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PMID: 23363980 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

TSLP elicits IL-33-independent innate lymphoid cell responses to promote skin inflammation.

Science translational medicine ·Vol. 5 ·No. 170 ·2013-01-30 ·Pages 170ra16

Kim BS, Siracusa MC, Saenz SA, Noti M, Monticelli LA, Sonnenberg GF, Hepworth MR, Van Voorhees AS, Comeau MR, Artis D

Abstract

Innate lymphoid cells (ILCs) are a recently identified family of heterogeneous immune cells that can be divided into three groups based on their differential developmental requirements and expression of effector cytokines. Among these, group 2 ILCs produce the type 2 cytokines interleukin-5 (IL-5) and IL-13 and promote type 2 inflammation in the lung and intestine. However, whether group 2 ILCs reside in the skin and contribute to skin inflammation has not been characterized. We identify a population of skin-resident group 2 ILCs present in healthy human skin that are enriched in lesional human skin from atopic dermatitis (AD) patients. Group 2 ILCs were also found in normal murine skin and were critical for the development of inflammation in a murine model of AD-like disease. Remarkably, in contrast to group 2 ILC responses in the intestine and lung, which are critically regulated by IL-33 and IL-25, group 2 ILC responses in the skin and skin-draining lymph nodes were independent of these canonical cytokines but were critically dependent on thymic stromal lymphopoietin (TSLP). Collectively, these results demonstrate an essential role for IL-33- and IL-25-independent group 2 ILCs in promoting skin inflammation.

