IFNγ binding to extracellular matrix prevents fatal systemic toxicity.


Journal

Nature immunology
ISSN: 1529-2916
Titre abrégé: Nat Immunol
Pays: United States
ID NLM: 100941354

Informations de publication

Date de publication:
03 2023
Historique:
received: 21 06 2022
accepted: 28 12 2022
pubmed: 3 2 2023
medline: 4 3 2023
entrez: 2 2 2023
Statut: ppublish

Résumé

Interferon-γ (IFNγ) is an important mediator of cellular immune responses, but high systemic levels of this cytokine are associated with immunopathology. IFNγ binds to its receptor (IFNγR) and to extracellular matrix (ECM) via four positively charged C-terminal amino acids (KRKR), the ECM-binding domain (EBD). Across evolution, IFNγ is not well conserved, but the EBD is highly conserved, suggesting a critical function. Here, we show that IFNγ lacking the EBD (IFNγ

Identifiants

pubmed: 36732425
doi: 10.1038/s41590-023-01420-5
pii: 10.1038/s41590-023-01420-5
pmc: PMC9977683
doi:

Substances chimiques

Cytokines 0
Interferon-gamma 82115-62-6

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

414-422

Commentaires et corrections

Type : ErratumIn
Type : ErratumIn

Informations de copyright

© 2023. The Author(s).

