Spatial proteomics identifies JAKi as treatment for a lethal skin disease.


Journal

Nature
ISSN: 1476-4687
Titre abrégé: Nature
Pays: England
ID NLM: 0410462

Informations de publication

Date de publication:
16 Oct 2024
Historique:
received: 13 09 2023
accepted: 17 09 2024
medline: 17 10 2024
pubmed: 17 10 2024
entrez: 16 10 2024
Statut: aheadofprint

Résumé

Toxic epidermal necrolysis (TEN) is a fatal drug-induced skin reaction triggered by common medications and is an emerging public health issue

Identifiants

pubmed: 39415009
doi: 10.1038/s41586-024-08061-0
pii: 10.1038/s41586-024-08061-0
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© 2024. The Author(s).

Références

Harris, V., Jackson, C. & Cooper, A. Review of toxic epidermal necrolysis. Int. J. Mol. Sci. 17, 2135 (2016).
pubmed: 27999358 doi: 10.3390/ijms17122135
Sekula, P. et al. Comprehensive survival analysis of a cohort of patients with Stevens–Johnson syndrome and toxic epidermal necrolysis. J. Invest. Dermatol. 133, 1197–1204 (2013).
pubmed: 23389396 doi: 10.1038/jid.2012.510
Lazarou, J., Pomeranz, B. H. & Corey, P. N. Incidence of adverse drug reactions in hospitalized patients: a meta-analysis of prospective studies. JAMA 279, 1200–1205 (1998).
pubmed: 9555760 doi: 10.1001/jama.279.15.1200
Downey, A., Jackson, C., Harun, N. & Cooper, A. Toxic epidermal necrolysis: review of pathogenesis and management. J. Am. Acad. Dermatol. 66, 995–1003 (2012).
pubmed: 22169256 doi: 10.1016/j.jaad.2011.09.029
Hoetzenecker, W. et al. Toxic epidermal necrolysis. F1000Research 5, 951 (2016).
doi: 10.12688/f1000research.7574.1
Chang, W. C. et al. SJS/TEN 2019: From science to translation. J. Dermatol. Sci. 98, 2–12 (2020).
pubmed: 32192826 doi: 10.1016/j.jdermsci.2020.02.003
Mund, A. et al. Deep Visual Proteomics defines single-cell identity and heterogeneity. Nat. Biotechnol. 40, 1231–1240 (2022).
pubmed: 35590073 doi: 10.1038/s41587-022-01302-5
Rosenberger, F. A. et al. Spatial single-cell mass spectrometry defines zonation of the hepatocyte proteome. Nat. Methods 20, 1530–1536(2023).
Del Pozzo-Magana, B. R. & Liy-Wong, C. Drugs and the skin: a concise review of cutaneous adverse drug reactions. Br. J. Clin. Pharmacol. 90, 1838–1855 (2024).
pubmed: 35974692 doi: 10.1111/bcp.15490
Hung, S. I. et al. HLA-B*5801 allele as a genetic marker for severe cutaneous adverse reactions caused by allopurinol. Proc. Natl Acad. Sci. USA 102, 4134–4139 (2005).
pubmed: 15743917 doi: 10.1073/pnas.0409500102
Chung, W. H., Hung, S. I. & Chen, Y. T. Human leukocyte antigens and drug hypersensitivity. Curr. Opin. Allergy Clin. Immunol. 7, 317–323 (2007).
pubmed: 17620823 doi: 10.1097/ACI.0b013e3282370c5f
Chung, W. H. et al. Medical genetics: a marker for Stevens–Johnson syndrome. Nature 428, 486 (2004).
pubmed: 15057820 doi: 10.1038/428486a
Ko, T. M. et al. Shared and restricted T-cell receptor use is crucial for carbamazepine-induced Stevens–Johnson syndrome. J. Allergy Clin. Immunol. 128, 1266–1276.e1211 (2011).
pubmed: 21924464 doi: 10.1016/j.jaci.2011.08.013
Nassif, A. et al. Toxic epidermal necrolysis: effector cells are drug-specific cytotoxic T cells. J. Allergy Clin. Immunol. 114, 1209–1215 (2004).
pubmed: 15536433 doi: 10.1016/j.jaci.2004.07.047
Le Cleach, L. et al. Blister fluid T lymphocytes during toxic epidermal necrolysis are functional cytotoxic cells which express human natural killer (NK) inhibitory receptors. Clin. Exp. Immunol. 119, 225–230 (2000).
pubmed: 10606987 doi: 10.1046/j.1365-2249.2000.01119.x
