Inflammation related responses of intestinal cells to plum and cabbage digesta with differential carotenoid and polyphenol profiles following simulated gastrointestinal digestion

Molecular Nutrition and Food Research

Volumn 60, Issue 5, 2016, Pages 992-1005

  Kaulmann, Anouk ^a   Legay, Sylvain ^a   Schneider, Yves Jacques ^b   Hoffmann, Lucien ^a   Bohn, Torsten ^a,c  

^a LUXEMBOURG INSTITUTE OF SCIENCE AND TECHNOLOGY   (Luxembourg)

^b UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

^c LUXEMBOURG INSTITUTE OF HEALTH   (Luxembourg)

Author keywords

Digestion; Epithelium; Inflammation models; Nuclear receptors and cytokines; Phytochemicals

Indexed keywords

CAROTENOID; CYCLOOXYGENASE 2; CYTOKINE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; NFE2L2 PROTEIN, HUMAN; NITRIC OXIDE; NOS2 PROTEIN, HUMAN; POLYPHENOL; PTGS2 PROTEIN, HUMAN; TRANSCRIPTION FACTOR NRF2; TUMOR NECROSIS FACTOR;

BRASSICA; CACO-2 CELL LINE; CELL SURVIVAL; CHEMISTRY; COCULTURE; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; HT-29 CELL LINE; HUMAN; INFLAMMATION; METABOLISM; OXIDATIVE STRESS; PLUM; SECRETION (PROCESS);

BRASSICA; CACO-2 CELLS; CAROTENOIDS; CELL SURVIVAL; COCULTURE TECHNIQUES; CYCLOOXYGENASE 2; CYTOKINES; GENE EXPRESSION REGULATION; HT29 CELLS; HUMANS; INFLAMMATION; NF-E2-RELATED FACTOR 2; NF-KAPPA B; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; OXIDATIVE STRESS; POLYPHENOLS; PRUNUS DOMESTICA; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84963930737     PISSN: 16134125     EISSN: 16134133     Source Type: Journal    
DOI: 10.1002/mnfr.201500947     Document Type: Article

References (66)

