Keratinocyte ATP binding cassette transporter expression is regulated by ultraviolet light

Journal of Photochemistry and Photobiology B: Biology

Volumn 116, Issue , 2012, Pages 79-88

  Markó, Lóránt ^a,b   Paragh, György ^a,c   Ugocsai, Péter ^a   Boettcher, Alfred ^a   Vogt, Thomas ^a   Schling, Petra ^a   Balogh, Attila ^a,b   Tarabin, Victoria ^a   Orsó, Evelyn ^a   Wikonkál, Norbert ^c   Mandl, József ^c   Remenyik, Éva ^b   Schmitz, Gerd ^a  

^a UNIVERSITY OF REGENSBURG   (Germany)

^b UNIVERSITY OF DEBRECEN   (Hungary)

^c SEMMELWEIS UNIVERSITY   (Hungary)

Author keywords

ABC transporter; Epidermal barrier; Keratinocyte; Lipid transport; UVB

Indexed keywords

ABC TRANSPORTER; ABC TRANSPORTER A1; ABC TRANSPORTER G1; GLUCOSYLCERAMIDE; LUCIFERASE; MESSENGER RNA; PROTEIN ATP BINDING CASSETTE TRANSPORTER A12; PROTEIN ATP BINDING CASSETTE TRANSPORTER C1; PROTEIN ATP BINDING CASSETTE TRANSPORTER F2; SPHINGOSINE 1 PHOSPHATE; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; DOWN REGULATION; HUMAN; HUMAN CELL; ICHTHYOSIS; IMMUNOBLOTTING; KERATINOCYTE; LIPID TRANSPORT; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; ULTRAVIOLET B RADIATION; ULTRAVIOLET RADIATION; UPREGULATION;

ATP-BINDING CASSETTE TRANSPORTERS; BIOLOGICAL TRANSPORT; CELL DIFFERENTIATION; DOWN-REGULATION; EPIDERMIS; GENE EXPRESSION REGULATION; HUMANS; KERATINOCYTES; LIPID METABOLISM; PROMOTER REGIONS, GENETIC; RADIATION-PROTECTIVE AGENTS; RNA, MESSENGER; ULTRAVIOLET RAYS;

EID: 84866001845     PISSN: 10111344     EISSN: 18732682     Source Type: Journal    
DOI: 10.1016/j.jphotobiol.2012.06.007     Document Type: Article

References (70)

