Human dendritic cell subsets in vaccination

Current Opinion in Immunology

Volumn 25, Issue 3, 2013, Pages 396-402

  Palucka, Karolina ^a   Banchereau, Jacques ^a  

^a BAYLOR INSTITUTE FOR IMMUNOLOGY RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; CD8 ANTIGEN; DENDRITIC CELL VACCINE; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; HUMAN IMMUNODEFICIENCY VIRUS ANTIGEN; IMMUNOLOGICAL ADJUVANT; INACTIVATED VACCINE; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; NY ESO1 CANCER ANTIGEN; PEPTIDE VACCINE; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 3 AGONIST; TOLL LIKE RECEPTOR 7 AGONIST; TOLL LIKE RECEPTOR 8 AGONIST; TOLL LIKE RECEPTOR AGONIST; UNCLASSIFIED DRUG; VIRUS VECTOR;

ADAPTIVE IMMUNITY; ALLERGIC ENCEPHALOMYELITIS; ANTIGEN SPECIFICITY; AUTOIMMUNE DISEASE; B LYMPHOCYTE DIFFERENTIATION; CANCER IMMUNOTHERAPY; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL EXPANSION; CELL FUNCTION; CELL SUBPOPULATION; CELLULAR IMMUNITY; CYTOTOXIC T LYMPHOCYTE; DENDRITIC CELL; DRUG EFFICACY; DRUG MEGADOSE; HELPER CELL; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; HUMORAL IMMUNITY; IMMUNOGENICITY; IMMUNOLOGICAL TOLERANCE; IMMUNOREGULATION; IN VIVO STUDY; INNATE IMMUNITY; MALIGNANT NEOPLASTIC DISEASE; MELANOMA; MEMORY CELL; NONHUMAN; REVIEW; T LYMPHOCYTE SUBPOPULATION; TARGET CELL; VACCINATION; VIRUS LOAD;

ANIMALS; CELL- AND TISSUE-BASED THERAPY; DENDRITIC CELLS; HUMANS; IMMUNITY, CELLULAR; IMMUNITY, HUMORAL; VACCINATION;

EID: 84879237232     PISSN: 09527915     EISSN: 18790372     Source Type: Journal    
DOI: 10.1016/j.coi.2013.05.001     Document Type: Review

References (92)

1. Banchereau J., Steinman R.M. Dendritic cells and the control of immunity. Nature 1998, 392:245-252.
2. Steinman R.M. Decisions about dendritic cells: past, present, and future. Annu Rev Immunol 2012, 30:1-22.
3. Bar-On L., Jung S. Defining dendritic cells by conditional and constitutive cell ablation. Immunol Rev 2010, 234:76-89.
4. Nabel G.J. Designing tomorrow's vaccines. N Engl J Med 2013, 368:551-560.
5. Hashimoto D., Miller J., Merad M. Dendritic cell and macrophage heterogeneity in vivo. Immunity 2011, 35:323-335.
6. Reis e Sousa C. Harnessing dendritic cells. Semin Immunol 2011, 23:1.
7. Dzionek A., Fuchs A., Schmidt P., Cremer S., Zysk M., Miltenyi S., Buck D.W., Schmitz J. BDCA-2, BDCA-3, and BDCA-4: three markers for distinct subsets of dendritic cells in human peripheral blood. J Immunol 2000, 165:6037-6046.
8. Dzionek A., Sohma Y., Nagafune J., Cella M., Colonna M., Facchetti F., Gunther G., Johnston I., Lanzavecchia A., Nagasaka T., et al. BDCA-2, a novel plasmacytoid dendritic cell-specific type II C-type lectin, mediates antigen capture and is a potent inhibitor of interferon alpha/beta induction. J Exp Med 2001, 194:1823-1834.
9. MacDonald K.P., Munster D.J., Clark G.J., Dzionek A., Schmitz J., Hart D.N. Characterization of human blood dendritic cell subsets. Blood 2002, 100:4512-4520.
10. Lauterbach H., Bathke B., Gilles S., Traidl-Hoffmann C., Luber C.A., Fejer G., Freudenberg M.A., Davey G.M., Vremec D., Kallies A., et al. Mouse CD8alpha+ DCs and human BDCA3+ DCs are major producers of IFN-lambda in response to poly IC. J Exp Med 2010, 207:2703-2717.
