Complex bile duct network formation within liver decellularized extracellular matrix hydrogels
Open accessAbstract
The biliary tree is an essential component of transplantable human liver tissue. Despite recent advances in liver tissue engineering, attempts at re-creating the intrahepatic biliary tree have not progressed significantly. The finer branches of the biliary tree are structurally and functionally complex and heterogeneous and require harnessing innate developmental processes for their regrowth. Here we demonstrate the ability of decellularized liver extracellular matrix (dECM) hydrogels to induce the in vitro formation of complex biliary networks using encapsulated immortalized mouse small biliary epithelial cells (cholangiocytes). This phenomenon is not observed using immortalized mouse large cholangiocytes, or with purified collagen 1 gels or Matrigel. We also show phenotypic stability via immunostaining for specific cholangiocyte markers. Moreover, tight junction formation and maturation was observed to occur between cholangiocytes, exhibiting polarization and transporter activity. To better define the mechanism of duct formation, we utilized three fluorescently labeled, but otherwise identical populations of cholangiocytes. The cells, in a proximity dependent manner, either branch out clonally, radiating from a single nucleation point, or assemble into multi-colored structures arising from separate populations. These findings present liver dECM as a promising biomaterial for intrahepatic bile duct tissue engineering and as a tool to study duct remodeling in vitro.
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Lewis et al. (2018) demonstrated formation of complex bile duct networks inside dLECM hydrogels, highlighting ability of matrix to guide morphogenesis.
“Significantly, Lewis et al. (2018) demonstrated the formation of the complex bile duct networks inside dLECM hydrogels, highlighting the ability of the matrix to guide morphogenesis [60].”
Cholangiocytes cultured in Matrigel formed cysts, while those in collagen I proliferated and spread in all directions without spontaneously forming structures.
“In contrast, cholangiocytes cultured in Matrigel formed cysts while those in collagen I proliferated and spread in all directions without spontaneously forming structures77.”
From Towards organoid culture without Matrigel (2021) · cites this paper as [77]
Growing murine small cholangiocytes in porcine liver ECM gel resulted in the formation of complex, branching structures similar to biliary ducts, and these cells secreted small amounts of bile.
“Lewis and colleagues observed that growing murine small cholangiocytes (a committed progenitor cell type) in porcine liver ECM gel resulted in the formation of complex, branching structures similar to biliary ducts, and these cells also secreted small amounts of bile.”
From Towards organoid culture without Matrigel (2021) · cites this paper as [77]
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1 retracted
Mancinelli, R., Franchitto, A., Glaser, S. S., Meng, F., Onori, P., DeMorrow, S., Francis, H., Venter, J. K., Carpino, G., Baker, K., et al. (2013) · Hepatology · doi:10.1002/hep.26308 · Cited by 46 · see citing works
Self-citationRetractedTissue Cells Feel and Respond to the Stiffness of Their Substrate
Discher, D. E., Janmey, P., & Wang, Y.-L. (2005) · Science · doi:10.1126/science.1116995 · Cited by 6,382 · see citing works
Organoid Models and Applications in Biomedical Research
Xinaris, C., Brizi, V., & Remuzzi, G. (2015) · The Nephron journals/Nephron journals · doi:10.1159/000433566 · Cited by 3,517 · see citing works
