Mouse CD163 deficiency strongly enhances experimental collagen-induced arthritis.

Tytuł:: Mouse CD163 deficiency strongly enhances experimental collagen-induced arthritis.
Autorzy:: Svendsen P; Department of Molecular Medicine, University of Southern Denmark, Odense, Denmark.; Department of Clinical Medicine, Aarhus University Hospital, Aarhus, Denmark.
Etzerodt A; Department of Biomedicine, Aarhus University, Aarhus, Denmark.
Deleuran BW; Department of Biomedicine, Aarhus University, Aarhus, Denmark.; Department of Rheumatology, Aarhus University Hospital, Aarhus, Denmark.
Moestrup SK; Department of Molecular Medicine, University of Southern Denmark, Odense, Denmark. .; Department of Clinical Medicine, Aarhus University Hospital, Aarhus, Denmark. .; Department of Clinical Biochemistry, Aarhus University Hospital, Aarhus, Denmark. .
Źródło:: Scientific reports [Sci Rep] 2020 Jul 24; Vol. 10 (1), pp. 12447. Date of Electronic Publication: 2020 Jul 24.
Typ publikacji:: Journal Article; Research Support, Non-U.S. Gov't
Język:: English
Imprint Name(s):: Original Publication: London : Nature Publishing Group, copyright 2011-
MeSH Terms:: Arthritis, Experimental/*immunology
Arthritis, Rheumatoid/*immunology
Receptors, Cell Surface/*deficiency
Animals ; Antigens, CD/genetics ; Antigens, CD/immunology ; Antigens, Differentiation, Myelomonocytic/genetics ; Antigens, Differentiation, Myelomonocytic/immunology ; Arthritis, Experimental/blood ; Arthritis, Experimental/diagnosis ; Arthritis, Experimental/pathology ; Arthritis, Rheumatoid/blood ; Arthritis, Rheumatoid/diagnosis ; Arthritis, Rheumatoid/pathology ; Collagen Type II/immunology ; Cytokines/blood ; Cytokines/immunology ; Cytokines/metabolism ; Disease Progression ; Humans ; Joints/immunology ; Joints/pathology ; Macrophages/immunology ; Macrophages/metabolism ; Male ; Mice ; Mice, Knockout ; Receptors, Cell Surface/genetics ; Receptors, Cell Surface/immunology ; Severity of Illness Index ; Synovial Fluid/immunology ; Th1 Cells/immunology ; Th1 Cells/metabolism ; Th1-Th2 Balance ; Th2 Cells/immunology ; Th2 Cells/metabolism
References:: Kristiansen, M. et al. Identification of the haemoglobin scavenger receptor. Nature 409, 198–201. https://doi.org/10.1038/35051594 (2001). (PMID: 10.1038/3505159411196644)
Barbe, E., Damoiseaux, J. G., Dopp, E. A. & Dijkstra, C. D. Characterization and expression of the antigen present on resident rat macrophages recognized by monoclonal antibody ED2. Immunobiology 182, 88–99. https://doi.org/10.1016/S0171-2985(11)80586-3 (1990). (PMID: 10.1016/S0171-2985(11)80586-32098324)
Etzerodt, A. et al. Plasma clearance of hemoglobin and haptoglobin in mice and effect of CD163 gene targeting disruption. Antioxid. Redox Signal. 18, 2254–2263. https://doi.org/10.1089/ars.2012.4605 (2013). (PMID: 10.1089/ars.2012.460522793784)
Etzerodt, A. et al. Tissue-resident macrophages in omentum promote metastatic spread of ovarian cancer. J. Exp. Med. https://doi.org/10.1084/jem.20191869 (2020). (PMID: 10.1084/jem.2019186931951251)
Etzerodt, A. & Moestrup, S. K. CD163 and inflammation: biological, diagnostic, and therapeutic aspects. Antioxid. Redox Signal. 18, 2352–2363. https://doi.org/10.1089/ars.2012.4834 (2013). (PMID: 10.1089/ars.2012.4834229008853638564)
