Mesenchymal origin of hepatic stellate cells, submesothelial cells, and perivascular mesenchymal cells during mouse liver development
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UNLABELLED: The knowledge concerning fetal hepatic stellate cells (HSCs) is scarce, and their cell lineage and functions are largely unknown. The current study isolated fetal liver mesenchymal cells from a mouse expressing beta-galactosidase under the control of Msx2 promoter by fluorescence-activated cell sorting (FACS) and surveyed marker genes by microarray analysis. Based on the location and immunostaining with conventional and newly disclosed markers, we have identified three distinct populations of fetal liver mesenchymal cells expressing both desmin and p75 neurotrophin receptor (p75NTR): HSCs in the liver parenchyma; perivascular mesenchymal cells expressing alpha-smooth muscle actin (alpha-SMA); and submesothelial cells associated with the basal lamina beneath mesothelial cells and expressing activated leukocyte cell adhesion molecule (ALCAM) and platelet-derived growth factor receptor alpha. A transitional cell type from the submesothelial cell phenotype to fetal HSCs was also identified near the liver surface. Mesothelial cells expressed podoplanin and ALCAM. Ki-67 staining showed that proliferative activity of the submesothelial cells is higher than that of mesothelial cells and transitional cells. Using anti-ALCAM antibodies, submesothelial and mesothelial cells were isolated by FACS. The ALCAM(+) cells expressed hepatocyte growth factor and pleiotrophin. In culture, the ALCAM(+) cells rapidly acquired myofibroblastic morphology and alpha-SMA expression. The ALCAM(+) cells formed intracellular lipid droplets when embedded in collagen gel and treated with retinol, suggesting the potential for ALCAM(+) cells to differentiate to HSCs. Finally, we demonstrated that fetal HSCs, submesothelial cells, and perivascular mesenchymal cells are all derived from mesoderm by using MesP1-Cre and ROSA26 reporter mice. CONCLUSION: Fetal HSCs, submesothelial cells, and perivascular mesenchymal cells are mesodermal in origin, and ALCAM(+) submesothelial cells may be a precursor for HSCs in developing liver.
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The STM gives rise to the liver mesenchyme, which in the adult liver encompasses the mesothelium and hepatic stellate cells (HSCs).
“The STM gives rise to the liver mesenchyme, which in the adult liver encompasses the mesothelium, the external cellular lining of the liver, and hepatic stellate cells (HSCs), the sinusoidal pericytes”
From Single-Cell Transcriptomics Reveals Early Emergence of Liver Parenchymal and Non-parenchymal Cell Lineages (2020) · cites this paper as Asahina et al., 2009
The introductory passage (page unavailable) describes septum transversum mesenchyme (STM) as a proposed source of HSCs, but says its contribution had not been definitively established. The Results, “Cell Lineage Analysis of Liver Mesenchymal Cells” (page unavailable), traces fetal HSCs and submesothelial cells to mesoderm and finds that some liver mesothelial cells share that lineage; it does not establish that STM gives rise to all these cells or demonstrate the claimed lineage in adults. (LLM, conf=0.86)
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Cites
Generalized lacZ expression with the ROSA26 Cre reporter strain
Soriano, P. (1999) · Nature Genetics · doi:10.1038/5007 · Cited by 5,237 · see citing works
Hepatic Stellate Cells: Protean, Multifunctional, and Enigmatic Cells of the Liver
Friedman, S. L. (2008) · Physiological Reviews · doi:10.1152/physrev.00013.2007 · Cited by 2,842 · see citing works
TRANSCRIPTIONAL REGULATION OF GENE EXPRESSION DURING ADIPOCYTE DIFFERENTIATION
MacDougald, O. A., & Lane, M. D. (1995) · Annual Review of Biochemistry · doi:10.1146/annurev.bi.64.070195.002021 · Cited by 1,064 · see citing works
History, Heterogeneity, Developmental Biology, and Functions of Quiescent Hepatic Stellate Cells
Geerts, A. (2001) · Seminars in Liver Disease · doi:10.1055/s-2001-17550 · Cited by 740 · see citing works
Saga, Y., Miyagawa‐Tomita, S., Takagi, A., Kitajima, S., Miyazaki, J., & Inoue, T. (1999) · Development · doi:10.1242/dev.126.15.3437 · Cited by 607 · see citing works
