Natural chlorophyll inhibits aflatoxin B1-induced multi-organ carcinogenesis in the rat

Carcinogenesis

Volumn 28, Issue 6, 2007, Pages 1294-1302

  Simonich, Michael T ^a   Egner, Patricia A ^c   Roebuck, Bill D ^d   Orner, Gayle A ^a   Jubert, Carole ^a   Pereira, Cliff ^b   Groopman, John D ^c   Kensler, Thomas W ^c   Dashwood, Roderick H ^a,b   Williams, David E ^a,b   Bailey, George S ^a,b  

^a OREGON STATE UNIVERSITY   (United States)

^b OREGON STATE UNIVERSITY   (United States)

^c JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

^d DARTMOUTH MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AFLATOXIN B1; ALBUMIN; CARCINOGEN; CHLOROPHYLL; DNA; GLUTATHIONE TRANSFERASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE (PHOSPHATE) DEHYDROGENASE (QUINONE);

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER PREVENTION; COLON CANCER; COLON CARCINOGENESIS; COMPLEX FORMATION; CONTROLLED STUDY; DRUG MECHANISM; DRUG STRUCTURE; ENZYME INDUCTION; FECES; FLUORESCENCE; IN VIVO STUDY; LIVER CANCER; LIVER CARCINOGENESIS; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; STOICHIOMETRY;

AFLATOXIN B1; ANIMALS; ANTICARCINOGENIC AGENTS; CARCINOGENS; CHLOROPHYLL; COLONIC NEOPLASMS; LIVER NEOPLASMS; MALE; RANDOM ALLOCATION; RATS; RATS, INBRED F344;

EID: 34447329571     PISSN: 01433334     EISSN: 14602180     Source Type: Journal    
DOI: 10.1093/carcin/bgm027     Document Type: Article

References (51)