11. Crozat K., Guiton R., Contreras V., Feuillet V., Dutertre C.A., Ventre E., Vu Manh T.P., Baranek T., Storset A.K., Marvel J., 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, 207:1283-1292.
12. Jongbloed S.L., Kassianos A.J., McDonald K.J., Clark G.J., Ju X., Angel C.E., Chen C.J., Dunbar P.R., Wadley R.B., Jeet V., 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, 207:1247-1260.
13. Bachem A., Guttler S., Hartung E., Ebstein F., Schaefer M., Tannert A., Salama A., Movassaghi K., Opitz C., Mages H.W., 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, 207:1273-1281.
14. Poulin L.F., Salio M., Griessinger E., Anjos-Afonso F., Craciun L., Chen J.L., Keller A.M., Joffre O., Zelenay S., Nye E., et al. Characterization of human DNGR-1+ BDCA3+ leukocytes as putative equivalents of mouse CD8alpha+ dendritic cells. J Exp Med 2010, 207:1261-1271.
15. Mittag D., Proietto A.I., Loudovaris T., Mannering S.I., Vremec D., Shortman K., Wu L., Harrison L.C. Human dendritic cell subsets from spleen and blood are similar in phenotype and function but modified by donor health status. J Immunol 2011, 186:6207-6217.
16. Haniffa M., Shin A., Bigley V., McGovern N., Teo P., See P., Wasan P.S., Wang X.N., Malinarich F., Malleret B., et al. Human tissues contain CD141(hi) cross-presenting dendritic cells with functional homology to mouse CD103(+) nonlymphoid dendritic cells. Immunity 2012, 37:60-73.
17. Klechevsky E., Morita R., Liu M., Cao Y., Coquery S., Thompson-Snipes L., Briere F., Chaussabel D., Zurawski G., Palucka A.K., et al. Functional specializations of human epidermal Langerhans cells and CD14+ dermal dendritic cells. Immunity 2008, 29:497-510.
18. Klechevsky E., Flamar A.L., Cao Y., Blanck J.P., Liu M., O'Bar A., Agouna-Deciat O., Klucar P., Thompson-Snipes L., Zurawski S., et al. Cross-priming CD8+ T cells by targeting antigens to human dendritic cells through DCIR. Blood 2010, 116:1685-1697.
19. Barber G.N. Innate immune DNA sensing pathways: STING, AIMII and the regulation of interferon production and inflammatory responses. Curr Opin Immunol 2011, 23:10-20.
20. Desmet C.J., Ishii K.J. Nucleic acid sensing at the interface between innate and adaptive immunity in vaccination. Nat Rev Immunol 2012, 12:479-491.
21. Zhang Z., Kim T., Bao M., Facchinetti V., Jung S.Y., Ghaffari A.A., Qin J., Cheng G., Liu Y.J. DDX1, DDX21, and DHX36 helicases form a complex with the adaptor molecule TRIF to sense dsRNA in dendritic cells. Immunity 2011, 34:866-878.
22. Zhang Z., Bao M., Lu N., Weng L., Yuan B., Liu Y.J. The E3 ubiquitin ligase TRIM21 negatively regulates the innate immune response to intracellular double-stranded DNA. Nat Immunol 2013, 14:172-178.
23. Bluestone J.A., Mackay C.R., O'Shea J.J., Stockinger B. The functional plasticity of T cell subsets. Nat Rev Immunol 2009, 9:811-816.
24. Ma C.S., Deenick E.K., Batten M., Tangye S.G. The origins, function, and regulation of T follicular helper cells. J Exp Med 2012, 209:1241-1253.
25. Vinuesa C.G., Cyster J.G. How T cells earn the follicular rite of passage. Immunity 2011, 35:671-680.
26. Morita R., Schmitt N., Bentebibel S.E., Ranganathan R., Bourdery L., Zurawski G., Foucat E., Dullaers M., Oh S., Sabzghabaei N., et al. Human blood CXCR5(+)CD4(+) T cells are counterparts of T follicular cells and contain specific subsets that differentially support antibody secretion. Immunity 2011, 34:108-121.
27. Schmitt N., Morita R., Bourdery L., Bentebibel S.E., Zurawski S.M., Banchereau J., Ueno H. Human dendritic cells induce the differentiation of interleukin-21-producing T follicular helper-like cells through interleukin-12. Immunity 2009, 31:158-169.
