Mesenchymal stem cells support hepatocyte function in engineered liver grafts
Open accessAbstract
Recent studies suggest that organ decellularization is a promising approach to facilitate the clinical application of regenerative therapy by providing a platform for organ engineering. This unique strategy uses native matrices to act as a reservoir for the functional cells which may show therapeutic potential when implanted into the body. Appropriate cell sources for artificial livers have been debated for some time. The desired cell type in artificial livers is primary hepatocytes, but in addition, other supportive cells may facilitate this stem cell technology. In this context, the use of mesenchymal stem cells (MSC) is an option meeting the criteria for therapeutic organ engineering. Ideally, supportive cells are required to (1) reduce the hepatic cell mass needed in an engineered liver by enhancing hepatocyte function, (2) modulate hepatic regeneration in a paracrine fashion or by direct contact, and (3) enhance the preservability of parenchymal cells during storage. Here, we describe enhanced hepatic function achieved using a strategy of sequential infusion of cells and illustrate the advantages of co-cultivating bone marrow-derived MSCs with primary hepatocytes in the engineered whole-liver scaffold. These co-recellularized liver scaffolds colonized by MSCs and hepatocytes were transplanted into live animals. After blood flow was established, we show that expression of adhesion molecules and proangiogenic factors was upregulated in the graft.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Enzymatic treatment, particularly involving nucleases and trypsin, is often combined with chemical detergents followed by various washing cycles for liver decellularization.
“Hence, enzymatic treatment, particularly involving nucleases and trypsin, is often combined with chemical detergents followed by various washing cycles for liver decellularization [110,123,149,150].”
From Liver tissue engineering using decellularized scaffolds: Current progress, challenges, and opportunities (2024) · cites this paper as [123]
Cites
1 retracted
RETRACTED ARTICLE: Pluripotency of mesenchymal stem cells derived from adult marrow
Jiang, Y., Jahagirdar, B., Reinhardt, R. L., Schwartz, R. E., Keene, C. D., Ortiz-Gonzalez, X. R., Reyes, M., Lenvik, T. R., Lund, T. C., Blackstad, M., et al. (2002) · Nature · doi:10.1038/nature00870 · Cited by 5,523 · see citing works
RetractedMatrix elasticity directs stem cell lineage specification
Engler, A. J., Sen, S., Sweeney, H. L., & Discher, D. E. (2006) · Cell · doi:10.1016/j.cell.2006.06.044 · Cited by 13,915 · see citing works
Lutolf, M. P., & Hubbell, J. A. (2005) · Nature Biotechnology · doi:10.1038/nbt1055 · Cited by 4,551 · see citing works
Di Nicola, M., Carlo-Stella, C., Magni, M., Milanesi, M., Longoni, P. D., Matteucci, P., Grisanti, S., & Gianni, A. M. (2002) · Blood · doi:10.1182/blood.v99.10.3838 · Cited by 3,226 · see citing works
Growth Factors, Matrices, and Forces Combine and Control Stem Cells
Discher, D. E., Mooney, D. J., & Zandstra, P. W. (2009) · Science · doi:10.1126/science.1171643 · Cited by 2,666 · see citing works
Perfusion-decellularized matrix: using nature's platform to engineer a bioartificial heart
Ott, H. C., Matthiesen, T. S., Goh, S.-K., Black, L. D., Kren, S. M., Netoff, T. I., & Taylor, D. A. (2008) · Nature Medicine · doi:10.1038/nm1684 · Cited by 2,650 · see citing works