Friedmann, P. S., Strickland, I., Pirmohamed, M. & Park, B. K. Investigation of mechanisms in toxic epidermal necrolysis induced by carbamazepine. Arch. Dermatol. 130, 598–604 (1994).
pubmed: 8179341 doi: 10.1001/archderm.1994.01690050066011
Villada, G., Roujeau, J. C., Clerici, T., Bourgault, I. & Revuz, J. Immunopathology of toxic epidermal necrolysis. Keratinocytes, HLA-DR expression, Langerhans cells, and mononuclear cells: an immunopathologic study of five cases. Arch. Dermatol. 128, 50–53 (1992).
pubmed: 1739287 doi: 10.1001/archderm.1992.01680110060006
Heng, M. C. & Allen, S. G. Efficacy of cyclophosphamide in toxic epidermal necrolysis. Clinical and pathophysiologic aspects. J. Am. Acad. Dermatol. 25, 778–786 (1991).
pubmed: 1802900 doi: 10.1016/S0190-9622(08)80969-3
Correia, O., Delgado, L., Ramos, J. P., Resende, C. & Torrinha, J. A. Cutaneous T-cell recruitment in toxic epidermal necrolysis. Further evidence of CD8
pubmed: 8466217 doi: 10.1001/archderm.1993.01680250078010
Viard, I. et al. Inhibition of toxic epidermal necrolysis by blockade of CD95 with human intravenous immunoglobulin. Science 282, 490–493 (1998).
pubmed: 9774279 doi: 10.1126/science.282.5388.490
Paul, C. et al. Apoptosis as a mechanism of keratinocyte death in toxic epidermal necrolysis. Br. J. Dermatol. 134, 710–714 (1996).
pubmed: 8733377 doi: 10.1111/j.1365-2133.1996.tb06976.x
Saito, N. et al. An annexin A1-FPR1 interaction contributes to necroptosis of keratinocytes in severe cutaneous adverse drug reactions. Sci. Transl. Med. 6, 245ra295 (2014).
doi: 10.1126/scitranslmed.3008227
Viard-Leveugle, I. et al. TNF-alpha and IFN-gamma are potential inducers of Fas-mediated keratinocyte apoptosis through activation of inducible nitric oxide synthase in toxic epidermal necrolysis. J. Invest. Dermatol. 133, 489–498 (2013).
pubmed: 22992806 doi: 10.1038/jid.2012.330
Chung, W. H. et al. Granulysin is a key mediator for disseminated keratinocyte death in Stevens–Johnson syndrome and toxic epidermal necrolysis. Nat. Med. 14, 1343–1350 (2008).
pubmed: 19029983 doi: 10.1038/nm.1884
Bruggen, M. C. et al. Supportive care in the acute phase of Stevens–Johnson syndrome and toxic epidermal necrolysis: an international, multidisciplinary Delphi-based consensus. Br. J. Dermatol. 185, 616–626 (2021).
pubmed: 33657677 doi: 10.1111/bjd.19893
Vandereyken, K., Sifrim, A., Thienpont, B. & Voet, T. Methods and applications for single-cell and spatial multi-omics. Nat. Rev. Genet. 24, 494–515 (2023).
pubmed: 36864178 doi: 10.1038/s41576-023-00580-2
Mund, A., Brunner, A. D. & Mann, M. Unbiased spatial proteomics with single-cell resolution in tissues. Mol. Cell 82, 2335–2349 (2022).
pubmed: 35714588 doi: 10.1016/j.molcel.2022.05.022
Fleckner, J., Martensen, P. M., Tolstrup, A. B., Kjeldgaard, N. O. & Justesen, J. Differential regulation of the human, interferon inducible tryptophanyl-tRNA synthetase by various cytokines in cell lines. Cytokine 7, 70–77 (1995).
pubmed: 7749068 doi: 10.1006/cyto.1995.1009
Lerner, L. H., Qureshi, A. A., Reddy, B. V. & Lerner, E. A. Nitric oxide synthase in toxic epidermal necrolysis and Stevens–Johnson syndrome. J. Invest. Dermatol. 114, 196–199 (2000).
pubmed: 10620138 doi: 10.1046/j.1523-1747.2000.00816.x
Quinn, A. M. et al. Uncovering histologic criteria with prognostic significance in toxic epidermal necrolysis. Arch. Dermatol. 141, 683–687 (2005).
pubmed: 15967913 doi: 10.1001/archderm.141.6.683
Kim, D. et al. Targeted therapy guided by single-cell transcriptomic analysis in drug-induced hypersensitivity syndrome: a case report. Nat. Med. 26, 236–243 (2020).