1. E. Proksch, J.M. Brandner, and J.M. Jensen The skin: an indispensable barrier Exp. Dermatol. 17 2008 1063 1072
2. M.E. Ming, H.A. Daryanani, L.P. Roberts, H.P. Baden, and J.C. Kvedar Binding of keratin intermediate filaments (K10) to the cornified envelope in mouse epidermis: implications for barrier function J. Invest. Dermatol. 103 1994 780 784
3. E. Fuchs Epidermal differentiation: the bare essentials J. Cell Biol. 111 1990 2807 2814
4. N.Y. Schurer, and P.M. Elias The biochemistry and function of stratum corneum lipids Adv. Lipid Res. 24 1991 27 56
5. M.H. Braff, A. Di Nardo, and R.L. Gallo Keratinocytes store the antimicrobial peptide cathelicidin in lamellar bodies J. Invest. Dermatol. 124 2005 394 400
6. P.M. Elias, D. Crumrine, U. Rassner, J.P. Hachem, G.K. Menon, W. Man, M.H. Choy, L. Leypoldt, K.R. Feingold, and M.L. Williams Basis for abnormal desquamation and permeability barrier dysfunction in RXLI J. Invest. Dermatol. 122 2004 314 319
7. S. Hamanaka, S. Nakazawa, M. Yamanaka, Y. Uchida, and F. Otsuka Glucosylceramide accumulates preferentially in lamellar bodies in differentiated keratinocytes Br. J. Dermatol. 152 2005 426 434
8. A. Ishida-Yamamoto, M. Simon, M. Kishibe, Y. Miyauchi, H. Takahashi, S. Yoshida, T.J. O'Brien, G. Serre, and H. Iizuka Epidermal lamellar granules transport different cargoes as distinct aggregates J. Invest. Dermatol. 122 2004 1137 1144
9. K.C. Madison Barrier function of the skin: "la raison d'etre" of the epidermis J. Invest. Dermatol. 121 2003 231 241
10. G. Grubauer, K.R. Feingold, R.M. Harris, and P.M. Elias Lipid content and lipid type as determinants of the epidermal permeability barrier J. Lipid Res. 30 1989 89 96
11. D.E. Brash Sunlight and the onset of skin cancer Trends Genet. 13 1997 410 414
12. W. Zhang, E. Remenyik, D. Zelterman, D.E. Brash, and N.M. Wikonkal Escaping the stem cell compartment: sustained UVB exposure allows p53-mutant keratinocytes to colonize adjacent epidermal proliferating units without incurring additional mutations Proc. Natl. Acad. Sci. USA 98 2001 13948 13953
13. T.R. Fears, C.C. Bird, D. Guerry, R.W. Sagebiel, M.H. Gail, D.E. Elder, A. Halpern, E.A. Holly, P. Hartge, and M.A. Tucker Average midrange ultraviolet radiation flux and time outdoors predict melanoma risk Cancer Res. 62 2002 3992 3996
14. L. Wunderlich, G. Paragh, N.M. Wikonkal, G. Banhegyi, S. Karpati, and J. Mandl UVB induces a biphasic response of HIF-1alpha in cultured human keratinocytes Exp. Dermatol. 17 2008 335 342
15. Y. Ibuki, A. Suzuki, and R. Goto UVA irradiation induces energy-independent phospholipid-flip in mammalian plasma membrane Photochem. Photobiol. 73 2001 513 517
16. A. Haratake, Y. Uchida, M. Schmuth, O. Tanno, R. Yasuda, J.H. Epstein, P.M. Elias, and W.M. Holleran UVB-induced alterations in permeability barrier function: roles for epidermal hyperproliferation and thymocyte-mediated response J. Invest. Dermatol. 108 1997 769 775
17. S.J. Jiang, A.W. Chu, Z.F. Lu, M.H. Pan, D.F. Che, and X.J. Zhou Ultraviolet B-induced alterations of the skin barrier and epidermal calcium gradient Exp. Dermatol. 16 2007 985 992
18. S.J. Jiang, J.Y. Chen, Z.F. Lu, J. Yao, D.F. Che, and X.J. Zhou Biophysical and morphological changes in the stratum corneum lipids induced by UVB irradiation J. Dermatol. Sci. 44 2006 29 36
19. S. Meguro, Y. Arai, K. Masukawa, K. Uie, and I. Tokimitsu Stratum corneum lipid abnormalities in UVB-irradiated skin Photochem. Photobiol. 69 1999 317 321
20. S. Meguro, Y. Arai, Y. Masukawa, K. Uie, and I. Tokimitsu Relationship between covalently bound ceramides and transepidermal water loss (TEWL) Arch. Dermatol. Res. 292 2000 463 468