28. Schmitt N., Bustamante J., Bourdery L., Bentebibel S.E., Boisson-Dupuis S., Hamlin F., Tran M.V., Blankenship D., Pascual V., Savino D.A., et al. IL-12 receptor beta1 deficiency alters in vivo T follicular helper cell response in humans. Blood 2013, 121:3375-3385.
29. Bentebibel S.E., Lopez S., Obermoser G., Schmitt N., Mueller C., Harrod C., Flano E., Mejias A., Albrecht R.A., Blankenship D., et al. Induction of ICOS+ CXCR3+ CXCR5+ TH cells correlates with antibody responses to influenza vaccination. Sci Transl Med 2013, 5. 176ra132.
30. Kaech S.M., Cui W. Transcriptional control of effector and memory CD8+ T cell differentiation. Nat Rev Immunol 2012, 12:749-761.
31. Appay V., Douek D.C., Price D.A. CD8+ T cell efficacy in vaccination and disease. Nat Med 2008, 14:623-628.
32. Joffre O.P., Segura E., Savina A., Amigorena S. Cross-presentation by dendritic cells. Nat Rev Immunol 2012, 12:557-569.
33. Caux C., Massacrier C., Vanbervliet B., Dubois B., Durand I., Cella M., Lanzavecchia A., Banchereau J. CD34+ hematopoietic progenitors from human cord blood differentiate along two independent dendritic cell pathways in response to granulocyte-macrophage colony-stimulating factor plus tumor necrosis factor alpha: II. Functional analysis. Blood 1997, 90:1458-1470.
34. Banchereau J., Thompson-Snipes L., Zurawski S., Blanck J.P., Cao Y., Clayton S., Gorvel J.P., Zurawski G., Klechevsky E. The differential production of cytokines by human Langerhans cells and dermal CD14(+) DCs controls CTL priming. Blood 2012, 119:5742-5749.
35. Romano E., Cotari J.W., Barreira da Silva R., Betts B.C., Chung D.J., Avogadri F., Fink M.J., St Angelo E.T., Mehrara B., Heller G., et al. Human Langerhans cells use an IL-15R-alpha/IL-15/pSTAT5-dependent mechanism to break T-cell tolerance against the self-differentiation tumor antigen WT1. Blood 2012, 119:5182-5190.
36. van der Aar A.M., de Groot R., Sanchez-Hernandez M., Taanman E.W., van Lier R.A., Teunissen M.B., de Jong E.C., Kapsenberg M.L. Cutting edge: virus selectively primes human langerhans cells for CD70 expression promoting CD8+ T cell responses. J Immunol 2011, 187:3488-3492.
37. Banchereau J., Zurawski S., Thompson-Snipes L., Blanck J.P., Clayton S., Munk A., Cao Y., Wang Z., Khandelwal S., Hu J., et al. Immunoglobulin-like transcript receptors on human dermal CD14+ dendritic cells act as a CD8-antagonist to control cytotoxic T cell priming. Proc Natl Acad Sci U S A 2012, 109:18885-18890.
38. Igyarto B.Z., Haley K., Ortner D., Bobr A., Gerami-Nejad M., Edelson B.T., Zurawski S.M., Malissen B., Zurawski G., Berman J., et al. Skin-resident murine dendritic cell subsets promote distinct and opposing antigen-specific T helper cell responses. Immunity 2011, 35:260-272.
39. Segura E., Valladeau-Guilemond J., Donnadieu M.H., Sastre-Garau X., Soumelis V., Amigorena S Characterization of resident and migratory dendritic cells in human lymph nodes. J Exp Med 2012, 209:653-660.
40. Jiang X., Clark R.A., Liu L., Wagers A.J., Fuhlbrigge R.C., Kupper T.S. Skin infection generates non-migratory memory CD8+ T(RM) cells providing global skin immunity. Nature 2012, 483:227-231.
41. Mueller S.N., Gebhardt T., Carbone F.R., Heath WR Memory T cell subsets, migration patterns, and tissue residence. Annu Rev Immunol 2012, 31:137-161.
42. Gebhardt T., Wakim L.M., Eidsmo L., Reading P.C., Heath W.R., Carbone F.R. Memory T cells in nonlymphoid tissue that provide enhanced local immunity during infection with herpes simplex virus. Nat Immunol 2009, 10:524-530.
