Gastroprotective and ulcer-healing mechanisms of ellagic acid in experimental rats

Journal of Agricultural and Food Chemistry

Volumn 59, Issue 13, 2011, Pages 6957-6965

  Beserra, Angela Márcia Selhorst E Silva ^a   Calegari, Pedro Ivo ^a   Souza, Maria Do Carmo ^a   Dos Santos, Rogério Alexandre Nunes ^b   Lima, Joaquim Corsino Da Silva ^a   Silva, Regilane Matos ^a   Balogun, Sikiru Olaitan ^a   Martins, Domingos Tabajara De Oliveira ^a  

^a FEDERAL UNIVERSITY OF MATO GROSSO   (Brazil)

^b UNIVERSITY OF CUIABÁ   (Brazil)

Author keywords

antioxidant; antiulcer mechanism; cytokines; ellagic acid; nitric oxide; ulcer healing

Indexed keywords

ANTIOXIDANT; ANTIULCER; CYTOKINES; ELLAGIC ACID; ULCER HEALING;

ACETIC ACID; ETHANOL; GLYCOPROTEINS; NITRIC OXIDE; PH; RATS;

DISEASES;

ACETIC ACID; ALCOHOL; ANTIULCER AGENT; CYTOKINE; ELLAGIC ACID; INDOMETACIN; LEUKOTRIENE B4; PROSTAGLANDIN E2;

ANIMAL; ARTICLE; BLOOD; CHEMICALLY INDUCED DISORDER; CHEMISTRY; DRUG EFFECT; FEMALE; MALE; MUCUS; RAT; STOMACH MUCOSA; STOMACH ULCER; WISTAR RAT;

ACETIC ACID; ANIMALS; ANTI-ULCER AGENTS; CYTOKINES; DINOPROSTONE; ELLAGIC ACID; ETHANOL; FEMALE; GASTRIC MUCOSA; INDOMETHACIN; LEUKOTRIENE B4; MALE; MUCUS; RATS; RATS, WISTAR; STOMACH ULCER;

RATTUS; RATTUS NORVEGICUS;

EID: 79960050613     PISSN: 00218561     EISSN: 15205118     Source Type: Journal    
DOI: 10.1021/jf2003267     Document Type: Article

References (62)

