Targeting dendritic cells - Why bother?

Blood

Volumn 121, Issue 15, 2013, Pages 2836-2844

  Kreutz, Martin ^a   Tacken, Paul J ^a   Figdor, Carl G ^a  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN; IMIQUIMOD; IMMUNOLOGICAL ADJUVANT; INTERLEUKIN 10; LENTIVIRUS VECTOR; LIPOSOME; NANOPARTICLE; POLYMER; TOLL LIKE RECEPTOR 7; VACCINE;

ACTIVE TRANSPORT; ADJUVANT THERAPY; ANTIGEN BINDING; ANTIGEN PRESENTATION; CELL ACTIVATION; CELLULAR IMMUNITY; CLINICAL TRIAL (TOPIC); CROSS PRESENTATION; DENDRITIC CELL; DRUG DELIVERY SYSTEM; HUMAN; IMMUNE RESPONSE; IMMUNE SYSTEM; IMMUNIZATION; IMMUNOTHERAPY; NONHUMAN; PASSIVE TRANSPORT; PATHOGENESIS; PHASE 1 CLINICAL TRIAL (TOPIC); PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; REVIEW; RISK ASSESSMENT; T LYMPHOCYTE; TARGET CELL; VACCINATION; ARTICLE; B LYMPHOCYTE; BIOLOGICAL MODEL; IMMUNOLOGY; METHODOLOGY;

ANTIGENS; B-LYMPHOCYTES; DENDRITIC CELLS; HUMANS; IMMUNITY, CELLULAR; IMMUNOTHERAPY; MODELS, IMMUNOLOGICAL; T-LYMPHOCYTES; VACCINES;

MLCS; MLOWN;

EID: 84879228653     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2012-09-452078     Document Type: Review

References (114)

1. Lombard M, Pastoret PP, Moulin AM. A brief history of vaccines and vaccination. Rev Sci Tech. 2007;26(1):29-48. (Pubitemid 47148811)
2. Jenner E. An Inquiry into the Causes and Effects of the Variolæ Vaccinæ. London: Sampson Low; 1798
3. Ramon G. Sur l'augmentation anormale de l'antitoxine chez les chevaux producteurs de serum antidipherique. Bull Soc Cent Med Vet. 1925;101:227-234.
4. Glenny AT, Pope CG, Waddington H, et al. Immunological notes XVLL.-XXIV. J Pathol Bacteriol. 1926;29(1):31-40.
5. Mbow ML, De Gregorio E, Ulmer JB. Alum's adjuvant action: grease is the word. Nat Med. 2011;17(4):415-416.
6. Bachmann MF, Jennings GT. Vaccine delivery: a matter of size, geometry, kinetics and molecular patterns. Nat Rev Immunol. 2010;10(11):787-796.
7. Kantoff PW, Higano CS, Shore ND, et al. Sipuleucel-T immunotherapy for castration-resistant prostate cancer. N Engl J Med. 2010;363(5):411-422.
8. Morse MA, Chapman R, Powderly J, et al. Phase I study utilizing a novel antigen-presenting cell-targeted vaccine with toll-like receptor stimulation to induce immunity to self-antigens in cancer patients. Clin Cancer Res. 2011;17(14):4844-4853.
9. Ueno H, Klechevsky E, Schmitt N, et al. Targeting human dendritic cell subsets for improved vaccines. Semin Immunol. 2011;23(1):21-27.
10. Reis e Sousa C. Dendritic cells in a mature age. Nat Rev Immunol. 2006;6(6):476-483.
11. Figdor CG, van Kooyk Y, Adema GJ. C-type lectin receptors on dendritic cells and Langerhans cells. Nat Rev Immunol. 2002;2(2):77-84. (Pubitemid 37323231)
12. Carayanniotis G, Barber BH. Adjuvant-free IgG responses induced with antigen coupled to antibodies against class II MHC. Nature. 1987;327(6117):59- 61.
