Vaccines to prevent chronic hepatitis C virus infection: Current experimental and preclinical developments

Journal of Gastroenterology

Volumn 42, Issue 6, 2007, Pages 424-432

  Wintermeyer, Philip ^a   Wands, Jack R ^a  

^a Liver Research Center Brown University Medical School   (United States)

Author keywords

HCV infection; Immune responses; Vaccines

Indexed keywords

1,2 DIOLEOYL 3 TRIMETHYLAMMONIOPROPANE; ADENOVIRUS VECTOR; ANTHRAX TOXIN; CPG OLIGODEOXYNUCLEOTIDE; DENDRITIC CELL VACCINE; DNA VACCINE; DRUG CARRIER; GLYCOPROTEIN E1; HEPATITIS C VACCINE; MONTIRELIN; N ACETYLMURAMYLALANYL DEXTRO ISOGLUTAMINYLALANYL DIPALMITOYLPHOSPHATIDYLETHANOLAMINE; NAKED DNA; PLASMID DNA; RECOMBINANT VACCINE; VIRUS PROTEIN;

ANTIVIRAL THERAPY; CLINICAL TRIAL; DNA IMMUNIZATION; HEPATITIS C; HEPATITIS C VIRUS; HUMAN; INFECTION PREVENTION; LIVER CELL CARCINOMA; LIVER CIRRHOSIS; LIVER FIBROSIS; NONHUMAN; PRIORITY JOURNAL; REVIEW; VACCINATION; VIRUS ATTENUATION; VIRUS STRAIN;

ANIMALS; DENDRITIC CELLS; DNA, VIRAL; HEPATITIS C, CHRONIC; HUMANS; VACCINES, DNA; VIRAL HEPATITIS VACCINES; VIRAL PROTEINS;

EID: 34447334805     PISSN: 09441174     EISSN: 14355922     Source Type: Journal    
DOI: 10.1007/s00535-007-2057-5     Document Type: Review

References (98)

