Cancer chemoprevention by dietary chlorophylls: A 12,000-animal dose-dose matrix biomarker and tumor study

Food and Chemical Toxicology

Volumn 50, Issue 2, 2012, Pages 341-352

  McQuistan, Tammie J ^a   Simonich, Michael T ^b   Pratt, M Margaret ^b   Pereira, Cliff B ^b   Hendricks, Jerry D ^b   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)

Author keywords

Chemoprevention; Chlorophyll; Dibenzo(def,p)chrysene; Liver cancer; Stomach cancer; Tumor incidence

Indexed keywords

CHLOROPHYLL; CHRYSENE DERIVATIVE; DIBENZO[DEF,P]CHRYSENE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER PREVENTION; CARCINOGEN DNA INTERACTION; CONCENTRATION RESPONSE; CONTROLLED STUDY; DIETARY INTAKE; DNA ADDUCT; GENE CONTROL; GENE EXPRESSION REGULATION; LIVER TUMOR; NONHUMAN; RAINBOW TROUT; STOMACH TUMOR; VEGETABLE;

ANIMAL FEED; ANIMALS; BENZOPYRENES; CHLOROPHYLL; DIET; DOSE-RESPONSE RELATIONSHIP, DRUG; FISH DISEASES; GENE EXPRESSION REGULATION; NEOPLASMS; ONCORHYNCHUS MYKISS;

ANIMALIA; ONCORHYNCHUS MYKISS; RODENTIA; SALMONIDAE;

EID: 84855286284     PISSN: 02786915     EISSN: 18736351     Source Type: Journal    
DOI: 10.1016/j.fct.2011.10.065     Document Type: Article

References (50)

