UVB-induced production of 1,25-dihydroxyvitamin D3 and vitamin D activity in human keratinocytes pretreated with a sterol Δ7- reductase inhibitor

Journal of Cellular Biochemistry

Volumn 98, Issue 1, 2006, Pages 81-92

  Vantieghem, Katleen ^a   Kissmeyer, Anne Marie ^b   De Haes, Petra ^a   Bouillon, Roger ^a,c   Segaert, Siegfried ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b LEO PHARMA A S   (Denmark)

^c LEGENDO   (Belgium)

Author keywords

1,25 dihydroxyvitamin D3; Keratinocyte; Ultraviolet B; Vitamin D3

Indexed keywords

4 [2 [1 (4 CHLOROCINNAMYL) 4 PIPERAZINYL]ETHYL]BENZOIC ACID; 7 DEHYDROCHOLESTEROL; CALCITRIOL; CYTOCHROME P450 INHIBITOR; KETOCONAZOLE; MESSENGER RNA; OXIDOREDUCTASE INHIBITOR; OXYGENASE; STEROL DELTA7 REDUCTASE INHIBITOR; UNCLASSIFIED DRUG; VITAMIN D; VITAMIN D 24 HYDROXYLASE; VITAMIN D BINDING PROTEIN; VITAMIN D RECEPTOR;

ARTICLE; AUTOCRINE EFFECT; BIOTRANSFORMATION; CONTROLLED STUDY; ENDOCRINE SYSTEM; ENZYME INHIBITION; EPIDERMIS; GENE ACTIVATION; GENETIC TRANSFECTION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HOMOGENATE; HUMAN; HUMAN CELL; KERATINOCYTE; NORMAL HUMAN; PARACRINE SIGNALING; PRIORITY JOURNAL; TANDEM MASS SPECTROMETRY; ULTRAVIOLET B RADIATION; VITAMIN D RESPONSIVE ELEMENT;

CALCITRIOL; CELL LINE, TRANSFORMED; EPIDERMIS; HUMANS; KERATINOCYTES; OXIDOREDUCTASES ACTING ON CH-CH GROUP DONORS; PIPERAZINES; ULTRAVIOLET RAYS; VITAMIN D;

EID: 33645973682     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.20756     Document Type: Article

References (80)

