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Sphigosine-1-Phosphate-Induced ERK Activation Protects Human Melanocytes from UVB-Induced Apoptosis  

Kim, Dong-Seok (Research Division for Human Life Sciences, Seoul National University, Department of Dermatology, Seoul National University College of Medicine)
Kim, Sook-Young (Department of Dermatology, Seoul National University College of Medicine)
Lee, Jai-Eun (Department of Dermatology, Seoul National University College of Medicine)
Kwon, Sun-Bang (Department of Dermatology, Seoul National University College of Medicine)
Joo, Young-Hyun (Department of Dermatology, Seoul National University College of Medicine)
Youn, Sang-Woong (Department of Dermatology, Seoul National University College of Medicine)
Park, Kyoung-Chan (Department of Dermatology, Seoul National University College of Medicine)
Publication Information
Archives of Pharmacal Research / v.26, no.9, 2003 , pp. 739-746 More about this Journal
Abstract
Ultraviolet B (UVB) is known to induce apoptosis in human melanocytes. Here we show the cytoprotective effect of sphingosine-1-phosphate (S1P) against UVB-induced apoptosis. We also show that UVB-induced apoptosis of melanocytes is mediated by caspase-3 activation and poly(ADP-ribose) polymerase (PARP) cleavage, and that S1P prevents apoptosis by inhibiting this apoptotic pathway. We further investigated three major mitogen-activated protein (MAP) kinases after UVB irradiation. UVB gradually activated c-Jun N-terminal kinase (JNK) and p38 MAP kinase, while extracellular signal-regulated protein kinase (ERK) was inactivated transiently. Blocking of the p38 MAP kinase pathway using SB203580 promoted cell survival and inhibited the activation of caspase-3 and PARP cleavage. These results suggest that p38 MAP kinase activation may play an important role in the UVB-induced apoptosis of human melanocytes. To explain this cytoprotective effect, we next examined whether S1P could inhibit UVB-induced JNK and p38 MAP kinase activation. However, S1P was not found to have any influence on UVB-induced JNK or p38 MAP kinase activation. In contrast, S1P clearly stimulated the phosphorylation of ERK, and the specific inhibition of the ERK pathway using PD98059 abolished the cytoprotective effect of S1P. Based on these results, we conclude that the activation of p38 MAP kinase plays an important role in UVB-induced apoptosis, and that S1P may show its cytoprotective effect through ERK activation in human melanocytes.
Keywords
Sphingolipid; Human melanocytes; ERK; UVB; Apoptosis;
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1 Bennett, B. L., Sasaki, D. T., Murray, B. W., O'Leary, E. C., Sakata, S. T., Xu, W., Leisten, J. C., Motiwala, A., Pierce, S., Satoh, Y., Bhagwat, S. S., Manning, A. M., and Anderson, D. W., SP600125, an anthrapyrazolone inhibitor of Jun N-terminal kinase. Proc. Natl. Acad. Sci. U.S.A., 98, 13681-6(2001)   DOI   ScienceOn
2 Bevan, P., Insulin signalling. J. Cell Sci., 114, 1429-30 (2001)   PUBMED
3 Dooley, T. P., Gadwood, R. C., Kilgore, K., and Thomasco, L. M., Development of an in vitro primary screen for skin depigmentation and antimelanoma agents. Skin Pharmacol., 7, 188-200 (1994)   DOI   PUBMED
4 Fischer, S. J., Podratz, J. L., and Windebank, A. J., Nerve growth factor rescue of cisplatin neurotoxicity is mediated through the high affinity receptor: studies in PC12 cells and p75 null mouse dorsal root ganglia. Neurosci. Lett., 308, 1-4 (2001)   DOI   ScienceOn
5 Kim, D. S., Hwang, E. S., Lee, J. E., Kim, S. Y., Kwon, S. B., and Park, K. C., Sphingosine-1-phosphate decreases melanin synthesis via sustained ERK activation and subsequent MITF degradation. J. Cell Sci., 116, 1699-1706 (2003)   DOI   ScienceOn
6 Manggau, M., Kim, D. S., Ruwisch, L., Vogler, R., Korting, H. C., Schafer-Korting, M., and Kleuser, B., 1Alpha,25-dihydroxy-vitamin D3 protects human keratinocytes from apoptosis by the formation of sphingosine-1-phosphate. J. Invest. Dermatol., 117, 1241-1249 (2001)   DOI   PUBMED   ScienceOn
