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2. Resolving sepsis-induced immunoparalysis via trained immunity by targeting interleukin-4 to myeloid cells

Author

Schrijver, David P., Röring, Rutger J., Deckers, Jeroen, de Dreu, Anne, Toner, Yohana C., Prevot, Geoffrey, Priem, Bram, Munitz, Jazz, Nugraha, Eveline G., van Elsas, Yuri, Azzun, Anthony, Anbergen, Tom, Groh, Laszlo A., Becker, Anouk M. D., Pérez-Medina, Carlos, Oosterwijk, Roderick S., Novakovic, Boris, Moorlag, Simone J. C. F. M., Jansen, Aron, Pickkers, Peter, Kox, Matthijs, Beldman, Thijs J., Kluza, Ewelina, van Leent, Mandy M. T., Teunissen, Abraham J. P., van der Meel, Roy, Fayad, Zahi A., Joosten, Leo A. B., Fisher, Edward A., Merkx, Maarten, Netea, Mihai G., and Mulder, Willem J. M.

Published
2023
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5. Fatty acid desaturation and lipoxygenase pathways support trained immunity

Author

Ferreira, Anaísa V., Alarcon-Barrera, Juan Carlos, Domínguez-Andrés, Jorge, Bulut, Özlem, Kilic, Gizem, Debisarun, Priya A., Röring, Rutger J., Özhan, Hatice N., Terschlüsen, Eva, Ziogas, Athanasios, Kostidis, Sarantos, Mohammed, Yassene, Matzaraki, Vasiliki, Renieris, George, Giamarellos-Bourboulis, Evangelos J., Netea, Mihai G., and Giera, Martin

Published
2023
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6. The impact of BNT162b2 mRNA vaccine on adaptive and innate immune responses

Author

Föhse, Konstantin, Geckin, Büsra, Zoodsma, Martijn, Kilic, Gizem, Liu, Zhaoli, Röring, Rutger J., Overheul, Gijs J., van de Maat, Josephine, Bulut, Ozlem, Hoogerwerf, Jacobien J., ten Oever, Jaap, Simonetti, Elles, Schaal, Heiner, Adams, Ortwin, Müller, Lisa, Ostermann, Philipp Niklas, van de Veerdonk, Frank L., Joosten, Leo A.B., Haagmans, Bart L., van Crevel, Reinout, van Rij, Ronald P., GeurtsvanKessel, Corine, de Jonge, Marien I., Li, Yang, Domínguez-Andrés, Jorge, and Netea, Mihai G.

Published
2023
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9. MMR vaccination induces trained immunity via functional and metabolic reprogramming of γδ T cells

Author

Röring, Rutger J., primary, Debisarun, Priya A., additional, Botey-Bataller, Javier, additional, Suen, Tsz Kin, additional, Bulut, Ozlem, additional, Kilic, Gizem, additional, Koeken, Valerie A.C.M., additional, Sarlea, Andrei, additional, Bahrar, Harsh, additional, Dijkstra, Helga, additional, Lemmers, Heidi, additional, Gössling, Katharina L., additional, Rüchel, Nadine, additional, Ostermann, Philipp N., additional, Müller, Lisa, additional, Schaal, Heiner, additional, Adams, Ortwin, additional, Borkhardt, Arndt, additional, Ariyurek, Yavuz, additional, de Meijer, Emile J., additional, Kloet, Susan L., additional, ten Oever, Jaap, additional, Placek, Katarzyna, additional, Li, Yang, additional, and Netea, Mihai G., additional

Published
2024
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10. Fatty acid desaturation and lipoxygenase pathways support trained immunity

