Dietary polyunsaturated fatty acids and heme iron induce oxidative stress biomarkers and a cancer promoting environment in the colon of rats

Free Radical Biology and Medicine

Volumn 83, Issue , 2015, Pages 192-200

  Guéraud, Françoise ^a   Taché, Sylviane ^a   Steghens, Jean Paul ^a   Milkovic, Lidija ^b   Borovic Sunjic, Suzana ^c   Zarkovic, Neven ^c   Gaultier, Eric ^a   Naud, Nathalie ^a   Héliès Toussaint, Cécile ^a   Pierre, Fabrice ^a   Priymenko, Nathalie ^a  

^a TOXALIM RESEARCH CENTRE IN FOOD TOXICOLOGY   (France)

^b UNIVERSITÉ LYON 1   (France)

^c RUDER BO KOVI INSTITUTE   (Croatia)

Author keywords

4 Hydroxynonenal; Biomarkers; Colorectal cancer; Heme iron; Lipid peroxidation; Malondialdehyde; Polyunsaturated fatty acids

Indexed keywords

4 HYDROXYNONENAL; BIOLOGICAL MARKER; C REACTIVE PROTEIN; FERRIC CITRATE; HEME; MALONALDEHYDE; MYELOPEROXIDASE; POLYUNSATURATED FATTY ACID; THIOBARBITURIC ACID REACTIVE SUBSTANCE; ANTIOXIDANT; IRON; REACTIVE OXYGEN METABOLITE; UNSATURATED FATTY ACID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BODY WEIGHT; CANCER RISK; COLON CARCINOGENESIS; CONTROLLED STUDY; CYTOTOXICITY; CYTOTOXICITY ASSAY; FAT INTAKE; FATTY ACID ANALYSIS; FEMALE; FOOD INTAKE; INTESTINE ABSORPTION; LIPID COMPOSITION; LIPID OXIDATION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT; URINARY EXCRETION; ADVERSE EFFECTS; ANIMAL; COLON; COLONIC NEOPLASMS; DIET; DRUG EFFECTS; FISCHER 344 RAT; LIPID PEROXIDATION; METABOLISM; MOUSE; PATHOLOGY; RECTAL NEOPLASMS; TUMOR CELL CULTURE; TUMOR MICROENVIRONMENT; URINE;

RATTUS;

ANIMALS; ANTIOXIDANTS; BIOMARKERS; COLON; COLONIC NEOPLASMS; DIET; FATTY ACIDS, UNSATURATED; FEMALE; HEME; IRON; LIPID PEROXIDATION; MALONDIALDEHYDE; MICE; OXIDATIVE STRESS; RATS; RATS, INBRED F344; REACTIVE OXYGEN SPECIES; RECTAL NEOPLASMS; THIOBARBITURIC ACID REACTIVE SUBSTANCES; TUMOR CELLS, CULTURED; TUMOR MICROENVIRONMENT;

EID: 84927938173     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2015.02.023     Document Type: Article

References (56)

