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Volume 63, Issue 1

Apoptosis-like death in promastigotes induced by eugenol-rich oil of Free

Abstract

Leishmaniasis consists of a complex spectrum of infectious diseases with worldwide distribution of which visceral leishmaniasis or kala-azar caused by is the most devastating. In the absence of vaccines, chemotherapy remains the mainstay for the control of leishmaniasis. The drugs of choice are expensive and associated with multiple adverse side effects. Because of these limitations, the development of new antileishmanial compounds is imperative and plants offer prospects in this regard. The present work was conducted to study the antileishmanial potential of oil from flower buds (clove). The oil was characterized by gas chromatography and GC-MS and eugenol as well as eugenyl acetate were found to be the most abundant compounds, composing 59.75 % and 29.24 %, respectively of the oil. Our findings have shown that eugenol-rich essential oil from (EROSA) possesses significant activity against , with 50 % inhibitory concentration of 21±0.16 µg ml and 15.24±0.14 µg ml, respectively, against promastigotes and intracellular amastigotes. Alterations in cellular morphology and growth reversibility assay substantiated the leishmanicidal activity of EROSA. The leishmanicidal effect was mediated via apoptosis as confirmed by externalization of phosphatidylserine, DNA nicking by TdT-mediated dUTP nick-end labelling (TUNEL) assay, dyskinetoplastidy, cell cycle arrest at sub-G–G phase, loss of mitochondrial membrane potential and reactive oxygen species generation. EROSA presented no adverse cytotoxic effects against murine macrophages even at 200 µg ml. Our studies authenticate the promising antileishmanial activity of EROSA, which is mediated by programmed cell death, and, accordingly, EROSA may be a source of novel agents for the treatment of leishmaniasis.

  • Received:
  • Accepted:
  • Published Online:
© 2014 SGM
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2014-01-01
2024-04-24
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References

