UVB radiation represses CYLD expression in melanocytes

Kuphal,Silke; Schneider,Nadja; Massoumi,Ramin; Hellerbrand,Claus; Bosserhoff,Anja  Katrin

doi:10.3892/ol.2017.7120

UVB radiation represses CYLD expression in melanocytes

Authors:
- Silke Kuphal
- Nadja Schneider
- Ramin Massoumi
- Claus Hellerbrand
- Anja Katrin Bosserhoff
View Affiliations

Affiliations: Emil‑Fischer‑Center, Institute of Biochemistry, Friedrich Alexander University Erlangen‑Nuremberg, D‑91054 Erlangen, Germany, Department of Laboratory Medicine, Translational Cancer Research, Lund University, SE‑221 00 Lund, Sweden
Published online on: October 3, 2017 https://doi.org/10.3892/ol.2017.7120
Pages: 7262-7268
Copyright: © Kuphal et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )

Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )

Cited By (CrossRef): 0 citations Loading Articles...

Abstract

CYLD lysine 63 deubiquitinase (CYLD) was originally identified as a tumor suppressor that is mutated in familial cylindromatosis. Unlike in cylindromatosis, downregulation of the deubiquitinase CYLD in melanoma, a highly aggressive tumor, is not caused by mutations in the CYLD gene, but rather by a constitutive and high expression of the snail family transcriptional repressor 1 (SNAIL1). A reduced CYLD level leads to B‑cell lymphoma‑3/p50/p52‑dependent nuclear factor‑κB activation, which in turn triggers the expression of genes such as cyclin D1 and N‑cadherin. Elevated levels of cyclin D1 and N‑cadherin promote melanoma proliferation and invasion. By analyzing the regulation of CYLD expression in melanocytes, the present study identified a signaling pathway that is regulated in response to ultraviolet B (UVB) radiation in melanocytes. UVB light leads to an extracellular signal‑regulated kinase‑mediated induction of SNAIL1 and subsequent downregulation of CYLD expression in normal human epithelial melanocytes. The UVB‑mediated suppression of CYLD in melanocytes may have a key role in the reaction to UV stimuli, and may also potentially be involved in the early malignant transformation processes.