1. K. Casós, M.C. Zaragozá, N. Zarkovic, K. Zarkovic, L. Andrisic, M. Portero-Otín, D. Cacabelos, and M.T. Mitjavila A fish-oil-rich diet reduces vascular oxidative stress in apoE(-/-) mice Free Radic. Res. 44 2010 821 829
2. H. Esterbauer, R.J. Schaur, and H. Zollner Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes Free Radic. Biol. Med. 11 1991 81 128
3. S.N. Dhanakoti, and H.H. Draper Response of urinary malondialdehyde to factors that stimulate lipid peroxidation in vivo Lipids 22 1987 643 646
4. M.S. Babu, Z. Bobby, and S. Habeebullah Increased inflammatory response and imbalance in blood and urinary oxidant-antioxidant status in South Indian women with gestational hypertension and preeclampsia Clin. Biochem. 45 2012 835 838
5. P. Gomes, S. Simão, E. Silva, V. Pinto, J.S. Amaral, J. Afonso, M.P. Serrão, M.J. Pinho, and P. Soares-da-Silva Aging increases oxidative stress and renal expression of oxidant and antioxidant enzymes that are associated with an increased trend in systolic blood pressure Oxid. Med. Cell. Longev. 2 2009 138 145
6. S. Bae, X.-C. Pan, S.-Y. Kim, K. Park, Y.-H. Kim, H. Kim, and Y.-C. Hong Exposures to particulate matter and polycyclic aromatic hydrocarbons and oxidative stress in schoolchildren Environ. Health Perspect. 118 2010 579 583
7. R. Sirota, S. Gorelik, R. Harris, R. Kohen, and J. Kanner Coffee polyphenols protect human plasma from postprandial carbonyl modifications Mol. Nutr. Food Res. 57 2013 916 919
8. S. Gorelik, M. Ligumsky, R. Kohen, and J. Kanner A novel function of red wine polyphenols in humans: prevention of absorption of cytotoxic lipid peroxidation products FASEB J. 22 2008 41 46
9. N. Zarkovic 4-Hydroxynonenal as a bioactive marker of pathophysiological processes Mol. Aspects Med. 24 2003 281 291
10. G. Peiro, J. Alary, J.-P. Cravedi, E. Rathahao, J.-P. Steghens, and F. Guéraud Dihydroxynonene mercapturic acid, a urinary metabolite of 4-hydroxynonenal, as a biomarker of lipid peroxidation BioFactors 24 2005 89 96
11. H.C. Kuiper, C.L. Miranda, J.D. Sowell, and J.F. Stevens Mercapturic acid conjugates of 4-hydroxy-2-nonenal and 4-oxo-2-nonenal metabolites are in vivo markers of oxidative stress J. Biol. Chem. 283 2008 17131 17138
12. H.C. Kuiper, R.S. Bruno, M.G. Traber, and J.F. Stevens Vitamin C supplementation lowers urinary levels of 4-hydroperoxy-2-nonenal metabolites in humans Free Radic. Biol. Med. 50 2011 848 853
13. F. Pierre, R. Santarelli, S. Taché, F. Guéraud, and D.E. Corpet Beef meat promotion of dimethylhydrazine-induced colorectal carcinogenesis biomarkers is suppressed by dietary calcium Br. J. Nutr. 99 2008 1000 1006
14. F. Pierre, G. Peiro, S. Taché, A.J. Cross, S.A. Bingham, N. Gasc, G. Gottardi, D.E. Corpet, and F. Guéraud New marker of colon cancer risk associated with heme intake: 1,4-dihydroxynonane mercapturic acid Cancer Epidemiol. Biomark. Prev. 15 2006 2274 2279
15. N. Gasc, S. Taché, E. Rathahao, J. Bertrand-Michel, V. Roques, and F. Guéraud 4-hydroxynonenal in foodstuffs: heme concentration, fatty acid composition and freeze-drying are determining factors Redox Rep. 12 2007 40 44
16. C.M. Seppanen, and A.S. Csallany Incorporation of the toxic aldehyde 4-hydroxy-2-trans-nonenal into food fried in thermally oxidized soybean oil J. Am. Oil Chem. Soc. 81 2004 1137 1141
17. C.M. Seppanen, and A.S. Csallany Formation of 4-hydroxynonenal, a toxic aldehyde, in soybean oil at frying temperature J. Am. Oil Chem. Soc. 79 2002 1033 1038
18. L.J. Roberts, and J.D. Morrow Measurement of F(2)-isoprostanes as an index of oxidative stress in vivo Free Radic. Biol. Med. 28 2000 505 513
19. N. Zarković, K. Zarković, R.J. Schaur, S. Stolc, G. Schlag, H. Redl, G. Waeg, S. Borović, I. Loncarić, G. Jurić, and V. Hlavka 4-Hydroxynonenal as a second messenger of free radicals and growth modifying factor Life Sci. 65 1999 1901 1904
