Mechanistic insight into beta-carotene-mediated protection against ulcerative colitis-associated local and systemic damage in mice

European Journal of Nutrition

Volumn 54, Issue 4, 2015, Pages 639-652

  Trivedi, P P ^a   Jena, G B ^a  

^a NATIONAL INSTITUTE OF PHARMACEUTICAL EDUCATION AND RESEARCH NIPER   (India)

Author keywords

DNA damage; Fibrosis; Inflammation; Oxidative stress; Ulcerative colitis; Carotene

Indexed keywords

BETA CAROTENE; CONNECTIVE TISSUE GROWTH FACTOR; CYCLOOXYGENASE 2; DOUBLE STRANDED DNA; GELATINASE B; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 17; INTERLEUKIN 6; OCCLUDIN; STAT3 PROTEIN; THIOBARBITURIC ACID REACTIVE SUBSTANCE; TRANSCRIPTION FACTOR NRF2; TUMOR NECROSIS FACTOR ALPHA; ANTIOXIDANT; CTGF PROTEIN, MOUSE; DEXTRAN SULFATE; GLUTATHIONE; LIPOPOLYSACCHARIDE; MMP9 PROTEIN, MOUSE; NFE2L2 PROTEIN, MOUSE; OCLN PROTEIN, MOUSE; PTGS2 PROTEIN, MOUSE; STAT3 PROTEIN, MOUSE; TIGHT JUNCTION PROTEIN; TUMOR NECROSIS FACTOR;

ABSCESS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BACTERIAL TRANSLOCATION; BIOCHEMICAL ANALYSIS; BODY WEIGHT; CELL DAMAGE; COMET ASSAY; COMPARATIVE STUDY; CONTROLLED STUDY; DIARRHEA; DNA DAMAGE; DRUG MECHANISM; IMMUNOHISTOCHEMISTRY; INFLAMMATION; LAMINA PROPRIA; MALE; MICRONUCLEUS TEST; MOUSE; NONHUMAN; OXIDATIVE STRESS; PROTECTION; PROTEIN BLOOD LEVEL; RECTUM HEMORRHAGE; REGULATORY MECHANISM; SUBMUCOSA; SYSTEMIC CIRCULATION; ULCERATIVE COLITIS; WESTERN BLOTTING; ANIMAL; BLOOD; CHEMICALLY INDUCED; COLITIS, ULCERATIVE; DISEASE MODEL; DOSE RESPONSE; DRUG EFFECTS; GENETICS; LIPID PEROXIDATION; METABOLISM;

MUS;

ANIMALS; ANTIOXIDANTS; BETA CAROTENE; COLITIS, ULCERATIVE; COMET ASSAY; CONNECTIVE TISSUE GROWTH FACTOR; CYCLOOXYGENASE 2; DEXTRAN SULFATE; DISEASE MODELS, ANIMAL; DNA DAMAGE; DOSE-RESPONSE RELATIONSHIP, DRUG; GLUTATHIONE; INFLAMMATION; INTERLEUKIN-17; INTERLEUKIN-6; LIPID PEROXIDATION; LIPOPOLYSACCHARIDES; MALE; MATRIX METALLOPROTEINASE 9; MICE; NF-E2-RELATED FACTOR 2; NF-KAPPA B; OCCLUDIN; OXIDATIVE STRESS; STAT3 TRANSCRIPTION FACTOR; TIGHT JUNCTION PROTEINS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84929708196     PISSN: 14366207     EISSN: 14366215     Source Type: Journal    
DOI: 10.1007/s00394-014-0745-5     Document Type: Article

References (64)

