Heme induces DNA damage and hyperproliferation of colonic epithelial cells via hydrogen peroxide produced by heme oxygenase: A possible mechanism of hemeinduced colon cancer

Molecular Nutrition and Food Research

Volumn 54, Issue 8, 2010, Pages 1182-1191

  Ishikawa, Shin Ichi ^a   Tamaki, Satoru ^a   Ohata, Motoko ^a   Arihara, Keizo ^a   Itoh, Makoto ^a  

^a KITASATO UNIVERSITY   (Japan)

Author keywords

Cell proliferation; Colon cancer; DNA damage; Heme oxygenase; Hydrogen peroxide

Indexed keywords

CATALASE; ENZYME INHIBITOR; HEME; HEME OXYGENASE; HYDROGEN PEROXIDE; IL8 PROTEIN, HUMAN; INTERLEUKIN 8; MESSENGER RNA; PROTOPORPHYRIN; PROTOPORPHYRIN ZINC;

ARTICLE; CELL PROLIFERATION; CELL STRAIN CACO 2; CELL SURVIVAL; CHEMICALLY INDUCED DISORDER; COLON TUMOR; DNA DAMAGE; DRUG ANTAGONISM; DRUG EFFECT; EPITHELIUM CELL; GENE EXPRESSION REGULATION; GENETICS; HUMAN; MEAT; METABOLISM; OSMOLARITY; OXIDATIVE STRESS; RISK FACTOR;

CACO-2 CELLS; CATALASE; CELL PROLIFERATION; CELL SURVIVAL; COLONIC NEOPLASMS; DNA DAMAGE; ENZYME INHIBITORS; EPITHELIAL CELLS; GENE EXPRESSION REGULATION, NEOPLASTIC; HEME; HEME OXYGENASE (DECYCLIZING); HUMANS; HYDROGEN PEROXIDE; INTERLEUKIN-8; MEAT; OSMOLAR CONCENTRATION; OXIDATIVE STRESS; PROTOPORPHYRINS; RISK FACTORS; RNA, MESSENGER;

ANIMALIA;

EID: 77955900385     PISSN: 16134125     EISSN: 16134133     Source Type: Journal    
DOI: 10.1002/mnfr.200900348     Document Type: Article

References (62)