Bover, L. C. et al. A previously unrecognized protein–protein interaction between TWEAK and CD163: potential biological implications. J. Immunol. 178, 8183–8194. https://doi.org/10.4049/jimmunol.178.12.8183 (2007). (PMID: 10.4049/jimmunol.178.12.818317548657)
Yang, H. et al. Identification of CD163 as an antiinflammatory receptor for HMGB1-haptoglobin complexes. JCI Insight 1, e85375. https://doi.org/10.1172/jci.insight.85375 (2016). (PMID: 10.1172/jci.insight.853754902170)
Etzerodt, A. et al. Structural basis for inflammation-driven shedding of CD163 ectodomain and tumor necrosis factor-alpha in macrophages. J. Biol. Chem. 289, 778–788. https://doi.org/10.1074/jbc.M113.520213 (2014). (PMID: 10.1074/jbc.M113.52021324275664)
Black, R. A. et al. A metalloproteinase disintegrin that releases tumour-necrosis factor-alpha from cells. Nature 385, 729–733. https://doi.org/10.1038/385729a0 (1997). (PMID: 10.1038/385729a09034190)
Etzerodt, A. et al. Soluble ectodomain CD163 and extracellular vesicle-associated CD163 are two differently regulated forms of “soluble CD163” in plasma. Sci. Rep. 7, 40286. https://doi.org/10.1038/srep40286 (2017). (PMID: 10.1038/srep40286280843215234032)
van Baarsen, L. G. et al. Synovial tissue heterogeneity in rheumatoid arthritis in relation to disease activity and biomarkers in peripheral blood. Arthritis Rheumatol. 62, 1602–1607. https://doi.org/10.1002/art.27415 (2010). (PMID: 10.1002/art.27415)
Liu, Y. C., Zou, X. B., Chai, Y. F. & Yao, Y. M. Macrophage polarization in inflammatory diseases. Int. J. Biol. Sci. 10, 520–529. https://doi.org/10.7150/ijbs.8879 (2014). (PMID: 10.7150/ijbs.8879249105314046879)
Culemann, S. et al. Locally renewing resident synovial macrophages provide a protective barrier for the joint. Nature 572, 670–675. https://doi.org/10.1038/s41586-019-1471-1 (2019). (PMID: 10.1038/s41586-019-1471-1313915806805223)
Baeten, D. et al. Association of CD163+ macrophages and local production of soluble CD163 with decreased lymphocyte activation in spondylarthropathy synovitis. Arthritis Rheumatol. 50, 1611–1623. https://doi.org/10.1002/art.20174 (2004). (PMID: 10.1002/art.20174)
Greisen, S. R. et al. Macrophage activity assessed by soluble CD163 in early rheumatoid arthritis: association with disease activity but different response patterns to synthetic and biologic DMARDs. Clin. Exp. Rheumatol. 33, 498–502 (2015). (PMID: 25962601)
Martinez, F. O. & Gordon, S. The M1 and M2 paradigm of macrophage activation: time for reassessment. F1000Prime Rep. 6, 13. https://doi.org/10.12703/P6-13 (2014). (PMID: 10.12703/P6-13246692943944738)
Inglis, J. J., Simelyte, E., McCann, F. E., Criado, G. & Williams, R. O. Protocol for the induction of arthritis in C57BL/6 mice. Nat. Protoc. 3, 612–618. https://doi.org/10.1038/nprot.2008.19 (2008). (PMID: 10.1038/nprot.2008.1918388943)
Brand, D. D., Latham, K. A. & Rosloniec, E. F. Collagen-induced arthritis. Nat. Protocols 2, 1269–1275. https://doi.org/10.1038/nprot.2007.173 (2007). (PMID: 10.1038/nprot.2007.17317546023)
Khachigian, L. M. Collagen antibody-induced arthritis. Nat. Protocols 1, 2512–2516 (2006). (PMID: 10.1038/nprot.2006.393)
