CD40-targeted dendritic cell delivery of PLGA-nanoparticle vaccines induce potent anti-tumor responses

Biomaterials

Volumn 40, Issue , 2015, Pages 88-97

  Rosalia, Rodney A ^a   Cruz, Luis J ^a   van Duikeren, Suzanne ^a   Tromp, Angelino T ^a   Silva, Ana L ^b   Jiskoot, Wim ^b   de Gruijl, Tanja ^c   Löwik, Clemens ^a   Oostendorp, Jaap ^a   van der Burg, Sjoerd H ^a   Ossendorp, Ferry ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^b LEIDEN UNIVERSITY   (Netherlands)

^c VU UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

CD40; DC; NP; PLGA; PLGA nanoparticles; Targeting; TLR ligands; TLRL; Vaccine

Indexed keywords

CYTOLOGY; NANOPARTICLES; NEPTUNIUM; PROTEINS; SILVER COMPOUNDS; TUMORS; VACCINES;

CD40; PLGA; PLGA NANOPARTICLES; TARGETING; TLRL;

T-CELLS;

CANCER VACCINE; CD40 ANTIGEN; DENDRITIC CELL VACCINE; NANOCARRIER; NP CD40 VACCINE; POLYGLACTIN; UNCLASSIFIED DRUG; GAMMA INTERFERON; LACTIC ACID; LIGAND; MONOCLONAL ANTIBODY; NANOPARTICLE; POLYGLYCOLIC ACID; POLYLACTIC ACID-POLYGLYCOLIC ACID COPOLYMER; TOLL LIKE RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER CONTROL; CANCER IMMUNIZATION; CANCER SURVIVAL; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL ENCAPSULATION; CELL PROLIFERATION; CONTROLLED STUDY; DENDRITIC CELL; DRUG DELIVERY SYSTEM; IN VITRO STUDY; MOUSE; NANOPHARMACEUTICS; NONHUMAN; TUMOR GROWTH; ANIMAL; ANTIGEN PRESENTING CELL; BIOSYNTHESIS; C57BL MOUSE; CHEMISTRY; ENDOCYTOSIS; IMMUNOLOGY; METABOLISM; NEOPLASM; PATHOLOGY; VACCINATION;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIGEN-PRESENTING CELLS; ANTIGENS, CD40; CANCER VACCINES; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELL PROLIFERATION; DENDRITIC CELLS; ENDOCYTOSIS; INTERFERON-GAMMA; LACTIC ACID; LIGANDS; MICE, INBRED C57BL; NANOPARTICLES; NEOPLASMS; POLYGLYCOLIC ACID; TOLL-LIKE RECEPTORS; VACCINATION;

EID: 84919667582     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2014.10.053     Document Type: Article

References (55)

