Home LiteratureArticle Details
PMID: 9207002 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Requirements for CD1d recognition by human invariant Valpha24+ CD4-CD8- T cells.

The Journal of experimental medicine ·Vol. 186 ·No. 1 ·1997-07-07 ·Pages 109-20

Exley M, Garcia J, Balk SP, Porcelli S

Abstract

A subset of human CD4-CD8- T cells that expresses an invariant Valpha24-JalphaQ T cell receptor (TCR)-alpha chain, paired predominantly with Vbeta11, has been identified. A series of these Valpha24 Vbeta11 clones were shown to have TCR-beta CDR3 diversity and express the natural killer (NK) locus-encoded C-type lectins NKR-P1A, CD94, and CD69. However, in contrast to NK cells, they did not express killer inhibitory receptors, CD16, CD56, or CD57. All invariant Valpha24(+) clones recognized the MHC class I-like CD16 molecule and discriminated between CD1d and other closely related human CD1 proteins, indicating that recognition was TCR-mediated. Recognition was not dependent upon an endosomal targeting motif in the cytoplasmic tail of CD1d. Upon activation by anti-CD3 or CD1d, the clones produced both Th1 and Th2 cytokines. These results demonstrate that human invariant Valpha24+ CD4-CD8- T cells, and presumably the homologous murine NK1+ T cell population, are CD1d reactive and functionally distinct from NK cells. The conservation of this cell population and of the CD1d ligand across species indicates an important immunological function.

MeSH Terms
Animals Antigens, CD/immunology Cytokines/biosynthesis,immunology Flow Cytometry Humans Immunophenotyping Major Histocompatibility Complex/immunology Mice Receptors, Antigen, T-Cell, alpha-beta/genetics,immunology T-Lymphocyte Subsets/immunology
Chemicals
Antigens, CD Cytokines Receptors, Antigen, T-Cell, alpha-beta
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Exley M
Cancer Biology Program, Hematology/Oncology Division, Beth Israel Deaconess Medical Center and Harvard Medical School, Boston, Massachusetts 02215, USA.
Garcia J
Balk S P
Porcelli S
References (70)
70 references, click to expand
  1. Two classes of CD1 genes.
    Eur J Immunol. 1989 Feb;19(2):285-92 PMID: 2467814
  2. Expression of HLA-C molecules confers target cell resistance to some non-major histocompatibility complex-restricted T cells in a manner analogous to allospecific natural killer cells.
    J Exp Med. 1995 Oct 1;182(4):1005-18 PMID: 7561674
  3. Expression of two T cell receptor alpha chains: dual receptor T cells.
    Science. 1993 Oct 15;262(5132):422-4 PMID: 8211163
  4. Human natural killer cell receptors for HLA-class I molecules. Evidence that the Kp43 (CD94) molecule functions as receptor for HLA-B alleles.
    J Exp Med. 1994 Aug 1;180(2):545-55 PMID: 8046333
  5. Critical role of CD28/B7 costimulation in the development of human Th2 cytokine-producing cells.
    Blood. 1995 Nov 1;86(9):3479-86 PMID: 7579453
  6. Analysis of T cell antigen receptor (TCR) expression by human peripheral blood CD4-8- alpha/beta T cells demonstrates preferential use of several V beta genes and an invariant TCR alpha chain.
    J Exp Med. 1993 Jul 1;178(1):1-16 PMID: 8391057
  7. Natural killer cell receptors: the offs and ons of NK cell recognition.
    Cell. 1995 Sep 8;82(5):697-700 PMID: 7671299
  8. Interferon gamma production by natural killer (NK) cells and NK1.1+ T cells upon NKR-P1 cross-linking.
    J Exp Med. 1996 May 1;183(5):2391-6 PMID: 8642351
  9. Characterization of a cell line, NKL, derived from an aggressive human natural killer cell leukemia.
    Exp Hematol. 1996 Feb;24(3):406-15 PMID: 8599969
  10. Role of NK1.1+ T cells in a TH2 response and in immunoglobulin E production.
    Science. 1995 Dec 15;270(5243):1845-7 PMID: 8525383
  11. Murine thymic CD4+ T cell subsets: a subset (Thy0) that secretes diverse cytokines and overexpresses the V beta 8 T cell receptor gene family.