1. Jackson,P.E. et al. (1999) Aflatoxin and liver cancer. Baillieres Best Pract. Res. Clin. Gastroenterol., 13, 545-555.
2. Kensler,T.W. et al. (2004) Chemoprevention of hepatocellular carcinoma in aflatoxin endemic areas. Gastroenterology, 127, S310-S318.
3. Kensler,T.W. et al. (1986) Modulation of aflatoxin metabolism, aflatoxin-N7-guanine formation, and hepatic tumorigenesis in rats fed ethoxyquin: Role of induction of glutathione S-transferases. Cancer Res., 46, 3924-3931.
4. Roebuck,B.D. et al. (1991) Protection against aflatoxin B1-induced hepatocarcinogenesis in F344 rats by 5-(2-pyrazinyl)-4-methyl-1,2-dithiole-3-thione (oltipraz): Predictive role for short-term molecular dosimetry. Cancer Res., 51, 5501-5506.
5. Groopman,J.D. et al. (1992) Molecular dosimetry of urinary aflatoxin-N7-guanine and serum aflatoxin-albumin adducts predicts chemoprotection by 1,2-dithiole-3-thione in rats. Carcinogenesis, 13, 101-106.
6. Bolton,M.G. et al. (1993) Transient intervention with oltipraz protects against aflatoxin-induced hepatic tumorigenesis. Cancer Res. 53, 3499-3504.
7. Kensler,T.W. et al. (1998) Use of aflatoxin adducts as intermediate end-points to assess the efficacy of chemopreventive interventions in animals and man. Mutat. Res., 402, 165-172.
8. Yates,M.S. et al. (2006) Potent protection against aflatoxin-induced tumorigenesis through induction of Nrf2-regulated pathways by the triterpenoid 1-[2-cyano-3-,12-dioxooleana-1,9(11)-dien-28-oy1]imidazole. Cancer Res., 66, 2488-2494.
9. Breinholt,V. et al. (1995) Dietary chlorophyllin is a potent inhibitor of aflatoxin B1 hepatocarcinogenesis in rainbow trout. Cancer Res., 55, 57-62.
10. Egner,P.A. et al. (2001) Chlorophyllin intervention reduces aflatoxin-DNA adducts in individuals at high risk for liver cancer. Proc. Natl Acad. Sci. USA, 98, 14601-14606.
11. Egner,P.A. et al. (2003) Chemoprevention with chlorophyllin in individuals exposed to dietary aflatoxin. Mutat. Res., 523-524 209-216.
12. Qian,G.S. et al. (1994) A follow-up study of urinary markers of aflatoxin exposure and liver cancer risk in Shanghai, People's Republic of China. Cancer Epidemiol. Biomarkers Prev., 3, 3-10.
13. Breinholt,V. et al. (1995) Mechanisms of chlorophyllin anticarcinogenesis against aflatoxin B1: Complex formation with the carcinogen. Chem. Res. Toxicol., 8, 506-514.
14. Dashwood,R. et al. (1996) Study of the forces of stabilizing complexes between chlorophylls and heterocyclic amine mutagens. Environ. Mol. Mutagen., 27, 211-218.
15. Reddy,A.P. et al. (1999) Inhibition of dibenzo[a,1]pyrene-induced multi-organ carcinogenesis by dietary chlorophyllin in rainbow trout. Carcinogenesis, 20, 1919-1926.
16. Dashwood,R. et al. (1998) Chemopreventive properties of chlorophylls towards aflatoxin B1: A review of the antimutagenicity and anticarcinogenicity data in rainbow trout. Mutat. Res., 399, 245-253.
17. Dashwood,R.H. (1997) The importance of using pure chemicals in (anti) mutagenicity studies: Chlorophyllin as a case in point. Mutat. Res. 381, 283-286.
18. Nelson,R.L. (1992) Chlorophyllin, an antimutagen, acts as a tumor promoter in the rat-dimethylhydrazine colon carcinogenesis model. Anticancer Res., 12, 737-739.
19. Xu,M. et al. (2001) Post-initiation effects of chlorophyllin and indole-3-carbinol in rats given 1,2-dimethylhydrazine or 2-amino-3-methyl-imidazo. Carcinogenesis, 22, 309-314.
20. Blum,C.A. et al. (2003) Promotion versus suppression of rat colon carcinogenesis by chlorophyllin and chlorophyll: Modulation of apoptosis, cell proliferation, and beta-catenin/Tcf signaling. Mutat. Res., 523-524, 217-223.
21. Negishi,T. et al. (1997) Antigenotoxic activity of natural chlorophylls. Mutat. Res., 376, 97-100.
22. Fahey,J.W. et al. (2005) chlorophyll, chlorophyllin and related tetrapyrroles are significant inducers of mammalian phase 2 cytoprotective genes. Carcinogenesis, 26, 1247-1255.
23. Harttig,U. et al. (1998) Chemoprotection by natural chlorophylls in vivo: Inhibition of dibenzo[a,1]pyrene-DNA adducts in rainbow trout liver. Carcinogenesis, 19, 1323-1326.
24. de Vogel,J. et al. (2005) Green vegetables, red meat and colon cancer: Chlorophyll prevents the cytotoxic and hyperproliferative effects of haem in rat colon. Carcinogenesis, 26, 387-393.
25. Sesink,A.L. et al. (1999) Red meat and colon cancer: The cytotoxic and hyperproliferative effects of dietary heme. Cancer Res., 59 5704-5709.
26. Wild,C.P. et al. (1990) Evaluation of methods for quantitation of aflatoxin-albumin adducts and their application to human exposure assessment. Cancer Res., 50, 245-251.
27. Groopman,J.D. et al. (1992) Molecular dosimetry of urinary aflatoxin-DNA adducts in people living in Guangxi Autonomous Region, People's Republic of China. Cancer Res., 52, 45-52.
