CD24-Positive Cells from Normal Adult Mouse Liver Are Hepatocyte Progenitor Cells
Open accessAbstract
The identification of specific cell surface markers that can be used to isolate liver progenitor cells will greatly facilitate experimentation to determine the role of these cells in liver regeneration and their potential for therapeutic transplantation. Previously, the cell surface marker, CD24, was observed to be expressed on undifferentiated bipotential mouse embryonic liver stem cells and 3,5-diethoxycarbonyl-1,4-dihydrocollidine-induced oval cells. Here, we describe the isolation and characterization of a rare, primary, nonhematopoietic, CD24+ progenitor cell population from normal, untreated mouse liver. By immunohistochemistry, CD24-expressing cells in normal adult mouse liver were colocalized with CK19-positive cholangiocytes. This nonhematopoietic (CD45-, Ter119-) CD24+ cell population isolated by flow cytometry represented 0.04% of liver cells and expressed several markers of liver progenitor/oval cells. The immunophenotype of nonhematopoietic CD24+ cells was CD133, Dlk, and Sca-1 high, but c-Kit, Thy-1, and CD34 low. The CD24+ cells had increased expression of CK19, epithelial cell adhesion molecule, Sox 9, and FN14 compared with the unsorted cells. Upon transplantation of nonhematopoietic CD24+ cells under the sub-capsule of the livers of Fah knockout mice, cells differentiated into mature functional hepatocytes. Analysis of X and Y chromosome complements were used to determine whether or not fusion of the engrafted cells with the recipient hepatocytes occurred. No cells were found that contained XXXY or any other combination of donor and host sex chromosomes as would be expected if cell fusion had occurred. These results suggested that CD24 can be used as a cell surface marker for isolation of hepatocyte progenitor cells from normal adult liver that are able to differentiate into hepatocytes.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
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?
Earlier FACS-based isolations of putative HPCs relied on a single selection marker or failed to fully exclude other non-parenchymal cell populations.
“Although previous studies have isolated putative HPCs using FACS isolation, these techniques are based on single selection markers37,8 or did not completely exclude other NPC populations37,52.”
From Hepatic progenitor cells of biliary origin with liver repopulation capacity (2015) · cites this paper as [37]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Isolation and functional properties of murine hematopoietic stem cells that are replicating in vivo.
Goodell, M. A., Brose, K., Paradis, G. A., Conner, A. N., & Mulligan, R. C. (1996) · The Journal of Experimental Medicine · doi:10.1084/jem.183.4.1797 · Cited by 2,902 · see citing works
Fusion of bone-marrow-derived cells with Purkinje neurons, cardiomyocytes and hepatocytes
Álvarez‐Dolado, M., Pardal, R., García‐Verdugo, J. M., Fike, J. R., Lee, H. O., Pfeffer, K., Lois, C., Morrison, S. J., & Álvarez-Buylla, A. (2003) · Nature · doi:10.1038/nature02069 · Cited by 1,617 · see citing works
Cell fusion is the principal source of bone-marrow-derived hepatocytes
Wang, X., Willenbring, H., Akkari, Y. M. N., Torimaru, Y., Foster, M., Al-Dhalimy, M., Lagasse, E., Finegold, M. J., Olson, S. B., & Grompe, M. (2003) · Nature · doi:10.1038/nature01531 · Cited by 1,569 · see citing works
Transplanted bone marrow regenerates liver by cell fusion
Vassilopoulos, G., Wang, P.-R., & Russell, D. W. (2003) · Nature · doi:10.1038/nature01539 · Cited by 1,282 · see citing works
The role of hepatocytes and oval cells in liver regeneration and repopulation
Fausto, N., & Campbell, J. S. (2002) · Mechanisms of Development · doi:10.1016/s0925-4773(02)00338-6 · Cited by 646 · see citing works
Human hepatic stem cells from fetal and postnatal donors
Schmelzer, E., Zhang, L., Bruce, A., Wauthier, E., Ludlow, J. W., Yao, H.-L., Moss, N., Melhem, A., McClelland, R., Turner, W. S., et al. (2007) · The Journal of Experimental Medicine · doi:10.1084/jem.20061603 · Cited by 585 · see citing works