1. Palucka K., Ueno H., Fay J., Banchereau J. Dendritic cells and immunity against cancer. JIntern Med 2011, 269:64-73.
2. Banchereau J., Steinman R.M. Dendritic cells and the control of immunity. Nature 1998, 392:245-252.
3. Palucka K., Banchereau J. Cancer immunotherapy via dendritic cells. Nat Rev Cancer 2012, 12:265-277.
4. Pasare C., Medzhitov R. Toll-like receptors: linking innate and adaptive immunity. Adv Exp Med Biol 2005, 560:11-18.
5. Tacken P.J., de Vries I.J., Torensma R., Figdor C.G. Dendritic-cell immunotherapy: from exvivo loading to invivo targeting. Nat Rev Immunol 2007, 7:790-802.
6. Melief C.J. Cancer immunotherapy by dendritic cells. Immunity 2008, 29:372-383.
7. Shen H., Ackerman A.L., Cody V., Giodini A., Hinson E.R., Cresswell P., et al. Enhanced and prolonged cross-presentation following endosomal escape of exogenous antigens encapsulated in biodegradable nanoparticles. Immunology 2006, 117:78-88.
8. Fischer S., Schlosser E., Mueller M., Csaba N., Merkle H.P., Groettrup M., et al. Concomitant delivery of a CTL-restricted peptide antigen and CpG ODN by PLGA microparticles induces cellular immune response. JDrug Target 2009, 17:652-661.
9. Silva A.L., Rosalia R.A., Sazak A., Carstens M.G., Ossendorp F., Oostendorp J., et al. Optimization of encapsulation of a synthetic long peptide in PLGA nanoparticles: low-burst release is crucial for efficient CD8(+) T cell activation. Eur J Pharm Biopharm Off J Arbeitsgemeinschaft fur Pharm Verfahrenstech eV 2013, 83:338-345.
10. Silva J.M., Videira M., Gaspar R., Preat V., Florindo H.F. Immune system targeting by biodegradable nanoparticles for cancer vaccines. JControl Release Off J Control Release Soc 2013, 168:179-199.
11. Mueller M., Schlosser E., Gander B., Groettrup M. Tumor eradication by immunotherapy with biodegradable PLGA microspheres - an alternative to incomplete Freund's adjuvant. Int J Cancer 2011, 129:407-416. Epub 2011 Mar 28. 10.1002/ijc.25914.
12. Bazile D., Prud'homme C., Bassoullet M.T., Marlard M., Spenlehauer G., Veillard M. Stealth Me.PEG-PLA nanoparticles avoid uptake by the mononuclear phagocytes system. JPharm Sci 1995, 84:493-498.
13. Tacken P.J., Zeelenberg I.S., Cruz L.J., van Hout-Kuijer M.A., van de Glind G., Fokkink R.G., et al. Targeted delivery of TLR ligands to human and mouse dendritic cells strongly enhances adjuvanticity. Blood 2011, 118:6836-6844. Epub 2011 Oct 3. 10.1182/blood-2011-07-367615.
14. Macho-Fernandez E., Cruz L.J., Ghinnagow R., Fontaine J., Bialecki E., Frisch B., et al. Targeted delivery of alpha-galactosylceramide to CD8alpha+ dendritic cells optimizes type I NKT cell-based antitumor responses. JImmunol 2014, 193:961-969.
15. Hamdy S., Haddadi A., Shayeganpour A., Samuel J., Lavasanifar A. Activation of antigen-specific T cell-responses by mannan-decorated PLGA nanoparticles. Pharm Res 2011, 28:2288-2301. Epub 2011 May 11. 10.1007/s11095-011-0459-9.
16. Han R., Zhu J., Yang X., Xu H. Surface modification of poly(D,L-lactic-co-glycolic acid) nanoparticles with protamine enhanced cross-presentation of encapsulated ovalbumin by bone marrow-derived dendritic cells. JBiomed Mater Res A 2011, 96:142-149.
17. Schoenberger S.P., Toes R.E., van der Voort E.I., Offringa R., Melief C.J. T-cell help for cytotoxic T lymphocytes is mediated by CD40-CD40L interactions. Nature 1998, 393:480-483.
18. Schuurhuis D.H., Laban S., Toes R.E., Ricciardi-Castagnoli P., Kleijmeer M.J., van der Voort E.I., et al. Immature dendritic cells acquire CD8(+) cytotoxic T lymphocyte priming capacity upon activation by T helper cell-independent or -dependent stimuli. JExp Med 2000, 192:145-150.
19. Cohn L., Chatterjee B., Esselborn F., Smed-Sorensen A., Nakamura N., Chalouni C., et al. Antigen delivery to early endosomes eliminates the superiority of human blood BDCA3+ dendritic cells at cross presentation. JExp Med 2013, 210:1049-1063.
