β-carotene inhibits UVA-induced matrix metalloprotease 1 and 10 expression in keratinocytes by a singlet oxygen-dependent mechanism

Free Radical Biology and Medicine

Volumn 37, Issue 5, 2004, Pages 654-670

  Wertz, Karin ^a   Seifert, Nicole ^a   Hunziker, Petra Buchwald ^a   Riss, Georges ^a   Wyss, Adrian ^a   Lankin, Christopher ^a   Goralczyk, Regina ^a  

^a DSM NUTRITIONAL PRODUCTS LTD   (Switzerland)

Author keywords

Carotene; CT; CT; Free radicals; Matrix metalloprotease; Photoprotection; Retinoic acid; Skin aging; threshold cycle: first PCR cycle in which amplification signal is detected

Indexed keywords

ALPHA TOCOPHEROL; BETA CAROTENE; INTERSTITIAL COLLAGENASE; OXYGEN; RETINOIC ACID; RETINOIC ACID RECEPTOR BETA; RETINOID X RECEPTOR; SINGLET OXYGEN; STROMELYSIN; STROMELYSIN 2;

ARTICLE; CELL CULTURE; CONCENTRATION RESPONSE; CONTROLLED STUDY; GENE CONTROL; HUMAN; HUMAN CELL; INSTRUMENTATION; KERATINOCYTE; LIGHT DAMAGE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REPORTER GENE; ULTRAVIOLET A RADIATION; UPREGULATION;

ANALYSIS OF VARIANCE; ANTIOXIDANTS; BASE SEQUENCE; BETA CAROTENE; BIOLOGICAL TRANSPORT; CELL LINE; DNA PRIMERS; EPIDERMIS; HUMANS; KERATINOCYTES; MATRIX METALLOPROTEINASE 1; MATRIX METALLOPROTEINASE 10; METALLOENDOPEPTIDASES; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA; SINGLET OXYGEN; SUNLIGHT; ULTRAVIOLET RAYS;

EID: 3342896728     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2004.05.018     Document Type: Article

References (116)

