Cited by 208Immunotherapy and Immune ResponsesHIV Research and TreatmentImmune Response and Inflammation

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Dendritic Cell-Specific Intercellular Adhesion Molecule 3-Grabbing Nonintegrin/CD209 Is Abundant on Macrophages in the Normal Human Lymph Node and Is Not Required for Dendritic Cell Stimulation of the Mixed Leukocyte Reaction

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Granelli-Piperno, Angela, Pritsker, Alla, Pack, Maggi, Shimeliovich, Irina, Arrighi, Jean-Francois, Park, Chae Gyu, Trumpfheller, Christine, Piguet, Vincent, Moran, Thomas M, Steinman, Ralph M·2005·The Journal of Immunology

DOI 10.4049/jimmunol.175.7.4265

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Abstract

The C-type lectin dendritic cell-specific ICAM 3-grabbing nonintegrin (DC-SIGN)/CD209 efficiently binds several pathogens, including HIV-1. DC-SIGN is expressed on monocyte-derived DCs in culture, and importantly, it is able to sequester HIV-1 within cells and facilitate transmission of virus to CD4+ T cells. To investigate DC-SIGN function, we have generated new mAbs. We report in this study that these and prior anti-DC-SIGN mAbs primarily label macrophages in the medullary sinuses of noninflamed human lymph node. In contrast, expression is not detected on most DCs in the T cell area, except for occasional cells. We also noted that IL-4 alone can induce expression of DC-SIGN in CD14+ monocytes and circulating blood DCs. However, blockade of DC-SIGN with Abs and DC-SIGN small interfering RNA did not result in a major reduction in the capacity of these DCs to transfer HIV to T cells, confirming significant DC-SIGN-independent mechanisms. The blocking approaches did reduce HIV-1 transmission by DC-SIGN-transfected cells by >90%. DC-SIGN blockade also did not reduce the ability of DCs to stimulate T cell proliferation in the MLR. These results indicate that DC-SIGN has the potential to contribute to macrophage function in normal human lymph node, and that DCs do not require DC-SIGN to transmit HIV or to initiate T cell responses.