Rejuvenation of aged progenitor cells by exposure to a young systemic environment
Conboy, I. M., Conboy, M. J., Wagers, A. J., Girma, E. R., Weissman, I. L., & Rando, T. A. (2005) · Nature · doi:10.1038/nature03260 · Cited by 2,287 · 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
Vascularized and functional human liver from an iPSC-derived organ bud transplant
Takebe, T., Sekine, K., Enomura, M., Koike, H., Kimura, M., Ogaeri, T., Zhang, R.-R., Ueno, Y., Zheng, Y.-W., Koike, N., et al. (2013) · Nature · doi:10.1038/nature12271 · Cited by 2,170 · 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
Self-citationKim, S., Turnbull, J. E., & Guimond, S. E. (2011) · Journal of Endocrinology · doi:10.1530/joe-10-0377 · Cited by 1,166 · see citing works
Regeneration and orthotopic transplantation of a bioartificial lung
Ott, H. C., Clippinger, B., Conrad, C., Schuetz, C., Pomerantseva, I., Ikonomou, L., Kotton, D., & Vacanti, J. P. (2010) · Nature Medicine · doi:10.1038/nm.2193 · Cited by 1,090 · 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
Treatment of the Crigler–Najjar Syndrome Type I with Hepatocyte Transplantation
Fox, I. J., Chowdhury, J. R., Kaufman, S. S., Goertzen, T. C., Chowdhury, N. R., Warkentin, P. I., Dorko, K., Sauter, B. V., & Strom, S. C. (1998) · New England Journal of Medicine · doi:10.1056/nejm199805143382004 · Cited by 1,022 · see citing works
Interactions Between Human Mesenchymal Stem Cells and Natural Killer Cells
Sotiropoulou, P. A., Perez, S. A., Gritzapis, A. D., Baxevanis, C. N., & Papamichail, M. (2006) · Stem Cells · doi:10.1634/stemcells.2004-0359 · Cited by 956 · see citing works
Liver Organogenesis Promoted by Endothelial Cells Prior to Vascular Function
Matsumoto, K., Yoshitomi, H., Rossant, J., & Zaret, K. S. (2001) · Science · doi:10.1126/science.1063889 · Cited by 877 · see citing works
Regeneration and experimental orthotopic transplantation of a bioengineered kidney
Song, J. J., Guyette, J. P., Gilpin, S. E., Gonzalez, G., Vacanti, J. P., & Ott, H. C. (2013) · Nature Medicine · doi:10.1038/nm.3154 · Cited by 793 · see citing works
Consequences of lack of beta 1 integrin gene expression in mice.Preprint
Fässler, R., & Meyer, M. (1995) · Genes & Development · doi:10.1101/gad.9.15.1896 · Cited by 733 · see citing works
Mesenchymal Stem Cells: Mechanisms of Immunomodulation and Homing
Yagi, H., Soto–Gutiérrez, A., Parekkadan, B., Kitagawa, Y., Tompkins, R. G., Kobayashi, N., & Yarmush, M. L. (2010) · Cell Transplantation · doi:10.3727/096368910x508762 · Cited by 699 · see citing works
Self-citationThe 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
Selective cell transplantation using bioabsorbable artificial polymers as matrices
Vacanti, J. P., Morse, M. A., Saltzman, W. M., Domb, A. J., Pérez‐Atayde, A. R., & Langer, R. (1988) · Journal of Pediatric Surgery · doi:10.1016/s0022-3468(88)80529-3 · Cited by 603 · see citing works
VEGF expression by mesenchymal stem cells contributes to angiogenesis in pancreatic carcinoma
Beckermann, B. M., Kallifatidis, G., Groth, A., Frommhold, D., Apel, A., Mattern, J., Salnikov, A. V., Moldenhauer, G., Wagner, W., Diehlmann, A., et al. (2008) · British Journal of Cancer · doi:10.1038/sj.bjc.6604508 · Cited by 406 · see citing works
Suzuki, A., Zheng, Y.-W., Kaneko, S., Onodera, M., Fukao, K., Nakauchi, H., & Taniguchi, H. (2002) · The Journal of Cell Biology · doi:10.1083/jcb.200108066 · Cited by 356 · see citing works
