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Stem Cells International
Volume 2019, Article ID 3975689, 13 pages
https://doi.org/10.1155/2019/3975689
Research Article

Development of Bifunctional Three-Dimensional Cysts from Chemically Induced Liver Progenitors

1Department of Surgery, Nagasaki University Graduate School of Biomedical Sciences, 1-7-1 Sakamoto, Nagasaki 852-8501, Japan
2Department of Hepato-Pancreato-Biliary Surgery, Guangzhou First People’s Hospital, School of Medicine, South China University of Technology, Guangzhou 510180, China
3Department of Chemical Engineering, Faculty of Engineering, Graduate School, Kyushu University, 744 Motooka, Nishi-ku, Fukuoka 819-0395, Japan
4Division of Molecular and Cellular Medicine, National Cancer Center Research Institute, 5-1-1 Tsukiji, Chuo-ku, Tokyo 104-0045, Japan

Correspondence should be addressed to Yusuke Sakai; moc.liamg@gneoib.iakas.y and Susumu Eguchi; pj.ca.u-ikasagan@ihcugeus

Received 7 June 2019; Revised 20 July 2019; Accepted 30 July 2019; Published 3 September 2019

Academic Editor: Francisco J. Rodríguez-Lozano

Copyright © 2019 Yu Huang et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. D. Yimlamai, C. Christodoulou, G. G. Galli et al., “Hippo pathway activity influences liver cell fate,” Cell, vol. 157, no. 6, pp. 1324–1338, 2014. View at Publisher · View at Google Scholar · View at Scopus
  2. K. Yanger, Y. Zong, L. R. Maggs et al., “Robust cellular reprogramming occurs spontaneously during liver regeneration,” Genes & Development, vol. 27, no. 7, pp. 719–724, 2013. View at Publisher · View at Google Scholar · View at Scopus
  3. B. D. Tarlow, C. Pelz, W. E. Naugler et al., “Bipotential adult liver progenitors are derived from chronically injured mature hepatocytes,” Cell Stem Cell, vol. 15, no. 5, pp. 605–618, 2014. View at Publisher · View at Google Scholar · View at Scopus
  4. N. Tanimizu, Y. Nishikawa, N. Ichinohe, H. Akiyama, and T. Mitaka, “Sry HMG box protein 9-positive (Sox9+) epithelial cell adhesion molecule-negative (EpCAM-) biphenotypic cells derived from hepatocytes are involved in mouse liver regeneration,” Journal of Biological Chemistry, vol. 289, no. 11, pp. 7589–7598, 2014. View at Publisher · View at Google Scholar · View at Scopus
  5. S. Masuda, J. Wu, T. Hishida, G. N. Pandian, H. Sugiyama, and J. C. Izpisua Belmonte, “Chemically induced pluripotent stem cells (CiPSCs): a transgene-free approach,” Journal of Molecular Cell Biology, vol. 5, no. 5, pp. 354-355, 2013. View at Publisher · View at Google Scholar · View at Scopus
  6. T. Katsuda, M. Kawamata, K. Hagiwara et al., “Conversion of terminally committed hepatocytes to culturable bipotent progenitor cells with regenerative capacity,” Cell Stem Cell, vol. 20, no. 1, pp. 41–55, 2017. View at Publisher · View at Google Scholar · View at Scopus
  7. Y. Kim, K. Kang, S. B. Lee et al., “Small molecule-mediated reprogramming of human hepatocytes into bipotent progenitor cells,” Journal of Hepatology, vol. 70, no. 1, pp. 97–107, 2019. View at Publisher · View at Google Scholar · View at Scopus
  8. G. B. Fu, W. J. Huang, M. Zeng et al., “Expansion and differentiation of human hepatocyte-derived liver progenitor-like cells and their use for the study of hepatotropic pathogens,” Cell Research, vol. 29, no. 1, pp. 8–22, 2019. View at Publisher · View at Google Scholar · View at Scopus
  9. K. Anzai, H. Chikada, K. Tsuruya et al., “Foetal hepatic progenitor cells assume a cholangiocytic cell phenotype during two-dimensional pre-culture,” Scientific Reports, vol. 6, no. 1, article 28283, 2016. View at Publisher · View at Google Scholar · View at Scopus
