Oral administration of recombinant Mycobacterium smegmatis expressing a tripeptide construct derived from endogenous and microbial antigens prevents atherosclerosis in ApoE(-/-) mice

Cardiovasc Ther. 2016 Oct;34(5):314-24. doi: 10.1111/1755-5922.12201.

Abstract

Introduction: Immunotherapy by inducing oral tolerance to atherogenic self-antigens is gaining importance as an alternative treatment modality for atherosclerosis. The use of live bacterial vectors to express the recombinant antigen in vivo will obviate the need for large-scale purification of recombinant protein and may also augment the efficacy of oral tolerance induction.

Aim: The objective of the study was to explore the use of recombinant Mycobacterium smegmatis as a live vector for oral delivery of antigens to induce immune tolerance.

Method and results: We developed a M. smegmatis vector to secrete a recombinant tripeptide construct (AHC; peptides from Apolipoprotein B, Heat-shock protein 60 and Chlamydia pneumoniae outer membrane protein) expressed in a dendroaspin protein scaffold in pJH154 background. Immune response and oral tolerance to the cloned peptides were studied in C57/BL6 mice. The efficacy of this live vaccine to control atherosclerosis was studied in ApoE(-/-) knockout mice in C57/BL6 background. Oral administration of M. smegmatis secreting the cloned AHC antigen was found to induce tolerance to cloned protein and reduce the development of atherosclerosis by 24.0% compared to control. Protection against atherosclerosis was associated with increase in expression of regulatory T cell-associated markers including CTLA4 (1.8-fold), Foxp3 (2.6-fold), TGF-β (2.8-fold), IL10 (2.9-fold), and reduction in lipids, macrophage infiltration, and expression of inflammatory mediators in aorta.

Conclusions: Our results suggest that M. smegmatis can be developed as an oral carrier of recombinant proteins to treat inflammatory autoimmune diseases.

Keywords: Apolipoprotein; Atherosclerosis; Autoimmune diseases; Heat-shock proteins; Immune tolerance; Live vaccine; Mycobacterium smegmatis; Regulatory T cells.

MeSH terms

  • Administration, Oral
  • Animals
  • Antigens / administration & dosage*
  • Antigens / genetics
  • Antigens / immunology
  • Antigens / metabolism
  • Aortic Diseases / genetics
  • Aortic Diseases / immunology
  • Aortic Diseases / metabolism
  • Aortic Diseases / prevention & control*
  • Apolipoproteins E / deficiency*
  • Apolipoproteins E / genetics
  • Atherosclerosis / genetics
  • Atherosclerosis / immunology
  • Atherosclerosis / metabolism
  • Atherosclerosis / prevention & control*
  • CTLA-4 Antigen / immunology
  • CTLA-4 Antigen / metabolism
  • Disease Models, Animal
  • Female
  • Forkhead Transcription Factors / immunology
  • Forkhead Transcription Factors / metabolism
  • Genetic Predisposition to Disease
  • Genetic Vectors*
  • Immune Tolerance
  • Immunization
  • Immunotherapy / methods*
  • Inflammation Mediators / immunology
  • Inflammation Mediators / metabolism
  • Interleukin-10 / immunology
  • Interleukin-10 / metabolism
  • Lipid Metabolism
  • Macrophages / immunology
  • Macrophages / metabolism
  • Male
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Mycobacterium smegmatis / genetics*
  • Mycobacterium smegmatis / immunology
  • Mycobacterium smegmatis / metabolism
  • Oligopeptides / administration & dosage*
  • Oligopeptides / genetics
  • Oligopeptides / immunology
  • Oligopeptides / metabolism
  • Phenotype
  • T-Lymphocytes, Regulatory / immunology
  • T-Lymphocytes, Regulatory / metabolism
  • Time Factors
  • Transforming Growth Factor beta / immunology
  • Transforming Growth Factor beta / metabolism
  • Vaccines, Synthetic / administration & dosage

Substances

  • Antigens
  • Apolipoproteins E
  • CTLA-4 Antigen
  • Ctla4 protein, mouse
  • Forkhead Transcription Factors
  • Foxp3 protein, mouse
  • IL10 protein, mouse
  • Inflammation Mediators
  • Oligopeptides
  • Transforming Growth Factor beta
  • Vaccines, Synthetic
  • Interleukin-10