Abstract
Early interactions between lung dendritic cells (LDCs) and Mycobacterium tuberculosis, the etiological agent of tuberculosis, are thought to be critical for mounting a protective anti-mycobacterial immune response and for determining the outcome of infection. However, these interactions are poorly understood, at least at the molecular level. Here we show that M. tuberculosis enters human monocyte-derived DCs after binding to the recently identified lectin DC-specific intercellular adhesion molecule-3 grabbing nonintegrin (DC-SIGN). By contrast, complement receptor (CR)3 and mannose receptor (MR), which are the main M. tuberculosis receptors on macrophages (Mphis), appeared to play a minor role, if any, in mycobacterial binding to DCs. The mycobacteria-specific lipoglycan lipoarabinomannan (LAM) was identified as a key ligand of DC-SIGN. Freshly isolated human LDCs were found to express DC-SIGN, and M. tuberculosis-derived material was detected in CD14(-)HLA-DR(+)DC-SIGN(+) cells in lymph nodes (LNs) from patients with tuberculosis. Thus, as for human immunodeficiency virus (HIV), which is captured by the same receptor, DC-SIGN-mediated entry of M. tuberculosis in DCs in vivo is likely to influence bacterial persistence and host immunity.
MeSH Terms
Antigens, CD
Cell Adhesion Molecules/metabolism
Dendritic Cells/cytology,immunology,metabolism
Flow Cytometry
HeLa Cells
Humans
Immunoglobulins/metabolism
Lectins, C-Type/metabolism
Lipopolysaccharides/metabolism
Lung/cytology,immunology,pathology
Macrophage-1 Antigen/metabolism
Mannose Receptor
Mannose-Binding Lectins
Membrane Glycoproteins/metabolism
Monocytes/cytology
Mycobacterium tuberculosis/immunology,physiology
Receptors, Cell Surface/metabolism
Time Factors
Tuberculosis/immunology,metabolism,microbiology
Chemicals
Antigens, CD
CD83 antigen
Cell Adhesion Molecules
DC-specific ICAM-3 grabbing nonintegrin
Immunoglobulins
Lectins, C-Type
Lipopolysaccharides
Macrophage-1 Antigen
Mannose Receptor
Mannose-Binding Lectins
Membrane Glycoproteins
Receptors, Cell Surface
lipoarabinomannan
Authors & Affiliations
13 authors, click to expand affiliations / ORCID
Tailleux Ludovic
INSERM EMI-0013 Institut Universitaire d'Hématologie, Assistance Publique-Hôpitaux de Paris, France.
Schwartz Olivier
Herrmann Jean-Louis
Pivert Elisabeth
Jackson Mary
Amara Ali
Legres Luc
Dreher Donatus
Nicod Laurent P
Gluckman Jean Claude
Lagrange Philippe H
Gicquel Brigitte
Neyrolles Olivier
References (31)
31 references, click to expand
-
Human lung dendritic cells have an immature phenotype with efficient mannose receptors.
Am J Respir Cell Mol Biol. 1999 Nov;21(5):547-54
PMID: 10536111
-
Host defense mechanisms triggered by microbial lipoproteins through toll-like receptors.
Science. 1999 Jul 30;285(5428):732-6
PMID: 10426995
-
Identification of DC-SIGN, a novel dendritic cell-specific ICAM-3 receptor that supports primary immune responses.
Cell. 2000 Mar 3;100(5):575-85
PMID: 10721994
-
DC-SIGN, a dendritic cell-specific HIV-1-binding protein that enhances trans-infection of T cells.
Cell. 2000 Mar 3;100(5):587-97
PMID: 10721995
-
Intersection of group I CD1 molecules and mycobacteria in different intracellular compartments of dendritic cells.
J Immunol. 2000 May 1;164(9):4843-52
PMID: 10779793
-
Essential role for cholesterol in entry of mycobacteria into macrophages.
Science. 2000 Jun 2;288(5471):1647-50
PMID: 10834844
-
IL-10 converts human dendritic cells into macrophage-like cells with increased antibacterial activity against virulent Mycobacterium tuberculosis.
J Immunol. 2000 Jul 15;165(2):978-87
PMID: 10878374
-
Antigen presentation in the lung.
Am J Respir Crit Care Med. 2000 Oct;162(4 Pt 2):S151-6
PMID: 11029385
-
Fate of Mycobacterium tuberculosis within murine dendritic cells.
