Stunning of neutrophils accounts for the anti-inflammatory effects of clodronate liposomes

Stephan Culemann; Katharina Knab; Maximilien Euler; Anja Wegner; Hilal Garibagaoglu; Jochen Ackermann; Kim Fischer; Deborah Kienhöfer; Georgiana Crainiciuc; Jonas Hahn; Anika Grüneboom; Falk Nimmerjahn; Stefan Uderhardt; Andrés Hidalgo; Georg Schett; Markus H. Hoffmann; Gerhard Krönke

doi:10.1084/jem.20220525

Stunning of neutrophils accounts for the anti-inflammatory effects of clodronate liposomes

Stephan Culemann, Katharina Knab, Maximilien Euler, Anja Wegner, Hilal Garibagaoglu, Jochen Ackermann, Kim Fischer, Deborah Kienhöfer, Georgiana Crainiciuc, Jonas Hahn, Anika Grüneboom, Falk Nimmerjahn, Stefan Uderhardt, Andrés Hidalgo, Georg Schett, Markus H. Hoffmann, Gerhard Krönke^*

^*Korrespondierende/r Autor/-in für diese Arbeit

Klinik für Dermatologie, Allergologie und Venerologie

61 Zitate (Scopus)

Abstract

Clodronate liposomes (Clo-Lip) have been widely used to deplete mononuclear phagocytes (MoPh) to study the function of these cells in vivo. Here, we revisited the effects of Clo-Lip together with genetic models of MoPh deficiency, revealing that Clo-Lip exert their anti-inflammatory effects independent of MoPh. Notably, not only MoPh but also polymorphonuclear neutrophils (PMN) ingested Clo-Lip in vivo, which resulted in their functional arrest. Adoptive transfer of PMN, but not of MoPh, reversed the anti-inflammatory effects of Clo-Lip treatment, indicating that stunning of PMN rather than depletion of MoPh accounts for the anti-inflammatory effects of Clo-Lip in vivo. Our data highlight the need for a critical revision of the current literature on the role of MoPh in inflammation.

Originalsprache	Englisch
Aufsatznummer	e20220525
Zeitschrift	Journal of Experimental Medicine
Jahrgang	220
Ausgabenummer	6
ISSN	0022-1007
DOIs	https://doi.org/10.1084/jem.20220525
Publikationsstatus	Veröffentlicht - 05.06.2023

Fördermittel

This work was supported by the Deutsche For-schungsgemeinschaft (FG 2886 “PANDORA” – B01/B02/A03/ B04 to G. Krönke, F. Nimmerjahn, G. Schett, and M.H. Hoffmann, respectively, and the CRC1181-A03/A01/A02/A07/C03 Z2 to G. Krönke, G. Schett, F. Nimmerjahn, and M.H. Hoffmann), the Emerging Field Initiative of the Friedrich-Alexander University Erlangen-Nürnberg (EFI_Verbund_Med_05_MIRACLE to G. Krönke), the Bundesministerium für Bildung und For-schung (MASCARA to G. Krönke and G. Schett; MelAutim to G. Krönke), and the European Union (Horizon 2020 ERC-2014-StG 640087 – SOS and ERC-2020-CoG 101001866 – INSPIRE to G. Krönke; and ERC-2018-SyG nanoSCOPE and RTCure to G. Schett). This work was supported by grants R01AI165661 from the National Institutes of Health/National Institute of Allergy and Infectious Diseases, H2020-FET-OPEN-2018-2020 (no. 861878) from the European Commission to A. Hidalgo and M.H. Hoffmann, and HR17_00527 from Fundacion La Caixa to A. Hidalgo. The CNIC is supported by the Min-isterio de Ciencia e Innovacion and the Pro-CNIC Foundation and is a Severo Ochoa Center of Excellence (MICINN award CEX2020-001041-S).