1. Zapata-Colindres, J. C.; Zepeda-Gomez, S.; Montano-Loza, A.; Vazquez-Ballesteros, E.; Jesus-Villalobos, J.; Valdovinos-Andraca, F. The association of Helicobacter pylori infection and nonsteroidal anti-inflammatory drugs in peptic ulcer disease Can. J. Gastroenterol. 2006, 20, 277-280
2. Syam, A. F.; Sadikin, M.; Wanandi, S. I.; Rani, A. A. Molecular mechanism on healing process of peptic ulcer Acta Med. Indones. 2009, 41, 95-98
3. Motawi, T. K.; Abd Elgawad, H. M.; Shahin, N. N. Modulation of indomethacin-induced gastric injury by spermine and taurine in rats J. Biochem. Mol. Toxicol. 2007, 21, 280-288 (Pubitemid 350006285)
4. Wallace, J. L. Prostaglandins, NSAIDs, and gastric mucosal protection: why doesnt the stomach digest itself? Physiol. Rev. 2008, 88, 1547-1565
5. Luo, J. C.; Shin, V. Y.; Liu, E. S.; Ye, Y. N.; Wu, W. K.; So, W. H.; Chang, F. Y.; Cho, C. H. Dexamethasone delays ulcer healing by inhibition of angiogenesis in rat stomachs Eur. J. Pharmacol. 2004, 485, 275-281 (Pubitemid 38134425)
6. Eswaran, S. M. D.; Roy, M. A. M. D. Medical management of acid-peptic disorders of the stomach Surg. Clin. Am. 2005, 85, 895-906
7. Shiomi, S.; Toriie, A.; Imamura, S.; Konishi, H.; Mitsufuji, S.; Iwakura, Y.; Yamaoka, Y.; Ota, H.; Yamamoto, T.; Imanishi, J.; Kita, M. IL-17 is involved in Helicobacter pylori-induced gastric inflammatory responses in a mouse model Helicobacter 2008, 13, 518-524
8. Szabo, G.; Mandrekar, P.; Girouard, L.; Catalano, D. Regulation of human monocyte functions by acute ethanol treatment: decreased tumor necrosis factor-α, interleukin-1 β and elevated interleukin-10, and transforming growth factor-β production Alcoholism, Clin. Exp. Res. 1996, 20, 900-907 (Pubitemid 26282325)
9. Hiraishi, H.; Shimada, T.; Terano, A. Involvement of oxidative stress in the pathogenesis of NSAID-induced gastric mucosal damage J. Gastroenterol. 2000, 35, 567-569 (Pubitemid 30468466)
10. Falcão, H. S.; Mariath, I. R.; Diniz, M. F. F. M.; Batista, L. M.; Barbosa-Filho, J. M. Plants of the American continent with antiulcer activity Phytomedicine 2008, 15, 132-146 (Pubitemid 350297902)
11. Wallace, J. L.; Ma, L. Inflammatory mediators in gastrointestinal defense and injury Exp. Biol. Med. (Maywood) 2001, 226, 1003-1015
12. Hsu, C.-L; Yen, G.-C. Phenolic compounds: evidence for inhibitory effects against obesity and their underlying molecular signaling mechanisms Mol. Nutr. Food Res. 2008, 52, 53-61 (Pubitemid 351211802)
13. Vattem, D. A.; Shetty, K. Biological functionality of ellagic acid: a review J. Food Biochem. 2005, 29, 234-266 (Pubitemid 41137813)
14. Tasaki, M.; Umemura, T.; Maeda, M.; Ishii, Y.; Okamura, T.; Inoue, T.; Kuroiwa, Y.; Hirose, M.; Nishikawa, A. Safety assessment of ellagic acid, a food additive, in a subchronic toxicity study using F344 rats Food Chem. Toxicol. 2008, 46, 1119-1124
15. Bae, J.-Y.; Choi, J.-S.; Kang, S.-W.; Lee, Y.-J.; Park, J.; Kang, Y.-H. Dietary compound ellagic acid alleviates skin wrinkle and inflammation induced by UV-B irradiation Exp. Dermatol. 2010, 19, e182-e190
16. Aggarwal, B. B.; Shishodia, S. Molecular targets of dietary agents for prevention and therapy of cancer Biochem. Pharmacol. 2006, 71, 1397-1421
17. Devipriya, N.; Srinivasan, M.; Sudheer, A. R.; Menon, V. P. Effect of ellagic acid, a natural polyphenol, on alcohol-induced prooxidant and antioxidant imbalance: a drug dose dependent study Singapore Med. J. 2007, 48, 311-318 (Pubitemid 351235428)
