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Evidence-Based Complementary and Alternative Medicine
Volume 2015, Article ID 296086, 10 pages
http://dx.doi.org/10.1155/2015/296086
Research Article

Antiviral Action of Hydromethanolic Extract of Geopropolis from Scaptotrigona postica against Antiherpes Simplex Virus (HSV-1)

1Instituto Butantan, Avenida Vital Brasil, No. 1500, Butantã, 05503-900 São Paulo, SP, Brazil
2Instituto Adolfo Lutz, Avenida Dr. Arnaldo 355, 01246-900 São Paulo, SP, Brazil
3CEBRID, Departamento de Medicina Preventiva, Universidade Federal de São Paulo, Rua Botucatu 740, Vila Clementino, 04023-900 São Paulo, SP, Brazil

Received 26 November 2014; Revised 13 February 2015; Accepted 15 February 2015

Academic Editor: Andreas Sandner-Kiesling

Copyright © 2015 Guilherme Rabelo Coelho 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. 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
  2. S. Huang, C.-P. Zhang, K. Wang, G. Li, and F.-L. Hu, “Recent advances in the chemical composition of propolis,” Molecules, vol. 19, no. 12, pp. 19610–19632, 2014. View at Publisher · View at Google Scholar
  3. R. P. Dutra, A. M. C. Nogueira, R. R. D. O. Marques, M. C. P. Costa, and M. N. S. Ribeiro, “Pharmacognostic evaluation of geopropolis of Melipona fasciculata Smith from Baixada Maranhense, Brazil,” Brazilian Journal of Pharmacognosy, vol. 18, no. 4, pp. 557–562, 2008. View at Publisher · View at Google Scholar · View at Scopus
  4. R. P. Dutra, B. V. D. Abreu, M. S. Cunha et al., “Phenolic acids, hydrolyzable tannins, and antioxidant activity of geopropolis from the stingless bee Melipona fasciculata smith,” Journal of Agricultural and Food Chemistry, vol. 62, no. 12, pp. 2549–2557, 2014. View at Publisher · View at Google Scholar · View at Scopus
  5. W. Kerr, “Abelhas indígenas brasileiras (meliponíneos) na polinização e na produção de mel, pólen, geopropolis e cera,” Informe Agropecuário, vol. 13, no. 1, pp. 15–27, 1987. View at Google Scholar
  6. P. Nogueira-Neto, A vida e criação de abelhas indígenas sem ferrão (Meliponinae), Nogueirapes, São Paulo, Brazil, 1997.
  7. M. G. da Cunha, M. Franchin, L. C. D. Galvão et al., “Antimicrobial and antiproliferative activities of stingless bee Melipona scutellaris geopropolis,” BMC Complementary and Alternative Medicine, vol. 13, article 23, 2013. View at Publisher · View at Google Scholar · View at Scopus
  8. E. C. C. da Silva, M. P. Muniz, R. D. C. S. Nunomura, S. M. Nunomura, and G. A. C. Zilse, “Phenolic constituents and antioxidant activity of geopropolis from two species of amazonian stingless bees,” Quimica Nova, vol. 36, no. 5, pp. 628–633, 2013. View at Publisher · View at Google Scholar · View at Scopus
  9. S. Alves De Souza, C. A. Camara, E. Monica Sarmento Da Silva, and T. M. S. Silva, “Composition and antioxidant activity of geopropolis collected by Melipona subnitida (jandaíra) bees,” Evidence-Based Complementary and Alternative Medicine, vol. 2013, Article ID 801383, 5 pages, 2013. View at Publisher · View at Google Scholar · View at Scopus
  10. J. F. Campos, U. P. dos Santos, L. F. B. Macorini et al., “Antimicrobial, antioxidant and cytotoxic activities of propolis from Melipona orbignyi (Hymenoptera, Apidae),” Food and Chemical Toxicology, vol. 65, no. 1, pp. 374–380, 2014. View at Publisher · View at Google Scholar · View at Scopus
