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In response to the accumulation of genetic mutations and cellular changes, ultraviolet radiation B (UVB) skin lesions undergo dysplasia and transform into a cutaneous squamous cell carcinoma (CSCC). Consistent with our previous findings that secreted frizzled-related protein 1 (SFRP1), a member of the SFRP gene family, was downregulated in human CSCC tissue samples, we found a significant downregulation of SFRP1 in HaCaT, A431, and SCL-1 cells after UVB irradiation. DNA methyltransferase 1 (DNMT1) was significantly increased in CSCC tissues as well as UVB-exposed A431 and SCL-1 cells. Bisulfite genomic sequencing analysis showed that the downregulation of SFRP1 was mainly due to methylation of the SFRP1 promoter, as indicated by increased methylation rate of SFRP1 after UVB irradiation in HaCaT cells. Moreover, demethylation treatment with 5-aza'-deoxycytidine (5-AzaC) increased SFRP1 expression and reduced the methylation rate of SFRP1 in HaCaT cells. Flow cytometry analyses demonstrated that 5-AzaC treatment or overexpression of SFRP1 ameliorated UVB-induced apoptosis, while knockdown of SFRP1 promoted UVB-induced apoptosis in HaCaT cells. In addition, a comet assay confirmed that 5-AzaC treatment reduced DNA damage following UVB irradiation, while knockdown of SFRP1 enhanced DNA damage following UVB irradiation. In conclusion, our study identified DNA methylation of SFRP1 as a key mediator in the UVB-induced apoptosis of keratinocytes. These findings indicate that reinforcing SFRP1 defences by 5-AzaC may help prevent UVB-induced skin damage.

Titel:	UVB-induced SFRP1 methylation potentiates skin damage by promoting cell apoptosis and DNA damage.
Autor/in / Beteiligte Person:	Liang, J ; Liu, L ; Tang, H ; Ma, Q ; Sang, Y ; Kang, X
Link:	Zum Volltext
Zeitschrift:	Experimental dermatology, Jg. 31 (2022-09-01), Heft 9, S. 1443-1453
Veröffentlichung:	Copenhagen : Munksgaard, c1992-, 2022
Medientyp:	academicJournal
ISSN:	1600-0625 (electronic)
DOI:	10.1111/exd.14621
Schlagwort:	Apoptosis DNA Damage DNA Methylation Humans Intracellular Signaling Peptides and Proteins Keratinocytes radiation effects Ultraviolet Rays adverse effects Carcinoma, Squamous Cell genetics Intercellular Signaling Peptides and Proteins metabolism Membrane Proteins metabolism Skin Neoplasms
Sonstiges:	Nachgewiesen in: MEDLINE Sprachen: English Publication Type: Journal Article Language: English [Exp Dermatol] 2022 Sep; Vol. 31 (9), pp. 1443-1453. <i>Date of Electronic Publication: </i>2022 Jun 13. MeSH Terms: Carcinoma, Squamous Cell* / genetics ; Skin Neoplasms* ; Intercellular Signaling Peptides and Proteins / metabolism ; Membrane Proteins / metabolism ; Apoptosis ; DNA Damage ; DNA Methylation ; Humans ; Intracellular Signaling Peptides and Proteins ; Keratinocytes / radiation effects ; Ultraviolet Rays / adverse effects References: Mouawad J, Saadeh F, Tabosh HA, Haddadin MJ, Gali-Muhtasib H. The photoprotective effects of 2-benzoyl-3-phenylquinoxaline 1,4-dioxide against UVB-induced damage in HaCaT cells. Med Oncol. 2016;33(8):86. ; Ullah I, Liao Y, Wan R, Tang L, Feng J. Alternative splicing of SMAD4 and its function in HaCaT cells in response to UVB irradiation. J Cancer. 2018;9(17):3177-3186. ; He Y, Hu Y, Jiang X, et al. Cyanidin-3-O-glucoside inhibits the UVB-induced ROS/COX-2 pathway in HaCaT cells. J Photochem Photobiol B. 2017;177:24-31. ; Khalil C, Shebaby W. UVB damage onset and progression 24 h post exposure in human-derived skin cells. Toxicol Rep. 2017;4:441-449. ; Rodriguez-Luna A, Avila-Roman J, Oliveira H, Motilva V, Talero E. Fucoxanthin and rosmarinic acid combination has anti-inflammatory effects through regulation of NLRP3 inflammasome in UVB-exposed HaCaT keratinocytes. Mar Drugs. 2019;17(8):451. ; Parekh V, Seykora JT. Cutaneous squamous cell carcinoma. Clin Lab Med. 2017;37(3):503-525. ; Que SKT, Zwald FO, Schmults CD. Cutaneous squamous cell carcinoma: incidence, risk factors, diagnosis, and staging. J Am Acad Dermatol. 2018;78(2):237-247. ; Zhou MJ, Zheng L, Guo L, et al. Differential responses to UVB irradiation in human keratinocytes and epidermoid carcinoma cells. Biomed Environ Sci. 2012;25(5):583-589. ; Li L, Jiang M, Feng Q, et al. Aberrant methylation changes detected in cutaneous squamous cell carcinoma of immunocompetent individuals. Cell Biochem Biophys. 