Table of Contents Author Guidelines Submit a Manuscript
Evidence-Based Complementary and Alternative Medicine
Volume 2013 (2013), Article ID 853976, 11 pages
http://dx.doi.org/10.1155/2013/853976
Research Article

Use of Propolis Hydroalcoholic Extract to Treat Colitis Experimentally Induced in Rats by 2,4,6-Trinitrobenzenesulfonic Acid

1Laboratory of Animal Histology, Department of Morphological Sciences, State University of Maringá, 87020-900 Maringá, PR, Brazil
2Laboratory of Inflammation, Department of Pharmacology and Therapeutics, State University of Maringá, 87020-900 Maringá, PR, Brazil
3Laboratory of Phytotherapy and Apitherapy Development, Department of Pharmacy, State University of Maringá, 87020-900 Maringá, PR, Brazil

Received 9 April 2013; Revised 25 July 2013; Accepted 1 August 2013

Academic Editor: H. Balaji Raghavendran

Copyright © 2013 Cely Cristina Martins Gonçalves 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. T. A. Judge and G. R. Lichtenstein, “Inflammatory bowel disease,” in Current Diagnosis and Treatment in Gastroenterology, S. L. Friedman, K. R. McQuaid, and J. H. Grendell, Eds., pp. 108–130, McGraw-Hill, New York, NY, USA, 2002. View at Google Scholar
  2. C. Fiocchi, “Inflammatory bowel disease: etiology and pathogenesis,” Gastroenterology, vol. 115, no. 1, pp. 182–205, 1998. View at Publisher · View at Google Scholar · View at Scopus
  3. R. B. Sartor, “Mechanisms of disease: pathogenesis of Crohn's disease and ulcerative colitis,” Nature Clinical Practice Gastroenterology and Hepatology, vol. 7, no. 3, pp. 390–407, 2006. View at Google Scholar · View at Scopus
  4. K. Sugimoto, H. Hanai, K. Tozawa et al., “Curcumin prevents and ameliorates trinitrobenzene sulfonic acid-induced colitis in mice,” Gastroenterology, vol. 123, no. 6, pp. 1912–1922, 2002. View at Publisher · View at Google Scholar · View at Scopus
  5. H. Jeon, H. Kim, D. Choi et al., “Quercetin activates an angiogenic pathway, hypoxia inducible factor (HIF)-1-vascular endothelial growth factor, by inhibiting HIF-prolyl hydroxylase: a structural analysis of quercetin for inhibiting HIF-prolyl hydroxylase,” Molecular Pharmacology, vol. 71, no. 6, pp. 1676–1684, 2007. View at Publisher · View at Google Scholar · View at Scopus
  6. D. M. Abdallah and N. R. Ismael, “Resveratrol abrogates adhesion molecules and protects against TNBS-induced ulcerative colitis in rats,” Canadian Journal of Physiology and Pharmacology, vol. 89, no. 11, pp. 811–818, 2011. View at Publisher · View at Google Scholar · View at Scopus
  7. P. A. Abboud, P. W. Hake, T. J. Burroughs et al., “Therapeutic effect of epigallocatechin-3-gallate in a mouse model of colitis,” European Journal of Pharmacology, vol. 579, no. 1–3, pp. 411–417, 2008. View at Publisher · View at Google Scholar · View at Scopus
  8. S. H. Cestari, J. K. Bastos, and L. C. Di Stasi, “Intestinal anti-inflammatory activity of Baccharis dracunculifolia in the trinitrobenzenosulfonic acid model rats of colitis,” Evidence-Based Complementary and Alternative Medicine, vol. 2011, Article ID 524349, 9 pages, 2011. View at Publisher · View at Google Scholar
  9. J. Y. Lee, H. S. Kang, B. E. Park, H. J. Moon, S. S. Sim, and C. J. Kim, “Inhibitory effects of Geijigajakyak-Tang on trinitrobenzene sulfonic acid-induced colitis,” Journal of Ethnopharmacology, vol. 126, no. 2, pp. 244–251, 2009. View at Publisher · View at Google Scholar · View at Scopus
