[en] Langerhans cells (LC), the immature dendritic cells (DC) that reside in epithelial tissues are among the first immune cells to encounter human papillomavirus (HPV) and are not activated by HPV virus-like particles (VLPs) in contrast to DC. The notion that the differences in response to HPV VLPs between LC and DC are associated with different types of cell binding and intracellular trafficking has been addressed. Inhibition experiments with heparin and sodium chlorate showed that heparan sulfates are necessary for HPV 16 VLPs to bind to DC but not to LC. Electron microscopy analysis demonstrated a colocalization of HPV 16 VLPs and langerin, which is expressed only by LC. This colocalization was observed on the cell surface but also in cytoplasmic vesicles. As anti-langerin antibodies, HPV 16 VLPs were associated with a faster entry kinetics in LC, as reflected by the fact that VLPs were observed near the nuclear membrane of LC within 10 min whereas more than 60 min were needed in DC. However, no difference between LC and DC was observed for the endocytosis pathway. HPV 16 VLPs entered in both DC and LC by a clathrin-dependent-pathway and were then localized in large cytoplasmic vesicles resembling endosomes.
Disciplines :
Immunology & infectious disease Oncology
Author, co-author :
Bousarghin, Latifa
Hubert, Pascale ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Anatomie et cytologie pathologiques
Franzen, Elisabeth
Jacobs, Nathalie ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Anatomie et cytologie pathologiques
Boniver, Jacques ; Centre Hospitalier Universitaire de Liège - CHU > Anatomie pathologique
Delvenne, Philippe ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Anatomie et cytologie pathologiques
Language :
English
Title :
Human papillomavirus 16 virus-like particles use heparan sulfates to bind dendritic cells and colocalize with langerin in Langerhans cells.
Publication date :
2005
Journal title :
Journal of General Virology
ISSN :
0022-1317
eISSN :
1465-2099
Publisher :
Society for General Microbiology, London, United Kingdom
Volume :
86
Issue :
Pt 5
Pages :
1297-305
Peer reviewed :
Peer Reviewed verified by ORBi
Funders :
F.R.S.-FNRS - Fonds de la Recherche Scientifique Fonds Léon Fredericq CAC - Centre anticancéreux près l'Université de Liège asbl Centre de Recherche InterUniversitaire en Vaccinologie (grant Région Wallonne et GSK) Politique Scientifique Fédérale (Belgique) = Belgian Federal Science Policy (IAP)
Bergsdorf, C., Beyer, C., Umansky, V., Werr, M. & Sapp, M. (2003). Highly efficient transport of carboxyfluorescein diacetate succinimidyl ester into COS7 cells using human papillomavirus-like particles. FEBS Lett 536, 120-124.
Bousarghin, L., Combita-Rojas, A. L., Touze, A., El Mehdaoui, S., Sizaret, P. Y., Bravo, M. M. & Coursaget, P. (2002). Detection of neutralizing antibodies against human papillomaviruses (HPV) by inhibition of gene transfer mediated by HPV pseudovirions. J Clin Microbiol 40, 926-932.
Bousarghin, L., Touze, A., Combita-Rojas, A. L. & Coursaget, P. (2003a). Positively charged sequences of human papillomavirus type 16 capsid proteins are sufficient to mediate gene transfer into target cells via the heparan sulfate receptor. J Gen Virol 84, 157-164.
Bousarghin, L., Touze, A., Sizaret, P. Y. & Coursaget, P. (2003b). Human papillomavirus types 16, 31, and 58 use different endocytosis pathways to enter cells. J Virol 77, 3846-3850.
Calore, E. E., Cavaliere, M. J. & Calore, N. M. (1998). Squamous intraepithelial lesions in cervical smears of human immunodeficiency virus-seropositive adolescents. Diagn Cytopathol 18, 91-92.
Chen, L., Ashe, S., Singhal, M. C., Galloway, D. A., Hellstrom, I. & Hellstrom, K. E. (1993). Metastatic conversion of cells by expression of human papillomavirus type 16 E6 and E7 genes. Proc Natl Acad Sci U S A 90, 6523-6527.
Christensen, N. D., Reed, C. A., Cladel, N. M., Hall, K. & Leiserowitz, G. S. (1996). Monoclonal antibodies to HPV-6 L1 virus-like particles identify conformational and linear neutralizing epitopes on HPV-11 in addition to type-specific epitopes on HPV-6. Virology 224, 477-486.
Day, P. M., Lowy, D. R. & Schiller, J. T. (2003). Papillomaviruses infect cells via a clathrin-dependent pathway. Virology 307, 1-11.
Drillien, R., Spehner, D., Bohbot, A. & Hanau, D. (2000). Vaccinia virus-related events and phenotypic changes after infection of dendritic cells derived from human monocytes. Virology 268, 471-481.
