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Activation and HLA-DO Is Induced by B Lymphocyte in Vivo and in Vitro

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Activation and HLA-DO Is Induced by B Lymphocyte in Vivo and in Vitro In Vivo and In Vitro Modulation of HLA-DM and HLA-DO Is Induced by B Lymphocyte Activation This information is current as Corinne Roucard, Claire Thomas, Marie-Anne Pasquier, John of September 30, 2021. Trowsdale, Jean-Jacques Sotto, Jacques Neefjes and Marieke van Ham J Immunol 2001; 167:6849-6858; ; doi: 10.4049/jimmunol.167.12.6849 http://www.jimmunol.org/content/167/12/6849 Downloaded from References This article cites 69 articles, 34 of which you can access for free at: http://www.jimmunol.org/content/167/12/6849.full#ref-list-1 http://www.jimmunol.org/ Why The JI? Submit online. • Rapid Reviews! 30 days* from submission to initial decision • No Triage! Every submission reviewed by practicing scientists • Fast Publication! 4 weeks from acceptance to publication by guest on September 30, 2021 *average Subscription Information about subscribing to The Journal of Immunology is online at: http://jimmunol.org/subscription Permissions Submit copyright permission requests at: http://www.aai.org/About/Publications/JI/copyright.html Email Alerts Receive free email-alerts when new articles cite this article. Sign up at: http://jimmunol.org/alerts The Journal of Immunology is published twice each month by The American Association of Immunologists, Inc., 1451 Rockville Pike, Suite 650, Rockville, MD 20852 Copyright © 2001 by The American Association of Immunologists All rights reserved. Print ISSN: 0022-1767 Online ISSN: 1550-6606. In Vivo and In Vitro Modulation of HLA-DM and HLA-DO Is Induced by B Lymphocyte Activation1 Corinne Roucard,2* Claire Thomas,† Marie-Anne Pasquier,* John Trowsdale,‡ Jean-Jacques Sotto,* Jacques Neefjes,§ and Marieke van Ham§¶ Ag presentation via HLA class II molecules in B lymphocytes depends on the coordinated action of HLA-DM, the catalyst of class II-peptide loading, and HLA-DO, a pH-dependent modulator of DM, the expression of which is almost completely restricted to B lymphocytes. The relative expression levels of both class II modulators are critical for the composition of the HLA class II peptide repertoire. The data in this work demonstrate that DO and DM expression are both dependent on the cellular activation status in primary human B lymphocytes. In vivo low-density activated primary human B lymphocytes show a prominent reduction in DO and DM expression when compared with high-density resting primary B lymphocytes. In vitro, reduction of DO and DM expression can be induced by B lymphocyte activation via the B cell receptor or by use of the phorbol ester, PMA. Specific Downloaded from inhibition of protein kinase C resulted in a significant reduction of HLA-DO and is potentially due to protein degradation in lysosomal compartments as the phenomenon is reversed by chloroquine. Thus, the expression of the dedicated HLA class II chaperone DM and its pH-dependent modulator DO is regulated and tightly controlled by the activation status of the B lymphocyte. The Journal of Immunology, 2001, 167: 6849–6858. ajor histocompatibility complex class II molecules In B lymphocytes, another MHC class II-like heterodimer, http://www.jimmunol.org/ present Ags derived from exogenous sources to the termed HLA-DO, associates with DM (6). The expression of the M TCR on CD4ϩ T lymphocytes. In the human, MHC DO complex (7, 8) and the murine equivalent H2-O, is unusual in class II molecules are composed of the HLA-DR, -DQ, and -DP. that it seems to be restricted to B lymphocytes and thymic epithe- Shortly after synthesis, the DR␣ and DR␤ chains form a complex lium (9, 10). B lymphocytes have unique features as APCs, in that with the invariant chain (Ii)3 (1), which targets the class II/Ii com- they can take up Ags via a specific receptor, the B cell receptor plex into the endocytic pathway (2). During transport to the Ag (BCR). Recent studies demonstrated that DO is a negative modu- loading compartments (dubbed MIIC for MHC class II-containing lator of the catalytic activity of DM (11–13). The action of DO compartment), Ii is degraded until only a class II-associated Ii depends on the pH of the compartment in which the DM/DO com- by guest on September 30, 2021 peptide (CLIP) remains bound to the class II peptide binding plex resides. DO effectively blocks DM function at the endosomal groove. In the MIICs, binding of incoming Ag to class II requires pH, while allowing DM action at the more acidic pH of the MIICs the action of HLA-DM that resides in endosomal/lysosomal com- (11, 14, 15). In this way, DO action may skew the class II-peptide partments, as it catalyzes the release of CLIP from the class II loading process toward acidic compartments. This may favor pre- backbone (3, 4). Finally, the class II-peptide complex is trans- sentation of specific peptides internalized via the BCR, as these ported to the cell