A Third-Generation Lentivirus Vector with a Conditional Packaging System
Dull, T., Zufferey, R., Kelly, M., Mandel, R. J., Nguyen, M., Trono, D., & Naldini, L. (1998) · Journal of Virology · doi:10.1128/jvi.72.11.8463-8471.1998 · Cited by 3,341 · see citing works
Decellularization of tissues and organs
Gilbert, T. W., Sellaro, T. L., & Badylak, S. F. (2006) · Biomaterials · doi:10.1016/j.biomaterials.2006.02.014 · Cited by 2,222 · see citing works
Long-Term Culture of Genome-Stable Bipotent Stem Cells from Adult Human Liver
Huch, M., Gehart, H., van Boxtel, R., Hamer, K., Blokzijl, F., Verstegen, M. M. A., Ellis, E., van Wenum, M., Fuchs, S. A., de Ligt, J., et al. (2015) · Cell · doi:10.1016/j.cell.2014.11.050 · Cited by 1,619 · see citing works
In vitro expansion of single Lgr5+ liver stem cells induced by Wnt-driven regeneration
Huch, M., Dorrell, C., Boj, S. F., van Es, J. H., Li, V. S. W., van de Wetering, M., Sato, T., Hamer, K., Sasaki, N., Finegold, M. J., et al. (2013) · Nature · doi:10.1038/nature11826 · Cited by 1,555 · see citing works
Uygun, B. E., Soto-Gutierrez, A., Yagi, H., Izamis, M.-L., Guzzardi, M. A., Shulman, C., Milwid, J., Kobayashi, N., Tilles, A., Berthiaume, F., et al. (2010) · Nature Medicine · doi:10.1038/nm.2170 · Cited by 1,370 · see citing works
Badylak, S. F., Taylor, D., & Uygun, K. (2011) · Annual Review of Biomedical Engineering · doi:10.1146/annurev-bioeng-071910-124743 · Cited by 1,041 · see citing works
Extracellular matrix hydrogels from decellularized tissues: Structure and function
Saldin, L. T., Cramer, M. C., Velankar, S., White, L. J., & Badylak, S. F. (2016) · Acta Biomaterialia · doi:10.1016/j.actbio.2016.11.068 · Cited by 818 · see citing works
Organogenesis and development of the liver
Si-Tayeb, K., Lemaigre, F. P., & Duncan, S. A. (2010) · Developmental Cell · doi:10.1016/j.devcel.2010.01.011 · Cited by 800 · see citing works
Roskams, T., Theise, N. D., Balabaud, C. P., Bhagat, G., Bhathal, P. S., Bioulac‐Sage, P., Brunt, E. M., Crawford, J. M., Crosby, H. A., Desmet, V. J., et al. (2004) · Hepatology · doi:10.1002/hep.20130 · Cited by 729 · see citing works
The use of whole organ decellularization for the generation of a vascularized liver organoid
Baptista, P. M., Siddiqui, M. M., Lozier, G., Rodriguez, S. R., Atala, A., & Soker, S. (2011) · Hepatology · doi:10.1002/hep.24067 · Cited by 681 · see citing works
Supramolecular design of self-assembling nanofibers for cartilage regeneration
Shah, R. N., Shah, N. A., Lim, M., Hsieh, C., Nuber, G., & Stupp, S. I. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0906501107 · Cited by 543 · see citing works
Self-citationPreparation and rheological characterization of a gel form of the porcine urinary bladder matrix
Freytes, D. O., Martin, J. D., Velankar, S., Lee, A. S., & Badylak, S. F. (2008) · Biomaterials · doi:10.1016/j.biomaterials.2007.12.014 · Cited by 531 · see citing works
Arnaoutova, I., George, J., Kleinman, H. K., & Benton, G. (2009) · Angiogenesis · doi:10.1007/s10456-009-9146-4 · Cited by 454 · see citing works
Skardal, A., Devarasetty, M., Kang, H.-W., Mead, I., Bishop, C., Shupe, T., Lee, S. J., Jackson, J., Yoo, J., Soker, S., et al. (2015) · Acta Biomaterialia · doi:10.1016/j.actbio.2015.07.030 · Cited by 428 · see citing works
A protocol for rheological characterization of hydrogels for tissue engineering strategies
Zuidema, J. M., Rivet, C. J., Gilbert, R. J., & Morrison, F. A. (2013) · Journal of Biomedical Materials Research Part B Applied Biomaterials · doi:10.1002/jbm.b.33088 · Cited by 395 · see citing works
