MPLA incorporation into DC-targeting glycoliposomes favours anti-tumour T cell responses

Journal of Controlled Release

Volumn 216, Issue , 2015, Pages 37-46

  Boks, Martine A ^a   Ambrosini, Martino ^a   Bruijns, Sven C ^a   Kalay, Hakan ^a   Van Bloois, Louis ^b   Storm, Gert ^b,c   Garcia Vallejo, Juan J ^a   Van Kooyk, Yvette ^a  

^a VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^b UTRECHT UNIVERSITY   (Netherlands)

^c UNIVERSITY OF TWENTE   (Netherlands)

Author keywords

Adjuvant MPLA; Anti tumour immunity; Antigen targeting; DC SIGN; Glycan Lewis^{X< sup>; Liposomes}

Indexed keywords

ANTIGENS; CELLS; CHEMICAL ACTIVATION; CYTOLOGY; LIGANDS; LIPOSOMES; PEPTIDES; POLYSACCHARIDES; TUMORS;

ADJUVANT MPLA; ANTI-TUMOUR IMMUNITY; ANTIGEN-TARGETING; CANCER IMMUNOTHERAPY; DC SIGNS; DENDRITIC CELLS; PRO-INFLAMMATORY CYTOKINES; T CELL ACTIVATION;

T-CELLS;

CD209 ANTIGEN; CD8 ANTIGEN; GLYCAN; GLYCOPROTEIN GP 100; LECTIN RECEPTOR; LIGAND; LIPOSOME; PHOSPHORYL LIPID A; RESIQUIMOD; TOLL LIKE RECEPTOR 4; TUMOR ANTIGEN; CANCER ANTIBODY; CYTOKINE; MELANOCYTE PROTEIN PMEL 17; TLR4 PROTEIN, HUMAN;

ANION EXCHANGE CHROMATOGRAPHY; ANTIGEN SPECIFICITY; ARTICLE; CANCER IMMUNOTHERAPY; CELL FUNCTION; CELL MATURATION; COMPARATIVE STUDY; CROSS PRESENTATION; CYTOKINE PRODUCTION; DENDRITIC CELL; ELECTROSPRAY MASS SPECTROMETRY; ENCAPSULATION; FLOW CYTOMETRY; HUMAN; HUMAN CELL; LIPOSOMAL DELIVERY; PRIORITY JOURNAL; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; TARGET CELL; ZETA POTENTIAL; ANTIGEN PRESENTATION; BIOSYNTHESIS; CD8+ T LYMPHOCYTE; CHEMISTRY; CYTOTOXIC T LYMPHOCYTE; DRUG DELIVERY SYSTEM; DRUG EFFECTS; EXPERIMENTAL MELANOMA; GENETICS; MACROPHAGE; NUCLEIC ACID AMPLIFICATION; PROCEDURES;

ANTIBODIES, NEOPLASM; ANTIGEN PRESENTATION; ANTIGENS, NEOPLASM; CD8-POSITIVE T-LYMPHOCYTES; CYTOKINES; DENDRITIC CELLS; DRUG DELIVERY SYSTEMS; GP100 MELANOMA ANTIGEN; HUMANS; LIPOSOMES; MACROPHAGES; MELANOMA, EXPERIMENTAL; NUCLEIC ACID AMPLIFICATION TECHNIQUES; T-LYMPHOCYTES, CYTOTOXIC; TOLL-LIKE RECEPTOR 4;

EID: 84939519087     PISSN: 01683659     EISSN: 18734995     Source Type: Journal    
DOI: 10.1016/j.jconrel.2015.06.033     Document Type: Article

References (55)

