NRF2, a crucial modulator of skin cells protection against vitiligo, psoriasis, and cancer.


Journal

BioFactors (Oxford, England)
ISSN: 1872-8081
Titre abrégé: Biofactors
Pays: Netherlands
ID NLM: 8807441

Informations de publication

Date de publication:
Mar 2023
Historique:
received: 30 08 2022
accepted: 05 10 2022
medline: 14 4 2023
pubmed: 1 11 2022
entrez: 31 10 2022
Statut: ppublish

Résumé

The skin represents a physical barrier between the organism and the environment that has evolved to confer protection against biological, chemical, and physical insults. The inner layer, known as dermis, is constituted by connective tissue and different types of immune cells whereas the outer layer, the epidermis, is composed by different layers of keratinocytes and an abundant number of melanocytes, localized in the stratum basale of the epidermis. Oxidative stress is a common alteration of inflammatory skin disorders such as vitiligo, dermatitis, or psoriasis but can also play a causal role in skin carcinogenesis and tumor progression. Nuclear factor (erythroid-derived 2)-like 2 (NRF2) has emerged as a crucial regulator of cell defense mechanisms activating complex transcriptional programs that facilitate reactive oxygen species detoxification, repair oxidative damage and prevent xenobiotic-induced toxicity. Accumulating evidence suggests that the keratinocytes, melanocytes, and other skin cell types express high levels of NRF2, which is known to play a pivotal role in the skin homeostasis, differentiation, and metabolism during normal and pathologic conditions. In the present review, we summarize the current evidence linking NRF2 to skin pathophysiology and we discuss some recent modulators of NRF2 activity that have shown a therapeutic efficacy in skin protection against tumor initiation and common inflammatory skin conditions such as vitiligo or psoriasis, with a particular emphasis on natural compounds.

Identifiants

pubmed: 36310374
doi: 10.1002/biof.1912
doi:

Substances chimiques

NF-E2-Related Factor 2 0

Types de publication

Journal Article Review

Langues

eng

Sous-ensembles de citation

IM

Pagination

228-250

Informations de copyright

© 2022 International Union of Biochemistry and Molecular Biology.