1. Andersson S, Davis DL, Dahlback H, Jornvall H, Russell DW. 1989. Cloning, structure, and expression of the mitochondrial cytochrome P-450 sterol 26-hydroxylase, a bile acid biosynthetic enzyme. J Biol Chem 264:8222-8229.
2. Bikle DD, Gee E. 1989. Free, and not total, 1,25-dihydroxyvitamin D regulates 25-hydroxyvitamin D metabolism by keratinocytes. Endocrinology 124:649-654.
3. Bikle DD, Pillai S. 1988. Vitamin D metabolite production and function in keratinocytes. Ann NY Acad Sci 548: 27-44.
4. Bikle DD, Pillai S. 1993. Endocr Rev 14:3-19.
5. Bikle DD, Nemanic MK, Gee E, Elias P. 1986a. 1,25-Dihydroxyvitamin D3 production by human keratinocytes. Kinetics and regulation. J Clin Invest 78:557-566.
6. Bikle DD, Nemanic MK, Whitney JO, Elias PW. 1986b. Neonatal human foreskin keratinocytes produce 1,25-dihydroxyvitamin D3. Biochemistry 25:1545-1548.
7. Bikle DD, Chang S, Crumrine D, Elalieh H, Man MQ, Choi EH, Dardenne O, Xie Z, Arnaud RS, Feingold K, Elias PM. 2004. 25 Hydroxyvitamin D 1 alpha-hydroxylase is required for optimal epidermal differentiation and permeability barrier homeostasis. J Invest Dermatol 122: 984-992.
8. Blunt JW, DeLuca HF, Schnoes HK. 1968. 25-hydroxycholecalciferol. A biologically active metabolite of vitamin D3. Biochemistry 7:3317-3322.
9. Bouillon R, Van Baelen H, De Moor P. 1980. Comparative study of the affinity of the serum vitamin D-binding protein. J Steroid Biochem 13:1029-1034.
10. Bouillon R, Okamura WH, Norman AW. 1995. Structure-function relationships in the vitamin D endocrine system. Endocr Rev 16:200-257.
11. Chen KS, Prahl JM, DeLuca HF. 1993. Isolation and expression of human 1,25-dihydroxyvitamin D3 24-hydroxylase cDNA. Proc Natl Acad Sci USA 90:4543-4547.
12. Chen ML, Heinrich G, Ohyama YI, Okuda K, Omdahl JL, Chen TC, Holick MF. 1994. Expression of 25-hydroxyvitamin D3-24-hydroxylase mRNA in cultured human keratinocytes. Proc Soc Exp Biol Med 207:57-61.
13. Cheng JB, Motola DL, Mangelsdorf DJ, Russell DW. 2003. De-orphanization of cytochrome P450 2R1: A microsomal vitamin D 25-hydroxilase. J Biol Chem 278:38084-38093.
14. Cheng JB, Levine MA, Bell NH, Mangelsdorf DJ, Russell DW. 2004. Genetic evidence that the human CYP2R1 enzyme is a key vitamin D 25-hydroxylase. Proc Natl Acad Sci USA 101:7711-7715.
15. Clydesdale GJ, Dandie GW, Muller HK. 2001. Ultraviolet light induced injury: Immunological and inflammatory effects. Immunol Cell Biol 79:547-568.
16. Courtois SJ, Segaert S, Degreef H, Bouillon R, Garmyn M. 1998. Ultraviolet B suppresses vitamin D receptor gene expression in keratinocytes. Biochem Biophys Res Commun 246:64-69.
17. Dam TN, Moller B, Hindkjaer J, Kragballe K. 1996. The vitamin D3 analog calcipotriol suppresses the number and antigen-presenting function of Langerhans cells in normal human skin. J Investig Dermatol Symp Proc 1: 72-77.
18. Dawson-Hughes B, Heaney RP, Holick MF, Lips P, Meunier PJ, Vieth R. 2005. Estimates of optimal vitamin D status. Osteoporos Int.
19. De Haes P, Garmyn M, Degreef H, Vantieghem K, Bouillon R, Segaert S. 2003. 1,25-Dihydroxyvitamin D3 inhibits ultraviolet B-induced apoptosis, Jun kinase activation, and interleukin-6 production in primary human keratinocytes. J Cell Biochem 89:663-673.
20. De Haes P, Garmyn M, Verstuyf A, De Clercq P, Vandewalle M, Degreef H, Vantieghem K, Bouillon R, Segaert S. 2005. 1,25-Dihydroxyvitamin D(3) and analogues protect primary human keratinocytes against UVB-induced DNA damage. J Photochem Photobiol B 78:141-148.
21. Delvin EE, Arabian A, Glorieux FH, Mamer OA. 1985. In vitro metabolism of 25-hydroxycholecalciferol by isolated cells from human decidua. J Clin Endocrinol Metab 60: 880-885.
