The role of stem cell potential in the regeneration of the liver in <em>Cyprinus carpio</em> during postеmbryogenesis

Elena Antonova; Dina Omarova; Natalia Firsova; Atabeg Achilov

doi:10.21638/spbu03.2024.403

Authors

Elena Antonova Scientific Research Centre for Fundamental and Applied Problems of Bioecology and Biotechnology, Ulyanovsk State Pedagogical University, pl. Lenina, 4/5, Ulyanovsk, 432071, Russian Federation; Laboratory of Genetic and Cellular Technologies, Institute of Fundamental Medicine and Biology, Kazan Federal University, ul. Kremlevskaya, 18, Kazan, 420008, Russian Federation https://orcid.org/0000-0002-3686-9686
Dina Omarova Omsk State Pedagogical University, nab. Tukhachevskogo, 14, Omsk, 644099, Russian Federation https://orcid.org/0009-0003-6151-171X
Natalia Firsova Scientific Research Centre for Fundamental and Applied Problems of Bioecology and Biotechnology, Ulyanovsk State Pedagogical University, pl. Lenina, 4/5, Ulyanovsk, 432071, Russian Federation https://orcid.org/0000-0002-9907-8857
Atabeg Achilov Scientific Research Centre for Fundamental and Applied Problems of Bioecology and Biotechnology, Ulyanovsk State Pedagogical University, pl. Lenina, 4/5, Ulyanovsk, 432071, Russian Federation

DOI:

https://doi.org/10.21638/spbu03.2024.403

Abstract

The polyfunctionality of the liver and the high level of regeneration explain the enormous interest in the study of regeneration mechanisms, which have been largely studied in mammals. At the same time, the study of regeneration mechanisms in lower vertebrates, such as fish, provides important information regarding the conserved mechanisms also present in higher vertebrates. The present study focuses on the role of stem potential in liver regeneration of fish species Cyprinus carpio under physiological normal conditions during postembryogenesis. From the first to the third year of postembryogenesis, a significant decrease in the number of haematopoietic stem CD34+CD45+ cells (haematopoietic progenitor cell population) was detected, whereas the number of CD34+CD45– cells (haemangioblast population) remains relatively constant. From the first to the third year of postembryogenesis, the number of intrahepatic stem cell precursors CK19+ cells (intrahepatic progenitor cells) increases.

Keywords:

oval cells, liver progenitor cells, regeneration, fish, postembryogenesis, stem cells, immunophenotyping, immunohistochemistry, hepatocyte, hepatic acinus

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References

Akiyoshi, H. and Inoue, A. 2004. Comparative histological study of teleost livers in relation to phylogeny. Zoological Science 21(8):841–850. https://doi.org/10.2108/zsj.21.841

Akoul, M. A. and AL-Jowari, S. A.-K. 2019. Comparative anatomical and histological study of some organs in two fish species Cyprinus carpio (Linnaeus, 1758) and Mesopotamichthys sharpeyi (Günther, 1874) (Cypriniformes, Cyprinidae). Bulletin of the Iraq Natural History Museum 15(4):425–441. https://doi.org/10.26842/binhm.7.2019.15.4.0425

Akulenko, N. M., Dziubenko, N. V., Marushchak, O. Yu., Nekrasova, O. D., and Oskyrko, O. S. 2019. Histological changes in common toad, Bufo bufo (Anura, Bufonidae), liver tissue under conditions of anthropogenically transformed ecosystems. Bulletin of Zoology 53(6):501–506. https://doi.org/10.2478/vzoo-2019-0045

Angilletta, M. J., Steury, Jr. T. D., and Sears, M. W. 2004. Temperature, growth rate, and body size in ectotherms: Fitting Pieces of a Life-History Puzzle. Integrative and Comparative Biology 44(6):498–509. https://doi.org/10.1093/icb/44.6.498

Angilletta, M. J., Wilson, R. S., Navas, C. A., and James, R. S. 2003. Tradeoffs and the evolution of thermal reaction norms. Trends in Ecology and Evolution 18(5):234−240. https://doi.org/10.1016/S0169-5347(03)00087-9