21. Y. Takagi, H. Nakagawa, H. Kondo, Y. Takema, and G. Imokawa Decreased levels of covalently bound ceramide are associated with ultraviolet B-induced perturbation of the skin barrier J. Invest. Dermatol. 123 2004 1102 1109
22. T. Abe, and J. Mayuzumi The change and recovery of human skin barrier functions after ultraviolet light irradiation Chem. Pharm. Bull. (Tokyo) 27 1979 458 462
23. M. Akiyama, and H. Shimizu An update on molecular aspects of the non-syndromic ichthyoses Exp. Dermatol. 17 2008 373 382
24. D. Kielar, W.E. Kaminski, G. Liebisch, A. Piehler, J.J. Wenzel, C. Mohle, S. Heimerl, T. Langmann, S.O. Friedrich, A. Bottcher, S. Barlage, W. Drobnik, and G. Schmitz Adenosine triphosphate binding cassette (ABC) transporters are expressed and regulated during terminal keratinocyte differentiation: a potential role for ABCA7 in epidermal lipid reorganization J. Invest. Dermatol. 121 2003 465 474
25. G. Schmitz, and W.E. Kaminski ABC transporters and cholesterol metabolism Front Biosci. 6 2001 D505 D514
26. G.F. Lewis, and D.J. Rader New insights into the regulation of HDL metabolism and reverse cholesterol transport Circ. Res. 96 2005 1221 1232
27. K. Sakai, M. Akiyama, Y. Sugiyama-Nakagiri, J.R. McMillan, D. Sawamura, and H. Shimizu Localization of ABCA12 from Golgi apparatus to lamellar granules in human upper epidermal keratinocytes Exp. Dermatol. 16 2007 920 926
28. M. Akiyama The roles of ABCA12 in keratinocyte differentiation and lipid barrier formation in the epidermis Dermatoendocrinol 3 2011 107 112
29. Y. Zuo, D.Z. Zhuang, R. Han, G. Isaac, J.J. Tobin, M. McKee, R. Welti, J.L. Brissette, M.L. Fitzgerald, and M.W. Freeman ABCA12 maintains the epidermal lipid permeability barrier by facilitating formation of ceramide linoleic esters J. Biol. Chem. 283 2008 36624 36635
30. V. Oji, G. Tadini, M. Akiyama, B.C. Blanchet, C. Bodemer, E. Bourrat, P. Coudiere, J.J. DiGiovanna, P. Elias, J. Fischer, P. Fleckman, M. Gina, J. Harper, T. Hashimoto, I. Hausser, H.C. Hennies, D. Hohl, A. Hovnanian, A. Ishida-Yamamoto, W.K. Jacyk, S. Leachman, I. Leigh, J. Mazereeuw-Hautier, L. Milstone, F. Morice-Picard, A.S. Paller, G. Richard, M. Schmuth, H. Shimizu, E. Sprecher, S.M. Van, A. Taieb, J.R. Toro, P. Vabres, A. Vahlquist, M. Williams, and H. Traupe Revised nomenclature and classification of inherited ichthyoses: results of the first ichthyosis consensus conference in Soreze J. Am. Acad. Dermatol. 63 2010 2009 607 641
31. Q. Li, Y. Kato, Y. Sai, T. Imai, and A. Tsuji Multidrug resistance-associated protein 1 functions as an efflux pump of xenobiotics in the skin Pharm. Res. 22 2005 842 846
32. E. Bakos, and L. Homolya Portrait of multifaceted transporter, the multidrug resistance-associated protein 1 (MRP1/ABCC1) Pflugers Arch. 453 2007 621 641
33. P. Mitra, C.A. Oskeritzian, S.G. Payne, M.A. Beaven, S. Milstien, and S. Spiegel Role of ABCC1 in export of sphingosine-1-phosphate from mast cells Proc. Natl. Acad. Sci. USA 103 2006 16394 16399
34. A. Bebes, K. Kis, T. Nagy, A. Kurunczi, H. Polyanka, Z. Bata-Csorgo, L. Kemeny, A. Dobozy, and M. Szell The expressions of ABCC4 and ABCG2 xenobiotic transporters in human keratinocytes are proliferation-related Arch. Dermatol. Res. 304 2012 57 63
35. A. Bebes, T. Nagy, Z. Bata-Csorgo, L. Kemeny, A. Dobozy, and M. Szell Specific inhibition of the ABCG2 transporter could improve the efficacy of photodynamic therapy J. Photochem. Photobiol. B 105 2011 162 166