surface (5) where interaction with an appropriate preferentially form a complex with class II in the MIICs (16, 17), T cell can occur. while counteracting presentation of peptides that are taken up via fluid phase endocytosis. Indeed, DO modulates the antigenic pep- tide repertoire associated with class II molecules both qualitatively and quantitatively (13). Moreover, mice knockout for H2-O have *Groupe de Recherche sur les Lymphomes, Institut Albert Bonniot, Domaine de la enhanced class II presentation of fluid phase Ags as opposed to Merci, La Tronche, France; †Molecular Neuropathobiology Laboratory, Imperial Ags internalized via BCR (11). ‡ Cancer Research Fund, London, United Kingdom; Division of Immunology, De- In this work, the expression and regulation of both modulators partment of Pathology, University of Cambridge, Cambridge CB2 1QP, United King- dom; §Division of Tumor Biology, The Netherlands Cancer Institute, Amsterdam, of class II-mediated Ag presentation as well as HLA class II mol- The Netherlands; and ¶Department of Pathology, Unit Experimental Oncopathology, ecules were studied in primary human B lymphocytes isolated Free University Hospital, Amsterdam, The Netherlands from peripheral blood. The expression of DO in primary B lym- Received for publication March 23, 2001. Accepted for publication October 15, 2001. phocytes is much higher than anticipated on the basis of previous The costs of publication of this article were defrayed in part by the payment of page studies with B cell lines. Strikingly, in in vivo low-density acti- charges. This article must therefore be hereby marked advertisement in accordance with 18 U.S.C. Section 1734 solely to indicate this fact. vated B lymphocytes the expression of both DM and DO is 1 C.R. was supported by grants from Fondation de France and the Association Espoir- strongly reduced compared with high-density resting B lympho- Ise`re Contre le Cancer. M.v.H. was supported by a Pioneer Grant from the Nether- cytes. In vitro B cell stimulation via the BCR or with the phorbol lands Organization for Scientific Research. J.T. was supported by a program grant from the Wellcome Foundation. J.N. and J.T. were supported by Training and Mo- ester PMA induced a reduction in DM and DO expression. Inac- bility of Researchers Network Grant CT960069 from the European Community. tivation of protein kinase C (PKC) with the bisindolylmaleimide 2 Address correspondence and reprint requests to Dr. Corinne Roucard, Groupe de Ro 31-8220 resulted in a significant loss of HLA-DO expression Recherche sur les Lymphomes, Institut Albert Bonniot, Domaine de la Merci, 38706 and, in some cases, of HLA-DM. Lysosomal degradation could be La Tronche, France. E-mail address: [email protected] involved as chloroquine (CQ) reverses the effect of Ro 31-8220. 3 Abbreviations used in this paper: Ii, invariant chain; BCR, B cell receptor; CHX, cycloheximide; CLIP, class II-associated Ii peptide; CQ, chloroquine; MIIC, MHC Thus, activation of primary B lymphocytes enable the cells to con- class II compartment; PKC, protein kinase C; MFI, mean fluorescence intensity. trol the efficacy of MHC class II-mediated Ag presentation. Copyright © 2001 by The American Association of Immunologists 0022-1767/01/$02.00 6850 DOWN-REGULATION OF HLA-DM AND HLA-DO IN HUMAN B LYMPHOCYTES Materials and Methods PKC inhibition Abs and peptides Freshly purified high-density B lymphocytes were incubated for 4 h with ␣ ␣ the PKC inhibitor bisindolylmaleimide Ro 31-8220 (final concentration 10 The mouse mAbs 5C1 (anti-DM ) (18), DA6-147 (anti-DR cytoplasmic ␮ tail) (19, 20), D1.12 (anti-DR␣) (21), and CerCLIP (22) were previously M; stock solution in DMSO; Calbiochem). Control cells were incubated described. The anti-PKC␣ and anti-PKC␤ mAbs were obtained from BD with equivalent amounts of DMSO, representing less than 0.1% of the total volume. For inhibition of de novo protein synthesis, cells were preincu- Transduction Laboratories (Lexington, KY) and the anti-actin mAb was ␮ obtained from Oncogene Research Products (Cambridge, MA). bated for 1 h with cycloheximide (CHX) (final concentration 20 M; stock The mAbs anti-CD80 labeled with FITC and anti-CD86 labeled with PE solution in ethanol; Sigma-Aldrich) followed by a 4-h incubation in the Ј presence or absence of Ro 31-8220 (10 ␮M). To neutralize the acidic pH were obtained from Immunotech (Marseille, France), and the rabbit F(ab )2 Abs against human IgD labeled with FITC, IgG labeled with FITC, and of endosomal/lysosomal compartments, cells were preincubated with 200 ␮M CQ for 15 min, followed by 4 h with both CQ and Ro 31-8220 (10 IgM labeled with PE were from DAKO (High Wycombe, U.K.). ␮ The rabbit anti-DO␤ serum was generated by immunizing a rabbit with M) or CQ alone. the C-terminal peptide (SGNEVSRAVLLPQSC) of DO␤ (8) conjugated SDS-PAGE and Western blot analysis via glutaraldehyde (Sigma-Aldrich, Poole, U.K.) to keyhole limpet hemo- cyanin (Calbiochem, La Jolla, CA).
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