Author

Ferreira, Anaisa V, primary, Alarcon-Barrera, Juan Carlos, additional, Domínguez-Andrés, Jorge, additional, Bulut, Ozlem, additional, Kilic, Gizem, additional, Debisarun, Priya A, additional, Röring, Rutger J, additional, Özhan, Hatice N, additional, Terschlüsen, Eva, additional, Ziogas, Athanasios, additional, Kostidis, Sarantos, additional, Mohammed, Yassene, additional, Matzaraki, Vasiliki, additional, Renieris, George, additional, Giamarellos-Bourboulis, Evangelos J, additional, Netea, Mihai G, additional, and Giera, Martin, additional

Published
2023
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11. Dexamethasone attenuates interferon-related cytokine hyperresponsiveness in COVID-19 patients

Author

Engel, Job J., primary, van der Made, Caspar I., additional, Keur, Nick, additional, Setiabudiawan, Todia, additional, Röring, Rutger J., additional, Damoraki, Georgia, additional, Dijkstra, Helga, additional, Lemmers, Heidi, additional, Ioannou, Sofia, additional, Poulakou, Garyfallia, additional, van der Meer, Jos W. M., additional, Giamarellos-Bourboulis, Evangelos J., additional, Kumar, Vinod, additional, van de Veerdonk, Frank L., additional, Netea, Mihai G., additional, and Ziogas, Athanasios, additional

Published
2023
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12. Resolving sepsis-induced immunoparalysis via trained immunity by targeting interleukin-4 to myeloid cells

Author

Schrijver, David P, Röring, Rutger J, Deckers, Jeroen, de Dreu, Anne, Toner, Yohana C, Prevot, Geoffrey, Priem, Bram, Munitz, Jazz, Nugraha, Eveline G, van Elsas, Yuri, Azzun, Anthony, Anbergen, Tom, Groh, Laszlo A, Becker, Anouk M D, Pérez-Medina, Carlos, Oosterwijk, Roderick S, Novakovic, Boris, Moorlag, Simone J C F M, Jansen, Aron, Pickkers, Peter, Kox, Matthijs, Beldman, Thijs J, Kluza, Ewelina, van Leent, Mandy M T, Teunissen, Abraham J P, van der Meel, Roy, Fayad, Zahi A, Joosten, Leo A B, Fisher, Edward A, Merkx, Maarten, Netea, Mihai G, Mulder, Willem J M, Schrijver, David P, Röring, Rutger J, Deckers, Jeroen, de Dreu, Anne, Toner, Yohana C, Prevot, Geoffrey, Priem, Bram, Munitz, Jazz, Nugraha, Eveline G, van Elsas, Yuri, Azzun, Anthony, Anbergen, Tom, Groh, Laszlo A, Becker, Anouk M D, Pérez-Medina, Carlos, Oosterwijk, Roderick S, Novakovic, Boris, Moorlag, Simone J C F M, Jansen, Aron, Pickkers, Peter, Kox, Matthijs, Beldman, Thijs J, Kluza, Ewelina, van Leent, Mandy M T, Teunissen, Abraham J P, van der Meel, Roy, Fayad, Zahi A, Joosten, Leo A B, Fisher, Edward A, Merkx, Maarten, Netea, Mihai G, and Mulder, Willem J M

Abstract

Immunoparalysis is a compensatory and persistent anti-inflammatory response to trauma, sepsis or another serious insult, which increases the risk of opportunistic infections, morbidity and mortality. Here, we show that in cultured primary human monocytes, interleukin-4 (IL4) inhibits acute inflammation, while simultaneously inducing a long-lasting innate immune memory named trained immunity. To take advantage of this paradoxical IL4 feature in vivo, we developed a fusion protein of apolipoprotein A1 (apoA1) and IL4, which integrates into a lipid nanoparticle. In mice and non-human primates, an intravenously injected apoA1-IL4-embedding nanoparticle targets myeloid-cell-rich haematopoietic organs, in particular, the spleen and bone marrow. We subsequently demonstrate that IL4 nanotherapy resolved immunoparalysis in mice with lipopolysaccharide-induced hyperinflammation, as well as in ex vivo human sepsis models and in experimental endotoxemia. Our findings support the translational development of nanoparticle formulations of apoA1-IL4 for the treatment of patients with sepsis at risk of immunoparalysis-induced complications.