1. Berneburg M., Clingen P.H., Harcourt S.A., Lowe J.E., Taylor E.M., Green M.H., Krutmann J., Arlett C.F., Lehmann A.R. The cancer-free phenotype in trichothi odystrophy is unrelated to its repair defect. Cancer Res. 60:2000;431-438
2. Kligman A.M. Early destructive effect of sunlight on human skin. JAMA. 210:1969;2377-2380
3. Solar and UV radiation. 1992;IARC, Lyon
4. Freeman R.G. Data on the action spectrum for ultraviolet carcinogenesis. J. Natl. Cancer Inst. 55:1975;1119-1122
5. Tyrrell R.M. Activation of mammalian gene expression by the UV component of sunlight: from models to reality. Bioessays. 18:1996;139-148
6. Tyrrell R.M. UV activation of mammalian stress proteins. EXS. 77:1996;255-271
7. Yasui H., Sakurai H. Chemiluminescent detection and imaging of reactive oxygen species in live mouse skin exposed to UVA. Biochem. Biophys. Res. Commun. 269:2000;131-136
8. Black H.S. Potential involvement of free radical reactions in ultraviolet light-mediated cutaneous damage. Photochem. Photobiol. 46:1987;213-221
9. Dalle Carbonare M., Pathak M.A. Skin photosensitizing agents and the role of reactive oxygen species in photoaging. J. Photochem. Photobiol. B. 14:1992;105-124
10. Grether-Beck S., Krutmann J. Gene regulation by ultraviolet A radiation and singlet oxygen. Methods Enzymol. 319:2000;280-290
11. Basu-Modak S., Tyrrell R.M. Singlet oxygen: a primary effector in the ultraviolet A/near-visible light induction of the human heme oxygenase gene. Cancer Res. 53:1993;4505-4510
12. Scharffetter-Kochanek K., Wlaschek M., Briviba K., Sies H. Singlet oxygen induces collagenase expression in human skin fibroblasts. FEBS Lett. 331:1993;304-306
13. Wlaschek M., Briviba K., Stricklin G.P., Sies H., Scharffetter-Kochanek K. Singlet oxygen may mediate the ultraviolet A-induced synthesis of interstitial collagenase. J. Invest. Dermatol. 104:1995;194-198
14. Keyse S.M., Tyrrell R.M. Heme oxygenase is the major 32-kDa stress protein induced in human skin fibroblasts by UVA radiation, hydrogen peroxide, and sodium arsenite. Proc. Natl. Acad. Sci. U S A. 86:1989;99-103
15. Wlaschek M., Heinen G., Poswig A., Schwarz A., Krieg T., Scharffetter-Kochanek K. UVA-induced autocrine stimulation of fibroblast-derived collagenase/MMP-1 by interrelated loops of interleukin-1 and interleukin-6. Photochem. Photobiol. 59:1994;550-556
16. Grether-Beck S., Olaizola-Horn S., Schmitt H., Grewe M., Jahnke A., Johnson J.P., Briviba K., Sies H., Krutmann J. Activation of transcription factor AP-2 mediates UVA radiation- and singlet oxygen-induced expression of the human intercellular adhesion molecule 1 gene. Proc. Natl. Acad. Sci. USA. 93:1996;14586-14591
17. Foote C.S. Mechanisms of photosensitized oxidation: there are several different types of photosensitized oxidation which may be important in biological systems. Science. 162:1968;963-970
18. Merkel P., Nilsson R., Kearns D.R. Deuterium effects on singlet oxygen lifetime in solutions: a new test of singlet oxygen reactions. J. Am. Chem. Soc. 94:1972;1030-1031
19. Truscott T. The photophysics and photochemistry of the carotenoids. J. Photochem. Photobiol. B. 6:1990;359-371
20. Conn P.F., Lambert C., Land E.J., Schalch W., Truscott T.G. Carotene-oxygen radical interactions. Free Radic. Res. Commun. 16:1992;401-408
21. Conn P.F., Schalch W., Truscott T.G. The singlet oxygen and carotenoid interaction. J. Photochem. Photobiol. B. 11:1991;41-47
22. Vahlquist A., Lee J.B., Michaelsson G., Rollman O. Vitamin A in human skin: II. Concentrations of carotene, retinol and dehydroretinol in various components of normal skin. J. Invest. Dermatol. 79:1982;94-97
23. Lee R., Mathews-Roth M.M., Pathak M.A., Parrish J.A. The detection of carotenoid pigments in human skin. J. Invest. Dermatol. 64:1975;175-177
