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Evidence-Based Complementary and Alternative Medicine
Volume 2016 (2016), Article ID 3475356, 15 pages
http://dx.doi.org/10.1155/2016/3475356
Research Article

Hydroalcoholic Extract from Inflorescences of Achyrocline satureioides (Compositae) Ameliorates Dextran Sulphate Sodium-Induced Colitis in Mice by Attenuation in the Production of Inflammatory Cytokines and Oxidative Mediators

Programa de Pós-Graduação em Ciências Farmacêuticas (PPGCF), Núcleo de Investigacões Químico-Farmacêuticas (NIQFAR), Universidade do Vale do Itajaí (UNIVALI), Rua Uruguai, 458, Centro, 88302-202 Itajaí, SC, Brazil

Received 15 June 2016; Accepted 21 September 2016

Academic Editor: Roberto K. N. Cuman

Copyright © 2016 Luisa Mota da 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. B. C. Da Silva, A. C. Lyra, R. Rocha, and G. O. Santana, “Epidemiology, demographic characteristics and prognostic predictors of ulcerative colitis,” World Journal of Gastroenterology, vol. 20, no. 28, pp. 9458–9467, 2014. View at Publisher · View at Google Scholar · View at Scopus
  2. N. A. Molodecky, I. S. Soon, D. M. Rabi et al., “Increasing incidence and prevalence of the inflammatory bowel diseases with time, based on systematic review,” Gastroenterology, vol. 142, no. 1, pp. 46–54.e42, 2012. View at Publisher · View at Google Scholar · View at Scopus
  3. A. Di Sabatino, P. Biancheri, L. Rovedatti, T. T. MacDonald, and G. R. Corazza, “Recent advances in understanding ulcerative colitis,” Internal and Emergency Medicine, vol. 7, no. 2, pp. 103–111, 2012. View at Publisher · View at Google Scholar · View at Scopus
  4. A. Kornbluth and D. B. Sachar, “Ulcerative colitis practice guidelines in adults: American college of gastroenterology, practice parameters committee,” The American Journal of Gastroenterology, vol. 105, no. 3, pp. 501–523, 2010. View at Publisher · View at Google Scholar · View at Scopus
  5. J. D. Feuerstein and A. S. Cheifetz, “Ulcerative colitis: epidemiology, diagnosis, and management,” Mayo Clinic Proceedings, vol. 89, no. 11, pp. 1553–1563, 2014. View at Publisher · View at Google Scholar · View at Scopus
  6. C. Bezzio, F. Furfaro, R. De Franchis, G. Maconi, A. K. Asthana, and S. Ardizzone, “Ulcerative colitis: current pharmacotherapy and future directions,” Expert Opinion on Pharmacotherapy, vol. 15, no. 12, pp. 1659–1670, 2014. View at Publisher · View at Google Scholar · View at Scopus
  7. H. Sales-Campos, P. J. Basso, V. B. F. Alves et al., “Classical and recent advances in the treatment of inflammatory bowel diseases,” Brazilian Journal of Medical and Biological Research, vol. 48, no. 2, pp. 96–107, 2015. View at Publisher · View at Google Scholar · View at Scopus
  8. G. Ferraro, C. Anesini, A. Ouviña et al., “Total phenolic content and antioxidant activity of extracts of Achyrocline satureioides flowers from different zones in Argentina,” Latin American Journal of Pharmacy, vol. 27, no. 4, pp. 626–628, 2008. View at Google Scholar · View at Scopus
  9. M. Bolson, S. R. Hefler, E. I. Dall'Oglio Chaves, A. Gasparotto Junior, and E. L. Cardozo Junior, “Ethno-medicinal study of plants used for treatment of human ailments, with residents of the surrounding region of forest fragments of Paraná, Brazil,” Journal of Ethnopharmacology, vol. 161, pp. 1–10, 2015. View at Publisher · View at Google Scholar · View at Scopus
  10. C. Kadarian, A. M. Broussalis, J. Miño et al., “Hepatoprotective activity of Achyrocline satureioides (Lam) D. C.,” Pharmacological Research, vol. 45, no. 1, pp. 57–61, 2002. View at Publisher · View at Google Scholar · View at Scopus
  11. M. Cosentino, R. Bombelli, E. Carcano et al., “Immunomodulatory properties of Achyrocline satureioides (Lam.) D.C. infusion: a study on human leukocytes,” Journal of Ethnopharmacology, vol. 116, no. 3, pp. 501–507, 2008. View at Publisher · View at Google Scholar · View at Scopus
  12. L. Taylor, The Healing Power of Rainforest Herbs—A Guide to Understanding and Using Herbal Medicinals, Square One, Garden City Park, NY, USA, 2005.