1. I. Caminschi, E. Maraskovsky, and W.R. Heath Targeting dendritic cells in vivo for cancer therapy Front. Immunol. 3 2012 13
2. P.J. Tacken, R. Torensma, and C.G. Figdor Targeting antigens to dendritic cells in vivo Immunobiology 211 2006 599 608
3. V. Appay, D.C. Douek, and D.A. Price CD8 + T cell efficacy in vaccination and disease Nat. Med. 14 2008 623 628
4. C.A. Janeway, and R. Medzhitov Innate immune recognition Annu. Rev. Immunol. 20 2002 197 216
5. J. Banchereau, F. Briere, C. Caux, J. Davoust, S. Lebecque, Y.J. Liu, B. Pulendran, and K. Palucka Immunobiology of dendritic cells Annu. Rev. Immunol. 18 2000 767 811
6. I. Mellman, and R.M. Steinman Dendritic cells: specialized and regulated antigen processing machines Cell 106 2001 255 258
7. P.E. Jensen Recent advances in antigen processing and presentation Nat. Immunol. 8 2007 1041 1048
8. F.R. Carbone, and M.J. Bevan Class I-restricted processing and presentation of exogenous cell-associated antigen in vivo J. Exp. Med. 171 1990 377 387
9. O.P. Joffre, E. Segura, A. Savina, and S. Amigorena Cross-presentation by dendritic cells Nat. Rev. Immunol. 12 2012 557 569
10. W.W. Unger, and Y. van Kooyk 'Dressed for success' C-type lectin receptors for the delivery of glyco-vaccines to dendritic cells Curr. Opin. Immunol. 23 2011 131 137
11. C. Trumpfheller, J.S. Finke, C.B. Lopez, T.M. Moran, B. Moltedo, H. Soares, Y. Huang, S.J. Schlesinger, C.G. Park, M.C. Nussenzweig, A. Granelli-Piperno, and R.M. Steinman Intensified and protective CD4 + T cell immunity in mice with anti-dendritic cell HIV gag fusion antibody vaccine J. Exp. Med. 203 2006 607 617
12. T. Tsuji, J. Matsuzaki, M.P. Kelly, V. Ramakrishna, L. Vitale, L.Z. He, T. Keler, K. Odunsi, L.J. Old, G. Ritter, and S. Gnjatic Antibody-targeted NY-ESO-1 to mannose receptor or DEC-205 in vitro elicits dual human CD8 + and CD4 + T cell responses with broad antigen specificity J. Immunol. 186 2011 1218 1227
13. L.C. Bonifaz, D.P. Bonnyay, A. Charalambous, D.I. Darguste, S. Fujii, H. Soares, M.K. Brimnes, B. Moltedo, T.M. Moran, and R.M. Steinman In vivo targeting of antigens to maturing dendritic cells via the DEC-205 receptor improves T cell vaccination J. Exp. Med. 199 2004 815 824
14. B.J. Flynn, K. Kastenmuller, U. Wille-Reece, G.D. Tomaras, M. Alam, R.W. Lindsay, A.M. Salazar, B. Perdiguero, C.E. Gomez, R. Wagner, M. Esteban, C.G. Park, C. Trumpfheller, T. Keler, G. Pantaleo, R.M. Steinman, and R. Seder Immunization with HIV Gag targeted to dendritic cells followed by recombinant New York vaccinia virus induces robust T-cell immunity in nonhuman primates Proc. Natl. Acad. Sci. U. S. A. 108 2011 7131 7136
15. M.V. Dhodapkar, M. Sznol, B. Zhao, D. Wang, R.D. Carvajal, M.L. Keohan, E. Chuang, R.E. Sanborn, J. Lutzky, J. Powderly, H. Kluger, S. Tejwani, J. Green, V. Ramakrishna, A. Crocker, L. Vitale, M. Yellin, T. Davis, and T. Keler Induction of antigen-specific immunity with a vaccine targeting NY-ESO-1 to the dendritic cell receptor DEC-205 Sci. Transl. Med. 6 2014 232ra51
16. T.B. Geijtenbeek, S.J. van Vliet, A. Engering, B.A. 't Hart, and Y. van Kooyk Self- and nonself-recognition by C-type lectins on dendritic cells Annu. Rev. Immunol. 22 2004 33 54