13. Snider DP, Kaubisch A, Segal DM. Enhanced antigen immunogenicity induced by bispecific antibodies. J Exp Med. 1990;171(6):1957-1963. (Pubitemid 20200236)
14. Mahnke K, Guo M, Lee S, et al. The dendritic cell receptor for endocytosis, DEC-205, can recycle and enhance antigen presentation via major histocompatibility complex class II-positive lysosomal compartments. J Cell Biol. 2000;151(3):673-684.
15. Hawiger D, Inaba K, Dorsett Y, et al. Dendritic cells induce peripheral T cell unresponsiveness under steady state conditions in vivo. J Exp Med. 2001;194(6):769-779. (Pubitemid 32983013)
16. Bonifaz LC, Bonnyay DP, Charalambous A, et al. In vivo targeting of antigens to maturing dendritic cells via the DEC-205 receptor improves T cell vaccination. J Exp Med. 2004;199(6):815-824. (Pubitemid 38375201)
17. He LZ, Crocker A, Lee J, et al. Antigenic targeting of the human mannose receptor induces tumor immunity. J Immunol. 2007;178(10):6259-6267. (Pubitemid 46717409)
18. Carter RW, Thompson C, Reid DM, Wong SY, Tough DF. Preferential induction of CD4+ T cell responses through in vivo targeting of antigen to dendritic cell-associated C-type lectin-1. J Immunol. 2006;177(4):2276-2284. (Pubitemid 44200987)
19. Freire T, Zhang X, Deriaud E, et al. Glycosidic Tn-based vaccines targeting dermal dendritic cells favor germinal center B-cell development and potent antibody response in the absence of adjuvant. Blood. 2010;116(18):3526- 3536.
20. Tacken PJ, Joosten B, Reddy A, et al. No advantage of cell-penetrating peptides over receptor-specific antibodies in targeting antigen to human dendritic cells for cross-presentation. J Immunol. 2008;180(11):7687-7696.
21. Meyer-Wentrup F, Benitez-Ribas D, Tacken PJ, et al. Targeting DCIR on human plasmacytoid dendritic cells results in antigen presentation and inhibits IFN-alpha production. Blood. 2008;111(8):4245-4253.
22. Sancho D, Joffre OP, Keller AM, et al. Identification of a dendritic cell receptor that couples sensing of necrosis to immunity. Nature. 2009;458(7240):899-903.
23. Zhang JG, Czabotar PE, Policheni AN, et al. The dendritic cell receptor Clec9A binds damaged cells via exposed actin filaments. Immunity. 2012;36(4):646-657.
24. Ahrens S, Zelenay S, Sancho D, et al. F-actin is an evolutionarily conserved damage-associated molecular pattern recognized by DNGR-1, a receptor for dead cells. Immunity. 2012;36(4):635-645.
25. Zelenay S, Keller AM, Whitney PG, et al. The dendritic cell receptor DNGR-1 controls endocytic handling of necrotic cell antigens to favor cross-priming of CTLs in virus-infected mice. J Clin Invest. 2012;122(5):1615-1627.
26. Iborra S, Izquierdo HM, Martinez-Lopez M, Blanco-Menendez N, Reis ESC, Sancho D. The DC receptor DNGR-1 mediates cross-priming of CTLs during vaccinia virus infection in mice. J Clin Invest. 2012;122(5):1628-1643.
27. Shortman K, Heath WR. The CD8+ dendritic cell subset. Immunol Rev. 2010;234(1):18-31.
28. Loschko J, Schlitzer A, Dudziak D, et al. Antigen delivery to plasmacytoid dendritic cells via BST2 induces protective T cell-mediated immunity. J Immunol. 2011;186(12):6718-6725.
29. Loschko J, Heink S, Hackl D, et al. Antigen targeting to plasmacytoid dendritic cells via Siglec-H inhibits Th cell-dependent autoimmunity. J Immunol. 2011. E-pub November 14, 2011 DOI jimmunol.1102307 [pii]
30. Zhang J, Raper A, Sugita N, et al. Characterization of Siglec-H as a novel endocytic receptor expressed on murine plasmacytoid dendritic cell precursors. Blood. 2006;107(9):3600-3608.
