Fetal liver development and implications for liver disease pathogenesis
Abstract
The metabolic, digestive and homeostatic roles of the liver are dependent on proper crosstalk and organization of hepatic cell lineages. These hepatic cell lineages are derived from their respective progenitors early in organogenesis in a spatiotemporally controlled manner, contributing to the liver's specialized and diverse microarchitecture. Advances in genomics, lineage tracing and microscopy have led to seminal discoveries in the past decade that have elucidated liver cell lineage hierarchies. In particular, single-cell genomics has enabled researchers to explore diversity within the liver, especially early in development when the application of bulk genomics was previously constrained due to the organ's small scale, resulting in low cell numbers. These discoveries have substantially advanced our understanding of cell differentiation trajectories, cell fate decisions, cell lineage plasticity and the signalling microenvironment underlying the formation of the liver. In addition, they have provided insights into the pathogenesis of liver disease and cancer, in which developmental processes participate in disease emergence and regeneration. Future work will focus on the translation of this knowledge to optimize in vitro models of liver development and fine-tune regenerative medicine strategies to treat liver disease. In this Review, we discuss the emergence of hepatic parenchymal and non-parenchymal cells, advances that have been made in in vitro modelling of liver development and draw parallels between developmental and pathological processes.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Cites
Mizgerd, J. P., Kubo, H., Kutkoski, G. J., Bhagwan, S. D., Scharffetter-Kochanek, K., Beaudet, A. L., & Doerschuk, C. M. (1997) · The Journal of Experimental Medicine · doi:10.1084/jem.186.8.1357 · Cited by 7,332 · see citing works
Tissue-resident macrophages originate from yolk-sac-derived erythro-myeloid progenitors
Gomez Perdiguero, E., Klapproth, K., Schulz, C., Busch, K., Azzoni, E., Crozet, L., Garner, H., Trouillet, C., de Bruijn, M. F., Geissmann, F., et al. (2015) · Nature · doi:10.1038/nature13989 · Cited by 2,339 · see citing works
Vascularized and functional human liver from an iPSC-derived organ bud transplant
Takebe, T., Sekine, K., Enomura, M., Koike, H., Kimura, M., Ogaeri, T., Zhang, R.-R., Ueno, Y., Zheng, Y.-W., Koike, N., et al. (2013) · Nature · doi:10.1038/nature12271 · Cited by 2,170 · see citing works
Landscape of Infiltrating T Cells in Liver Cancer Revealed by Single-Cell Sequencing
Zheng, C., Zheng, L., Yoo, J.-K., Guo, H., Zhang, Y., Guo, X., Kang, B., Hu, R., Huang, J. Y., Zhang, Q., et al. (2017) · Cell · doi:10.1016/j.cell.2017.05.035 · Cited by 2,152 · see citing works
Endothelial and perivascular cells maintain haematopoietic stem cells
Ding, L., Saunders, T. L., Enikolopov, G., & Morrison, S. J. (2012) · Nature · doi:10.1038/nature10783 · Cited by 1,934 · see citing works
Resolving the fibrotic niche of human liver cirrhosis at single-cell level
Ramachandran, P., Dobie, R., Wilson-Kanamori, J. R., Dora, E. F., Henderson, B. E. P., Luu, N. T., Portman, J. R., Matchett, K. P., Brice, M., Marwick, J. A., et al. (2019) · Nature · doi:10.1038/s41586-019-1631-3 · Cited by 1,784 · see citing works
Exploring tissue architecture using spatial transcriptomics
Rao, A., Barkley, D., França, G. S., & Yanai, I. (2021) · Nature · doi:10.1038/s41586-021-03634-9 · Cited by 1,700 · see citing works
SoupX removes ambient RNA contamination from droplet-based single-cell RNA sequencing data
Young, M. D., & Behjati, S. (2020) · GigaScience · doi:10.1093/gigascience/giaa151 · Cited by 1,619 · see citing works
Pioneer transcription factors: establishing competence for gene expression
Zaret, K. S., & Carroll, J. S. (2011) · Genes & Development · doi:10.1101/gad.176826.111 · Cited by 1,589 · see citing works
Single cell RNA sequencing of human liver reveals distinct intrahepatic macrophage populations
MacParland, S. A., Liu, J. C., Ma, X.-Z., Innes, B. T., Bartczak, A. M., Gage, B. K., Manuel, J., Khuu, N., Echeverri, J., Linares, I., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-06318-7 · Cited by 1,552 · see citing works
Definitive Hematopoiesis Is Autonomously Initiated by the AGM Region
Medvinsky, A., & Dzierzak, E. A. (1996) · Cell · doi:10.1016/s0092-8674(00)80165-8 · Cited by 1,548 · see citing works
Mederacke, I., Hsu, C. C., Troeger, J. S., Huebener, P., Mu, X., Dapito, D. H., Pradere, J.-P., & Schwabe, R. F. (2013) · Nature Communications · doi:10.1038/ncomms3823 · Cited by 1,443 · see citing works
Highly efficient generation of human hepatocyte-like cells from induced pluripotent stem cells
Si-Tayeb, K., Noto, F. K., Nagaoka, M., Li, J., Battle, M. A., Duris, C., North, P. E., Dalton, S., & Duncan, S. A. (2010) · Hepatology · doi:10.1002/hep.23354 · Cited by 1,282 · see citing works
Alagille syndrome is caused by mutations in human Jagged1, which encodes a ligand for Notch1
Li, L., Krantz, I. D., Deng, Y., Genin, A., Banta, A. B., Collins, C. C., Qi, M., Trask, B. J., Kuo, W. L., Cochran, J., et al. (1997) · Nature Genetics · doi:10.1038/ng0797-243 · Cited by 1,277 · see citing works
Tie2-Cre Transgenic Mice: A New Model for Endothelial Cell-Lineage Analysis in Vivo
Kisanuki, Y. Y., Hammer, R. E., Miyazaki, J.-I., Williams, S. C., Richardson, J. A., & Yanagisawa, M. (2001) · Developmental Biology · doi:10.1006/dbio.2000.0106 · Cited by 1,241 · see citing works
A human liver cell atlas reveals heterogeneity and epithelial progenitors
Aizarani, N., Saviano, A., Sagar, Mailly, L., Durand, S., Herman, J. S., Pessaux, P., Baumert, T. F., & Grün, D. (2019) · Nature · doi:10.1038/s41586-019-1373-2 · Cited by 1,147 · see citing works
Hayhurst, G. P., Lee, Y.-H., Lambert, G., Ward, J. M., & Gonzalez, F. J. (2001) · Molecular and Cellular Biology · doi:10.1128/mcb.21.4.1393-1403.2001 · Cited by 1,107 · see citing works
Single-cell spatial reconstruction reveals global division of labour in the mammalian liver
Halpern, K. B., Shenhav, R., Matcovitch-Natan, O., Tóth, B., Lemze, D., Golan, M., Massasa, E. E., Baydatch, S., Landen, S., Moor, A. E., et al. (2017) · Nature · doi:10.1038/nature21065 · Cited by 1,059 · see citing works
