Lipid hydroperoxide-induced and hemoglobin-enhanced oxidative damage to colon cancer cells

Free Radical Biology and Medicine

Volumn 51, Issue 2, 2011, Pages 503-515

  Angeli, José Pedro F ^a   Garcia, Camila Carrião M ^a   Sena, Fernanda ^a   Freitas, Florencio P ^a   Miyamoto, Sayuri ^a   Medeiros, Marisa Helena G ^a   Di Mascio, Paolo ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

DNA adducts; DNA damage; Free radicals; HPLC ESI MS MS; Lipid hydroperoxide; Oxidative stress

Indexed keywords

1,N2 ETHENO 2' DEOXYGUANOSINE; 8 HYDROXYDEOXYGUANOSINE; DEOXYGUANOSINE DERIVATIVE; DNA; HEME; HEMOGLOBIN; IRON; LINOLEIC ACID HYDROPEROXIDE; LIPID HYDROPEROXIDE; MALONALDEHYDE; UNCLASSIFIED DRUG;

ARTICLE; CANCER CELL; CELL DEATH; CELL LEVEL; COLON CANCER; CONTROLLED STUDY; CYTOTOXICITY; DNA DAMAGE; DNA FRAGMENTATION; GENOTOXICITY; HUMAN; HUMAN CELL; LIPID PEROXIDATION; OXIDATION; OXIDATION REDUCTION STATE; OXIDATIVE STRESS; PRIORITY JOURNAL;

CELL LINE, TUMOR; COLONIC NEOPLASMS; COMET ASSAY; HEMOGLOBINS; HUMANS; LIPID PEROXIDES; MALONDIALDEHYDE; OXIDATION-REDUCTION; OXIDATIVE STRESS;

EID: 79959346587     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2011.04.015     Document Type: Article

References (76)

