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Effects of carotenoids on human immune function

Published online by Cambridge University Press:  28 February 2007

David A. Hughes*
Affiliation:
Diet, Health and Consumer Science Division, Institute of Food Research, Norwich Research Park, Norwich NR4 7UA, UK
*
Corresponding Author: Dr D. A. Hughes, fax +44 (0)1603 255237, email [email protected]
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Abstract

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Many epidemiological studies have shown an association between diets rich in carotenoids and a reduced incidence of many forms of cancer, and it has been suggested that the antioxidant properties of these compounds are a causative factor. Attention has focused on the potential role of one specific carotenoid, β-carotene, in preventing cancer, and numerous publications have described in vitro experiments and animal studies which suggest that not only can this carotenoid protect against the development of cancer, but also several other chronic diseases. Since the immune system plays a major role in cancer prevention, it has been suggested that β-carotene may enhance immune cell function. Several human trials, using dietary β-carotene supplementation with a wide range of intakes, have been undertaken to address this hypothesis. The general conclusion of these studies is that this compound can enhance cell-mediated immune responses, particularly in the elderly. The present article will review some of these human studies and, hopefully, complement the reviews of other authors associated with the present symposium, some of whom will also describe work in this area. Potential mechanisms for the effects of carotenoids on immune function will also be reviewed. Finally, possible reasons for the failure of three major prospective studies to demonstrate a beneficial effect of β-carotene supplementation on lung cancer risk will be discussed.

Type
Symposium on ’Nutrition, infection and immunity‘
Copyright
Copyright © The Nutrition Society 1999

