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Cited by 613D Printing in Biomedical ResearchTissue Engineering and Regenerative MedicineHydrogels: synthesis, properties, applications

Directing the growth and alignment of biliary epithelium within extracellular matrix hydrogels

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Lewis, Phillip L., Yan, Ming, Su, Jimmy, Shah, Ramille N.·2019·Acta Biomaterialia
DOI 10.1016/j.actbio.2018.12.039PMC PMC6768828
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Abstract

Three-dimensional (3D) printing of decellularized extracellular matrix (dECM) hydrogels is a promising technique for regenerative engineering. 3D-printing enables the reproducible and precise patterning of multiple cells and biomaterials in 3D, while dECM has high organ-specific bioactivity. However, dECM hydrogels often display poor printability on their own and necessitate additives or support materials to enable true 3D structures. In this study, we used a sacrificial material, 3D-printed Pluronic F-127, to serve as a platform into which dECM hydrogel can be incorporated to create specifically designed structures made entirely up of dECM. The effects of 3D dECM are studied in the context of engineering the intrahepatic biliary tree, an often-understudied topic in liver tissue engineering. Encapsulating biliary epithelial cells (cholangiocytes) within liver dECM has been shown to lead to the formation of complex biliary trees in vitro. By varying several aspects of the dECM structures' geometry, such as width and angle, we show that we can guide the directional formation of biliary trees. This is confirmed by computational 3D image analysis of duct alignment. This system also enables fabrication of a true multi-layer dECM structure and the formation of 3D biliary trees into which other cell types can be seeded. For example, we show that hepatocyte spheroids can be easily incorporated within this system, and that the seeding sequence influences the resulting structures after seven days in culture. STATEMENT OF SIGNIFICANCE: The field of liver tissue engineering has progressed significantly within the past several years, however engineering the intrahepatic biliary tree has remained a significant challenge. In this study, we utilize the inherent bioactivity of decellularized extracellular matrix (dECM) hydrogels and 3D-printing of a sacrificial biomaterial to create spatially defined, 3D biliary trees. The creation of patterned, 3D dECM hydrogels in the past has only been possible with additives to the gel that may stifle its bioactivity, or with rigid and permanent support structures that may present issues upon implantation. Additionally, the biological effect of 3D spatially patterned liver dECM has not been demonstrated independent of the effects of dECM bioactivity alone. This study demonstrates that sacrificial materials can be used to create pure, multi-layer dECM structures, and that strut width and angle can be changed to influence the formation and alignment of biliary trees encapsulated within. Furthermore, this strategy allows co-culture of other cells such as hepatocytes. We demonstrate that not only does this system show promise for tissue engineering the intrahepatic biliary tree, but it also aids in the study of duct formation and cell-cell interactions.

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  • Porcine liver was used in approximately 51 studies.

    “The papers mentioned indicate that porcine liver has been the prominent material utilized in the creation of decellularized liver extracellular matrix (dLECM) that was utilized in approximately 51 studies.”

    From From scaffold to function: A systematic review on dLECM-based hydrogels for liver tissue engineering — Fabrication, properties, and translational applications (2026) · cites this paper as [61]

    The Materials and methods section (Liver decellularization and digestion; page unavailable) says the authors made decellularized extracellular matrix from pig livers. It does not report that porcine liver was used in approximately 51 studies or establish that it was the predominant source across studies; the '51' in the References is a citation number, not a study count. (LLM, conf=0.88)

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  • Nineteen studies explored use in organoid culture, wherein the biomimetic microenvironment supported spontaneous self-organization of stem cells and hepatocytes into complex structures, including bile duct networks and hepatocyte spheroids.

    “Nineteen studies have explored their use in organoid culture, wherein the biomimetic microenvironment supported the spontaneous self-organization of stem cells and hepatocytes into complex structures, including bile duct networks and hepatocyte spheroids [61,79].”

    From From scaffold to function: A systematic review on dLECM-based hydrogels for liver tissue engineering — Fabrication, properties, and translational applications (2026) · cites this paper as [61]

    The Abstract and Conclusion report bile-duct formation in dECM hydrogels and patterned co-culture with hepatocytes. However, the Materials and methods section says the hepatocyte spheroids were formed in agarose microwells before being seeded into the scaffold, and the study used cell lines rather than demonstrating spontaneous self-organization of stem cells. The paper also does not substantiate the citing sentence’s count of nineteen organoid-culture studies. (LLM, conf=0.88)

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Cited by

Sorted by citations

Authors
Lewis, P. L., Yan, M., Su, J., & Shah, R. N.
Affiliations
Northwestern University (US)
Corresponding author
Shah, Ramille N.
ORCID
Venue
Acta Biomaterialia
Publisher
Elsevier BV
Published
2019-02
Volume
85
Pages
84-93
ISSN
1742-7061 (ISSN-L)
DOI
10.1016/j.actbio.2018.12.039
PMC
PMC6768828
OpenAlex
W2905937254
Cited by
61
References
3
Citations by year
2026: 7 · 2025: 6 · 2024: 6 · 2023: 11 · 2022: 8 · 2021: 10 · 2020: 8 · 2019: 4 · 2018: 1
FWCI
2.24
Type
journal article
Language
en
Open access
Licence
Locations
  • Acta Biomaterialia (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
Funders
  • National Cancer Institute (P30CA060553)
  • National Institute of General Medical Sciences (T32GM008449)
  • National Institute of Diabetes and Digestive and Kidney Diseases (K01DK099454, F31DK108544)
Topics
  • Physical Sciences › Engineering › Biomedical Engineering › 3D Printing in Biomedical Research
  • Health Sciences › Medicine › Surgery › Tissue Engineering and Regenerative Medicine
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Medicine › Hydrogels: synthesis, properties, applications
Keywords
3D bioprinting, cholangiocytes, liver tissue engineering, hepatocyte spheroids, printability, computational image analysis
MeSH terms
Animals, Bile Ducts, Biliary Tract, Epithelium, Extracellular Matrix, Female, Humans, Swine, Coculture Techniques, Hydrogels, Hepatocytes, Mice, Tissue Scaffolds, Printing, Three-Dimensional

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