A Whole-Organ Regenerative Medicine Approach for Liver Replacement
Soto-Gutierrez, A., Zhang, L., Medberry, C., Fukumitsu, K., Faulk, D., Jiang, H., Reing, J., Gramignoli, R., Komori, J., Ross, M., et al. (2011) · Tissue Engineering Part C: Methods · doi:10.1089/ten.tec.2010.0698 · Cited by 311 · see citing works
Replacement of Liver Function in Rats by Transplantation of Microcarrier-Attached Hepatocytes
Demetriou, A. A., Whiting, J. F., Feldman, D., Levenson, S. Μ., Chowdhury, N. R., Moscioni, A. D., Kram, M. T., & Chowdhury, J. R. (1986) · Science · doi:10.1126/science.2426782 · Cited by 294 · see citing works
Regeneration of Rat Liver: Transfer of Humoral Agent by Cross Circulation
Moolten, F. L., & Bucher, N. L. R. (1967) · Science · doi:10.1126/science.158.3798.272 · Cited by 277 · see citing works
Use of Decellularized Porcine Liver for Engineering Humanized Liver Organ
Barakat, O., Abbasi, S., Rodriguez, G., Rios, J., Wood, R. P., Ozaki, C., Holley, L. S., & Gauthier, P. K. (2012) · Journal of Surgical Research · doi:10.1016/j.jss.2011.09.033 · Cited by 208 · see citing works
Major Challenges Limiting Liver Transplantation in the United States
Wertheim, J. A., Petrowsky, H., Saab, S., Kupiec‐Weglinski, J. W., & Busuttil, R. W. (2011) · American Journal of Transplantation · doi:10.1111/j.1600-6143.2011.03587.x · Cited by 188 · see citing works
Human-Scale Whole-Organ Bioengineering for Liver Transplantation: A Regenerative Medicine Approach
Yagi, H., Fukumitsu, K., Fukuda, K., Kitago, M., Shinoda, M., Obara, H., Itano, O., Kawachi, S., Tanabe, M., Coudriet, G. M., et al. (2013) · Cell Transplantation · doi:10.3727/096368912x654939 · Cited by 188 · see citing works
Self-citationReactive Bone Marrow Stromal Cells Attenuate Systemic Inflammation via sTNFR1
Yagi, H., Soto–Gutiérrez, A., Navarro–Álvarez, N., Nahmias, Y., Goldwasser, Y., Kitagawa, Y., Tilles, A. W., Tompkins, R. G., Parekkadan, B., & Yarmush, M. L. (2010) · Molecular Therapy · doi:10.1038/mt.2010.155 · Cited by 166 · see citing works
Self-citationOPTN/SRTR 2011 Annual Data Report: Liver
Kim, W. R., Stock, P. G., Smith, J. M., Heimbach, J. K., Skeans, M. A., Edwards, E., Harper, A. M., Snyder, J. J., Israni, A. K., & Kasiske, B. L. (2012) · American Journal of Transplantation · doi:10.1111/ajt.12021 · Cited by 162 · see citing works
Oh, S., Witek, R. P., Bae, S., Zheng, D., Jung, Y., Piscaglia, A. C., & Petersen, B. E. (2007) · Gastroenterology · doi:10.1053/j.gastro.2007.01.001 · Cited by 147 · see citing works
Bao, J., Shi, Y., Sun, H., Yin, X., Yang, R., Li, L., Chen, X., & Bu, H. (2011) · Cell Transplantation · doi:10.3727/096368910x536572 · Cited by 133 · see citing works
Soto–Gutiérrez, A., Navarro–Álvarez, N., Zhao, D., Rivas‐Carrillo, J. D., LEBKOWSKI, J. S., Tanaka, N., Fox, I. J., & Kobayashi, N. (2007) · Nature Protocols · doi:10.1038/nprot.2007.18 · Cited by 132 · see citing works
Oertel, M., Menthena, A., Chen, Y., Teisner, B., Jensen, C. H., & Shafritz, D. A. (2008) · Gastroenterology · doi:10.1053/j.gastro.2008.01.007 · Cited by 125 · see citing works
Liver damage in the rat induces hepatocyte stem cells from biliary epithelial cells
Alison, M., Golding, M., Sarraf, C., Edwards, R., & Lalani, E. (1996) · Gastroenterology · doi:10.1053/gast.1996.v110.pm8613008 · Cited by 119 · see citing works
Perspectives on whole-organ assembly: moving toward transplantation on demand