Antonova, E. I., Omarova, D. I., Firsova, N. V., and Krasnikova, K. A. 2024. Role of liver progenitor cells of amphibian Rana terrestris in postembryonic development under physiological norm. Uchenye zapiski Kazanskogo universiteta. Seriia: Estestvennye nauki 166(1):38−65. https://doi.org/10.26907/2542-064X.2024.1.38-65 (In Russian)

Baker, M. E. 2003. Evolution of adrenal and sex steroid action in vertebrates: A ligand-based mechanism for complexity. BioEssays 25(4):396−400. https://doi.org/10.1002/bies.10252

Bayne, B. L. 2004. Phenotypic flexibility and physiological tradeoffs in the feeding and growth of marine bivalve mollusks. Integrative and Comparative Biology 44(6):425–432. https://doi.org/10.1093/icb/44.6.425

Beznos, O. A., Grivtsova, L. Yu., Popa, A. V., Shervashidze, M. A., Serebryakova, I. N., Baranova, O. Yu., Osmanov, E. A., and Tupitsyn, N. N. 2017. Evaluation of minimal residual disease in B-lineage acute lymphoblastic leukemia using EuroFlow approaches. Rossiiskii bioterapevticheskii zhurnal 10(2):158–168. https://doi.org/10.17650/1726-9784-2017-16-4-18-24 (In Russian)

Bram, Y., Nguyen, D.-H. T., Gupta, V., Park, J., Richardson, C., Chandar, V., and Schwartz, R. E. 2021. Cell and tissue therapy for the treatment of chronic liver disease. Annual Review of Biomedical Engineering 23:517–546. https://doi.org/10.1146/annurev-bioeng-112619-044026

Bruno, S., Sanchez, M. B. H., Chiabotto, G., Fonsato, V., Navarro-Tableros, V., Pasquino, C., Tapparo, M., and Camussi, G. 2021. Human liver stem cells: A liver-derived mesenchymal stromal cell-like population with pro-regenerative properties. Frontiers in Cell and Developmental Biology 9:e644088. https://doi.org/10.3389/fcell.2021.644088

Budd, G. E. and Jensen, S. 2000. A critical reappraisal of the fossil record of the bilaterian phyla. Biological Reviews 75(2):253–295. https://doi.org/10.1017/s000632310000548x

Cardinale, V., Wang, Y., Carpino, G., Cui C.-B., Gatto, M., Rossi, M., Berloco, P. B., Cantafora, A., Wauthier, E., Furth, M. E., Inverardi, L., Dominguez-Bendala, J., Ricordi, C., Gerber, D., Gaudio, E., Alvaro, D., and Reid, L. 2011. Multipotent stem/progenitor cells in human biliary tree give rise to hepatocytes, cholangiocytes, and pancreatic islets. Hepatology 54(6):2159–2172. https://doi.org/10.1002/hep.24590

Castorina, S., Luca, T., Torrisi, A., Privitera, G., and Panebianco, M. 2008. Isolation of epithelial cells with hepatobiliary phenotype. Italian Journal of Anatomy and Embryology 113(4):199–207

Chen, F., Jimenez, R. J., Sharma, K., Luu, H. Y., Hsu, B., Ravindranathan, A., Stohr, B. A., and Willenbring, H. 2020. Broad distribution of hepatocyte proliferation in liver homeostasis and regeneration. Cell Stem Cell 26(1):27–33. https://doi.org/10.1016/j.stem.2019.11.001

Chen, J., Chen, L., Zern, M. A., Theise, N. D., Diehl, A. M., Liu, P., and Duan, Y. 2017. The diversity and plasticity of adult hepatic progenitor cells and their niche. Liver International 37(9):1260–1271. https://doi.org/10.1111/liv.13377

Chen, L., Zhang, W., Zhou, Q., Yang, H., Liang, H., Zhang, B., Long, X., and Chen, X. 2012. HSCs play a distinct role in different phases of oval cell-mediated liver regeneration. Cell Biochemistry and Function 30(7):588–596. https://doi.org/10.1002/cbf.2838

Choi, J., Kang, S., Kim, B., So, S., Han, J., Kim, G.-N., Lee, M.-Y., Roh, S., Lee, J.-Y., Oh, S. J., Sung, Y. H., Lee, Y., Kim, S. H., and Kang, E. 2021. Efficient hepatic differentiation and regeneration potential under xeno-free conditions using mass-producible amnionderived mesenchymal stem cells. Stem Cell Research and Therapy 12:569. https://doi.org/10.1186/s13287-021-02470-y

