Clonal identification and characterization of self-renewing pluripotent stem cells in the developing liver
Open accessAbstract
Using flow cytometry and single cell–based assays, we prospectively identified hepatic stem cells with multilineage differentiation potential and self-renewing capability. These cells could be clonally propagated in culture where they continuously produced hepatocytes and cholangiocytes as descendants while maintaining primitive stem cells. When cells that expanded in vitro were transplanted into recipient animals, they morphologically and functionally differentiated into hepatocytes and cholangiocytes with reconstitution of hepatocyte and bile duct structures. Furthermore, these cells differentiated into pancreatic ductal and acinar cells or intestinal epithelial cells when transplanted into pancreas or duodenal wall. These data indicate that self-renewing pluripotent stem cells persist in the developing mouse liver and that such cells can be induced to become cells of other organs of endodermal origin under appropriate microenvironment. Manipulation of hepatic stem cells may provide new insight into therapies for diseases of the digestive system.
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Isolating c-Met+ c-Kit- CD45- Ter119- cells achieves a much higher enrichment of hepatoblasts.
“Isolating c-Met + c-Kit - CD45 -Ter119 -(also known as Met, Kit, Ptprc and Ly76, respectively -Mouse Genome Informatics) cells achieved a much higher enrichment of hepatoblasts, and thus this method could facilitate the identification of a discrete set of transcription factors that are activated in this specific cell population.”
From Tbx3 controls the fate of hepatic progenitor cells in liver development by suppressing <i>p19ARF</i> expression (2008) · cites this paper as Suzuki et al., 2002
The Results section, “Flow cytometric fractionation of fetal mouse liver cells” (page unavailable), reports 560-fold enrichment of hepatic colony-forming cells. But that enrichment required sorting for CD49f+/low as well as the four markers named in the claim; the paper does not establish the same enrichment for the four-marker selection alone. (LLM, conf=0.88)
Experimental — accuracy not yet measuredc-Met+ cells display self-renewing cell divisions and differentiation into both hepatocytes and cholangiocytes in response to Hgf stimulus.
“In particular, cells marked by the hepatocyte growth factor (Hgf) receptor c-Met displayed distinctive activities in response to Hgf stimulus, including self-renewing cell divisions and differentiation into both hepatocytes and cholangiocytes (Suzuki et al., 2002;Suzuki et al., 2003a).”
From Tbx3 controls the fate of hepatic progenitor cells in liver development by suppressing <i>p19ARF</i> expression (2008) · cites this paper as Suzuki et al., 2002
The Results (Flow cytometric fractionation; Clonal expansion and self-renewal capability) identify self-renewing, multilineage H-CFU-C within the c-Met+ cell subpopulation and state that HGF is required for their proliferation. The Discussion (Self-renewal of H-CFU-C in vitro and in vivo) reports divisions yielding both hepatocytes and cholangiocytes, but the cited passages do not establish that HGF stimulus drives differentiation into both lineages. (LLM, conf=0.84)
Experimental — accuracy not yet measured
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Cites
A Direct Measurement of the Radiation Sensitivity of Normal Mouse Bone Marrow Cells1
Till, J. E., & McCulloch, E. A. (2010) · Radiation Research · doi:10.1667/rrxx28.1 · Cited by 4,036 · see citing works
Histopathologic Technic and Practical Histochemistry.
Small, J. A., & Lillie, R. D. (1954) · Bulletin of the Torrey Botanical Club · doi:10.2307/2481951 · Cited by 2,971 · see citing works
Michalopoulos, G. K., & DeFrances, M. C. (1997) · Science · doi:10.1126/science.276.5309.60 · Cited by 2,828 · see citing works
‘Green mice’ as a source of ubiquitous green cells
Okabe, M., Ikawa, M., Kominami, K., Nakanishi, T., & Nishimune, Y. (1997) · FEBS Letters · doi:10.1016/s0014-5793(97)00313-x · Cited by 2,581 · see citing works
Long-Term Lymphohematopoietic Reconstitution by a Single CD34-Low/Negative Hematopoietic Stem Cell
Osawa, M., Hanada, K., Hamada, H., & Nakauchi, H. (1996) · Science · doi:10.1126/science.273.5272.242 · Cited by 2,141 · see citing works
Self-citationScatter factor/hepatocyte growth factor is essential for liver development
Schmidt, C. S., Bladt, F., Gödecke, S., Brinkmann, V., Zschiesche, W., Sharpe, M. J., Gherardi, E., & Birchmeler, C. (1995) · Nature · doi:10.1038/373699a0 · Cited by 1,395 · see citing works
Control of endodermal endocrine development by Hes-1
Jensen, J. N., Pedersen, E. E., Galante, P. E., Hald, J., Heller, R. S., Ishibashi, M., Kageyama, R., Guillemot, F., Serup, P., & Madsen, O. D. (2000) · Nature Genetics · doi:10.1038/71657 · Cited by 1,155 · see citing works
Placental defect and embryonic lethality in mice lacking hepatocyte growth factor/scatter factor
Uehara, Y., Minowa, O., Mori, C., Shiota, K., Kuno, J., Noda, T., & Kitamura, N. (1995) · Nature · doi:10.1038/373702a0 · Cited by 1,041 · see citing works
Ory, D., Neugeboren, B. I., & Mulligan, R. C. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.21.11400 · Cited by 926 · see citing works
Zulewski, H., Abraham, E. J., Gerlach, M. J., Daniel, P. B., Moritz, W., Müller-Stich, B. P., Vallejo, M., Thomas, M. K., & Habener, J. F. (2001) · Diabetes · doi:10.2337/diabetes.50.3.521 · Cited by 785 · see citing works
RAFF, M. C., Lillien, L. E., Richardson, W. D., Burne, J. F., & Noble, M. (1988) · Nature · doi:10.1038/333562a0 · Cited by 761 · see citing works
Morrison, S. J., White, P. M., Zock, C., & Anderson, D. J. (1999) · Cell · doi:10.1016/s0092-8674(00)80583-8 · Cited by 749 · see citing works
Mowry, R. W. (1963) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1963.tb16654.x · Cited by 687 · see citing works
A bipotential precursor population for pancreas and liver within the embryonic endoderm
Deutsch, G., Jung, J., Zheng, M., Lóra, J., & Zaret, K. S. (2001) · Development · doi:10.1242/dev.128.6.871 · Cited by 611 · see citing works
Serial transplantation reveals the stem-cell-like regenerative potential of adult mouse hepatocytes.
