Home LiteratureArticle Details
PMID: 16505141 Published · ppublish English Journal Article Research Support, N.I.H., Extramural

Intensified and protective CD4+ T cell immunity in mice with anti-dendritic cell HIV gag fusion antibody vaccine.

The Journal of experimental medicine ·Vol. 203 ·No. 3 ·2006-03-20 ·Pages 607-17

Trumpfheller C, Finke JS, López CB, Moran TM, Moltedo B, Soares H, Huang Y, Schlesinger SJ, Park CG, Nussenzweig MC, Granelli-Piperno A, Steinman RM

Abstract

Current human immunodeficiency virus (HIV) vaccine approaches emphasize prime boost strategies comprising multiple doses of DNA vaccine and recombinant viral vectors. We are developing a protein-based approach that directly harnesses principles for generating T cell immunity. Vaccine is delivered to maturing dendritic cells in lymphoid tissue by engineering protein antigen into an antibody to DEC-205, a receptor for antigen presentation. Here we characterize the CD4+ T cell immune response to HIV gag and compare efficacy with other vaccine strategies in a single dose. DEC-205-targeted HIV gag p24 or p41 induces stronger CD4+ T cell immunity relative to high doses of gag protein, HIV gag plasmid DNA, or recombinant adenovirus-gag. High frequencies of interferon (IFN)-gamma- and interleukin 2-producing CD4+ T cells are elicited, including double cytokine-producing cells. In addition, the response is broad because the primed mice respond to an array of peptides in different major histocompatibility complex haplotypes. Long-lived T cell memory is observed. After subcutaneous vaccination, CD4+ and IFN-gamma-dependent protection develops to a challenge with recombinant vaccinia-gag virus at a mucosal surface, the airway. We suggest that a DEC-targeted vaccine, in part because of an unusually strong and protective CD4+ T cell response, will improve vaccine efficacy as a stand-alone approach or with other modalities.