Published
2023

13. MMR vaccination induces a trained immunity program characterized by functional and metabolic reprogramming of γδ T cells

Author

Röring, Rutger J., primary, Debisarun, Priya A., additional, Botey-Bataller, Javier, additional, Suen, Tsz Kin, additional, Bulut, Özlem, additional, Kilic, Gizem, additional, Koeken, Valerie A. C. M., additional, Sarlea, Andrei, additional, Bahrar, Harsh, additional, Dijkstra, Helga, additional, Lemmers, Heidi, additional, Gössling, Katharina L., additional, Rüchel, Nadine, additional, Ostermann, Philipp N., additional, Müller, Lisa, additional, Schaal, Heiner, additional, Adams, Ortwin, additional, Borkhardt, Arndt, additional, Ariyurek, Yavuz, additional, de Meijer, Emile J., additional, Kloet, Susan, additional, ten Oever, Jaap, additional, Placek, Katarzyna, additional, Li, Yang, additional, and Netea, Mihai G., additional

Published
2022
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14. Colony-Stimulating Factor-1 Receptor and Interleukin-6 Receptor Inhibition Prevents Conversion of cDC2s Into Tumor-Induced DC3s

Author

Becker, Anouk M.D., primary, Flórez-Grau, Georgina, additional, Bakdash, Ghaith, additional, Röring, Rutger J., additional, Stelloo, Suzan, additional, Vermeulen, Michiel, additional, Piet, Berber, additional, Aarntzen, Erik H. J. G., additional, Verdoes, Martijn, additional, and de Vries, I. Jolanda M., additional

Published
2022
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15. induction of trained immunity in adherent human monocytes

Author

Domínguez-Andrés, Jorge, Arts, Rob J W, Bekkering, Siroon, Bahrar, Harsh, Blok, Bastiaan A, de Bree, L Charlotte J, Bruno, Mariolina, Bulut, Özlem, Debisarun, Priya A, Dijkstra, Helga, Cristina Dos Santos, Jéssica, Ferreira, Anaísa V, Flores-Gomez, Daniela, Groh, Laszlo A, Grondman, Inge, Helder, Leonie, Jacobs, Cor, Jacobs, Liesbeth, Jansen, Trees, Kilic, Gizem, Klück, Viola, Koeken, Valerie A C M, Lemmers, Heidi, Moorlag, Simone J C F M, Mourits, Vera P, van Puffelen, Jelmer H, Rabold, Katrin, Röring, Rutger J, Rosati, Diletta, Tercan, Helin, van Tuijl, Julia, Quintin, Jessica, van Crevel, Reinout, Riksen, Niels P, Joosten, Leo A B, Netea, Mihai G, and CiiM, Zentrum für individualisierte Infektionsmedizin, Feodor-Lynen-Str.7, 30625 Hannover.

Subjects
Cell biology, Cell isolation, Immunology, Cell-based assays
Abstract

A growing number of studies show that innate immune cells can undergo functional reprogramming, facilitating a faster and enhanced response to heterologous secondary stimuli. This concept has been termed "trained immunity." We outline here a protocol to recapitulate this in vitro using adherent monocytes from consecutive isolation of peripheral blood mononuclear cells. The induction of trained immunity and the associated functional reprogramming of monocytes is described in detail using β-glucan (from Candida albicans) and Bacillus Calmette-Guérin as examples. For complete details on the use and execution of this protocol, please refer to Repnik et al. (2003) and Bekkering et al. (2016).

