Amelioration of brain pathology and behavioral dysfunction in mice with lupus following treatment with a tolerogenic peptide

Arthritis Rheum. 2009 Dec;60(12):3744-54. doi: 10.1002/art.25013.

Abstract

Objective: Central nervous system (CNS) involvement in systemic lupus erythematosus (SLE) is manifested by neurologic deficits and psychiatric disorders. The aim of this study was to examine SLE-associated CNS pathology in lupus-prone (NZBxNZW)F1 (NZB/NZW) mice, and to evaluate the ameliorating effects of treatment with a tolerogenic peptide, hCDR1 (human first complementarity-determining region), on these manifestations.

Methods: Histopathologic analyses of brains from lupus-prone NZB/NZW mice treated with vehicle, hCDR1, or a control scrambled peptide were performed. The messenger RNA expression of SLE-associated cytokines and apoptosis-related molecules from the hippocampi was determined. Anxiety-like behavior was assessed by open-field tests and dark/light transfer tests, and memory deficit was assessed using a novel object recognition test.

Results: Infiltration was evident in the hippocampi of the lupus-afflicted mice, and the presence of CD3+ T cells as well as IgG and complement C3 complex deposition was observed. Furthermore, elevated levels of gliosis and loss of neuronal nuclei immunoreactivity were also observed in the hippocampi of the mice with lupus. Treatment with hCDR1 ameliorated the histopathologic changes. Treatment with hCDR1 down-regulated the high expression of interleukin-1beta (IL-1beta), IL-6, IL-10, interferon-gamma, transforming growth factor beta, and the proapoptotic molecule caspase 8 in the hippocampi of the mice with lupus, and up-regulated expression of the antiapoptotic bcl-xL gene. Diseased mice exhibited increased anxiety-like behavior and memory deficit. Treatment with hCDR1 improved these parameters, as assessed by behavior tests.

Conclusion: Treatment with hCDR1 ameliorated CNS pathology and improved the tested cognitive and mood-related behavior of the mice with lupus. Thus, hCDR1 is a novel candidate for the treatment of CNS lupus.

MeSH terms

  • Animals
  • Antigen-Antibody Complex / drug effects
  • Antigen-Antibody Complex / immunology
  • Anxiety / genetics
  • Anxiety / immunology*
  • Anxiety / metabolism
  • Apoptosis / drug effects
  • Behavior, Animal / physiology
  • CD3 Complex / metabolism
  • Complementarity Determining Regions / immunology*
  • Cytokines / genetics
  • Cytokines / metabolism
  • Disease Models, Animal
  • Female
  • Gene Expression / drug effects
  • Hippocampus / drug effects*
  • Hippocampus / metabolism
  • Hippocampus / pathology
  • Humans
  • Immunization
  • Lupus Erythematosus, Systemic / drug therapy*
  • Lupus Erythematosus, Systemic / genetics
  • Lupus Erythematosus, Systemic / immunology
  • Memory Disorders / drug therapy
  • Memory Disorders / immunology
  • Memory Disorders / pathology
  • Mice
  • Mice, Inbred NZB
  • Nervous System Diseases / drug therapy*
  • Nervous System Diseases / genetics
  • Nervous System Diseases / immunology
  • Peptide Fragments / therapeutic use*
  • RNA, Messenger / metabolism
  • T-Lymphocytes / metabolism
  • T-Lymphocytes / pathology
  • bcl-X Protein / genetics
  • bcl-X Protein / metabolism

Substances

  • Antigen-Antibody Complex
  • Bcl2l1 protein, mouse
  • CD3 Complex
  • Complementarity Determining Regions
  • Cytokines
  • Peptide Fragments
  • RNA, Messenger
  • bcl-X Protein