1. L. Tomatis, A. Aitio, N.E. Day, and E. Heseltine Cancer: Causes, Occurrence and Control 1990 IARC Publ. Lyon
2. J.H. Cummings, and S.A. Bingham Diet and the prevention of cancer BMJ 317 1998 1636 1640 (Pubitemid 128719737)
3. W.L. Stone, and A.M. Papas Tocopherols and the etiology of colon cancer J. Natl Cancer Inst. 89 1997 1006 1014 (Pubitemid 27327865)
4. T. Sjoblom, S. Jones, L.D. Wood, D.W. Parsons, J. Lin, T.D. Barber, D. Mandelker, R.J. Leary, J. Ptak, N. Silliman, S. Szabo, P. Buckhaults, C. Farrell, P. Meeh, S.D. Markowitz, J. Willis, D. Dawson, J.K. Willson, A.F. Gazdar, J. Hartigan, L. Wu, C. Liu, G. Parmigiani, B.H. Park, K.E. Bachman, N. Papadopoulos, B. Vogelstein, K.W. Kinzler, and V.E. Velculescu The consensus coding sequences of human breast and colorectal cancers Science 314 2006 268 274 (Pubitemid 44571966)
5. L.R. Ferguson Dietary influences on mutagenesis-where is this field going? Environ. Mol. Mutagen. 51 2010 909 918
6. E.L. Wynder, T. Kajitani, S. Ishikawa, H. Dodo, and A. Takano Environmental factors of cancer of the colon and rectum. II. Japanese epidemiological data Cancer 23 1969 1210 1220
7. N. Bakker, P. Van't Veer, and P.L. Zock Adipose fatty acids and cancers of the breast, prostate and colon: an ecological study Int. J. Cancer 72 1997 587 591 (Pubitemid 27356157)
8. G.R. Howe, K.J. Aronson, and E. Benito The relationship between dietary fat intake and risk of colorectal cancer: evidence from the combined analysis of 13 case-control studies Cancer Causes Control 8 1997 215 228 (Pubitemid 27170377)
9. World Cancer Research Fund Food, Nutrition and the Prevention of Cancer: a Global Perspective 1997 Am. Inst. Cancer Res Washington, DC
10. A. Nkondjock, B. Shatenstein, P. Maisonneuve, and P. Ghadirian Assessment of risk associated with specific fatty acids and colorectal cancer among French-Canadians in Montreal: a case-control study Int. J. Epidemiol. 32 2003 200 209 (Pubitemid 36622263)
11. H. Bartsch, J. Nair, and R.W. Owen Dietary polyunsaturated fatty acids and cancers of the breast and colorectum: emerging evidence for their role as risk modifiers Carcinogenesis 20 1999 2209 2218 (Pubitemid 30015890)
12. S.A. Broitman, J.J. Vitale, E. Vavrousek-Jakuba, and L.S. Gottlieb Polyunsaturated fat, cholesterol and large bowel tumorigenesis Cancer 40 1977 2455 2463 (Pubitemid 8237747)
13. K.K. Carroll, and H.T. Khor Effects of level and type of dietary fat on incidence of mammary tumors induced in female Sprague-Dawley rats by 7,12-dimethylbenzanthracene Lipids 6 1971 415 420
14. R.L. Prentice, and L. Sheppard Dietary fat and cancer: consistency of the epidemiologic data, and disease prevention that may follow from a practical reduction in fat consumption Cancer Causes Control 1 1990 81 97
15. S. Sasaki, M. Horacsek, and H. Kesteloot An ecological study of the relationship between dietary fat intake and breast cancer mortality Prev. Med. 22 1993 187 202 (Pubitemid 23150663)
16. T.M. de Kok, I. Zwingman, E.J. Moonen, P.A. Schilderman, E. Rhijnsburger, G.R. Haenen, and J.C. Kleinjans Analysis of oxidative DNA damage after human dietary supplementation with linoleic acid Food Chem. Toxicol. 41 2003 351 358 (Pubitemid 36015772)
17. C.W. Welsch Enhancement of mammary tumorigenesis by fat: review of potential mechanisms Am. J. Clin. Nutr. 45 1987 192 202
18. B.N. Ames Dietary carcinogens and anticarcinogens: oxygen radicals and degenerative diseases Science 221 1983 1256 1264
19. D.A. Parks, G.B. Bulkley, and D.N. Granger Role of oxygen-derived free radicals in digestive tract diseases Surgery 94 1983 415 422 (Pubitemid 13007943)
20. I.A. Blair Lipid hydroperoxide-mediated DNA damage Exp. Gerontol. 19 2010 280 291
21. M.H.G. Medeiros Exocyclic DNA adducts as biomarkers of lipid oxidation and predictors of disease: challenges in developing sensitive and specific methods for clinical studies Chem. Res. Toxicol. 22 2009 419 425