    J Exp Med. 1992 Jul 1;176(1):269-74 PMID: 1351921
  12. NK1.1+ CD4+ CD8- thymocytes with specific lymphokine secretion.
    Eur J Immunol. 1993 Jan;23(1):307-10 PMID: 8419184
  13. Peptide binding and presentation by mouse CD1.
    Science. 1995 Jul 14;269(5221):223-6 PMID: 7542403
  14. Oligoclonal expansion and CD1 recognition by human intestinal intraepithelial lymphocytes.
    Science. 1991 Sep 20;253(5026):1411-5 PMID: 1716785
  15. Targeting of membrane proteins to endosomes and lysosomes.
    Trends Cell Biol. 1994 Aug;4(8):292-7 PMID: 14731593
  16. CD1-restricted T cell recognition of microbial lipoglycan antigens.
    Science. 1995 Jul 14;269(5221):227-30 PMID: 7542404
  17. Class I dependence of the development of CD4+ CD8- NK1.1+ thymocytes.
    J Exp Med. 1994 Jul 1;180(1):395-9 PMID: 8006596
  18. Recognition of a lipid antigen by CD1-restricted alpha beta+ T cells.
    Nature. 1994 Dec 15;372(6507):691-4 PMID: 7527500
  19. Cytolytic T lymphocytes displaying natural killer (NK)-like activity: expression of NK-related functional receptors for HLA class I molecules (p58 and CD94) and inhibitory effect on the TCR-mediated target cell lysis or lymphokine production.
    Int Immunol. 1995 Apr;7(4):697-703 PMID: 7547697
  20. Interaction of the unique N-terminal region of tyrosine kinase p56lck with cytoplasmic domains of CD4 and CD8 is mediated by cysteine motifs.
    Cell. 1990 Mar 9;60(5):755-65 PMID: 2107025
  21. A subset of CD4+ thymocytes selected by MHC class I molecules.
    Science. 1994 Mar 25;263(5154):1774-8 PMID: 7907820
  22. An invariant V alpha 24-J alpha Q/V beta 11 T cell receptor is expressed in all individuals by clonally expanded CD4-8- T cells.
    J Exp Med. 1994 Sep 1;180(3):1171-6 PMID: 8064234
  23. In vivo persistence of expanded clones specific for bacterial antigens within the human T cell receptor alpha/beta CD4-8- subset.
    J Exp Med. 1993 Jun 1;177(6):1763-71 PMID: 7684433
  24. 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
  25. CD1b restricts the response of human CD4-8- T lymphocytes to a microbial antigen.
    Nature. 1992 Dec 10;360(6404):593-7 PMID: 1281285
  26. Expansion of natural (NK1+) T cells that express alpha beta T cell receptors in transporters associated with antigen presentation-1 null and thymus leukemia antigen positive mice.
    J Exp Med. 1996 Oct 1;184(4):1579-84 PMID: 8879233
  27. Selective reduction of V alpha 14+ NK T cells associated with disease development in autoimmune-prone mice.
    J Immunol. 1996 May 15;156(10):4035-40 PMID: 8621946
  28. Expression cloning of the early activation antigen CD69, a type II integral membrane protein with a C-type lectin domain.
    J Immunol. 1993 Jun 1;150(11):4920-7 PMID: 8496594
  29. Expression of a nonpolymorphic MHC class I-like molecule, CD1D, by human intestinal epithelial cells.
    J Immunol. 1991 Oct 15;147(8):2518-24 PMID: 1717564
  30. Structure and function of the CD1 family of MHC-like cell surface proteins.
    Immunol Rev. 1995 Oct;147:5-29 PMID: 8847079
  31. Isolation and characterization of a cDNA and gene coding for a fourth CD1 molecule.
    Proc Natl Acad Sci U S A. 1989 Jan;86(1):252-6 PMID: 2463622
  32. TAP-independent, beta 2-microglobulin-dependent surface expression of functional mouse CD1.1.
    J Exp Med. 1995 Dec 1;182(6):1913-9 PMID: 7500037
  33. Inhibition of gamma delta T cell recognition by receptors for MHC class I molecules.
    J Immunol. 1995 Nov 1;155(9):4139-42 PMID: 7594567
  34. Isolation and expression of cDNA encoding the murine homologues of CD1.
    J Immunol. 1991 Jan 15;146(2):768-74 PMID: 1702817
  35. Mouse NKR-P1. A family of genes selectively coexpressed in adherent lymphokine-activated killer cells.
    J Immunol. 1991 Sep 1;147(5):1701-8 PMID: 1880421
  36. DNA sequence analysis of NKG2, a family of related cDNA clones encoding type II integral membrane proteins on human natural killer cells.
