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Evidence-Based Complementary and Alternative Medicine
Volume 2015 (2015), Article ID 319240, 10 pages
http://dx.doi.org/10.1155/2015/319240
Research Article

Antifungal and Antibacterial Metabolites from a French Poplar Type Propolis

1EA 921 SONAS/SFR 4207 QUASAV, Université d’Angers, 16 boulevard Daviers, 49045 Angers Cedex 01, France
2Laboratoire de Bactériologie-Hygiène, Centre Hospitalier Universitaire, 4 rue Larrey, 49933 Angers Cedex 09, France
3Groupe d’Etude des Interactions Hôte Pathogène (GEIHP), Université d’Angers, 4 rue Larrey, 49933 Angers Cedex, France
4Ballot-Flurin Apiculteurs-Abeilles Santé, 75 place Lagardère, 65700 Maubourguet, France

Received 2 February 2015; Revised 3 March 2015; Accepted 4 March 2015

Academic Editor: Veronique Seidel

Copyright © 2015 Séverine Boisard et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. S. M. Cottica, A. C. H. F. Sawaya, M. N. Eberlin, S. L. Franco, L. M. Zeoula, and J. V. Visentainer, “Antioxidant activity and composition of propolis obtained by different methods of extraction,” Journal of the Brazilian Chemical Society, vol. 22, no. 5, pp. 929–935, 2011. View at Publisher · View at Google Scholar · View at Scopus
  2. M. G. Miguel, S. Nunes, S. A. Dandlen, A. M. Cavaco, and M. D. Antunes, “Phenols and antioxidant activity of hydro-alcoholic extracts of propolis from Algarve, South of Portugal,” Food and Chemical Toxicology, vol. 48, no. 12, pp. 3418–3423, 2010. View at Publisher · View at Google Scholar · View at Scopus
  3. I. Gülçin, E. Bursal, M. H. Şehitoĝlu, M. Bilsel, and A. C. Gören, “Polyphenol contents and antioxidant activity of lyophilized aqueous extract of propolis from Erzurum, Turkey,” Food and Chemical Toxicology, vol. 48, no. 8-9, pp. 2227–2238, 2010. View at Publisher · View at Google Scholar · View at Scopus
  4. C. Ota, C. Unterkircher, V. Fantinato, and M. T. Shimizu, “Antifungal activity of propolis on different species of Candida,” Mycoses, vol. 44, no. 9-10, pp. 375–378, 2001. View at Publisher · View at Google Scholar · View at Scopus
  5. A. C. H. F. Sawaya, A. M. Palma, F. M. Caetano et al., “Comparative study of in vitro methods used to analyse the activity of propolis extracts with different compositions against species of Candida,” Letters in Applied Microbiology, vol. 35, no. 3, pp. 203–207, 2002. View at Publisher · View at Google Scholar · View at Scopus
  6. R. Raghukumar, L. Vali, D. Watson, J. Fearnley, and V. Seidel, “Antimethicillin-resistant Staphylococcus aureus (MRSA) activity of ‘pacific propolis’ and isolated prenylflavanones,” Phytotherapy Research, vol. 24, no. 8, pp. 1181–1187, 2010. View at Publisher · View at Google Scholar · View at Scopus
  7. A. Kujumgiev, I. Tsvetkova, Y. Serkedjieva, V. Bankova, R. Christov, and S. Popov, “Antibacterial, antifungal and antiviral activity of propolis of different geographic origin,” Journal of Ethnopharmacology, vol. 64, no. 3, pp. 235–240, 1999. View at Publisher · View at Google Scholar · View at Scopus
  8. M. Popova, S. Silici, O. Kaftanoglu, and V. Bankova, “Antibacterial activity of Turkish propolis and its qualitative and quantitative chemical composition,” Phytomedicine, vol. 12, no. 3, pp. 221–228, 2005. View at Publisher · View at Google Scholar · View at Scopus
  9. S. Castaldo and F. Capasso, “Propolis, an old remedy used in modern medicine,” Fitoterapia, vol. 73, supplement 1, pp. S1–S6, 2002. View at Publisher · View at Google Scholar · View at Scopus