pubmed: 31959990 doi: 10.1038/s41591-019-0733-7
Chaudhuri, B., Xu, H., Todorov, I., Dutta, A. & Yates, J. L. Human DNA replication initiation factors, ORC and MCM, associate with oriP of Epstein–Barr virus. Proc. Natl Acad. Sci. USA 98, 10085–10089 (2001).
pubmed: 11517328 doi: 10.1073/pnas.181347998
Thielert, M. et al. Robust dimethyl-based multiplex-DIA doubles single-cell proteome depth via a reference channel. Mol. Syst. Biol. 19, e11503 (2023).
pubmed: 37602975 doi: 10.15252/msb.202211503
Guzman, U. H. et al. Ultra-fast label-free quantification and comprehensive proteome coverage with narrow-window data-independent acquisition. Nat. Biotechnol. https://doi.org/10.1038/s41587-023-02099-7 (2024).
Linkermann, A., Stockwell, B. R., Krautwald, S. & Anders, H. J. Regulated cell death and inflammation: an auto-amplification loop causes organ failure. Nat. Rev. Immunol. 14, 759–767 (2014).
pubmed: 25324125 doi: 10.1038/nri3743
Levy, D. E., Kessler, D. S., Pine, R., Reich, N. & Darnell, J. E. Jr. Interferon-induced nuclear factors that bind a shared promoter element correlate with positive and negative transcriptional control. Genes Dev. 2, 383–393 (1988).
pubmed: 3371658 doi: 10.1101/gad.2.4.383
Tretina, K., Park, E. S., Maminska, A. & MacMicking, J. D. Interferon-induced guanylate-binding proteins: Guardians of host defense in health and disease. J. Exp. Med. 216, 482–500 (2019).
pubmed: 30755454 doi: 10.1084/jem.20182031
Sung, Y., Yoon, I., Han, J. M. & Kim, S. Functional and pathologic association of aminoacyl-tRNA synthetases with cancer. Exp. Mol. Med. 54, 553–566 (2022).
pubmed: 35501376 doi: 10.1038/s12276-022-00765-5
Lewis, C. E., McCarthy, S. P., Lorenzen, J. & McGee, J. O. Differential effects of LPS, IFN-gamma and TNF alpha on the secretion of lysozyme by individual human mononuclear phagocytes: relationship to cell maturity. Immunology 69, 402–408 (1990).
pubmed: 2107146
Liao, W. et al. A novel anti-apoptotic role for apolipoprotein L2 in IFN-gamma-induced cytotoxicity in human bronchial epithelial cells. J. Cell. Physiol. 226, 397–406 (2011).
pubmed: 20665705 doi: 10.1002/jcp.22345
Wang, F. et al. Diverse expression of TNF-alpha and CCL27 in serum and blister of Stevens–Johnson syndrome/toxic epidermal necrolysis. Clin. Transl. Allergy 8, 12 (2018).
pubmed: 29713456 doi: 10.1186/s13601-018-0199-6
Wustner, L. S. Generating iPSCs with a high-efficient, non-invasive method-an improved way to cultivate keratinocytes from plucked hair for reprogramming. Cells 11, 1955 (2022).
pubmed: 35741085 doi: 10.3390/cells11121955
Anderton, H., Rickard, J. A., Varigos, G. A., Lalaoui, N. & Silke, J. Inhibitor of apoptosis proteins (IAPs) limit RIPK1-mediated skin inflammation. J. Invest. Dermatol. 137, 2371–2379 (2017).
pubmed: 28647349 doi: 10.1016/j.jid.2017.05.031
Saito, N. et al. Stevens–Johnson syndrome/toxic epidermal necrolysis mouse model generated by using PBMCs and the skin of patients. J. Allergy Clin. Immunol. 131, 434–441 e431-439 (2013).
pubmed: 23111236 doi: 10.1016/j.jaci.2012.09.014
Varfolomeev, E. et al. IAP antagonists induce autoubiquitination of c-IAPs, NF-kappaB activation, and TNFalpha-dependent apoptosis. Cell 131, 669–681 (2007).
pubmed: 18022362 doi: 10.1016/j.cell.2007.10.030
Vasilikos, L., Spilgies, L. M., Knop, J. & Wong, W. W. Regulating the balance between necroptosis, apoptosis and inflammation by inhibitors of apoptosis proteins. Immunol. Cell Biol. 95, 160–165 (2017).
pubmed: 27904150 doi: 10.1038/icb.2016.118