22. H. Esternbauer Cytotoxicity and genotoxicity of lipid oxidation products Am. J. Clin. Nutr. 57 1993 779 785
23. H. Bartsch, J. Nair, and R.W. Owen Dietary polyunsaturated fatty acids and cancer of the breast and colorectum: emerging evidence for their role as risk modifiers Carcinogenesis 12 1999 2209 2218 (Pubitemid 30015890)
24. B.S. Reddy, C. Burill, and J. Rigotty Effect of diets high in omega-3 and omega-6 fatty acids on initiation and postinitiation stages of colon carcinogenesis Cancer Res. 51 1991 487 491
25. I.A. Brouwer, M.B. Katan, and P.L. Zock Dietary alpha-linolenic acid is associated with reduced risk of fatal coronary heart disease, but increased prostate cancer risk: a meta-analysis J. Nutr. 134 2004 919 922 (Pubitemid 38456264)
26. S.P. Wolff, and J. Nourooz-Zadeh Hypothesis: UK consumption of dietary lipid hydroperoxides-a possible contributory factor to atherosclerosis Atherosclerosis 119 1996 261 263 (Pubitemid 26029451)
27. N.V. Rohr-Udilova, K. Stolze, S. Sagmeister, H. Nohl, R. Schulte-Hermann, and B. Grasl-Kraupp Lipid hydroperoxides from processed dietary oils enhance growth of hepatocarcinoma cells Mol. Nutr. Food Res. 52 2008 352 359
28. K. Kanazawa, and H. Ashida Catabolic fate of dietary trilinoleoylglycerol hydroperoxides in rat gastrointestines Biochim. Biophys. Acta 1393 1998 336 348 (Pubitemid 28467059)
29. K. Kanazawa, and H. Ashida Dietary hydroperoxides of linoleic acid decompose to aldehydes in stomach before being absorbed into the body Biochim. Biophys. Acta 1393 1998 349 361 (Pubitemid 28467060)
30. S. Miyamoto, C. Dupas, K. Murota, and J. Terao Phospholipid hydroperoxides are detoxified by phospholipase A2 and GSH peroxidase in rat gastric mucosa Lipids 38 2003 641 649 (Pubitemid 36944698)
31. E. Friedman, P. Isaksson, J. Rafter, B. Marian, S. Winawer, and H. Newmark Fecal diglycerides as selective endogenous mitogens for premalignant and malignant human colonic epithelial cells Cancer Res. 49 1989 544 548 (Pubitemid 19050312)
32. D. Jurek, N. Udilova, A. Jozkowicz, H. Nohl, B. Marian, and R. Schulte-Hermann Dietary lipid hydroperoxides induce expression of vascular endothelial growth factor (VEGF) in human colorectal tumor cells FASEB J. 19 2005 97 99 (Pubitemid 40069930)
33. T. Norat, S. Bingham, P. Ferrari, N. Slimani, M. Jenab, M. Mazuir, K. Overvad, A. Olsen, A. Tjønneland, F. Clavel, M.C. Boutron-Ruault, E. Kesse, H. Boeing, M.M. Bergmann, A. Nieters, J. Linseisen, A. Trichopoulou, D. Trichopoulos, Y. Tountas, F. Berrino, D. Palli, S. Panico, R. Tumino, P. Vineis, H.B. Bueno-de-Mesquita, P.H. Peeters, D. Engeset, E. Lund, G. Skeie, E. Ardanaz, C. González, C. Navarro, J.R. Quirós, M.J. Sanchez, G. Berglund, I. Mattisson, G. Hallmans, R. Palmqvist, N.E. Day, K.T. Khaw, T.J. Key, M. San Joaquin, B. Hémon, R. Saracci, R. Kaaks, and E. Riboli Meat, fish, and colorectal cancer risk: the European prospective investigation into cancer and nutrition J. Natl Cancer Inst. 97 2005 906 916 (Pubitemid 41417942)
34. D.H. Lee, K.E. Anderson, L.J. Harnack, A.R. Folsom, and D.R. Jacobs Jr. Heme iron, zinc, alcohol consumption, and colon cancer: Iowa Women's Health Study J. Natl Cancer Inst. 96 2004 403 407 (Pubitemid 38351302)
35. A. Tappel Heme of consumed red meat can act as a catalyst of oxidative damage and could initiate colon, breast and prostate cancers, heart disease and other diseases Med. Hypotheses 68 2007 562 564 (Pubitemid 46037986)
36. T. Sawa, T. Akaike, K. Kida, Y. Fukushima, K. Takagi, and H. Maeda Lipid peroxyl radicals from oxidized oils and heme-iron: implication of a high-fat diet in colon carcinogenesis Cancer Epidemiol. Biomarkers Prev. 7 1998 1007 1012 (Pubitemid 28514101)
37. M. Glei, S. Klenow, J. Sauer, U. Wegewitz, K. Richter, and B.L. Pool-Zobel Hemoglobin and hemin induce DNA damage in human colon tumor cells HT29 clone 19A and in primary human colonocytes Mutat. Res. 594 2006 162 171 (Pubitemid 43170996)