Soto–Gutiérrez, A., Wertheim, J. A., Ott, H. C., & Gilbert, T. W. (2012) · Journal of Clinical Investigation · doi:10.1172/jci61974 · Cited by 115 · see citing works
Zhou, P., Lessa, N. C., Estrada, D. K., Severson, E. B., Lingala, S., Zern, M. Α., Nolta, J. A., & Wu, J. (2011) · Liver Transplantation · doi:10.1002/lt.22270 · Cited by 108 · see citing works
Remodelling of extracellular matrix is a requirement for the hepatic progenitor cell response
Kallis, Y. N., Robson, A. J., Fallowfield, J. A., Thomas, H. C., Alison, M. R., Wright, N. A., Goldin, R. D., Iredale, J. P., & Forbes, S. J. (2010) · Gut · doi:10.1136/gut.2010.224436 · Cited by 106 · see citing works
Wang, Y., Yao, H.-L., Cui, C.-B., Wauthier, E., Barbier, C., Costello, M. J., Moss, N., Yamauchi, M., Sricholpech, M., Gerber, D. A., et al. (2010) · Hepatology · doi:10.1002/hep.23829 · Cited by 106 · see citing works
Wang, L., Wang, X., Wang, L., Chiu, J. D., van de Ven, G., Gaarde, W. A., & DeLeve, L. D. (2012) · Gastroenterology · doi:10.1053/j.gastro.2012.08.008 · Cited by 88 · see citing works
McClelland, R., Wauthier, E., Uronis, J., & Reid, L. M. (2008) · Tissue Engineering Part A · doi:10.1089/ten.a.2007.0058 · Cited by 79 · see citing works
Application of whole-organ tissue engineering in hepatology
Uygun, B. E., Yarmush, M. L., & Uygun, K. (2012) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/nrgastro.2012.140 · Cited by 76 · see citing works
Yagi, H., Parekkadan, B., Suganuma, K., Soto–Gutiérrez, A., Tompkins, R. G., Tilles, A. W., & Yarmush, M. L. (2009) · Tissue Engineering Part A · doi:10.1089/ten.tea.2008.0681 · Cited by 63 · see citing works
Self-citationStolz, D. B., Ross, M. A., Ikeda, A., Tomiyama, K., Kaizu, T., Geller, D. A., & Murase, N. (2007) · Hepatology · doi:10.1002/hep.21887 · Cited by 51 · see citing works
Sugiyama, Y., Takabe, Y., Nakakura, T., Tanaka, S., Koike, T., & Shiojiri, N. (2009) · Developmental Dynamics · doi:10.1002/dvdy.22162 · Cited by 34 · see citing works
Significance of portal venous flow in graft regeneration after living related liver transplantation
Kato, Y., Shimazu, M., Wakabayashi, G., Tanabe, M., Morikawa, Y., Hoshino, K., Harada, H., Kadomura, T., Obara, H., Urakami, H., et al. (2001) · Transplantation Proceedings · doi:10.1016/s0041-1345(00)02562-8 · Cited by 33 · see citing works
Self-citationXu, H., Shi, B., Lü, X., Liang, F., Jin, X., Tai-huang, W., & Xu, J. (2008) · World Journal of Gastroenterology · doi:10.3748/wjg.14.2349 · Cited by 27 · see citing works
Growth of Animal Tissue Cells on Three-Dimensional Substrates
Earle, W. R., Schilling, E. L., & Shannon, J. E. (1951) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/12.1.179 · Cited by 22 · see citing works
Laminin expression during bone marrow mononuclear cell transplantation in hepatectomized rats
de Carvalho, S. N., Cortez, E. A. C., Stumbo, A. C., Thole, A. A., Caetano, C., Marques, R. G., Pelajo‐Machado, M., Pôrto, L. C., & de Carvalho, L. (2008) · Cell Biology International · doi:10.1016/j.cellbi.2008.04.003 · Cited by 8 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
A review of cellularization strategies for tissue engineering of whole organs
Scarritt, M. E. (2015) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2015.00043 · Cited by 234 · see citing works
Naturally-Derived Biomaterials for Tissue Engineering Applications