24. Biesalski H.K., Hemmes C., Hopfenmuller W., Schmid C., Gollnick H.P. Effects of controlled exposure of sunlight on plasma and skin levels of beta-carotene. Free Radic. Res. 24:1996;215-224
25. Davison P.A., Hunter C.N., Horton P. Overexpression of beta-carotene hydroxylase enhances stress tolerance in Arabidopsis. Nature. 418:2002;203-206
26. Mathews-Roth M.M., Pathak M.A., Parrish J., Fitzpatrick T.B., Kass E.H., Toda K., Clemens W. A clinical trial of the effects of oral beta-carotene on the responses of human skin to solar radiation. J. Invest. Dermatol. 59:1972;349-353
27. Mathews-Roth M.M., Pathak M.A., Fitzpatrick T.B., Harber L.H., Kass E.H. Beta carotene therapy for erythropoietic protoporphyria and other photosensitivity diseases. Arch. Dermatol. 113:1977;1229-1232
28. Mathews-Roth M.M. Erythropoietic protoporphyria: treatment with antioxidants and otential cure with gene therapy. Methods Enzymol. 319:2000;479-484
29. Anstey A.V., Ryan A., Rhodes L.E., Charman C.R., Arlett C.F., Tyrrell R.M., Taylor C.R., Pearse A.D. Characterization of photosensitivity in the Smith-Lemli-Opitz syndrome: a new congenital photosensitivity syndrome. Br. J. Dermatol. 141:1999;406-414
30. Thomas J.P., Hall R.D., Girotti A.W. Singlet oxygen intermediacy in the photodynamic action of membrane-bound hematoporphyrin derivative. Cancer Lett. 35:1987;295-302
31. Heinrich U., Gartner C., Wiebusch M., Eichler O., Sies H., Tronnier H., Stahl W. Supplementation with beta-carotene or a similar smount of mixed carotenoids protects humans from UV-induced erythema. J. Nutr. 133:2003;98-101
32. Stahl W., Sies H. Carotenoids and protection against solar UV radiation. Skin Pharmacol. Appl. Skin Physiol. 15:2002;291-296
33. Stahl W., Heinrich U., Jungmann H., Sies H., Tronnier H. Carotenoids and carotenoids plus vitamin E protect against ultraviolet light-induced erythema in humans. Am. J. Clin. Nutr. 71:2000;795-798
34. Alaluf S., Heinrich U., Stahl W., Tronnier H., Wiseman S. Dietary carotenoids contribute to normal human skin color and UV photosensitivity. J. Nutr. 132:2002;399-403
35. Gollnick H.P.M., Hopfenmüller W., Hemmes C., Chun S.C., Schmid C., Sundermeier K., Biesalski H.K. Systemic b-carotene plus topical UV-sunscreen are an optimal protection against harmful effects of natural UV-sunlight: results of the Berlin-Eilath study. Eur. J. Dermatol. 6:1996;200-205
36. Lee J., Jiang S., Levine N., Watson R.R. Carotenoid supplementation reduces erythema in human skin after simulated solar radiation exposure. Proc. Soc. Exp. Biol. Med. 223:2000;170-174
37. Bialy T.L., Rothe M.J., Grant-Kels J.M. Dietary factors in the prevention and treatment of nonmelanoma skin cancer and melanoma. Dermatol. Surg. 28:2002;1143-1152
38. Sayre R.M., Black H.S. Beta-carotene does not act as an optical filter in skin. J. Photochem. Photobiol. B. 12:1992;83-90
39. Wei R.R., Wamer W.G., Lambert L.A., Kornhauser A. Beta-carotene uptake and effects on intracellular levels of retinol in vitro. Nutr. Cancer. 30:1998;53-58
40. Andersson E., Vahlquist A., Rosdahl I. Beta-carotene uptake and bioconversion to retinol differ between human melanocytes and keratinocytes. Nutr. Cancer. 39:2001;300-306
41. Griffiths C.E., Kang S., Ellis C.N., Kim K.J., Finkel L.J., Ortiz-Ferrer L.C., White G.M., Hamilton T.A., Voorhees J.J. Two concentrations of topical tretinoin (retinoic acid) cause similar improvement of photoaging but different degrees of irritation: a double-blind, vehicle-controlled comparison of 0.1% and 0.025% tretinoin creams. Arch. Dermatol. 131:1995;1037-1044
42. Kligman A.M. Topical retinoic acid (tretinoin) for photoaging: conceptions and misperceptions. Cutis. 57:1996;142-144