View Figures

View References

1	Rowe CJ and Khosrotehrani K: Clinical and biological determinants of melanoma progression: Should all be considered for clinical management? Australas J Dermatol. 57:175–181. 2016. View Article : Google Scholar : PubMed/NCBI
2	Qadir MI: Skin cancer: Etiology and management. Pak J Pharm Sci. 29:999–1003. 2016.PubMed/NCBI
3	Cui R, Widlund HR, Feige E, Lin JY, Wilensky DL, Igras VE, D'Orazio J, Fung CY, Schanbacher CF, Granter SR and Fisher DE: Central role of p53 in the suntan response and pathologic hyperpigmentation. Cell. 128:853–864. 2007. View Article : Google Scholar : PubMed/NCBI
4	Bastian BC: The molecular pathology of melanoma: An integrated taxonomy of melanocytic neoplasia. Annu Rev Pathol. 9:239–271. 2014. View Article : Google Scholar : PubMed/NCBI
5	Premi S, Wallisch S, Mano CM, Weiner AB, Bacchiocchi A, Wakamatsu K, Bechara EJ, Halaban R, Douki T and Brash DE: Photochemistry. Chemiexcitation of melanin derivatives induces DNA photoproducts long after UV exposure. Science. 347:842–847. 2015. View Article : Google Scholar : PubMed/NCBI
6	Nishisgori C: Current concept of photocarcinogenesis. Photochem Photobiol Sci. 14:1713–1721. 2015. View Article : Google Scholar : PubMed/NCBI
7	de Gruijl FR: Photocarcinogenesis: UVA vs UVB. Methods Enzymol. 319:359–366. 2000. View Article : Google Scholar : PubMed/NCBI
8	Tornaletti S and Pfeifer GP: UV damage and repair mechanisms in mammalian cells. Bioessays. 18:221–228. 1996. View Article : Google Scholar : PubMed/NCBI
9	Seebode C, Lehmann J and Emmert S: Photocarcinogenesis and Skin Cancer Prevention Strategies. Anticancer Res. 36:1371–1378. 2016.PubMed/NCBI
10	De Fabo EC, Noonan FP, Fears T and Merlino G: Ultraviolet B but not ultraviolet A radiation initiates melanoma. Cancer Res. 64:6372–6376. 2004. View Article : Google Scholar : PubMed/NCBI
11	Noonan FP, Recio JA, Takayama H, Duray P, Anver MR, Rush WL, De Fabo EC and Merlino G: Neonatal sunburn and melanoma in mice. Nature. 413:271–272. 2001. View Article : Google Scholar : PubMed/NCBI
12	Halliday GM, Agar NS, Barnetson RS, Ananthaswamy HN and Jones AM: UV-A fingerprint mutations in human skin cancer. Photochem Photobiol. 81:3–8. 2005. View Article : Google Scholar : PubMed/NCBI
13	Gandini S, Sera F, Cattaruzza MS, Pasquini P, Picconi O, Boyle P and Melchi CF: Meta-analysis of risk factors for cutaneous melanoma: II. Sun exposure. Eur J Cancer. 41:45–60. 2005. View Article : Google Scholar : PubMed/NCBI
14	Bignell GR, Warren W, Seal S, Takahashi M, Rapley E, Barfoot R, Green H, Brown C, Biggs PJ, Lakhani SR, et al: Identification of the familial cylindromatosis tumour-suppressor gene. Nat Genet. 25:160–165. 2000. View Article : Google Scholar : PubMed/NCBI
15	Kuphal S, Shaw-Hallgren G, Eberl M, Karrer S, Aberger F, Bosserhoff AK and Massoumi R: GLI1-dependent transcriptional repression of CYLD in basal cell carcinoma. Oncogene. 30:4523–4530. 2011. View Article : Google Scholar : PubMed/NCBI
16	Massoumi R, Kuphal S, Hellerbrand C, Haas B, Wild P, Spruss T, Pfeifer A, Fässler R and Bosserhoff AK: Down-regulation of CYLD expression by Snail promotes tumor progression in malignant melanoma. J Exp Med. 206:221–232. 2009. View Article : Google Scholar : PubMed/NCBI
17	Kuphal S, Palm HG, Poser I and Bosserhoff AK: Snail-regulated genes in malignant melanoma. Melanoma Res. 15:305–313. 2005. View Article : Google Scholar : PubMed/NCBI
18	Ziegler-Heitbrock HW, Munker R, Johnson J, Petersmann I, Schmoeckel C and Riethmuller G: In vitro differentiation of human melanoma cells analyzed with monoclonal antibodies. Cancer Res. 45:1344–1350. 1985.PubMed/NCBI
19	Tsuji T and Karasek M: A procedure for the isolation of primary cultures of melanocytes from newborn and adult human skin. J Invest Dermatol. 81:179–180. 1983. View Article : Google Scholar : PubMed/NCBI