TWEAK induces liver progenitor cell proliferation
Jakubowski, A., Ambrose, C., Parr, M., Lincecum, J. M., Wang, M. Z., Zheng, T. S., Browning, B., Michaelson, J. S., Baestcher, M., Wang, B., et al. (2005) · Journal of Clinical Investigation · doi:10.1172/jci23486 · Cited by 419 · see citing works
Isolation and Characterization of a Stem Cell Population from Adult Human Liver
Sanchez, M. B. H., Bruno, S., Buttiglieri, S., Tetta, C., Gatti, S., Deregibus, M. C., Bussolati, B., & Camussi, G. (2006) · Stem Cells · doi:10.1634/stemcells.2006-0114 · Cited by 411 · see citing works
The origin and liver repopulating capacity of murine oval cells
Wang, X., Foster, M., Al-Dhalimy, M., Lagasse, E., Finegold, M., & Grompe, M. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1734199100 · Cited by 410 · see citing works
Myelomonocytic cells are sufficient for therapeutic cell fusion in liver
Willenbring, H., Bailey, A. S., Foster, M., Akkari, Y. M. N., Dorrell, C., Olson, S. B., Finegold, M. J., Fleming, W., & Grompe, M. (2004) · Nature Medicine · doi:10.1038/nm1062 · Cited by 386 · 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
Isolation of hepatoblasts based on the expression of Dlk/Pref-1
Tanimizu, N., Nishikawa, M., Saito, H., Tsujimura, T., & Miyajima, A. (2003) · Journal of Cell Science · doi:10.1242/jcs.00388 · Cited by 335 · see citing works
Oyama, T., Nagai, T., Wada, H., Naito, A. T., Matsuura, K., Iwanaga, K., Takahashi, T., Goto, M., Mikami, Y., Yasuda, N., et al. (2007) · The Journal of Cell Biology · doi:10.1083/jcb.200603014 · Cited by 325 · see citing works
Origin and Structural Evolution of the Early Proliferating Oval Cells in Rat Liver
Paku, S., Schnur, J., Nagy, P., & Thorgeirsson, S. S. (2001) · American Journal Of Pathology · doi:10.1016/s0002-9440(10)64082-5 · Cited by 286 · see citing works
Wolf, N. S., Koné, A., Priestley, G. V., & Bartelmez, S. (1993) · PubMed · Cited by 257 · see citing works
Hematopoietic myelomonocytic cells are the major source of hepatocyte fusion partners
Camargo, F. D., Finegold, M. J., & Goodell, M. A. (2004) · Journal of Clinical Investigation · doi:10.1172/jci21301 · Cited by 246 · see citing works
Identification of adult hepatic progenitor cells capable of repopulating injured rat liver
Yovchev, M. I., Grozdanov, P. N., Zhou, H., Racherla, H., Guha, C., & Dabeva, M. D. (2007) · Hepatology · doi:10.1002/hep.22047 · Cited by 241 · see citing works
Human hepatic stem-like cells isolated using c-kit or CD34 can differentiate into biliary epithelium
Crosby, H. A., Kelly, D. A., & Strain, A. J. (2001) · Gastroenterology · doi:10.1053/gast.2001.21175 · Cited by 241 · see citing works
Mouse A6-Positive Hepatic Oval Cells Also Express Several Hematopoietic Stem Cell Markers
Petersen, B. E., Grossbard, B. L., Hatch, H. M., Pi, L., Deng, J., & Scott, E. W. (2003) · Hepatology · doi:10.1053/jhep.2003.50104 · Cited by 237 · see citing works
CD133+ hepatic stellate cells are progenitor cells
Kordes, C., Sawitza, I., Müller-Marbach, A., Ale‐Agha, N., Keitel, V., Klonowski-Stumpe, H., & Häussinger, D. (2006) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2006.11.029 · Cited by 224 · see citing works
Petersen, B. E., Zajac, V. F., & Michalopoulos, G. K. (1998) · Hepatology · doi:10.1002/hep.510270419 · Cited by 203 · see citing works
Fate-Mapping Evidence That Hepatic Stellate Cells Are Epithelial Progenitors in Adult Mouse Livers
Yang, L., Jung, Y., Omenetti, A., Witek, R. P., Choi, S. S., VanDongen, H. M. A., Huang, J., Alpini, G. D., & Diehl, A. M. (2008) · Stem Cells · doi:10.1634/stemcells.2008-0115 · Cited by 200 · see citing works
Shimano, K., Satake, M., Okaya, A., Kitanaka, J., Kitanaka, N., Takemura, M., Sakagami, M., Terada, N., & Tsujimura, T. (2003) · American Journal Of Pathology · doi:10.1016/s0002-9440(10)63624-3 · Cited by 195 · see citing works
Novel hepatic progenitor cell surface markers in the adult rat liver
Yovchev, M. I., Grozdanov, P. N., Joseph, B., Gupta, S. K., & Dabeva, M. D. (2006) · Hepatology · doi:10.1002/hep.21448 · Cited by 171 · see citing works
Generation of hepatocytes from oval cell precursors in culture.