Published
2021

16. Nanoengineering Apolipoprotein A1-Based Immunotherapeutics

Author

Schrijver, David P., de Dreu, Anne, Hofstraat, Stijn R. J., Kluza, Ewelina, Zwolsman, Robby, Deckers, Jeroen, Anbergen, Tom, de Bruin, Koen, Trines, Mirre M., Nugraha, Eveline G., Ummels, Floor, Röring, Rutger J., Beldman, Thijs J., Teunissen, Abraham J. P., Fayad, Zahi A., van der Meel, Roy, Mulder, Willem J.M., Schrijver, David P., de Dreu, Anne, Hofstraat, Stijn R. J., Kluza, Ewelina, Zwolsman, Robby, Deckers, Jeroen, Anbergen, Tom, de Bruin, Koen, Trines, Mirre M., Nugraha, Eveline G., Ummels, Floor, Röring, Rutger J., Beldman, Thijs J., Teunissen, Abraham J. P., Fayad, Zahi A., van der Meel, Roy, and Mulder, Willem J.M.

Abstract

In the slipstream of targeting the adaptive immune system, innate immunotherapy strategies are being developed. In this context, technologies based on natural carrier vehicles that inherently interact with the innate immune system, are increasingly being considered. Immunoregulatory nanotherapeutics based on natural apolipoprotein A1 (apoA1) are discussed here. This protein is a helical, amphipathic macromolecule and the main constituent of high-density lipoprotein. In that capacity, apoA1 interacts specifically with innate immune cells, such as monocytes and macrophages, to collect and transport lipophilicmolecules throughout the body. Exactly these unique features make apoA1 a compelling elementary constituent of biocompatible self-assembled nanotherapeutics. Such apoA1-based nanotherapeutics (A1-nanotherapeutics) can be engineered and functionalized to induce or mitigate an innate immune response or to orchestrate an adaptive immune response through antigen delivery to dendritic cells. The authors first discuss apoA1's properties and how these can be exploited to generate libraries of A1-nanotherapeutics using advanced manufacturing approaches such as microfluidics or continuous flow methods. Using high-throughput in vitro screening methods and in vivo imagingto identify promising formulations are then recommend. Finally, Three distinct immunotherapy strategies are proposed to effectively treat a variety of diseases—including cancer, infection, and cardiovascular disease—and promote allograft survival in transplantation.

Published
2021

17. Nanoengineering Apolipoprotein A1‐Based Immunotherapeutics

Author

Schrijver, David P., primary, Dreu, Anne, additional, Hofstraat, Stijn R. J., additional, Kluza, Ewelina, additional, Zwolsman, Robby, additional, Deckers, Jeroen, additional, Anbergen, Tom, additional, Bruin, Koen, additional, Trines, Mirre M., additional, Nugraha, Eveline G., additional, Ummels, Floor, additional, Röring, Rutger J., additional, Beldman, Thijs J., additional, Teunissen, Abraham J. P., additional, Fayad, Zahi A., additional, Meel, Roy, additional, and Mulder, Willem J. M., additional

Published
2021
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18. The impact of BNT162b2 mRNA vaccine on adaptive and innate immune responses

Author

Föhse, Konstantin, primary, Geckin, Büsra, additional, Zoodsma, Martijn, additional, Kilic, Gizem, additional, Liu, Zhaoli, additional, Röring, Rutger J., additional, Overheul, Gijs J., additional, van de Maat, Josephine S., additional, Bulut, Ozlem, additional, Hoogerwerf, Jacobien J., additional, Oever, Jaap ten, additional, Simonetti, Elles, additional, Schaal, Heiner, additional, Adams, Ortwin, additional, Müller, Lisa, additional, Ostermann, Philipp Niklas, additional, van de Veerdonk, Frank L., additional, Joosten, Leo A.B., additional, Haagmans, Bart L., additional, van Crevel, Reinout, additional, van Rij, Ronald P., additional, GeurtsvanKessel, Corine, additional, de Jonge, Marien I., additional, Li, Yang, additional, Domínguez-Andrés, Jorge, additional, and Netea, Mihai G., additional

Published
2021
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19. In vitro induction of trained immunity in adherent human monocytes

