Abstract
The interaction of CD4(+) T cells with MHC class II (MHCII)-expressing hematopoietic APCs plays a critical role in both the generation of protective immune responses and maintenance of tolerance in the lung. The functional significance of MHCII expression by nonhematopoietic stromal cells, however, has not been defined in vivo. Using a novel mouse model of orthotopic left lung transplantation, we demonstrate that selective elimination of MHCII expression on nonhematopoietic cells leads to an inflammatory response as a result of reduced peripheral generation of regulatory CD4(+) T cells. Absence of MHCII expression on nonhematopoietic cells also inhibits local growth of metastatic pulmonary tumor. These findings indicate that nonhematopoietic cells play a previously unrecognized role in downregulating inflammatory responses in nonlymphoid tissues.
MeSH Terms
Adoptive Transfer
Animals
Antigen Presentation/immunology
CD8-Positive T-Lymphocytes/immunology,metabolism
Cell Separation
Endothelial Cells/immunology,metabolism
Epithelial Cells/immunology,metabolism
Flow Cytometry
Histocompatibility Antigens Class II/immunology,metabolism
Inflammation/immunology,metabolism
Lung Transplantation/immunology
Male
Mice
Mice, Inbred C57BL
Mice, Transgenic
Stromal Cells/immunology,metabolism
T-Lymphocyte Subsets/immunology,metabolism
T-Lymphocytes, Regulatory/immunology,metabolism
Chemicals
Histocompatibility Antigens Class II
Authors & Affiliations
9 authors, click to expand affiliations / ORCID
Kreisel Daniel
Department of Surgery, Washington University School of Medicine, St. Louis, MO 63110, USA.
Richardson Steven B
Li Wenjun
Lin Xue
Kornfeld Christopher G
Sugimoto Seiichiro
Hsieh Chyi-Song
Gelman Andrew E
Krupnick Alexander S
References (17)
17 references, click to expand
-
Orthotopic mouse lung transplantation as experimental methodology to study transplant and tumor biology.
Nat Protoc. 2009;4(1):86-93
PMID: 19131960
-
Non-hematopoietic allograft cells directly activate CD8+ T cells and trigger acute rejection: an alternative mechanism of allorecognition.
Nat Med. 2002 Mar;8(3):233-9
PMID: 11875493
-
Peripheral expression of self-MHC-II influences the reactivity and self-tolerance of mature CD4(+) T cells: evidence from a lymphopenic T cell model.
Immunity. 2002 Oct;17(4):425-36
PMID: 12387737
-
Survival of mature CD4 T lymphocytes is dependent on major histocompatibility complex class II-expressing dendritic cells.
J Exp Med. 1997 Oct 20;186(8):1223-32
PMID: 9334361
-
CD4+ T lymphocytes are not necessary for the acute rejection of vascularized mouse lung transplants.
J Immunol. 2008 Apr 1;180(7):4754-62
PMID: 18354199
-
Resident lung antigen-presenting cells have the capacity to promote Th2 T cell differentiation in situ.
J Clin Invest. 2002 Nov;110(10):1441-8
PMID: 12438442
-
Alveolar type II epithelial cells present antigen to CD4(+) T cells and induce Foxp3(+) regulatory T cells.
Am J Respir Crit Care Med. 2009 Mar 1;179(5):344-55
PMID: 19096007
-
Liver sinusoidal endothelial cells are insufficient to activate T cells.
J Immunol. 2004 Jul 1;173(1):230-5
PMID: 15210779
-
Epithelial cells expressing aberrant MHC class II determinants can present antigen to cloned human T cells.
Nature. 1984 Dec 13-19;312(5995):639-41
PMID: 6334239
-
Murine vascular endothelium activates and induces the generation of allogeneic CD4+25+Foxp3+ regulatory T cells.
J Immunol. 2005 Nov 15;175(10):6265-70
PMID: 16272276
-
Depletion of CD4+ T cells in major histocompatibility complex class II-deficient mice.
Science. 1991 Sep 20;253(5026):1417-20
PMID: 1910207
-
Mice lacking all conventional MHC class II genes.
Proc Natl Acad Sci U S A. 1999 Aug 31;96(18):10338-43
PMID: 10468609
-
Regulatory T cell lineage specification by the forkhead transcription factor foxp3.
Immunity. 2005 Mar;22(3):329-41
PMID: 15780990
-
Hepatic stellate cells preferentially expand allogeneic CD4+ CD25+ FoxP3+ regulatory T cells in an IL-2-dependent manner.
Transplantation. 2008 Dec 15;86(11):1492-502
PMID: 19077880
-
Self-reactive T cells selected on thymic cortical epithelium are polyclonal and are pathogenic in vivo.
J Immunol. 1999 May 1;162(9):5078-84
PMID: 10227976
-
Initiation of the adaptive immune response to Mycobacterium tuberculosis depends on antigen production in the local lymph node, not the lungs.
J Exp Med. 2008 Jan 21;205(1):105-15
PMID: 18158321
-
Cutting edge: Acute lung allograft rejection is independent of secondary lymphoid organs.
J Immunol. 2009 Apr 1;182(7):3969-73
PMID: 19299693