Overturf, K., Al-Dhalimy, M., Ou, C. N., Finegold, M. J., & Grompe, M. (1997) · Europe PMC (PubMed Central) · Cited by 599 · see citing works
Cell lineages and oval cell progenitors in rat liver development.
Shiojiri, N., Lemire, J. M., & Fausto, N. (1991) · PubMed · Cited by 390 · see citing works
Improved Methods of Retroviral Vector Transduction and Production for Gene Therapy
Kotani, H., Newton, P. B., Zhang, S., Chiang, Y. L., Otto, E., Weaver, L., Blaese, R. M., Anderson, W. F., & McGarrity, G. J. (1994) · Human Gene Therapy · doi:10.1089/hum.1994.5.1-19 · Cited by 369 · see citing works
Hepatic oval cells express the hematopoietic stem cell marker thy-1 in the rat
Petersen, B. E., Goff, J. P., Greenberger, J. S., & Michalopoulos, G. K. (1998) · Hepatology · doi:10.1002/hep.510270218 · Cited by 358 · see citing works
Hepatic stem cells in liver regeneration
Thorgeirsson, S. S. (1996) · The FASEB Journal · doi:10.1096/fasebj.10.11.8836038 · Cited by 305 · see citing works
Evidence for the stem cell origin of hepatocellular carcinoma and cholangiocarcinoma.
Sell, S., & Dunsford, H. A. (1989) · PubMed · Cited by 298 · see citing works
Flow–Cytometric Separation and Enrichment of Hepatic Progenitor Cells in the Developing Mouse Liver
Suzuki, A., Zheng, Y.-W., Kondo, R., Kusakabe, M., Takada, Y., Fukao, K., Nakauchi, H., & Taniguchi, H. (2000) · Hepatology · doi:10.1053/jhep.2000.20349 · Cited by 294 · see citing works
Self-citationFujio, K., Evarts, R. P., Hu, Z., Marsden, E. R., & Thorgeirsson, S. S. (1994) · PubMed · Cited by 286 · see citing works
KUBOTA, H. Y., & Reid, L. M. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.22.12132 · Cited by 242 · 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
The Repopulation Potential of Hepatocyte Populations Differing in Size and Prior Mitotic Expansion
Overturf, K., Al-Dhalimy, M., Finegold, M. J., & Grompe, M. (1999) · American Journal Of Pathology · doi:10.1016/s0002-9440(10)65531-9 · Cited by 202 · see citing works
Dabeva, M. D., Petkov, P. M., Sandhu, J., Oren, R., Laconi, E., Hurston, E., & Shafritz, D. A. (2000) · American Journal Of Pathology · doi:10.1016/s0002-9440(10)65074-2 · Cited by 171 · see citing works
Hu, Z., Evarts, R. P., Fujio, K., Marsden, E. R., & Thorgeirsson, S. S. (1993) · PubMed Central · Cited by 153 · see citing works
Rao, M. S. R., Dwivedi, R. S., Yeldandi, A. V., Subbarao, V., Tan, X., Usman, M. I., Thangada, S., Nemali, M. R., Kumar, S., & Scarpelli, D. G. (1989) · Europe PMC (PubMed Central) · Cited by 128 · see citing works
Omori, N., Omori, M., Evarts, R. P., TERAMOTO, T., Miller, M. J., Hoang, T. N., & Thorgeirsson, S. S. (1997) · Hepatology · doi:10.1002/hep.510260325 · Cited by 127 · see citing works
Johnson, M., Koukoulis, G. Κ., Matsumoto, K., Nakamura, T., & Iyer, A. (1993) · Hepatology · doi:10.1002/hep.1840170618 · Cited by 115 · see citing works
The origin of intrahepatic bile duct cells in the mouse
Shiojiri, N. (1984) · Development · doi:10.1242/dev.79.1.25 · Cited by 107 · see citing works
Pinkus, G. S., O'Connor, E. M., Etheridge, C. L., & Corson, J. M. (1985) · Journal of Histochemistry & Cytochemistry · doi:10.1177/33.5.2580883 · Cited by 87 · see citing works
Pack, R., Heck, R., Dienes, H. P., Oesch, F., & Steinberg, P. (1993) · Experimental Cell Research · doi:10.1006/excr.1993.1025 · Cited by 80 · see citing works
Paulus, U., Loeffler, M., Zeidler, J., Owen, G., & Potten, C. S. (1993) · Journal of Cell Science · doi:10.1242/jcs.106.2.473 · Cited by 76 · see citing works
Isolation Culture, and Transplantation of Rat Hepatocytic Precursor (Stem-like) Cells
Grisham, J. W., Coleman, W. B., & Smith, G. J. (1993) · Experimental Biology and Medicine · doi:10.3181/00379727-204-43663 · Cited by 74 · see citing works
Matsusaka, S., Tsujimura, T., Toyosaka, A., Nakasho, K., Sugihara, A., Okamoto, E., Uematsu, K., & Terada, N. (1999) · Hepatology · doi:10.1002/hep.510290304 · Cited by 72 · see citing works