1. QL Choo G Kuo AJ Weiner LR Overby DW Bradley M Houghton 1989 Isolation of a cDNA clone derived from a blood-borne non-A, non-B viral hepatitis genome Science 244 359-62 2523562 10.1126/science.2523562
2. DY Chien QL Choo A Tabrizi C Kuo J McFarland K Berger 1992 Diagnosis of hepatitis C virus (HCV) infection using an immunodominant chimeric polyprotein to capture circulating antibodies: Reevaluation of the role of HCV in liver disease Proc Natl Acad Sci USA 89 10011-5 1279666 10.1073/pnas.89.21.10011
3. G Kuo QL Choo HJ Alter GL Gitnick AG Redeker RH Purcell 1989 An assay for circulating antibodies to a major etiologic virus of human non-A, non-B hepatitis Science 244 362-4 2496467 10.1126/science.2496467
4. HJ Alter LB Seeff 2000 Recovery, persistence, and sequelae in hepatitis C virus infection: A perspective on long-term outcome Semin Liver Dis 20 17-35 10895429 10.1055/s-2000-9505
5. P Simmonds 2004 Genetic diversity and evolution of hepatitis C virus - 15 years on J Gen Virol 85 3173-88 15483230 10.1099/vir.0.80401-0
6. ME Lai AP Mazzoleni F Argiolu S De Virgilis A Balestrieri RH Purcell 1994 Hepatitis C virus in multiple episodes of acute hepatitis in polytransfused thalassaemic children Lancet 343 388-90 7905553 10.1016/ S0140-6736(94)91224-6
7. + T cells Curr Opin Immunol 10 444-9 9722921 10.1016/S0952-7915(98)80119-2
8. FV Chisari 2005 Unscrambling hepatitis C virus-host interactions Nature 436 930-2 16107831 10.1038/nature04076 930-2
9. R Thimme D Oldach KM Chang C Steiger SC Ray FV Chisari 2001 Determinants of viral clearance and persistence during acute hepatitis C virus infection J Exp Med 194 1395-406 11714747 10.1084/jem.194.10.1395
10. B Rehermann M Nascimbeni 2005 Immunology of hepatitis B virus and hepatitis C virus infection Nat Rev Immunol 5 215-29 15738952 10.1038/ nri1573
11. BD Lindenbach MJ Evans AJ Syder B Wolk TL Tellinghuisen CC Liu 2005 Complete replication of hepatitis C virus in cell culture Science 309 623-6 15947137 10.1126/science.1114016
12. T Wakita T Pietschmann T Kato T Date M Miyamoto Z Zhao 2005 Production of infectious hepatitis C virus in tissue culture from a cloned viral genome Nat Med 11 791-6 15951748 10.1038/nm1268 Kato T T Date M Miyamoto Z Zhao 2005 Production of infectious hepatitis C virus in tissue culture from a cloned viral genome Nat Med 11 791-6 15951748 10.1038/nm1268
13. J Zhong P Gastaminza G Cheng S Kapadia T Kato DR Burton 2005 Robust hepatitis C virus infection in vitro Proc Natl Acad Sci USA 102 9294-9 15939869 10.1073/pnas.0503596102
14. QL Choo G Kuo R Ralston A Weiner D Chien G Van Nest 1994 Vaccination of chimpanzees against infection by the hepatitis C virus Proc Natl Acad Sci USA 91 1294-8 7509068 10.1073/pnas.91.4.1294
15. M Houghton S Abrignani 2005 Prospects for a vaccine against the hepatitis C virus Nature 436 961-6 16107836 10.1038/nature04081
16. X Forns PJ Payette X Ma W Satterfield G Eder IK Mushahwar 2000 Vaccination of chimpanzees with plasmid DNA encoding the hepatitis C virus (HCV) envelope E2 protein modified the infection after challenge with homologous monoclonal HCV Hepatology 32 618-25 10960458 10.1053/ jhep.2000.9877
17. M Puig ME Major K Mihalik SM Feinstone 2004 Immunization of chimpanzees with an envelope protein-based vaccine enhances specific humoral and cellular immune responses that delay hepatitis C virus infection Vaccine 22 991-1000 15161076 10.1016/j.vaccine.2003.09.010
