Abstract
Isolated peripheral blood CD4 cells from allergic individuals express CC chemokine receptor (CCR)3 and CCR4 after expansion in vitro. In addition, human T helper type 2 (Th2) cells polarized in vitro selectively express CCR3 and CCR4 at certain stages of activation/differentiation and respond preferentially to the ligands eotaxin and monocyte-derived chemokine (MDC). However, controversy arises when the in vivo significance of this distinct expression is discussed. To address the functional role of CCR3/eotaxin and CCR4/MDC during the in vivo recruitment of Th2 cells, we have transferred effector Th cells into naive mice to induce allergic airway disease. Tracking of these cells after repeated antigen challenge has established that both CCR3/eotaxin and CCR4/MDC axes contribute to the recruitment of Th2 cells to the lung, demonstrating the in vivo relevance of the expression of these receptors on Th2 cells. We have shown that involvement of the CCR3/eotaxin pathway is confined to early stages of the response in vivo, whereas repeated antigen stimulation results in the predominant use of the CCR4/MDC pathway. We propose that effector Th2 cells respond to both CCR3/eotaxin and CCR4/MDC pathways initially, but that a progressive increase in CCR4-positive cells results in the predominance of the CCR4/MDC axis in the long-term recruitment of Th2 cells in vivo.
MeSH Terms
Adoptive Transfer
Allergens/immunology
Animals
CD4-Positive T-Lymphocytes/cytology,immunology
CD8-Positive T-Lymphocytes/immunology
Cells, Cultured
Female
Gene Expression
Humans
Lung/cytology,immunology
Mice
Mice, Inbred BALB C
Mice, Transgenic
Ovalbumin/immunology
Receptors, CCR3
Receptors, CCR4
Receptors, Chemokine/genetics,immunology,metabolism
Th1 Cells/immunology
Th2 Cells/immunology,metabolism
Chemicals
Allergens
CCR3 protein, human
CCR4 protein, human
Ccr3 protein, mouse
Ccr4 protein, mouse
Receptors, CCR3
Receptors, CCR4
Receptors, Chemokine
Ovalbumin
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Lloyd C M
Millennium Pharmaceuticals, Inc., Cambridge, Massachusetts 02139, USA. c.lloyd@ic.ac.uk
Delaney T
Nguyen T
Tian J
Martinez-A C
Coyle A J
Gutierrez-Ramos J C
References (22)
22 references, click to expand
-
The major histocompatibility complex-restricted antigen receptor on T cells. IV. An antiidiotypic antibody predicts both antigen and I-specificity.
J Exp Med. 1983 Nov 1;158(5):1635-46
PMID: 6195288
-
Crucial role of the interleukin 1 receptor family member T1/ST2 in T helper cell type 2-mediated lung mucosal immune responses.
J Exp Med. 1999 Oct 4;190(7):895-902
PMID: 10510079
-
Molecular cloning of the human eosinophil peroxidase. Evidence for the existence of a peroxidase multigene family.
J Exp Med. 1989 May 1;169(5):1757-69
PMID: 2541222
-
Induction by antigen of intrathymic apoptosis of CD4+CD8+TCRlo thymocytes in vivo.
Science. 1990 Dec 21;250(4988):1720-3
PMID: 2125367
-
Cloning, expression, and characterization of the human eosinophil eotaxin receptor.
J Exp Med. 1996 May 1;183(5):2349-54
PMID: 8642344
-
Molecular cloning and characterization of a human eotaxin receptor expressed selectively on eosinophils.
J Exp Med. 1996 Jun 1;183(6):2437-48
PMID: 8676064
-
Eosinophil recruitment to the lung in a murine model of allergic inflammation. The role of T cells, chemokines, and adhesion receptors.
J Clin Invest. 1996 Nov 15;98(10):2332-45
PMID: 8941651
-
Chemokine receptors and T cell chemotaxis.
J Exp Med. 1996 Sep 1;184(3):799-802
PMID: 9064339
-
Human macrophage-derived chemokine (MDC), a novel chemoattractant for monocytes, monocyte-derived dendritic cells, and natural killer cells.
J Exp Med. 1997 May 5;185(9):1595-604
PMID: 9151897
-
Selective expression of the eotaxin receptor CCR3 by human T helper 2 cells.
Science. 1997 Sep 26;277(5334):2005-7
PMID: 9302298
-
Induction of airway mucus production By T helper 2 (Th2) cells: a critical role for interleukin 4 in cell recruitment but not mucus production.
J Exp Med. 1997 Nov 17;186(10):1737-47
PMID: 9362533
-
Differential expression of chemokine receptors and chemotactic responsiveness of type 1 T helper cells (Th1s) and Th2s.
J Exp Med. 1998 Jan 5;187(1):129-34
PMID: 9419219
-
Selective expression of a stable cell surface molecule on type 2 but not type 1 helper T cells.
J Exp Med. 1998 Mar 2;187(5):787-94
PMID: 9480988
-
Flexible programs of chemokine receptor expression on human polarized T helper 1 and 2 lymphocytes.
J Exp Med. 1998 Mar 16;187(6):875-83
PMID: 9500790
-
The coordinated action of CC chemokines in the lung orchestrates allergic inflammation and airway hyperresponsiveness.
J Exp Med. 1998 Jul 6;188(1):157-67
PMID: 9653092
-
Th2-induced eotaxin expression and eosinophilia coexist with Th1 responses at the effector stage of lung inflammation.
J Immunol. 1998 Sep 15;161(6):3128-35
PMID: 9743380
-
STCP-1 (MDC) CC chemokine acts specifically on chronically activated Th2 lymphocytes and is produced by monocytes on stimulation with Th2 cytokines IL-4 and IL-13.
J Immunol. 1998 Nov 1;161(9):5027-38
PMID: 9794440
-
Selective up-regulation of chemokine receptors CCR4 and CCR8 upon activation of polarized human type 2 Th cells.
J Immunol. 1998 Nov 15;161(10):5111-5
PMID: 9820476
-
Allergen-specific Th1 cells fail to counterbalance Th2 cell-induced airway hyperreactivity but cause severe airway inflammation.
J Clin Invest. 1999 Jan;103(2):175-83
PMID: 9916129
-
Th2-induced airway mucus production is dependent on IL-4Ralpha, but not on eosinophils.
J Immunol. 1999 May 15;162(10):6178-83
PMID: 10229862
-
Mouse monocyte-derived chemokine is involved in airway hyperreactivity and lung inflammation.
J Immunol. 1999 Jul 1;163(1):403-11
PMID: 10384142
-
TH1 and TH2 cells: different patterns of lymphokine secretion lead to different functional properties.
Annu Rev Immunol. 1989;7:145-73
PMID: 2523712