Inglis, J. J. et al. Collagen-induced arthritis in C57BL/6 mice is associated with a robust and sustained T-cell response to type II collagen. Arthritis Res. Therapy 9, R113. https://doi.org/10.1186/ar2319 (2007). (PMID: 10.1186/ar2319)
Campbell, I. K., Hamilton, J. A. & Wicks, I. P. Collagen-induced arthritis in C57BL/6 (H-2b) mice: new insights into an important disease model of rheumatoid arthritis. Eur. J. Immunol. https://doi.org/10.1002/1521-4141(200006)30:6<1568::AID-IMMU1568>3.0.CO;2-R (2000). (PMID: 10.1002/1521-4141(200006)30:6<1568::AID-IMMU1568>3.0.CO;2-R10898492)
Holmdahl, R., Bockermann, R., Backlund, J. & Yamada, H. The molecular pathogenesis of collagen-induced arthritis in mice—a model for rheumatoid arthritis. Ageing Res Rev. https://doi.org/10.1016/s0047-6374(01)00371-2 (2002). (PMID: 10.1016/s0047-6374(01)00371-212039453)
Watanabe, H., Numata, K., Ito, T., Takagi, K. & Matsukawa, A. Innate immune response in Th1- and Th2-dominant mouse strains. Shock (Augusta, Ga.) 22, 460–466 (2004). (PMID: 10.1097/01.shk.0000142249.08135.e9)
Muraille, E., Leo, O. & Moser, M. Th1/Th2 paradigm extended: macrophage polarization as an unappreciated pathogen-driven escape mechanism?. Front. Immunol. 5, 603. https://doi.org/10.3389/fimmu.2014.00603 (2014). (PMID: 10.3389/fimmu.2014.00603255054684244692)
Brand, D. D. et al. Autoantibodies to murine type II collagen in collagen-induced arthritis: a comparison of susceptible and nonsusceptible strains. J. Immunol. 157, 5178–5184 (1996). (PMID: 8943430)
Finkelman, F. D. et al. Lymphokine control of in vivo immunoglobulin isotype selection. Annu. Rev. Immunol. 8, 303–333. https://doi.org/10.1146/annurev.iy.08.040190.001511 (1990). (PMID: 10.1146/annurev.iy.08.040190.0015111693082)
Coffman, R. L., Lebman, D. A. & Rothman, P. Mechanism and regulation of immunoglobulin isotype switching. Adv. Immunol. 54, 229–270 (1993). (PMID: 10.1016/S0065-2776(08)60536-2)
Hashimoto, M. Th17 in animal models of rheumatoid arthritis. J Clin Med. https://doi.org/10.3390/jcm6070073 (2017). (PMID: 10.3390/jcm6070073287539825532581)
Madsen, D. H. et al. M2-like macrophages are responsible for collagen degradation through a mannose receptor–mediated pathway. J. Cell Biol. 202, 951–966. https://doi.org/10.1083/jcb.201301081 (2013). (PMID: 10.1083/jcb.201301081240195373776354)
Hagert, C., Sareila, O., Kelkka, T., Jalkanen, S. & Holmdahl, R. The macrophage mannose receptor regulate mannan-induced psoriasis, psoriatic arthritis, and rheumatoid arthritis-like disease models. Front. Immunol. 9, 114. https://doi.org/10.3389/fimmu.2018.00114 (2018). (PMID: 10.3389/fimmu.2018.00114294677565808283)
Nandakumar, K. S., Bäcklund, J., Vestberg, M. & Holmdahl, R. Collagen type II (CII)-specific antibodies induce arthritis in the absence of T or B cells but the arthritis progression is enhanced by CII-reactive T cells. Arthritis Res. Ther. 6, R544. https://doi.org/10.1186/ar1217 (2004). (PMID: 10.1186/ar1217155358321064861)
Hagert, C. et al. Chronic active arthritis driven by macrophages without involvement of T cells. Arthritis Rheumatol. (Hoboken, N.J.) https://doi.org/10.1002/art.40482 (2018). (PMID: 10.1002/art.40482)
