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 Frueh, Daniel Lamarre, Viktor Steimle

Research output: Contribution to journalArticle

105 Citations (Scopus)

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 languageEnglish (US)
Pages (from-to)1225-1230
Number of pages6
JournalEuropean Journal of Immunology
Volume38
Issue number5
DOIs
StatePublished - May 2008

Fingerprint

Interleukin-10
Monocytes
Down-Regulation
Antigen Presentation
Immunosuppressive Agents
Ligases
Ubiquitin
Immunoprecipitation
Small Interfering RNA
Anti-Inflammatory Agents
Cytokines
Messenger RNA
Membranes
Proteins

Keywords

  • Antigen-presenting cells
  • Cytokines
  • Immune regulation
  • Inflammation
  • MHC

ASJC Scopus subject areas

  • Immunology
  • Immunology and Allergy

Cite this

Thibodeau, J., Bourgeois-Daigneault, M. C., Huppé, G., Tremblay, J., Aumont, A., Houde, M., ... 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

Interleukin-10-induced MARCH1 mediates intracellular sequestration of MHC class II in monocytes. / Thibodeau, Jacques; Bourgeois-Daigneault, Marie Claude; Huppé, Gabrielle; Tremblay, Jessy; Aumont, Angélique; Houde, Mathieu; Bartee, Eric; Brunet, Alexandre; Gauvreau, Marie Elaine; de Gassart, Aude; Gatti, Evelina; Baril, Martin; Cloutier, Maryse; Bontron, Séverine; Frueh, Klaus; Lamarre, Daniel; Steimle, Viktor.

In: European Journal of Immunology, Vol. 38, No. 5, 05.2008, p. 1225-1230.

Research output: Contribution to journalArticle

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, Frueh, 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
Thibodeau J, Bourgeois-Daigneault MC, Huppé G, Tremblay J, Aumont A, Houde M et al. Interleukin-10-induced MARCH1 mediates intracellular sequestration of MHC class II in monocytes. European Journal of Immunology. 2008 May;38(5):1225-1230. https://doi.org/10.1002/eji.200737902
Thibodeau, Jacques ; Bourgeois-Daigneault, Marie Claude ; Huppé, Gabrielle ; Tremblay, Jessy ; Aumont, Angélique ; Houde, Mathieu ; Bartee, Eric ; Brunet, Alexandre ; Gauvreau, Marie Elaine ; de Gassart, Aude ; Gatti, Evelina ; Baril, Martin ; Cloutier, Maryse ; Bontron, Séverine ; Frueh, Klaus ; Lamarre, Daniel ; Steimle, Viktor. / Interleukin-10-induced MARCH1 mediates intracellular sequestration of MHC class II in monocytes. In: European Journal of Immunology. 2008 ; Vol. 38, No. 5. pp. 1225-1230.
@article{d3307230b68c4d3e9ece6daefd928341,
title = "Interleukin-10-induced MARCH1 mediates intracellular sequestration of MHC class II in monocytes",
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.",
keywords = "Antigen-presenting cells, Cytokines, Immune regulation, Inflammation, MHC",
author = "Jacques Thibodeau and Bourgeois-Daigneault, {Marie Claude} and Gabrielle Hupp{\'e} and Jessy Tremblay and Ang{\'e}lique Aumont and Mathieu Houde and Eric Bartee and Alexandre Brunet and Gauvreau, {Marie Elaine} and {de Gassart}, Aude and Evelina Gatti and Martin Baril and Maryse Cloutier and S{\'e}verine Bontron and Klaus Frueh and Daniel Lamarre and Viktor Steimle",
year = "2008",
month = "5",
doi = "10.1002/eji.200737902",
language = "English (US)",
volume = "38",
pages = "1225--1230",
journal = "European Journal of Immunology",
issn = "0014-2980",
publisher = "Wiley-VCH Verlag",
number = "5",

}

TY - JOUR

T1 - Interleukin-10-induced MARCH1 mediates intracellular sequestration of MHC class II in monocytes

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 - Frueh, Klaus

AU - Lamarre, Daniel

AU - Steimle, Viktor

PY - 2008/5

Y1 - 2008/5

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.

KW - Antigen-presenting cells

KW - Cytokines

KW - Immune regulation

KW - Inflammation

KW - MHC

UR - http://www.scopus.com/inward/record.url?scp=47049098137&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=47049098137&partnerID=8YFLogxK

U2 - 10.1002/eji.200737902

DO - 10.1002/eji.200737902

M3 - Article

VL - 38

SP - 1225

EP - 1230

JO - European Journal of Immunology

JF - European Journal of Immunology

SN - 0014-2980

IS - 5

ER -