UN SDGs

Dieser Output leistet einen Beitrag zu folgendem(n) Ziel(en) für nachhaltige Entwicklung

SDG 3 – Gesundheit und Wohlergehen

Strategische Forschungsbereiche und Zentren

Forschungsschwerpunkt: Infektion und Entzündung - Zentrum für Infektions- und Entzündungsforschung Lübeck (ZIEL)
Zentren: Center for Research on Inflammation of the Skin (CRIS)

DFG-Fachsystematik

2.21-05 Immunologie

Dokumente

10.1084/jem.20220525

Weitere Links

SFB 1526, PANTAU: Pathomechanismen Antikörpervermittelter Autoimmunerkrankungen
Sadik, C. (Sprecher*in), Zillikens, D. (Sprecher*in), Scheffold, A. (Projektleiter*in (PI)), Schmidt, E. (Projektleiter*in (PI)), Heine, G. (Projektleiter*in (PI)), Manz, R. (Projektleiter*in (PI)), Köhl, J. (Projektleiter*in (PI)), Ludwig, R. (Projektleiter*in (PI)), Peipp, M. (Projektleiter*in (PI)), Hammers, M. C. (Projektleiter*in (PI)), Verschoor, A. (Projektleiter*in (PI)), Karsten, C. (Projektleiter*in (PI)), Nimmerjahn, F. (Projektleiter*in (PI)), Hutloff, A. (Projektleiter*in (PI)), Ibrahim, S. (Projektleiter*in (PI)), Wettschureck, N. (Projektleiter*in (PI)), Bieber, K. (Projektleiter*in (PI)), Schilf, P. (Projektleiter*in (PI)), Vaeth, M. (Projektleiter*in (PI)), Hirose, M. (Projektleiter*in (PI)), Vaeth, M. (Projektleiter*in (PI)), Baines, J. F. (Projektleiter*in (PI)), Bacher, P. (Projektleiter*in (PI)), Hoffmann, M. (Projektleiter*in (PI)), Busch, H. S. (Projektleiter*in (PI)), Höppner, M. (Projektleiter*in (PI)), Becker, M. (Projektleiter*in (PI)), Holtsche, M. M. (Projektleiter*in (PI)), Fähnrich, A. (Projektleiter*in (PI)), Szymczak, S. (Projektleiter*in (PI)), Murthy, S. (Projektleiter*in (PI)) & Lux, A. (Projektleiter*in (PI))
01.01.22 → …
Projekt: DFG Verbundprojekte › DFG Sonderforschungsbereiche / Transregios (SFB/TR)

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Culemann, S., Knab, K., Euler, M., Wegner, A., Garibagaoglu, H., Ackermann, J., Fischer, K., Kienhöfer, D., Crainiciuc, G., Hahn, J., Grüneboom, A., Nimmerjahn, F., Uderhardt, S., Hidalgo, A., Schett, G., Hoffmann, M. H., & Krönke, G. (2023). Stunning of neutrophils accounts for the anti-inflammatory effects of clodronate liposomes. Journal of Experimental Medicine, 220(6), Artikel e20220525. https://doi.org/10.1084/jem.20220525

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title = "Stunning of neutrophils accounts for the anti-inflammatory effects of clodronate liposomes",

abstract = "Clodronate liposomes (Clo-Lip) have been widely used to deplete mononuclear phagocytes (MoPh) to study the function of these cells in vivo. Here, we revisited the effects of Clo-Lip together with genetic models of MoPh deficiency, revealing that Clo-Lip exert their anti-inflammatory effects independent of MoPh. Notably, not only MoPh but also polymorphonuclear neutrophils (PMN) ingested Clo-Lip in vivo, which resulted in their functional arrest. Adoptive transfer of PMN, but not of MoPh, reversed the anti-inflammatory effects of Clo-Lip treatment, indicating that stunning of PMN rather than depletion of MoPh accounts for the anti-inflammatory effects of Clo-Lip in vivo. Our data highlight the need for a critical revision of the current literature on the role of MoPh in inflammation.",

author = "Stephan Culemann and Katharina Knab and Maximilien Euler and Anja Wegner and Hilal Garibagaoglu and Jochen Ackermann and Kim Fischer and Deborah Kienh{\"o}fer and Georgiana Crainiciuc and Jonas Hahn and Anika Gr{\"u}neboom and Falk Nimmerjahn and Stefan Uderhardt and Andr{\'e}s Hidalgo and Georg Schett and Hoffmann, \{Markus H.\} and Gerhard Kr{\"o}nke",