Chung, W. H. & Hung, S. I. Recent advances in the genetics and immunology of Stevens–Johnson syndrome and toxic epidermal necrosis. J. Dermatol. Sci. 66, 190–196 (2012).
pubmed: 22541332 doi: 10.1016/j.jdermsci.2012.04.002
Bastuji-Garin, S. et al. SCORTEN: a severity-of-illness score for toxic epidermal necrolysis. J. Invest. Dermatol. 115, 149–153 (2000).
pubmed: 10951229 doi: 10.1046/j.1523-1747.2000.00061.x
Bieber, T. et al. Abrocitinib versus placebo or dupilumab for atopic dermatitis. N. Engl. J. Med. 384, 1101–1112 (2021).
pubmed: 33761207 doi: 10.1056/NEJMoa2019380
Bracken, A. P. et al. EZH2 is downstream of the pRB–E2F pathway, essential for proliferation and amplified in cancer. EMBO J. 22, 5323–5335 (2003).
pubmed: 14532106 doi: 10.1093/emboj/cdg542
Hall, J. C. & Rosen, A. Type I interferons: crucial participants in disease amplification in autoimmunity. Nat. Rev. Rheumatol. 6, 40–49 (2010).
pubmed: 20046205 doi: 10.1038/nrrheum.2009.237
Zhu, J. et al. Stevens–Johnson syndrome/toxic epidermal necrolysis in patients treated with immune checkpoint inhibitors: A safety analysis of clinical trials and FDA pharmacovigilance database. eClinicalMedicine 37, 100951 (2021).
pubmed: 34386743 doi: 10.1016/j.eclinm.2021.100951
Ireland, P. A., Jansson, N., Spencer, S. K. R., Braden, J. & Sebaratnam, D. Short-term cardiovascular complications in dermatology patients receiving JAK-STAT inhibitors: a meta-analysis of randomized clinical trials. JAMA Dermatol. 160, 281–289 (2024).
pubmed: 38294793 doi: 10.1001/jamadermatol.2023.5509
Ytterberg, S. R. et al. Cardiovascular and cancer risk with tofacitinib in rheumatoid arthritis. N. Engl. J. Med. 386, 316–326 (2022).
pubmed: 35081280 doi: 10.1056/NEJMoa2109927
Nordmann, T. M. et al. A standardized and reproducible workflow for membrane glass slides in routine histology and spatial proteomics. Mol. Cell Proteomics 22, 100643 (2023).
pubmed: 37683827 doi: 10.1016/j.mcpro.2023.100643
Pachitariu, M. & Stringer, C. Cellpose 2.0: how to train your own model. Nat. Methods 19, 1634–1641 (2022).
pubmed: 36344832 doi: 10.1038/s41592-022-01663-4
Meier, F. et al. diaPASEF: parallel accumulation-serial fragmentation combined with data-independent acquisition. Nat. Methods 17, 1229–1236 (2020).
pubmed: 33257825 doi: 10.1038/s41592-020-00998-0
Brunner, A. D. et al. Ultra-high sensitivity mass spectrometry quantifies single-cell proteome changes upon perturbation. Mol. Syst. Biol. 18, e10798 (2022).
pubmed: 35226415 doi: 10.15252/msb.202110798
Demichev, V., Messner, C. B., Vernardis, S. I., Lilley, K. S. & Ralser, M. DIA-NN: neural networks and interference correction enable deep proteome coverage in high throughput. Nat. Methods 17, 41–44 (2020).
pubmed: 31768060 doi: 10.1038/s41592-019-0638-x
Al Tarrass, M. et al. Large-scale phosphoproteomics reveals activation of the MAPK/GADD45beta/P38 axis and cell cycle inhibition in response to BMP9 and BMP10 stimulation in endothelial cells. Cell Commun. Signal. 22, 158 (2024).
pubmed: 38439036 doi: 10.1186/s12964-024-01486-0
Walter, W., Sanchez-Cabo, F. & Ricote, M. GOplot: an R package for visually combining expression data with functional analysis. Bioinformatics 31, 2912–2914 (2015).
pubmed: 25964631 doi: 10.1093/bioinformatics/btv300
Krug, K. et al. A curated resource for phosphosite-specific signature analysis. Mol. Cell Proteomics 18, 576–593 (2019).
pubmed: 30563849 doi: 10.1074/mcp.TIR118.000943
Liao, Y., Wang, J., Jaehnig, E. J., Shi, Z. & Zhang, B. WebGestalt 2019: gene set analysis toolkit with revamped UIs and APIs. Nucleic Acids Res. 47, W199–W205 (2019).
pubmed: 31114916 doi: 10.1093/nar/gkz401

