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PMID: 16439533 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Multimeric soluble CD40 ligand and GITR ligand as adjuvants for human immunodeficiency virus DNA vaccines.

Journal of virology ·Vol. 80 ·No. 4 ·2006-02-00 ·Pages 1762-72

Stone GW, Barzee S, Snarsky V, Kee K, Spina CA, Yu XF, Kornbluth RS

Abstract

For use in humans, human immunodeficiency virus (HIV) DNA vaccines may need to include immunostimulatory adjuvant molecules. CD40 ligand (CD40L), a member of the tumor necrosis factor (TNF) superfamily (TNFSF), is one candidate adjuvant, but it has been difficult to use because it is normally expressed as a trimeric membrane molecule. Soluble trimeric forms of CD40L have been produced, but in vitro data indicate that multimeric, many-trimer forms of soluble CD40L are more active. This multimerization requirement was evaluated in mice using plasmids that encoded either 1-trimer, 2-trimer, or 4-trimer soluble forms of CD40L. Fusion with the body of Acrp30 was used to produce the 2-trimer form, and fusion with the body of surfactant protein D was used to produce the 4-trimer form. Using plasmids for secreted HIV-1 antigens Gag and Env, soluble CD40L was active as an adjuvant in direct proportion to the valence of the trimers (1 < 2 < 4). These CD40L-augmented DNA vaccines elicited strong CD8(+) T-cell responses but did not elicit significant CD4(+) T-cell or antibody responses. To test the applicability of the multimeric fusion protein approach to other TNFSFs, a 4-trimer construct for the ligand of glucocorticoid-induced TNF family-related receptor (GITR) was also prepared. Multimeric soluble GITR ligand (GITRL) augmented the CD8(+) T-cell, CD4(+) T-cell, and antibody responses to DNA vaccination. In summary, multimeric CD40L and GITRL are new adjuvants for DNA vaccines. Plasmids for expressing multimeric TNFSF fusion proteins permit the rapid testing of TNFSF molecules in vivo.

MeSH Terms
AIDS Vaccines/immunology Adiponectin/genetics Adjuvants, Immunologic/administration & dosage Animals CD4-Positive T-Lymphocytes/immunology CD40 Ligand/genetics,immunology CD8-Positive T-Lymphocytes/immunology Enzyme-Linked Immunosorbent Assay Female Gene Products, env/genetics,immunology Gene Products, gag/genetics,immunology HIV Antibodies/blood HIV-1/immunology Immunologic Memory Interferon-gamma/administration & dosage Mice Plasmids Pulmonary Surfactant-Associated Protein D/genetics Recombinant Fusion Proteins/genetics,immunology Tumor Necrosis Factors/genetics,immunology Vaccines, DNA/immunology
Chemicals
AIDS Vaccines Adiponectin Adipoq protein, mouse Adjuvants, Immunologic Gene Products, env Gene Products, gag HIV Antibodies Pulmonary Surfactant-Associated Protein D Recombinant Fusion Proteins Tnfsf18 protein, mouse Tumor Necrosis Factors Vaccines, DNA CD40 Ligand Interferon-gamma
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Stone Geoffrey W
Department of Medicine-0679, Stein Clinical Sciences Bldg., Room 304, University of California, San Diego, 9500 Gilman Dr., La Jolla, CA 92093-0679, USA. [email protected]
Barzee Suzanne
Snarsky Victoria
Kee Kristin
Spina Celsa A
Yu Xiao-Fang
Kornbluth Richard S
References (97)
97 references, click to expand
  1. Developing DNA vaccines that call to dendritic cells.
    J Clin Invest. 2004 Nov;114(9):1241-4 PMID: 15520855
  2. Recruitment and expansion of dendritic cells in vivo potentiate the immunogenicity of plasmid DNA vaccines.
    J Clin Invest. 2004 Nov;114(9):1334-42 PMID: 15520866
  3. CD80 and CD86, but not CD154, augment DNA vaccine-induced protection in experimental bovine tuberculosis.
    Vaccine. 2004 Dec 21;23(6):769-79 PMID: 15542201
  4. The role of cytokine DNAs as vaccine adjuvants for optimizing cellular immune responses.
    Immunol Rev. 2004 Dec;202:266-74 PMID: 15546399
  5. Immunomodulatory effect of plasmids co-expressing cytokines in classical swine fever virus subunit gp55/E2-DNA vaccination.