Bisgaard, H. C., & Thorgeirsson, S. S. (1991) · Journal of Cellular Physiology · doi:10.1002/jcp.1041470220 · Cited by 67 · see citing works
Methylene dianiline: Acute toxicity and effects on biliary function
Kanz, M. F., Kaphalia, L., Kaphalia, B. S., Romagnoli, E., & Ansari, G. A. S. (1992) · Toxicology and Applied Pharmacology · doi:10.1016/0041-008x(92)90221-d · Cited by 47 · see citing works
Sasaki, K., Adachi, S., Yamamoto, T., Murakami, T., Tanaka, K., & Takahashi, M. (1988) · Cytometry · doi:10.1002/cyto.990090115 · Cited by 41 · see citing works
Kaneko, S., Onodera, M., 藤木, 豊., Nagasawa, T., & Nakauchi, H. (2001) · Human Gene Therapy · doi:10.1089/104303401450942 · Cited by 39 · see citing works
Self-citationA rapid and simple estimation of cell cycle parameters by continuous labeling with bromodeoxyuridine
Sasaki, K., Murakami, T., & Takahashi, M. (1987) · Cytometry · doi:10.1002/cyto.990080514 · Cited by 36 · see citing works
Chen, J.-R., Tsao, M., & Duguid, W. P. (1995) · Europe PMC (PubMed Central) · Cited by 29 · see citing works
Flagged first, then by citations
1 of the 43 references couldn’t be matched to a known paper.
Research works printed but not linked: 3
- Fausto, N. 1994. Liver stem cells. The Liver. 3rd ed. I.M. Arias, J.L. Boyer, N. Fausto, W.B. Jakoby, D.A. Schachter, and D.A. Shafritz, editors. Ed. 3. Raven Press, New York. 1501–1518.
- Fausto, N., and E.M. Webber. 1994. Liver regeneration. The Liver. 3rd ed. I.M. Arias, J.L. Boyer, N. Fausto, W.B. Jakoby, D.A. Schachter, and D.A. Shafritz, editors. Raven Press, New York. 1059–1084.
- Metcalf, D., and M.A.S. Moore. 1971. Hematopoietic cells. Frontiers of Biology. A. Neuberger and E.L. Tatum, editors. Vol. 25. North-Holland, Amsterdam.
Cited by
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Godoy, P., Hewitt, N. J., Albrecht, U., Andersen, M. E., Ansari, N., Bhattacharya, S., Bode, J. G., Bolleyn, J., Borner, C., Böttger, J., et al. (2013) · Archives of Toxicology · doi:10.1007/s00204-013-1078-5 · Cited by 1,280 · see citing works
Direct conversion of mouse fibroblasts to hepatocyte-like cells by defined factors
Sekiya, S., & Suzuki, A. (2011) · Nature · doi:10.1038/nature10263 · Cited by 846 · see citing works
Self-citationChiba, T., Kita, K., Zheng, Y., Yokosuka, O., Saisho, H., Iwama, A., Nakauchi, H., & Taniguchi, H. (2006) · Hepatology · doi:10.1002/hep.21227 · Cited by 664 · see citing works
Self-citationStem Cells and Liver Regeneration
Duncan, A. W., Dorrell, C., & Grompe, M. (2009) · Gastroenterology · doi:10.1053/j.gastro.2009.05.044 · Cited by 547 · see citing works
Invasive growth: a MET-driven genetic programme for cancer and stem cells
Boccaccio, C., & Comoglio, P. M. (2006) · Nature reviews. Cancer · doi:10.1038/nrc1912 · Cited by 540 · see citing works
Fate tracing of mature hepatocytes in mouse liver homeostasis and regeneration
Malato, Y., Naqvi, S., Schürmann, N., Ng, R., Wang, B., Zape, J., Kay, M. A., Grimm, D., & Willenbring, H. (2011) · Journal of Clinical Investigation · doi:10.1172/jci59261 · Cited by 434 · see citing works
How cells change their phenotype
Tosh, D., & Slack, J. M. W. (2002) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm761 · Cited by 404 · see citing works
Concise Review: Notch Signaling in Stem Cell Systems
Chiba, S. (2006) · Stem Cells · doi:10.1634/stemcells.2005-0661 · Cited by 400 · see citing works
Known and novel roles of the MET oncogene in cancer: a coherent approach to targeted therapy
Comoglio, P. M., Trusolino, L., & Boccaccio, C. (2018) · Nature reviews. Cancer · doi:10.1038/s41568-018-0002-y · Cited by 380 · see citing works
Brittan, M., & Wright, N. A. (2002) · The Journal of Pathology · doi:10.1002/path.1155 · Cited by 330 · 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
Tanimizu, N., & Miyajima, A. (2004) · Journal of Cell Science · doi:10.1242/jcs.01169 · Cited by 290 · see citing works
Genetic programming of liver and pancreas progenitors: lessons for stem-cell differentiation