Antoniou, A., Raynaud, P., Cordi, S., Zong, Y., Tronche, F., Stanger, B. Z., Jacquemin, P., Pierreux, C. E., Clotman, F., & Lemaigre, F. P. (2009) · Gastroenterology · doi:10.1053/j.gastro.2009.02.051 · Cited by 362 · see citing works
Lee, H., Han, W., Kim, H., Ha, D., Jang, J., Kim, B. S., & Cho, D. (2017) · Biomacromolecules · doi:10.1021/acs.biomac.6b01908 · Cited by 329 · see citing works
Directed differentiation of cholangiocytes from human pluripotent stem cells
Ogawa, M., Ogawa, S., Bear, C. E., Ahmadi, S., Chin, S., Li, B., Grompe, M., Keller, G. M., Kamath, B. M., & Ghanekar, A. (2015) · Nature Biotechnology · doi:10.1038/nbt.3294 · Cited by 318 · see citing works
Cell and tissue engineering for liver disease
Bhatia, S. N., Underhill, G. H., Zaret, K. S., & Fox, I. J. (2014) · Science Translational Medicine · doi:10.1126/scitranslmed.3005975 · Cited by 309 · see citing works
Sampaziotis, F., Justin, A. W., Tysoe, O. C., Sawiak, S., Godfrey, E. M., Upponi, S. S., Gieseck, R. L., de Brito, M. C., Berntsen, N. L., Gómez-Vázquez, M. J., et al. (2017) · Nature Medicine · doi:10.1038/nm.4360 · Cited by 296 · see citing works
Maintenance of Human Hepatocyte Function In Vitro by Liver-Derived Extracellular Matrix Gels
Sellaro, T. L., Ranade, A. R., Faulk, D. M., McCabe, G. P., Dorko, K., Badylak, S. F., & Strom, S. C. (2009) · Tissue Engineering Part A · doi:10.1089/ten.tea.2008.0587 · Cited by 276 · see citing works
Choi, T., Ninov, N., Stainier, D. Y. R., & Shin, D. (2013) · Gastroenterology · doi:10.1053/j.gastro.2013.10.019 · Cited by 238 · see citing works
Lee, J. S., Shin, J., Park, H.-M., Kim, Y.-G., Kim, B.-G., Oh, J.-W., & Cho, S.-W. (2014) · Biomacromolecules · doi:10.1021/bm4015039 · Cited by 236 · see citing works
Assessing Porcine Liver-Derived Biomatrix for Hepatic Tissue Engineering
Lin, P., Chan, W. C. W., Badylak, S. F., & Bhatia, S. N. (2004) · Tissue Engineering · doi:10.1089/ten.2004.10.1046 · Cited by 236 · see citing works
Morphological, molecular, and functional heterogeneity of cholangiocytes from normal rat liver
Alpini, G. D., Roberts, S. K., Kuntz, S., Ueno, Y., Gubba, S., Podila, P. V., LeSage, G., & LaRusso, N. F. (1996) · Gastroenterology · doi:10.1053/gast.1996.v110.pm8613073 · Cited by 236 · see citing works
Self-citationGaudio, E., Barbaro, B., Alvaro, D., Glaser, S. S., Francis, H., Ueno, Y., Meininger, C. J., Franchitto, A., Onori, P., Marzioni, M., et al. (2006) · Gastroenterology · doi:10.1053/j.gastro.2005.12.034 · Cited by 235 · see citing works
Self-citationEsteller, A. (2008) · World Journal of Gastroenterology · doi:10.3748/wjg.14.5641 · Cited by 235 · see citing works
Wang, Y., Cui, C.-B., Yamauchi, M., Miguez, P., Roach, M., Malavarca, R., Costello, J. M., Cardinale, V., Wauthier, E., Barbier, C., et al. (2011) · Hepatology · doi:10.1002/hep.24012 · Cited by 220 · see citing works
Expression of the vHNF1/HNF1β homeoprotein gene during mouse organogenesis
Coffinier, C., Barra, J., Babinet, C., et al. (1999) · Mechanisms of Development · doi:10.1016/s0925-4773(99)00221-x · Cited by 218 · see citing works
Generation of functional cholangiocyte-like cells from human pluripotent stem cells and HepaRG cells
Dianat, N., Dubois‐Pot‐Schneider, H., Steichen, C., Desterke, C., Leclerc, P., Raveux, A., Combettes, L., Weber, A., Corlu, A., & Dubart‐Kupperschmitt, A. (2014) · Hepatology · doi:10.1002/hep.27165 · Cited by 213 · see citing works
Grabinger, T., Luks, L., Kostadinova, F. I., Zimberlin, C. D., Medema, J. P., Leist, M., & Brunner, T. B. (2014) · Cell Death and Disease · doi:10.1038/cddis.2014.183 · Cited by 210 · see citing works
