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2. Soluble mannose receptor induces proinflammatory macrophage activation and metaflammation

Author

Embgenbroich, Maria, van der Zande, Hendrik J. P., Hussaarts, Leonie, Schulte-Schrepping, Jonas, Pelgrom, Leonard R., García-Tardón, Noemí, Schlautmann, Laura, Stoetzel, Isabel, Händler, Kristian, Lambooij, Joost M., Zawistowska-Deniziak, Anna, Hoving, Lisa, de Ruiter, Karin, Wijngaarden, Marjolein A., Pijl, Hanno, van Dijk, Ko Willems, Everts, Bart, van Harmelen, Vanessa, Yazdanbakhsh, Maria, Schultze, Joachim L., Guigas, Bruno, and Burgdorf, Sven

Published
2021

4. Dendritic cell–intrinsic LKB1-AMPK/SIK signaling controls metabolic homeostasis by limiting the hepatic Th17 response during obesity

Author

van der Zande, Hendrik J.P., primary, Brombacher, Eline C., additional, Lambooij, Joost M., additional, Pelgrom, Leonard R., additional, Zawistowska-Deniziak, Anna, additional, Patente, Thiago A., additional, Heieis, Graham A., additional, Otto, Frank, additional, Ozir-Fazalalikhan, Arifa, additional, Yazdanbakhsh, Maria, additional, Everts, Bart, additional, and Guigas, Bruno, additional

Published
2023
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5. Metabolic sensor AMPK licenses CD103+dendritic cells to induce Treg responses

Author

Patente, Thiago A, primary, Brombacher, Eline C, additional, Heieis, Graham A, additional, Pelgrom, Leonard R, additional, Zawistowska-Deniziak, Anna, additional, Otto, Frank, additional, Ozir-Fazalalikhan, Arifa, additional, van der Ham, Alwin J, additional, Guigas, Bruno A, additional, Barbuto, José AM, additional, and Everts, Bart, additional

Published
2023
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9. LKB1 signalling in dendritic cells controls whole-body metabolic homeostasis by limiting T helper 17 priming

Author

van der Zande, Hendrik J.P., primary, Brombacher, Eline C., additional, Lambooij, Joost M., additional, Pelgrom, Leonard R., additional, Zawistowska-Deniziak, Anna, additional, Patente, Thiago A., additional, Heieis, Graham A., additional, Otto, Frank, additional, Ozir-Fazalalikhan, Arifa, additional, Yazdanbakhsh, Maria, additional, Everts, Bart, additional, and Guigas, Bruno, additional

Published
2021
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10. The helminth glycoprotein omega‐1 improves metabolic homeostasis in obese mice through type 2 immunity‐independent inhibition of food intake

Author

Zande, Hendrik J.P., van der, Gonzalez, Michael A., Ruiter, Karin, Wilbers, Ruud H.P., García‐Tardón, Noemí, Huizen, Mariska, van, Noort, Kim, van, Pelgrom, Leonard R., Lambooij, Joost M., Zawistowska‐Deniziak, Anna, Otto, Frank, Ozir‐Fazalalikhan, Arifa, Willigen, Danny, van, Welling, Mick, Poles, Jordan, Leeuwen, Fijs, Hokke, Cornelis H., Schots, Arjen, Yazdanbakhsh, Maria, Loke, P., Guigas, Bruno, Zande, Hendrik J.P., van der, Gonzalez, Michael A., Ruiter, Karin, Wilbers, Ruud H.P., García‐Tardón, Noemí, Huizen, Mariska, van, Noort, Kim, van, Pelgrom, Leonard R., Lambooij, Joost M., Zawistowska‐Deniziak, Anna, Otto, Frank, Ozir‐Fazalalikhan, Arifa, Willigen, Danny, van, Welling, Mick, Poles, Jordan, Leeuwen, Fijs, Hokke, Cornelis H., Schots, Arjen, Yazdanbakhsh, Maria, Loke, P., and Guigas, Bruno

