Abstract
The inhibitory receptor programmed death 1 (PD-1) is upregulated on antigen-specific CD8+ T cells during persistent viral infections. Interaction with PD-1 ligand 1 (PD-L1) contributes to functional exhaustion of responding T cells and may limit immunopathology during infection. PD-L1 is expressed on both hematopoietic and nonhematopoietic cells in tissues. However, the exact roles of PD-L1 on hematopoietic versus nonhematopoietic cells in modulating immune responses are unclear. Here we used bone marrow chimeric mice to examine the effects of PD-L1 deficiency in hematopoietic or nonhematopoietic cells during lymphocytic choriomeningitis virus clone 13 (LCMV CL-13) infection. We found that PD-L1 expression on hematopoietic cells inhibited CD8+ T cell numbers and function after LCMV CL-13 infection. In contrast, PD-L1 expression on nonhematopoietic cells limited viral clearance and immunopathology in infected tissues. Together, these data demonstrate that there are distinct roles for PD-L1 on hematopoietic and nonhematopoietic cells in regulating CD8+ T cell responses and viral clearance during chronic viral infection.
MeSH Terms
Animals
Bone Marrow/immunology,pathology,virology
Chronic Disease
Female
Ligands
Lymphocyte Count
Lymphocytic Choriomeningitis/immunology,pathology,virology
Mice
Mice, Inbred C57BL
Mice, Knockout
T-Lymphocytes/metabolism,virology
Virus Diseases/immunology,pathology,virology
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Mueller Scott N
Emory Vaccine Center and Department of Microbiology and Immunology, Emory University School of Medicine, Atlanta, Georgia 30322, USA. smue@unimelb.edu.au
Vanguri Vijay K
Ha Sang-Jun
West Erin E
Keir Mary E
Glickman Jonathan N
Sharpe Arlene H
Ahmed Rafi
References (27)
27 references, click to expand
-
Restoring function in exhausted CD8 T cells during chronic viral infection.
Nature. 2006 Feb 9;439(7077):682-7
PMID: 16382236
-
The role of regulatory T cells in chronic and acute viral infections.
Clin Infect Dis. 2008 Apr 1;46(7):1046-52
PMID: 18444822
-
Selective expansion of a subset of exhausted CD8 T cells by alphaPD-L1 blockade.
Proc Natl Acad Sci U S A. 2008 Sep 30;105(39):15016-21
PMID: 18809920
-
Tissue expression of PD-L1 mediates peripheral T cell tolerance.
J Exp Med. 2006 Apr 17;203(4):883-95
PMID: 16606670
-
Viral targeting of fibroblastic reticular cells contributes to immunosuppression and persistence during chronic infection.
Proc Natl Acad Sci U S A. 2007 Sep 25;104(39):15430-5
PMID: 17878315
-
Viral immune evasion due to persistence of activated T cells without effector function.
J Exp Med. 1998 Dec 21;188(12):2205-13
PMID: 9858507
-
PD-1 is a regulator of virus-specific CD8+ T cell survival in HIV infection.
J Exp Med. 2006 Oct 2;203(10):2281-92
PMID: 16954372
-
Virus-induced transient bone marrow aplasia: major role of interferon-alpha/beta during acute infection with the noncytopathic lymphocytic choriomeningitis virus.
J Exp Med. 1997 Feb 3;185(3):517-30
PMID: 9053452
-
PD-1 expression on HIV-specific T cells is associated with T-cell exhaustion and disease progression.
Nature. 2006 Sep 21;443(7109):350-4
PMID: 16921384
-
Interaction between B7-H1 and PD-1 determines initiation and reversal of T-cell anergy.
Blood. 2007 Jul 1;110(1):180-5
PMID: 17289811
-
Immunosuppression and resultant viral persistence by specific viral targeting of dendritic cells.
J Exp Med. 2000 Nov 6;192(9):1249-60
PMID: 11067874
-
PD-L1 regulates the development, maintenance, and function of induced regulatory T cells.
J Exp Med. 2009 Dec 21;206(13):3015-29
PMID: 20008522
-
Counting antigen-specific CD8 T cells: a reevaluation of bystander activation during viral infection.
Immunity. 1998 Feb;8(2):177-87
PMID: 9491999
-
PD-1 inhibits antiviral immunity at the effector phase in the liver.
J Exp Med. 2003 Jul 7;198(1):39-50
PMID: 12847136
-
Upregulation of PD-1 expression on HIV-specific CD8+ T cells leads to reversible immune dysfunction.
Nat Med. 2006 Oct;12(10):1198-202
PMID: 16917489
-
Programmed death-1 ligand 1 interacts specifically with the B7-1 costimulatory molecule to inhibit T cell responses.
Immunity. 2007 Jul;27(1):111-22
PMID: 17629517
-
Aplastic anemia rescued by exhaustion of cytokine-secreting CD8+ T cells in persistent infection with lymphocytic choriomeningitis virus.
J Exp Med. 1998 Jun 1;187(11):1903-20
PMID: 9607930
-
Viral persistence alters CD8 T-cell immunodominance and tissue distribution and results in distinct stages of functional impairment.
J Virol. 2003 Apr;77(8):4911-27
PMID: 12663797
-
Chronic hepatitis. An update on terminology and reporting.
Am J Surg Pathol. 1995 Dec;19(12):1409-17
PMID: 7503362
-
Induction and exhaustion of lymphocytic choriomeningitis virus-specific cytotoxic T lymphocytes visualized using soluble tetrameric major histocompatibility complex class I-peptide complexes.
J Exp Med. 1998 May 4;187(9):1383-93
PMID: 9565631
-
PD-L1-deficient mice show that PD-L1 on T cells, antigen-presenting cells, and host tissues negatively regulates T cells.
Proc Natl Acad Sci U S A. 2004 Jul 20;101(29):10691-6
PMID: 15249675
-
Resting dendritic cells induce peripheral CD8+ T cell tolerance through PD-1 and CTLA-4.
Nat Immunol. 2005 Mar;6(3):280-6
PMID: 15685176
-
CD8 T cell dysfunction during chronic viral infection.
Curr Opin Immunol. 2007 Aug;19(4):408-15
PMID: 17656078
-
The function of programmed cell death 1 and its ligands in regulating autoimmunity and infection.
Nat Immunol. 2007 Mar;8(3):239-45
PMID: 17304234
-
Selection of genetic variants of lymphocytic choriomeningitis virus in spleens of persistently infected mice. Role in suppression of cytotoxic T lymphocyte response and viral persistence.
J Exp Med. 1984 Aug 1;160(2):521-40
PMID: 6332167
-
PD-L1 negatively regulates CD4+CD25+Foxp3+ Tregs by limiting STAT-5 phosphorylation in patients chronically infected with HCV.
J Clin Invest. 2009 Mar;119(3):551-64
PMID: 19229109
-
High antigen levels are the cause of T cell exhaustion during chronic viral infection.
Proc Natl Acad Sci U S A. 2009 May 26;106(21):8623-8
PMID: 19433785