Cannabidiol induces antioxidant pathways in keratinocytes by targeting BACH1

Redox Biology - Tập 28 - Trang 101321 - 2020
Laura Casares1, Víctor García2,3, Martín Garrido-Rodríguez2,3, Estrella Millán2, Juan A. Collado2,3, Adela García-Martín4, Jon Peñarando4, Marco A. Calzado3,5,6, Laureano de la Vega1, Eduardo Muñoz3,5,6
1Jacqui Wood Cancer Centre, Division of Cellular Medicine, School of Medicine, University of Dundee, Dundee, Scotland, UK
2Innohealth Group, Madrid, Spain
3Instituto Maimónides de Investigación Biomédica de Córdoba (IMIBIC), Córdoba, Spain
4Emerald Health Biotechnology, Córdoba, Spain
5Departamento de Biología Celular, Fisiología e Inmunología, Universidad de Córdoba, Spain
6Hospital Universitario Reina Sofía, Córdoba, Spain

Tài liệu tham khảo

Finkel, 2011, Signal transduction by reactive oxygen species, J. Cell Biol., 194, 7, 10.1083/jcb.201102095 Cross, 1987, Oxygen radicals and human disease, Ann. Intern. Med., 107, 526, 10.7326/0003-4819-107-4-526 Bickers, 2006, Oxidative stress in the pathogenesis of skin disease, J. Investig. Dermatol., 126, 2565, 10.1038/sj.jid.5700340 Itoh, 1999, Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Neh2 domain, Genes Dev., 13, 76, 10.1101/gad.13.1.76 McMahon, 2003, Keap1-dependent proteasomal degradation of transcription factor Nrf2 contributes to the negative regulation of antioxidant response element-driven gene expression, J. Biol. Chem., 278, 21592, 10.1074/jbc.M300931200 Kobayashi, 2006, Nrf2-Keap1 regulation of cellular defense mechanisms against electrophiles and reactive oxygen species, Adv. Enzym. Regul., 46, 113, 10.1016/j.advenzreg.2006.01.007 Itoh, 1997, An Nrf2/small Maf heterodimer mediates the induction of phase II detoxifying enzyme genes through antioxidant response elements, Biochem. Biophys. Res. Commun., 236, 313, 10.1006/bbrc.1997.6943 Maines, 1997, The heme oxygenase system: a regulator of second messenger gases, Annu. Rev. Pharmacol. Toxicol., 37, 517, 10.1146/annurev.pharmtox.37.1.517 Gozzelino, 2010, Mechanisms of cell protection by heme oxygenase-1, Annu. Rev. Pharmacol. Toxicol., 50, 323, 10.1146/annurev.pharmtox.010909.105600 Keyse, 1989, Heme oxygenase is the major 32-kDa stress protein induced in human skin fibroblasts by UVA radiation, hydrogen peroxide, and sodium arsenite, Proc. Natl. Acad. Sci. U. S. A., 86, 99, 10.1073/pnas.86.1.99 Dhakshinamoorthy, 2005, Bach1 competes with Nrf2 leading to negative regulation of the antioxidant response element (ARE)-mediated NAD(P)H:quinone oxidoreductase 1 gene expression and induction in response to antioxidants, J. Biol. Chem., 280, 16891, 10.1074/jbc.M500166200 Shan, 2006, Role of Bach1 and Nrf2 in up-regulation of the heme oxygenase-1 gene by cobalt protoporphyrin, FASEB J., 20, 2651, 10.1096/fj.06-6346fje Reichard, 2007, Heme oxygenase-1 induction by NRF2 requires inactivation of the transcriptional repressor BACH1, Nucleic Acids Res., 35, 7074, 10.1093/nar/gkm638 MacLeod, 2009, Characterization of the cancer chemopreventive NRF2-dependent gene battery in human keratinocytes: demonstration that the KEAP1-NRF2 pathway, and not the BACH1-NRF2 pathway, controls cytoprotection against electrophiles as well as redox-cycling compounds, Carcinogenesis, 30, 1571, 10.1093/carcin/bgp176 Warnatz, 2011, The BTB and CNC homology 1 (BACH1) target genes are involved in the oxidative stress response and in control of the cell cycle, J. Biol. Chem., 286, 23521, 10.1074/jbc.M111.220178 Numata, 