  11. A. A. Righi, G. Negri, and A. Salatino, “Comparative chemistry of propolis from eight brazilian localities,” Evidence-Based Complementary and Alternative Medicine, vol. 2013, Article ID 267878, 14 pages, 2013. View at Publisher · View at Google Scholar · View at Scopus
  12. 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
  13. 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
  14. C. F. Massaro, M. Katouli, T. Grkovic et al., “Anti-staphylococcal activity of C-methyl flavanones from propolis of Australian stingless bees (Tetragonula carbonaria) and fruit resins of Corymbia torelliana (Myrtaceae),” Fitoterapia, vol. 95, no. 1, pp. 247–257, 2014. View at Publisher · View at Google Scholar · View at Scopus
  15. M. Boppré, S. M. Colegate, and J. A. Edgar, “Pyrrolizidine alkaloids of Echium vulgare honey found in pure pollen,” Journal of Agricultural and Food Chemistry, vol. 53, no. 3, pp. 594–600, 2005. View at Publisher · View at Google Scholar · View at Scopus
  16. M. Boppré, S. M. Colegate, J. A. Edgar, and O. W. Fischer, “Hepatotoxic pyrrolizidine alkaloids in pollen and drying-related implications for commercial processing of bee pollen,” Journal of Agricultural and Food Chemistry, vol. 56, no. 14, pp. 5662–5672, 2008. View at Publisher · View at Google Scholar · View at Scopus
  17. M. Boppré, “The ecological context of pyrrolizidine alkaloids in food, feed and forage: an overview,” Food Additives and Contaminants Part A: Chemistry, Analysis, Control, Exposure and Risk Assessment, vol. 28, no. 3, pp. 260–281, 2011. View at Publisher · View at Google Scholar · View at Scopus
  18. L. Cramer, H.-M. Schiebel, L. Ernst, and T. Beuerle, “Pyrrolizidine alkaloids in the food chain: development, validation, and application of a new HPLC-ESI-MS/MS sum parameter method,” Journal of Agricultural and Food Chemistry, vol. 61, no. 47, pp. 11382–11391, 2013. View at Publisher · View at Google Scholar · View at Scopus
  19. A. Azwa and S. E. Barton, “Aspects of herpes simplex virus: a clinical review,” Journal of Family Planning and Reproductive Health Care, vol. 35, no. 4, pp. 237–242, 2009. View at Publisher · View at Google Scholar · View at Scopus
  20. F. Morfin and D. Thouvenot, “Herpes simplex virus resistance to antiviral drugs,” Journal of Clinical Virology, vol. 26, no. 1, pp. 29–37, 2003. View at Publisher · View at Google Scholar · View at Scopus
  21. L. J. Reed and H. Muench, “A simple method of estimating fifty per cent endpoints,” American Journal of Epidemiology, vol. 27, no. 3, pp. 493–497, 1938. View at Google Scholar · View at Scopus
  22. T. K. Nagasse-Sugahara, J. J. Kisielius, M. Ueda-Ito et al., “Human vaccinia-like virus outbreaks in São Paulo and Goiás States, Brazil: virus detection, isolation and identification,” Revista do Instituto de Medicina Tropical de Sao Paulo, vol. 46, no. 6, pp. 315–322, 2004. View at Publisher · View at Google Scholar · View at Scopus
  23. S. J. Read and J. B. Kurtz, “Laboratory diagnosis of common viral infections of the central nervous system by using a single multiplex PCR screening assay,” Journal of Clinical Microbiology, vol. 37, no. 5, pp. 1352–1355, 1999. View at Google Scholar · View at Scopus