31. Colonna M, Krug A, Cella M. Interferon-producing cells: on the front line in immune responses against pathogens. Curr Opin Immunol. 2002;14(3):373-379. (Pubitemid 34327981)
32. Cheong C, Matos I, Choi JH, et al. Microbial stimulation fully differentiates monocytes to DC-SIGN/CD209(+) dendritic cells for immune T cell areas. Cell. 2010;143(3):416-429.
33. Schliehe C, Redaelli C, Engelhardt S, et al. CD8- dendritic cells and macrophages cross-present poly(D,L-lactate-co-glycolate) acid microsphere-encapsulated antigen in vivo. J Immunol. 2011;187(5):2112-2121.
34. Sancho D, Mourão-Sá D, Joffre OP, et al. Tumor therapy in mice via antigen targeting to a novel, DC-restricted C-type lectin. J Clin Invest. 2008;118(6):2098-2110.
35. Galibert L, Diemer GS, Liu Z, et al. Nectin-like protein 2 defines a subset of T-cell zone dendritic cells and is a ligand for class-I-restricted T-cell-associated molecule. J Biol Chem. 2005;280(23):21955-21964. (Pubitemid 40827848)
36. Robbins SH, Walzer T, Dembele D, et al. Novel insights into the relationships between dendritic cell subsets in human and mouse revealed by genome-wide expression profiling. Genome Biol. 2008;9(1):R17.
37. Caminschi I, Proietto AI, Ahmet F, et al. The dendritic cell subtype-restricted C-type lectin Clec9A is a target for vaccine enhancement. Blood. 2008;112(8):3264-3273.
38. Huysamen C, Willment JA, Dennehy KM, Brown GD. CLEC9A is a novel activation C-type lectin-like receptor expressed on BDCA3+ dendritic cells and a subset of monocytes. J Biol Chem. 2008;283(24):16693-16701.
39. Bachem A, Güttler S, Hartung E, et al. Superior antigen cross-presentation and XCR1 expression define human CD11c+CD141+ cells as homologues of mouse CD8+ dendritic cells. J Exp Med. 2010;207(6):1273-1281.
40. Crozat K, Guiton R, Contreras V, et al. The XC chemokine receptor 1 is a conserved selective marker of mammalian cells homologous to mouse CD8alpha+ dendritic cells. J Exp Med. 2010;207(6):1283-1292.
41. Jongbloed SL, Kassianos AJ, McDonald KJ, et al. Human CD141+ (BDCA-3)+ dendritic cells (DCs) represent a unique myeloid DC subset that cross-presents necrotic cell antigens. J Exp Med. 2010;207(6):1247-1260.
42. Poulin LF, Salio M, Griessinger E, et al. Characterization of human DNGR-1+ BDCA3+ leukocytes as putative equivalents of mouse CD8alpha+ dendritic cells. J Exp Med. 2010;207(6):1261-1271.
43. Villadangos JA, Shortman K. Found in translation: the human equivalent of mouse CD8+ dendritic cells. J Exp Med. 2010;207(6):1131-1134.
44. Schreibelt G, Klinkenberg LJ, Cruz LJ, et al. The C type lectin receptor CLEC9A mediates antigen uptake and (cross-)presentation by human blood BDCA3+ myeloid dendritic cells. Blood. 2012;119(10):2284-2292.
45. Mittag D, Proietto AI, Loudovaris T, et al. Human dendritic cell subsets from spleen and blood are similar in phenotype and function but modified by donor health status. J Immunol. 2011;186(11):6207-6217.
46. Haniffa M, Shin A, Bigley V, et al. Human tissues contain CD141(hi) cross-presenting dendritic cells with functional homology to mouse CD103 (+) nonlymphoid dendritic cells. Immunity. 2012;37(1):60-73.
47. Chu CC, Ali N, Karagiannis P, et al. Resident CD141 (BDCA3)+ dendritic cells in human skin produce IL-10 and induce regulatory T cells that suppress skin inflammation. J Exp Med. 2012;209(5):935-945.