Références

Hedrick, S. M. The acquired immune system: a vantage from beneath. Immunity 21, 607–615 (2004).
doi: 10.1016/j.immuni.2004.08.020 pubmed: 15539148
Barber, D. L. et al. Restoring function in exhausted CD8 T cells during chronic viral infection. Nature 439, 682–687 (2006).
doi: 10.1038/nature04444 pubmed: 16382236
Sakaguchi, S., Fukuma, K., Kuribayashi, K. & Masuda, T. Organ-specific autoimmune diseases induced in mice by elimination of T cell subset. I. Evidence for the active participation of T cells in natural self-tolerance; deficit of a T cell subset as a possible cause of autoimmune disease. J. Exp. Med. 161, 72–87 (1985).
doi: 10.1084/jem.161.1.72 pubmed: 3871469
Tivol, E. A. et al. Loss of CTLA-4 leads to massive lymphoproliferation and fatal multiorgan tissue destruction, revealing a critical negative regulatory role of CTLA-4. Immunity 3, 541–547 (1995).
doi: 10.1016/1074-7613(95)90125-6 pubmed: 7584144
Toyonaga, T. et al. Chronic active hepatitis in transgenic mice expressing interferon-γ in the liver. Proc. Natl Acad. Sci. USA 91, 614–618 (1994).
doi: 10.1073/pnas.91.2.614 pubmed: 8290572 pmcid: 42999
Alexander, W. S. et al. SOCS1 is a critical inhibitor of interferon γ signaling and prevents the potentially fatal neonatal actions of this cytokine. Cell 98, 597–608 (1999).
doi: 10.1016/S0092-8674(00)80047-1 pubmed: 10490099
Thibaut, R. et al. Bystander IFN-γ activity promotes widespread and sustained cytokine signaling altering the tumor microenvironment. Nat. Cancer 1, 302–314 (2020).
doi: 10.1038/s43018-020-0038-2 pubmed: 32803171 pmcid: 7115926
Hoekstra, M. E. et al. Long-distance modulation of bystander tumor cells by CD8
doi: 10.1038/s43018-020-0036-4 pubmed: 32566933 pmcid: 7305033
Lortat-Jacob, H., Kleinman, H. K. & Grimaud, J. A. High-affinity binding of interferon-γ to a basement membrane complex (Matrigel). J. Clin. Invest. 87, 878–883 (1991).
doi: 10.1172/JCI115093 pubmed: 1900310 pmcid: 329877
Dobeli, H. et al. Role of the carboxy-terminal sequence on the biological-activity of human immune interferon (IFN-γ). J. Biotechnol. 7, 199–216 (1988).
doi: 10.1016/0168-1656(88)90052-1
Subramaniam, P. S., Larkin, J. 3rd, Mujtaba, M. G., Walter, M. R. & Johnson, H. M. The COOH-terminal nuclear localization sequence of interferon γ regulates STAT1 α nuclear translocation at an intracellular site. J. Cell Sci. 113, 2771–2781 (2000).
doi: 10.1242/jcs.113.15.2771 pubmed: 10893192
Sadir, R., Forest, E. & Lortat-Jacob, H. The heparan sulfate binding sequence of interferon-γ increased the on rate of the interferon-γ–interferon-γ receptor complex formation. J. Biol. Chem. 273, 10919–10925 (1998).
doi: 10.1074/jbc.273.18.10919 pubmed: 9556569
Savan, R., Ravichandran, S., Collins, J. R., Sakai, M. & Young, H. A. Structural conservation of interferon γ among vertebrates. Cytokine Growth Factor Rev. 20, 115–124 (2009).
doi: 10.1016/j.cytogfr.2009.02.006 pubmed: 19268624 pmcid: 2755191
Hemmi, S. et al. Cloning of murine interferon γ receptor cDNA: expression in human cells mediates high-affinity binding but is not sufficient to confer sensitivity to murine interferon γ. Proc. Natl Acad. Sci. USA 86, 9901–9905 (1989).
doi: 10.1073/pnas.86.24.9901 pubmed: 2532365 pmcid: 298610
Kammertoens, T. et al. Tumour ischaemia by interferon-γ resembles physiological blood vessel regression. Nature 545, 98–102 (2017).
doi: 10.1038/nature22311 pubmed: 28445461 pmcid: 5567674
Saesen, E. et al. Insights into the mechanism by which interferon-γ basic amino acid clusters mediate protein binding to heparan sulfate. J. Am. Chem. Soc. 135, 9384–9390 (2013).
doi: 10.1021/ja4000867 pubmed: 23734709
van der Loos, C. M. et al. Immunohistochemical detection of interferon-γ: fake or fact? J. Histochem. Cytochem. 49, 699–710 (2001).
doi: 10.1177/002215540104900604 pubmed: 11373317
Tsiantoulas, D. et al. APRIL limits atherosclerosis by binding to heparan sulfate proteoglycans. Nature 597, 92–96 (2021).
doi: 10.1038/s41586-021-03818-3 pubmed: 34433968
Ferran, C. et al. Inter-mouse strain differences in the in vivo anti-CD3 induced cytokine release. Clin. Exp. Immunol. 86, 537–543 (1991).
doi: 10.1111/j.1365-2249.1991.tb02966.x pubmed: 1721015 pmcid: 1554204
Kohler, J. et al. IFN-γ involvement in the severity of Gram-negative infections in mice. J. Immunol. 151, 916–921 (1993).
doi: 10.4049/jimmunol.151.2.916 pubmed: 8335919
Listopad, J. J. et al. Fas expression by tumor stroma is required for cancer eradication. Proc. Natl Acad. Sci. USA 110, 2276–2281 (2013).
doi: 10.1073/pnas.1218295110 pubmed: 23341634 pmcid: 3568383
Mendoza, J. L. et al. Structure of the IFNγ receptor complex guides design of biased agonists. Nature 567, 56–60 (2019).
doi: 10.1038/s41586-019-0988-7 pubmed: 30814731 pmcid: 6561087
Vallet, S. D., Clerc, O. & Ricard-Blum, S. Glycosaminoglycan–protein interactions: the first draft of the glycosaminoglycan interactome. J. Histochem. Cytochem. 69, 93–104 (2021).
doi: 10.1369/0022155420946403 pubmed: 32757871
Simon Davis, D. A. & Parish, C. R. Heparan sulfate: a ubiquitous glycosaminoglycan with multiple roles in immunity. Front. Immunol. 4, 470 (2013).
doi: 10.3389/fimmu.2013.00470 pubmed: 24391644 pmcid: 3866581
Collins, L. E. & Troeberg, L. Heparan sulfate as a regulator of inflammation and immunity. J. Leukoc. Biol. 105, 81–92 (2019).
doi: 10.1002/JLB.3RU0618-246R pubmed: 30376187
Oyler-Yaniv, J. et al. Catch and release of cytokines mediated by tumor phosphatidylserine converts transient exposure into long-lived inflammation. Mol. Cell 66, 635–647 (2017).
doi: 10.1016/j.molcel.2017.05.011 pubmed: 28575659 pmcid: 6611463
Lortat-Jacob, H., Baltzer, F. & Grimaud, J. A. Heparin decreases the blood clearance of interferon-γ and increases its activity by limiting the processing of its carboxyl-terminal sequence. J. Biol. Chem. 271, 16139–16143 (1996).
doi: 10.1074/jbc.271.27.16139 pubmed: 8663206
Lortat-Jacob, H. & Grimaud, J. A. Interferon-γ C-terminal function: new working hypothesis. Heparan sulfate and heparin, new targets for IFN-γ, protect, relax the cytokine and regulate its activity. Cell Mol. Biol. 37, 253–260 (1991).
pubmed: 1934005
Medzhitov, R., Schneider, D. S. & Soares, M. P. Disease tolerance as a defense strategy. Science 335, 936–941 (2012).
doi: 10.1126/science.1214935 pubmed: 22363001 pmcid: 3564547
Netea, M. G. et al. Trained immunity: a program of innate immune memory in health and disease. Science 352, aaf1098 (2016).
doi: 10.1126/science.aaf1098 pubmed: 27102489 pmcid: 5087274
Niec, R. E., Rudensky, A. Y. & Fuchs, E. Inflammatory adaptation in barrier tissues. Cell 184, 3361–3375 (2021).
doi: 10.1016/j.cell.2021.05.036 pubmed: 34171319 pmcid: 8336675
Rosshart, S. P. et al. Laboratory mice born to wild mice have natural microbiota and model human immune responses. Science 365, eaaw4361 (2019).
doi: 10.1126/science.aaw4361 pubmed: 31371577 pmcid: 7377314
Jasnin, M. et al. Dynamics of heparan sulfate explored by neutron scattering. Phys. Chem. Chem. Phys. 12, 3360–3362 (2010).
doi: 10.1039/b923878f pubmed: 20336244
Fidler, I. J. Selection of successive tumour lines for metastasis. Nat. New Biol. 242, 148–149 (1973).
doi: 10.1038/newbio242148a0 pubmed: 4512654
Willimsky, G. & Blankenstein, T. Sporadic immunogenic tumours avoid destruction by inducing T-cell tolerance. Nature 437, 141–146 (2005).
doi: 10.1038/nature03954 pubmed: 16136144
Haeussler, M. et al. Evaluation of off-target and on-target scoring algorithms and integration into the guide RNA selection tool CRISPOR. Genome Biol. 17, 148 (2016).
doi: 10.1186/s13059-016-1012-2 pubmed: 27380939 pmcid: 4934014
Chen, S. et al. Highly efficient mouse genome editing by CRISPR ribonucleoprotein electroporation of zygotes. J. Biol. Chem. 291, 14457–14467 (2016).
doi: 10.1074/jbc.M116.733154 pubmed: 27151215 pmcid: 4938170
Battegay, M. et al. Quantification of lymphocytic choriomeningitis virus with an immunological focus assay in 24- or 96-well plates. J. Virol. Methods 33, 191–198 (1991).
doi: 10.1016/0166-0934(91)90018-U pubmed: 1939506

