Future considerations for dendritic cell immunotherapy against chronic viral infections

References

• W H O. Hepatitis C Fact sheet. Available from: www.who.int/mediacentre/factsheets/fs164/en/accessed 2013
   Google Scholar
• W H O. Hepatitis B Fact Sheets. Available from: http://who.int/mediacentre/factsheets/fs204/en/index.html [Last accessed 3 June 2013]
   Google Scholar
• UNAIDS report on the global AIDS epidemic. Available from: http://www.unaids.org/en/media/unaids/contentassets/documents/epidemiology/2012/gr2012/20121120_UNAIDS_Global_Report_2012_en.pdf [Last accessed 3 June 2013]
   Google Scholar
• Jamma S, Hussain G, Lau DT. Current concepts of HBV/HCV coinfection: coexistence, but not necessarily in harmony. Curr Hepat Rep 2010;9(4):260-9
   Google Scholar
• Lacombe K, Rockstroh J. HIV and viral hepatitis coinfections: advances and challenges. Gut 2012;61(Suppl 1):i47-58
   PubMed Web of Science ®Google Scholar
• Bartenschlager R, Lohmann V, Penin F. The molecular and structural basis of advanced antiviral therapy for hepatitis C virus infection. Nat Rev Microbiol 2013;11(7):482-96
   PubMed Web of Science ®Google Scholar
• Fujii S, Liu K, Smith C, et al. The linkage of innate to adaptive immunity via maturing dendritic cells in vivo requires CD40 ligation in addition to antigen presentation and CD80/86 costimulation. J Exp Med 2004;199(12):1607-18
   PubMed Web of Science ®Google Scholar
• Cella M, Scheidegger D, Palmer-Lehmann K, et al. Ligation of CD40 on dendritic cells triggers production of high levels of interleukin-12 and enhances T cell stimulatory capacity: T-T help via APC activation. J Exp Med 1996;184(2):747-52
   PubMed Web of Science ®Google Scholar
• Pashine A, Valiante NM, Ulmer JB. Targeting the innate immune response with improved vaccine adjuvants. Nat Med 2005;11(4 Suppl):S63-8
   PubMed Web of Science ®Google Scholar
• Tacken PJ, Zeelenberg IS, Cruz LJ, et al. Targeted delivery of TLR ligands to human and mouse dendritic cells strongly enhances adjuvanticity. Blood 2011;118(26):6836-44
   PubMed Web of Science ®Google Scholar
• Rissoan MC, Soumelis V, Kadowaki N, et al. Reciprocal control of T helper cell and dendritic cell differentiation. Science 1999;283(5405):1183-6
   PubMed Web of Science ®Google Scholar
• Ohshima Y, Yang LP, Uchiyama T, et al. OX40 costimulation enhances interleukin-4 (IL-4) expression at priming and promotes the differentiation of naive human CD4(+) T cells into high IL-4-producing effectors. Blood 1998;92(9):3338-45
   Google Scholar
• Freer G, Matteucci D. Influence of dendritic cells on viral pathogenicity. PLoS Pathog 2009;5(7):e1000384
   Google Scholar
• Op den Brouw ML, Binda RS, van Roosmalen MH, et al. Hepatitis B virus surface antigen impairs myeloid dendritic cell function: a possible immune escape mechanism of hepatitis B virus. Immunology 2009;126(2):280-9
   PubMed Web of Science ®Google Scholar
• Higano CS, Schellhammer PF, Small EJ, et al. Integrated data from 2 randomized, double-blind, placebo-controlled, phase 3 trials of active cellular immunotherapy with sipuleucel-T in advanced prostate cancer. Cancer 2009;115(16):3670-9
   PubMed Web of Science ®Google Scholar
• Manz MG, Traver D, Miyamoto T, et al. Dendritic cell potentials of early lymphoid and myeloid progenitors. Blood 2001;97(11):3333-41
   Google Scholar