The biliary tree—a reservoir of multipotent stem cells
Cardinale, V., Wang, Y.-F., Carpino, G., Mendel, G. L., Alpini, G., Gaudio, E., Reid, L., & Alvaro, D. (2012) · Nature Reviews Gastroenterology &Hepatology · doi:10.1038/nrgastro.2012.23 · Cited by 206 · see citing works
Self-citationExpression of claudins 1, 2, 3, 4, 5 and 7 in various types of tumours
Soini, Y. (2005) · Histopathology · doi:10.1111/j.1365-2559.2005.02127.x · Cited by 200 · see citing works
Heterogeneity of the proliferative capacity of rat cholangiocytes after bile duct ligation
Alpini, G. D., Glaser, S. S., Ueno, Y., et al. (1998) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.1998.274.4.g767 · Cited by 195 · see citing works
Self-citationLin, H., Yang, G., Tan, J., & Tuan, R. S. (2012) · Biomaterials · doi:10.1016/j.biomaterials.2012.03.012 · Cited by 193 · see citing works
The biliary epithelium gives rise to liver progenitor cells
Rodrigo-Torres, D., Affò, S., Coll, M., Morales-Ibanez, O., Millán, C., Blaya, D., Alvarez-Guaita, A., Rentero, C., José Lozano, J., Maestro, M. A., et al. (2014) · Hepatology · doi:10.1002/hep.27078 · Cited by 189 · see citing works
Tissue specific synthetic ECM hydrogels for 3-D in vitro maintenance of hepatocyte function
Skardal, A., Smith, L., Bharadwaj, S., Atala, A., Soker, S., & Zhang, Y. (2012) · Biomaterials · doi:10.1016/j.biomaterials.2012.03.034 · Cited by 183 · see citing works
Liver Progenitor Cells Develop Cholangiocyte-Type Epithelial Polarity in Three-dimensional Culture
Tanimizu, N., Miyajima, A., & Mostov, K. E. (2007) · Molecular Biology of the Cell · doi:10.1091/mbc.e06-09-0848 · Cited by 170 · see citing works
Lewis, P. L., Green, R. M., & Shah, R. N. (2018) · Acta Biomaterialia · doi:10.1016/j.actbio.2017.12.042 · Cited by 168 · see citing works
Self-citationGratzer, P. F., Harrison, R. D., & Woods, T. (2006) · Tissue Engineering · doi:10.1089/ten.2006.12.2975 · Cited by 160 · see citing works
Functional heterogeneity of the intrahepatic biliary epithelium
Kanno, N., LeSage, G., Glaser, S. S., Alvaro, D., & Alpini, G. D. (2000) · Hepatology · doi:10.1002/hep.510310302 · Cited by 158 · see citing works
Self-citationLarge but not small intrahepatic bile ducts are involved in secretin-regulated ductal bile secretion
Alpini, G. D., Glaser, S. S., Robertson, W. E., Rodgers, R., Phinizy, J. L., Lasater, J., & LeSage, G. (1997) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.1997.272.5.g1064 · Cited by 154 · see citing works
Self-citationBiliary differentiation and bile duct morphogenesis in development and disease
Raynaud, P., Carpentier, R., Antoniou, A., & Lemaigre, F. P. (2009) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2009.07.020 · Cited by 154 · see citing works
Wang, J., Elghazi, L., Parker, S. E., et al. (2003) · Developmental Biology · doi:10.1016/j.ydbio.2003.10.018 · Cited by 151 · see citing works
Molecular and functional heterogeneity of cholangiocytes from rat liver after bile duct ligation
Alpini, G. D., Ulrich, C. D., Roberts, S. K., Phillips, J. O., Ueno, Y., Podila, P. V., Colegio, O. R., LeSage, G., Miller, L. J., & LaRusso, N. F. (1997) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.1997.272.2.g289 · Cited by 151 · see citing works
Self-citationSparks, E. E., Huppert, K. A., Brown, M. A., Washington, M. K., & Huppert, S. S. (2009) · Hepatology · doi:10.1002/hep.23431 · Cited by 139 · see citing works
Morphological and functional heterogeneity of the mouse intrahepatic biliary epithelium