Lázaro, C. A., Rhim, J. A., Yamada, Y., & Fausto, N. (1998) · PubMed · Cited by 170 · see citing works
Suzuki, A., Sekiya, S., Onishi, M., Oshima, N., Kiyonari, H., Nakauchi, H., & Taniguchi, H. (2008) · Hepatology · doi:10.1002/hep.22558 · Cited by 167 · see citing works
Jensen, C. H., Jauho, E. I., Santoni‐Rugiu, E., Holmskov, U., Teisner, B., Tygstrup, N., & Bisgaard, H. C. (2004) · American Journal Of Pathology · doi:10.1016/s0002-9440(10)63221-x · Cited by 144 · see citing works
A CD133-Expressing Murine Liver Oval Cell Population with Bilineage Potential
Rountree, C. B., Barsky, L. W., Ge, S., Zhu, J., Senadheera, S., & Crooks, G. M. (2007) · Stem Cells · doi:10.1634/stemcells.2007-0176 · Cited by 141 · see citing works
A simplified method for enrichment of mouse hematopoietic stem cells.
Spangrude, G. J., & Scollay, R. G. (1990) · PubMed · Cited by 128 · see citing works
Tirnitz‐Parker, J. E. E., Tonkin, J. N., Knight, B., Olynyk, J. K., & Yeoh, G. C. (2007) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2007.06.008 · Cited by 103 · see citing works
mCD24 expression in the developing mouse brain and in zones of secondary neurogenesis in the adult
Calaora, V., Chazal, G., Nielsen, P. J., Rougon, G. N., & Moreau, H. (1996) · Neuroscience · doi:10.1016/0306-4522(96)00042-5 · Cited by 103 · see citing works
Surface markers for the murine oval cell response†
Dorrell, C., Erker, L. R., Lanxon-Cookson, K. M., Abraham, S. L., Victoroff, T. M., Ro, S. W., Canaday, P. S., Streeter, P. R., & Grompe, M. (2008) · Hepatology · doi:10.1002/hep.22468 · Cited by 95 · see citing works
Redvers, R. P., Li, A., & Kaur, P. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0602579103 · Cited by 87 · see citing works
Isolation and Characterization of Bipotent Liver Progenitor Cells from Adult Mouse
Li, W., Su, J., Yao, Y., Tao, X., Yan, Y.-B., Yu, H.-Y., Wang, X., Li, J., Yang, Y., Lau, J. T. Y., et al. (2005) · Stem Cells · doi:10.1634/stemcells.2005-0108 · Cited by 74 · see citing works
Dezső, K., Jelnes, P., László, V., Baghy, K., Bödör, C., Paku, S., Tygstrup, N., Bisgaard, H. C., & Nagy, P. (2007) · American Journal Of Pathology · doi:10.2353/ajpath.2007.070273 · Cited by 74 · see citing works
Molecular and functional properties of lung SP cells
Reynolds, S. D., Shen, H., Reynolds, P. R., Betsuyaku, T., Pilewski, J. M., Gambelli, F., DeGuiseppe, M., Ortiz, L. A., & Stripp, B. R. (2006) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.00090.2006 · Cited by 63 · see citing works
Nierhoff, D., LeVoci, L., Schulte, S., Goeser, T., Rogler, L. E., & Shafritz, D. A. (2007) · Hepatology · doi:10.1002/hep.21721 · Cited by 45 · see citing works
Isolation and characterization of a murine resident liver stem cell
Conigliaro, A., Colletti, M., Cicchini, C., Guerra, M. T., Manfredini, R., Zini, R., Bordoni, V., Siepi, F., Leopizzi, M., Tripodi, M., et al. (2007) · Cell Death and Differentiation · doi:10.1038/sj.cdd.4402236 · Cited by 36 · see citing works
Ochsner, S. A., Strick‐Marchand, H., Qiu, Q., Venable, S. F., Dean, A. M., Wilde, M. D., Weiss, M. C., & Darlington, G. (2007) · Stem Cells · doi:10.1634/stemcells.2007-0101 · Cited by 33 · see citing works
Self-citationEnrichment of a bipotent hepatic progenitor cell from naïve adult liver tissue
Wright, N., Samuelson, L., Walkup, M. H., Chandrasekaran, P., & Gerber, D. A. (2007) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2007.11.129 · Cited by 32 · see citing works
Monoclonal side population progenitors isolated from human fetal pancreas
