Changes in mouse epidermal DNA methylation during development of squamous cell carcinoma in response to UVR.
DNA methylation
UVR exposure
epidermis
squamous cell carcinoma
Journal
Experimental dermatology
ISSN: 1600-0625
Titre abrégé: Exp Dermatol
Pays: Denmark
ID NLM: 9301549
Informations de publication
Date de publication:
Jun 2024
Jun 2024
Historique:
revised:
13
05
2024
received:
29
06
2023
accepted:
07
06
2024
medline:
30
9
2024
pubmed:
30
9
2024
entrez:
30
9
2024
Statut:
ppublish
Résumé
Squamous cell carcinoma (SCC) is a common skin cancer, often caused by exposure to ultraviolet radiation (UVR). Recent studies have shown that changes in DNA methylation play a crucial role in the development of cancers. However, methylation patterns of SCC are not well characterised. Identifying biomarkers for the risk of developing SCC could be helpful for early detection and diagnosis and can potentially improve treatment and prevention strategies. This study aimed to investigate methylation changes in the epidermis of mice exposed to UVR for 24 weeks. We examined the DNA methylation levels of 260 199 CpGs using the Illumina Infinium Mouse Methylation BeadChip and studied the epidermis of UVR-exposed and unexposed mice every 4 weeks for 24 weeks (n = 39). We identified CpGs with large differences in methylation levels (β-values) between UVR-exposed and unexposed mice. We also observed differences in the epigenetic age of these mice. We identified CpGs in Rev, Ipmk, Rad51b, Fgfr2, Fgfr3 and Ctnnb1 that may serve as potential biomarkers for SCC risk and could be helpful for the early detection and prevention of SCC. Further investigations are necessary to determine the biological functions and clinical significance of these CpGs.
Substances chimiques
Biomarkers, Tumor
0
beta Catenin
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
e15123Subventions
Organisme : Danish Research Center for Skin Cancer
Organisme : Skin Cancer Innovation Clinical Academic Group (SCIN CAG)
Organisme : Greater Copenhagen Health Science Partners
Organisme : The Lundbeck Foundation
ID : R307-2018-3318
Informations de copyright
© 2024 The Author(s). Experimental Dermatology published by John Wiley & Sons Ltd.
Références
Fitzmaurice C, Abate D, Abbasi N, et al. Global, regional, and national cancer incidence, mortality, years of life lost, years lived with disability, and disability‐adjusted life‐years for 29 cancer groups, 1990 to 2017: a systematic analysis for the global burden of disease study. JAMA Oncol. 2019;5:1749‐1768.
Nehal KS, Bichakjian CK. Update on keratinocyte carcinomas. N Engl J Med. 2018;379:363‐374.
Halliday GM, Byrne SN, Damian DL. Ultraviolet A radiation: its role in immunosuppression and carcinogenesis. Semin Cutan Med Surg. 2011;30:214‐221.
Rangwala S, Tsai KY. Roles of the immune system in skin cancer. Br J Dermatol. 2011;165:953‐965.
Schwarz T, Schwarz A. Molecular mechanisms of ultraviolet radiation‐induced immunosuppression. Eur J Cell Biol. 2011;90:560‐564.
Hu W, Fang L, Ni R, Zhang H, Pan G. Changing trends in the disease burden of non‐melanoma skin cancer globally from 1990 to 2019 and its predicted level in 25 years. BMC Cancer. 2022;22(1):836. doi: 10.1186/s12885‐022‐09940‐3.
Leiter U, Keim U, Eigentler T, et al. Incidence, mortality, and trends of nonmelanoma skin cancer in Germany. J Invest Dermatol. 2017;137:1860‐1867.
Mouret S, Baudouin C, Charveron M, Favier A, Cadet J, Douki T. Cyclobutane pyrimidine dimers are predominant DNA lesions in whole human skin exposed to UVA radiation. Proc Natl Acad Sci USA. 2006;103:13765‐13770.
Galloway AM, Liuzzi M, Paterson MC. Metabolic processing of cyclobutyl pyrimidine dimers and (6‐4) photoproducts in UV‐treated human cells. Evidence for distinct excision‐ repair pathways. J Biol Chem. 1994;269:974‐980.