1. Aggarwal B.B., Shishodia S. Molecular targets of dietary agents for prevention and therapy of cancer. Biochem. Pharmacol. 2006, 71:1397-1421.
2. Bailey G.S., Reddy A.P., Pereira C.B., Harttig U., Baird W., Spitsbergen J.M., Hendricks J.D., Orner G.A., Williams D.E., Swenberg J.A. Nonlinear cancer response at ultralow dose: a 40800-animal ED(001) tumor and biomarker study. Chem. Res. Toxicol. 2009, 22:1264-1276.
3. Baird W.M., Hooven L.A., Mahadevan B. Carcinogenic polycyclic aromatic hydrocarbon-DNA adducts and mechanism of action. Environ. Mol. Mutagen. 2005, 45:106-114.
4. Barrett J.R. Cancer. Plants provide prevention. Environ. Health Perspect. 2002, 110:A180.
5. Benninghoff A.D., Williams D.E. Identification of a transcriptional fingerprint of estrogen exposure in rainbow trout liver. Toxicol. Sci. 2008, 101:65-80.
6. Breinholt V., Schimerlik M., Dashwood R., Bailey G. Mechanisms of chlorophyllin anticarcinogenesis against aflatoxin B1: complex formation with the carcinogen. Chem. Res. Toxicol. 1995, 8:506-514.
7. Busby W.F., Smith H., Crespi C.L., Penman B.W. Mutagenicity of benzo[a]pyrene and dibenzopyrenes in the Salmonella typhimurium TM677 and the MCL-5 human cell forward mutation assays. Mutat. Res. 1995, 342:9-16.
8. Cavalieri E.L., Higginbotham S., RamaKrishna N.V., Devanesan P.D., Todorovic R., Rogan E.G., Salmasi S. Comparative dose-response tumorigenicity studies of dibenzo[alpha,l]pyrene versus 7,12-dimethylbenz[alpha]anthracene, benzo[alpha]pyrene and two dibenzo[alpha,l]pyrene dihydrodiols in mouse skin and rat mammary gland. Carcinogenesis 1991, 12:1939-1944.
9. Cavalieri E.L., Rogan E.G., Higginbotham S., Cremonesi P., Salmasi S. Tumor-initiating activity in mouse skin and carcinogenicity in rat mammary gland of dibenzo[a]pyrenes: the very potent environmental carcinogen dibenzo[a,l]pyrene. J. Cancer Res. Clin. Oncol. 1989, 115:67-72.
10. Dashwood R., Negishi T., Hayatsu H., Breinholt V., Hendricks J., Bailey G. Chemopreventive properties of chlorophylls towards aflatoxin B1: a review of the antimutagenicity and anticarcinogenicity data in rainbow trout. Mutat. Res. 1998, 399:245-253.
11. Dashwood R., Yamane S., Larsen R. Study of the forces of stabilizing complexes between chlorophylls and heterocyclic amine mutagens. Environ. Mol. Mutagen. 1996, 27:211-218.
12. Dashwood R.H., Arbogast D.N., Fong A.T., Pereira C., Hendricks J.D., Bailey G.S. Quantitative inter-relationships between aflatoxin B1 carcinogen dose, indole-3-carbinol anti-carcinogen dose, target organ DNA adduction and final tumor response. Carcinogenesis 1989, 10:175-181.
13. Deraat W.K., Kooijman S.A.L.M., Gielen J.W.J. Concentrations of polycyclic-hydrocarbons in airborne particles in the Netherlands and their correlation with mutagenicity. Sci. Total Environ. 1987, 66:95-114.
14. Durant J.L., Lafleur A.L., Busby W.F., Donhoffner L.L., Penman B.W., Crespi C.L. Mutagenicity of C24H14 PAH in human cells expressing CYP1A1. Mutat. Res. 1999, 446:1-14.
15. Egner P.A., Munoz A., Kensler T.W. Chemoprevention with chlorophyllin in individuals exposed to dietary aflatoxin. Mutat. Res. 2003, 523-524:209-216.
16. Egner P.A., Wang J.B., Zhu Y.R., Zhang B.C., Wu Y., Zhang Q.N., Qian G.S., Kuang S.Y., Gange S.J., Jacobson L.P., Helzlsouer K.J., Bailey G.S., Groopman J.D., Kensler T.W. Chlorophyllin intervention reduces aflatoxin-DNA adducts in individuals at high risk for liver cancer. Proc. Natl. Acad. Sci. USA 2001, 98:14601-14606.
17. Fahey J.W., Stephenson K.K., Dinkova-Kostova A.T., Egner P.A., Kensler T.W., Talalay P. Chlorophyll, chlorophyllin and related tetrapyrroles are significant inducers of mammalian phase 2 cytoprotective genes. Carcinogenesis 2005, 26:1247-1255.
18. Guyton K.Z., Kensler T.W. Prevention of liver cancer. Curr. Oncol. Rep. 2002, 4:464-470.
19. Harttig U., Bailey G.S. Chemoprotection by natural chlorophylls in vivo: inhibition of dibenzo[a,l]pyrene-DNA adducts in rainbow trout liver. Carcinogenesis 1998, 19:1323-1326.
