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BioMed Research International
Volume 2017 (2017), Article ID 5948936, 7 pages
https://doi.org/10.1155/2017/5948936
Research Article

Teratogenic Effect of Usnic Acid from Cladonia substellata Vainio during Organogenesis

1Laboratory of Chemistry of Natural Products, Department of Biochemistry, UFPE, Recife, PE, Brazil
2Department of Morphology and Animal Physiology, UFRPE, Recife, PE, Brazil
3Laboratory Biotechnology and Pharmaceuticals, Academic Center Academic of Vitória, UFPE, Recife, PE, Brazil
4Department of Geographical Sciences, UFPE, Recife, PE, Brazil

Correspondence should be addressed to E. C. Pereira; moc.liamg@sirallicitrev

Received 30 September 2016; Revised 6 January 2017; Accepted 18 January 2017; Published 27 February 2017

Academic Editor: Paul M. Tulkens

Copyright © 2017 C. R. Silva 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. K. Müller, “Pharmaceutically relevant metabolites from lichens,” Applied Microbiology and Biotechnology, vol. 56, no. 1-2, pp. 9–16, 2001. View at Publisher · View at Google Scholar · View at Scopus
  2. M. Cocchietto, N. Skert, P. Nimis, and G. Sava, “A review on usnic acid, an interesting natural compound,” Naturwissenschaften, vol. 89, no. 4, pp. 137–146, 2002. View at Publisher · View at Google Scholar · View at Scopus
  3. C. S. Vijayakumar, S. Viswanathan, M. Kannappa Reddy, S. Parvathavarthini, A. B. Kundu, and E. Sukumar, “Anti-inflammatory activity of (+)-usnic acid,” Fitoterapia, vol. 71, no. 5, pp. 564–566, 2000. View at Publisher · View at Google Scholar · View at Scopus
  4. N. P. da Silva Santos, S. C. Nascimento, M. S. O. Wanderley et al., “Nanoencapsulation of usnic acid: an attempt to improve antitumour activity and reduce hepatotoxicity,” European Journal of Pharmaceutics and Biopharmaceutics, vol. 64, no. 2, pp. 154–160, 2006. View at Publisher · View at Google Scholar · View at Scopus
  5. N. K. Honda, F. R. Pavan, R. G. Coelho et al., “Antimycobacterial activity of lichen substances,” Phytomedicine, vol. 17, no. 5, pp. 328–332, 2010. View at Publisher · View at Google Scholar · View at Scopus
  6. B. C. Behera, N. Mahadik, and M. Morey, “Antioxidative and cardiovascular-protective activities of metabolite usnic acid and psoromic acid produced by lichen species Usnea complanata under submerged fermentation,” Pharmaceutical Biology, vol. 50, no. 8, pp. 968–979, 2012. View at Publisher · View at Google Scholar · View at Scopus
  7. B. Segatore, P. Bellio, D. Setacci et al., “In vitro interaction of usnic acid in combination with antimicrobial agents against methicillin-resistant Staphylococcus aureus clinical isolates determined by FICI and Δe model methods,” Phytomedicine, vol. 19, no. 3-4, pp. 341–347, 2012. View at Publisher · View at Google Scholar · View at Scopus
  8. D. N. Sokolov, V. V. Zarubaev, A. A. Shtro et al., “Anti-viral activity of (−)- and (+)-usnic acids and their derivatives against influenza virus A(H1N1)2009,” Bioorganic and Medicinal Chemistry Letters, vol. 22, no. 23, pp. 7060–7064, 2012. View at Publisher · View at Google Scholar · View at Scopus
  9. F. Brisdelli, M. Perilli, D. Sellitri et al., “Cytotoxic activity and antioxidant capacity of purified lichen metabolites: an in vitro study,” Phytotherapy Research, vol. 27, no. 3, pp. 431–437, 2013. View at Publisher · View at Google Scholar · View at Scopus
  10. M. C. B. Martins, M. C. Silva, L. R. S. Silva et al., “Usnic acid potassium salt: an alternative for the control of Biomphalaria glabrata (Say, 1818),” PLoS ONE, vol. 9, no. 11, Article ID e111102, 2014. View at Publisher · View at Google Scholar · View at Scopus
  11. D. M. Bissell, G. J. Gores, D. L. Laskin, and J. H. Hoofnagle, “Drug-induced liver injury: mechanisms and test systems,” Hepatology, vol. 33, no. 4, pp. 1009–1013, 2001. View at Publisher · View at Google Scholar · View at Scopus
  12. J. T. Favreau, M. L. Ryu, G. Braunstein et al., “Severe hepatotoxicity associated with the dietary supplement LipoKinetix,” Annals of Internal Medicine, vol. 136, no. 8, pp. 590–595, 2002. View at Publisher · View at Google Scholar · View at Scopus