    Vet Res. 2005 Jul-Aug;36(4):571-87 PMID: 15955282
  6. DNA vaccines: progress and challenges.
    J Immunol. 2005 Jul 15;175(2):633-9 PMID: 16002657
  7. High-level primary CD8(+) T-cell response to human immunodeficiency virus type 1 gag and env generated by vaccination with recombinant vesicular stomatitis viruses.
    J Virol. 2002 Mar;76(6):2730-8 PMID: 11861840
  8. CD4(+)CD25(+) immunoregulatory T cells: gene expression analysis reveals a functional role for the glucocorticoid-induced TNF receptor.
    Immunity. 2002 Feb;16(2):311-23 PMID: 11869690
  9. Short-circuiting long-lived humoral immunity by the heightened engagement of CD40.
    J Clin Invest. 2002 Mar;109(5):613-20 PMID: 11877469
  10. CD40 stimulation leads to effective therapy of CD40(-) tumors through induction of strong systemic cytotoxic T lymphocyte immunity.
    Proc Natl Acad Sci U S A. 2002 Apr 16;99(8):5561-6 PMID: 11929985
  11. HIV preferentially infects HIV-specific CD4+ T cells.
    Nature. 2002 May 2;417(6884):95-8 PMID: 11986671
  12. Collectins and ficolins: sugar pattern recognition molecules of the mammalian innate immune system.
    Biochim Biophys Acta. 2002 Sep 19;1572(2-3):387-400 PMID: 12223281
  13. The molecular architecture of the TNF superfamily.
    Trends Biochem Sci. 2002 Jan;27(1):19-26 PMID: 11796220
  14. Stimulation of CD25(+)CD4(+) regulatory T cells through GITR breaks immunological self-tolerance.
    Nat Immunol. 2002 Feb;3(2):135-42 PMID: 11812990
  15. DNA vaccines against human immunodeficiency virus type 1 in the past decade.
    Clin Microbiol Rev. 2004 Apr;17(2):370-89 PMID: 15084506
  16. Cutting edge: the natural ligand for glucocorticoid-induced TNF receptor-related protein abrogates regulatory T cell suppression.
    J Immunol. 2004 May 15;172(10):5823-7 PMID: 15128759
  17. Costimulation via glucocorticoid-induced TNF receptor in both conventional and CD25+ regulatory CD4+ T cells.
    J Immunol. 2004 Jun 15;172(12):7306-14 PMID: 15187106
  18. Enhancement of DNA vaccine potency in rhesus macaques by electroporation.
    Vaccine. 2004 Jun 23;22(19):2489-93 PMID: 15193413
  19. Prospects for an AIDS vaccine: three big questions, no easy answers.
    Lancet Infect Dis. 2004 Jul;4(7):397-413 PMID: 15219551
  20. Poly-beta amino ester-containing microparticles enhance the activity of nonviral genetic vaccines.
    Proc Natl Acad Sci U S A. 2004 Jun 29;101(26):9534-9 PMID: 15210954
  21. DNA vaccines against human immunodeficiency virus type 1.
    Immunol Rev. 2004 Jun;199:144-55 PMID: 15233732
  22. Enhanced SIV replication and accelerated progression to AIDS in macaques primed to mount a CD4 T cell response to the SIV envelope protein.
    Proc Natl Acad Sci U S A. 2004 Aug 31;101(35):13026-31 PMID: 15326293
  23. C1q and tumor necrosis factor superfamily: modularity and versatility.
    Trends Immunol. 2004 Oct;25(10):551-61 PMID: 15364058
  24. Engagement of glucocorticoid-induced TNFR family-related receptor on effector T cells by its ligand mediates resistance to suppression by CD4+CD25+ T cells.
    J Immunol. 2004 Oct 15;173(8):5008-20 PMID: 15470044
  25. Cognate CD4(+) T cell licensing of dendritic cells in CD8(+) T cell immunity.
    Nat Immunol. 2004 Nov;5(11):1143-8 PMID: 15475958
  26. Genetic immunization is a simple method for eliciting an immune response.
    Nature. 1992 Mar 12;356(6365):152-4 PMID: 1545867
  27. B-cell activation mediated by interactions with membranes from helper T cells.
    Adv Exp Med Biol. 1992;323:139-48 PMID: 1485560
  28. Systemic immunological effects of cytokine genes injected into skeletal muscle.
    Proc Natl Acad Sci U S A. 1993 May 15;90(10):4523-7 PMID: 8506293
  29. The TNF receptor superfamily of cellular and viral proteins: activation, costimulation, and death.
    Cell. 1994 Mar 25;76(6):959-62 PMID: 8137429
  30. Molecular structure of pulmonary surfactant protein D (SP-D).
    J Biol Chem. 1994 Jun 24;269(25):17311-9 PMID: 8006040
  31. Collectins--soluble proteins containing collagenous regions and lectin domains--and their roles in innate immunity.
    Protein Sci. 1994 Aug;3(8):1143-58 PMID: 7987210
  32. The transmembrane form of tumor necrosis factor is the prime activating ligand of the 80 kDa tumor necrosis factor receptor.