1. Boyle, P., Levin, B. (Eds.), World Cancer Report 2008, IARC Publications, Lyon 2008.
2. Parkin, D. M., Bray, F., Ferlay, J., Pisani, P., Global cancer statistics, 2002. CA Cancer J. Clin. 2005, 55, 74-108.
3. Tomatis, L., Aitio, A., Day, N. E., Heseltine, E. et al. (Eds.), Cancer: Causes, Occurrence and Control. IARC Publications, Lyon 1990.
4. Norat, T., Lukanova, A., Ferrari, P., Riboli, E., Meat consumption and colorectal cancer risk: dose-response meta-analysis of epidemiological studies. Int. J. Cancer 2002, 98, 241-256.
5. Norat, T., Bingham, S., Ferrari, P., Meat, fish, and colorectal cancer risk: the European Prospective Investigation into cancer and nutrition. J. Natl. Cancer Inst. 2005, 97, 906-916.
6. Larsson, S. C., Wolk, A., Meat consumption and risk of colorectal cancer: a meta-analysis of prospective studies. Int. J. Cancer 2006, 119, 2657-2664.
7. Sesink, A. L., Termont, D. S., Kleibeuker, J. H., van der Meer, R., Red meat and colon cancer: the cytotoxic and hyperproliferative effects of dietary heme. Cancer Res. 1999, 59, 5704-5709.
8. Schwartz, S., Ellefson, M., Quantitative fecal recovery of ingested hemoglobin-heme in blood: comparisons by HemoQuant assay with ingested meat and fish. Gastroenterology 1985, 89, 19-26.
9. Glei, M., Klenow, S., Sauer, J., Wegewitz, U. et al., Hemoglobin and hemin induce DNA damage in human colon tumor cells HT29 clone 19A and in primary human colonocytes. Mutat. Res. 2006, 594, 162-171.
10. Knöbel, Y., Weise, A., Glei, M., Sendt, W. et al., Ferric iron is genotoxic in non-transformed and preneoplastic human colon cells. Food Chem. Toxicol. 2007, 45, 804-811.
11. Park, E., Glei, M., Knöbel, Y., Pool-Zobel, B. L., 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. 2007, 619, 59-67.
12. Benhar, M., Engelberg, D., Levitzki, A., ROS, stress-activated kinases and stress signaling in cancer. EMBO Rep. 2002, 3, 420-425.
13. Klaunig, J. E., Kamendulis, L. M., The role of oxidative stress in carcinogenesis. Annu. Rev. Pharmacol. Toxicol. 2004, 44, 239-267.
14. Franco, R., Schoneveld, O., Georgakilas, A. G., Panayiotidis, M. I., Oxidative stress, DNA methylation and carcinogenesis. Cancer Lett. 2008, 266, 6-11.
15. Burdon, R. H., Superoxide and hydrogen peroxide in relation to mammalian cell proliferation. Free Radic. Biol. Med. 1995, 18, 775-794.
16. Rhee, S. G., Redox signaling: hydrogen peroxide as intracellular messenger. Exp. Mol. Med. 1999, 31, 53-59.
17. Arnold, R. S., Shi, J., Murad, E., Whalen, A. M. et al., Hydrogen peroxide mediates the cell growth and transformation caused by the mitogenic oxidase Nox1. Proc. Natl. Acad. Sci. USA 2001, 98, 5550-5555.
18. Sesink, A. L., Termont, D. S., Kleibeuker, J. H., van der Meer, R., Red meat and colon cancer: dietary haem, but not fat, has cytotoxic and hyperproliferative effects on rat colonic epithelium. Carcinogenesis 2000, 21, 1909-1915.
19. de Vogel, J., van-Eck, W. B., Sesink, A. L., Jonker-Termont, D. S. et al., Dietary heme injures surface epithelium resulting in hyperproliferation, inhibition of apoptosis and crypt hyperplasia in rat colon. Carcinogenesis 2008, 29, 398-403.
20. Pierre, F., Taché, S., Petit, C. R., van der Meer, R. et al., Meat and cancer: haemoglobin and haemin in a low-calcium diet promote colorectal carcinogenesis at the aberrant crypt stage in rats. Carcinogenesis 2003, 24, 1683-1690.
21. Pierre, F., Freeman, A., Taché, S., van der Meer, R. et al., Beef meat and blood sausage promote the formation of azoxymethane-induced mucin-depleted foci and aberrant crypt foci in rat colons. J. Nutr. 2004, 134, 2711-2716.
22. Sesink, A. L., Termont, D. S., Kleibeuker, J. H., van der Meer, R., Red meat and colon cancer: dietary haem-induced colonic cytotoxicity and epithelial hyperproliferation are inhibited by calcium. Carcinogenesis 2001, 22, 1653-1659.