Author

Domínguez-Andrés, Jorge, primary, Arts, Rob J.W., additional, Bekkering, Siroon, additional, Bahrar, Harsh, additional, Blok, Bastiaan A., additional, de Bree, L. Charlotte J., additional, Bruno, Mariolina, additional, Bulut, Özlem, additional, Debisarun, Priya A., additional, Dijkstra, Helga, additional, Cristina dos Santos, Jéssica, additional, Ferreira, Anaísa V., additional, Flores-Gomez, Daniela, additional, Groh, Laszlo A., additional, Grondman, Inge, additional, Helder, Leonie, additional, Jacobs, Cor, additional, Jacobs, Liesbeth, additional, Jansen, Trees, additional, Kilic, Gizem, additional, Klück, Viola, additional, Koeken, Valerie A.C.M., additional, Lemmers, Heidi, additional, Moorlag, Simone J.C.F.M., additional, Mourits, Vera P., additional, van Puffelen, Jelmer H., additional, Rabold, Katrin, additional, Röring, Rutger J., additional, Rosati, Diletta, additional, Tercan, Helin, additional, van Tuijl, Julia, additional, Quintin, Jessica, additional, van Crevel, Reinout, additional, Riksen, Niels P., additional, Joosten, Leo A.B., additional, and Netea, Mihai G., additional

Published
2021
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20. A single-cell view on host immune transcriptional response to in vivoBCG-induced trained immunity

Author

Li, Wenchao, Moorlag, Simone J.C.F.M., Koeken, Valerie A.C.M., Röring, Rutger J., de Bree, L. Charlotte J., Mourits, Vera P., Gupta, Manoj K., Zhang, Bowen, Fu, Jianbo, Zhang, Zhenhua, Grondman, Inge, van Meijgaarden, Krista E., Zhou, Liang, Alaswad, Ahmed, Joosten, Leo A.B., van Crevel, Reinout, Xu, Cheng-Jian, Netea, Mihai G., and Li, Yang

Abstract

Bacillus Calmette-Guérin (BCG) vaccination is a prototype model for the study of trained immunity (TI) in humans, and results in a more effective response of innate immune cells upon stimulation with heterologous stimuli. Here, we investigate the heterogeneity of TI induction by single-cell RNA sequencing of immune cells collected from 156 samples. We observe that both monocytes and CD8+T cells show heterologous transcriptional responses to lipopolysaccharide, with an active crosstalk between these two cell types. Furthermore, the interferon-γ pathway is crucial in BCG-induced TI, and it is upregulated in functional high responders. Data-driven analyses and functional experiments reveal STAT1to be one of the important transcription factors for TI shared in all identified monocyte subpopulations. Finally, we report the role of type I interferon-related and neutrophil-related TI transcriptional programs in patients with sepsis. These findings provide comprehensive insights into the importance of monocyte heterogeneity during TI in humans.

Published
2023
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21. In vitroinduction of trained immunity in adherent human monocytes

Author

Domínguez-Andrés, Jorge, Arts, Rob J.W., Bekkering, Siroon, Bahrar, Harsh, Blok, Bastiaan A., de Bree, L. Charlotte J., Bruno, Mariolina, Bulut, Özlem, Debisarun, Priya A., Dijkstra, Helga, Cristina dos Santos, Jéssica, Ferreira, Anaísa V., Flores-Gomez, Daniela, Groh, Laszlo A., Grondman, Inge, Helder, Leonie, Jacobs, Cor, Jacobs, Liesbeth, Jansen, Trees, Kilic, Gizem, Klück, Viola, Koeken, Valerie A.C.M., Lemmers, Heidi, Moorlag, Simone J.C.F.M., Mourits, Vera P., van Puffelen, Jelmer H., Rabold, Katrin, Röring, Rutger J., Rosati, Diletta, Tercan, Helin, van Tuijl, Julia, Quintin, Jessica, van Crevel, Reinout, Riksen, Niels P., Joosten, Leo A.B., and Netea, Mihai G.