48. Hoeffel G, Ripoche AC, Matheoud D, et al. Antigen crosspresentation by human plasmacytoid dendritic cells. Immunity. 2007;27(3):481-492. (Pubitemid 47418679)
49. Di Pucchio T, Chatterjee B, Smed-Sorensen A, et al. Direct proteasome-independent cross-presentation of viral antigen by plasmacytoid dendritic cells on major histocompatibility complex class I. Nat Immunol. 2008;9(5):551-557. (Pubitemid 351560524)
50. Tel J, Lambeck AJ, Cruz LJ, Tacken PJ, de Vries IJ, Figdor CG. Human plasmacytoid dendritic cells phagocytose, process, and present exogenous particulate antigen. J Immunol. 2010;184(8):4276-4283.
51. van de Ven R, van den Hout MF, Lindenberg JJ, et al. Characterization of four conventional dendritic cell subsets in human skin-draining lymph nodes in relation to T-cell activation. Blood. 2011;118(9):2502-2510.
52. Alexopoulou L, Holt AC, Medzhitov R, Flavell RA. Recognition of double-stranded RNA and activation of NF-kappaB by Toll-like receptor 3. Nature. 2001;413(6857):732-738. (Pubitemid 33009951)
53. Diebold SS, Massacrier C, Akira S, et al. Nucleic acid agonists for Toll-like receptor 7 are defined by the presence of uridine ribonucleotides. Eur J Immunol. 2006;36(12):3256-3267.
54. Jurk M, Heil F, Vollmer J, et al. Human TLR7 or TLR8 independently confer responsiveness to the antiviral compound R-848. Nat Immunol. 2002;3(6):499. (Pubitemid 34669818)
55. Hemmi H, Kaisho T, Takeuchi O, et al. Small anti-viral compounds activate immune cells via the TLR7 MyD88-dependent signaling pathway. Nat Immunol. 2002;3(2):196-200. (Pubitemid 34141451)
56. Klinman DM, Klaschik S, Sato T, Tross D. CpG oligonucleotides as adjuvants for vaccines targeting infectious diseases. Adv Drug Deliv Rev. 2009;61(3):248-255.
57. Krieg AM, Yi AK, Matson S, et al. CpG motifs in bacterial DNA trigger direct B-cell activation. Nature. 1995;374(6522):546-549.
58. Bonifaz L, Bonnyay D, Mahnke K, et al. Efficient targeting of protein antigen to the dendritic cell receptor DEC-205 in the steady state leads to antigen presentation on major histocompatibility complex class I products and peripheral CD8+ T cell tolerance. J Exp Med. 2002;196(12):1627-1638. (Pubitemid 36026474)
59. Li D, Romain G, Flamar AL, et al. Targeting self- and foreign antigens to dendritic cells via DC-ASGPR generates IL-10-producing suppressive CD4+ T cells. J Exp Med. 2012;209(1):109-121.
60. Idoyaga J, Lubkin A, Fiorese C, et al. Comparable T helper 1 (Th1) and CD8 T-cell immunity by targeting HIV gag p24 to CD8 dendritic cells within antibodies to Langerin, DEC205, and Clec9A. Proc Natl Acad Sci U S A. 2011;108(6):2384-2389.
61. Kasturi SP, Skountzou I, Albrecht RA, et al. Programming the magnitude and persistence of antibody responses with innate immunity. Nature. 2011;470(7335):543-547.
62. Maurer T, Heit A, Hochrein H, et al. CpG-DNA aided cross-presentation of soluble antigens by dendritic cells. Eur J Immunol. 2002;32(8):2356-2364. (Pubitemid 34965899)
63. Cho HJ, Takabayashi K, Cheng PM, et al. Immunostimulatory DNA-based vaccines induce cytotoxic lymphocyte activity by a T-helper cell-independent mechanism. Nat Biotechnol. 2000;18(5):509-514. (Pubitemid 30313954)
64. Cruz LJ, Tacken PJ, Fokkink R, et al. Targeted PLGA nano- but not microparticles specifically deliver antigen to human dendritic cells via DC-SIGN in vitro. J Control Release. 2010;144(2):118-126.