Zhang, L., Hu, J., Hong, T., Liu, Y.-N., Wu, Y., & Li, L. (2005) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2005.05.111 · Cited by 30 · see citing works
Tsuchiya, A., Heike, T., Baba, S., Fujino, H., Umeda, K., Matsuda, Y., Nomoto, M., Ichida, T., Aoyagi, Y., & Nakahata, T. (2007) · Stem Cells · doi:10.1634/stemcells.2006-0558 · Cited by 28 · see citing works
Hematopoietic myelomonocytic cells are the major source of hepatocyte fusion partners
Camargo, F. D., Finegold, M. J., & Goodell, M. A. (2004) · Journal of Clinical Investigation · doi:10.1172/jci200421301 · Cited by 24 · see citing works
Mouse CD24 is required for homeostatic cell renewal
Nieoullon, V., Belvindrah, R., Rougon, G. N., & Chazal, G. (2007) · Cell and Tissue Research · doi:10.1007/s00441-007-0395-5 · Cited by 23 · see citing works
Testis development in a mouse with 10% of XY cells
Singh, L., Matsukuma, S., & Jones, K. W. (1987) · Developmental Biology · doi:10.1016/0012-1606(87)90353-8 · Cited by 23 · see citing works
Establishment and Characterization of Hepatic Stem-like Cell lines from Normal Adult Rat Liver
Hirata, M., Amano, K., Miyashita, A., Yasunaga, M., Nakanishi, T., & Sato, K. (2008) · The Journal of Biochemistry · doi:10.1093/jb/mvn146 · Cited by 14 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Stem/progenitor cells in liver development, homeostasis, regeneration, and reprogramming
Miyajima, A., Tanaka, M., & Itoh, T. (2014) · Cell Stem Cell · doi:10.1016/j.stem.2014.04.010 · Cited by 570 · see citing works
Cancer stem cells in the development of liver cancer
Yamashita, T., & Wang, X. W. (2013) · Journal of Clinical Investigation · doi:10.1172/jci66024 · Cited by 526 · see citing works
Hepatic progenitor cells of biliary origin with liver repopulation capacity
Lu, W.-Y., Bird, T. G., Boulter, L., Tsuchiya, A., Cole, A. M., Hay, T., Guest, R. V., Wojtacha, D., Man, T. Y., Mackinnon, A., et al. (2015) · Nature Cell Biology · doi:10.1038/ncb3203 · Cited by 479 · see citing works
Ductular reaction in liver diseases: pathological mechanisms and translational significances
Sato, K., Marzioni, M., Meng, F., Francis, H., Glaser, S., & Alpini, G. (2019) · Hepatology · doi:10.1002/hep.30150 · Cited by 423 · see citing works
Orchestrating liver development
Gordillo, M., Evans, T., & Gouon-Evans, V. (2015) · Development · doi:10.1242/dev.114215 · Cited by 375 · see citing works
Guha, P., Morgan, J. W., Mostoslavsky, G., Rodrigues, N. P., & Boyd, A. S. (2013) · Cell stem cell · doi:10.1016/j.stem.2013.01.006 · Cited by 368 · see citing works
The evolving concept of liver cancer stem cells
Nio, K., Yamashita, T., & Kaneko, S. (2017) · Molecular Cancer · doi:10.1186/s12943-016-0572-9 · Cited by 271 · see citing works
Cancer Stem Cell Functions in Hepatocellular Carcinoma and Comprehensive Therapeutic Strategies
Liu, Y., Yeh, C., & Lin, K. (2020) · Cells · doi:10.3390/cells9061331 · Cited by 254 · see citing works
Conversion of Stem Cells to Cancer Stem Cells: Undercurrent of Cancer Initiation
Afify, S. M., & Seno, M. (2019) · Cancers · doi:10.3390/cancers11030345 · Cited by 151 · see citing works
Myofibroblastic cells function as progenitors to regenerate murine livers after partial hepatectomy
Swiderska-Syn, M., Syn, W. K., Xie, G., Krüger, L., Machado, M. V., Karaca, G., Michelotti, G. A., Choi, S. S., Premont, R. T., & Diehl, A. M. (2014) · Gut · doi:10.1136/gutjnl-2013-305962 · Cited by 115 · see citing works
Temporal analyses of postnatal liver development and maturation by single-cell transcriptomics
Liang, Y., Kaneko, K., Xin, B., Lee, J., Sun, X., Zhang, K., & Feng, G.-S. (2022) · Developmental Cell · doi:10.1016/j.devcel.2022.01.004 · Cited by 116 · see citing works