7 Marshall, C. J., Specificity of receptor tyrosine kinase signaling: transient versus sustained extracellular signal-regulated kinase activation. Cell, 80, 179-185 (1995)   DOI   PUBMED   ScienceOn
8 Njoo, M. D. and Westerhof, W., Vitiligo. Pathogenesis and treatment. Am. J. Clin. Dermatol., 2, 167-181 (2001)   DOI   ScienceOn
9 Pebay, A., Toutant, M., Premont, J., Calvo, C. F., Venance, L., Cordier, J., Glowinski, J., and Tence, M., Sphingosine-1-phosphate induces proliferation of astrocytes: regulation by intracellular signalling cascades. Eur. J. Neurosci., 13, 2067-2076 (2001)   DOI   ScienceOn
10 Spiegel, S., Sphingosine 1-phosphate: a prototype of a new class of second messengers. J. Leukoc Biol., 65, 341-344 (1999)   DOI   PUBMED
11 Waetzig, V. and Herdegen, T., A single c-Jun N-terminal kinase isoform (JNK3-p54) is an effector in both neuronal differentiation and cell death. J. Biol. Chem. (2002)
12 Yanase, H., Ando, H., Horikawa, M., Watanabe, M., Mori, T., and Matsuda, N., Possible involvement of ERK 1/2 in UVAinduced melanogenesis in cultured normal human epidermal melanocytes. Pigment. Cell Res., 14, 103-109 (2001)   DOI   ScienceOn
13 Pyne, S. and Pyne, N. J., Sphingosine 1-phosphate signalling in mammalian cells. Biochem. J., 349, 385-402 (2000)   DOI   ScienceOn
14 Harper, S. J. and LoGrasso, P., Signalling for survival and death in neurones: the role of stress-activated kinases, JNK and p38. Cell Signal, 13, 299-310 (2001)   DOI   ScienceOn
15 Nava, V. E., Hobson, J. P., Murthy, S., Milstien, S., and Spiegel, S., Sphingosine kinase type 1 promotes estrogen-dependent tumorigenesis of breast cancer MCF-7 cells. Exp. Cell. Res., 281, 115-127 (2002)   DOI   ScienceOn
16 Zhai, S., Yaar, M., Doyle, S. M., and Gilchrest, B. A., Nerve growth factor rescues pigment cells from ultraviolet-induced apoptosis by upregulating BCL-2 levels. Exp. Cell Res., 224, 335-343 (1996)   DOI   ScienceOn
17 Kolch, W., Meaningful relationships: the regulation of the Ras/Raf/MEK/ERK pathway by protein interactions. Biochem. J. 351 Pt 2, 289-305 (2000)   DOI   ScienceOn
18 Medrano, E. E. and Nordlund, J. J., Successful culture of adult human melanocytes obtained from normal and vitiligo donors. J. Invest. Dermatol., 95, 441-445 (1990)   PUBMED
19 Chang, L. and Karin, M., Mammalian MAP kinase signalling cascades. Nature., 410, 37-40 (2001)   DOI   ScienceOn
20 Han, Z., Boyle, D. L., Chang, L., Bennett, B., Karin, M., Yang, L., Manning, A. M., and Firestein, G. S., c-Jun N-terminal kinase is required for metalloproteinase expression and joint destruction in inflammatory arthritis. J. Clin. Invest., 108, 73-81 (2001)   DOI   PUBMED
21 Van Brocklyn, J. R., Graler, M. H., Bernhardt, G., Hobson, J. P., Lipp, M., and Spiegel, S., Sphingosine-1-phosphate is a ligand for the G protein-coupled receptor EDG-6. Blood., 95, 2624-2629 (2000)   PUBMED
22 Watanabe, N., Iwamoto, T., Dickinson, D. A., Iles, K. E., and Forman, H. J., Activation of the mitochondrial caspase cascade in the absence of protein synthesis does not require c-Jun Nterminal kinase. Arch. Biochem. Biophys., 405, 231-240 (2002)   DOI   ScienceOn
23 Cuvillier, O., Pirianov, G., Kleuser, B., Vanek, P. G., Coso, O. A., Gutkind, S., and Spiegel, S., Suppression of ceramide-mediated programmed cell death by sphingosine-1-phosphate. Nature, 381, 800-803 (1996)   DOI   ScienceOn
24 Zhang, H., Shi, X., Zhang, Q. J., Hampong, M., Paddon, H., Wahyuningsih, D., and Pelech, S., Nocodazole-induced p53-dependent c-Jun N-terminal Kinase Activation Reduces Apoptosis in Human Colon Carcinoma HCT116 Cells. J. Biol. Chem., 277, 43648-43658 (2002)   DOI   ScienceOn
25 Cuvillier, O., Rosenthal, D. S., Smulson, M. E., and Spiegel, S., Sphingosine 1-phosphate inhibits activation of caspases that cleave poly(ADP-ribose) polymerase and lamins during Fasand ceramide-mediated apoptosis in Jurkat T lymphocytes. J. Biol. Chem., 273, 2910-2916 (1998)   DOI   ScienceOn