43. Liu L., Zhong Q., Tian T., Dubin K., Athale S.K., Kupper T.S. Epidermal injury and infection during poxvirus immunization is crucial for the generation of highly protective T cell-mediated immunity. Nat Med 2010, 16:224-227.
44. Clark R.A., Watanabe R., Teague J.E., Schlapbach C., Tawa M.C., Adams N., Dorosario A.A., Chaney K.S., Cutler C.S., Leboeuf N.R., et al. Skin effector memory T cells do not recirculate and provide immune protection in alemtuzumab-treated CTCL patients. Sci Transl Med 2012, 4. 117ra117.
45. Shaw S.K., Brenner M.B. The beta 7 integrins in mucosal homing and retention. Semin Immunol 1995, 7:335-342.
46. Sheridan B.S., Lefrancois L. Regional and mucosal memory T cells. Nat Immunol 2011, 12:485-491.
47. Le Floc'h A., Jalil A., Vergnon I., Le Maux Chansac B., Lazar V., Bismuth G., Chouaib S., Mami-Chouaib F. Alpha E beta 7 integrin interaction with E-cadherin promotes antitumor CTL activity by triggering lytic granule polarization and exocytosis. J Exp Med 2007, 204:559-570.
48. Seneschal J., Clark R.A., Gehad A., Baecher-Allan C.M., Kupper T.S. Human epidermal Langerhans cells maintain immune homeostasis in skin by activating skin resident regulatory T cells. Immunity 2012, 36:873-884.
49. Sandoval F., Terme M., Nizard M., Badoual C., Bureau M.F., Freyburger L., Clement O., Marcheteau E., Gey A., Fraisse G., et al. Mucosal imprinting of vaccine-induced CD8+ T cells is crucial to inhibit the growth of mucosal tumors. Sci Transl Med 2013, 5. 172ra120.
50. Le D.T., Pardoll D.M., Jaffee E.M. Cellular vaccine approaches. Cancer J 2010, 16:304-310.
51. Le D.T., Dubenksy T.W., Brockstedt D.G. Clinical development of Listeria monocytogenes-based immunotherapies. Semin Oncol 2012, 39:311-322.
52. Palucka K., Banchereau J. Cancer immunotherapy via dendritic cells. Nat Rev Cancer 2012, 12:265-277.
53. Schuler G. Dendritic cells in cancer immunotherapy. Eur J Immunol 2010, 40:2123-2130.
54. Kalinski P., Edington H., Zeh H.J., Okada H., Butterfield L.H., Kirkwood J.M., Bartlett D.L. Dendritic cells in cancer immunotherapy: vaccines or autologous transplants?. Immunol Res 2011, 50:235-247.
55. Galluzzi L., Senovilla L., Vacchelli E., Eggermont A., Fridman W.H., Galon J., Sautes-Fridman C., Tartour E., Zitvogel L., Kroemer G. Trial watch: dendritic cell-based interventions for cancer therapy. Oncoimmunology 2012, 1:1111-1134.
56. Aarntzen E.H., De Vries I.J., Lesterhuis W.J., Schuurhuis D., Jacobs J.F., Bol K., Schreibelt G., Mus R., De Wilt J.H., Haanen J.B., et al. Targeting CD4(+) T-helper cells improves the induction of antitumor responses in dendritic cell-based vaccination. Cancer Res 2013, 73:19-29.
57. Sharma A., Koldovsky U., Xu S., Mick R., Roses R., Fitzpatrick E., Weinstein S., Nisenbaum H., Levine B.L., Fox K., et al. HER-2 pulsed dendritic cell vaccine can eliminate HER-2 expression and impact ductal carcinoma in situ. Cancer 2012, 118:4354-4362.
58. Kandalaft L.E., Powell D.J., Chiang C.L., Tanyi J., Kim S., Bosch M., Montone K., Mick R., Levine B.L., Torigian D.A., et al. Autologous lysate-pulsed dendritic cell vaccination followed by adoptive transfer of vaccine-primed ex vivo co-stimulated T cells in recurrent ovarian cancer. Oncoimmunology 2013, 2:e22664.
59. Tel J., Aarntzen E.H., Baba T., Schreibelt G., Schulte B.M., Benitez-Ribas D., Boerman O.C., Croockewit S., Oyen W.J., van Rossum M., et al. Natural human plasmacytoid dendritic cells induce antigen-specific T-cell responses in melanoma patients. Cancer Res 2013, 73:1063-1075.