17. B.J. Appelmelk, I. van Die, S.J. van Vliet, C.M. Vandenbroucke-Grauls, T.B. Geijtenbeek, and Y. van Kooyk Cutting edge: carbohydrate profiling identifies new pathogens that interact with dendritic cell-specific ICAM-3-grabbing nonintegrin on dendritic cells J. Immunol. 170 2003 1635 1639
18. D.A. Mitchell, A.J. Fadden, and K. Drickamer A novel mechanism of carbohydrate recognition by the C-type lectins DC-SIGN and DC-SIGNR. Subunit organization and binding to multivalent ligands J. Biol. Chem. 276 2001 28939 28945
19. T.B. Geijtenbeek, R. Torensma, S.J. van Vliet, G.C. van Duijnhoven, G.J. Adema, Y. van Kooyk, and C.G. Figdor Identification of DC-SIGN, a novel dendritic cell-specific ICAM-3 receptor that supports primary immune responses Cell 100 2000 575 585
20. A. Engering, T.B. Geijtenbeek, S.J. van Vliet, M. Wijers, L.E. van, N. Demaurex, A. Lanzavecchia, J. Fransen, C.G. Figdor, V. Piguet, and Y. van Kooyk The dendritic cell-specific adhesion receptor DC-SIGN internalizes antigen for presentation to T cells J. Immunol. 168 2002 2118 2126
21. A. Cambi, D.S. Lidke, D.J. Arndt-Jovin, C.G. Figdor, and T.M. Jovin Ligand-conjugated quantum dots monitor antigen uptake and processing by dendritic cells Nano Lett. 7 2007 970 977
22. S.K. Singh, J. Stephani, M. Schaefer, H. Kalay, J.J. Garcia-Vallejo, J. den Haan, E. Saeland, T. Sparwasser, and Y. van Kooyk Targeting glycan modified OVA to murine DC-SIGN transgenic dendritic cells enhances MHC class I and II presentation Mol. Immunol. 47 2009 164 174
23. C.A. Aarnoudse, M. Bax, M. Sanchez-Hernandez, J.J. Garcia-Vallejo, and Y. van Kooyk Glycan modification of the tumor antigen gp100 targets DC-SIGN to enhance dendritic cell induced antigen presentation to T cells Int. J. Cancer 122 2008 839 846
24. J. Wang, Y. Zhang, J. Wei, X. Zhang, B. Zhang, Z. Zhu, W. Zou, Y. Wang, Z. Mou, B. Ni, and Y. Wu Lewis X oligosaccharides targeting to DC-SIGN enhanced antigen-specific immune response Immunology 121 2007 174 182
25. M.D. Joshi, W.J. Unger, G. Storm, Y. van Kooyk, and E. Mastrobattista Targeting tumor antigens to dendritic cells using particulate carriers J. Control. Release 161 2012 25 37
26. V.P. Torchilin Recent advances with liposomes as pharmaceutical carriers Nat. Rev. Drug Discov. 4 2005 145 160
27. W.W. Unger, A.J. van Beelen, S.C. Bruijns, M. Joshi, C.M. Fehres, L. van Bloois, M.I. Verstege, M. Ambrosini, H. Kalay, K. Nazmi, J.G. Bolscher, E. Hooijberg, T.D. de Gruijl, G. Storm, and Y. van Kooyk Glycan-modified liposomes boost CD4 + and CD8 + T-cell responses by targeting DC-SIGN on dendritic cells J. Control. Release 160 2012 88 95
28. S. Burgdorf, A. Kautz, V. Bohnert, P.A. Knolle, and C. Kurts Distinct pathways of antigen uptake and intracellular routing in CD4 and CD8 T cell activation Science 316 2007 612 616
29. C.M. Fehres, W.W. Unger, J.J. Garcia-Vallejo, and Y. van Kooyk Understanding the biology of antigen cross-presentation for the design of vaccines against cancer Front. Immunol. 5 2014 149