20	Spangler B, Kappelmann M, Schittek B, Meierjohann S, Vardimon L, Bosserhoff AK and Kuphal S: ETS-1/RhoC signaling regulates the transcription factor c-Jun in melanoma. Int J Cancer. 130:2801–2811. 2012. View Article : Google Scholar : PubMed/NCBI
21	Massoumi R, Chmielarska K, Hennecke K, Pfeifer A and Fässler R: Cyld inhibits tumor cell proliferation by blocking Bcl-3-dependent NF-kappaB signaling. Cell. 125:665–677. 2006. View Article : Google Scholar : PubMed/NCBI
22	Jobin C, Hellerbrand C, Licato LL, Brenner DA and Sartor RB: Mediation by NF-kappa B of cytokine induced expression of intercellular adhesion molecule 1 (ICAM-1) in an intestinal epithelial cell line, a process blocked by proteasome inhibitors. Gut. 42:779–787. 1998. View Article : Google Scholar : PubMed/NCBI
23	Kuphal S, Poser I, Jobin C, Hellerbrand C and Bosserhoff AK: Loss of E-cadherin leads to upregulation of NFkappaB activity in malignant melanoma. Oncogene. 23:8509–8519. 2004. View Article : Google Scholar : PubMed/NCBI
24	Barberà MJ, Puig I, Domínguez D, Julien-Grille S, Guaita-Esteruelas S, Peiró S, Baulida J, Francí C, Dedhar S, Larue L, et al: Regulation of Snail transcription during epithelial to mesenchymal transition of tumor cells. Oncogene. 23:7345–7354. 2004. View Article : Google Scholar : PubMed/NCBI
25	Hellerbrand C, Jobin C, Iimuro Y, Licato L, Sartor RB and Brenner DA: Inhibition of NFkappaB in activated rat hepatic stellate cells by proteasome inhibitors and an IkappaB super-repressor. Hepatology. 27:1285–1295. 1998. View Article : Google Scholar : PubMed/NCBI
26	Schartl M, Larue L, Goda M, Bosenberg MW, Hashimoto H and Kelsh RN: What is a vertebrate pigment cell? Pigment Cell Melanoma Res. 29:8–14. 2016. View Article : Google Scholar : PubMed/NCBI
27	Guadarrama-Orozco JA, Ortega-Gómez A, Ruiz-García EB, Astudillo-de la Vega H, Meneses-García A and Lopez-Camarillo C: Braf V600E mutation in melanoma: Translational current scenario. Clin Transl Oncol. 18:863–871. 2016. View Article : Google Scholar : PubMed/NCBI
28	Brenner M, Degitz K, Besch R and Berking C: Differential expression of melanoma-associated growth factors in keratinocytes and fibroblasts by ultraviolet A and ultraviolet B radiation. Br J Dermatol. 153:733–739. 2005. View Article : Google Scholar : PubMed/NCBI
29	Jhappan C, Noonan FP and Merlino G: Ultraviolet radiation and cutaneous malignant melanoma. Oncogene. 22:3099–3112. 2003. View Article : Google Scholar : PubMed/NCBI
30	Esparza-Soto M, Fox P and Westerhoff P: Transformation of molecular weight distributions of dissolved organic carbon and UV-absorbing compounds at full-scale wastewater-treatment plants. Water Environ Res. 78:253–262. 2006. View Article : Google Scholar : PubMed/NCBI
31	Pak BJ, Lee J, Thai BL, Fuchs SY, Shaked Y, Ronai Z, Kerbel RS and Ben-David Y: Radiation resistance of human melanoma analysed by retroviral insertional mutagenesis reveals a possible role for dopachrome tautomerase. Oncogene. 23:30–38. 2004. View Article : Google Scholar : PubMed/NCBI
32	Peus D, Meves A, Vasa RA, Beyerle A, O'Brien T and Pittelkow MR: H2O2 is required for UVB-induced EGF receptor and downstream signaling pathway activation. Free Radic Biol Med. 27:1197–1202. 1999. View Article : Google Scholar : PubMed/NCBI
33	Ip YT: Transcriptional regulation. Converting an activator into a repressor. Curr Biol. 5:1–3. 1995. View Article : Google Scholar : PubMed/NCBI
34	Ip YT, Park RE, Kosman D, Yazdanbakhsh K and Levine M: dorsal-twist interactions establish snail expression in the presumptive mesoderm of the Drosophila embryo. Genes Dev. 6:1518–1530. 1992. View Article : Google Scholar : PubMed/NCBI
35	Marchal L, Foucaul A, Patissier G, Rosant JM and Legrand J: Influence of flow patterns on chromatographic efficiency in centrifugal partition chromatography. J Chromatogr A. 869:339–352. 2000. View Article : Google Scholar : PubMed/NCBI