Abstract
The effector functions of CD4+ cells in vivo are presumed to reflect a combination of lymphokine-mediated bystander reactions and direct cytotoxic T lymphocyte activity. To assess the relative importance of these two mechanisms, we studied the effects of transferring small doses of purified unprimed CD4+ cells to lightly irradiated (600 cGy) recipients expressing major histocompatibility complex class II (Ia) differences. Within the first week after transfer, the host marrow was rapidly repopulated with hemopoietic cells. Thereafter, however, the donor CD4+ cells caused massive destruction of hemopoietic cells, both in marrow and spleen. Marrow aplasia did not affect stromal cells and was prevented by coinjecting donor but not host bone marrow. The use of allotypic markers and fluorescence-activated cell sorter analysis indicated that the destructive effects of CD4+ cells were directed selectively to host Ia+ hemopoietic cells, including stem cells; donor hemopoietic cells and Ia- host T cells were spared. No evidence could be found that the ongoing destruction of host cells impaired the capacity of donor stem cells to repopulate marrow, spleen, or thymus. Moreover, CD4+ cells failed to destroy host-type hemopoietic cells from Ia-deficient mice. Tissue destruction by CD4+ cells thus did not seem to reflect a bystander reaction. We conclude that, under defined conditions, CD4+ cells can manifest extremely potent Ia-restricted CTL activity in vivo, probably through recognition of covert Ia expression on stem cells and/or their immediate progeny.
MeSH Terms
Animals
Atrophy
Bone Marrow/pathology
CD4-Positive T-Lymphocytes/immunology
Cell Movement
Graft vs Host Disease/etiology
Hematopoietic Stem Cells/pathology
Histocompatibility Antigens Class II/analysis,physiology
Mice
Chemicals
Histocompatibility Antigens Class II
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Sprent J
Department of Immunology, Scripps Research Institute, La Jolla, California 92037.
Surh C D
Agus D
Hurd M
Sutton S
Heath W R
References (20)
20 references, click to expand
-
A monoclonal antibody discriminating between subsets of T and B cells.
J Immunol. 1981 Dec;127(6):2496-501
PMID: 6975326
-
The role of host T cell subsets in bone marrow rejection directed to isolated major histocompatibility complex class I versus class II differences of bm1 and bm12 mutant mice.
Transplantation. 1994 Jan;57(2):249-56
PMID: 7906058
-
GVHR elicited by products of class I or class II loci of the MHC: analysis of the response of mouse T lymphocytes to products of class I and class II loci of the MHC in correlation with GVHR-induced mortality, medullary aplasia, and enteropathy.
J Immunol. 1985 Sep;135(3):1637-43
PMID: 2410497
-
Cytolytic T lymphocytes.
Annu Rev Immunol. 1983;1:273-306
PMID: 6085785
-
Properties of purified T cell subsets. I. In vitro responses to class I vs. class II H-2 alloantigens.
J Exp Med. 1985 Dec 1;162(6):2068-88
PMID: 2933483
-
Two types of murine helper T cell clone. II. Delayed-type hypersensitivity is mediated by TH1 clones.
J Immunol. 1987 Jun 1;138(11):3688-94
PMID: 2953788
-
Tumor necrosis factor/cachectin is an effector of skin and gut lesions of the acute phase of graft-vs.-host disease.
J Exp Med. 1987 Nov 1;166(5):1280-9
PMID: 3316469
-
The generation of antigen-specific, major histocompatibility complex-restricted cytotoxic T lymphocytes of the CD4+ phenotype. Enhancement by the cutaneous administration of interleukin 2.
J Exp Med. 1989 Mar 1;169(3):909-19
PMID: 2522499
-
CD4+ T cell-mediated killing of MHC class II-positive antigen-presenting cells. I. Characterization of target cell recognition by in vivo or in vitro activated CD4+ killer T cells.
J Immunol. 1990 Feb 1;144(3):790-5
PMID: 1967273
-
Role of T cell subsets in lethal graft-versus-host disease (GVHD) directed to class I versus class II H-2 differences. II. Protective effects of L3T4+ cells in anti-class II GVHD.
J Immunol. 1990 Apr 15;144(8):2946-54
PMID: 1969878
-
Specific killing of cytotoxic T cells and antigen-presenting cells by CD4+ cytotoxic T cell clones. A novel potentially immunoregulatory T-T cell interaction in man.
J Exp Med. 1990 Jun 1;171(6):2011-24
PMID: 1972178
-
Evidence of a role for TNF-alpha in cytolysis by CD4+, class II MHC-restricted cytotoxic T cells.
Immunology. 1990 Oct;71(2):208-12
PMID: 2228021
-
Depletion of CD4+ T cells in major histocompatibility complex class II-deficient mice.
Science. 1991 Sep 20;253(5026):1417-20
PMID: 1910207
-
CD4+ T cell-mediated killing of major histocompatibility complex class II-positive antigen-presenting cells (APC). III. CD4+ cytotoxic T cells induce apoptosis of APC.
Eur J Immunol. 1992 Jan;22(1):267-72
PMID: 1346113
-
Relationship between cytokine-dependent cell cycle progression and MHC class II antigen expression by human CD34+ HLA-DR- bone marrow cells.
J Immunol. 1992 Feb 1;148(3):815-20
PMID: 1370518
-
Cellular basis of skin allograft rejection: an in vivo model of immune-mediated tissue destruction.
Annu Rev Immunol. 1992;10:333-58
PMID: 1590990
-
Lymphocyte development from stem cells.
Annu Rev Immunol. 1992;10:759-83
PMID: 1375474
-
Stimulation of mature unprimed CD8+ T cells by semiprofessional antigen-presenting cells in vivo.
J Exp Med. 1992 Nov 1;176(5):1291-302
PMID: 1402675
-
Mycobacteria induce CD4+ T cells that are cytotoxic and display Th1-like cytokine secretion profile: heterogeneity in cytotoxic activity and cytokine secretion levels.
Eur J Immunol. 1993 Sep;23(9):2189-95
PMID: 8103743
-
Specificity, phenotype, and precursor frequency of primary cytolytic T lymphocytes specific for class II major histocompatibility antigens.
J Immunol. 1985 Sep;135(3):1610-5
PMID: 3874902