  10. M. S. da Silva, S. Sánchez-Fidalgo, E. Talero et al., “Anti-inflammatory intestinal activity of Abarema cochliacarpos (Gomes) Barneby & Grimes in TNBS colitis model,” Journal of Ethnopharmacology, vol. 128, no. 2, pp. 467–475, 2010. View at Publisher · View at Google Scholar · View at Scopus
  11. L. R. Fitzpatrick, J. Wang, and T. Le, “Caffeic acid phenethyl ester, an inhibitor of nuclear factor-κB, attenuates bacterial peptidoglycan polysaccharide-induced Colitis in rats,” Journal of Pharmacology and Experimental Therapeutics, vol. 299, no. 3, pp. 915–920, 2001. View at Google Scholar · View at Scopus
  12. X. Wang, S. Stavchansky, P. D. Bowman, and S. M. Kerwin, “Cytoprotective effect of caffeic acid phenethyl ester (CAPE) and catechol ring-fluorinated CAPE derivatives against menadione-induced oxidative stress in human endothelial cells,” Bioorganic and Medicinal Chemistry, vol. 14, no. 14, pp. 4879–4887, 2006. View at Publisher · View at Google Scholar · View at Scopus
  13. M. Ahn, S. Kumazawa, Y. Usui et al., “Antioxidant activity and constituents of propolis collected in various areas of China,” Food Chemistry, vol. 101, no. 4, pp. 1383–1392, 2007. View at Publisher · View at Google Scholar · View at Scopus
  14. J. H. Park, J. K. Lee, H. S. Kim et al., “Immunomodulatory effect of caffeic acid phenethyl ester in Balb/c mice,” International Immunopharmacology, vol. 4, no. 3, pp. 429–436, 2004. View at Publisher · View at Google Scholar · View at Scopus
  15. 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
  16. E. Sehn, L. Hernandes, S. L. Franco, C. C. M. Gonçalves, and M. L. Baesso, “Dynamics of reepithelialisation and penetration rate of a bee propolis formulation during cutaneous wounds healing,” Analytica Chimica Acta, vol. 635, no. 1, pp. 115–120, 2009. View at Publisher · View at Google Scholar · View at Scopus
  17. M. Marcucci, “Propolis: chemical composition, biological properties and therapeutic activity,” Apidologie, vol. 26, no. 2, pp. 83–99, 1995. View at Google Scholar · View at Scopus
  18. É. W. Teixeira, D. Message, G. Negri, A. Salatino, and P. C. Stringheta, “Seasonal variation, chemical composition and antioxidant activity of brazilian propolis samples,” Evidence-Based Complementary and Alternative Medicine, vol. 7, no. 3, pp. 307–315, 2010. View at Publisher · View at Google Scholar · View at Scopus
  19. B. H. Havsteen, “The biochemistry and medical significance of the flavonoids,” Pharmacology and Therapeutics, vol. 96, no. 2-3, pp. 67–202, 2002. View at Publisher · View at Google Scholar · View at Scopus
  20. J. M. Sforcin, R. O. Orsi, and V. Bankova, “Effect of propolis, some isolated compounds and its source plant on antibody production,” Journal of Ethnopharmacology, vol. 98, no. 3, pp. 301–305, 2005. View at Publisher · View at Google Scholar · View at Scopus
  21. N. Oršolić, A. H. knežević, L. Šver, S. Terzić, and I. Bašić, “Immunomodulatory and antimetastatic action of propolis and related polyphenolic compounds,” Journal of Ethnopharmacology, vol. 94, no. 2-3, pp. 307–315, 2004. View at Google Scholar
  22. S. L. Franco and J. H. F. Bueno, “Propolis-otimização de processo extrativo,” Infarma, vol. 11, no. 17, pp. 48–51, 1999. View at Google Scholar