MeSH Terms
AIDS Vaccines/administration & dosage,genetics,immunology Adenoviridae Animals Antibodies, Monoclonal/administration & dosage,genetics,immunology Antigen Presentation/drug effects,immunology Antigens, CD/genetics,immunology CD4-Positive T-Lymphocytes/immunology Dendritic Cells/immunology Dose-Response Relationship, Immunologic Gene Products, gag/administration & dosage,genetics,immunology Genetic Vectors/administration & dosage,genetics,immunology HIV-1/genetics,immunology Haplotypes/genetics,immunology Humans Immunity, Mucosal/drug effects,immunology Immunologic Memory/drug effects,immunology Injections, Subcutaneous Lectins, C-Type/deficiency,genetics,immunology Major Histocompatibility Complex/immunology Mice Mice, Inbred BALB C Mice, Inbred C3H Mice, Knockout Minor Histocompatibility Antigens Receptors, Cell Surface/deficiency,genetics,immunology Recombinant Fusion Proteins/administration & dosage,genetics,immunology Vaccinia virus
Chemicals
AIDS Vaccines Antibodies, Monoclonal Antigens, CD DEC-205 receptor Gene Products, gag Lectins, C-Type Minor Histocompatibility Antigens Receptors, Cell Surface Recombinant Fusion Proteins
Authors & Affiliations
12 authors, click to expand affiliations / ORCID
Trumpfheller Christine
Laboratory of Cellular Physiology and Immunology, Chris Browne Center for Immunology and Immune Diseases, The Rockefeller University, New York, NY 10021, USA.
Finke Jennifer S
López Carolina B
Moran Thomas M
Moltedo Bruno
Soares Helena
Huang Yaoxing
Schlesinger Sarah J
Park Chae Gyu
Nussenzweig Michel C
Granelli-Piperno Angela
Steinman Ralph M
References (52)
52 references, click to expand
  1. Vaccine development strategies for improving immunization: the role of modern immunology.
    Nat Immunol. 2004 May;5(5):460-4 PMID: 15116108
  2. Correlates of immune protection in HIV-1 infection: what we know, what we don't know, what we should know.
    Nat Med. 2004 Aug;10(8):806-10 PMID: 15286782
  3. Immunological unresponsiveness characterized by increased expression of CD5 on peripheral T cells induced by dendritic cells in vivo.
    Immunity. 2004 Jun;20(6):695-705 PMID: 15189735
  4. Helping the CD8(+) T-cell response.
    Nat Rev Immunol. 2004 Aug;4(8):595-602 PMID: 15286726
  5. Progress on new vaccine strategies against chronic viral infections.
    J Clin Invest. 2004 Aug;114(4):450-62 PMID: 15314679
  6. Loss of HIV-1-specific CD8+ T cell proliferation after acute HIV-1 infection and restoration by vaccine-induced HIV-1-specific CD4+ T cells.
    J Exp Med. 2004 Sep 20;200(6):701-12 PMID: 15381726
  7. Contribution of dendritic cells to stimulation of the murine syngeneic mixed leukocyte reaction.
    J Exp Med. 1980 May 1;151(5):1196-212 PMID: 6445399
  8. Protein-specific helper T-lymphocyte formation initiated by dendritic cells.
    Science. 1985 Aug 2;229(4712):475-9 PMID: 3160115
  9. Langerhans' cells, veiled cells, and interdigitating cells in the mouse recognized by a monoclonal antibody.
    J Exp Med. 1986 Apr 1;163(4):981-97 PMID: 3950549
  10. Dendritic cells pulsed with protein antigens in vitro can prime antigen-specific, MHC-restricted T cells in situ.
    J Exp Med. 1990 Aug 1;172(2):631-40 PMID: 2373994
  11. The dendritic cell system and its role in immunogenicity.
    Annu Rev Immunol. 1991;9:271-96 PMID: 1910679
  12. Monoclonal antibodies to murine CD40 define two distinct functional epitopes.
    Eur J Immunol. 1994 Aug;24(8):1828-34 PMID: 7519997
  13. The receptor DEC-205 expressed by dendritic cells and thymic epithelial cells is involved in antigen processing.
    Nature. 1995 May 11;375(6527):151-5 PMID: 7753172
  14. Tissue distribution of the DEC-205 protein that is detected by the monoclonal antibody NLDC-145. I. Expression on dendritic cells and other subsets of mouse leukocytes.
    Cell Immunol. 1995 Jun;163(1):148-56 PMID: 7758125
  15. Tissue distribution of the DEC-205 protein that is detected by the monoclonal antibody NLDC-145. II. Expression in situ in lymphoid and nonlymphoid tissues.
    Cell Immunol. 1995 Jun;163(1):157-62 PMID: 7758126
  16. 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. 1997 Jul 15;159(2):565-73 PMID: 9218570
  17. Immunobiology of dendritic cells.
    Annu Rev Immunol. 2000;18:767-811 PMID: 10837075
  18. Analysis of CD8 T cell reactivity to cytomegalovirus using protein-spanning pools of overlapping pentadecapeptides.
    Eur J Immunol. 2000 Jun;30(6):1676-82 PMID: 10898504
  19. 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 Oct 30;151(3):673-84 PMID: 11062267
  20. Dendritic cell regulation of TH1-TH2 development.
    Nat Immunol. 2000 Sep;1(3):199-205 PMID: 10973276
  21. Use of overlapping peptide mixtures as antigens for cytokine flow cytometry.
    J Immunol Methods. 2001 Sep 1;255(1-2):27-40 PMID: 11470284
  22. Regulation of T cell immunity by dendritic cells.
    Cell. 2001 Aug 10;106(3):263-6 PMID: 11509174
  23. Dendritic cells induce peripheral T cell unresponsiveness under steady state conditions in vivo.
    J Exp Med. 2001 Sep 17;194(6):769-79 PMID: 11560993