20. Schjetne K.W., Fredriksen A.B., Bogen B. Delivery of antigen to CD40 induces protective immune responses against tumors. JImmunol 2007, 178:4169-4176.
21. Schuurhuis D.H., van Montfoort N., Ioan-Facsinay A., Jiawan R., Camps M., Nouta J., et al. Immune complex-loaded dendritic cells are superior to soluble immune complexes as antitumor vaccine. JImmunol 2006, 176:4573-4580.
22. 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.
23. Cruz L.J., Tacken P.J., Fokkink R., Joosten B., Stuart M.C., Albericio F., et al. Targeted PLGA nano- but not microparticles specifically deliver antigen to human dendritic cells via DC-SIGN invitro. JControl Release 2010, 144:118-126. Epub Feb 13. 10.1016/j.jconrel.2010.02.013.
24. Ossendorp F., Mengede E., Camps M., Filius R., Melief C.J. Specific T helper cell requirement for optimal induction of cytotoxic T lymphocytes against major histocompatibility complex class II negative tumors. JExp Med 1998, 187:693-702.
25. Mackey M.F., Wang Z., Eichelberg K., Germain R.N. Distinct contributions of different CD40 TRAF binding sites to CD154-induced dendritic cell maturation and IL-12 secretion. Eur J Immunol 2003, 33:779-789.
26. Brown J., Wang H., Hajishengallis G.N., Martin M. TLR-signaling networks: an integration of adaptor molecules, kinases, and cross-talk. JDent Res 2011, 90:417-427.
27. Manolova V., Flace A., Bauer M., Schwarz K., Saudan P., Bachmann M.F. Nanoparticles target distinct dendritic cell populations according to their size. Eur J Immunol 2008, 38:1404-1413. 10.1002/eji.200737984.
28. Raghuwanshi D., Mishra V., Suresh M.R., Kaur K. Asimple approach for enhanced immune response using engineered dendritic cell targeted nanoparticles. Vaccine 2012, 30:7292-7299.
29. Schreibelt G., Klinkenberg L.J., Cruz L.J., Tacken P.J., Tel J., Kreutz M., et al. The C-type lectin receptor CLEC9A mediates antigen uptake and (cross-)presentation by human blood BDCA3+ myeloid dendritic cells. Blood 2012, 119:2284-2292.
30. Merad M., Sathe P., Helft J., Miller J., Mortha A. The dendritic cell lineage: ontogeny and function of dendritic cells and their subsets in the steady state and the inflamed setting. Annu Rev Immunol 2013, 31:563-604.
31. Kreutz M., Tacken P.J., Figdor C.G. Targeting dendritic cells - why bother?. Blood 2013, 121:2836-2844. Epub 2013 Feb 6. 10.1182/blood-2012-09-452078.
32. Idoyaga J., Fiorese C., Zbytnuik L., Lubkin A., Miller J., Malissen B., et al. Specialized role of migratory dendritic cells in peripheral tolerance induction. JClin Invest 2013, 123:844-854. Epub 2013 Jan 9. 10.1172/JCI65260.
33. Gottschalk C., Damuzzo V., Gotot J., Kroczek R.A., Yagita H., Murphy K.M., et al. Batf3-dependent dendritic cells in the renal lymph node induce tolerance against circulating antigens. JAm Soc Nephrol JASN 2013, 24:543-549.
34. Kroczek R.A., Henn V. The role of XCR1 and its ligand XCL1 in antigen cross-presentation by murine and human dendritic cells. Front Immunol 2012, 3:14.
35. Dresch C., Leverrier Y., Marvel J., Shortman K. Development of antigen cross-presentation capacity in dendritic cells. Trends Immunol 2012, 33:381-388.
36. Shortman K., Liu Y.J. Mouse and human dendritic cell subtypes. Nat Rev Immunol 2002, 2:151-161.
37. van Montfoort N., Mangsbo S.M., Camps M.G., van Maren W.W., Verhaart I.E., Waisman A., et al. Circulating specific antibodies enhance systemic cross-priming by delivery of complexed antigen to dendritic cells invivo. Eur J Immunol 2012, 42:598-606.
38. Cruz L.J., Rosalia R.A., Kleinovink J.W., Rueda F., Lowik C.W., Ossendorp F. Targeting nanoparticles to CD40, DEC-205 or CD11c molecules on dendritic cells for efficient CD8(+) T cell response: a comparative study. J Controlled Release. 2014, 192:209-218.