A single-cell molecular map of mouse gastrulation and early organogenesis
Pijuan-Sala, B., Griffiths, J. A., Guibentif, C., Hiscock, T. W., Jawaid, W., Calero-Nieto, F. J., Mulas, C., Ibarra-Soria, X., Tyser, R. C. V., Ho, D. L. L., et al. (2019) · Nature · doi:10.1038/s41586-019-0933-9 · Cited by 1,033 · see citing works
Human MAIT cells are xenobiotic-resistant, tissue-targeted, CD161hi IL-17–secreting T cells
Dusséaux, M., Martin, E., Serriari, N., Péguillet, I., Prémel, V., Louis, D., Milder, M., Bourhis, L. L., Soudais, C., Treiner, E., et al. (2010) · Blood · doi:10.1182/blood-2010-08-303339 · Cited by 1,031 · see citing works
Epicardial progenitors contribute to the cardiomyocyte lineage in the developing heart
Zhou, B., Ma, Q., Rajagopal, S., Wu, S. M., Domian, I., Rivera-Feliciano, J., Jiang, D., von Gise, A., Ikeda, S., Chien, K. R., et al. (2008) · Nature · doi:10.1038/nature07060 · Cited by 1,019 · see citing works
Runx1 is required for the endothelial to haematopoietic cell transition but not thereafter
Chen, M. J., Yokomizo, T., Zeigler, B. M., Dzierzak, E. A., & Speck, N. A. (2009) · Nature · doi:10.1038/nature07619 · Cited by 1,016 · see citing works
Liver regeneration: biological and pathological mechanisms and implications
Michalopoulos, G. K., & Bhushan, B. (2021) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/s41575-020-0342-4 · Cited by 998 · see citing works
Deterministically patterned biomimetic human iPSC-derived hepatic model via rapid 3D bioprinting
Ma, X., Qu, X., Zhu, W. Z., Li, Y.-S. J., Yuan, S., Zhang, H., Liu, J., Wang, P., Lai, C. S. E., Zanella, F., et al. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1524510113 · Cited by 881 · see citing works
Hartley, J., Davenport, M., & Kelly, D. A. (2009) · The Lancet · doi:10.1016/s0140-6736(09)60946-6 · Cited by 880 · see citing works
Liver Organogenesis Promoted by Endothelial Cells Prior to Vascular Function
Matsumoto, K., Yoshitomi, H., Rossant, J., & Zaret, K. S. (2001) · Science · doi:10.1126/science.1063889 · Cited by 877 · see citing works
Bone marrow-derived monocytes give rise to self-renewing and fully differentiated Kupffer cells
Scott, C. L., Zheng, F., De Baetselier, P., Martens, L., Saeys, Y., De Prijck, S., Lippens, S., Abels, C., Schoonooghe, S., Raes, G., et al. (2016) · Nature Communications · doi:10.1038/ncomms10321 · Cited by 860 · see citing works
Role of Kupffer cells in host defense and liver disease
Bilzer, M., Roggel, F., & Gerbes, A. L. (2006) · Liver International · doi:10.1111/j.1478-3231.2006.01342.x · Cited by 857 · see citing works
Long-Term Expansion of Functional Mouse and Human Hepatocytes as 3D Organoids
Hu, H., Gehart, H., Artegiani, B., LÖpez-Iglesias, C., Dekkers, F., Basak, O., van Es, J., Chuva de Sousa Lopes, S. M., Begthel, H., Korving, J., et al. (2018) · Cell · doi:10.1016/j.cell.2018.11.013 · Cited by 837 · see citing works
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
NOTCH2 Mutations Cause Alagille Syndrome, a Heterogeneous Disorder of the Notch Signaling Pathway
McDaniell, R. M., Warthen, D. M., Sanchez-Lara, P. A., Pai, A. A., Krantz, I. D., Piccoli, D. A., & Spinner, N. B. (2006) · The American Journal of Human Genetics · doi:10.1086/505332 · Cited by 747 · see citing works
Kattman, S. J., Huber, T. L., & Keller, G. M. (2006) · Developmental Cell · doi:10.1016/j.devcel.2006.10.002 · Cited by 730 · see citing works
Initiation of Mammalian Liver Development from Endoderm by Fibroblast Growth Factors
Jung, J., Zheng, M., Goldfarb, M., & Zaret, K. S. (1999) · Science · doi:10.1126/science.284.5422.1998 · Cited by 721 · see citing works
Wisse, E., Zanger, R. D., Charels, K., Smissen, P. V. D., & McCuskey, R. S. (1985) · Hepatology · doi:10.1002/hep.1840050427 · Cited by 712 · see citing works
Alagille, D., Odièvre, M., Gautier, M., et al. (1975) · The Journal of Pediatrics · doi:10.1016/s0022-3476(75)80706-2 · Cited by 696 · see citing works
Fate tracing reveals the endothelial origin of hematopoietic stem cells
Zovein, A. C., Hofmann, J. J., Lynch, M., French, W. J., Turlo, K. A., Yang, Y., Becker, M. S., Zanetta, L., Dejana, E., Gasson, J. C., et al. (2008) · Cell Stem Cell · doi:10.1016/j.stem.2008.09.018 · Cited by 691 · see citing works
Sharma, A., Seow, J. J. W., Dutertre, C.-A., Pai, R., Blériot, C., Mishra, A., Wong, R. M. M., Singh, G. S. N., Sudhagar, S., Khalilnezhad, S., et al. (2020) · Cell · doi:10.1016/j.cell.2020.08.040 · Cited by 677 · see citing works
An electron microscopic study of the fenestrated endothelial lining of rat liver sinusoids
Wisse, E. (1970) · Journal of Ultrastructure Research · doi:10.1016/s0022-5320(70)90150-4 · Cited by 655 · see citing works
Alagille, D., Estrada, A., Hadchouel, M., Gautler, M., Odièvre, M., & Dommergues, J. P. (1987) · The Journal of Pediatrics · doi:10.1016/s0022-3476(87)80153-1 · Cited by 650 · see citing works
Rossi, J. M., Dunn, N. R., Hogan, B. L. M., & Zaret, K. S. (2001) · Genes & Development · doi:10.1101/gad.904601 · Cited by 646 · see citing works
Decoding human fetal liver haematopoiesis
Popescu, D.-M., Botting, R. A., Stephenson, E., Green, K., Webb, S., Jardine, L., Calderbank, E. F., Polanski, K., Goh, I., Efremova, M., et al. (2019) · Nature · doi:10.1038/s41586-019-1652-y · Cited by 606 · see citing works
Hepatic specification of the gut endoderm in vitro: cell signaling and transcriptional control.Preprint
Gualdi, R., Bossard, P., Zheng, M., Hamada, Y., Coleman, J. R., & Zaret, K. S. (1996) · Genes & Development · doi:10.1101/gad.10.13.1670 · Cited by 590 · see citing works
The initiation of liver development is dependent on Foxa transcription factors
Lee, C. S., Friedman, J. R., Fulmer, J. T., & Kaestner, K. H. (2005) · Nature · doi:10.1038/nature03649 · Cited by 581 · see citing works
Lineage tracing demonstrates the venous origin of the mammalian lymphatic vasculaturePreprint
Srinivasan, R. S., Dillard, M. E., Lagutin, O. V., Lin, F., Tsai, S. Y., Tsai, M., Samokhvalov, I. M., & Oliver, G. C. (2007) · Genes & Development · doi:10.1101/gad.1588407 · Cited by 580 · see citing works
Global Epidemiology of Chronic Liver Disease
Cheemerla, S., & Balakrishnan, M. (2021) · Clinical Liver Disease · doi:10.1002/cld.1061 · Cited by 571 · see citing works
Immunomodulation by endothelial cells — partnering up with the immune system?