    Cell. 1995 Dec 1;83(5):793-802 PMID: 8521496
  33. CD40 cross-linking inhibits specific antibody production by human B cells.
    Int Immunol. 1995 Nov;7(11):1809-15 PMID: 8580079
  34. 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. 2002 Sep 1;13(13):1551-60 PMID: 12228010
  35. Efficient priming of CD4+ and CD8+ T cells by DNA vaccination depends on appropriate targeting of sufficient levels of immunologically relevant antigen to appropriate processing pathways.
    J Immunol. 2002 Nov 1;169(9):4951-60 PMID: 12391208
  36. An expanding role for CD40L and other tumor necrosis factor superfamily ligands in HIV infection.
    J Hematother Stem Cell Res. 2002 Oct;11(5):787-801 PMID: 12427285
  37. Second-generation rabies virus-based vaccine vectors expressing human immunodeficiency virus type 1 gag have greatly reduced pathogenicity but are highly immunogenic.
    J Virol. 2003 Jan;77(1):237-44 PMID: 12477829
  38. Regulatory CD4+CD25+ T cells restrict memory CD8+ T cell responses.
    J Exp Med. 2002 Dec 16;196(12):1585-92 PMID: 12486101
  39. A simian replication-defective adenoviral recombinant vaccine to HIV-1 gag.
    J Immunol. 2003 Feb 1;170(3):1416-22 PMID: 12538702
  40. Two adjacent trimeric Fas ligands are required for Fas signaling and formation of a death-inducing signaling complex.
    Mol Cell Biol. 2003 Feb;23(4):1428-40 PMID: 12556501
  41. Collections and ficolins: humoral lectins of the innate immune defense.
    Annu Rev Immunol. 2003;21:547-78 PMID: 12524383
  42. Structure-function studies of the adipocyte-secreted hormone Acrp30/adiponectin. Implications fpr metabolic regulation and bioactivity.
    J Biol Chem. 2003 Mar 14;278(11):9073-85 PMID: 12496257
  43. Cytokine, chemokine, and costimulatory molecule modulation to enhance efficacy of HIV vaccines.
    Curr Mol Med. 2003 May;3(3):285-301 PMID: 12699364
  44. A potent adjuvant effect of CD40 antibody attached to antigen.
    Immunology. 2003 May;109(1):87-92 PMID: 12709021
  45. The induction of HIV Gag-specific CD8+ T cells in the spleen and gut-associated lymphoid tissue by parenteral or mucosal immunization with recombinant Listeria monocytogenes HIV Gag.
    J Immunol. 2003 May 15;170(10):5176-87 PMID: 12734365
  46. CD40 ligand (CD154) improves the durability of respiratory syncytial virus DNA vaccination in BALB/c mice.
    Vaccine. 2003 Jun 20;21(21-22):2964-79 PMID: 12798640
  47. Kunjin virus replicon vectors for human immunodeficiency virus vaccine development.
    J Virol. 2003 Jul;77(14):7796-803 PMID: 12829819
  48. Distinct dendritic cell populations sequentially present antigen to CD4 T cells and stimulate different aspects of cell-mediated immunity.
    Immunity. 2003 Jul;19(1):47-57 PMID: 12871638
  49. Inactivation of TNF signaling by rationally designed dominant-negative TNF variants.
    Science. 2003 Sep 26;301(5641):1895-8 PMID: 14512626
  50. Computational design of variant TNF molecules: a novel methodology for inhibition of proinflammatory cascades.
    Sci STKE. 2003 Nov 11;2003(208):PE51 PMID: 14612594
  51. Role of disulfide bonds in Acrp30/adiponectin structure and signaling specificity. Different oligomers activate different signal transduction pathways.
    J Biol Chem. 2003 Dec 12;278(50):50810-7 PMID: 14522956
  52. Cutting edge: a potent adjuvant effect of ligand to receptor activator of NF-kappa B gene for inducing antigen-specific CD8+ T cell response by DNA and viral vector vaccination.
    J Immunol. 2003 Dec 15;171(12):6344-8 PMID: 14662831
  53. Mouse glucocorticoid-induced tumor necrosis factor receptor ligand is costimulatory for T cells.
    Proc Natl Acad Sci U S A. 2003 Dec 9;100(25):15059-64 PMID: 14608036
  54. DNA immunisation: altering the cellular localisation of expressed protein and the immunisation route allows manipulation of the immune response.