  13. C. M. O. Simões, E. P. Schenkel, L. Bauer, and A. Langeloh, “Pharmacological investigations on Achyrocline satureioides (Lam.) DC., compositae,” Journal of Ethnopharmacology, vol. 22, no. 3, pp. 281–293, 1988. View at Publisher · View at Google Scholar · View at Scopus
  14. E. D. Barioni, J. R. Santin, I. D. Machado et al., “Achyrocline satureioides (Lam.) D.C. hydroalcoholic extract inhibits neutrophil functions related to innate host defense,” Evidence-Based Complementary and Alternative Medicine, vol. 2013, Article ID 787916, 12 pages, 2013. View at Publisher · View at Google Scholar · View at Scopus
  15. J. R. Santin, M. Lemos, L. C. K. Júnior, R. Niero, and S. F. de Andrade, “Antiulcer effects of Achyrocline satureoides (Lam.) DC (Asteraceae) (Marcela), a folk medicine plant, in different experimental models,” Journal of Ethnopharmacology, vol. 130, no. 2, pp. 334–339, 2010. View at Publisher · View at Google Scholar · View at Scopus
  16. A. Arnous, D. P. Makris, and P. Kefalas, “Effect of principal polyphenolic components in relation to antioxidant characteristics of aged red wines,” Journal of Agricultural and Food Chemistry, vol. 49, no. 12, pp. 5736–5742, 2001. View at Publisher · View at Google Scholar · View at Scopus
  17. J. L. Lamaison, C. Petijean-Freytet, and A. Carnat, “Teneurs en acide rosmarinique, en dérivés hydroxycinnamiques totaux et activités antioxydantes chez les Apiacées, les Borraginacées et les Lamiacées médicinales,” Annales Pharmaceutiques Françaises, vol. 48, no. 2, pp. 103–108, 1990. View at Google Scholar
  18. B. Chassaing, J. D. Aitken, M. Malleshappa, and M. Vijay-Kumar, “Dextran sulfate sodium (DSS)-induced colitis in mice,” Current Protocols in Immunology, vol. 104, unit 15-25, 2014. View at Publisher · View at Google Scholar · View at Scopus
  19. M. P. Utrilla, M. J. Peinado, R. Ruiz et al., “Pea (Pisum sativum L.) seed albumin extracts show anti-inflammatory effect in the DSS model of mouse colitis,” Molecular Nutrition and Food Research, vol. 59, no. 4, pp. 807–819, 2015. View at Publisher · View at Google Scholar · View at Scopus
  20. D. Camuesco, M. Comalada, M. E. Rodríguez-Cabezas et al., “The intestinal anti-inflammatory effect of quercitrin is associated with an inhibition in iNOS expression,” British Journal of Pharmacology, vol. 143, no. 7, pp. 908–918, 2004. View at Publisher · View at Google Scholar · View at Scopus
  21. J. Sedlak and R. H. Lindsay, “Estimation of total, protein-bound, and nonprotein sulfhydryl groups in tissue with Ellman's reagent,” Analytical Biochemistry, vol. 25, no. 1, pp. 192–205, 1968. View at Publisher · View at Google Scholar · View at Scopus
  22. Z.-Y. Jiang, J. V. Hunt, and S. P. Wolff, “Ferrous ion oxidation in the presence of xylenol orange for detection of lipid hydroperoxide in low density lipoprotein,” Analytical Biochemistry, vol. 202, no. 2, pp. 384–389, 1992. View at Publisher · View at Google Scholar · View at Scopus
  23. S. Marklund and G. Marklund, “Involvement of the superoxide anion radical in the autoxidation of pyrogallol and a convenient assay for superoxide dismutase,” European Journal of Biochemistry, vol. 47, no. 3, pp. 469–474, 1974. View at Publisher · View at Google Scholar · View at Scopus
