Home LiteratureArticle Details
PMID: 14657217 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Superior protection against malaria and melanoma metastases by a C-glycoside analogue of the natural killer T cell ligand alpha-Galactosylceramide.

The Journal of experimental medicine ·Vol. 198 ·No. 11 ·2003-12-01 ·Pages 1631-41

Schmieg J, Yang G, Franck RW, Tsuji M

Abstract

alpha-Galactosylceramide (alpha-GalCer) is a glycolipid that stimulates natural killer T cells to produce both T helper (Th) 1 and Th2 cytokines. This property enables alpha-GalCer to ameliorate a wide variety of infectious, neoplastic, and autoimmune diseases; however, its effectiveness against any one disease is limited by the opposing activities of the induced Th1 and Th2 cytokines. Here, we report that a synthetic C-glycoside analogue of alpha-GalCer, alpha-C-galactosylceramide (alpha-C-GalCer), acts as natural killer T cell ligand in vivo, and stimulates an enhanced Th1-type response in mice. In two disease models requiring Th1-type responses for control, namely malaria and melanoma metastases, alpha-C-GalCer exhibited a 1,000-fold more potent antimalaria activity and a 100-fold more potent antimetastatic activity than alpha-GalCer. Moreover, alpha-C-GalCer consistently stimulated prolonged production of the Th1 cytokines interferon-gamma and interleukin (IL)-12, and decreased production of the Th2 cytokine IL-4 compared with alpha-GalCer. Finally, alpha-C-GalCer's enhanced therapeutic activity required the presence of IL-12, which was needed to stimulate natural killer cells for optimal interferon-gamma production, but did not affect IL-4. Overall, our results suggest that alpha-C-GalCer may one day be an excellent therapeutic option for diseases resolved by Th1-type responses.