Choi, T. Y., Ninov, N., Stainier, D. Y., and Shin, D. 2014. Extensive conversion of hepatic biliary epithelial cells to hepatocytes after near total loss of hepatocytes in zebrafish. Gastroenterology 146(3):776–788. https://doi.org/10.1053/j.gastro.2013.10.019

Cienfuegos, J. A., Rotellar, F., Baixauli, J., Martínez-Regueira, F., Pardo, F., and Hernández-Lizoáin, J. L. 2014. Liver regeneration - the best kept secret. A model of tissue injury response. Revista Española de Enfermedades Digestivas 106(3):171–194

Clevers, H. and Watt, F. M. 2018. Defining adult stem cells by function, not by phenotype. Annual Review of Biochemistry 87(1):1015–1027. https://doi.org/10.1146/annurev-biochem-062917-012341

Conway, M. S. 2000. The Cambrian “explosion”: Slow-fuse or megatonnage? PNAS 97(9):4426–4429. https://doi.org/10.1073/pnas.97.9.4426

Cox, A. G., Saunders, D. C., Kelsey, P. B. Jr., Conway, A. A., Tesmenitsky, Y., Marchini, J. F., Brown, K. K., Stamler, J. S., Colagiovanni, D. B., Rosenthal, G. J., Croce, K. J., North, T. E., and Goessling, W. 2014. S-nitrosothiol signaling regulates liver development and improves outcome following toxic liver injury. Cell Reports 6(1):56–69. https://doi.org/10.1016/j.celrep.2013.12.007

Danielson, P. B. 2002. The cytochrome P450 superfamily: Biochemistry, evolution and drug metabolism in humans. Current Drug Metabolism 3(6):561–597. https://doi.org/10.2174/1389200023337054

Delgado-Coello, B. 2021. Liver regeneration observed across the different classes of vertebrates from an evolutionary perspective. Heliyon 7(3):1–10. https://doi.org/10.1016/j.heliyon.2021.e06449

Dollé, L., Best, J., Mei, J., Battah, F. A., Reynaert, H., van Grunsven, L. A., and Geerts, A. 2010. The quest for liver progenitor cells: A practical point of view. Journal of Hepatology 52(1):117–129. https://doi.org/10.1016/j.jhep.2009.10.009

Dorrell, C., Erker, L., Schug, J., Kopp, J. L., Canaday, P. S., Fox, A. J., Smirnova, O., Duncan, A. W., Finegold, M. J., Sander, M., Kaestner, K. H., and Grompe, M. 2011. Prospective isolation of a bipotential clonogenic liver progenitor cell in adult mice. Genes & Development 25(11):1193–1203. https://doi.org/10.1101/gad.2029411

Duncan, A. W., Dorrell, C., and Grompe, M. 2009. Stem cells and liver regeneration. Gastroenterology 137(2):466–481. https://doi.org/10.1053/j.gastro.2009.05.044

Duret, C., Gerbal-Chaloin, S., Ramos, J., Fabre, J.-M., Jacquet, E., Navarro, F., Blanc, P., Sa-Cunha, A., Maurel, P., and Daujat-Chavanieu, M. 2007. Isolation, characterization, and differentiation to hepatocyte-like cells of nonparenchymal epithelial cells from adult human liver. Stem Cells 25(7):1779–1790. https://doi.org/10.1634/stemcells.2006-0664

Durnez, A., Verslype, C., Nevens, F., Fevery, J., Aerts R., Pirenne, J., Lesaffre, E., Libbrecht, L., Desmet, V., and Roskams T. 2006. The clinicopathological and prognostic relevance of cytokeratin 7 and 19 expression in hepatocellular carcinoma. A possible progenitor cell origin. Histopathology 49(2):138–151. https://doi.org/10.1111/j.1365-2559.2006.02468.x

Ellis, J. L., Bove, K. E., Schuetz, E. G., Leino, D., Valencia, C. A., Schuetz, J. D., Miethke, A., and Yin, C. 2018. Zebrafish abcb11b mutant reveals strategies to restore bile excretion impaired by bile salt export pump deficiency. Hepatology 67(4):1531–1545. https://doi.org/10.1002/hep.29632

Farber, E. 1956. Similarities in the sequence of early histological changes induced in the liver of the rat by ethionine, 2-acetylamino-fluorene, and 3′-methyl-4-dimethylaminoazobenzene. Cancer Research 16(2):142–148.

