Oroxylin A attenuates psoriasiform skin inflammation by direct targeting p62 (sequestosome 1) via suppressing M1 macrophage polarization.
NF‐κB
autophagy
macrophage polarization
oroxylin A
sequestosome 1/p62
Journal
British journal of pharmacology
ISSN: 1476-5381
Titre abrégé: Br J Pharmacol
Pays: England
ID NLM: 7502536
Informations de publication
Date de publication:
23 Sep 2024
23 Sep 2024
Historique:
revised:
21
08
2024
received:
22
09
2023
accepted:
22
08
2024
medline:
24
9
2024
pubmed:
24
9
2024
entrez:
24
9
2024
Statut:
aheadofprint
Résumé
Psoriasis results from the interplay of innate and adaptive immunity in the skin. Oroxylin A (OA) has shown anti-inflammatory effects in various disorders. This study explores oroxylin A potential in treating psoriasis, particularly its impact on type I macrophage (Mφ1) polarization. Oroxylin A-mediated therapeutic effects were evaluated using imiquimod-induced or IL-23-injected psoriatic mice models, followed by proteomics assays to predict potential signalling and targeting proteins. Immunofluorescence and immunoblot assays verified that oroxylin A suppresses NF-kB signalling in M1 macrophages. Co-immunoprecipitation and microscale thermophoresis (MST) assays further demonstrated that p62 (sequestosome 1) is the target protein for oroxylin A in macrophages. Oroxylin A-p62-mediated suppression of psoriasis was validated in an imiquimod-induced p62 conditional knockout (cKO) mice model. Oroxylin A demonstrated therapeutic efficacy in murine models induced by imiquimod or IL-23 by attenuating cutaneous inflammation and mitigating Mφ1 polarization via NF-κB signalling. Proteomics analysis suggested SQSTM1/p62 as a key target, confirmed to interact directly with oroxylin A. Oroxylin A disrupted the p62-PKCζ interaction by binding to PB1 domain of p62. Its anti-inflammatory effects were significantly reduced in macrophages from p62 cKO mice compared to the wild-type (WT) mice in psoriasis model, supporting oroxylin A role in suppressing Mφ1 polarization through its interaction with p62. Our findings demonstrated oroxylin A suppressed psoriasiform skin inflammation in mouse models by blocking the PKCζ-p62 interaction, subsequently inhibiting the activation of NF-κB p65 phosphorylation in macrophages.
Sections du résumé
BACKGROUND AND PURPOSE
OBJECTIVE
Psoriasis results from the interplay of innate and adaptive immunity in the skin. Oroxylin A (OA) has shown anti-inflammatory effects in various disorders. This study explores oroxylin A potential in treating psoriasis, particularly its impact on type I macrophage (Mφ1) polarization.
EXPERIMENTAL APPROACH
METHODS
Oroxylin A-mediated therapeutic effects were evaluated using imiquimod-induced or IL-23-injected psoriatic mice models, followed by proteomics assays to predict potential signalling and targeting proteins. Immunofluorescence and immunoblot assays verified that oroxylin A suppresses NF-kB signalling in M1 macrophages. Co-immunoprecipitation and microscale thermophoresis (MST) assays further demonstrated that p62 (sequestosome 1) is the target protein for oroxylin A in macrophages. Oroxylin A-p62-mediated suppression of psoriasis was validated in an imiquimod-induced p62 conditional knockout (cKO) mice model.
KEY RESULTS
RESULTS
Oroxylin A demonstrated therapeutic efficacy in murine models induced by imiquimod or IL-23 by attenuating cutaneous inflammation and mitigating Mφ1 polarization via NF-κB signalling. Proteomics analysis suggested SQSTM1/p62 as a key target, confirmed to interact directly with oroxylin A. Oroxylin A disrupted the p62-PKCζ interaction by binding to PB1 domain of p62. Its anti-inflammatory effects were significantly reduced in macrophages from p62 cKO mice compared to the wild-type (WT) mice in psoriasis model, supporting oroxylin A role in suppressing Mφ1 polarization through its interaction with p62.
CONCLUSION AND IMPLICATIONS
CONCLUSIONS
Our findings demonstrated oroxylin A suppressed psoriasiform skin inflammation in mouse models by blocking the PKCζ-p62 interaction, subsequently inhibiting the activation of NF-κB p65 phosphorylation in macrophages.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Basic Ability Enhancement Program for Young and Middle-aged Teachers of Guilin Medical University
ID : 2022KY0513
Organisme : Natural Science Foundation of Jiangsu Province
ID : BK20210419
Organisme : Natural Science Foundation of Jiangsu Province
ID : BK20211578
Organisme : National Natural Science Foundation of China
ID : 81974425
Organisme : National Natural Science Foundation of China
ID : 82002907
Organisme : National Natural Science Foundation of China
ID : 82360718
Organisme : Special Fund for Talents of Guangxi
ID : AD220359310
Informations de copyright
© 2024 British Pharmacological Society.
