Graft dysfunction in chronic antibody-mediated rejection correlates with B-cell-dependent indirect antidonor alloresponses and autocrine regulation of interferon-γ production by Th1 cells

Kidney Int. 2017 Feb;91(2):477-492. doi: 10.1016/j.kint.2016.10.009. Epub 2016 Dec 15.

Abstract

Chronic antibody-mediated rejection, a common cause of renal transplant failure, has a variable clinical phenotype. Understanding why some with chronic antibody-mediated rejection progress slowly may help develop more effective therapies. B lymphocytes act as antigen-presenting cells for in vitro indirect antidonor interferon-γ production in chronic antibody-mediated rejection, but many patients retain the ability to regulate these responses. Here we test whether particular patterns of T and B cell antidonor response associate with the variability of graft dysfunction in chronic antibody-mediated rejection. Our results confirm that dynamic changes in indirect antidonor CD4+ T-cell responses correlate with changes in estimated glomerular filtration rates, independent of other factors. Graft dysfunction progressed rapidly in patients who developed unregulated B-cell-driven interferon-γ production. However, conversion to a regulated or nonreactive pattern, which could be achieved by optimization of immunosuppression, associated with stabilization of graft function. Functional regulation by B cells appeared to activate an interleukin-10 autocrine pathway in CD4+ T cells that, in turn, impacted on antigen-specific responses. Thus, our data significantly enhance the understanding of graft dysfunction associated with chronic antibody-mediated rejection and provide the foundation for strategies to prolong renal allograft survival, based on regulation of interferon-γ production.

Keywords: B lymphocyte; ELISPOT; chronic allograft nephropathy; indirect alloresponses; interferon-γ.

Publication types

  • Observational Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Area Under Curve
  • Autocrine Communication* / drug effects
  • B-Lymphocytes / drug effects
  • B-Lymphocytes / immunology*
  • B-Lymphocytes / metabolism
  • Biopsy
  • Chi-Square Distribution
  • Chronic Disease
  • Disease Progression
  • Enzyme-Linked Immunospot Assay
  • Female
  • Glomerular Filtration Rate
  • Graft Rejection / blood
  • Graft Rejection / drug therapy
  • Graft Rejection / immunology*
  • Graft Rejection / physiopathology
  • Graft Survival
  • HLA Antigens / immunology*
  • Histocompatibility
  • Humans
  • Immunosuppressive Agents / therapeutic use
  • Interferon-gamma / immunology*
  • Interferon-gamma / metabolism
  • Interferon-gamma Release Tests
  • Interleukin-10 / immunology
  • Interleukin-10 / metabolism
  • Isoantibodies / blood*
  • Kidney / drug effects
  • Kidney / immunology*
  • Kidney / metabolism
  • Kidney / physiopathology
  • Kidney Transplantation / adverse effects*
  • Linear Models
  • Logistic Models
  • Male
  • Middle Aged
  • Multivariate Analysis
  • Predictive Value of Tests
  • ROC Curve
  • Risk Factors
  • Signal Transduction
  • Th1 Cells / drug effects
  • Th1 Cells / immunology*
  • Th1 Cells / metabolism
  • Time Factors
  • Treatment Outcome

Substances

  • HLA Antigens
  • IFNG protein, human
  • IL10 protein, human
  • Immunosuppressive Agents
  • Isoantibodies
  • Interleukin-10
  • Interferon-gamma