Presentation of lipopeptide by dendritic cells induces anti-tumor responses via an endocytosis-independent pathway in vivo

Journal of Leukocyte Biology

Volumn 90, Issue 2, 2011, Pages 323-332

  Song, Ying Chyi ^a   Chou, Ai Hsiang ^a   Homhuan, Atthachai ^a   Huang, Ming Hsi ^a   Chiang, Sheng Kuo ^a   Shen, Kuan Yin ^a   Chuang, Po Wei ^a   Leng, Chih Hsiang ^a,b   Tao, Mi Hua ^c   Chong, Pele ^a,b   Liu, Shih Jen ^a,b  

^a NATIONAL HEALTH RESEARCH INSTITUTES   (Taiwan)

^b CHINA MEDICAL UNIVERSITY   (Taiwan)

^c ACADEMIA SINICA   (Taiwan)

Author keywords

Cross presentation; Lymphoid; T cell

Indexed keywords

FLUORESCEIN ISOTHIOCYANATE; LIPOPEPTIDE;

ACTIN FILAMENT; ANIMAL CELL; ANTINEOPLASTIC ACTIVITY; ARTICLE; BARE LYMPHOCYTE SYNDROME; CANCER IMMUNIZATION; CD8+ T LYMPHOCYTE; CELL DEGENERATION; CONTROLLED STUDY; DENDRITIC CELL; DEPOLYMERIZATION; ENDOCYTOSIS; ENDOSOME; HUMAN; HUMAN CELL; IN VIVO CULTURE; LEUKEMIA CELL LINE; LOW TEMPERATURE; MICROTUBULE; MOUSE; NONHUMAN; PRIORITY JOURNAL; TUMOR;

ANTIGEN PRESENTATION; CD8-POSITIVE T-LYMPHOCYTES; DENDRITIC CELLS; ENDOCYTOSIS; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; JURKAT CELLS; LIPOPEPTIDES; LYMPHOCYTE ACTIVATION; NEOPLASMS; PROTEASOME ENDOPEPTIDASE COMPLEX;

EID: 79961077781     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.0111046     Document Type: Article

References (39)