Références
Alexander, S. P. H., Fabbro, D., Kelly, E., Mathie, A. A., Peters, J. A., Veale, E. L., Armstrong, J. F., Faccenda, E., Harding, S. D., Davies, J. A., Beuve, A., Brouckaert, P., Bryant, C., Burnett, J. C., Farndale, R. W., Friebe, A., Garthwaite, J., Hobbs, A. J., Jarvis, G. E., … Waldman, S. A. (2023). The Concise Guide to PHARMACOLOGY 2023/24: Catalytic receptors. British Journal of Pharmacology, 180(Suppl 2), S241–S288. https://doi.org/10.1111/bph.16180
Alexander, S. P. H., Kelly, E., Mathie, A., Peters, J. A., Veale, E. L., Armstrong, J. F., Buneman, O. P., Faccenda, E., Harding, S. D., Spedding, M., Cidlowski, J. A., Fabbro, D., Davenport, A. P., Striessnig, J., Davies, J. A., Ahlers‐Dannen, K. E., … Zolghadri, Y. (2023). The Concise Guide to PHARMACOLOGY 2023/24: Introduction and other protein targets. British Journal of Pharmacology, 180, S1–S22. https://doi.org/10.1111/bph.16176
Alexander, S. P. H., Roberts, R. E., Broughton, B. R. S., Sobey, C. G., George, C. H., Stanford, S. C., Cirino, G., Docherty, J. R., Giembycz, M. A., Hoyer, D., Insel, P. A., Izzo, A. A., Ji, Y., MacEwan, D. J., Mangum, J., Wonnacott, S., & Ahluwalia, A. (2018). Goals and practicalities of immunoblotting and immunohistochemistry: A guide for submission to the British Journal of Pharmacology. British Journal of Pharmacology, 175, 407–411. https://doi.org/10.1111/bph.14112
Antal, D., Alimohammadi, S., Bai, P., Szöllősi, A. G., & Szántó, M. (2022). Antigen‐presenting cells in psoriasis. Life (Basel), 12(2), 234. https://doi.org/10.3390/life12020234
Asahina, A., Etoh, T., Igarashi, A., Imafuku, S., Saeki, H., Shibasaki, Y., Tomochika, Y., Toyoizumi, S., Nagaoka, M., & Ohtsuki, M. (2016). Oral tofacitinib efficacy, safety and tolerability in Japanese patients with moderate to severe plaque psoriasis and psoriatic arthritis: A randomized, double‐blind, phase 3 study. The Journal of Dermatology, 43(8), 869–880. https://doi.org/10.1111/1346-8138.13258
Blasius, A. L., & Beutler, B. (2010). Intracellular toll‐like receptors. Immunity, 32(3), 305–315. https://doi.org/10.1016/j.immuni.2010.03.012
Blauvelt, A., Armstrong, A. W., Langley, R. G., Gebauer, K., Thaçi, D., Bagel, J., Guenther, L. C., Paul, C., Randazzo, B., Flavin, S., Hsu, M. C., You, Y., & Reich, K. (2022). Efficacy of guselkumab versus secukinumab in subpopulations of patients with moderate‐to‐severe plaque psoriasis: Results from the ECLIPSE study. The Journal of Dermatological Treatment, 33(4), 2317–2324. https://doi.org/10.1080/09546634.2021.1959504
Cao, H. J., Zhou, W., Xian, X. L., Sun, S. J., Ding, P. J., Tian, C. Y., Tian, F. L., Jiang, C. H., Fu, T. T., Zhao, S., & Dai, J. Y. (2021). A mixture of baicalein, wogonin, and oroxylin‐A inhibits EMT in the A549 cell line via the PI3K/AKT‐TWIST1‐glycolysis pathway. Frontiers in Pharmacology, 12, 821485. https://doi.org/10.3389/fphar.2021.821485
Celhar, T., Magalhães, R., & Fairhurst, A. M. (2012). TLR7 and TLR9 in SLE: When sensing self goes wrong. Immunologic Research, 53(1–3), 58–77. https://doi.org/10.1007/s12026-012-8270-1
Chen, D. H., Zheng, G., Zhong, X. Y., Lin, Z. H., Yang, S. W., Liu, H. X., & Shang, P. (2021). Oroxylin A attenuates osteoarthritis progression by dual inhibition of cell inflammation and hypertrophy. Food & Function, 12(1), 328–339. https://doi.org/10.1039/d0fo02159h
Chen, Y., Yan, Y., Liu, H., Qiu, F., Liang, C.‐L., Zhang, Q., Huang, R.‐Y., Han, L., Lu, C., & Dai, Z. (2020). Dihydroartemisinin ameliorates psoriatic skin inflammation and its relapse by diminishing CD8+ T‐cell memory in wild‐type and humanized mice. Theranostics, 10(23), 10466–10482. https://doi.org/10.7150/thno.45211
Chiang, C. C., Cheng, W. J., Korinek, M., Lin, C. Y., & Hwang, T. L. (2019). Neutrophils in psoriasis. Frontiers in Immunology, 10, 2376. https://doi.org/10.3389/fimmu.2019.02376
Coates, L. C., Smolen, J. S., Mease, P. J., Husni, M. E., Merola, J. F., Lespessailles, E., Kishimoto, M., Macpherson, L., Bradley, A. J., Bolce, R., & Helliwell, P. S. (2022). Comparative performance of composite measures from two phase III clinical trials of ixekizumab in psoriatic arthritis. RMD Open, 8(2), e002457. https://doi.org/10.1136/rmdopen-2022-002457
