Basic Study
Copyright ©The Author(s) 2019. Published by Baishideng Publishing Group Inc. All rights reserved.
World J Stem Cells. Sep 26, 2019; 11(9): 705-721
Published online Sep 26, 2019. doi: 10.4252/wjsc.v11.i9.705
Enhanced hepatic differentiation in the subpopulation of human amniotic stem cells under 3D multicellular microenvironment
Kinji Furuya, Yun-Wen Zheng, Daisuke Sako, Kenichi Iwasaki, Dong-Xu Zheng, Jian-Yun Ge, Li-Ping Liu, Tomoaki Furuta, Kazunori Akimoto, Hiroya Yagi, Hiromi Hamada, Hiroko Isoda, Tatsuya Oda, Nobuhiro Ohkohchi
Kinji Furuya, Yun-Wen Zheng, Daisuke Sako, Kenichi Iwasaki, Dong-Xu Zheng, Jian-Yun Ge, Li-Ping Liu, Tomoaki Furuta, Tatsuya Oda, Nobuhiro Ohkohchi, Department of Gastrointestinal and Hepato-Biliary-Pancreatic Surgery, Faculty of Medicine, University of Tsukuba, Tsukuba, Ibaraki 305-8575, Japan
Yun-Wen Zheng, Li-Ping Liu, Institute of Regenerative Medicine and Affiliated Hospital, Jiangsu University, Zhenjiang 212001, Jiangsu Province, China
Yun-Wen Zheng, Department of Regenerative Medicine, School of Medicine, Yokohama City University, Yokohama 236-0004, Japan
Daisuke Sako, Kazunori Akimoto, Department of Medicinal and Life Sciences, Faculty of Pharmaceutical Sciences, Tokyo University of Science, Noda 278-8510, Japan
Hiroya Yagi, Hiromi Hamada, Department of Obstetrics and Gynecology, Faculty of Medicine, University of Tsukuba, Tsukuba 305-8575, Japan
Hiroko Isoda, Faculty of Life and Environmental Sciences, University of Tsukuba, Tsukuba 305-8572, Japan
Author contributions: Furuya K, Sako D, Iwasaki K, Ge JY, Liu LP and Furuta T performed the experiments; Furuya K, Sako D and Iwasaki K analyzed the data; Zheng DX performed bioinformatics; Akimoto K, Yagi H, Hamada H, Isoda H supplied experimental materials and resources; Ohkohchi N and Zheng YW conceived the study; Furuya K drafted the manuscript; Zheng YW and Oda T contributed to discuss and review the final manuscript; all the authors approved the final manuscript; Furuya K, Zheng YW and Sako D contributed equally to this work.
Supported by National Natural Science Foundation of China, No. 81770621; Ministry of Education, Culture, Sports, Science, and Technology of Japan, KAKENHI, No. 16K15604, No. 18H02866; Japan Science and Technology Agency-Japan International Cooperation Agency's (JST-JICA) Science and Technology Research Partnership for Sustainable Development (SATREPS) Project.
Institutional review board statement: All specimens and cells from the patients were obtained after their informed consent and ethical permission was obtained for participation in the study.
Conflict-of-interest statement: The authors report no relevant conflicts of interest.
Data sharing statement: Transcriptome datasets of primary amniotic epithelial cells from the Sequence Read Archive (SRA) of the NCBI are available in the website. SRA number is listed in Table 2. Participants gave informed consent for publication.
Open-Access: This article is an open-access article which was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: http://creativecommons.org/licenses/by-nc/4.0/
Corresponding author: Yun-Wen Zheng, PhD, Associate Professor, Department of Gastrointestinal and Hepato-Biliary-Pancreatic Surgery, University of Tsukuba Faculty of Medicine, Tennodai 1-1-1, Tsukuba, Ibaraki 305-8575, Japan. ywzheng@md.tsukuba.ac.jp
Telephone: +81-29-8533221 Fax: +81-29-8533222
Received: February 26, 2019
Peer-review started: February 27, 2019
Revised: August 6, 2019
Accepted: August 27, 2019
Article in press: August 27, 2019
Published online: September 26, 2019
Processing time: 211 Days and 2.6 Hours
Abstract
BACKGROUND

To solve the problem of liver transplantation donor insufficiency, an alternative cell transplantation therapy was investigated. We focused on amniotic epithelial cells (AECs) as a cell source because, unlike induced pluripotent stem cells, they are cost-effective and non-tumorigenic. The utilization of AECs in regenerative medicine, however, is in its infancy. A general profile for AECs has not been comprehensively analyzed. Moreover, no hepatic differentiation protocol for AECs has yet been established. To this end, we independently compiled human AEC libraries, purified amniotic stem cells (ASCs), and co-cultured them with mesenchymal stem cells (MSCs) and human umbilical vein endothelial cell (HUVECs) in a 3D system which induces functional hepatic organoids.

AIM

To characterize AECs and generate functional hepatic organoids from ASCs and other somatic stem cells

METHODS

AECs, MSCs, and HUVECs were isolated from the placentae and umbilical cords of cesarean section patients. Amnion and primary AEC stemness characteristics and heterogeneity were analyzed by immunocytochemistry, Alkaline phosphatase (AP) staining, and flow cytometry. An adherent AEC subpopulation was selected and evaluated for ASC purification quality by a colony formation assay. AEC transcriptomes were compared with those for other hepatocytes cell sources by bioinformatics. The 2D and 3D culture were compared by relative gene expression using several differentiation protocols. ASCs, MSCs, and HUVECs were combined in a 3D co-culture system to generate hepatic organoids whose structure was compared with a 3D AEC sphere and whose function was elucidated by immunofluorescence imaging, periodic acid Schiff, and an indocyanine green (ICG) test.

RESULTS

AECs have certain stemness markers such as EPCAM, SSEA4, and E-cadherin. One AEC subpopulation was also either positive for AP staining or expressed the TRA-1-60 and TRA-1-81 stemness markers. Moreover, it could form colonies and its frequency was enhanced ten-fold in the adherent subpopulation after selective primary passage. Bioinformatics analysis of ribose nucleic acid sequencing revealed that the total AEC gene expression was distant from those of pluripotent stem cells and hepatocytes but some gene expression overlapped among these cells. TJP1, associated with epidermal growth factor receptor, and MET, associated with hepatocyte growth factor receptor, were upregulated and may be important for hepatic differentiation. In conventional flat culture, the cells turned unviable and did not readily differentiate into hepatocytes. In 3D culture, however, hepatic gene expression of the AEC sphere was elevated even under a two-step differentiation protocol. Furthermore, the organoids derived from the MSC and HUVEC co-culture showed 3D structure with polarity, hepatic-like glycogen storage, and ICG absorption/elimination.

CONCLUSION

Human amniotic epithelial cells are heterogeneous and certain subpopulations have high stemness. Under a 3D co-culture system, functional hepatic organoids were generated in a multicellular microenvironment.

Keywords: 3D micropattern; Amniotic epithelial cells; Amniotic stem cells; Hepatic differentiation; Heterogeneity; Human placental tissue; Human umbilical vein endothelial cells; Mesenchymal stem cells; Multicellular microenvironment; Organoid

Core tip: Amniotic stem cells were exploited as a cell source alternative to liver transplantation therapy instead of induced pluripotent stem cells. However, they presented with low hepatic function efficiency. We used 3D co-culture and a combination of supportive somatic stem cells to simulate an in vivo microenvironment. Our selected subpopulation of adherent amniotic stem cells self-organized ex vivo and generated functional organoids. Cell selection methods and bioinformatics may help refine the differentiation protocol.