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UVB-Induced Conversion of 7-Dehydrocholesterol to 1Α,25-Dihydroxyvitamin D3 in an in Vitro Human Skin Equivalent Model

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UVB-Induced Conversion of 7-Dehydrocholesterol to 1Α,25-Dihydroxyvitamin D3 in an in Vitro Human Skin Equivalent Model View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Elsevier - Publisher Connector UVB-Induced Conversion of 7-Dehydrocholesterol to 1a,25- Dihydroxyvitamin D3 in an In Vitro Human Skin Equivalent Model Bodo Lehmann, Thurid Genehr, Peter Knuschke, Jens Pietzsch,* and Michael Meurer Department of Dermatology, *Institute and Policlinic of Clinical Metabolic Research, Carl Gustav Carus Medical School, Dresden University of Technology, Germany We have previously shown that keratinocytes in vitro hydroxyvitamin D3, and ultimately calcitriol in the can convert biologically inactive vitamin D3 to the femtomolar range. Unirradiated cultures and irradi- hormone calcitriol (1a,25-dihydroxyvitamin D3). ated cultures without keratinocytes generated no cal- This study was initiated to test whether the ultra- citriol. Irradiation of skin equivalents at wavelengths violet-B-induced photolysis of provitamin D3 (7-de- > 315 nm generated no or only trace amounts of cal- hydrocholesterol), which results in the formation of citriol. The ultraviolet-B-triggered conversion of vitamin D3, can generate calcitriol in an in vivo-like 7-dehydrocholesterol to calcitriol was strongly human skin equivalent model made of ®broblasts in inhibited by ketoconazole indicating the involvement a collagen matrix as the dermal component and of P450 mixed function oxidases. The amount of cal- keratinocytes as the epidermal component. Cultures citriol generated was dependent on the 7-dehydro- were preincubated with increasing concentrations cholesterol concentration, on wavelength, and on of 7-dehydrocholesterol (0.53±5.94 nmol per cm2 ultraviolet B dose. Hence, keratinocytes in the pres- human skin equivalent) at 37°C and irradiated with ence of physiologic concentrations of 7-dehydro- monochromatic ultraviolet B at wavelengths ranging cholesterol and irradiated with therapeutic doses of from 285 to 315 nm (effective ultraviolet doses 7.5± ultraviolet B may be a potential source of biologic- 45 mJ per cm2). In our in vitro model irradiation ally active calcitriol within the epidermis. Key words: with ultraviolet B resulted in a sequential metabolic keratinocyte/metabolism/vitamin D3. J Invest Dermatol process with generation of previtamin D3 followed 117:1179±1185, 2001 by the time-dependent formation of vitamin D3, 25- alcitriol (1a,25-dihydroxyvitamin D3,1a,25(OH)2- exogenous calcidiol (25-hydroxyvitamin D3, 25OHD3) to calcitriol D3), the most potent biologically active form of (Bikle et al, 1986; Matsumoto et al, 1991; Lehmann, 1997) and we vitamin D3 (VD3), is produced by a cascade of have previously demonstrated that keratinocytes can convert reactions including photochemical synthesis of VD3 in exogenous alphacalcidol (1a-hydroxyvitamin D3,1a-OHD3) and Cthe skin and after release into the circulation VD to calcitriol (Lehmann et al, 1998; 2000a) implicating 3 subsequent hydroxylation at the C25 atom in the liver and at the functionally active 1a- and 25-hydroxylases present in keratino- C-1a position in the kidney (Haussler, 1986). Calcitriol and other cytes. Provitamin D3 (7-dehydrocholesterol, 7-DHC) exposed to vitamin D analogs have antiproliferative and prodifferentiative ultraviolet B (UVB) radiation (spectral range 290±315 nm) converts effects on epidermal keratinocytes (Hosomi et al, 1983; Smith et al, in vivo (Holick et al, 1980) and in vitro (Nemanic et al, 1985) to 1986; McLane et al, 1990) and have become potent therapeutic previtamin D3 (pre-VD3), which in turn isomerizes to VD3. Until agents for the treatment of proliferative skin disorders such as now, the complete pathway from 7-DHC to 1a,25(OH)2D3 has psoriasis. It has been shown that cultured keratinocytes can convert only been shown in the transformed cell line HaCaT (Lehmann et al, 2000b) and not under in vivo-like conditions. Furthermore, the question of possible intermediate products on the pathway from Manuscript received January 8, 2001; revised May 29, 2001; accepted for VD3 to 1a,25(OH)2D3 remains unanswered. It was the aim of this publication July 19, 2001. study to demonstrate that photolysis of 7-DHC results in the Reprint requests to: Dr. Bodo Lehmann, Carl Gustav Carus Medical formation of 1a,25(OH) D not only in HaCaT cells but also in an School, Dresden University of Technology, Department of Dermatology, 2 3 Fetscherstrasse 74, D-01307 Dresden, Germany. Email: Bodo.lehmann@ in vivo-like human skin equivalent (HSE) model. Our skin mailbox.tu-dresden.de equivalent culture system consists of ®broblasts in a collagen matrix as the dermal component and keratinocytes as the epidermal Abbreviations: 1a,25(OH)2D3, 1a,25-dihydroxyvitamin D3; 1a- OHD3, 1a-hydroxyvitamin D3; Deff, effective ultraviolet B dose; 7- component (Bell et al, 1981; Prunieras et