Amersfoort, J., Eelen, G., & Carmeliet, P. (2022) · Nature reviews. Immunology · doi:10.1038/s41577-022-00694-4 · Cited by 549 · see citing works
Modeling Steatohepatitis in Humans with Pluripotent Stem Cell-Derived Organoids
Ouchi, R., Togo, S., Kimura, M., Shinozawa, T., Koido, M., Koike, H., Thompson, W., Karns, R. A., Mayhew, C. N., McGrath, P. S., et al. (2019) · Cell Metabolism · doi:10.1016/j.cmet.2019.05.007 · Cited by 537 · see citing works
Bipotential Adult Liver Progenitors Are Derived from Chronically Injured Mature Hepatocytes
Tarlow, B. D., Pelz, C., Naugler, W. E., Wakefield, L., Wilson, E. M., Finegold, M. J., & Grompe, M. (2014) · Cell Stem Cell · doi:10.1016/j.stem.2014.09.008 · Cited by 533 · see citing works
Cholangiocarcinomas can originate from hepatocytes in mice
Fan, B., Malato, Y., Calvisi, D. F., Naqvi, S., Razumilava, N., Ribback, S., Gores, G. J., Dombrowski, F., Evert, M., Chen, X., et al. (2012) · Journal of Clinical Investigation · doi:10.1172/jci63212 · Cited by 529 · see citing works
Solar, M., Cardalda, C., Houbracken, I., Martín, M., Maestro, M., Demedts, N., Xu, X.-B., Grau, V., Heimberg, H., Bouwens, L., et al. (2009) · Developmental Cell · doi:10.1016/j.devcel.2009.11.003 · Cited by 516 · see citing works
Mammalian hepatocyte differentiation requires the transcription factor HNF-4alpha.
(2000) · PubMed Central · Cited by 489 · see citing works
Hybrid Periportal Hepatocytes Regenerate the Injured Liver without Giving Rise to Cancer
Font-Burgada, J., Shalapour, S., Ramaswamy, S., Hsueh, B., Rossell, D., Umemura, A., Taniguchi, K., Nakagawa, H., Valasek, M. A., Ye, L., et al. (2015) · Cell · doi:10.1016/j.cell.2015.07.026 · Cited by 486 · see citing works
Spatial heterogeneity in the mammalian liver
Ben-Moshe, S., & Itzkovitz, S. (2019) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/s41575-019-0134-x · Cited by 485 · see citing works
Robust cellular reprogramming occurs spontaneously during liver regeneration
Yanger, K., Zong, Y., Maggs, L. R., Shapira, S. N., Maddipati, R., Aiello, N. M., Thung, S. N., Wells, R. G., Greenbaum, L. E., & Stanger, B. Z. (2013) · Genes & Development · doi:10.1101/gad.207803.112 · Cited by 484 · see citing works
Deciphering human macrophage development at single-cell resolution
Bian, Z., Gong, Y., Huang, T., Lee, C., Bian, L., Bai, Z., Shi, H., Zeng, Y., Liu, C., He, J., et al. (2020) · Nature · doi:10.1038/s41586-020-2316-7 · Cited by 478 · see citing works
He, G., Dhar, D., Nakagawa, H., Font-Burgada, J., Ogata, H., Jiang, Y., Shalapour, S., Seki, E., Yost, S. E., Jepsen, K., et al. (2013) · Cell · doi:10.1016/j.cell.2013.09.031 · Cited by 469 · see citing works
Reversal of Left-Right Asymmetry: a Situs Inversus Mutation
Yokoyama, T., Copeland, N. G., Jenkins, N. A., Montgomery, C. A., Elder, F. F. B., & Overbeek, P. A. (1993) · Science · doi:10.1126/science.8480178 · Cited by 462 · see citing works
Mammalian hepatocyte differentiation requires the transcription factor HNF-4αPreprint
Li, J., Ning, G., & Duncan, S. A. (2000) · Genes & Development · doi:10.1101/gad.14.4.464 · Cited by 458 · see citing works
Notch signaling controls liver development by regulating biliary differentiation
Zong, Y., Panikkar, A., Xu, J., Antoniou, A., Raynaud, P., Lemaigre, F. P., & Stanger, B. Z. (2009) · Development · doi:10.1242/dev.029140 · Cited by 443 · see citing works
Expansion of hematopoietic stem cells in the developing liver of a mouse embryo
Ema, H., & Nakauchi, H. (2000) · Blood · doi:10.1182/blood.v95.7.2284 · Cited by 440 · 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
Adult Hepatocytes Are Generated by Self-Duplication Rather than Stem Cell Differentiation
Yanger, K., Knigin, D., Zong, Y., Maggs, L., Gu, G., Akiyama, H., Pikarsky, E., & Stanger, B. Z. (2014) · Cell Stem Cell · doi:10.1016/j.stem.2014.06.003 · Cited by 426 · see citing works
Single-cell transcriptomics uncovers zonation of function in the mesenchyme during liver fibrosis
Dobie, R., Wilson-Kanamori, J. R., Henderson, B. E. P., Smith, J. R., Matchett, K. P., Portman, J. R., Wallenborg, K., Picelli, S., Zagorska, A., Pendem, S. V., et al. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.10.024 · Cited by 420 · see citing works
Loh, K. M., Ang, L. T., Zhang, J., Kumar, V., Ang, J., Auyeong, J. Q., Lee, K. L., Choo, S. H., Lim, C. Y. Y., Nichane, M., et al. (2014) · Cell Stem Cell · doi:10.1016/j.stem.2013.12.007 · Cited by 418 · see citing works
Two distinct endothelial lineages in ontogeny, one of them related to hemopoiesis
Pardanaud, L., Luton, D., Prigent, M., Bourcheix, L.-M., Catala, M., & Dieterlen‐Lièvre, F. (1996) · Development · doi:10.1242/dev.122.5.1363 · Cited by 417 · see citing works
ISSCR Guidelines for Stem Cell Research and Clinical Translation: The 2021 update
Lovell-Badge, R. H., Anthony, E., Barker, R. A., Bubela, T. M., Brivanlou, A. H., Carpenter, M., Charo, R. A., Clark, A. T., Clayton, E. W., Cong, Y., et al. (2021) · Stem Cell Reports · doi:10.1016/j.stemcr.2021.05.012 · Cited by 411 · see citing works
Massive 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
Kwon, G. S., Viotti, M., & Hadjantonakis, A.-K. (2008) · Developmental Cell · doi:10.1016/j.devcel.2008.07.017 · Cited by 402 · see citing works
The role of TGFβ1 in initiating hepatic stellate cell activation in vivo
Hellerbrand, C., Stefanovic, B., Giordano, F., Burchardt, E. R., & Brenner, D. A. (1999) · Journal of Hepatology · doi:10.1016/s0168-8278(99)80010-5 · Cited by 393 · see citing works
Iwafuchi-Doi, M., Donahue, G., Kakumanu, A., Watts, J. A., Mahony, S., Pugh, B. F., Lee, D., Kaestner, K. H., & Zaret, K. S. (2016) · Molecular Cell · doi:10.1016/j.molcel.2016.03.001 · Cited by 390 · see citing works
The emergent landscape of the mouse gut endoderm at single-cell resolution