65. Zhang Z, Tongchusak S, Mizukami Y, et al. Induction of anti-tumor cytotoxic T cell responses through PLGA-nanoparticle mediated antigen delivery. Biomaterials. 2011;32(14):3666-3678.
66. Thomann JS, Heurtault B, Weidner S, et al. Antitumor activity of liposomal ErbB2/HER2 epitope peptide-based vaccine constructs incorporating TLR agonists and mannose receptor targeting. Biomaterials. 2011;32(20):4574-4583.
67. Speiser DE, Schwarz K, Baumgaertner P, et al. Memory and effector CD8 T-cell responses after nanoparticle vaccination of melanoma patients. J Immunother. 2010;33(8):848-858.
68. Ali OA, Emerich D, Dranoff G, Mooney DJ. In situ regulation of DC subsets and T cells mediates tumor regression in mice. Sci Transl Med. 2009;1(8):8ra19.
69. Kimura Y, Sonehara K, Kuramoto E, et al. Binding of oligoguanylate to scavenger receptors is required for oligonucleotides to augment NK cell activity and induce IFN. J Biochem. 1994;116(5):991-994. (Pubitemid 24354646)
70. Zhu FG, Reich CF, Pisetsky DS. The role of the macrophage scavenger receptor in immune stimulation by bacterial DNA and synthetic oligonucleotides. Immunology. 2001;103(2):226-234. (Pubitemid 32521352)
71. Blander JM, Medzhitov R. Toll-dependent selection of microbial antigens for presentation by dendritic cells. Nature. 2006;440(7085):808-812.
72. Kratky W, Reis ESC, Oxenius A, Sporri R. Direct activation of antigen-presenting cells is required for CD8+ T-cell priming and tumor vaccination. Proc Natl Acad Sci U S A. 2011;108(42):17414-17419.
73. Kastenmuller K, Wille-Reece U, Lindsay RW, et al. Protective T cell immunity in mice following protein-TLR7/8 agonist-conjugate immunization requires aggregation, type I IFN, and multiple DC subsets. J Clin Invest. 2011;121(5):1782-1796.
74. Oh JZ, Kurche JS, Burchill MA, Kedl RM. TLR7 enables cross-presentation by multiple dendritic cell subsets through a type I IFN-dependent pathway. Blood. 2011;118(11):3028-3038.
75. Fuertes MB, Kacha AK, Kline J, et al. Host type I IFN signals are required for antitumor CD8+ T cell responses through CD8{alpha}+ dendritic cells. J Exp Med. 2011;208(10):2005-2016.
76. McCartney SA, Vermi W, Lonardi S, et al. RNA sensor-induced type I IFN prevents diabetes caused by a beta cell-tropic virus in mice. J Clin Invest. 2011;121(4):1497-1507.
77. Piccioli D, Sammicheli C, Tavarini S, et al. Human plasmacytoid dendritic cells are unresponsive to bacterial stimulation and require a novel type of cooperation with myeloid dendritic cells for maturation. Blood. 2009;113(18):4232-4239.
78. Longhi MP, Trumpfheller C, Idoyaga J, et al. Dendritic cells require a systemic type I interferon response to mature and induce CD4+ Th1 immunity with poly IC as adjuvant. J Exp Med. 2009;206(7):1589-1602.
79. Bourquin C, Anz D, Zwiorek K, et al. Targeting CpG oligonucleotides to the lymph node by nanoparticles elicits efficient antitumoral immunity. J Immunol. 2008;181(5):2990-2998.