28. Wang,J.S. et al. (1999) Protective alterations in phase 1 and 2 metabolism of aflatoxin B1 by oltipraz in residents of Qidong, People's Republic of China. J. Natl Cancer Inst., 91, 347-354.
29. Groopman,J.D. et al. (1992) Molecular dosimetry in rat urine of aflatoxin-N7-guanine and other aflatoxin metabolites by multiple monoclonal antibody affinity chromatography and immunoaffinity/high performance liquid chromatography. Cancer Res., 52, 267-274.
30. Walton,M. et al. (2001) Liquid chromatography electrospray-mass spectrometry of urinary aflatoxin biomarkers: Characterization and application to dosimetry and chemoprevention in rats. Chem. Res. Toxicol., 14, 919-926.
31. Hayashi,J. et al. (1999) Mechanisms of chlorophyllin anticarcinogenesis: Dose-responsive inhibition of aflatoxin uptake and biodistribution following oral co-administration in rainbow trout. Toxicol. Appl. Pharmacol., 158, 132-140.
32. Prochaska,H.J. et al. (1988) Direct measurement of NAD(P)H:qUinone reductase from cells cultured in microtiter wells: A screening assay for anti-carcinogenic enzyme inducers. Anal. Biochem., 169, 328-336.
33. Sato,Y. et al. (1986) The AMeX method. A simplified technique of tissue processing and paraffin embedding with improved preservation of antigens for immunostaining. Am. J. Pathol., 125, 431-435.
34. Maxuitenko,Y.Y. et al. (1996) Protection against aflatoxin B1-induced hepatic toxicity as short-term screen of cancer chemopreventive dithiolethiones. Fundam. Appl. Toxicol., 32, 250-259.
35. Pugh,T.D. et al. (1983) Reliable stereological method for estimating the number of microscopic hepatocellular foci from their transections. Cancer Res., 43, 1261-1268.
36. Orner,G.A. et al. (2006) Post-initiation chlorophyllin exposure does not modulate aflatoxin-induced foci in the liver and colon of rats. J. Carcinog., 5, 6.
37. Tachino,N. et al. (1995) Evidence for ras gene mutation in 2-amino-3-methylimidazo[4,5-f]quinoline-induced colonic aberrant crypts in the rat. Mol. Carcinog., 12, 187-192.
38. Croy,R.G. et al. (1981) Temporal patterns of covalent DNA adducts in rat liver after single and multiple doses of aflatoxin B1. Cancer Res., 41, 197-203.
39. Liu,Y.L. et al. (1988) Protection by 5-(2-pyrazinyl)-4-methyl-1,2-dithiol-3-thione (oltipraz) against the hepatotoxicity of aflatoxin B1 in the rat. Toxicol. Appl. Pharmacol. 93, 442-451.
40. Wild,C.P. et al. (1986) Aflatoxin B1 binding to plasma albumin and liver DNA upon chronic administration to rats. Carcinogenesis, 7, 853-858.
41. Gorelick,N.J. (1990) Risk assessment for aflatoxin: I. Metabolism of aflatoxin B1 by different species. Risk Anal., 10, 539-559.
42. Bennett,R.A. et al. (1981) Excretion of an aflatoxin-guanine adduct in the urine of aflatoxin B1-treated rats. Cancer Res., 41, 650-654.
43. Groopman,J.D. et al. (1992) Molecular dosimetry of aflatoxin DNA adducts in humans and experimental rat models. Prog. Clin. Biol. Res. 374, 139-155.
44. Talalay,P. et al. (2003) Importance of phase 2 gene regulation in protection against electrophile and reactive oxygen toxicity and carcinogenesis. Adv. Enzyme Regul., 43, 121-134.
45. Kensler,T.W. et al. (2004) Inducers of enzymes that protect against carcinogens and oxidants. In Kelloff,G.J.,Hawk,E.T. and Sigman,C.C. (eds) Cancer Chemoprevention, Vol. 1. Promising Cancer Chemoprevention Agents. Humana Press Totowa, NJ, pp. 3-20.
46. Kensler,T.W. et al. (1992) Potent inhibition of aflatoxin-induced hepatic tumorigenesis by the monofunctional enzyme inducer 1,2-dithiole-3-thione. Carcinogenesis, 13, 95-100.
47. Dashwood,R.H. et al. (1991) Chemopreventive properties of chlorophyllin: Inhibition of aflatoxin B1 (AFB1)-DNA binding in vivo and anti-mutagenic activity against AFB1 and two heterocyclic amines in the Salmonella mutagenicity assay. Carcinogenesis, 12, 939-942.
48. Breinholt,V. et al. (1999) Chlorophyllin chemoprevention in trout initiated by aflatoxin B(1) bath treatment: An evaluation of reduced bioavailability vs. target organ protective mechanisms. Toxicol. Appl. Pharmacol., 158, 141-151.
49. Egner,P.A. et al. (2000) Identification and characterization of chlorin e(4) ethyl ester in sera of individuals participating in the chlorophyllin chemoprevention trial. Chem. Res. Toxicol., 13 900-906.
50. Dingley,K.H. et al. (2003) Effect of dietary constituents with chemopreventive potential on adduct formation of a low dose of the heterocyclic amines PhIP and IQ and phase II hepatic enzymes. Nutr. Cancer, 46, 212-221.
51. de Vogel,J. et al. (2005) Natural chlorophyll but not chlorophyllin prevents heme-induced cytotoxic and hyperproliferative effects in rat colon. J. Nutr., 135, 1995-2000.