Zaret, K. S. (2008) · Nature Reviews Genetics · doi:10.1038/nrg2318 · Cited by 285 · see citing works
Potential hepatic stem cells reside in EpCAM+ cells of normal and injured mouse liver
Okabe, M., Tsukahara, Y., Tanaka, M., Suzuki, K., Saito, S., Kamiya, Y., Tsujimura, T., Nakamura, K., & Miyajima, A. (2009) · Development · doi:10.1242/dev.031369 · Cited by 287 · see citing works
Liver development update: new embryo models, cell lineage control, and morphogenesis
Lemaigre, F. P., & Zaret, K. S. (2004) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2004.08.004 · Cited by 282 · see citing works
Poulsom, R., Alison, M. R., Forbes, S. J., & Wright, N. A. (2002) · The Journal of Pathology · doi:10.1002/path.1176 · Cited by 277 · see citing works
Zalzman, M., Gupta, S. K., Giri, R. K., Berkovich, I., Sappal, B. S., Karnieli, O., Zern, M. Α., Fleischer, N., & Efrat, S. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1136854100 · Cited by 268 · see citing works
Lakshmipathy, U., & Verfaillie, C. M. (2004) · Blood Reviews · doi:10.1016/j.blre.2004.03.001 · Cited by 264 · see citing works
Little evidence of transdifferentiation of bone marrow-derived cells into pancreatic beta cells
Choi, J. B., Uchino, H., Azuma, K., Iwashita, N., Tanaka, Y., Mochizuki, H., Migita, M., Shimada, T., Kawamori, R., & Watada, H. (2003) · Diabetologia · doi:10.1007/s00125-003-1182-9 · Cited by 241 · see citing works
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Dorrell, C., Erker, L. R., Schug, J., Kopp, J. L., Canaday, P. S., Fox, A. J., Smirnova, O., Duncan, A. W., Finegold, M. J., Sander, M., et al. (2011) · Genes & Development · doi:10.1101/gad.2029411 · Cited by 236 · see citing works
Carpino, G., Cardinale, V., Onori, P., Franchitto, A., Berloco, P. B., Rossi, M., Wang, Y., Semeraro, R., Anceschi, M. M., Brunelli, R., et al. (2011) · Journal of Anatomy · doi:10.1111/j.1469-7580.2011.01462.x · Cited by 224 · see citing works
Verfaillie, C. M., Pera, M. F., & Lansdorp, P. M. (2002) · Hematology · doi:10.1182/asheducation-2002.1.369 · Cited by 222 · see citing works
Hisatomi, Y., Okumura, K., Nakamura, K., Matsumoto, S., Satoh, A., Nagano, K., Yamamoto, T., & Endo, F. (2004) · Hepatology · doi:10.1002/hep.20063 · Cited by 219 · see citing works
Prospective Isolation of Multipotent Pancreatic Progenitors Using Flow-Cytometric Cell Sorting
Suzuki, A., Nakauchi, H., & Taniguchi, H. (2004) · Diabetes · doi:10.2337/diabetes.53.8.2143 · Cited by 218 · see citing works
Self-citationStem cells in liver regeneration, fibrosis and cancer: the good, the bad and the ugly
Alison, M. R., Islam, S., & Lim, S. G. (2008) · The Journal of Pathology · doi:10.1002/path.2453 · Cited by 211 · see citing works
Enhanced Self-Renewal Capability in Hepatic Stem/Progenitor Cells Drives Cancer Initiation
Chiba, T., Zheng, Y., Kita, K., Yokosuka, O., Saisho, H., Onodera, M., Miyoshi, H., Nakano, M., Zen, Y., Nakanuma, Y., et al. (2007) · Gastroenterology · doi:10.1053/j.gastro.2007.06.016 · Cited by 204 · see citing works
Self-citationForbes, S. J., Vig, P., Poulsom, R., Thomas, H. C., & Alison, M. R. (2002) · The Journal of Pathology · doi:10.1002/path.1163 · Cited by 195 · see citing works
Development of the biliary tract
Lemaigre, F. P. (2002) · Mechanisms of Development · doi:10.1016/s0925-4773(02)00334-9 · Cited by 191 · see citing works
Fukada, S., Higuchi, S., Segawa, M., Koda, K.-I., Yamamoto, Y., Tsujikawa, K., Kohama, Y., Uezumi, A., Imamura, M., Miyagoe‐Suzuki, Y., et al. (2004) · Experimental Cell Research · doi:10.1016/j.yexcr.2004.02.018 · Cited by 190 · see citing works
Khan, A. A., Shaik, M. V., Parveen, N., Rajendraprasad, A., Aleem, M. A., Aejaz, M., Srinivas, G., Avinash, T., Tiwari, S. K., Kumaresan, K., et al. (2010) · Cell Transplantation · doi:10.3727/096368910x498241 · Cited by 183 · see citing works
O’Donoghue, K., & Fisk, N. M. (2004) · Best Practice & Research Clinical Obstetrics & Gynaecology · doi:10.1016/j.bpobgyn.2004.06.010 · Cited by 179 · see citing works