Curtis, M. J., Alexander, S. P. H., Cirino, G., George, C. H., Kendall, D. A., Insel, P. A., Izzo, A. A., Ji, Y., Panettieri, R. A., Patel, H. H., Sobey, C. G., Stanford, S. C., Stanley, P., Stefanska, B., Stephens, G. J., Teixeira, M. M., Vergnolle, N., & Ahluwalia, A. (2022). Planning experiments: Updated guidance on experimental design and analysis and their reporting III. British Journal of Pharmacology., 179, 3907–3913. https://doi.org/10.1111/bph.15868
Diaz‐Meco, M. T., & Moscat, J. (2012). The atypical PKCs in inflammation: NF‐κB and beyond. Immunological Reviews, 246(1), 154–167. https://doi.org/10.1111/j.1600-065X.2012.01093.x
Duan, H., Koga, T., Kohda, F., Hara, H., Urabe, K., & Furue, M. (2001). Interleukin‐8‐positive neutrophils in psoriasis. Journal of Dermatological Science, 26(2), 119–124. https://doi.org/10.1016/s0923-1811(00)00167-5
Dykukha, I., Schoenenberger, A., Kasujee, I., Mrowietz, U., & Vonthein, R. (2022). Application of the statistical method to convert published PASI 50/75/90/100 into absolute PASI response rate in patients with moderate‐to‐severe plaque psoriasis treated with tildrakizumab based on data from the two pivotal phase 3 studies reSURFACE 1 and reSURFACE 2. Dermatology, 238(5), 910–918. https://doi.org/10.1159/000522009
Ellis, C. N., Gorsulowsky, D. C., Hamilton, T. A., Billings, J. K., Brown, M. D., Headington, J. T., Cooper, K. D., Baadsgaard, O., Duell, E. A., & Annesley, T. M. (1986). Cyclosporine improves psoriasis in a double‐blind study. Jama, 256(22), 3110–3116. https://doi.org/10.1001/jama.1986.03380220076026
Feng, Y., & Longmore, G. D. (2005). The LIM protein Ajuba influences interleukin‐1‐induced NF‐κB activation by affecting the assembly and activity of the protein kinase Czeta/p62/TRAF6 signaling complex. Molecular and Cellular Biology, 25(10), 4010–4022. https://doi.org/10.1128/MCB.25.10.4010-4022.2005
Fore, F., Indriputri, C., Mamutse, J., & Nugraha, J. (2020). TLR10 and its unique anti‐inflammatory properties and potential use as a target in therapeutics. Immune Network, 20(3), e21. https://doi.org/10.4110/in.2020.20.e21
Fuentes‐Duculan, J., Bonifacio, K. M., Hawkes, J. E., Kunjravia, N., Cueto, I., Li, X., Gonzalez, J., Garcet, S., & Krueger, J. G. (2017). Autoantigens ADAMTSL5 and LL37 are significantly upregulated in active psoriasis and localized with keratinocytes, dendritic cells and other leukocytes. Experimental Dermatology, 26(11), 1075–1082. https://doi.org/10.1111/exd.13378
Gangwar, R. S., Gudjonsson, J. E., & Ward, N. L. (2022). Mouse models of psoriasis: A comprehensive review. The Journal of Investigative Dermatology, 142(3 Pt B), 884–897. https://doi.org/10.1016/j.jid.2021.06.019
Gao, J., Ding, Y., Wang, Y., Liang, P., Zhang, L., & Liu, R. (2021). Oroxylin A is a severe acute respiratory syndrome coronavirus 2‐spiked pseudotyped virus blocker obtained from Radix Scutellariae using angiotensin‐converting enzyme II/cell membrane chromatography. Phytotherapy Research, 35(6), 3194–3204. https://doi.org/10.1002/ptr.7030
Griffiths, C. E. M., Armstrong, A. W., Gudjonsson, J. E., & Barker, J. (2021). Psoriasis. Lancet, 397(10281), 1301–1315. https://doi.org/10.1016/s0140-6736(20)32549-6
Hawkes, J. E., Chan, T. C., & Krueger, J. G. (2017). Psoriasis pathogenesis and the development of novel targeted immune therapies. The Journal of Allergy and Clinical Immunology, 140(3), 645–653. https://doi.org/10.1016/j.jaci.2017.07.004
Horvath, C. M. (2004). The Jak‐STAT pathway stimulated by interferon gamma. Science's STKE, 2004(260), tr8. https://doi.org/10.1126/stke.2602004tr8
Hou, Y., Zhu, L., Tian, H., Sun, H. X., Wang, R., Zhang, L., & Zhao, Y. (2018). IL‐23‐induced macrophage polarization and its pathological roles in mice with imiquimod‐induced psoriasis. Protein & Cell, 9(12), 1027–1038. https://doi.org/10.1007/s13238-018-0505-z