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doi = "10.1084/jem.20220525",

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Culemann, S, Knab, K, Euler, M, Wegner, A, Garibagaoglu, H, Ackermann, J, Fischer, K, Kienhöfer, D, Crainiciuc, G, Hahn, J, Grüneboom, A, Nimmerjahn, F, Uderhardt, S, Hidalgo, A, Schett, G, Hoffmann, MH & Krönke, G 2023, 'Stunning of neutrophils accounts for the anti-inflammatory effects of clodronate liposomes', Journal of Experimental Medicine, Jg. 220, Nr. 6, e20220525. https://doi.org/10.1084/jem.20220525

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T1 - Stunning of neutrophils accounts for the anti-inflammatory effects of clodronate liposomes

AU - Culemann, Stephan

AU - Knab, Katharina

AU - Euler, Maximilien

AU - Wegner, Anja

AU - Garibagaoglu, Hilal

AU - Ackermann, Jochen

AU - Fischer, Kim

AU - Kienhöfer, Deborah

AU - Crainiciuc, Georgiana

AU - Hahn, Jonas

AU - Grüneboom, Anika

AU - Nimmerjahn, Falk

AU - Uderhardt, Stefan

AU - Hidalgo, Andrés

AU - Schett, Georg

AU - Hoffmann, Markus H.

AU - Krönke, Gerhard

PY - 2023/6/5

Y1 - 2023/6/5

N2 - Clodronate liposomes (Clo-Lip) have been widely used to deplete mononuclear phagocytes (MoPh) to study the function of these cells in vivo. Here, we revisited the effects of Clo-Lip together with genetic models of MoPh deficiency, revealing that Clo-Lip exert their anti-inflammatory effects independent of MoPh. Notably, not only MoPh but also polymorphonuclear neutrophils (PMN) ingested Clo-Lip in vivo, which resulted in their functional arrest. Adoptive transfer of PMN, but not of MoPh, reversed the anti-inflammatory effects of Clo-Lip treatment, indicating that stunning of PMN rather than depletion of MoPh accounts for the anti-inflammatory effects of Clo-Lip in vivo. Our data highlight the need for a critical revision of the current literature on the role of MoPh in inflammation.

AB - Clodronate liposomes (Clo-Lip) have been widely used to deplete mononuclear phagocytes (MoPh) to study the function of these cells in vivo. Here, we revisited the effects of Clo-Lip together with genetic models of MoPh deficiency, revealing that Clo-Lip exert their anti-inflammatory effects independent of MoPh. Notably, not only MoPh but also polymorphonuclear neutrophils (PMN) ingested Clo-Lip in vivo, which resulted in their functional arrest. Adoptive transfer of PMN, but not of MoPh, reversed the anti-inflammatory effects of Clo-Lip treatment, indicating that stunning of PMN rather than depletion of MoPh accounts for the anti-inflammatory effects of Clo-Lip in vivo. Our data highlight the need for a critical revision of the current literature on the role of MoPh in inflammation.

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JO - Journal of Experimental Medicine

JF - Journal of Experimental Medicine

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Stunning of neutrophils accounts for the anti-inflammatory effects of clodronate liposomes

Abstract

Fördermittel

UN SDGs

Strategische Forschungsbereiche und Zentren

DFG-Fachsystematik

Dokumente

Weitere Links

Fingerprint

Projekte

SFB 1526, PANTAU: Pathomechanismen Antikörpervermittelter Autoimmunerkrankungen

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