  24. R. E. Kingsley and N. L. Cole, “Preparation of cultured mammalian cells for transmission and scanning electron microscopy using Aclar film,” Journal of Electron Microscopy Technique, vol. 10, no. 1, pp. 77–85, 1988. View at Publisher · View at Google Scholar · View at Scopus
  25. G. Mariappan, N. Sundaraganesan, and S. Manoharan, “The spectroscopic properties of anticancer drug Apigenin investigated by using DFT calculations, FT-IR, FT-Raman and NMR analysis,” Spectrochimica Acta Part A: Molecular and Biomolecular Spectroscopy, vol. 95, no. 1, pp. 86–99, 2012. View at Publisher · View at Google Scholar · View at Scopus
  26. J. A. Manthey, “Fourier transform infrared spectroscopic analysis of the polymethoxylated flavone content of orange oil residues,” Journal of Agricultural and Food Chemistry, vol. 54, no. 9, pp. 3215–3218, 2006. View at Publisher · View at Google Scholar · View at Scopus
  27. B. Abad-García, L. A. Berrueta, S. Garmón-Lobato, B. Gallo, and F. Vicente, “A general analytical strategy for the characterization of phenolic compounds in fruit juices by high-performance liquid chromatography with diode array detection coupled to electrospray ionization and triple quadrupole mass spectrometry,” Journal of Chromatography A, vol. 1216, no. 28, pp. 5398–5415, 2009. View at Publisher · View at Google Scholar · View at Scopus
  28. S. C. Gouveia and P. C. Castilho, “Characterization of phenolic compounds in Helichrysum melaleucum by high-performance liquid chromatography with on-line ultraviolet and mass spectrometry detection,” Rapid Communications in Mass Spectrometry, vol. 24, no. 13, pp. 1851–1868, 2010. View at Publisher · View at Google Scholar · View at Scopus
  29. F. Ferreres, R. F. Gonçalves, A. Gil-Izquierdo et al., “Further knowledge on the phenolic profile of Colocasia esculenta (L.) Shott,” Journal of Agricultural and Food Chemistry, vol. 60, no. 28, pp. 7005–7015, 2012. View at Publisher · View at Google Scholar · View at Scopus
  30. D. Barreca, C. Bisignano, G. Ginestra et al., “Polymethoxylated, C- and O-glycosyl flavonoids in tangelo (Citrus reticulata × Citrus paradisi) juice and their influence on antioxidant properties,” Food Chemistry, vol. 141, no. 2, pp. 1481–1488, 2013. View at Publisher · View at Google Scholar · View at Scopus
  31. D. Barreca, E. Bellocco, U. Leuzzi, and G. Gattuso, “First evidence of C- and O-glycosyl flavone in blood orange (Citrus sinensis (L.) Osbeck) juice and their influence on antioxidant properties,” Food Chemistry, vol. 149, pp. 244–252, 2014. View at Publisher · View at Google Scholar · View at Scopus
  32. G. Negri, R. Mattei, and F. R. Mendes, “Antinociceptive activity of the HPLC- and MS-standardized hydroethanolic extract of Pterodon emarginatus Vogel leaves,” Phytomedicine, vol. 21, no. 4, pp. 1062–1069, 2014. View at Publisher · View at Google Scholar · View at Scopus
  33. U. Gašić, S. Kečkeš, D. Dabić et al., “Phenolic profile and antioxidant activity of Serbian polyfloral honeys,” Food Chemistry, vol. 145, no. 3, pp. 599–607, 2014. View at Publisher · View at Google Scholar
  34. Y. Sapozhnikova, “Development of liquid chromatography-tandem mass spectrometry method for analysis of polyphenolic compounds in liquid samples of grape juice, green tea and coffee,” Food Chemistry, vol. 150, no. 1, pp. 87–93, 2014. View at Publisher · View at Google Scholar · View at Scopus