60. Gajewski T.F. Failure at the effector phase: immune barriers at the level of the melanoma tumor microenvironment. Clin Cancer Res 2007, 13:5256-5261.
61. Fuertes M.B., Kacha A.K., Kline J., Woo S.R., Kranz D.M., Murphy K.M., Gajewski T.F. Host type I IFN signals are required for antitumor CD8+ T cell responses through CD8{alpha}+ dendritic cells. J Exp Med 2011, 208:2005-2016.
62. Levy Y. Preparation for antiretroviral interruption by boosting the immune system. Curr Opin HIV AIDS 2008, 3:118-123.
63. Johnston M.I., Fauci A.S. HIV vaccine development - improving on natural immunity. N Engl J Med 2011, 365:873-875.
64. Saunders K.O., Rudicell R.S., Nabel G.J. The design and evaluation of HIV-1 vaccines. AIDS 2012, 26:1293-1302.
65. Garcia F., Routy J.P. Challenges in dendritic cells-based therapeutic vaccination in HIV-1 infection Workshop in dendritic cell-based vaccine clinical trials in HIV-1. Vaccine 2011, 29:6454-6463.
66. Lu W., Arraes L.C., Ferreira W.T., Andrieu J.M. Therapeutic dendritic-cell vaccine for chronic HIV-1 infection. Nat Med 2004, 10:1359-1365.
67. Garcia F., Climent N., Guardo A.C., Gil C., Leon A., Autran B., Lifson J.D., Martinez-Picado J., Dalmau J., Clotet B., et al. A dendritic cell-based vaccine elicits T cell responses associated with control of HIV-1 replication. Sci Transl Med 2013, 5. 166ra162.
68. Van Gulck E., Vlieghe E., Vekemans M., Van Tendeloo V.F., Van De Velde A., Smits E., Anguille S., Cools N., Goossens H., Mertens L., et al. mRNA-based dendritic cell vaccination induces potent antiviral T-cell responses in HIV-1-infected patients. AIDS 2012, 26:F1-F12.
69. Banchereau J., Pascual V: Type I interferon in systemic lupus erythematosus and other autoimmune diseases. Immunity 2006, 25:383-392.
70. Steinman R.M., Hawiger D., Nussenzweig M.C. Tolerogenic dendritic cells. Annu Rev Immunol 2003, 21:685-711.
71. Gross C.C., Wiendl H. Dendritic cell vaccination in autoimmune disease. Curr Opin Rheumatol 2013, 25:268-274.
72. Gross C.C., Jonuleit H., Wiendl H. Fulfilling the dream: tolerogenic dendritic cells to treat multiple sclerosis. Eur J Immunol 2012, 42:569-572.
73. Idoyaga J., Fiorese C., Zbytnuik L., Lubkin A., Miller J., Malissen B., Mucida D., Merad M., Steinman R.M. Specialized role of migratory dendritic cells in peripheral tolerance induction. J Clin Invest 2013, 123:844-854.
74. Mukhopadhaya A., Hanafusa T., Jarchum I., Chen Y.G., Iwai Y., Serreze D.V., Steinman R.M., Tarbell K.V., DiLorenzo T.P. Selective delivery of beta cell antigen to dendritic cells in vivo leads to deletion and tolerance of autoreactive CD8+ T cells in NOD mice. Proc Natl Acad Sci U S A 2008, 105:6374-6379.
75. Hawiger D., Inaba K., Dorsett Y., Guo K., Mahnke K., Rivera M., Ravetch J.V., Steinman R.M., Nussenzweig M.C. Dendritic cells induce peripheral T cell unresponsiveness under steady state conditions in vivo. J Exp Med 2001, 194:769-780.
76. Bonifaz L., Bonnyay D., Mahnke K., Rivera M., Nussenzweig M.C., Steinman R.M. 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, 196:1627-1638.
77. Soares H., Waechter H., Glaichenhaus N., Mougneau E., Yagita H., Mizenina O., Dudziak D., Nussenzweig M.C., Steinman R.M. subset of dendritic cells induces CD4+ T cells to produce IFN-{gamma} by an IL-12-independent but CD70-dependent mechanism in vivo. J Exp Med 2007, 204:1095-1106.