  23. G. P. Morris, P. L. Beck, M. S. Herridge, W. T. Depew, M. R. Szewczuk, and J. L. Wallace, “Hapten-induced model of chronic inflammation and ulceration in the rat colon,” Gastroenterology, vol. 96, no. 3, pp. 795–803, 1989. View at Google Scholar · View at Scopus
  24. Y. Jung, H. Kim, H. Kim et al., “Evaluation of 5-aminosalicyltaurine as a colon-specific prodrug of 5-aminosalicylic acid for treatment of experimental colitis,” European Journal of Pharmaceutical Sciences, vol. 28, no. 1-2, pp. 26–33, 2006. View at Publisher · View at Google Scholar · View at Scopus
  25. A. Lamprecht, U. Schäfer, and C.-M. Lehr, “Size-dependent bioadhesion of micro- and nanoparticulate carriers to the inflamed colonic mucosa,” Pharmaceutical Research, vol. 18, no. 6, pp. 788–793, 2001. View at Publisher · View at Google Scholar · View at Scopus
  26. M. A. Jordan, D. Thrower, and L. Wilson, “Effects of vinblastine, podophyllotoxin and nocodazole on mitotic spindles. Implications for the role of microtubule dynamics in mitosis,” Journal of Cell Science, vol. 102, no. 3, pp. 401–416, 1992. View at Google Scholar · View at Scopus
  27. H. Yano, F. Hirayama, M. Kamada, H. Arima, and K. Uekama, “Colon-specific delivery of prednisolone-appended α-cyclodextrin conjugate: alleviation of systemic side effect after oral administration,” Journal of Controlled Release, vol. 79, no. 1–3, pp. 103–112, 2002. View at Publisher · View at Google Scholar · View at Scopus
  28. J. E. Krawisz, P. Sharon, and W. F. Stenson, “Quantitative assay for acute intestinal inflammation based on myeloperoxidase activity. Assessment of inflammation in rat and hamster models,” Gastroenterology, vol. 87, no. 6, pp. 1344–1350, 1984. View at Google Scholar · View at Scopus
  29. R. Fabia, A. Ar'Rajab, M.-L. Johansson et al., “The effect of exogenous administration of Lactobacillus reuteri R2LC and oat fiber on acetic acid-induced colitis in the rat,” Scandinavian Journal of Gastroenterology, vol. 28, no. 2, pp. 155–162, 1993. View at Google Scholar · View at Scopus
  30. N. Wrigth and M. Alison, The Biology of Epithelial Cell Population, Clarendon Press, Oxford, UK, 1984.
  31. I. F. Tannock, “A comparison of the relative efficiencies of various metaphase arrest agents,” Experimental Cell Research, vol. 47, no. 1-2, pp. 345–356, 1967. View at Google Scholar · View at Scopus
  32. F. R. Victorino, S. L. Franco, T. I. E. Svidzinski et al., “Pharmacological evaluation of propolis solutions for endodontic use,” Pharmaceutical Biology, vol. 45, no. 9, pp. 721–727, 2007. View at Publisher · View at Google Scholar · View at Scopus
  33. A. C. P. Oliveira, C. S. Shinobu, R. Longhini, S. L. Franco, and T. I. E. Svidzinski, “Antifungal activity of propolis extract against yeasts isolated from onychomycosis lesions,” Memorias do Instituto Oswaldo Cruz, vol. 101, no. 5, pp. 493–497, 2006. View at Google Scholar · View at Scopus
  34. E. Poli, M. Lazzaretti, D. Grandi, C. Pozzoli, and G. Coruzzi, “Morphological and functional alterations of the myenteric plexus in rats with TNBS-induced colitis,” Neurochemical Research, vol. 26, no. 8-9, pp. 1085–1093, 2001. View at Publisher · View at Google Scholar · View at Scopus
  35. M. W. Musch, L. L. Clarke, D. Mamah et al., “T cell activation causes diarrhea by increasing intestinal permeability and inhibiting epithelial Na+/K+-ATPase,” The Journal of Clinical Investigation, vol. 110, no. 11, pp. 1739–1747, 2002. View at Publisher · View at Google Scholar · View at Scopus