Schmitt-Gräff, A., Krüger, S., Bochard, F., Gabbiani, G., & Denk, H. (1991) · PubMed Central · Cited by 331 · see citing works
Hazra, S., Xiong, S., Wang, J., Rippe, R. A., Krishna, V., Chatterjee, K., & Tsukamoto, H. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m310284200 · Cited by 320 · see citing works
Self-citationAdipogenic Transcriptional Regulation of Hepatic Stellate Cells*
She, H.-Y., Xiong, S., Hazra, S., & Tsukamoto, H. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m410078200 · Cited by 295 · see citing works
Self-citationVogel, S., Piantedosi, R., Frank, J., Lalazar, A., Rockey, D. C., Friedman, S. L., & Blaner, W. S. (2000) · Journal of Lipid Research · doi:10.1016/s0022-2275(20)32030-7 · Cited by 283 · see citing works
Hentsch, B., Lyons, I. G., Li, R., Hartley, L., Lints, T., Adams, J. M., & Harvey, R. P. (1996) · Genes & Development · doi:10.1101/gad.10.1.70 · Cited by 180 · see citing works
Han, Y., Zhou, L., Wang, J., Xiong, S., Garner, W. L., French, S. W., & Tsukamoto, H. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m310999200 · Cited by 153 · see citing works
Self-citationBerg, T., Rountree, B. C., Lee, L., Estrada, J. J., Sala, F. G., Choe, A., Veltmaat, J. M., Langhe, S. D., Lee, R., Tsukamoto, H., et al. (2007) · Hepatology · doi:10.1002/hep.21814 · Cited by 138 · see citing works
Self-citationKalinichenko, V. V., Bhattacharyya, D., Zhou, Y., Gusarova, G. A., Kim, W., Shin, B., & Costa, R. H. (2003) · Hepatology · doi:10.1053/jhep.2003.50005 · Cited by 135 · see citing works
Role of Mesenchymal Cell Populations in Porcine Serum–Induced Rat Liver Fibrosis
Bhunchet, E., & Wake, K. (1992) · Hepatology · doi:10.1002/hep.1840160623 · Cited by 128 · see citing works
Wt1 and retinoic acid signaling are essential for stellate cell development and liver morphogenesis
IJpenberg, A., Pérez-Pomares, J. M., Guadix, J. A., Carmona, R., Portillo-Sánchez, V., Macías, D., Hohenstein, P., Miles, C., Hastie, N. D., & Muñoz‐Chápuli, R. (2007) · Developmental Biology · doi:10.1016/j.ydbio.2007.09.014 · Cited by 126 · see citing works
Brugger, S. M., Merrill, A. E., Torres‐Vázquez, J., Wu, N. L., Ting, M.-C., Cho, J. Y.-M., Dobias, S. L., Yi, S. E., Lyons, K. M., Bell, J. R., et al. (2004) · Development · doi:10.1242/dev.01390 · Cited by 117 · see citing works
Self-citationLunter, P. C., van Kilsdonk, J. W. J., van Beek, H., Cornelissen, I. M. H. A., Bergers, M., Willems, P. H. G. M., van Muijen, G. N. P., & Swart, G. W. M. (2005) · Cancer Research · doi:10.1158/0008-5472.can-05-0378 · Cited by 110 · see citing works
Nitou, M., Sugiyama, Y., Ishikawa, K., & Shiojiri, N. (2002) · Experimental Cell Research · doi:10.1006/excr.2002.5615 · Cited by 95 · see citing works
Lhx2 <sup>–/–</sup> mice develop liver fibrosis
Wandzioch, E., Kolterud, Å., Jacobsson, M., Friedman, S. L., & Carlsson, L. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0404678101 · Cited by 95 · see citing works
Suzuki, K., Tanaka, M., Watanabe, N., Saito, S., Nonaka, H., & Miyajima, A. (2008) · Gastroenterology · doi:10.1053/j.gastro.2008.03.075 · Cited by 92 · see citing works
Asahina, K., Sato, H., Yamasaki, C., Kataoka, M., Shiokawa, M., Katayama, S., Tateno, C., & Yoshizato, K. (2002) · American Journal Of Pathology · doi:10.1016/s0002-9440(10)61167-4 · Cited by 86 · 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
Hepatic stellate cells do not derive from the neural crest
Cassiman, D. M., Barlow, A. J., Borght, S. V., Libbrecht, L. J., & Pachnis, V. (2005) · Journal of Hepatology · doi:10.1016/j.jhep.2005.09.023 · Cited by 83 · see citing works
Contribution of mesothelium‐derived cells to liver sinusoids in avian embryos
Pérez-Pomares, J. M., Carmona, R., González‐Iriarte, M., Macías, D., Guadix, J. A., & Muñoz‐Chápuli, R. (2004) · Developmental Dynamics · doi:10.1002/dvdy.10455 · Cited by 71 · see citing works
Ogawa, T., Tateno, C., Asahina, K., Fujii, H., Kawada, N., Obara, M., & Yoshizato, K. (2006) · Histochemistry and Cell Biology · doi:10.1007/s00418-006-0237-7 · Cited by 39 · see citing works
Self-citationOrigin of stellate cells from submesothelial cells in a developing human liver
Loo, C. K. C., & Wu, X. (2008) · Liver International · doi:10.1111/j.1478-3231.2008.01788.x · Cited by 36 · see citing works