18. Rogerio, A. P.; Fontanari, C.; Borducchi, E.; Keller, A. C.; Russo, M.; Soares, E. G.; Albuquerque, D. A.; Faccioli, L. H. Antiinflammatory effects of Lafoensia pacari and ellagic acid in a murine model of asthma Eur. J. Pharmacol. 2008, 580, 262-270
19. Reddy, M. K.; Gupta, S. K.; Jacob, M. R.; Khan, S. I.; Ferreira, D. Antioxidant, antimalarial and antimicrobial activities of tannin-rich fractions, ellagitannins and phenolic acids from Punica granatum L Planta Med. 2007, 73, 461-467 (Pubitemid 46917461)
20. +-ATPase and acid secretion by ellagic acid Planta Med. 1991, 57, 305-308
21. Iino, T.; Nakahara, K.; Miki, W.; Kiso, Y.; Ogawa, Y.; Kato, S.; Takeuchi, K. Less damaging effect of whisky in rat stomachs in comparison with pure ethanol. Role of ellagic acid, the nonalcoholic component Digestion 2001, 64, 214-221 (Pubitemid 34158327)
22. Iino, T.; Tashima, K.; Umeda, M.; Ogawa, Y.; Takeeda, M.; Takata, K.; Takeuchi, K. Effect of ellagic acid on gastric damage induced in ischemic rat stomachs following ammonia or reperfusion Life Sci. 2002, 70, 1139-1150 (Pubitemid 34137082)
23. Chung, J. G. Inhibitory actions of ellagic acid on growth and arylamine N-acetyltransferase activity in strains of Helicobacter pylori from peptic ulcer patients Microbios 1998, 93 (375) 115-127 (Pubitemid 128557754)
24. Yu, Y. M.; Wang, Z. H.; Liu, C. H.; Chen, C. S. Ellagic acid inhibits IL-1β-induced cell adhesion molecule expression in human umbilical vein endothelial cells Br. J. Nutr. 2007, 97, 692-698
25. Papoutsi, Z.; Kassi, E.; Chinou, I.; Halabalaki, M.; Skaltsounis, L. A.; Moutsatsou, P. Walnut extract (Juglans regia L.) and its component ellagic acid exhibit anti-inflammatory activity in human aorta endothelial cells and osteoblastic activity in the cell line KS483 Br. J. Nutr. 2007, 99, 715-722 (Pubitemid 351351624)
26. Robert, A.; Nezamis, J. E.; Lancaster, C.; Hanchar, A. J. Cytoprotection by prostaglandins in rats. Prevention of gastric necrosis produced by alcohol, HCl, NaOH, hypertonic NaCl and thermal injury Gastroenterology 1979, 77, 433-443 (Pubitemid 10132046)
27. Sedlak, J.; Lindsay, R. H. Estimation of total protein bound and nonprotein sulphydryl groups in tissue with Ellman's reagent Anal. Biochem. 1968, 25, 192-205
28. Corne, S. J.; Morrisey, S. M.; Woods, R. J. A method for the quantitative estimation of gastric barrier mucus J. Physiol. (London) 1974, 242, 116-117
29. Djahanguiri, B. The production of acute ulceration by indomethacin in the rat Scand. J. Gastroenterol. 1969, 4, 265-267
30. Gamberini, M. T.; Skorupa, L. A.; Souccar, C.; Lapa, A. J. Inhibition of gastric secretion by a water extract from Baccharis triptera, Mart Mem. Inst. Oswaldo Cruz 1991, 86, 137-139
31. Takagi, K.; Okabe, S.; Saziki, R. A new method for the production of chronic gastric ulcer in rats and the effect of several drugs on its healing Jpn. J. Pharmacol. 1969, 19, 418-426
32. Whittle, B. J. R.; Lopez-Belmonte, J.; Moncada, S. Regulation of gastric mucosal integrity by endogenous nitric oxide: interactions with prostanoids and sensory neuropeptides in the rat Br. J. Pharmacol. 1990, 99, 607-611 (Pubitemid 20069172)