    Vaccine. 2004 Jan 2;22(3-4):447-56 PMID: 14670327
  55. 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
  56. Collectins: players of the innate immune system.
    Eur J Biochem. 2004 Apr;271(7):1229-49 PMID: 15030473
  57. Functional impairment of CD8(+) T cells by regulatory T cells during persistent retroviral infection.
    Immunity. 2004 Mar;20(3):293-303 PMID: 15030773
  58. CD40/CD154 interactions at the interface of tolerance and immunity.
    Annu Rev Immunol. 2004;22:307-28 PMID: 15032580
  59. Naturally arising CD4+ regulatory t cells for immunologic self-tolerance and negative control of immune responses.
    Annu Rev Immunol. 2004;22:531-62 PMID: 15032588
  60. Selective expression of IL-7 receptor on memory T cells identifies early CD40L-dependent generation of distinct CD8+ memory T cell subsets.
    Proc Natl Acad Sci U S A. 2004 Apr 13;101(15):5610-5 PMID: 15044705
  61. Enhancement of antibody responses by DNA immunization using expression vectors mediating efficient antigen secretion.
    J Immunol Methods. 1999 Aug 31;228(1-2):121-30 PMID: 10556549
  62. Immunomodulatory effect of a plasmid expressing CD40 ligand on DNA vaccination against human immunodeficiency virus type-1.
    Immunology. 1999 Nov;98(3):436-42 PMID: 10583605
  63. DNA vaccines: immunology, application, and optimization*.
    Annu Rev Immunol. 2000;18:927-74 PMID: 10837079
  64. Enhancement of primary and secondary cellular immune responses against human immunodeficiency virus type 1 gag by using DNA expression vectors that target Gag antigen to the secretory pathway.
    J Virol. 2000 Jul;74(13):5997-6005 PMID: 10846081
  65. Microbial and T cell-derived stimuli regulate antigen presentation by dendritic cells in vivo.
    J Immunol. 2000 Nov 1;165(9):5027-34 PMID: 11046031
  66. DNA vaccines for viral infections: basic studies and applications.
    Adv Virus Res. 2000;55:1-74 PMID: 11050940
  67. Functional cooperation between T helper cell determinants.
    Proc Natl Acad Sci U S A. 2000 Nov 21;97(24):13269-74 PMID: 11069291
  68. Plasmids encoding granulocyte-macrophage colony-stimulating factor and CD154 enhance the immune response to genetic vaccines.
    Vaccine. 2001 Feb 28;19(15-16):2181-9 PMID: 11228391
  69. The TNF and TNF receptor superfamilies: integrating mammalian biology.
    Cell. 2001 Feb 23;104(4):487-501 PMID: 11239407
  70. Modulation of cellular responses by plasmid CD40L: CD40L plasmid vectors enhance antigen-specific helper T cell type 1 CD4+ T cell-mediated protective immunity against herpes simplex virus type 2 in vivo.
    Hum Gene Ther. 2001 Jun 10;12(9):1091-102 PMID: 11399230
  71. Phase I study of recombinant human CD40 ligand in cancer patients.
    J Clin Oncol. 2001 Jul 1;19(13):3280-7 PMID: 11432896
  72. Biophysical characterization of a soluble CD40 ligand (CD154) coiled-coil trimer: evidence of a reversible acid-denatured molten globule.
    Arch Biochem Biophys. 2001 Aug 15;392(2):208-18 PMID: 11488594
  73. Induction of potent immune responses by cationic microparticles with adsorbed human immunodeficiency virus DNA vaccines.
    J Virol. 2001 Oct;75(19):9037-43 PMID: 11533167
  74. Analysis of the oligomeric requirement for signaling by CD40 using soluble multimeric forms of its ligand, CD154.
    Eur J Immunol. 2001 Oct;31(10):3094-100 PMID: 11592086
  75. A dual-function DNA vaccine encoding carcinoembryonic antigen and CD40 ligand trimer induces T cell-mediated protective immunity against colon cancer in carcinoembryonic antigen-transgenic mice.
    J Immunol. 2001 Oct 15;167(8):4560-5 PMID: 11591784
  76. High-affinity T helper epitope induces complementary helper and APC polarization, increased CTL, and protection against viral infection.