  10. M. Marcucci, “Propolis: chemical composition, biological properties and therapeutic activity,” Apidologie, vol. 26, no. 2, pp. 83–99, 1995. View at Publisher · View at Google Scholar · View at Scopus
  11. V. S. Bankova, S. L. De Castro, and M. C. Marcucci, “Propolis: recent advances in chemistry and plant origin,” Apidologie, vol. 31, no. 1, pp. 3–15, 2000. View at Publisher · View at Google Scholar · View at Scopus
  12. S. Kumazawa, T. Hamasaka, and T. Nakayama, “Antioxidant activity of propolis of various geographic origins,” Food Chemistry, vol. 84, no. 3, pp. 329–339, 2004. View at Publisher · View at Google Scholar · View at Scopus
  13. V. Bankova, “Chemical diversity of propolis and the problem of standardization,” Journal of Ethnopharmacology, vol. 100, no. 1-2, pp. 114–117, 2005. View at Publisher · View at Google Scholar · View at Scopus
  14. A. Salatino, C. C. Fernandes-Silva, A. A. Righi, and M. L. F. Salatino, “Propolis research and the chemistry of plant products,” Natural Product Reports, vol. 28, no. 5, pp. 925–936, 2011. View at Publisher · View at Google Scholar · View at Scopus
  15. C. Velazquez, M. Navarro, A. Acosta et al., “Antibacterial and free-radical scavenging activities of Sonoran propolis,” Journal of Applied Microbiology, vol. 103, no. 5, pp. 1747–1756, 2007. View at Publisher · View at Google Scholar · View at Scopus
  16. M. B. Agüero, M. Gonzalez, B. Lima et al., “Argentinean propolis from Zuccagnia punctata cav. (Caesalpinieae) exudates: phytochemical characterization and antifungal activity,” Journal of Agricultural and Food Chemistry, vol. 58, no. 1, pp. 194–201, 2010. View at Publisher · View at Google Scholar · View at Scopus
  17. F. A. Santos, E. M. A. Bastos, M. Uzeda et al., “Antibacterial activity of Brazilian propolis and fractions against oral anaerobic bacteria,” Journal of Ethnopharmacology, vol. 80, no. 1, pp. 1–7, 2002. View at Publisher · View at Google Scholar · View at Scopus
  18. H. Koo, B. P. F. A. Gomes, P. L. Rosalen, G. M. B. Ambrosano, Y. K. Park, and J. A. Cury, “In vitro antimicrobial activity of propolis and Arnica montana against oral pathogens,” Archives of Oral Biology, vol. 45, no. 2, pp. 141–148, 2000. View at Publisher · View at Google Scholar · View at Scopus
  19. S. Mohammadzadeh, M. Shariatpanahi, M. Hamedi, R. Ahmadkhaniha, N. Samadi, and S. N. Ostad, “Chemical composition, oral toxicity and antimicrobial activity of Iranian propolis,” Food Chemistry, vol. 103, no. 4, pp. 1097–1103, 2007. View at Publisher · View at Google Scholar · View at Scopus
  20. R. M. Darwish, R. J. A. Fares, M. H. A. Zarga, and I. K. Nazer, “Antibacterial effect of Jordanian propolis and isolated flavonoids against human pathogenic bacteria,” African Journal of Biotechnology, vol. 9, no. 36, pp. 5966–5974, 2010. View at Google Scholar · View at Scopus
  21. N. Kalogeropoulos, S. J. Konteles, E. Troullidou, I. Mourtzinos, and V. T. Karathanos, “Chemical composition, antioxidant activity and antimicrobial properties of propolis extracts from Greece and Cyprus,” Food Chemistry, vol. 116, no. 2, pp. 452–461, 2009. View at Publisher · View at Google Scholar · View at Scopus
  22. A. G. Hegazi, F. K. Abd El Hady, and F. A. M. Abd Allah, “Chemical composition and antimicrobial activity of European propolis,” Zeitschrift fur Naturforschung, Section C, vol. 55, no. 1-2, pp. 70–75, 2000. View at Google Scholar · View at Scopus