36. S. Heimerl, A.K. Bosserhoff, T. Langmann, J. Ecker, and G. Schmitz Mapping ATP-binding cassette transporter gene expression profiles in melanocytes and melanoma cells Melanoma Res. 17 2007 265 273
37. I.E. Dumitriu, R.E. Voll, W. Kolowos, U.S. Gaipl, P. Heyder, J.R. Kalden, and M. Herrmann UV irradiation inhibits ABC transporters via generation of ADP-ribose by concerted action of poly(ADP-ribose) polymerase-1 and glycohydrolase Cell Death. Differ. 11 2004 314 320
38. Z. Hu, S. Jin, and K.W. Scotto Transcriptional activation of the MDR1 gene by UV irradiation. Role of NF-Y and Sp1 J. Biol. Chem. 275 2000 2979 2985
39. H. Sasaki, T. Itoh, H. Akamatsu, H. Okamoto, and T. Horio Effects of calcium concentration on the SOD activity and UVB-induced cytotoxicity in cultured human keratinocytes Photodermatol. Photoimmunol. Photomed. 21 2005 9 14
40. A. Balogh, G. Paragh Jr., A. Juhasz, T. Kobling, D. Torocsik, E. Miko, V. Varga, G. Emri, I. Horkay, B. Scholtz, and E. Remenyik Reference genes for quantitative real time PCR in UVB irradiated keratinocytes J. Photochem. Photobiol. B 93 2008 133 139
41. T. Langmann, R. Mauerer, A. Zahn, C. Moehle, M. Probst, W. Stremmel, and G. Schmitz Real-time reverse transcription-PCR expression profiling of the complete human ATP-binding cassette transporter superfamily in various tissues Clin. Chem. 49 2003 230 238
42. T. Langmann, M. Porsch-Ozcurumez, U. Unkelbach, J. Klucken, and G. Schmitz Genomic organization and characterization of the promoter of the human ATP-binding cassette transporter-G1 (ABCG1) gene Biochim. Biophys. Acta 1494 2000 175 180
43. K.R. Feingold Thematic review series: skin lipids. The role of epidermal lipids in cutaneous permeability barrier homeostasis J. Lipid Res. 48 2007 2531 2546
44. K.R. Feingold The outer frontier: the importance of lipid metabolism in the skin J. Lipid Res. 50 2009 S417 S422
45. M. Akiyama, Y. Sugiyama-Nakagiri, K. Sakai, J.R. McMillan, M. Goto, K. Arita, Y. Tsuji-Abe, N. Tabata, K. Matsuoka, R. Sasaki, D. Sawamura, and H. Shimizu Mutations in lipid transporter ABCA12 in harlequin ichthyosis and functional recovery by corrective gene transfer J. Clin. Invest. 115 2005 1777 1784
46. A. Baldan, P. Tarr, R. Lee, and P.A. Edwards ATP-binding cassette transporter G1 and lipid homeostasis Curr. Opin. Lipidol. 17 2006 227 232
47. M. Dean, A. Rzhetsky, and R. Allikmets The human ATP-binding cassette (ABC) transporter superfamily Genome Res. 11 2001 1156 1166
48. W. Jessup, I.C. Gelissen, K. Gaus, and L. Kritharides Roles of ATP binding cassette transporters A1 and G1, scavenger receptor BI and membrane lipid domains in cholesterol export from macrophages Curr. Opin. Lipidol. 17 2006 247 257
49. M.A. Kennedy, G.C. Barrera, K. Nakamura, A. Baldan, P. Tarr, M.C. Fishbein, J. Frank, O.L. Francone, and P.A. Edwards ABCG1 has a critical role in mediating cholesterol efflux to HDL and preventing cellular lipid accumulation Cell Metab. 1 2005 121 131
50. J.J. Wenzel, A. Piehler, and W.E. Kaminski ABC A-subclass proteins: gatekeepers of cellular phospho- and sphingolipid transport Front Biosci. 12 2007 3177 3193
51. C. Cao, and Y. Wan Parameters of protection against ultraviolet radiation-induced skin cell damage J. Cell Physiol. 220 2009 277 284
52. J.G. Madson, and L.A. Hansen Multiple mechanisms of Erbb2 action after ultraviolet irradiation of the skin Mol. Carcinog. 46 2007 624 628
53. T. Gambichler, F. Breuckmann, S. Boms, P. Altmeyer, and A. Kreuter Narrowband UVB phototherapy in skin conditions beyond psoriasis J. Am. Acad. Dermatol. 52 2005 660 670
54. Y.J. Jiang, B. Lu, P. Kim, G. Paragh, G. Schmitz, P.M. Elias, and K.R. Feingold PPAR and LXR activators regulate ABCA12 expression in human keratinocytes J. Invest. Dermatol. 128 2008 104 109