Mansuroglu, T., Dudás, J., Elmaouhoub, A., Joza, T. Z., & Ramadori, G. P. (2009) · Histochemistry and Cell Biology · doi:10.1007/s00418-009-0596-y · Cited by 14 · see citing works
de Villeroché, V. J., & Brouty‐Boyé, D. (2008) · Cell Biology International · doi:10.1016/j.cellbi.2008.01.003 · Cited by 5 · see citing works
Enzan (1997) · doi:10.1002/(sici)1097-0029(19971115)39:4
Flagged first, then by citations
Cited by
Sorted by citations
Myofibroblasts revert to an inactive phenotype during regression of liver fibrosis
Kisseleva, T., Cong, M., Paik, Y., Scholten, D., Jiang, C., Benner, C., Iwaisako, K., Moore-Morris, T., Scott, B., Tsukamoto, H., et al. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1201840109 · Cited by 805 · see citing works
Self-citationOrganogenesis and development of the liver
Si-Tayeb, K., Lemaigre, F. P., & Duncan, S. A. (2010) · Developmental Cell · doi:10.1016/j.devcel.2010.01.011 · Cited by 800 · see citing works
Hepatic Stellate Cells and Liver Fibrosis
Puche, J. E., Saiman, Y., & Friedman, S. L. (2013) · Comprehensive physiology · doi:10.1002/cphy.c120035 · Cited by 736 · see citing works
Hepatic stellate cells in liver development, regeneration, and cancer
Yin, C., Evason, K. J., Asahina, K., & Stainier, D. Y. R. (2013) · Journal of Clinical Investigation · doi:10.1172/jci66369 · Cited by 719 · see citing works
Self-citationOrigin of myofibroblasts in the fibrotic liver in mice
Iwaisako, K., Jiang, C., Zhang, M., Cong, M., Moore-Morris, T. J., Park, T. J., Liu, X., Xu, J., Wang, P., Paik, Y.-H., et al. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1400062111 · Cited by 535 · see citing works
Platelets regulate lymphatic vascular development through CLEC-2–SLP-76 signaling
Bertozzi, C. C., Schmaier, A. A., Mericko, P. A., Hess, P. R., Zou, Z., Chen, M., Chen, C., Xu, B., Lu, M., Zhou, D. D., et al. (2010) · Blood · doi:10.1182/blood-2010-02-270876 · Cited by 432 · see citing works
The Power of Plasticity—Metabolic Regulation of Hepatic Stellate Cells
Trivedi, P., Wang, S., & Friedman, S. L. (2021) · Cell Metabolism · doi:10.1016/j.cmet.2020.10.026 · Cited by 427 · see citing works
StellaTUM: current consensus and discussion on pancreatic stellate cell research
Erkan, M., Adler, G., Apte, M. V., Bachem, M. G., Buchholz, M., Detlefsen, S., Esposito, I., Frieß, H., Gress, T. M., Habisch, H., et al. (2011) · Gut · doi:10.1136/gutjnl-2011-301220 · Cited by 411 · see citing works
Self-citationMassive and Reproducible Production of Liver Buds Entirely from Human Pluripotent Stem Cells
Takebe, T., Sekine, K., Kimura, M., Yoshizawa, E., Ayano, S., Koido, M., Funayama, S., Nakanishi, N., Hisai, T., Kobayashi, T., et al. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.11.005 · Cited by 405 · see citing works
Organotypic liver culture models: meeting current challenges in toxicity testing
LeCluyse, E. L., Witek, R. P., Andersen, M. E., & Powers, M. J. (2012) · Critical Reviews in Toxicology · doi:10.3109/10408444.2012.682115 · Cited by 363 · see citing works
Experimental models of liver fibrosis
Yanguas, S. C., Cogliati, B., Willebrords, J., Maes, M., Colle, I. O., Bossche, B. V. D., de Oliveira, C. P. M. S., Andraus, W., Alves, V. A. F., Leclercq, I. A., et al. (2015) · Archives of Toxicology · doi:10.1007/s00204-015-1543-4 · Cited by 351 · see citing works
Hepatic stellate cells in physiology and pathology
Kamm, D. R., & McCommis, K. S. (2022) · The Journal of Physiology · doi:10.1113/jp281061 · Cited by 351 · see citing works
Asahina, K., Zhou, B., Pu, W. T., & Tsukamoto, H. (2010) · Hepatology · doi:10.1002/hep.24119 · Cited by 308 · see citing works
Self-citationEpithelial‐to‐mesenchymal transitions in the liver†
Choi, S. S., & Diehl, A. M. (2009) · Hepatology · doi:10.1002/hep.23196 · Cited by 305 · see citing works
Portal fibroblasts: Underappreciated mediators of biliary fibrosis†
Dranoff, J. A., & Wells, R. G. (2010) · Hepatology · doi:10.1002/hep.23405 · Cited by 273 · see citing works
Coll, M., Perea, L., Boon, R., Leite, S. B., Vallverdú, J., Mannaerts, I., Smout, A., El Taghdouini, A., Blaya, D., Rodrigo-Torres, D., et al. (2018) · Cell Stem Cell · doi:10.1016/j.stem.2018.05.027 · Cited by 233 · see citing works
