Reorganization of multivesicular bodies regulates MHC class II antigen presentation by dendritic cells

doi:10.1083/jcb.200103071

Published 1 October 2001. doi:10.1083/jcb.200103071

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© The Rockefeller University Press, 0021-9525/2001/10/53 $5.00
The Journal of Cell Biology, Volume 155, Number 1, October 1, 2001 53-64

Article

Reorganization of multivesicular bodies regulates MHC class II antigen presentation by dendritic cells

Monique Kleijmeer¹, Georg Ramm¹, Danita Schuurhuis², Janice Griffith¹, Maria Rescigno³, Paola Ricciardi-Castagnoli³, Alexander Y. Rudensky⁴, Ferry Ossendorp⁴, Cornelis J.M. Melief⁴, Willem Stoorvogel¹ and Hans J. Geuze¹

¹ Department of Cell Biology, University Medical Center, Institute of Biomembranes and Center for Biomedical Genetics, 3584 CX Utrecht, Netherlands
² Department of Immunohaematology and Blood Transfusion, Leiden University Medical Center, 2300 RC Leiden, Netherlands
³ Department of Biotechnology and Bioscience, University of Milano-Bicocca, 20126 Milan, Italy
⁴ Howard Hughes Medical Institute, University of Washington, School of Medicine, Seattle, WA 98195

Address correspondence to Hans J. Geuze, Dept. of Cell Biology, UMC, Institute of Biomembranes, Heidelberglaan 100, Rm. G02.525, 3584 CX Utrecht, Netherlands. Tel.: 31-30-2507652. Fax: 31-30-2541797. E-mail: h.j.geuze{at}lab.azu.nl

Immature dendritic cells (DCs) sample their environment forantigens and after stimulation present peptide associated withmajor histocompatibility complex class II (MHC II) to naiveT cells. We have studied the intracellular trafficking of MHCII in cultured DCs. In immature cells, the majority of MHC IIwas stored intracellularly at the internal vesicles of multivesicularbodies (MVBs). In contrast, DM, an accessory molecule requiredfor peptide loading, was located predominantly at the limitingmembrane of MVBs. After stimulation, the internal vesicles carryingMHC II were transferred to the limiting membrane of the MVB,bringing MHC II and DM to the same membrane domain. Concomitantly,the MVBs transformed into long tubular organelles that extendedinto the periphery of the cells. Vesicles that were formed atthe tips of these tubules nonselectively incorporated MHC IIand DM and presumably mediated transport to the plasma membrane.We propose that in maturing DCs, the reorganization of MVBsis fundamental for the timing of MHC II antigen loading andtransport to the plasma membrane.

Key Words: antigen presentation; dendritic cells; endosomes; lysosomes; major histocompatibility complex

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