Fausto, N. and Campbell, J. S. 2003. The role of hepatocytes and oval cells in liver regeneration and repopulation. Mechanisms of Development 120(1):117–130. https://doi.org/10.1016/S0925-4773(02)00338-6

Fischer, H., Koenig, U., Eckhart, L., and Tschachler, E. 2002. Human caspase 12 has acquired deleterious mutations. Biochemical and Biophysical Research Communications 293(2):722–726. https://doi.org/10.1016/S0006-291X(02)00289-9

Font-Burgada, J., Shalapour, S., Ramaswamy, S., Hsueh, B., Rossell, D., Umemura, A., Taniguchi, K., Nakagawa, H., Valasek, M. A., Ye, L., Kopp, J. L., Sander, M., Carter, H., Deisseroth, K., Verma, I. M., and Kari, M. 2015. Hybrid periportal hepatocytes regenerate the injured liver without giving rise to cancer. Cell 162(4):766–779. https://doi.org/10.1016/j.cell.2015.07.026

Frampton, J., Irmisch, A., Green, C. M., Neiss, A., Trickey, M., Ulrich, H. D., Furuya, K., Watts, F. Z., Carr, A. M., and Lehmann, A. R. 2006. Postreplication repair and PCNA modification in Schizosaccharomyces pombe. Molecular Biology of the Cell 17(7):2976–2985. https://doi.org/10.1091/mbc.e05-11-1008

Furuyama, K., Kawaguchi, Y., Akiyama, H., Horiguchi, M., Kodama, S., Kuhara T., Hosokawa, S., Elbahrawy, A., Soeda, T., Koizumi, M., Masui, T., Kawaguchi, M., Takaori, K., Doi, R., Nishi, E., Kakinoki, R., Deng, J. M., Behringer, R. R, Nakamura, T., and Uemoto, S. 2011. Continuous cell supply from a Sox9-expressing progenitor zone in adult liver, exocrine pancreas and intestine. Nature Genetics 43(1):34–41. https://doi.org/10.1038/ng.722

Gao, C. and Peng, J. 2021. All routes lead to Rome: multifaceted origin of hepatocytes during liver regeneration. Cell Regeneration 10:2. https://doi.org/10.1186/s13619-020-00063-3

Gardner, J. D., Laurin, M., and Organ, C. L. 2020. The relationship between genome size and metabolic rate in extant vertebrates. Philosophical Transactions of the Royal Society B 375(1793):e20190146. https://doi.org/10.1098/rstb.2019.0146

Gaudio, E., Carpino, G., Cardinale, V., Franchitto, A., Onori, P., and Alvaro, D. 2009. New insights into liver stem cells. Digestive and Liver Disease 41(7):455–462. https://doi.org/10.1016/j.dld.2009.03.009

Gernhöfer, M., Pawert, M., Schramm, M., Müller, E., and Triebskorn, R. 2001. Ultrastructural biomarkers as tools to characterize the health status of fish in contaminated streams. Journal of Aquatic Ecosystem Stress and Recovery 8:241–260. https://doi.org/10.1023/A:1012958804442

Goessling, W., North, T. E., Lord, A. M., Ceol, C., Lee, S., Weidinger, G., Bourque, C., Strijbosch, R., Haramis, A. P., Puder, M., Clevers, H., Moon, R. T., and Zon, L. I. 2008. APC mutant zebrafish uncover a changing temporal requirement for wnt signaling in liver development. Developmental Biology 320(1):161–174. https://doi.org/10.1016/j.ydbio.2008.05.526

Hahn, M. H. and Wray, G. 2002. The g-value paradox. Evolution and Development 4(2):73–75. https://doi.org/10.1046/j.1525-142X.2002.01069.x

He, J., Chen, J., Wei, X., Leng, H., Mu, H., Cai, P., and Luo, L. 2019. Mammalian target of rapamycin complex 1 signaling is required for the dedifferentiation from biliary cell to bipotential progenitor cell in zebrafish liver regeneration. Hepatology 70(6):2092–2106. https://doi.org/10.1002/hep.30790