Références

Proksch E, Brandner JM, Jensen JM. The skin: an indispensable barrier. Exp Dermatol. 2008;17:1063-72.
Hennig P, Fenini G, Di Filippo M, Beer HD. Electrophiles against (skin) diseases: More than Nrf2. Biomolecules. 2020;10(2):271.
Kanitakis J. Anatomy, histology and immunohistochemistry of normal human skin. Eur J Dermatol. 2002;12:390-9. quiz 400-391.
Madison KC. Barrier function of the skin: “la raison d'etre” of the epidermis. J Invest Dermatol. 2003;121:231-41.
Menon GK, Cleary GW, Lane ME. The structure and function of the stratum corneum. Int J Pharm. 2012;435:3-9.
Chambers ES, Vukmanovic-Stejic M. Skin barrier immunity and ageing. Immunology. 2020;160:116-25.
Boo YC. Natural Nrf2 modulators for skin protection. Antioxidants (Basel). 2020;9(9):812.
Moi P, Chan K, Asunis I, Cao A, Kan YW. Isolation of NF-E2-related factor 2 (Nrf2), a NF-E2-like basic leucine zipper transcriptional activator that binds to the tandem NF-E2/AP1 repeat of the beta-globin locus control region. Proc Natl Acad Sci U S A. 1994;91:9926-30.
Rushmore TH, King RG, Paulson KE, Pickett CB. Regulation of glutathione S-transferase Ya subunit gene expression: identification of a unique xenobiotic-responsive element controlling inducible expression by planar aromatic compounds. Proc Natl Acad Sci U S A. 1990;87:3826-30.
Rushmore TH, Pickett CB. Transcriptional regulation of the rat glutathione S-transferase Ya subunit gene. Characterization of a xenobiotic-responsive element controlling inducible expression by phenolic antioxidants. J Biol Chem. 1990;265:14648-53.
Rushmore TH, Morton MR, Pickett CB. The antioxidant responsive element. Activation by oxidative stress and identification of the DNA consensus sequence required for functional activity. J Biol Chem. 1991;266:11632-9.
Itoh K, Wakabayashi N, Katoh Y, Ishii T, Igarashi K, Engel JD, et al. Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Neh2 domain. Genes Dev. 1999;13:76-86.
Cullinan SB, Gordan JD, Jin J, Harper JW, Diehl JA. The Keap1-BTB protein is an adaptor that bridges Nrf2 to a Cul3-based E3 ligase: oxidative stress sensing by a Cul3-Keap1 ligase. Mol Cell Biol. 2004;24:8477-86.
Kobayashi A, Kang MI, Okawa H, Ohtsuji M, Zenke Y, Chiba T, et al. Oxidative stress sensor Keap1 functions as an adaptor for Cul3-based E3 ligase to regulate proteasomal degradation of Nrf2. Mol Cell Biol. 2004;24:7130-9.
Zhang DD, Lo SC, Cross JV, Templeton DJ, Hannink M. Keap1 is a redox-regulated substrate adaptor protein for a Cul3-dependent ubiquitin ligase complex. Mol Cell Biol. 2004;24:10941-53.
Suzuki T, Yamamoto M. Molecular basis of the Keap1-Nrf2 system. Free Radic Biol Med. 2015;88:93-100.
Zipper LM, Mulcahy RT. The Keap1 BTB/POZ dimerization function is required to sequester Nrf2 in cytoplasm. J Biol Chem. 2002;277:36544-52.
McMahon M, Thomas N, Itoh K, Yamamoto M, Hayes JD. Redox-regulated turnover of Nrf2 is determined by at least two separate protein domains, the redox-sensitive Neh2 degron and the redox-insensitive Neh6 degron. J Biol Chem. 2004;279:31556-67.
Wang H, Liu K, Geng M, Gao P, Wu X, Hai Y, et al. RXRalpha inhibits the NRF2-ARE signaling pathway through a direct interaction with the Neh7 domain of NRF2. Cancer Res. 2013;73:3097-108.
Motohashi H, Katsuoka F, Engel JD, Yamamoto M. Small Maf proteins serve as transcriptional cofactors for keratinocyte differentiation in the Keap1-Nrf2 regulatory pathway. Proc Natl Acad Sci U S A. 2004;101:6379-84.
Kansanen E, Kuosmanen SM, Leinonen H, Levonen AL. The Keap1-Nrf2 pathway: mechanisms of activation and dysregulation in cancer. Redox Biol. 2013;1:45-9.
Katoh Y, Itoh K, Yoshida E, Miyagishi M, Fukamizu A, Yamamoto M. Two domains of Nrf2 cooperatively bind CBP, a CREB binding protein, and synergistically activate transcription. Genes Cells. 2001;6:857-68.
Nioi P, Nguyen T, Sherratt PJ, Pickett CB. The carboxy-terminal Neh3 domain of Nrf2 is required for transcriptional activation. Mol Cell Biol. 2005;25:10895-906.
Rada P, Rojo AI, Chowdhry S, McMahon M, Hayes JD, Cuadrado A. SCF/{beta}-TrCP promotes glycogen synthase kinase 3-dependent degradation of the Nrf2 transcription factor in a Keap1-independent manner. Mol Cell Biol. 2011;31:1121-33.
Chowdhry S, Zhang Y, McMahon M, Sutherland C, Cuadrado A, Hayes JD. Nrf2 is controlled by two distinct beta-TrCP recognition motifs in its Neh6 domain, one of which can be modulated by GSK-3 activity. Oncogene. 2013;32:3765-81.
Li X, Zhang D, Hannink M, Beamer LJ. Crystal structure of the Kelch domain of human Keap1. J Biol Chem. 2004;279:54750-8.