18. C Rollier E Depla JA Drexhage EJ Verschoor BE Verstrepen A Fatmi 2004 Control of heterologous hepatitis C virus infection in chimpanzees is associated with the quality of vaccine-induced peripheral T-helper immune response J Virol 78 187-96 14671100 10.1128/JVI.78.1.187-196.2004
19. K Rispeter M Lu SE Behrens C Fumiko T Yoshida M Roggendorf 2000 Hepatitis C virus variability: Sequence analysis of an isolate after 10 years of chronic infection Virus Genes 21 179-88 11129633 10.1023/ A:1008135413215
20. YK Shimizu M Hijikata A Iwamoto HJ Alter RH Purcell H Yoshikura 1994 Neutralizing antibodies against hepatitis C virus and the emergence of neutralization escape mutant viruses J Virol 68 1494-500 8107212
21. TF Baumert S Ito DT Wong TJ Liang 1998 Hepatitis C virus structural proteins assemble into viruslike particles in insect cells J Virol 72 3827-36 9557666
22. SH Jeong M Qiao M Nascimbeni Z Hu B Rehermann K Murthy 2004 Immunization with hepatitis C virus-like particles induces humoral and cellular immune responses in nonhuman primates J Virol 78 6995-7003 15194776 10.1128/JVI.78.13.6995-7003.2004
23. M Lechmann K Murata J Satoi J Vergalla TF Baumert TJ Liang 2001 Hepatitis C virus-like particles induce virus-specific humoral and cellular immune responses in mice Hepatology 34 417-23 11481628 10.1053/ jhep.2001.26523
24. K Murata M Lechmann M Qiao T Gunji HJ Alter TJ Liang 2003 Immunization with hepatitis C virus-like particles protects mice from recombinant hepatitis C virus-vaccinia infection Proc Natl Acad Sci U S A 100 6753-8 12748380 10.1073/pnas.1131929100
25. G Leroux-Roels E Depla F Hulstaert L Tobback S Dincq J Desmet 2004 A candidate vaccine based on the hepatitis C E1 protein: Tolerability and immunogenicity in healthy volunteers Vaccine 22 3080-6 15297058 10.1016/ j.vaccine.2004.02.002
26. F Nevens T Roskams H Van Vlierberghe Y Horsmans D Sprengers A Elewaut 2003 A pilot study of therapeutic vaccination with envelope protein E1 in 35 patients with chronic hepatitis C Hepatology 38 1289-96 14578869 10.1053/jhep.2003.50474
27. JA Wolff RW Malone P Williams W Chong G Acsadi A Jani 1990 Direct gene transfer into mouse muscle in vivo Science 247 1465-8 1690918 10.1126/ science.1690918
28. HL Davis ML Michel RG Whalen 1993 DNA-based immunization induces continuous secretion of hepatitis B surface antigen and high levels of circulating antibody Hum Mol Genet 2 1847-51 8281146 10.1093/hmg/ 2.11.1847
29. HL Robinson LA Hunt RG Webster 1993 Protection against a lethal influenza virus challenge by immunization with a haemagglutinin-expressing plasmid DNA Vaccine 11 957-60 8212843 10.1016/ 0264-410X(93)90385-B
30. DC Tang M DeVit SA Johnston 1992 Genetic immunization is a simple method for eliciting an immune response Nature 356 152-4 1545867 10.1038/ 356152a0
31. JB Ulmer JJ Donnelly SE Parker GH Rhodes PL Felgner VJ Dwarki 1993 Heterologous protection against influenza by injection of DNA encoding a viral protein Science 259 1745-9 8456302 10.1126/science.8456302
32. B Wang KE Ugen V Srikantan MG Agadjanyan K Dang Y Refaeli 1993 Gene inoculation generates immune responses against human immunodeficiency virus type 1 Proc Natl Acad Sci USA 90 4156-60 8483929 10.1073/ pnas.90.9.4156
33. ZQ Xiang S Spitalnik M Tran WH Wunner J Cheng HC Ertl 1994 Vaccination with a plasmid vector carrying the rabies virus glycoprotein gene induces protective immunity against rabies virus Virology 199 132-40 8116236 10.1006/viro.1994.1105
34. LM Lagging K Meyer D Hoft M Houghton RB Belshe R Ray 1995 Immune responses to plasmid DNA encoding the hepatitis C virus core protein J Virol 69 5859-63 7637033