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BackgroundResult
Relative Levels of M-CSF and GM-CSF Influence the Specific Generation of Macrophage Populations during Infection with Mycobacterium tuberculosis
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Research Progress and Applications of Multivalent, Multispecific and Modified Nanobodies for Disease Treatment
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Gram-positive bacteria enhance HIV-1 susceptibility in Langerhans cells, but not in dendritic cells, via Toll-like receptor activation
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Engineering Magnetosomes for High-Performance Cancer Vaccination
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Plasminogen Activator Pla of Yersinia pestis Utilizes Murine DEC-205 (CD205) as a Receptor to Promote Dissemination
Zhang, S., Park, C. G., Zhang, P., Bartra, S. S., Plano, G. V., Klena, J. D., Skurnik, M., Hinnebusch, B. J., & Chen, T. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m804646200 · Cited by 80
Self-citation
Broad Antiviral Activity of Carbohydrate-Binding Agents against the Four Serotypes of Dengue Virus in Monocyte-Derived Dendritic Cells
Alen, M., Burghgraeve, T. D., Kaptein, S. J. F., Balzarini, J., Neyts, J., & Schols, D. (2011) · PLoS ONE · doi:10.1371/journal.pone.0021658 · Cited by 73
DC-SIGN and mannosylated surface structures of Mycobacterium tuberculosis: a deceptive liaison.
Ehlers, S. (2010) · European Journal of Cell Biology · doi:10.1016/j.ejcb.2009.10.004 · Cited by 72
The Achilles Heel of the Trojan Horse Model of HIV-1 trans-Infection
Cavrois, M., Neidleman, J. A., & Greene, W. C. (2008) · PLoS Pathogens · doi:10.1371/journal.ppat.1000051 · Cited by 67
“Some reports indicate that trans-infection of T cells by DCs derived in vitro from monocytes (MDDCs) involves DC-SIGN [9,18,20,26,27], while other studies suggest the involvement of alternative C-type lectin receptors [16,28,29,30].”
Background
HIV-1 and HTLV-1 Transmission Modes: Mechanisms and Importance for Virus Spread
Kalinichenko, S., Komkov, D., & Mazurov, D. (2022) · Viruses · doi:10.3390/v14010152 · Cited by 68
Human Dendritic Cell-Specific Intercellular Adhesion Molecule-Grabbing Nonintegrin (CD209) Is a Receptor forYersinia pestisThat Promotes Phagocytosis by Dendritic Cells
Zhang, P., Skurnik, M., Zhang, S.-S., Schwartz, O., Kalyanasundaram, R., Bulgheresi, S., He, J. J., Klena, J. D., Hinnebusch, B. J., & Chen, T. (2008) · Infection and Immunity · doi:10.1128/iai.01246-07 · Cited by 68
“DC-SIGN is also expressed in certain types of macrophages (23), including human alveolar macrophages (54).”
Background
Glycosphingolipid Composition of Human Immunodeficiency Virus Type 1 (HIV-1) Particles Is a Crucial Determinant for Dendritic Cell-Mediated HIV-1 trans-Infection
Hatch, S., Archer, J., & Gummuluru, S. (2009) · Journal of Virology · doi:10.1128/jvi.02249-08 · Cited by 66
Straight to the point: targeted mRNA-delivery to immune cells for improved vaccine design
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CD4 Coexpression Regulates DC-SIGN-Mediated Transmission of Human Immunodeficiency Virus Type 1
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“DC-SIGN-independent mechanisms are also involved in DC-mediated HIV-1 trans infection of CD4 T cells (4, 21, 22, 53, 59, 63).”
Background
DEC‐205/CD205+ dendritic cells are abundant in the white pulp of the human spleen, including the border region between the red and white pulp
Pack, M., Trumpfheller, C., Thomas, D. A., Park, C. G., Granelli‐Piperno, A., Münz, C., & Steinman, R. M. (2007) · Immunology · doi:10.1111/j.1365-2567.2007.02710.x · Cited by 59
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A full scale comparative study of methods for generation of functional Dendritic cells for use as cancer vaccines
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Surfactant Protein A Binds to HIV and Inhibits Direct Infection of CD4+ Cells, but Enhances Dendritic Cell-Mediated Viral Transfer1
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Distribution and lateral mobility of DC-SIGN on immature dendritic cells–implications for pathogen uptake
Neumann, A. K., Thompson, N. L., & Jacobson, K. (2008) · Journal of Cell Science · doi:10.1242/jcs.022418 · Cited by 61
“DC-SIGN knockdown and blocking ligands are poor inhibitors of in vitro HIV-1 transmission to T cells via human dendritic cells; however, these approaches do significantly attenuate infection in trans when Raji-DCSIGN cell lines are used as donor cells in T cell co-cultures (Boggiano et al., 2007; Granelli-Piperno et a…”
Background