The Role of Integrin α6 (CD49f) in Stem Cells: More than a Conserved Biomarker
Krebsbach, P. H., & Villa-Diaz, L. G. (2017) · Stem Cells and Development · doi:10.1089/scd.2016.0319 · Cited by 177 · see citing works
Suzuki, A., Iwama, A., Miyashita, H., Nakauchi, H., & Taniguchi, H. (2003) · Development · doi:10.1242/dev.00459 · Cited by 177 · see citing works
Self-citationSuzuki, 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
Self-citationLiver Progenitors and Adult Cell Plasticity in Hepatic Injury and Repair: Knowns and Unknowns
Ko, S., Russell, J. O., Molina, L. M., & Monga, S. P. (2019) · Annual Review of Pathology Mechanisms of Disease · doi:10.1146/annurev-pathmechdis-012419-032824 · Cited by 164 · see citing works
Oval cell‐mediated liver regeneration: Role of cytokines and growth factors
Lowes, K. N., Croager, E. J., Olynyk, J. K., Abraham, L. J., & Yeoh, G. C. (2002) · Journal of Gastroenterology and Hepatology · doi:10.1046/j.1440-1746.2003.02906.x · Cited by 163 · see citing works
Stem cells, cell transplantation and liver repopulation
Oertel, M., & Shafritz, D. A. (2007) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2007.12.004 · Cited by 162 · see citing works
Okumura, K., Nakamura, K., Hisatomi, Y., Nagano, K., Tanaka, Y., Terada, K., Sugiyama, T., Umeyama, K., Matsumoto, K., Yamamoto, T., et al. (2003) · Hepatology · doi:10.1053/jhep.2003.50259 · Cited by 160 · see citing works
The new stem cell biology: something for everyone
Preston, S. L., Alison, M. R., Forbes, S. J., Direkze, N. C., Poulsom, R., & Wright, N. A. (2003) · Molecular Pathology · doi:10.1136/mp.56.2.86 · Cited by 158 · see citing works
Fetal liver stroma consists of cells in epithelial-to-mesenchymal transition
Chagraoui, J., Lepage, A., Anjo, A., Uzan, G., & Charbord, P. (2003) · Blood · doi:10.1182/blood-2002-05-1341 · Cited by 156 · see citing works
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Alison, M. R., Vig, P., Russo, F. P., Bigger, B., Amofah, E., Themis, M., & Forbes, S. J. (2004) · Cell Proliferation · doi:10.1111/j.1365-2184.2004.00297.x · Cited by 146 · see citing works
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Park, J.-K., & Lee, D. (2005) · Journal of Bioscience and Bioengineering · doi:10.1263/jbb.99.311 · Cited by 141 · see citing works
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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
Glucagon-like peptide 1 (1–37) converts intestinal epithelial cells into insulin-producing cells
Suzuki, A., Nakauchi, H., & Taniguchi, H. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0936260100 · Cited by 140 · see citing works
Self-citationOshima, Y., Suzuki, A., Kawashimo, K., Ishikawa, M., Ohkohchi, N., & Taniguchi, H. (2006) · Gastroenterology · doi:10.1053/j.gastro.2006.11.027 · Cited by 137 · see citing works
Self-citationSuzuki, A., Sekiya, S., Büscher, D., Izpisúa Belmonte, J. C., & Taniguchi, H. (2008) · Development · doi:10.1242/dev.016634 · Cited by 136 · see citing works
Self-citationIshkitiev, N., Yaegaki, K., Calenic, B., Nakahara, T., Ishikawa, H., Mitev, V., & Haapasalo, M. (2010) · Journal of Endodontics · doi:10.1016/j.joen.2009.12.022 · Cited by 135 · see citing works
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Allen, J. W., & Bhatia, S. N. (2002) · Tissue Engineering · doi:10.1089/10763270260424097 · Cited by 133 · see citing works
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Shafritz, D. A., Oertel, M., Menthena, A., Nierhoff, D., & Dabeva, M. D. (2006) · Hepatology · doi:10.1002/hep.21047 · Cited by 132 · see citing works
Liver tissue engineering and cell sources: issues and challenges
Palakkan, A. A., Hay, D. C., PR, A. K., TV, K., & Ross, J. A. (2013) · Liver International · doi:10.1111/liv.12134 · Cited by 130 · see citing works
Wang, X., Yang, L. C., Wang, Y., Xu, Z., Ye, F., Zhang, J., Wang, Y., & Xu, C. (2020) · Cell Research · doi:10.1038/s41422-020-0378-6 · Cited by 127 · 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