35. K Tokushige T Wakita C Pachuk D Moradpour DB Weiner VR Zurawski Jr 1996 Expression and immune response to hepatitis C virus core DNA-based vaccine constructs Hepatology 24 14-20 8707253 10.1002/hep.510240104
36. T Saito GJ Sherman K Kurokohchi ZP Guo M Donets MY Yu 1997 Plasmid DNA-based immunization for hepatitis C virus structural proteins: Immune responses in mice Gastroenterology 112 1321-30 9098018 10.1016/ S0016-5085(97)70146-X
37. GJ Hu RY Wang DS Han HJ Alter JW Shih 1999 Characterization of the humoral and cellular immune responses against hepatitis C virus core induced by DNA-based immunization Vaccine 17 3160-70 10462252 10.1016/ S0264-410X(99)00130-9
38. G Missale R Bertoni V Lamonaca A Valli M Massari C Mori 1996 Different clinical behaviors of acute hepatitis C virus infection are associated with different vigor of the anti-viral cell-mediated immune response J Clin Invest 98 706-14 8698862
39. HM Diepolder R Zachoval RM Hoffmann EA Wierenga T Santantonio MC Jung 1995 Possible mechanism involving T-lymphocyte response to non-structural protein 3 in viral clearance in acute hepatitis C virus infection Lancet 346 1006-7 7475549 10.1016/S0140-6736(95)91691-1
40. J Encke J zu Putlitz M Geissler JR Wands 1998 Genetic immunization generates cellular and humoral immune responses against the nonstructural proteins of the hepatitis C virus in a murine model J Immunol 161 4917-23 9794426
41. EJ Gordon R Bhat Q Liu YF Wang C Tackney AM Prince 2000 Immune responses to hepatitis C virus structural and nonstructural proteins induced by plasmid DNA immunizations J Infect Dis 181 42-50 10608749 10.1086/315162
42. S Calarota G Bratt S Nordlund J Hinkula AC Leandersson E Sandstrom 1998 Cellular cytotoxic response induced by DNA vaccination in HIV-1-infected patients Lancet 351 1320-5 9643795 10.1016/S0140-6736(97)09440-3
43. R Wang DL Doolan TP Le RC Hedstrom KM Coonan Y Charoenvit 1998 Induction of antigen-specific cytotoxic T lymphocytes in humans by a malaria DNA vaccine Science 282 476-80 9774275 10.1126/science.282.5388.476
44. AJ Comerota RC Throm KA Miller T Henry N Chronos J Laird 2002 Naked plasmid DNA encoding fibroblast growth factor type 1 for the treatment of end-stage unreconstructible lower extremity ischemia: Preliminary results of a phase I trial J Vasc Surg 35 930-6 12021709 10.1067/ mva.2002.123677
45. RM Conry DT Curiel TV Strong SE Moore KO Allen DL Barlow 2002 Safety and immunogenicity of a DNA vaccine encoding carcinoembryonic antigen and hepatitis B surface antigen in colorectal carcinoma patients Clin Cancer Res 8 2782-7 12231517
46. JE Epstein EJ Gorak Y Charoenvit R Wang N Freydberg O Osinowo 2002 Safety, tolerability, and lack of antibody responses after administration of a PfCSP DNA malaria vaccine via needle or needle-free jet injection, and comparison of intramuscular and combination intramuscular/intradermal routes Hum Gene Ther 13 1551-60 12228010 10.1089/10430340260201644
47. B Klencke M Matijevic RG Urban JL Lathey ML Hedley M Berry 2002 Encapsulated plasmid DNA treatment for human papillomavirus 16-associated anal dysplasia: A phase I study of ZYC101 Clin Cancer Res 8 1028-37 12006515
48. RR MacGregor JD Boyer RB Ciccarelli RS Ginsberg DB Weiner 2000 Safety and immune responses to a DNA-based human immunodeficiency virus (HIV) type I env/rev vaccine in HIV-infected recipients: Follow-up data J Infect Dis 181 406 10608800 10.1086/315199
49. WE Swain D Heydenburg Fuller MS Wu LJ Barr JT Fuller J Culp 2000 Tolerability and immune responses in humans to a PowderJect DNA vaccine for hepatitis B Dev Biol (Basel) 104 115-9