1. Jena G, Trivedi PP, Sandala B (2012) Oxidative stress in ulcerative colitis: an old concept but a new concern. Free Radic Res 46:1339–1345
2. Trivedi PP, Jena GB (2012) Dextran sulfate sodium-induced ulcerative colitis leads to increased hematopoiesis and induces both local as well as systemic genotoxicity in mice. Mutat Res 744:172–183
3. Trivedi PP, Jena GB (2013) Role of alpha-lipoic acid in dextran sulfate sodium-induced ulcerative colitis in mice: studies on inflammation, oxidative stress, DNA damage and fibrosis. Food Chem Toxicol 59:339–355
4. Trivedi PP, Jena GB (2013) Ulcerative colitis-induced hepatic damage in mice: studies on inflammation, fibrosis, oxidative DNA damage and GST-P expression. Chem Biol Interact 201:19–30
5. Gassull MA (2003) Nutrition and inflammatory bowel disease: its relation to pathophysiology, outcome and therapy. Dig Dis 21:220–227
6. Sakamoto N, Kono S, Wakai K, Fukuda Y, Satomi M, Shimoyama T, Inaba Y, Miyake Y, Sasaki S, Okamoto K, Kobashi G, Washio M, Yokoyama T, Date C, Tanaka H (2005) Dietary risk factors for inflammatory bowel disease: a multicenter case-control study in Japan. Inflamm Bowel Dis 11:154–163
7. Fernandez-Banares F, Hinojosa J, Sanchez-Lombrana JL, Navarro E, Martinez-Salmeron JF, Garcia-Puges A, Gonzalez-Huix F, Riera J, Gonzalez-Lara V, Dominguez-Abascal F, Gine JJ, Moles J, Gomollon F, Gassull MA (1999) Randomized clinical trial of Plantago ovata seeds (dietary fiber) as compared with mesalamine in maintaining remission in ulcerative colitis. Spanish Group for the Study of Crohn’s Disease and Ulcerative Colitis (GETECCU). Am J Gastroenterol 94:427–433
8. Geerling BJ, Dagnelie PC, Badart-Smook A, Russel MG, Stockbrugger RW, Brummer RJ (2000) Diet as a risk factor for the development of ulcerative colitis. Am J Gastroenterol 95:1008–1013
9. Nair S, Norkus EP, Hertan H, Pitchumoni CS (2000) Micronutrient antioxidants in gastric mucosa and serum in patients with gastritis and gastric ulcer: does Helicobacter pylori infection affect the mucosal levels? J Clin Gastroenterol 30:381–385
10. Grune T, Lietz G, Palou A, Ross AC, Stahl W, Tang G, Thurnham D, Yin SA, Biesalski HK (2010) Beta-carotene is an important vitamin A source for humans. J Nutr 140:2268S–2285S
11. Dewan V, Patwari AK, Jain M, Dewan N (1995) A randomized controlled trial of vitamin A supplementation in acute diarrhea. Indian Pediatr 32:21–25
12. Zile M, Bunge C, Deluca HF (1977) Effect of vitamin A deficiency on intestinal cell proliferation in the rat. J Nutr 107:552–560
13. Chen P, Soares AM, Lima AA, Gamble MV, Schorling JB, Conway M, Barrett LJ, Blaner WS, Guerrant RL (2003) Association of vitamin A and zinc status with altered intestinal permeability: analyses of cohort data from northeastern Brazil. J Health Popul Nutr 21:309–315
14. Vieira MM, Paik J, Blaner WS, Soares AM, Mota RM, Guerrant RL, Lima AA (2008) Carotenoids, retinol, and intestinal barrier function in children from northeastern Brazil. J Pediatr Gastroenterol Nutr 47:652–659
15. Bero T, Nemeth A, Mozsik G, Javor T (1984) The effect of gastric cytoprotective drugs (atropine, cimetidine, vitamin-A) on the indomethacin induced intestinal ulcers in rats. Acta Physiol Hung 64:343–347