43. Fisher G.J., Wang Z.Q., Datta S.C., Varani J., Kang S., Voorhees J.J. Pathophysiology of premature skin aging induced by ultraviolet light. N. Engl. J. Med. 337:1997;1419-1428
44. Fisher G.J., Talwar H.S., Lin J., Lin P., McPhillips F., Wang Z., Li X., Wan Y., Kang S., Voorhees J.J. Retinoic acid inhibits induction of c-Jun protein by ultraviolet radiation that occurs subsequent to activation of mitogen-activated protein kinase pathways in human skin in vivo. J. Clin. Invest. 101:1998;1432-1440
45. Fisher G.J., Talwar H.S., Lin J., Voorhees J.J. Molecular mechanisms of photoaging in human skin in vivo and their prevention by all-trans retinoic acid. Photochem. Photobiol. 69:1999;154-157
46. Fisher G.J., Datta S., Wang Z., Li X.Y., Quan T., Chung J.H., Kang S., Voorhees J.J. c-Jun-dependent inhibition of cutaneous procollagen transcription following ultraviolet irradiation is reversed by all-trans retinoic acid. J. Clin. Invest. 106:2000;663-670
47. Griffiths C.E. Dowling oration delivered at the Royal College of Physicians, London, Friday 5 June 1998. Retinoids: renaissance and reformation. Clin. Exp. Dermatol. 24:1999;329-335
48. Kang S., Duell E.A., Fisher G.J., Datta S.C., Wang Z.Q., Reddy A.P., Tavakkol A., Yi J.Y., Griffiths C.E., Elder J.T., et al. Application of retinol to human skin in vivo induces epidermal hyperplasia and cellular retinoid binding proteins characteristic of retinoic acid but without measurable retinoic acid levels or irritation. J. Invest. Dermatol. 105:1995;549-556
49. Fuchs E. Epidermal differentiation and keratin gene expression. J. Cell. Sci. Suppl. 17:1993;197-208
50. 2+. Differentiation. 54:1993;201-217
51. Varani J., Zeigler M., Dame M.K., Kang S., Fisher G.J., Voorhees J.J., Stoll S.W., Elder J.T. Heparin-binding epidermal-growth-factor-like growth factor activation of keratinocyte ErbB receptors mediates epidermal hyperplasia, a prominent side-effect of retinoid therapy. J. Invest. Dermatol. 117:2001;1335-1341
52. Frederick J., Alberts A. The natural UVA radiation environment. Urbach F. Biological responses to UV A radiation. 1992;7-18 Valdenmar, KS
53. Wertz, K.; Buchwald Hunziker, P.; Seifert, N.; Riss, G.; Neeb, M.; Steiner, G.; Hunziker, W.; Goralczyk, R. β-Carotene interferes with UVA-induced gene expression by multiple pathways. In preparation
54. Ahn K.S., Moon K.Y., Lee J., Kim Y.S. Downregulation of NF-kappaB activation in human keratinocytes by melanogenic inhibitors. J. Dermatol. Sci. 31:2003;193-201
55. Fukunaga M., Oka M., Ichihashi M., Yamamoto T., Matsuzaki H., Kikkawa U. UV-induced tyrosine phosphorylation of PKC delta and promotion of apoptosis in the HaCaT cell line. Biochem. Biophys. Res. Commun. 289:2001;573-579
56. Chen W., Tang Q., Gonzales M.S., Bowden G.T. Role of p38 MAP kinases and ERK in mediating ultraviolet-B induced cyclooxygenase-2 gene expression in human keratinocytes. Oncogene. 20:2001;3921-3926
57. Saliou C., Kitazawa M., McLaughlin L., Yang J.P., Lodge J.K., Tetsuka T., Iwasaki K., Cillard J., Okamoto T., Packer L. Antioxidants modulate acute solar ultraviolet radiation-induced NF-kappa-B activation in a human keratinocyte cell line. Free Radic. Biol. Med. 26:1999;174-183
58. Assefa Z., Garmyn M., Bouillon R., Merlevede W., Vandenheede J.R., Agostinis P. Differential stimulation of ERK and JNK activities by ultraviolet B irradiation and epidermal growth factor in human keratinocytes. J. Invest. Dermatol. 108:1997;886-891
59. Sitailo L.A., Tibudan S.S., Denning M.F. Activation of caspase-9 is required for UV-induced apoptosis of human keratinocytes. J. Biol. Chem. 277:2002;19346-19352
60. Leccia M.T., Richard M.J., Joanny-Crisci F., Beani J.C. UV-A1 cytotoxicity and antioxidant defence in keratinocytes and fibroblasts. Eur. J. Dermatol. 8:1998;478-482