References

Alexander, M, Newmark, H & Miller, G (1985) Oral beta-carotene can increase the number of OKT4 positive cells in human blood. Immunology 9, 221224.Google Scholar
Allard, JP, Aghdassi, E, Chau, J, Tam, C, Kovacs, CM, Salit, IE & Walmsley, SL (1998) Effects of vitamin E and C supplementation on oxidative stress and viral load in HIV-infected subjects. AIDS 12, 16531659.CrossRefGoogle Scholar
Bach, FH (1985) Class II genes and products of the HLA-D region. Immunology Today 6, 8994.CrossRefGoogle ScholarPubMed
Baker, KR & Meydani, M (1994) Beta-carotene in immunity and cancer. Journal of Optimal Nutrition 3, 3950.Google Scholar
Bendich, A (1996) Antioxidant vitamins and human immune responses. Vitamins and Hormones 52, 3562.CrossRefGoogle ScholarPubMed
Block, G, Patterson, B & Subar, A (1992) Fruit, vegetables, and cancer prevention: a review of the epidemiological evidence. Nutrition and Cancer 18, 129.CrossRefGoogle ScholarPubMed
Chandra, RK (1992) Effect of vitamin and trace-element supplementation on immune responses and infection in elderly subjects. Lancet 340, 11241127.CrossRefGoogle ScholarPubMed
Fernandes, G (1997) Beta-carotene supplementation: Friend or foe? Journal of Laboratory and Clinical Medicine 129, 285287.CrossRefGoogle ScholarPubMed
Fryburg, DA, Mark, RJ, Griffith, BP, Askenase, PW & Patterson, TF (1995) The effect of supplemental beta-carotene on immunological indices in patients with AIDS: a pilot study. Yale Journal of Biological Medicine 68, 1923.Google ScholarPubMed
Fuller, CJ, Faulkner, H, Bendich, A, Parker, RS & Roe, DA (1992) Effect of beta-carotene supplementation on photosuppression of delayed-type hypersensitivity in normal young men. American Journal of Clinical Nutrition 56, 684690.CrossRefGoogle ScholarPubMed
Gollnick, PM, Hopfenmuller, W, Hemmes, C, Chun, SC, Schmid, C, Sundermeier, K & Biesalski, HK (1996) Systemic beta-carotene plus topical UV-sunscreen are an optimal protection against harmful effects of natural UV-sunlight: results of the Berlin-Eilath study. European Journal of Dermatology 6, 200205.Google Scholar
Greenwald, ED & Greenwald, ES (1983) Skin cancer. In Cancer Epidemiology, pp. 2629 [Greenwald, ED, editor]. New York: Medical Examination Publishing Co. Inc.Google Scholar
Gruner, S, Volk, H-D, Falck, P & Baehr, RV (1986) The influence of phagocytic stimuli on the expression of HLA-DR antigens; role of reactive oxygen intermediates. European Journal of Immunology 16, 212215.CrossRefGoogle ScholarPubMed
Halevy, O & Sklan, D (1987) Inhibition of arachidonic acid oxidation by beta-carotene, retinol and α-tocopherol. Biochimica et Biophysica Acta 918, 304307.CrossRefGoogle ScholarPubMed
Hennekens, CH, Buring, JE, Manson, JE & Stampfer, M (1996) Lack of effect of long term supplementation with beta carotene on the incidence of malignant neoplasms and cardiovascular disease. New England Journal of Medicine 334, 11451149.CrossRefGoogle ScholarPubMed
Hughes, DA (1999) Effects of dietary antioxidants on the immune function of middle-aged adults. Proceedings of the Nutrition Society 58, 7984.CrossRefGoogle ScholarPubMed
Hughes, DA, Pinder, AC, Piper, Z, Johnson, IT & Lund, EK (1996) Fish oil supplementation inhibits the expression of major histocompatibility complex class II molecules and adhesion molecules on human monocytes. American Journal of Clinical Nutrition 63, 267272.CrossRefGoogle ScholarPubMed
Hughes, DA, Wright, AJA, Finglas, PM, Peerless, ACJ, Bailey, AL, Astley, SB, Pinder, AC & Southon, S (1997 a) The effect of beta-carotene supplementation on the immune function of blood monocytes from healthy male nonsmokers. Journal of Laboratory and Clinical Medicine 129, 309317.CrossRefGoogle ScholarPubMed
Hughes, DA, Wright, AJA, Finglas, PM, Peerless, ACJ, Bailey, AL, Astley, SB, Pinder, AC & Southon, S (1997 b) Comparison of effects of beta-carotene and lycopene supplementation on the expression of functionally associated molecules on human monocytes. Biochemical Society Transactions 25, 206S.CrossRefGoogle ScholarPubMed
Hughes, DA, Wright, AJA, Finglas, PM, Polley, ACJ, Bailey, AL, Astley, SB, Pinder, AC & Southon, S (1998) Effect of lutein supplementation on the expression of functionally associated molecules on human blood monocytes. Immunology 95, Suppl. 1, 61.Google Scholar
Jackson, MJ, McArdle, A & McArdle, F (1998) Antioxidant micronutrients and gene expression. Proceedings of the Nutrition Society 57, 301305.CrossRefGoogle ScholarPubMed
