Interleukin-10-induced MARCH1 mediates intracellular sequestration of MHC class II in monocytes

Jacques Thibodeau; Marie Claude Bourgeois-Daigneault; Gabrielle Huppé; Jessy Tremblay; Angélique Aumont; Mathieu Houde; Eric Bartee; Alexandre Brunet; Marie Elaine Gauvreau; Aude de Gassart; Evelina Gatti; Martin Baril; Maryse Cloutier; Séverine Bontron; Klaus Früh; Daniel Lamarre; Viktor Steimle

doi:10.1002/eji.200737902

Interleukin-10-induced MARCH1 mediates intracellular sequestration of MHC class II in monocytes

Jacques Thibodeau, Marie Claude Bourgeois-Daigneault, Gabrielle Huppé, Jessy Tremblay, Angélique Aumont, Mathieu Houde, Eric Bartee, Alexandre Brunet, Marie Elaine Gauvreau, Aude de Gassart, Evelina Gatti, Martin Baril, Maryse Cloutier, Séverine Bontron, Klaus Früh, Daniel Lamarre, Viktor Steimle

Vaccine and Gene Therapy Institute

Research output: Contribution to journal › Article › peer-review

127 Scopus citations

Abstract

IL-10 is a potent anti-inflammatory cytokine interfering with antigen presentation by inducing the intracellular sequestration of MHC class II (MHC-II) molecules. Here we studied the contribution of membrane-associated RING-CH (MARCH) ubiquitin ligase family members to the IL-10-induced down-regulation of MHC-II molecules. We found that MARCH1 and MARCH8 proteins are the most potent family members for the downregulation of MHC-II surface expression in transfected cells, but only MARCH1 mRNA expression is strongly induced by IL-10 in human primary monocytes.We detected mono-and poly-ubiquitinated forms of MHC-II molecules both in IL-10-treated monocytes and in cells transfected with MARCH1. We also show direct interaction between MHC-II and MARCH1 molecules in co-immunoprecipitation assays. Finally, we found that siRNA-mediated knockdown of MARCH1 reverses IL-10-induced MHC-II down-regulation in primary monocytes. Thus, the immunosuppressive effect of IL-10 on antigen presentation is mediated through induced expression of MARCH1.

Original language	English (US)
Pages (from-to)	1225-1230
Number of pages	6
Journal	European Journal of Immunology
Volume	38
Issue number	5
DOIs	https://doi.org/10.1002/eji.200737902
State	Published - May 2008

Keywords

Antigen-presenting cells
Cytokines
Immune regulation
Inflammation
MHC

ASJC Scopus subject areas

Immunology and Allergy
Immunology

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10.1002/eji.200737902

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Thibodeau, J., Bourgeois-Daigneault, M. C., Huppé, G., Tremblay, J., Aumont, A., Houde, M., Bartee, E., Brunet, A., Gauvreau, M. E., de Gassart, A., Gatti, E., Baril, M., Cloutier, M., Bontron, S., Früh, K., Lamarre, D., & Steimle, V. (2008). Interleukin-10-induced MARCH1 mediates intracellular sequestration of MHC class II in monocytes. European Journal of Immunology, 38(5), 1225-1230. https://doi.org/10.1002/eji.200737902

Thibodeau, J, Bourgeois-Daigneault, MC, Huppé, G, Tremblay, J, Aumont, A, Houde, M, Bartee, E, Brunet, A, Gauvreau, ME, de Gassart, A, Gatti, E, Baril, M, Cloutier, M, Bontron, S, Früh, K, Lamarre, D & Steimle, V 2008, 'Interleukin-10-induced MARCH1 mediates intracellular sequestration of MHC class II in monocytes', European Journal of Immunology, vol. 38, no. 5, pp. 1225-1230. https://doi.org/10.1002/eji.200737902

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abstract = "IL-10 is a potent anti-inflammatory cytokine interfering with antigen presentation by inducing the intracellular sequestration of MHC class II (MHC-II) molecules. Here we studied the contribution of membrane-associated RING-CH (MARCH) ubiquitin ligase family members to the IL-10-induced down-regulation of MHC-II molecules. We found that MARCH1 and MARCH8 proteins are the most potent family members for the downregulation of MHC-II surface expression in transfected cells, but only MARCH1 mRNA expression is strongly induced by IL-10 in human primary monocytes.We detected mono-and poly-ubiquitinated forms of MHC-II molecules both in IL-10-treated monocytes and in cells transfected with MARCH1. We also show direct interaction between MHC-II and MARCH1 molecules in co-immunoprecipitation assays. Finally, we found that siRNA-mediated knockdown of MARCH1 reverses IL-10-induced MHC-II down-regulation in primary monocytes. Thus, the immunosuppressive effect of IL-10 on antigen presentation is mediated through induced expression of MARCH1.",

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AU - Thibodeau, Jacques

AU - Bourgeois-Daigneault, Marie Claude

AU - Huppé, Gabrielle

AU - Tremblay, Jessy

AU - Aumont, Angélique

AU - Houde, Mathieu

AU - Bartee, Eric

AU - Brunet, Alexandre

AU - Gauvreau, Marie Elaine

AU - de Gassart, Aude

AU - Gatti, Evelina

AU - Baril, Martin

AU - Cloutier, Maryse

AU - Bontron, Séverine

AU - Früh, Klaus

AU - Lamarre, Daniel

AU - Steimle, Viktor

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N2 - IL-10 is a potent anti-inflammatory cytokine interfering with antigen presentation by inducing the intracellular sequestration of MHC class II (MHC-II) molecules. Here we studied the contribution of membrane-associated RING-CH (MARCH) ubiquitin ligase family members to the IL-10-induced down-regulation of MHC-II molecules. We found that MARCH1 and MARCH8 proteins are the most potent family members for the downregulation of MHC-II surface expression in transfected cells, but only MARCH1 mRNA expression is strongly induced by IL-10 in human primary monocytes.We detected mono-and poly-ubiquitinated forms of MHC-II molecules both in IL-10-treated monocytes and in cells transfected with MARCH1. We also show direct interaction between MHC-II and MARCH1 molecules in co-immunoprecipitation assays. Finally, we found that siRNA-mediated knockdown of MARCH1 reverses IL-10-induced MHC-II down-regulation in primary monocytes. Thus, the immunosuppressive effect of IL-10 on antigen presentation is mediated through induced expression of MARCH1.

AB - IL-10 is a potent anti-inflammatory cytokine interfering with antigen presentation by inducing the intracellular sequestration of MHC class II (MHC-II) molecules. Here we studied the contribution of membrane-associated RING-CH (MARCH) ubiquitin ligase family members to the IL-10-induced down-regulation of MHC-II molecules. We found that MARCH1 and MARCH8 proteins are the most potent family members for the downregulation of MHC-II surface expression in transfected cells, but only MARCH1 mRNA expression is strongly induced by IL-10 in human primary monocytes.We detected mono-and poly-ubiquitinated forms of MHC-II molecules both in IL-10-treated monocytes and in cells transfected with MARCH1. We also show direct interaction between MHC-II and MARCH1 molecules in co-immunoprecipitation assays. Finally, we found that siRNA-mediated knockdown of MARCH1 reverses IL-10-induced MHC-II down-regulation in primary monocytes. Thus, the immunosuppressive effect of IL-10 on antigen presentation is mediated through induced expression of MARCH1.

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KW - Cytokines

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KW - Inflammation

KW - MHC

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Interleukin-10-induced MARCH1 mediates intracellular sequestration of MHC class II in monocytes

Abstract

Keywords

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