Huang, H., Zhang, X., & Li, J. (2015). Protective effect of oroxylin A against lipopolysaccharide and/or D‐galactosamine‐induced acute liver injury in mice. The Journal of Surgical Research, 195(2), 522–528. https://doi.org/10.1016/j.jss.2015.01.047
Ikeda, S., Takahashi, H., Suga, Y., Eto, H., Etoh, T., Okuma, K., Takahashi, K., Kanbara, T., Seishima, M., Morita, A., Imai, Y., & Kanekura, T. (2013). Therapeutic depletion of myeloid lineage leukocytes in patients with generalized pustular psoriasis indicates a major role for neutrophils in the immunopathogenesis of psoriasis. Journal of the American Academy of Dermatology, 68(4), 609–617. https://doi.org/10.1016/j.jaad.2012.09.037
Jeong, S. J., Zhang, X., Rodriguez‐Velez, A., Evans, T. D., & Razani, B. (2019). p62/SQSTM1 and selective autophagy in cardiometabolic diseases. Antioxidants & Redox Signaling, 31(6), 458–471. https://doi.org/10.1089/ars.2018.7649
Jorch, S. K., & Kubes, P. (2017). An emerging role for neutrophil extracellular traps in noninfectious disease. Nature Medicine, 23(3), 279–287. https://doi.org/10.1038/nm.4294
Kaneko, J., Okinaga, T., Hikiji, H., Ariyoshi, W., Yoshiga, D., Habu, M., Tominaga, K., & Nishihara, T. (2018). Zoledronic acid exacerbates inflammation through M1 macrophage polarization. Inflammation and Regeneration, 38, 16. https://doi.org/10.1186/s41232-018-0074-9
Katsuragi, Y., Ichimura, Y., & Komatsu, M. (2015). p62/SQSTM1 functions as a signaling hub and an autophagy adaptor. The FEBS Journal, 282(24), 4672–4678. https://doi.org/10.1111/febs.13540
Kawai, T., & Akira, S. (2007). Signaling to NF‐κB by Toll‐like receptors. Trends in Molecular Medicine, 13(11), 460–469. https://doi.org/10.1016/j.molmed.2007.09.002
Kawai, T., & Akira, S. (2010). The role of pattern‐recognition receptors in innate immunity: Update on Toll‐like receptors. Nature Immunology, 11(5), 373–384. https://doi.org/10.1038/ni.1863
Keijsers, R., Hendriks, A. G. M., van Erp, P. E. J., van Cranenbroek, B., van de Kerkhof, P. C. M., Koenen, H., & Joosten, I. (2014). In vivo induction of cutaneous inflammation results in the accumulation of extracellular trap‐forming neutrophils expressing RORγt and IL‐17. The Journal of Investigative Dermatology, 134(5), 1276–1284. https://doi.org/10.1038/jid.2013.526
Kim, G. Y., Nigro, P., Fujiwara, K., Abe, J., & Berk, B. C. (2012). p62 binding to protein kinase C ζ regulates tumor necrosis factor α‐induced apoptotic pathway in endothelial cells. Arteriosclerosis Thrombosis and Vascular Biology, 32(12), 2974–2980. https://doi.org/10.1161/atvbaha.112.300054
Kryczek, I., Bruce, A. T., Gudjonsson, J. E., Johnston, A., Aphale, A., Vatan, L., Szeliga, W., Wang, Y., Liu, Y., Welling, T. H., Elder, J. T., & Zou, W. (2008). Induction of IL‐17+ T cell trafficking and development by IFN‐gamma: Mechanism and pathological relevance in psoriasis. Journal of Immunology, 181(7), 4733–4741. https://doi.org/10.4049/jimmunol.181.7.4733
Kumar, A. V., Mills, J., & Lapierre, L. R. (2022). Selective autophagy receptor p62/SQSTM1, a pivotal player in stress and aging. Frontiers in Cell and Developmental Biology, 10, 793328. https://doi.org/10.3389/fcell.2022.793328
Lamark, T., Svenning, S., & Johansen, T. (2017). Regulation of selective autophagy: The p62/SQSTM1 paradigm. Essays in Biochemistry, 61(6), 609–624. https://doi.org/10.1042/ebc20170035
Langley, R. G., Sofen, H., Dei‐Cas, I., Reich, K., Sigurgeirsson, B., Warren, R. B., Paul, C., Szepietowski, J. C., Tsai, T. F., Hampele, I., You, R., Charef, P., & Papavassilis, C. (2023). Secukinumab long‐term efficacy and safety in psoriasis through to year 5 of treatment: Results of a randomized extension of the phase III ERASURE and FIXTURE trials. The British Journal of Dermatology, 188(2), 198–207. https://doi.org/10.1093/bjd/ljac040
Lee, H. M., Shin, D. M., Yuk, J. M., Shi, G., Choi, D. K., Lee, S. H., Huang, S. M., Kim, J. M., Kim, C. D., Lee, J. H., & Jo, E. K. (2011). Autophagy negatively regulates keratinocyte inflammatory responses via scaffolding protein p62/SQSTM1. Journal of Immunology, 186(2), 1248–1258. https://doi.org/10.4049/jimmunol.1001954
