Targeting PI3Kδ function for amelioration of murine chronic graft-versus-host disease

Am J Transplant. 2019 Jun;19(6):1820-1830. doi: 10.1111/ajt.15305. Epub 2019 Mar 19.

Abstract

Chronic graft-versus-host disease (cGVHD) is a leading cause of morbidity and mortality following allotransplant. Activated donor effector T cells can differentiate into pathogenic T helper (Th)-17 cells and germinal center (GC)-promoting T follicular helper (Tfh) cells, resulting in cGVHD. Phosphoinositide-3-kinase-δ (PI3Kδ), a lipid kinase, is critical for activated T cell survival, proliferation, differentiation, and metabolism. We demonstrate PI3Kδ activity in donor T cells that become Tfh cells is required for cGVHD in a nonsclerodermatous multiorgan system disease model that includes bronchiolitis obliterans (BO), dependent upon GC B cells, Tfhs, and counterbalanced by T follicular regulatory cells, each requiring PI3Kδ signaling for function and survival. Although B cells rely on PI3Kδ pathway signaling and GC formation is disrupted resulting in a substantial decrease in Ig production, PI3Kδ kinase-dead mutant donor bone marrow-derived GC B cells still supported BO cGVHD generation. A PI3Kδ-specific inhibitor, compound GS-649443, that has superior potency to idelalisib while maintaining selectivity, reduced cGVHD in mice with active disease. In a Th1-dependent and Th17-associated scleroderma model, GS-649443 effectively treated mice with active cGVHD. These data provide a foundation for clinical trials of US Food and Drug Administration (FDA)-approved PI3Kδ inhibitors for cGVHD therapy in patients.

Keywords: basic (laboratory) research/science; graft-versus-host disease (GVHD); immunobiology; immunosuppressant - other.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • B-Lymphocytes / immunology
  • Bone Marrow Transplantation / adverse effects
  • Bronchiolitis Obliterans / drug therapy
  • Bronchiolitis Obliterans / enzymology
  • Bronchiolitis Obliterans / etiology
  • Chronic Disease
  • Class I Phosphatidylinositol 3-Kinases / antagonists & inhibitors*
  • Class I Phosphatidylinositol 3-Kinases / deficiency
  • Class I Phosphatidylinositol 3-Kinases / genetics
  • Disease Models, Animal
  • Graft vs Host Disease / drug therapy*
  • Graft vs Host Disease / enzymology*
  • Graft vs Host Disease / immunology
  • Humans
  • Mice
  • Mice, Inbred BALB C
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Mice, Mutant Strains
  • Phosphoinositide-3 Kinase Inhibitors / pharmacology*
  • Scleroderma, Localized / drug therapy
  • Scleroderma, Localized / enzymology
  • Scleroderma, Localized / etiology
  • T-Lymphocytes, Helper-Inducer / immunology

Substances

  • Phosphoinositide-3 Kinase Inhibitors
  • Class I Phosphatidylinositol 3-Kinases
  • Pik3cd protein, mouse