16. Mozsik G, Moron F, Nagy L, Ruzsa CS, Tarnok F, Javor T (1986) Evidence of the gastric cytoprotective effects of vitamin A, atropine and cimetidine on the development of gastric mucosal damage produced by administration of indomethacin in healthy subjects. Int J Tissue React 8:85–90
17. Hozawa A, Jacobs DR Jr, Steffes MW, Gross MD, Steffen LM, Lee DH (2007) Relationships of circulating carotenoid concentrations with several markers of inflammation, oxidative stress, and endothelial dysfunction: the Coronary Artery Risk Development in Young Adults (CARDIA)/Young Adult Longitudinal Trends in Antioxidants (YALTA) study. Clin Chem 53:447–455
18. Thomson CA, Stendell-Hollis NR, Rock CL, Cussler EC, Flatt SW, Pierce JP (2007) Plasma and dietary carotenoids are associated with reduced oxidative stress in women previously treated for breast cancer. Cancer Epidemiol Biomark Prev 16:2008–2015
19. Kim Y, Seo JH, Kim H (2011) Beta-carotene and lutein inhibit hydrogen peroxide-induced activation of NF-kappaB and IL-8 expression in gastric epithelial AGS cells. J Nutr Sci Vitaminol (Tokyo) 57:216–223
20. Jang SH, Lim JW, Kim H (2009) Beta-carotene inhibits Helicobacter pylori-induced expression of inducible nitric oxide synthase and cyclooxygenase-2 in human gastric epithelial AGS cells. J Physiol Pharmacol 60(Suppl 7):131–137
21. de Oliveira BF, Veloso CA, Nogueira-Machado JA, de Moraes EN, Santos RR, Cintra MT, Chaves MM (2012) Ascorbic acid, alpha-tocopherol, and beta-carotene reduce oxidative stress and proinflammatory cytokines in mononuclear cells of Alzheimer’s disease patients. Nutr Neurosci, in press
22. Maritim A, Dene BA, Sanders RA, Watkins JB 3rd (2002) Effects of beta-carotene on oxidative stress in normal and diabetic rats. J Biochem Mol Toxicol 16:203–208
23. Terao J, Minami Y, Bando N (2011) Singlet molecular oxygen-quenching activity of carotenoids: relevance to protection of the skin from photoaging. J Clin Biochem Nutr 48:57–62
24. Ben-Dor A, Steiner M, Gheber L, Danilenko M, Dubi N, Linnewiel K, Zick A, Sharoni Y, Levy J (2005) Carotenoids activate the antioxidant response element transcription system. Mol Cancer Ther 4:177–186
25. Ryden M, Garvin P, Kristenson M, Leanderson P, Ernerudh J, Jonasson L (2012) Provitamin A carotenoids are independently associated with matrix metalloproteinase-9 in plasma samples from a general population. J Intern Med 272:371–384
26. Fitzgerald KC, O’Reilly EJ, Fondell E, Falcone GJ, McCullough ML, Park Y, Kolonel LN, Ascherio A (2013) Intakes of vitamin C and carotenoids and risk of amyotrophic lateral sclerosis: pooled results from 5 cohort studies. Ann Neurol 73:236–245
27. Kaliappan G, Nagarajan P, Moorthy R, Kalai Gana Selvi S, Avinash Raj T, Mahesh Kumar J (2013) Ang II induce kidney damage by recruiting inflammatory cells and up regulates PPAR gamma and Renin 1 gene: effect of beta carotene on chronic renal damage. J Thromb Thrombolysis 36:277–285
28. Ogawa M, Kariya Y, Kitakaze T, Yamaji R, Harada N, Sakamoto T, Hosotani K, Nakano Y, Inui H (2013) The preventive effect of beta-carotene on denervation-induced soleus muscle atrophy in mice. Br J Nutr 109:1349–1358
29. Rachmilewitz D, Simon PL, Schwartz LW, Griswold DE, Fondacaro JD, Wasserman MA (1989) Inflammatory mediators of experimental colitis in rats. Gastroenterology 97:326–337
30. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275
31. Ohkawa H, Ohishi N, Yagi K (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95:351–358
32. Moron MS, Depierre JW, Mannervik B (1979) Levels of glutathione, glutathione reductase and glutathione S-transferase activities in rat lung and liver. Biochim Biophys Acta 582:67–78
33. Yoshihara K, Yajima T, Kubo C, Yoshikai Y (2006) Role of interleukin 15 in colitis induced by dextran sulphate sodium in mice. Gut 55:334–341
34. Kasamatsu T, Kohda K, Kawazoe Y (1996) Comparison of chemically induced DNA breakage in cellular and subcellular systems using the comet assay. Mutat Res 369:1–6
35. Speit G, Hartmann A (1999) The comet assay (single-cell gel test). A sensitive genotoxicity test for the detection of DNA damage and repair. Methods Mol Biol 113:203–212
36. Tripathi DN, Pawar AA, Vikram A, Ramarao P, Jena GB (2008) Use of the alkaline comet assay for the detection of transplacental genotoxins in newborn mice. Mutat Res 653:134–139
37. Holden HE, Majeska JB, Studwell D (1997) A direct comparison of mouse and rat bone marrow and blood as target tissues in the micronucleus assay. Mutat Res 391:87–89
38. Bhupathiraju SN, Wedick NM, Pan A, Manson JE, Rexrode KM, Willett WC, Rimm EB, Hu FB (2013) Quantity and variety in fruit and vegetable intake and risk of coronary heart disease. Am J Clin Nutr 98:1514–1523
39. Jansen RJ, Robinson DP, Stolzenberg-Solomon RZ, Bamlet WR, de Andrade M, Oberg AL, Rabe KG, Anderson KE, Olson JE, Sinha R, Petersen GM (2013) Nutrients from fruit and vegetable consumption reduce the risk of pancreatic cancer. J Gastrointest Cancer 44:152–161
40. Muzakova V, Kand’ar R, Meloun M, Skalicky J, Kralovec K, Zakova P, Vojtisek P (2010) Inverse correlation between plasma Beta-carotene and interleukin-6 in patients with advanced coronary artery disease. Int J Vitam Nutr Res 80:369–377
41. Liang J, Zhang B, Shen RW, Liu JB, Gao MH, Li Y, Li YY, Zhang W (2013) Preventive effect of halofuginone on concanavalin a-induced liver fibrosis. PLoS One 8:e82232
42. Liou GY, Doppler H, Necela B, Krishna M, Crawford HC, Raimondo M, Storz P (2013) Macrophage-secreted cytokines drive pancreatic acinar-to-ductal metaplasia through NF-kappaB and MMPs. J Cell Biol 202:563–577
43. Pan Y, Zhang X, Wang Y, Cai L, Ren L, Tang L, Wang J, Zhao Y, Wang Y, Liu Q, Li X, Liang G (2013) Targeting JNK by a new curcumin analog to inhibit NF-kB-mediated expression of cell adhesion molecules attenuates renal macrophage infiltration and injury in diabetic mice. PLoS One 8:e79084
44. Hegazy SK, El-Bedewy MM (2010) Effect of probiotics on pro-inflammatory cytokines and NF-kappaB activation in ulcerative colitis. World J Gastroenterol 16:4145–4151
45. Jena G, Trivedi PP (2013) A review of the use of melatonin in ulcerative colitis: experimental evidence and new approaches. Inflamm Bowel Dis 20:553–563
46. Trivedi PP, Jena GB (2013) Melatonin reduces ulcerative colitis-associated local and systemic damage in mice: investigation on possible mechanisms. Dig Dis Sci 58:3460–3474
47. Bai SK, Lee SJ, Na HJ, Ha KS, Han JA, Lee H, Kwon YG, Chung CK, Kim YM (2005) Beta-carotene inhibits inflammatory gene expression in lipopolysaccharide-stimulated macrophages by suppressing redox-based NF-kappaB activation. Exp Mol Med 37:323–334