1. Rekhy, R., McConchie, R., Promoting consumption of fruit and vegetables for better health. Have campaigns delivered on the goals? Appetite 2014, 79, 113-123.
2. Gan, Y., Tong, X., Li, L., Cao, S. et al., Consumption of fruit and vegetable and risk of coronary heart disease: a meta-analysis of prospective cohort studies. Int. J. Cardiol. 2015, 183, 129-137.
3. Wang, Y., Li, F., Wang, Z., Qiu, T. et al., Fruit and vegetable consumption and risk of lung cancer: a dose-response meta-analysis of prospective cohort studies. Lung Cancer 2015, 88, 124-130.
4. Wu, Y., Zhang, D., Jiang, X., Jiang, W., Fruit and vegetable consumption and risk of type 2 diabetes mellitus: a dose-reponse meta-analysis of prospective cohort studies. Nutr. Metab. Cardiovasc. Dis. 2015, 25, 140-147.
5. Siti, H. N., Kamisah, Y., Kamsiah, J., The role of oxidative stress, antioxidants and vascular inflammation in cardiovascular disease (a review). Vascul. Pharmacol. 2015, 71, 40-56.
6. Reuter, S., Gupta, S. C., Chaturvedi, M. M., Aggarwal, B. B., Oxidative stress, inflammation, and cancer: how are they linked? Free Radic. Biol. Med. 2010, 49, 1603-1616.
7. Kasinathan, N. K., Subramaniya, B. R., Pandian, I., Sivasithamparam, N. D., Aegle marmelos fruit extract abates dextran sodium sulfate induced acute colitis in mice: Repression of pro-inflammatory cytokines during colonic inflammation. Biomed. Prev. Nutr. 2014, 4, 307-317.
8. Ham, Y. M., Ko, Y. J., Song, S. M., Kim, J. et al., Anti-inflammatory effect of litsenolide B2 isolated from Litsea japonica fruit via suppressing NF-kB and MAPK pathways in LPS-induced RAW264.7 cells. J. Funct. Foods 2015, 13, 80-88.
9. Jiang, Y., Wu, S. H., Shu, X. O., Xiang, Y. B. et al., Cruciferous vegetable intake is inversely correlated with circulating levels of proinflammatory markers in women. J. Acad. Nutr. Diet 2014, 114, 700-708.
10. Cheng, A., Yan, H., Han, C., Wang, W. et al., Polyphenols from blueberries modulate inflammation cytokines in LPS-induced RAW264.7 macrophages. Int. J. Biol. Macromol. 2014, 69, 382-387.
11. Kaulmann, A., Bohn, T., Carotenoids, inflammation, and oxidative stress-implications of cellular signaling pathways and relation to chronic disease prevention. Nutr. Res. 2014, 34, 907-929.
12. Abhilash, P. A., Harikrishnan, R., Indira, M., Ascorbic acid suppresses endotoxemia and NF-kappaB signaling cascade in alcoholic liver fibrosis in guinea pigs: a mechanistic approach. Toxicol. Appl. Pharmacol. 2014, 274, 215-224.
13. Godbout, J. P., Berg, B. M., Kelley, K. W., Johnson, R. W., alpha-Tocopherol reduces lipopolysaccharide-induced peroxide radical formation and interleukin-6 secretion in primary murine microglia and in brain. J. Neuroimmunol. 2004, 149, 101-109.
14. Naska, A., Vasdekis, V. G., Trichopoulou, A., Friel, S. et al., Fruit and vegetable availability among ten European countries: how does it compare with the 'five-a-day' recommendation? DAFNE I and II projects of the European Commission. Br. J. Nutr. 2000, 84, 549-556.
15. Biehler, E., Alkerwi, A., Hoffmann, L., Krause, E. et al., Contribution of violaxanthin, neoxanthin, phytoene and phytofluene to total carotenoid intake: Assessment in Luxembourg. J. Food Compos. Anal. 2012, 25, 56-65.
16. Kaulmann, A., Jonville, M.C., Schneider, Y.J., Hoffmann, L., Bohn, T., Carotenoids, polyphenols and micronutrient profiles of Brassica oleraceae and plum varieties and their contribution to measures of total antioxidant capacity. Food Chem. 2014, 155, 240-250.
17. Sobczak, M., Fabisiak, A., Murawska, N., Wesolowska, E. et al., Current overview of extrinsic and intrinsic factors in etiology and progression of inflammatory bowel diseases. Pharmacol. Rep. 2014, 66, 766-775.
18. Roessner, A., Kuester, D., Malfertheiner, P., Schneider-Stock, R., Oxidative stress in ulcerative colitis-associated carcinogenesis. Pathol. Res. Pract. 2008, 204, 511-524.
19. Head, K., Jurenka, J. S., Inflammatory bowel disease. Part II: Crohn's disease-pathophysiology and conventional and alternative treatment options. Altern. Med. Rev. 2004, 9, 360-401.
20. Bleier, L., Wittig, I., Heide, H., Steger, M. et al., Generator-specific targets of mitochondrial reactive oxygen species. Free Radic. Biol. Med. 2015, 78, 1-10.
21. Holzerova, E., Prokisch, H., Mitochondria: much ado about nothing? How dangerous is reactive oxygen species production? Int. J. Biochem. Cell Biol. 2015, 63, 16-20.
22. Bouayed, J., Bohn, T., Exogenous antioxidants - Double-edged swords in cellular redox state: health beneficial effects at physiologic doses versus deleterious effects at high doses. Oxid. Med. Cell Longev. 2010, 3, 228-237.