Drobni, P., Mistry, N., McMillan, N. & Evander, M. (2003). Carboxy-fluorescein diacetate, succinimidyl ester labeled papillomavirus virus-like particles fluoresce after internalization and interact with heparan sulfate for binding and entry. Virology 310, 163-172.
Ellerbrock, T. V., Chiasson, M. A., Bush, T. J., Sun, X. W., Sawo, D., Brudney, K. & Wright, T. C., Jr (2000). Incidence of cervical squamous intraepithelial lesions in HIV-infected women. JAMA 283, 1031-1037.
Engelmayer, J., Larsson, M., Subklewe, M., Chahroudi, A., Cox, W. I., Steinman, R. M. & Bhardwaj, N. (1999). Vaccinia virus inhibits the maturation of human dendritic cells: a novel mechanism of immune evasion. J Immunol 163, 6762-6768.
Evander, M., Frazer, I. H., Payne, E., Qi, Y. M., Hengst, K. & McMillan, N. A. (1997). Identification of the α 6 integrin as a candidate receptor for papillomaviruses. J Virol 71, 2449-2456.
Evans, T. G., Bonnez, W., Rose, R. C. & 8 other authors (2001). A phase 1 study of a recombinant viruslike particle vaccine against human papillomavirus type 11 in healthy adult volunteers. J Infect Dis 183, 1485-1493.
Farley, J. R., Nakayama, G., Cryns, D. & Segel, I. H. (1978). Adenosine triphosphate sulfurylase from Penicillium chrysogenum equilibrium binding, substrate hydrolysis, and isotope exchange studies. Arch Biochem Biophys 185, 376-390.
Fausch, S. C., Da Silva, D. M., Rudolf, M. P. & Kast, W. M. (2002). Human papillomavirus virus-like particles do not activate Langerhans cells: a possible immune escape mechanism used by human papillomaviruses. J Immunol 169, 3242-3249.
Fausch, S. C., Da Silva, D. M. & Kast, W. M. (2003). Differential uptake and cross-presentation of human papillomavirus virus-like particles by dendritic cells and Langerhans cells. Cancer Res 63, 3478-3482.
Fithian, E., Kung, P., Goldstein, G., Rubenfeld, M., Fenoglio, C. & Edelson, R. (1981). Reactivity of Langerhans cells with hybridoma antibody. Proc Natl Acad Sci U S A 78, 2541-2544.
Gantner, B. N., Simmons, R. M., Canavera, S. J., Akira, S. & Underhill, D. M. (2003). Collaborative induction of inflammatory responses by dectin-1 and toll-like receptor 2. J Exp Med 197, 1107-1117.
Giannini, S. L., Hubert, P., Doyen, J., Boniver, J. & Delvenne, P. (2002). Influence of the mucosal epithelium microenvironment on Langerhans cells: implications for the development of squamous intraepithelial lesions of the cervix. Int J Cancer 97, 654-659.
Giroglou, T., Florin, L., Schafer, F., Streeck, R. E. & Sapp, M. (2001). Human papillomavirus infection requires cell surface heparan sulfate. J Virol 75, 1565-1570.
Grosjean, I., Caux, C., Bella, C., Berger, I., Wild, F., Banchereau, J. & Kaiserlian, D. (1997). Measles virus infects human dendritic cells and blocks their allostimulatory properties for CD4+ T cells. J Exp Med 186, 801-812.
Hagensee, M. E., Yaegashi, N. & Galloway, D. A. (1993). Self-assembly of human papillomavirus type 1 capsids by expression of the L1 protein alone or by coexpression of the L1 and L2 capsid proteins. J Virol 67, 315-322.
Harro, C. D., Pang, Y. Y., Roden, R. B. & 10 other authors (2001). Safety and immunogenicity trial in adult volunteers of a human papillomavirus 16 L1 virus-like particle vaccine. J Natl Cancer Inst 93, 284-292.
Janeway, C. A., Jr & Medzhitov, R. (2002). Innate immune recognition. Annu Rev Immunol 20, 197-216.
Johnson, G. B., Brunn, G. J., Kodaira, Y. & Platt, J. L. (2002). Receptor-mediated monitoring of tissue well-being via detection of soluble heparan sulfate by toll-like receptor 4. J Immunol 168, 5233-5239.
Joyce, J. G., Tung, J. S., Przysiecki, C. T., Cook, J. C., Lehman, E. D., Sands, J. A., Jansen, K. U. & Keller, P. M. (1999). The L1 major capsid protein of human papillomavirus type 11 recombinant virus-like particles interacts with heparin and cell-surface glycosaminoglycans on human keratinocytes. J Biol Chem 274, 5810-5822.
Kirnbauer, R., Taub, J., Greenstone, H., Roden, R., Durst, M., Gissmann, L., Lowy, D. R. & Schiller, J. T. (1993). Efficient self-assembly of human papillomavirus type 16 L1 and L1-L2 into virus-like particles. J Virol 67, 6929-6936.