  23. J. M. Grange and R. W. Davey, “Antibacterial properties of propolis (bee glue),” Journal of the Royal Society of Medicine, vol. 83, no. 3, pp. 159–160, 1990. View at Google Scholar · View at Scopus
  24. S. Boisard, A.-M. Le Ray, J. Gatto et al., “Chemical composition, antioxidant and anti-AGEs activities of a French poplar type propolis,” Journal of Agricultural and Food Chemistry, vol. 62, no. 6, pp. 1344–1351, 2014. View at Publisher · View at Google Scholar · View at Scopus
  25. V. F. de Castro Ishida, G. Negri, A. Salatino, and M. F. C. L. Bandeira, “A new type of Brazilian propolis: prenylated benzophenones in propolis from Amazon and effects against cariogenic bacteria,” Food Chemistry, vol. 125, no. 3, pp. 966–972, 2011. View at Publisher · View at Google Scholar · View at Scopus
  26. N. Sha, S.-H. Guan, Z.-Q. Lu et al., “Cytotoxic constituents of Chinese propolis,” Journal of Natural Products, vol. 72, no. 4, pp. 799–801, 2009. View at Publisher · View at Google Scholar · View at Scopus
  27. K. Alomar, V. Gaumet, M. Allain, G. Bouet, and A. Landreau, “Synthesis, crystal structure, characterisation, and antifungal activity of 3-thiophene aldehyde semicarbazone (3STCH), 2,3-thiophene dicarboxaldehyde bis(semicarbazone) (2,3BSTCH2) and their nickel (II) complexes,” Journal of Inorganic Biochemistry, vol. 115, pp. 36–43, 2012. View at Publisher · View at Google Scholar · View at Scopus
  28. National Commitee for Clinical Laboratory Standards, Reference Method for Broth Dilution Antifungal Susceptibility Testing of Yeasts, National Commitee for Clinical Laboratory Standards, Villanova, Pa, USA, 1997.
  29. National Commitee for Clinical Laboratory Standards, “Reference method for broth dilution antifungal susceptibility testing of filamentous fungi, approved standard,” NCCLS Document M38-A, Clinical and Laboratory Standards Institute, Villanova, Pa, USA, 2002. View at Google Scholar
  30. K. Alomar, A. Landreau, M. Kempf, M. A. Khan, M. Allain, and G. Bouet, “Synthesis, crystal structure, characterization of zinc(II), cadmium(II) complexes with 3-thiophene aldehyde thiosemicarbazone (3TTSCH). Biological activities of 3TTSCH and its complexes,” Journal of Inorganic Biochemistry, vol. 104, no. 4, pp. 397–404, 2010. View at Publisher · View at Google Scholar · View at Scopus
  31. F. Pellati, G. Orlandini, D. Pinetti, and S. Benvenuti, “HPLC-DAD and HPLC-ESI-MS/MS methods for metabolite profiling of propolis extracts,” Journal of Pharmaceutical and Biomedical Analysis, vol. 55, no. 5, pp. 934–948, 2011. View at Publisher · View at Google Scholar · View at Scopus
  32. S. I. Falcão, N. Vale, P. Gomes et al., “Phenolic profiling of Portuguese propolis by LC-MS spectrometry: uncommon propolis rich in flavonoid glycosides,” Phytochemical Analysis, vol. 24, no. 4, pp. 309–318, 2013. View at Publisher · View at Google Scholar · View at Scopus
  33. F. Li, S. Awale, Y. Tezuka, H. Esumi, and S. Kadota, “Study on the constituents of mexican propolis and their cytotoxic activity against PANC-1 human pancreatic cancer cells,” Journal of Natural Products, vol. 73, no. 4, pp. 623–627, 2010. View at Publisher · View at Google Scholar · View at Scopus
  34. P. Rubiolo, C. Casetta, C. Cagliero, H. Brevard, B. Sgorbini, and C. Bicchi, “Populus nigra L. bud absolute: a case study for a strategy of analysis of natural complex substances,” Analytical and Bioanalytical Chemistry, vol. 405, no. 4, pp. 1223–1235, 2013. View at Publisher · View at Google Scholar · View at Scopus
