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Original Contribution Free Radical Biology & Medicine, Vol. 32, No. 12, pp. 1293–1303, 2002 Copyright © 2002 Elsevier Science Inc. Printed in the USA. All rights reserved 0891-5849/02/$–see front matter PII S0891-5849(02)00831-6 Original Contribution PHOTOPROTECTIVE POTENTIAL OF LYCOPENE, ␤-CAROTENE, VITAMIN E, VITAMIN C AND CARNOSIC ACID IN UVA-IRRADIATED HUMAN SKIN FIBROBLASTS 1 † ‡ ELIZABETH A. OFFORD,* JEAN-CHARLES GAUTIER,* ORNELLA AVANTI,* CORINNE SCALETTA, FRANK RUNGE, ‡ † KLAUS KRAMER¨ , and LEE ANN APPLEGATE *Nestle´ Research Center, Department of Nutrition, Lausanne, Switzerland; †University Hospital of the Canton of Vaud, Department of Gynecology and Obstetrics, Lausanne, Switzerland; and ‡BASF Aktiengesellschaft, Strategic Marketing Fine Chemicals, Ludwigshafen, Germany (Received 3 December 2001; Revised 1 March 2002; Accepted 1 March 2002) Abstract—The photoprotective potential of the dietary antioxidants vitamin C, vitamin E, lycopene, ␤-carotene, and the rosemary polyphenol, carnosic acid, was tested in human dermal fibroblasts exposed to ultraviolet-A (UVA) light. The carotenoids were prepared in special nanoparticle formulations together with vitamin C and/or vitamin E. Nanoparticle formulations, in contrast to dimethylsulphoxide, stablized lycopene in the cell culture medium and allowed efficient cellular uptake. The presence of vitamin E in the formulation further increased the stability and cellular uptake of lycopene. UVA irradiation of the human skin fibroblasts led to a 10–15-fold rise in metalloproteinase 1 (MMP-1) mRNA. This rise was suppressed in the presence of low ␮M concentrations of vitamin E, vitamin C, or carnosic acid but not with ␤-carotene or lycopene. Indeed, in the presence of 0.5–1.0 ␮M ␤-carotene or lycopene, the UVA-induced MMP-1 mRNA was further increased by 1.5–2-fold. This increase was totally suppressed when vitamin E was included in the nanoparticle formulation. Heme-oxygenase 1 (HO-1) mRNA expression was strongly induced by UVA irradiation but none of the antioxidants inhibited this effect at the concentrations used in this study. Indeed, ␤-carotene or lycopene (0.5–1.0 ␮M) led to a further 1.5-fold rise in the UVA-induced HO-1 mRNA levels. In conclusion, vitamin C, vitamin E, and carnosic acid showed photoprotective potential. Lycopene and ␤-carotene did not protect on their own but in the presence of vitamin E, their stability in culture was improved and the rise in MMP-1 mRNA expression was suppressed, suggesting a requirement for antioxidant protection of the carotenoids against formation of oxidative derivatives that can influence the cellular and molecular responses. © 2002 Elsevier Science Inc. Keywords—Oxidative stress, UVA, Heme oxygenase, Metalloproteinase I, Skin, Lycopene, ␤-carotene, Vitamin C, Vitamin E, Rosemary, Carnosic acid, Free radicals INTRODUCTION stress marker gene, heme-oxygenase I (HO-1) [3,4]. Sin- glet oxygen is strongly implicated as mediator in induc- Ultraviolet (UV) irradiation is well known to induce tion of these two genes [5,6]. photodamage and premature skin aging [1]. Ultravio- While topical application of sun screens provides a let-A (UVA) light is particularly associated with oxida- barrier protection to the skin epithelium, protection of the tive processes involved in photoaging. A cascade of gene more profound dermal layers may be offered by dietary expression is initiated following UVA irradiation, which antioxidants acting from within. Up until now, the most results in the upregulation of interstitial collagenase intensively studied dietary antioxidants for prevention of (metalloproteinase 1 [MMP-1]) [2] and the oxidative skin photodamage have been vitamin C, vitamin E, and ␤ Address correspondence to: Dr. Elizabeth Offord, Nestle´ Research -carotene [7]. Short-term clinical studies on the ability Center, Department of Nutrition, P. O. Box 44, CH-1000 Lausanne 26, of these antioxidants to protect against UV-induced er- Switzerland; Tel: ϩ41 (21) 785 8809; Fax: ϩ41 (21) 785 8925; ythema have shown varying degrees of success [7–11]. E-Mail: [email protected]. ␤ 1Present address: Aventis Pharma, Drug Safety Evaluation, 13, Quai Protection by -carotene is enhanced when combined Jules guesde, BP 14, 94403 Vitry-sur-Seine, France. with vitamin E [9]. Another carotenoid found in toma- 1293 1294 E. A. OFFORD et al. toes, lycopene, has received much attention for its po- ing [1] and of HO-1 as a general marker of cellular tential health properties [12], particularly with respect to oxidative stress [3,4]. protection against gastrointestinal tract, prostate, and lung cancers [13–16]. Lycopene is an acyclic carotenoid MATERIALS AND METHODS with 11 linearly arranged conjugated double bonds and is the most potent singlet oxygen scavenger among the carotenoids [17]. Lycopene is present in skin and could Antioxidant preparations play a role for protecting against UV radiation as it is the Powdered nanoparticles containing various amounts antioxidant most quickly depleted in skin upon exposure of lycopene, ␤-carotene, vitamin E (all-rac-␣-tocopher- to solar radiation [18]. Recently, it was reported for