Arend, W. P. & Dayer, J. M. Inhibition of the production and effects of interleukin-1 and tumor necrosis factor alpha in rheumatoid arthritis. Arthritis Rheumatol. 38, 151–160 (1995). (PMID: 10.1002/art.1780380202)
Horsfall, A. C. et al. Suppression of collagen-induced arthritis by continuous administration of IL-4. J. Immunol. 159, 5687–5696 (1997). (PMID: 9548513)
Inglis, J. J. et al. Collagen-induced arthritis in C57BL/6 mice is associated with a robust and sustained T-cell response to type II collagen. Arthritis Res. Ther. 9, R113. https://doi.org/10.1186/ar2319 (2007). (PMID: 10.1186/ar2319179671862212575)
Nandakumar, K. S. & Holmdahl, R. Arthritis induced with cartilage-specific antibodiesis IL-4-dependent. Eur. J. Immunol. 36, 1608–1618. https://doi.org/10.1002/eji.200535633 (2006). (PMID: 10.1002/eji.20053563316688680)
Miller, A. M. Role of IL-33 in inflammation and disease. J. Inflamm. (London, England) 8, 22–22. https://doi.org/10.1186/1476-9255-8-22 (2011). (PMID: 10.1186/1476-9255-8-22)
Xu, D. et al. IL-33 exacerbates antigen-induced arthritis by activating mast cells. Proc. Natl. Acad. Sci. USA 105, 10913–10918. https://doi.org/10.1073/pnas.0801898105 (2008). (PMID: 10.1073/pnas.080189810518667700)
Liu, X. et al. Crucial role of interleukin-7 in T helper type 17 survival and expansion in autoimmune disease. Nat. Med. 16, 191–197. https://doi.org/10.1038/nm.2077 (2010). (PMID: 10.1038/nm.207720062065)
Churchman, S. M. & Ponchel, F. Interleukin-7 in rheumatoid arthritis. Rheumatology (Oxford) 47, 753–759. https://doi.org/10.1093/rheumatology/ken053 (2008). (PMID: 10.1093/rheumatology/ken053)
Zhu, J., Yamane, H., Cote-Sierra, J., Guo, L. & Paul, W. E. GATA-3 promotes Th2 responses through three different mechanisms: induction of Th2 cytokine production, selective growth of Th2 cells and inhibition of Th1 cell-specific factors. Cell Res. 16, 3–10. https://doi.org/10.1038/sj.cr.7310002 (2006). (PMID: 10.1038/sj.cr.731000216467870)
Guo, L. et al. Innate immunological function of TH2 cells in vivo. Nat. Immunol. 16, 1051–1059. https://doi.org/10.1038/ni.3244 (2015). (PMID: 10.1038/ni.3244263224824575627)
Graversen, J. H. et al. Targeting the hemoglobin scavenger receptor CD163 in macrophages highly increases the anti-inflammatory potency of dexamethasone. Mol. Ther. 20, 1550–1558. https://doi.org/10.1038/mt.2012.103 (2012). (PMID: 10.1038/mt.2012.103226438643412497)
Granfeldt, A. et al. Targeting dexamethasone to macrophages in a porcine endotoxemic model. Crit Care Med. 41, e309-318. https://doi.org/10.1097/CCM.0b013e31828a45ef (2013). (PMID: 10.1097/CCM.0b013e31828a45ef23928834)
Moestrup, S. K. & Moller, H. J. CD163: a regulated hemoglobin scavenger receptor with a role in the anti-inflammatory response. Ann. Med. 36, 347–354 (2004). (PMID: 10.1080/07853890410033171)
Sekiya, T. & Yoshimura, A. In vitro Th differentiation protocol. Methods Mol. Biol. 1344, 183–191. https://doi.org/10.1007/978-1-4939-2966-5_10 (2016). (PMID: 10.1007/978-1-4939-2966-5_1026520124)
Livak, K. J. & Schmittgen, T. D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods (San Diego, Calif.) 25, 402–408. https://doi.org/10.1006/meth.2001.1262 (2001). (PMID: 10.1006/meth.2001.1262)
