Low doses of β-carotene and lutein inhibit AOM-induced rat colonic ACF formation but high doses augment ACF incidence

International Journal of Cancer

Volumn 113, Issue 5, 2005, Pages 798-802

  Raju, Jayadev ^a   Swamy, Malisetty V ^a   Cooma, Indranie ^a   Patlolla, Jagan M R ^a   Pittman, Brian ^a   Reddy, Bandaru S ^a   Steele, Vernon E ^b   Rao, Chinthalapally V ^a,c  

^a AMERICAN HEALTH FOUNDATION   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

^c UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

Author keywords

carotene; Aberrant crypt foci; Chemoprevention; Colon cancer; Lutein

Indexed keywords

AZOXYMETHANE; BETA CAROTENE; XANTHOPHYLL;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; CHEMOPROPHYLAXIS; COLON CARCINOGENESIS; CONTROLLED STUDY; DIET SUPPLEMENTATION; DOSE RESPONSE; DRUG EFFICACY; DRUG TOLERABILITY; HISTOPATHOLOGY; MALE; NONHUMAN; PRIORITY JOURNAL; RAT;

ANIMALS; ANTIOXIDANTS; AZOXYMETHANE; BETA CAROTENE; CARCINOGENS; CHEMOPREVENTION; COLONIC NEOPLASMS; DIET; DOSE-RESPONSE RELATIONSHIP, DRUG; LUTEIN; MALE; PRECANCEROUS CONDITIONS; RATS; RATS, INBRED F344;

EID: 11944261867     PISSN: 00207136     EISSN: None     Source Type: Journal    
DOI: 10.1002/ijc.20640     Document Type: Article

References (57)

