Home LiteratureArticle Details
PMID: 19498172 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Halofuginone inhibits TH17 cell differentiation by activating the amino acid starvation response.

Science (New York, N.Y.) ·Vol. 324 ·No. 5932 ·2009-06-05 ·Pages 1334-8

Sundrud MS, Koralov SB, Feuerer M, Calado DP, Kozhaya AE, Rhule-Smith A, Lefebvre RE, Unutmaz D, Mazitschek R, Waldner H, Whitman M, Keller T, Rao A

Abstract

A central challenge for improving autoimmune therapy is preventing inflammatory pathology without inducing generalized immunosuppression. T helper 17 (TH17) cells, characterized by their production of interleukin-17, have emerged as important and broad mediators of autoimmunity. Here we show that the small molecule halofuginone (HF) selectively inhibits mouse and human TH17 differentiation by activating a cytoprotective signaling pathway, the amino acid starvation response (AAR). Inhibition of TH17 differentiation by HF is rescued by the addition of excess amino acids and is mimicked by AAR activation after selective amino acid depletion. HF also induces the AAR in vivo and protects mice from TH17-associated experimental autoimmune encephalomyelitis. These results indicate that the AAR pathway is a potent and selective regulator of inflammatory T cell differentiation in vivo.

MeSH Terms
Activating Transcription Factor 4/metabolism Amino Acids/metabolism,pharmacology Animals Autoimmunity/drug effects Cell Differentiation/drug effects Cytokines/metabolism Encephalomyelitis, Autoimmune, Experimental/drug therapy,immunology Eukaryotic Initiation Factor-2/metabolism Gene Expression Humans Interleukin-17/biosynthesis,genetics Lymphopoiesis/drug effects Mice Mice, Inbred C57BL Phosphorylation Piperidines/pharmacology,therapeutic use Protein Serine-Threonine Kinases/metabolism Quinazolinones/pharmacology,therapeutic use Signal Transduction T-Lymphocyte Subsets/cytology,drug effects,immunology,metabolism T-Lymphocytes, Helper-Inducer/cytology,drug effects,immunology,metabolism
Chemicals
Amino Acids Atf4 protein, mouse Cytokines Eukaryotic Initiation Factor-2 Interleukin-17 Piperidines Quinazolinones Activating Transcription Factor 4 EIF2AK4 protein, human Eif2ak4 protein, mouse Protein Serine-Threonine Kinases halofuginone
Authors & Affiliations
13 authors, click to expand affiliations / ORCID
Sundrud Mark S
Department of Pathology, Harvard Medical School and Immune Disease Institute, Boston, MA 02115, USA.
Koralov Sergei B
Feuerer Markus
Calado Dinis Pedro
Kozhaya Aimee Elhed
Rhule-Smith Ava
Lefebvre Rachel E
Unutmaz Derya
Mazitschek Ralph
Waldner Hanspeter
Whitman Malcolm
Keller Tracy
Rao Anjana
References (28)
28 references, click to expand
  1. Target of rapamycin (TOR): an integrator of nutrient and growth factor signals and coordinator of cell growth and cell cycle progression.
    Oncogene. 2004 Apr 19;23(18):3151-71 PMID: 15094765
  2. TH17 cells in development: an updated view of their molecular identity and genetic programming.
    Nat Rev Immunol. 2008 May;8(5):337-48 PMID: 18408735
  3. IDO and regulatory T cells: a role for reverse signalling and non-canonical NF-kappaB activation.
    Nat Rev Immunol. 2007 Oct;7(10):817-23 PMID: 17767193
  4. Indoleamine 2,3-dioxygenase-expressing dendritic cells are involved in the generation of CD4+CD25+ regulatory T cells in Peyer's patches in an orally tolerized, collagen-induced arthritis mouse model.
    Arthritis Res Ther. 2008;10(1):R11 PMID: 18221522
  5. C-C chemokine receptor 6-regulated entry of TH-17 cells into the CNS through the choroid plexus is required for the initiation of EAE.
    Nat Immunol. 2009 May;10(5):514-23 PMID: 19305396
  6. Halofuginone: a novel antifibrotic therapy.
    Gen Pharmacol. 1998 Apr;30(4):445-50 PMID: 9522159
  7. Gene expression during chemically induced liver fibrosis: effect of halofuginone on TGF-beta signaling.