33. Matsuda, H.; Li, Y.; Yoshikawa, M. Roles of capsaicin-sensitive sensory nerves, endogenous nitric oxide, sulfhydryls and prostaglandins in gastroprotection by momordin Ic, an oleanolic acid oligoglycoside, on ethanol-induced gastric mucosal lesions in rats Life Sci. 1999, 65, 27-32 (Pubitemid 29292827)
34. Ishii, H.; Kurose, I.; Kato, S. Pathogenesis of alcoholic liver disease with particular emphasis on oxidative stress J. Gastroenterol. Hepatol. 1997, 12, S272-282
35. Sartori, N. T.; Canepelle, D.; de Sousa, P. T.; Martins, D. T. O. Gastroprotective effect from Calophyllum brasiliense Camb. bark on experimental gastric lesions in rats and mice J. Ethnopharmacol. 1999, 67, 149-156 (Pubitemid 29421669)
36. Hiruma-Lima, C. A.; Rodrigues, C. M.; Kushima, H.; Moraes, T. M.; Lolis, S. F.; Feitosa, S. B.; Magri, L. P.; Soares, F. R.; Cola, M. M.; Andrade, F. D. P.; Vilegas, W.; Brito, A. R. M. S. The anti-ulcerogenic effects of Curatella americana L J. Ethnopharmacol. 2009, 121, 425-432
37. Schlorff, E. C.; Husain, K.; Somani, S. M. Dose-and time-dependent effects of ethanol on plasma antioxidant system in rat Alcohol 1999, 17, 97-105 (Pubitemid 29096196)
38. Sudheer, A. R.; Muthukumaran, S.; Devipriya, N.; Menon, V. P. Ellagic acid, a natural polyphenol protects rat peripheral blood lymphocytes against nicotine-induced cellular and DNA damage in vitro: with the comparison of N-acetylcysteine Toxicology 2007, 230, 11-21 (Pubitemid 46073326)
39. Repetto, M. G.; Llesuy, S. F. Antioxidant properties of natural compounds used in popular medicine for gastric ulcers Braz. J. Med. Biol. Res. 2002, 35, 523-534 (Pubitemid 34568220)
40. Nagy, L.; Nagata, M.; Szabo, S. Protein and non-protein sulfhydryls and disulfides in gastric mucosa and liver after gastrotoxic chemicals and sucralfate: possible new targets of pharmacologic agents World J. Gastroenterol. 2007, 13, 2053-2060 (Pubitemid 46795841)
41. Takeuchi, K.; Okada, M.; Niida, H.; Okabe, S. Role of sulfhydryls in mucosal injury caused by ethanol: relation to microvascular permeability, gastric motility and cytoprotection J. Pharmacol. Exp. Ther. 1989, 248, 836-841 (Pubitemid 19090261)
42. Natale, G.; Lazzeri, G.; Lubrano, V.; Colucci, R.; Vassalle, C.; Fornai, M.; Blandizzi, C.; Taccab, M. D. Mechanisms of gastroprotection by lansoprazole pretreatment against experimentally induced injury in rats: role of mucosal oxidative damage and sulfhydryl compounds Toxicol. Appl. Pharmacol. 2004, 195, 62-72 (Pubitemid 38177500)
43. Yu, Y. M.; Chang, W. C.; Wu, C. H.; Chiang, S. Y. Reduction of oxidative stress and apoptosis in hyperlipidemic rabbits by ellagic acid J. Nutr. Biochem. 2005, 16, 675-681
44. Ogawa, Y.; Kanatsu, K.; Iino, T.; Kato, S.; Jeong, Y. I.; Shibata, N.; Takada, K.; Takeuchi, K. Protection against dextran sulphate sodium-induced colitis by microspheres of ellagic acid in rats Life Sci. 2002, 71, 827-839 (Pubitemid 34628824)
45. Brzozowski, T.; Konturek, P. C.; Sliwowski, Z.; Kwiecie, S.; Drozdowicz, D.; Pawlik, M.; Mach, K.; Konturek, S. J.; Pawlik, W. W. Interaction of nonsteroidal anti-inflammatory drugs (NSAID) with Helicobacter pylori in the stomach of humans and experimental animals J. Physiol. Pharmacol. 2006, 57 (Suppl. 3) 67-79 (Pubitemid 44617511)
46. Takahashi, S.; Shigeta, J. I.; Inoue, H.; Tanabe, T.; Okabe, S. Localization of cyclooxygenase-2 and regulation of its mRNA expression in gastric ulcers in rats Am. J. Physiol. 1998, 275, 1137-1145
