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Lutein, a Nonprovitamin A, Activates the Retinoic Acid Receptor to Induce HAS3-Dependent Hyaluronan Synthesis in Keratinocytes

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Lutein, a Nonprovitamin A, Activates the Retinoic Acid Receptor to Induce HAS3-Dependent Hyaluronan Synthesis in Keratinocytes Biosci. Biotechnol. Biochem., 77 (6), 1282–1286, 2013 Lutein, a Nonprovitamin A, Activates the Retinoic Acid Receptor to Induce HAS3-Dependent Hyaluronan Synthesis in Keratinocytes y Tetsuya SAYO, Yoshinori SUGIYAMA, and Shintaro INOUE Innovative Beauty Science Laboratory, Kanebo Cosmetics Inc., Kotobuki-cho, Odawara 250-0002, Japan Received February 15, 2013; Accepted March 13, 2013; Online Publication, June 7, 2013 [doi:10.1271/bbb.130124] Carotenoids have been reported to have potent -Cryptoxanthin, which has a structure similar to - antioxidant activities and to protect tissues and cells carotene, can also be cleaved by -carotene 15, 150- from certain diseases and environmental insults. The monooxygenase (BCO1) to produce retinal and retinoic molecular mechanism of the action of provitamin A acid.7) It has been reported that high doses of -carotene carotenoids such as -carotene and -cryptoxanthin is substantially reduced the malignant conversion of mediated in part by retinoic acid, an active form of papillomae to carcinomas as well as retinoic acid.8,9) provitamin A, but the molecular basis of the biological Because both provitamin A carotenoids and retinoids are activities of non-provitamin A carotenoids such as used as potential protective agents in tumor formation, lutein, zeaxanthin, and astaxanthin is not fully under- the molecular mechanisms of the action of carotenoids is stood. In this study, we investigated to determine probably mediated at least in part by retinoic acid. whether the actions of non-provitamin A carotenoids Topical treatments of retinoic acid have been found are mediated via retinoid signaling by monitoring to be beneficial to photodamaged skin.10,11) Retinoic retinoic acid receptor (RAR)-dependent hyaluronan acid inhibits UV-caused loss of procollagen synthe- production in cultured human keratinocytes. Not only sis,12) the induction of matrix metalloproteinases,13) and -carotene and -cryptoxanthin, but also lutein, zeax- the tortuosity of elastic fibers.14) In addition to these anthin, and astaxanthin, upregulated HAS3 gene ex- effects, it increases the synthesis of epidermal hyalur- pression and were followed by hyaluronan synthesis. We onan,15,16) a high molecular mass glycosaminoglycan found that LE540, an antagonist of retinoic acid that might support epidermal homeositasis by main- receptors, abolished lutein dependent hyaluronan syn- taining the extracellular space, facilitating the exchange thesis and that lutein significantly increased retinoic of nutrients and waste products.17) This suggests the acid responsive element (RARE)-driven transcript aci- possible involvement of hyaluronan in retinoic acid- tivity. In addition, we found that citral, an inhibitor of induced repair, because hyaluronan has been reported retinal dehydrogenases, decreased lutein-stimulated to be closely involved in keratinocyte proliferation and hyaluronan synthesis, indicating that lutein metabolites differentiation.18–20) rather than lutein itself act as an RAR ligand in RAR- Hyaluronan is synthesized by hyaluronan synthase mediated transcription activity in keratinocytes. A proteins (HAS1, HAS2, and HAS3) at the inner surface series of non-provitamin A can be substituted for of the plasma membrane.21) In human epidermal retinoids and should be considered as a potential means keratinocytes, HAS3 mRNA is dominantly expressed of improving skin health. and primarily regulates hyaluronan synthesis.22–24) In- duction of HAS3 gene expression by -carotene stim- Key words: provitamin A; non-provitamin A; lutein; ulation was also found in keratinocytes.25) Since the retinoic acid receptor; hyaluronan expression of BCO17,26) and the conversion from retinal to retinoic acid have been confirmed in the skin,27) the Carotenoids are plant pigments with roles in photo- molecular mechanism of action of provitamin A is synthesis and photoprotection. It has been found that probably mediated by retinoic acid receptors (RARs) in carotenoids have antitumor,1) photoprotective,2) radical the keratinocytes. quenching,3) and antioxidant4) activities. They display On the other hand, non-provitamin A carotenoids these beneficial effects, as well as the ability to act as have also been found to have physiological activities. provitamin A and precursors of retinoic acid. The major Suppression of mouse skin papilloma28) and morpho- provitamin A carotenoids in mammals are -carotene, - logical changes in human mammary cells29) were cryptoxanthin, and -carotene. In contrast, it is currently observed in response not only to -carotene, but also thought that non-provitamin A carotenoids