Abstract

A growing number of studies show that innate immune cells can undergo functional reprogramming, facilitating a faster and enhanced response to heterologous secondary stimuli. This concept has been termed “trained immunity.” We outline here a protocol to recapitulate this in vitrousing adherent monocytes from consecutive isolation of peripheral blood mononuclear cells. The induction of trained immunity and the associated functional reprogramming of monocytes is described in detail using β-glucan (from Candida albicans) and Bacillus Calmette-Guérin as examples.

Published
2021
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22. Interleukin-10 inhibits important components of trained immunity in human monocytes.

Author

Röring RJ, Scognamiglio F, de Jong LC, Groh LA, Matzaraki V, Koeken VACM, Joosten LAB, Ziogas A, and Netea MG

Abstract

Trained immunity induces antigen-agnostic enhancement of host defense and protection against secondary infections, but inappropriate activation can contribute to the pathophysiology of inflammatory diseases. Tight regulation of trained immunity is therefore needed to avoid pathology, but little is known about the endogenous processes that modulate it. Here, we investigated the potential of IL-10, a prototypical anti-inflammatory cytokine, to inhibit trained immunity. IL-10 induced tolerance and inhibited trained immunity in primary human monocytes at both functional and transcriptional levels. Inhibition of STAT3, a signaling route that mediates IL-10 signals, induced trained immunity. IL-10 downregulated glycolytic and oxidative metabolism in monocytes, but did not impact the metabolic effects of β-glucan-induced trained immunity. Furthermore, IL-10 prevented increased ROS production in BCG-induced training, but did not influence phagocytosis upregulation. In a cohort study of healthy volunteers vaccinated with BCG, genetic variants that influenced IL-10 or its receptor modulated BCG-induced trained immunity. Furthermore, circulating IL-10 concentrations were negatively correlated with induction of trained immunity after BCG vaccination in a sex-specific manner. In conclusion, IL-10 inhibited several, albeit not all, immunological functions amplified after induction of trained immunity. Follow-up studies should explore the precise molecular mechanism that mediate the effects of IL-10 on trained immunity. Addressing these knowledge gaps is an important step towards optimizing IL-10's potential as a therapeutic target in diseases characterized by inappropriate induction of trained immunity., (© The Author(s) 2024. Published by Oxford University Press on behalf of Society for Leukocyte Biology.)

Published
2024
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23. Comparative host transcriptome in response to pathogenic fungi identifies common and species-specific transcriptional antifungal host response pathways.

Author

Bruno M, Dewi IMW, Matzaraki V, Ter Horst R, Pekmezovic M, Rösler B, Groh L, Röring RJ, Kumar V, Li Y, Carvalho A, Netea MG, Latgé JP, Gresnigt MS, and van de Veerdonk FL

Abstract

Candidiasis, aspergillosis, and mucormycosis cause the majority of nosocomial fungal infections in immunocompromised patients. Using an unbiased transcriptional profiling in PBMCs exposed to the fungal species causing these infections, we found a core host response in healthy individuals that may govern effective fungal clearance: it consists of 156 transcripts, involving canonical and non-canonical immune pathways. Systematic investigation of key steps in antifungal host defense revealed fungal-specific signatures. As previously demonstrated, Candida albicans induced type I and Type II interferon-related pathways. In contrast, central pattern recognition receptor, reactive oxygen species production, and host glycolytic pathways were down-regulated in response to Rhizopus oryzae , which was associated with an ER-stress response. TLR5 was identified to be uniquely regulated by Aspergillus fumigatus and to control cytokine release in response to this fungus. In conclusion, our data reveals the transcriptional profiles induced by C. albicans, A. fumigatus, and R. oryzae , and describes both the common and specific antifungal host responses that could be exploited for novel therapeutic strategies., Competing Interests: The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper., (© 2021 The Authors.)

Published
2020
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