Grape seed extract dose-responsively decreases disease severity in a rat model of mucositis; concomitantly enhancing chemotherapeutic effectiveness in colon cancer cells

PLoS ONE

Volumn 9, Issue 1, 2014, Pages

  Cheah, Ker Yeaw ^a,b   Howarth, Gordon Stanley ^a,b   Bastian, Susan Elaine Putnam ^a  

^a UNIVERSITY OF ADELAIDE   (Australia)

^b Centre for Paediatric and Adolescent Gastroenterology Children Youth and Women's Health Service ^*  (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

FLUOROURACIL; GRAPE SEED EXTRACT; MYELOPEROXIDASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER CELL; CANCER CHEMOTHERAPY; CANCER INHIBITION; CELL STRAIN CACO 2; CELL VIABILITY; COLON CANCER; CONTROLLED STUDY; DISEASE SEVERITY; DRUG EFFICACY; DRUG POTENCY; ENZYME ACTIVITY; FEMALE; HISTOPATHOLOGY; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; INTESTINE INJURY; INTESTINE MUCOSA; JEJUNUM; MUCOSA INFLAMMATION; NONHUMAN; RAT;

ADMINISTRATION, ORAL; ANIMALS; ANTIOXIDANTS; CACO-2 CELLS; CELL PROLIFERATION; CELL SURVIVAL; FEMALE; FLUOROURACIL; GRAPE SEED EXTRACT; HUMANS; INJECTIONS, INTRAPERITONEAL; INTESTINAL MUCOSA; JEJUNUM; MUCOSITIS; PEROXIDASE; RATS; SEVERITY OF ILLNESS INDEX;

EID: 84908086411     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0085184     Document Type: Article

References (44)