Nowotschin, S., Setty, M., Kuo, Y.-Y., Liu, V., Garg, V., Sharma, R., Simon, C. S., Saiz, N., Gardner, R., Boutet, S. C., et al. (2019) · Nature · doi:10.1038/s41586-019-1127-1 · Cited by 383 · see citing works
Self-citationHepatocyte migration during liver development requires Prox1
Sosa-Pineda, B., Wigle, J. T., & Oliver, G. (2000) · Nature Genetics · doi:10.1038/76996 · Cited by 381 · 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
Ara, T., Tokoyoda, K., Sugiyama, T., Egawa, T., Kawabata, K., & Nagasawa, T. (2003) · Immunity · doi:10.1016/s1074-7613(03)00201-2 · Cited by 369 · see citing works
Paired-cell sequencing enables spatial gene expression mapping of liver endothelial cells
Halpern, K. B., Shenhav, R., Massalha, H., Toth, B., Egozi, A., Massasa, E. E., Medgalia, C., David, E., Giladi, A., Moor, A. E., et al. (2018) · Nature Biotechnology · doi:10.1038/nbt.4231 · Cited by 368 · see citing works
The onecut transcription factor HNF6 is required for normal development of the biliary tract
Clotman, F., Lannoy, V. J., Reber, M., Cereghini, S., Cassiman, D. M., Jacquemin, P., Roskams, T., Rousseau, G. G., & Lemaigre, F. P. (2002) · Development · doi:10.1242/dev.129.8.1819 · Cited by 368 · see citing works
Clotman, F., Jacquemin, P., Plumb–Rudewiez, N., Pierreux, C. E., Smissen, P. V. D., Dietz, H. C., Courtoy, P. J., Rousseau, G. G., & Lemaigre, F. P. (2005) · Genes & Development · doi:10.1101/gad.340305 · Cited by 363 · 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
Liver Progenitor Cells Yield Functional Hepatocytes in Response to Chronic Liver Injury in Mice
Español–Suñer, R., Carpentier, R., Van Hul, N., Legry, V., Achouri, Y., Cordi, S., Jacquemin, P., Lemaigre, F., & Leclercq, I. A. (2012) · Gastroenterology · doi:10.1053/j.gastro.2012.08.024 · Cited by 356 · see citing works
Bile system morphogenesis defects and liver dysfunction upon targeted deletion of HNF1β
Coffinier, C., Gresh, L., Fiette, L., Tronche, F., Schütz, G., Babinet, C., Pontoglio, M., Yaniv, M., & Barra, J. (2002) · Development · doi:10.1242/dev.129.8.1829 · Cited by 354 · see citing works
Doherty, D. G., Norris, S., Madrigal-Estebas, L., McEntee, G., Traynor, O., Hegarty, J. E., & O’Farrelly, C. (1999) · The Journal of Immunology · doi:10.4049/jimmunol.163.4.2314 · Cited by 350 · see citing works
Intrahepatic cholangiocarcinoma can arise from Notch-mediated conversion of hepatocytes
Sekiya, S., & Suzuki, A. (2012) · Journal of Clinical Investigation · doi:10.1172/jci63065 · Cited by 348 · see citing works
Hepatocytes Do Not Undergo Epithelial-Mesenchymal Transition in Liver Fibrosis in Mice
Taura, K., Miura, K., Iwaisako, K., Österreicher, C. H., Kodama, Y., Penz-Österreicher, M., & Brenner, D. A. (2010) · Hepatology · doi:10.1002/hep.23368 · Cited by 336 · see citing works
Hirsch, E., Iglesias, A. H., Potocnik, A. J., Hartmann, U., & Fässler, R. (1996) · Nature · doi:10.1038/380171a0 · Cited by 332 · see citing works
Modelling human hepato-biliary-pancreatic organogenesis from the foregut–midgut boundary
Koike, H., Iwasawa, K., Ouchi, R., Maezawa, M., Giesbrecht, K., Saiki, N., Ferguson, A., Kimura, M., Thompson, W. L., Wells, J. M., et al. (2019) · Nature · doi:10.1038/s41586-019-1598-0 · Cited by 325 · see citing works
Michalopoulos, G. K., Barua, L., & Bowen, W. C. (2005) · Hepatology · doi:10.1002/hep.20600 · Cited by 319 · see citing works
Human Hepatic Stem Cell and Maturational Liver Lineage Biology Δ
Turner, R., Lozoya, O. A., Wang, Y., Cardinale, V., Gaudio, E., Alpini, G. D., Mendel, G., Wauthier, E., Barbier, C., Alvaro, D., et al. (2011) · Hepatology · doi:10.1002/hep.24157 · Cited by 316 · see citing works
Building consensus on definition and nomenclature of hepatic, pancreatic, and biliary organoids
Marsee, A., Roos, F. J. M., Verstegen, M. M. A., Marsee, A., Roos, F., Verstegen, M., Clevers, H., Vallier, L., Takebe, T., Huch, M., et al. (2021) · Cell Stem Cell · doi:10.1016/j.stem.2021.04.005 · Cited by 310 · 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
Andrews, T. S., Atif, J., Liu, J. C., Perciani, C. T., Ma, X., Thoeni, C., Slyper, M., Eraslan, G., Segerstolpe, A., Manuel, J., et al. (2022) · Hepatology Communications · doi:10.1002/hep4.1854 · Cited by 307 · see citing works
Artegiani, B., Hendriks, D. F. G., Beumer, J., Kok, R. N. U., Zheng, X., Joore, I. P., Lopes, S. M. C. D. S., van Zon, J. S., Tans, S. J., & Clevers, H. C. (2020) · Nature Cell Biology · doi:10.1038/s41556-020-0472-5 · Cited by 302 · see citing works
Wisse, E. (1972) · Journal of Ultrastructure Research · doi:10.1016/0022-5320(72)90089-5 · Cited by 300 · see citing works
Tremblay, K. D., & Zaret, K. S. (2005) · Developmental Biology · doi:10.1016/j.ydbio.2005.01.003 · Cited by 299 · see citing works
Chronic Liver Injury Induces Conversion of Biliary Epithelial Cells into Hepatocytes
Deng, X., Zhang, X., Li, W., Feng, R.-X., Li, L., Yi, G.-R., Zhang, X.-N., Yin, C., Yu, H.-Y., Zhang, J.-P., et al. (2018) · Cell Stem Cell · doi:10.1016/j.stem.2018.05.022 · Cited by 289 · see citing works
Bort, R., Signore, M., Tremblay, K. D., Martı́nez-Barberá, J. P., & Zaret, K. S. (2005) · Developmental Biology · doi:10.1016/j.ydbio.2005.11.006 · Cited by 285 · see citing works
Human Pluripotent Stem Cell-Derived Organoids as Models of Liver Disease
Ramli, M. N. B., Lim, Y. S., Koe, C. T., Demircioglu, D., Tng, W., Gonzales, K. A. U., Tan, C. P., Szczerbinska, I., Liang, H., Soe, E. L., et al. (2020) · Gastroenterology · doi:10.1053/j.gastro.2020.06.010 · Cited by 278 · see citing works
Role of stem cell migration in initiation of mouse foetal liver haemopoiesis
Johnson, G. R., & Moore, M. A. S. (1975) · Nature · doi:10.1038/258726a0 · Cited by 273 · see citing works