• Naik SH, Proietto AI, Wilson NS, et al. Cutting edge: generation of splenic CD8+ and CD8- dendritic cell equivalents in Fms-like tyrosine kinase 3 ligand bone marrow cultures. J Immunol 2005;174(11):6592-7
   PubMed Web of Science ®Google Scholar
• Geissmann F, Jung S, Littman DR. Blood monocytes consist of two principal subsets with distinct migratory properties. Immunity 2003;19(1):71-82
   PubMed Web of Science ®Google Scholar
• Nakano H, Lin KL, Yanagita M, et al. Blood-derived inflammatory dendritic cells in lymph nodes stimulate acute T helper type 1 immune responses. Nat Immunol 2009;10(4):394-402
   Google Scholar
• Kool M, Soullie T, van Nimwegen M, et al. Alum adjuvant boosts adaptive immunity by inducing uric acid and activating inflammatory dendritic cells. J Exp Med 2008;205(4):869-82
   PubMed Web of Science ®Google Scholar
• Segura E, Touzot M, Bohineust A, et al. Human inflammatory dendritic cells induce Th17 cell differentiation. Immunity 2013;38(2):336-48
   PubMed Web of Science ®Google Scholar
• 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):1261-71
   PubMed Web of Science ®Google Scholar
• Shortman K, Heath WR. The CD8+ dendritic cell subset. Immunol Rev 2010;234(1):18-31
   PubMedGoogle Scholar
• Villadangos JA, Shortman K. Found in translation: the human equivalent of mouse CD8+ dendritic cells. J Exp Med 2010;207(6):1131-4
   PubMed Web of Science ®Google Scholar
• Vremec D, O’Keeffe M, Wilson A, et al. Factors determining the spontaneous activation of splenic dendritic cells in culture. Innate Immun 2011;17(3):338-52
   Google Scholar
• Maldonado-Lopez R, De Smedt T, Michel P, et al. CD8alpha+ and CD8alpha- subclasses of dendritic cells direct the development of distinct T helper cells in vivo. J Exp Med 1999;189(3):587-92
   PubMed Web of Science ®Google Scholar
• Belz GT, Behrens GM, Smith CM, et al. The CD8alpha(+) dendritic cell is responsible for inducing peripheral self-tolerance to tissue-associated antigens. J Exp Med 2002;196(8):1099-104
   PubMed Web of Science ®Google Scholar
• De Smedt T, Butz E, Smith J, et al. CD8alpha(-) and CD8alpha(+) subclasses of dendritic cells undergo phenotypic and functional maturation in vitro and in vivo. J Leukoc Biol 2001;69(6):951-8
   Google Scholar
• 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):6207-17
   PubMed Web of Science ®Google Scholar
• Nizzoli G, Krietsch J, Weick A, et al. Human CD1c+ dendritic cells secrete high levels of IL-12 and potently prime cytotoxic T-cell responses. Blood 2013;122(6):932-42
   PubMed Web of Science ®Google Scholar
• Lauterbach H, Bathke B, Gilles S, 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(12):2703-17
   PubMed Web of Science ®Google Scholar
• 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):1247-60
   PubMed Web of Science ®Google Scholar
• Segura E, Valladeau-Guilemond J, Donnadieu MH, et al. Characterization of resident and migratory dendritic cells in human lymph nodes. J Exp Med 2012;209(4):653-60
   PubMed Web of Science ®Google Scholar
• Penna G, Sozzani S, Adorini L. Cutting edge: selective usage of chemokine receptors by plasmacytoid dendritic cells. J Immunol 2001;167(4):1862-6
   Google Scholar
• Fearnley DB, Whyte LF, Carnoutsos SA, et al. Monitoring human blood dendritic cell numbers in normal individuals and in stem cell transplantation. Blood 1999;93(2):728-36
   Google Scholar