Abstract

Type 2 immunity plays an essential role in the maintenance of metabolic homeostasis and its disruption during obesity promotes meta‐inflammation and insulin resistance. Infection with the helminth parasite Schistosoma mansoni and treatment with its soluble egg antigens (SEA) induce a type 2 immune response in metabolic organs and improve insulin sensitivity and glucose tolerance in obese mice, yet, a causal relationship remains unproven. Here, we investigated the effects and underlying mechanisms of the T2 ribonuclease omega‐1 (ω1), one of the major S mansoni immunomodulatory glycoproteins, on metabolic homeostasis. We show that treatment of obese mice with plant‐produced recombinant ω1, harboring similar glycan motifs as present on the native molecule, decreased body fat mass, and improved systemic insulin sensitivity and glucose tolerance in a time‐ and dose‐dependent manner. This effect was associated with an increase in white adipose tissue (WAT) type 2 T helper cells, eosinophils, and alternatively activated macrophages, without affecting type 2 innate lymphoid cells. In contrast to SEA, the metabolic effects of ω1 were still observed in obese STAT6‐deficient mice with impaired type 2 immunity, indicating that its metabolic effects are independent of the type 2 immune response. Instead, we found that ω1 inhibited food intake, without affecting locomotor activity, WAT thermogenic capacity or whole‐body energy expenditure, an effect also occurring in leptin receptor‐deficient obese and hyperphagic db/db mice. Altogether, we demonstrate that while the helminth glycoprotein ω1 can induce type 2 immunity, it improves whole‐body metabolic homeostasis in obese mice by inhibiting food intake via a STAT6‐independent mechanism.

Published
2021

11. The helminth glycoprotein omega‐1 improves metabolic homeostasis in obese mice through type 2 immunity‐independent inhibition of food intake

Author

Zande, Hendrik J.P., primary, Gonzalez, Michael A., additional, Ruiter, Karin, additional, Wilbers, Ruud H.P., additional, García‐Tardón, Noemí, additional, Huizen, Mariska, additional, Noort, Kim, additional, Pelgrom, Leonard R., additional, Lambooij, Joost M., additional, Zawistowska‐Deniziak, Anna, additional, Otto, Frank, additional, Ozir‐Fazalalikhan, Arifa, additional, Willigen, Danny, additional, Welling, Mick, additional, Poles, Jordan, additional, Leeuwen, Fijs, additional, Hokke, Cornelis H., additional, Schots, Arjen, additional, Yazdanbakhsh, Maria, additional, Loke, P'ng, additional, and Guigas, Bruno, additional

Published
2021
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13. Soluble mannose receptor induces pro-inflammatory macrophage activation and metaflammation

Author

Embgenbroich, Maria, primary, van der Zande, Hendrik J.P., additional, Hussaarts, Leonie, additional, Schulte-Schrepping, Jonas, additional, Pelgrom, Leonard R., additional, García-Tardón, Noemí, additional, Schlautmann, Laura, additional, Stoetzel, Isabel, additional, Händler, Kristian, additional, Lambooij, Joost M., additional, Zawistowska-Deniziak, Anna, additional, Hoving, Lisa, additional, de Ruiter, Karin, additional, Wijngaarden, Marjolein, additional, Pijl, Hanno, additional, van Dijk, Ko Willems, additional, Everts, Bart, additional, van Harmelen, Vanessa, additional, Yazdanbakhsh, Maria, additional, Schultze, Joachim L., additional, Guigas, Bruno, additional, and Burgdorf, Sven, additional

Published
2020
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14. Plasmodium sporozoites induce regulatory macrophages

Author

Winkel, Béatrice M. F., primary, Pelgrom, Leonard R., additional, van Schuijlenburg, Roos, additional, Baalbergen, Els, additional, Ganesh, Munisha S., additional, Gerritsma, Heleen, additional, de Korne, Clarize M., additional, Duszenko, Nikolas, additional, Langenberg, Marijke C. C., additional, Chevalley-Maurel, Séverine C., additional, Smits, Hermelijn H., additional, de Jong, Esther C., additional, Everts, Bart, additional, Franke-Fayard, Blandine, additional, and Roestenberg, Meta, additional

Published
2020
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15. The helminth glycoprotein omega-1 improves metabolic homeostasis in obese mice through type-2 immunity-independent inhibition of food intake

Author

van der Zande, Hendrik J.P., primary, Gonzalez, Michael A., additional, de Ruiter, Karin, additional, Wilbers, Ruud, additional, Garcia-Tardón, Noemi, additional, van Huizen, Mariska, additional, van Noort, Kim, additional, Pelgrom, Leonard R., additional, Lambooij, Joost M., additional, Zawistowska-Deniziak, Anna, additional, Otto, Frank, additional, Ozir-Fazalalikhan, Arifa, additional, van Willigen, Danny, additional, Welling, Mick, additional, Poles, Jordan, additional, van Leeuwen, Fijs, additional, Hokke, Cornelis H., additional, Schots, Arjen, additional, Yazdanbakhsh, Maria, additional, Loke, P’ng, additional, and Guigas, Bruno, additional

Published
2020
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19. The helminth glycoprotein omega‐1 improves metabolic homeostasis in obese mice through type 2 immunity‐independent inhibition of food intake.