61. Li D., Turi T.G., Schuck A., Freedberg I.M., Khitrov G., Blumenberg M. Rays and arrays: the transcriptional program in the response of human epidermal keratinocytes to UVB illumination. FASEB J. 15:2001;2533-2535
62. Takao J., Ariizumi K., Dougherty I.I., Cruz P.D. Jr. Genomic scale analysis of the human keratinocyte response to broad-band ultraviolet-B irradiation. Photodermatol. Photoimmunol. Photomed. 18:2002;5-13
63. Djavaheri-Mergny M., Mergny J.L., Bertrand F., Santus R., Maziere C., Dubertret L., Maziere J.C. Ultraviolet-A induces activation of AP-1 in cultured human keratinocytes. FEBS Lett. 384:1996;92-96
64. Boukamp P., Petrussevska R.T., Breitkreutz D., Hornung J., Markham A., Fusenig N.E. Normal keratinization in a spontaneously immortalized aneuploid human keratinocyte cell line. J. Cell Biol. 106:1988;761-771
65. Edstrom D.W., Porwit A., Ros A.M. Effects on human skin of repetitive ultraviolet-A1 (UVA1) irradiation and visible light. Photodermatol. Photoimmunol. Photomed. 17:2001;66-70
66. Cantrell A., McGarvey D.J., George Truscott T., Rancan F., Bohm F. Singlet oxygen quenching by dietary carotenoids in a model membrane environment. Arch. Biochem. Biophys. 412:2003;47-54
67. Truscott G. Reduction potential and radical reactions of carotenoids. Meeting abstract, 13th International Carotenoid Symposium, Honolulu. 2002
68. Yin L., Morita A., Tsuji T. Alterations of extracellular matrix induced by tobacco smoke extract. Arch. Dermatol. Res. 292:2000;188-194
69. Herrmann G., Wlaschek M., Bolsen K., Prenzel K., Goerz G., Scharffetter-Kochanek K. Photosensitization of uroporphyrin augments the ultraviolet A-induced synthesis of matrix metalloproteinases in human dermal fibroblasts. J. Invest. Dermatol. 107:1996;398-403
70. Fisher G.J., Datta S.C., Talwar H.S., Wang Z.Q., Varani J., Kang S., Voorhees J.J. Molecular basis of sun-induced premature skin ageing and retinoid antagonism. Nature. 379:1996;335-339
71. Wlaschek M., Wenk J., Brenneisen P., Briviba K., Schwarz A., Sies H., Scharffetter-Kochanek K. Singlet oxygen is an early intermediate in cytokine-dependent ultraviolet-A induction of interstitial collagenase in human dermal fibroblasts in vitro. FEBS Lett. 413:1997;239-242
72. Gack S., Vallon R., Schaper J., Ruther U., Angel P. Phenotypic alterations in fos-transgenic mice correlate with changes in Fos/Jun-dependent collagenase type I expression: regulation of mouse metalloproteinases by carcinogens, tumor promoters, cAMP, and Fos oncoprotein. J. Biol. Chem. 269:1994;10363-10369
73. Edge R., Land E.J., McGarvey D., Mulroy L., Truscott T.G. Relative one-electron reduction potentials of carotenoid radical cations with the vitamin E radical cation. J. Am. Chem. Soc. 120:1998
74. Paik J., During A., Harrison E.H., Mendelsohn C.L., Lai K., Blaner W.S. Expression and characterization of a murine enzyme able to cleave beta-carotene: the formation of retinoids. J. Biol. Chem. 276:2001;32160-32168
75. Yan W., Jang G.F., Haeseleer F., Esumi N., Chang J., Kerrigan M., Campochiaro M., Campochiaro P., Palczewski K., Zack D.J. Cloning and characterization of a human beta,beta-carotene-15,15′-dioxygenase that is highly expressed in the retinal pigment epithelium. Genomics. 72:2001;193-202
76. von Lintig J., Wyss A. Molecular analysis of vitamin A formation: cloning and characterization of beta-carotene 15,15′-dioxygenases. Arch. Biochem. Biophys. 385:2001;47-52
77. Wyss A., Wirtz G., Woggon W., Brugger R., Wyss M., Friedlein A., Bachmann H., Hunziker W. Cloning and expression of beta,beta-carotene 15,15′-dioxygenase. Biochem. Biophys. Res. Commun. 271:2000;334-336
78. Kiefer C., Hessel S., Lampert J.M., Vogt K., Lederer M.O., Breithaupt D.E., von Lintig J. Identification and characterization of a mammalian enzyme catalyzing the asymmetric oxidative cleavage of provitamin A. J. Biol. Chem. 276:2001;14110-14116