• Donaghy H, Pozniak A, Gazzard B, et al. Loss of blood CD11c(+) myeloid and CD11c(-) plasmacytoid dendritic cells in patients with HIV-1 infection correlates with HIV-1 RNA virus load. Blood 2001;98(8):2574-6
   Google Scholar
• Venkatachari NJ, Alber S, Watkins SC, Ayyavoo V. HIV-1 infection of DC: evidence for the acquisition of virus particles from infected T cells by antigen uptake mechanism. PLoS One 2009;4(10):e7470
   Google Scholar
• McIlroy D, Autran B, Cheynier R, et al. Infection frequency of dendritic cells and CD4+ T lymphocytes in spleens of human immunodeficiency virus-positive patients. J Virol 1995;69(8):4737-45
   Google Scholar
• Brown KN, Wijewardana V, Liu X, Barratt-Boyes SM. Rapid influx and death of plasmacytoid dendritic cells in lymph nodes mediate depletion in acute simian immunodeficiency virus infection. PLoS Pathog 2009;5(5):e1000413
   PubMed Web of Science ®Google Scholar
• Dillon SM, Friedlander LJ, Rogers LM, et al. Blood myeloid dendritic cells from HIV-1-infected individuals display a proapoptotic profile characterized by decreased Bcl-2 levels and by caspase-3+ frequencies that are associated with levels of plasma viremia and T cell activation in an exploratory study. J Virol 2011;85(1). 397-409
   Google Scholar
• Dolganiuc A, Chang S, Kodys K, et al. Hepatitis C virus (HCV) core protein-induced, monocyte-mediated mechanisms of reduced IFN-alpha and plasmacytoid dendritic cell loss in chronic HCV infection. J Immunol 2006;177(10):6758-68
   PubMed Web of Science ®Google Scholar
• Kanto T, Inoue M, Miyatake H, et al. Reduced numbers and impaired ability of myeloid and plasmacytoid dendritic cells to polarize T helper cells in chronic hepatitis C virus infection. J Infect Dis 2004;190(11):1919-26
   PubMed Web of Science ®Google Scholar
• Goutagny N, Fatmi A, De Ledinghen V, et al. Evidence of viral replication in circulating dendritic cells during hepatitis C virus infection. J Infect Dis 2003;187(12):1951-8
   PubMed Web of Science ®Google Scholar
• Duan XZ, Zhuang H, Wang M, et al. Decreased numbers and impaired function of circulating dendritic cell subsets in patients with chronic hepatitis B infection (R2). J Gastroenterol Hepatol 2005;20(2):234-42
   Google Scholar
• Untergasser A, Zedler U, Langenkamp A, et al. Dendritic cells take up viral antigens but do not support the early steps of hepatitis B virus infection. Hepatology 2006;43(3):539-47
   PubMed Web of Science ®Google Scholar
• Martinet J, Dufeu-Duchesne T, Bruder Costa J, et al. Altered functions of plasmacytoid dendritic cells and reduced cytolytic activity of natural killer cells in patients with chronic HBV infection. Gastroenterology 2012;143(6):1586-96. e1588
   PubMed Web of Science ®Google Scholar
• Tavakoli S, Mederacke I, Herzog et al. Peripheral blood dendritic cells are phenotypically and functionally intact in chronic hepatitis B virus (HBV) infection. Clin Exp Immunol 2008;151(1):61-70
   Google Scholar
• Miller E, Bhardwaj N. Dendritic cell dysregulation during HIV-1 infection. Immunol Rev 2013;254(1):170-89
   PubMedGoogle Scholar
• Chen Y, Hwang SL, Chan VS, et al. Binding of HIV-1 gp120 to DC-SIGN promotes ASK-1-dependent activation-induced apoptosis of human dendritic cells. PLoS Pathog 2013;9(1):e1003100
   Google Scholar
• Fairman P, Angel JB. The effect of human immunodeficiency virus-1 on monocyte-derived dendritic cell maturation and function. Clin Exp Immunol 2012;170(1):101-13