23. Ma, X., Dang, C., Kang, H., Dai, Z. et al., Saikosaponin-D reduces cisplatin-induced nephrotoxicity by repressing ROS-mediated activation of MAPK and NF-kappaB signalling pathways. Int. Immunopharmacol. 2015, 28, 399-408.
24. Boeing, H., Bechthold, A., Bub, A., Ellinger, S. et al., Critical review: vegetables and fruit in the prevention of chronic diseases. Eur. J. Nutr. 2012, 51, 637-663.
25. Hur, S. J., Kang, S. H., Jung, H. S., Kim, S. C. et al., Review of natural products actions on cytokines in inflammatory bowel disease. Nutr. Res. 2012, 32, 801-816.
26. Somani, S. J., Modi, K. P., Majumdar, A. S., Sadarani, B. N., Phytochemicals and their potential usefulness in inflammatory bowel disease. Phytother. Res. 2015, 29, 339-350.
27. Rosillo, M. A., Alcaraz, M. J., Sanchez-Hidalgo, M., Fernandez-Bolanos, J. G. et al., Anti-inflammatory and joint protective effects of extra-virgin olive-oil polyphenol extract in experimental arthritis. J. Nutr. Biochem. 2014, 25, 1275-1281.
28. Ciccone, M. M., Cortese, F., Gesualdo, M., Carbonara, S. et al., Dietary intake of carotenoids and their antioxidant and anti-inflammatory effects in cardiovascular care. Mediators Inflamm. 2013, doi: 10.1155/2013/782137.
29. Linnewiel-Hermoni, K., Motro, Y., Miller, Y., Levy, J., Sharoni, Y., Carotenoid derivatives inhibit nuclear factor kappa B activity in bone and cancer cells by targeting key thiol groups. Free Radic. Biol. Med. 2014, 75, 105-120.
30. Romier, B., Van De, W. J., During, A., Larondelle, Y., Schneider, Y.J., Modulation of signalling nuclear factor-kappaB activation pathway by polyphenols in human intestinal Caco-2 cells. Br. J. Nutr. 2008, 100, 542-551.
31. Kaulmann, A., André, C. M., Schneider, Y. J., Hoffmann, L., Bohn, T., Carotenoid and polyphenol bioaccessibility and cellular uptake from plum and cabbage varieties Food Chem. 2016, 197, 325-332.
32. Chantret, I., Rodolosse, A., Barbat, A., Dussaulx, E. et al., Differential expression of sucrase-isomaltase in clones isolated from early and late passages of the cell line Caco-2: evidence for glucose-dependent negative regulation. J. Cell. Sci. 1994, 107 213-225.
33. Klein, S. G., Serchi, T., Hoffmann, L., Blomeke, B., Gutleb, A. C., An improved 3D tetraculture system mimicking the cellular organisation at the alveolar barrier to study the potential toxic effects of particles on the lung. Part Fibre Toxicol. 2013, 10, 31, doi: 10.1186/1743-8977-10-31.
34. Biehler, E., Bohn, T., Methods for assessing aspects of carotenoid bioavailability. Curr. Nutr. Food Sci. 2010, 6, 44-69.
35. Chanput, W., Mes, J. J., Wichers, H. J., THP-1 cell line: an in vitro cell model for immune modulation approach. Int. Immunopharmacol. 2014, 23, 37-45.
36. Kaulmann, A., Serchi, T., Renaut, J., Hoffmann, L., Bohn, T., Carotenoid exposure of Caco-2 intestinal epithelial cells did not affect selected inflammatory markers but altered their proteomic response. Br. J. Nutr. 2012, 108, 963-973.
37. Bustin, S. A., Benes, V., Garson, J. A., Hellemans, J. et al., The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin. Chem. 2009, 55, 611-622.
38. Hellemans, J., Mortier, G., De Paepe, A., Speleman, F., Vandesompele, J., qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data. Genome Biol. 2007, 8, R19.
39. Vandesompele, J., De Preter, K., Pattyn, F., Poppe, B. et al., Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 2002, 3, 1-11.
40. Bank, S., Andersen, P. S., Burisch, J., Pedersen, N. et al., Effectiveness of anti-tumour necrosis factor-alpha therapy in Danish patients with inflammatory bowel diseases. Dan. Med. J. 2014, 61, pii: A4994.
41. Araki, Y., Fujiyama, Y., Andoh, A., Nakamura, F. et al., Hydrophilic and hydrophobic bile acids exhibit different cytotoxicities through cytolysis, interleukin-8 synthesis and apoptosis in the intestinal epithelial cell lines IEC-6 and Caco-2 cells. Scand. J. Gastroenterol. 2001, 36, 533-539.
42. Neurath, M. F., Cytokines in inflammatory bowel disease. Nat. Rev. Immunol. 2014, 14, 329-342.
43. Schreiber, S., Nikolaus, S., Hampe, J., Activation of nuclear factor kappa B inflammatory bowel disease. Gut 1998, 42, 477-484.
44. DiDonato, J. A., Mercurio, F., Karin, M., NF-kappaB and the link between inflammation and cancer. Immunol. Rev. 2012, 246, 379-400.
45. Farzaei, M. H., Rahimi, R., Abdollahi, M., The role of dietary polyphenols in the management of inflammatory bowel disease. Curr. Pharm. Biotechnol. 2015, 16, 196-210.