Auteurs

Thierry M Nordmann (TM)

Department of Proteomics and Signal Transduction; Max Planck Institute of Biochemistry, Martinsried, Germany. nordmann@biochem.mpg.de.
Department of Dermatology, University Hospital Zurich, University of Zurich, Zurich, Switzerland. nordmann@biochem.mpg.de.
Department of Dermatology and Allergy, University Hospital, Ludwig Maximilian University (LMU) Munich, Munich, Germany. nordmann@biochem.mpg.de.

Holly Anderton (H)

Inflammation division, Walter and Eliza Hall Institute of Medical Research, Melbourne, Victoria, Australia.
Department of Medical Biology, University of Melbourne, Parkville, Victoria, Australia.

Akito Hasegawa (A)

Division of Dermatology, Niigata University Graduate School of Medical and Dental Sciences, Niigata, Japan.

Lisa Schweizer (L)

Department of Proteomics and Signal Transduction; Max Planck Institute of Biochemistry, Martinsried, Germany.

Peng Zhang (P)

Department of Dermatology, The First Affiliated Hospital of Fujian Medical University, Fuzhou, China.

Pia-Charlotte Stadler (PC)

Department of Proteomics and Signal Transduction; Max Planck Institute of Biochemistry, Martinsried, Germany.
Department of Dermatology and Allergy, University Hospital, Ludwig Maximilian University (LMU) Munich, Munich, Germany.

Ankit Sinha (A)

Department of Proteomics and Signal Transduction; Max Planck Institute of Biochemistry, Martinsried, Germany.

Andreas Metousis (A)

Department of Proteomics and Signal Transduction; Max Planck Institute of Biochemistry, Martinsried, Germany.

Florian A Rosenberger (FA)

Department of Proteomics and Signal Transduction; Max Planck Institute of Biochemistry, Martinsried, Germany.

Maximilian Zwiebel (M)

Department of Proteomics and Signal Transduction; Max Planck Institute of Biochemistry, Martinsried, Germany.

Takashi K Satoh (TK)

Department of Dermatology and Allergy, University Hospital, Ludwig Maximilian University (LMU) Munich, Munich, Germany.

Florian Anzengruber (F)

Department of Dermatology, University Hospital Zurich, University of Zurich, Zurich, Switzerland.
Department of Internal Medicine, Division of Dermatology, Cantonal Hospital Graubuenden, Chur, Switzerland.

Maximilian T Strauss (MT)

Proteomics Program, Novo Nordisk Foundation Center for Protein Research, University of Copenhagen, Faculty of Health and Medical Sciences, Copenhagen, Denmark.