48. Lin HW, Chang TJ, Yang DJ, Chen YC, Wang M, Chang YY (2012) Regulation of virus-induced inflammatory response by beta-carotene in RAW264.7 cells. Food Chem 134:2169–2175
49. Vivekananthan DP, Penn MS, Sapp SK, Hsu A, Topol EJ (2003) Use of antioxidant vitamins for the prevention of cardiovascular disease: meta-analysis of randomised trials. Lancet 361:2017–2023
50. Heliovaara M, Knekt P, Aho K, Aaran RK, Alfthan G, Aromaa A (1994) Serum antioxidants and risk of rheumatoid arthritis. Ann Rheum Dis 53:51–53
51. Kaulmann A, Serchi T, Renaut J, Hoffmann L, Bohn T (2012) Carotenoid exposure of Caco-2 intestinal epithelial cells did not affect selected inflammatory markers but altered their proteomic response. Br J Nutr 108:963–973
52. Smith TA (1998) Carotenoids and cancer: prevention and potential therapy. Br J Biomed Sci 55:268–275
53. Burton GW, Ingold KU (1984) Beta-carotene: an unusual type of lipid antioxidant. Science 224:569–573
54. Schafer FQ, Wang HP, Kelley EE, Cueno KL, Martin SM, Buettner GR (2002) Comparing beta-carotene, vitamin E and nitric oxide as membrane antioxidants. Biol Chem 383:671–681
55. Jin W, Wang HD, Hu ZG, Yan W, Chen G, Yin HX (2009) Transcription factor Nrf2 plays a pivotal role in protection against traumatic brain injury-induced acute intestinal mucosal injury in mice. J Surg Res 157:251–260
56. Aggarwal A, Shetti A, Keluskar V, Bagewadi A (2011) Estimation of serum beta carotene levels in patients with oral submucous fibrosis in India. J Oral Sci 53:427–431
57. Minami Y, Kawabata K, Kubo Y, Arase S, Hirasaka K, Nikawa T, Bando N, Kawai Y, Terao J (2009) Peroxidized cholesterol-induced matrix metalloproteinase-9 activation and its suppression by dietary beta-carotene in photoaging of hairless mouse skin. J Nutr Biochem 20:389–398
58. Wertz K, Seifert N, Hunziker PB, Riss G, Wyss A, Lankin C, Goralczyk R (2004) Beta-carotene inhibits UVA-induced matrix metalloprotease 1 and 10 expression in keratinocytes by a singlet oxygen-dependent mechanism. Free Radic Biol Med 37:654–670
59. Chen K, Wei Y, Sharp GC, Braley-Mullen H (2007) Decreasing TNF-alpha results in less fibrosis and earlier resolution of granulomatous experimental autoimmune thyroiditis. J Leukoc Biol 81:306–314
60. Cheresh P, Kim SJ, Tulasiram S, Kamp DW (2013) Oxidative stress and pulmonary fibrosis. Biochim Biophys Acta 1832:1028–1040
61. Galli F, Battistoni A, Gambari R, Pompella A, Bragonzi A, Pilolli F, Iuliano L, Piroddi M, Dechecchi MC, Cabrini G (2012) Oxidative stress and antioxidant therapy in cystic fibrosis. Biochim Biophys Acta 1822:690–713
62. Luedde T, Schwabe RF (2011) NF-kappaB in the liver-linking injury, fibrosis and hepatocellular carcinoma. Nat Rev Gastroenterol Hepatol 8:108–118
63. Chen H, Hu Y, Fang Y, Djukic Z, Yamamoto M, Shaheen NJ, Orlando RC, Chen X (2013) Nrf2 deficiency impairs the barrier function of mouse oesophageal epithelium. Gut 63:711–719
64. Filteau SM, Rollins NC, Coutsoudis A, Sullivan KR, Willumsen JF, Tomkins AM (2001) The effect of antenatal vitamin A and beta-carotene supplementation on gut integrity of infants of HIV-infected South African women. J Pediatr Gastroenterol Nutr 32:464–470