  24. M. S. Blois, “Antioxidant determinations by the use of a stable free radical,” Nature, vol. 181, no. 4617, pp. 1199–1200, 1958. View at Publisher · View at Google Scholar · View at Scopus
  25. F.-A. Chen, A.-B. Wu, and C.-Y. Chen, “The influence of different treatments on the free radical scavenging activity of burdock and variations of its active components,” Food Chemistry, vol. 86, no. 4, pp. 479–484, 2004. View at Publisher · View at Google Scholar · View at Scopus
  26. P. P. Bradley, D. A. Priebat, R. D. Christensen, and G. Rothstein, “Measurement of cutaneous inflammation: estimation of neutrophil content with an enzyme marker,” The Journal of Investigative Dermatology, vol. 78, no. 3, pp. 206–209, 1982. View at Publisher · View at Google Scholar · View at Scopus
  27. L. M. De Young, J. B. Kheifets, S. J. Ballaron, and J. M. Young, “Edema and cell infiltration in the phorbol ester-treated mouse ear are temporally separate and can be differentially modulated by pharmacologic agents,” Agents and Actions, vol. 26, no. 3-4, pp. 335–341, 1989. View at Publisher · View at Google Scholar · View at Scopus
  28. M. B. Grisham, G. G. Johnson, and J. R. Lancaster Jr., “Quantitation of nitrate and nitrite in extracellular fluids,” Methods in Enzymology, vol. 268, pp. 237–246, 1996. View at Publisher · View at Google Scholar
  29. H. Zhang, H. Wu, L. Liu, H. Li, D. Q. Shih, and X. Zhang, “1,25-dihydroxyvitamin D3 regulates the development of chronic colitis by modulating both T helper (Th)1 and Th17 activation,” APMIS, vol. 123, no. 6, pp. 490–501, 2015. View at Publisher · View at Google Scholar · View at Scopus
  30. L. Kruidenier, I. Kuiper, C. B. H. W. Lamers, and H. W. Verspaget, “Intestinal oxidative damage in inflammatory bowel disease: semi-quantification, localization, and association with mucosal antioxidants,” The Journal of Pathology, vol. 201, no. 1, pp. 28–36, 2003. View at Publisher · View at Google Scholar · View at Scopus
  31. Y. Yeom and Y. Kim, “The Sasa quelpaertensis leaf extract inhibits the dextran sulfate sodium-induced mouse colitis through modulation of antioxidant enzyme expression,” Journal of Cancer Prevention, vol. 20, no. 2, pp. 136–146, 2015. View at Publisher · View at Google Scholar
  32. J. R. Santin, Marivanelemos, L. C. Klein-Júnior et al., “Gastro protective and anti-Helicobacter pylori effects of a flavonoid rich fraction obtained from Achyrocline satureoides (LAM) D.C,” International Journal of Pharmacy and Pharmaceutical Sciences, vol. 6, no. 7, pp. 417–422, 2014. View at Google Scholar · View at Scopus
  33. N. Goyal, A. Rana, A. Ahlawat, K. R. V. Bijjem, and P. Kumar, “Animal models of inflammatory bowel disease: a review,” Inflammopharmacology, vol. 22, no. 4, pp. 219–233, 2014. View at Publisher · View at Google Scholar · View at Scopus
  34. G. K. Zorzi, F. Caregnato, J. C. Moreira, H. F. Teixeira, and E. L. Carvalho, “Antioxidant effect of nanoemulsions containing extract of Achyrocline satureioides (Lam) D.C.-asteraceae,” AAPS PharmSciTech, vol. 17, no. 4, pp. 844–850, 2016. View at Publisher · View at Google Scholar
