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antioxidant and prooxidant roles for Β-carotene, Α-tocopherol and ascorbic acid in human lung...

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  • Antioxidant and Prooxidant Roles for Β-carotene, Α-Tocopherol and Ascorbic Acid in Human Lung Cells
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Antioxidant and prooxidant roles for b-carotene, a-tocopherol and ascorbic acid in human lung cells P. Zhang, S.T. Omaye * Environmental Sciences and Health Graduate Program and the Department of Nutrition, Mail Stop 142, University of Nevada, Reno, NV 89557, USA Accepted 1 September 2000 Abstract Experiments were conducted to determine the antioxidant and prooxidant eects of b-carotene, a-tocopherol and ascorbic acid on human lung cells at dierent oxygen (O 2 ) tensions. Free radical initiator, 2,2 0 -azobis (2-amidinopropane) dihydrochloride (AAPH), was used to induce the cellular damage associated with lipid peroxidation, protein oxidation and DNA breaks. Under hypoxic conditions (0 torr O 2 tension) all compounds produced a concentration-dependent antioxidant eect. Mixtures of the three compounds exhibited greater protective aects than any individual compound. At 143 torr O 2 tension, all compounds exhibited concentration-dependent protective eects against AAPH-induced cellular lipid, protein and DNA damage. At 722 torr O 2 tension, cells exhibited a consistent increase in lipid peroxidation (isoprostane formation), protein oxidation (carbonyl formation) and DNA damage (p53 protein accumulation). b-Carotene (1.5 mm) produced a prooxidant eect by promoting 12% isoprostane formation. Protein oxidation and DNA damage at 722 torr O 2 tension was not increased by b-carotene; however, the antioxidant eect of b- carotene was attenuated. The antioxidant eects of a-tocopherol, ascorbic acid, and mixtures of the three antioxidant compounds also were reduced by the high O 2 conditions. These results partially substantiate the hypothesis that the antioxidant and prooxidant eects of b-carotene are dependent on O 2 tension and concentration of b-carotene. Such ®ndings may partially explain why selected populations, such as smokers, respond adversely when supplemented with b-carotene. # 2001 Elsevier Science Ltd. All rights reserved. Keywords: b-Carotene; a-Tocopherol; Ascorbic acid; Human lung cell line CCD-8Lu; Antioxidant; Prooxidant 1. Introduction Intervention trials and animal studies exploring the relationship between b-carotene and disease suggest that b-carotene is of little or no value in preventing cardio- vascular disease and the major cancers that occur in well-nourished populations (ATBC Study Group, 1994; Greenberg et al., 1996; Hennekens et al., 1996; Omenn et al., 1996a; Wang et al., 1999). The mechanism involved, so far understood, is the prooxidant eect of b-carotene at high oxygen concentration. The relation- ship between the prooxidant eect of b-carotene and oxygen concentration and consequences of the proox- idant eect of b-carotene have been studied in in vitro (Vile and Winterbourn, 1988; Palozza et al., 1995, 1997). In vitro, whether b-carotene is antioxidant or prooxidant is dependent on oxygen tension and the concentration of b-carotene (Zhang and Omaye, 2000). The purpose of this study was to test the anti- or prooxidant eects of b-carotene on human lung cells with respect to dierent oxygen tensions, thus allowing us to examine the eects of intact cells on the interac- tions between b-carotene, oxidation and the subsequent impact of antioxidant mixtures. Several epidemiological studies provided data showing the negative eects of b- carotene on lung cancer incidence (ATBC Study Group, 1994; Omenn et al., 1996a,b; Omenn, 1998; Albanes, 1999; Wang et al., 1999). However, the mechanism of such negative eects is unclear. Wang et al. (1999) sug- gested that diminished retinoid signalling, resulting from the suppression of RAR b gene expression and over- expression of activator protein-1, could be a mechanism 0887-2333/01/$ - see front matter # 2001 Elsevier Science Ltd. All rights reserved. PII: S0887-2333(00)00054-0 Toxicology in Vitro 15 (2001) 13±24 www.elsevier.com/locate/toxinvit Abbreviations: AAPH, 2,2 0 -azobis (2-amidinopropane) dihy- drochloride; BHT, butylated hydroxytoluene; BSA, bovine serum albumin; DNP, 2,4-dinitrophenylhydrozine; HRP, disodium horse- radish peroxidase; PBS, phosphate buered saline; pNPP, p-nitrophe- nylphosphate; THF, tetrahydro¯uran; * Corresponding author. Tel.: +1-775-784-6447; fax: +1-775-784- 6449. E-mail address: [email protected] (S.T. Omaye).

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