23. Nagababu, E., Rifkind, J. M., Heme degradation by reactive oxygen species. Antioxid. Redox Signal. 2004, 6, 967-978.
24. Kikuchi, G., Yoshida, T., Noguchi, M., Heme oxygenase and heme degradation. Biochem. Biophys. Res. Commun. 2005, 338, 558-567.
25. Noguchi, M., Yoshida, T., Kikuchi, G., A stoichiometric study of heme degradation catalyzed by the reconstituted heme oxygenase system with special consideration of the production of hydrogen peroxide during the reaction. J. Biochem. 1982, 93, 1027-1036.
26. Galbraith, R., Heme oxygenase: Who needs it? Proc. Soc. Exp. Biol. Med. 1999, 222, 299-305.
27. Henle, E. S., Han, Z., Tang, N., Rai, P. et al., Sequencespecific DNA cleavage by Fe2+-mediated Fenton reactions has possible biological implications. J. Biol. Chem. 1999, 274, 962-971.
28. Karin, M., Shaulian, E., AP-1: Linking hydrogen peroxide and oxidative stress to the control of cell proliferation and death. IUBMB Life 2001, 52, 17-24.
29. Noda, T., Iwakiri, R., Fujimoto, K., Aw, T. Y., Induction of mild intracellular redox inhibits proliferation of Caco-2 cells. FASEB J. 2001, 15, 2131-2139.
30. Yoshida, Y., Maruyama, M., Fujita, T., Arai, N. et al., Reactive oxygen intermediates stimulate interleukin-6 production in human bronchial epithelial cells. Am. J. Physiol. 1999, 276, L900-L908.
31. Haddad, J. J., Safieh-Garabedian, B., Saadé, N. E., Kanaan, S. A., Chemioxyexcitation (Δp O2/ROS)-dependent release of IL-1β, IL-6 and TNF-α: evidence of cytokines as oxygensensitive mediators in the alveolar epithelium. Cytokine 2001, 13, 138-147.
32. Yamamoto, K., Kushima, R., Kisaki, O., Fujiyama, Y. et al., Combined effect of hydrogen peroxide induced oxidative stress and IL-1 α on IL-8 production in Caco-2 cells (a human colon carcinoma cell line) and normal intestinal epithelial cells. Inflammation 2003, 27, 123-128.
33. Singh, N. P., McCoy, M. T., Tice, R. R., Schneider, E. L., A simple technique for quantitation of low levels of DNA damage in individual cells. Exp. Cell Res. 1988, 175, 184-191.
34. Aust, S. D., Chignell, C. F., Bray, T. M., Kalyanaraman, B. et al., Free radicals in toxicology. Toxicol. Appl. Pharmacol. 1993, 120, 168-178.
35. Simon, H. U., Haj-Yehia, A., Levi-Schaffer, F., Role of reactive oxygen species (ROS) in apoptosis induction. Apoptosis 2000, 5, 415-418.
36. Sundaresan, M., Yu, Z. X., Ferrans, V. J., Irani, K. et al., Requirement for generation of H2O2 for platelet-derived growth factor signal transduction. Science 1995, 270, 296-299.
37. Chowers, Y., Cahalon, L., Lahav, M., Schor, H. et al., Somatostatin through its specific receptor inhibits spontaneous and TNF-α- and bacteria-induced IL-8 and IL-1β secretion from intestinal epithelial cells. J. Immunol. 2000, 165, 2955-2961.
38. Lang, A., Lahav, M., Sakhnini, E., Barshack, I. et al., Allicin inhibits spontaneous and TNF-α-induced secretion of proinflammatory cytokines and chemokines from intestinal epithelial cells. Clin. Nutr. 2004, 23, 1199-1208.
39. Alzoghaibi, M. A., Walsh, S. W., Willey, A., Yager, D. R. et al., Linoleic acid induces interleukin-8 production by Crohn's human intestinal smooth muscle cells via arachidonic acid metabolites. Am. J. Physiol. Gastrointest. Liver Physiol. 2004, 286, G528-G537.
40. Son, D. O., Satsu, H., Shimizu, M., Histidine inhibits oxidative stress- and TNF-α-induced interleukin-8 secretion in intestinal epithelial cells. FEBS Lett. 2005, 579, 4671-4677.
41. Lee, D. H., Anderson, K. E., Harnack, L. J., Folsom, A. R. et al., Heme iron, zinc, alcohol consumption, and colon cancer: Iowa Women's Health Study. J. Natl. Cancer Inst. 2004, 96, 403-407.
42. Larsson, S. C., Adami, H. O., Giovannucci, E., Wolk, A. et al., Re: Heme iron, zinc, alcohol consumption, and risk of colon cancer. J. Natl. Cancer Inst. 2005, 97, 232-233.