55. M. Herget, and R. Tampe Intracellular peptide transporters in human - compartmentalization of the "peptidome" Pflugers Arch. 453 2007 591 600
56. A. Miyake, S. Higashijima, D. Kobayashi, T. Narita, T. Jindo, D.H. Setiamarga, S. Ohisa, N. Orihara, K. Hibiya, S. Konno, S. Sakaguchi, K. Horie, Y. Imai, K. Naruse, A. Kudo, and H. Takeda Mutation in the abcb7 gene causes abnormal iron and fatty acid metabolism in developing medaka fish Dev. Growth Differ. 50 2008 703 716
57. A. Zutz, S. Gompf, H. Schagger, and R. Tampe Mitochondrial ABC proteins in health and disease Biochim. Biophys. Acta 1787 2009 681 690
58. C. Kolly, M.M. Suter, and E.J. Muller Proliferation, cell cycle exit, and onset of terminal differentiation in cultured keratinocytes: pre-programmed pathways in control of C-Myc and Notch1 prevail over extracellular calcium signals J. Invest. Dermatol. 124 2005 1014 1025
59. M. Mao-Qiang, K.R. Feingold, and P.M. Elias Inhibition of cholesterol and sphingolipid synthesis causes paradoxical effects on permeability barrier homeostasis J. Invest. Dermatol. 101 1993 185 190
60. W.M. Holleran, Y. Uchida, L. Halkier-Sorensen, A. Haratake, M. Hara, J.H. Epstein, and P.M. Elias Structural and biochemical basis for the UVB-induced alterations in epidermal barrier function Photodermatol. Photoimmunol. Photomed. 13 1997 117 128
61. G. Schmitz, and T. Langmann Transcriptional regulatory networks in lipid metabolism control ABCA1 expression Biochim. Biophys. Acta 1735 2005 1 19
62. S. Nishimura, H. Tsuda, Y. Miyagi, A. Hirasawa, A. Suzuki, F. Kataoka, H. Nomura, T. Chiyoda, K. Banno, T. Fujii, N. Susumu, and D. Aoki Can ABCF2 protein expression predict the prognosis of uterine cancer? Br. J. Cancer 99 2008 1651 1655
63. Y. Ogawa, H. Tsuda, E. Hai, N. Tsuji, S. Yamagata, S. Tokunaga, K. Nakazawa, Y. Tamamori, M. Ogawa, S. Shimizu, T. Inoue, and Y. Nishiguchi Clinical role of ABCF2 expression in breast cancer Anticancer Res. 26 2006 1809 1814
64. M.A. Kennedy, A. Venkateswaran, P.T. Tarr, I. Xenarios, J. Kudoh, N. Shimizu, and P.A. Edwards Characterization of the human ABCG1 gene: liver X receptor activates an internal promoter that produces a novel transcript encoding an alternative form of the protein J. Biol. Chem. 276 2001 39438 39447
65. Y. Yamanaka, M. Akiyama, Y. Sugiyama-Nakagiri, K. Sakai, M. Goto, J.R. McMillan, M. Ota, D. Sawamura, and H. Shimizu Expression of the keratinocyte lipid transporter ABCA12 in developing and reconstituted human epidermis Am. J. Pathol. 171 2007 43 52
66. A. Hovnanian Harlequin ichthyosis unmasked: a defect of lipid transport J. Clin. Invest. 115 2005 1708 1710
67. M. Schmuth, Y.J. Jiang, S. Dubrac, P.M. Elias, and K.R. Feingold Thematic review series: skin lipids. Peroxisome proliferator-activated receptors and liver X receptors in epidermal biology J. Lipid Res. 49 2008 499 509
68. B. Canguilhem, A. Pradines, C. Baudouin, C. Boby, I. Lajoie-Mazenc, M. Charveron, and G. Favre RhoB protects human keratinocytes from UVB-induced apoptosis through epidermal growth factor receptor signaling J. Biol. Chem. 280 2005 43257 43263
69. T.R. Berton, D.L. Mitchell, R. Guo, and D.G. Johnson Regulation of epidermal apoptosis and DNA repair by E2F1 in response to ultraviolet B radiation Oncogene 24 2005 2449 2460
70. C. Duval, M. Regnier, and R. Schmidt Distinct melanogenic response of human melanocytes in mono-culture, in co-culture with keratinocytes and in reconstructed epidermis, to UV exposure Pigment Cell Res. 14 2001 348 355