  36. D. R. Linden, J. M. Couvrette, A. Ciolino et al., “Indiscriminate loss of myenteric neurones in the TNBS-inflamed guinea-pig distal colon,” Neurogastroenterology and Motility, vol. 17, no. 5, pp. 751–760, 2005. View at Publisher · View at Google Scholar · View at Scopus
  37. A. Aslan, M. Temiz, E. Atik et al., “Effectiveness of mesalamine and propolis in experimental colitis,” Advances in Therapy, vol. 24, no. 5, pp. 1085–1097, 2007. View at Publisher · View at Google Scholar · View at Scopus
  38. O. K. Mirzoeva and P. C. Calder, “The effect of propolis and its components on eicosanoid production during the inflammatory response,” Prostaglandins Leukotrienes and Essential Fatty Acids, vol. 55, no. 6, pp. 441–449, 1996. View at Publisher · View at Google Scholar · View at Scopus
  39. W. Krol, S. Scheller, Z. Czuba et al., “Inhibition of neutrophils' chemiluminescence by ethanol extract of propolis (EEP) and its phenolic components,” Journal of Ethnopharmacology, vol. 55, no. 1, pp. 19–25, 1996. View at Publisher · View at Google Scholar · View at Scopus
  40. H. Miyataka, M. Nishiki, H. Matsumoto, T. Fujimoto, M. Matsuka, and T. Satoh, “Evaluation of propolis. I. Evaluation of Brazilian and Chinese propolis by enzymatic and physico-chemical methods,” Biological and Pharmaceutical Bulletin, vol. 20, no. 5, pp. 496–501, 1997. View at Google Scholar · View at Scopus
  41. R. O. Orsi, R. S. C. Funari, A. M. V. C. Soares et al., “Immunomodulatory action of propolis on macrophage activation,” Journal of Venomous Animals and Toxins, vol. 6, no. 2, pp. 205–219, 2000. View at Google Scholar
  42. K. W. Lee, K. Chun, J. Lee, K. Kang, Y. Surh, and H. J. Lee, “Inhibition of cyclooxygenase-2 expression and restoration of gap junction intercellular communication in H-ras-transformed rat liver epithelial cells by caffeic acid phenethyl ester,” Annals of the New York Academy of Sciences, vol. 1030, pp. 501–507, 2004. View at Publisher · View at Google Scholar · View at Scopus
  43. K. Natarajan, S. Singh, T. R. Burke, D. Grunberger, and B. B. Aggarwal, “Caffeic acid phenethyl ester is a potent and specific inhibitor of activation of nuclear transcription factor NF-κB,” Proceedings of the National Academy of Sciences of the United States of America, vol. 93, no. 17, pp. 9090–9095, 1996. View at Publisher · View at Google Scholar · View at Scopus
  44. A. Mizoguchi, E. Mizoguchi, and A. K. Bhan, “Immune networks in animal models of inflammatory bowel disease,” Inflammatory Bowel Diseases, vol. 9, no. 4, pp. 246–259, 2003. View at Google Scholar · View at Scopus
  45. M. Blonska, J. Bronikowska, G. Pietsz, Z. P. Czuba, S. Scheller, and W. Krol, “Effects of ethanol extract of propolis (EEP) and its flavones on inducible gene expression in J774A.1 macrophages,” Journal of Ethnopharmacology, vol. 91, no. 1, pp. 25–30, 2004. View at Publisher · View at Google Scholar · View at Scopus
  46. Y. Okamoto, T. Hara, T. Ebato, T. Fukui, and T. Masuzawa, “Brazilian propolis ameliorates trinitrobenzene sulfonic acid-induced colitis in mice by inhibiting Th1 differentiation,” International Immunopharmacology, vol. 16, no. 2, pp. 178–183, 2013. View at Google Scholar