    J Exp Med. 1991 Apr 1;173(4):1017-20 PMID: 2007850
  37. Mouse CD1 is distinct from and co-exists with TL in the same thymus.
    EMBO J. 1988 Oct;7(10):3081-6 PMID: 2460336
  38. Major histocompatibility complex class I related molecules control the development of CD4+8- and CD4-8- subsets of natural killer 1.1+ T cell receptor-alpha/beta+ cells in the liver of mice.
    J Exp Med. 1994 Aug 1;180(2):699-704 PMID: 8046344
  39. NK1.1+ T cell receptor-alpha/beta+ cells: new clues to their origin, specificity, and function.
    J Exp Med. 1995 Sep 1;182(3):633-8 PMID: 7650474
  40. Selective reduction of T cells bearing invariant V alpha 24J alpha Q antigen receptor in patients with systemic sclerosis.
    J Exp Med. 1995 Oct 1;182(4):1163-8 PMID: 7561690
  41. CD1 recognition by mouse NK1+ T lymphocytes.
    Science. 1995 May 12;268(5212):863-5 PMID: 7538697
  42. Relationships between intermediate TCR cells and NK1.1+ T cells in various immune organs. NK1.1+ T cells are present within a population of intermediate TCR cells.
    J Immunol. 1995 Sep 15;155(6):2972-83 PMID: 7673715
  43. Therapeutic potentiation of the immune system by costimulatory Schiff-base-forming drugs.
    Nature. 1995 Sep 7;377(6544):71-5 PMID: 7659167
  44. Crystal structure of mouse CD1: An MHC-like fold with a large hydrophobic binding groove.
    Science. 1997 Jul 18;277(5324):339-45 PMID: 9219685
  45. An invariant T cell receptor alpha chain is used by a unique subset of major histocompatibility complex class I-specific CD4+ and CD4-8- T cells in mice and humans.
    J Exp Med. 1994 Sep 1;180(3):1097-106 PMID: 7520467
  46. Cytokine production by mature and immature CD4-CD8- T cells. Alpha beta-T cell receptor+ CD4-CD8- T cells produce IL-4.
    J Immunol. 1992 Aug 15;149(4):1211-5 PMID: 1386860
  47. Tissue distribution of the non-polymorphic major histocompatibility complex class I-like molecule, CD1d.
    Immunology. 1993 Dec;80(4):561-5 PMID: 7508419
  48. Superantigen-dependent, cell-mediated cytotoxicity inhibited by MHC class I receptors on T lymphocytes.
    Science. 1995 Apr 21;268(5209):403-5 PMID: 7716542
  49. TCR-independent activation of human CD4+ 45RO- T cells by anti-CD28 plus IL-2: Induction of clonal expansion and priming for a Th2 phenotype.
    J Immunol. 1996 Jun 1;156(11):4100-6 PMID: 8666775
  50. Dominant expression of a distinctive V14+ T-cell antigen receptor alpha chain in mice.
    Proc Natl Acad Sci U S A. 1991 Sep 1;88(17):7518-22 PMID: 1881891
  51. Molecular characterization of human CD94: a type II membrane glycoprotein related to the C-type lectin superfamily.
    Eur J Immunol. 1995 Sep;25(9):2433-7 PMID: 7589107
  52. Positive selection of invariant V alpha 14+ T cells by non-major histocompatibility complex-encoded class I-like molecules expressed on bone marrow-derived cells.