Ogura T, Tong KI, Mio K, Maruyama Y, Kurokawa H, Sato C, et al. Keap1 is a forked-stem dimer structure with two large spheres enclosing the intervening, double glycine repeat, and C-terminal domains. Proc Natl Acad Sci U S A. 2010;107:2842-7.
Quinto I, Scala G, Mallardo M, Arcucci A, Ruocco MR, De Lorenzo F. Spontaneous and mutagen-mediated amplification of a neo gene integrated at different genomic sites in rat 2 fibroblasts. Carcinogenesis. 1992;13:439-45.
Tong KI, Katoh Y, Kusunoki H, Itoh K, Tanaka T, Yamamoto M. Keap1 recruits Neh2 through binding to ETGE and DLG motifs: characterization of the two-site molecular recognition model. Mol Cell Biol. 2006;26:2887-900.
Taguchi K, Motohashi H, Yamamoto M. Molecular mechanisms of the Keap1-Nrf2 pathway in stress response and cancer evolution. Genes Cells. 2011;16:123-40.
Motohashi H, O'Connor T, Katsuoka F, Engel JD, Yamamoto M. Integration and diversity of the regulatory network composed of Maf and CNC families of transcription factors. Gene. 2002;294:1-12.
Xu C, Li CY, Kong AN. Induction of phase I, II and III drug metabolism/transport by xenobiotics. Arch Pharm Res. 2005;28:249-68.
Wu KC, Cui JY, Klaassen CD. Effect of graded Nrf2 activation on phase-I and -II drug metabolizing enzymes and transporters in mouse liver. PLoS one. 2012;7:e39006.
Itoh K, Chiba T, Takahashi S, Ishii T, Igarashi K, Katoh Y, et al. An Nrf2/small Maf heterodimer mediates the induction of phase II detoxifying enzyme genes through antioxidant response elements. Biochem Biophys Res Commun. 1997;236:313-22.
Keum YS. Regulation of Nrf2-mediated phase II detoxification and anti-oxidant genes. Biomol Ther (Seoul). 2012;20:144-51.
Vollrath V, Wielandt AM, Iruretagoyena M, Chianale J. Role of Nrf2 in the regulation of the Mrp2 (ABCC2) gene. Biochem J. 2006;395:599-609.
Cornejo P, Vargas R, Videla LA. Nrf2-regulated phase-II detoxification enzymes and phase-III transporters are induced by thyroid hormone in rat liver. Biofactors. 2013;39:514-21.
Higgins LG, Kelleher MO, Eggleston IM, Itoh K, Yamamoto M, Hayes JD. Transcription factor Nrf2 mediates an adaptive response to sulforaphane that protects fibroblasts in vitro against the cytotoxic effects of electrophiles, peroxides and redox-cycling agents. Toxicol Appl Pharmacol. 2009;237:267-80.
Kumar H, Kim IS, More SV, Kim BW, Choi DK. Natural product-derived pharmacological modulators of Nrf2/ARE pathway for chronic diseases. Nat Prod Rep. 2014;31:109-39.
Hawkes HJ, Karlenius TC, Tonissen KF. Regulation of the human thioredoxin gene promoter and its key substrates: a study of functional and putative regulatory elements. Biochim Biophys Acta. 2014;1840:303-14.
He F, Antonucci L, Karin M. NRF2 as a regulator of cell metabolism and inflammation in cancer. Carcinogenesis. 2020;41:405-16.
Ding H, Chen Z, Wu K, Huang SM, Wu WL, LeBoeuf SE, et al. Activation of the NRF2 antioxidant program sensitizes tumors to G6PD inhibition. Sci Adv. 2021;7:eabk1023.
Mitsuishi Y, Taguchi K, Kawatani Y, Shibata T, Nukiwa T, Aburatani H, et al. Nrf2 redirects glucose and glutamine into anabolic pathways in metabolic reprogramming. Cancer Cell. 2012;22:66-79.
Harland AT, Rosen CJ. Impediments to the recovery of restitution by crime victims. Violence Vict. 1990;5:127-40.
Dinkova-Kostova AT, Abramov AY. The emerging role of Nrf2 in mitochondrial function. Free Radic Biol Med. 2015;88:179-88.
Liu Y, Pang Y, Caisova V, Ding J, Yu D, Zhou Y, et al. Targeting NRF2-governed glutathione synthesis for SDHB-mutated Pheochromocytoma and Paraganglioma. Cancer. 2020;12(2):280.
Wardyn JD, Ponsford AH, Sanderson CM. Dissecting molecular cross-talk between Nrf2 and NF-kappaB response pathways. Biochem Soc Trans. 2015;43:621-6.
Li W, Khor TO, Xu C, Shen G, Jeong WS, Yu S, et al. Activation of Nrf2-antioxidant signaling attenuates NFkappaB-inflammatory response and elicits apoptosis. Biochem Pharmacol. 2008;76:1485-9.
Yu M, Li H, Liu Q, Liu F, Tang L, Li C, et al. Nuclear factor p65 interacts with Keap1 to repress the Nrf2-ARE pathway. Cell Signal. 2011;23:883-92.
Liu GH, Qu J, Shen X. NF-kappaB/p65 antagonizes Nrf2-ARE pathway by depriving CBP from Nrf2 and facilitating recruitment of HDAC3 to MafK. Biochim Biophys Acta. 2008;1783:713-27.
Soares MP, Seldon MP, Gregoire IP, Vassilevskaia T, Berberat PO, Yu J, et al. Heme oxygenase-1 modulates the expression of adhesion molecules associated with endothelial cell activation. J Immunol. 2004;172:3553-63.
Ganesh Yerra V, Negi G, Sharma SS, Kumar A. Potential therapeutic effects of the simultaneous targeting of the Nrf2 and NF-kappaB pathways in diabetic neuropathy. Redox Biol. 2013;1:394-7.