1. Sonis ST, Eilers JP, Epstein JB, LeVeque FG, Liggett WH, et al. (1999) Validation of a new scoring system for the assessment of clinical trial research of oral mucositis induced by radiation or chemotherapy. Cancer 85: 2103-2113. (Pubitemid 29215547)
2. Stringer AM, Gibson RJ, Bowen JM, Logan RM, Yeoh AS, et al. (2007) Chemotherapy-induced mucositis: the role of gastrointestinal microflora and mucins in the luminal environment. J Support Oncol 5: 259-267. (Pubitemid 46995361)
3. Duncan M, Grant G (2003) Oral and intestinal mucositis - causes and possible treatments. Aliment Pharmacol Ther 18: 853-874. (Pubitemid 37346671)
4. Logan RM, Stringer AM, Bowen JM, Yeoh AS, Gibson RJ, et al. (2007) The role of pro-inflammatory cytokines in cancer treatment-induced alimentary tract mucositis: pathobiology, animal models and cytotoxic drugs. Cancer Treat Rev 33: 448-460. (Pubitemid 47324227)
5. Keefe DM, Sonis ST, Bowen JM (2008) Emerging drugs for chemotherapy-induced mucositis. Expert Opin Emerg Drugs 13: 511-522.
6. Bagchi D, Sen CK, Ray SD, Das DK, Bagchi M, et al. (2003) Molecular mechanisms of cardioprotection by a novel grape seed proanthocyanidin extract. Mutat Res 523-524: 87-97. (Pubitemid 36293235)
7. Cho ML, Heo YJ, Park MK, Oh HJ, Park JS, et al. (2009) Grape seed proanthocyanidin extract (GSPE) attenuates collagen-induced arthritis. Immunol Lett 124: 102-110.
8. Dinicola S, Cucina A, Pasqualato A, Proietti S, D'Anselmi F, et al. (2010) Apoptosis-inducing factor and caspase-dependent apoptotic pathways triggered by different grape seed extracts on human colon cancer cell line Caco-2. Br J Nutr 104: 824-832.
9. Fine AM (2000) Oligomeric proanthocyanidin complexes: history, structure, and phytopharmaceutical applications. Altern Med Rev 5: 144-151.
10. Santos-Buelga C, Scalbert A (2000) Proanthocyanidins and tannin-like compounds - nature, occurrence, dietary intake and effects on nutrition and health. J Sci Food Agric 80: 1094-1117. (Pubitemid 30319402)
11. Gu L, Kelm MA, Hammerstone JF, Beecher G, Holden J, et al. (2004) Concentrations of proanthocyanidins in common foods and estimations of normal consumption. J Nutr 134: 613-617. (Pubitemid 38298505)
12. Scalbert A, Morand C, Manach C, Remesy C (2002) Absorption and metabolism of polyphenols in the gut and impact on health. Biomed Pharmacother 56: 276-282. (Pubitemid 35245310)
13. Cheah KY, Howarth GS, Yazbeck R, Wright TH, Whitford EJ, et al. (2009) Grape seed extract protects IEC-6 cells from chemotherapy-induced cytotoxicity and improves parameters of small intestinal mucositis in rats with experimentally-induced mucositis. Cancer Biol Ther 8: 382-390.
14. Cheah KY, Bastian SE, Acott TM, Abimosleh SM, Lymn KA, et al. (2013) Grape seed extract reduces the severity of selected disease markers in the proximal colon of dextran sulphate sodium-induced colitis in rats. Dig Dis Sci 58: 970-977.
15. Bindon KA, Smith PA, Kennedy JA (2010) Interaction between grape-derived proanthocyanidins and cell wall material. 1. Effect on proanthocyanidin composition and molecular mass. J Agric Food Chem 58: 2520-2528.
16. Tomas FM, Knowles SE, Owens PC, Read LC, Chandler CS, et al. (1991) Increased weight gain, nitrogen retention and muscle protein synthesis following treatment of diabetic rats with insulin-like growth factor (IGF)-I and des(1- 3)IGF-I. Biochem J 276 (Pt 2): 547-554.
17. Tooley KL, Saxon BR, Webster J, Zacharakis B, McNeil Y, et al. (2006) A novel non-invasive biomarker for assessment of small intestinal mucositis in children with cancer undergoing chemotherapy. Cancer Biol Ther 5: 1275-1281. (Pubitemid 44772251)
18. Krawisz JE, Sharon P, Stenson WF (1984) Quantitative assay for acute intestinal inflammation based on myeloperoxidase activity. Assessment of inflammation in rat and hamster models. Gastroenterology 87: 1344-1350. (Pubitemid 15201434)
19. Howarth GS, Francis GL, Cool JC, Xu X, Byard RW, et al. (1996) Milk growth factors enriched from cheese whey ameliorate intestinal damage by methotrexate when administered orally to rats. J Nutr 126: 2519-2530. (Pubitemid 26339666)
20. Huynh-Delerme C, Huet H, Noël L, Frigieri A, Kolf-Clauw M (2005) Increased functional expression of P-glycoprotein in Caco-2 TC7 cells exposed long-term to cadmium. Toxicology in Vitro 19: 439-447.
21. Pelton NS, Tivey DR, Howarth GS, Davidson GP, Butler RN (2004) A novel breath test for the non-invasive assessment of small intestinal mucosal injury following methotrexate administration in the rat. Scand J Gastroenterol 39: 1015-1016. (Pubitemid 39388469)
22. Soares PM, Mota JM, Gomes AS, Oliveira RB, Assreuy AM, et al. (2008) Gastrointestinal dysmotility in 5-fluorouracil-induced intestinal mucositis outlasts inflammatory process resolution. Cancer Chemother Pharmacol 63: 91-98.