  35. K. S. Robbins, Y. Ma, M. L. Wells, P. Greenspan, and R. B. Pegg, “Separation and characterization of phenolic compounds from U.S. pecans by liquid chromatography-tandem mass spectrometry,” Journal of Agricultural and Food Chemistry, vol. 62, no. 19, pp. 4332–4341, 2014. View at Publisher · View at Google Scholar · View at Scopus
  36. A. Delcambre and C. Saucier, “Identification of new flavan-3-ol monoglycosides by UHPLC-ESI-Q-TOF in grapes and wine,” Journal of Mass Spectrometry, vol. 47, no. 6, pp. 727–736, 2012. View at Publisher · View at Google Scholar · View at Scopus
  37. M. B. Ucar, G. Ucar, A. Pizzi, and O. Gonultas, “Characterization of Pinus brutia bark tannin by MALDI-TOF MS and 13C NMR,” Industrial Crops and Products, vol. 49, pp. 697–704, 2013. View at Publisher · View at Google Scholar · View at Scopus
  38. C. T. Griffin, M. Danaher, C. T. Elliott, D. Glenn Kennedy, and A. Furey, “Detection of pyrrolizidine alkaloids in commercial honey using liquid chromatography-ion trap mass spectrometry,” Food Chemistry, vol. 136, no. 3-4, pp. 1577–1583, 2013. View at Publisher · View at Google Scholar · View at Scopus
  39. F. Xu, J. A. Schillinger, M. R. Sternberg et al., “Seroprevalence and coinfection with herpes simplex virus type 1 and type 2 in the United States, 1988–1994,” Journal of Infectious Diseases, vol. 185, no. 8, pp. 1019–1024, 2002. View at Publisher · View at Google Scholar · View at Scopus
  40. G. Andrei and R. Snoeck, “Herpes simplex virus drug-resistance: new mutations and insights,” Current Opinion in Infectious Diseases, vol. 26, no. 6, pp. 551–560, 2013. View at Publisher · View at Google Scholar · View at Scopus
  41. M. T. H. Khan, A. Ather, K. D. Thompson, and R. Gambari, “Extracts and molecules from medicinal plants against herpes simplex viruses,” Antiviral Research, vol. 67, no. 2, pp. 107–119, 2005. View at Publisher · View at Google Scholar · View at Scopus
  42. C. Koch, J. Reichling, J. Schneele, and P. Schnitzler, “Inhibitory effect of essential oils against herpes simplex virus type 2,” Phytomedicine, vol. 15, no. 1-2, pp. 71–78, 2008. View at Publisher · View at Google Scholar · View at Scopus
  43. M. Amoros, E. Lurton, J. Boustie, L. Girre, F. Sauvager, and M. Cormier, “Comparison of the anti-herpes simplex virus activities of propolis and 3-methyl-but-2-enyl caffeate,” Journal of Natural Products, vol. 57, no. 5, pp. 644–647, 1994. View at Publisher · View at Google Scholar · View at Scopus
  44. M. Huleihel and V. Isanu, “Anti-herpes simplex virus effect of an aqueous extract of propolis,” Israel Medical Association Journal, vol. 4, no. 11, pp. 923–927, 2002. View at Google Scholar · View at Scopus
  45. J. Melchjorsen, S. Matikainen, and S. R. Paludan, “Activation and evasion of innate antiviral immunity by herpes simplex virus,” Viruses, vol. 1, no. 3, pp. 737–759, 2009. View at Publisher · View at Google Scholar · View at Scopus
  46. T. C. I. Mettenleiter, B. G. Klupp, and H. Granzow, “Herpesvirus assembly: an update,” Virus Research, vol. 143, no. 2, pp. 222–234, 2009. View at Publisher · View at Google Scholar · View at Scopus
  47. P. Schnitzler, A. Neuner, S. Nolkemper et al., “Antiviral activity and mode of action of propolis extracts and selected compounds,” Phytotherapy Research, vol. 24, no. 1, pp. S20–S28, 2010. View at Publisher · View at Google Scholar · View at Scopus