Hou Y, Wang Y, He Q, Li L, Xie H, Zhao Y, et al. Nrf2 inhibits NLRP3 inflammasome activation through regulating Trx1/TXNIP complex in cerebral ischemia reperfusion injury. Behav Brain Res. 2018;336:32-9.
Girotti AW, Kriska T. Role of lipid hydroperoxides in photo-oxidative stress signaling. Antioxid Redox Signal. 2004;6:301-10.
Eiberger W, Volkmer B, Amouroux R, Dhérin C, Radicella JP, Epe B. Oxidative stress impairs the repair of oxidative DNA base modifications in human skin fibroblasts and melanoma cells. DNA Repair. 2008;7:912-21.
Watson RE, Gibbs NK, Griffiths CE, Sherratt MJ. Damage to skin extracellular matrix induced by UV exposure. Antioxid Redox Signal. 2014;21:1063-77.
Venza M, Visalli M, Beninati C, De Gaetano GV, Teti D, Venza I. Cellular mechanisms of oxidative stress and action in melanoma. Oxid Med Cell Longev. 2015;2015:481782.
Karthikeyan R, Kanimozhi G, Prasad NR, Agilan B, Ganesan M, Srithar G. Alpha pinene modulates UVA-induced oxidative stress, DNA damage and apoptosis in human skin epidermal keratinocytes. Life Sci. 2018;212:150-8.
Noh EM, Park J, Song HR, Kim JM, Lee M, Song HK, et al. Skin aging-dependent activation of the PI3K signaling pathway via downregulation of PTEN increases intracellular ROS in human dermal fibroblasts. Oxid Med Cell Longev. 2016;2016:6354261.
Zhan JY, Wang XF, Liu YH, Zhang ZB, Wang L, Chen JN, et al. Andrographolide sodium bisulfate prevents UV-induced skin photoaging through inhibiting oxidative stress and inflammation. Mediators Inflamm. 2016;2016:3271451.
Li S, Zhu G, Yang Y, Jian Z, Guo S, Dai W, et al. Oxidative stress drives CD8(+) T-cell skin trafficking in patients with vitiligo through CXCL16 upregulation by activating the unfolded protein response in keratinocytes. J Allergy Clin Immunol. 2017;140(1):177-189.e179.
Simonetti O, Bacchetti T, Ferretti G, Molinelli E, Rizzetto G, Bellachioma L, et al. Oxidative stress and alterations of Paraoxonases in atopic dermatitis. Antioxidants (Basel). 2021;10(5):697.
Braun S, Hanselmann C, Gassmann MG, Keller UA, Born-Berclaz C, Chan K, et al. Nrf2 transcription factor, a novel target of keratinocyte growth factor action which regulates gene expression and inflammation in the healing skin wound. Mol Cell Biol. 2002;22:5492-505.
Lee Y, Shin JM, Jang S, Choi DK, Seo MS, Kim HR, et al. Role of nuclear factor E2-related factor 2 (Nrf2) in epidermal differentiation. Arch Dermatol Res. 2014;306:677-82.
Jeayeng S, Wongkajornsilp A, Slominski AT, Jirawatnotai S, Sampattavanich S, Panich U. Nrf2 in keratinocytes modulates UVB-induced DNA damage and apoptosis in melanocytes through MAPK signaling. Free Radic Biol Med. 2017;108:918-28.
Kurinna S, Seltmann K, Bachmann AL, Schwendimann A, Thiagarajan L, Hennig P, et al. Interaction of the NRF2 and p63 transcription factors promotes keratinocyte proliferation in the epidermis. Nucleic Acids Res. 2021;49:3748-63.
Tao S, Park SL, Rojo de la Vega M, Zhang DD, Wondrak GT. Systemic administration of the apocarotenoid bixin protects skin against solar UV-induced damage through activation of NRF2. Free Radic Biol Med. 2015;89:690-700.
Wu W, Peng G, Yang F, Zhang Y, Mu Z, Han X. Sulforaphane has a therapeutic effect in an atopic dermatitis murine model and activates the Nrf2/HO-1 axis. Mol Med Rep. 2019;20:1761-71.
Wu R, Zhang H, Zhao M, Li J, Hu Y, Fu J, et al. Nrf2 in keratinocytes protects against skin fibrosis via regulating epidermal lesion and inflammatory response. Biochem Pharmacol. 2020;174:113846.
Du P, Zhang S, Li S, Yang Y, Kang P, Chen J, et al. Folic acid protects melanocytes from oxidative stress via activation of Nrf2 and inhibition of HMGB1. Oxid Med Cell Longev. 2021;2021:1608586.
Chaiprasongsuk A, Panich U. Role of phytochemicals in skin Photoprotection via regulation of Nrf2. Front Pharmacol. 2022;13:823881.
Edamitsu T, Taguchi K, Okuyama R, Yamamoto M. AHR and NRF2 in skin homeostasis and atopic dermatitis. Antioxidants (Basel). 2022;11(2):227.
Kahremany S, Hofmann L, Gruzman A, Dinkova-Kostova AT, Cohen G. NRF2 in dermatological disorders: pharmacological activation for protection against cutaneous photodamage and photodermatosis. Free Radic Biol Med. 2022;188:262-76.
Bergqvist C, Ezzedine K. Vitiligo: a review. Dermatology (Basel). 2020;236:571-92.
Seneschal J, Boniface K, D'Arino A, Picardo M. An update on vitiligo pathogenesis. Pigment Cell Melanoma Res. 2021;34:236-43.
Maresca V, Roccella M, Roccella F, Camera E, Del Porto G, Passi S, et al. Increased sensitivity to peroxidative agents as a possible pathogenic factor of melanocyte damage in vitiligo. J Invest Dermatol. 1997;109:310-3.