Inflammation-Induced Hepatocellular Carcinoma Is Dependent on Ccr5 in Mice
Barashi, N., Weiss, I. D., Wald, O., Wald, H., Beider, K., Abraham, M., Klein, S., Goldenberg, D., Axelrod, J. H., Pikarsky, E., et al. (2013) · Hepatology · doi:10.1002/hep.26403 · Cited by 77 · see citing works
Ling, L., Camilleri, E. T., Helledie, T., Samsonraj, R. M., Titmarsh, D. M., Chua, R. J. E., Dreesen, O., Dombrowski, C., Rider, D. A., Galindo, M. A., et al. (2015) · Gene · doi:10.1016/j.gene.2015.10.039 · Cited by 76 · see citing works
A novel model of liver cancer stem cells developed from induced pluripotent stem cells
Afify, S. M., Calle, A. S., Hassan, G., Kumon, K., Nawara, H. M., Zahra, M. H., Mansour, H. M., Khayrani, A. C., Alam, M. J., Du, J., et al. (2020) · British Journal of Cancer · doi:10.1038/s41416-020-0792-z · Cited by 69 · see citing works
Rodrigues‐Pinto, R., Berry, A. A., Hanley, K. P., Hanley, N. A., Richardson, S. M., & Hoyland, J. A. (2016) · Journal of Orthopaedic Research® · doi:10.1002/jor.23205 · Cited by 68 · see citing works
Successful Isolation of Liver Progenitor Cells by Aldehyde Dehydrogenase Activity in Na"ve Mice
Dollé, L., Best, J., Empsen, C., Mei, J., Rossen, E. V., Roelandt, P. R., Snykers, S., Najimi, M., Battah, F. A., Theise, N. D., et al. (2011) · Hepatology · doi:10.1002/hep.24693 · Cited by 58 · see citing works
Rizvi, F., Lee, Y., Díaz‐Aragon, R., Bawa, P., So, J., Florentino, R. M., Wu, S. Y., Sarjoo, A., Truong, E., Smith, A. R., et al. (2023) · Cell stem cell · doi:10.1016/j.stem.2023.10.008 · Cited by 59 · see citing works
The role of liver progenitor cells during liver regeneration, fibrogenesis, and carcinogenesis
Köhn‐Gaone, J., Gogoi-Tiwari, J., Ramm, G. A., Olynyk, J. K., & Tirnitz‐Parker, J. E. E. (2015) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00215.2015 · Cited by 57 · see citing works
Road to stemness in hepatocellular carcinoma
Flores-Téllez, T. D. N. J., Villa‐Treviño, S., & Piña‐Vázquez, C. (2017) · World Journal of Gastroenterology · doi:10.3748/wjg.v23.i37.6750 · Cited by 51 · see citing works
The plastic cellular states of liver cells: Are EpCAM and Lgr5 fit for purpose?
Huch, M., & Dollé, L. (2016) · Hepatology · doi:10.1002/hep.28469 · Cited by 48 · see citing works
Involvement of inflammation and its related microRNAs in hepatocellular carcinoma
Jin, K., Li, T., Sánchez‐Duffhues, G., Zhou, F., & Zhang, L. (2016) · Oncotarget · doi:10.18632/oncotarget.13530 · Cited by 47 · see citing works
Re-evaluation of liver stem/progenitor cells
Tanimizu, N., & Mitaka, T. (2014) · Organogenesis · doi:10.4161/org.27591 · Cited by 46 · see citing works
The Origin, Biology, and Therapeutic Potential of Facultative Adult Hepatic Progenitor Cells
Shin, S., & Kaestner, K. H. (2014) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/b978-0-12-416022-4.00010-x · Cited by 45 · see citing works
Orchestration of hepatocellular carcinoma development by diverse liver cancer stem cells
Yamashita, T., & Kaneko, S. (2014) · Journal of Gastroenterology · doi:10.1007/s00535-014-0951-1 · Cited by 45 · see citing works
Zhao, H., Ling, Y., He, J., Dong, J., Mo, Q., Wang, Y., Zhang, Y., Hongbin, Y., & Tang, C. (2024) · Drug Resistance Updates · doi:10.1016/j.drup.2024.101084 · Cited by 38 · see citing works
Analysis of the structure, evolution, and expression of CD24, an important regulator of cell fate
Ayre, D. C., Pallegar, N. K., Fairbridge, N. A., Canuti, M., Lang, A. S., & Christian, S. L. (2016) · Gene · doi:10.1016/j.gene.2016.05.038 · Cited by 37 · see citing works
