXPHOS complexes II and III. Hum. Mol. Genet. 15: 3063-3081.
65. Morais P, Piazzon C, Lamas J, Mallo N, Leiro JM. 2013. Effect of resveratrol on oxygen consumption by Philasterides dicentrarchi, a scuticociliate parasite of turbot. Protist 164:206-217.
66. Vilela R, Menna-Barreto RF, Benchimol M. 2010. Methyl jasmonate induces cell death and loss of hydrogenosomal membrane potential in Trichomonas vaginalis. Parasitol. Int. 59:387-393.
67. Mead JR, Fernández M, Romagnoli PA, Secor WE. 2006. Use of Trichomonas vaginalis to evaluate correlation of gene expression and metronidazole resistance. J. Parasitol. 92:196-199.
68. Land KM, Delgadillo-Correa MG, Tachezy J, Vanacova S, Hsieh CL, Sutak R, Johnson PJ. 2004. Targeted gene replacement of a ferredoxin gene in Trichomonas vaginalis does not lead to metronidazole resistance. Mol. Microbiol. 51:115-122.
69. Bui ET, Bradley PJ, Johnson PJ. 1996. A common evolutionary origin for mitochondria and hydrogenosomes. Proc. Natl. Acad. Sci. U. S. A. 93: 9651-9656.
70. Yang H, Zhou X, Liu X, Yang L, Chen Q, Zhao D, Zuo J, Liu W. 2011. Mitochondrial dysfunction induced by knockdown of mortalin is rescued by Parkin. Biochem. Biophys. Res. Commun. 410:114-120.