Carpentier, R., Español‐Suñer, R., Hul, N. V., Kopp, J. L., Beaudry, J., Cordi, S., Antoniou, A., Raynaud, P., Lepreux, S., Jacquemin, P., et al. (2011) · Gastroenterology · doi:10.1053/j.gastro.2011.06.049 · Cited by 271 · see citing works
Pepe-Mooney, B. J., Dill, M. T., Alemany, A., Ordovas-Montanes, J., Matsushita, Y., Rao, A., Sen, A., Miyazaki, M., Anakk, S., Dawson, P. A., et al. (2019) · Cell Stem Cell · doi:10.1016/j.stem.2019.04.004 · Cited by 266 · see citing works
Wang, A., Yue, F., Li, Y., Xie, R., Harper, T. C., Patel, N. A., Muth, K., Palmer, J., Qiu, Y., Wang, J., et al. (2015) · Cell stem cell · doi:10.1016/j.stem.2015.02.013 · Cited by 263 · see citing works
Schaub, J. R., Malato, Y., Gormond, C., & Willenbring, H. (2014) · Cell Reports · doi:10.1016/j.celrep.2014.07.003 · Cited by 254 · see citing works
Ex utero mouse embryogenesis from pre-gastrulation to late organogenesis
Aguilera-Castrejon, A., Oldak, B., Shani, T., Ghanem, N., Itzkovich, C., Slomovich, S., Tarazi, S., Bayerl, J., Chugaeva, V., Ayyash, M., et al. (2021) · Nature · doi:10.1038/s41586-021-03416-3 · Cited by 251 · see citing works
Hofmann, J. J., Zovein, A. C., Koh, H., Radtke, F., Weinmaster, G., & Iruela‐Arispe, M. L. (2010) · Development · doi:10.1242/dev.052118 · Cited by 247 · see citing works
Human hepatic organoids for the analysis of human genetic diseases
Guan, Y., Xu, D., Garfin, P. M., Ehmer, U., Hurwitz, M., Enns, G., Michie, S., Wu, M., Zheng, M., Nishimura, T., et al. (2017) · JCI Insight · doi:10.1172/jci.insight.94954 · Cited by 243 · see citing works
Fetal liver hematopoietic stem cell niches associate with portal vessels
Khan, J. A., Mendelson, A., Kunisaki, Y., Birbrair, A., Kou, Y., Estape, A. A., Pinho, S., Ciero, P., Nakahara, F., Ma’ayan, A., et al. (2015) · Science · doi:10.1126/science.aad0084 · Cited by 242 · see citing works
Hepatocyte Nuclear Factor 4α Suppresses the Development of Hepatocellular Carcinoma
Ning, B., Ding, J., Yin, C., Zhong, W. H., Wu, K., Zeng, X. Y., Yang, W. K., Chen, Y.-X., Zhang, J., Zhang, X., et al. (2010) · Cancer Research · doi:10.1158/0008-5472.can-10-0824 · Cited by 241 · see citing works
Zf9, a Kruppel-like transcription factor up-regulated in vivo during early hepatic fibrosis
Ratziu, V., Lalazar, A., Wong, L., Dang, Q., Collins, C. C., Shaulian, E., Jensen, S., & Friedman, S. L. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.16.9500 · Cited by 240 · see citing works
The role of notch signaling in the development of intrahepatic bile ducts
Kodama, Y., Hijikata, M., Kageyama, R., Shimotohno, K., & Chiba, T. (2004) · Gastroenterology · doi:10.1053/j.gastro.2004.09.004 · Cited by 240 · see citing works
He, J., Lu, H., Zou, Q., & Luo, L. (2013) · Gastroenterology · doi:10.1053/j.gastro.2013.11.045 · Cited by 240 · see citing works
Choi, T., Ninov, N., Stainier, D. Y. R., & Shin, D. (2013) · Gastroenterology · doi:10.1053/j.gastro.2013.10.019 · Cited by 238 · see citing works
Asahina, K., Tsai, S. Y., Li, P., Ishii, M., Maxson, R. E., Sucov, H. M., & Tsukamoto, H. (2009) · Hepatology · doi:10.1002/hep.22721 · Cited by 238 · see citing works
Single-cell RNA sequencing reveals the heterogeneity of liver-resident immune cells in human
Zhao, J., Zhang, S., Liu, Y., He, X., Qu, M., Xu, G., Wang, H., Huang, M., Pan, J., Liu, Z., et al. (2020) · Cell Discovery · doi:10.1038/s41421-020-0157-z · Cited by 237 · see citing works
Scholten, D., Österreicher, C. H., Scholten, A., Iwaisako, K., Gu, G., Brenner, D. A., & Kisseleva, T. (2010) · Gastroenterology · doi:10.1053/j.gastro.2010.05.005 · Cited by 225 · see citing works
The spatiotemporal program of zonal liver regeneration following acute injury
Ben-Moshe, S., Veg, T., Manco, R., Dan, S., Papinutti, D., Lifshitz, A., Kolodziejczyk, A. A., Bahar Halpern, K., Elinav, E., & Itzkovitz, S. (2022) · Cell Stem Cell · doi:10.1016/j.stem.2022.04.008 · Cited by 224 · 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
A Roadmap for Human Liver Differentiation from Pluripotent Stem Cells
Ang, L. T., Tan, A. K. Y., Autio, M. I., Goh, S. H., Choo, S. H., Lee, K. L., Tan, J., Pan, B., Lee, J. J. H., Lum, J. J., et al. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.01.087 · Cited by 220 · see citing works
Clonal Tracing of Sox9+ Liver Progenitors in Mouse Oval Cell Injury
Tarlow, B., Finegold, M. J., & Grompe, M. (2014) · Hepatology · doi:10.1002/hep.27084 · Cited by 220 · see citing works
HNF4A is essential for specification of hepatic progenitors from human pluripotent stem cells
DeLaForest, A., Nagaoka, M., Si-Tayeb, K., Noto, F. K., Konopka, G., Battle, M. A., & Duncan, S. A. (2011) · Development · doi:10.1242/dev.062547 · Cited by 219 · see citing works
Wu, J., Meng, Z., Jiang, M., Zhang, E., Trippler, M., Broering, R., Bucchi, A., Krux, F., Dittmer, U., Yang, D., et al. (2009) · Immunology · doi:10.1111/j.1365-2567.2009.03179.x · Cited by 213 · 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
Houssaint, E. (1980) · Cell Differentiation · doi:10.1016/0045-6039(80)90026-3 · Cited by 209 · 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
Small-Molecule-Driven Hepatocyte Differentiation of Human Pluripotent Stem Cells
Siller, R., Greenhough, S., Naumovska, E., & Sullivan, G. J. (2015) · Stem Cell Reports · doi:10.1016/j.stemcr.2015.04.001 · Cited by 203 · see citing works
Hildebrandt, F., Andersson, A., Saarenpää, S., Larsson, L., Hul, N. V., Kanatani, S., Masek, J., Ellis, E. C. S., Barragán, A., Mollbrink, A., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-27354-w · Cited by 195 · see citing works
Liver sinusoidal endothelial cell progenitor cells promote liver regeneration in rats
Wang, L., Wang, X., Xie, G., Wang, L., Hill, C. K., & DeLeve, L. D. (2012) · Journal of Clinical Investigation · doi:10.1172/jci58789 · Cited by 194 · see citing works
Lymph Circulation in the Liver