22. Friedrich M, Villena-Heinsen C, Axt-Fliedner R, Meyberg R, Tilgen W, Schmidt W, Reichrath J. 2002. Analysis of 25-hydroxyvitamin D3-1alpha- hydroxylase in cervical tissue. Anticancer Res 22:183-186.
23. Fu GK, Lin D, Zhang MY, Bikle DD, Shackleton CH, Miller WL, Portale AA. 1997. Cloning of human 25-hydroxyvitamin D-1 alpha-hydroxylase and mutations causing vitamin D-dependent rickets type 1. Mol Endocrinol 11: 1961-1970.
24. Gibbs S, Lohman F, Teubel W, van de PP, Backendorf C. 1990. Characterization of the human spr2 promoter: Induction after UV irradiation or TPA treatment and regulation during differentiation of cultured primary keratinocytes. Nucleic Acids Res 18:4401-4407.
25. Gibbs S, Fijneman R, Wiegant J, van Kessel AG, van de PP, Backendorf C. 1993. Molecular characterization and evolution of the SPRR family of keratinocyte differentiation markers encoding small proline-rich proteins. Genomics 16:630-637.
26. Gilchrest BA, Park HY, Eller MS, Yaar M. 1996. Mechanisms of ultraviolet light-induced pigmentation. Photochem Photobiol 63:1-10.
27. Hansson M, Ellis E, Hunt MC, Schmitz G, Babiker A. 2003. Marked induction of sterol 27-hydroxylase activity and mRNA levels during differentiation of human cultured monocytes into macrophages. Biochim Biophys Acta 1593:283-289.
28. Holick MF. 1988. Skin: Site of the synthesis of vitamin D and a target tissue for the active form, 1,25-dihydroxyvitamin D3. Ann NY Acad Sci 548:14-26.
29. Holick MF. 2001. Sunlight "D"ilemma: Risk of skin cancer or bone disease and muscle weakness. Lancet 357:4-6.
30. Holick MF. 2003. Vitamin D: A millenium perspective. J Cell Biochem 88:296-307.
31. Holick MF. 2004. Sunlight and vitamin D for bone health and prevention of autoimmune diseases, cancers, and cardiovascular disease. Am J Clin Nutr 80:1678S-1688S.
32. Holick MF, MacLaughlin JA, Clark MB, Holick SA, Potts JT Jr, Anderson RR, Blank IH, Parrish JA, Elias P. 1980. Photosynthesis of previtamin D3 in human skin and the physiologic consequences. Science 210:203-205.
33. Howard GA, Turner RT, Sherrard DJ, Baylink DJ. 1981. Human bone cells in culture metabolize 25-hydroxyvitamin D3 to 1,25-dihydroxyvitamin D3 and 24,25-dihydroxyvitamin D3. J Biol Chem 256:7738-7740.
34. Ichikawa F, Sato K, Nanjo M, Nishii Y, Shinki T, Takahashi N, Suda T. 1995. Mouse primary osteoblasts express vitamin D3 25-hydroxylase mRNA and convert 1 alpha-hydroxyvitamin D3 into 1 alpha,25-dihydroxyvitamin D3. Bone 16:129-135.
35. Kitano Y, Okada N. 1983. Separation of the epidermal sheet by dispase. Br J Dermatol 108:555-560.
36. Kricker A, Armstrong BK, English DR, Heenan PJ. 1995. A dose-response curve for sun exposure and basal cell carcinoma. Int J Cancer 60:482-488.
37. Lawson DE, Fraser DR, Kodicek E, Morris HR, Williams DH. 1971. Identification of 1,25-dihydroxycholecalciferol, a new kidney hormone controlling calcium metabolism. Nature 230:228-230.
38. Lehmann B. 1997. HaCaT cell line as a model system for vitamin D3 metabolism in human skin. J Invest Dermatol 108:78-82.
39. Lehmann B, Tiebel O, Meurer M. 1999. Expression of vitamin D3 25-hydroxylase (CYP27) mRNA after induction by vitamin D3 or UVB radiation in keratinocytes of human skin equivalents-A preliminary study. Arch Dermatol Res 291:507-510.
40. Lehmann B, Knuschke P, Meurer M. 2000. UVB-induced conversion of 7-dehydrocholesterol to 1 alpha,25-dihydroxyvitamin D3 (calcitriol) in the human keratinocyte line HaCaT. Photochem Photobiol 72:803-809.
41. Lehmann B, Genehr T, Knuschke P, Pietzsch J, Meurer M. 2001. UVB-induced conversion of 7-dehydrocholesterol to 1alpha,25-dihydroxyvitamin D3 in an in vitro human skin equivalent model. J Invest Dermatol 117:1179-1185.
