Blockade of Tim-1 and Tim-4 Enhances Atherosclerosis in Low-Density Lipoprotein Receptor-Deficient Mice

Arterioscler Thromb Vasc Biol. 2016 Mar;36(3):456-65. doi: 10.1161/ATVBAHA.115.306860. Epub 2016 Jan 28.

Abstract

Objective: T cell immunoglobulin and mucin domain (Tim) proteins are expressed by numerous immune cells, recognize phosphatidylserine on apoptotic cells, and function as costimulators or coinhibitors. Tim-1 is expressed by activated T cells but is also found on dendritic cells and B cells. Tim-4, present on macrophages and dendritic cells, plays a critical role in apoptotic cell clearance, regulates the number of phosphatidylserine-expressing activated T cells, and is genetically associated with low low-density lipoprotein and triglyceride levels. Because these functions of Tim-1 and Tim-4 could affect atherosclerosis, their modulation has potential therapeutic value in cardiovascular disease.

Approach and results: ldlr(-/-) mice were fed a high-fat diet for 4 weeks while being treated with control (rat immunoglobulin G1) or anti-Tim-1 (3D10) or -Tim-4 (21H12) monoclonal antibodies that block phosphatidylserine recognition and phagocytosis. Both anti-Tim-1 and anti-Tim-4 treatments enhanced atherosclerosis by 45% compared with controls by impairment of efferocytosis and increasing aortic CD4(+)T cells. Consistently, anti-Tim-4-treated mice showed increased percentages of activated T cells and late apoptotic cells in the circulation. Moreover, in vitro blockade of Tim-4 inhibited efferocytosis of oxidized low-density lipoprotein-induced apoptotic macrophages. Although anti-Tim-4 treatment increased T helper cell (Th)1 and Th2 responses, anti-Tim-1 induced Th2 responses but dramatically reduced the percentage of regulatory T cells. Finally, combined blockade of Tim-1 and Tim-4 increased atherosclerotic lesion size by 59%.

Conclusions: Blockade of Tim-4 aggravates atherosclerosis likely by prevention of phagocytosis of phosphatidylserine-expressing apoptotic cells and activated T cells by Tim-4-expressing cells, whereas Tim-1-associated effects on atherosclerosis are related to changes in Th1/Th2 balance and reduced circulating regulatory T cells.

Keywords: T cells; Tim; apoptosis; atherosclerosis; inflammation; macrophage.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antibodies, Monoclonal / toxicity*
  • Aortic Diseases / chemically induced*
  • Aortic Diseases / genetics
  • Aortic Diseases / immunology
  • Aortic Diseases / metabolism
  • Aortic Diseases / pathology
  • Apoptosis / drug effects
  • Atherosclerosis / chemically induced*
  • Atherosclerosis / genetics
  • Atherosclerosis / immunology
  • Atherosclerosis / metabolism
  • Atherosclerosis / pathology
  • CD4-Positive T-Lymphocytes / drug effects*
  • CD4-Positive T-Lymphocytes / immunology
  • CD4-Positive T-Lymphocytes / pathology
  • Cell Proliferation / drug effects
  • Cells, Cultured
  • Coculture Techniques
  • Diet, High-Fat
  • Disease Models, Animal
  • Female
  • Hepatitis A Virus Cellular Receptor 1
  • Lipoproteins, LDL / metabolism
  • Lymphocyte Activation / drug effects
  • Macrophages / drug effects*
  • Macrophages / immunology
  • Macrophages / pathology
  • Male
  • Membrane Proteins / antagonists & inhibitors*
  • Membrane Proteins / immunology
  • Membrane Proteins / metabolism
  • Mice, Knockout
  • Phagocytosis / drug effects
  • Plaque, Atherosclerotic
  • Receptors, LDL / deficiency*
  • Receptors, LDL / genetics
  • Signal Transduction / drug effects
  • T-Lymphocytes, Regulatory / drug effects
  • T-Lymphocytes, Regulatory / immunology
  • Th1 Cells / drug effects
  • Th1 Cells / immunology
  • Th2 Cells / drug effects
  • Th2 Cells / immunology

Substances

  • Antibodies, Monoclonal
  • Havcr1 protein, mouse
  • Hepatitis A Virus Cellular Receptor 1
  • Lipoproteins, LDL
  • Membrane Proteins
  • Receptors, LDL
  • TIM-4 protein, mouse
  • oxidized low density lipoprotein