80. Storni T, Ruedl C, Schwarz K, Schwendener RA, Renner WA, Bachmann MF. Nonmethylated CG motifs packaged into virus-like particles induce protective cytotoxic T cell responses in the absence of systemic side effects. J Immunol. 2004;172(3):1777-1785. (Pubitemid 38116826)
81. Miller LS, Modlin RL. Toll-like receptors in the skin. Semin Immunopathol. 2007;29(1):15-26. (Pubitemid 47596385)
82. Mills KH. TLR-dependent T cell activation in autoimmunity. Nat Rev Immunol. 2011;11(12):807-822.
83. Wu JK, Siller G, Strutton G. Psoriasis induced by topical imiquimod. Australas J Dermatol. 2004;45(1):47-50. (Pubitemid 38315850)
84. Rajan N, Langtry JA. Generalized exacerbation of psoriasis associated with imiquimod cream treatment of superficial basal cell carcinomas. Clin Exp Dermatol. 2006;31(1):140-141.
85. Reddy ST, van der Vlies AJ, Simeoni E, et al. Exploiting lymphatic transport and complement activation in nanoparticle vaccines. Nat Biotechnol. 2007;25(10):1159-1164. (Pubitemid 47538111)
86. Manolova V, Flace A, Bauer M, Schwarz K, Saudan P, Bachmann MF. Nanoparticles target distinct dendritic cell populations according to their size. Eur J Immunol. 2008;38(5):1404-1413.
87. Raphael AP, Prow TW, Crichton ML, Chen X, Fernando GJ, Kendall MA. Targeted, needle-free vaccinations in skin using multilayered, densely-packed dissolving microprojection arrays. Small. 2010;6(16):1785-1793.
88. Langlet C, Tamoutounour S, Henri S, et al. CD64 expression distinguishes monocyte-derived and conventional dendritic cells and reveals their distinct role during intramuscular immunization. J Immunol. 2012;188(4):1751-1760.
89. Jakubzick C, Helft J, Kaplan TJ, Randolph GJ. Optimization of methods to study pulmonary dendritic cell migration reveals distinct capacities of DC subsets to acquire soluble versus particulate antigen. J Immunol Methods. 2008;337(2):121-131.
90. Nembrini C, Stano A, Dane KY, et al. Nanoparticle conjugation of antigen enhances cytotoxic T-cell responses in pulmonary vaccination. Proc Natl Acad Sci U S A. 2011;108(44):E989-E997.
91. Tacken PJ, Zeelenberg IS, Cruz LJ, et al. Targeted delivery of Toll-like receptor ligands to human and mouse dendritic cells strongly enhances adjuvanticity. Blood. 2011;118(26):6836-6844.
92. Jewell CM, Bustamante Lopez SC, Irvine DJ. In situ engineering of the lymph node microenvironment via intranodal injection of adjuvant-releasing polymer particles. Proc Natl Acad Sci U S A. 2011;108(38):15745-15750.
93. Kreutz M, Giquel B, Hu Q, et al. Antibody-antigen- adjuvant conjugates enable co-delivery of antigen and adjuvant to dendritic cells in cis but only have partial targeting specificity. PLoS One. 2012;7(7):e40208.
94. Yang L, Yang H, Rideout K, et al. Engineered lentivector targeting of dendritic cells for in vivo immunization. Nat Biotechnol. 2008;26(3):326-334. (Pubitemid 351355129)
95. Hangalapura BN, Oosterhoff D, de Groot J, et al. Potent antitumor immunity generated by a CD40-targeted adenoviral vaccine. Cancer Res. 2011;71(17):5827-5837.
96. van Broekhoven CL, Parish CR, Demangel C, Britton WJ, Altin JG. Targeting dendritic cells with antigen-containing liposomes: a highly effective procedure for induction of antitumor immunity and for tumor immunotherapy. Cancer Res. 2004;64(12):4357-4365. (Pubitemid 38802444)
97. Bennett CL, Fallah-Arani F, Conlan T, et al. Langerhans cells regulate cutaneous injury by licensing CD8 effector cells recruited to the skin. Blood. 2011;117(26):7063-7069.
98. King IL, Kroenke MA, Segal BM. GM-CSF-dependent, CD1031 dermal dendritic cells play a critical role in Th effector cell differentiation after subcutaneous immunization. J Exp Med. 2010;207(5):953-961.