  10. N. Dianat, H. Dubois-Pot-Schneider, C. Steichen et al., “Generation of functional cholangiocyte-like cells from human pluripotent stem cells and HepaRG cells,” Hepatology, vol. 60, no. 2, pp. 700–714, 2014. View at Publisher · View at Google Scholar · View at Scopus
  11. M. Ogawa, S. Ogawa, C. E. Bear et al., “Directed differentiation of cholangiocytes from human pluripotent stem cells,” Nature Biotechnology, vol. 33, no. 8, pp. 853–861, 2015. View at Publisher · View at Google Scholar · View at Scopus
  12. F. Sampaziotis, M. C. de Brito, I. Geti, A. Bertero, N. R. F. Hannan, and L. Vallier, “Directed differentiation of human induced pluripotent stem cells into functional cholangiocyte-like cells,” Nature Protocols, vol. 12, no. 4, pp. 814–827, 2017. View at Publisher · View at Google Scholar · View at Scopus
  13. F. Sampaziotis, M. Cardoso de Brito, P. Madrigal et al., “Cholangiocytes derived from human induced pluripotent stem cells for disease modeling and drug validation,” Nature Biotechnology, vol. 33, no. 8, pp. 845–852, 2015. View at Publisher · View at Google Scholar · View at Scopus
  14. F. Wu, D. Wu, Y. Ren et al., “Generation of hepatobiliary organoids from human induced pluripotent stem cells,” Journal of Hepatology, vol. 70, no. 6, pp. 1145–1158, 2019. View at Publisher · View at Google Scholar · View at Scopus
  15. P. O. Seglen, “Chapter 4 Preparation of isolated rat liver cells,” Methods in Cell Biology, vol. 13, pp. 29–83, 1976. View at Publisher · View at Google Scholar · View at Scopus
  16. Y. Sakai, M. Koike, D. Kawahara et al., “Controlled cell morphology and liver-specific function of engineered primary hepatocytes by fibroblast layer cell densities,” Journal of Bioscience and Bioengineering, vol. 126, no. 2, pp. 249–257, 2018. View at Publisher · View at Google Scholar · View at Scopus
  17. T. Katsuda and T. Ochiya, “Chemically induced liver progenitors (CLiPs): a novel cell source for hepatocytes and biliary epithelial cells,” Methods in Molecular Biology, vol. 1905, pp. 117–130, 2019. View at Publisher · View at Google Scholar · View at Scopus
  18. A. DeLaForest, M. Nagaoka, K. Si-Tayeb et al., “HNF4A is essential for specification of hepatic progenitors from human pluripotent stem cells,” Development, vol. 138, no. 19, pp. 4143–4153, 2011. View at Publisher · View at Google Scholar · View at Scopus
  19. F. P. Lemaigre, “Molecular mechanisms of biliary development,” Progress in Molecular Biology and Translational Science, vol. 97, pp. 103–126, 2010. View at Publisher · View at Google Scholar · View at Scopus
  20. P. B. Limaye, G. Alarcón, A. L. Walls et al., “Expression of specific hepatocyte and cholangiocyte transcription factors in human liver disease and embryonic development,” Laboratory Investigation, vol. 88, no. 8, pp. 865–872, 2008. View at Publisher · View at Google Scholar · View at Scopus
  21. F. Clotman, V. J. Lannoy, M. Reber et al., “The onecut transcription factor HNF6 is required for normal development of the biliary tract,” Development, vol. 129, pp. 1819–1828, 2002. View at Google Scholar
  22. A. Gigliozzi, F. Fraioli, P. Sundaram et al., “Molecular identification and functional characterization of mdr1a in rat cholangiocytes,” Gastroenterology, vol. 119, no. 4, pp. 1113–1122, 2000. View at Publisher · View at Google Scholar · View at Scopus