2009, Functional expression of heme oxygenase-1 in human differentiated epidermis and its regulation by cytokines, J. Investig. Dermatol., 129, 2594, 10.1038/jid.2009.119 Capasso, 2008, Cannabidiol, extracted from Cannabis sativa, selectively inhibits inflammatory hypermotility in mice, Br. J. Pharmacol., 154, 1001, 10.1038/bjp.2008.177 Mukhopadhyay, 2011, Cannabidiol protects against hepatic ischemia/reperfusion injury by attenuating inflammatory signaling and response, oxidative/nitrative stress, and cell death, Free Radic. Biol. Med., 50, 1368, 10.1016/j.freeradbiomed.2011.02.021 Pan, 2009, Cannabidiol attenuates cisplatin-induced nephrotoxicity by decreasing oxidative/nitrosative stress, inflammation, and cell death, J. Pharmacol. Exp. Ther., 328, 708, 10.1124/jpet.108.147181 Petrosino, 2018, Anti-inflammatory properties of cannabidiol, a nonpsychotropic cannabinoid, in experimental allergic contact dermatitis, J. Pharmacol. Exp. Ther., 365, 652, 10.1124/jpet.117.244368 Ramot, 2018, Cover Image: neuroendocrine treatment of inherited keratin disorders by cannabinoids?, Br. J. Dermatol., 178, 1469, 10.1111/bjd.16570 Chelliah, 2018, Self-initiated use of topical cannabidiol oil for epidermolysis bullosa, Pediatr. Dermatol., 35, e224, 10.1111/pde.13545 Juknat, 2012, Differential transcriptional profiles mediated by exposure to the cannabinoids cannabidiol and Delta9-tetrahydrocannabinol in BV-2 microglial cells, Br. J. Pharmacol., 165, 2512, 10.1111/j.1476-5381.2011.01461.x Juknat, 2013, Microarray and pathway analysis reveal distinct mechanisms underlying cannabinoid-mediated modulation of LPS-induced activation of BV-2 microglial cells, PLoS One, 8, 10.1371/journal.pone.0061462 Del Prete, 2016, Turmeric sesquiterpenoids: expeditious resolution, comparative bioactivity, and a new bicyclic turmeronoid, J. Nat. Prod., 79, 267, 10.1021/acs.jnatprod.5b00637 Torrente, 2017, Crosstalk between NRF2 and HIPK2 shapes cytoprotective responses, Oncogene, 36, 6204, 10.1038/onc.2017.221 Bolger, 2014, Trimmomatic: a flexible trimmer for Illumina sequence data, Bioinformatics, 30, 2114, 10.1093/bioinformatics/btu170 Kim, 2015, HISAT: a fast spliced aligner with low memory requirements, Nat. Methods, 12, 357, 10.1038/nmeth.3317 Liao, 2014, featureCounts: an efficient general purpose program for assigning sequence reads to genomic features, Bioinformatics, 30, 923, 10.1093/bioinformatics/btt656 Love, 2014, Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2, Genome Biol., 15, 550, 10.1186/s13059-014-0550-8 Kuleshov, 2016, Enrichr: a comprehensive gene set enrichment analysis web server 2016 update, Nucleic Acids Res., 44, W90, 10.1093/nar/gkw377 Benjamini, 1995, Controlling the false discovery rate - a practical and powerful approach to multiple testing, J. R. Stat. Soc. B, 57, 289 Perez-Riverol, 2019, The PRIDE database and related tools and resources in 2019: improving support for quantification data, Nucleic Acids Res., 47, D442, 10.1093/nar/gky1106 Schafer, 2015, Nrf2--A regulator of keratinocyte redox signaling, Free Radic. Biol. Med., 88, 243, 10.1016/j.freeradbiomed.2015.04.018 Kensler, 2013, Keap1-nrf2 signaling: a target for cancer prevention by sulforaphane, Top. Curr. Chem., 329, 163, 10.1007/128_2012_339 Dinkova-Kostova, 2005, Extremely potent triterpenoid inducers of the phase 2 response: correlations of protection against oxidant and inflammatory stress, Proc. Natl. Acad. Sci. U. S. A., 102, 4584, 10.1073/pnas.0500815102 