Li, W., Ling, H.-P., You, W., Liu, H., Sun, Q., Zhou, M., Shen, W., Zhao, J., Zhu, L., & Hang, C. (2013) · Molecular Neurobiology · doi:10.1007/s12035-013-8509-4 · Cited by 31 · see citing works
Zhang, H., Siegel, C. T., Shuai, L., Lai, J., Zeng, L., Zhang, Y., Lai, X., Bie, P., & Bai, L. (2016) · Scientific Reports · doi:10.1038/srep21783 · Cited by 30 · see citing works
Progressive induction of hepatocyte progenitor cells in chronically injured liver
Tanimizu, N., Ichinohe, N., Yamamoto, M., Akiyama, H., Nishikawa, Y., & Mitaka, T. (2017) · Scientific Reports · doi:10.1038/srep39990 · Cited by 29 · see citing works
Advances in Liver Cancer Stem Cell Isolation and their Characterization
Liu, L., & Borlak, J. T. (2021) · Stem Cell Reviews and Reports · doi:10.1007/s12015-020-10114-6 · Cited by 28 · see citing works
Pluripotency inducing Yamanaka factors: role in stemness and chemoresistance of liver cancer
Fatma, H., & Siddique, H. R. (2021) · Expert Review of Anticancer Therapy · doi:10.1080/14737140.2021.1915137 · Cited by 27 · see citing works
Cell and Tissue Therapy for the Treatment of Chronic Liver Disease
Bram, Y., Nguyen, D.-H. T., Gupta, V., Park, J., Richardson, C., Chandar, V., & Schwartz, R. E. (2021) · Annual Review of Biomedical Engineering · doi:10.1146/annurev-bioeng-112619-044026 · Cited by 24 · see citing works
Liu, W., Ren, L., Wang, T., Navarro–Álvarez, N., & Tang, L. (2016) · International Journal of Biological Sciences · doi:10.7150/ijbs.15715 · Cited by 25 · see citing works
Liver Renewal: Detecting Misrepair and Optimizing Regeneration
Machado, M. V., & Diehl, A. M. (2014) · Mayo Clinic Proceedings · doi:10.1016/j.mayocp.2013.10.009 · Cited by 23 · see citing works
Liver stem cells: Plasticity of the liver epithelium
Tsuchiya, A., & Lu, W. (2019) · World Journal of Gastroenterology · doi:10.3748/wjg.v25.i9.1037 · Cited by 23 · see citing works
Aguilar, P., & Lertchirakarn, V. (2016) · Tissue and Cell · doi:10.1016/j.tice.2016.08.008 · Cited by 22 · see citing works
Hepatic progenitor cells in canine and feline medicine: potential for regenerative strategies
Kruitwagen, H. S., Spee, B., & Schotanus, B. A. (2014) · BMC Veterinary Research · doi:10.1186/1746-6148-10-137 · Cited by 19 · see citing works
Comerford, S. A., Schultz, N. D., Hinnant, E. A., Klapproth, S., & Hammer, R. E. (2012) · Oncogenesis · doi:10.1038/oncsis.2012.27 · Cited by 18 · see citing works
DNA Methyltransferases Modulate Hepatogenic Lineage Plasticity of Mesenchymal Stromal Cells
Lee, C., Huang, W.-C., Huang, H., Huang, Y., Ho, J. H., Yang, M., Yang, V. W., & Lee, O. K. (2017) · Stem Cell Reports · doi:10.1016/j.stemcr.2017.05.008 · Cited by 16 · see citing works
Schievenbusch, S., Sauer, E., Curth, H., Schulte, S., Demir, M., Toex, U., Goeser, T., & Nierhoff, D. (2012) · Stem Cells and Development · doi:10.1089/scd.2011.0579 · Cited by 14 · see citing works
Tsuruya, K., Chikada, H., Ida, K., Anzai, K., Kagawa, T., Inagaki, Y., Mine, T., & Kamiya, A. (2015) · Stem Cells and Development · doi:10.1089/scd.2014.0479 · Cited by 13 · see citing works
Ping, D., Qi, J., Li, M., Sun, X., Peng, Y. Y., & Liu, C. (2023) · Journal of Ethnopharmacology · doi:10.1016/j.jep.2023.117001 · Cited by 13 · see citing works
The potential role of liver stem cells in initiation of primary liver cancer
Zhi, X., Xiong, J., Zi, X., & Hu, Y. (2016) · Hepatology International · doi:10.1007/s12072-016-9730-9 · Cited by 12 · see citing works
Heterogeneity of The CD90+ Population in Different Stages of Hepatocarcinogenesis
Thakolwiboon, S. (2014) · Journal of Proteomics & Bioinformatics · doi:10.4172/jpb.1000332 · Cited by 12 · see citing works