2015;72(2):599-604. ; Liang J, Kang X, Halifu Y, et al. Secreted frizzled-related protein promotors are hypermethylated in cutaneous squamous carcinoma compared with normal epidermis. BMC Cancer. 2015;15:641. ; Zheng L, Sun D, Fan W, Zhang Z, Li Q, Jiang T. Diagnostic value of SFRP1 as a favorable predictive and prognostic biomarker in patients with prostate cancer. PLoS One. 2015;10(2):e0118276. ; Garcia-Tobilla P, Solorzano SR, Salido-Guadarrama I, et al. SFRP1 repression in prostate cancer is triggered by two different epigenetic mechanisms. Gene. 2016;593(2):292-301. ; Halifu Y, Liang JQ, Zeng XW, et al. Wnt1 and SFRP1 as potential prognostic factors and therapeutic targets in cutaneous squamous cell carcinoma. Genet Mol Res. 2016;15(2):gmr8187. ; Suzuki H, Watkins DN, Jair KW, et al. Epigenetic inactivation of SFRP genes allows constitutive WNT signaling in colorectal cancer. Nat Genet. 2004;36(4):417-422. ; van de Wetering M, Sancho E, Verweij C, et al. The beta-catenin/TCF-4 complex imposes a crypt progenitor phenotype on colorectal cancer cells. Cell. 2002;111(2):241-250. ; Liu-Smith F, Jia J, Zheng Y. UV-induced molecular signaling differences in melanoma and non-melanoma skin cancer. Adv Exp Med Biol. 2017;996:27-40. ; Gregory KJ, Schneider SS. Estrogen-mediated signaling is differentially affected by the expression levels of Sfrp1 in mammary epithelial cells. Cell Biol Int. 2015;39(7):873-879. ; You J, Munoz-Erazo L, Wen L, Hodge C, Madigan MC, Sutton G. In-vitro effects of secreted frizzled-related protein 1 (SFRP1) on human corneal epithelial cells. Curr Eye Res. 2018;43(4):455-459. ; Qiao B, He BX, Cai JH, Tao Q, King-Yin LA. MicroRNA-27a-3p modulates the Wnt/beta-catenin signaling pathway to promote epithelial-mesenchymal transition in oral squamous carcinoma stem cells by targeting SFRP1. Sci Rep. 2017;7:44688. ; Fuchs E, Raghavan S. Getting under the skin of epidermal morphogenesis. Nat Rev Genet. 2002;3(3):199-209. ; Lai FJ, Cheng CL, Chen ST, et al. WOX1 is essential for UVB irradiation-induced apoptosis and down-regulated via translational blockade in UVB-induced cutaneous squamous cell carcinoma in vivo. Clin Cancer Res. 2005;11(16):5769-5777. ; Yoshiki R, Kabashima K, Sakabe J, et al. The mandatory role of IL-10-producing and OX40 ligand-expressing mature Langerhans cells in local UVB-induced immunosuppression. J Immunol. 2010;184(10):5670-5677. ; Nasti TH, Iqbal O, Tamimi IA, Geise JT, Katiyar SK, Yusuf N. Differential roles of T-cell subsets in regulation of ultraviolet radiation induced cutaneous photocarcinogenesis. Photochem Photobiol. 2011;87(2):387-398. ; Ahmad I, Nasti TH, Rihan HM, Jimenez H, Elmets CA, Yusuf N. Toll-like receptor-4 deficiency inhibits ultraviolet radiation-induced tumor development by modulation of immune and inflammatory responses. Mol Carcinog. 2021;60(1):60-70. ; Song XL, Huang B, Zhou BW, et al. miR-1301-3p promotes prostate cancer stem cell expansion by targeting SFRP1 and GSK3beta. Biomed Pharmacother. 2018;99:369-374. ; Hu J, Zhao W, Huang Y, Wang Z, Jiang T, Wang L. MiR-1180 from bone marrow MSCs promotes cell proliferation and glycolysis in ovarian cancer cells via SFRP1/Wnt pathway. Cancer Cell Int. 2019;19:66. ; de Lau W, Barker N, Clevers H. WNT signaling in the normal intestine and colorectal cancer. Front Biosci. 2007;12:471-491. ; Lewis DA, Hengeltraub SF, Gao FC, Leivant MA, Spandau DF. Aberrant NF-kappaB activity in HaCaT cells alters their response to UVB signaling. J Invest Dermatol. 2006;126(8):1885-1892. Contributed Indexing: Keywords: UVB; cutaneous carcinogenesis; methylation; secreted frizzled-related protein 1; β-Catenin Substance Nomenclature: 0 (Intercellular Signaling Peptides and Proteins) ; 0 (Intracellular Signaling Peptides and Proteins) ; 0 (Membrane Proteins) ; 0 (SFRP1 protein, human) ; 0 (WD repeat containing planar cell polarity effector) Entry Date(s): Date Created: 20220603 Date Completed: 20220908 Latest Revision: 20220916 Update Code: 20231215

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UVB-induced SFRP1 methylation potentiates skin damage by promoting cell apoptosis and DNA damage.