Liver sinusoidal endothelial cells promote the differentiation and survival of mouse vascularised hepatobiliary organoids

Journal article

Yap, Kiryu K., Gerrand, Yi-Wen, Dingle, Aaron M., Yeoh, George C., Morrison, Wayne A. and Mitchell, Geraldine M.. (2020). Liver sinusoidal endothelial cells promote the differentiation and survival of mouse vascularised hepatobiliary organoids. Biomaterials. 251, p. 120091. https://doi.org/10.1016/j.biomaterials.2020.120091
AuthorsYap, Kiryu K., Gerrand, Yi-Wen, Dingle, Aaron M., Yeoh, George C., Morrison, Wayne A. and Mitchell, Geraldine M.
Abstract

The structural and physiological complexity of currently available liver organoids is limited, thereby reducing their relevance for drug studies, disease modelling, and regenerative therapy. In this study we combined mouse liver progenitor cells (LPCs) with mouse liver sinusoidal endothelial cells (LSECs) to generate hepatobiliary organoids with liver-specific vasculature. Organoids consisting of 5x103 cells were created from either LPCs, or a 1:1 combination of LPC/LSECs. LPC organoids demonstrated mild hepatobiliary differentiation in vitro with minimal morphological change; in contrast LPC/LSEC organoids developed clusters of polygonal hepatocyte-like cells and biliary ducts over a 7 day period. Hepatic (albumin, CPS1, CYP3A11) and biliary (GGT1) genes were significantly upregulated in LPC/LSEC organoids compared to LPC organoids over 7 days, as was albumin secretion. LPC/LSEC organoids also had significantly higher in vitro viability compared to LPC organoids. LPC and LPC/LSEC organoids were transplanted into vascularised chambers created in Fah−/−/Rag2−/−/Il2rg−/− mice (50 LPC organoids, containing 2.5x105 LPCs, and 100 LPC/LSEC organoids, containing 2.5x105 LPCs). At 2 weeks, minimal LPCs survived in chambers with LPC organoids, but robust hepatobiliary ductular tissue was present in LPC/LSEC organoids. Morphometric analysis demonstrated a 115-fold increase in HNF4α+ cells in LPC/LSEC organoid chambers (17.26 ± 4.34 cells/mm2 vs 0.15 ± 0.15 cells/mm2, p = 0.018), and 42-fold increase in Sox9+ cells in LPC/LSEC organoid chambers (28.29 ± 6.05 cells/mm2 vs 0.67 ± 0.67 cells/mm2, p = 0.011). This study presents a novel method to develop vascularised hepatobiliary organoids, with both in vitro and in vivo results confirming that incorporating LSECs with LPCs into organoids significantly increases the differentiation of hepatobiliary tissue within organoids and their survival post-transplantation.

Keywordsliver organoids; liver progenitor cells; liver sinusoidal endothelial cells; liver disease; bio-engineering; vascularised chambers
Year2020
JournalBiomaterials
Journal citation251, p. 120091
PublisherElsevier Ltd
ISSN0142-9612
Digital Object Identifier (DOI)https://doi.org/10.1016/j.biomaterials.2020.120091
Scopus EID2-s2.0-85084341180
Research or scholarlyScholarly
Page range1-15
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License
All rights reserved
File Access Level
Controlled
Output statusPublished
Publication dates
Online05 May 2020
Publication process dates
Accepted02 May 2020
Deposited23 Jul 2021
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