23. Mauger CA, Butler RN, Geier MS, Tooley KL, Howarth GS (2007) Probiotic effects on 5-fluorouracil-induced mucositis assessed by the sucrose breath test in rats. Dig Dis Sci 52: 612-619.
24. D'Archivio M, Filesi C, Di Benedetto R, Gargiulo R, Giovannini C, et al. (2007) Polyphenols, dietary sources and bioavailability. Ann Ist Super Sanita 43: 348-361.
25. Manach C, Scalbert A, Morand C, Remesy C, Jimenez L (2004) Polyphenols: food sources and bioavailability. Am J Clin Nutr 79: 727-747. (Pubitemid 41103873)
26. Tsang C, Auger C, Mullen W, Bornet A, Rouanet JM, et al. (2005) The absorption, metabolism and excretion of flavan-3-ols and procyanidins following the ingestion of a grape seed extract by rats. Br J Nutr 94: 170-181. (Pubitemid 41357787)
27. Appeldoorn MM, Vincken JP, Aura AM, Hollman PC, Gruppen H (2009) Procyanidin dimers are metabolized by human microbiota with 2-(3,4- dihydroxyphenyl)acetic acid and 5-(3,4-dihydroxyphenyl)-gamma-valerolactone as the major metabolites. J Agric Food Chem 57: 1084-1092.
28. Urpi-Sarda M, Monagas M, Khan N, Lamuela-Raventos RM, Santos-Buelga C, et al. (2009) Epicatechin, procyanidins, and phenolic microbial metabolites after cocoa intake in humans and rats. Anal Bioanal Chem 394: 1545-1556.
29. Bagchi D, Garg A, Krohn RL, Bagchi M, Tran MX, et al. (1997) Oxygen free radical scavenging abilities of vitamins C and E, and a grape seed proanthocyanidin extract in vitro. Res Commun Mol Pathol Pharmacol 95: 179-189. (Pubitemid 27147562)
30. Terra X, Montagut G, Bustos M, Llopiz N, Ardevol A, et al. (2009) Grape-seed procyanidins prevent low-grade inflammation by modulating cytokine expression in rats fed a high-fat diet. J Nutr Biochem 20: 210-218.
31. Terra X, Pallares V, Ardevol A, Blade C, Fernandez-Larrea J, et al. (2011) Modulatory effect of grape-seed procyanidins on local and systemic inflammation in diet-induced obesity rats. J Nutr Biochem 22: 380-387.
32. Li WG, Zhang XY, Wu YJ, Tian X (2001) Anti-inflammatory effect and mechanism of proanthocyanidins from grape seeds. Acta Pharmacol Sin 22: 1117-1120.
33. Glick Z, Joslyn MA (1970) Food intake depression and other metabolic effects of tannic acid in the rat. J Nutr 100: 509-515.
34. Wren AF, Cleary M, Frantz C, Melton S, Norris L (2002) 90-Day oral toxicity study of a grape seed extract (IH636) in rats. J Agric Food Chem 50: 2180-2192. (Pubitemid 34260030)
35. Yamakoshi J, Saito M, Kataoka S, Kikuchi M (2002) Safety evaluation of proanthocyanidin-rich extract from grape seeds. Food Chem Toxicol 40: 599-607. (Pubitemid 34310425)
36. Jordan A, Stein J (2003) Effect of an omega-3 fatty acid containing lipid emulsion alone and in combination with 5-fluorouracil (5-FU) on growth of the colon cancer cell line Caco-2. Eur J Nutr 42: 324-331. (Pubitemid 38055612)
37. Sasaki K, Tsuno NH, Sunami E, Tsurita G, Kawai K, et al. (2010) Chloroquine potentiates the anti-cancer effect of 5-fluorouracil on colon cancer cells. BMC Cancer 10: 370.
38. Kodach LL, Bos CL, Duran N, Peppelenbosch MP, Ferreira CV, et al. (2006) Violacein synergistically increases 5-fluorouracil cytotoxicity, induces apoptosis and inhibits Akt-mediated signal transduction in human colorectal cancer cells. Carcinogenesis 27: 508-516. (Pubitemid 43372880)
39. Fishbein AB, Wang CZ, Li XL, Mehendale SR, Sun S, et al. (2009) Asian ginseng enhances the anti-proliferative effect of 5-fluorouracil on human colorectal cancer: comparison between white and red ginseng. Arch Pharm Res 32: 505-513.
40. Agarwal C, Singh RP, Agarwal R (2002) Grape seed extract induces apoptotic death of human prostate carcinoma DU145 cells via caspases activation accompanied by dissipation of mitochondrial membrane potential and cytochrome c release. Carcinogenesis 23: 1869-1876. (Pubitemid 35355936)
41. Engelbrecht AM, Mattheyse M, Ellis B, Thomas M, Smith R, et al. (2007) Proanthocyanidin from grape seeds inactivates the PI3-kinase/PKB pathway and induces apoptosis in a colon cancer cell line. Cancer Letters 258: 144-153. (Pubitemid 47600495)
42. Hsu CP, Lin YH, Chou CC, Zhou SP, Hsu YC, et al. (2009) Mechanisms of grape seed procyanidin-induced apoptosis in colorectal carcinoma cells. Anticancer Res 29: 283-289.
43. Bowen JM, Gibson RJ, Cummins AG, Tyskin A, Keefe DM (2007) Irinotecan changes gene expression in the small intestine of the rat with breast cancer. Cancer Chemother Pharmacol 59: 337-348. (Pubitemid 46025521)
44. Watanabe H, Kashimoto N, Ushijima M, Tamura K (2013) Effects of a watersoluble extract of Ganoderma lucidum mycelia on aberrant crypt foci induced by azoxymethane and small-intestinal injury by 5-FU in F344 rats. Med Mol Morphol 46: 97-103.