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Science 305 (5687): 1153-1157

Copyright © 2004 by the American Association for the Advancement of Science

Enhanced Dendritic Cell Antigen Capture via Toll-Like Receptor-Induced Actin Remodeling

Michele A. West,1* Robert P. A. Wallin,1,2,3* Stephen P. Matthews,1 Henrik G. Svensson,1 Rossana Zaru,1 Hans-Gustaf Ljunggren,3 Alan R. Prescott,1 Colin Watts1{dagger}

Abstract: Microbial products are sensed through Toll-like receptors (TLRs) and trigger a program of dendritic cell (DC) maturation that enables DCs to activate T cells. Although an accepted hallmark of this response is eventual down-regulation of DC endocytic capacity, we show that TLR ligands first acutely stimulate antigen macropinocytosis, leading to enhanced presentation on class I and class II major histocompatibility complex molecules. Simultaneously, actin-rich podosomes disappear, which suggests a coordinated redeployment of actin to fuel endocytosis. These reciprocal changes are transient and require p38 and extracellular signal–regulated kinase activation. Thus, the DC actin cytoskeleton can be rapidly mobilized in response to innate immune stimuli to enhance antigen capture and presentation.

1 Division of Cell Biology and Immunology, Wellcome Trust Biocentre, School of Life Sciences, University of Dundee, Dundee DD1 5EH, UK.
2 Microbiology and Tumor Biology Center, Karolinska Institutet, Stockholm, Sweden.
3 Center for Infectious Medicine, Department of Medicine, Karolinska Institutet, Karolinska University Hospital, Stockholm, Sweden.

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* These authors contributed equally to this work.

{dagger} To whom correspondence should be addressed. E-mail: c.watts{at}dundee.ac.uk


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S. F. G. van Helden, D. J. E. B. Krooshoop, K. C. M. Broers, R. A. P. Raymakers, C. G. Figdor, and F. N. van Leeuwen (2006)
J. Immunol. 177, 1567-1574
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ICSBP/IRF-8 differentially regulates antigen uptake during dendritic-cell development and affects antigen presentation to CD4+ T cells.
F. Mattei, G. Schiavoni, P. Borghi, M. Venditti, I. Canini, P. Sestili, I. Pietraforte, H. C. Morse III, C. Ramoni, F. Belardelli, et al. (2006)
Blood 108, 609-617
   Abstract »    Full Text »    PDF »
Inhibition of calpain stabilises podosomes and impairs dendritic cell motility.
Y. Calle, N. O. Carragher, A. J. Thrasher, and G. E. Jones (2006)
J. Cell Sci. 119, 2375-2385
   Abstract »    Full Text »    PDF »
A transforming growth factor-beta-induced protein stimulates endocytosis and is up-regulated in immature dendritic cells.
W. Cao, P. Tan, C. H. Lee, H. Zhang, and J. Lu (2006)
Blood 107, 2777-2785
   Abstract »    Full Text »    PDF »
Protection against Heterologous Burkholderia pseudomallei Strains by Dendritic Cell Immunization.
S. J. Elvin, G. D. Healey, A. Westwood, S. C. Knight, J. E. Eyles, and E. D. Williamson (2006)
Infect. Immun. 74, 1706-1711
   Abstract »    Full Text »    PDF »
A Polymeric Bacterial Protein Activates Dendritic Cells via TLR4.
P. M. Berguer, J. Mundinano, I. Piazzon, and F. A. Goldbaum (2006)
J. Immunol. 176, 2366-2372
   Abstract »    Full Text »    PDF »
Discovery of novel immunostimulants by dendritic-cell-based functional screening.
N. Mizumoto, J. Gao, H. Matsushima, Y. Ogawa, H. Tanaka, and A. Takashima (2005)
Blood 106, 3082-3089
   Abstract »    Full Text »    PDF »
Virus-Induced Inhibition of CD1d1-Mediated Antigen Presentation: Reciprocal Regulation by p38 and ERK.
G. J. Renukaradhya, T. J. R. Webb, M. A. Khan, Y. L. Lin, W. Du, J. Gervay-Hague, and R. R. Brutkiewicz (2005)
J. Immunol. 175, 4301-4308
   Abstract »    Full Text »    PDF »
Chloroquine enhances human CD8+ T cell responses against soluble antigens in vivo.
D. Accapezzato, V. Visco, V. Francavilla, C. Molette, T. Donato, M. Paroli, M. U. Mondelli, M. Doria, M. R. Torrisi, and V. Barnaba (2005)
J. Exp. Med. 202, 817-828
   Abstract »    Full Text »    PDF »
Chaperon and Adjuvant Activity of hsp70: Different Natural Killer Requirement for Cross-Priming of Chaperoned and Bystander Antigens.
C. Massa, C. Melani, and M. P. Colombo (2005)
Cancer Res. 65, 7942-7949
   Abstract »    Full Text »    PDF »
B7-DC cross-linking restores antigen uptake and augments antigen-presenting cell function by matured dendritic cells.
S. Radhakrishnan, E. Celis, and L. R. Pease (2005)
PNAS 102, 11438-11443
   Abstract »    Full Text »    PDF »
Response to Staphylococcus aureus requires CD36-mediated phagocytosis triggered by the COOH-terminal cytoplasmic domain.
L. M. Stuart, J. Deng, J. M. Silver, K. Takahashi, A. A. Tseng, E. J. Hennessy, R. A. B. Ezekowitz, and K. J. Moore (2005)
J. Cell Biol. 170, 477-485
   Abstract »    Full Text »    PDF »
Asparagine Deamidation Perturbs Antigen Presentation on Class II Major Histocompatibility Complex Molecules.
C. X. Moss, S. P. Matthews, D. J. Lamont, and C. Watts (2005)
J. Biol. Chem. 280, 18498-18503
   Abstract »    Full Text »    PDF »
Saturated and Polyunsaturated Fatty Acids Reciprocally Modulate Dendritic Cell Functions Mediated through TLR4.
A. R. Weatherill, J. Y. Lee, L. Zhao, D. G. Lemay, H. S. Youn, and D. H. Hwang (2005)
J. Immunol. 174, 5390-5397
   Abstract »    Full Text »    PDF »
Clearance of apoptotic neurons without inflammation by microglial triggering receptor expressed on myeloid cells-2.
K. Takahashi, C. D.P. Rochford, and H. Neumann (2005)
J. Exp. Med. 201, 647-657
   Abstract »    Full Text »    PDF »

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