50. CO Tacket MJ Roy G Widera WF Swain S Broome R Edelman 1999 Phase 1 safety and immune response studies of a DNA vaccine encoding hepatitis B surface antigen delivered by a gene delivery device Vaccine 17 2826-9 10438052 10.1016/S0264-410X(99)00094-8
51. R Weber W Bossart R Cone R Luethy K Moelling 2001 Phase I clinical trial with HIV-1 gp160 plasmid vaccine in HIV-1-infected asymptomatic subjects Eur J Clin Microbiol Infect Dis 20 800-3 11783696 10.1007/s100960000412
52. CA Janeway R Medzhitov Jr 2002 Innate immune recognition Annu Rev Immunol 20 197-216 11861602 10.1146/annurev.immunol.20.083001.084359
53. J Encke J zu Putlitz W Stremmel JR Wands 2003 CpG immuno-stimulatory motifs enhance humoral immune responses against hepatitis C virus core protein after DNA-based immunization Arch Virol 148 435-48 12607097 10.1007/s00705-002-0935-y
54. X Ma X Forns R Gutierrez IK Mushahwar T Wu PJ Payette 2002 DNA-based vaccination against hepatitis C virus (HCV): Effect of expressing different forms of HCV E2 protein and use of CpG-optimized vectors in mice Vaccine 20 3263-71 12213395 10.1016/S0264-410X(02)00304-3
55. H Yu LA Babiuk S van Drunen Littel-van den Hurk 2004 Priming with CpG-enriched plasmid and boosting with protein formulated with CpG oligodeoxynucleotides and Quil A induces strong cellular and humoral immune responses to hepatitis C virus NS3 J Gen Virol 85 1533-43 15166437 10.1099/vir.0.79821-0
56. M Geissler A Gesien K Tokushige JR Wands 1997 Enhancement of cellular and humoral immune responses to hepatitis C virus core protein using DNA-based vaccines augmented with cytokine-expressing plasmids J Immunol 158 1231-7 9013964
57. M Matsui O Moriya T Akatsuka 2003 Enhanced induction of hepatitis C virus-specific cytotoxic T lymphocytes and protective efficacy in mice by DNA vaccination followed by adenovirus boosting in combination with the interleukin-12 expression plasmid Vaccine 21 1629-39 12639484 10.1016/S0264-410X(02)00704-1
58. P Ou-Yang LH Hwang MH Tao BL Chiang DS Chen 2002 Co-delivery of GM-CSF gene enhances the immune responses of hepatitis C viral core protein-expressing DNA vaccine: Role of dendritic cells J Med Virol 66 320-8 11793383 10.1002/jmv.2148
59. J Encke J Bernardin J Geib G Barbakadze R Bujdoso W Stremmel 2006 Genetic vaccination with Flt3-L and GM-CSF as adjuvants: Enhancement of cellular and humoral immune responses that results in protective immunity in a murine model of hepatitis C virus infection World J Gastroenterol 12 7118-25 17131473
60. S Gehring SH Gregory N Kuzushita JR Wands 2005 Type 1 interferon augments DNA-based vaccination against hepatitis C virus core protein J Med Virol 75 249-57 15602727 10.1002/jmv.20264
61. JD Abraham N Himoudi F Kien JL Berland A Codran B Bartosch 2004 Comparative immunogenicity analysis of modified vaccinia Ankara vectors expressing native or modified forms of hepatitis C virus E1 and E2 glycoproteins Vaccine 22 3917-28 15364440 10.1016/j.vaccine.2004.04.005
62. C Brinster M Chen D Boucreux G Paranhos-Baccala P Liljestrom F Lemmonier 2002 Hepatitis C virus non-structural protein 3-specific cellular immune responses following single or combined immunization with DNA or recombinant Semliki Forest virus particles J Gen Virol 83 369-81 11807230
63. D Catalucci E Sporeno A Cirillo G Ciliberto A Nicosia S Colloca 2005 An adenovirus type 5 (Ad5) amplicon-based packaging cell line for production of high-capacity helper-independent deltaE1-E2-E3-E4 Ad5 vectors J Virol 79 6400-9 15858023 10.1128/JVI.79.10.6400-6409.2005