al, 1983). DHC, 7-dehydrocholesterol; Ee, irradiance; GC-MS, gas chromatogra- phy±mass spectrometry; HSE, human skin equivalent; 19-nor,10-keto- MATERIALS AND METHODS 25OHD3, 19-nor,10-keto-25-hydroxyvitamin D3; pre-VD3, previtamin D3; 25OHD3, 25-hydroxyvitamin D3; VD3, vitamin D3; VDR, vitamin D Chemicals and reagents Dulbecco's modi®ed Eagle's medium receptor. (DMEM) and fetal bovine serum were provided from Gibco 0022-202X/01/$15.00 ´ Copyright # 2001 by The Society for Investigative Dermatology, Inc. 1179 1180 LEHMANN ET AL THE JOURNAL OF INVESTIGATIVE DERMATOLOGY (Eggenstein, Germany). Keratinocyte growth medium (KGM) and 6±8) and 1a,25(OH)2D3 (fraction number 20±22) were collected and, keratinocyte basal medium (KBM) were purchased from Clonetics (San after drying, analyzed for calcidiol [gas chromatography±mass Diego, CA). Culture dishes (® 30 mm) were from Falcon (Heidelberg, spectrometry (GC-MS)] and calcitriol (GC-MS and radioreceptor assay). Germany). 1a,25(OH)2D3 was kindly provided by Hoffmann-La Roche In reversed phase (RP) HPLC the calcitriol generated was identi®ed by 3 3 3 ã (Basel, Switzerland). 25-hydroxy[26,27-methyl- H]vitamin D3 ( H- cochromatography of the H-labeled standard using a Hibar column, 3 25OHD3, 177 Ci per mmol), 1a,25-dihydroxy[26,27-methyl- H]vitamin 250-4, LiChrospher 100RP-18, 5 mm (Merck, Darmstadt, Germany), 3 D3 ( H-1a,25(OH)2D3, 173.5 Ci per mmol), and 24R,25-dihydroxy- with solvent system 3 (methanol:water 85:15 vol/vol, ¯ow rate 1 ml per 3 3 [26,27-methyl- H]vitamin D3 ( H-24R,25(OH)2D3, 170 Ci per mmol) min). Calcitriol-containing fractions were dried and analyzed for their were purchased from Amersham, Braunschweig, Germany. The content of calcitriol. Concentrations of VD3 and calcitriol were corrected 1a,25(OH)2D3-radioreceptor assay kit from Nichols Institute (Bad for their recoveries [VD3 (500 pmol), 63.69% 6 4.61%, N = 5; calcitriol 2 Nauheim, Germany) was used. VD3 solvents for high performance liquid (720 fmol), 50.11% 6 4.87%, N = 5) and normalized to 1 cm HSE. chromatography (HPLC) (n-hexane, 2-propanol, and methanol) were GC-MS The dried HPLC fractions containing 25OHD or provided by Merck (Darmstadt, Germany). Lumisterol and tachysterol 3 1a,25(OH)2D3 were derivatized to the trimethylsilyl ether derivatives were donated by Dr. A. Kissmeyer (Leo Pharmaceutical Products, and analyzed by GC-MS. The samples were treated with 40 ml of Ballerup, Denmark). Ketoconazole was bought from Paesel & Lorei MSTFA:BSA:TMCS:TMSI (10:5:5:2, vol/vol) at 95°C for 45 min. One (Frankfurt/M, Germany). Bovine serum albumin (BSA), purity > 99% microliter of the derivatized sample was directly and manually injected (product number A 0281), and 7-DHC were from Sigma (Deisenhofen, into a model 5890/II gas chromatograph equipped with a 25 m 3 0.2 Germany). Scintillation cocktail, Ready Protein+, was purchased from mm HP-1 capillary column (cross-linked methylsiloxane, 0.33 mm) and Beckman Instruments (Fullerton). N,O-bis(trimethylsilyl) acetamide interfaced with a model 5989 A MS-Engine (Hewlett-Packard, Palo (BSA), N-methyl-N-(trimethylsilyl) tri¯uoroacetamide (MSTFA), N- Alto, CA). GC conditions were the following: carrier gas, helium; trimethylsilylimidazole (TMSI), and trimethylchlorosilane (TMCS) were column head pressure, 10 psi; injector temperature, 260°C; oven purchased from Macherey-Nagel (Dueren, Germany). Pre-VD3 was temperature gradient, maintained at 200°C for 1 min, increased to prepared by thermal treatment of an ethanolic solution of VD3 (1.0 mg 260°C at 30°C per min, then increased to 300°C at 20°C per min, held per ml) at 60°C for 16 h under nitrogen according to the literature (Isler at 300°C for 10 min; interface temperature, 300°C. Electron impact MS and Brubacher, 1982). VD3 (retention time 10.57 min) and generated conditions were the following: source temperature, 250°C; analyzer pre-VD3 (retention time 8.22 min) were separated by normal phase (NP) temperature, 120°C; energy, 70 eV. All samples were run in triplicate HPLC (eluent 1, see HPLC analysis). Pre-VD3 was fractionated from under the control of the HP-ChemStation data system. For selective ion 8.00 to 9.00 min. The UV spectrum of pre-D3 (lmax 260 nm, lmin monitoring, the most abundant ions at m/z 452 and m/z 501 were 230 nm) was identical to that described in the literature (Holick et al, monitored for 1a,25(OH) D . The most abundant ion at m/z 439 was 1977). 2 3 monitored for 25OHD3. Preparation of the HSE model Keratinocytes from the epidermis of Statistical analysis Results are presented as mean or mean 6 SD. normal skin from young patients undergoing plastic surgery were used as Data were analyzed by one-way analysis of variance (Bonferroni second-passage cells. Dermal ®broblasts from the same patients were method). cultured in DMEM supplemented with 10% (vol/vol) fetal bovine serum. The ®broblasts were embedded in rat tail collagen type 1 lattices 2 d before the keratinocytes were inoculated onto the gel matrix in the RESULTS culture dishes at a density of 4 3 104 per cm2.
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