The CD24hi smooth muscle subpopulation is the predominant fraction in uterine fibroids
Drosch, M., Schmidt, N., Markowski, D. N., Zollner, T. M., Koch, M., & Bullerdiek, J. (2014) · Molecular Human Reproduction · doi:10.1093/molehr/gau022 · Cited by 12 · see citing works
Serrano, F., Garcı́a-Bravo, M., Blazquez, M., Torres, J., Castell, J. V., Segovia, J. C., & Bort, R. (2016) · Stem Cell Research & Therapy · doi:10.1186/s13287-016-0349-5 · Cited by 12 · see citing works
Jeong, J., Tanaka, M., Yang, Y., Arefyev, N., DiRito, J. R., Tietjen, G. T., Zhang, X., McConnell, M. J., Utsumi, T., & Iwakiri, Y. (2023) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00139.2023 · Cited by 11 · see citing works
Graumann, F., Churin, Y., Tschuschner, A., Reifenberg, K., Glebe, D., Roderfeld, M., & Roeb, E. (2015) · PLoS ONE · doi:10.1371/journal.pone.0146099 · Cited by 11 · see citing works
Reduced DAXX Expression Is Associated with Reduced CD24 Expression in Colorectal Cancer
Chen, Y.-C., Lee, T., & Tzeng, S. (2019) · Cells · doi:10.3390/cells8101242 · Cited by 11 · see citing works
Role of microRNA-regulated cancer stem cells in recurrent hepatocellular carcinoma
Li, L., Chen, X., & Yu, C.-H. (2022) · World Journal of Hepatology · doi:10.4254/wjh.v14.i12.1985 · Cited by 10 · see citing works
Kamiya, A., Ito, K., Yanagida, A., Chikada, H., Iwama, A., & Nakauchi, H. (2015) · Stem Cells and Development · doi:10.1089/scd.2015.0015 · Cited by 10 · see citing works
Single‐cell landscape of the intrahepatic ecosystem in alcohol‐related liver disease
Zhao, X., Wang, S., Liu, Q., Wei, W., Sun, X., Song, H., Xu, J., Zhang, S., Wang, H., & Fu, J. (2025) · Clinical and Translational Medicine · doi:10.1002/ctm2.70198 · Cited by 9 · see citing works
Liu, K., Guo, M., Lou, X., Li, X., Xu, Y., Ji, W., Huang, X., Yang, J., & Duan, J.-C. (2015) · World Journal of Gastroenterology · doi:10.3748/wjg.v21.i19.5856 · Cited by 8 · see citing works
Deciphering hepatocellular responses to metabolic and oncogenic stress
Marcelo, K. L., Lin, F., Rajapakshe, K., Dean, A. M., Gonzales, N. M., Coarfa, C., Means, A. R., Goldie, L. C., & York, B. (2015) · Journal of Biological Methods · doi:10.14440/jbm.2015.77 · Cited by 7 · see citing works
Self-citationFounder cells for hepatocytes during liver regeneration: from identification to application
Wei, S., Tang, J., & Cai, X. (2020) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-020-03457-3 · Cited by 6 · see citing works
Diverse perspectives to address for the future treatment of heterogeneous hepatocellular carcinoma
Tsuchiya, A., Ogawa, M., Watanabe, T., Takeuchi, S., Kojima, Y., Watanabe, Y., Kimura, N., Hayashi, K., Yokoyama, J., & Terai, S. (2019) · Heliyon · doi:10.1016/j.heliyon.2019.e01325 · Cited by 5 · see citing works
Sharpen Your Look on Liver Progenitor Cells
Dollé, L., Streetz, K. L., & van Grunsven, L. A. (2011) · Hepatology · doi:10.1002/hep.24727 · Cited by 4 · see citing works
Liver Injury Models for Induction of Hepatic Oval Cells in Rodents
Cohen, A. J. (2015) · Journal of Liver Research Disorders & Therapy · doi:10.15406/jlrdt.2015.01.00005 · Cited by 4 · see citing works
Update on Hepatobiliary Plasticity
Kim, M., Rizvi, F., Shin, D., & Gouon–Evans, V. (2023) · Seminars in Liver Disease · doi:10.1055/s-0042-1760306 · Cited by 4 · see citing works
Liver Progenitor Cells, Cancer Stem Cells and Hepatocellular Carcinoma
Janina, E. E., George, C. T., & John, K. (2012) · InTech eBooks · doi:10.5772/48005 · Cited by 3 · see citing works
Translation From Mice to Men: Are Dogs a Dodgy Intermediate?