  24. Effector and memory T-cell differentiation: implications for vaccine development.
    Nat Rev Immunol. 2002 Apr;2(4):251-62 PMID: 12001996
  25. Rapid induction of tumor-specific type 1 T helper cells in metastatic melanoma patients by vaccination with mature, cryopreserved, peptide-loaded monocyte-derived dendritic cells.
    J Exp Med. 2002 May 20;195(10):1279-88 PMID: 12021308
  26. 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 Dec 16;196(12):1627-38 PMID: 12486105
  27. Inducible transgenic mice reveal resting dendritic cells as potent inducers of CD8+ T cell tolerance.
    Immunity. 2003 May;18(5):713-20 PMID: 12753747
  28. Enhanced T-cell immunogenicity of plasmid DNA vaccines boosted by recombinant modified vaccinia virus Ankara in humans.
    Nat Med. 2003 Jun;9(6):729-35 PMID: 12766765
  29. HIV vaccines 1983-2003.
    Nat Med. 2003 Jul;9(7):874-80 PMID: 12835708
  30. Influenza virus-induced dendritic cell maturation is associated with the induction of strong T cell immunity to a coadministered, normally nonimmunogenic protein.
    J Exp Med. 2003 Jul 7;198(1):133-44 PMID: 12847140
  31. Dendritic cells in immunity and tolerance-do they display opposite functions?
    Immunity. 2003 Jul;19(1):5-8 PMID: 12871634
  32. Prevention of cervical cancer through papillomavirus vaccination.
    Nat Rev Immunol. 2004 Jan;4(1):46-54 PMID: 14704767
  33. Combined TLR and CD40 triggering induces potent CD8+ T cell expansion with variable dependence on type I IFN.
    J Exp Med. 2004 Mar 15;199(6):775-84 PMID: 15007094
  34. In vivo targeting of antigens to maturing dendritic cells via the DEC-205 receptor improves T cell vaccination.
    J Exp Med. 2004 Mar 15;199(6):815-24 PMID: 15024047
  35. Dendritic cells: unique leukocyte populations which control the primary immune response.
    Blood. 1997 Nov 1;90(9):3245-87 PMID: 9345009
  36. Vigorous HIV-1-specific CD4+ T cell responses associated with control of viremia.
    Science. 1997 Nov 21;278(5342):1447-50 PMID: 9367954
  37. The MHC class I-restricted immune response to HIV-gag in BALB/c mice selects a single epitope that does not have a predictable MHC-binding motif and binds to Kd through interactions between a glutamine at P3 and pocket D.
    J Immunol. 1998 Sep 15;161(6):2985-93 PMID: 9743362
  38. CD8alpha+ and CD8alpha- subclasses of dendritic cells direct the development of distinct T helper cells in vivo.
    J Exp Med. 1999 Feb 1;189(3):587-92 PMID: 9927520
  39. Reciprocal and dynamic control of CD8 T cell homing by dendritic cells from skin- and gut-associated lymphoid tissues.
    J Exp Med. 2005 Jan 17;201(2):303-16 PMID: 15642741
  40. Resting dendritic cells induce peripheral CD8+ T cell tolerance through PD-1 and CTLA-4.
    Nat Immunol. 2005 Mar;6(3):280-6 PMID: 15685176
  41. Toll-like receptor 3 promotes cross-priming to virus-infected cells.
    Nature. 2005 Feb 24;433(7028):887-92 PMID: 15711573
  42. Cell biology of antigen processing in vitro and in vivo.
    Annu Rev Immunol. 2005;23:975-1028 PMID: 15771591
  43. Combination of HIV-1-specific CD4 Th1 cell responses and IgG2 antibodies is the best predictor for persistence of long-term nonprogression.
    J Infect Dis. 2005 Jun 15;191(12):2053-63 PMID: 15897991
  44. DNA vaccines: progress and challenges.
    J Immunol. 2005 Jul 15;175(2):633-9 PMID: 16002657
  45. Recall proliferation potential of memory CD8+ T cells and antiviral protection.
    J Immunol. 2005 Oct 1;175(7):4677-85 PMID: 16177115
  46. Antibodies and CD8+ T cells are complementary and essential for natural resistance to a highly lethal cytopathic virus.
    J Immunol. 2005 Nov 15;175(10):6829-36 PMID: 16272340
  47. Innate NKT lymphocytes confer superior adaptive immunity via tumor-capturing dendritic cells.
    J Exp Med. 2005 Dec 5;202(11):1507-16 PMID: 16330814
  48. Antigen targeting to dendritic cells elicits long-lived T cell help for antibody responses.
    J Exp Med. 2006 Mar 20;203(3):599-606 PMID: 16505139
  49. 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 Jun 21;199(12):1607-18 PMID: 15197224
  50. AIDS/HIV. Developing an AIDS vaccine: need, uncertainty, hope.
    Science. 2004 Jun 25;304(5679):1913-4 PMID: 15218131
  51. Modulating vaccine responses with dendritic cells and Toll-like receptors.
    Immunol Rev. 2004 Jun;199:227-50 PMID: 15233738
  52. Cellular and humoral immunity against vaccinia virus infection of mice.
    J Immunol. 2004 May 15;172(10):6265-71 PMID: 15128815
Article Info
Journal
The Journal of experimental medicine
Abbr.
J Exp Med
ISSN
0022-1007
Published
2006-03-20
Epub
2006-00-27
Pages
607-17
Language
English
Region
United States
NLM ID
2985109R
PMCID
PMC2118242
Subset
IM
Grants
NIAID NIH HHS · R01 AI041111 · United States
NIAID NIH HHS · AI40874 · United States
NIAID NIH HHS · R01 AI040874 · United States
NIAID NIH HHS · R01 AI41111 · United States
NIAID NIH HHS · U19 AI062623 · United States
NIAID NIH HHS · R01 AI013013 · United States
NIAID NIH HHS · AI13013 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com