42. Lehmann B, Sauter W, Knuschke P, Dressler S, Meurer M. 2003. Demonstration of UVB-induced synthesis of 1 alpha,25-dihydroxyvitamin D3 (calcitriol) in human skin by microdialysis. Arch Dermatol Res 295:24-28.
43. Lehmann B, Knuschke P, Meurer M. 2005. Effect of UVB radiation emitted from the narrowband TL-01 lamp (311 nm) on the calcitriol synthesis in organotypic cultures of keratinocytes. Experimental Dermatology 14:153.
44. Li YC, Pirro AE, Amling M, Delling G, Baron R, Bronson R, Demay MB. 1997. Targeted ablation of the vitamin D receptor: An animal model of vitamin D-dependent rickets type II with alopecia. Proc Natl Acad Sci USA 94:9831-9835.
45. Lips P. 2004. Which circulating level of 25-hydroxyvitamin D is appropriate? J Steroid Biochem Mol Biol 89-90:611-614.
46. MacLaughlin J, Holick MF. 1985. Aging decreases the capacity of human skin to produce vitamin D3. J Clin Invest 76:1536-1538.
47. Makin G, Lohnes D, Byford V, Ray R, Jones G. 1989. Target cell metabolism of 1,25-dihydroxyvitamin D3 to calcitroic acid. Evidence for a pathway in kidney and bone involving 24-oxidation. Biochem J 262:173-180.
48. Malloy PJ, Pike JW, Feldman D. 1999. The vitamin D receptor and the syndrome of hereditary 1,25-dihydroxyvitamin D-resistant rickets. Endocr Rev 20:156-188.
49. Matsumura Y, Ananthaswamy HN. 2004. Toxic effects of ultraviolet radiation on the skin. Toxicol Appl Pharmacol 195:298-308.
50. Mawer EB, Backhouse J, Holman CA, Lumb GA, Stanbury SW. 1972. The distribution and storage of vitamin D and its metabolites in human tissues. Clin Sci 43:413-431.
51. Monkawa T, Yoshida T, Hayashi M, Saruta T. 2000. Identification of 25-hydroxyvitamin D3 1alpha-hydroxylase gene expression in macrophages. Kidney Int 58: 559-568.
52. Morris JG. 1999. Ineffective vitamin D synthesis in cats is reversed by an inhibitor of 7-dehydrocholestrol-delta7-reductase. J Nutr 129:903-908.
53. Nemanic MK, Whitney J, Elias PM. 1985. In vitro synthesis of vitamin D-3 by cultured human keratinocytes and fibroblasts: Action spectrum and effect of AY-9944. Biochim Biophys Acta 841:267-277.
54. Norman AW. 1998. Sunlight, season, skin pigmentation, vitamin D, and 25-hydroxyvitamin D: Integral components of the vitamin D endocrine system. Am J Clin Nutr 67:1108-1110.
55. Nykjaer A, Fyfe JC, Kozyraki R, Leheste JR, Jacobsen C, Nielsen MS, Verroust PJ, Aminoff M, de la CA, Moestrup SK, Ray R, Gliemann J, Willnow TE, Christensen EI. 2001. Cubilin dysfunction causes abnormal metabolism of the steroid hormone 25(OH) vitamin D(3). Proc Natl Acad Sci USA 98:13895-13900.
56. Obi-Tabot ET, Tian XQ, Chen TC, Holick MF. 2000. A human skin equivalent model that mimics the photo-production of vitamin D3 in human skin. In Vitro Cell Dev Biol Anim 36:201-204.
57. Pascussi JM, Robert A, Nguyen M, Walrant-Debray O, Garabedian M, Martin P, Pineau T, Saric J, Navarro F, Maurel P, Vilarem MJ. 2005. Possible involvement of pregnane X receptor-enhanced CYP24 expression in drug-induced osteomalacia. J Clin Invest 115:177-186.
58. Prystowsky JH, Muzio PJ, Sevran S, Clemens TL. 1996. Effect of UVB phototherapy and oral calcitriol (1,25-dihydroxyvitamin D3) on vitamin D photosynthesis in patients with psoriasis. J Am Acad Dermatol 35:690-695.
59. Quack M, Szafranski K, Rouvinen J, Carlberg C. 1998. The role of the T-box for the function of the vitamin D receptor on different types of response elements. Nucleic Acids Res 26:5372-5378.
60. Rosenstreich SJ, Rich C, Volwiler W. 1971. Deposition in and release of vitamin D3 from body fat: Evidence for a storage site in the rat. J Clin Invest 50:679-687.
61. Schoenmakers E, Verrijdt G, Peeters B, Verhoeven G, Rombauts W, Claessens F. 2000. Differences in DNA binding characteristics of the androgen and glucocorticoid receptors can determine hormone-specific responses. J Biol Chem 275:12290-12297.