43. Balder, H. F., Vogel, J., Jansen, M. C., Weijenberg, M. P. et al., Heme and chlorophyll intake and risk of colorectal cancer in the Netherlands cohort study. Cancer Epidemiol. Biomarkers Prev. 2006, 15, 717-725.
44. de Vogel, J., Jonker-Termont, D. S., Katan, M. B., van der Meer, R., Natural chlorophyll but not chlorophyllin prevents heme-induced cytotoxic and hyperproliferative effects in rat colon. J. Nutr. 2005, 135, 1995-2000.
45. Sawa, T., Akaike, T., Kida, K., Fukushima, Y. et al., Lipid peroxyl radicals from oxidized oils and heme-iron: implication of a high-fat diet in colon carcinogenesis. Cancer Epidemiol. Biomarkers Prev. 1998, 7, 1007-1012.
46. Minetti, M., Mallozzi, C., Di Stasi, A. M., Pietraforte, D., Bilirubin is an effective antioxidant of peroxynitrite-mediated protein oxidation in human blood plasma. Arch. Biochem. Biophys. 1998, 352, 165-174.
47. Petrache, I., Otterbein, L. E., Alam, J., Wiegand, G. W. et al., Heme oxygenase-1 inhibits TNF-α-induced apoptosis in cultured fibroblasts. Am. J. Physiol. Lung Cell Mol. Physiol. 2000, 278, L312-L319.
48. Otterbein, L. E., Mantell, L. L., Choi, A. M., Carbon monoxide provides protection against hyperoxic lung injury. Am. J. Physiol. 1999, 276, L688-L694.
49. Oates, P. S., West, A. R., Heme in intestinal epithelial cell turnover, differentiation, detoxification, inflammation, carcinogenesis, absorption and motility. World J. Gastroenterol. 2006, 12, 4281-4295.
50. Ryter, S. W., Tyrrell, R. M., The heme synthesis and degradation pathways: role in oxidant sensitivity. Heme oxygenase has both pro- and antioxidant properties. Free Radic. Biol. Med. 2000, 28, 289-309.
51. Uc, A., Britigan, B. E., Does heme oxygenase-1 have a role in Caco-2 cell cycle progression? Exp. Biol. Med. (Maywood) 2003, 228, 590-595.
52. Ferris, C. D., Jaffrey, S. R., Sawa, A., Takahashi, M. et al., Haem oxygenase-1 prevents cell death by regulating cellular iron. Nat. Cell Biol. 1999, 1, 152-157.
53. Paul, G., Bataille, F., Obermeier, F., Bock, J. et al., Analysis of intestinal haem-oxygenase-1 (HO-1) in clinical and experimental colitis. Clin. Exp. Immunol. 2005, 140, 547-555.
54. Goodman, A. I., Choudhury, M., da Silva, J. L., Schwartzman, M. L. et al., Overexpression of the heme oxygenase gene in renal cell carcinoma. Proc. Soc. Exp. Biol. Med. 1997, 214, 54-61.
55. Doi, K., Akaike, T., Fujii, S., Tanaka, S. et al., Induction of haem oxygenase-1 nitric oxide and ischaemia in experimental solid tumours and implications for tumour growth. Br. J. Cancer 1999, 80, 1945-1954.
56. Fang, J., Sawa, T., Akaike, T., Akuta, T. et al., In vivo antitumor activity of pegylated zinc protoporphyrin: targeted inhibition of heme oxygenase in solid tumor. Cancer Res. 2003, 63, 3567-3574.
57. Tanaka, S., Akaike, T., Fang, J., Beppu, T. et al., Antiapoptotic effect of haem oxygenase-1 induced by nitric oxide in experimental solid tumour. Br. J. Cancer 2003, 88, 902-909.
58. Schröder, E., Eaton, P., Hydrogen peroxide as an endogenous mediator and exogenous tool in cardiovascular research: issues and considerations. Curr. Opin. Pharmacol. 2008, 8, 153-159.
59. Burdon, R. H., Gill, V., Rice-Evans, C., Oxidative stress and tumour cell proliferation. Free Radic. Res. Commun. 1990, 11, 65-76.
60. Gong, X., Li, Q., Xu, K., Liu, X. et al., A new route for simple and rapid determination of hydrogen peroxide in RAW264.7 macrophages by microchip electrophoresis. Electrophoresis 2009, 30, 1983-1990.
61. Morcillo, E. J., Estrela, J., Cortijo, J., Oxidative stress and pulmonary inflammation: pharmacological intervention with antioxidants. Pharmacol. Res. 1999, 40, 393-404.
62. Chang, L., Karin, M., Mammalian MAP kinase signalling cascades. Nature 2001, 410, 37-40.