64. P Pancholi M Perkus N Tricoche Q Liu AM Prince 2003 DNA immunization with hepatitis C virus (HCV) polycistronic genes or immunization by HCV DNA priming-recombinant canarypox virus boosting induces immune responses and protection from recombinant HCV-vaccinia virus infection in HLA-A2.1-transgenic mice J Virol 77 382-90 12477843 10.1128/ JVI.77.1.382-390.2003
65. S Perri CE Greer K Thudium B Doe H Legg H Liu 2003 An alphavirus replicon particle chimera derived from Venezuelan equine encephalitis and sindbis viruses is a potent gene-based vaccine delivery vector J Virol 77 10394-403 12970424 10.1128/JVI.77.19.10394-10403.2003
66. T Wuest GW Both AM Prince C Hofmann P Loser 2004 Recombinant ovine atadenovirus induces a strong and sustained T cell response against the hepatitis C virus NS3 antigen in mice Vaccine 22 2717-21 15246602 10.1016/j.vaccine.2004.01.048
67. DT O'Hagan M Singh C Dong M Ugozzoli K Berger E Glazer 2004 Cationic microparticles are a potent delivery system for a HCV DNA vaccine Vaccine 23 672-80 15542189 10.1016/j.vaccine.2004.06.037
68. J Banchereau RM Steinman 1998 Dendritic cells and the control of immunity Nature 392 245-52 9521319 10.1038/32588
69. P Guermonprez J Valladeau L Zitvogel C Thery S Amigorena 2002 Antigen presentation and T cell stimulation by dendritic cells Annu Rev Immunol 20 621-67 11861614 10.1146/annurev.immunol.20.100301.064828
70. S Gurunathan DM Klinman RA Seder 2000 DNA vaccines: Immunology, application, and optimization Annu Rev Immunol 18 927-74 10837079 10.1146/annurev.immunol.18.1.927
71. + T cells after gene gun immunization J Exp Med 188 1075-82 9743526 10.1084/jem.188.6.1075
72. K Inaba JP Metlay MT Crowley RM Steinman 1990 Dendritic cells pulsed with protein antigens in vitro can prime antigen-specific, MHC-restricted T cells in situ J Exp Med 172 631-40 2373994 10.1084/ jem.172.2.631
73. C Ardavin 2003 Origin, precursors and differentiation of mouse dendritic cells Nat Rev Immunol 3 582-90 12876560 10.1038/nri1127
74. D Vremec K Shortman 1997 Dendritic cell subtypes in mouse lymphoid organs: Cross-correlation of surface markers, changes with incubation, and differences among thymus, spleen, and lymph nodes J Immunol 159 565-73 9218570
75. + T cell tolerance J Exp Med 196 1627-38 12486105 10.1084/jem.20021598
76. D Hawiger K Inaba Y Dorsett M Guo K Mahnke M Rivera 2001 Dendritic cells induce peripheral T cell unresponsiveness under steady state conditions in vivo J Exp Med 194 769-79 11560993 10.1084/jem.194.6.769
77. K Mahnke M Guo S Lee H Sepulveda SL Swain M Nussenzweig 2000 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 151 673-84 11062267 10.1083/jcb.151.3.673
78. RM Steinman D Hawiger K Liu L Bonifaz D Bonnyay K Mahnke 2003 Dendritic cell function in vivo during the steady state: A role in peripheral tolerance Ann N Y Acad Sci 987 15-25 12727620
79. + T cells J Clin Invest 94 797-807 8040335
80. MV Dhodapkar RM Steinman M Sapp H Desai C Fossella J Krasovsky 1999 Rapid generation of broad T-cell immunity in humans after a single injection of mature dendritic cells J Clin Invest 104 173-80 10411546
81. S Auffermann-Gretzinger EB Keeffe S Levy 2001 Impaired dendritic cell maturation in patients with chronic, but not resolved, hepatitis C virus infection Blood 97 3171-6 11342445 10.1182/blood.V97.10.3171
82. C Bain A Fatmi F Zoulim JP Zarski C Trepo G Inchauspe 2001 Impaired allostimulatory function of dendritic cells in chronic hepatitis C infection Gastroenterology 120 512-24 11159892 10.1053/gast.2001.21212