Significant Virus Replication in Langerhans Cells following Application of HIV to Abraded Skin: Relevance to Occupational Transmission of HIV
Kawamura, T., Koyanagi, Y., Nakamura, Y., Ogawa, Y., Yamashita, A., Iwamoto, T., Ito, M., Blauvelt, A., & Shimada, S. (2008) · The Journal of Immunology · doi:10.4049/jimmunol.180.5.3297 · Cited by 57
“HIV from MDDC to T cells (18, 19), DC-SIGN may be involved”
Background
Dermal-Type Macrophages Expressing CD209/DC-SIGN Show Inherent Resistance to Dengue Virus Growth
Kwan, W.-H., Navarro-Sánchez, E., Dumortier, H., Decossas, M., Vachon, H., dos Santos, F. D., Fridman, H., Rey, F., Harris, E., Desprès, P., et al. (2008) · PLoS Neglected Tropical Diseases · doi:10.1371/journal.pntd.0000311 · Cited by 57
“Western blotting of cell lysates confirmed the presence of CD209 as a major band of 49 kDa in both cell-types [13] (Figure S1B).”
Background
The pro and anti-inflammatory activities of immunoglobulin G
Lux, A., Aschermann, S., Biburger, M., & Nimmerjahn, F. (2009) · Annals of the Rheumatic Diseases · doi:10.1136/ard.2009.117101 · Cited by 52
LILRA2 Activation Inhibits Dendritic Cell Differentiation and Antigen Presentation to T Cells
Lee, D. J., Sieling, P. A., Ochoa, M. T., Krutzik, S. R., Guo, B., Hernandez, M., Rea, T. H., Cheng, G., Colonna, M., & Modlin, R. L. (2007) · The Journal of Immunology · doi:10.4049/jimmunol.179.12.8128 · Cited by 53
“activated tonsil (30), lymph node (31), and rheumatoid arthritis”
Background
Functional comparison of mouse CIRE/mouse DC-SIGN and human DC-SIGN
Caminschi, I., Corbett, A., Zahra, C., Lahoud, M., Lucas, K., Sofi, M., Vremec, D., Gramberg, T., Pöhlmann, S., Curtis, J., et al. (2006) · International Immunology · doi:10.1093/intimm/dxl011 · Cited by 54
“(57) .”
Background
Dendritic Cells From the Cervical Mucosa Capture and Transfer HIV-1 via Siglec-1
Perez‐Zsolt, D., Cantero-Pérez, J., Erkizia, I., Benet, S., Pino, M., Serra‐Peinado, C., Hernández-Gallego, A., Castellví, J., Tapia, G., Arnau-Saz, V., et al. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.00825 · Cited by 61
“Alternatively, supernatants from these co-cultures were transferred to 0.2× 106 DCs to assess Siglec-1 induction 24 h later with a FACSCalibur, labeling cells with a mAb anti-Siglec-1-PE or a matched isotypePE control (both from AbD Serotec).”
MethodInfluential
HIV-1 Trans Infection of CD4 + T Cells by Professional Antigen Presenting Cells
Rinaldo, C. R. (2013) · Scientifica · doi:10.1155/2013/164203 · Cited by 49
Antigen structure affects cellular routing through DC-SIGN
Jarvis, C. M., Zwick, D. B., Grim, J. C., Alam, M. M., Prost, L. R., Gardiner, J. C., Park, S., Zimdars, L. L., Sherer, N. M., & Kiessling, L. L. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1820165116 · Cited by 61
“Consistent with these data, prior studies have shown that HIV internalization and transmission is inhibited by α-DC-SIGN blocking antibodies in Raji/DCSIGN cells but not in DCs, implicating that other lectins are capable of facilitating viral uptake in when DC-SIGN is unavailable (50, 51).”
Result
HIV gag protein is efficiently cross-presented when targeted with an antibody towards the DEC-205 receptor in Flt3 ligand-mobilized murine dendritic cells
Bozzacco, L., Trumpfheller, C., Huang, Y.-X., Longhi, M. P., Shimeliovich, I., Schauer, J. D., Park, C. G., & Steinman, R. (2009) · European Journal of Immunology · doi:10.1002/eji.200939748 · Cited by 50
Self-citation
Immune recruitment or suppression by glycan engineering of endogenous and therapeutic antibodies
Le, N. P. L., Bowden, T. A., Struwe, W. B., & Crispin, M. (2016) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2016.04.016 · Cited by 48
“phages [254,255], murine SIGN-R1 is not expressed on such cell types.”
Background
Dendritic Cells Are Less Susceptible to Human Immunodeficiency Virus Type 2 (HIV-2) Infection than to HIV-1 Infection
Duvall, M. G., Loré, K., Blaak, H., Ambrozak, D. R., Adams, W. C. T., Santos, K., Geldmacher, C., Mascola, J. R., McMichael, A. J., Jaye, A., et al. (2007) · Journal of Virology · doi:10.1128/jvi.00976-07 · Cited by 48
“, by becoming productively infected and passing virus to T cells (11, 35, 38, 47, 66), by transmitting virus through an infectious synapse of DCs and T cells (1, 45), or by capturing virions in the absence of productive infection and transferring the virus to CD4 T cells in trans (3, 26, 27, 29, 30, 65, 68, 70, 71).”
Background
Single‐domain llama antibodies as specific intracellular inhibitors of SpvB, the actin ADP‐ribosylating toxin of Salmonella typhimurium
Alzogaray, V., Danquah, W., Aguirre, A., Urrutia, M., Berguer, P. M., Véscovi, E. G., Haag, F., Koch‐Nolte, F., & Goldbaum, F. A. (2010) · The FASEB Journal · doi:10.1096/fj.10-162958 · Cited by 41