  13. G. W. Neff, K. Rajender Reddy, F. A. Durazo, D. Meyer, R. Marrero, and N. Kaplowitz, “Severe hepatotoxicity associated with the use of weight loss diet supplements containing ma huang or usnic acid,” Journal of Hepatology, vol. 41, no. 6, pp. 1062–1064, 2004. View at Publisher · View at Google Scholar · View at Scopus
  14. D. Han, K. Matsumaru, D. Rettori, and N. Kaplowitz, “Usnic acid-induced necrosis of cultured mouse hepatocytes: inhibition of mitochondrial function and oxidative stress,” Biochemical Pharmacology, vol. 67, no. 3, pp. 439–451, 2004. View at Publisher · View at Google Scholar · View at Scopus
  15. W. Sanchez, J. T. Maple, L. J. Burgart, and P. S. Kamath, “Severe hepatotoxicity associated with use of a dietary supplement containing usnic acid,” Mayo Clinic Proceedings, vol. 81, no. 4, pp. 541–544, 2006. View at Publisher · View at Google Scholar · View at Scopus
  16. S. Chen, V. N. Dobrovolsky, F. Liu et al., “The role of autophagy in usnic acid-induced toxicity in hepatic cells,” Toxicological Sciences, vol. 142, no. 1, pp. 33–44, 2014. View at Publisher · View at Google Scholar · View at Scopus
  17. P. Pramyothin, W. Janthasoot, N. Pongnimitprasert, S. Phrukudom, and N. Ruangrungsi, “Hepatotoxic effect of (+) usnic acid from Usnea siamensis Wainio in rats, isolated rat hepatocytes and isolated rat liver mitochondria,” Journal of Ethnopharmacology, vol. 90, no. 2-3, pp. 381–387, 2004. View at Publisher · View at Google Scholar · View at Scopus
  18. A. Joseph, T. Lee, C. L. Moland et al., “Effect of (+)-usnic acid on mitochondrial functions as measured by mitochondria-specific oligonucleotide microarray in liver of B6C3F1 mice,” Mitochondrion, vol. 9, no. 2, pp. 149–158, 2009. View at Publisher · View at Google Scholar · View at Scopus
  19. S. B. M. Barros and S. C. Davino, “Avaliação da toxicidade,” in Fundamentos de Toxicologia, vol. 3, pp. 59–71, Atheneu, São Paulo, Brazil, 2008. View at Google Scholar
  20. I. P. Lemonica, S. Oga, M. M. A. Camargo, and J. A. O. Batistuzzo, Fundamentos de Toxicologia, Editora Atheneu, São Paulo, Brazil, 3rd edition, 2008.
  21. L. Schüler-Faccini, J. C. Leite, M. T. Sanseverino, and R. M. Peres, “Avaliação de teratógenos potenciais na população brasileira,” Ciência & Saúde Coletiva, vol. 7, no. 1, pp. 65–71, 2002. View at Publisher · View at Google Scholar
  22. L. Guo, Q. Shi, J.-L. Fang et al., “Review of usnic acid and Usnea barbata toxicity,” Journal of Environmental Science and Health—Part C Environmental Carcinogenesis and Ecotoxicology Reviews, vol. 26, no. 4, pp. 317–338, 2008. View at Publisher · View at Google Scholar · View at Scopus
  23. E. Einarsdóttir, J. Groeneweg, G. G. Björnsdóttir et al., “Cellular mechanisms of the anticancer effects of the lichen compound usnic acid,” Planta Medica, vol. 76, no. 10, pp. 969–974, 2010. View at Publisher · View at Google Scholar · View at Scopus
  24. C. Kohlhardt-Floehr, F. Boehm, S. Troppens, J. Lademann, and T. G. Truscott, “Prooxidant and antioxidant behaviour of usnic acid from lichens under UVB-light irradiation - Studies on human cells,” Journal of Photochemistry and Photobiology B: Biology, vol. 101, no. 1, pp. 97–102, 2010. View at Publisher · View at Google Scholar · View at Scopus
  25. B. Paudel, H. D. Bhattarai, H. K. Lee, H. Oh, H. W. Shin, and J. H. Yim, “Antibacterial activities of Ramalin, usnic acid and its three derivatives isolated from the antarctic lichen Ramalina terebrata,” Zeitschrift fur Naturforschung C, vol. 65, no. 1-2, pp. 34–38, 2010. View at Google Scholar · View at Scopus
  26. R. Lucarini, M. G. Tozatti, A. I. De Oliveira et al., “Antimycobacterial activity of Usnea steineri and its major constituent (+)-usnic acid,” African Journal of Biotechnology, vol. 11, pp. 4636–4639, 2014. View at Google Scholar
  27. Y. Asahina and S. Shibata, Chemistry of Lichen Substances, Japanese Society for the Promotion of Science, Tokyo, Japan, 1954.
  28. O. E. Virtanen and N. Karki, “On the toxicity of an usnic acid preparation with the trade name USNO,” Suomen Kemistilehti, vol. 29, pp. 225–226, 1956. View at Google Scholar
  29. M. Windholz, The Merck Index: An Encyclopedia of Chemicals and Drugs, seccion 9556. Usnic Acid, Merck & Co., Rahway, NJ, USA, 9th edition, 1976.