Mammalian plasma membrane proteomics
Josić, D., & Clifton, J. G. (2007) · PROTEOMICS · doi:10.1002/pmic.200700139 · Cited by 125 · see citing works
Salama, H., Zekri, A. N., Zern, M. Α., Bahnassy, A. A., Loutfy, S. A., Shalaby, S., Vigen, C. L. P., Burke, W. S., Mostafa, M., Medhat, E., et al. (2010) · Cell Transplantation · doi:10.3727/096368910x514314 · Cited by 123 · see citing works
Pluripotency: Toward a gold standard for human ES and iPS cells
Smith, K. P., Luong, M. X., & Stein, G. (2009) · Journal of Cellular Physiology · doi:10.1002/jcp.21681 · Cited by 126 · see citing works
Molecular Mechanism of Liver Development and Regeneration
Tanimizu, N., & Miyajima, A. (2007) · International review of cytology · doi:10.1016/s0074-7696(06)59001-1 · Cited by 112 · see citing works
Stem cells in liver regeneration and therapy
Cantz, T., Manns, M. P., & Ott, M. (2007) · Cell and Tissue Research · doi:10.1007/s00441-007-0483-6 · Cited by 113 · see citing works
Differentiation of mouse and human embryonic stem cells into hepatic lineages
Shiraki, N., Umeda, K., Sakashita, N., Takeya, M., Kume, K., & Kume, S. (2008) · Genes to Cells · doi:10.1111/j.1365-2443.2008.01201.x · Cited by 112 · see citing works
Specific fate decisions in adult hepatic progenitor cells driven by MET and EGFR signalingPreprint
Kitade, M., Factor, V. M., Andersen, J. B., Tomokuni, A., Kaji, K., Akita, H., Holczbauer, Á., Seo, D., Marquardt, J. U., Conner, E. A., et al. (2013) · Genes & Development · doi:10.1101/gad.214601.113 · Cited by 111 · see citing works
Sall4 regulates cell fate decision in fetal hepatic stem/progenitor cells
Oikawa, T., Kamiya, A., Kakinuma, S., Zeniya, M., Nishinakamura, R., Tajiri, H., & Nakauchi, H. (2009) · Gastroenterology · doi:10.1053/j.gastro.2008.11.018 · Cited by 108 · see citing works
Self-citationHosen, N., Yamane, T., Muijtjens, M., Pham, K., Clarke, M. F., & Weissman, I. L. (2007) · Stem Cells · doi:10.1634/stemcells.2006-0229 · Cited by 105 · see citing works
Nierhoff, D., Ogawa, A., Oertel, M., Chen, Y., & Shafritz, D. A. (2005) · Hepatology · doi:10.1002/hep.20735 · Cited by 105 · see citing works
Clonal proliferation of multipotent stem/progenitor cells in the neonatal and adult salivary glands
Kishi, T., Takao, T., FUJITA, K., & Taniguchi, H. (2005) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2005.12.031 · Cited by 103 · see citing works
Self-citationDerivation and Characterization of Hepatic Progenitor Cells from Human Embryonic Stem Cells
Zhao, D., Chen, S., Cai, J., Guo, Y., Song, Z., Che, J., Liu, C., Wu, C., Ding, M., & Deng, H. (2009) · PLoS ONE · doi:10.1371/journal.pone.0006468 · Cited by 101 · see citing works
Enrichment and Clonal Culture of Progenitor Cells During Mouse Postnatal Liver Development in Mice
Kamiya, A., Kakinuma, S., Yamazaki, Y., & Nakauchi, H. (2009) · Gastroenterology · doi:10.1053/j.gastro.2009.06.001 · Cited by 99 · see citing works
Self-citationMokkapati, S., Niopek, K., Huang, L., Cunniff, K. J., Ruteshouser, E. C., deCaestecker, M. P., Finegold, M. J., & Huff, V. (2014) · Cancer Research · doi:10.1158/0008-5472.can-13-3275 · Cited by 98 · see citing works
The application of human embryonic stem cell technologies to drug discovery
Sartipy, P., Björquist, P., Strehl, R., & Hyllner, J. (2007) · Drug Discovery Today · doi:10.1016/j.drudis.2007.07.005 · Cited by 96 · see citing works
Rodríguez, R. S., & Belkind‐Gerson, J. (2004) · Stem Cells · doi:10.1634/stemcells.2003-0049 · Cited by 96 · see citing works
Rountree, C. B., Senadheera, S., Mato, J. M., Crooks, G. M., & Lu, S. C.-L. (2007) · Hepatology · doi:10.1002/hep.22141 · Cited by 95 · see citing works
Human embryonic stem cells: Current technologies and emerging industrial applications
Améen, C., Strehl, R., Björquist, P., Lindahl, A. H., Hyllner, J., & Sartipy, P. (2007) · Critical Reviews in Oncology/Hematology · doi:10.1016/j.critrevonc.2007.06.012 · Cited by 94 · see citing works