Kemp MG, Sancar A. DNA excision repair. Cell Cycle. 2012;11:2997‐3002.
Kulis M, Esteller M. DNA Methylation and Cancer. Adv Genet. 2010;70:27‐56.
Moore LD, Le T, Fan G. DNA methylation and its basic function. Neuropsychopharmacology. 2013;38:23‐38.
Meyer OS, Andersen MM, Børsting C, et al. Comparison of global DNA methylation analysis by whole genome bisulfite sequencing and the Infinium mouse methylation BeadChip using fresh and fresh‐frozen mouse epidermis. Epigenetics. 2023;18:2144574.
Zhou W, Hinoue T, Barnes B, et al. DNA methylation dynamics and dysregulation delineated by high‐throughput profiling in the mouse. Cell Genomics. 2022;2:100144.
Garcia‐Prieto CA, Álvarez‐Errico D, Musulen E, et al. Validation of a DNA methylation microarray for 285,000 CpG sites in the mouse genome. Epigenetics. 2022;17(12):1677‐1685.
Bibikova M, Barnes B, Tsan C, et al. High density DNA methylation array with single CpG site resolution. Genomics. 2011;98:288‐295.
Herceg Z, Hainaut P. Genetic and epigenetic alterations as biomarkers for cancer detection, diagnosis and prognosis. Mol Oncol. 2007;1:26‐41.
Baylin SB, Jones PA. A decade of exploring the cancer epigenome‐biological and translational implications. Nat Rev Cancer. 2011;11:726‐734.
Liouta G, Adamaki M, Tsintarakis A, et al. DNA methylation as a diagnostic, prognostic, and predictive biomarker in head and neck cancer. Int J Mol Sci. 2023;24:2996.
Micevic G, Theodosakis N, Bosenberg M. Aberrant DNA methylation in melanoma: biomarker and therapeutic opportunities. Clin Epigenetics. 2017;9:34.
Murao K, Kubo Y, Ohtani N, Hara E, Arase S. Epigenetic abnormalities in cutaneous squamous cell carcinomas: frequent inactivation of the RB1/p16 and p53 pathways. Br J Dermatol. 2006;155:999‐1005.
Rodríguez‐Paredes M, Bormann F, Raddatz G, et al. Methylation profiling identifies two subclasses of squamous cell carcinoma related to distinct cells of origin. Nat Commun. 2018;9:9.
Vandiver AR, Irizarry RA, Hansen KD, et al. Age and sun exposure‐related widespread genomic blocks of hypomethylation in nonmalignant skin. Genome Biol. 2015;16:80.
Hervás‐Marín D, Higgins F, Sanmartín O, et al. Genome wide DNA methylation profiling identifies specific epigenetic features in highrisk cutaneous squamous cell carcinoma. PLoS One. 2019;14:e0223341.
Lerche CM, Al‐Chaer RN, Wulf HC. Does systemic hydrochlorothiazide increase the risk of developing ultraviolet radiation‐induced skin tumours in hairless mice? Exp Dermatol. 2022;32:341‐347.
Hansen AB, Bech‐Thomsen N, Wulf HC. In vivo estimation of pigmentation in ultraviolet‐exposed hairless mice. Photodermatol Photoimmunol Photomed. 1995;11:14‐17.
Zhou W, Triche TJ, Laird PW, et al. SeSAMe: reducing artifactual detection of DNA methylation by Infinium BeadChips in genomic deletions. Nucleic Acids Res. 2018;46(20):e123. doi: 10.1093/nar/gky691.
R Core Team. R Core Team 2021 R: A language and environment for statistical computing. R foundation for statistical computing. 2021. https://www.R‐project.org/.
Repana D, Nulsen J, Dressler L, et al. The network of cancer genes (NCG): a comprehensive catalogue of known and candidate cancer genes from cancer sequencing screens. Genome Biol. 2019;20:1.
Baxter LL, Watkins‐Chow DE, Pavan WJ, Loftus SK. A curated gene list for expanding the horizons of pigmentation biology. Pigment Cell Melanoma Res. 2019;32:348‐358.
Lerche CM, Pinto FE, Philipsen PA, et al. High Oral vitamin D3 intake does not protect against UVR‐induced squamous cell carcinoma in mice. Anticancer Res. 2022;42:5083‐5090.