78. Meyer-Wentrup F., Cambi A., Joosten B., Looman M.W., de Vries I.J., Figdor C.G., Adema G.J. DCIR is endocytosed into human dendritic cells and inhibits TLR8-mediated cytokine production. J Leukoc Biol 2009, 85:518-525.
79. Dakappagari N., Maruyama T., Renshaw M., Tacken P., Figdor C., Torensma R., Wild M.A., Wu D., Bowdish K., Kretz-Rommel A. Internalizing antibodies to the C-type lectins, L-SIGN and DC-SIGN, inhibit viral glycoprotein binding and deliver antigen to human dendritic cells for the induction of T cell responses. J Immunol 2006, 176:426-440.
80. Ni L., Gayet I., Zurawski S., Duluc D., Flamar A.L., Li X.H., O'Bar A., Clayton S., Palucka A.K., Zurawski G., et al. Concomitant activation and antigen uptake via human dectin-1 results in potent antigen-specific CD8+ T cell responses. J Immunol 2010, 185:3504-3513.
81. Sancho D., Mourao-Sa D., Joffre O.P., Schulz O., Rogers N.C., Pennington D.J., Carlyle J.R., Reis e Sousa C. Tumor therapy in mice via antigen targeting to a novel. DC-restricted C-type lectin. J Clin Invest 2008, 118:2098-2110.
82. Flacher V., Sparber F., Tripp C.H., Romani N., Stoitzner P. Targeting of epidermal Langerhans cells with antigenic proteins: attempts to harness their properties for immunotherapy. Cancer Immunol Immunother 2009, 58:1137-1147.
83. Tacken P.J., Figdor C.G. Targeted antigen delivery and activation of dendritic cells in vivo: steps towards cost effective vaccines. Semin Immunol 2011, 23:12-20.
84. Dudziak D., Kamphorst A.O., Heidkamp G.F., Buchholz V.R., Trumpfheller C., Yamazaki S., Cheong C., Liu K., Lee H.W., Park C.G., et al. Differential antigen processing by dendritic cell subsets in vivo. Science 2007, 315:107-111.
85. Soares H., Waechter H., Glaichenhaus N., Mougneau E., Yagita H., Mizenina O., Dudziak D., Nussenzweig M.C., Steinman R.M. A subset of dendritic cells induces CD4+ T cells to produce IFN-gamma by an IL-12-independent but CD70-dependent mechanism in vivo. J Exp Med 2007, 204:1095-1106.
86. Caminschi I., Vremec D., Ahmet F., Lahoud M.H., Villadangos J.A., Murphy K.M., Heath W.R., Shortman K. Antibody responses initiated by Clec9A-bearing dendritic cells in normal and Batf3(-/-) mice. Mol Immunol 2012, 50:9-17.
87. Lahoud M.H., Ahmet F., Kitsoulis S., Wan S.S., Vremec D., Lee C.N., Phipson B., Shi W., Smyth G.K., Lew A.M., et al. Targeting antigen to mouse dendritic cells via Clec9A induces potent CD4 T cell responses biased toward a follicular helper phenotype. J Immunol 2011, 187:842-850.
88. Sancho D., Joffre O.P., Keller A.M., Rogers N.C., Martinez D., Hernanz-Falcon P., Rosewell I., Reis e Sousa C. Identification of a dendritic cell receptor that couples sensing of necrosis to immunity. Nature 2009, 458:899-903.
89. Li D., Romain G., Flamar A.L., Duluc D., Dullaers M., Li X.H., Zurawski S., Bosquet N., Palucka A.K., Le Grand R., 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, 209:109-121.
90. Chatterjee B., Smed-Sorensen A., Cohn L., Chalouni C., Vandlen R., Lee B.C., Widger J., Keler T., Delamarre L., Mellman I. Internalization and endosomal degradation of receptor-bound antigens regulate the efficiency of cross presentation by human dendritic cells. Blood 2012, 120:2011-2020.
91. Flynn B.J., Kastenmuller K., Wille-Reece U., Tomaras G.D., Alam M., Lindsay R.W., Salazar A.M., Perdiguero B., Gomez C.E., Wagner R., et al. 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 2011, 108:7131-7136.
92. Morse M.A., Chapman R., Powderly J., Blackwell K., Keler T., Green J., Riggs R., He L.Z., Ramakrishna V., Vitale L., 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, 17:4844-4853.