  23. J. E. Ros, L. Libbrecht, M. Geuken, P. L. M. Jansen, and T. A. D. Roskams, “High expression of MDR1, MRP1, and MRP3 in the hepatic progenitor cell compartment and hepatocytes in severe human liver disease,” The Journal of Pathology, vol. 200, no. 5, pp. 553–560, 2003. View at Publisher · View at Google Scholar · View at Scopus
  24. D. Čížková, J. Mokrý, S. Mičuda, J. Österreicher, and J. Martínková, “Expression of MRP2 and MDR1 transporters and other hepatic markers in rat and human liver and in WRL 68 cell line,” Physiological Research, vol. 54, pp. 419–428, 2005. View at Google Scholar
  25. K. Köck and K. L. R. Brouwer, “A perspective on efflux transport proteins in the liver,” Clinical Pharmacology and Therapeutics, vol. 92, no. 5, pp. 599–612, 2012. View at Publisher · View at Google Scholar · View at Scopus
  26. B. Stieger, “The role of the sodium-taurocholate cotransporting polypeptide (NTCP) and of the bile salt export pump (BSEP) in physiology and pathophysiology of bile formation,” Handbook of Experimental Pharmacology, vol. 201, pp. 205–259, 2011. View at Publisher · View at Google Scholar · View at Scopus
  27. P. A. Dawson, T. Lan, and A. Rao, “Bile acid transporters,” Journal of Lipid Research, vol. 50, no. 12, pp. 2340–2357, 2009. View at Publisher · View at Google Scholar · View at Scopus
  28. A. Jetter and G. A. Kullak-Ublick, “Drugs and hepatic transporters: a review,” Pharmacological Research, 2019. View at Publisher · View at Google Scholar
  29. M. Mijnders, B. Kleizen, and I. Braakman, “Correcting CFTR folding defects by small-molecule correctors to cure cystic fibrosis,” Current Opinion in Pharmacology, vol. 34, pp. 83–90, 2017. View at Publisher · View at Google Scholar · View at Scopus
  30. B. J. Scholte, W. H. Colledge, M. Wilke, and H. de Jonge, “Cellular and animal models of cystic fibrosis, tools for drug discovery,” Drug Discovery Today: Disease Models, vol. 3, no. 3, pp. 251–259, 2006. View at Publisher · View at Google Scholar · View at Scopus
  31. K. Takayama, N. Akita, N. Mimura et al., “Generation of safe and therapeutically effective human induced pluripotent stem cell-derived hepatocyte-like cells for regenerative medicine,” Hepatology Communications, vol. 1, no. 10, pp. 1058–1069, 2017. View at Publisher · View at Google Scholar
  32. K. Takayama, K. Kawabata, Y. Nagamoto et al., “3D spheroid culture of hESC/hiPSC-derived hepatocyte-like cells for drug toxicity testing,” Biomaterials, vol. 34, no. 7, pp. 1781–1789, 2013. View at Publisher · View at Google Scholar · View at Scopus
  33. A. Shlomai, R. E. Schwartz, V. Ramanan et al., “Modeling host interactions with hepatitis B virus using primary and induced pluripotent stem cell-derived hepatocellular systems,” Proceedings of the National Academy of Sciences, vol. 111, no. 33, pp. 12193–12198, 2014. View at Publisher · View at Google Scholar · View at Scopus
  34. R. Ouchi, S. Togo, M. Kimura et al., “Modeling steatohepatitis in humans with pluripotent stem cell-derived organoids,” Cell Metabolism, vol. 30, no. 2, pp. 374–384.e6, 2019. View at Publisher · View at Google Scholar
  35. J. H. Tabibian, A. I. Masyuk, T. V. Masyuk, S. P. O'Hara, and N. F. LaRusso, “Physiology of cholangiocytes,” Comprehensive Physiology, vol. 3, pp. 541–565, 2013. View at Publisher · View at Google Scholar · View at Scopus
  36. E. A. Ober and F. P. Lemaigre, “Development of the liver: insights into organ and tissue morphogenesis,” Journal of Hepatology, vol. 68, no. 5, pp. 1049–1062, 2018. View at Publisher · View at Google Scholar · View at Scopus