79. Trekli M.C., Riss G., Goralczyk R., Tyrrell R.M. Beta-carotene suppresses UVA-induced HO-1 gene expression in cultured FEK4. Free Radic. Biol. Med. 34:2003;456-464
80. Sorg O., Tran C., Carraux P., Didierjean L., Falson F., Saurat J.H. Oxidative stress-independent depletion of epidermal vitamin A by UVA. J. Invest. Dermatol. 118:2002;513-518
81. Roe D.A. Photodegradation of carotenoids in human subjects. Fed. Proc. 46:1987;1886-1889
82. Brenneisen P., Sies H., Scharffetter-Kochanek K. Ultraviolet-B irradiation and matrix metalloproteinases: from induction via signaling to initial events. Ann. NY Acad. Sci. 973:2002;31-43
83. Kick G., Messer G., Plewig G., Kind P., Goetz A.E. Strong and prolonged induction of c-jun and c-fos proto-oncogenes by photodynamic therapy. Br. J. Cancer. 74:1996;30-36
84. Gange R.W. Comparison of pigment responses in human skin to UVB and UVA radiation. Prog. Clin. Biol. Res. 256:1988;475-485
85. Ariizumi K., Bergstresser P.R., Takashima A. Wavelength-specific induction of immediate early genes by ultraviolet radiation. J. Dermatol. Sci. 12:1996;147-155
86. Obermuller-Jevic U.C., Francz P.I., Frank J., Flaccus A., Biesalski H.K. Enhancement of the UVA induction of haem oxygenase-1 expression by beta-carotene in human skin fibroblasts. FEBS Lett. 460:1999;212-216
87. Obermuller-Jevic U.C., Schlegel B., Flaccus A., Biesalski H.K. The effect of beta-carotene on the expression of interleukin-6 and heme oxygenase-1 in UV-irradiated human skin fibroblasts in vitro. FEBS Lett. 509:2001;186-190
88. Offord E.A., Gautier J.C., Avanti O., Scaletta C., Runge F., Kramer K., Applegate L.A. Photoprotective potential of lycopene, beta-carotene, vitamin E, vitamin C and carnosic acid in UVA-irradiated human skin fibroblasts. Free Radic. Biol. Med. 32:2002;1293-1303
89. Moran M., Miceli M.C. Engagement of GPI-linked CD48 contributes to TCR signals and cytoskeletal reorganization: a role for lipid rafts in T cell activation. Immunity. 9:1998;787-796
90. Roy S., Luetterforst R., Harding A., Apolloni A., Etheridge M., Stang E., Rolls B., Hancock J.F., Parton R.G. Dominant-negative caveolin inhibits H-Ras function by disrupting cholesterol-rich plasma membrane domains. Nat. Cell Biol. 1:1999;98-105
91. Eicker J., Kurten V., Wild S., Riss G., Goralczyk R., Krutmann J., Berneburg M. Betacarotene supplementation protects from photoaging-associated mitochondrial DNA mutation. Photochem. Photobiol. Sci. 2:2003;655-659
92. Eichler O., Sies H., Stahl W. Divergent optimum levels of lycopene, beta-carotene and lutein protecting against UVB irradiation in human fibroblastst. Photochem. Photobiol. 75:2002;503-506
93. Kahari V.M., Saarialho-Kere U. Matrix metalloproteinases in skin. Exp. Dermatol. 6:1997;199-213
94. Sternlicht M.D., Werb Z. How matrix metalloproteinases regulate cell behavior. Annu. Rev. Cell Dev. Biol. 17:2001;463-516
95. Brennan M., Bhatti H., Nerusu K.C., Bhagavathula N., Kang S., Fisher G.J., Varani J., Voorhees J.J. Matrix metalloproteinase-1 is the major collagenolytic enzyme responsible for collagen damage in UV-irradiated human skin. Photochem. Photobiol. 78:2003;43-48
96. Berneburg M., Grether-Beck S., Kurten V., Ruzicka T., Briviba K., Sies H., Krutmann J. Singlet oxygen mediates the UVA-induced generation of the photoaging-associated mitochondrial common deletion. J. Biol. Chem. 274:1999;15345-15349
97. Valacchi G., Rimbach G., Saliou C., Weber S.U., Packer L. Effect of benzoyl peroxide on antioxidant status, NF-kappaB activity and interleukin-1alpha gene expression in human keratinocytes. Toxicology. 165:2001;225-234
