Home LiteratureArticle Details
PMID: 18663128 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Human interleukin 17-producing cells originate from a CD161+CD4+ T cell precursor.

The Journal of experimental medicine ·Vol. 205 ·No. 8 ·2008-08-04 ·Pages 1903-16

Cosmi L, De Palma R, Santarlasci V, Maggi L, Capone M, Frosali F, Rodolico G, Querci V, Abbate G, Angeli R, Berrino L, Fambrini M, Caproni M, Tonelli F, Lazzeri E, Parronchi P, Liotta F, Maggi E, Romagnani S, Annunziato F

Abstract

We demonstrate that CD161 is a highly up-regulated gene in human interleukin (IL) 17 T helper cell (Th17) clones and that all IL-17-producing cells are contained in the CD161(+) fraction of CD4(+) T cells present in the circulation or in inflamed tissues, although they are not CD1-restricted natural killer T cells. More importantly, we show that all IL-17-producing cells originate from CD161(+) naive CD4(+) T cells of umbilical cord blood, as well as of the postnatal thymus, in response to the combined activity of IL-1 beta and IL-23. These findings implicate CD161 as a novel surface marker for human Th17 cells and demonstrate the exclusive origin of these cells from a CD161(+)CD4(+) T cell progenitor.

MeSH Terms
Adult Antigens, Surface/genetics,metabolism CD4-Positive T-Lymphocytes/cytology,immunology Case-Control Studies Cell Differentiation Crohn Disease/genetics,immunology Fetal Blood/cytology,immunology Hematopoietic Stem Cells/cytology,immunology Humans Infant, Newborn Inflammation/genetics,immunology,pathology Interleukin-17/biosynthesis Lectins, C-Type/genetics,metabolism NK Cell Lectin-Like Receptor Subfamily B Nuclear Receptor Subfamily 1, Group F, Member 3 Psoriasis/genetics,immunology RNA, Messenger/genetics,metabolism Receptors, Interleukin/genetics Receptors, Retinoic Acid/genetics Receptors, Thyroid Hormone/genetics T-Lymphocyte Subsets/cytology,immunology Th1 Cells/cytology,immunology Th2 Cells/cytology,immunology Thymus Gland/cytology,immunology Up-Regulation
Chemicals
Antigens, Surface IL23R protein, human Interleukin-17 KLRB1 protein, human Lectins, C-Type NK Cell Lectin-Like Receptor Subfamily B Nuclear Receptor Subfamily 1, Group F, Member 3 RNA, Messenger RORC protein, human Receptors, Interleukin Receptors, Retinoic Acid Receptors, Thyroid Hormone
Authors & Affiliations
20 authors, click to expand affiliations / ORCID
Cosmi Lorenzo
Department of Internal Medicine and DENOTHE Center, University of Florence, Florence 50134, Italy.
De Palma Raffaele
Santarlasci Veronica
Maggi Laura
Capone Manuela
Frosali Francesca
Rodolico Gabriella
Querci Valentina
Abbate Gianfranco
Angeli Roberta
Berrino Liberato
Fambrini Massimiliano
Caproni Marzia
Tonelli Francesco
Lazzeri Elena
Parronchi Paola
Liotta Francesco
Maggi Enrico
Romagnani Sergio
Annunziato Francesco
References (49)
49 references, click to expand
  1. Direct access to CD4+ T cells specific for defined antigens according to CD154 expression.
    Nat Med. 2005 Oct;11(10):1118-24 PMID: 16186818
  2. Distinct subsets of CD1d-restricted T cells recognize self-antigens loaded in different cellular compartments.
    J Exp Med. 1999 Jan 4;189(1):103-10 PMID: 9874567
  3. Natural killer T-cell characterization through gene expression profiling: an account of versatility bridging T helper type 1 (Th1), Th2 and Th17 immune responses.
    Immunology. 2008 Jan;123(1):45-56 PMID: 17916165
  4. Demonstration of circulating allergen-specific CD4+CD25highFoxp3+ T-regulatory cells in both nonatopic and atopic individuals.
    J Allergy Clin Immunol. 2007 Aug;120(2):429-36 PMID: 17604089