Kroll TM, Bommiasamy H, Boissy RE, Hernandez C, Nickoloff BJ, Mestril R, et al. 4-Tertiary butyl phenol exposure sensitizes human melanocytes to dendritic cell-mediated killing: relevance to vitiligo. J Invest Dermatol. 2005;124:798-806.
Al-Shobaili HA, Rasheed Z. Oxidized tyrosinase: a possible antigenic stimulus for non-segmental vitiligo autoantibodies. J Dermatol Sci. 2015;79:203-13.
Xie H, Zhou F, Liu L, Zhu G, Li Q, Li C, et al. Vitiligo: how do oxidative stress-induced autoantigens trigger autoimmunity? J Dermatol Sci. 2016;81:3-9.
Jimbow K, Chen H, Park JS, Thomas PD. Increased sensitivity of melanocytes to oxidative stress and abnormal expression of tyrosinase-related protein in vitiligo. Br J Dermatol. 2001;144:55-65.
Regazzetti C, Joly F, Marty C, Rivier M, Mehul B, Reiniche P, et al. Transcriptional analysis of vitiligo skin reveals the alteration of WNT pathway: a promising target for Repigmenting vitiligo patients. J Invest Dermatol. 2015;135:3105-14.
Schallreuter KU, Wood JM, Berger J. Low catalase levels in the epidermis of patients with vitiligo. J Invest Dermatol. 1991;97:1081-5.
Schallreuter KU, Rübsam K, Gibbons NC, Maitland DJ, Chavan B, Zothner C, et al. Methionine sulfoxide reductases a and B are deactivated by hydrogen peroxide (H2O2) in the epidermis of patients with vitiligo. J Invest Dermatol. 2008;128:808-15.
Zhou Z, Li CY, Li K, Wang T, Zhang B, Gao TW. Decreased methionine sulphoxide reductase a expression renders melanocytes more sensitive to oxidative stress: a possible cause for melanocyte loss in vitiligo. Br J Dermatol. 2009;161:504-9.
Guan CP, Zhou MN, Xu AE, Kang KF, Liu JF, Wei XD, et al. The susceptibility to vitiligo is associated with NF-E2-related factor2 (Nrf2) gene polymorphisms: a study on Chinese Han population. Exp Dermatol. 2008;17:1059-62.
Sorour NE, Abd El-Kareem HM, Ibrahim AE, Salem RM. Nuclear factor Erythroid-2-related factor 2 gene polymorphisms in vitiligo. J Clin Aesthet Dermatol. 2021;14:14-7.
Song P, Li K, Liu L, Wang X, Jian Z, Zhang W, et al. Genetic polymorphism of the Nrf2 promoter region is associated with vitiligo risk in Han Chinese populations. J Cell Mol Med. 2016;20:1840-50.
Jian Z, Li K, Song P, Zhu G, Zhu L, Cui T, et al. Impaired activation of the Nrf2-ARE signaling pathway undermines H2O2-induced oxidative stress response: a possible mechanism for melanocyte degeneration in vitiligo. J Invest Dermatol. 2014;134:2221-30.
Natarajan VT, Singh A, Kumar AA, Sharma P, Kar HK, Marrot L, et al. Transcriptional upregulation of Nrf2-dependent phase II detoxification genes in the involved epidermis of vitiligo vulgaris. J Invest Dermatol. 2010;130:2781-9.
Manga P, Elbuluk N, Orlow SJ. Recent advances in understanding vitiligo. F1000Res. 2016;5:F1000 Faculty Rev-2234.
Kim SK, Kim HJ, Choi SE, Park KH, Choi HK, Lee MW. Anti-oxidative and inhibitory activities on nitric oxide (NO) and prostaglandin E2 (COX-2) production of flavonoids from seeds of Prunus tomentosa Thunberg. Arch Pharm Res. 2008;31:424-8.
Jung E, Kim JH, Kim MO, Lee SY, Lee J. Melanocyte-protective effect of afzelin is mediated by the Nrf2-ARE signalling pathway via GSK-3β inactivation. Exp Dermatol. 2017;26:764-70.
Yang L, Yang F, Teng L, Katayama I. 6-Shogaol protects human melanocytes against oxidative stress through activation of the Nrf2-antioxidant response element signaling pathway. Int J Mol Sci. 2020;21(10):3537.
Lim HS, Jin S, Yun SJ. Modulation of Melanogenesis by Heme Oxygenase-1 via p53 in Normal human melanocytes. Chonnam Med J. 2016;52:45-52.
Hu Y, Huang J, Li Y, Jiang L, Ouyang Y, Li Y, et al. Cistanche deserticola polysaccharide induces melanogenesis in melanocytes and reduces oxidative stress via activating NRF2/HO-1 pathway. J Cell Mol Med. 2020;24:4023-35.
Arowojolu OA, Orlow SJ, Elbuluk N, Manga P. The nuclear factor (erythroid-derived 2)-like 2 (NRF2) antioxidant response promotes melanocyte viability and reduces toxicity of the vitiligo-inducing phenol monobenzone. Exp Dermatol. 2017;26:637-44.
Ma J, Li S, Zhu L, Guo S, Yi X, Cui T, et al. Baicalein protects human vitiligo melanocytes from oxidative stress through activation of NF-E2-related factor2 (Nrf2) signaling pathway. Free Radic Biol Med. 2018;129:492-503.
Mou K, Pan W, Han D, Wen X, Cao F, Miao Y, et al. Glycyrrhizin protects human melanocytes from H2O2-induced oxidative damage via the Nrf2-dependent induction of HO-1. Int J Mol Med. 2019;44:253-61.
Zhang B, Wang J, Zhao G, Lin M, Lang Y, Zhang D, et al. Apigenin protects human melanocytes against oxidative damage by activation of the Nrf2 pathway. Cell Stress Chaperones. 2020;25:277-85.
Parsad D, Pandhi R, Juneja A. Effectiveness of oral Ginkgo biloba in treating limited, slowly spreading vitiligo. Clin Exp Dermatol. 2003;28:285-7.