Brovold, M., Almeida, J. I., Plá-Palacín, I., Sainz‐Arnal, P., Sánchez‐Romero, N., Rivas, J. J., Almeida, H., Dachary, P. R., Serrano, T., Söker, S., et al. (2018) · Advances in experimental medicine and biology · doi:10.1007/978-981-13-0947-2_23 · Cited by 163 · see citing works
In Vivo Performance of Decellularized Vascular Grafts: A Review Article
Lin, C., Hsia, K., Ma, H., Lee, H., & Lu, J. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19072101 · Cited by 154 · see citing works
The multiple functional roles of mesenchymal stem cells in participating in treating liver diseases
Liu, W., Song, F., Ren, L., Guo, W., Wang, T., Feng, Y., Tang, L., & Li, K. (2015) · Journal of Cellular and Molecular Medicine · doi:10.1111/jcmm.12482 · Cited by 139 · see citing works
Liver tissue engineering: From implantable tissue to whole organ engineering
Mazza, G., Al‐Akkad, W., Rombouts, K., & Pinzani, M. (2017) · Hepatology Communications · doi:10.1002/hep4.1136 · Cited by 127 · see citing works
Heterotopic transplantation of a decellularized and recellularized whole porcine heart
Kitahara, H., Yagi, H., Tajima, K., Okamoto, K., Yoshitake, A., Aeba, R., Kudo, M., Kashima, I., Kawaguchi, S., Hirano, A., et al. (2016) · Interactive Cardiovascular and Thoracic Surgery · doi:10.1093/icvts/ivw022 · Cited by 97 · see citing works
Self-citationNakamura, N., Kimura, T., & Kishida, A. (2016) · ACS Biomaterials Science & Engineering · doi:10.1021/acsbiomaterials.6b00506 · Cited by 96 · see citing works
The Therapeutic Promise of Mesenchymal Stem Cells for Liver Restoration
Christ, B., Brückner, S., & Winkler, S. (2015) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2015.09.004 · Cited by 74 · see citing works
Whole Organ Tissue Vascularization: Engineering the Tree to Develop the Fruits
Pellegata, A. F., Tedeschi, A., & Coppi, P. D. (2018) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2018.00056 · Cited by 68 · see citing works
Kojima, H., Yasuchika, K., Fukumitsu, K., Ishii, T., Ogiso, S., Miyauchi, Y., Yamaoka, R., Kawai, T., Katayama, H., Yoshitoshi-Uebayashi, E. Y., et al. (2018) · American Journal of Transplantation · doi:10.1111/ajt.14666 · Cited by 60 · see citing works
A Hepatic Scaffold from Decellularized Liver Tissue: Food for Thought
Croce, S., Peloso, A., Zoro, T., Avanzini, M. A., & Cobianchi, L. (2019) · Biomolecules · doi:10.3390/biom9120813 · Cited by 58 · see citing works
Endocrine pancreas engineered using porcine islets and partial pancreatic scaffolds
Katsuki, Y., Yagi, H., Okitsu, T., Kitago, M., Tajima, K., Kadota, Y., Hibi, T., Abe, Y., Shinoda, M., Itano, O., et al. (2016) · Pancreatology · doi:10.1016/j.pan.2016.06.007 · Cited by 46 · see citing works
Self-citationHussein, K. H., Park, K.-M., Yu, L., Song, S.-H., Woo, H.-M., & Kwak, H.-H. (2020) · Acta Biomaterialia · doi:10.1016/j.actbio.2019.12.029 · Cited by 44 · see citing works
Advances in Hepatic Tissue Bioengineering with Decellularized Liver Bioscaffold
Rossi, E. A., Quintanilha, L. F., Nonaka, C. K. V., & Souza, B. S. D. F. (2019) · Stem Cells International · doi:10.1155/2019/2693189 · Cited by 42 · see citing works
Medical 3D Printing: Tools and Techniques, Today and Tomorrow
Willson, K., & Atala, A. (2022) · Annual Review of Chemical and Biomolecular Engineering · doi:10.1146/annurev-chembioeng-092220-015404 · Cited by 41 · see citing works
Jin, S., Li, H., Mingzi, H., Ruan, M., Liu, Z., Zhang, F., Zhang, C., Choi, Y., & Liu, B. (2016) · Cellular Physiology and Biochemistry · doi:10.1159/000453166 · Cited by 39 · see citing works