  35. C. Casero, F. Machín, S. Méndez-Álvarez et al., “Structure and antimicrobial activity of phloroglucinol derivatives from Achyrocline satureioides,” Journal of Natural Products, vol. 78, no. 1, pp. 93–102, 2015. View at Publisher · View at Google Scholar · View at Scopus
  36. M. J. González, V. G. Beoletto, A. M. Agnese, M. C. Audisio, and J. M. Marioli, “Purification of substances from achyrocline satureioides with inhibitory activity against paenibacillus larvae, the causal agent of american foulbrood in Honeybees’ larvae,” Applied Biochemistry and Biotechnology, vol. 175, no. 7, pp. 3349–3359, 2015. View at Publisher · View at Google Scholar · View at Scopus
  37. J. Bidone, D. F. Argenta, J. Kratz et al., “Antiherpes activity and skin/mucosa distribution of flavonoids from achyrocline satureioides extract incorporated into topical nanoemulsions,” BioMed Research International, vol. 2015, Article ID 238010, 7 pages, 2015. View at Publisher · View at Google Scholar · View at Scopus
  38. Y. Nishitani, K. Yamamoto, M. Yoshida et al., “Intestinal anti-inflammatory activity of luteolin: role of the aglycone in NF-κB inactivation in macrophages co-cultured with intestinal epithelial cells,” BioFactors, vol. 39, no. 5, pp. 522–533, 2013. View at Publisher · View at Google Scholar · View at Scopus
  39. D. Dodda, R. Chhajed, J. Mishra, and M. Padhy, “Targeting oxidative stress attenuates trinitrobenzene sulphonic acid induced inflammatory bowel disease like symptoms in rats: role of quercetin,” Indian Journal of Pharmacology, vol. 46, no. 3, pp. 286–291, 2014. View at Publisher · View at Google Scholar · View at Scopus
  40. H. Yu, L.-H. Wu, Z.-L. Xu, D. Dong, and S.-A. He, “Protective effect of anthocyanins extract from blueberry on TNBS-induced IBD model of mice,” Evidence-Based Complementary and Alternative Medicine, vol. 2011, Article ID 525462, 8 pages, 2011. View at Publisher · View at Google Scholar · View at Scopus
  41. S. P. L. Travis, “Which 5-ASA?” Gut, vol. 51, no. 4, pp. 548–549, 2002. View at Publisher · View at Google Scholar · View at Scopus
  42. V. G. Pillarisetty, A. B. Shah, G. Miller, J. I. Bleier, and R. P. DeMatteo, “Liver dendritic cells are less immunogenic than spleen dendritic cells because of differences in subtype composition,” The Journal of Immunology, vol. 172, no. 2, pp. 1009–1017, 2004. View at Publisher · View at Google Scholar · View at Scopus
  43. S. Cornick, A. Tawiah, and K. Chadee, “Roles and regulation of the mucus barrier in the gut,” Tissue Barriers, vol. 3, no. 1-2, Article ID e982426, 2015. View at Publisher · View at Google Scholar
  44. Y. Merga, B. J. Campbell, and J. M. Rhodes, “Mucosal barrier, bacteria and inflammatory bowel disease: possibilities for therapy,” Digestive Diseases, vol. 32, no. 4, pp. 475–483, 2014. View at Publisher · View at Google Scholar · View at Scopus
  45. D. R. Clayburgh, L. Shen, and J. R. Turner, “A porous defense: the leaky epithelial barrier in intestinal disease,” Laboratory Investigation, vol. 84, no. 3, pp. 282–291, 2004. View at Publisher · View at Google Scholar · View at Scopus