Liver fibrosis in NAFLD/NASH: from pathophysiology towards diagnostic and therapeutic strategies
Parola, M., & Pinzani, M. (2023) · Molecular Aspects of Medicine · doi:10.1016/j.mam.2023.101231 · Cited by 226 · see citing works
Choi, S. S., Omenetti, A., Witek, R. P., Moylan, C. A., Syn, W.-K., Jung, Y., Yang, L., Sudan, D. L., Sicklick, J. K., Michelotti, G. A., et al. (2009) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00292.2009 · Cited by 219 · see citing works
Li, Y., Wang, J., & Asahina, K. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1214136110 · Cited by 211 · see citing works
Self-citationTian, Y., Xu, J., Li, Y., Zhao, R., Du, S., Lv, C., Wu, W. H., Liu, R., Sheng, X., Song, Y., et al. (2019) · Gastroenterology · doi:10.1053/j.gastro.2019.02.023 · Cited by 215 · see citing works
Chu, A. S., Díaz, R., Hui, J., Yanger, K., Zong, Y., Alpini, G. D., Stanger, B. Z., & Wells, R. G. (2011) · Hepatology · doi:10.1002/hep.24206 · Cited by 207 · see citing works
Liu, X., Xu, J., Rosenthal, S., Zhang, L., McCubbin, R., Meshgin, N., Shang, L., Koyama, Y., Ma, H., Sharma, S., et al. (2020) · Gastroenterology · doi:10.1053/j.gastro.2020.01.027 · Cited by 205 · see citing works
Pancreatic stellate cell: Pandora's box for pancreatic disease biology
Bynigeri, R. R., Jakkampudi, A., Jangala, R., Subramanyam, C., Sasikala, M., Rao, G. V., Reddy, D. N., & Talukdar, R. (2017) · World Journal of Gastroenterology · doi:10.3748/wjg.v23.i3.382 · Cited by 179 · see citing works
Merrill, M. A. L., Karey, E., Moshier, E. L., Lindtner, C., Frano, M. R. L., Newman, J. W. I., & Buettner, C. (2014) · PLoS ONE · doi:10.1371/journal.pone.0103337 · Cited by 176 · see citing works
Cancer-associated fibroblasts in hepatocellular carcinoma
Kubo, N., Araki, K., Kuwano, H., & Shirabe, K. (2016) · World Journal of Gastroenterology · doi:10.3748/wjg.v22.i30.6841 · Cited by 173 · see citing works
Anti-fibrogenic strategies and the regression of fibrosis
Kisseleva, T., & Brenner, D. A. (2011) · Best Practice & Research Clinical Gastroenterology · doi:10.1016/j.bpg.2011.02.011 · Cited by 169 · see citing works
Hepatic stellate cells contribute to progenitor cells and liver regeneration
Kordes, C., Sawitza, I., Götze, S., Herebıan, D., & Häussinger, D. (2014) · Journal of Clinical Investigation · doi:10.1172/jci74119 · Cited by 170 · see citing works
Bondue, A., & Blanpain, C. (2010) · Circulation Research · doi:10.1161/circresaha.110.227058 · Cited by 169 · see citing works
An In Vitro Human Liver Model by iPSC-Derived Parenchymal and Non-parenchymal Cells
Koui, Y., Kido, T., Ito, T., Oyama, H., Chen, S.-W., Katou, Y., Shirahige, K., & Miyajima, A. (2017) · Stem Cell Reports · doi:10.1016/j.stemcr.2017.06.010 · Cited by 163 · see citing works
Lua, I., Li, Y., Zagory, J. A., Wang, K. S., French, S. W., Sévigny, J., & Asahina, K. (2016) · Journal of Hepatology · doi:10.1016/j.jhep.2016.01.010 · Cited by 153 · see citing works
Self-citationChen, Y., Chang, Y.-T., Pan, S., Chou, Y., Chang, F., Yeh, P.-Y., Liu, Y.-H., Chiang, W., Chen, Y., Wu, K., et al. (2014) · Journal of the American Society of Nephrology · doi:10.1681/asn.2013101079 · Cited by 151 · see citing works
Friend or foe? The elusive role of hepatic stellate cells in liver cancer
Cogliati, B., Yashaswini, C. N., Wang, S., Sia, D., & Friedman, S. L. (2023) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/s41575-023-00821-z · Cited by 157 · see citing works
Liver regeneration requires Yap1-TGFβ-dependent epithelial-mesenchymal transition in hepatocytes
Oh, S.-H., Swiderska-Syn, M., Jewell, M. L., Premont, R. T., & Diehl, A. M. (2018) · Journal of Hepatology · doi:10.1016/j.jhep.2018.05.008 · Cited by 148 · see citing works
Single-cell atlas of human liver development reveals pathways directing hepatic cell fates
Wesley, B. T., Ross, A. D. B., Muraro, D., Miao, Z., Saxton, S., Tomaz, R. A., Morell, C. M., Ridley, K., Zacharis, E. D., Petrus-Reurer, S., et al. (2022) · Nature Cell Biology · doi:10.1038/s41556-022-00989-7 · Cited by 146 · see citing works
The niche of stellate cells within rat liver #
Sawitza, I., Kordes, C., Reister, S., & Häussinger, D. (2009) · Hepatology · doi:10.1002/hep.23184 · Cited by 142 · see citing works
Hepatic stellate cells—the pericytes in the liver