“With respect to macrophages and other antigen-presenting cells, targeted delivery of SpvB-neutralizing VHHs to the endosomal compart- ment of macrophages might also be achieved by genetic fusion of the nanobody to an antibody specific for an endocytosis receptor such as CD209/DCSIGN (60).”
The pathogen receptor liver and lymph node sinusoidal endotelial cell C‐type lectin is expressed in human Kupffer cells and regulated by PU.1†
Domínguez-Soto, A., Aragoneses‐Fenoll, L., Gómez-Aguado, F., Corcuera, M., Clària, J., García-Monzón, C., Bustos, M., & Corbí, Á. (2008) · Hepatology · doi:10.1002/hep.22678 · Cited by 47
“7, 8 DC-SIGN is expressed on myeloid dendritic cells (DCs), 1, 9 alternatively activated in vitro macrophages, 10 interstitial DCs, 11 a subset of CD14ϩ peripheral blood DCs, 12 and macrophages from various tissues, [13] [14] [15] whereas L-SIGN is exclusively expressed on endothelial cells of the liver, lymph nodes,…”
Background
Identification of the Optimal DC-SIGN Binding Site on Human Immunodeficiency Virus Type 1 gp120
Hong, P. W.-P., Nguyen, S., Young, S., Su, S. V., & Lee, B. (2007) · Journal of Virology · doi:10.1128/jvi.01765-06 · Cited by 45
“While the cis enhancement effect of DC-SIGN appears to be real (11, 28), the trans enhancement effect of DC-SIGN remains controversial, especially with regard to its role in DCmediated viral transfer to T cells (2, 11, 14, 21, 36, 58, 59).”
Background
DC-SIGN–LEF1/TCF1–miR-185 feedback loop promotes colorectal cancer invasion and metastasis
Yuan, M.-L., Zhang, X.-S., Zhang, J., Wang, K., Zhang, Y., Shang, W., Zhang, Y.-N., Cui, J.-Y., Shi, X., Na, H., et al. (2019) · Cell Death and Differentiation · doi:10.1038/s41418-019-0361-2 · Cited by 45
Single nucleotide polymorphisms in immune system genes and their association with clinical symptoms persistence in dengue-infected persons.
Dettogni, R. S., Tristão-Sá, R., dos Santos, M. D., da Silva, F. F., & Louro, I. (2015) · Human Immunology · doi:10.1016/j.humimm.2015.09.026 · Cited by 45
DNA vaccines targeting the encoded antigens to dendritic cells induce potent antitumor immunity in mice
Cao, J., Jin, Y., Li, W., Zhang, B., He, Y., Liu, H., Xia, N., Wei, H., & Yan, J. (2013) · BMC Immunology · doi:10.1186/1471-2172-14-39 · Cited by 45
“tissues [45], and this give perspective for its application”
Background
Newcastle Disease Virus Expressing a Dendritic Cell-Targeted HIV Gag Protein Induces a Potent Gag-Specific Immune Response in Mice
Maamary, J., Array, F., Gao, Q., García-Sastre, A., Steinman, R., Palese, P., & Nchinda, G. (2010) · Journal of Virology · doi:10.1128/jvi.02036-10 · Cited by 45
“DEC205 is an endocytic receptor of the macrophage mannose receptor family and is expressed on DCs in the T cell area of lymphoid organs (15).”
BackgroundSelf-citation
The Polymorphisms in DC-SIGNR Affect Susceptibility to HIV Type 1 Infection
Wichukchinda, N., Kitamura, Y., Rojanawiwat, A., Nakayama, E., Song, H.-H., Pathipvanich, P., Auwanit, W., Sawanpanyalert, P., Iwamoto, A., Shioda, T., et al. (2007) · AIDS Research and Human Retroviruses · doi:10.1089/aid.2006.0212 · Cited by 45
Super Potent Bispecific Llama VHH Antibodies Neutralize HIV via a Combination of gp41 and gp120 Epitopes
Strokappe, N. M., Hock, M., Rutten, L., McCoy, L. E., Back, J. W., Caillat, C., Haffke, M., Weiss, R. A., Weissenhorn, W., & Verrips, T. C. (2019) · Antibodies · doi:10.3390/antib8020038 · Cited by 44
“While antiretroviral therapy and careful clinical management can render HIV a chronic disease, the treatment is expensive and has many adverse effects [1].”
Background
Fungal Surface and Innate Immune Recognition of Filamentous Fungi
Figueiredo, R. T., Carneiro, L. A. M., & Bozza, M. T. (2011) · Frontiers in Microbiology · doi:10.3389/fmicb.2011.00248 · Cited by 43
“(Serrano-Gómez et al., 2004).”
Background
Increased influx of myeloid dendritic cells during acute rejection is associated with interstitial fibrosis and tubular atrophy and predicts poor outcome.
Zuidwijk, K., de Fijter, J., Mallat, M., Eikmans, M., van Groningen, M. V., Goemaere, N., Bajema, I., & van Kooten, C. (2012) · Kidney International · doi:10.1038/ki.2011.289 · Cited by 41
Syndecan-3 in Inflammation and Angiogenesis
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CD205 antigen targeting combined with dendritic cell recruitment factors and antigen-linked CD40L activation primes and expands significant antigen-specific antibody and CD4(+) T cell responses following DNA vaccination of outbred animals.
Njongmeta, L., Bray, J., Davies, C., Davis, W., Howard, C., Hope, J., Palmer, G., Brown, W., & Mwangi, W. (2012) · Vaccine · doi:10.1016/j.vaccine.2011.12.110 · Cited by 40