Ли, Б., Zheng, Y., Sano, Y., & Taniguchi, H. (2011) · PLoS ONE · doi:10.1371/journal.pone.0017092 · Cited by 89 · see citing works
Self-citationNowak, G., Ericzon, B.-G., Nava, S., Jaksch, M., Westgren, M., & Sumitran-Holgersson, S. (2005) · Gut · doi:10.1136/gut.2005.064477 · Cited by 89 · see citing works
Characterization of cells in the developing human liver
Nava, S., Westgren, M., Jaksch, M., Tibell, A., Broomé, U., Ericzon, B., & Sumitran–Holgersson, S. (2005) · Differentiation · doi:10.1111/j.1432-0436.2005.00019.x · Cited by 88 · see citing works
Long-term culture of hepatic progenitors derived from mouse Dlk+ hepatoblasts
Tanimizu, N., Saito, H., Mostov, K. E., & Miyajima, A. (2004) · Journal of Cell Science · doi:10.1242/jcs.01572 · Cited by 87 · see citing works
Expression of Dlk/Pref-1 defines a subpopulation in the oval cell compartment of rat liver
Tanimizu, N., Tsujimura, T., Kohro, T., Kodama, T., Nakamura, K., & Miyajima, A. (2004) · Gene Expression Patterns · doi:10.1016/j.modgep.2004.08.003 · Cited by 86 · see citing works
Suzuki, A., Sekiya, S., Gunshima, E., Fujii, S., & Taniguchi, H. (2010) · Laboratory Investigation · doi:10.1038/labinvest.2010.150 · Cited by 84 · see citing works
Self-citationKUBOTA, H. Y., Yao, H.-L., & Reid, L. M. (2007) · Stem Cells · doi:10.1634/stemcells.2006-0316 · Cited by 83 · see citing works
The quest for liver progenitor cells: A practical point of view
Dollé, L., Best, J., Mei, J., Battah, F. A., Reynaert, H., van Grunsven, L. A., & Geerts, A. E. (2009) · Journal of Hepatology · doi:10.1016/j.jhep.2009.10.009 · Cited by 83 · see citing works
Liver stem cells: A scientific and clinical perspective
Dan, Y. Y., & Yeoh, G. C. (2008) · Journal of Gastroenterology and Hepatology · doi:10.1111/j.1440-1746.2008.05383.x · Cited by 82 · see citing works
Mesenchymal Progenitor Cells from Canine Fetal Tissues: Yolk Sac, Liver, and Bone Marrow
Wenceslau, C. V., Miglino, M. A., Martins, D. D. S., Ambrósio, C. E., Lizier, N. F., Pignatari, G. C., & Kerkis, I. (2011) · Tissue Engineering Part A · doi:10.1089/ten.tea.2010.0678 · Cited by 81 · see citing works
Fetal and adult liver stem cells for liver regeneration and tissue engineering
Fiegel, H. C., Lange, C., Kneser, U., Lambrecht, W., Zander, A. R., Rogiers, X., & Kluth, D. (2006) · Journal of Cellular and Molecular Medicine · doi:10.1111/j.1582-4934.2006.tb00422.x · Cited by 80 · see citing works
Cancer stem cells in hepatocellular carcinoma: Recent progress and perspective
Chiba, T., Kamiya, A., Yokosuka, O., & Iwama, A. (2009) · Cancer Letters · doi:10.1016/j.canlet.2009.04.027 · Cited by 79 · see citing works
Kwon, G. S., Fraser, S. T., Eakin, G. S., Mangano, M., Isern, J., Sahr, K. E., Hadjantonakis, A., & Baron, M. H. (2006) · Developmental Dynamics · doi:10.1002/dvdy.20843 · Cited by 80 · see citing works
Epigenetic gene regulation in stem cells and correlation to cancer
Mathews, L., Crea, F., & Farrar, W. L. (2009) · Differentiation · doi:10.1016/j.diff.2009.04.002 · Cited by 76 · see citing works
The influence of donor age on liver regeneration and hepatic progenitor cell populations
Ono, Y., Kawachi, S., Hayashida, T., Wakui, M., Tanabe, M., Itano, O., Obara, H., Shinoda, M., Hibi, T., Oshima, G., et al. (2011) · Surgery · doi:10.1016/j.surg.2011.05.004 · Cited by 76 · see citing works
Identification and enrichment of colony-forming cells from the adult murine pituitary
Lepore, D. A., Roeszler, K. N., Wagner, J., Ross, S. A., Bauer, K., & Thomas, P. Q. (2005) · Experimental Cell Research · doi:10.1016/j.yexcr.2005.04.023 · Cited by 75 · see citing works
Label-Retaining Cells in the Rat Pancreas
Duvillié, B., Attali, M., Aïello, V., Quéméneur, É., & Scharfmann, R. (2003) · Diabetes · doi:10.2337/diabetes.52.8.2035 · Cited by 75 · 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
Hepatoblast-Like Progenitor Cells Derived From Embryonic Stem Cells Can Repopulate Livers of Mice