Szczurko O, Shear N, Taddio A, Boon H. Ginkgo biloba for the treatment of vitilgo vulgaris: an open label pilot clinical trial. BMC Complement Altern Med. 2011;11:21.
Zhang S, Yi X, Su X, Jian Z, Cui T, Guo S, et al. Ginkgo biloba extract protects human melanocytes from H2O2-induced oxidative stress by activating Nrf2. J Cell Mol Med. 2019;23:5193-9.
Jiang W, Li S, Chen X, Zhang W, Chang Y, He Y, et al. Berberine protects immortalized line of human melanocytes from H2O2-induced oxidative stress via activation of Nrf2 and Mitf signaling pathway. J Dermatol Sci. 2019;94:236-43.
Li XS, Tang XY, Su W, Li X. Vitexin protects melanocytes from oxidative stress via activating MAPK-Nrf2/ARE pathway. Immunopharmacol Immunotoxicol. 2020;42:594-603.
Zhang M, Goyert G, Lim HW. Folate and phototherapy: what should we inform our patients? J Am Acad Dermatol. 2017;77:958-64.
Griffiths CEM, van der Walt JM, Ashcroft DM, Flohr C, Naldi L, Nijsten T, et al. The global state of psoriasis disease epidemiology: a workshop report. Br J Dermatol. 2017;177:e4-7.
Griffiths CE, Barker JN. Pathogenesis and clinical features of psoriasis. Lancet. 2007;370:263-71.
Korman NJ. Management of psoriasis as a systemic disease: what is the evidence? Br J Dermatol. 2020;182:840-8.
Diani M, Altomare G, Reali E. T cell responses in psoriasis and psoriatic arthritis. Autoimmun Rev. 2015;14:286-92.
Ambrożewicz E, Wójcik P, Wroński A, Łuczaj W, Jastrząb A, Žarković N, et al. Pathophysiological alterations of redox signaling and endocannabinoid system in granulocytes and plasma of psoriatic patients. Cells. 2018;7(10):159.
Medovic MV, Jakovljevic VL, Zivkovic VI, Jeremic NS, Jeremic JN, Bolevich SB, et al. Psoriasis between autoimmunity and oxidative stress: changes induced by different therapeutic approaches. Oxid Med Cell Longev. 2022;2022:2249834.
Ortiz-Lopez LI, Choudhary V, Bollag WB. Updated perspectives on keratinocytes and psoriasis: keratinocytes are More than innocent bystanders. Psoriasis. 2022;12:73-87.
Baliwag J, Barnes DH, Johnston A. Cytokines in psoriasis. Cytokine. 2015;73:342-50.
Ghazawi FM, Mahmood F, Kircik L, Poulin Y, Bourcier M, Vender R, et al. A review of the efficacy and safety for biologic agents targeting IL-23 in treating psoriasis with the focus on Tildrakizumab. Front Med. 2021;8:702776.
Marson JW, Snyder ML, Lebwohl MG. Newer therapies in psoriasis. Med Clin North Am. 2021;105:627-41.
Liang Y, Sarkar MK, Tsoi LC, Gudjonsson JE. Psoriasis: a mixed autoimmune and autoinflammatory disease. Curr Opin Immunol. 2017;49:1-8.
Hu P, Wang M, Gao H, Zheng A, Li J, Mu D, et al. The role of helper T cells in psoriasis. Front Immunol. 2021;12:788940.
Anstey AV. Fumaric acid esters in the treatment of psoriasis. Br J Dermatol. 2010;162:237-8.
Heelan K, Markham T. Fumaric acid esters as a suitable first-line treatment for severe psoriasis: an Irish experience. Clin Exp Dermatol. 2012;37:793-5.
Nieboer C, de Hoop D, Langendijk PN, van Loenen AC, Gubbels J. Fumaric acid therapy in psoriasis: a double-blind comparison between fumaric acid compound therapy and monotherapy with dimethylfumaric acid ester. Dermatologica. 1990;181:33-7.
Altmeyer PJ, Matthes U, Pawlak F, Hoffmann K, Frosch PJ, Ruppert P, et al. Antipsoriatic effect of fumaric acid derivatives. Results of a multicenter double-blind study in 100 patients. J Am Acad Dermatol. 1994;30:977-81.
Fallah Arani S, Neumann H, Hop WC, Thio HB. Fumarates vs. methotrexate in moderate to severe chronic plaque psoriasis: a multicentre prospective randomized controlled clinical trial. Br J Dermatol. 2011;164:855-61.
Linker RA, Lee DH, Ryan S, van Dam AM, Conrad R, Bista P, et al. Fumaric acid esters exert neuroprotective effects in neuroinflammation via activation of the Nrf2 antioxidant pathway. Brain. 2011;134:678-92.
Scannevin RH, Chollate S, Jung MY, Shackett M, Patel H, Bista P, et al. Fumarates promote cytoprotection of central nervous system cells against oxidative stress via the nuclear factor (erythroid-derived 2)-like 2 pathway. J Pharmacol Exp Ther. 2012;341:274-84.
Brennan MS, Matos MF, Li B, Hronowski X, Gao B, Juhasz P, et al. Dimethyl fumarate and monoethyl fumarate exhibit differential effects on KEAP1, NRF2 activation, and glutathione depletion in vitro. PLoS one. 2015;10:e0120254.
Lee YJ, Bae JH, Kang SG, Cho SW, Chun DI, Nam SM, et al. Pro-oxidant status and Nrf2 levels in psoriasis vulgaris skin tissues and dimethyl fumarate-treated HaCaT cells. Arch Pharm Res. 2017;40:1105-16.