   PubMed Web of Science ®Google Scholar
• Miller EA, Spadaccia MR, O’Brien MP, et al. Plasma factors during chronic HIV-1 infection impair IL-12 secretion by myeloid dendritic cells via a virus-independent pathway. J Acquir Immune Defic Syndr 2012;61(5):535-44
   Google Scholar
• Benlahrech A, Gotch F, Kelleher P, Patterson S. Loss of NK stimulatory capacity by plasmacytoid and monocyte-derived DC but not myeloid DC in HIV-1 infected patients. PLoS One 2011;6(3):e17525
   Google Scholar
• Chaperot L, Blum A, Manches O, et al. Virus or TLR agonists induce TRAIL-mediated cytotoxic activity of plasmacytoid dendritic cells. J Immunol 2006;176(1):248-55
   PubMed Web of Science ®Google Scholar
• Chehimi J, Papasavvas E, Tomescu C, et al. Inability of plasmacytoid dendritic cells to directly lyse HIV-infected autologous CD4+ T cells despite induction of tumor necrosis factor-related apoptosis-inducing ligand. J Virol 2010;84(6):2762-73
   Google Scholar
• Barblu L, Machmach K, Gras C, et al. Plasmacytoid dendritic cells (pDCs) from HIV controllers produce interferon-alpha and differentiate into functional killer pDCs under HIV activation. J Infect Dis 2012;206(5):790-801
   PubMed Web of Science ®Google Scholar
• Herbeuval JP, Grivel JC, Boasso A, et al. CD4+ T-cell death induced by infectious and noninfectious HIV-1: role of type 1 interferon-dependent, TRAIL/DR5-mediated apoptosis. Blood 2005;106(10):3524-31
   PubMed Web of Science ®Google Scholar
• Benlahrech A, Yasmin A, Westrop SJ, et al. Dysregulated immunophenotypic attributes of plasmacytoid but not myeloid dendritic cells in HIV-1 infected individuals in the absence of highly active anti-retroviral therapy. Clin Exp Immunol 2012;170(2):212-21
   Google Scholar
• Favre D, Mold J, Hunt PW, et al. Tryptophan catabolism by indoleamine 2,3-dioxygenase 1 alters the balance of TH17 to regulatory T cells in HIV disease. Sci Transl Med 2010;2(32):32ra36
   PubMed Web of Science ®Google Scholar
• Manches O, Munn D, Fallahi A, et al. HIV-activated human plasmacytoid DCs induce Tregs through an indoleamine 2,3-dioxygenase-dependent mechanism. J Clin Invest 2008;118(10):3431-9
   PubMed Web of Science ®Google Scholar
• Liang CC, Liu CH, Lin YL, et al. Functional impairment of dendritic cells in patients infected with hepatitis C virus genotype 1 who failed peginterferon plus ribavirin therapy. J Med Virol 2011;83(7):1212-20
   Google Scholar
• Levings MK, Gregori S, Tresoldi E, et al. Differentiation of Tr1 cells by immature dendritic cells requires IL-10 but not CD25+CD4+ Tr cells. Blood 2005;105(3):1162-9
   PubMed Web of Science ®Google Scholar
• Longman RS, Talal AH, Jacobson IM, et al. Presence of functional dendritic cells in patients chronically infected with hepatitis C virus. Blood 2004;103(3):1026-9
   Google Scholar
• Ciesek S, Liermann H, Hadem J, et al. Impaired TRAIL-dependent cytotoxicity of CD1c-positive dendritic cells in chronic hepatitis C virus infection. J Viral Hepat 2008;15(3):200-11
   Google Scholar
• Dental C, Florentin J, Aouar B, et al. Hepatitis C virus fails to activate NF-kappaB signaling in plasmacytoid dendritic cells. J Virol 2012;86(2):1090-6
   Google Scholar
• Florentin J, Aouar B, Dental C, et al. HCV glycoprotein E2 is a novel BDCA-2 ligand and acts as an inhibitor of IFN production by plasmacytoid dendritic cells. Blood 2012;120(23):4544-51
   Google Scholar