Infect Immun. 2001 Feb;69(2):800-9
PMID: 11159971
-
Immunology of tuberculosis.
Annu Rev Immunol. 2001;19:93-129
PMID: 11244032
-
Mycobacterium tuberculosis: here today, and here tomorrow.
Nat Rev Mol Cell Biol. 2001 Aug;2(8):569-77
PMID: 11483990
-
Dendritic cells: specialized and regulated antigen processing machines.
Cell. 2001 Aug 10;106(3):255-8
PMID: 11509172
-
cis Expression of DC-SIGN allows for more efficient entry of human and simian immunodeficiency viruses via CD4 and a coreceptor.
J Virol. 2001 Dec;75(24):12028-38
PMID: 11711593
-
Structural basis for selective recognition of oligosaccharides by DC-SIGN and DC-SIGNR.
Science. 2001 Dec 7;294(5549):2163-6
PMID: 11739956
-
Dendritic cells are host cells for mycobacteria in vivo that trigger innate and acquired immunity.
J Immunol. 2002 Feb 1;168(3):1294-301
PMID: 11801668
-
HIV-1 Nef-induced upregulation of DC-SIGN in dendritic cells promotes lymphocyte clustering and viral spread.
Immunity. 2002 Jan;16(1):145-55
PMID: 11825573
-
Constitutive and induced expression of DC-SIGN on dendritic cell and macrophage subpopulations in situ and in vitro.
J Leukoc Biol. 2002 Mar;71(3):445-57
PMID: 11867682
-
DC-SIGN (CD209) expression is IL-4 dependent and is negatively regulated by IFN, TGF-beta, and anti-inflammatory agents.
J Immunol. 2002 Mar 15;168(6):2634-43
PMID: 11884427
-
How can immunology contribute to the control of tuberculosis?
Nat Rev Immunol. 2001 Oct;1(1):20-30
PMID: 11905811
-
C-type lectin receptors on dendritic cells and Langerhans cells.
Nat Rev Immunol. 2002 Feb;2(2):77-84
PMID: 11910898
-
Mouse and human dendritic cell subtypes.
Nat Rev Immunol. 2002 Mar;2(3):151-61
PMID: 11913066
-
Dendritic cell (DC)-specific intercellular adhesion molecule 3 (ICAM-3)-grabbing nonintegrin (DC-SIGN, CD209), a C-type surface lectin in human DCs, is a receptor for Leishmania amastigotes.
J Biol Chem. 2002 Sep 27;277(39):36766-9
PMID: 12122001
-
Lipoarabinomannan of Mycobacterium tuberculosis. Capping with mannosyl residues in some strains.
J Biol Chem. 1992 Mar 25;267(9):6234-9
PMID: 1556132
-
Macrophage phagocytosis of virulent but not attenuated strains of Mycobacterium tuberculosis is mediated by mannose receptors in addition to complement receptors.
J Immunol. 1993 Apr 1;150(7):2920-30
PMID: 8454864
-
Dendritic cell progenitors phagocytose particulates, including bacillus Calmette-Guerin organisms, and sensitize mice to mycobacterial antigens in vivo.
J Exp Med. 1993 Aug 1;178(2):479-88
PMID: 7688024
-
Activation of human dendritic cells following infection with Mycobacterium tuberculosis.
J Immunol. 1997 Jul 15;159(2):635-43
PMID: 9218578
-
A macrophage invasion mechanism of pathogenic mycobacteria.
Science. 1997 Aug 22;277(5329):1091-3
PMID: 9262476
-
Macrophage receptors for Mycobacterium tuberculosis.
Infect Immun. 1998 Apr;66(4):1277-81
PMID: 9529042
-
Molecular interaction of CD1b with lipoglycan antigens.
Immunity. 1998 Mar;8(3):331-40
PMID: 9529150
-
Interactions between Mycobacterium tuberculosis and host cells: are mycobacterial sugars the key?
Trends Microbiol. 1998 Aug;6(8):328-35
PMID: 9746944
-
Surfactant protein D binds to Mycobacterium tuberculosis bacilli and lipoarabinomannan via carbohydrate-lectin interactions resulting in reduced phagocytosis of the bacteria by macrophages.
J Immunol. 1999 Jul 1;163(1):312-21
PMID: 10384130