Maria C Tanzer (MC)

Inflammation division, Walter and Eliza Hall Institute of Medical Research, Melbourne, Victoria, Australia.
Department of Medical Biology, University of Melbourne, Parkville, Victoria, Australia.
Advanced Technology and Biology division, Walter and Eliza Hall Institute of Medical Research, Melbourne, Victoria, Australia.

Yuki Saito (Y)

Division of Dermatology, Niigata University Graduate School of Medical and Dental Sciences, Niigata, Japan.

Ting Gong (T)

Department of Dermatology, The First Affiliated Hospital of Fujian Medical University, Fuzhou, China.

Marvin Thielert (M)

Department of Proteomics and Signal Transduction; Max Planck Institute of Biochemistry, Martinsried, Germany.

Haruna Kimura (H)

Division of Dermatology, Niigata University Graduate School of Medical and Dental Sciences, Niigata, Japan.

Natasha Silke (N)

Inflammation division, Walter and Eliza Hall Institute of Medical Research, Melbourne, Victoria, Australia.
Department of Medical Biology, University of Melbourne, Parkville, Victoria, Australia.

Edwin H Rodriguez (EH)

Department of Proteomics and Signal Transduction; Max Planck Institute of Biochemistry, Martinsried, Germany.

Gaetana Restivo (G)

Department of Dermatology, University Hospital Zurich, University of Zurich, Zurich, Switzerland.

Hong Ha Nguyen (HH)

Division of Dermatology, Niigata University Graduate School of Medical and Dental Sciences, Niigata, Japan.

Annette Gross (A)

Immunoregulation Research Group, Max Planck Institute of Biochemistry, Martinsried, Germany.

Laurence Feldmeyer (L)

Department of Dermatology, Inselspital, Bern University Hospital, University of Bern, Bern, Switzerland.

Lukas Joerg (L)

Division of Allergology and Clinical Immunology, Department of Pneumology, Allergology and Clinical Immunology, Inselspital, Bern University Hospital, University of Bern, Bern, Switzerland.

Mitchell P Levesque (MP)

Department of Dermatology, University Hospital Zurich, University of Zurich, Zurich, Switzerland.

Peter J Murray (PJ)

Immunoregulation Research Group, Max Planck Institute of Biochemistry, Martinsried, Germany.

Saskia Ingen-Housz-Oro (S)

Dermatology Department, AP-HP, Henri Mondor Hospital, Créteil, France.

Andreas Mund (A)

Proteomics Program, Novo Nordisk Foundation Center for Protein Research, University of Copenhagen, Faculty of Health and Medical Sciences, Copenhagen, Denmark.

Riichiro Abe (R)

Division of Dermatology, Niigata University Graduate School of Medical and Dental Sciences, Niigata, Japan.

John Silke (J)

Inflammation division, Walter and Eliza Hall Institute of Medical Research, Melbourne, Victoria, Australia.
Department of Medical Biology, University of Melbourne, Parkville, Victoria, Australia.

Chao Ji (C)

Department of Dermatology, The First Affiliated Hospital of Fujian Medical University, Fuzhou, China. jichaofy@fjmu.edu.cn.
Key Laboratory of Skin Cancer of Fujian Higher Education Institutions, Fujian Medical University, Fuzhou, China. jichaofy@fjmu.edu.cn.

Lars E French (LE)

Department of Dermatology and Allergy, University Hospital, Ludwig Maximilian University (LMU) Munich, Munich, Germany. Lars.French@med.uni-muenchen.de.
Dr. Philip Frost Department of Dermatology and Cutaneous Surgery, University of Miami Miller School of Medicine, Miami, FL, USA. Lars.French@med.uni-muenchen.de.

Matthias Mann (M)

Department of Proteomics and Signal Transduction; Max Planck Institute of Biochemistry, Martinsried, Germany. mmann@biochem.mpg.de.
Proteomics Program, Novo Nordisk Foundation Center for Protein Research, University of Copenhagen, Faculty of Health and Medical Sciences, Copenhagen, Denmark. mmann@biochem.mpg.de.

Classifications MeSH