39. Rabinovitch M. Professional and non-professional phagocytes: an introduction. Trends Cell Biol 1995, 5:85-87.
40. Lim T.S., Goh J.K., Mortellaro A., Lim C.T., Hammerling G.J., Ricciardi-Castagnoli P. CD80 and CD86 differentially regulate mechanical interactions of T-cells with antigen-presenting dendritic cells and B-cells. PLoS One 2012, 7:e45185.
41. Schliehe C., Redaelli C., Engelhardt S., Fehlings M., Mueller M., van Rooijen N., et al. CD8- dendritic cells and macrophages cross-present poly(D,L-lactate-co-glycolate) acid microsphere-encapsulated antigen invivo. JImmunol 2011, 187:2112-2121.
42. Gref R., Luck M., Quellec P., Marchand M., Dellacherie E., Harnisch S., et al. 'Stealth' corona-core nanoparticles surface modified by polyethylene glycol (PEG): influences of the corona (PEG chain length and surface density) and of the core composition on phagocytic uptake and plasma protein adsorption. Colloids Surf B Biointerfaces 2000, 18:301-313.
43. Shortman K., Heath W.R. The CD8+ dendritic cell subset. Immunol Rev 2010, 234:18-31.
44. Schnorrer P., Behrens G.M., Wilson N.S., Pooley J.L., Smith C.M., El-Sukkari D., et al. The dominant role of CD8+ dendritic cells in cross-presentation is not dictated by antigen capture. Proc Natl Acad Sci U S A 2006, 103:10729-10734.
45. Kamphorst A.O., Guermonprez P., Dudziak D., Nussenzweig M.C. Route of antigen uptake differentially impacts presentation by dendritic cells and activated monocytes. JImmunol 2010, 185:3426-3435.
46. Gao X., Wang S., Fan Y., Bai H., Yang J., Yang X. CD8+ DC, but not CD8(-)DC, isolated from BCG-infected mice reduces pathological reactions induced by mycobacterial challenge infection. PLoS One 2010, 5:e9281.
47. Hangalapura B.N., Oosterhoff D., de Groot J., Boon L., Tuting T., van den Eertwegh A.J., et al. Potent antitumor immunity generated by a CD40-targeted adenoviral vaccine. Cancer Res 2011, 71:5827-5837.
48. Kempf M., Mandal B., Jilek S., Thiele L., Voros J., Textor M., et al. Improved stimulation of human dendritic cells by receptor engagement with surface-modified microparticles. JDrug Target 2003, 11:11-18.
49. Broos S., Sandin L.C., Apel J., Totterman T.H., Akagi T., Akashi M., et al. Synergistic augmentation of CD40-mediated activation of antigen-presenting cells by amphiphilic poly(gamma-glutamic acid) nanoparticles. Biomaterials 2012, 33:6230-6239.
50. Gu L., Ruff L.E., Qin Z., Corr M., Hedrick S.M., Sailor M.J. Multivalent porous silicon nanoparticles enhance the immune activation potency of agonistic CD40 antibody. Adv Mater Deerf Beach Fla 2012, 24:3981-3987.
51. Welters M.J., Bijker M.S., van den Eeden S.J., Franken K.L., Melief C.J., Offringa R., et al. Multiple CD4 and CD8 T-cell activation parameters predict vaccine efficacy invivo mediated by individual DC-activating agonists. Vaccine 2007, 25:1379-1389.
52. Fransen M.F., Sluijter M., Morreau H., Arens R., Melief C.J. Local activation of CD8 T cells and systemic tumor eradication without toxicity via slow release and local delivery of agonistic CD40 antibody. Clin Cancer Res Off J Am Assoc Cancer Res 2011, 17:2270-2280.
53. Kasturi S.P., Skountzou I., Albrecht R.A., Koutsonanos D., Hua T., Nakaya H.I., et al. Programming the magnitude and persistence of antibody responses with innate immunity. Nature 2011, 470:543-547.
54. Zhu Q., Egelston C., Gagnon S., Sui Y., Belyakov I.M., Klinman D.M., et al. Using 3 TLR ligands as a combination adjuvant induces qualitative changes in T cell responses needed for antiviral protection in mice. JClin Investig 2010, 120:607-616.
55. Slutter B., Pewe L.L., Lauer P., Harty J.T. Cutting edge: rapid boosting of cross-reactive memory CD8 T cells broadens the protective capacity of the Flumist vaccine. JImmunol 2013, 190:3854-3858.