Ohtani, O., & Ohtani, Y. (2008) · The Anatomical Record · doi:10.1002/ar.20681 · Cited by 193 · see citing works
The biliary epithelium gives rise to liver progenitor cells
Rodrigo-Torres, D., Affò, S., Coll, M., Morales-Ibanez, O., Millán, C., Blaya, D., Alvarez-Guaita, A., Rentero, C., José Lozano, J., Maestro, M. A., et al. (2014) · Hepatology · doi:10.1002/hep.27078 · Cited by 189 · see citing works
Dong, J., Hu, Y., Fan, X., Wu, X., Mao, Y., Hu, B., Guo, H., Wen, L., & Tang, F. (2018) · Genome Biology · doi:10.1186/s13059-018-1416-2 · Cited by 187 · see citing works
Means, A. L., Xu, Y., Zhao, A., Ray, K. C., & Gu, G. (2008) · genesis · doi:10.1002/dvg.20397 · Cited by 183 · see citing works
Han, L., Chaturvedi, P., Kishimoto, K., Koike, H., Nasr, T., Iwasawa, K., Giesbrecht, K., Witcher, P. C., Eicher, A. K., Haines, L. E., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-17968-x · Cited by 178 · see citing works
Efficient temporally controlled targeted somatic mutagenesis in hepatocytes of the mouse
Schuler, M. J., Dierich, A., Chambon, P., & METZGER, D. (2004) · genesis · doi:10.1002/gene.20039 · Cited by 175 · see citing works
Shetty, S., Weston, C. J., Oo, Y. H., Westerlund, N., Stamataki, Z., Youster, J., Hübscher, S. G., Salmi, M., Jalkanen, S., Lalor, P. F., et al. (2011) · The Journal of Immunology · doi:10.4049/jimmunol.1002961 · Cited by 174 · see citing works
Mechanosensing by β1 integrin induces angiocrine signals for liver growth and survival
Lorenz, L., Axnick, J., Buschmann, T., Henning, C., Urner, S., Fang, S., Nurmi, H., Eichhorst, N., Holtmeier, R., Bódis, K., et al. (2018) · Nature · doi:10.1038/s41586-018-0522-3 · Cited by 171 · see citing works
Winkler, M., Staniczek, T., Kürschner, S. W., Schmid, C. D., Schönhaber, H., Cordero, J., Kessler, L., Mathes, A., Sticht, C., Neßling, M., et al. (2020) · Journal of Hepatology · doi:10.1016/j.jhep.2020.08.033 · Cited by 170 · see citing works
AFP promotes HCC progression by suppressing the HuR-mediated Fas/FADD apoptotic pathway
Chen, T., Dai, X., Dai, J., Ding, C., Zhang, Z., Lin, Z., Hu, J., Lu, M., Wang, Z., Qi, Y., et al. (2020) · Cell Death and Disease · doi:10.1038/s41419-020-03030-7 · Cited by 168 · see citing works
Géraud, C., Reiners-Koch, P.-S., Zierow, J., Klapproth, K., Busch, K., Olsavszky, V., Leibing, T., Demory, A., Ulbrich, F., Diett, M., et al. (2017) · Journal of Clinical Investigation · doi:10.1172/jci90086 · Cited by 164 · see citing works
Bioprinting of Multiscaled Hepatic Lobules within a Highly Vascularized Construct
Kang, D., Hong, G., An, S., Jang, I., Yun, W., Shim, J., & Jin, S. (2020) · Small · doi:10.1002/smll.201905505 · Cited by 164 · see citing works
Yang, L. C., Wang, W., Qiu, W., Guo, Z., Bi, E., & Xu, C. (2017) · Hepatology · doi:10.1002/hep.29353 · Cited by 162 · see citing works
Single-cell RNA sequencing of human liver reveals hepatic stellate cell heterogeneity
Payen, V. L., Lavergne, A., Alevra Sarika, N., Colonval, M., Karim, L., Deckers, M., Najimi, M., Coppieters, W., Charloteaux, B., Sokal, E. M., et al. (2021) · JHEP Reports · doi:10.1016/j.jhepr.2021.100278 · Cited by 160 · see citing works
Hendriks, D. F. G., Artegiani, B., Hu, H., Lopes, S. M. C. D. S., & Clevers, H. C. (2020) · Nature Protocols · doi:10.1038/s41596-020-00411-2 · Cited by 159 · see citing works
Passive and Active Mechanisms Trap Activated CD8+ T Cells in the Liver
John, B., & Crispe, I. N. (2004) · The Journal of Immunology · doi:10.4049/jimmunol.172.9.5222 · Cited by 157 · see citing works
LeSage, G., Glaser, S., Gubba, S., Robertson, W., Phinizy, J. L., Lasater, J., Rodgers, R., & Alpini, G. D. (1996) · Gastroenterology · doi:10.1016/s0016-5085(96)70027-6 · Cited by 152 · 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
Increased Activities of Glycogenolytic Enzymes in Liver after Splanchnic-Nerve Stimulation
Shimazu, T., & Fukuda, A. (1965) · Science · doi:10.1126/science.150.3703.1607 · Cited by 144 · see citing works
Origin and development of the epicardium in the mouse embryo
Komiyama, M., Ito, K., & Shimada, Y. (1987) · Anatomy and Embryology · doi:10.1007/bf00310051 · Cited by 144 · see citing works
Alvaro, D., Alpini, G. D., Jezequel, A. M., Bassotti, C., Francia, C., FRAIOLI, F., Roméo, R., Marucci, L., LeSage, G., Glaser, S. S., et al. (1997) · Journal of Clinical Investigation · doi:10.1172/jci119655 · Cited by 137 · see citing works
MMP2 activation by collagen I and concanavalin A in cultured human hepatic stellate cells
Théret, N., Lehti, K., Musso, O. C., & Clément, B. (1999) · Hepatology · doi:10.1002/hep.510300236 · Cited by 137 · see citing works
Emambokus, N. R., & Frampton, J. (2003) · Immunity · doi:10.1016/s1074-7613(03)00173-0 · Cited by 135 · see citing works
Developments and Opportunities for 3D Bioprinted Organoids
Ya, R., Yang, X., Ma, Z., Sun, X., Zhang, Y., Li, W., Yang, H. S., Qiang, L., Yang, Z., Liu, Y., et al. (2021) · International Journal of Bioprinting · doi:10.18063/ijb.v7i3.364 · Cited by 129 · 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
Segal, J. M., Kent, D., Wesche, D. J., Ng, S. S., Serra, M. P., Oulès, B., Kar, G., Emerton, G., Blackford, S. J. I., Darmanis, S., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-11266-x · Cited by 126 · see citing works
Transcription factors SOX4 and SOX9 cooperatively control development of bile ducts
Poncy, A., Antoniou, A., Cordi, S., Pierreux, C. E., Jacquemin, P., & Lemaigre, F. P. (2015) · Developmental Biology · doi:10.1016/j.ydbio.2015.05.012 · Cited by 125 · see citing works
ER71 directs mesodermal fate decisions during embryogenesis
Rasmussen, T. L., Kweon, J., Diekmann, M. A., Belema-Bedada, F., Song, Q., Bowlin, K., Shi, X., Ferdous, A., Li, T., Kyba, M., et al. (2011) · Development · doi:10.1242/dev.070912 · Cited by 123 · see citing works
