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By P-Selectin Glycoprotein Ligand 1 Through a Juxtacrine Mechanism Follicular Dendritic Cells Activate HIV-1 Replication in Monocytes/Macrophages through a Juxtacrine Mechanism Mediated by P-Selectin Glycoprotein Ligand 1 This information is current as of September 24, 2021. Kenji Ohba, Akihide Ryo, Md. Zahidunnabi Dewan, Mayuko Nishi, Toshio Naito, Xiaohua Qi, Yoshio Inagaki, Yoji Nagashima, Yuetsu Tanaka, Takashi Okamoto, Kazuo Terashima and Naoki Yamamoto J Immunol 2009; 183:524-532; ; Downloaded from doi: 10.4049/jimmunol.0900371 http://www.jimmunol.org/content/183/1/524 http://www.jimmunol.org/ Supplementary http://www.jimmunol.org/content/suppl/2009/06/18/183.1.524.DC1 Material References This article cites 54 articles, 17 of which you can access for free at: http://www.jimmunol.org/content/183/1/524.full#ref-list-1 Why The JI? Submit online. by guest on September 24, 2021 • 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 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 © 2009 by The American Association of Immunologists, Inc. All rights reserved. Print ISSN: 0022-1767 Online ISSN: 1550-6606. The Journal of Immunology Follicular Dendritic Cells Activate HIV-1 Replication in Monocytes/Macrophages through a Juxtacrine Mechanism Mediated by P-Selectin Glycoprotein Ligand 11 Kenji Ohba,*† Akihide Ryo,2* Md. Zahidunnabi Dewan,*†‡ Mayuko Nishi,* Toshio Naito,§ Xiaohua Qi,† Yoshio Inagaki,† Yoji Nagashima,¶ Yuetsu Tanaka,ʈ Takashi Okamoto,# Kazuo Terashima,† and Naoki Yamamoto2*† Follicular dendritic cells (FDCs) are located in the lymphoid follicles of secondary lymphoid tissues and play a pivotal role in the selection of memory B lymphocytes within the germinal center, a major site for HIV-1 infection. Germinal centers are composed of highly activated B cells, macrophages, CD4؉T cells, and FDCs. However, the physiological role of FDCs in HIV-1 replication remains largely unknown. We demonstrate in our current study that FDCs can efficiently activate HIV-1 replication in latently Downloaded from infected monocytic cells via an intercellular communication network mediated by the P-selectin/P-selectin glycoprotein ligand 1 (PSGL-1) interaction. Upon coculture with FDCs, HIV-1 replication was significantly induced in infected monocytic cell lines, primary monocytes, or macrophages. These cocultures were found to synergistically induce the expression of P-selectin in FDCs via NF-␬B activation and its cognate receptor PSGL-1 in HIV-1-infected cells. Consistent with this observation, we find that this response is significantly blocked by antagonistic Abs against PSGL-1 and almost completely inhibited by PSGL-1 small interfering RNA. More- over, a selective inhibitor for Syk, which is a downstream effector of PSGL-1, blocked HIV-1 replication in our cultures. We have thus http://www.jimmunol.org/ elucidated a novel regulatory mechanism in which FDCs are a potent positive bystander that facilitates HIV-1 replication in adjacent infected monocytic cells via a juxtacrine signaling mechanism. The Journal of Immunology, 2009, 183: 524–532. he natural progression of HIV-1 infection consists of Lymphoid organs have been proposed to function as a major acute and chronic stages (1, 2). In the acute phase of viral reservoir for HIV-1 (7). During the course of HIV infection, T T infection, an initial peak level of plasma viremia appears cells and macrophages in secondary lymphoid organs also become within a couple of weeks of transmission. At this early time point major reservoir cells for HIV-1 (8). Several in vitro studies have in the course of infection, HIV-1 has disseminated to the lymphoid now identified potentially stable reservoirs of inducible latently by guest on September 24, 2021 organs and viral reservoirs and latency have been established. The infected CD4ϩ cells carrying an integrated form of the viral ge- HIV-1 viral load stabilizes at a relatively low level after a period nome (7–9). In addition to CD4ϩ T cells, monocytes are thought of acute viral infection, defined as the “set point,” during which an to be major reservoirs for HIV-1 in vivo, since a number of blood immunological activation against HIV-1 is initiated. However, in monocytes are maintained in HIV-1-infected patients even during tandem with seroconversion, HIV-1 production in reservoir or la- the late disease stages when T cells can be practically undetectable tently infected cells will eventually resume upon specific immu- (10, 11). These observations suggest that infected CD4ϩ T cells nological responses such as host cytokine secretion or cell-medi- and macrophages provide sites as a stable reservoir and producer ated immune reactions (3–6). of HIV-1, causing the persistent