Italiani, P. & Boraschi, D. From Monocytes to M1/M2 macrophages: phenotypical vs. functional differentiation. Front. Immunol. https://doi.org/10.3389/fimmu.2014.00514 (2014). (PMID: 10.3389/fimmu.2014.00514253686184201108)
Mantovani, A. et al. The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol. 25, 677–686. https://doi.org/10.1016/j.it.2004.09.015 (2004). (PMID: 10.1016/j.it.2004.09.01515530839)
Wang, N., Liang, H. & Zen, K. Molecular mechanisms that influence the macrophage M1–M2 polarization balance. Front. Immunol. https://doi.org/10.3389/fimmu.2014.00614 (2014). (PMID: 10.3389/fimmu.2014.00614255063464246889)
Xuan, W., Qu, Q., Zheng, B., Xiong, S. & Fan, G. H. The chemotaxis of M1 and M2 macrophages is regulated by different chemokines. J. Leukoc. Biol. 97, 61–69. https://doi.org/10.1189/jlb.1A0314-170R (2015). (PMID: 10.1189/jlb.1A0314-170R25359998)
Hirahara, K. & Nakayama, T. CD4+ T-cell subsets in inflammatory diseases: beyond the Th1/Th2 paradigm. Int. Immunol. 28, 163–171. https://doi.org/10.1093/intimm/dxw006 (2016). (PMID: 10.1093/intimm/dxw006268743554889886)
Mauri, C., Feldmann, M. & Williams, R. O. Down-regulation of Th1-mediated pathology in experimental arthritis by stimulation of the Th2 arm of the immune response. Arthritis Rheumatol. 48, 839–845. https://doi.org/10.1002/art.10832 (2003). (PMID: 10.1002/art.10832)
Schulze-Koops, H. & Kalden, J. R. The balance of Th1/Th2 cytokines in rheumatoid arthritis. Best Pract. Res. Clin. Rheumatol. 15, 677–691. https://doi.org/10.1053/berh.2001.0187 (2001). (PMID: 10.1053/berh.2001.018711812015)
Udalova, I. A., Mantovani, A. & Feldmann, M. Macrophage heterogeneity in the context of rheumatoid arthritis. Nat. Rev. Rheumatol. 12, 472–485. https://doi.org/10.1038/nrrheum.2016.91 (2016). (PMID: 10.1038/nrrheum.2016.9127383913)
Substance Nomenclature:: 0 (Antigens, CD)
0 (Antigens, Differentiation, Myelomonocytic)
0 (CD163 antigen)
0 (Collagen Type II)
0 (Cytokines)
0 (Receptors, Cell Surface)
Entry Date(s):: Date Created: 20200726 Date Completed: 20201221 Latest Revision: 20210724
Update Code:: 20240104
PubMed Central ID:: PMC7382459
DOI:: 10.1038/s41598-020-69018-7
PMID:: 32710083
: Czasopismo naukowe

Pełny tekst

The scavenger receptor CD163 is highly expressed in macrophages in sites of chronic inflammation where it has a not yet defined role. Here we have investigated development of collagen-induced arthritis (CIA) and collagen antibody-induced arthritis (CAIA) in CD163-deficient C57BL/6 mice. Compared to wild-type mice, the CIA in CD163-deficient mice had a several-fold higher arthritis score with early onset, prolonged disease and strongly enhanced progression. Further, the serum anti-collagen antibody isotypes as well as the cytokine profiles and T cell markers in the inflamed joints revealed that CD163-deficient mice after 52 days had a predominant Th2 response in opposition to a predominant Th1 response in CD163+/+ mice. Less difference in disease severity between the CD163+/+ and CD163-/- mice was seen in the CAIA model that to a large extent induces arthritis independently of T-cell response and endogenous Th1/Th2 balance. In conclusion, the present set of data points on a novel strong anti-inflammatory role of CD163.

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