  48. I. T. Silva, G. M. Costa, P. H. Stoco, E. P. Schenkel, F. H. Reginatto, and C. M. O. Simões, “In vitro antiherpes effects of a C-glycosylflavonoid-enriched fraction of Cecropia glaziovii Sneth,” Letters in Applied Microbiology, vol. 51, no. 2, pp. 143–148, 2010. View at Publisher · View at Google Scholar · View at Scopus
  49. D. D. Orhan, B. Özçelik, S. Özgen, and F. Ergun, “Antibacterial, antifungal, and antiviral activities of some flavonoids,” Microbiological Research, vol. 165, no. 6, pp. 496–504, 2010. View at Publisher · View at Google Scholar · View at Scopus
  50. Y. Wang, M. Chen, J. Zhang et al., “Flavone C-glycosides from the leaves of Lophatherum gracile and their in vitro antiviral activity,” Planta Medica, vol. 78, no. 1, pp. 46–51, 2012. View at Publisher · View at Google Scholar · View at Scopus
  51. P. Ji, C. M. Chen, Y. A. Hu et al., “Antiviral activity of Paulownia tomentosa against enterovirus 71 of hand, foot, and mouth disease,” Biological & Pharmaceutical Bulletin, vol. 38, no. 1, pp. 1–6, 2015. View at Publisher · View at Google Scholar
  52. X. W. Lv, M. Qiu, D. Y. Chen, N. Zheng, Y. Jin, and Z. W. Wu, “Apigenin inhibits enterovirus 71 replication through suppressing viral IRES activity and modulating cellular JNK pathway,” Antiviral Research, vol. 109, no. 1, pp. 30–41, 2014. View at Publisher · View at Google Scholar
  53. L. Yarmolinsky, M. Huleihel, M. Zaccai, and S. Ben-Shabat, “Potent antiviral flavone glycosides from Ficus benjamina leaves,” Fitoterapia, vol. 83, no. 2, pp. 362–367, 2012. View at Publisher · View at Google Scholar · View at Scopus
  54. S. Nolkemper, J. Reichling, K. H. Sensch, and P. Schnitzler, “Mechanism of herpes simplex virus type 2 suppression by propolis extracts,” Phytomedicine, vol. 17, no. 2, pp. 132–138, 2010. View at Publisher · View at Google Scholar · View at Scopus
  55. P. Schnitzler, S. Schneider, F. C. Stintzing, R. Carle, and J. Reichling, “Efficacy of an aqueous Pelargonium sidoides extract against herpesvirus,” Phytomedicine, vol. 15, no. 12, pp. 1108–1116, 2008. View at Publisher · View at Google Scholar · View at Scopus
  56. M. Kurokawa, T. Shimizu, Y. Takeshita et al., “Efficacy of Brazilian propolis against herpes simplex virus type 1 infection in mice and their modes of antiherpetic efficacies,” Evidence-Based Complementary and Alternative Medicine, vol. 2011, Article ID 976196, 9 pages, 2011. View at Publisher · View at Google Scholar · View at Scopus
  57. F. Jiang, W. Chen, K. Yi et al., “The evaluation of catechins that contain a galloyl moiety as potential HIV-1 integrase inhibitors,” Clinical Immunology, vol. 137, no. 3, pp. 347–356, 2010. View at Publisher · View at Google Scholar · View at Scopus
  58. H.-Y. Ho, M.-L. Cheng, S.-F. Weng, Y.-L. Leu, and D. T.-Y. Chiu, “Antiviral effect of epigallocatechin gallate on enterovirus 71,” Journal of Agricultural and Food Chemistry, vol. 57, no. 14, pp. 6140–6147, 2009. View at Publisher · View at Google Scholar · View at Scopus
  59. K. Kuwata, T. Takemura, T. Urushisaki et al., “3,4-dicaffeoylquinic acid, a major constituent of Brazilian propolis, increases TRAIL expression and extends the lifetimes of mice infected with the influenza a virus,” Evidence-based Complementary and Alternative Medicine, vol. 2012, Article ID 946867, 7 pages, 2012. View at Publisher · View at Google Scholar · View at Scopus