20. F. Pierre, S. Taché, C.R. Petit, R. Van der Meer, and D.E. Corpet Meat and cancer: haemoglobin and haemin in a low-calcium diet promote colorectal carcinogenesis at the aberrant crypt stage in rats Carcinogenesis 24 2003 1683 1690
21. F. Pierre, A. Freeman, S. Taché, R. Van der Meer, and D.E. Corpet Beef meat and blood sausage promote the formation of azoxymethane-induced mucin-depleted foci and aberrant crypt foci in rat colons J. Nutr. 134 2004 2711 2716
22. F. Pierre, S. Tache, F. Guéraud, A.L. Rerole, M.-L. Jourdan, and C. Petit Apc mutation induces resistance of colonic cells to lipoperoxide-triggered apoptosis induced by faecal water from haem-fed rats Carcinogenesis 28 2007 321 327
23. C. Van Der Meer-Van Kraaij, E.M.M. Van Lieshout, E. Kramer, R. Van Der Meer, and J. Keijer Mucosal pentraxin (Mptx), a novel rat gene 10-fold down-regulated in colon by dietary heme FASEB J. 17 2003 1277 1285
24. A.L. Sesink, D.S. Termont, J.H. Kleibeuker, and R. Van der Meer Red meat and colon cancer: the cytotoxic and hyperproliferative effects of dietary heme Cancer Res. 59 1999 5704 5709
25. J.P. Steghens, A.L. van Kappel, I. Denis, and C. Collombel Diaminonaphtalene, a new highly specific reagent for HPLC-UV measurement of total and free malondialdehyde in human plasma or serum Free Radic. Biol. Med. 31 2001 242 249
26. F. Guéraud, G. Peiro, H. Bernard, J. Alary, C. Créminon, L. Debrauwer, E. Rathahao, M.-F. Drumare, C. Canlet, J.-M. Wal, and G. Bories Enzyme immunoassay for a urinary metabolite of 4-hydroxynonenal as a marker of lipid peroxidation Free Radic. Biol. Med. 40 2006 54 62
27. P. Pradelles, J. Grassi, and J. Maclouf Enzyme immunoassays of eicosanoids using acetylcholine esterase as label: an alternative to radioimmunoassay Anal. Chem. 57 1985 1170 1173
28. Z. Wang, G. Ciabattoni, C. Créminon, J. Lawson, G.A. Fitzgerald, C. Patrono, and J. Maclouf Immunological characterization of urinary 8-epi-prostaglandin F2 alpha excretion in man J. Pharmacol. Exp. Ther. 275 1995 94 100
29. J. Folch, M. Lees, and G.H. Sloane Stanley A simple method for the isolation and purification of total lipides from animal tissues J. Biol. Chem. 226 1957 497 509
30. S. Borovic, F. Rabuzin, G. Waeg, and N. Zarkovic Enzyme-linked immunosorbent assay for 4-hydroxynonenal-histidine conjugates Free Radic. Res. 40 2006 809 820
31. G. Waeg, G. Dimsity, and H. Esterbauer Monoclonal antibodies for detection of 4-hydroxynonenal modified proteins Free Radic. Res. 25 1996 149 159
32. P.P. Bradley, D.A. Priebat, R.D. Christensen, and G. Rothstein Measurement of cutaneous inflammation: estimation of neutrophil content with an enzyme marker J. Invest. Dermatol. 78 1982 206 209
33. H. Ohkawa, N. Ohishi, and K. Yagi Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction Anal. Biochem. 95 1979 351 358
34. V. Forest, M. Clement, F. Pierre, K. Meflah, and J. Menanteau Butyrate restores motile function and actin cytoskeletal network integrity in apc mutated mouse colon epithelial cells Nutr. Cancer 45 2003 84 92
35. B. Lorrain, O. Dangles, M. Loonis, M. Armand, and C. Dufour Dietary iron-initiated lipid oxidation and its inhibition by polyphenols in gastric conditions J. Agric. Food Chem. 60 2012 9074 9081
36. V. Roginsky, G.A. Zheltukhina, and V.E. Nebolsin Efficacy of metmyoglobin and hemin as a catalyst of lipid peroxidation determined by using a new testing system J. Agric. Food Chem. 55 2007 6798 6806
37. N. IJssennagger, M. Derrien, G.M. van Doorn, A. Rijnierse, B. van den Bogert, M. Müller, J. Dekker, M. Kleerebezem, and R. van der Meer Dietary heme alters microbiota and mucosa of mouse colon without functional changes in host-microbe cross-talk PloS One 7 2012 e49868
