Home LiteratureArticle Details
PMID: 18519811 Published · ppublish English Clinical Trial Journal Article Research Support, N.I.H., Extramural

Depletion of human regulatory T cells specifically enhances antigen-specific immune responses to cancer vaccines.

Blood ·Vol. 112 ·No. 3 ·2008-08-01 ·Pages 610-8

Morse MA, Hobeika AC, Osada T, Serra D, Niedzwiecki D, Lyerly HK, Clay TM

Abstract

CD4(+)CD25(high)FoxP3(+) regulatory T (Treg) cells limit antigen-specific immune responses and are a cause of suppressed anticancer immunity. In preclinical and clinical studies, we assessed the immune consequences of FoxP3(+) Treg-cell depletion in patients with advanced malignancies. We demonstrated that a CD25(high) targeting immunotoxin (denileukin diftitox) depleted FoxP3(+) Treg cells, decreased Treg-cell function, and enhanced antigen-specific T-cell responses in vitro. We then attempted to enhance antitumor immune responses in patients with carcinoembryonic antigen (CEA)-expressing malignancies by Treg-cell depletion. In a pilot study (n = 15), denileukin diftitox, given as a single dose or repeated dosing, was followed by immunizations with dendritic cells modified with the fowlpox vector rF-CEA(6D)-TRICOM. By flow cytometric analysis, we report the first direct evidence that circulating CD4(+)CD25(high)FoxP3(+) Treg cells are depleted after multiple doses of denileukin diftitox. Earlier induction of, and overall greater exposure to, the T-cell response to CEA was observed in the multiple-dose group, but not the single-dose group. These results indicate the potential for combining Treg-cell depletion with anticancer vaccines to enhance tumor antigen-specific immune responses and the need to explore dose and schedule of Treg depletion strategies in optimizing vaccine efforts.