Yang L, Fan X, Cui T, Dang E, Wang G. Nrf2 promotes keratinocyte proliferation in psoriasis through up-regulation of keratin 6, keratin 16, and keratin 17. J Invest Dermatol. 2017;137:2168-76.
Zhang J, Li X, Wei J, Chen H, Lu Y, Li L, et al. Gallic acid inhibits the expression of keratin 16 and keratin 17 through Nrf2 in psoriasis-like skin disease. Int Immunopharmacol. 2018;65:84-95.
Ogawa T, Ishitsuka Y, Inoue S, Nakamura Y, Saito A, Okiyama N, et al. Nuclear factor erythroid 2-related factor 2 (Nrf2) regulates epidermal keratinization under psoriatic skin inflammation. Am J Pathol. 2020;190:577-85.
Mrowietz U, Szepietowski JC, Loewe R, van de Kerkhof P, Lamarca R, Ocker WG, et al. Efficacy and safety of LAS41008 (dimethyl fumarate) in adults with moderate-to-severe chronic plaque psoriasis: a randomized, double-blind, Fumaderm(®) - and placebo-controlled trial (BRIDGE). Br J Dermatol. 2017;176:615-23.
Basketter DA, White IR, Burleson FG, Burleson GR, Kimber I. Dimethylfumarate: potency prediction and clinical experience. Contact Dermatitis. 2013;68:269-72.
Bojanowski K, Ibeji CU, Singh P, Swindell WR, Chaudhuri RK. A sensitization-free dimethyl fumarate prodrug, Isosorbide Di-(methyl fumarate), provides a topical treatment candidate for psoriasis. JID Innov. 2021;1:100040.
Helwa I, Patel R, Karempelis P, Kaddour-Djebbar I, Choudhary V, Bollag WB. The antipsoriatic agent monomethylfumarate has antiproliferative, prodifferentiative, and anti-inflammatory effects on keratinocytes. J Pharmacol Exp Ther. 2015;352:90-7.
Helwa I, Choudhary V, Chen X, Kaddour-Djebbar I, Bollag WB. Anti-psoriatic drug Monomethylfumarate increases nuclear factor erythroid 2-related factor 2 levels and induces Aquaporin-3 mRNA and protein expression. J Pharmacol Exp Ther. 2017;362:243-53.
Wang W, Yuhai HW, Chasuna B. Astilbin reduces ROS accumulation and VEGF expression through Nrf2 in psoriasis-like skin disease. Biol Res. 2019;52:49.
Wójcik P, Gęgotek A, Wroński A, Jastrząb A, Żebrowska A, Skrzydlewska E. Effect of redox imbalance on protein modifications in lymphocytes of psoriatic patients. J Biochem. 2020;167:323-31.
Sunkari S, Thatikonda S, Pooladanda V, Challa VS, Godugu C. Protective effects of ambroxol in psoriasis like skin inflammation: exploration of possible mechanisms. Int Immunopharmacol. 2019;71:301-12.
Lee J, Song K, Hiebert P, Werner S, Kim TG, Kim YS. Tussilagonone ameliorates psoriatic features in keratinocytes and Imiquimod-induced psoriasis-like lesions in mice via NRF2 activation. J Invest Dermatol. 2020;140:1223-1232.e1224.
Ng CY, Yen H, Hsiao HY, Su SC. Phytochemicals in skin cancer prevention and treatment: an updated review. Int J Mol Sci. 2018;19:941.
Zhang W, Zeng W, Jiang A, He Z, Shen X, Dong X, et al. Global, regional and national incidence, mortality and disability-adjusted life-years of skin cancers and trend analysis from 1990 to 2019: an analysis of the global burden of disease study 2019. Cancer Med. 2021;10:4905-22.
Pritchard JB, French JE, Barbara JD, Haseman JK. The role of transgenic mouse models in carcinogen identification. Environ Health Perspect. 2003;111:12-454.
Radhiga T, Agilan B, Muzaffer U, Karthikeyan R, Kanimozhi G, Paul V, et al. Phytochemicals as modulators of ultraviolet-B radiation induced cellular and molecular events: a review. J Radiat Cancer Res. 2016;7:2-12.
Frenkel K, Wei L, Wei H. 7,12-dimethylbenza.Anthracene induces oxidative DNA modification in vivo. Free Radic Biol Med. 1995;19:373-80.
Kvam E, Tyrrell RM. Induction of oxidative DNA base damage in human skin cells by UV and near visible radiation. Carcinogenesis. 1997;18:2379-84.
Nakamura Y, Kozuka M, Naniwa K, Takabayashi S, Torikai K, Hayashi R, et al. Arachidonic acid cascade inhibitors modulate phorbol ester-induced oxidative stress in female ICR mouse skin: differential roles of 5-lipoxygenase and cyclooxygenase-2 in leukocyte infiltration and activation. Free Radic Biol Med. 2003;35:997-1007.
Khan AQ, Khan R, Qamar W, Lateef A, Rehman MU, Tahir M, et al. Geraniol attenuates 12-O-tetradecanoylphorbol-13-acetate (TPA)-induced oxidative stress and inflammation in mouse skin: possible role of p38 MAP kinase and NF-κB. Exp Mol Pathol. 2013;94:419-29.
Carrara IM, Melo GP, Bernardes SS, Neto FS, Ramalho LNZ, Marinello PC, et al. Looking beyond the skin: cutaneous and systemic oxidative stress in UVB-induced squamous cell carcinoma in hairless mice. J Photochem Photobiol B Biol. 2019;195:17-26.
Chun KS, Kundu J, Kundu JK, Surh YJ. Targeting Nrf2-Keap1 signaling for chemoprevention of skin carcinogenesis with bioactive phytochemicals. Toxicol Lett. 2014;229:73-84.