  30. L. Y.-S. Chan, P.-Y. Chiu, and T.-K. Lau, “A study of hypericin-induced teratogenicity during organogenesis using a whole rat embryo culture model,” Fertility and Sterility, vol. 76, no. 5, pp. 1073–1074, 2001. View at Publisher · View at Google Scholar · View at Scopus
  31. B. Gregoretti, M. Stebel, L. Candussio, E. Crivellato, F. Bartoli, and G. Decorti, “Toxicity of Hypericum perforatum (St. John's wort) administered during pregnancy and lactation in rats,” Toxicology and Applied Pharmacology, vol. 200, no. 3, pp. 201–205, 2004. View at Publisher · View at Google Scholar · View at Scopus
  32. A. C. P. Silva, D. E. P. De Faria, N. B. D. E. Santo Borges, I. A. De Souza, V. M. Peters, and M. De Oliveira Guerra, “Toxicological screening of Euphorbia tirucalli L.: developmental toxicity studies in rats,” Journal of Ethnopharmacology, vol. 110, no. 1, pp. 154–159, 2007. View at Publisher · View at Google Scholar
  33. C. B. Hollenbach, C. E. Bortolini, J. M. Batista et al., “Neonatal development and teratogenic potential of Wistar rats offspring in the study of reproductive toxicity of two commercial phytotherapic preparations with soy Glycine max (L.) Merr,” Arquivo Brasileiro de Medicina Veterinaria e Zootecnia, vol. 62, no. 4, pp. 845–852, 2010. View at Publisher · View at Google Scholar · View at Scopus
  34. T. de Sousa Soares, D. C. Damasceno, W. D. G. Kempinas et al., “Effect of himatanthus sucuuba in maternal reproductive outcome and fetal anomaly frequency in rats,” Birth Defects Research Part B—Developmental and Reproductive Toxicology, vol. 104, no. 5, pp. 190–195, 2015. View at Publisher · View at Google Scholar · View at Scopus
  35. A. F. Louzada, H. Ramos, J. K. Rodrigues, and L. R. Silva, “Desenvolvimento embrionário em ratas tratadas com tacrolimus durante a fase de pré-implantação,” Revista Brasileira de Ginecologia e Obstetrícia, vol. 30, pp. 219–224, 2008. View at Google Scholar
  36. E. R. De Almeida, F. R. S. Lucena, C. V. N. S. Silva et al., “Toxicological assessment of beta-lapachone on organs from pregnant and non-pregnant rats,” Phytotherapy Research, vol. 23, no. 9, pp. 1276–1280, 2009. View at Publisher · View at Google Scholar · View at Scopus
  37. G. J. Krinke, “History, strains and models,” in The Laboratory Rat, G. R. Bullock, Ed., p. 316, Academic Press, San Diego, Calif, USA, 2000. View at Google Scholar
  38. P. E. Sharp and M. C. Laregina, “Experimental methodology,” in The Laboratory Rat, CRC Press, 1998. View at Google Scholar
  39. M. R. S. Toledo, M. T. L. P. Peres, M. C. Vieira, T. S. C. Bazzano, and I. R. Teixeira, “Fitoxicidade do extrato aquoso Duguetia furfuraceae (St. Hil) B em ratas (Rattus norvegicus),” Revista Brasileira de Plantas Medicinais. Botucatu, vol. 8, pp. 218–222, 2006. View at Google Scholar
  40. M. M. Bernardi, Farmacologia Aplicada à Medicina Veterinária, Editora Guanabara Koogan, 2nd edition, 2003.
  41. G. K. Michalopoulos and M. DeFrances, “Liver regeneration,” Advances in Biochemical Engineering/Biotechnology, vol. 93, pp. 101–134, 2005. View at Publisher · View at Google Scholar · View at Scopus
  42. G. K. Michalopoulos, “Liver regeneration,” Journal of Cellular Physiology, vol. 213, no. 2, pp. 286–300, 2007. View at Publisher · View at Google Scholar · View at Scopus
  43. K. Si-Tayeb, F. P. Lemaigre, and S. A. Duncan, “Organogenesis and development of the liver,” Developmental Cell, vol. 18, no. 2, pp. 175–189, 2010. View at Publisher · View at Google Scholar · View at Scopus
  44. Y. Ito, N. W. Bethea, E. R. Abril, and R. S. McCuskey, “Early hepatic microvascular injury in response to acetaminophen toxicity,” Microcirculation, vol. 10, no. 5, pp. 391–400, 2003. View at Publisher · View at Google Scholar · View at Scopus
  45. M. Ono, B. Yu, E. G. Hardison, M.-A. A. Mastrangelo, and D. J. Tweardy, “Increased susceptibility to liver injury after hemorrhagic shock in rats chronically fed ethanol: role of nuclear factor-κB, interleukin-6, and granulocyte colony-stimulating factor,” Shock (Augusta, Ga.), vol. 21, no. 6, pp. 519–525, 2004. View at Publisher · View at Google Scholar · View at Scopus
  46. G. Kolios, V. Valatas, and E. Kouroumalis, “Role of Kupffer cells in the pathogenesis of liver disease,” World Journal of Gastroenterology, vol. 12, no. 46, pp. 7413–7420, 2006. View at Publisher · View at Google Scholar · View at Scopus