  35. M. Sova, A. Perdih, M. Kotnik et al., “Flavonoids and cinnamic acid esters as inhibitors of fungal 17β-hydroxysteroid dehydrogenase: a synthesis, QSAR and modelling study,” Bioorganic & Medicinal Chemistry, vol. 14, no. 22, pp. 7404–7418, 2006. View at Publisher · View at Google Scholar · View at Scopus
  36. R. Correia and P. DeShong, “Palladium-catalyzed arylation of allylic benzoates using hypervalent siloxane derivatives,” The Journal of Organic Chemistry, vol. 66, no. 21, pp. 7159–7165, 2001. View at Publisher · View at Google Scholar · View at Scopus
  37. S. Athikomkulchai, S. Awale, N. Ruangrungsi, S. Ruchirawat, and S. Kadota, “Chemical constituents of Thai propolis,” Fitoterapia, vol. 88, pp. 96–100, 2013. View at Publisher · View at Google Scholar · View at Scopus
  38. D. Bertelli, G. Papotti, L. Bortolotti, G. L. Marcazzan, and M. Plessi, “1H-NMR simultaneous identification of health-relevant compounds in propolis extracts,” Phytochemical Analysis, vol. 23, no. 3, pp. 260–266, 2012. View at Publisher · View at Google Scholar · View at Scopus
  39. J. Gripenberg, E. Honkanen, K. Silander, E. Stenhagen, and B. Thorell, “The structure of alpinone,” Acta Chemica Scandinavica, vol. 10, pp. 393–396, 1956. View at Publisher · View at Google Scholar
  40. Y. Park, B.-H. Moon, H. Yang, Y. Lee, E. Lee, and Y. Lim, “Complete assignments of NMR data of 13 hydroxymethoxyflavones,” Magnetic Resonance in Chemistry, vol. 45, no. 12, pp. 1072–1075, 2007. View at Publisher · View at Google Scholar · View at Scopus
  41. K. R. Markham, K. A. Mitchell, A. L. Wilkins, J. A. Daldy, and Y. Lu, “HPLC and GC-MS identification of the major organic constituents in New Zealand propolis,” Phytochemistry, vol. 42, no. 1, pp. 205–211, 1996. View at Publisher · View at Google Scholar · View at Scopus
  42. V. S. Bankova, “Synthesis of natural esters of substituted cinnamic acids,” Journal of Natural Products, vol. 53, no. 4, pp. 821–824, 1990. View at Publisher · View at Google Scholar · View at Scopus
  43. J.-M. Fang, W.-C. Su, and Y.-S. Cheng, “Flavonoids and stilbenes from armand pine,” Phytochemistry, vol. 27, no. 5, pp. 1395–1397, 1988. View at Publisher · View at Google Scholar · View at Scopus
  44. W. Greenaway, T. Scaysbrook, and F. R. Whatley, “Composition of propolis in Oxfordshire, U.K. and its relation to poplar bud exudate,” Zeitschrift für Naturforschung C: Journal of Biosciences, vol. 43, no. 3-4, pp. 301–304, 1988. View at Google Scholar
  45. F. Mazille, T. Schoettl, A. Lopez, and C. Pulgarin, “Physico-chemical properties and photo-reactivity relationship for para-substituted phenols in photo-assisted Fenton system,” Journal of Photochemistry and Photobiology A: Chemistry, vol. 210, no. 2-3, pp. 193–199, 2010. View at Publisher · View at Google Scholar · View at Scopus
  46. R. Sanyal and B. V. Badami, “A new Synthesis of 3-arylpropenoic acids and 5-phenyl-2,4- pentadienoic acid from 4-acetyl-3-arylsydnones and arylaldehydes,” Organic Communications, vol. 2, no. 2, pp. 42–48, 2009. View at Google Scholar · View at Scopus
  47. R. Yamauchi, K. Kato, S. Oida, J. Kanaeda, and Y. Ueno, “Benzyl caffeate, an antioxidative compound isolated from propolis,” Bioscience, Biotechnology and Biochemistry, vol. 56, no. 8, pp. 1321–1322, 2014. View at Publisher · View at Google Scholar
  48. A. H. Banskota, T. Nagaoka, L. Y. Sumioka et al., “Antiproliferative activity of the Netherlands propolis and its active principles in cancer cell lines,” Journal of Ethnopharmacology, vol. 80, no. 1, pp. 67–73, 2002. View at Publisher · View at Google Scholar · View at Scopus