38. M.P. Richards, M.A. Dettmann, and E.W. Grunwald Pro-oxidative characteristics of trout hemoglobin and myoglobin: a role for released heme in oxidation of lipids J. Agric. Food Chem. 53 2005 10231 10238 (Pubitemid 43081240)
39. E. Park, M. Glei, Y. Knöbel, and B.L. Pool-Zobel Blood mononucleocytes are sensitive to the DNA damaging effects of iron overload-in vitro and ex vivo results with human and rat cells Mutat. Res. 619 2007 59 67 (Pubitemid 46602442)
40. Y. Knöbel, A. Weise, M. Glei, M. Sendt, W.U. Claussen, and B.L. Pool-Zobel Ferric iron is genotoxic in non-transformed and preneoplastic human colon cells Food Chem. Toxicol. 45 2007 804 811 (Pubitemid 46452878)
41. A. Pierre, S. Freeman, M.R. Tache, 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 (Pubitemid 39315277)
42. E.K. Lund, S.G. Wharf, S.J. Fairweather-Tait, and I.T. Johnson Oral ferrous sulfate supplements increase the free radical-generating capacity of feces from healthy volunteers Am. J. Clin. Nutr. 69 1999 250 255 (Pubitemid 29065547)
43. P.S. Oates, and A.R. West Heme in intestinal epithelial cell turnover, differentiation, detoxification, inflammation, carcinogenesis, absorption and motility World J. Gastroenterol. 12 2006 4281 4295 (Pubitemid 44194519)
44. F. Pierre, S. Tache, 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 (Pubitemid 37304675)
45. M.J. Govers, D.S. Termont, J.A. Lapre, J.H. Kleibeuker, R.J. Vonk, and R. Van der Meer Calcium in milk products precipitates intestinal fatty acids and secondary bile acids and thus inhibits colonic cytotoxicity in humans Cancer Res. 56 1996 3270 3275 (Pubitemid 26242975)
46. g)] production in the reaction of linoleic acid hydroperoxide with peroxynitrite J. Am. Chem. Soc. 125 2003 4510 4517 (Pubitemid 36418698)
47. H. Wang, and J.A. Joseph Quantifying cellular oxidative stress by dichlorofluorescein assay using microplate reader Free Radic. Biol. Med. 27 1999 612 616 (Pubitemid 29408648)
48. V.L. Tatum, C. Ghangchit, and C.K. Chow Measurement of malonaldehyde by high performance liquid chromatography with fluorescence detection Lipids 25 1990 226 229 (Pubitemid 20135055)
49. R. Dringen, and B. Hamprecht Involvement of glutathione peroxidase and catalase in the disposal of exogenous hydrogen peroxide by cultured astroglial cells Brain Res. 759 1997 67 75 (Pubitemid 27286345)
50. C.A. Gay, and J.M. Gebicki Measurement of protein and lipid hydroperoxides in biological systems by the ferric-xylenol orange method Anal. Biochem. 315 2003 29 35 (Pubitemid 36379103)
51. M. Uhl, C. Helma, and S. Knasmuüller Single-cell gel electrophoresis assay with human-derived hepatoma (HepG2) cells Mutat. Res. 441 1999 215 224 (Pubitemid 29225093)
52. L. Wang, K. Hirayasu, M. Ishizawa, and Y. Kobayashi Purification of genomic DNA from human whole blood by isopropanol-fractionation with concentrated NaI and SDS Nucleic Acids Res. 22 1994 1774 1775 (Pubitemid 24155844)
53. A.P. Loureiro, P. Di Mascio, O.F. Gomes, and M.H.G. Medeiros Trans, trans-2,4-decadienal-induced 1, N(2)-etheno-2′-deoxyguanosine adduct formation Chem. Res. Toxicol. 13 2000 601 609 (Pubitemid 30491121)
54. C.C.M. Garcia, F.P. Freitas, P. Di Mascio, and M.H.G. Medeiros Ultra-sensitive simultaneous quantification of 1, N2-etheno-2′- deoxyguanosine and 1, N2-propano-2′-deoxyguanosine in DNA by on-line liquid chromatography-electrospray tandem mass spectrometry assay Chem. Res. Toxicol. 23 2010 1245 1255
55. M. Lipkin, B. Reddy, H. Newmark, and S.A. Lamprecht Dietary factors in human colorectal cancer Annu. Rev. Nutr. 19 1999 545 586 (Pubitemid 29380616)
56. H.P. Misra, and I. Fridovich The generation of superoxide radical during the autoxidation of hemoglobin J. Biol. Chem. 247 1972 6960 6962
57. T. Kaneko, and S. Tahara Formation of 8-oxo-2′-deoxyguanosine in the DNA of human diploid fibroblasts by treatment with linoleic acid hydroperoxide and ferric ion Lipids 35 2000 961 965
58. J.L. Sheridan, M. Wang, M. Tosetto, K. Sheahan, J. Hyland, D. Fennelly, D. O'Donoghue, H. Mulcahy, and J. O'Sullivan Nuclear oxidative damage correlates with poor survival in colorectal cancer Br. J. Cancer 100 2009 381 388