Construction of sinusoid-scale microvessels in perfusion culture of a decellularized liver
Watanabe, M., Yano, K., Okawa, K., Yamashita, T., Tajima, K., Sawada, K., Yagi, H., Kitagawa, Y., Tanishita, K., & Sudo, R. (2019) · Acta Biomaterialia · doi:10.1016/j.actbio.2018.12.042 · Cited by 38 · see citing works
Self-citationRecent Advances in Decellularization and Recellularization for Tissue-Engineered Liver Grafts
Wang, Y., Nicolas, C. T., Chen, H. S., Ross, J. J., Lorenzo, S. B. D., & Nyberg, S. L. (2016) · Cells Tissues Organs · doi:10.1159/000452761 · Cited by 36 · 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
Recent Advances in Decellularization and Recellularization for Tissue-Engineered Liver Grafts
Wang, Y., Nicolas, C. T., Chen, H. S., Ross, J. J., Lorenzo, S. B. D., & Nyberg, S. L. (2017) · Cells Tissues Organs · doi:10.1159/000479597 · Cited by 33 · see citing works
New Perspectives in Liver Transplantation: From Regeneration to Bioengineering
Bizzaro, D., Russo, F. P., & Burra, P. (2019) · Bioengineering · doi:10.3390/bioengineering6030081 · Cited by 32 · see citing works
Prevascularization of Decellularized Porcine Myocardial Slice for Cardiac Tissue Engineering
Kc, P., Shah, M., Liao, J., & Zhang, G. (2016) · ACS Applied Materials & Interfaces · doi:10.1021/acsami.6b15291 · Cited by 30 · see citing works
Raasch, M., Fritsche, E., Kurtz, A., Bauer, M. W., & Mosig, A. S. (2018) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2018.06.008 · Cited by 30 · see citing works
Winkler, S., Hempel, M., Brückner, S., Tautenhahn, H., Kaufmann, R., & Christ, B. (2016) · International Journal of Molecular Sciences · doi:10.3390/ijms17071099 · Cited by 28 · 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
“Hence, enzymatic treatment, particularly involving nucleases and trypsin, is often combined with chemical detergents followed by various washing cycles for liver decellularization [110,123, 149,150].”
BackgroundEvolution of graft morphology and function after recellularization of decellularized rat livers
Butter, A., Aliyev, K., Hillebrandt, K. H., Raschzok, N., Kluge, M., Seiffert, N., Tang, P., Napierala, H., Muhamma, A. I., Reutzel‐Selke, A., et al. (2016) · Journal of Tissue Engineering and Regenerative Medicine · doi:10.1002/term.2383 · Cited by 24 · see citing works
Asadi, M., Khalili, M., Lotfi, H., Moghaddam, S. V., Zarghami, N., André, H., & Alizadeh, E. (2021) · Life Sciences · doi:10.1016/j.lfs.2021.119373 · Cited by 22 · see citing works
An organ-derived extracellular matrix triggers in situ kidney regeneration in a preclinical model
Tajima, K., Yagi, H., Morisaku, T., Nishi, K., Kushige, H., Kojima, H., Higashi, H., Kuroda, K., Kitago, M., Adachi, S., et al. (2022) · npj Regenerative Medicine · doi:10.1038/s41536-022-00213-y · Cited by 20 · see citing works
Self-citationPapanikolaou, I. G., Katselis, C., Apostolou, K. G., Feretis, T., Lymperi, M., Konstadoulakis, M. M., Papalois, A. E., & Zografos, G. (2017) · Stem Cells International · doi:10.1155/2017/7567958 · Cited by 20 · see citing works
Current status of stem cell therapy: opportunities and limitations
Rusu, E. E., Necula, L. G., Neagu, A. I., Alecu, M., Stan, C., Albulescu, R., & Tănase, C. (2016) · TURKISH JOURNAL OF BIOLOGY · doi:10.3906/biy-1506-95 · Cited by 18 · see citing works
The Crosstalk between Mesenchymal Stromal/Stem Cells and Hepatocytes in Homeostasis and under Stress
Kholodenko, I. V., Kholodenko, R. V., & Yarygin, K. N. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms242015212 · Cited by 16 · see citing works