99. Kretz-Rommel A, Qin F, Dakappagari N, et al. 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. 2007;30(7):715-726. (Pubitemid 47480755)
100. Joffre OP, Sancho D, Zelenay S, Keller AM, Reis e Sousa C. Efficient and versatile manipulation of the peripheral CD4+ T-cell compartment by antigen targeting to DNGR-1/CLEC9A. Eur J Immunol. 2010;40(5):1255-1265.
101. Singh SK, Stephani J, Schaefer M, et al. Targeting glycan modified OVA to murine DC-SIGN transgenic dendritic cells enhances MHC class I and II presentation. Mol Immunol. 2009;47(2-3):164-174.
102. Bozzacco L, Trumpfheller C, Siegal FP, et al. DEC-205 receptor on dendritic cells mediates presentation of HIV gag protein to CD8+ T cells in a spectrum of human MHC I haplotypes. Proc Natl Acad Sci USA. 2007;104(4):1289- 1294. (Pubitemid 46183997)
103. Ramakrishna V, Vasilakos JP, Tario JD Jr., Berger MA, Wallace PK, Keler T. Toll-like receptor activation enhances cell-mediated immunity induced by an antibody vaccine targeting human dendritic cells. J Transl Med. 2007;5:5.
104. Klechevsky E, Morita R, Liu M, et al. Functional specializations of human epidermal Langerhans cells and CD14+ dermal dendritic cells. Immunity. 2008;29(3):497-510.
105. Apostolopoulos V, Pietersz GA, Tsibanis A, et al. Pilot phase III immunotherapy study in early-stage breast cancer patients using oxidized mannan-MUC1 [ISRCTN71711835]. Breast Cancer Res. 2006;8(3):R27.
106. Kwon YJ, James E, Shastri N, et al. In vivo targeting of dendritic cells for activation of cellular immunity using vaccine carriers based on pH-responsive microparticles. Proc Natl Acad Sci USA. 2005;102(51):18264-18268. (Pubitemid 43011215)
107. Joshi MD, Unger WW, van Beelen AJ, et al. DC-SIGN mediated antigen-targeting using glycan-modified liposomes: formulation considerations. Int J Pharm. 2011;416(2):426-432.
108. Singh SK, Streng-Ouwehand I, Litjens M, et al. Design of neo-glycoconjugates that target the mannose receptor and enhance TLR-independent cross-presentation and Th1 polarization. Eur J Immunol. 2011;41(4):916-925.
109. Fukasawa M, Shimizu Y, Shikata K, et al. Liposome oligomannose-coated with neoglycolipid, a new candidate for a safe adjuvant for induction of CD8+ cytotoxic T lymphocytes. FEBS Lett. 1998;441(3):353-356. (Pubitemid 29065313)
110. Badiee A, Davies N, McDonald K, et al. Enhanced delivery of immunoliposomes to human dendritic cells by targeting the multilectin receptor DEC-205. Vaccine. 2007;25(25):4757-4766. (Pubitemid 46818617)
111. Gieseler RK, Marquitan G, Hahn MJ, et al. DC-SIGN-specific liposomal targeting and selective intracellular compound delivery to human myeloid dendritic cells: implications for HIV disease. Scand J Immunol. 2004;59(5):415-424. (Pubitemid 38725550)
112. Korokhov N, de Gruijl TD, Aldrich WA, et al. High efficiency transduction of dendritic cells by adenoviral vectors targeted to DC-SIGN. Cancer Biol Ther. 2005;4(3):289-294. (Pubitemid 41351288)
113. Brandao JG, Scheper RJ, Lougheed SM, et al. CD40-targeted adenoviral gene transfer to dendritic cells through the use of a novel bispecific single-chain Fv antibody enhances cytotoxic T cell activation. Vaccine. 2003;21(19-20):2268- 2272. (Pubitemid 36561319)
114. Belousova N, Korokhov N, Krendelshchikova V, et al. Genetically targeted adenovirus vector directed to CD40-expressing cells. J Virol. 2003;77(21):11367-11377. (Pubitemid 37271635)