Differential cytosolic delivery and presentation of antigen by listeriolysin O-liposomes to macrophages and dendritic cells

Molecular Pharmaceutics

Volumn 2, Issue 1, 2005, Pages 74-82

  Stier, Ethan M ^a,b   Mandal, Manas ^a,c   Lee, Kyung Dall ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

^b CENTER FOR DRUG EVALUATION AND RESEARCH   (United States)

^c CENTER FOR MOLECULAR MEDICINE AND INFECTIOUS DISEASES   (United States)

Author keywords

Antigen delivery; Dendritic cells; Liposomes; Listeriolysin O; Macrophages; MHC I

Indexed keywords

ANTIGEN; CD8 ANTIGEN; LIPOSOME; LISTERIOLYSIN; LISTERIOLYSIN O; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIGEN PRESENTATION; ANTIGEN PRESENTING CELL; ARTICLE; CYTOSOL; DENDRITIC CELL; ENDOSOME; FEMALE; IMMUNE RESPONSE; LISTERIA MONOCYTOGENES; LYSOSOME; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE;

ANIMALS; ANTIGEN PRESENTATION; ANTIGEN-PRESENTING CELLS; BACTERIAL TOXINS; CELLS, CULTURED; CYTOSOL; DENDRITIC CELLS; DRUG DELIVERY SYSTEMS; FEMALE; FLOW CYTOMETRY; HEAT-SHOCK PROTEINS; HEMOLYSIN PROTEINS; HYBRIDOMAS; LIPOSOMES; MACROPHAGES; MICE; MICE, INBRED C57BL; RECOMBINANT PROTEINS; T-LYMPHOCYTES;

EID: 14644423915     PISSN: 15438384     EISSN: None     Source Type: Journal    
DOI: 10.1021/mp049896v     Document Type: Article

References (43)