Shrivastava, 2011, Cannabidiol induces programmed cell death in breast cancer cells by coordinating the cross-talk between apoptosis and autophagy, Mol. Cancer Ther., 10, 1161, 10.1158/1535-7163.MCT-10-1100 Wu, 2018, Cannabidiol induced apoptosis in human monocytes through mitochondrial permeability transition pore-mediated ROS production, Free Radic. Biol. Med., 124, 311, 10.1016/j.freeradbiomed.2018.06.023 Suzuki, 2004, Heme regulates gene expression by triggering Crm1-dependent nuclear export of BACH1, EMBO J., 23, 2544, 10.1038/sj.emboj.7600248 Zenke-Kawasaki, 2007, Heme induces ubiquitination and degradation of the transcription factor BACH1, Mol. Cell. Biol., 27, 6962, 10.1128/MCB.02415-06 Leigh, 1995, Keratins (K16 and K17) as markers of keratinocyte hyperproliferation in psoriasis in vivo and in vitro, Br. J. Dermatol., 133, 501, 10.1111/j.1365-2133.1995.tb02696.x Coulombe, 2004, Great promises yet to be fulfilled: defining keratin intermediate filament function in vivo, Eur. J. Cell Biol., 83, 735, 10.1078/0171-9335-00443 Rio, 2018, The endocannabinoid system of the skin. A potential approach for the treatment of skin disorders, Biochem. Pharmacol., 157, 122, 10.1016/j.bcp.2018.08.022 Toth, 2019, Cannabinoid signaling in the skin: therapeutic potential of the "C(ut)annabinoid" system, Molecules, 24, 10.3390/molecules24050918 Lignitto, 2019, Nrf2 activation promotes lung cancer metastasis by inhibiting the degradation of BACH1, Cell, 178, 316, 10.1016/j.cell.2019.06.003 Ichimura, 2013, Phosphorylation of p62 activates the Keap1-Nrf2 pathway during selective autophagy, Mol. Cell, 51, 618, 10.1016/j.molcel.2013.08.003 Sun, 2002, Hemoprotein Bach1 regulates enhancer availability of heme oxygenase-1 gene, EMBO J., 21, 5216, 10.1093/emboj/cdf516 Alam, 2007, How many transcription factors does it take to turn on the heme oxygenase-1 gene?, Am. J. Respir. Cell Mol. Biol., 36, 166, 10.1165/rcmb.2006-0340TR Pucci, 2013, Epigenetic control of skin differentiation genes by phytocannabinoids, Br. J. Pharmacol., 170, 581, 10.1111/bph.12309 Wilkinson, 2007, Cannabinoids inhibit human keratinocyte proliferation through a non-CB1/CB2 mechanism and have a potential therapeutic value in the treatment of psoriasis, J. Dermatol. Sci., 45, 87, 10.1016/j.jdermsci.2006.10.009 Clark, 1997, Involvement of the heme oxygenase-carbon monoxide pathway in keratinocyte proliferation, Biochem. Biophys. Res. Commun., 241, 215, 10.1006/bbrc.1997.7742 Kerns, 2007, Reprogramming of keratin biosynthesis by sulforaphane restores skin integrity in epidermolysis bullosa simplex, Proc. Natl. Acad. Sci. U. S. A., 104, 14460, 10.1073/pnas.0706486104 Kerns, 2010, Differential modulation of keratin expression by sulforaphane occurs via Nrf2-dependent and -independent pathways in skin epithelia, Mol. Biol. Cell, 21, 4068, 10.1091/mbc.e10-02-0153 Schrader, 2019, Combined tetrahydrocannabinol and cannabidiol to treat pain in epidermolysis bullosa: a report of three cases, Br. J. Dermatol., 180, 922, 10.1111/bjd.17341 Ota, 2014, Bach1 deficiency and accompanying overexpression of heme oxygenase-1 do not influence aging or tumorigenesis in mice, Oxid Med Cell Longev, 2014, 757901, 10.1155/2014/757901 Lee, 2019, Effective breast cancer combination therapy targeting BACH1 and mitochondrial metabolism, Nature, 568, 254, 10.1038/s41586-019-1005-x Wiel, 2019, BACH1 stabilization by antioxidants stimulates lung cancer metastasis, Cell, 178, 330, 10.1016/j.cell.2019.06.005