Li, F., Liu, P., Liu, C., Xiang, D., Deng, L., Li, W., Wangensteen, K. J., Jianguo, S., Ma, Y., Hui, L., et al. (2010) · Gastroenterology · doi:10.1053/j.gastro.2010.08.042 · Cited by 72 · see citing works
Progenitor cells in the adult pancreas
Holland, A. M., Gonez, L. J., & Harrison, L. (2004) · Diabetes/Metabolism Research Reviews · doi:10.1002/dmrr.430 · Cited by 71 · see citing works
Gridelli, B. G., Vizzini, G. B., Pietrosi, G., Luca, A., Spada, M., Gruttadauria, S., Cintorino, D., Amico, G., Chinnici, C. M., Miki, T., et al. (2011) · Liver Transplantation · doi:10.1002/lt.22322 · Cited by 72 · see citing works
Hepatic Stem Cells: In Search of
Walkup, M. H., & Gerber, D. A. (2006) · Stem Cells · doi:10.1634/stemcells.2006-0063 · Cited by 70 · see citing works
Hirose, Y., Itoh, T., & Miyajima, A. (2009) · Experimental Cell Research · doi:10.1016/j.yexcr.2009.06.018 · Cited by 63 · see citing works
Analyses of cell surface molecules on hepatic stem/progenitor cells in mouse fetal liver
Kakinuma, S., Ohta, H., Kamiya, A., Yamazaki, Y., Oikawa, T., Okada, K., & Nakauchi, H. (2009) · Journal of Hepatology · doi:10.1016/j.jhep.2009.02.033 · Cited by 63 · see citing works
Self-citationHoppo, T., Fujii, H., Hirose, T., Yasuchika, K., Azuma, H., Baba, S., Naito, M., Machimoto, T., & Ikai, I. (2004) · Hepatology · doi:10.1002/hep.20180 · Cited by 63 · see citing works
Zhou, Q., Xiang, L., Shao, J., Hu, R., Lu, Y., Yao, H. P., & Dai, L. (2006) · Journal of Cellular Biochemistry · doi:10.1002/jcb.20970 · Cited by 62 · see citing works
Origin of hepatocellular carcinoma: Role of stem cells
Wu, X., & Chen, D. (2006) · Journal of Gastroenterology and Hepatology · doi:10.1111/j.1440-1746.2006.04485.x · Cited by 62 · see citing works
Hepatic stem/progenitor cells and stem-cell transplantation for the treatment of liver disease
Kakinuma, S., Nakauchi, H., & Watanabe, M. (2009) · Journal of Gastroenterology · doi:10.1007/s00535-008-2297-z · Cited by 60 · see citing works
Self-citationA novel stem-cell population in adult liver with potent hematopoietic-reconstitution activity
Kotton, D. N., Fabian, A. J., & Mulligan, R. C. (2005) · Blood · doi:10.1182/blood-2005-03-1017 · Cited by 60 · see citing works
- Authors
- Suzuki, A., Zheng, Y.-W., Kaneko, S., Onodera, M., Fukao, K., Nakauchi, H., & Taniguchi, H.
- Affiliations
- University of Tsukuba (JP)
- Venue
- The Journal of Cell Biology
- Publisher
- Rockefeller University Press
- Published
- 2002-01-07
- Volume
- 156
- Issue
- 1
- Pages
- 173-184
- ISSN
- 0021-9525 (ISSN-L)
- 1540-8140
- PMC
- PMC2173576
- OpenAlex
- W2121054813
- Cited by
- 356
- References
- 43
- Citations by year
- 2025: 2 · 2024: 3 · 2023: 4 · 2022: 3 · 2021: 1 · 2020: 7 · 2019: 8 · 2018: 10 · 2017: 9 · 2016: 5 · 2015: 4 · 2014: 14 · 2013: 19 · 2012: 15
- FWCI
- 20.45
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- cc-by-nc-sa
- Locations
- The Journal of Cell Biology (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion, cc-by-nc-sa)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Hepatology › Liver physiology and pathology
- Health Sciences › Medicine › Genetics › Mesenchymal stem cell research
- Health Sciences › Medicine › Hematology › Hematopoietic Stem Cell Transplantation
- Keywords
- hepatic stem cells, pluripotent stem cells, self-renewal, clonal propagation, liver development, hepatocyte differentiation, cholangiocyte differentiation, multilineage differentiation, pancreatic differentiation, intestinal epithelial differentiation, cell transplantation
- MeSH terms
- Animals, Bile Ducts, Cell Differentiation, Cells, Cultured, Clone Cells, Epithelial Cells, Fetus, Flow Cytometry, Intestines, Liver, Liver Regeneration, Microscopy, Electron, Pancreas, Stem Cells, Biomarkers, Cell Transplantation, Proto-Oncogene Proteins c-kit, Cell Lineage, Proto-Oncogene Proteins c-met, Reverse Transcriptase Polymerase Chain Reaction, Hepatocytes, Mice
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