Extracellular Vesicles Released from Human Umbilical Cord-Derived Mesenchymal Stromal Cells Prevent Life-Threatening Acute Graft-Versus-Host Disease in a Mouse Model of Allogeneic Hematopoietic Stem Cell Transplantation

Stem Cells Dev. 2016 Dec 15;25(24):1874-1883. doi: 10.1089/scd.2016.0107. Epub 2016 Oct 24.

Abstract

Mesenchymal stromal cells (MSCs) are attractive agents for the prophylaxis of acute graft-versus-host disease (aGVHD) after allogeneic hematopoietic stem cell transplantation (allo-HSCT). However, safety concerns remain about their clinical application. In this study, we explored whether extracellular vesicles released from human umbilical cord-derived MSCs (hUC-MSC-EVs) could prevent aGVHD in a mouse model of allo-HSCT. hUC-MSC-EVs were intravenously administered to recipient mice on days 0 and 7 after allo-HSCT, and the prophylactic effects of hUC-MSC-EVs were assessed by observing the in vivo manifestations of aGVHD, histologic changes in target organs, and recipient mouse survival. We evaluated the effects of hUC-MSC-EVs on immune cells and inflammatory cytokines by flow cytometry and ProcartaPlex™ Multiplex Immunoassays, respectively. The in vitro effects of hUC-MSC-EVs were determined by mitogen-induced proliferation assays. hUC-MSC-EVs alleviated the in vivo manifestations of aGVHD and the associated histologic changes and significantly reduced the mortality of the recipient mice. Recipients treated with hUC-MSC-EVs had significantly lower frequencies and absolute numbers of CD3+CD8+ T cells; reduced serum levels of IL-2, TNF-α, and IFN-γ; a higher ratio of CD3+CD4+ and CD3+CD8+ T cells; and higher serum levels of IL-10. An in vitro experiment demonstrated that hUC-MSC-EVs inhibited the mitogen-induced proliferation of splenocytes in a dose-dependent manner, and the cytokine changes were similar to those observed in vivo. This study indicated that hUC-MSC-EVs can prevent life-threatening aGVHD by modulating immune responses. These data provide the first evidence that hUC-MSC-EVs represent an ideal alternative in the prophylaxis of aGVHD after allo-HSCT.

Keywords: exosomes; extracellular vesicles; graft-versus-host disease; hematopoietic stem cell transplantation; mesenchymal stromal cells; microvesicles.

MeSH terms

  • Acute Disease
  • Animals
  • Antigens, CD / metabolism
  • Cytokines / metabolism
  • Disease Models, Animal
  • Extracellular Vesicles / metabolism*
  • Flow Cytometry
  • Graft vs Host Disease / etiology
  • Graft vs Host Disease / pathology
  • Graft vs Host Disease / prevention & control*
  • Graft vs Host Disease / therapy*
  • Hematopoietic Stem Cell Transplantation / adverse effects*
  • Humans
  • Immunosuppression Therapy
  • Inflammation Mediators / metabolism
  • Lymphocyte Count
  • Male
  • Mesenchymal Stem Cells / metabolism*
  • Mice, Inbred BALB C
  • Mice, Inbred C57BL
  • T-Lymphocytes / cytology
  • Transplantation, Homologous / adverse effects
  • Umbilical Cord / cytology*

Substances

  • Antigens, CD
  • Cytokines
  • Inflammation Mediators