Misfeldt, A. M., Boyle, S. C., Tompkins, K. L., Bautch, V. L., Labosky, P. A., & Baldwin, H. S. (2009) · Developmental Biology · doi:10.1016/j.ydbio.2009.06.033 · Cited by 123 · see citing works
Models of haematopoiesis: seeing the wood for the trees
Ceredig, R. H., Rolink, A. G., & Brown, G. (2009) · Nature reviews. Immunology · doi:10.1038/nri2525 · Cited by 123 · see citing works
CHARACTERIZATION OF INTERSTITIAL DENDRITIC CELLS IN HUMAN LIVER
Prickett, T. C. R., McKenzie, J. L., & Hart, D. N. J. (1988) · Transplantation · doi:10.1097/00007890-198811000-00024 · Cited by 119 · see citing works
Takeishi, K., Collin de l’Hortet, A., Wang, Y., Handa, K., Guzman-Lepe, J., Matsubara, K., Morita, K., Jang, S., Haep, N., Florentino, R. M., et al. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.107711 · Cited by 118 · see citing works
Hepatic Stellate Cell Regulation of Liver Regeneration and Repair
Kitto, L. J., & Henderson, N. C. (2020) · Hepatology Communications · doi:10.1002/hep4.1628 · Cited by 117 · see citing works
Lüdtke, T. H. ‐., Christoffels, V. M., Petry, M., & Kispert, A. (2009) · Hepatology · doi:10.1002/hep.22700 · Cited by 117 · 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
Hippo Signaling Influences HNF4A and FOXA2 Enhancer Switching during Hepatocyte Differentiation
Alder, O., Cullum, R., Lee, S., Kan, A. C., Wei, W., Yi, Y., Garside, V. C., Bilenky, M., Griffith, M., Morrissy, A. S., et al. (2014) · Cell Reports · doi:10.1016/j.celrep.2014.08.046 · Cited by 113 · see citing works
Self-citationGao, S., Shi, Q., Zhang, Y., Liang, G., Kang, Z., Huang, B., Ma, D., Wang, L., Jiao, J., Fang, X., et al. (2021) · Cell Research · doi:10.1038/s41422-021-00540-7 · Cited by 112 · see citing works
Paraxial Mesoderm Is the Major Source of Lymphatic Endothelium
Stone, O. A., & Stainier, D. Y. R. (2019) · Developmental Cell · doi:10.1016/j.devcel.2019.04.034 · Cited by 112 · see citing works
Izumi, T., Imai, J., Yamamoto, J., Kawana, Y., Endo, A., Sugawara, H., Kohata, M., Asai, Y., Takahashi, K., Kodama, S., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-07747-0 · Cited by 109 · see citing works
Genetic lineage tracing identifies endocardial origin of liver vasculature
Zhang, H., Pu, W., Tian, X., Huang, X., He, L., Liu, Q., Li, Y., Zhang, L., He, L., Liu, K., et al. (2016) · Nature Genetics · doi:10.1038/ng.3536 · Cited by 105 · see citing works
Gouysse, G., Couvelard, A., Collardeau‐Frachon, S., Bouvier, R., Nejjari, M., Dauge, M., Feldmann, G., Hénin, D., & Scoazec, J. (2002) · Journal of Hepatology · doi:10.1016/s0168-8278(02)00282-9 · Cited by 104 · see citing works
Gage, B. K., Liu, J. C., Innes, B. T., MacParland, S. A., McGilvray, I. D., Bader, G. D., & Keller, G. M. (2020) · Cell stem cell · doi:10.1016/j.stem.2020.06.007 · Cited by 104 · see citing works
Single-cell and bulk transcriptomics of the liver reveals potential targets of NASH with fibrosis
Wang, Z.-Y., Keogh, A., Waldt, A., Cuttat, R., Neri, M., Zhu, S., Schuierer, S., Ruchti, A., Crochemore, C., Knehr, J., et al. (2021) · Scientific Reports · doi:10.1038/s41598-021-98806-y · Cited by 103 · see citing works
Functional compensation precedes recovery of tissue mass following acute liver injury
Walesky, C. M., Kolb, K. E., Winston, C. L., Henderson, J., Kruft, B., Fleming, I., Ko, S., Monga, S. P., Mueller, F., Apte, U., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-19558-3 · Cited by 103 · see citing works
Fetal stem cell transplantation: Past, present, and future
Ishii, T. (2014) · World Journal of Stem Cells · doi:10.4252/wjsc.v6.i4.404 · Cited by 100 · see citing works
Schulte, I., Schlueter, J., Abu‐Issa, R., Brand, T., & Männer, J. (2007) · Developmental Dynamics · doi:10.1002/dvdy.21065 · Cited by 100 · see citing works
CFC1 Gene Involvement in Biliary Atresia With Polysplenia Syndrome
Spraul, A., Baussan, C., Hermeziu, B., et al. (2008) · Journal of Pediatric Gastroenterology and Nutrition · doi:10.1097/01.mpg.0000304465.60788.f4 · Cited by 99 · see citing works
Lei, L., Bruneau, A., El Mourabit, H., Guégan, J., Folseraas, T., Lemoinne, S., Karlsen, T. H., Hoareau, B., Morichon, R., Gonzalez‐Sanchez, E., et al. (2022) · Hepatology · doi:10.1002/hep.32456 · Cited by 94 · see citing works
System for tamoxifen‐inducible expression of cre‐recombinase from the Foxa2 locus in mice
Park, E. J., Sun, X., Nichol, P. F., Saijoh, Y., Martin, J. F., & Moon, A. (2007) · Developmental Dynamics · doi:10.1002/dvdy.21415 · Cited by 94 · see citing works
Alvarez, M., Benhammou, J. N., Darci-Maher, N., French, S. W., Han, S. B., Sinsheimer, J. S., Agopian, V. G., Pisegna, J. R., & Pajukanta, P. (2022) · Genome Medicine · doi:10.1186/s13073-022-01055-5 · Cited by 90 · see citing works
Steiniger, B. S., Klempnauer, J. L., & Wonigeit, K. (1984) · Transplantation · doi:10.1097/00007890-198408000-00016 · Cited by 90 · 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
Self-citationTan, C. E. L., & Moscoso, G. J. (1994) · Pathology International · doi:10.1111/j.1440-1827.1994.tb01719.x · Cited by 84 · 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
Gómez-Salinero, J. M., Izzo, F., Lin, Y., Houghton, S., Itkin, T., Geng, F., Bram, Y., Adelson, R. P., Lu, T. M., Inghirami, G., et al. (2022) · Cell stem cell · doi:10.1016/j.stem.2022.03.002 · Cited by 81 · see citing works
Single-cell RNA-Seq analysis reveals dynamic trajectories during mouse liver development
Su, X., Shi, Y. Y., Zou, X., Lu, Z., Xie, G., Yang, J. Y. H., Wu, C.-C., Cui, X., He, K., Luo, Q., et al. (2017) · BMC Genomics · doi:10.1186/s12864-017-4342-x · Cited by 81 · see citing works
Lee, L. K., Ghorbanian, Y., Wang, W., Wang, Y., Kim, Y. J., Weissman, I. L., Inlay, M. A., & Mikkola, H. K. A. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.10.080 · Cited by 79 · see citing works