46. Toh, J. Y., Tan, V. M., Lim, P. C., Lim, S. T., Chong, M. F., Flavonoids from fruit and vegetables: a focus on cardiovascular risk factors. Curr. Atheroscler. Rep. 2013, 15, 368. doi: 10.1007/s11883-013-0368-y.
47. Xie, C., Kang, J., Ferguson, M. E., Nagarajan, S. et al., Blueberries reduce pro-inflammatory cytokine TNF-alpha and IL-6 production in mouse macrophages by inhibiting NF-kappaB activation and the MAPK pathway. Mol. Nutr. Food Res. 2011, 55, 1587-1591.
48. Feng, D., Ling, W. H., Duan, R. D., Lycopene suppresses LPS-induced NO and IL-6 production by inhibiting the activation of ERK, p38MAPK, and NF-kappaB in macrophages. Inflamm. Res. 2010, 59, 115-121.
49. Joo, Y. E., Karrasch, T., Muhlbauer, M., Allard, B. et al., Tomato lycopene extract prevents lipopolysaccharide-induced NF-kappaB signaling but worsens dextran sulfate sodium-induced colitis in NF-kappa BEGFP mice. PLoS One, 2009, e4562 doi: 10.1371/journal.pone.0004562.
50. Basanta, M. F., Ponce, N. M., Rojas, A. M., Stortz, C. A., Effect of extraction time and temperature on the characteristics of loosely bound pectins from Japanese plum. Carbohydr. Polym. 2012, 89, 230-235.
51. Broom, O. J., Widjaya, B., Troelsen, J., Olsen, J., Nielsen, O. H., Mitogen activated protein kinases: a role in inflammatory bowel disease? Clin. Exp. Immunol. 2009, 158, 272-280.
52. Kang, S. R., Park, K., Park, H. S., Lee, D. H. et al., Anti-inflammatory effect of flavonoids isolated from Korea Citrus aurantium L. on lipopolysaccharide-induced mouse macrophage RAW 264.7 cells by blocking of nuclear factor-kappa B (NF-κB) and mitogen-activated protein kinase (MAPK) signalling pathways. Food Chem. 2011, 129, 1721-1728.
53. Lidder, S., Webb, A. J., Vascular effects of dietary nitrate (as found in green leafy vegetables and beetroot) via the nitrate-nitrite-nitric oxide pathway. Br. J. Clin. Pharmacol. 2013, 75, 677-696.
54. Sporn, M. B., Liby, K. T., NRF2 and cancer: the good, the bad and the importance of context. Nat. Rev. Cancer 2012, 12, 564-571.
55. Myers, J. N., Schaffer, M. W., Korolkova, O. Y., Williams, A. D. et al., Implications of the colonic deposition of free hemoglobin-alpha chain: a previously unknown tissue by-product in inflammatory bowel disease. Inflamm. Bowel Dis. 2014, 20, 1530-1547.
56. Ben-Dor, A., Steiner, M., Gheber, L., Danilenko, M. et al., Carotenoids activate the antioxidant response element transcription system. Mol. Cancer Ther. 2005, 4, 177-186.
57. Sriram, N., Kalayarasan, S., Sudhandiran, G., Epigallocatechin-3-gallate augments antioxidant activities and inhibits inflammation during bleomycin-induced experimental pulmonary fibrosis through Nrf2-Keap1 signaling. Pulm Pharmacol. Ther. 2009, 22, 221-236.
58. Palozza, P., Prooxidant actions of carotenoids in biologic systems. Nutr. Rev. 1998, 56, 257-265.
59. Martin, D. A., Bolling, B. W., A review of the efficacy of dietary polyphenols in experimental models of inflammatory bowel diseases. Food Funct. 2015, 6, 1773-1786.
60. Hartel, C., Strunk, T., Bucsky, P., Schultz, C., Effects of vitamin C on intracytoplasmic cytokine production in human whole blood monocytes and lymphocytes. Cytokine 2004, 27, 101-106.
61. Son, E. W., Mo, S. J., Rhee, D. K., Pyo, S., Vitamin C blocks TNF-alpha-induced NF-kappaB activation and ICAM-1 expression in human neuroblastoma cells. Arch. Pharm. Res. 2004, 27, 1073-1079.
62. Navarro, S. L., Schwarz, Y., Song, X., Wang, C. Y. et al., Cruciferous vegetables have variable effects on biomarkers of systemic inflammation in a randomized controlled trial in healthy young adults. J. Nutr. 2014, 144, 1850-1857.
63. Broadbelt, N. V., Stahl, P. J., Chen, J., Mizrahi, M. et al., Early upregulation of iNOS mRNA expression and increase in NO metabolites in pressurized renal epithelial cells. Am. J. Physiol. Renal Physiol. 2007, 293, F1877-1888.
64. Kalita, M., Tian, B., Gao, B., Choudhary, S. et al., Systems approaches to modeling chronic mucosal inflammation. Biomed. Res. Int. 2013, 2013, 505864. doi: 10.1155/2013/505864. Epub 2013 Oct 21.
65. Garbin, U., Fratta Pasini, A., Stranieri, C., Cominacini, M. et al., Cigarette smoking blocks the protective expression of Nrf2/ARE pathway in peripheral mononuclear cells of young heavy smokers favouring inflammation. PLoS One 2009, 4, e8225. doi: 10.1371/journal.pone.0008225.
66. Novitskiy, S. V., Ryzhov, S., Zaynagetdinov, R., Goldstein, A. E. et al., Adenosine receptors in regulation of dendritic cell differentiation and function. Blood 2008, 112, 1822-1831.