Brahma deficiency in keratinocytes promotes UV carcinogenesis by accelerating the escape from cell cycle arrest and the formation of DNA photolesions

Botchkarev, 2012, Epigenetic regulation of gene expression in keratinocytes, J. Invest. Dermatol., 132, 2505, 10.1038/jid.2012.182 Smith, 2003, Structural analysis of the yeast SWI/SNF chromatin remodeling complex, Nat. Struct. Biol., 10, 141, 10.1038/nsb888 Masliah-Planchon, 2015, SWI/SNF chromatin remodeling and human malignancies, Annu. Rev. Pathol., 10, 145, 10.1146/annurev-pathol-012414-040445 Halliday, 2009, SWI/SNF: a chromatin remodelling complex with a role in carcinogenesis, Int. J. Biochem. Cell Biol., 41, 725, 10.1016/j.biocel.2008.04.026 Farrell, 2011, Chromatin structure following UV-induced DNA damage – repair or death?, Int. J. Mol. Sci., 12, 8063, 10.3390/ijms12118063 Brownlee, 2015, The SWI/SNF chromatin remodelling complex: its role in maintaining genome stability and preventing tumourigenesis, DNA Repair, 32, 127, 10.1016/j.dnarep.2015.04.023 Reyes, 1998, Altered control of cellular proliferation in the absence of mammalian brahma (SNF2alpha), EMBO J., 17, 6979, 10.1093/emboj/17.23.6979 Muchardt, 1998, Ras transformation is associated with decreased expression of the brm/SNF2alpha ATPase from the mammalian SWI-SNF complex, EMBO J., 17, 223, 10.1093/emboj/17.1.223 Xu, 2007, The activity of p53 is differentially regulated by Brm- and Brg1-containing SWI/SNF chromatin remodeling complexes, J. Biol. Chem., 282, 37429, 10.1074/jbc.M706039200 Pasic, 2018, Two BRM promoter polymorphisms predict poor survival in patients with hepatocellular carcinoma, Mol. Carcinog., 57, 106, 10.1002/mc.22736 Soufir, 2004, INK4a-ARF mutations in skin carcinomas from UV irradiated hairless mice, Mol. Carcinog., 39, 195, 10.1002/mc.20004 Rebel, 2012, UV-induced ablation of the epidermal basal layer including p53-mutant clones resets UV carcinogenesis showing squamous cell carcinomas to originate from interfollicular epidermis, Carcinogenesis, 10.1093/carcin/bgs004 Versteege, 1998, Truncating mutations of hSNF5/INI1 in aggressive paediatric cancer, Nature, 394, 203, 10.1038/28212 Kadoch, 2013, Proteomic and bioinformatic analysis of mammalian SWI/SNF complexes identifies extensive roles in human malignancy, Nat. Genet., 45, 592, 10.1038/ng.2628 Reisman, 2003, Loss of BRG1/BRM in human lung cancer cell lines and primary lung cancers: correlation with poor prognosis, Cancer Res., 63, 560 Shain, 2013, The spectrum of SWI/SNF mutations, ubiquitous in human cancers, PLoS One, 8, 10.1371/journal.pone.0055119 Moloney, 2009, Hotspot mutation of BRM in non-melanoma skin cancer, J. Invest. Dermatol., 129, 1012, 10.1038/jid.2008.319 Bock, 2011, BRM and BRG1 subunits of the SWI/SNF chromatin remodelling complex are downregulated upon progression of benign skin lesions into invasive tumours, Br. J. Dermatol., 164, 1221, 10.1111/j.1365-2133.2011.10267.x Halliday, 2012, The absence of Brm exacerbates photocarcinogenesis, Exp. Dermatol., 21, 599, 10.1111/j.1600-0625.2012.01522.x Hassan, 2014, Brm inhibits the proliferative response of keratinocytes and corneal epithelial cells to ultraviolet radiation-induced damage, PLoS One, 9, 10.1371/journal.pone.0107931 Dlugosz, 1995, Isolation and utilization of epidermal keratinocytes for oncogene research, Methods Enzymol., 254, 3, 10.1016/0076-6879(95)54003-2 Boukamp, 1988, Normal keratinization in a spontaneously immortalized aneuploid human keratinocyte cell line, J. Cell Biol., 106, 761, 10.1083/jcb.106.3.761 Thompson, 2015, Nicotinamide enhances repair of arsenic and ultraviolet radiation-induced DNA damage in HaCaT keratinocytes and ex vivo human skin, PLoS One, 10, 10.1371/journal.pone.0117491 Thompson, 2015, Induction of functional Brm protein from Brm knockout mice, Oncoscience, 2, 349, 10.18632/oncoscience.153 Halliday, 2008, Inflammatory doses of UV may not be necessary for skin carcinogenesis, Photochem. Photobiol., 84, 272, 10.1111/j.1751-1097.2007.00247.x Wikonkal, 1999, Ultraviolet radiation induced signature mutations in photocarcinogenesis, J. Investig. Dermatol. Symp. Proc., 