production of progeny virus in lymphoid organs. However, it has not been well investigated how these reservoir cells can maintain sufficient levels of viral replica- *AIDS Research Center, National Institute of Infectious Diseases, Toyama, Shin- tion that will retain a sufficient viral load during the long course of jyuku-ku, Tokyo, Japan; †Department of Molecular Virology, Graduate School of this disease. Medicine, Tokyo Medical and Dental University, Yushima, Bunkyo-ku, Tokyo, Japan; ‡Department of Pathology, New York University School of Medicine, New It is generally believed that the central point in the immune York, NY 10016; §Department of General Medicine, Juntendo University School of system is the lymphoid organs and germinal centers (GCs)3 where ¶ Medicine, Hongo, Bunkyo-ku, Tokyo, Japan; Department of Pathology, Graduate several immune cell types are localized, although these circulate School of Medicine, Yokohama City University, Fukuura, Kanazawa-ku, Kanagawa, Japan; ʈDepartment of Immunology, Graduate School of Medicine, University of the throughout the whole body (12–14). The GCs of secondary lym- ϩ Ryukyus, Uehara, Okinawa, Japan; and #Department of Molecular and Cellular Bi- phoid tissues are composed of B cells, CD4 T cells, macro- ology, Nagoya City University Graduate School of Medical Sciences, Kawasumi, phages, and follicular dendritic cells (FDCs) (15–17). FDCs are Mizuho-cho, Mizuho-ku, Nagoya, Aichi, Japan characterized by the expression of CD21, CD35, CD40, and spe- Received for publication February 3, 2009. Accepted for publication April 25, 2009. cific cell surface adhesion molecules including ICAM-1, The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked advertisement in accordance VCAM-1, and the surface dendritic cell (DC) markers DC-SIGN with 18 U.S.C. Section 1734 solely to indicate this fact. and DRC-1 (16, 18–21). The FDCs play an important role in the 1 This work was supported in part by grants from the Japanese Ministries of Educa- tion, Culture, Sports, Science and Technology (20390136, 13226027, 14406009, and 1941075) Health, Labour and Welfare (H18-005) and Human Health Science (H19- 3 Abbreviations used in this paper: GC, germinal center; FDC, follicular dendritic 001) to N.Y. and A.R. cell; DC, dendritic cell; PSGL-1, P-selectin glycoprotein ligand 1; Syk, spleen ty- 2 Address correspondence and reprint requests to Dr. Akihide Ryo and Dr. Naoki rosine kinase; LTR, long terminal repeat; MOI, multiplicity of infection; siRNA, Yamamoto, AIDS Research Center, National Institute of Infectious Diseases, 1-23-1 small interfering RNA. Toyama, Shinjyuku-ku, Tokyo 162-8640, Japan. E-mail addresses: [email protected] and [email protected] Copyright © 2009 by The American Association of Immunologists, Inc. 0022-1767/09/$2.00 www.jimmunol.org/cgi/doi/10.4049/jimmunol.0900371 The Journal of Immunology 525 immune response by interacting with CD4ϩ T or B cells and in Virus preparation and infection organization of the follicular structure. HIV-1JR-FL or HIV-1NL4-3 viruses were generated by transfection of the In HIV infection, human FDCs can capture and retain infectious pJR-FL or pNL4-3 construct in 293T cells, respectively. Virus preparations HIV particles in a stable manner on their cell surfaces for several were passed through a 0.4-␮m filter and titrated using a conventional months or even years via Fc receptors or other molecules (22–25). method as described previously (28). For the HIV-1 infection of primary cells, PBMCs were infected with HIV-1 for 24 h following stimulation Unlike conventional DCs, FDCs are not themselves infected with JR-FL with PHA-P (3 ␮g/ml) for 3 days. To adjust the culture condition for HIV despite expression of chemokine receptors and DC-SIGN monocytes/macrophages with that for PBMCs, monocytes or macrophages (24). Furthermore, active HIV infection is largely confined to sites were also infected with HIV-1JR-FL for 24 h following stimulation with surrounding the FDCs (24), suggesting that this microenvironment PHA-P (3 ␮g/ml) for 3 days. All primary cell cultures were maintained in is highly conducive to infection with this virus. FDCs have also the absence of IL-2. Jurkat or FDCs were infected with HIV-1NL-4-3 (mul- tiplicity of infection (MOI) ϭ 0.05) for 1, 3, or 5 days. been shown to transmit signals to the GC microenvironment which also appears to increase HIV infection and replication (24, 25). Antibodies Our previous study showed that FDCs stimulated virus production Polyclonal Abs raised against phospho-p65 (Ser536), phospho-Syk in MOLT-4 T cells preexposed to HIV-1(23). Very recently, (Tyr352), phospho-I␬B␣ (Ser32), and unmodified Syk were purchased from Thacker et al.
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