1. Oldstone, M. The role of cytotoxic T lymphocytes in infectious disease: History, criteria, and state of the art. Curr. Top. Microbiol. Immunol. 1994, 189, 1-8.
2. Rock, K. L.; Goldberg, A. L. Degradation of cell proteins and the generation of MHC class I-presented peptides. Annu. Rev. Immunol. 1999, 17, 739-779.
3. San Mateo, L. R.; Chua, M. M.; Weiss, S. R.; Shen, H. Perforin-mediated CTL cytolysis counteracts direct cell-cell spread of Listeria monocytogenes. J. Immunol. 2002, 169, 5202-5208.
4. Shimizu, K.; Thomas, E. K.; Giedlin, M.; Mule, J. J. Enhancement of tumor lysate- and peptide-pulsed dendritic cell-based vaccines by the addition of foreign helper protein. Cancer Res. 2001, 61, 2618-2624.
5. Germain, R. N. MHC-dependent antigen processing and peptide presentation, providing ligands for T lymphocyte activation. Cell 1994, 76, 287-299.
6. Provoda, C. J.; Lee, K. D. Bacterial pore-forming hemolysins and their use in the cytosolic delivery of macromolecules. Adv. Drug Delivery Rev. 2000, 41, 209-221.
7. York, I. A.; Goldberg, A. L.; Mo, X. Y.; Rock, K. L. Proteolysis and class I major histocompatibility complex antigen presentation. Immunol. Rev. 1999, 172, 49-66.
8. Moore, M. W.; Carbone, F. R.; Bevan, M. J. Introduction of soluble protein into the class I pathway of antigen processing and presentation. Cell 1988, 54, 777-785.
9. Harding, C. V.; Collins, D. S.; Kanagawa, O.; Unanue, E. R. Liposome-encapsulated antigens engender lysosomal processing for class II MHC presentation and cytosolic processing for class I presentation. J. Immunol. 1991, 147, 2860-2863.
10. Nair, S.; Zhou, F.; Reddy, R.; Huang, L.; Rouse, B. T. Soluble proteins delivered to dendritic cells via pH-sensitive liposomes induce primary cytotoxic T lymphocyte responses in vitro. J. Exp. Med. 1992, 175, 609-612.
11. Kovacsovics-Bankowski, M.; Clark, K.; Benacerraf, B.; Rock, K. L. Efficient major histocompatibility complex class I presentation of exogenous antigen upon phagocytosis by macrophages. Proc. Natl. Acad. Sci. U.S.A. 1993, 90, 4942-4946.
12. Lee, K. D.; Oh, Y. K.; Portnoy, D. A.; Swanson, J. A. Delivery of macromolecules into cytosol using liposomes containing hemolysin from Listeria monocytogenes. J. Biol. Chem. 1996, 271, 7249-7252.
13. Mandal, M.; Lee, K. D. Listeriolysin O-liposome-mediated cytosolic delivery of macromolecule antigen in vivo, enhancement of antigen-specific cytotoxic T lymphocyte frequency, activity, and tumor protection. Biochim. Biophys. Acta 2002, 1563, 7-17.
14. Portnoy, D. A.; Auerbuch, V.; Glomski, I. J. The cell biology of Listeria monocytogenes infection, the intersection of bacterial pathogenesis and cell-mediated immunity. J. Cell Biol. 2002, 158, 409-414.
15. Portnoy, D. A.; Jone, S. The cell biology of Listeria monocytogenes infection (escape from a vacuole). Ann. N.Y. Acad. Sci. 1994, 730, 15-25.
16. Beauregard, K. E.; Lee, K. D.; Collier, R. J.; Swanson, J. A. pH-dependent perforation of macrophage phagosomes by listeriolysin O from Listeria monocytogenes. J. Exp. Med. 1997, 186, 1159-1163.
17. Banchereau, J.; Briere, F.; Caux, C.; Davoust, J.; Lebecque, S.; Liu, Y. J.; Pulendran, B.; Palucka, K. Immunobiology of dendritic cells. Annu. Rev. Immunol. 2000, 18, 767-811.
18. Mellman, I.; Turley, S. J.; Steinman, R. M. Antigen processing for amateurs and professionals. Trends Cell Biol. 1998, 8, 231-237.
19. Papahadjopoulos, D.; Allen, T. M.; Gabizon, A.; Mayhew, E.; Matthay, K.; Huang, S. K.; Lee, K. D.; Woodle, M. C.; Lasic, D. D.; Redemann, C.; et al. Sterically stabilized liposomes, improvements in pharmacokinetics and antitumor therapeutic efficacy. Proc. Natl. Acad. Sci. U.S.A. 1991, 88, 11460-11464.
20. Harshyne, L. A.; Watkins, S. C.; Gambotto, A.; Barratt-Boyes, S. M. Dendritic cells acquire antigens from live cells for cross-presentation to CTL. J. Immunol. 2001, 166, 3717-3723.
21. Harding, C. V. Techniques for studying phagocytic processing of bacteria for class I or II MHC-restricted antigen recognition by T lymphocytes. Methods Cell Biol. 1994, 45, 313-326.
22. Rock, K. L.; Rothstein, L.; Gamble, S. Generation of class I MHC-restricted T-T hybridomas. J. Immunol. 1990, 145, 804-811.