4, 6, 10.1038/sj.jidsp.5640173 Nakagawa, 1998, Three-dimensional visualization of ultraviolet-induced DNA damage and its repair in human cell nuclei, J. Invest. Dermatol., 110, 143, 10.1046/j.1523-1747.1998.00100.x Sreevidya, 2010, Agents that reverse UV-Induced immune suppression and photocarcinogenesis affect DNA repair, J. Invest. Dermatol., 130, 1428, 10.1038/jid.2009.329 Limsirichaikul, 2009, A rapid non-radioactive technique for measurement of repair synthesis in primary human fibroblasts by incorporation of ethynyl deoxyuridine (EdU), Nucl. Acids Res., 37, e31, 10.1093/nar/gkp023 Kao, 2001, Detection of repair activity during the DNA damage-induced G2 delay in human cancer cells, Oncogene, 20, 3486, 10.1038/sj.onc.1204445 Al-Khalaf, 2014, ATR controls the UV-related upregulation of the CDKN1A mRNA in a Cdk1/HuR-dependent manner, Mol. Carcinog., 53, 979, 10.1002/mc.22066 Agami, 2000, Distinct initiation and maintenance mechanisms cooperate to induce G1 cell cycle arrest in response to DNA damage, Cell, 102, 55, 10.1016/S0092-8674(00)00010-6 Berton, 2001, Ultraviolet-B irradiation alters the cell cycle machinery in murine epidermis in vivo, J. Invest. Dermatol., 117, 1171, 10.1046/j.0022-202x.2001.01536.x Kim, 2002, Ultraviolet-B-induced G1 arrest is mediated by downregulation of cyclin-dependent kinase 4 in transformed keratinocytes lacking functional p53, J. Invest. Dermatol., 118, 818, 10.1046/j.1523-1747.2002.01734.x Santra, 2009, F-box protein FBXO31 mediates cyclin D1 degradation to induce G1 arrest after DNA damage, Nature, 459, 722, 10.1038/nature08011 Pontano, 2008, Genotoxic stress-induced cyclin D1 phosphorylation and proteolysis are required for genomic stability, Mol. Cell. Biol., 28, 7245, 10.1128/MCB.01085-08 Athar, 2000, Mechanism of ultraviolet B-induced cell cycle arrest in G2/M phase in immortalized skin keratinocytes with defective p53, Biochem. Biophys. Res. Commun., 277, 107, 10.1006/bbrc.2000.3436 Pavey, 2001, G2 phase cell cycle arrest in human skin following UV irradiation, Oncogene, 20, 6103, 10.1038/sj.onc.1204707 Bourachot, 2003, Growth inhibition by the mammalian SWI-SNF subunit Brm is regulated by acetylation, EMBO J., 22, 6505, 10.1093/emboj/cdg621 Otto, 2017, Cell cycle proteins as promising targets in cancer therapy, Nat. Rev. Cancer, 17, 93, 10.1038/nrc.2016.138 Trouche, 1997, RB and hbrm cooperate to repress the activation functions of E2F1, Proc. Natl. Acad. Sci. U.S.A., 94, 11268, 10.1073/pnas.94.21.11268 Strober, 1996, Functional interactions between the hBRM/hBRG1 transcriptional activators and the pRB family of proteins, Mol. Cell. Biol., 16, 1576, 10.1128/MCB.16.4.1576 Takeshima, 2015, Frequent involvement of chromatin remodeler alterations in gastric field cancerization, Cancer Lett., 357, 328, 10.1016/j.canlet.2014.11.038 Zhang, 2017, BRM/SMARCA2 promotes the proliferation and chemoresistance of pancreatic cancer cells by targeting JAK2/STAT3 signaling, Cancer Lett., 402, 213, 10.1016/j.canlet.2017.05.006 Indra, 2005, Temporally controlled targeted somatic mutagenesis in embryonic surface ectoderm and fetal epidermal keratinocytes unveils two distinct developmental functions of BRG1 in limb morphogenesis and skin barrier formation, Development, 132, 4533, 10.1242/dev.02019 Strobeck, 2002, Compensation of BRG-1 function by Brm: insight into the role of the core SWI-SNF subunits in retinoblastoma tumor suppressor signaling, J. Biol. Chem., 277, 4782, 10.1074/jbc.M109532200 Marquez-Vilendrer, 2016, BRG1 and BRM loss selectively impacts RB and P53, respectively: BRG1 and BRM have differential functions in vivo, Oncoscience, 3, 337, 10.18632/oncoscience.333 Maeda, 2002, Role of p21(Waf-1) in regulating the G1 and G2/M checkpoints in ultraviolet-irradiated keratinocytes, J. Invest. Dermatol., 119, 513, 10.1046/j.1523-1747.2002.01828.x Hanahan, 2011, Hallmarks of cancer: the next generation, Cell, 144, 646, 10.1016/j.cell.2011.02.013 Pfeifer, 2012, UV wavelength-dependent DNA damage and human non-melanoma and melanoma skin cancer, Photochem. Photobiol. Sci., 11, 90, 10.1039/C1PP05144J