Lerche CM, Togsverd‐Bo K, Philipsen PA, et al. Impact of UVR exposure pattern on squamous cell carcinoma‐a dose–delivery and dose–response study in pigmented hairless mice. Int J Mol Sci. 2017;18(12):2738. doi: 10.3390/ijms18122738.
Guo C, Fischhaber PL, Luk‐Paszyc MJ, et al. Mouse Rev1 protein interacts with multiple DNA polymerases involved in translesion DNA synthesis. EMBO J. 2003;22:6621‐6630.
Makridakis NM, Reichardt JKV. Translesion DNA polymerases and cancer. Front Genet. 2012;3:174.
Knobel PA, Marti TM. Translesion DNA synthesis in the context of cancer research. Cancer Cell Int. 2011;11:39.
Sasatani M, Zaharieva EK, Kamiya K. The in vivo role of Rev1 in mutagenesis and carcinogenesis. Genes Environ. 2020;42:9.
Lee B, Park SJ, Hong S, Kim K, Kim S. Inositol polyphosphate multikinase signaling: multifaceted functions in health and disease. Mol Cells. 2021;44:187‐194.
Wickramasinghe VO, Savill JM, Chavali S, et al. Human inositol polyphosphate multikinase regulates transcript‐selective nuclear mRNA export to preserve genome integrity. Mol Cell. 2013;51:737‐750.
Sei Y, Zhao X, Forbes J, et al. A hereditary form of small intestinal carcinoid associated with a germline mutation in inositol polyphosphate multikinase. Gastroenterology. 2015;149:67‐78.
Takata M, Sasaki MS, Sonoda E, et al. The Rad51 paralog Rad51B promotes homologous recombinational repair. Mol Cell Biol. 2000;20:6476‐6482.
Pelttari LM, Khan S, Vuorela M, et al. RAD51B in familial breast cancer. PLoS One. 2016;11:e0153788.
Setton J, Selenica P, Mukherjee S, et al. Germline RAD51B variants confer susceptibility to breast and ovarian cancers deficient in homologous recombination. Npj. Breast Cancer. 2021;7(1):135. doi: 10.1038/s41523‐021‐00339‐0.
Yun YR, Won JE, Jeon E, et al. Fibroblast growth factors: biology, function, and application for tissue regeneration. J Tissue Eng. 2010;1:1‐18.
Hunter DJ, Kraft P, Jacobs KB, et al. A genome‐wide association study identifies alleles in FGFR2 associated with risk of sporadic postmenopausal breast cancer. Nat Genet. 2007;39:870‐874.
Katoh M, Nakagama H. FGF receptors: cancer biology and therapeutics. Med Res Rev. 2014;34:280‐300.
Qing J, Du X, Chen Y, et al. Antibody‐based targeting of FGFR3 in bladder carcinoma and t(4;14)‐positive multiple myeloma in mice. J Clin Invest. 2009;119:1216‐1229.
Liu J, Xiao Q, Xiao J, et al. Wnt/β‐catenin signalling: function, biological mechanisms, and therapeutic opportunities. Signal Transduct Target Ther. 2022;7:3.
Shang S, Hua F, Hu ZW. The regulation of β‐catenin activity and function in cancer: therapeutic opportunities. Oncotarget. 2017;8:33972‐33989.
Lau CHE, Robinson O. DNA methylation age as a biomarker for cancer. Int J Cancer. 2021;148:2652‐2663.
Yu M, Hazelton WD, Luebeck GE, Grady WM. Epigenetic aging: more than just a clock when it comes to cancer. Cancer Res. 2020;80:367‐374.
Perna L, Zhang Y, Mons U, Holleczek B, Saum KU, Brenner H. Epigenetic age acceleration predicts cancer, cardiovascular, and all‐cause mortality in a German case cohort. Clin. Epigenetics. 2016;8:8.
Zheng Y, Joyce BT, Colicino E, et al. Blood epigenetic age may predict cancer incidence and mortality. EBioMedicine. 2016;5:68‐73.
Illingworth R, Kerr A, DeSousa D, et al. A novel CpG Island set identifies tissue‐specific methylation at developmental gene loci. PLoS Biol. 2008;6:37‐51.