Glaser, S. S., Gaudio, E., Rao, A., Pierce, L. M., Onori, P., Franchitto, A., Francis, H., Dostal, D. E., Venter, J. K., DeMorrow, S., et al. (2009) · Laboratory Investigation · doi:10.1038/labinvest.2009.6 · Cited by 138 · see citing works
Self-citationFrancis, H., Glaser, S. S., DeMorrow, S., Gaudio, E., Ueno, Y., Venter, J. K., Dostal, D. E., Onori, P., Franchitto, A., Marzioni, M., et al. (2008) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00369.2007 · Cited by 136 · see citing works
Self-citation"Tissue Papers" from organ-specific decellularized extracellular matrices
Jakus, A. E., Laronda, M. M., Rashedi, A. S., Robinson, C. M., Lee, C., Jordan, S. W., Orwig, K. E., Woodruff, T. K., & Shah, R. N. (2017) · Advanced Functional Materials · doi:10.1002/adfm.201700992 · Cited by 133 · see citing works
Self-citationUeno, Y., Alpini, G. D., Yahagi, K., Kanno, N., Moritoki, Y., Fukushima, K., Glaser, S. S., LeSage, G., & Shimosegawa, T. (2003) · Liver International · doi:10.1111/j.1478-3231.2003.00876.x · Cited by 126 · see citing works
Self-citationOhashi, K., Waugh, J. M., Dake, M. D., Yokoyama, T., Kuge, H., Nakajima, Y., Yamanouchi, M., Naka, H., Yoshioka, A., & Kay, M. A. (2005) · Hepatology · doi:10.1002/hep.20484 · Cited by 125 · see citing works
Park, K.-M., Hussein, K. H., Hong, S.-H., Ahn, C., Yang, S.-R., Park, S.-M., Kweon, O.-K., Kim, B.-M., & Woo, H.-M. (2016) · Tissue Engineering Part A · doi:10.1089/ten.tea.2015.0313 · Cited by 113 · see citing works
Heterogeneity of the intrahepatic biliary epithelium
Glaser, S. S. (2006) · World Journal of Gastroenterology · doi:10.3748/wjg.v12.i22.3523 · Cited by 92 · see citing works
Self-citationHepatic Transport Mechanisms of Cholyl-l-Lysyl-Fluorescein
de Waart, D. R., Häusler, S., Vlaming, M. L. H., Kunne, C., Hänggi, E., Gruss, H.-J., Elferink, R. P. J. O., & Stieger, B. (2010) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.110.166991 · Cited by 92 · see citing works
A Tissue-Engineered Artificial Bile Duct Grown to Resemble The Native Bile Duct
Miyazawa, M., Torii, T., Toshimitsu, Y., et al. (2005) · American Journal of Transplantation · doi:10.1111/j.1600-6143.2005.00845.x · Cited by 80 · see citing works
Mancinelli, R., Franchitto, A., Gaudio, E., et al. (2010) · American Journal Of Pathology · doi:10.2353/ajpath.2010.090677 · Cited by 79 · see citing works
Enomoto, M., Bunge, M. B., & Tsoulfas, P. (2013) · Experimental Neurology · doi:10.1016/j.expneurol.2013.06.013 · Cited by 61 · see citing works
Molecular identification and functional characterization of Mdr1a in rat cholangiocytes
Gigliozzi, A., Fraioli, F., Sundaram, P., Lee, J., Mennone, A., Alvaro, D., & Boyer, J. L. (2000) · Gastroenterology · doi:10.1053/gast.2000.18156 · Cited by 52 · see citing works
Auth, M. K. H. (2001) · Hepatology · doi:10.1053/jhep.2001.22703 · Cited by 51 · see citing works
Seth, A., Ye, J., Yu, N., Guez, F., Bedford, D. C., Neale, G. A., Cordi, S., Brindle, P. K., Lemaigre, F. P., Kaestner, K. H., et al. (2014) · Development · doi:10.1242/dev.099481 · Cited by 50 · see citing works
Self-citationGriffith, L. G., Wells, A. H., & Stolz, D. B. (2014) · Hepatology · doi:10.1002/hep.27150 · Cited by 50 · see citing works
Li, Q., Tao, L., Chen, B., et al. (2012) · Biomaterials · doi:10.1016/j.biomaterials.2012.03.003 · Cited by 48 · see citing works
Barralet, J. E., Wallace, L. L., & Strain, A. J. (2003) · Tissue Engineering · doi:10.1089/107632703322495673 · Cited by 44 · see citing works
Hassanein, W., Uluer, M. C., Langford, J. T., Woodall, J. D., Cimeno, A., Dhru, U., Werdesheim, A., Harrison, J., Rivera-Pratt, C., Klepfer, S., et al. (2016) · Organogenesis · doi:10.1080/15476278.2016.1276146 · Cited by 36 · see citing works