MeSH Terms
Antigens, Neoplasm/immunology Cancer Vaccines/immunology Carcinoembryonic Antigen/immunology Dendritic Cells/transplantation Diphtheria Toxin/administration & dosage,pharmacology Humans Immunity Immunotherapy, Adoptive/methods Interleukin-2/administration & dosage,pharmacology Lymphocyte Depletion/methods Pilot Projects Recombinant Fusion Proteins/administration & dosage,pharmacology T-Lymphocytes, Regulatory Treatment Outcome
Chemicals
Antigens, Neoplasm Cancer Vaccines Carcinoembryonic Antigen Diphtheria Toxin Interleukin-2 Recombinant Fusion Proteins denileukin diftitox
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Morse Michael A
Department ofMedicine, Duke University Medical Center, Durham, NC 27710, USA. morse004@mc.duke.edu
Hobeika Amy C
Osada Takuya
Serra Delila
Niedzwiecki Donna
Lyerly H Kim
Clay Timothy M
References (27)
27 references, click to expand
  1. IL-2 immunotoxin denileukin diftitox reduces regulatory T cells and enhances vaccine-mediated T-cell immunity.
    Blood. 2007 Nov 1;110(9):3192-201 PMID: 17616639
  2. Placebo-controlled phase III trial of immunologic therapy with sipuleucel-T (APC8015) in patients with metastatic, asymptomatic hormone refractory prostate cancer.
    J Clin Oncol. 2006 Jul 1;24(19):3089-94 PMID: 16809734
  3. Regulatory T cells in ovarian cancer: biology and therapeutic potential.
    Am J Reprod Immunol. 2005 Dec;54(6):369-77 PMID: 16305662
  4. CD4+/CD25+ regulatory cells inhibit activation of tumor-primed CD4+ T cells with IFN-gamma-dependent antiangiogenic activity, as well as long-lasting tumor immunity elicited by peptide vaccination.
    J Immunol. 2003 Dec 1;171(11):5931-9 PMID: 14634104
  5. In vivo elimination of CD25+ regulatory T cells leads to tumor rejection of B16F10 melanoma, when combined with interleukin-12 gene transfer.
    Exp Dermatol. 2004 Oct;13(10):613-20 PMID: 15447721
  6. Enhancement of vaccine-mediated antitumor immunity in cancer patients after depletion of regulatory T cells.
    J Clin Invest. 2005 Dec;115(12):3623-33 PMID: 16308572
  7. Immunologic monitoring of cancer vaccine therapy: results of a workshop sponsored by the Society for Biological Therapy.
    J Immunother. 2002 Mar-Apr;25(2):97-138 PMID: 12074049
  8. Enumerating antigen-specific T-cell responses in peripheral blood: a comparison of peptide MHC Tetramer, ELISpot, and intracellular cytokine analysis.
    J Immunother. 2005 Jan-Feb;28(1):63-72 PMID: 15614046
  9. The lifestyle of naturally occurring CD4+ CD25+ Foxp3+ regulatory T cells.
    Immunol Rev. 2006 Aug;212:60-73 PMID: 16903906
  10. Naturally-occurring CD4+CD25+ immunoregulatory T cells: central players in the arena of peripheral tolerance.
    Semin Immunol. 2004 Apr;16(2):81-8 PMID: 15036231
  11. Interleukin 2 receptor-targeted cytotoxicity. Receptor binding requirements for entry of a diphtheria toxin-related interleukin 2 fusion protein into cells.
    Eur J Immunol. 1990 Apr;20(4):785-91 PMID: 2140788
  12. IL-2 immunotoxin therapy modulates tumor-associated regulatory T cells and leads to lasting immune-mediated rejection of breast cancers in neu-transgenic mice.
    J Immunol. 2006 Jul 1;177(1):84-91 PMID: 16785502
  13. Immunoregulatory T cells in tumor immunity.
    Curr Opin Immunol. 2004 Apr;16(2):157-62 PMID: 15023407
  14. Cutting edge: control of CD8+ T cell activation by CD4+CD25+ immunoregulatory cells.
    J Immunol. 2001 Aug 1;167(3):1137-40 PMID: 11466326
  15. Concomitant tumor immunity to a poorly immunogenic melanoma is prevented by regulatory T cells.
    J Exp Med. 2004 Sep 20;200(6):771-82 PMID: 15381730
  16. Cutting edge: Regulatory T cells from lung cancer patients directly inhibit autologous T cell proliferation.
    J Immunol. 2002 May 1;168(9):4272-6 PMID: 11970966
  17. Escape from immunotherapy: possible mechanisms that influence tumor regression/progression.
    Cancer Immunol Immunother. 2004 Oct;53(10):844-54 PMID: 15197495
  18. Pivotal phase III trial of two dose levels of denileukin diftitox for the treatment of cutaneous T-cell lymphoma.
    J Clin Oncol. 2001 Jan 15;19(2):376-88 PMID: 11208829
  19. CD4+ CD25+ suppressor T cells: more questions than answers.
    Nat Rev Immunol. 2002 Jun;2(6):389-400 PMID: 12093005
  20. Inability of a fusion protein of IL-2 and diphtheria toxin (Denileukin Diftitox, DAB389IL-2, ONTAK) to eliminate regulatory T lymphocytes in patients with melanoma.
    J Immunother. 2005 Nov-Dec;28(6):582-92 PMID: 16224276
  21. Depletion of CD4+CD25+ human regulatory T cells in vivo: kinetics of Treg depletion and alterations in immune functions in vivo and in vitro.
    Int J Cancer. 2007 Jun 15;120(12):2723-33 PMID: 17315189
  22. Phase I study of immunization with dendritic cells modified with fowlpox encoding carcinoembryonic antigen and costimulatory molecules.
    Clin Cancer Res. 2005 Apr 15;11(8):3017-24 PMID: 15837756
  23. Increase of regulatory T cells in the peripheral blood of cancer patients.
    Clin Cancer Res. 2003 Feb;9(2):606-12 PMID: 12576425
  24. Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival.
    Nat Med. 2004 Sep;10(9):942-9 PMID: 15322536
  25. Foxp3 expressing CD4+CD25(high) regulatory T cells are overrepresented in human metastatic melanoma lymph nodes and inhibit the function of infiltrating T cells.
    J Immunol. 2004 Jul 15;173(2):1444-53 PMID: 15240741
  26. Immunologic tolerance maintained by CD25+ CD4+ regulatory T cells: their common role in controlling autoimmunity, tumor immunity, and transplantation tolerance.
    Immunol Rev. 2001 Aug;182:18-32 PMID: 11722621
  27. CD4+CD25+ regulatory T cells that secrete TGFbeta and IL-10 are preferentially induced by a vaccine vector.
    J Immunother. 2004 Sep-Oct;27(5):339-46 PMID: 15314542
Article Info
Journal
Blood
Abbr.
Blood
ISSN
1528-0020
Published
2008-08-01
Epub
2008-00-02
Pages
610-8
Language
English
Region
United States
NLM ID
7603509
PMCID
PMC2481547
Subset
IM
Grants
NCI NIH HHS · P01 CA078673 · United States
NCI NIH HHS · R21 CA117126 · United States
NCI NIH HHS · 5P0L-CA078673 · United States
NCI NIH HHS · 1R21-CA117126-01A1 · United States
Databases
ClinicalTrials.gov
NCT00128622
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