30. P. Nair-Gupta, A. Baccarini, N. Tung, F. Seyffer, O. Florey, Y. Huang, M. Banerjee, M. Overholtzer, P.A. Roche, R. Tampe, B.D. Brown, D. Amsen, S.W. Whiteheart, and J.M. Blander TLR signals induce phagosomal MHC-I delivery from the endosomal recycling compartment to allow cross-presentation Cell 158 2014 506 521
31. M.D. Joshi, W.W. Unger, A.J. van Beelen, S.C. Bruijns, M. Litjens, L. van Bloois, H. Kalay, Y. van Kooyk, and G. Storm DC-SIGN mediated antigen-targeting using glycan-modified liposomes: formulation considerations Int. J. Pharm. 416 2011 426 432
32. T.B. Geijtenbeek, G.C. van Duijnhoven, S.J. van Vliet, E. Krieger, G. Vriend, C.G. Figdor, and Y. van Kooyk Identification of different binding sites in the dendritic cell-specific receptor DC-SIGN for intercellular adhesion molecule 3 and HIV-1 J. Biol. Chem. 277 2002 11314 11320
33. J.J. Garcia-Vallejo, K. Bloem, L. Knippels, J. Garssen, S. van Vliet, and Y. Van Kooyk The consequences of multiple simultaneous C-type lectin-ligand interactions: DCIR alters the endo-lysosomal routing of DC-SIGN Front. Immunol. 6 2015
34. N. Schaft, R.A. Willemsen, J. de Vries, B. Lankiewicz, B.W. Essers, J.W. Gratama, C.G. Figdor, R.L. Bolhuis, R. Debets, and G.J. Adema Peptide fine specificity of anti-glycoprotein 100 CTL is preserved following transfer of engineered TCR alpha beta genes into primary human T lymphocytes J. Immunol. 170 2003 2186 2194
35. A. Kretz-Rommel, F. Qin, N. Dakappagari, R. Torensma, S. Faas, D. Wu, and K.S. Bowdish In vivo targeting of antigens to human dendritic cells through DC-SIGN elicits stimulatory immune responses and inhibits tumor growth in grafted mouse models J. Immunother. 30 2007 715 726
36. P.J. Tacken, I.J. de Vries, K. Gijzen, B. Joosten, D. Wu, R.P. Rother, S.J. Faas, C.J. Punt, R. Torensma, G.J. Adema, and C.G. Figdor Effective induction of naive and recall T-cell responses by targeting antigen to human dendritic cells via a humanized anti-DC-SIGN antibody Blood 106 2005 1278 1285
37. P.J. Tacken, M. Ter Huurne, R. Torensma, and C.G. Figdor Antibodies and carbohydrate ligands binding to DC-SIGN differentially modulate receptor trafficking Eur. J. Immunol. 42 2012 1989 1998
38. S. De Koker, B.G. De Geest, S.K. Singh, R. De Rycke, T. Naessens, Y. van Kooyk, J. Demeester, S.C. De Smedt, and J. Grooten Polyelectrolyte microcapsules as antigen delivery vehicles to dendritic cells: uptake, processing, and cross-presentation of encapsulated antigens Angew. Chem. Int. Ed. Engl. 48 2009 8485 8489
39. S.D. Xiang, A. Scholzen, G. Minigo, C. David, V. Apostolopoulos, P.L. Mottram, and M. Plebanski Pathogen recognition and development of particulate vaccines: does size matter? Methods 40 2006 1 9
40. T.B. Geijtenbeek, and Y. van Kooyk Pathogens target DC-SIGN to influence their fate DC-SIGN functions as a pathogen receptor with broad specificity APMIS 111 2003 698 714
41. K.K. Tran, and H. Shen The role of phagosomal pH on the size-dependent efficiency of cross-presentation by dendritic cells Biomaterials 30 2009 1356 1362
42. R. van der Meel, L.J. Vehmeijer, R.J. Kok, G. Storm, and E.V. van Gaal Ligand-targeted particulate nanomedicines undergoing clinical evaluation: current status Adv. Drug Deliv. Rev. 65 2013 1284 1298