Hellerbrand, C. (2013) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-012-1209-5 · Cited by 144 · see citing works
Liver stem/progenitor cells: their characteristics and regulatory mechanisms
Tanaka, M., Itoh, T., Tanimizu, N., & Miyajima, A. (2011) · The Journal of Biochemistry · doi:10.1093/jb/mvr001 · Cited by 135 · see citing works
Liver Organoids: Recent Developments, Limitations and Potential
Harrison, S. P., Baumgarten, S., Verma, R., Lunov, O., Dejneka, A., & Sullivan, G. J. (2021) · Frontiers in Medicine · doi:10.3389/fmed.2021.574047 · Cited by 141 · see citing works
The characteristics of activated portal fibroblasts/myofibroblasts in liver fibrosis
Karin, D., Koyama, Y., Brenner, D. A., & Kisseleva, T. (2016) · Differentiation · doi:10.1016/j.diff.2016.07.001 · Cited by 133 · see citing works
Yang, M. D., Chiang, Y., Higashiyama, R., Asahina, K., Mann, D. A., Mann, J., Wang, C. C. C., & Tsukamoto, H. (2011) · Hepatology · doi:10.1002/hep.24792 · Cited by 131 · see citing works
Self-citationWang, 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
The types of hepatic myofibroblasts contributing to liver fibrosis of different etiologies
Xu, J., Liu, X., Koyama, Y., Wang, P., Lan, T., Kim, I., Kim, I. H., Ma, H., & Kisseleva, T. (2014) · Frontiers in Pharmacology · doi:10.3389/fphar.2014.00167 · Cited by 126 · see citing works
Forbes, S. J., & Parola, M. (2011) · Best Practice & Research Clinical Gastroenterology · doi:10.1016/j.bpg.2011.02.006 · Cited by 113 · see citing works
Erkan, M., Weis, N., Zheng, P., Schwager, C., Samkharadze, T., Jiang, X., Wirkner, U., Giese, N. A., Ansorge, W. J., Debus, J., et al. (2010) · Molecular Cancer · doi:10.1186/1476-4598-9-88 · Cited by 107 · see citing works
Brade, T., Kumar, S., Cunningham, T. J., Chatzi, C. A., Zhao, X., Cavallero, S., Li, P., Sucov, H. M., Ruiz‐Lozano, P., & Duester, G. (2010) · Development · doi:10.1242/dev.054239 · Cited by 103 · see citing works
Self-citationStellate Cells in Tissue Repair, Inflammation, and Cancer
Sherman, M. H. (2018) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-100617-062855 · Cited by 102 · see citing works
Macrophages and Fibroblasts, Key Players in Cancer Chemoresistance
Ireland, L., & Mielgo, A. (2018) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2018.00131 · Cited by 105 · see citing works
Evidence for and against epithelial-to-mesenchymal transition in the liver
Xie, G., & Diehl, A. M. (2013) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00289.2013 · Cited by 98 · see citing works
The phenotypic fate and functional role for bone marrow-derived stem cells in liver fibrosis
Kisseleva, T., & Brenner, D. A. (2011) · Journal of Hepatology · doi:10.1016/j.jhep.2011.09.021 · Cited by 93 · see citing works
Hepatic Stellate Cells and Liver Fibrosis
Puche, J. E., Saiman, Y., & Friedman, S. L. (2013) · Comprehensive Physiology · doi:10.1002/j.2040-4603.2013.tb00529.x · Cited by 89 · see citing works
Sancho‐Bru, P., Roelandt, P. R., Narain, N., Pauwelyn, K. A., Notelaers, T., Shimizu, T., Ott, M., & Verfaillie, C. M. (2010) · Journal of Hepatology · doi:10.1016/j.jhep.2010.06.014 · Cited by 89 · see citing works
Nakano, Y., Kamiya, A., Sumiyoshi, H., Tsuruya, K., Kagawa, T., & Inagaki, Y. (2020) · Hepatology · doi:10.1002/hep.30965 · Cited by 86 · see citing works
Lotto, J., Drissler, S., Cullum, R., Wei, W., Setty, M., Bell, E. M., Boutet, S. C., Nowotschin, S., Kuo, Y.-Y., Garg, V., et al. (2020) · Cell · doi:10.1016/j.cell.2020.09.012 · Cited by 86 · see citing works
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Zhu, N., Asahina, K., Wang, J., Ueno, A. M., Lazaro, R. G., Miyaoka, Y., Miyajima, A., & Tsukamoto, H. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.312751 · Cited by 85 · see citing works
Self-citationThe role of stem cells in liver repair and fibrosis
Greenbaum, L. E., & Wells, R. G. (2009) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2009.11.006 · Cited by 83 · see citing works
Cellular and Molecular Basis of Liver Development
Shin, D., & Monga, S. P. (2013) · Comprehensive physiology · doi:10.1002/cphy.c120022 · Cited by 90 · see citing works
Koopmans, T., & Rinkevich, Y. (2018) · Communications Biology · doi:10.1038/s42003-018-0180-x · Cited by 78 · see citing works