47. Khalifa, M. A.; Hassan, M. K. A.; Ashour, O. M.; Heeba, G. Evaluation of the antiulcer activity of pibutidine hydrochloride (IT-066); the new histamine H2-receptor antagonist, in cold-restraint stress-and ethanol-induced ulcer models in rats Al Azhar Med. J. 2002, 31, 33-47
48. Peters-Golden, M.; Canetti, C.; Mancuso, P.; Coffey, M. J. Leukotrienes: underappreciated mediators of innate immune responses J. Immunol. 2004, 174, 589-594
49. 4, and tumor necrosis factor-α in children with Helicobacter pylori Dig. Dis. Sci. 1999, 44, 675-679 (Pubitemid 29186308)
50. Kirchner, T.; Aparicio, B.; Argentieri, D. C.; Lau, C. Y.; Ritchie, D. M. Effects of tepoxalin, a dual inhibitor of cyclooxygenase/5-lipoxygenase, on events associated with NSAID-induced gastrointestinal inflammation Prostaglandins, Leukotrienes Essent. Fatty Acids 1997, 56, 417-423 (Pubitemid 27276173)
51. Rainsford, K. D. Gastric ulcerogenicity of non-steroidal anti-inflammatory drugs in mice with mucosa sensitized by cholinomimetic treatment J. Pharm. Pharmacol. 1978, 39, 669-672
52. 2 in human monocytes Br. J. Nutr. 2010, 103, 1102-1109
53. Okabe, S.; Amagase, K. An overview of acetic acid ulcer models: the history and state of the art of peptic ulcer research Biol. Pharm. Bull. 2005, 28, 1321-1341 (Pubitemid 41386414)
54. Sprague, A. H.; Khalil, R. A. Inflammatory cytokines in vascular dysfunction and vascular disease Biochem. Pharmacol. 2009, 78, 539-552
55. Tedgui, A.; Mallat, Z. Cytokines in atherosclerosis: pathogenic and regulatory pathways Physiol. Rev. 2006, 86, 515-518
56. Martin, G. R.; Wallace, J. L. Gastrointestinal inflammation: a central component of mucosal defence and repair Exp. Biol. Med. (Maywood) 2006, 231, 130-137 (Pubitemid 43213449)
57. Kwiecien, S.; Brzozowski, T.; Konturek, S. J. Effects of reactive oxygen species action on gastric mucosa in various models of mucosal injury J. Physiol. Pharm. 2002, 53, 39-50 (Pubitemid 34266310)
58. Brzozowska, I.; Targosz, A.; Sliwowski, Z.; Kwiecien, S.; Drozdowicz, D.; Pajdo, R.; Konturek, P. C.; Brzozowski, T.; Pawlik, M.; Konturek, S. J.; Pawlik, W. W.; Hahn, E. G. Healing of chronic gastric ulcers in diabetic rats treated with native aspirin, nitric oxide (NO)-derivative of aspirin and cyclooxygenase (COX)-2 inhibitor J. Physiol. Pharm. 2004, 55, 773-790 (Pubitemid 40053045)
59. Harsch, I. A.; Brzozowski, T.; Bazela, K.; Konturek, S. J.; Kukharsky, V.; Pawlik, T.; Pawlowski, E.; Hahn, E. G.; Konturek, P. C. Impaired gastric ulcer healing in diabetic rats: role of heat shock protein, growth factors, prostaglandins and proinflammatory cytokines Eur. J. Pharmacol. 2003, 481, 249-260 (Pubitemid 37464977)
60. Maciorkowska, E.; Panasiuk, A.; Kaczmarski, M. Concentrations of gastric mucosal cytokines in children with food allergy and Helicobacter pylori infection World J. Gastroenterol. 2005, 11, 6751-6756 (Pubitemid 43092443)
61. Spedding, M. Resolution of controversies in drug/receptor interactions by protein structure. Limitations and pharmacological solutions Neuropharmacology 2011, 60, 3-6
62. Ou, H. C.; Lee, W. J.; Lee, S. D.; Huang, C. Y.; Chiu, T. H.; Tsai, K. L.; Hsu, W. C.; Sheu, W. H. H. Ellagic acid protects endothelial cells from oxidized low-density lipoprotein-induced apoptosis by modulating the PI3K/Akt/eNOS pathway Toxicol. Appl. Pharmacol. 2010, 248, 134-143