the ol), and sodium ascorbate either alone or in combination, first time that ingestion of tomato paste daily for 10 were provided by BASF (Ludwigshafen, Germany). The weeks, protected against UV light-induced erythema on carotenoid formulations were prepared using a precipi- the dorsal skin [19]. tation process by mixing a carotenoid solution in alcohol The natural spice and flavoring agent, rosemary, is a with an aqueous gelatin solution (so-called mixing cham- potent source of natural antioxidants, such as the poly- ber micronization), as previously described [36–38]. The phenolic diterpenes carnosol and carnosic acid [20–23]. resulting nanoscale carotenoid dispersions were trans- Rosemary extracts or their active constituents have anti- ferred into dry powders by conventional spray drying. carcinogenic properties [24] and reduce skin tumorige- The vitamin E formulations were prepared by an emul- nicity [25–27]. Their mode of action has principally been sification/spray drying process. The corresponding con- described to involve scavenging of free radicals and modulation of xenobiotic-metabolizing enzymes [28– trol powders contained gelatin and glucose syrup mixed 30]. In this study, we were interested in further investi- or not mixed with ascorbyl palmitate, a lipophilic form of ␮ gating whether carnosic acid showed protection against vitamin C (0.5% in powder; 0.7 M final concentration UVA-induced photodamage. in cell culture medium). Ascorbyl palmitate was used as Cell culture systems provide the opportunity to inves- an additive in the mixing chamber micronization process tigate the molecular and cellular processes involved in to achieve the proper stability of the carotenoid nanopar- photoprotection by antioxidants; however, certain tech- ticles. The powders were stored at room temperature nical difficulties may be encountered with substances sealed under argon, and were dissolved in the culture that are either unstable or lipid soluble. Carotenoids are medium. Equivalent amounts of control matrix powders very hydrophobic molecules that are often solubilized in were added in all experiments. Crystalline lycopene was organic solvents such as tetrahydrofuran (THF) or dim- prepared in DMSO as a stock concentration of 1 mM and ethylsulphoxide (DMSO); however, an uncontrolled pre- diluted in cell culture medium preheated to 37°C, to a cipitation process occurs upon addition of these solutions final concentration of 1 ␮M. The stock and final culture to aqueous media. In this process, carotenoid crystals are medium concentrations were checked by HPLC as de- formed with a noncontrollable particle size which is scribed below. Carnosic acid, purifed from rosemary typically in the order of several micrometers, depending leaves [39], was prepared as a stock solution of 1 mg/ml on the experimental conditions. The solubility and up- in DMSO and used at a final concentration of 0.1–1.0 take of these large crystals in the cells is quite limited and ␮g/ml (equivalent to 0.3–3.0 ␮M). Control cells were there is almost no protection against chemical degrada- treated with 0.1% DMSO alone. tion. Alternative ways of delivering lipid-soluble com- pounds include micelles, microemulsions, nanoparticles, water-dispersible beadlets, artificial liposomes, enriched Cell cultures bovine serum, or specialized formulations, each of which has an influence on the uptake and stability of the com- Human dermal fibroblasts GT-F were prepared from a pounds [31–35]. 26-year-old male with skin type III (brown hair, brown The aim of the present study was to test the dietary eyes) and were used between the 10th and 15th passages, antioxidants, vitamin C, vitamin E, lycopene, ␤-carotene, as previously described [40]. Fibroblasts were plated out and carnosic acid for their ability to protect against in 100-mm-diameter petri dishes in DMEM medium photoaging in primary cultures of human dermal fibro- containing Glutamax I, glucose 4.5 g/l (GibcoBRL, blasts irradiated with UVA. The lipid-soluble com- Basel, Switzerland) supplemented with 10% fetal bovine pounds were formulated in special nanoparticle formu- serum (50 ml for 500 ml medium), and penicillin/strep- lations. The photoprotective effect of the antioxidants tomycin (0.5 ml of 0.1% stock solution for 500 ml was monitored by studying the expression of MMP-1 as medium). Cells were incubated in a saturated 10% CO2/ a marker of potential collagen degradation and photoag- 90% air atmosphere at 37°C and grown to confluency. Photoprotective effects of dietary antioxidants 1295 Cell treatment and UVA irradiation and 100 ␮l for cell lysates) were injected onto a C18 Hypersil precolumn (20 ϫ 4 mm, 5 ␮m internal diame- Cells were first treated with test compounds 24 h ter, Hewlett Packard) followed by a C18 Nova-pak col- before UVA irradiation to allow penetration into the umn (300 ϫ 3.9 mm, Waters). Tocopherols and carote- ϫ 6 cells. Just prior to the irradiation, 2 10 cells were noids were separated under isocratic conditions with a washed with 10 ml of phosphate buffered saline (PBS) mobile phase consisting of acetonitrile/tetrahydrofuran/ and 5 ml was added.
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