  47. S. Sanovic, D. P. Lamb, and M. G. Blennerhassett, “Damage to the enteric nervous system in experimental colitis,” American Journal of Pathology, vol. 155, no. 4, pp. 1051–1057, 1999. View at Google Scholar · View at Scopus
  48. L. Pontell, P. Castelucci, M. Bagyánszki et al., “Structural changes in the epithelium of the small intestine and immune cell infiltration of enteric ganglia following acute mucosal damage and local inflammation,” Virchows Archiv, vol. 455, no. 1, pp. 55–65, 2009. View at Publisher · View at Google Scholar · View at Scopus
  49. R. M. Glickman, “Inflammatory bowel disease: ulcerative colitis and Crohn’s disease,” in Harrison’s Principles of Internal Medicine, T. R. Harrison, Ed., McGraw Hill, New York, NY, USA, 1998. View at Google Scholar
  50. S. P. Dunlop, D. Jenkins, and R. C. Spiller, “Distinctive clinical, psychological, and histological features of postinfective irritable bowel syndrome,” American Journal of Gastroenterology, vol. 98, no. 7, pp. 1578–1583, 2003. View at Google Scholar · View at Scopus
  51. R. Thoreson and J. J. Cullen, “Pathophysiology of inflammatory bowel disease: an overview,” Surgical Clinics of North America, vol. 87, no. 3, pp. 575–585, 2007. View at Publisher · View at Google Scholar · View at Scopus
  52. M. Jerkic, M. Peter, D. Ardelean, M. Fine, M. A. Konerding, and M. Letarte, “Dextran sulfate sodium leads to chronic colitis and pathological angiogenesis in endoglin heterozygous mice,” Inflammatory Bowel Diseases, vol. 16, no. 11, pp. 1859–1870, 2010. View at Publisher · View at Google Scholar · View at Scopus
  53. J. M. Hosseini, J. M. Goldhill, C. Bossone, V. Pineiro-Carrero, and T. Shea-Donohue, “Progressive alterations in circular smooth muscle contractility in TNBS-induced colitis in rats,” Neurogastroenterology and Motility, vol. 11, no. 5, pp. 347–356, 1999. View at Publisher · View at Google Scholar · View at Scopus
  54. A. U. Dignass, “Mechanisms and modulation of intestinal epithelial repair,” Inflammatory Bowel Diseases, vol. 7, no. 1, pp. 68–77, 2001. View at Google Scholar · View at Scopus
  55. M. I. Torres, M. Garcia-Mártin, M. I. Fernándes, N. Nieto, A. Gil, and A. Ríos, “Experimental colitis induced by trinitrobezenesulphonic acid: an ultraestructural and histochemical study,” Digestive Disease and Sciences, vol. 44, no. 12, pp. 2523–2529, 1999. View at Google Scholar
  56. A. Vetuschi, G. Latella, R. Sferra, R. Caprilli, and E. Gaudio, “Increased proliferation and apoptosis of colonic epithelial cells in dextran sulfate sodium-induced colitis in rats,” Digestive Diseases and Sciences, vol. 47, no. 7, pp. 1447–1457, 2002. View at Publisher · View at Google Scholar · View at Scopus
  57. Y. Araki, K. Mukaisyo, H. Sugihara, Y. Fujiyama, and T. Hattori, “Increased apoptosis and decreased proliferation of colonic epithelium in dextran sulfate sodium-induced colitis in mice,” Oncology Reports, vol. 24, no. 4, pp. 869–874, 2010. View at Publisher · View at Google Scholar · View at Scopus
  58. E. Dundar, E. G. Olgun, S. Isiksoy, M. Kurkcuoglu, K. H. C. Baser, and C. Bal, “The effects of intra-rectal and intra-peritoneal application of Origanum onites L. essential oil on 2,4,6-trinitrobenzenesulfonic acid-induced colitis in the rat,” Experimental and Toxicologic Pathology, vol. 59, no. 6, pp. 399–408, 2008. View at Publisher · View at Google Scholar · View at Scopus