23. Inaba, K.; Swiggard, W. J.; Inaba, M.; Meltzer, J.; Mirza, A.; Sasagawa, T.; Nussenzweig, M. C.; Steinman, R. M. Tissue distribution of the DEC-205 protein that is detected by the monoclonal antibody NLDC-145. I. Expression on dendritic cells and other subsets of mouse leukocytes. Cell. Immunol. 1995, 163, 148-156.
24. Porgador, A.; Yewdell, J. W.; Deng, Y.; Bennink, J. R.; Germain, R. N. Localization, quantitation, and in situ detection of specific peptide-MHC class I complexes using a monoclonal antibody. Immunity 1997, 6, 715-726.
25. Bartlett, G. R. J. Biol. Chem. 1959, 234, 466-468.
26. Inaba, K.; Inaba, M.; Romani, N.; Aya, H.; Deguchi, M.; Ikehara, S.; Muramatsu, S.; Steinman, R. M. Generation of large numbers of dendritic cells from mouse bone marrow cultures supplemented with granulocyte/macrophage colony-stimulating factor. J. Exp. Med. 1992, 176, 1693-1702.
27. Fields, R. C.; Shimizu, K.; Mule, J. J. Murine dendritic cells pulsed with whole tumor lysates mediate potent antitumor immune responses in vitro and in vivo. Proc. Natl. Acad. Sci. U.S.A. 1998, 95, 9482-9487.
28. Racoosin, E. L.; Swanson, J. A. Macrophage colony-stimulating factor (rM-CSF) stimulates pinocytosis in bone marrow-derived macrophages. J. Exp. Med. 1989, 170, 1635-1648.
29. Hollenbeck, P. J. Products of endocytosis and autophagy are retrieved from axons by regulated retrograde organelle transport. J. Cell Biol. 1993, 121, 305-315.
30. Clarke, M. S.; McNeil, P. L. Syringe loading introduces macro-molecules into living mammalian cell cytosol. J. Cell Sci. 1992, 102 (Part 3), 533-541.
31. Oh, Y. K.; Harding, C. V.; Swanson, J. A. The efficiency of antigen delivery from macrophage phagosomes into cytoplasm for MHC class I-restricted antigen presentation. Vaccine 1997, 15, 511-518.
32. Gursel, I.; Gursel, M.; Ishii, K. J.; Klinman, D. M. Sterically stabilized cationic liposomes improve the uptake and immunostimulatory activity of CpG oligonucleotides. J. Immunol. 2001, 167, 3324-3328.
33. Machy, P.; Serre, K.; Leserman, L. Class I-restricted presentation of exogenous antigen acquired by Fcγ receptor-mediated endocytosis is regulated in dendritic cells. Eur. J. Immunol. 2000, 30, 848-857.
34. Liu, Y. J. Dendritic cell subsets and lineages, and their functions in innate and adaptive immunity. Cell 2001, 106, 259-262.
35. Kolb-Maurer, A.; Gentschev, I.; Fries, H. W.; Fiedler, F.; Brocker, E. B.; Kampgen, E.; Goebel, W. Listeria monocytogenes-infected human dendritic cells, uptake and host cell response. Infect. Immun. 2000, 68, 3680-3688.
36. Pron, B.; Boumaila, C.; Jaubert, F.; Berche, P.; Milon, G.; Geissmann, F.; Gaillard, J. L. Dendritic cells are early cellular targets of Listeria monocytogenes after intestinal delivery and are involved in bacterial spread in the host. Cell. Microbiol. 2001, 3, 331-340.
37. Radford, K. J.; Higgins, D. E.; Pasquini, S.; Cheadle, E. J.; Carta, L.; Jackson, A. M.; Lemoine, N. R.; Vassaux, G. A recombinant E. coli vaccine to promote MHC class I-dependent antigen presentation, application to cancer immunotherapy. Gene Ther. 2002, 9, 1455-1463.
38. Paschen, A.; Dittmar, K. E.; Grenningloh, R.; Rohde, M.; Schadendorf, D.; Domann, E.; Chakraborty, T.; Weiss, S. Human dendritic cells infected by Listeria monocytogenes, induction of maturation, requirements for phagolysosomal escape and antigen presentation capacity. Eur. J. Immunol. 2000, 30, 3447-3456.
39. + T cells by exogenous cell-associated antigens. Immunity 2002, 17, 211-220.
40. Straubinger, R. M. pH-sensitive liposomes for delivery of macromolecules into cytoplasm of cultured cells. Methods Enzymol. 1993, 221, 361-376.
41. Glomski, I. J.; Gedde, M. M.; Tsang, A. W.; Swanson, J. A.; Portnoy, D. A. The Listeria monocytogenes hemolysin has an acidic pH optimum to compartmentalize activity and prevent damage to infected host cells. J. Cell Biol. 2002, 156, 1029-1038.
42. Maxfield, F. R.; Wustner, D. Intracellular cholesterol transport. J. Clin. Invest. 2002, 110, 891-898.
43. Rossjohn, J.; Feil, S. C.; McKinstry, W. J.; Tweten, R. K.; Parker, M. W. Structure of a cholesterol-binding, thiol-activated cytolysin and a model of its membrane form. Cell 1997, 89, 685-692.