Janeway, CA, Bottomly, K, Babich, J, Conrad, P, Conzen, S, Jones, B, Kaye, J, Katz, M, McVay, L, Murphy, DB & Tite, J (1984) Quantitative variation in Ia antigen expression plays a central role in immune regulation. Immunology Today 5, 99104.CrossRefGoogle Scholar
Khan, IU, Boehm, KD & Elmets, CA (1993) Modulation of interferon-gamma-induced HLA-DR expression on the human keratinocyte cell line SCC-13 by ultraviolet radiation. Photochemistry and Photobiology 57, 285290.CrossRefGoogle ScholarPubMed
Mathews-Roth, MM (1989) Beta-carotene: clinical aspects. In New Protective Roles for Selected Nutrients, pp. 1738 [Spiller, GA and Scala, J, editors]. New York: Alan R. Liss Inc.Google Scholar
Mayne, SM (1996) Beta-carotene, carotenoids, and disease prevention in humans. FASEB Journal 10, 690701.CrossRefGoogle ScholarPubMed
Murata, T, Tamai, H, Morinobu, T, Manago, M, Takenaka, H, Hayashi, K & Mino, M (1994) Effect of long-term administration of beta-carotene on lymphocyte subsets in humans. American Journal of Clinical Nutrition 60, 597602.CrossRefGoogle ScholarPubMed
Omenn, GS, Goodman, GE & Thornquist, MD (1996) Effects of a combination of beta carotene and vitamin A on lung cancer and cardiovascular disease. New England Journal of Medicine 334, 11501155.CrossRefGoogle ScholarPubMed
Palozza, P (1998) Prooxidant actions of carotenoids in biological systems. Nutrition Reviews 56, 257265.CrossRefGoogle Scholar
Peto, R, Doll, R, Buckley, JD & Sporn, MB (1981) Can dietary beta-carotene materially reduce human cancer rates? Nature 290, 201208.CrossRefGoogle ScholarPubMed
Prabhala, RH, Garewal, HS, Hicks, MJ, Sampliner, RE & Watson, RR (1991) The effects of 13-cis-retinoic acid and beta-carotene on cellular immunity in humans. Cancer 67, 15561560.3.0.CO;2-O>CrossRefGoogle Scholar
Riondel, J, Glise, D, Fernandez-Carlos, T & Favier, A (1998) In vitro comparative study of cytolysis mediated by natural killer cells towards malignant cells preincubated with antioxidants. Anticancer Research 18, 17571764.Google ScholarPubMed
Rivers, JK, Norris, PG, Murphy, GM, Chu, AC, Midgley, G, Morris, J, Morris, RW, Young, AR & Hawk, JL (1989) UVA sunbeds: tanning, photoprotection, acute adverse effects and immunological changes. British Journal of Dermatology 120, 767777.CrossRefGoogle ScholarPubMed
Santos, MS, Leka, LS, Ribaya-Mercado, JD, Russell, RM, Meydani, M, Hennekens, CH, Gaziano, JM & Meydani, SN (1997) Short- and long-term beta-carotene supplementation do not influence T cell-mediated immunity in healthy elderly persons. American Journal of Clinical Nutrition 66, 917924.CrossRefGoogle Scholar
Santos, MS, Meydani, SN, Leka, L, Wu, D, Fotouhi, N, Meydani, M, Hennekens, CH & Gaziano, JM (1996) Natural killer cell activity in elderly men is enhanced by beta-carotene supplementation. American Journal of Clinical Nutrition 64, 772777.CrossRefGoogle ScholarPubMed
Sen, CK & Packer, L (1996) Antioxidant and redox regulation of gene transcription. FASEB Journal 10, 709720.CrossRefGoogle ScholarPubMed
Snyder, DS, Beller, DI & Unanue, ER (1982) Prostaglandins modulate macrophage Ia expression. Nature 299, 163165.CrossRefGoogle ScholarPubMed
Springer, TA (1990) Adhesion receptors of the immune system. Nature 346, 425434.CrossRefGoogle ScholarPubMed
Tang, A & Udey, MC (1991) Inhibition of epidermal Langerhans cell function by low dose ultraviolet B radiation. Ultraviolet B radiation selectively modulates ICAM-1 (CD54) expression by murine Langerhans cells. Journal of Immunology 146, 33473355.CrossRefGoogle ScholarPubMed
The Alpha-tocopherol Beta-carotene Cancer Prevention Study Group (1994) The effect of vitamin E and beta-carotene on the incidence of lung cancer and other cancers in male smokers. New England Journal of Medicine 330, 10291035.CrossRefGoogle Scholar
Toyokuni, S, Okamoto, K, Yodoi, J & Hiai, H (1995) Persistent oxidative stress in cancer. FEBS Letters 358, 13.CrossRefGoogle ScholarPubMed
Watson, RR, Prabhala, RH, Plezia, PM & Alberts, DS (1991) Effect of beta-carotene on lymphocyte subpopulations in elderly humans: evidence for a dose-response relationship. American Journal of Clinical Nutrition 53, 9094.CrossRefGoogle ScholarPubMed
Wayne, SJ, Rhyne, RL, Garry, PJ & Goodwin, JS (1990) Cell-mediated immunity as a predictor of morbidity and mortality in subjects over 60. Journal of Gerontology 45, M45M48.CrossRefGoogle ScholarPubMed
Zeigler, RG, Mayne, ST & Swanson, CA (1996) Nutrition and lung cancer. Cancer Causes and Controls 7, 157177.CrossRefGoogle Scholar