Singh, G., Senapati, S., Satpathi, S., Behera, P. K., Das, B., & Nayak, B. (2022) · The FASEB Journal · doi:10.1096/fj.202200807r · Cited by 15 · see citing works
Furuta, T., Furuya, K., Zheng, Y., & Oda, T. (2020) · World Journal of Transplantation · doi:10.5500/wjt.v10.i3.64 · Cited by 14 · see citing works
Kojima, H., Yagi, H., Kushige, H., Toda, Y., Takayama, K., Masuda, S., Morisaku, T., Tsuchida, T., Kuroda, K., Hirukawa, K., et al. (2022) · Cells · doi:10.3390/cells11081258 · Cited by 13 · see citing works
Self-citationMontanari, E., Pimenta, J., Szabó, L., Noverraz, F., Passemard, S., Meier, R. P. H., Meyer, J., Sidibé, J., Thomas, A., Schuurman, H., et al. (2018) · Journal of Immunology Research · doi:10.1155/2018/1078547 · Cited by 12 · see citing works
Human-Scale Liver Harvest and Decellularization for Preclinical Research
Tajima, K., Yagi, H., & Kitagawa, Y. (2018) · Methods in molecular biology · doi:10.1007/7651_2018_195 · Cited by 11 · see citing works
Self-citationShimada, T., Tsuruta, M., Hasegawa, H., Okabayashi, K., Shigeta, K., Ishida, T., Asada, Y., Suzumura, H., Koishikawa, K., Akimoto, S., et al. (2018) · Oncology Reports · doi:10.3892/or.2018.6180 · Cited by 11 · see citing works
Self-citationRecent advances in re-engineered liver: de-cellularization and re-cellularization techniques
Wang, L., Lin, Y.-Q., Wang, J., Pan, L., Huang, K., Wan, L., Zhu, G., Liu, W., Braddock, M., & Zheng, M. (2015) · Cytotherapy · doi:10.1016/j.jcyt.2015.04.003 · Cited by 10 · see citing works
Kalinin, E. V., Chalenko, Y. M., Владимировна, С. Е., Midiber, K. Y., Gusarov, A., Kechko, O. I., Kulikova, A. A., Михалева, Л. М., Mukhachev, A. Y., Станишевский, Я. М., et al. (2020) · Drug Development Research · doi:10.1002/ddr.21737 · Cited by 10 · see citing works
Wnt ligands 3a and 5a regulate proliferation and migration in human fetal liver progenitor cells
Liu, Z., Kuna, V. K., Xu, B., & Sumitran–Holgersson, S. (2021) · Translational Gastroenterology and Hepatology · doi:10.21037/tgh.2020.01.12 · Cited by 9 · see citing works
New advances in liver decellularization and recellularization: innovative and critical technologies
Lin, Y.-Q., Wang, L., Wang, J., Pan, L., Zhu, G., Liu, W., Braddock, M., & Zheng, M. (2015) · Expert Review of Gastroenterology & Hepatology · doi:10.1586/17474124.2015.1058155 · Cited by 8 · see citing works
Redko, O., Dovgalyuk, A., Довбуш, А. В., Небесна, З. М., Yakubyshyna, L. V., & Krynytska, І. (2021) · Cell and Organ Transplantology · doi:10.22494/cot.v9i2.130 · Cited by 8 · see citing works
Bioengineering of vascularized porcine flaps using perfusion-recellularization
Xu, M. S., D’Elia, A., Hadžimustafić, N., Adil, A., Karoubi, G., Waddell, T. K., & Haykal, S. (2024) · Scientific Reports · doi:10.1038/s41598-024-58095-7 · Cited by 7 · see citing works
Artificial liver research output and citations from 2004 to 2017: a bibliometric analysis
Li, Y., He, M., Zou, Z., Bian, X., Huang, X., Yang, C., Wei, S., & Dai, S. (2019) · PeerJ · doi:10.7717/peerj.6178 · Cited by 7 · see citing works
Liver Scaffolds Support Survival and Metabolic Function of Multilineage Neonatal Allogenic Cells
Hassanein, W., Cimeno, A., Werdesheim, A., Buckingham, B., Harrison, J., Uluer, M. C., Khalifeh, A., Rivera-Pratt, C., Klepfer, S., Woodall, J. D., et al. (2017) · Tissue Engineering Part A · doi:10.1089/ten.tea.2017.0279 · Cited by 6 · see citing works