  1. Afrin F., Dey T., Anam K., Ali N. 2001; Leishmanicidal activity of stearylamine-bearing liposomes in vitro. . J Parasitol 87:188–193[PubMed] [CrossRef]
     [Google Scholar]
  2. Ashford R. W., Desjeux P., Deraadt P. 1992; Estimation of population at risk of infection and number of cases of leishmaniasis. Parasitol Today 8:104–105 [View Article][PubMed]
     [Google Scholar]
  3. Azmi A. S., Bhat S. H., Hanif S., Hadi S. M. 2006; Plant polyphenols mobilize endogenous copper in human peripheral lymphocytes leading to oxidative DNA breakage: a putative mechanism for anticancer properties. FEBS Lett 580:533–538 [View Article][PubMed]
     [Google Scholar]
  4. Bagavan A., Rahuman A. A., Kaushik N. K., Sahal D. 2011; In vitro antimalarial activity of medicinal plant extracts against Plasmodium falciparum. . Parasitol Res 108:15–22 [View Article][PubMed]
     [Google Scholar]
  5. Burt S. A., Reinders R. D. 2003; Antibacterial activity of selected plant essential oils against Escherichia coli O157 : H7. Lett Appl Microbiol 36:162–167 [View Article][PubMed]
     [Google Scholar]
  6. Chaieb K., Hajlaoui H., Zmantar T., Kahla-Nakbi A. B., Rouabhia M., Mahdouani K., Bakhrouf A. 2007; The chemical composition and biological activity of clove essential oil, Eugenia caryophyllata (Syzigium aromaticum L. Myrtaceae): a short review. Phytother Res 21:501–506 [View Article][PubMed]
     [Google Scholar]
  7. Chipuk J. E., Green D. R. 2005; Do inducers of apoptosis trigger caspase-independent cell death?. Nat Rev Mol Cell Biol 6:268–275 [View Article][PubMed]
     [Google Scholar]
  8. Croft S. L., Coombs G. H. 2003; Leishmaniasis – current chemotherapy and recent advances in the search for novel drugs. Trends Parasitol 19:502–508 [View Article][PubMed]
     [Google Scholar]
  9. Das R., Roy A., Dutta N., Majumder H. K. 2008; Reactive oxygen species and imbalance of calcium homeostasis contributes to curcumin induced programmed cell death in Leishmania donovani. . Apoptosis 13:867–882 [View Article][PubMed]
     [Google Scholar]
  10. Debrabant A., Lee N., Bertholet S., Duncan R., Nakhasi H. L. 2003; Programmed cell death in trypanosomatids and other unicellular organisms. Int J Parasitol 33:257–267 [View Article][PubMed]
     [Google Scholar]
  11. Dutta A., Ghoshal A., Mandal D., Mondal N. B., Banerjee S., Sahu N. P., Mandal C. 2007; Racemoside A, an anti-leishmanial, water-soluble, natural steroidal saponin, induces programmed cell death in Leishmania donovani. . J Med Microbiol 56:1196–1204 [View Article][PubMed]
     [Google Scholar]
  12. Dutta A., Sarkar D., Gurib-Fakim A., Mandal C., Chatterjee M. 2008; In vitro and in vivo activity of Aloe vera leaf exudate in experimental visceral leishmaniasis. Parasitol Res 102:1235–1242 [View Article][PubMed]
     [Google Scholar]
  13. Fujisawa S., Atsumi T., Kadoma Y., Sakagami H. 2002; Antioxidant and prooxidant action of eugenol-related compounds and their cytotoxicity. Toxicology 177:39–54 [View Article][PubMed]
     [Google Scholar]
  14. Fyfe L., Armstrong F., Stewart J. 1998; Inhibition of Listeria monocytogenes and Salmonella enteriditis by combinations of plant oils and derivatives of benzoic acid: the development of synergistic antimicrobial combinations. Int J Antimicrob Agents 9:195–199 [View Article][PubMed]
     [Google Scholar]
  15. Gottlieb O. R., Guimaraes M. T. 1960; Modified distillation trap. Chemist Analyst 49:114–116
     [Google Scholar]
  16. Iwu M. M., Jackson J. E., Schuster B. G. 1994; Medicinal plants in the fight against leishmaniasis. Parasitol Today 10:65–68 [View Article][PubMed]
     [Google Scholar]
  17. Jiménez Del Río M., Vélez-Pardo C. 2004; Transition metal-induced apoptosis in lymphocytes via hydroxyl radical generation, mitochondria dysfunction, and caspase-3 activation: an in vitro model for neurodegeneration. Arch Med Res 35:185–193 [View Article][PubMed]
     [Google Scholar]
  18. Kim G. C., Choi D. S., Lim J. S., Jeong H. C., Kim, I . R., Lee M. H., Park B. S. 2006; Caspases‐dependent apoptosis in human melanoma cell by eugenol. Korean J Anat 39:245–253
     [Google Scholar]
  19. Li Q., Zhou Y., Yao C., Ma X., Wang L., Xu W., Wang Z., Qiao Z. 2009; Apoptosis caused by Hsp90 inhibitor geldanamycin in Leishmania donovani during promastigote-to-amastigote transformation stage. Parasitol Res 105:1539–1548 [View Article][PubMed]
     [Google Scholar]
  20. Mishra R. K., Singh S. K. 2008; Safety assessment of Syzygium aromaticum flower bud (clove) extract with respect to testicular function in mice. Food Chem Toxicol 46:3333–3338 [View Article][PubMed]
     [Google Scholar]
  21. Misra P., Kumar A., Gupta S., Khare P., Kumar N., Dube A. 2009; Pro-apoptotic effect of landrace Bangla Mahoma of Piper betle- on Leishmania donovani may be due to high content of eugenol. J Med Microbiol 58:1058–1066 [View Article][PubMed]
     [Google Scholar]
  22. Mohamed A. H. H., El-Sayed M. A., Hegazy M. E., Helaly S. E., Esmail A. M., Mohamed N. S. 2010; Chemical constituents and biological activities of Artemisia herba-alba. . Rec Nat Products 4:1–25
     [Google Scholar]
  23. Mukherjee P., Sen P. C., Ghose A. C. 2006; Lymph node cells from BALB/c mice with chronic visceral leishmaniasis exhibiting cellular anergy and apoptosis: involvement of Ser/Thr phosphatase. Apoptosis 11:2013–2029 [View Article][PubMed]
     [Google Scholar]