59. P. Lim, G.E. Wuenschell, V. Holland, D.H. Lee, G.P. Pfeifer, H. Rodriguez, and J. Termini Peroxyl radical mediated oxidative DNA base damage: implications for lipid peroxidation induced mutagenesis Biochemistry 43 2004 15339 15348 (Pubitemid 39647460)
60. G.D. Ouédraogo, and R.W. Redmond Secondary reactive oxygen species extend the range of photosensitization effects in cells: DNA damage produced via initial membrane photosensitization Photochem. Photobiol. 77 2003 192 203
61. A.W. Girotti Translocation as a means of disseminating lipid hydroperoxide-induced oxidative damage and effector action Free Radic. Biol. Med. 44 2008 956 968
62. S. Miyamoto, G.R. Martinez, D. Rettori, O. Augusto, M.H.G. Medeiros, and P. Di Mascio Linoleic acid hydroperoxide reacts with hypochlorous acid, generating peroxyl radical intermediates and singlet molecular oxygen Proc. Natl Acad. Sci. U. S. A. 103 2006 293 298 (Pubitemid 43122394)
63. J.L. Ravanat, P. Di Mascio, G.R. Martinez, M.H.G. Medeiros, and J. Cadet Singlet oxygen induces oxidation of cellular DNA J. Biol. Chem. 275 2000 40601 40604 (Pubitemid 32064699)
64. J.L. Ravanat, S. Sauvaigo, S. Caillat, G.R. Martinez, M.H.G. Medeiros, P. Di Mascio, A. Favier, and J. Cadet Singlet oxygen-mediated damage to cellular DNA determined by the comet assay associated with DNA repair enzymes Biol. Chem. 385 2004 17 20 (Pubitemid 38240290)
65. J. Cadet, and P. Di Mascio Peroxides in biological systems Z. Rappoport, The Chemistry of Peroxides vol. 2 2006 Wiley New York 915 999
66. Y. Kawai, S. Takeda, and J. Terao Lipidomic analysis for lipid peroxidation-derived aldehydes using gas chromatography-mass spectrometry Chem. Res. Toxicol. 20 2007 99 107 (Pubitemid 46220160)
67. U. Nair, H. Bartsch, and J. Nair Lipid peroxidation-induced DNA damage in cancer-prone inflammatory diseases: a review of published adduct types and levels in humans Free Radic. Biol. Med. 43 2007 1109 1120 (Pubitemid 47374441)
68. A.R. West, and P.S. Oates Mechanisms of heme iron absorption: current questions and controversies World J. Gastroenterol. 14 2008 4101 4110
69. S.B. Raffin, C.H. Woo, K.T. Roost, D.C. Price, and R. Schmid Intestinal absorption of hemoglobin iron-heme cleavage by mucosal heme oxygenase J. Clin. Invest. 54 1974 1344 1352
70. A.T. McKie, D. Barrow, G.O. Latunde-Dada, A. Rolfs, G. Sager, E. Mudaly, M. Mudaly, C. Richardson, D. Barlow, A. Bromford, T.J. Peters, K.B. Raja, S. Shirali, M.A. Hediger, F. Farzaneh, and R.J. Simpson An iron-regulated ferric reductase associated with the absorption of dietary iron Science 291 2001 1755 1759 (Pubitemid 32198974)
71. T. Kriska, V.V. Levchenko, W. Korytowski, B.P. Atshaves, F. Schroeder, and A.W. Girotti Intracellular dissemination of peroxidative stress: internalization, transport, and lethal targeting of a cholesterol hydroperoxide species by sterol carrier protein-2-overexpressing hepatoma cells J. Biol. Chem. 281 2006 23643 23651 (Pubitemid 44274139)
72. C.U. Carlsen, J.K.S. Moller, and L.H. Skibsted Heme-iron in lipid oxidation Coord. Chem. Rev. 249 2005 485 498 (Pubitemid 40093753)
73. A. Wright, C.L. Hawkins, and M.J. Davies Photo-oxidation of cells generates long-lived intracellular protein peroxides Free Radic. Biol. Med. 34 2003 637 647 (Pubitemid 36288530)
74. A. Furukawa, Y. Hiraku, S. Oikawa, C. Luxford, M.J. Davies, and S. Kawanishi Guanine-specific DNA damage induced by gamma-irradiated histone Biochem. J. 388 2005 813 818 (Pubitemid 40941567)
75. C. Luxford, R.T. Dean, and M.J. Davies Induction of DNA damage by oxidised amino acids and proteins Biogerontology 3 2002 95 102 (Pubitemid 34284985)
76. P.D. MacLean, E.C. Drake, L. Ross, and C. Barclay Billirubin as an antioxidant in micelles and lipid bilayers: its contribution to the total antioxidant capacity of human blood plasma Free Radic. Biol. Med. 43 2007 600 609 (Pubitemid 47058238)