62. Schuessler M, Astecker N, Herzig G, Vorisek G, Schuster I. 2001. Skin is an autonomous organ in synthesis, two-step activation and degradation of vitamin D(3): CYP27 in epidermis completes the set of essential vitamin D(3)-hydroxylases. Steroids 66:399-408.
63. Schwartz GG, Whitlatch LW, Chen TC, Lokeshwar BL, Holick MF. 1998. Human prostate cells synthesize 1,25-dihydroxyvitamin D3 from 25-hydroxyvitamin D3. Cancer Epidemiol Biomarkers Prev 7:391-395.
64. Segaert S. 1998. Vitamin D and regulation of gene expression. Curr Opin Clin Nutr Metab Care 1:347-354.
65. Segaert S, Garmyn M, Degreef H, Bouillon R. 1997. Retinoic acid modulates the anti-proliferative effect of 1,25-dihydroxyvitamin D3 in cultured human epidermal keratinocytes. J Invest Dermatol 109:46-54.
66. Segaert S, Degreef H, Bouillon R. 2000a. Vitamin D receptor expression is linked to cell cycle control in normal human keratinocytes. Biochem Biophys Res Commun 279:89-94.
67. Segaert S, Garmyn M, Degreef H, Bouillon R. 2000b. Suppression of vitamin D receptor and induction of retinoid X receptor alpha expression during squamous differentiation of cultured keratinocytes. J Invest Dermatol 114:494-501.
68. Segersten U, Correa P, Hewison M, Hellman P, Dralle H, Carling T, Akerstrom G, Westin G. 2002. 25-hydroxyvitamin D(3)-lalpha-hydroxylase expression in normal and pathological parathyroid glands. J Clin Endocrinol Metab 87:2967-2972.
69. Sesto A, Navarro M, Burslem F, Jorcano JL. 2002. Analysis of the ultraviolet B response in primary human keratinocytes using oligonucleotide microarrays. Proc Natl Acad Sci USA 99:2965-2970.
70. Shefer S, Salen G, Honda A, Batta AK, Nguyen LB, Tint GS, Ioannou YA, Desnick R. 1998. Regulation of rat hepatic 3beta-hydroxysterol delta7-reductase: Substrate specificity, competitive and non-competitive inhibition, and phosphorylation/dephosphorylation. J Lipid Res 39: 2471-2476.
71. Takada K. 1983. Formation of fatty acid esterified vitamin D3 in rat skin by exposure to ultraviolet radiation. J Lipid Res 24:441-448.
72. Taylor CR, Sober AJ. 1996. Sun exposure and skin disease. Annu Rev Med 47:181-191.
73. Usui E, Noshiro M, Okuda K. 1990. Molecular cloning of cDNA for vitamin D3 25-hydroxylase from rat liver mitochondria. FEBS Lett 262:135-138.
74. Van Baelen H, Bouillon R, De Moor P. 1980. Vitamin D-binding protein (Gc-globulin) binds actin. J Biol Chem 255:2270-2272.
75. van de Kerkhof PC. 1995. Biological activity of vitamin D analogues in the skin, with special reference to anti-psoriatic mechanisms. Br J Dermatol 132:675-682.
76. Vieth R. 2004. Why the optimal requirement for vitamin D3 is probably much higher than what is officially recommended for adults. J Steroid Biochem Mol Biol 89-90: 575-579.
77. Xie Z, Komuves L, Yu QC, Elalieh H, Ng DC, Leary C, Chang S, Crumrine D, Yoshizawa T, Kato S, Bikle DD. 2002. Lack of the vitamin D receptor is associated with reduced epidermal differentiation and hair follicle growth. J Invest Dermatol 118:11-16.
78. Yoshizawa T, Handa Y, Uematsu Y, Takeda S, Sekine K, Yoshihara Y, Kawakami T, Arioka K, Sato H, Uchiyama Y, Masushige S, Fukamizu A, Matsumoto T, Kato S. 1997. Mice lacking the vitamin D receptor exhibit impaired bone formation, uterine hypoplasia and growth retardation after weaning. Nat Genet 16:391-396.
79. Zehnder D, Bland R, Williams MC, McNinch RW, Howie AJ, Stewart PM, Hewison M. 2001. Extrarenal expression of 25-hydroxyvitamin d(3)-1 alpha-hydroxylase. J Clin Endocrinol Metab 86:888-894.
80. Zittermann A. 2003. Vitamin D in preventive medicine: Are we ignoring the evidence? Br J Nutr 89:552-572.