A novel prevascularized tissue-engineered chamber as a site for allogeneic and xenogeneic islet transplantation to establish a bioartificial pancreas

PLoS One. 2020 Dec 3;15(12):e0234670. doi: 10.1371/journal.pone.0234670. eCollection 2020.

Abstract

Although sites for clinical or experimental islet transplantation are well established, pancreatic islet survival and function in these locations remain unsatisfactory. A possible factor that might account for this outcome is local hypoxia caused by the limited blood supply. Here, we modified a prevascularized tissue-engineered chamber (TEC) that facilitated the viability and function of the seeded islets in vivo by providing a microvascular network prior to transplantation. TECs were created, filled with Growth Factor-Matrigel™ (Matrigel™) and then implanted into the groins of mice with streptozotocin-induced diabetes. The degree of microvascularization in each TECs was analyzed by histology, real-time PCR, and Western blotting. Three hundred syngeneic islets were seeded into each chamber on days 0, 14, and 28 post-chamber implantation, and 300, 200, or 100 syngeneic islets were seeded into additional chambers on day 28 post-implantation, respectively. Furthermore, allogeneic or xenogeneic islet transplantation is a potential solution for organ shortage. The feasibility of TECs as transplantation sites for islet allografts or xenografts and treatment with anti-CD45RB and/or anti-CD40L (MR-1) was therefore explored. A highly developed microvascularized network was established in each TEC on day 28 post-implantation. Normalization of blood glucose levels in diabetic mice was negatively correlated with the duration of prevascularization and the number of seeded syngeneic islets. Combined treatment with anti-CD45RB and MR-1 resulted in long-term survival of the grafts following allotransplantation (5/5, 100%) and xenotransplantation (16/20, 80%). Flow cytometry demonstrated that the frequency of CD4+Foxp3-Treg and CD4+IL-4+-Th2 cells increased significantly after tolerogenic xenograft transplantation, while the number of CD4+IFN-γ-Th1 cells decreased. These findings demonstrate that highly developed microvascularized constructs can facilitate the survival of transplanted islets in a TECs, implying its potential application as artificial pancreas in the future.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Blood Glucose / immunology
  • CD4-Positive T-Lymphocytes / immunology
  • Glucose Tolerance Test / methods
  • Graft Survival / immunology
  • Interferon-gamma / immunology
  • Islets of Langerhans / immunology
  • Islets of Langerhans / surgery*
  • Islets of Langerhans Transplantation / methods*
  • Male
  • Mice
  • Mice, Inbred BALB C
  • Mice, Inbred C57BL
  • Rats
  • Rats, Sprague-Dawley
  • T-Lymphocytes, Regulatory / immunology
  • Th1 Cells / immunology
  • Tissue Engineering / methods*
  • Transplantation Tolerance / immunology
  • Transplantation, Heterologous / methods*
  • Transplantation, Homologous / methods

Substances

  • Blood Glucose
  • Interferon-gamma

Grants and funding

This study was supported by grants from the National Natural Science Foundation of China (nos. 81172832 and 81771723), Sichuan Youth Science and Technology Foundation (no. 2013JQ0020), and Special Program for Sichuan Youth Science and Technology Innovation (no. 2014TD0010).