Myelin protein zero is naturally processed in the B cells of monoclonal gammopathy of undetermined significance of immunoglobulin M isotype: aberrant triggering of a patient's T cells

Haematologica. 2010 Apr;95(4):627-36. doi: 10.3324/haematol.2009.015123. Epub 2009 Dec 16.

Abstract

Background: Monoclonal gammopathy of undetermined significance of immunoglobulin M isotype is a condition with clonally expanded B cells, recently suggested to have an infectious origin. This monoclonal gammopathy is frequently associated with polyneuropathy and antibodies against myelin protein zero, whereas the role of the T cells remains largely unknown. We analyzed protein zero-specific B cells, as antigen-presenting cells, and their capacity to activate T helper cells.

Design and methods: We used a well-characterized monoclonal gammopathy of undetermined significance-derived B-cell line, TJ2, expressing anti-protein zero immunoglobulin M. The ability of TJ2 cells to bind, endocytose, process, and present protein zero was investigated by receptor-clustering and immunofluorescence. The activation of protein zero-specific autologous T cells was studied by measuring interleukin-2 and interferon-gamma with flow cytometry, immunobeads, and enzyme-linked immunospot assays.

Results: Surface-receptor clustering and endocytosis of receptor-ligand (immunoglobulin M/protein zero) complexes were pronounced after exposure to protein zero. Naturally processed or synthetic protein zero peptide (194-208)-pulsed TJ2 cells significantly induced interleukin-2 secretion from autologous T cells compared to control antigen-pulsed cells (P<0.001). The numbers of interferon-gamma-producing T helper cells, including CD4(+)/CD8(+) cells, were also significantly increased (P=0.0152). Affinity-isolated naturally processed myelin peptides were potent interferon-gamma stimulators for autologous peripheral blood mononuclear cells, but not for control peripheral blood mononuclear cells.

Conclusions: We show for the first time that myelin protein zero is naturally processed in B cells from monoclonal gammopathy of undetermined significance of immunoglobulin M isotype, acting as aberrant antigen-presenting cells in activation of a patient's T helper cells. Our findings cast new light on the important role of autoreactive protein zero-specific B cells in the induction of the pathogenic T-cell responses found in nerve lesions of patients with monoclonal gammopathy of undetermined significance with peripheral neuropathy.

Publication types

  • Case Reports
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Aged
  • Antigen-Presenting Cells / immunology
  • Autoantibodies / immunology
  • B-Lymphocytes / immunology*
  • Female
  • Humans
  • Immunoglobulin M / immunology*
  • Interferon-gamma / metabolism
  • Monoclonal Gammopathy of Undetermined Significance / immunology*
  • Monoclonal Gammopathy of Undetermined Significance / pathology
  • Myelin P0 Protein / immunology
  • Myelin P0 Protein / metabolism*
  • Peripheral Nervous System Diseases / immunology*
  • Peripheral Nervous System Diseases / pathology
  • Receptors, Antigen, B-Cell / immunology
  • T-Lymphocytes / immunology*
  • T-Lymphocytes, Helper-Inducer / immunology
  • T-Lymphocytes, Helper-Inducer / metabolism

Substances

  • Autoantibodies
  • Immunoglobulin M
  • Myelin P0 Protein
  • Receptors, Antigen, B-Cell
  • Interferon-gamma