Author

van der Zande, Hendrik J.P., Gonzalez, Michael A., de Ruiter, Karin, Wilbers, Ruud H.P., García‐Tardón, Noemí, van Huizen, Mariska, van Noort, Kim, Pelgrom, Leonard R., Lambooij, Joost M., Zawistowska‐Deniziak, Anna, Otto, Frank, Ozir‐Fazalalikhan, Arifa, van Willigen, Danny, Welling, Mick, Poles, Jordan, van Leeuwen, Fijs, Hokke, Cornelis H., Schots, Arjen, Yazdanbakhsh, Maria, and Loke, P'ng

Published
2021
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20. Early Induction of Human Regulatory Dermal Antigen Presenting Cells by Skin-Penetrating Schistosoma Mansoni Cercariae

Author

Winkel, Béatrice M. F., primary, Dalenberg, Mirjam R., additional, de Korne, Clarize M., additional, Feijt, Carola, additional, Langenberg, Marijke C. C., additional, Pelgrom, Leonard, additional, Ganesh, Munisha S., additional, Yazdanbakhsh, Maria, additional, Smits, Hermelijn Helene, additional, de Jong, Esther C., additional, Everts, Bart, additional, van Leeuwen, Fijs W. B., additional, Hokke, Cornelis H., additional, and Roestenberg, Meta, additional

Published
2018
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22. Dectin-1/2–induced autocrine PGE2 signaling licenses dendritic cells to prime Th2 responses

Author

Kaisar, Maria M. M., primary, Ritter, Manuel, additional, del Fresno, Carlos, additional, Jónasdóttir, Hulda S., additional, van der Ham, Alwin J., additional, Pelgrom, Leonard R., additional, Schramm, Gabriele, additional, Layland, Laura E., additional, Sancho, David, additional, Prazeres da Costa, Clarissa, additional, Giera, Martin, additional, Yazdanbakhsh, Maria, additional, and Everts, Bart, additional

Published
2018
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25. Dectin-1/2–induced autocrine PGE2 signaling licenses dendritic cells to prime Th2 responses.

Author

Kaisar, Maria M. M., Ritter, Manuel, del Fresno, Carlos, Jónasdóttir, Hulda S., van der Ham, Alwin J., Pelgrom, Leonard R., Schramm, Gabriele, Layland, Laura E., Sancho, David, Prazeres da Costa, Clarissa, Giera, Martin, Yazdanbakhsh, Maria, and Everts, Bart

Subjects
DENDRITIC cells, ANTIGEN presenting cells, LYMPHOID tissue, AUTOCRINE mechanisms, DINOPROSTONE
Abstract

The molecular mechanisms through which dendritic cells (DCs) prime T helper 2 (Th2) responses, including those elicited by parasitic helminths, remain incompletely understood. Here, we report that soluble egg antigen (SEA) from Schistosoma mansoni, which is well known to drive potent Th2 responses, triggers DCs to produce prostaglandin E2 (PGE2), which subsequently—in an autocrine manner—induces OX40 ligand (OX40L) expression to license these DCs to drive Th2 responses. Mechanistically, SEA was found to promote PGE2 synthesis through Dectin-1 and Dectin-2, and via a downstream signaling cascade involving spleen tyrosine kinase (Syk), extracellular signal-regulated kinase (ERK), cytosolic phospholipase A2 (cPLA2), and cyclooxygenase 1 and 2 (COX-1 and COX-2). In addition, this pathway was activated independently of the actions of omega-1 (ω-1), a previously described Th2-priming glycoprotein present in SEA. These findings were supported by in vivo murine data showing that ω-1–independent Th2 priming by SEA was mediated by Dectin-2 and Syk signaling in DCs. Finally, we found that Dectin-2−/−, and to a lesser extent Dectin-1−/− mice, displayed impaired Th2 responses and reduced egg-driven granuloma formation following S. mansoni infection, highlighting the physiological importance of this pathway in Th2 polarization during a helminth infection. In summary, we identified a novel pathway in DCs involving Dectin-1/2-Syk-PGE2-OX40L through which Th2 immune responses are induced. [ABSTRACT FROM AUTHOR]

Published
2018
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26. Peripheral cannabinoid 1 receptor blockade activates brown adipose tissue and diminishes dyslipidemia and obesity

Author

Boon, Mariëtte R., primary, Kooijman, Sander, additional, Dam, Andrea D., additional, Pelgrom, Leonard R., additional, Berbée, Jimmy F. P., additional, Visseren, Cheryl A. R., additional, Aggele, Robin C., additional, Hoek, Anita M., additional, Sips, Hetty C. M., additional, Lombès, Marc, additional, Havekes, Louis M., additional, Tamsma, Jouke T., additional, Guigas, Bruno, additional, Meijer, Onno C., additional, Jukema, J. Wouter, additional, and Rensen, Patrick C. N., additional