  46. A. Bhattacharyya, R. Chattopadhyay, S. Mitra, and S. E. Crowe, “Oxidative stress: an essential factor in the pathogenesis of gastrointestinal mucosal diseases,” Physiological Reviews, vol. 94, no. 2, pp. 329–354, 2014. View at Publisher · View at Google Scholar · View at Scopus
  47. Y. J. Kim, E.-H. Kim, and K. B. Hahm, “Oxidative stress in inflammation-based gastrointestinal tract diseases: challenges and opportunities,” Journal of Gastroenterology and Hepatology, vol. 27, no. 6, pp. 1004–1010, 2012. View at Publisher · View at Google Scholar · View at Scopus
  48. J. Zhao, T. Hong, M. Dong, Y. Meng, and J. Mu, “Protective effect of myricetin in dextran sulphate sodium-induced murine ulcerative colitis,” Molecular Medicine Reports, vol. 7, no. 2, pp. 565–570, 2013. View at Publisher · View at Google Scholar · View at Scopus
  49. J. Pedersen, M. Coskun, C. Soendergaard, M. Salem, and O. H. Nielsen, “Inflammatory pathways of importance for management of inflammatory bowel disease,” World Journal of Gastroenterology, vol. 20, no. 1, pp. 64–77, 2014. View at Publisher · View at Google Scholar · View at Scopus
  50. C. Banks, A. Bateman, R. Payne, P. Johnson, and N. Sheron, “Chemokine expression in IBD. Mucosal chemokine expression is unselectively increased in both ulcerative colitis and Crohn's disease,” The Journal of Pathology, vol. 199, no. 1, pp. 28–35, 2003. View at Publisher · View at Google Scholar · View at Scopus
  51. R. Sreedhar, S. Arumugam, V. Karuppagounder et al., “Jumihaidokuto effectively inhibits colon inflammation and apoptosis in mice with acute colitis,” International Immunopharmacology, vol. 29, no. 2, pp. 957–963, 2015. View at Publisher · View at Google Scholar · View at Scopus
  52. L. A. Dieleman, M. J. H. J. Palmen, H. Akol et al., “Chronic experimental colitis induced by dextran sulphate sodium (DSS) is characterized by Th1 and Th2 cytokines,” Clinical and Experimental Immunology, vol. 114, no. 3, pp. 385–391, 1998. View at Publisher · View at Google Scholar · View at Scopus
  53. K. V. Barros, R. A. N. Xavier, G. G. Abreu et al., “Soybean and fish oil mixture increases IL-10, protects against DNA damage and decreases colonic inflammation in rats with dextran sulfate sodium (DSS) colitis,” Lipids in Health and Disease, vol. 9, article 68, 2010. View at Publisher · View at Google Scholar · View at Scopus
  54. G. Paul, V. Khare, and C. Gasche, “Inflamed gut mucosa: downstream of interleukin-10,” European Journal of Clinical Investigation, vol. 42, no. 1, pp. 95–109, 2012. View at Publisher · View at Google Scholar · View at Scopus
  55. J. O. Lindsay, A. Sandison, P. Cohen, F. M. Brennan, and H. J. F. Hodgson, “IL-10 gene therapy is therapeutic for dextran sodium sulfate-induced murine colitis,” Digestive Diseases and Sciences, vol. 49, no. 7-8, pp. 1327–1334, 2004. View at Publisher · View at Google Scholar · View at Scopus
  56. H. Groux, A. O'Garra, M. Bigler et al., “A CD4+ T-cell subset inhibits antigen-specific T-cell responses and prevents colitis,” Nature, vol. 389, no. 6652, pp. 737–742, 1997. View at Publisher · View at Google Scholar · View at Scopus