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Lipid Rafts Presentation of Macrophage by Disrupting Affects Antigen Leishmania Donovani

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Lipid Rafts Presentation of Macrophage by Disrupting Affects Antigen Leishmania Donovani Leishmania donovani Affects Antigen Presentation of Macrophage by Disrupting Lipid Rafts This information is current as Debabani Chakraborty, Subha Banerjee, Abhik Sen, Kalyan of October 3, 2021. K. Banerjee, Pradip Das and Syamal Roy J Immunol 2005; 175:3214-3224; ; doi: 10.4049/jimmunol.175.5.3214 http://www.jimmunol.org/content/175/5/3214 Downloaded from References This article cites 91 articles, 37 of which you can access for free at: http://www.jimmunol.org/content/175/5/3214.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 *average by guest on October 3, 2021 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 © 2005 by The American Association of Immunologists All rights reserved. Print ISSN: 0022-1767 Online ISSN: 1550-6606. The Journal of Immunology Leishmania donovani Affects Antigen Presentation of Macrophage by Disrupting Lipid Rafts1 Debabani Chakraborty,2* Subha Banerjee,2* Abhik Sen,† Kalyan K. Banerjee,† Pradip Das,† and Syamal Roy3* Leishmania donovani-infected splenic macrophages and P388D1 (P388D1(I)) failed to activate T cells in response to low dose of exogenous peptide. The membrane fluidity of P388D1(I) was greater than that of the normal counterpart P388D1(N), but could be reduced either by exposing the cell below phase transition point or by loading cholesterol into membrane (L-P388D1(I)), and this was associated with enhanced Ag-presenting ability of P388D1(I). Presentation of endogenous leishmanial Ag, kinetoplastid membrane protein-11, was also defective, but could be corrected by loading cholesterol into membrane. Because membrane rafts are important for Ag presentation at a low peptide dose, raft architecture of P388D1(I) was studied using raft (CD48 and cholera toxin-B) and non-raft (CD71) markers in terms of their colocalization with I-Ad. Binding of anti-CD48 mAb and cholera toxin B Downloaded from subunit decreased significantly in P388D1(I), and consequently, colocalization with I-Ad was not seen, but this could be restored in L-P388D1(I). Conversely, colocalization between I-Ad and CD71 remained unaffected regardless of the presence or the absence of intracellular parasites. P388D1(N) and L-P388D1(I), but not P388D1(I), formed peptide-dependent synapse with T cells quite efficiently and this was found to be corroborated with both intracellular Ca2؉ mobilization in T cells and IL-2 production. This indicated that intracellular parasites disrupt the membrane rafts, possibly by increasing the membrane fluidity, which could be corrected by making the membrane rigid. This may be a strategy that intracellular L. donovani adopts to evade host immune http://www.jimmunol.org/ system. The Journal of Immunology, 2005, 175: 3214–3224. eishmaniasis is a vector-borne parasitic disease with a show that human blood monocyte-derived DCs could be infected broad range of clinical manifestation from local cutane- with Leishmania donovani (LD) (6), and maturation of mouse L ous lesion to life-threatening visceral disease, mainly bone marrow-derived DCs is inhibited by Leishmania amazonen- caused by differences among Leishmania species and the immu- sis (7). The present study is concerned with the Ag-presenting nological status of the mammalian hosts (1). The parasite exists in ability of M␾ as a general mechanism to understand how intra- two different stages; the flagellated promastigotes are transmitted cellular Leishmania parasites modulate the surface phenomena of with the bite of the sandfly to the mammalian hosts, where they APCs, which, in turn, may affect Ag presentation. by guest on October 3, 2021 4 transform into the amastigote stage. Although macrophage (M␾) The disease visceral leishmaniasis or kala-azar, caused by the are generally considered to be the main or only host cells allowing protozoan parasite LD, is characterized by defective cell-mediated Leishmania to survive and multiply (2), other cells can harbor immunity (8–13), the cause of which is still unknown. Leishma- intact viable parasites at least transiently. For example, Leishmania nia-infected M␾ are unable to present even processing-indepen- major parasites have been observed in polymorphonuclear leuko- dent peptide sequences to T cell hybridoma, and this inability is cytes, fibroblast, and dendritic cells (DC) at different stages of not due to defective MHC expression (14). Recent studies