MeSH Terms
Adaptive Immunity Animals Cytokines/metabolism Dermatitis, Atopic/immunology,pathology Disease Models, Animal Humans Immunity, Innate/immunology Inflammation/immunology,pathology Interleukin-33 Interleukins/metabolism Lymphocytes/immunology Mice Mice, Inbred C57BL Protein Binding Skin/immunology,pathology
Chemicals
Cytokines IL33 protein, human Il33 protein, mouse Interleukin-33 Interleukins thymic stromal lymphopoietin
Authors & Affiliations
10 authors, click to expand affiliations / ORCID
Kim Brian S
Department of Microbiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA.
Siracusa Mark C
Saenz Steven A
Noti Mario
Monticelli Laurel A
Sonnenberg Gregory F
Hepworth Matthew R
Van Voorhees Abby S
Comeau Michael R
Artis David
References (34)
34 references, click to expand
  1. Retinoic-acid-receptor-related orphan nuclear receptor alpha is required for natural helper cell development and allergic inflammation.
    Immunity. 2012 Sep 21;37(3):463-74 PMID: 22981535
  2. Human IL-25- and IL-33-responsive type 2 innate lymphoid cells are defined by expression of CRTH2 and CD161.
    Nat Immunol. 2011 Sep 11;12(11):1055-62 PMID: 21909091
  3. Innate lymphoid cells--a proposal for uniform nomenclature.
    Nat Rev Immunol. 2013 Feb;13(2):145-9 PMID: 23348417
  4. Rorγt+ innate lymphocytes and γδ T cells initiate psoriasiform plaque formation in mice.
    J Clin Invest. 2012 Jun;122(6):2252-6 PMID: 22546855
  5. Innate lymphoid cells: critical regulators of allergic inflammation and tissue repair in the lung.
    Curr Opin Immunol. 2012 Jun;24(3):284-9 PMID: 22521139
  6. The transcription factor GATA3 is essential for the function of human type 2 innate lymphoid cells.
    Immunity. 2012 Oct 19;37(4):649-59 PMID: 23063330
  7. Innate lymphoid cells promote anatomical containment of lymphoid-resident commensal bacteria.
    Science. 2012 Jun 8;336(6086):1321-5 PMID: 22674331
  8. Transcription factor RORα is critical for nuocyte development.
    Nat Immunol. 2012 Jan 22;13(3):229-36 PMID: 22267218
  9. Intradermal administration of thymic stromal lymphopoietin induces a T cell- and eosinophil-dependent systemic Th2 inflammatory response.
    J Immunol. 2008 Sep 15;181(6):4311-9 PMID: 18768889
  10. Genetic variants in thymic stromal lymphopoietin are associated with atopic dermatitis and eczema herpeticum.
    J Allergy Clin Immunol. 2010 Jun;125(6):1403-1407.e4 PMID: 20466416
  11. Human epithelial cells trigger dendritic cell mediated allergic inflammation by producing TSLP.
    Nat Immunol. 2002 Jul;3(7):673-80 PMID: 12055625
  12. Cutting edge: direct action of thymic stromal lymphopoietin on activated human CD4+ T cells.
    J Immunol. 2007 Jun 1;178(11):6720-4 PMID: 17513717
  13. Innate lymphoid cells mediate influenza-induced airway hyper-reactivity independently of adaptive immunity.
    Nat Immunol. 2011 May 29;12(7):631-8 PMID: 21623379
  14. Nuocytes represent a new innate effector leukocyte that mediates type-2 immunity.
    Nature. 2010 Apr 29;464(7293):1367-70 PMID: 20200518
  15. Induction of thymic stromal lymphopoietin expression in keratinocytes is necessary for generating an atopic dermatitis upon application of the active vitamin D3 analogue MC903 on mouse skin.
    J Invest Dermatol. 2009 Feb;129(2):498-502 PMID: 18650845
  16. Innate lymphoid cells--how did we miss them?
    Nat Rev Immunol. 2013 Feb;13(2):75-87 PMID: 23292121
  17. Langerhans cells are critical in the development of atopic dermatitis-like inflammation and symptoms in mice.
    J Cell Mol Med. 2009 Aug;13(8B):2658-2672 PMID: 19538461
  18. Innate lymphoid cells: balancing immunity, inflammation, and tissue repair in the intestine.
    Cell Host Microbe. 2012 Oct 18;12(4):445-57 PMID: 23084914
  19. Innate lymphoid cells responding to IL-33 mediate airway hyperreactivity independently of adaptive immunity.
    J Allergy Clin Immunol. 2012 Jan;129(1):216-27.e1-6 PMID: 22119406
  20. Innate lymphoid cells promote lung-tissue homeostasis after infection with influenza virus.
    Nat Immunol. 2011 Nov;12(11):1045-54 PMID: 21946417
  21. Human dendritic cells activated by TSLP and CD40L induce proallergic cytotoxic T cells.
    J Exp Med. 2003 Apr 21;197(8):1059-63 PMID: 12707303
  22. Lung natural helper cells are a critical source of Th2 cell-type cytokines in protease allergen-induced airway inflammation.
    Immunity. 2012 Mar 23;36(3):451-63 PMID: 22425247
  23. TSLP produced by keratinocytes promotes allergen sensitization through skin and thereby triggers atopic march in mice.
    J Invest Dermatol. 2013 Jan;133(1):154-63 PMID: 22832486
  24. IL-25 in atopic dermatitis: a possible link between inflammation and skin barrier dysfunction?
    J Invest Dermatol. 2011 Jan;131(1):150-7 PMID: 20861853
  25. The transcription factor GATA-3 controls cell fate and maintenance of type 2 innate lymphoid cells.
    Immunity. 2012 Oct 19;37(4):634-48 PMID: 23063333
  26. TSLP promotes interleukin-3-independent basophil haematopoiesis and type 2 inflammation.
    Nature. 2011 Aug 14;477(7363):229-33 PMID: 21841801
  27. Thymic stromal lymphopoietin overproduced by keratinocytes in mouse skin aggravates experimental asthma.
    Proc Natl Acad Sci U S A. 2009 Feb 3;106(5):1536-41 PMID: 19188585
  28. Innate lymphoid cells: emerging insights in development, lineage relationships, and function.
    Annu Rev Immunol. 2012;30:647-75 PMID: 22224763
  29. Innate production of T(H)2 cytokines by adipose tissue-associated c-Kit(+)Sca-1(+) lymphoid cells.
    Nature. 2010 Jan 28;463(7280):540-4 PMID: 20023630
  30. Langerhans cells are critical in epicutaneous sensitization with protein antigen via thymic stromal lymphopoietin receptor signaling.
    J Allergy Clin Immunol. 2012 Apr;129(4):1048-55.e6 PMID: 22385635
  31. Systemically dispersed innate IL-13-expressing cells in type 2 immunity.
    Proc Natl Acad Sci U S A. 2010 Jun 22;107(25):11489-94 PMID: 20534524
  32. The U.K. Working Party's Diagnostic Criteria for Atopic Dermatitis. I. Derivation of a minimum set of discriminators for atopic dermatitis.
    Br J Dermatol. 1994 Sep;131(3):383-96 PMID: 7918015
  33. Innate lymphoid cell interactions with microbiota: implications for intestinal health and disease.
    Immunity. 2012 Oct 19;37(4):601-10 PMID: 23084357
  34. Human TSLP promotes CD40 ligand-induced IL-12 production by myeloid dendritic cells but maintains their Th2 priming potential.
    Blood. 2005 Jun 15;105(12):4749-51 PMID: 15741223
Article Info
Journal
Science translational medicine
Abbr.
Sci Transl Med
ISSN
1946-6242
Published
2013-01-30
Pages
170ra16
Language
English
Region
United States
NLM ID
101505086
PMCID
PMC3637661
Subset
IM
Grants
NIAID NIH HHS · R01 AI095466 · United States
NIAID NIH HHS · AI061570 · United States
NIAID NIH HHS · AI087990 · United States
NCI NIH HHS · 2-P30 CA016520 · United States
NIAMS NIH HHS · 5-P30-AR-057217 · United States
NIAID NIH HHS · R21 AI083480 · United States
NIAID NIH HHS · U01 AI095608 · United States
NIAID NIH HHS · R01 AI074878 · United States
NIAID NIH HHS · AI085828 · United States
NIDDK NIH HHS · P30 DK050306 · United States
NIAID NIH HHS · T32 AI007532 · United States
NCRR NIH HHS · KL2-RR024132 · United States
NIAID NIH HHS · AI102942 · United States
NIH HHS · DP5OD012116 · United States
NIH HHS · DP5 OD012116 · United States
NIAID NIH HHS · F32 AI085828 · United States
NIAID NIH HHS · AI074878 · United States
NIAID NIH HHS · T32-AI007532 · United States
NIAID NIH HHS · AI083480 · United States
NIAID NIH HHS · R01 AI102942 · United States
NIAID NIH HHS · R21 AI087990 · United States
NCRR NIH HHS · KL2 RR024132 · United States
NIAMS NIH HHS · T32 AR007465 · United States
NIAID NIH HHS · AI095608 · United States
NCI NIH HHS · P30 CA016520 · United States
NCATS NIH HHS · KL2TR000139 · United States
NIDDK NIH HHS · P30-DK050306 · United States
NIAID NIH HHS · R01 AI061570 · United States
NIAMS NIH HHS · P30 AR057217 · United States
NIAID NIH HHS · R01 AI097333 · United States
NIAID NIH HHS · AI095466 · United States
NIAID NIH HHS · AI097333 · United States
NCATS NIH HHS · KL2 TR000139 · United States
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