  49. H. Koshino, S.-I. Terada, T. Yoshihara et al., “Three phenolic acid derivatives from stromata of Epichloe typhina on Phleum pratense,” Phytochemistry, vol. 27, no. 5, pp. 1333–1338, 1988. View at Publisher · View at Google Scholar · View at Scopus
  50. R. Cooper, H. E. Gottlieb, and D. Lavie, “New phenolic diglycerides from Aegilops ovata,” Phytochemistry, vol. 17, no. 9, pp. 1673–1675, 1978. View at Publisher · View at Google Scholar · View at Scopus
  51. M. B. Agüero, L. Svetaz, M. Sánchez et al., “Argentinean Andean propolis associated with the medicinal plant Larrea nitida Cav. (Zygophyllaceae). HPLC–MS and GC–MS characterization and antifungal activity,” Food and Chemical Toxicology, vol. 49, no. 9, pp. 1970–1978, 2011. View at Publisher · View at Google Scholar · View at Scopus
  52. J. L. Ríos and M. C. Recio, “Medicinal plants and antimicrobial activity,” Journal of Ethnopharmacology, vol. 100, no. 1-2, pp. 80–84, 2005. View at Publisher · View at Google Scholar · View at Scopus
  53. W. Krol, S. Scheller, J. Shani, G. Pietsz, and Z. Czuba, “Synergistic effect of ethanolic extract of propolis and antibiotics on the growth of Staphylococcus aureus,” Arzneimittel-Forschung, vol. 43, no. 5, pp. 607–609, 1993. View at Google Scholar · View at Scopus
  54. O. K. Mirzoeva, R. N. Grishanin, and P. C. Calder, “Antimicrobial action of propolis and some of its components: the effects on growth, membrane potential and motility of bacteria,” Microbiological Research, vol. 152, no. 3, pp. 239–246, 1997. View at Publisher · View at Google Scholar · View at Scopus
  55. J. S. Bonvehí, F. V. Coll, and R. E. Jordà, “The composition, active components and bacteriostatic activity of propolis in dietetics,” Journal of the American Oil Chemists' Society, vol. 71, no. 5, pp. 529–532, 1994. View at Publisher · View at Google Scholar · View at Scopus
  56. R. D. Wojtyczka, A. Dziedzic, D. Idzik et al., “Susceptibility of Staphylococcus aureus clinical isolates to propolis extract alone or in combination with antimicrobial drugs,” Molecules, vol. 18, no. 8, pp. 9623–9640, 2013. View at Publisher · View at Google Scholar · View at Scopus
  57. S. Stepanović, N. Antić, I. Dakić, and M. Švabić-Vlahović, “In vitro antimicrobial activity of propolis and synergism between propolis and antimicrobial drugs,” Microbiological Research, vol. 158, no. 4, pp. 353–357, 2003. View at Publisher · View at Google Scholar · View at Scopus
  58. A. Fernandes Jr., E. C. Balestrin, J. E. C. Betoni, R. D. O. Orsi, M. D. L. R. D. S. da Cunha, and A. C. Montelli, “Propolis: anti-Staphylococcus aureus activity and synergism with antimicrobial drugs,” Memórias do Instituto Oswaldo Cruz, vol. 100, no. 5, pp. 563–566, 2005. View at Publisher · View at Google Scholar · View at Scopus
  59. J. Davies and D. Davies, “Origins and evolution of antibiotic resistance,” Microbiology and Molecular Biology Reviews, vol. 74, no. 3, pp. 417–433, 2010. View at Publisher · View at Google Scholar · View at Scopus
  60. L. C. Pamplona-Zomenhan, B. C. Pamplona, C. B. da Silva, M. C. Marcucci, and L. M. J. Mimica, “Evaluation of the in vitro antimicrobial activity of an ethanol extract of Brazilian classified propolis on strains of Staphylococcus aureus,” Brazilian Journal of Microbiology, vol. 42, no. 4, pp. 1259–1264, 2011. View at Google Scholar · View at Scopus