1. Burgdorf, S., Scholz, C., Kautz, A., Tampe, R., Kurts, C. (2008) Spatial and mechanistic separation of cross-presentation and endogenous antigen presentation. Nat. Immunol. 9, 558-566.
2. Rock, K. L., Shen, L. (2005) Cross-presentation: underlying mechanisms and role in immune surveillance. Immunol. Rev. 207, 166-183.
3. Amigorena, S., Savina, A. (2010) Intracellular mechanisms of antigen cross presentation in dendritic cells. Curr. Opin. Immunol. 22, 109-117.
4. Norbury, C. C., Basta, S., Donohue, K. B., Tscharke, D. C., Princiotta, M. F., Berglund, P., Gibbs, J., Bennink, J. R., Yewdell, J. W. (2004) CD8 + T cell cross-priming via transfer of proteasome substrates. Science 304, 1318-1321.
5. Palmowski, M. J., Gileadi, U., Salio, M., Gallimore, A., Millrain, M., James, E., Addey, C., Scott, D., Dyson, J., Simpson, E., Cerundolo, V. (2006) Role of immunoproteasomes in cross-presentation. J. Immunol. 177, 983-990.
6. Shen, L., Sigal, L. J., Boes, M., Rock, K. L. (2004) Important role of cathepsin S in generating peptides for TAP-independent MHC class I crosspresentation in vivo. Immunity 21, 155-165.
7. Belizaire, R., Unanue, E. R. (2009) Targeting proteins to distinct subcellular compartments reveals unique requirements for MHC class I and II presentation. Proc. Natl. Acad. Sci. USA 106, 17463-17468.
8. BenMohamed, L., Wechsler, S. L., Nesburn, A. B. (2002) Lipopeptide vaccines-yesterday, today, and tomorrow. Lancet Infect. Dis. 2, 425-431.
9. Moyle, P. M., Toth, I. (2008) Self-adjuvanting lipopeptide vaccines. Curr. Med. Chem. 15, 506-516.
10. Verheul, A. F., Udhayakumar, V., Jue, D. L., Wohlhueter, R. M., Lal, A. A. (1995) Monopalmitic acid-peptide conjugates induce cytotoxic T cell responses against malarial epitopes: importance of spacer amino acids. J. Immunol. Methods 182, 219-226.
11. Zhang, X., Issagholian, A., Berg, E. A., Fishman, J. B., Nesburn, A. B., BenMohamed, L. (2005) Th-cytotoxic T-lymphocyte chimeric epitopes extended by N+-palmitoyl lysines induce herpes simplex virus type 1-specific effector CD8+ Tc1 responses and protect against ocular infection. J. Virol. 79, 15289-15301.
12. Zhu, X., Ramos, T. V., Gras-Masse, H., Kaplan, B. E., BenMohamed, L. (2004) Lipopeptide epitopes extended by an N+-palmitoyl-lysine moiety increase uptake and maturation of dendritic cells through a Toll-like receptor-2 pathway and trigger a Th1-dependent protective immunity. Eur. J. Immunol. 34, 3102-3114.
13. Andrieu, M., Loing, E., Desoutter, J. F., Connan, F., Choppin, J., Gras- Masse, H., Hanau, D., Dautry-Varsat, A., Guillet, J. G., Hosmalin, A. (2000) Endocytosis of an HIV-derived lipopeptide into human dendritic cells followed by class I-restricted CD8(+) T lymphocyte activation. Eur. J. Immunol. 30, 3256-3265.
14. Coutsinos, Z., Villefroy, P., Gras-Masse, H., Guillet, J. G., Bourgault-Villada, I. (2005) Evaluation of SIV-lipopeptide immunizations administered by the intradermal route in their ability to induce antigen specific T-cell responses in rhesus macaques. FEMS Immunol. Med. Microbiol. 43, 357-366.
15. Gahéry-Ségard, H., Pialoux, G., Charmeteau, B., Sermet, S., Poncelet, H., Raux, M., Tartar, A., Levy, J. P., Gras-Masse, H., Guillet, J. G. (2000) Multiepitopic B- and T-cell responses induced in humans by a human immunodeficiency virus type 1 lipopeptide vaccine. J. Virol. 74, 1694-1703.
16. Gahéry-Ségard, H., Pialoux, G., Figueiredo, S., Igea, C., Surenaud, M., Gaston, J., Gras-Masse, H., Levy, J. P., Guillet, J. G. (2003) Long-term specific immune responses induced in humans by a human immunodeficiency virus type 1 lipopeptide vaccine: characterization of CD8+-T-cell epitopes recognized. J. Virol. 77, 11220-11231.
17. Pialoux, G., Quercia, R. P., Gahery, H., Daniel, N., Slama, L., Girard, P. M., Bonnard, P., Rozenbaum, W., Schneider, V., Salmon, D., Guillet, J. G. (2008) Immunological responses and long-term treatment interruption after human immunodeficiency virus type 1 (HIV-1) lipopeptide immunization of HIV-1-infected patients: the LIPTHERA study. Clin. Vaccine Immunol. 15, 562-568.
18. Gahery, H., Daniel, N., Charmeteau, B., Ourth, L., Jackson, A., Andrieu, M., Choppin, J., Salmon, D., Pialoux, G., Guillet, J. G. (2006) New CD4+ and CD8+ T cell responses induced in chronically HIV type-1-infected patients after immunizations with an HIV type 1 lipopeptide vaccine. AIDS Res. Hum. Retroviruses 22, 684-694.
19. Chen, W., Huang, L. (2008) Induction of cytotoxic T-lymphocytes and antitumor activity by a liposomal lipopeptide vaccine. Mol. Pharm. 5, 464-471.
20. Hoeffel, G., Ripoche, A. C., Matheoud, D., Nascimbeni, M., Escriou, N., Lebon, P., Heshmati, F., Guillet, J. G., Gannage, M., Caillat-Zucman, S., Casartelli, N., Schwartz, O., De la Salle, H., Hanau, D., Hosmalin, A., Maranõń, C. (2007) Antigen crosspresentation by human plasmacytoid dendritic cells. Immunity 27, 481-492.