1. Ahmedin J, Taylor M, Alicia S, Asma G, Elizabeth W, Michael JT. Cancer Statistics. CA Cancer J Clin 2003;53:5-26.
2. Giovannucci E. Modifiable risk factors for colon cancer. Gastroenterol Clin North Am 2002;31:925-43.
3. Bruce WR, Giacca A, Medline A. Possible mechanisms relating diet and risk of colon cancer. Cancer Epidemiol Biomarkers Prev 2000;9:1271-9.
4. Mannisto S, Smith-Warner SA, Spiegelman D, Albanes D, Anderson K, Van Den Brandt PA, Cerhan JR, Colditz G, Feskanich D, Freudenheim JL, Giovannucci E, Goldbohm RA, et al. Dietary Carotenoids and risk of lung cancer in a pooled analysis of seven cohort studies. Cancer Epidemiol Biomarkers Prev 2004;13:40-8.
5. Jain M, Rohan T, Howe G, Miller A. A cohort study of nutritional factors and endometrial cancer. Euro J Epidemiol 2000;16:899-905.
6. Levi F, Pasche C, Lucchini F, La Vecchia C. Selected micronutrients and colorectal cancer. a case-control study from the canton of Vaud, Switzerland. Eur J Cancer 2000;36:2115-9.
7. Michaud D, Feskanich D, Rimm E, Colditz G, Speizer F, Willett W, Giovannucci E. Intake of specific carotenoids and risk of lung cancer in two prospective US cohorts. Am J Clin Nutr 2000;72:990-7.
8. Granado F, Olmedilla B, Blanco I. Nutritional and clinical relevance of lutein in human health. Br J Nutr 2003;90:487-502.
9. Ito Y, Wakai K, Suzuki K, Tamakoshi A, Seki N, Ando M, Nishino Y, Kondo T, Watanabe Y, Ozasa K, Ohno Y; JACC Study Group. Serum carotenoids and mortality from lung cancer: a case-control study nested in the Japan Collaborative Cohort (JACC) study. Cancer Sci 2003;94:57-63.
10. Holick CN, Michaud DS, Stolzenberg-Solomon R, Mayne ST, Pietinen P, Taylor PR, Virtamo J, Albanes D. Dietary carotenoids, serum beta-carotene, and retinol and risk of lung cancer in the alpha-tocopherol, beta-carotene cohort study. Am J Epidemiol 2000;156:536-47.
11. Nomura AM, Ziegler RG, Stemmermann GN, Chyou PH, Craft NE. Serum micronutrients and upper aerodigestive tract cancer. Cancer Epidemiol Biomarkers Prev 1997;6:407-12.
12. Nair S, Norkus EP, Hertan H, Pitchumoni CS. Serum and colon mucosa micronutrient antioxidants: differences between adenomatous polyp patients and controls. Am J Gastroenterol 2001;96:3400-5.
13. Maiani G, Pappalardo G, Ferro-Luzzi A, Raguzzini A, Azzini E, Guadalaxara A, Trifero M, Frommel T, Mobarhan S. Accumulation of beta-carotene in normal colorectal mucosa and colonic neoplastic lesions in humans. Nutr Cancer 1995;24:23-31.
14. The Alpha-Tocopherol, Beta Carotene Cancer Prevention Study Group. The effect of vitamin E and beta carotene on the incidence of lung cancer and other cancers in male smokers. N Engl J Med 1994;330:1029-35.
15. Omenn GS, Goodman GE, Thornquist MD, Balmes J, Cullen MR, Glass A, Keogh JP, Meyskens FL, Valanis B, Williams JH, Barnhart S, Hammar S. Effects of a combination of β-carotene and vitamin A on lung cancer and cardiovascular disease. N Engl J Med 1996;334:1150-5.
16. Hennekens CH, Buring JE, Manson JE, Stampfer M, Rosner B, Cook NR, Belanger C, LaMotte F, Gaziano JM, Ridker PM, Willett W, Peto R. Lack of effect of long-term supplementation with β-carotene on the incidence of malignant neoplasms and cardiovascular disease. N Engl J Med 1996;334:1145-9.
17. Russel RB. The enigma of β-carotene in carcinogenesis: what can be learned from animal studies. J Nutr 2004;134:262S-8S.
18. Lee CM, Boileau AC, Boileau TWM, Williams AW, Swanson KS, Heintz KA, Erdman Jr JW. Review of animal models in carotenoid research. J Nutr 1999;129:2271-7.
19. Rijken PJ, Timmer WG, van de Kooij AJ, van Benschop IM, Wiseman SA, Meijers M, Tijburg LB. Effect of vegetable and carotenoid consumption on aberrant crypt multiplicity, a surrogate end-point marker for colorectal cancer in azoxymethane-induced rats. Carcinogenesis 1999;20:2267-72.
20. Narisawa T, Fukaura Y, Hasebe M, Ito M, Aizawa R, Murakoshi M, Uemura S, Khachik F, Nishino H. Inhibitory effects of natural carotenoids, alpha-carotene, beta-carotene, lycopene and lutein, on colonic aberrant crypt foci formation in rats. Cancer Lett 1996;107:137-42.
21. Komaki C, Okuno M, Onogi N, Moriwaki H, Kawamori T, Tanaka T, Mori H, Muto Y. Synergistic suppression of azoxymethane-induced foci of colonic aberrant crypts by the combination of beta-carotene and perilla oil in rats. Carcinogenesis 1996;17:1897-901.
22. Temple NJ, Basu TK. Protective effect of beta-carotene against colon tumors in mice. J Natl Cancer Inst 1987;78:1211-4.
23. Steinel HH, Baker RSU. Effects of β-carotene on chemically-induced skin tumors in HRA/Skh hairless mice. Cancer Lett 1990;51:163-8.
24. Moreno FS, S-Wu T, Naves MM, Silveira ER, Oloris SC, da Costa MA, Dagli ML, Ong TP. Inhibitory effects of beta-carotene and vitamin A during the progression phase of hepatocarcinogenesis involve inhibition of cell proliferation but not alterations in DNA methylation. Nutr Cancer 2002;44:80-8.
25. Appel MJ, Woutersen RA. Effects of dietary beta-carotene and selenium on initiation and promotion of pancreatic carcinogenesis in azaserine-treated rats. Carcinogenesis 1996;17:1411-6.
26. Tanaka T, Makita H, Ohnishi M, Hirose Y, Wang A, Mori H, Satoh K, Hara A, Ogawa H. Chemoprevention of 4-nitroquinoline 1-oxide-induced oral carcinogenesis by dietary curcumin and hesperidin: comparison with the protective effect of beta-carotene. Cancer Res 1994;54:4653-9.