Auteurs

Josephine Kemna (J)

Max-Delbrück Center for Molecular Medicine in the Helmholtz Association, Molecular Immunology and Gene Therapy, Berlin, Germany.

Evelyne Gout (E)

Institut de Biologie Structurale, UMR 5075, University Grenoble Alpes, Centre National de la Recherche Scientifique, Commissariat à l'Énergie Atomique et aux Énergies Alternatives, Grenoble, France.

Leon Daniau (L)

Institute for Immunodeficiency, Medical Center-University of Freiburg, Faculty of Medicine, University of Freiburg, Freiburg, Germany.
Faculty of Biology, Albert-Ludwigs-University of Freiburg, Freiburg, Germany.

Jessica Lao (J)

Institute for Immunodeficiency, Medical Center-University of Freiburg, Faculty of Medicine, University of Freiburg, Freiburg, Germany.
Faculty of Biology, Albert-Ludwigs-University of Freiburg, Freiburg, Germany.

Kristoffer Weißert (K)

Institute for Immunodeficiency, Medical Center-University of Freiburg, Faculty of Medicine, University of Freiburg, Freiburg, Germany.
Faculty of Biology, Albert-Ludwigs-University of Freiburg, Freiburg, Germany.
Center for Chronic Immunodeficiency (CCI), Medical Center-University of Freiburg, Faculty of Medicine, University of Freiburg, Freiburg, Germany.

Sandra Ammann (S)

Institute for Immunodeficiency, Medical Center-University of Freiburg, Faculty of Medicine, University of Freiburg, Freiburg, Germany.
Center for Chronic Immunodeficiency (CCI), Medical Center-University of Freiburg, Faculty of Medicine, University of Freiburg, Freiburg, Germany.

Ralf Kühn (R)

Transgenic Core Facility, Max-Delbrück Center for Molecular Medicine in the Helmholtz Association, Berlin, Germany.

Matthias Richter (M)

Advanced Light Microscopy Core Facility, Max-Delbrück Center for Molecular Medicine in the Helmholtz Association, Berlin, Germany.

Christine Molenda (C)

Advanced Light Microscopy Core Facility, Max-Delbrück Center for Molecular Medicine in the Helmholtz Association, Berlin, Germany.

Anje Sporbert (A)

Advanced Light Microscopy Core Facility, Max-Delbrück Center for Molecular Medicine in the Helmholtz Association, Berlin, Germany.

Dario Zocholl (D)

Charité-Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Institute of Biometry and Clinical Epidemiology, Berlin, Germany.

Robert Klopfleisch (R)

Department of Veterinary Medicine, Institute of Veterinary Pathology, Freie Universität Berlin, Berlin, Germany.

Anja Schütz (A)

Protein Production & Characterization Core Facility, Max-Delbrück Center for Molecular Medicine in the Helmholtz Association, Berlin, Germany.

Hugues Lortat-Jacob (H)

Institut de Biologie Structurale, UMR 5075, University Grenoble Alpes, Centre National de la Recherche Scientifique, Commissariat à l'Énergie Atomique et aux Énergies Alternatives, Grenoble, France.

Peter Aichele (P)

Institute for Immunodeficiency, Medical Center-University of Freiburg, Faculty of Medicine, University of Freiburg, Freiburg, Germany.
Center for Chronic Immunodeficiency (CCI), Medical Center-University of Freiburg, Faculty of Medicine, University of Freiburg, Freiburg, Germany.

Thomas Kammertoens (T)

Max-Delbrück Center for Molecular Medicine in the Helmholtz Association, Molecular Immunology and Gene Therapy, Berlin, Germany.
Institute of Immunology, Charité Unversitätsmedizin, Campus Buch, Berlin, Germany.

Thomas Blankenstein (T)

Max-Delbrück Center for Molecular Medicine in the Helmholtz Association, Molecular Immunology and Gene Therapy, Berlin, Germany. tblanke@mdc-berlin.de.

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