Li, J., Tong, D., Liu, J., Chen, F., & Shen, Y. (2016). Oroxylin A attenuates cigarette smoke‐induced lung inflammation by activating Nrf2. International Immunopharmacology, 40, 524–529. https://doi.org/10.1016/j.intimp.2016.10.011
Lilley, E., Stanford, S. C., Kendall, D. E., Alexander, S. P. H., Cirino, G., Docherty, J. R., George, C. H., Insel, P. A., Izzo, A. A., Ji, Y., Panettieri, R. A., Sobey, C. G., Stefanska, B., Stephens, G., Teixeira, M., & Ahluwalia, A. (2020). ARRIVE 2.0 and the British Journal of Pharmacology: Updated guidance for 2020. British Journal of Pharmacology, 177(16), 3611–3616. https://doi.org/10.1111/BPH.15178
Lin, A. M., Rubin, C. J., Khandpur, R., Wang, J. Y., Riblett, M., Yalavarthi, S., Shah, P., Kaplan, M. J., & Bruce, A. T. (2011). Mast cells and neutrophils release IL‐17 through extracellular trap formation in psoriasis. Journal of Immunology, 187(1), 490–500. https://doi.org/10.4049/jimmunol.1100123
Liu, J. M., Jin, Q. X., Fujimoto, M., Li, F. F., Jin, L. B., Yu, R., Yan, G. H., Zhu, L. H., Meng, F. P., Zhang, Q. G., & Jin, G. H. (2021). Dihydroartemisinin alleviates imiquimod‐induced psoriasis‐like skin lesion in mice involving modulation of IL‐23/Th17 axis. Frontiers in Pharmacology, 12, 704481. https://doi.org/10.3389/fphar.2021.704481
Liu, P. W., Chen, M. F., Tsai, A. P., & Lee, T. J. (2012). STAT1 mediates oroxylin a inhibition of iNOS and pro‐inflammatory cytokines expression in microglial BV‐2 cells. PLoS ONE, 7(12), e50363. https://doi.org/10.1371/journal.pone.0050363
Liu, Y., Wang, H., Taylor, M., Cook, C., Martínez‐Berdeja, A., North, J. P., Harirchian, P., Hailer, A. A., Zhao, Z., Ghadially, R., Ricardo‐Gonzalez, R. R., Grekin, R. C., Mauro, T. M., Kim, E., Choi, J., Purdom, E., Cho, R. J., & Cheng, J. B. (2022). Classification of human chronic inflammatory skin disease based on single‐cell immune profiling. Science Immunology, 7(70), eabl9165. https://doi.org/10.1126/sciimmunol.abl9165
Lowes, M. A., Suarez‐Farinas, M., & Krueger, J. G. (2014). Immunology of psoriasis. Annual Review of Immunology, 32, 227–255. https://doi.org/10.1146/annurev-immunol-032713-120225
Ma, S., Attarwala, I. Y., & Xie, X. Q. (2019). SQSTM1/p62: A potential target for neurodegenerative disease. ACS Chemical Neuroscience, 10(5), 2094–2114. https://doi.org/10.1021/acschemneuro.8b00516
Mahla, R. S., Reddy, M. C., Prasad, D. V., & Kumar, H. (2013). Sweeten PAMPs: Role of sugar complexed PAMPs in innate immunity and vaccine biology. Frontiers in Immunology, 4, 248. https://doi.org/10.3389/fimmu.2013.00248
Moorchung, N., Kulaar, J. S., Chatterjee, M., Vasudevan, B., Tripathi, T., & Dutta, V. (2014). Role of NF‐κB in the pathogenesis of psoriasis elucidated by its staining in skin biopsy specimens. International Journal of Dermatology, 53(5), 570–574. https://doi.org/10.1111/ijd.12050
Moscat, J., & Diaz‐Meco, M. T. (2002). The atypical PKC scaffold protein P62 is a novel target for anti‐inflammatory and anti‐cancer therapies. Advances in Enzyme Regulation, 42, 173–179. https://doi.org/10.1016/s0065-2571(01)00029-2
Murray, P. J., & Wynn, T. A. (2011). Protective and pathogenic functions of macrophage subsets. Nature Reviews. Immunology, 11(11), 723–737. https://doi.org/10.1038/nri3073
Nussbaum, L., Chen, Y. L., & Ogg, G. S. (2021). Role of regulatory T cells in psoriasis pathogenesis and treatment. The British Journal of Dermatology, 184(1), 14–24. https://doi.org/10.1111/bjd.19380
Paliogiannis, P., Satta, R., Deligia, G., Farina, G., Bassu, S., Mangoni, A. A., Carru, C., & Zinellu, A. (2019). Associations between the neutrophil‐to‐lymphocyte and the platelet‐to‐lymphocyte ratios and the presence and severity of psoriasis: A systematic review and meta‐analysis. Clinical and Experimental Medicine, 19(1), 37–45. https://doi.org/10.1007/s10238-018-0538-x
Pankiv, S., Clausen, T. H., Lamark, T., Brech, A., Bruun, J. A., Outzen, H., Øvervatn, A., Bjørkøy, G., & Johansen, T. (2007). p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. The Journal of Biological Chemistry, 282(33), 24131–24145. https://doi.org/10.1074/jbc.M702824200
Papp, K., Reich, K., Leonardi, C. L., Kircik, L., Chimenti, S., Langley, R. G., Hu, C., Stevens, R. M., Day, R. M., Gordon, K. B., Korman, N. J., & Griffiths, C. E. (2015). Apremilast, an oral phosphodiesterase 4 (PDE4) inhibitor, in patients with moderate to severe plaque psoriasis: Results of a phase III, randomized, controlled trial (efficacy and safety trial evaluating the effects of apremilast in psoriasis [ESTEEM] 1). Journal of the American Academy of Dermatology, 73(1), 37–49. https://doi.org/10.1016/j.jaad.2015.03.049
Papp, K. A., Lebwohl, M. G., Puig, L., Ohtsuki, M., Beissert, S., Zeng, J., Rubant, S., Sinvhal, R., Zhao, Y., Soliman, A. M., Alperovich, G., & Leonardi, C. (2021). Long‐term efficacy and safety of risankizumab for the treatment of moderate‐to‐severe plaque psoriasis: Interim analysis of the LIMMitless open‐label extension trial beyond 3 years of follow‐up. The British Journal of Dermatology, 185(6), 1135–1145. https://doi.org/10.1111/bjd.20595
Peng, X., Wang, Y., Li, H., Fan, J., Shen, J., Yu, X., Zhou, Y., & Mao, H. (2019). ATG5‐mediated autophagy suppresses NF‐κB signaling to limit epithelial inflammatory response to kidney injury. Cell Death & Disease, 10(4), 253. https://doi.org/10.1038/s41419-019-1483-7
Percie du Sert, N., Hurst, V., Ahluwalia, A., Alam, S., Avey, M. T., Baker, M., Browne, W. J., Clark, A., Cuthill, I. C., Dirnagl, U., Emerson, M., Garner, P., Holgate, S. T., Howells, D. W., Karp, N. A., Lazic, S. E., Lidster, K., MacCallum, C. J., Macleod, M., … Würbel, H. (2020). The ARRIVE guidelines 2.0: updated guidelines for reporting animal research. PLoS Biology, 18(7), e3000410. https://doi.org/10.1371/journal.pbio.3000410
Qiang, L., Yang, S., Cui, Y. H., & He, Y. Y. (2021). Keratinocyte autophagy enables the activation of keratinocytes and fibroblastsand facilitates wound healing. Autophagy, 17(9), 2128–2143. https://doi.org/10.1080/15548627.2020.1816342
Reich, K., Papp, K. A., Matheson, R. T., Tu, J. H., Bissonnette, R., Bourcier, M., Gratton, D., Kunynetz, R. A., Poulin, Y., Rosoph, L. A., Stingl, G., Bauer, W. M., Salter, J. M., Falk, T. M., Blödorn‐Schlicht, N. A., Hueber, W., Sommer, U., Schumacher, M. M., Peters, T., … Bleul, C. C. (2015). Evidence that a neutrophil‐keratinocyte crosstalk is an early target of IL‐17A inhibition in psoriasis. Experimental Dermatology, 24(7), 529–535. https://doi.org/10.1111/exd.12710
Roenigk, H. H. Jr., Auerbach, R., Maibach, H. I., & Weinstein, G. D. (1988). Methotrexate in psoriasis: Revised guidelines. Journal of the American Academy of Dermatology, 19(1 Pt 1), 145–156. https://doi.org/10.1016/s0190-9622(88)80237-8
Sanchez, P., De Carcer, G., Sandoval, I. V., Moscat, J., & Diaz‐Meco, M. T. (1998). Localization of atypical protein kinase C isoforms into lysosome‐targeted endosomes through interaction with p62. Molecular and Cellular Biology, 18(5), 3069–3080. https://doi.org/10.1128/mcb.18.5.3069
Sanz, L., Diaz‐Meco, M. T., Nakano, H., & Moscat, J. (2000). The atypical PKC‐interacting protein p62 channels NF‐κB activation by the IL‐1‐TRAF6 pathway. EMBO Journal, 19(7), 1576–1586. https://doi.org/10.1093/emboj/19.7.1576
Sanz, L., Sanchez, P., Lallena, M. J., Diaz‐Meco, M. T., & Moscat, J. (1999). The interaction of p62 with RIP links the atypical PKCs to NF‐κB activation. EMBO Journal, 18(11), 3044–3053. https://doi.org/10.1093/emboj/18.11.3044
Savkovic, S. D., Koutsouris, A., & Hecht, G. (2003). PKC zeta participates in activation of inflammatory response induced by enteropathogenic E. coli. American Journal of Physiology. Cell Physiology, 285(3), C512–C521. https://doi.org/10.1152/ajpcell.00444.2002
Schön, M. P., & Erpenbeck, L. (2018). The interleukin‐23/interleukin‐17 axis links adaptive and innate immunity in psoriasis. Frontiers in Immunology, 9, 1323. https://doi.org/10.3389/fimmu.2018.01323
Schots, L., Soenen, R., Blanquart, B., Thomas, D., & Lambert, J. (2023). Blocking interleukin‐17 in psoriasis: Real‐world experience from the PsoPlus cohort. Journal of the European Academy of Dermatology and Venereology, 37(4), 698–710. https://doi.org/10.1111/jdv.18827
Singh, T. P., Zhang, H. H., Hwang, S. T., & Farber, J. M. (2019). IL‐23‐ and imiquimod‐induced models of experimental psoriasis in mice. Current Protocols in Immunology, 125(1), e71. https://doi.org/10.1002/cpim.71
Sukseree, S., Bakiri, L., Palomo‐Irigoyen, M., Uluçkan, Ö., Petzelbauer, P., & Wagner, E. F. (2021). Sequestosome 1/p62 enhances chronic skin inflammation. Journal of Allergy and Clinical Immunology, 147(6), 2386–2393.e2384. https://doi.org/10.1016/j.jaci.2021.02.028
Sulczewski, F. B., Martino, L. A., Almeida, B. D. S., Zaneti, A. B., Ferreira, N. S., Amorim, K., Yamamoto, M. M., Apostolico, J. S., Rosa, D. S., & Boscardin, S. B. (2020). Conventional type 1 dendritic cells induce T(H) 1, T(H) 1‐like follicular helper T cells and regulatory T cells after antigen boost via DEC205 receptor. European Journal of Immunology, 50(12), 1895–1911. https://doi.org/10.1002/eji.202048694
Sumida, H., Yanagida, K., Kita, Y., Abe, J., Matsushima, K., Nakamura, M., Ishii, S., Sato, S., & Shimizu, T. (2014). Interplay between CXCR2 and BLT1 facilitates neutrophil infiltration and resultant keratinocyte activation in a murine model of imiquimod‐induced psoriasis. Journal of Immunology, 192(9), 4361–4369. https://doi.org/10.4049/jimmunol.1302959
Sun, W., Gao, Y., Yu, X., Yuan, Y., Yi, J., Zhang, Z., Cheng, Y., Li, Y., Peng, X., & Cha, X. (2018). ‘Psoriasis 1’ reduces psoriasis‐like skin inflammation by inhibiting the VDR‐mediated nuclear NF‐κB and STAT signaling pathways. Molecular Medicine Reports, 18(3), 2733–2743. https://doi.org/10.3892/mmr.2018.9262
Tao, M., Liu, T., You, Q., & Jiang, Z. (2020). p62 as a therapeutic target for tumor. European Journal of Medicinal Chemistry, 193, 112231. https://doi.org/10.1016/j.ejmech.2020.112231
Tomar, Y., Gorantla, S., & Singhvi, G. (2023). Insight into the pivotal role of signaling pathways in psoriasis pathogenesis, potential therapeutic molecules and drug delivery approaches. Drug Discovery Today, 28(2), 103465. https://doi.org/10.1016/j.drudis.2022.103465
van der Does, A. M., Beekhuizen, H., Ravensbergen, B., Vos, T., Ottenhoff, T. H., van Dissel, J. T., Drijfhout, J. W., Hiemstra, P. S., & Nibbering, P. H. (2010). LL‐37 directs macrophage differentiation toward macrophages with a proinflammatory signature. Journal of Immunology, 185(3), 1442–1449. https://doi.org/10.4049/jimmunol.1000376
Vinter, H., Iversen, L., Steiniche, T., Kragballe, K., & Johansen, C. (2015). Aldara®‐induced skin inflammation: Studies of patients with psoriasis. The British Journal of Dermatology, 172(2), 345–353. https://doi.org/10.1111/bjd.13236
Walker, F., Adamczyk, A., Kellerer, C., Belge, K., Brück, J., Berner, T., Merten, K., Núnez Gómez, N., Neureither, M., Röcken, M., & Ghoreschi, K. (2014). Fumaderm® in daily practice for psoriasis: Dosing, efficacy and quality of life. The British Journal of Dermatology, 171(5), 1197–1205. https://doi.org/10.1111/bjd.13098
Wang, W., Guo, W., Li, L., Fu, Z., Liu, W., Gao, J., Shu, Y., Xu, Q., Sun, Y., & Gu, Y. (2016). Andrographolide reversed 5‐FU resistance in human colorectal cancer by elevating BAX expression. Biochemical Pharmacology, 121, 8–17. https://doi.org/10.1016/j.bcp.2016.09.024
Wang, Y. L., Gao, J. M., & Xing, L. Z. (2016). Therapeutic potential of oroxylin A in rheumatoid arthritis. International Immunopharmacology, 40, 294–299. https://doi.org/10.1016/j.intimp.2016.09.006
Wang, Z., Zhou, H., Zheng, H., Zhou, X., Shen, G., Teng, X., Liu, X., Zhang, J., Wei, X., Hu, Z., Zeng, F., Hu, Y., Hu, J., Wang, X., Chen, S., Cheng, J., Zhang, C., Gui, Y., Zou, S., … Li, J. (2021). Autophagy‐based unconventional secretion of HMGB1 by keratinocytes plays a pivotal role in psoriatic skin inflammation. Autophagy, 17(2), 529–552. https://doi.org/10.1080/15548627.2020.1725381
Xi, G., Shen, X., Wai, C., Vilas, C. K., & Clemmons, D. R. (2015). Hyperglycemia stimulates p62/PKCζ interaction, which mediates NF‐κB activation, increased Nox4 expression, and inflammatory cytokine activation in vascular smooth muscle. The FASEB Journal, 29(12), 4772–4782. https://doi.org/10.1096/fj.15-275453
Yamanaka, K., Umezawa, Y., Yamagiwa, A., Saeki, H., Kondo, M., Gabazza, E. C., Nakagawa, H., & Mizutani, H. (2014). Biologic therapy improves psoriasis by decreasing the activity of monocytes and neutrophils. The Journal of Dermatology, 41(8), 679–685. https://doi.org/10.1111/1346-8138.12560
Yang, S., Qiang, L., Sample, A., Shah, P., & He, Y. Y. (2017). NF‐κB signaling activation induced by chloroquine requires autophagosome, p62 protein, and c‐Jun N‐terminal kinase (JNK) signaling and promotes tumor cell resistance. The Journal of Biological Chemistry, 292(8), 3379–3388. https://doi.org/10.1074/jbc.M116.756536
Zaba, L. C., Cardinale, I., Gilleaudeau, P., Sullivan‐Whalen, M., Suárez‐Fariñas, M., Fuentes‐Duculan, J., Novitskaya, I., Khatcherian, A., Bluth, M. J., Lowes, M. A., & Krueger, J. G. (2007). Amelioration of epidermal hyperplasia by TNF inhibition is associated with reduced Th17 responses. Journal of Experimental Medicine, 204(13), 3183–3194. https://doi.org/10.1084/jem.20071094
Zaba, L. C., Krueger, J. G., & Lowes, M. A. (2009). Resident and “inflammatory” dendritic cells in human skin. Journal of Investigative Dermatology, 129(2), 302–308. https://doi.org/10.1038/jid.2008.225
Zachariae, C., Mrowietz, U., Strodl Andersen, J., & Puig, L. (2022). Multistate modelling of probability of on‐treatment clinical response and time remaining in response in patients with moderate‐to‐severe psoriasis treated with brodalumab or ustekinumab in the AMAGINE‐2 and ‐3 studies. European Journal of Dermatology, 32(4), 530–535. https://doi.org/10.1684/ejd.2022.4304
Zhang, J., Tsai, T. F., Lee, M. G., Zheng, M., Wang, G., Jin, H., Gu, J., Li, R., Liu, Q., Chen, J., Tu, C., Qi, C., Zhu, H., Ports, W. C., Crook, T., & Crook, T. (2017). The efficacy and safety of tofacitinib in Asian patients with moderate to severe chronic plaque psoriasis: A phase 3, randomized, double‐blind, placebo‐controlled study. Journal of Dermatological Science, 88(1), 36–45. https://doi.org/10.1016/j.jdermsci.2017.05.004
Zhang, X., Jin, J. Y., Wu, J., Qin, X., Streilein, R., Hall, R. P., & Zhang, J. Y. (2015). RNA‐Seq and ChIP‐Seq reveal SQSTM1/p62 as a key mediator of JunB suppression of NF‐κB‐dependent inflammation. The Journal of Investigative Dermatology, 135(4), 1016–1024. https://doi.org/10.1038/jid.2014.519
Zhang, Y., Weng, Q., Chen, J., Li, M., & Han, J. (2021). Oroxylin A attenuates IL‐1β‐induced inflammatory reaction via inhibiting the activation of the ERK and PI3K/AKT signaling pathways in osteoarthritis chondrocytes. Experimental and Therapeutic Medicine, 21(4), 388. https://doi.org/10.3892/etm.2021.9819
Zhao, Y., Zhu, Q., Bu, X., Zhou, Y., Bai, D., Guo, Q., Gao, Y., & Lu, N. (2020). Triggering apoptosis by oroxylin A through caspase‐8 activation and p62/SQSTM1 proteolysis. Redox Biology, 29, 101392. https://doi.org/10.1016/j.redox.2019.101392
Zheng, Y., Danilenko, D. M., Valdez, P., Kasman, I., Eastham‐Anderson, J., Wu, J., & Ouyang, W. (2007). Interleukin‐22, a T(H)17 cytokine, mediates IL‐23‐induced dermal inflammation and acanthosis. Nature, 445(7128), 648–651. https://doi.org/10.1038/nature05505
Zhong, Z., Umemura, A., Sanchez‐Lopez, E., Liang, S., Shalapour, S., Wong, J., He, F., Boassa, D., Perkins, G., Ali, S. R., McGeough, M. D., Ellisman, M. H., Seki, E., Gustafsson, A. B., Hoffman, H. M., Diaz‐Meco, M. T., Moscat, J., & Karin, M. (2016). NF‐κB restricts Inflammasome activation via elimination of damaged mitochondria. Cell, 164(5), 896–910. https://doi.org/10.1016/j.cell.2015.12.057
Zou, B., Liu, J., Klionsky, D. J., Tang, D., & Kang, R. (2020). Extracellular SQSTM1 as an inflammatory mediator. Autophagy, 16(12), 2313–2315. https://doi.org/10.1080/15548627.2020.1843253
Zwicky, P., Unger, S., & Becher, B. (2020). Targeting interleukin‐17 in chronic inflammatory disease: A clinical perspective. Journal of Experimental Medicine, 217(1), e20191123. https://doi.org/10.1084/jem.20191123