    Proc Natl Acad Sci U S A. 1995 Feb 14;92(4):1200-4 PMID: 7862661
  53. CD1 expression is not affected by human peptide transporter deficiency.
    Hum Immunol. 1994 Sep;41(1):61-8 PMID: 7530699
  54. Early defect of immunoregulatory T cells in autoimmune diabetes.
    C R Acad Sci III. 1996 Feb;319(2):125-9 PMID: 8680958
  55. Human natural killer cell receptors involved in MHC class I recognition are disulfide-linked heterodimers of CD94 and NKG2 subunits.
    J Immunol. 1996 Dec 1;157(11):4741-5 PMID: 8943374
  56. A novel functional cell surface dimer (Kp43) expressed by natural killer cells and T cell receptor-gamma/delta+ T lymphocytes. I. Inhibition of the IL-2-dependent proliferation by anti-Kp43 monoclonal antibody.
    J Immunol. 1990 Apr 15;144(8):3238-47 PMID: 1691231
  57. SR alpha promoter: an efficient and versatile mammalian cDNA expression system composed of the simian virus 40 early promoter and the R-U5 segment of human T-cell leukemia virus type 1 long terminal repeat.
    Mol Cell Biol. 1988 Jan;8(1):466-72 PMID: 2827008
  58. The CD1 family: a third lineage of antigen-presenting molecules.
    Adv Immunol. 1995;59:1-98 PMID: 7484459
  59. Inhibitory MHC class I receptors on NK cells and T cells.
    Immunol Today. 1996 Feb;17(2):86-91 PMID: 8808056
  60. Predominant expression of invariant V alpha 14+ TCR alpha chain in NK1.1+ T cell populations.
    Int Immunol. 1995 Jul;7(7):1157-61 PMID: 8527413
  61. Human T cells expressing an invariant V alpha 24-J alpha Q TCR alpha are CD4- and heterogeneous with respect to TCR beta expression.
    Hum Immunol. 1996 Jun-Jul;48(1-2):63-7 PMID: 8824574
  62. CD94 and a novel associated protein (94AP) form a NK cell receptor involved in the recognition of HLA-A, HLA-B, and HLA-C allotypes.
    Immunity. 1996 Aug;5(2):163-72 PMID: 8769479
  63. CD4pos, NK1.1pos T cells promptly produce interleukin 4 in response to in vivo challenge with anti-CD3.
    J Exp Med. 1994 Apr 1;179(4):1285-95 PMID: 7908323
  64. Natural T cells. Cells that co-express NKRP-1 and TCR.
    J Immunol. 1995 Aug 1;155(3):1020-2 PMID: 7636176
  65. CD1c restricts responses of mycobacteria-specific T cells. Evidence for antigen presentation by a second member of the human CD1 family.
    J Immunol. 1996 Oct 1;157(7):2795-803 PMID: 8816382
  66. The HLA-A,B "negative" mutant cell line C1R expresses a novel HLA-B35 allele, which also has a point mutation in the translation initiation codon.
    J Immunol. 1992 Mar 15;148(6):1941-8 PMID: 1541831
  67. Expression of cDNA clones encoding the thymocyte antigens CD1a, b, c demonstrates a hierarchy of exclusion in fibroblasts.
    J Immunol. 1989 Sep 1;143(5):1723-30 PMID: 2701945
  68. An NK1.1+ CD4+8- single-positive thymocyte subpopulation that expresses a highly skewed T-cell antigen receptor V beta family.
    Proc Natl Acad Sci U S A. 1992 Jul 15;89(14):6506-10 PMID: 1378629
  69. Structure and expression of the human thymocyte antigens CD1a, CD1b, and CD1c.
    Proc Natl Acad Sci U S A. 1987 Dec;84(24):9189-93 PMID: 2447586
  70. Cytoplasmic tail-dependent localization of CD1b antigen-presenting molecules to MIICs.
    Science. 1996 Jul 19;273(5273):349-52 PMID: 8662520
Article Info
Journal
The Journal of experimental medicine
Abbr.
J Exp Med
ISSN
0022-1007
Published
1997-07-07
Pages
109-20
Language
English
Region
United States
NLM ID
2985109R
PMCID
PMC2198960
Subset
IM
Grants
NIAID NIH HHS · R01 AI40135 · United States
NIAID NIH HHS · R01-AI33911 · 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: [email protected]