83. T Kanto N Hayashi T Takehara T Tatsumi N Kuzushita A Ito 1999 Impaired allostimulatory capacity of peripheral blood dendritic cells recovered from hepatitis C virus-infected individuals J Immunol 162 5584-91 10228041
84. J Banchereau B Schuler-Thurner AK Palucka G Schuler 2001 Dendritic cells as vectors for therapy Cell 106 271-4 11509176 10.1016/ S0092-8674(01)00448-2
85. O Moriya M Matsui M Osorio H Miyazawa CM Rice SM Feinstone 2001 Induction of hepatitis C virus-specific cytotoxic T lymphocytes in mice by immunization with dendritic cells treated with an anthrax toxin fusion protein Vaccine 20 789-96 11738742 10.1016/S0264-410X(01)00407-8
86. M Matsui O Moriya N Abdel-Aziz Y Matsuura T Miyamura T Akatsuka 2002 Induction of hepatitis C virus-specific cytotoxic T lymphocytes in mice by immunization with dendritic cells transduced with replication-defective recombinant adenovirus Vaccine 21 211-20 12450696 10.1016/S0264-410X(02)00460-7
87. H Yu H Huang J Xiang LA Babiuk S van Drunen Littel-van den Hurk 2006 Dendritic cells pulsed with hepatitis C virus NS3 protein induce immune responses and protection from infection with recombinant vaccinia virus expressing NS3 J Gen Virol 87 1-10 16361412 10.1099/vir.0.81423-0
88. S Fujii K Liu C Smith AJ Bonito RM Steinman 2004 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 199 1607-18 15197224 10.1084/jem.20040317
89. N Kuzushita SH Gregory NA Monti R Carlson S Gehring JR Wands 2006 Vaccination with protein-transduced dendritic cells elicits a sustained response to hepatitis C viral antigens Gastroenterology 130 453-64 16472599 10.1053/j.gastro.2005.10.048
90. Y He AA Pimenov JV Nayak J Plowey LD Falo Jr L Huang 2000 Intravenous injection of naked DNA encoding secreted flt3 ligand dramatically increases the number of dendritic cells and natural killer cells in vivo Hum Gene Ther 11 547-54 10724033 10.1089/10430340050015734
91. E Maraskovsky K Brasel M Teepe ER Roux SD Lyman K Shortman 1996 Dramatic increase in the numbers of functionally mature dendritic cells in Flt3 ligand-treated mice: Multiple dendritic cell subpopulations identified J Exp Med 184 1953-62 8920882 10.1084/jem.184.5.1953
92. B Pulendran J Lingappa MK Kennedy J Smith M Teepe A Rudensky 1997 Developmental pathways of dendritic cells in vivo: Distinct function, phenotype, and localization of dendritic cell subsets in FLT3 ligand-treated mice J Immunol 159 2222-31 9278310
93. + and CD8alpha-subclasses of dendritic cells direct the development of distinct T helper cells in vivo J Exp Med 189 587-92 9927520 10.1084/jem.189.3.587
94. J Encke J Findeklee J Geib E Pfaff W Stremmel 2005 Prophylactic and therapeutic vaccination with dendritic cells against hepatitis C virus infection Clin Exp Immunol 142 362-9 16232225 10.1111/ j.1365-2249.2005.02919.x
95. M Xiang C Eisenbach CM Lupu E Ernst W Stremmel J Encke 2006 Induction of antigen-specific immune responses in vivo after vaccination with dendritic cells transduced with adenoviral vectors encoding hepatitis C virus NS3 Viral Immunol 19 210-9 16817764 10.1089/vim.2006.19.210
96. JF Arthur LH Butterfield MD Roth LA Bui SM Kiertscher R Lau 1997 A comparison of gene transfer methods in human dendritic cells Cancer Gene Ther 4 17-25 9012447
97. AS Irvine PK Trinder DL Laughton H Ketteringham RH McDermott SC Reid 2000 Efficient nonviral transfection of dendritic cells and their use for in vivo immunization Nat Biotechnol 18 1273-8 11101806 10.1038/82383
98. + T cells and antiviral immunity Immunity 20 47-58 14738764 10.1016/S1074-7613(03)00353-4