Authors: Granelli-Piperno, A., Pritsker, A., Pack, M., Shimeliovich, I., Arrighi, J.-F., Park, C. G., Trumpfheller, C., Piguet, V., Moran, T. M., & Steinman, R. M.
Affiliations: Laboratory of Cellular Physiology and Immunology and Chris Browne Center for Immunology and Immune Diseases, Rockefeller University , New York, NY 10021
Icahn School of Medicine at Mount Sinai (US)
Rockefeller University (US)
University Hospital of Geneva (CH)
Corresponding author: Pack, Maggi
Shimeliovich, Irina
Trumpfheller, Christine
ORCID: Shimeliovich, Irina
Park, Chae Gyu
Trumpfheller, Christine
Piguet, Vincent
Moran, Thomas M
Venue: The Journal of Immunology
Publisher: Oxford University Press (OUP)
Published: 2005-10-01
Volume: 175
Issue: 7
Pages: 4265-4273
ISSN: 0022-1767 (ISSN-L)
1550-6606
DOI: 10.4049/jimmunol.175.7.4265
OpenAlex: W1646818583
Cited by: 208
References: 0
Citations by year: 2026: 2 · 2025: 4 · 2024: 3 · 2023: 5 · 2022: 6 · 2021: 7 · 2020: 3 · 2019: 7 · 2018: 3 · 2017: 3 · 2016: 5 · 2015: 3 · 2014: 9 · 2013: 15 · 2012: 15
FWCI: 8.18
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: academic.oup.com/pages/standard-publication-reuse-rights (vor)
Locations: The Journal of Immunology (publishedVersion)
PubMed (publishedVersion)
Digital Commons - RU (Rockefeller University) (submittedVersion)
YUHSpace (Yonsei University Medical Library) (submittedVersion, cc-by-nc-nd)
Funders: National Institutes of Health (2m01rr000102-41)
National Institute of Allergy and Infectious Diseases (R01 AI40045, 5P30AI42848-04, P30AI042848, R01AI040045)
National Center for Research Resources (M01-RR000102, M0-1 RR00102)
Topics: Life Sciences › Immunology and Microbiology › Immunology › Immunotherapy and Immune Responses
Life Sciences › Immunology and Microbiology › Virology › HIV Research and Treatment
Life Sciences › Immunology and Microbiology › Immunology › Immune Response and Inflammation
Keywords: DC-SIGN, C-type lectin, macrophages, lymph nodes, HIV-1 transmission, dendritic cells, mixed lymphocyte reaction, T cell proliferation, IL-4, monocytes
MeSH terms: DC-Specific ICAM-3 Grabbing Nonintegrin, Animals, Antibodies, Monoclonal, Cell Line, Clone Cells, Dendritic Cells, Dogs, Humans, Lymphocyte Culture Test, Mixed, Lymph Nodes, Macrophages, Mice, Inbred BALB C, Receptors, Cell Surface, Recombinant Proteins, T-Lymphocytes, Transfection, HIV-1, Cell Adhesion Molecules, RNA, Small Interfering, Lectins, C-Type, Mice

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Dendritic Cell-Specific Intercellular Adhesion Molecule 3-Grabbing Nonintegrin/CD209 Is Abundant on Macrophages in the Normal Human Lymph Node and Is Not Required for Dendritic Cell Stimulation of the Mixed Leukocyte Reaction

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