Characterization and Functional Analyses of Hepatic Mesothelial Cells in Mouse Liver Development
Onitsuka, I., Tanaka, M., & Miyajima, A. (2010) · Gastroenterology · doi:10.1053/j.gastro.2009.12.059 · Cited by 77 · see citing works
Next-Generation Liver Medicine Using Organoid Models
Akbari, S., Arslan, N., Senturk, S., & Erdal, E. (2019) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2019.00345 · Cited by 72 · see citing works
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Wu, Y. F., Zhang, C., Jiang, K., Werner, J. M., Bazhin, A. V., & D’Haese, J. G. (2021) · Frontiers in Oncology · doi:10.3389/fonc.2020.621937 · Cited by 70 · see citing works
Cell Signals Influencing Hepatic Fibrosis
Cong, M., Iwaisako, K., Jiang, C., & Kisseleva, T. (2012) · International Journal of Hepatology · doi:10.1155/2012/158547 · Cited by 70 · see citing works
Pancreatic stellate cells – Multi-functional cells in the pancreas
Masamune, A., & Shimosegawa, T. (2013) · Pancreatology · doi:10.1016/j.pan.2012.12.058 · Cited by 69 · see citing works
Myofibroblastic Conversion and Regeneration of Mesothelial Cells in Peritoneal and Liver Fibrosis
Lua, I., Li, Y., Pappoe, L. S., & Asahina, K. (2015) · American Journal Of Pathology · doi:10.1016/j.ajpath.2015.08.009 · Cited by 63 · see citing works
Self-citationWang, S., Miller, S. R., Ober, E. A., & Sadler, K. C. (2017) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/bs.ctdb.2016.11.012 · Cited by 61 · see citing works
GATA4 loss in the septum transversum mesenchyme promotes liver fibrosis in mice
Delgado‐Sainz, I., Carrasco, M., Cano, E., Carmona, R., García‐Carbonero, R., Gómez, L. M. M., Soria, B., Martín, F., Cano, D. A., Muñoz‐Chápuli, R., et al. (2014) · Hepatology · doi:10.1002/hep.27005 · Cited by 60 · see citing works
Fibrotic Events in the Progression of Cholestatic Liver Disease
Wu, H., Chen, C., Ziani, S., Nelson, L. J., Avila, M. A., Nevzorova, Y. A., & Cubero, F. J. (2021) · Cells · doi:10.3390/cells10051107 · Cited by 59 · see citing works
Epigenetic cell fate regulation of hepatic stellate cells
Tsukamoto, H., Zhu, N., Asahina, K., Mann, D. A., & Mann, J. (2011) · Hepatology Research · doi:10.1111/j.1872-034x.2011.00804.x · Cited by 57 · see citing works
Self-citationHepatic stellate cell progenitor cells
Asahina, K. (2012) · Journal of Gastroenterology and Hepatology · doi:10.1111/j.1440-1746.2011.07001.x · Cited by 57 · see citing works
Self-citationMesenchymal stem cells: potential application for the treatment of hepatic cirrhosis
Zhang, Y., Li, Y., Zhang, L., Li, J., & Zhu, C. (2018) · Stem Cell Research & Therapy · doi:10.1186/s13287-018-0814-4 · Cited by 57 · see citing works
Lua, I., James, D., Wang, J., Wang, K. S., & Asahina, K. (2014) · Hepatology · doi:10.1002/hep.27035 · Cited by 55 · see citing works
Self-citationThe Role of Mesothelial Cells in Liver Development, Injury, and Regeneration
Lua, I., & Asahina, K. (2016) · Gut and Liver · doi:10.5009/gnl15226 · Cited by 55 · see citing works
Self-citationDiverse properties of the mesothelial cells in health and disease
Kawanishi, K. (2016) · Pleura and Peritoneum · doi:10.1515/pp-2016-0009 · Cited by 56 · see citing works
Shentu, Y., Li, Y., Xie, S., Jiang, H., Sun, S., Lin, R., Chen, C., Bai, Y., Zhang, Y., Zheng, C., et al. (2021) · International Immunopharmacology · doi:10.1016/j.intimp.2021.107374 · Cited by 55 · see citing works
Berardis, S., Lombard, C. A., Evraerts, J., Taghdouini, A. E., Rosseels, V., Sancho‐Bru, P., Lozano, J. J., van Grunsven, L. A., Sokal, E. M., & Najimi, M. (2014) · PLoS ONE · doi:10.1371/journal.pone.0086137 · Cited by 55 · see citing works
Zhu, N., Wang, J., & Tsukamoto, H. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.156703 · Cited by 55 · see citing works
Self-citationCastilho–Fernandes, A., de Almeida, D. C., Fontes, A. M., Melo, F. U. F., Picanço‐Castro, V., de Freitas, M. C. C., Orellana, M. D., Palma, P. V. B., Hackett, P. B., Friedman, S. L., et al. (2011) · Experimental and Molecular Pathology · doi:10.1016/j.yexmp.2011.09.002 · Cited by 56 · see citing works
Post-Surgical Peritoneal Scarring and Key Molecular Mechanisms
Herrick, S. E., & Wilm, B. (2021) · Biomolecules · doi:10.3390/biom11050692 · Cited by 53 · see citing works
Mesenchymal Stem Cells in the Adult Human Liver: Hype or Hope?