Published
2014
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27. mTORC1 signaling in antigen-presenting cells of the skin restrains CD8+T cell priming

Author

Pelgrom, Leonard R., Patente, Thiago A., Otto, Frank, Nouwen, Lonneke V., Ozir-Fazalalikhan, Arifa, van der Ham, Alwin J., van der Zande, Hendrik J.P., Heieis, Graham A., Arens, Ramon, and Everts, Bart

Abstract

How mechanistic target of rapamycin complex 1 (mTORC1), a key regulator of cellular metabolism, affects dendritic cell (DC) metabolism and T cell-priming capacity has primarily been investigated in vitro, but how mTORC1 regulates this in vivoremains poorly defined. Here, using mice deficient for mTORC1 component raptor in DCs, we find that loss of mTORC1 negatively affects glycolytic and fatty acid metabolism and maturation of conventional DCs, particularly cDC1s. Nonetheless, antigen-specific CD8+T cell responses to infection are not compromised and are even enhanced following skin immunization. This is associated with increased activation of Langerhans cells and a subpopulation of EpCAM-expressing cDC1s, of which the latter show an increased physical interaction with CD8+T cells in situ. Together, this work reveals that mTORC1 limits CD8+T cell priming in vivoby differentially orchestrating the metabolism and immunogenicity of distinct antigen-presenting cell subsets, which may have implications for clinical use of mTOR inhibitors.

Published
2022
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30. mTORC1 signaling in antigen-presenting cells of the skin restrains CD8 + T cell priming.

Author

Pelgrom LR, Patente TA, Otto F, Nouwen LV, Ozir-Fazalalikhan A, van der Ham AJ, van der Zande HJP, Heieis GA, Arens R, and Everts B

Subjects
Animals, Langerhans Cells immunology, Langerhans Cells metabolism, Mice, Signal Transduction, CD8-Positive T-Lymphocytes immunology, CD8-Positive T-Lymphocytes metabolism, Mechanistic Target of Rapamycin Complex 1 metabolism, Skin immunology, Skin metabolism
Abstract

How mechanistic target of rapamycin complex 1 (mTORC1), a key regulator of cellular metabolism, affects dendritic cell (DC) metabolism and T cell-priming capacity has primarily been investigated in vitro, but how mTORC1 regulates this in vivo remains poorly defined. Here, using mice deficient for mTORC1 component raptor in DCs, we find that loss of mTORC1 negatively affects glycolytic and fatty acid metabolism and maturation of conventional DCs, particularly cDC1s. Nonetheless, antigen-specific CD8 + T cell responses to infection are not compromised and are even enhanced following skin immunization. This is associated with increased activation of Langerhans cells and a subpopulation of EpCAM-expressing cDC1s, of which the latter show an increased physical interaction with CD8 + T cells in situ. Together, this work reveals that mTORC1 limits CD8 + T cell priming in vivo by differentially orchestrating the metabolism and immunogenicity of distinct antigen-presenting cell subsets, which may have implications for clinical use of mTOR inhibitors., Competing Interests: Declaration of interests The authors declare no competing interests., (Copyright © 2022 The Author(s). Published by Elsevier Inc. All rights reserved.)

Published
2022
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31. Analysis of TLR-Induced Metabolic Changes in Dendritic Cells Using the Seahorse XF(e)96 Extracellular Flux Analyzer.

Author

Pelgrom LR, van der Ham AJ, and Everts B

Subjects
Animals, Glycolysis, High-Throughput Screening Assays, Mice, Mitochondria metabolism, Oxidative Phosphorylation, Dendritic Cells metabolism, Energy Metabolism, Metabolome, Metabolomics methods, Toll-Like Receptors metabolism
Abstract

Engagement of Toll-like receptors (TLRs) on dendritic cells (DCs) triggers the expression of a large set of genes involved in DC activation and maturation, which allow them to act efficiently as antigen-presenting cells. Recently, it has become clear that TLR signalling in DCs also results in dramatic metabolic changes that are integral to their changed biology. Here, we describe a detailed protocol on how DC metabolism can be studied after TLR stimulation using the 96-well format Extracellular Flux (XF(e)96) Analyzer from Seahorse Bioscience, a machine that allows one to simultaneously assess rates of oxidative phosphorylation and glycolysis in real-time, in live cells and in a high-throughput manner.

Published
2016
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