• Lechner F, Wong DK, Dunbar PR, et al. Analysis of successful immune responses in persons infected with hepatitis C virus. J Exp Med 2000;191(9):1499-512
   Google Scholar
• Zhao L, Tyrrell DL. Myeloid dendritic cells can kill T cells during chronic hepatitis C virus infection. Viral Immunol 2013;26(1):25-39
   Google Scholar
• Shi B, Ren G, Hu Y, et al. HBsAg inhibits IFN-alpha production in plasmacytoid dendritic cells through TNF-alpha and IL-10 induction in monocytes. PLoS One 2012;7(9):e44900
   PubMed Web of Science ®Google Scholar
• Brasel K, McKenna HJ, Morrissey PJ, et al. Hematologic effects of flt3 ligand in vivo in mice. Blood 1996;88(6):2004-12
   Google Scholar
• Esashi E, Wang YH, Perng O, et al. The signal transducer STAT5 inhibits plasmacytoid dendritic cell development by suppressing transcription factor IRF8. Immunity 2008;28(4):509-20
   PubMed Web of Science ®Google Scholar
• Hobo W, Novobrantseva TI, Fredrix H, et al. Improving dendritic cell vaccine immunogenicity by silencing PD-1 ligands using siRNA-lipid nanoparticles combined with antigen mRNA electroporation. Cancer Immunol Immunother 2013;62(2):285-97
   PubMed Web of Science ®Google Scholar
• Yu H, Babiuk LA, van Drunen Littel-van den Hurk S. Strategies for loading dendritic cells with hepatitis C NS5a antigen and inducing protective immunity. J Viral Hepat 2008;15(6):459-70
   Google Scholar
• Maraskovsky E, Daro E, Roux E, et al. In vivo generation of human dendritic cell subsets by Flt3 ligand. Blood 2000;96(3):878-84
   PubMed Web of Science ®Google Scholar
• Reeves RK, Wei Q, Stallworth J, Fultz PN. Systemic dendritic cell mobilization associated with administration of FLT3 ligand to SIV- and SHIV-infected macaques. AIDS Res Hum Retroviruses 2009;25(12):1313-28
   Google Scholar
• Maraskovsky E, Brasel K, Teepe M, et al. Dramatic increase in the numbers of functionally mature dendritic cells in Flt3 ligand-treated mice: multiple dendritic cell subpopulations identified. J Exp Med 1996;184(5):1953-62
   PubMed Web of Science ®Google Scholar
• Klein O, Ebert LM, Zanker D, et al. Flt3 ligand expands CD4+ FoxP3+ regulatory T cells in human subjects. Eur J Immunol 2013;43(2):533-9
   PubMed Web of Science ®Google Scholar
• Jefford M, Schnurr M, Toy T, et al. Functional comparison of DCs generated in vivo with Flt3 ligand or in vitro from blood monocytes: differential regulation of function by specific classes of physiologic stimuli. Blood 2003;102(5):1753-63
   PubMed Web of Science ®Google Scholar
• Davis ID, Chen Q, Morris L, et al. Blood dendritic cells generated with Flt3 ligand and CD40 ligand prime CD8+ T cells efficiently in cancer patients. J Immunother 2006;29(5):499-511
   PubMed Web of Science ®Google Scholar
• Bozzacco L, Trumpfheller C, Huang Y, et al. HIV gag protein is efficiently cross-presented when targeted with an antibody towards the DEC-205 receptor in Flt3 ligand-mobilized murine DC. Eur J Immunol 2010;40(1):36-46
   Google Scholar
• Gehring S, Gregory SH, Wintermeyer P, et al. Generation of immune responses against hepatitis C virus by dendritic cells containing NS5 protein-coated microparticles. Clin Vaccine Immunol 2009;16(2):163-71
   Google Scholar
• Trumpfheller C, Longhi MP, Caskey M, et al. Dendritic cell-targeted protein vaccines: a novel approach to induce T-cell immunity. J Intern Med 2012;271(2):183-92
   PubMed Web of Science ®Google Scholar