Kholodenko, I. V., Kurbatov, L. K., Kholodenko, R. V., Manukyan, G. V., & Yarygin, K. N. (2019) · Cells · doi:10.3390/cells8101127 · Cited by 52 · see citing works
Perivascular Mesenchymal Progenitors in Human Fetal and Adult Liver
Gerlach, J. C., Over, P., Turner, M. E., Thompson, R. L., Foka, H. G., Chen, W. C. W., Péault, B., Gridelli, B. G., & Schmelzer, E. (2012) · Stem Cells and Development · doi:10.1089/scd.2012.0296 · Cited by 50 · see citing works
Bobowski, M., Zummo, F. P., Staels, B., Lefèbvre, P., & Eeckhoute, J. (2018) · Cells · doi:10.3390/cells7090137 · Cited by 49 · see citing works
Kostallari, E., & Shah, V. H. (2019) · Advances in experimental medicine and biology · doi:10.1007/978-3-030-11093-2_9 · Cited by 49 · see citing works
Bone marrow contributes to the population of pancreatic stellate cells in mice
Watanabe, T., Masamune, A., Kikuta, K., Hirota, M., Kume, K., Satoh, K., & Shimosegawa, T. (2009) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00123.2009 · Cited by 48 · see citing works
Crosstalk Between the Hepatic and Hematopoietic Systems During Embryonic Development
Soares‐da‐Silva, F., Peixoto, M. M., Cumano, A., & Pinto‐do‐Ó, P. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.00612 · Cited by 45 · see citing works
Fetal liver development and implications for liver disease pathogenesis
Lotto, J., Stephan, T. L., & Hoodless, P. A. (2023) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/s41575-023-00775-2 · Cited by 47 · see citing works
An Eye on Kupffer Cells: Development, Phenotype and the Macrophage Niche
Elchaninov, A. V., Vishnyakova, P., Menyailo, E., Sukhikh, G. T., & Fatkhudinov, T. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23179868 · Cited by 47 · see citing works
Meurer, S. K., Alsamman, M., Sahin, H., Wasmuth, H. E., Kisseleva, T., Brenner, D. A., Trautwein, C., Weiskirchen, R., & Scholten, D. (2013) · PLoS ONE · doi:10.1371/journal.pone.0056116 · Cited by 47 · see citing works
Directed differentiation of human induced pluripotent stem cells to hepatic stellate cells
Vallverdú, J., de la Torre, R. A. M. G., Mannaerts, I., Verhulst, S., Smout, A., Coll, M., Ariño, S., Rubio‐Tomás, T., Aguilar‐Bravo, B., Martínez–Sánchez, C., et al. (2021) · Nature Protocols · doi:10.1038/s41596-021-00509-1 · Cited by 47 · see citing works
Clinical Implications of Advances in the Basic Science of Liver Repair and Regeneration
Karp, S. J. (2009) · American Journal of Transplantation · doi:10.1111/j.1600-6143.2009.02731.x · Cited by 43 · see citing works
Activation of hepatic stellate cell in Pten null liver injury model
He, L., Gubbins, J., Peng, Z., Medina, V., Fei, F., Asahina, K., Wang, J., Kahn, M., Rountree, C. B., & Stiles, B. L. (2016) · Fibrogenesis & Tissue Repair · doi:10.1186/s13069-016-0045-1 · Cited by 44 · see citing works
Self-citationZhou, Y., Fan, J., Zheng, C., Yin, P., Wu, H., Li, X., Luo, N., Yu, X., & Chen, C. (2018) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2018.10.106 · Cited by 43 · see citing works
Modulation of retinoid signaling: therapeutic opportunities in organ fibrosis and repair
Wang, S., Yu, J., Kane, M. A., & Moise, A. R. (2019) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2019.107415 · Cited by 43 · see citing works
Determining the fate of hepatic cells by lineage tracing: Facts and pitfalls
Lemaigre, F. P. (2014) · Hepatology · doi:10.1002/hep.27659 · Cited by 43 · see citing works
Hepatic stellate cells: fibrogenic, regenerative or both? Heterogeneity and context are key
