B-Cell Depletion Promotes Aortic Infiltration of Immunosuppressive Cells and Is Protective of Experimental Aortic Aneurysm

Arterioscler Thromb Vasc Biol. 2016 Nov;36(11):2191-2202. doi: 10.1161/ATVBAHA.116.307559. Epub 2016 Sep 15.

Abstract

Objective: B-cell depletion therapy is widely used for treatment of cancers and autoimmune diseases. B cells are abundant in abdominal aortic aneurysms (AAA); however, it is unknown whether B-cell depletion therapy affects AAA growth. Using experimental models of murine AAA, we aim to examine the effect of B-cell depletion on AAA formation.

Approach and results: Wild-type or apolipoprotein E-knockout mice were treated with mouse monoclonal anti-CD20 or control antibodies and subjected to an elastase perfusion or angiotensin II infusion model to induce AAA, respectively. Anti-CD20 antibody treatment significantly depleted B1 and B2 cells, and strikingly suppressed AAA growth in both models. B-cell depletion resulted in lower circulating IgM levels, but did not affect the levels of IgG or cytokine/chemokine levels. Although the total number of leukocyte remained unchanged in elastase-perfused aortas after anti-CD20 antibody treatment, the number of B-cell subtypes was significantly lower. Interestingly, plasmacytoid dendritic cells expressing the immunomodulatory enzyme indole 2,3-dioxygenase were detected in the aortas of B-cell-depleted mice. In accordance with an increase in indole 2,3-dioxygenase+ plasmacytoid dendritic cells, the number of regulatory T cells was higher, whereas the expression of proinflammatory genes was lower in aortas of B-cell-depleted mice. In a coculture model, the presence of B cells significantly lowered the number of indole 2,3-dioxygenase+ plasmacytoid dendritic cells without affecting total plasmacytoid dendritic cell number.

Conclusions: The present results demonstrate that B-cell depletion protects mice from experimental AAA formation and promotes emergence of an immunosuppressive environment in aorta.

Keywords: B1 and B2 cells; abdominal aortic aneurysm; anti-CD20 treatment; plasmacytoid dendritic cells; regulatory T cell.

Publication types

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

MeSH terms

  • Angiotensin II
  • Animals
  • Antibodies / pharmacology*
  • Antigens, CD20 / immunology
  • Antigens, CD20 / metabolism
  • Aorta, Abdominal / drug effects*
  • Aorta, Abdominal / immunology
  • Aorta, Abdominal / metabolism
  • Aorta, Abdominal / pathology
  • Aortic Aneurysm, Abdominal / chemically induced
  • Aortic Aneurysm, Abdominal / immunology
  • Aortic Aneurysm, Abdominal / metabolism
  • Aortic Aneurysm, Abdominal / prevention & control*
  • Apolipoproteins E / deficiency
  • Apolipoproteins E / genetics
  • B-Lymphocytes / drug effects*
  • B-Lymphocytes / immunology
  • B-Lymphocytes / metabolism
  • Biomarkers / blood
  • Cells, Cultured
  • Cellular Microenvironment
  • Coculture Techniques
  • Cytokines / blood
  • Dendritic Cells / drug effects
  • Dendritic Cells / immunology
  • Dendritic Cells / metabolism
  • Disease Models, Animal
  • Down-Regulation
  • Genetic Predisposition to Disease
  • Immunoglobulin M / blood
  • Indoleamine-Pyrrole 2,3,-Dioxygenase / metabolism
  • Inflammation Mediators / blood
  • Lymphocyte Depletion / methods*
  • Male
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Pancreatic Elastase
  • Phenotype
  • T-Lymphocytes, Regulatory / drug effects
  • T-Lymphocytes, Regulatory / immunology
  • T-Lymphocytes, Regulatory / metabolism

Substances

  • Antibodies
  • Antigens, CD20
  • Apolipoproteins E
  • Biomarkers
  • Cytokines
  • Immunoglobulin M
  • Indoleamine-Pyrrole 2,3,-Dioxygenase
  • Inflammation Mediators
  • Angiotensin II
  • Pancreatic Elastase