Zhao, Y., Xu, B., Liang, W., Ding, Y., Li, J., Zhang, Y., Xu, F., Zhou, H., & Xu, Y. (2019) · Tissue Engineering Part A · doi:10.1089/ten.tea.2018.0107 · Cited by 5 · see citing works
Tissue-Engineered Hepatocyte Sheets Supplemented with Adipose-Derived Stem Cells
Suzushino, S., Sato, N., Ishigame, T., Okada, R., Kofunato, Y., Watanabe, J., Muto, M., Tsukida, S., Nishimagi, A., Kimura, T., et al. (2023) · Tissue Engineering Part A · doi:10.1089/ten.tea.2022.0197 · Cited by 4 · see citing works
Harper, S., Hoff, M., Skepper, J. N., Davies, S. E., & Huguet, E. (2020) · Journal of Tissue Engineering and Regenerative Medicine · doi:10.1002/term.3117 · Cited by 4 · see citing works
Bioengineering Liver Transplantation
van der Laan, L. J. W., Spee, B., & Verstegen, M. M. A. (2019) · MDPI eBooks · doi:10.3390/books978-3-03921-745-8 · Cited by 1 · see citing works
Goh, S. K. (2015) · D-Scholarship@Pitt (University of Pittsburgh)
Clinical Aspects of Regenerative Medicine
Szilagyi, E., Sundivakkam, P., Nunez, T., Premenand, K., Kenyon, N. S., & Bartholomew, A. M. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-410396-2.00037-2
Engenharia tecidual hepática utilizando células tronco pluripotentes induzidas
Guimarães, E. D. S. G. (2019) · doi:10.11606/t.41.2019.tde-27082019-093823
Decellularized liver extracellular matrix for iPSC-based liver engineering
Acun, A., & Uygun, B. E. (2021) · Elsevier eBooks · doi:10.1016/b978-0-323-85766-6.00006-1
A review on decellularization scaffolding for liver regeneration in transplantation
Liu, Y., Liu, S.-Y., Chung, W.-Y., Bowrey, D. J., & Huang, K.-W. (2026) · Hepatoma Research · doi:10.20517/2394-5079.2026.09
- Authors
- Kadota, Y., Yagi, H., Inomata, K., Matsubara, K., Hibi, T., Abe, Y., Kitago, M., Shinoda, M., Obara, H., Itano, O., & Kitagawa, Y.
- Affiliations
- Keio University (JP)
- Corresponding author
- Yagi, Hiroshi
- ORCID
- Venue
- Organogenesis
- Publisher
- Informa UK Limited
- Published
- 2014-01-31
- Volume
- 10
- Issue
- 2
- Pages
- 268-277
- ISSN
- 1547-6278 (ISSN-L)
- 1555-8592
- PMC
- PMC4154962
- OpenAlex
- W2142076588
- Cited by
- 58
- References
- 50
- Citations by year
- 2026: 1 · 2024: 2 · 2023: 2 · 2022: 4 · 2021: 4 · 2020: 3 · 2019: 12 · 2018: 9 · 2017: 4 · 2016: 10 · 2015: 5 · 2014: 2
- FWCI
- 6.95
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Organogenesis (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Takeda Science Foundation
- Research Center Network for Realization of Regenerative Medicine
- Keio University
- Japan Society for the Promotion of Science (23689059)
- Japan Science and Technology Agency
- Topics
- Health Sciences › Medicine › Surgery › Tissue Engineering and Regenerative Medicine
- Health Sciences › Medicine › Genetics › Mesenchymal stem cell research
- Physical Sciences › Engineering › Biomedical Engineering › 3D Printing in Biomedical Research
- Keywords
- mesenchymal stem cells, hepatocyte function, bone marrow-derived stem cells, artificial liver, liver regeneration, paracrine signaling, co-culture, adhesion molecules, angiogenic factors, cell storage
- MeSH terms
- Animals, Cell Count, Female, Liver, Rats, Inbred Lew, Cell Adhesion Molecules, Liver Transplantation, Hepatocytes, Tissue Engineering, Angiogenesis Inducing Agents, Tissue Scaffolds, Mesenchymal Stem Cells
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 ›
Are you an author, or do you see a problem with this page? Request a review