TY - JOUR
T1 - Scalable production of tissue-like vascularized liver organoids from human PSCs
AU - Harrison, Sean P
AU - Siller, Richard
AU - Tanaka, Yoshiaki
AU - Chollet, Maria Eugenia
AU - de la Morena-Barrio, María Eugenia
AU - Xiang, Yangfei
AU - Patterson, Benjamin
AU - Andersen, Elisabeth
AU - Bravo-Pérez, Carlos
AU - Kempf, Henning
AU - Åsrud, Kathrine S
AU - Lunov, Oleg
AU - Dejneka, Alexandr
AU - Mowinckel, Marie-Christine
AU - Stavik, Benedicte
AU - Sandset, Per Morten
AU - Melum, Espen
AU - Baumgarten, Saphira
AU - Bonanini, Flavio
AU - Kurek, Dorota
AU - Mathapati, Santosh
AU - Almaas, Runar
AU - Sharma, Kulbhushan
AU - Wilson, Steven R
AU - Skottvoll, Frøydis S
AU - Boger, Ida C
AU - Bogen, Inger Lise
AU - Nyman, Tuula A
AU - Wu, Jun Jie
AU - Bezrouk, Ales
AU - Cizkova, Dana
AU - Corral, Javier
AU - Mokry, Jaroslav
AU - Zweigerdt, Robert
AU - Park, In-Hyun
AU - Sullivan, Gareth J.
N1 - Funding: GJS, SB, and SPH were partly supported by the Research Council of Norway through its Centres of Excellence funding scheme (project number 262613), and financial support from UiO:Life Science (Project MORGI-20493) is gratefully acknowledged. GJS and RS were supported by the Research Council of Norway through project number 247624. This work was also supported by the Norwegian Center for Stem Cell Research and National Core Facility for Human Pluripotent Stem Cells. MEC, EA, PMS were partly supported by South-Eastern Norway Regional Health Authority (HSØ) (project number 2019071). Mass spectrometry-based proteomic analyses were performed by the Proteomics Core Facility, Department of Immunology, University of Oslo/Oslo University Hospital, which is supported by the Core Facilities program of the South-Eastern Norway Regional Health Authority. This core facility is also a member of the National Network of Advanced Proteomics Infrastructure (NAPI), which is funded by the Research Council of Norway INFRASTRUKTUR-program (project number: 295910). JJW is grateful to Rosetrees Trust for their interdisciplinary award. FB is partially funded by the Horizon 2020 research and innovation program under the Marie Skłodowska-Curie grant agreement No 812616. EM and KSÅ were supported by the Research Council of Norway through project number 275124. DC and JM were supported by Progres Q40/06.
PY - 2023/9/1
Y1 - 2023/9/1
N2 - The lack of physiological parity between 2D cell culture and in vivo culture has led to the development of more organotypic models, such as organoids. Organoid models have been developed for a number of tissues, including the liver. Current organoid protocols are characterized by a reliance on extracellular matrices (ECMs), patterning in 2D culture, costly growth factors and a lack of cellular diversity, structure, and organization. Current hepatic organoid models are generally simplistic and composed of hepatocytes or cholangiocytes, rendering them less physiologically relevant compared to native tissue. We have developed an approach that does not require 2D patterning, is ECM independent, and employs small molecules to mimic embryonic liver development that produces large quantities of liver-like organoids. Using single-cell RNA sequencing and immunofluorescence, we demonstrate a liver-like cellular repertoire, a higher order cellular complexity, presenting with vascular luminal structures, and a population of resident macrophages: Kupffer cells. The organoids exhibit key liver functions, including drug metabolism, serum protein production, urea synthesis and coagulation factor production, with preserved post-translational modifications such as N-glycosylation and functionality. The organoids can be transplanted and maintained long term in mice producing human albumin. The organoids exhibit a complex cellular repertoire reflective of the organ and have de novo vascularization and liver-like function. These characteristics are a prerequisite for many applications from cellular therapy, tissue engineering, drug toxicity assessment, and disease modeling to basic developmental biology.
AB - The lack of physiological parity between 2D cell culture and in vivo culture has led to the development of more organotypic models, such as organoids. Organoid models have been developed for a number of tissues, including the liver. Current organoid protocols are characterized by a reliance on extracellular matrices (ECMs), patterning in 2D culture, costly growth factors and a lack of cellular diversity, structure, and organization. Current hepatic organoid models are generally simplistic and composed of hepatocytes or cholangiocytes, rendering them less physiologically relevant compared to native tissue. We have developed an approach that does not require 2D patterning, is ECM independent, and employs small molecules to mimic embryonic liver development that produces large quantities of liver-like organoids. Using single-cell RNA sequencing and immunofluorescence, we demonstrate a liver-like cellular repertoire, a higher order cellular complexity, presenting with vascular luminal structures, and a population of resident macrophages: Kupffer cells. The organoids exhibit key liver functions, including drug metabolism, serum protein production, urea synthesis and coagulation factor production, with preserved post-translational modifications such as N-glycosylation and functionality. The organoids can be transplanted and maintained long term in mice producing human albumin. The organoids exhibit a complex cellular repertoire reflective of the organ and have de novo vascularization and liver-like function. These characteristics are a prerequisite for many applications from cellular therapy, tissue engineering, drug toxicity assessment, and disease modeling to basic developmental biology.
KW - Humans
KW - Animals
KW - Mice
KW - Liver
KW - Organoids
KW - Tissue engineering
KW - Hepatocytes
KW - Cells, cultured
U2 - 10.1038/s12276-023-01074-1
DO - 10.1038/s12276-023-01074-1
M3 - Article
C2 - 37653039
SN - 1226-3613
VL - 55
SP - 2005
EP - 2024
JO - Experimental & Molecular Medicine
JF - Experimental & Molecular Medicine
IS - 9
ER -