98. Shindo Y., Witt E., Packer L. Antioxidant defense mechanisms in murine epidermis and dermis and their responses to ultraviolet light. J. Invest. Dermatol. 100:1993;260-265
99. Shindo Y., Witt E., Han D., Packer L. Dose-response effects of acute ultraviolet irradiation on antioxidants and molecular markers of oxidation in murine epidermis and dermis. J. Invest. Dermatol. 102:1994;470-475
100. Torma H., Rollman O., Vahlquist A. The vitamin A metabolism and expression of retinoid-binding proteins differ in HaCaT cells and normal human keratinocytes. Arch. Dermatol. Res. 291:1999;339-345
101. Popa C., Dicker A.J., Dahler A.L., Saunders N.A. Cytochrome P450, CYP26AI, is expressed at low levels in human epidermal keratinocytes and is not retinoic acid-inducible. Br. J. Dermatol. 141:1999;460-468
102. Wang X.D., Russell R.M., Liu C., Stickel F., Smith D.E., Krinsky N.I. Beta-oxidation in rabbit liver in vitro and in the perfused ferret liver contributes to retinoic acid biosynthesis from beta-apocarotenoic acids. J. Biol. Chem. 271:1996;26490-26498
103. Bachmann H., Desbarats A., Pattison P., Sedgewick M., Riss G., Wyss A., Cardinault N., Duszka C., Goralczyk R., Grolier P. Feedback regulation of beta,beta-carotene 15,15′-monooxygenase by retinoic acid in rats and chickens. J. Nutr. 132:2002;3616-3622
104. Boulanger A., McLemore P., Copeland N.G., Gilbert D.J., Jenkins N.A., Yu S.S., Gentleman S., Redmond T.M. Identification of beta-carotene 15, 15′-monooxygenase as a peroxisome proliferator-activated receptor target gene. FASEB J. 17:2003;1304-1306
105. Takeda A., Morinobu T., Takitani K., Kimura M., Tamai H. Measurement of retinoids and beta-carotene 15,15′-dioxygenase activity in HR-1 hairless mouse skin with UV exposure. J. Nutr. Sci. Vitaminol. (Tokyo). 49:2003;69-72
106. Elder J.T., Fisher G.J., Zhang Q.Y., Eisen D., Krust A., Kastner P., Chambon P., Voorhees J.J. Retinoic acid receptor gene expression in human skin. J. Invest. Dermatol. 96:1991;425-433
107. Wang Z., Boudjelal M., Kang S., Voorhees J.J., Fisher G.J. Ultraviolet irradiation of human skin causes functional vitamin A deficiency, preventable by all-trans retinoic acid pre-treatment. Nat. Med. 5:1999;418-422
108. Hoffmann B., Lehmann J.M., Zhang X.K., Hermann T., Husmann M., Graupner G., Pfahl M. A retinoic acid receptor-specific element controls the retinoic acid receptor-beta promoter. Mol. Endocrinol. 4:1990;1727-1736
109. Sucov H.M., Murakami K.K., Evans R.M. Characterization of an autoregulated response element in the mouse retinoic acid receptor type beta gene. Proc. Natl. Acad. Sci. U S A. 87:1990;5392-5396
110. Brand N.J., Petkovich M., Chambon P. Characterization of a functional promoter for the human retinoic acid receptor-alpha (hRAR-alpha). Nucleic Acids Res. 18:1990;6799-6806
111. Lehmann J.M., Zhang X.K., Pfahl M. RAR gamma 2 expression is regulated through a retinoic acid response element embedded in Sp1 sites. Mol. Cell Biol. 12:1992;2976-2985
112. Barger P.M., Kelly D.P. Identification of a retinoid/chicken ovalbumin upstream promoter transcription factor response element in the human retinoid X receptor gamma2 gene promoter. J. Biol. Chem. 272:1997;2722-2728
113. Guerin E., Ludwig M.G., Basset P., Anglard P. Stromelysin-3 induction and interstitial collagenase repression by retinoic acid: therapeutical implication of receptor-selective retinoids dissociating transactivation and AP-1-mediated transrepression. J. Biol. Chem. 272:1997;11088-11095
114. Pan L., Eckhoff C., Brinckerhoff C.E. Suppression of collagenase gene expression by all-trans and 9-cis retinoic acid is ligand dependent and requires both RARs and RXRs. J. Cell Biochem. 57:1995;575-589
115. 3 metabolism in human skin. J. Invest. Dermatol. 108:1997;78-82
116. 2 production by cells of the rheumatoid lesion. Arthritis Res. 1:1999;63-70