21. Hosmalin, A., Andrieu, M., Loing, E., Desoutter, J. F., Hanau, D., Gras- Masse, H., Dautry-Varsat, A., Guillet, J. G. (2001) Lipopeptide presentation pathway in dendritic cells. Immunol. Lett. 79, 97-100.
22. Andrieu, M., Desoutter, J. F., Loing, E., Gaston, J., Hanau, D., Guillet, J. G., Hosmalin, A. (2003) Two human immunodeficiency virus vaccinal lipopeptides follow different cross-presentation pathways in human dendritic cells. J. Virol. 77, 1564-1570.
23. Gras-Masse, H. (2001) Single-chain lipopeptide vaccines for the induction of virus-specific cytotoxic T cell responses in randomly selected populations. Mol. Immunol. 38, 423-431.
24. Loing, E., Andrieu, M., Thiam, K., Schorner, D., Wiesmuller, K. H., Hosmalin, A., Jung, G., Gras-Masse, H. (2000) Extension of HLA-A*0201-restricted minimal epitope by N +-palmitoyl-lysine increases the life span of functional presentation to cytotoxic T cells. J. Immunol. 164, 900-907.
25. Babu, J. S., Nair, S., Kanda, P., Rouse, B. T. (1995) Priming for virus-specific CD8+ but not CD4+ cytotoxic T lymphocytes with synthetic lipopeptide is influenced by acylation units and liposome encapsulation. Vaccine 13, 1669-1676.
26. Chen, H. W., Liu, S. J., Liu, H. H., Kwok, Y., Lin, C. L., Lin, L. H., Chen, M. Y., Tsai, J. P., Chang, L. S., Chiu, F. F., Lai, L. W., Lian, W. C., Yang, C. Y., Hsieh, S. Y., Chong, P., Leng, C. H. (2009) A novel technology for the production of a heterologous lipoprotein immunogen in high yield has implications for the field of vaccine design. Vaccine 27, 1400-1409.
27. Song, Y. C., Sun, G. H., Lee, T. P., Huang, J. C., Yu, C. L., Chen, C. H., Tang, S. J., Sun, K. H. (2008) Arginines in the CDR of anti-dsDNA autoantibodies facilitate cell internalization via electrostatic interactions. Eur. J. Immunol. 38, 3178-3190.
28. Chen, H. W., Leng, C. H., Liu, H. Y., Cheng, W. F., Chang, Y. W., Wu, P. Y., Lien, S. P., Huang, T. Y., Chiang, S. K., Lin, M. H., Tao, M. H., Chong, P., Liu, S. J. (2009) Identification of HLA-A11-restricted CTL epitopes derived from HPV type 18 using DNA immunization. Cancer Biol. Ther. 8, 2025-2032.
29. Jutras, I., Desjardins, M. (2005) Phagocytosis: at the crossroads of innate and adaptive immunity. Annu. Rev. Cell Dev. Biol. 21, 511-527.
30. Hans, D., Young, P. R., Fairlie, D. P. (2006) Current status of short synthetic peptides as vaccines. Med. Chem. 2, 627-646.
31. van der Burg, S. H., Bijker, M. S., Welters, M. J., Offringa, R., Melief, C. J. (2006) Improved peptide vaccine strategies, creating synthetic artificial infections to maximize immune efficacy. Adv. Drug Deliv. Rev. 58, 916-930.
32. Ye, Z., Gan, Y. H. (2007) Flagellin contamination of recombinant heat shock protein 70 is responsible for its activity on T cells. J. Biol. Chem. 282, 4479-4484.
33. Pfender, N. A., Grosch, S., Roussel, G., Koch, M., Trifilieff, E., Greer, J. M. (2008) Route of uptake of palmitoylated encephalitogenic peptides of myelin proteolipid protein by antigen-presenting cells: importance of the type of bond between lipid chain and peptide and relevance to autoimmunity. J. Immunol. 180, 1398-1404.
34. Stittelaar, K. J., Hoogerhout, P., Ovaa, W., van Binnendijk, R. R., Poelen, M. C., Roholl, P., van Els, C. A., Osterhaus, A. D., Wiertz, E. J. (2001) In vitro processing and presentation of a lipidated cytotoxic T-cell epitope derived from measles virus fusion protein. Vaccine 20, 249-261.
35. BenMohamed, L., Belkaid, Y., Loing, E., Brahimi, K., Gras-Masse, H., Druilhe, P. (2002) Systemic immune responses induced by mucosal administration of lipopeptides without adjuvant. Eur. J. Immunol. 32, 2274-2281.
36. Tsunoda, I., Sette, A., Fujinami, R. S., Oseroff, C., Ruppert, J., Dahlberg, C., Southwood, S., Arrhenius, T., Kuang, L. Q., Kubo, R. T., Chesnut, R. W., Ishioka, G. Y. (1999) Lipopeptide particles as the immunologically active component of CTL inducing vaccines. Vaccine 17, 675-685.
37. Jancic, C., Savina, A., Wasmeier, C., Tolmachova, T., El-Benna, J., Dang, P. M., Pascolo, S., Gougerot-Pocidalo, M. A., Raposo, G., Seabra, M. C., Amigorena, S. (2007) Rab27a regulates phagosomal pH and NADPH oxidase recruitment to dendritic cell phagosomes. Nat. Cell Biol. 9, 367-378.
38. Xu, D. H., Zhou, C. H., Xia, Y. P., Qiu, Z. Y., Wu, Y. Z., Jia, Z. C., Zhou, W. (2007) Cytotoxic T lymphocyte response induced by an improved synthetic lipopeptide vaccine against cervical cancer. Acta Pharmacol. Sin. 28, 695-702.
39. Fu, N., Khan, S., Quinten, E., de Graaf, N., Pemberton, A. J., Rivett, A. J., Melief, C. J., Ossendorp, F. (2009) Effective CD8(+) T cell priming and tumor protection by enterotoxin B subunit-conjugated peptides targeted to dendritic cells. Vaccine 27, 5252-5258.