Impairment of the programmed cell death-1 pathway increases atherosclerotic lesion development and inflammation

Arterioscler Thromb Vasc Biol. 2011 May;31(5):1100-7. doi: 10.1161/ATVBAHA.111.224709. Epub 2011 Mar 10.

Abstract

Objective: Programmed cell death-1 (PD-1) is a member of the CD28 superfamily that delivers negative signals on interaction with its 2 ligands, PD-L1 and PD-L2. We studied the contribution of the PD-1 pathway to regulation of T cells that promote atherosclerotic lesion formation and inflammation.

Methods and results: We show that compared with Ldlr-/- control mice, Pd1-/-Ldlr-/- mice developed larger lesions with more abundant CD4+ and CD8+ T cells and macrophages, accompanied by higher levels of serum tumor necrosis factor-α. Iliac lymph node T cells from Pd1-/-Ldlr-/- mice proliferated more to αCD3 or oxidized low-density lipoprotein stimulation compared with controls. CD8+ T cells from Pd1-/-Ldlr-/- mice displayed more cytotoxic activity compared with controls in vivo and in vitro. Administration of a blocking anti-PD-1 antibody increased lesional inflammation in hypercholesterolemic Ldlr-/- mice with more lesional T cells and more activated T cells in paraaortic lymph nodes. The changes in lesional T-cell content when PD-1 was absent or blocked were also observed in bone marrow chimeric Ldlr-/- mice lacking PD-L1 and PD-L2 on hematopoietic cells.

Conclusions: PD-1 has an important role in downregulating proatherogenic T-cell responses, and blockade of this molecule for treatment of viral infections or cancer may increase risk of cardiovascular complications.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Antibodies, Blocking / pharmacology
  • Antigens, Surface / genetics
  • Antigens, Surface / metabolism*
  • Apoptosis
  • Apoptosis Regulatory Proteins / antagonists & inhibitors
  • Apoptosis Regulatory Proteins / deficiency
  • Apoptosis Regulatory Proteins / genetics
  • Apoptosis Regulatory Proteins / metabolism*
  • Atherosclerosis / genetics
  • Atherosclerosis / immunology
  • Atherosclerosis / metabolism*
  • Atherosclerosis / pathology
  • B7-1 Antigen / genetics
  • B7-1 Antigen / metabolism
  • B7-H1 Antigen
  • Bone Marrow Transplantation
  • CD3 Complex / metabolism
  • CD4-Positive T-Lymphocytes / immunology
  • CD4-Positive T-Lymphocytes / metabolism
  • CD8-Positive T-Lymphocytes / immunology
  • CD8-Positive T-Lymphocytes / metabolism
  • Cell Proliferation
  • Cells, Cultured
  • Disease Models, Animal
  • Genes, T-Cell Receptor
  • Genotype
  • Hypercholesterolemia / genetics
  • Hypercholesterolemia / immunology
  • Hypercholesterolemia / metabolism
  • Inflammation / genetics
  • Inflammation / immunology
  • Inflammation / metabolism*
  • Inflammation / pathology
  • Lipoproteins, LDL / metabolism
  • Lymph Nodes / immunology
  • Lymph Nodes / metabolism
  • Lymphocyte Activation* / drug effects
  • Macrophages / immunology
  • Macrophages / metabolism
  • Male
  • Membrane Glycoproteins / deficiency
  • Membrane Glycoproteins / genetics
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Peptides / deficiency
  • Peptides / genetics
  • Phenotype
  • Programmed Cell Death 1 Ligand 2 Protein
  • Programmed Cell Death 1 Receptor
  • Receptors, LDL / deficiency
  • Receptors, LDL / genetics
  • Signal Transduction
  • T-Lymphocyte Subsets / drug effects
  • T-Lymphocyte Subsets / immunology
  • T-Lymphocyte Subsets / metabolism*
  • T-Lymphocytes, Cytotoxic / immunology
  • T-Lymphocytes, Cytotoxic / metabolism
  • Time Factors
  • Tumor Necrosis Factor-alpha / blood

Substances

  • Antibodies, Blocking
  • Antigens, Surface
  • Apoptosis Regulatory Proteins
  • B7-1 Antigen
  • B7-H1 Antigen
  • CD3 Complex
  • Cd274 protein, mouse
  • Lipoproteins, LDL
  • Membrane Glycoproteins
  • Pdcd1 protein, mouse
  • Pdcd1lg2 protein, mouse
  • Peptides
  • Programmed Cell Death 1 Ligand 2 Protein
  • Programmed Cell Death 1 Receptor
  • Receptors, LDL
  • Tumor Necrosis Factor-alpha
  • oxidized low density lipoprotein