Auth, M. K. H., Woitaschek, D., Beste, M., Schreiter, T., Kim, H. S., Oppermann, E., Joplin, R., Baumann, U., Hilgard, P. A., Nadalin, S., et al. (2005) · Liver Transplantation · doi:10.1002/lt.20367 · Cited by 32 · see citing works
Ishida, Y. Y., Smith, S., Wallace, L. M., et al. (2001) · Journal of Hepatology · doi:10.1016/s0168-8278(01)00078-2 · Cited by 31 · see citing works
Hashimoto, W., Sudo, R., Fukasawa, K., et al. (2008) · American Journal Of Pathology · doi:10.2353/ajpath.2008.071024 · Cited by 30 · see citing works
Regenerative Medicine and the Biliary Tree
de Assuncao, T. M., Jalan‐Sakrikar, N., & Huebert, R. C. (2017) · Seminars in Liver Disease · doi:10.1055/s-0036-1597818 · Cited by 30 · see citing works
Katsuda, T., Kojima, N., Ochiya, T., & Sakai, Y. (2013) · Tissue Engineering Part A · doi:10.1089/ten.tea.2013.0021 · Cited by 24 · see citing works
Regeneration of extrahepatic bile ducts by tissue engineering with a bioabsorbable polymer
Miyazawa, M., Aikawa, M., Okada, K., et al. (2011) · Journal of Artificial Organs · doi:10.1007/s10047-011-0590-8 · Cited by 20 · see citing works
Functional Heterogeneity of the Intrahepatic Biliary Epithelium
Glaser, S. S., Francis, H., Marzioni, M., et al. (2020) · CRC Press eBooks · doi:10.1201/9780367813888-23 · Cited by 3 · see citing works
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- [47]Saldin LT Cramer MC Velankar SS White LJ Badylak SF Extracellular matrix hydrogels from decellularized tissues: Structure and function Acta Biomater. 2017 49 1 15 10.1016/j.actbio.2016.11.068 27915024 PMC5253110 · DOI
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Kozlowski, M. T., Crook, C. J., & Ku, H. T. (2021) · Communications Biology · doi:10.1038/s42003-021-02910-8 · Cited by 409 · see citing works
Extracellular matrix-derived biomaterials in engineering cell function
Xing, H., Lee, H., Luo, L., & Kyriakides, T. R. (2020) · Biotechnology Advances · doi:10.1016/j.biotechadv.2019.107421 · Cited by 302 · see citing works
Brown, M., Li, J., Moraes, C., Tabrizian, M., & Li-Jessen, N. Y. K. (2022) · Biomaterials · doi:10.1016/j.biomaterials.2022.121786 · Cited by 282 · see citing works
Tao, M., Ao, T., Mao, X., Yan, X., Javed, R., Hou, W., Wang, Y., Sun, C., Lin, S., Yu, T., et al. (2021) · Bioactive Materials · doi:10.1016/j.bioactmat.2021.02.010 · Cited by 119 · see citing works
Willemse, J., van Tienderen, G., van Hengel, E., Schurink, I., van der Ven, D., Kan, Y., de Ruiter, P., Rosmark, O., Westergren-Thorsson G, G., Schneeberger, K., et al. (2022) · Biomaterials · doi:10.1016/j.biomaterials.2022.121473 · Cited by 106 · see citing works
Recent advances in liver engineering with decellularized scaffold
Dai, Q., Jiang, W., Huang, F., Song, F., Zhang, J., & Zhao, H. (2022) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2022.831477 · Cited by 57 · see citing works
Constructing biomimetic liver models through biomaterials and vasculature engineering
Lv, W., Zhou, H., Aazmi, A., Yu, M., Xu, X., Yang, H., Huang, Y. Y. S., & Ma, L. (2022) · Regenerative Biomaterials · doi:10.1093/rb/rbac079 · Cited by 45 · see citing works
Hussein, K. H., Ahmadzada, B., Correa, J. C., Sultan, A., Wilken, S., Amiot, B., & Nyberg, S. L. (2024) · Bioactive Materials · doi:10.1016/j.bioactmat.2024.06.001 · Cited by 28 · see citing works
“These changes in ECM microstructure can increase resistance to enzymatic digestion of the ECM and lead to significant discrepancies between human livers [30,31,35 – 38].”