20. Hayashi T., Schimerlik M., Bailey G. Mechanisms of chlorophyllin anticarcinogenesis: dose-responsive inhibition of aflatoxin uptake and biodistribution following oral co-administration in rainbow trout. Toxicol. Appl. Pharmacol. 1999, 158:132-140.
21. Hendricks J.D., Meyers T.R., Shelton D.W. Histological progression of hepatic neoplasia in rainbow trout (Salmo gairdneri). Natl. Cancer Inst. Monogr. 1984, 65:321-336.
22. Hendricks J.D., Shelton D.W., Loveland P.M., Pereira C.B., Bailey G.S. Carcinogenicity of dietary dimethylnitrosomorpholine, N-methyl-N'-nitro-N-nitrosoguanidine, and dibromoethane in rainbow trout. Toxicol. Pathol. 1995, 23:447-457.
23. Higginbotham S., RamaKrishna N.V., Johansson S.L., Rogan E.G., Cavalieri E.L. Tumor-initiating activity and carcinogenicity of dibenzo[a,l]pyrene versus 7,12-dimethylbenz[a]anthracene and benzo[a]pyrene at low doses in mouse skin. Carcinogenesis 1993, 14:875-878.
24. Hirose M., Nishikawa A., Shibutani M., Imai T., Shirai T. Chemoprevention of heterocyclic amine-induced mammary carcinogenesis in rats. Environ. Mol. Mutagen. 2002, 39:271-278.
25. Hoffmann D., Hoffmann I. Tobacco smoke components. Beitr. Tabakforsch. 1998, 18:49-52.
26. Jacobson L.P., Zhang B.C., Zhu Y.R., Wang J.B., Wu Y., Zhang Q.N., Yu L.Y., Qian G.S., Kuang S.Y., Li Y.F., Fang X., Zarba A., Chen B., Enger C., Davidson N.E., Gorman M.B., Gordon G.B., Prochaska H.J., Egner P.A., Groopman J.D., Munoz A., Helzlsouer K.J., Kensler T.W. Oltipraz chemoprevention trial in Qidong, People's Republic of China: study design and clinical outcomes. Cancer Epidemiol. Biomarkers Prev. 1997, 6:257-265.
27. Jubert C., Bailey G. Isolation of chlorophylls a and b from spinach by counter-current chromatography. J. Chromatogr. A 2007, 1140:95-100.
28. Jubert C., Mata J., Bench G., Dashwood R., Pereira C., Tracewell W., Turteltaub K., Williams D., Bailey G. Effects of chlorophyll and chlorophyllin on low-dose aflatoxin B(1) pharmacokinetics in human volunteers. Cancer Prev. Res. (Phila Pa) 2009, 2:1015-1022.
29. Kelloff G.J., Lippman S.M., Dannenberg A.J., Sigman C.C., Pearce H.L., Reid B.J., Szabo E., Jordan V.C., Spitz M.R., Mills G.B., Papadimitrakopoulou V.A., Lotan R., Aggarwal B.B., Bresalier R.S., Kim J., Arun B., Lu K.H., Thomas M.E., Rhodes H.E., Brewer M.A., Follen M., Shin D.M., Parnes H.L., Siegfried J.M., Evans A.A., Blot W.J., Chow W.H., Blount P.L., Maley C.C., Wang K.K., Lam S., Lee J.J., Dubinett S.M., Engstrom P.F., Meyskens F.L., O'Shaughnessy J., Hawk E.T., Levin B., Nelson W.G., Hong W.K. Progress in chemoprevention drug development: the promise of molecular biomarkers for prevention of intraepithelial neoplasia and cancer - a plan to move forward. Clin. Cancer Res. 2006, 12:3661-3697.
30. Kensler T.W.a.T.P. Inducers of enzymes that protect against carcinogens and oxidants. Cancer Chemoprevention, Vol 1: Promising Cancer Chemoprevention Agents 2004, 3-20. Humana Press Inc., Totowa, NJ. G.J. Kelloff, E.T. Hawk, C.C. Sigman (Eds.).
31. Kozin I.S., Gooijer C., Velthorst N.H. Direct determination of dibenzo[a,L]pyrene in crude extracts of environmental-samples by laser-excited Shpolskii spectroscopy. Anal. Chem. 1995, 67:1623-1626.
32. LaVoie E.J., He Z.M., Meegalla R.L., Weyand E.H. Exceptional tumor-initiating activity of 4-fluorobenzo[j]-fluoranthene on mouse skin: comparison with benzo[j]-fluoranthene, 10-fluoro-benzo[j]fluoranthene, benzo[a]pyrene, dibenzo[a, l]pyrene and 7,12-dimethylbenz[a]anthracene. Cancer Lett. 1993, 70:7-14.
33. Lee, B.C., Hendricks, J.D., Bailey, G.S., 1991. Toxicity of mycotoxins in the feed of fish. Mycotoxins and Animal Feeding stuff: Natural Occurrence, Tox. Control, 607-626.
34. Loveland P.M., Reddy A.P., Pereira C.B., Field J.A., Bailey G.S. Application of matrix solid-phase dispersion in the determination of dibenzo[a,l]pyrene content of experimental animal diets used in a large-scale tumor study. J. Chromatogr. A 2001, 932:33-41.