  24. Mukherjee P., Majee S. B., Ghosh S., Hazra B. 2009; Apoptosis-like death in Leishmania donovani promastigotes induced by diospyrin and its ethanolamine derivative. Int J Antimicrob Agents 34:596–601 [View Article][PubMed]
     [Google Scholar]
  25. Nguewa P. A., Fuertes M. A., Cepeda V., Iborra S., Carrión J., Valladares B., Alonso C., Pérez J. M. 2005; Pentamidine is an antiparasitic and apoptotic drug that selectively modifies ubiquitin. Chem Biodivers 2:1387–1400 [View Article][PubMed]
     [Google Scholar]
  26. Pérez S. G., Ramos-López M. A., Sánchez-miranda E., Fresán-orozco M. C., Pérez-Ramos J. 2012; Antiprotozoa activity of some essential oils. J Medicinal Plants Res 6:2901–2908
     [Google Scholar]
  27. Richter C., Schlegel J. 1993; Mitochondrial calcium release induced by prooxidants. Toxicol Lett 67:119–127 [View Article][PubMed]
     [Google Scholar]
  28. Rocha L. G., Almeida J. R., Macêdo R. O., Barbosa-Filho J. M. 2005; A review of natural products with antileishmanial activity. Phytomedicine 12:514–535 [View Article][PubMed]
     [Google Scholar]
  29. Rodrigues K. A. F., Amorim L. V., de Oliveira J. M., Dias C. N., Moraes D. F. C., Andrade E. H. A., Maia J. G. S., Carneiro S. M. P., Carvalho F. A. A. 2013; Eugenia uniflora L. essential oil as a potential anti-Leishmania agent: effects on Leishmania amazonensis and possible mechanisms of action. Evid Based Complement Alternat Med 2013:279726 [View Article][PubMed]
     [Google Scholar]
  30. Rosa M. S. S., Mendonça-Filho R. R., Bizzo H. R., Rodrigues I. A, Soares R. M. A., Souto-Padrón T., Alviano C. S., Lopes A. H. C. S. . 2003; Antileishmanial activity of a linalool-rich essential oil from Croton cajucara. . Antimicrob Agents Chemother 47:1895–1901 [View Article][PubMed]
     [Google Scholar]
  31. Saha P., Sen R., Hariharan C., Kumar D., Das P., Chatterjee M. 2009; Berberine chloride causes a caspase-independent, apoptotic-like death in Leishmania donovani promastigotes. Free Radic Res 43:1101–1110 [View Article][PubMed]
     [Google Scholar]
  32. Sanchez-Suarez J. F., Riveros I., Delgado G. 2013; Evaluation of the leishmanicidal and cytotoxic potential of essential oils derived from ten Colombian plants. Iran J Parasitol 8:129–136[PubMed]
     [Google Scholar]
  33. Santoro G. F., Cardoso M. G., Guimarães L. G., Mendonça L. Z., Soares M. J. 2007; Trypanosoma cruzi: activity of essential oils from Achillea millefolium L., Syzygium aromaticum L. and Ocimum basilicum L. on epimastigotes and trypomastigotes. Exp Parasitol 116:283–290 [View Article][PubMed]
     [Google Scholar]
  34. Sen N., Das B. B., Ganguly A., Mukherjee T., Tripathi G., Bandyopadhyay S., Rakshit S., Sen T., Majumder H. K. 2004; Camptothecin induced mitochondrial dysfunction leading to programmed cell death in unicellular hemoflagellate Leishmania donovani. . Cell Death Differ 11:924–936 [View Article][PubMed]
     [Google Scholar]
  35. Sen R., Bandyopadhyay S., Dutta A., Mandal G., Ganguly S., Saha P., Chatterjee M. 2007; Artemisinin triggers induction of cell-cycle arrest and apoptosis in Leishmania donovani promastigotes. J Med Microbiol 56:1213–1218 [View Article][PubMed]
     [Google Scholar]
  36. Singh G., Dey C. S. 2007; Induction of apoptosis-like cell death by pentamidine and doxorubicin through differential inhibition of topoisomerase II in arsenite-resistant L. donovani. . Acta Trop 103:172–185 [View Article][PubMed]
     [Google Scholar]
  37. Singh N., Kaur J., Kumar P., Gupta S., Singh N., Ghosal A., Dutta A., Kumar A., Tripathi R. other authors 2009; An orally effective dihydropyrimidone (DHPM) analogue induces apoptosis-like cell death in clinical isolates of Leishmania donovani overexpressing pteridine reductase 1. Parasitol Res 105:1317–1325 [View Article][PubMed]
     [Google Scholar]
  38. Sudhandiran G., Shaha C. 2003; Antimonial-induced increase in intracellular Ca2+ through non-selective cation channels in the host and the parasite is responsible for apoptosis of intracellular Leishmania donovani amastigotes. J Biol Chem 278:25120–25132 [View Article][PubMed]
     [Google Scholar]
  39. Suzuki Y., Sugiyama K., Furuta H. 1985; Eugenol-mediated superoxide generation and cytotoxicity in guinea pig neutrophils. Jpn J Pharmacol 39:381–386 [View Article][PubMed]
     [Google Scholar]
  40. Ueda-Nakamura T. R., Mendonça-Filho R. R., Morgado-Díaz J. A., Korehisa Maza P., Prado Dias Filho B., Aparício Garcia Cortez D., Alviano D. S., Rosa M. S., Lopes A. H. other authors 2006; Antileishmanial activity of eugenol-rich essential oil from Ocimum gratissimum. . Parasitol Int 55:99–105 [View Article][PubMed]
     [Google Scholar]
  41. Van Houten B., Woshner V., Santos J. H. 2006; Role of mitochondrial DNA in toxic responses to oxidative stress. DNA Repair (Amst) 5:145–152 [View Article][PubMed]
     [Google Scholar]
  42. Yoon H. S., Moon S. C., Kim N. D., Park B. S., Jeong M. H., Yoo Y. H. 2000; Genistein induces apoptosis of RPE-J cells by opening mitochondrial PTP. Biochem Biophys Res Commun 276:151–156 [View Article][PubMed]
     [Google Scholar]
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Apoptosis-like death in Leishmania donovani promastigotes induced by eugenol-rich oil of Syzygium aromaticum
J. Med. Microbiol. 63, 74 (2014); https://doi.org/10.1099/jmm.0.064709-0
/content/journal/jmm/10.1099/jmm.0.064709-0
/content/journal/jmm/10.1099/jmm.0.064709-0
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