    J Clin Invest. 2001 Dec;108(11):1677-85 PMID: 11733563
  77. CD40-CD40 ligand interactions are critical in T-B cooperation but not for other anti-viral CD4+ T cell functions.
    J Exp Med. 1996 May 1;183(5):2209-18 PMID: 8642330
  78. The tumor necrosis factor ligand and receptor families.
    N Engl J Med. 1996 Jun 27;334(26):1717-25 PMID: 8637518
  79. Memory B cells are biased towards terminal differentiation: a strategy that may prevent repertoire freezing.
    J Exp Med. 1997 Sep 15;186(6):931-40 PMID: 9294147
  80. Membrane Fas ligand kills human peripheral blood T lymphocytes, and soluble Fas ligand blocks the killing.
    J Exp Med. 1997 Dec 15;186(12):2045-50 PMID: 9396774
  81. Increased immune response elicited by DNA vaccination with a synthetic gp120 sequence with optimized codon usage.
    J Virol. 1998 Feb;72(2):1497-503 PMID: 9445053
  82. Influence of cellular location of expressed antigen on the efficacy of DNA vaccination: cytotoxic T lymphocyte and antibody responses are suboptimal when antigen is cytoplasmic after intramuscular DNA immunization.
    Int Immunol. 1997 Dec;9(12):1897-906 PMID: 9466317
  83. Immunostimulatory effects of a plasmid expressing CD40 ligand (CD154) on gene immunization.
    J Immunol. 1997 Dec 15;159(12):5777-81 PMID: 9550372
  84. Conversion of membrane-bound Fas(CD95) ligand to its soluble form is associated with downregulation of its proapoptotic activity and loss of liver toxicity.
    J Exp Med. 1998 Apr 20;187(8):1205-13 PMID: 9547332
  85. CD40 ligand (CD154) stimulation of macrophages to produce HIV-1-suppressive beta-chemokines.
    Proc Natl Acad Sci U S A. 1998 Apr 28;95(9):5205-10 PMID: 9560254
  86. A conditioned dendritic cell can be a temporal bridge between a CD4+ T-helper and a T-killer cell.
    Nature. 1998 Jun 4;393(6684):474-8 PMID: 9624003
  87. Help for cytotoxic-T-cell responses is mediated by CD40 signalling.
    Nature. 1998 Jun 4;393(6684):478-80 PMID: 9624004
  88. T-cell help for cytotoxic T lymphocytes is mediated by CD40-CD40L interactions.
    Nature. 1998 Jun 4;393(6684):480-3 PMID: 9624005
  89. Arrest of B lymphocyte terminal differentiation by CD40 signaling: mechanism for lack of antibody-secreting cells in germinal centers.
    Immunity. 1998 Jun;8(6):733-42 PMID: 9655487
  90. CD40 ligand/trimer DNA enhances both humoral and cellular immune responses and induces protective immunity to infectious and tumor challenge.
    J Immunol. 1998 Nov 1;161(9):4563-71 PMID: 9794383
  91. Incorporation of an isoleucine zipper motif enhances the biological activity of soluble CD40L (CD154).
    J Biol Chem. 1999 Jan 1;274(1):418-23 PMID: 9867859
  92. Interaction of B cells with activated T cells reduces the threshold for CD40-mediated B cell activation.
    Int Immunol. 1999 Jan;11(1):71-9 PMID: 10050675
  93. CD40 antibody evokes a cytotoxic T-cell response that eradicates lymphoma and bypasses T-cell help.
    Nat Med. 1999 May;5(5):548-53 PMID: 10229232
  94. Immune responses to DNA vaccines.
    Cell Mol Life Sci. 1999 May;55(5):751-70 PMID: 10379361
  95. Conversion of tumor-specific CD4+ T-cell tolerance to T-cell priming through in vivo ligation of CD40.
    Nat Med. 1999 Jul;5(7):780-7 PMID: 10395323
  96. Modular organization of proteins containing C1q-like globular domain.
    Immunopharmacology. 1999 May;42(1-3):15-21 PMID: 10408361
  97. Cloning of gp-340, a putative opsonin receptor for lung surfactant protein D.
    Proc Natl Acad Sci U S A. 1999 Sep 14;96(19):10794-9 PMID: 10485905
Article Info
Journal
Journal of virology
Abbr.
J Virol
ISSN
0022-538X
Published
2006-02-00
Pages
1762-72
Language
English
Region
United States
NLM ID
0113724
PMCID
PMC1367159
Subset
IM
Grants
NIAID NIH HHS · R21 AI052842 · United States
NIAID NIH HHS · R21AI52842 · United States
NIAID NIH HHS · T32AI007384 · United States
NIAID NIH HHS · T32 AI007384 · United States
NIAID NIH HHS · P30 AI036214 · United States
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