Kodaira, Y. & Platt, J. L. (2000). Modification of antigen-presenting cell functions by heparan sulfate. Transplant Proc 32, 947.
Koutsky, L. A., Ault, K. A., Wheeler, C. M., Brown, D. R., Barr, E., Alvarez, F. B., Chiacchierini, L. M. & Jansen, K. U. (2002). A controlled trial of a human papillomavirus type 16 vaccine. N Engl J Med 347, 1645-1651.
Lenz, P., Day, P. M., Pang, Y. Y., Frye, S. A., Jensen, P. N., Lowy, D. R. & Schiller, J. T. (2001). Papillomavirus-like particles induce acute activation of dendritic cells. J Immunol 166, 5346-5355.
Matyszak, M. K., Young, J. L. & Gaston, J. S. (2002). Uptake and processing of Chlamydia trachomatis by human dendritic cells. Eur J Immunol 32, 742-751.
McDermott, R., Ziylan, U., Spehner, D. & 9 other authors (2002). Birbeck granules are subdomains of endosomal recycling compartment in human epidermal Langerhans cells, which form where Langerin accumulates. Mol Biol Cell 13, 317-335.
Mummert, M. E., Mummert, D., Edelbaum, D., Hui, F., Matsue, H. & Takashima, A. (2002). Synthesis and surface expression of hyaluronan by dendritic cells and its potential role in antigen presentation. J Immunol 169, 4322-4351.
Narayan, S., Barnard, R. J. & Young, J. A. (2003). Two retroviral entry pathways distinguished by lipid raft association of the viral receptor and differences in viral infectivity. J Virol 77, 1977-1983.
Niedergang, F., Didierlaurent, A., Kraehenbuhl, J. P. & Sirard, J. C. (2004). Dendritic cells: the host Achille's heel for mucosal pathogens? Trends Microbiol 12, 79-88.
Petry, K. U., Scheffel, D., Bode, U. & 7 other authors (1994). Cellular immunodeficiency enhances the progression of human papillomavirus-associated cervical lesions. Int J Cancer 57, 836-840.
Richart, R. M. (1987). Causes and management of cervical intraepithelial neoplasia. Cancer 60, 1951-1959.
Richart, R. M. & Barron, B. A. (1967). The intrauterine device and cervical neoplasia. A prospective study of patients with cervical dysplasia. JAMA 199, 817-819.
Rose, R. C., Bonnez, W., Reichman, R. C. & Garcea, R. L. (1993). Expression of human papillomavirus type 11 L1 protein in insect cells: in vivo and in vitro assembly of viruslike particles. J Virol 67, 1936-1944.
Rudolf, M. P., Fausch, S. C., Da Silva, D. M. & Kast, W. M. (2001). Human dendritic cells are activated by chimeric human papillomavirus type-16 virus-like particles and induce epitope-specific human T cell responses in vitro. J Immunol 166, 5917-5924.
Selinka, H. C., Giroglou, T. & Sapp, M. (2002). Analysis of the infectious entry pathway of human papillomavirus type 33 pseudovirions. Virology 299, 279-287.
Tassaneetrithep, B., Burgess, T. H., Granelli-Piperno, A. & 10 other authors (2003). DC-SIGN (CD209) mediates dengue virus infection of human dendritic cells. J Exp Med 197, 823-829.
Touze, A., El Mehdaoui, S., Sizaret, P. Y., Mougin, C., Munoz, N. & Coursaget, P. (1998). The L1 major capsid protein of human papillomavirus type 16 variants affects yield of virus-like particles produced in an insect cell expression system. J Clin Microbiol 36, 2046-2051.
Turville, S. G., Cameron, P. U., Handley, A., Lin, G., Pohlmann, S., Doms, R. W. & Cunningham, A. L. (2002). Diversity of receptors binding HIV on dendritic cell subsets. Nat Immunol 3, 975-983.
Valladeau, J., Duvert-Frances, V., Pin, J. J. & 9 other authors (1999). The monoclonal antibody DCGM4 recognizes Langerin, a protein specific of Langerhans cells, and is rapidly internalized from the cell surface. Eur J Immunol 29, 2695-2704.
Valladeau, J., Ravel, O., Dezutter-Dambuyant, C. & 10 other authors (2000). Langerin, a novel C-type lectin specific to Langerhans cells, is an endocytic receptor that induces the formation of Birbeck granules. Immunity 12, 71-81.
Wrenshall, L. E., Cerra, F. B., Carlson, A., Bach, F. H. & Platt, J. L. (1991). Regulation of murine splenocyte responses by heparan sulfate. J Immunol 147, 455-459.
Yan, M., Peng, J., Jabbar, I. A., Liu, X., Filgueira, L., Frazer, I. H. & Thomas, R. (2004). Despite differences between dendritic cells and Langerhans cells in the mechanism of papillomavirus-like particle antigen uptake, both cells cross-prime T cells. Virology 324, 297-310.