MeSH Terms
Animals Base Sequence DNA Primers Female Galactosylceramides/immunology Interferon-gamma/biosynthesis Killer Cells, Natural/immunology,metabolism Ligands Malaria/immunology Melanoma, Experimental/pathology Mice Mice, Inbred BALB C Neoplasm Metastasis/immunology
Chemicals
DNA Primers Galactosylceramides Ligands Interferon-gamma
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Schmieg John
Dept. of Medical and Molecular Parasitology, New York University School of Medicine, 341 E. 25th St., New York, NY 10010. email: moriya.tsuji@med.nyu.edu
Yang Guangli
Franck Richard W
Tsuji Moriya
References (30)
30 references, click to expand
  1. Requirement for Valpha14 NKT cells in IL-12-mediated rejection of tumors.
    Science. 1997 Nov 28;278(5343):1623-6 PMID: 9374462
  2. A phase I study of the natural killer T-cell ligand alpha-galactosylceramide (KRN7000) in patients with solid tumors.
    Clin Cancer Res. 2002 Dec;8(12):3702-9 PMID: 12473579
  3. CD1d-mediated recognition of an alpha-galactosylceramide by natural killer T cells is highly conserved through mammalian evolution.
    J Exp Med. 1998 Oct 19;188(8):1521-8 PMID: 9782129
  4. The natural killer T (NKT) cell ligand alpha-galactosylceramide demonstrates its immunopotentiating effect by inducing interleukin (IL)-12 production by dendritic cells and IL-12 receptor expression on NKT cells.
    J Exp Med. 1999 Apr 5;189(7):1121-8 PMID: 10190903
  5. A novel function of Valpha14+CD4+NKT cells: stimulation of IL-12 production by antigen-presenting cells in the innate immune system.
    J Immunol. 1999 Jul 1;163(1):93-101 PMID: 10384104
  6. Cutting edge: Cross-talk between cells of the innate immune system: NKT cells rapidly activate NK cells.
    J Immunol. 1999 Nov 1;163(9):4647-50 PMID: 10528160
  7. Selective induction of NK cell proliferation and cytotoxicity by activated NKT cells.
    Eur J Immunol. 2000 Apr;30(4):985-92 PMID: 10760785
  8. Convergent C-glycolipid synthesis via the Ramberg-Bäcklund reaction: active antiproliferative glycolipids.
    Org Lett. 1999 Dec 30;1(13):2149-51 PMID: 10836068
  9. alpha -galactosylceramide-activated Valpha 14 natural killer T cells mediate protection against murine malaria.
    Proc Natl Acad Sci U S A. 2000 Jul 18;97(15):8461-6 PMID: 10900007
  10. Tracking the response of natural killer T cells to a glycolipid antigen using CD1d tetramers.
    J Exp Med. 2000 Sep 4;192(5):741-54 PMID: 10974039
  11. Selective bystander proliferation of memory CD4+ and CD8+ T cells upon NK T or T cell activation.
    J Immunol. 2000 Oct 15;165(8):4305-11 PMID: 11035065
  12. NKT cells: facts, functions and fallacies.
    Immunol Today. 2000 Nov;21(11):573-83 PMID: 11094262
  13. Requirement for IFN-gamma in IL-12 production induced by collaboration between v(alpha)14(+) NKT cells and antigen-presenting cells.
    Int Immunol. 2000 Dec;12(12):1669-75 PMID: 11099306
  14. Costimulation-dependent modulation of experimental autoimmune encephalomyelitis by ligand stimulation of V alpha 14 NK T cells.
    J Immunol. 2001 Jan 1;166(1):662-8 PMID: 11123351
  15. Synthesis and growth inhibitory properties of glucosamine-derived glycerolipids.
    Org Lett. 2001 Jan 25;3(2):197-200 PMID: 11430033
  16. A synthetic glycolipid prevents autoimmune encephalomyelitis by inducing TH2 bias of natural killer T cells.
    Nature. 2001 Oct 4;413(6855):531-4 PMID: 11586362
  17. Detection of malaria liver-stages in mice infected through the bite of a single Anopheles mosquito using a highly sensitive real-time PCR.
    Int J Parasitol. 2001 Nov;31(13):1499-502 PMID: 11595237
  18. Sequential production of interferon-gamma by NK1.1(+) T cells and natural killer cells is essential for the antimetastatic effect of alpha-galactosylceramide.
    Blood. 2002 Feb 15;99(4):1259-66 PMID: 11830474
  19. Synthesis of homoceramides, novel ceramide analogues, and their lack of effect on the growth of hippocampal neurons.
    J Org Chem. 2002 Feb 8;67(3):988-96 PMID: 11856049
  20. Immunotherapy with ligands of natural killer T cells.
    Trends Mol Med. 2002 May;8(5):225-31 PMID: 12067632
  21. Prolonged IFN-gamma-producing NKT response induced with alpha-galactosylceramide-loaded DCs.
    Nat Immunol. 2002 Sep;3(9):867-74 PMID: 12154358
  22. Human peripheral blood Valpha24+ Vbeta11+ NKT cells expand following administration of alpha-galactosylceramide-pulsed dendritic cells.
    Vox Sang. 2002 Oct;83(3):250-3 PMID: 12366768
  23. Mouse V alpha 14i natural killer T cells are resistant to cytokine polarization in vivo.
    Proc Natl Acad Sci U S A. 2003 Jul 8;100(14):8395-400 PMID: 12829795
  24. The response of natural killer T cells to glycolipid antigens is characterized by surface receptor down-modulation and expansion.
    Proc Natl Acad Sci U S A. 2003 Sep 16;100(19):10913-8 PMID: 12960397
  25. Induction of interferon gamma production by natural killer cell stimulatory factor: characterization of the responder cells and synergy with other inducers.
    J Exp Med. 1991 Apr 1;173(4):869-79 PMID: 1672545
  26. Structure-activity relationship of alpha-galactosylceramides against B16-bearing mice.
    J Med Chem. 1995 Jun 9;38(12):2176-87 PMID: 7783149
  27. Altered peptide ligand-induced partial T cell activation: molecular mechanisms and role in T cell biology.
    Annu Rev Immunol. 1996;14:1-27 PMID: 8717505
  28. Impaired NK1+ T cell development and early IL-4 production in CD1-deficient mice.
    Immunity. 1997 Apr;6(4):459-67 PMID: 9133425
  29. Mouse CD1-specific NK1 T cells: development, specificity, and function.
    Annu Rev Immunol. 1997;15:535-62 PMID: 9143699
  30. CD1d-restricted and TCR-mediated activation of valpha14 NKT cells by glycosylceramides.
    Science. 1997 Nov 28;278(5343):1626-9 PMID: 9374463
Article Info
Journal
The Journal of experimental medicine
Abbr.
J Exp Med
ISSN
0022-1007
Published
2003-12-01
Pages
1631-41
Language
English
Region
United States
NLM ID
2985109R
PMCID
PMC2194137
Subset
IM
Grants
NIGMS NIH HHS · R01 GM060271 · United States
NIAID NIH HHS · AI-47840 · United States
NIGMS NIH HHS · GM-60271 · 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