35. Mahadevan B., Luch A., Bravo C.F., Atkin J., Steppan L.B., Pereira C., Kerkvliet N.I., Baird W.M. Dibenzo[a,l]pyrene induced DNA adduct formation in lung tissue in vivo. Cancer Lett. 2005, 227:25-32.
36. Mumford J.L., Harris D.B., Williams K., Chuang J.C., Cooke M. Indoor air sampling and mutagenicity studies of emissions from unvented coal combustion. Environ. Sci. Technol. 1987, 21:308-311.
37. Mumford J.L., Li X., Hu F., Lu X.B., Chuang J.C. Human exposure and dosimetry of polycyclic aromatic hydrocarbons in urine from Xuan Wei, China with high lung cancer mortality associated with exposure to unvented coal smoke. Carcinogenesis 1995, 16:3031-3036.
38. Prahalad A.K., Ross J.A., Nelson G.B., Roop B.C., King L.C., Nesnow S., Mass M.J. Dibenzo[a,l]pyrene-induced DNA adduction, tumorigenicity, and Ki-ras oncogene mutations in strain A/J mouse lung. Carcinogenesis 1997, 18:1955-1963.
39. Pratt M.M., Reddy A.P., Hendricks J.D., Pereira C., Kensler T.W., Bailey G.S. The importance of carcinogen dose in chemoprevention studies: quantitative interrelationships between, dibenzo[a,l]pyrene dose, chlorophyllin dose, target organ DNA adduct biomarkers and final tumor outcome. Carcinogenesis 2007, 28:611-624.
40. Qian G.S., Ross R.K., Yu M.C., Yuan J.M., Gao Y.T., Henderson B.E., Wogan G.N., Groopman J.D. 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. 1994, 3:3-10.
41. Ralston S.L., Seidel A., Luch A., Platt K.L., Baird W.M. Stereoselective activation of dibenzo[a,l]pyrene to (-)-anti (11R, 12S, 13S, 14R)- and (+)-syn(11S, 12R, 13S, 14R)-11, 12-diol-13, 14-epoxides which bind extensively to deoxyadenosine residues of DNA in the human mammary carcinoma cell line MCF-7. Carcinogenesis 1995, 16:2899-2907.
42. Reddy A.P., Harttig U., Barth M.C., Baird W.M., Schimerlik M., Hendricks J.D., Bailey G.S. Inhibition of dibenzo[a,l]pyrene-induced multi-organ carcinogenesis by dietary chlorophyllin in rainbow trout. Carcinogenesis 1999, 20:1919-1926.
43. Seidel A., Frank H., Behnke A., Schneider D., Jacob J. Determination of dibenzo[a]pyrene and other fjord-region PAH isomers with MW 302 in environmental samples. Polycyclic Aromat. Compd. 2004, 24:759-771.
44. Shaughnessy D.T., Gangarosa L.M., Schliebe B., Umbach D.M., Xu Z., Macintosh B., Knize M.G., Matthews P.P., Swank A.E., Sandler R.S., Demarini D.M., Taylor J.A. Inhibition of fried meat-induced colorectal DNA damage and altered systemic genotoxicity in humans by crucifera, chlorophyllin, and yogurt. PLoS One 2011, 6:e18707.
45. Simonich M.T., Egner P.A., Roebuck B.D., Orner G.A., Jubert C., Pereira C., Groopman J.D., Kensler T.W., Dashwood R.H., Williams D.E., Bailey G.S. Natural chlorophyll inhibits aflatoxin B1-induced multi-organ carcinogenesis in the rat. Carcinogenesis 2007, 28:1294-1302.
46. Simonich M.T., McQuistan T., Jubert C., Pereira C., Hendricks J.D., Schimerlik M., Zhu B., Dashwood R.H., Williams D.E., Bailey G.S. Low-dose dietary chlorophyll inhibits multi-organ carcinogenesis in the rainbow trout. Food Chem. Toxicol. 2008, 46:1014-1024.
47. Sinnhuber R.O., Hendricks J.D., Wales J.H., Putnam G.B. Neoplasms in rainbow trout, a sensitive animal model for environmental carcinogenesis. Ann. NY Acad. Sci. 1978, 298:389-408.
48. Snook M.E., Severson R.F., Arrendale R.F., Higman H.C., Chortyk O.T. Identification of high molecular-weight polynuclear aromatic-hydrocarbons in a biologically-active fraction of cigarette-smoke condensate. Beitr. Tabakforsch. 1977, 9:79-101.
49. Tilton S.C., Gerwick L.G., Hendricks J.D., Rosato C.S., Corley-Smith G., Givan S.A., Bailey G.S., Bayne C.J., Williams D.E. Use of a rainbow trout oligonucleotide microarray to determine transcriptional patterns in aflatoxin B1-induced hepatocellular carcinoma compared to adjacent liver. Toxicol. Sci. 2005, 88:319-330.
50. Wright T.I., Spencer J.M., Flowers F.P. Chemoprevention of nonmelanoma skin cancer. J. Am. Acad. Dermatol. 2006, 54:933-946.