Kruitwagen, H. S., Spee, B., Fieten, H., van Steenbeek, F. G., Schotanus, B. A., & Penning, L. C. (2014) · EMJ Hepatology · doi:10.33590/emjhepatol/10314316 · Cited by 3 · see citing works
Xu, C., Fang, X., Song, Y., Xiang, Z., Xu, X., & Wei, X. (2024) · International Journal of Biological Sciences · doi:10.7150/ijbs.93739 · Cited by 2 · see citing works
Modeling hepatic fibrosis in TP53 knockout iPSC ‐derived human liver organoids
Karabicici, M., Akbari, S., Çalışkan, C., Celiker, C., Öz, Ö., Binokay, L., Karakülah, G., Şentürk, Ş., & Erdal, E. (2025) · Molecular Oncology · doi:10.1002/1878-0261.70119 · Cited by 2 · see citing works
Model systems and clinical applications of hepatic stem cells for liver regeneration
Zhang, M., Zhong, Y., & Chen, J. (2011) · Hepatology International · doi:10.1007/s12072-011-9323-6 · Cited by 2 · see citing works
Aktaş, R. G. (2019) · Trakya University Journal of Natural Sciences · doi:10.23902/trkjnat.486558 · Cited by 2 · see citing works
Manohar, R., & Lagasse, E. (2013) · Elsevier eBooks · doi:10.1016/b978-0-12-398358-9.00045-8 · Cited by 1 · see citing works
Emerging signals regulating liver tumor initiating cells
Chen, J., Chen, C.-Y., Nguyen, C. C., Chen, L., Lee, K., & Stiles, B. L. (2018) · Liver Research · doi:10.1016/j.livres.2018.08.003 · Cited by 1 · see citing works
Liver Regeneration in Health and Disease
Alison, M. R., & Islam, S. (2013) · Springer eBooks · doi:10.1007/978-1-4614-7696-2_22
Isolation and expansion of a unique stem cell population from human and mouse gallbladders
Manohar, R. (2012) · D-Scholarship@Pitt (University of Pittsburgh)
The Stem Cells in Liver Cancers and the Controversies
Tomita, H., Kanayama, T., Niwa, A., Noguchi, K., Tanaka, T., & Hara, A. (2018) · Elsevier eBooks · doi:10.1016/b978-0-12-812301-0.00013-x
Wang, F., Gao, Y., Xue, S.-T., Zhao, L., Zhang, T., Li, Y., Zhao, C., Wu, F. H., Liu, Y., Wu, J., et al. (2022) · Research Square · doi:10.21203/rs.3.rs-1313420/v1
Metabolic Alterations of Hepatocellular Cancer Stem Cells
David, J. C., Afonso, M. B., & Rodrigues, C. M. P. (2022) · Interdisciplinary cancer research · doi:10.1007/16833_2022_43
Erdal, E., Karabicici, M., Akbari, S., Çalışkan, C., Celiker, C., Öz, Ö., Binokay, L., Karakülah, G., & Şentürk, Ş. (2024) · Research Square · doi:10.21203/rs.3.rs-3935080/v1
Jiang, N., Li, G., Luo, S., Kong, X., Yin, S., Peng, J., Jiang, Y., Tao, W., Cheng, L., Xie, H., et al. (2025) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-025-05677-x
The plastic cellular states of liver cells
Huch, M. (2016) · VUBIR (Vrije Universiteit Brussel)
Bai, X., Dong, X., Sun, Q., Yang, N., Du, L., & Zhao, L. (2026) · Medicine · doi:10.1097/md.0000000000046654
Bellesis, A., Li, X., Moore-Frederick, D., Xu, D., Delbridge, K., Ma, J., Vaccaro, G., Edward, B. A. A., Kellogg, M., Creeger, Y., et al. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.06.05.730479
- Authors
- Qiu, Q., Hernandez, J. C., Dean, A. M., Rao, P. H., & Darlington, G. J.
- Affiliations
- Duke University (US)
- Baylor College of Medicine (US)
- Corresponding author
- Darlington, Gretchen J.
- Venue
- Stem Cells and Development
- Publisher
- SAGE Publications
- Published
- 2011-12
- Volume
- 20
- Issue
- 12
- Pages
- 2177-2188
- ISSN
- 1525-8165 (ISSN-L)
- 1547-3287
- 1557-8534
- PMC
- PMC3225069
- OpenAlex
- W1989035229
- Cited by
- 79
- References
- 45
- Citations by year
- 2026: 2 · 2025: 3 · 2024: 3 · 2023: 4 · 2022: 4 · 2021: 3 · 2020: 3 · 2019: 5 · 2018: 3 · 2017: 4 · 2016: 11 · 2015: 11 · 2014: 9 · 2013: 7 · 2012: 4
- FWCI
- 4.68
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Stem Cells and Development (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- National Institute on Aging (AG028865, R01AG028865)
- Topics
- Health Sciences › Medicine › Hepatology › Liver physiology and pathology
- Health Sciences › Medicine › Genetics › Mesenchymal stem cell research
- Health Sciences › Medicine › Surgery › Tissue Engineering and Regenerative Medicine
- Keywords
- CD24, hepatic progenitor cells, liver progenitor cells, cell surface markers, oval cells, cholangiocytes, CK19, hepatocyte differentiation, cell fusion, liver regeneration, cell transplantation, immunophenotype
- MeSH terms
- Aging, Animals, Cell Aggregation, Cell Differentiation, Cell Separation, Flow Cytometry, Gene Expression Regulation, Hydrolases, Kupffer Cells, Liver, Mice, Inbred C57BL, Pyridines, Sex Chromosomes, Stem Cells, Biomarkers, Mice, Knockout, Hepatocytes, Cell Proliferation, Mice, CD24 Antigen, Hepatic Stellate 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