  5. Human CD4+ central and effector memory T cells produce IL-21: effect on cytokine-driven proliferation of CD4+ T cell subsets.
    Int Immunol. 2007 Oct;19(10):1191-9 PMID: 17698559
  6. Commensal gut flora drives the expansion of proinflammatory CD4 T cells in the colonic lamina propria under normal and inflammatory conditions.
    J Immunol. 2008 Jan 1;180(1):559-68 PMID: 18097058
  7. T(H)-17 differentiation: of mice and men.
    Nat Immunol. 2007 Sep;8(9):903-5 PMID: 17712339
  8. T-cell repertoire diversity and clonal expansions in normal and clinical samples.
    Immunol Today. 1995 Apr;16(4):176-81 PMID: 7734044
  9. Expression of CD161 (NKR-P1A) defines subsets of human CD4 and CD8 T cells with different functional activities.
    J Immunol. 2006 Jan 1;176(1):211-6 PMID: 16365412
  10. Control points in NKT-cell development.
    Nat Rev Immunol. 2007 Jul;7(7):505-18 PMID: 17589542
  11. Interleukins 1beta and 6 but not transforming growth factor-beta are essential for the differentiation of interleukin 17-producing human T helper cells.
    Nat Immunol. 2007 Sep;8(9):942-9 PMID: 17676045
  12. CD1d-restricted NKT cells: an interstrain comparison.
    J Immunol. 2001 Aug 1;167(3):1164-73 PMID: 11466330
  13. Surface phenotype and antigenic specificity of human interleukin 17-producing T helper memory cells.
    Nat Immunol. 2007 Jun;8(6):639-46 PMID: 17486092
  14. Complexes of heparin and platelet factor 4 specifically stimulate T cells from patients with heparin-induced thrombocytopenia/thrombosis.
    Blood. 1999 Jul 1;94(1):208-15 PMID: 10381515
  15. Optimal induction of T helper 17 cells in humans requires T cell receptor ligation in the context of Toll-like receptor-activated monocytes.
    Proc Natl Acad Sci U S A. 2007 Oct 23;104(43):17034-9 PMID: 17942669
  16. Cutting edge: lectin-like transcript-1 is a ligand for the inhibitory human NKR-P1A receptor.
    J Immunol. 2005 Dec 15;175(12):7796-9 PMID: 16339513
  17. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells.
    Nature. 2006 May 11;441(7090):235-8 PMID: 16648838
  18. CD1d-specific NK1.1+ T cells with a transgenic variant TCR.
    J Immunol. 2000 Jul 1;165(1):168-74 PMID: 10861049
  19. Prognostic value of pretransplantation host thymic function in HLA-identical sibling hematopoietic stem cell transplantation.
    Blood. 2005 Mar 15;105(6):2608-13 PMID: 15546951
  20. Ozone exposure in a mouse model induces airway hyperreactivity that requires the presence of natural killer T cells and IL-17.
    J Exp Med. 2008 Feb 18;205(2):385-93 PMID: 18250191
  21. Transcriptional regulation of Th1/Th2 polarization.
    Immunol Today. 2000 Oct;21(10):479-83 PMID: 11071525
  22. Diverse populations of T cells with NK cell receptors accumulate in the human intestine in health and in colorectal cancer.
    Eur J Immunol. 2004 Aug;34(8):2110-9 PMID: 15259008
  23. Development, cytokine profile and function of human interleukin 17-producing helper T cells.
    Nat Immunol. 2007 Sep;8(9):950-7 PMID: 17676044
  24. IL-12- and IL-23-induced T helper cell subsets: birds of the same feather flock together.
    J Exp Med. 2005 Jan 17;201(2):169-71 PMID: 15657286
  25. Upregulation of interleukin-12 and -17 in active inflammatory bowel disease.
    Scand J Gastroenterol. 2003 Feb;38(2):180-5 PMID: 12678335
  26. Tissue-specific segregation of CD1d-dependent and CD1d-independent NK T cells.
    J Immunol. 1999 Jun 1;162(11):6410-9 PMID: 10352254
  27. Increased cell division but not thymic dysfunction rapidly affects the T-cell receptor excision circle content of the naive T cell population in HIV-1 infection.
