Apoptosis Susceptibility Prolongs the Lack of Memory B Cells in Acute Leukemic Patients After Allogeneic Hematopoietic Stem Cell Transplantation

Biol Blood Marrow Transplant. 2015 Nov;21(11):1895-906. doi: 10.1016/j.bbmt.2015.08.008. Epub 2015 Aug 10.

Abstract

Long-term survival after allogeneic hematopoietic stem cell transplantation requires intact immunosurveillance, which is hampered by lymphoid organ damage associated with conditioning therapy, graft-versus-host disease, and immunosuppression. Our study aimed to identify the mechanisms contributing to sustained low memory B cell numbers after transplantation. Peripheral B and T cell subset recovery and functional marker expression were investigated in 35 acute leukemic patients up to 1 year after transplantation. Apoptosis of B cells after CD40/TLR-9, CD40/BCR, and CD40/BCR/TLR-9-dependent stimulation and drug efflux capacity were analyzed. One half of the patients suffered from infections after day 180. All patients had strongly diminished CD27(+) memory B cells despite already normalized total B cell numbers and fully recovered CD27(-)IgD(-) memory B cells, putatively of extra-follicular origin. Circulating memory follicular helper T cells were reduced in the majority of patients as well. Naïve B cells exhibited a decreased expression of CXCR5, which mediates follicular B cell entry. Additionally, a lower HLA-DR expression was found on naïve B cells, impairing antigen presentation. Upon CD40/TLR-9-dependent activation, B cells underwent significantly increased apoptosis paralleled by an aberrant up-regulation of Fas-L on activated T cells and Fas on resting B cells. Significantly increased B cell apoptosis was also observed after CD40/BCR and CD40/BCR/TLR-9-dependent activation. Drug efflux capacity of naïve B cells was diminished in cyclosporin A-treated patients, additionally contributing to an apoptosis-prone phenotype. We conclude that B cell survival and migration and T cell communication defects are contributing candidates for an impaired germinal center formation of memory B cells after allogeneic hematopoietic stem cell transplantation. Follow-up studies should evaluate effectiveness of revaccinations on the cellular level and should address the long-term sequelae of B cell defects after transplantation.

Keywords: Allogeneic hematopoietic stem cell transplantation; B cell intrinsic and germinal center defects; Long-term memory B cell paucity.

MeSH terms

  • Adult
  • Apoptosis / immunology
  • B-Lymphocyte Subsets / immunology*
  • B-Lymphocyte Subsets / pathology
  • Biomarkers / metabolism
  • CD40 Antigens / genetics
  • CD40 Antigens / immunology
  • Case-Control Studies
  • Female
  • Gene Expression
  • HLA-DR Antigens / genetics
  • HLA-DR Antigens / immunology
  • Hematopoietic Stem Cell Transplantation*
  • Histocompatibility Testing
  • Humans
  • Immunoglobulin D / genetics
  • Immunologic Memory*
  • Leukemia, Myeloid, Acute / genetics
  • Leukemia, Myeloid, Acute / immunology*
  • Leukemia, Myeloid, Acute / pathology
  • Leukemia, Myeloid, Acute / therapy
  • Lymphocyte Count
  • Male
  • Middle Aged
  • Precursor Cell Lymphoblastic Leukemia-Lymphoma / genetics
  • Precursor Cell Lymphoblastic Leukemia-Lymphoma / immunology*
  • Precursor Cell Lymphoblastic Leukemia-Lymphoma / pathology
  • Precursor Cell Lymphoblastic Leukemia-Lymphoma / therapy
  • Primary Cell Culture
  • Receptors, Antigen, B-Cell / genetics
  • Receptors, Antigen, B-Cell / immunology
  • Receptors, CXCR5 / genetics
  • Receptors, CXCR5 / immunology
  • T-Lymphocyte Subsets / immunology*
  • T-Lymphocyte Subsets / pathology
  • Toll-Like Receptor 9 / genetics
  • Toll-Like Receptor 9 / immunology
  • Transplantation Conditioning
  • Transplantation, Homologous
  • Tumor Necrosis Factor Receptor Superfamily, Member 7 / genetics
  • Tumor Necrosis Factor Receptor Superfamily, Member 7 / immunology
  • Unrelated Donors

Substances

  • Biomarkers
  • CD40 Antigens
  • CXCR5 protein, human
  • HLA-DR Antigens
  • Immunoglobulin D
  • Receptors, Antigen, B-Cell
  • Receptors, CXCR5
  • TLR9 protein, human
  • Toll-Like Receptor 9
  • Tumor Necrosis Factor Receptor Superfamily, Member 7