Bansal, M. B. (2016) · Hepatology International · doi:10.1007/s12072-016-9758-x · Cited by 42 · see citing works
Trasino, S. E., Tang, X., Jessurun, J., & Gudas, L. J. (2016) · Journal of Molecular Medicine · doi:10.1007/s00109-016-1434-z · Cited by 41 · see citing works
Michelotti, G. A., Tucker, A., Swiderska-Syn, M., Machado, M. V., Choi, S. S., Kruger, L., Soderblom, E., Thompson, J. W., Mayer-Salman, M., Himburg, H. A., et al. (2016) · Gut · doi:10.1136/gutjnl-2014-308176 · Cited by 40 · see citing works
PDGFRα in Liver Pathophysiology: Emerging Roles in Development, Regeneration, Fibrosis, and Cancer
Kikuchi, A., & Monga, S. P. (2015) · Gene Expression · doi:10.3727/105221615x14181438356210 · Cited by 42 · see citing works
Morphogens and hepatic stellate cell fate regulation in chronic liver disease
Tsukamoto, H., Zhu, N., Wang, J., Asahina, K., & Machida, K. (2012) · Journal of Gastroenterology and Hepatology · doi:10.1111/j.1440-1746.2011.07022.x · Cited by 37 · see citing works
Self-citationZhou, Y., Sun, B., Li, W., Zhou, J., Gao, F., Wang, X., Cai, M., & Sun, Z. (2019) · Frontiers in Physiology · doi:10.3389/fphys.2019.00218 · Cited by 37 · see citing works
Targeting the tumor microenvironment in pancreatic ductal adenocarcinoma
Pandey, V., & Störz, P. (2019) · Expert Review of Anticancer Therapy · doi:10.1080/14737140.2019.1622417 · Cited by 37 · see citing works
Colunga, T., Hayworth, M. K., Kreß, S., Reynolds, D. M., Chen, L., Nazor, K. L., Baur, J., Singh, A. M., Loring, J. F., Metzger, M., et al. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.02.016 · Cited by 33 · see citing works
- Authors
- Asahina, K., Tsai, S. Y., Li, P., Ishii, M., Maxson, R. E., Sucov, H. M., & Tsukamoto, H.
- Affiliations
- University of Southern California (US)
- Corresponding author
- Asahina, Kinji
- Venue
- Hepatology
- Published
- 2009-03
- Volume
- 49
- Issue
- 3
- Pages
- 998-1011
- ISSN
- 0270-9139 (ISSN-L)
- PMC
- PMC2673117
- OpenAlex
- W2091764094
- Cited by
- 238
- References
- 29
- Citations by year
- 2026: 8 · 2025: 10 · 2024: 6 · 2023: 15 · 2022: 6 · 2021: 15 · 2020: 11 · 2019: 15 · 2018: 18 · 2017: 12 · 2016: 13 · 2015: 20 · 2014: 19 · 2013: 15 · 2012: 17
- FWCI
- 9.09
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Hepatology (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute on Alcohol Abuse and Alcoholism (R24 AA12885, P50-AA11999, R24AA012885, P50AA011999)
- Topics
- Health Sciences › Medicine › Hepatology › Liver physiology and pathology
- Health Sciences › Medicine › Genetics › Mesenchymal stem cell research
- Health Sciences › Medicine › Epidemiology › Liver Disease Diagnosis and Treatment
- Keywords
- hepatic stellate cells, fetal liver development, mesodermal origin, ALCAM, mesothelial cells, cell lineage, myofibroblast differentiation, lipid droplets, hepatocyte growth factor, pleiotrophin, alpha-smooth muscle actin, podoplanin, Ki-67 proliferation index, mouse liver
- MeSH terms
- Podoplanin, Animals, Cell Differentiation, Cells, Cultured, Desmin, Endothelium, Vascular, Epithelial Cells, Female, Lac Operon, Liver, Male, Membrane Glycoproteins, Mice, Transgenic, Receptors, Nerve Growth Factor, Homeodomain Proteins, Activated-Leukocyte Cell Adhesion Molecule, Organogenesis, Mice, Basic Helix-Loop-Helix Transcription Factors, Basic Helix-Loop-Helix Proteins, Hepatic Stellate Cells, Mesenchymal Stem Cells
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