27. Jones RC, Sugie S, Braley J, Weisburger JH. Dietary beta-carotene in rat models of gastrointestinal cancer. J Nutr 1989;119:508-14.
28. Chen LC, Sly L, Jones CS, Tarone R, De Luca LM. Differential effects of dietary beta-carotene on papilloma and carcinoma formation induced by an initiation-promotion protocol in SENCAR mouse skin. Carcinogenesis 1993;14:713-7.
29. Wang X-D, Liu C, Bronson RT, Smith DE, Krinsky NI, Russell RM. Retinoid signaling and activator protein-1 expression in ferrets given β-carotene supplements and exposed to tobacco smoke. J Natl Cancer Inst 1999;91:60-6.
30. Salgado-Oloris SC, Dagli ML, Guerra JL. Effect of beta-carotene on the development of the solid Ehrlich tumor in mice. Life Sci 2002;71:717-24.
31. Slattery ML, Benson J, Curtin K, Ma KN, Schaeffer D, Potter JD. Carotenoids and colon cancer. Am J Clin Nutr 2000;71:575-82.
32. Zhang S, Hunter DJ, Forman MR, Rosner BA, Speizer FE, Colditz GA, Manson JE, Hankinson SE, Willett WC. Dietary carotenoids and vitamins A, C, and E and risk of breast cancer. J Natl Cancer Inst 1999;91:547-56.
33. Dorgan JF, Sowell A, Swanson CA, Potischman N, Miller R, Schussler N, Stephenson HE Jr. Relationships of serum carotenoids, retinol, alpha-tocopherol, and selenium with breast cancer risk: results from a prospective study in Columbia, Missouri (United States). Cancer Causes Control 1998;9:89-97.
34. Kim JM, Araki S, Kim DJ, Park CB, Takasuka N, Baba-Toriyama H, Ota T, Nir Z, Khachik F, Shimidzu N, Tanaka Y, Osawa T, Uraji T, Murakoshi M, Nishino H, Tsuda H. Chemopreventive effects of carotenoids and curcumins on mouse colon carcinogenesis after 1,2-dimethylhydrazine initiation. Carcinogenesis 1998;19:81-5.
35. Park JS, Chew BP, Wong TS. Dietary lutein from marigold extract inhibits mammary tumor development in BALB/c mice. J Nutr 1998;128:1650-6.
36. Bendich A. From 1989 to 2001: what have we learned about the "biological actions of beta-carotene". J Nutr 2004;134:225S-30S.
37. Bendich A, Olson JA. Biological actions of carotenoids. FASEB J 1998;3:1927-32.
38. Olson JA, Hayaishi O. The enzymatic cleavage of β-carotene into vitamin A by soluble enzymes of rat liver and intestines. Proc Natl Acad Sci U S A 1965;54:1364-9.
39. Goodman DS, Huang HS, Shiratori T. Mechanism of biosynthesis of vitamin A from β-carotene. J Biol Chem 1966;242:1929-321.
40. Young AJ, Lowe GM. Antioxidant and prooxidant properties of carotenoids. Arch Biochem Biophys 2001;385:20-7.
41. Krinsky NI. Carotenoids as antioxidants. Nutrition 2001;17:815-817.
42. Chew BP, Park JS. Carotenoid action on the immune response. J Nutr 2004;134:257S-261S.
43. Hughes DA. Dietary carotenoids and human immune function. Nutrition 2001;17:823-7.
44. Landrum JT, Bone RA. Lutein, zeaxanthin, and the macular pigment. Arch Biochem Biophys 2001;385:28-40.
45. American Institute of Nutrition. Report of the American Institute of Nutrition ad hoc committee on standards for nutritional studies. J Nutr 1977;107:1340-8.
46. Bird RP. Observation and quantification of aberrant crypts in the murine colon treated with a colon carcinogen: preliminary findings. Cancer Lett 1987;37:147-51.
47. Corpet DE, Tache S. Most effective colon cancer chemopreventive agents in rats: a systematic review of aberrant crypt foci and tumor data, ranked by potency. Nutr Cancer 2002;43:1-21.
48. Bird RP, Good CK. The significance of aberrant crypt foci in understanding the pathogenesis of colon cancer. Toxicol Lett 2000;112-113:395-402.
49. Pretlow TP, O'Riordan MA, Somich GA, Amini SB, Pretlow TG. Aberrant crypts correlate with tumor incidence in F344 rats treated with azoxymethane and phytate. Carcinogenesis 1992;13:1509-12.
50. Dietary References Intakes for Vitamin C, Vitamin A, Selenium and Carotenoids. Washington, D.C.: Food and Nutrition Board, Institute of Medicine, National Academy Press, 2000.
51. Martin KR, Eailla ML, Smith JC. β-Carotene and lutein protect HepG2 human liver cells against oxidant-induced damage. J Nutr 1996;126:2098-106.
52. Bertram JS, Bortkiewicz H. Dietary carotenoids inhibit neoplastic transformation and modulate gene expression in mouse and human cells. Am J Clin Nutr 1995;62:1327S-36S.
53. Palozza P, Serini S, Torsello A, Di Nicuolo F, Maggiano N, Ranelletti FO, Wolf FI, Calviello G. Mechanism of activation of caspase cascade during beta-carotene-induced apoptosis in human tumor cells. Nutr Cancer 2003;47:76-87.
54. Palozza P, Serini S, Torsello A, Di Nicuolo F, Piccioni E, Ubaldi V, Pioli C, Wolf FI, Calviello G. Beta-carotene regulates NF-kappaB DNA-binding activity by a redox mechanism in human leukemia and colon adenocarcinoma cells. J Nutr 2003;133:381-8.
55. Paolini M, Cantelli-Forti G., Perocco P, Pedulli GF, Abdel-Rahman S, Legator MS. Cocarcinogenic effect of β-carotene. Nature 1999;398,760-1.
56. Paolini M, Antelli O, Pozetti L, Spetlova D, Perocco P, Valgimigli L, Pedulli GF, Cantelli-Forti G. Induction of Cytochrome P450 enzymes and over-generation of oxygen radicals in β-carotene supplemented rats. Carcinogenesis 2001;22:1483-557. Burton GW, Ingold KU. β-carotene: an unusual type of lipid antioxidant. Science 1984;224:569-73.
57. Paolini M, Antelli O, Pozetti L, Spetlova D, Perocco P, Valgimigli L, Pedulli GF, Cantelli-Forti G. Induction of Cytochrome P450 enzymes and over-generation of oxygen radicals in β-carotene supplemented rats. Carcinogenesis 2001;22:1483-557. Burton GW, Ingold KU. β-carotene: an unusual type of lipid antioxidant. Science 1984;224:569-73.