    Nat Med. 2000 Sep;6(9):1036-42 PMID: 10973325
  28. The biology of NKT cells.
    Annu Rev Immunol. 2007;25:297-336 PMID: 17150027
  29. Autoimmunity: IL-21: a new player in Th17-cell differentiation.
    Immunol Cell Biol. 2007 Oct;85(7):503-5 PMID: 17768419
  30. IL-17 family cytokines and the expanding diversity of effector T cell lineages.
    Annu Rev Immunol. 2007;25:821-52 PMID: 17201677
  31. CLEC2A: a novel, alternatively spliced and skin-associated member of the NKC-encoded AICL-CD69-LLT1 family.
    Immunogenetics. 2007 Dec;59(12):903-12 PMID: 18046548
  32. Phenotypic and functional features of human Th17 cells.
    J Exp Med. 2007 Aug 6;204(8):1849-61 PMID: 17635957
  33. Interleukin-17 in inflammatory skin disorders.
    Curr Opin Allergy Clin Immunol. 2007 Oct;7(5):374-81 PMID: 17873575
  34. Diverse TCRs recognize murine CD1.
    J Immunol. 1999 Jan 1;162(1):161-7 PMID: 9886382
  35. Interleukin-23 promotes a distinct CD4 T cell activation state characterized by the production of interleukin-17.
    J Biol Chem. 2003 Jan 17;278(3):1910-4 PMID: 12417590
  36. Functional diversity of helper T lymphocytes.
    Nature. 1996 Oct 31;383(6603):787-93 PMID: 8893001
  37. The Th1/Th2 paradigm.
    Immunol Today. 1997 Jun;18(6):263-6 PMID: 9190109
  38. CD8beta/CD28 expression defines functionally distinct populations of peripheral blood T lymphocytes.
    Clin Exp Immunol. 2003 Sep;133(3):334-43 PMID: 12930358
  39. Restricted and conserved T-cell repertoires involved in allorecognition of class II major histocompatibility complex.
    Proc Natl Acad Sci U S A. 1995 Sep 12;92(19):8836-40 PMID: 7568027
  40. NKT cells: what's in a name?
    Nat Rev Immunol. 2004 Mar;4(3):231-7 PMID: 15039760
  41. NKRP1A molecule is involved in transendothelial migration of CD4+ human T lymphocytes.
    Immunol Lett. 1997 Jun 1;57(1-3):121-3 PMID: 9232437
  42. Interleukin (IL)-22 and IL-17 are coexpressed by Th17 cells and cooperatively enhance expression of antimicrobial peptides.
    J Exp Med. 2006 Oct 2;203(10):2271-9 PMID: 16982811
  43. IL-12-mediated NKRP1A up-regulation and consequent enhancement of endothelial transmigration of V delta 2+ TCR gamma delta+ T lymphocytes from healthy donors and multiple sclerosis patients.
    J Immunol. 1999 Apr 1;162(7):4349-54 PMID: 10201968
  44. Identification of an IL-17-producing NK1.1(neg) iNKT cell population involved in airway neutrophilia.
    J Exp Med. 2007 May 14;204(5):995-1001 PMID: 17470641
  45. Distinct regulation of interleukin-17 in human T helper lymphocytes.
    Arthritis Rheum. 2007 Sep;56(9):2936-46 PMID: 17763419
  46. Human NKR-P1A. A disulfide-linked homodimer of the C-type lectin superfamily expressed by a subset of NK and T lymphocytes.
    J Immunol. 1994 Sep 15;153(6):2417-28 PMID: 8077657
  47. Stimulation of the intracellular bacterial sensor NOD2 programs dendritic cells to promote interleukin-17 production in human memory T cells.
    Immunity. 2007 Oct;27(4):660-9 PMID: 17919942
  48. Interleukin 17-producing CD4+ effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages.
    Nat Immunol. 2005 Nov;6(11):1123-32 PMID: 16200070
  49. 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
Article Info
Journal
The Journal of experimental medicine
Abbr.
J Exp Med
ISSN
1540-9538
Published
2008-08-04
Epub
2008-00-28
Pages
1903-16
Language
English
Region
United States
NLM ID
2985109R
PMCID
PMC2525581
Subset
IM
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: [email protected]