show infection (3). The ability of Langerhans cells and DCs to take up that Leishmania-infected M␾ efficiently stimulate Ag-independent Leishmania is still a matter of debate (4, 5). Murine fetal skin- and Ag-dependent TCR-mediated capping of F-actin in T cells derived DCs are preferentially infected by L. major amastigotes (15). Infected M␾ are less efficient at promoting the sustained T compared with metacyclic promastigotes (5). Recently, studies cell signaling events, but this is not due to altered levels of surface- expressed peptide-MHC complexes (15). *Department of Immunology, Indian Institute of Chemical Biology; and †National Physiological stimulation of T cells by antigenic peptides pre- Institute of Cholera and Enteric Diseases, Scheme XM, Beliaghata, Kolkata, India sented in the context of MHC molecules requires a stable contact Received for publication May 24, 2005. Accepted for publication June 13, 2005. between T cells and APCs to enable the generation of efficient The costs of publication of this article were defrayed in part by the payment of page activation signals (16, 17). The area of contact between the two charges. This article must therefore be hereby marked advertisement in accordance with 18 U.S.C. Section 1734 solely to indicate this fact. cells, the immunological synapse, has recently become a fruitful focus of investigation (18, 19). Recent work on the membrane 1 This work was supported by the Council for Scientific and Industrial Research, New Delhi, India (Project CMM002). D.C. and S.B. are recipients of Council of Scientific features that affect presentation of Ags by APCs to T cells indi- and Industrial research fellowships. cates that lipid rafts in the outer leaflet of the membrane lipid 2 D.C. and S.B. contributed equally to the work. bilayer induce clustering of the peptide-MHC complex on the APC 3 Address correspondence and reprint requests to Dr. Syamal Roy, Department of surface. This leads to an effective increase in the surface density of Immunology, 4 Raja S. C. Mullick Road, Kolkata 700032, India. E-mail address: the MHC-Ag and up-regulation of the T cell response (20–22). [email protected] Lipid rafts are cholesterol- or sphingolipid-rich microdomains with 4 Abbreviations used in this paper: M␾, macrophage; LD, Leishmania donovani; CTX-B, cholera toxin B subunit; DC, dendritic cell; DPH, 1,6-diphenyl-1,3,5- high melting temperatures caused by ordered packing of molecules hexatriene; FA, fluorescence anisotropy; HEL, hen egg lysozyme; I-M␾, infected (23). The proposed functions of lipid rafts include cholesterol splenic macrophage; KMP-11, kinetoplastid membrane protein-11; L-P388D1(I), cholesterol-loaded P388D1(I); P388D1(I), infected P388D1 cell; P388D1(N), unin- transport (24, 25), endocytosis (26), signal transduction (27–29), fected P388D1 cell; SLA, soluble leishmanial Ag. potocytosis (30), and pathogen portals (31–34). The concept of Copyright © 2005 by The American Association of Immunologists, Inc. 0022-1767/05/$02.00 The Journal of Immunology 3215 lipid rafts as pathogen portals has gained considerable interest in Mice, infection, and preparation of splenic and peritoneal M␾ recent years. When Plasmodium invades RBC, host cell plasma BALB/c mice were obtained from the animal facility of the institute. membrane lipids are incorporated into the parasite-containing vac- CBA/J mice were a gift from Dr. S. K. Basu (National Institute of Immu- uole, whereas transmembrane proteins are excluded (35). Simi- nology, New Delhi, India). Mice were housed under conventional condi- larly, in Toxoplasma gondii infection, GPI-anchored surface pro- tions, with food and water ad libitum. Animals were used for experimental teins are incorporated into parasitophorous vacuole, whereas host purposes with prior approval of the institutional animal ethics committee. Spleens of BALB/c mice were isolated and macerated between the frosted cell transmembrane proteins are excluded from it (36). Cholesterol ends of a pair of glass slides in PBS (pH 7.2). The cell suspension was then appears to play a key role in organizing the lipid domain, which is layered over Ficoll-Hypaque, and density gradient centrifugation was per- required for the entry of mycobacteria (37) and Leishmania (38) formed at 1600 rpm for 20 min. The cells in the interface were collected into the host cells. Disruption of lipid rafts by sequestration of and washed twice in PBS. The splenic M␾ were purified as previously ␤ described (12). Similarly, peritoneal M␾ of CBA/J mice were isolated as cholesterol after treatment
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