38. A. Marquez-Quiñones, A. Cipak, K. Zarkovic, S. Fattel-Fazenda, S. Villa-Treviño, G. Waeg, N. Zarkovic, and F. Guéraud HNE-protein adducts formation in different pre-carcinogenic stages of hepatitis in LEC rats Free Radic. Res. 44 2010 119 127
39. N. Zarkovic, A. Cipak, M. Jaganjac, S. Borovic, and K. Zarkovic Pathophysiological relevance of aldehydic protein modifications J. Proteomics 92 2013 239 247
40. K. Larsson, L. Cavonius, M. Alminger, and I. Undeland Oxidation of cod liver oil during gastrointestinal in vitro digestion J. Agric. Food Chem. 60 2012 7556 7564
41. J. Kanner, and T. Lapidot The stomach as a bioreactor: dietary lipid peroxidation in the gastric fluid and the effects of plant-derived antioxidants Free Radic. Biol. Med. 31 2001 1388 1395
42. J.D. Morrow, K.E. Hill, R.F. Burk, T.M. Nammour, K.F. Badr, and L.J. Roberts 2nd A series of prostaglandin F2-like compounds are produced in vivo in humans by a non-cyclooxygenase, free radical-catalyzed mechanism Proc. Natl. Acad. Sci. USA 87 1990 9383 9387
43. D. Li, A. Ng, N.J. Mann, and A.J. Sinclair Contribution of meat fat to dietary arachidonic acid Lipids 33 1998 437 440
44. N.K. Gopaul, B. Halliwell, and E.E. Anggård Measurement of plasma F2-isoprostanes as an index of lipid peroxidation does not appear to be confounded by diet Free Radic. Res. 33 2000 115 127
45. J. Kanner Oxidative processes in meat and meat products: quality implications Meat Sci. 36 1994 169 189
46. World Cancer Research Fund. WCRF Food, nutrition, physical activity, and the prevention of cancer: a global perspective 2007 World Cancer Research Fund and American Institute for Cancer Research Washington, DC
47. M. Cindric, A. Cipak, E. Zapletal, M. Jaganjac, L. Milkovic, G. Waeg, S. Stolc, N. Zarkovic, and S. Sunjic Borovic Stobadine attenuates impairment of an intestinal barrier model caused by 4-hydroxynonenal Toxicol. In Vitro 27 2013 426 432
48. N. Merendino, L. Costantini, L. Manzi, R. Molinari, D. D'Eliseo, and F. Velotti Dietary ω -3 polyunsaturated fatty acid DHA: a potential adjuvant in the treatment of cancer BioMed Res. Int. 2013/310186 2013
49. C.H. MacLean, S.J. Newberry, W.A. Mojica, P. Khanna, A.M. Issa, M.J. Suttorp, Y.-W. Lim, S.B. Traina, L. Hilton, R. Garland, and S.C. Morton Effects of omega-3 fatty acids on cancer risk: a systematic review J. Am. Med. Assoc. 295 2006 403 415
50. A. Geelen, J.M. Schouten, C. Kamphuis, B.E. Stam, J. Burema, J.M.S. Renkema, E.-J. Bakker, P. van't Veer, and E. Kampman Fish consumption, n-3 fatty acids, and colorectal cancer: a meta-analysis of prospective cohort studies Am. J. Epidemiol. 166 2007 1116 1125
51. M. Gerber Omega-3 fatty acids and cancers: a systematic update review of epidemiological studies Br. J. Nutr. 107 Suppl. 2 2012 S228 S239
52. P.C. Calder n-3 polyunsaturated fatty acids, inflammation, and inflammatory diseases Am. J. Clin. Nutr. 83 2006 1505S 1519S
53. H.F. Turk, and R.S. Chapkin Membrane lipid raft organization is uniquely modified by n-3 polyunsaturated fatty acids Prostaglandins Leukot. Essent. Fatty Acids 88 2013 43 47
54. S.C. Dyall Methodological issues and inconsistencies in the field of omega-3 fatty acids research Prostaglandins Leukot. Essent. Fatty Acids 85 2011 281 285
55. M. Awada, C.O. Soulage, A. Meynier, C. Debard, P. Plaisancié, B. Benoit, G. Picard, E. Loizon, M.-A. Chauvin, M. Estienne, N. Peretti, M. Guichardant, M. Lagarde, C. Genot, and M.-C. Michalski Dietary oxidized n-3 PUFA induce oxidative stress and inflammation: role of intestinal absorption of 4-HHE and reactivity in intestinal cells J. Lipid Res. 53 2012 2069 2080
56. N. Bastide, F. Chenni, M. Audebert, R. Santarelli, S. Tache, N. Naud, M. Baradat, I. Jouanin, R. Surya, D.A. Hobbs, G.G. Kuhnle, I. Raymond-Letron, F. Gueraud, D. Corpet, and F. Pierre A central role for heme iron in colon carcinogenesis associated with red meat intake Cancer Res. 75 2015 870 879