Keller U a d, Huber M, Beyer TA, Kümin A, Siemes C, Braun S, et al. Nrf transcription factors in keratinocytes are essential for skin tumor prevention but not for wound healing. Mol Cell Biol. 2006;26:3773-84.
Xu C, Huang MT, Shen G, Yuan X, Lin W, Khor TO, et al. Inhibition of 7,12-dimethylbenz(a)anthracene-induced skin tumorigenesis in C57BL/6 mice by sulforaphane is mediated by nuclear factor E2-related factor 2. Cancer Res. 2006;66:8293-6.
Hong F, Freeman ML, Liebler DC. Identification of sensor cysteines in human Keap1 modified by the cancer chemopreventive agent sulforaphane. Chem Res Toxicol. 2005;18:1917-26.
Wagner AE, Ernst I, Iori R, Desel C, Rimbach G. Sulforaphane but not ascorbigen, indole-3-carbinole and ascorbic acid activates the transcription factor Nrf2 and induces phase-2 and antioxidant enzymes in human keratinocytes in culture. Exp Dermatol. 2010;19:137-44.
Dinkova-Kostova AT, Jenkins SN, Fahey JW, Ye L, Wehage SL, Liby KT, et al. Protection against UV-light-induced skin carcinogenesis in SKH-1 high-risk mice by sulforaphane-containing broccoli sprout extracts. Cancer Lett. 2006;240:243-52.
Sirerol JA, Feddi F, Mena S, Rodriguez ML, Sirera P, Aupí M, et al. Topical treatment with pterostilbene, a natural phytoalexin, effectively protects hairless mice against UVB radiation-induced skin damage and carcinogenesis. Free Radic Biol Med. 2015;85:1-11.
Lee J, Mailar K, Yoo OK, Choi WJ, Keum YS. Marliolide inhibits skin carcinogenesis by activating NRF2/ARE to induce heme oxygenase-1. Eur J Med Chem. 2018;150:113-26.
Su ZY, Zhang C, Lee JH, Shu L, Wu TY, Khor TO, et al. Requirement and epigenetics reprogramming of Nrf2 in suppression of tumor promoter TPA-induced mouse skin cell transformation by sulforaphane. Cancer Prev Res (Phila). 2014;7:319-29.
Yang Y, Yang I, Cao M, Su ZY, Wu R, Guo Y, et al. Fucoxanthin elicits epigenetic modifications, Nrf2 activation and blocking transformation in mouse skin JB6 P+ cells. AAPS J. 2018;20:32.
Kim H, Ramirez CN, Su ZY, Kong AN. Epigenetic modifications of triterpenoid ursolic acid in activating Nrf2 and blocking cellular transformation of mouse epidermal cells. J Nutr Biochem. 2016;33:54-62.
Saw CL, Huang MT, Liu Y, Khor TO, Conney AH, Kong AN. Impact of Nrf2 on UVB-induced skin inflammation/photoprotection and photoprotective effect of sulforaphane. Mol Carcinog. 2011;50:479-86.
Lin W, Wu RT, Wu T, Khor TO, Wang H, Kong AN. Sulforaphane suppressed LPS-induced inflammation in mouse peritoneal macrophages through Nrf2 dependent pathway. Biochem Pharmacol. 2008;76:967-73.
Wang H, Khor TO, Saw CL, Lin W, Wu T, Huang Y, et al. Role of Nrf2 in suppressing LPS-induced inflammation in mouse peritoneal macrophages by polyunsaturated fatty acids docosahexaenoic acid and eicosapentaenoic acid. Mol Pharm. 2010;7:2185-93.
Kobayashi EH, Suzuki T, Funayama R, Nagashima T, Hayashi M, Sekine H, et al. Nrf2 suppresses macrophage inflammatory response by blocking proinflammatory cytokine transcription. Nat Commun. 2016;7:11624.
Early JO, Menon D, Wyse CA, Cervantes-Silva MP, Zaslona Z, Carroll RG, et al. Circadian clock protein BMAL1 regulates IL-1β in macrophages via NRF2. Proc Natl Acad Sci U S A. 2018;115:E8460-8.
Landskron G, De la Fuente M, Thuwajit P, Thuwajit C, Hermoso MA. Chronic inflammation and cytokines in the tumor microenvironment. J Immunol Res. 2014;2014:149185.
Seo SH, Jeong GS. Fisetin inhibits TNF-α-induced inflammatory action and hydrogen peroxide-induced oxidative damage in human keratinocyte HaCaT cells through PI3K/AKT/Nrf-2-mediated heme oxygenase-1 expression. Int Immunopharmacol. 2015;29:246-53.
Knatko EV, Ibbotson SH, Zhang Y, Higgins M, Fahey JW, Talalay P, et al. Nrf2 activation protects against solar-simulated ultraviolet radiation in mice and humans. Cancer Prev Res (Phila). 2015;8:475-86.
Knatko EV, Higgins M, Fahey JW, Dinkova-Kostova AT. Loss of Nrf2 abrogates the protective effect of Keap1 downregulation in a preclinical model of cutaneous squamous cell carcinoma. Sci Rep. 2016;6:25804.

Auteurs

Emiliano Panieri (E)

Department of Physiology and Pharmacology "Vittorio Erspamer", Sapienza University of Rome, Rome, Italy.
Department of General Direction (DG), Section of Hazardous Substances, Environmental Education and Training for the Technical Coordination of Management Activities (DGTEC), Italian Institute for Environmental Protection and Research, Rome, Italy.

Pelin Telkoparan-Akillilar (P)

Department of Medical Biology, Faculty of Medicine, Yuksek Ihtisas University, Ankara, Turkey.

Luciano Saso (L)

Department of Physiology and Pharmacology "Vittorio Erspamer", Sapienza University of Rome, Rome, Italy.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH