Skin Inflammation Induced by the Synergistic Action of IL-17A, IL-22, Oncostatin M, IL-1α, and TNF-α Recapitulates Some Features of Psoriasis
Open accessAbstract
Keratinocytes play a crucial role in the regulation of skin inflammation, responding to environmental and immune cells stimuli. They produce soluble factors that can act in an autocrine or paracrine manner on immune cells or directly on aggressors. A screening of the activities of 36 cytokines on keratinocyte gene expression identified IL-17A, IL-22, oncostatin M, TNF-α, and IL-1α as potent cytokines in inducing cutaneous inflammation. These five proinflammatory cytokines synergistically increased production of CXCL8 and β-defensin 2 (BD2). In addition, ex vivo studies on human skin explants demonstrated upregulation of BD2, S100A7, and CXCL8 expression in response to the same combination of cytokines. In vivo intradermal injection of these five cytokines in mouse increased CXCL1, CXCL2, CXCL3, S100A9, and BD3 expression, associated with neutrophil infiltration. We confirmed and extended this synergistic effect using quantitative real-time PCR analysis and observed increased expression of nine chemokines and 12 antimicrobial peptides. Production of CXCL, CXCL5, and CXCL8 by keratinocytes stimulated in the presence of this cytokine combination was associated with increased neutrophil chemotactic activity. Similarly, high production of BD2, BD3, and S100A7 was associated with an increased antimicrobial activity. Finally, the transcriptional profile observed in this in vitro model of inflammatory keratinocytes correlated with the one of lesional psoriatic skin. Our results demonstrate the important potentiating activities of IL-17A, IL-22, oncostatin M, TNF-α, and IL-1α on keratinocytes. This is particularly interesting in the context of psoriasis where these cytokines are overexpressed and could synergize to play an important role in upregulation of chemokines and antimicrobial peptides production.
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In this patient, IL-6, TNF-α and IL-17A were elevated during rejection phase and were likely promoting observed skin and gastrointestinal toxicities.
“In this patient, several other inflammatory cytokines, mainly IL-6, TNF-α and IL-17A, were also elevated during the rejection phase, and were likely promoting the observed concomitant skin and gastrointestinal toxicities29–31.”
From Targeting the mTOR pathway uncouples the efficacy and toxicity of PD-1 blockade in renal transplantation (2019) · cites this paper as [30]
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Nakajima, K., Kanda, T., Takaishi, M., Shiga, T., Miyoshi, K., Nakajima, H., Kamijima, R., Tarutani, M., Benson, J., Elloso, M. M., et al. (2011) · The Journal of Immunology · doi:10.4049/jimmunol.1000148 · Cited by 160 · see citing works
“studies (22, 23, 32) and suggests that although IL-17A is a cytokine induced by IL-23, IL-22 is another cytokine downstream of IL-23 that might be critical for development of psoriasis (Figs.”
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“There were no differences in IL-17A or IFN-g production from cutaneous CD8+ or gd T cells between Treg-cell-sufficient and Treg-cell-depleted animals, and we did not observe any appreciable amounts of Th2 cytokines (IL-5 and IL-13) being produced by effector T (Teff) cells (Figures 2F and Immunity 50, 655–667, March 1…”
InfluentialImplantable synthetic cytokine converter cells with AND-gate logic treat experimental psoriasis
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“IL22 synergizes with other proinflammatory cytokines (13), particularly TNF (14), to drive psoriasis-promoting activities, such as the proliferation of keratinocytes (14, 15).”
BackgroundRabeony, H., Petit-Paris, I., Garnier, J., Barrault, C., Pedretti, N., Guilloteau, K., Jégou, J., Guillet, G., Huguier, V., Lecron, J., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0101937 · Cited by 141 · see citing works
“showing their inflammatory activities on keratinocyte [10,16,17].”
BackgroundMethodInfluentialSelf-citationRole of Th22 Cells in the Pathogenesis of Autoimmune Diseases
Jiang, Q., Yang, G., Xiao, F., Xie, J., Wang, S., Lu, L., & Cui, D. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.688066 · Cited by 138 · see citing works
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A Double Edged Sword Role of Interleukin-22 in Wound Healing and Tissue Regeneration
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“Pro-inflammatory activity performed by IL-22 has also been associated with several inflammatory diseases such as psoriasis and atopic dermatitis (61, 62).”
BackgroundThe TNF/IL‐23/IL‐17 axis—Head‐to‐head trials comparing different biologics in psoriasis treatment
ten Bergen, L. L., Petrovic, A., Aarebrot, A. K., & Appel, S. (2020) · Scandinavian Journal of Immunology · doi:10.1111/sji.12946 · Cited by 130 · see citing works
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“infiltration and an early epidermal acanthosis [14] (and”
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The Biology and Functions of Th22 Cells
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Distinct roles of IL-22 in human psoriasis and inflammatory bowel disease
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“Furthermore, IL-22, IL-17, OSM, IL-1a and TNF-a can synergistically induce some skin features recapitulating psoriasis closely both in vitro and in vivo [80].”
BackgroundSkin Pigmentation and Pigmentary Disorders: Focus on Epidermal/Dermal Cross-Talk
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New pathogenic and therapeutic paradigms in atopic dermatitis
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“sible for the production of IL-22, are elevated in patients with chronic AD [75,157,158].”
BackgroundHuman αβ and γδ T Cells in Skin Immunity and Disease
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“Secukinumab binds and blocks the activation of IL-17A which inhibits the production of β-defensin 2 and CXCL8 in human keratinocytes increasing pro-inflammatory cytokine production (119, 120).”
BackgroundReviews of Interleukin-37: Functions, Receptors, and Roles in Diseases
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“Psoriasis is an autoimmunemediated chronic inflammatory skin disorder and abnormal expression of inflammatory mediators plays an important role in the pathogenesis of this disease [66, 67].”
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The skin surface as antimicrobial barrier: present concepts and future outlooks
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“5 Anti-TNF agents Anti-TNF agents have been successful in treating psoriasis [134-136,138-140]; probably because TNF and its synergistic interaction with IL-17 mediate the pathogenesis of psoriasis [117,121].”
BackgroundFunctional role of IL-22 in psoriatic arthritis
Mitra, A., Raychaudhuri, S. K., & Raychaudhuri, S. P. (2012) · Arthritis Research & Therapy · doi:10.1186/ar3781 · Cited by 104 · see citing works
Antiviral and Immunomodulatory Properties of Antimicrobial Peptides Produced by Human Keratinocytes
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“In addition, incubation of primary human keratinocytes with pro-inflammatory cytokines can stimulate AMP synthesis (Guilloteau et al., 2010; Firat et al., 2014).”
BackgroundEmerging role of IL-35 in inflammatory autoimmune diseases
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Molecular Biology of Atopic Dermatitis
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Insights into IL-37, the role in autoimmune diseases
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Psoriasis and Atopic Dermatitis
Griffiths, C. E. M., van de Kerkhof, P., & Czarnecka-Operacz, M. M. (2017) · Dermatology and Therapy · doi:10.1007/s13555-016-0167-9 · Cited by 88 · see citing works
“Several cytokines have been implicated in atopic allergic disease [70, 71].”
BackgroundConventional NK Cells Can Produce IL-22 and Promote Host Defense in Klebsiella pneumoniae Pneumonia
Xu, X., Weiss, I. D., Zhang, H. H., Singh, S. P., Wynn, T. A., Wilson, M. S., & Farber, J. M. (2014) · The Journal of Immunology · doi:10.4049/jimmunol.1300039 · Cited by 88 · see citing works
“The diminished expression of Tnfa might have had broader consequences, because TNF-a was shown to synergize with IL-22 in promoting an inflammatory response (61, 62), and the loss of TNF-a might have compounded the effects of decreased IL-22 in the infected, NK cell–depleted mice.”
BackgroundDermatophyte infection: from fungal pathogenicity to host immune responses
Deng, R., Wang, X., & Li, R. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1285887 · Cited by 86 · see citing works
Cellular Mechanisms of Psoriasis Pathogenesis: A Systemic Review
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“High levels of IL-22 induce the expression and release of antimicrobial peptides (AMPs), such as S100A7, S100A8, S100A9, and β-defensin, as well as neutrophil chemokines, including CXCL8, CXCL5, and CXCL1, in the epidermis.(88) All these upregulated molecules contribute directly or indirectly to facilitating the devel…”
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Self-citationIL-22 Binding Protein (IL-22BP) in the Regulation of IL-22 Biology
Zenewicz, L. A. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.766586 · Cited by 77 · see citing works
“These responses can be further modulated by the presence of other cytokines, such as IFNg and IL-17 (38, 39).”
BackgroundOne SNP at a Time: Moving beyond GWAS in Psoriasis
Ray-Jones, H. F., Eyre, S., Barton, A. C., & Warren, R. B. (2016) · Journal of Investigative Dermatology · doi:10.1016/j.jid.2015.11.025 · Cited by 73 · see citing works
“Stimulation is also likely to be an important factor, especially because psoriatic lesions are thought to be subjected to a range of cytokines, such as tumor necrosis factor-a, OSM IL-22, IL-17A, and IL-1a (Bernard et al., 2012; Guilloteau et al., 2010; Rabeony et al., 2014).”
BackgroundNFATc1 supports imiquimod-induced skin inflammation by suppressing IL-10 synthesis in B cells
Alrefai, H., Muhammad, K., Rudolf, R., Pham, D. A. T., Klein‐Hessling, S., Patra, A. K., Avots, A., Bukur, V., Şahin, U., Tenzer, S., et al. (2016) · Nature Communications · doi:10.1038/ncomms11724 · Cited by 72 · see citing works
Th17 cell pathogenicity in autoimmune disease
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“Preclinical disease models also demonstrate the role of IL-17E in inducing keratinocyte proliferation and production of proin fl am-matory cytokines and chemokines 80 , which further recruit neutrophils to the in fl amed skin 81 .”
IL-23-Mediated Epidermal Hyperplasia Is Dependent on IL-6
Lindroos, J., Svensson, L. G., Norsgaard, H., Lovato, P., Moller, K., Hagedorn, P., Olsen, G. M., & Labuda, T. (2011) · Journal of Investigative Dermatology · doi:10.1038/jid.2010.432 · Cited by 69 · see citing works
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Chopra, D., Arens, R. A., Amornpairoj, W., Lowes, M. A., Tomic‐Canic, M., Štrbo, N., Lev‐Tov, H. A., & Pastar, I. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.960488 · Cited by 65 · see citing works
“The increase of S100 proteins may occur in response to elevated inflammatory cytokines such as interleukin (IL)-17 and IL-22, as in psoriasis (110, 111).”
BackgroundConjunctival Transcriptome in Scarring Trachoma
Burton, M. J., Rajak, S. N., Bauer, J., Weiss, H. A., Tolbert, S. B., Shoo, A., Habtamu, E., Manjurano, A. M., Emerson, P. M., Mabey, D. C. W., et al. (2010) · Infection and Immunity · doi:10.1128/iai.00888-10 · Cited by 65 · see citing works
A Systems Model for Immune Cell Interactions Unravels the Mechanism of Inflammation in Human Skin
Valeyev, N. V., Hundhausen, C., Umezawa, Y., Kotov, N. V., Williams, G. H., Clop, A., Ainali, C., Ouzounis, C. A., Tsoka, S., & Nestle, F. O. (2010) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1001024 · Cited by 62 · see citing works
IL-17: Balancing Protective Immunity and Pathogenesis
Sun, L., Wang, L., Moore, B. B., Zhang, S., Xiao, P., Decker, A. M., & Wang, H. (2023) · Journal of Immunology Research · doi:10.1155/2023/3360310 · Cited by 60 · see citing works
“TNF-α can have an additional synergistic effect with IL-17 to increase the production of AMPs, such as β-defensin 2 and S100A7 by keratinocytes [80, 81].”
BackgroundEffect of IL-17 receptor A blockade with brodalumab in inflammatory diseases
Nirula, A., Nilsen, J., Klekotka, P. A., Kricorian, G., Erondu, N., Towne, J. E., Russell, C. B., Martin, D. A., & Budelsky, A. (2016) · Lara D. Veeken · doi:10.1093/rheumatology/kew346 · Cited by 59 · see citing works
Chiliveru, S., Rahbek, S. H., Jensen, S. K., Jørgensen, S. E., Nissen, S. K., Christiansen, S. H., Mogensen, T. H., Jakobsen, M. R., Iversen, L., Johansen, C., et al. (2014) · The Journal of Immunology · doi:10.4049/jimmunol.1302120 · Cited by 57 · see citing works
“ulates some features of psoriasis (28).”
Pohin, M., Guesdon, W., Mekouo, A. A. T., Rabeony, H., Pâris, I., Atanassov, H., Favot, L., Mcheik, J. N., Bernard, F., Richards, C. D., et al. (2016) · European Journal of Immunology · doi:10.1002/eji.201546216 · Cited by 58 · see citing works
Self-citationAn ex vivo Human Skin Model to Study Superficial Fungal Infections
Corzo-León, D., Munro, C. A., & MacCallum, D. M. (2019) · Frontiers in Microbiology · doi:10.3389/fmicb.2019.01172 · Cited by 57 · see citing works
“…been used to investigate skin barrier repair (Danso et al., 2015), wound healing (Xu et al., 2012), chemical toxicity (Nakamura et al., 1990), chronic inflammatory diseases (Guilloteau et al., 2010), DNA vaccination (Ng et al., 2009) and fungal infection (Peres et al., 2016; Poyntner et al., 2016).”
BackgroundSmall molecule inhibitors of RORγt for Th17 regulation in inflammatory and autoimmune diseases
Zeng, J., Li, M., Zhao, Q., Chen, M., Zhao, L., Wei, S., Yang, H., Zhao, Y., Wang, A., Shen, J., et al. (2023) · Journal of Pharmaceutical Analysis · doi:10.1016/j.jpha.2023.05.009 · Cited by 58 · see citing works
Cytokine Signature and Involvement in Chronic Rhinosinusitis with Nasal Polyps
Carsuzaa, F., Béquignon, É., Dufour, X., de Bonnecaze, G., Lecron, J., & Favot, L. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms23010417 · Cited by 55 · see citing works
“In vitro and in vivo data indicate that on keratinocytes, IL-17 acts synergistically with IL-1, IL-22, OSM and TNF-α to induce powerful inflammation [92,93].”
BackgroundSelf-citationTWEAK/Fn14 activation induces keratinocyte proliferation under psoriatic inflammation
Cheng, H., Xu, M., Liu, X.-M., Zou, X., Zhan, N., & Xia, Y. (2015) · Experimental Dermatology · doi:10.1111/exd.12820 · Cited by 55 · see citing works
IL-22 capacitates dermal fibroblast responses to TNF in scleroderma
Brembilla, N. C., Dufour, A. M., Alvarez, M., Hugues, S., Montanari, E., Truchetet, M., Lonati, P. A., Fontao, L., Gabrielli, A., Vettori, S., et al. (2015) · Annals of the Rheumatic Diseases · doi:10.1136/annrheumdis-2015-207477 · Cited by 54 · see citing works
Role of Aryl Hydrocarbon Receptor Activation and Autophagy in Psoriasis-Related Inflammation
Kim, H. R., Kang, S. Y., Kim, H. O., Park, C. W., & Chung, B. Y. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21062195 · Cited by 52 · see citing works
“HaCaT cells were stimulated with M5, causing inflammation and presenting a variety of features of psoriasis [17].”
InfluentialA critical role for donor-derived IL-22 in cutaneous chronic GVHD
Gartlan, K. H., Bommiasamy, H., Paz, K. G., Wilkinson, A., Owen, M., Reichenbach, D. K., Banovic, T., Wehner, K., Buchanan, F. B., Varelias, A., et al. (2017) · American Journal of Transplantation · doi:10.1111/ajt.14513 · Cited by 51 · see citing works
Yan, D., Gudjonsson, J. E., Le, S. T., Maverakis, E. M., Plazyo, O., Ritchlin, C. T., Scher, J. U., Gangwar, R. S., Ward, N. L., Bell, S. J., et al. (2021) · Journal of Investigative Dermatology · doi:10.1016/j.jid.2021.02.764 · Cited by 51 · see citing works
IL-17A and IFN-γ Synergistically Induce RNase 7 Expression via STAT3 in Primary Keratinocytes
Simanski, M., Rademacher, F., Schröder, L. C., Schumacher, H. M., Gläser, R., & Harder, J. (2013) · PLoS ONE · doi:10.1371/journal.pone.0059531 · Cited by 50 · see citing works
Son, E. D., Kim, H.-J., Kim, K. H., Bin, B., Bae, I., Lim, K., Yu, S. J., Cho, E., & Lee, T. R. (2016) · Experimental Dermatology · doi:10.1111/exd.13023 · Cited by 48 · see citing works
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Burton, M. J., Ramadhani, A. M., Weiss, H. A., Hu, V. H., Massae, P., Burr, S. E., Shangali, W., Holland, M. J., Mabey, D. C. W., & Bailey, R. L. (2011) · Infection and Immunity · doi:10.1128/iai.05718-11 · Cited by 47 · see citing works
“S100A7 production is triggered by some bacterial components through PRRs and by proinflammatory cytokines (2, 22, 56).”
BackgroundC10orf99 contributes to the development of psoriasis by promoting the proliferation of keratinocytes
Chen, C., Wu, N., Duan, Q., Yang, H., Wang, X., Yang, P., Zhang, M., Liu, J., Liu, Z., Shao, Y., et al. (2018) · Scientific Reports · doi:10.1038/s41598-018-26996-z · Cited by 47 · see citing works
Rioux, G., Ridha, Z., Simard, M., Turgeon, F., Guérin, S. L., & Pouliot, R. (2020) · Genes · doi:10.3390/genes11101155 · Cited by 46 · see citing works
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Psoriasis and Cardiovascular Diseases: An Immune-Mediated Cross Talk?
Orlando, G., Molon, B., Viola, A., Alaibac, M., Angioni, R., & Piaserico, S. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.868277 · Cited by 46 · see citing works
Isothiocyanates inhibit psoriasis-related proinflammatory factors in human skin
Yehuda, H., Soroka, Y., Frušić‐Zlotkin, M., Gilhar, A., Milner, Y., & Tamir, S. (2012) · Inflammation Research · doi:10.1007/s00011-012-0465-3 · Cited by 45 · see citing works
“This type of culture has been employed as a basis for skin inflammation studies [32], and recently in a psoriasis model [33].”
MethodKinetic Cytokine Secretion Profile of LPS-Induced Inflammation in the Human Skin Organ Culture
Gvirtz, R., Ogen‐Shtern, N., & Cohen, G. (2020) · Pharmaceutics · doi:10.3390/pharmaceutics12040299 · Cited by 45 · see citing works
“Moreover, by using different inflammatory stimuli, such as IL-17 and TNFα instead of LPS, the HSOC can be used as a model for specific skin disorders, such as psoriasis [11,14,23].”
MethodKnockdown of lncRNA MIR31HG inhibits cell proliferation in human HaCaT keratinocytes
Gao, J., Chen, F., Hua, M., Guo, J., Nong, Y., Tang, Q., Zhong, F., & Qin, L. (2018) · Biological Research · doi:10.1186/s40659-018-0181-8 · Cited by 44 · see citing works
“In psoriasis, pro-inflammatory cytokines including IL-17A, IL-22, TNF-α and IL-1α may contribute to the pathophysiology of the disease [2, 19].”
Wang, Y., Han, D., Huang, Y., Dai, Y., Wang, Y., Liu, M., Wang, N., Yin, T., Du, W., He, K., et al. (2023) · Phytotherapy Research · doi:10.1002/ptr.8071 · Cited by 43 · see citing works
“HEKa and HaCaT cells were stimulated with M5 (a cocktail of cytokines, 10 ng/mL), which includes TNF-α , IL-17A, IL-22, IL-1 α , and Oncostatin-M (Peprotech, Cranbury, New Jersey, USA) for 24 h to induce psoriatic inflammation in cells (Guilloteau et al., 2010).”
MethodCheng, Z., Liang, X., Liang, S., Yin, N., & Faiola, F. (2019) · Journal of Environmental Sciences · doi:10.1016/j.jes.2019.06.016 · Cited by 42 · see citing works
IL-22 Protects against Tissue Damage during Cutaneous Leishmaniasis
Gimblet, C., Loesche, M. A., Carvalho, L. P., Carvalho, E. M., Grice, E. A., Artis, D., & Scott, P. (2015) · PLoS ONE · doi:10.1371/journal.pone.0134698 · Cited by 41 · see citing works
- Authors
- Guilloteau, K., Paris, I., Pedretti, N., Boniface, K., Juchaux, F., Huguier, V., Guillet, G., Bernard, F.-X., Lecron, J.-C., & Morel, F.
- Affiliations
- Laboratoire Inflammation, Tissus Épithéliaux et Cytokines (FR)
- Université de Poitiers (FR)
- Centre de Chirurgie Plastique (CH)
- Centre Hospitalier Universitaire de Poitiers (FR)
- Corresponding author
- Guilloteau, Karline
- Paris, Isabelle
- Pedretti, Nathalie
- Boniface, Katia
- Juchaux, Franck
- Morel, Franck
- ORCID
- Venue
- The Journal of Immunology
- Publisher
- Oxford University Press (OUP)
- Published
- 2010-05-01
- Volume
- 184
- Issue
- 9
- Pages
- 5263-5270
- ISSN
- 0022-1767 (ISSN-L)
- 1550-6606
- OpenAlex
- W1560379370
- Cited by
- 353
- References
- 51
- Citations by year
- 2026: 14 · 2025: 23 · 2024: 31 · 2023: 39 · 2022: 22 · 2021: 29 · 2020: 32 · 2019: 16 · 2018: 17 · 2017: 18 · 2016: 16 · 2015: 18 · 2014: 24 · 2013: 12 · 2012: 14
- FWCI
- 7.43
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- The Journal of Immunology (publishedVersion)
- PubMed (publishedVersion)
- HAL (submittedVersion)
- Funders
- Ligue Contre le Cancer
- Centre Hospitalier Universitaire de Poitiers
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › Psoriasis: Treatment and Pathogenesis
- Health Sciences › Medicine › Dermatology › Dermatology and Skin Diseases
- Health Sciences › Medicine › Oncology › Cytokine Signaling Pathways and Interactions
- Keywords
- psoriasis, skin inflammation, keratinocytes, IL-17A, IL-22, oncostatin M, IL-1α, TNF-α, cytokine synergy, chemokines, antimicrobial peptides, human beta-defensin 2, human beta-defensin 3, S100A7, S100A9, interleukin-8, neutrophil infiltration
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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