BackgroundSerna-Márquez, N., Rodríguez-Hernández, A., Ayala-Reyes, M., Martínez-Hernández, L. O., Peña-Rico, M. Á., Carretero-Ortega, J., Hautefeuille, M., & Vázquez-Victorio, G. (2020) · Biomimetics · doi:10.3390/biomimetics5020030 · Cited by 15 · see citing works
Udagawa, D., Nagata, S., Yagi, H., Nishi, K., Morisaku, T., Adachi, S., Nakano, Y., Tanaka, M., Hori, S., Hasegawa, Y., et al. (2024) · Cell Transplantation · doi:10.1177/09636897241253700 · Cited by 11 · see citing works
Bhatt, S., Krishnakumar, J., Mounica, K. L., & Nune, M. (2025) · Macromolecular Materials and Engineering · doi:10.1002/mame.202400451 · Cited by 6 · see citing works
Majidi, Z., Sarvi, M. M., Rajabi, M. A., Firouzian, H., Seyhoun, I., & Majidi Zolbin, M. (2026) · Regenerative Therapy · doi:10.1016/j.reth.2025.11.006 · Cited by 5 · see citing works
- Authors
- Lewis, P. L., Su, J., Yan, M., Meng, F., Glaser, S. S., Alpini, G. D., Green, R. M., Sosa-Pineda, B., & Shah, R. N.
- Affiliations
- Northwestern University (US)
- Central Texas Veterans Health Care System (US)
- Corresponding author
- Shah, Ramille N.
- ORCID
- Venue
- Scientific Reports
- Published
- 2018-08-15
- Volume
- 8
- Issue
- 1
- Pages
- 12220-12220
- ISSN
- 2045-2322 (ISSN-L)
- PMC
- PMC6093899
- OpenAlex
- W2886315925
- Cited by
- 68
- References
- 74
- Citations by year
- 2026: 4 · 2025: 6 · 2024: 11 · 2023: 8 · 2022: 15 · 2021: 13 · 2020: 5 · 2019: 5 · 2018: 1
- FWCI
- 6.24
- Type
- journal article
- Language
- en
- Update notices
- correction (2023-01-17)
- Open access
- gold
- doi.org
- Locations
- Scientific Reports (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, other-oa)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- U.S. Department of Health & Human Services | National Institutes of Health (1F31DK108544-01A1, GM008449, DK076898, 1K01DK099454)
- U.S. Department of Veterans Affairs (1I01BX001724, 5I01BX002192, 5I01BX000574)
- PSC Partners Seeking a Cure (7280909288FF)
- Topics
- Health Sciences › Medicine › Surgery › Tissue Engineering and Regenerative Medicine
- Physical Sciences › Engineering › Biomedical Engineering › 3D Printing in Biomedical Research
- Health Sciences › Medicine › Hepatology › Liver physiology and pathology
- Keywords
- hydrogels, cholangiocytes, liver tissue engineering, tight junction formation, cell polarization
- MeSH terms
- Animals, Bile Ducts, Bile Ducts, Intrahepatic, Biliary Tract, Cell Line, Epithelial Cells, Extracellular Matrix, Female, Liver, Swine, Hydrogels, Mice
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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