    Cell Tissue Res. 2007 Apr;328(1):153-66 PMID: 17180598
  8. IL-12- and IL-23-modulated T cells induce distinct types of EAE based on histology, CNS chemokine profile, and response to cytokine inhibition.
    J Exp Med. 2008 Jul 7;205(7):1535-41 PMID: 18573909
  9. Halofuginone inhibits NF-kappaB and p38 MAPK in activated T cells.
    J Leukoc Biol. 2006 Aug;80(2):399-406 PMID: 16769768
  10. Transforming growth factor-beta regulation of immune responses.
    Annu Rev Immunol. 2006;24:99-146 PMID: 16551245
  11. The orphan nuclear receptor RORgammat directs the differentiation program of proinflammatory IL-17+ T helper cells.
    Cell. 2006 Sep 22;126(6):1121-33 PMID: 16990136
  12. GCN2 kinase in T cells mediates proliferative arrest and anergy induction in response to indoleamine 2,3-dioxygenase.
    Immunity. 2005 May;22(5):633-42 PMID: 15894280
  13. A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17.
    Nat Immunol. 2005 Nov;6(11):1133-41 PMID: 16200068
  14. STAT3 regulates cytokine-mediated generation of inflammatory helper T cells.
    J Biol Chem. 2007 Mar 30;282(13):9358-9363 PMID: 17277312
  15. Coping with stress: eIF2 kinases and translational control.
    Biochem Soc Trans. 2006 Feb;34(Pt 1):7-11 PMID: 16246168
  16. IL-23 drives a pathogenic T cell population that induces autoimmune inflammation.
    J Exp Med. 2005 Jan 17;201(2):233-40 PMID: 15657292
  17. IL-6 programs T(H)-17 cell differentiation by promoting sequential engagement of the IL-21 and IL-23 pathways.
    Nat Immunol. 2007 Sep;8(9):967-74 PMID: 17581537
  18. XBP-1 regulates a subset of endoplasmic reticulum resident chaperone genes in the unfolded protein response.
    Mol Cell Biol. 2003 Nov;23(21):7448-59 PMID: 14559994
  19. IL-6 blockade inhibits the induction of myelin antigen-specific Th17 cells and Th1 cells in experimental autoimmune encephalomyelitis.
    Proc Natl Acad Sci U S A. 2008 Jul 1;105(26):9041-6 PMID: 18577591
  20. An integrated stress response regulates amino acid metabolism and resistance to oxidative stress.
    Mol Cell. 2003 Mar;11(3):619-33 PMID: 12667446
  21. Regulated translation initiation controls stress-induced gene expression in mammalian cells.
    Mol Cell. 2000 Nov;6(5):1099-108 PMID: 11106749
  22. T helper 17 lineage differentiation is programmed by orphan nuclear receptors ROR alpha and ROR gamma.
    Immunity. 2008 Jan;28(1):29-39 PMID: 18164222
  23. Amino acid limitation regulates the expression of genes involved in several specific biological processes through GCN2-dependent and GCN2-independent pathways.
    FEBS J. 2009 Feb;276(3):707-18 PMID: 19120448
  24. Activation of antigen-presenting cells by microbial products breaks self tolerance and induces autoimmune disease.
    J Clin Invest. 2004 Apr;113(7):990-7 PMID: 15057305
  25. Halofuginone to treat fibrosis in chronic graft-versus-host disease and scleroderma.
    Biol Blood Marrow Transplant. 2003 Jul;9(7):417-25 PMID: 12869955
  26. IL-17 and Th17 Cells.
    Annu Rev Immunol. 2009;27:485-517 PMID: 19132915
  27. Creating immune privilege: active local suppression that benefits friends, but protects foes.
    Nat Rev Immunol. 2008 Jan;8(1):74-80 PMID: 18064049
  28. Signal integration in the endoplasmic reticulum unfolded protein response.
    Nat Rev Mol Cell Biol. 2007 Jul;8(7):519-29 PMID: 17565364
Article Info
Journal
Science (New York, N.Y.)
Abbr.
Science
ISSN
1095-9203
Published
2009-06-05
Pages
1334-8
Language
English
Region
United States
NLM ID
0404511
PMCID
PMC2803727
Subset
IM
Grants
NIAID NIH HHS · R01 AI040127-09 · United States
NIAID NIH HHS · R01 AI040127 · United States
NIAID NIH HHS · R01 AI048213 · United States
NCI NIH HHS · R01 CA042471 · United States
NIAID NIH HHS · R01 AI048213-01 · United States
Corrections
CommentIn
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