43. A. Badiee, N. Davies, K. McDonald, K. Radford, H. Michiue, D. Hart, and M. Kato Enhanced delivery of immunoliposomes to human dendritic cells by targeting the multilectin receptor DEC-205 Vaccine 25 2007 4757 4766
44. R.K. Gieseler, G. Marquitan, M.J. Hahn, L.A. Perdon, W.H. Driessen, S.M. Sullivan, and M.J. Scolaro DC-SIGN-specific liposomal targeting and selective intracellular compound delivery to human myeloid dendritic cells: implications for HIV disease Scand. J. Immunol. 59 2004 415 424
45. S. Espuelas, C. Thumann, B. Heurtault, F. Schuber, and B. Frisch Influence of ligand valency on the targeting of immature human dendritic cells by mannosylated liposomes Bioconjug. Chem. 19 2008 2385 2393
46. M.J. Copland, M.A. Baird, T. Rades, J.L. McKenzie, B. Becker, F. Reck, P.C. Tyler, and N.M. Davies Liposomal delivery of antigen to human dendritic cells Vaccine 21 2003 883 890
47. N. Kojima, L. Biao, T. Nakayama, M. Ishii, Y. Ikehara, and K. Tsujimura Oligomannose-coated liposomes as a therapeutic antigen-delivery and an adjuvant vehicle for induction of in vivo tumor immunity J. Control. Release 129 2008 26 32
48. P.J. Tacken, I.J. de Vries, R. Torensma, and C.G. Figdor Dendritic-cell immunotherapy: from ex vivo loading to in vivo targeting Nat. Rev. Immunol. 7 2007 790 802
49. M. Ishii, C. Kato, A. Hakamata, and N. Kojima Targeting with oligomannose-coated liposomes promotes maturation and splenic trafficking of dendritic cells in the peritoneal cavity Int. Immunopharmacol. 11 2011 164 171
50. E. Schlosser, M. Mueller, S. Fischer, S. Basta, D.H. Busch, B. Gander, and M. Groettrup TLR ligands and antigen need to be coencapsulated into the same biodegradable microsphere for the generation of potent cytotoxic T lymphocyte responses Vaccine 26 2008 1626 1637
51. V. Jerome, A. Graser, R. Muller, R.E. Kontermann, and A. Konur Cytotoxic T lymphocytes responding to low dose TRP2 antigen are induced against B16 melanoma by liposome-encapsulated TRP2 peptide and CpG DNA adjuvant J. Immunother. 29 2006 294 305
52. P. Nordly, E.M. Agger, P. Andersen, H.M. Nielsen, and C. Foged Incorporation of the TLR4 agonist monophosphoryl lipid A into the bilayer of DDA/TDB liposomes: physico-chemical characterization and induction of CD8 + T-cell responses in vivo Pharm. Res. 28 2011 553 562
53. T. Nakamura, R. Moriguchi, K. Kogure, and H. Harashima Incorporation of polyinosine-polycytidylic acid enhances cytotoxic T cell activity and antitumor effects by octaarginine-modified liposomes encapsulating antigen, but not by octaarginine-modified antigen complex Int. J. Pharm. 441 2013 476 481
54. D. Chen, J. Koropatnick, N. Jiang, X. Zheng, X. Zhang, H. Wang, K. Yuan, K.S. Siu, A. Shunnar, C. Way, and W.P. Min Targeted siRNA silencing of indoleamine 2, 3-dioxygenase in antigen-presenting cells using mannose-conjugated liposomes: a novel strategy for treatment of melanoma J. Immunother. 37 2014 123 134
55. J.S. Thomann, B. Heurtault, S. Weidner, M. Braye, J. Beyrath, S. Fournel, F. Schuber, and B. Frisch Antitumor activity of liposomal ErbB2/HER2 epitope peptide-based vaccine constructs incorporating TLR agonists and mannose receptor targeting Biomaterials 32 2011 4574 4583