• Birkholz K, Schwenkert M, Kellner C, et al. Targeting of DEC-205 on human dendritic cells results in efficient MHC class II-restricted antigen presentation. Blood 2010;116(13):2277-85
   Google Scholar
• Flynn BJ, Kastenmuller K, Wille-Reece U, 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 USA 2011;108(17):7131-6
   PubMed Web of Science ®Google Scholar
• 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):1289-94
   Web of Science ®Google Scholar
• 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 USA 2011;108(6):2384-9
   PubMed Web of Science ®Google Scholar
• Kamphorst AO, Guermonprez P, Dudziak D, Nussenzweig MC. Route of antigen uptake differentially impacts presentation by dendritic cells and activated monocytes. J Immunol 2010;185(6):3426-35
   PubMed Web of Science ®Google Scholar
• Smed-Sorensen A, Lore K. Targeting dendritic cells for improved HIV-1 vaccines. Adv Exp Med Biol 2013;762:263-88
   Google Scholar
• Yusim K, Fischer W, Yoon H, et al. Genotype 1 and global hepatitis C T-cell vaccines designed to optimize coverage of genetic diversity. J Gen Virol 2010;91(Pt 5):1194-206
   Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Luo J, Li J, Chen RL, et al. Autologous dendritic cell vaccine for chronic hepatitis B carriers: a pilot, open label, clinical trial in human volunteers. Vaccine 2010;28(13):2497-504
   PubMed Web of Science ®Google Scholar
• Chen M, Li YG, Zhang DZ, et al. Therapeutic effect of autologous dendritic cell vaccine on patients with chronic hepatitis B: a clinical study. World J Gastroenterol 2005;11(12):1806-8
   PubMed Web of Science ®Google Scholar
• Gowans EJ, Roberts S, Jones K, et al. A phase I clinical trial of dendritic cell immunotherapy in HCV-infected individuals. J Hepatol 2010;53(4):599-607
   Google Scholar
• Garcia F, Climent N, Assoumou L, et al. A therapeutic dendritic cell-based vaccine for HIV-1 infection. J Infect Dis 2011;203(4):473-8
   PubMed Web of Science ®Google Scholar
• Kloverpris H, Karlsson I, Bonde J, et al. Induction of novel CD8+ T-cell responses during chronic untreated HIV-1 infection by immunization with subdominant cytotoxic T-lymphocyte epitopes. AIDS 2009;23(11):1329-40
   PubMed Web of Science ®Google Scholar
• Lu W, Arraes LC, Ferreira WT, Andrieu JM. Therapeutic dendritic-cell vaccine for chronic HIV-1 infection. Nat Med 2004;10(12):1359-65
   PubMed Web of Science ®Google Scholar
• Allard SD, De Keersmaecker B, de Goede AL, et al. A phase I/IIa immunotherapy trial of HIV-1-infected patients with Tat, Rev and Nef expressing dendritic cells followed by treatment interruption. Clin Immunol 2012;142(3):252-68
   PubMed Web of Science ®Google Scholar
• Garcia F, Climent N, Guardo AC, et al. A dendritic cell-based vaccine elicits T cell responses associated with control of HIV-1 replication. Sci Transl Med 2013;5(166):166ra162
   Web of Science ®Google Scholar
• Garcia F, Lejeune M, Climent N, et al. Therapeutic immunization with dendritic cells loaded with heat-inactivated autologous HIV-1 in patients with chronic HIV-1 infection. J Infect Dis 2005;191(10):1680-5
   PubMed Web of Science ®Google Scholar
• Gandhi RT, O’Neill D, Bosch RJ, et al. A randomized therapeutic vaccine trial of canarypox-HIV-pulsed dendritic cells vs. canarypox-HIV alone in HIV-1-infected patients on antiretroviral therapy. Vaccine 2009;27(43):6088-94
   PubMed Web of Science ®Google Scholar