Forkel, M., Berglin, L., Kekäläinen, E., Carlsson, A., Svedin, E., Michaëlsson, J., Nagasawa, M., Erjefalt, J. S., Mori, M., Flodström‐Tullberg, M., et al. (2017) · European Journal of Immunology · doi:10.1002/eji.201646890 · Cited by 79 · see citing works
Tannour‐Louet, M., Porteu, A., Vaulont, S., Kahn, A., & Vasseur-Cognet, M. (2002) · Hepatology · doi:10.1053/jhep.2002.33164 · Cited by 78 · see citing works
Lgr5+ stem and progenitor cells reside at the apex of a heterogeneous embryonic hepatoblast pool
Prior, N., Hindley, C. J., Rost, F., Esteban, E. M., Lau, W. W. Y., Göttgens, B., Rulands, S., Simons, B. D., & Huch, M. (2019) · Development · doi:10.1242/dev.174557 · Cited by 76 · see citing works
Thakur, A., Wong, J. C. H., Wang, E. Y., Lotto, J., Kim, D., Cheng, J., Mingay, M., Cullum, R., Moudgil, V., Ahmed, N., et al. (2019) · Hepatology · doi:10.1002/hep.30631 · Cited by 75 · see citing works
Self-citationCordero-Espinoza, L., Dowbaj, A. M., Kohler, T. N., Strauss, B., Sarlidou, O., Belenguer, G., Pacini, C., Martins, N. P., Dobie, R., Wilson-Kanamori, J. R., et al. (2021) · Cell Stem Cell · doi:10.1016/j.stem.2021.07.002 · Cited by 74 · see citing works
Fabris, L., Cadamuro, M., Libbrecht, L. J., Raynaud, P., Spirlı̀, C., Fiorotto, R., Okolicsànyi, L., Lemaigre, F. P., Strazzabosco, M., & Roskams, T. (2007) · Hepatology · doi:10.1002/hep.22015 · Cited by 71 · see citing works
Heslop, J. A., Pournasr, B., Liu, J.-T., & Duncan, S. A. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.109145 · Cited by 70 · see citing works
Liu, K., Jin, H., & Zhou, B. (2020) · Journal of Biological Chemistry · doi:10.1074/jbc.rev120.011631 · Cited by 69 · see citing works
Lu, Y., Liu, M., Yang, J., Weissman, S. M., Pan, X., Katz, S. G., & Wang, S. (2021) · Cell Discovery · doi:10.1038/s41421-021-00266-1 · Cited by 68 · see citing works
The Dynamics of Transcriptional Activation by Hepatic Reprogramming Factors
Horisawa, K., Udono, M., Ueno, K., Ohkawa, Y., Nagasaki, M., Sekiya, S., & Suzuki, A. (2020) · Molecular Cell · doi:10.1016/j.molcel.2020.07.012 · Cited by 68 · see citing works
Fenestration patterns in endothelial cells of rat liver sinusoids
Vidal‐Vanaclocha, F., & Barberá‐Guillem, E. (1985) · Journal of Ultrastructure Research · doi:10.1016/0889-1605(85)90102-8 · Cited by 67 · see citing works
Innervation of the liver: morphology and function
TINIAKOS, D. G., Lee, J. A., & Burt, A. D. (1996) · Liver International · doi:10.1111/j.1600-0676.1996.tb00721.x · Cited by 64 · see citing works
Innervation of the sinusoidal wall: Regulation of the sinusoidal diameter
Ueno, T., Bioulac‐Sage, P., Balabaud, C. P., & Rosenbaum, J. (2004) · The Anatomical Record Part A Discoveries in Molecular Cellular and Evolutionary Biology · doi:10.1002/ar.a.20092 · Cited by 64 · see citing works
Wohlfeil, S. A., Häfele, V., Dietsch, B., Schledzewski, K., Winkler, M., Zierow, J., Leibing, T., Mohammadi, M. M., Heineke, J., Sticht, C., et al. (2018) · Cancer Research · doi:10.1158/0008-5472.can-18-1752 · Cited by 62 · 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
Collapse of the hepatic gene regulatory network in the absence of FoxA factors
Reizel, Y., Morgan, A., Gao, L., Lan, Y., Manduchi, E., Waite, E. L., Wang, A. W., Wells, A., & Kaestner, K. H. (2020) · Genes & Development · doi:10.1101/gad.337691.120 · Cited by 60 · see citing works
Geusz, R. J., Wang, A., Lam, D. K., Vinckier, N. K., Alysandratos, K., Roberts, D. A., Wang, J., Kefalopoulou, S., Ramirez, A., Qiu, Y., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-26950-0 · Cited by 60 · see citing works
Endoderm generates endothelial cells during liver development
Goldman, O., Han, S., Hamou, W., Jodon de Villeroche, V., Uzan, G., Lickert, H., & Gouon-Evans, V. (2014) · Stem Cell Reports · doi:10.1016/j.stemcr.2014.08.009 · Cited by 56 · see citing works
Flagged first, then by citations
Research works printed but not linked: 2
- Rabesandratana, T. E.U. Commission rejects plea to block stem cell research funding. SCIENCEINSIDER https://www.science.org/content/article/eu-commission-rejects-plea-block-stem-cell-research-funding (2014).
- Kellendonk, C., Opherk, C., Anlag, K., Schütz, G. & Tronche, F. Hepatocyte‐specific expression of Cre recombinase. Genesis 26, 151–153 (2000). · DOI
Cited by
Sorted by citations
TBX3 advances the developmental chromatin landscape toward the hepatic fate
Stephan, T. L., Cullum, R., Drissler, S., Thomas, A., Fuglerud, B. M., Clement-Ranney, M., Lotto, J., Krentz, N. A. J., Duncan, S. A., & Hoodless, P. A. (2025) · Developmental Cell · doi:10.1016/j.devcel.2025.05.014 · Cited by 1 · see citing works
Self-citation
- Authors
- Lotto, J., Stephan, T. L., & Hoodless, P. A.
- Affiliations
- BC Cancer Agency (CA)
- Venue
- Nature Reviews Gastroenterology & Hepatology
- Published
- 2023-05-19
- Volume
- 20
- Issue
- 9
- Pages
- 561-581
- ISSN
- 1759-5045 (ISSN-L)
- 1759-5053
- OpenAlex
- W4377094439
- Semantic Scholar
- 96833556ed058105f0015c276ab521d92c4bc026
- Cited by
- 47
- References
- 254
- Citations by year
- 2026: 14 · 2025: 18 · 2024: 11 · 2023: 4
- FWCI
- 2.46
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- Locations
- Nature Reviews Gastroenterology & Hepatology (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Hepatology › Liver physiology and pathology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Congenital heart defects research
- Keywords
- fetal liver development, liver organogenesis, liver disease pathogenesis, liver regeneration, single-cell genomics, lineage tracing, cell fate determination, lineage plasticity, hepatic parenchymal cells, non-parenchymal cells, in vitro liver models, liver cancer, regenerative medicine
- MeSH terms
- Cell Differentiation, Humans, Liver, Liver Diseases, Cell Lineage, Hepatocytes
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