26 Edsall, L. C., Pirianov, G. G., and Spiegel, S., Involvement of sphingosine 1-phosphate in nerve growth factor-mediated neuronal survival and differentiation. J. Neurosci., 17, 6952-6960 (1997)   PUBMED
27 Zanke, B. W., Boudreau, K., Rubie, E., Winnett, E., Tibbles, L. A., Zon, L., Kyriakis, J., Liu, F. F., and Woodgett, J. R., The stress-activated protein kinase pathway mediates cell death following injury induced by cis-platinum, UV irradiation or heat. Curr. Biol., 6, 606-613 (1996)   DOI   ScienceOn
28 Butterfield, L., Storey, B., Maas, L.. and Heasley, L. E., c-Jun $NH_2$-terminal kinase regulation of the apoptotic response of small cell lung cancer cells to ultraviolet radiation. J. Biol. Chem., 272, 10110-10116 (1997)   DOI   ScienceOn
29 Karliner, J. S., Honbo, N., Summers, K., Gray, M. O., and Goetzl, E. J., The lysophospholipids sphingosine-1-phosphate and lysophosphatidic acid enhance survival during hypoxia in neonatal rat cardiac myocytes. J. Mol. Cell Cardiol., 33, 1713-1717 (2001)   DOI   ScienceOn
30 Peus, D., Vasa, R. A., Beyerle, A., Meves, A., Krautmacher, C., and Pittelkow, M. R., UVB activates ERK1/2 and p38 signaling pathways via reactive oxygen species in cultured keratinocytes. J. Invest. Dermatol., 112, 751-756 (1999)   DOI   ScienceOn
31 Huang, C. L., Nordlund, J. J., and Boissy, R., Vitiligo: a manifestation of apoptosis? Am. J. Clin. Dermatol., 3, 301-308 (2002)   DOI   ScienceOn
32 Tada, A., Pereira, E., Beitner-Johnson, D., Kavanagh, R., and Abdel-Malek, Z. A., Mitogen- and ultraviolet-B-induced signaling pathways in normal human melanocytes. J. Invest. Dermatol., 118, 316-322 (2002)   DOI   ScienceOn
33 van Koppen, C. J., Meyer zu Heringdorf, D., Alemany, R., and Jakobs, K. H., Sphingosine kinase-mediated calcium signaling by muscarinic acetylcholine receptors. Life Sci., 68, 2535-2540 (2001)   DOI   ScienceOn
34 Kleuser, B., Cuvillier, O., and Spiegel, S., 1Alpha,25-dihydroxyvitamin D3 inhibits programmed cell death in HL-60 cells by activation of sphingosine kinase. Cancer Res., 58, 1817-1824 (1998)   PUBMED
35 Kwon, Y. G., Min, J. K., Kim, K. M., Lee, D. J., Billiar, T. R., and Kim, Y. M., Sphingosine 1-phosphate protects human umbilical vein endothelial cells from serum-deprived apoptosis by nitric oxide production. J. Biol. Chem., 276, 10627-10633 (2001)   DOI   ScienceOn
36 Park, K. C., Kim, D. S., Choi, H. O., Kim, K. H., Chung, J. H., Eun, H. C., Lee, J. S., and Seo, J. S., Overexpression of HSP70 prevents ultraviolet B-induced apoptosis of a human melanoma cell line. Arch. Dermatol. Res., 292, 482-487 (2000)   DOI   ScienceOn
37 Kim, Y. G., Kim, H. J., Kim, D. S., Kim, S. D., Han, W. S., Kim, K. H., Chung, J. H., and Park, K. C., Up-Regulation and redistribution of Bax in ultraviolet B-irradiated melanocytes. Pigment. Cell Res., 13, 352-357 (2000)   DOI   ScienceOn
38 Edsall, L. C., Cuvillier, O., Twitty, S., Spiegel, S., and Milstien, S., Sphingosine kinase expression regulates apoptosis and caspase activation in PC12 cells. J. Neurochem., 76, 1573-1584 (2001)   DOI   ScienceOn
39 Bain, J., McLauchlan, H., Elliott, M., and Cohen, P., The specificities of protein kinase inhibitors: an update. Biochem J, 371, 199-204 (2003)   DOI   ScienceOn
40 Eisinger, M. and Marko, O., Selective proliferation of normal human melanocytes in vitro in the presence of phorbol ester and cholera toxin. Proc. Natl. Acad. Sci. U.S.A., 79, 2018-2022 (1982)   DOI   ScienceOn
41 Park, K. H., Choi, H. O., Jang, D. D., Park, Y. I., and Park, K. C., Downregulation of Bcl-2 and activation of caspase-8 in the UVB-induced apoptosis of a cultured human melanoma cell line. Photodermatol. Photoimmunol. Photomed., 17, 218-222 (2001)   DOI   ScienceOn
42 Xia, Z., Dickens, M., Raingeaud, J., Davis, R. J., and Greenberg, M. E., Opposing effects of ERK and JNK-p38 MAP kinases on apoptosis. Science, 270, 1326-1331 (1995)   DOI   PUBMED   ScienceOn
43 Hengartner, M. O., The biochemistry of apoptosis. Nature., 407, 770-776 (2000)   DOI   PUBMED   ScienceOn