including to canthaxanthin, a non-provitamin A carotenoid. These lutein, zeaxanthin, and astaxanthin, are not precursors of effects have been observed in response to both provi- retinoic acid in mammals.5) tamin A and non-provitamin A, suggesting that retinoid- -Carotene, a major dietary source of vitamin A, is like metabolites converted from non-provitamin A act in converted to retinoic acid, an active form of vitamin A, these biological effects. Recently, Sangeetha reported by a series of enzymatic steps in the intestinal mucosa.6) that astaxanthin, a non-provitamin A carotenoid, is y To whom correspondence should be addressed. Tel: +81-465-34-6116; Fax: +81-465-34-3037; E-mail: [email protected] Abbreviations: HAS, hyaluronan synthase; RA, retinoic acid; RAL, retinal; RAR, retinoic acid receptor; RARE, retinoic acid responsive element; SEAP, secreted alkaline phosphatase; BCO1, -carotene 15, 150-monooxygenase; RALDH, retinal dehydrogenase; BPE, bovine pituitary extracts Lutein Activates the Retinoic Acid Receptor in Keratinocytes 1283 converted to -carotene and retinol in retinol-deficient promoter (Clontech, Palo Alto, CA). A pSEAP2-Basic vector rats,30) but the details as to where and how astaxanthin is (Clontech) containing a SEAP gene without a promoter was used as converted to retinoids have remained obscure. negative control to measure the background signal associated with the cell culture media. Keratinocytes in a 12-well plate were transfected In view of the above, we hypothesized that non- with pRARE-TA-SEAP or pSEAP2-Basic vector with Fugene 6 provitamin A can be converted to carboxylic acids transfection reagent (Roche Diagnostics, Mannheim, Germany), as corresponding to retinoic acid in the skin, and have indicated in the manual. After transfection for 24 h, the cells were similar functions. treated with lutein and incubated for 24 h. SEAP activities in the In the present study, we examined the effects of non- conditioned media were measured by the EscApe SEAP chemilumi- provitamin A carotenoids on hyaluronan production in nescence detection system (Clontech) and Luminescencer PSN human keratinocytes. Furthermore, we sought to deter- AB2200 (ATTO, Tokyo). mine whether the physiological effects of non-provita- Statistical analysis. Results were expressed as means Æ SD. All min A carotenoids in cultured keratinocytes is due to statistical calculations were performed using SASÒ software. The data RAR activation. were analyzed using Dunnett’s multiple comparison test. Dose dependency was determined by the Williams test. A p value of less Materials and Methods than 0.05 was considered to be statistically significant. Chemicals and materials. Human foreskin keratinocytes and bovine Results pituitary extracts (BPE) were purchased from Kurabo (Osaka, Japan). MCDB153 medium, LE540, and Am80 were from Wako Pure Chemical (Osaka, Japan). -Cryptoxanthin, lutein, zeaxanthin, Effects of carotenoids on HAS3-mediated hyaluronan astaxanthin, lycopene, -ionone, -ionone, and citral were from synthesis in keratinocytes Extrasynthese (Genay, France). Phytoene was from Carotenature We evaluated hyaluronan synthesis in human kerati- (Lupsingen, Switzerland). All-trans retinoic acid, all-trans retinal, nocytes by various carotenoids, including -carotene as and -carotene were from Sigma (St. Louis, MO). Ch55 was from positive control,25) and related compounds to investigate Tocris Bioscience (Bristol, UK). structure-activity relationships (Fig. 1). The structure of Cell culture. Human epidermal keratinocytes were grown routinely each of the compounds investigated is shown in Fig. 2. in MCDB153 (0.1 mM Ca2þ) supplemented with 5 mg/L of insulin, Hyaluronan increased significantly when keratino- 180 mg/L hydrocortisone, 14.1 mg/L O-phosphorylethanolamine, cytes were exposed not only to the provitamin A 6.1 mg/L 2-aminoethanol, 100 ng/L EGF, and 0.4% (vol/vol)BPE. carotenoids -carotene and -cryptoxanthin, but also to When the cells reached confluence, they were subcultured in either 24- non-provitamin A carotenoids lutein, zeaxanthin, and well plates or 12-well plates in the same medium. After subculturing, astaxanthin (Fig. 1a). In contrast, lycopene, phytoene, the cells were confluent and the medium was exchanged for an identical medium, except that hydrocortisone and EGF were depleted -ionone, and -ionone did not exhibit significant and BPE was reduced to a concentration of 0.04%. Agents were added to the medium and cultured for the time of indicated in the legends to the figures. The conditioned media of the 24-well plates were assayed a b for hyaluronan production, and the cells were used in RT-PCR HAS3 analyses. The cells of the 12-well plates were used in secreted alkaline HAS3 phosphatase (SEAP) reporter assays. G3PDH G3PDH RT-PCR. Total RNA from the cultured cells was extracted using ** 1200 1200 TRIzol reagent (Invitrogen, Carlsbad, CA) folloing the manufacturer’s *** **
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