He, J., Lu, H., Zou, Q., and Luo, L. 2014. Regeneration of liver after extreme hepatocyte loss occurs mainly via biliary transdifferentiation in zebrafish. Gastroenterology 146(3):789–800. https://doi.org/10.1053/j.gastro.2013.11.045

Hong, N., Li, Z., and Hong, Y. 2011. Fish stem cell cultures. International Journal of Biological Sciences 7(4):392–402. https://doi.org/10.7150/ijbs.7.392

Hsieh, M. J., Chiu, T.-J., Lin, Y.-Ch., Weng, C.-C., Weng, Y.-T., Hsiao, C.-C., and Cheng, K.-H. 2020. Inactivation of APC induces CD34 upregulation to promote epithelial-mesenchymal transition and cancer stem cell traits in pancreatic cancer. International Journal of Molecular Sciences 21(12):4473. https://doi.org/10.3390/ijms21124473

Huang, M., Chang, A., Choi, M., Zhou, D., Anania, F. A., and Shin, C. H. 2014. Antagonistic interaction between Wnt and Notch activity modulates the regenerative capacity of a zebrafish liver model. Developmental Biology 388(1):91–100. https://doi.org/10.1016/j.ydbio.2014.01.003

Huang, R. Zhang, X., Gracia-Sancho, J., and Xie, W.-F. 2022. Liver regeneration: Cellular origin and molecular mechanisms. Liver International 42(7):1486–1495. https://doi.org/10.1111/liv.15174

Itoh, T. 2016. Stem/progenitor cells in liver regeneration. Hepatology 64(2):663–668. https://doi.org/10.1002/hep.28661

Jayatri, D. 2006. The role of mitochondrial respiration in physiological and evolutionary adaptation. Bio Essays 28(1):890–901. https://doi.org/10.1002/bies.20463

Jensen, C. H., Jauho, E. I., Santoni-Rugiu, E., Holmskov, U., Teisner, B., Tygstrup, N., and Bisgaard, H. C. 2004. Transit amplifying ductular (oval) cells and their hepatocytic progeny are characterized by a novel and distinctive expression of delta like protein/preadipocyte factor 1/fetal antigen 1. The American Journal of Pathology 164(4):1347–1359. https://doi.org/10.1016/S0002-9440(10)63221-X

Kalina, T., Flores-Montero, J., van der Velden, V. H., Martin-Ayuso, M., Böttcher, S., Ritgen, M., Almeida, J., Lhermitte, L., Asnafi, V., Mendonça, A., de Tute, R., Cullen, M., Sedek, L., Vidriales, M. B., Pérez, J. J., te Marvelde, J. G., Mejstrikova, E., Hrusak. O., Szczepański, T., van Dongen, J. J., and Orfao, A. 2012. EuroFlow standardization of flow cytometer instrument settings and immunophenotyping protocols. Leukemia 26(9):1986-2010. https://doi.org/10.1038/leu.2012.122

Kang, L.-I., Mars, W. M., and Michalopoulos, G. K. 2012. Signals and cells involved in regulating liver regeneration. Cells 1(4):1261–1292. https://doi.org/10.3390/cells1041261

Kholodenko, I. V., Kurbatov, L. K., Kholodenko, R. V., Manukyan, G. V., and Yarygin, K. N. 2019. Mesenchymal stem cells in the adult human liver: Hype or hope? Cells 8(10):e1127. https://doi.org/10.3390/cells8101127

King, A., Houlihan, D. D., Kavanagh, D., Haldar, D., Luu, N., Owen, A., Suresh, S., Than, N. N., Reynolds, G., Penny, J., Sumption, H., Ramachandran, P., Henderson, N. C., Kalia, N., Frampton, J., Adams, D. H., and Newsome, P. N. 2017. Sphingosine-1-phosphate prevents egress of hematopoietic stem cells from liver to reduce fibrosis. Gastroenterology 153(1):233–248. https://doi.org/10.1053/j.gastro.2017.03.022

Ko, S., Russell, J. O., Tian, J., Gao, C., Kobayashi, M., Feng, R., Yuan, X., Shao, C., Ding, H., Poddar, M., Singh, S., Locker, J., Weng, H. L., Monga, S. P., and Shin, D. 2019. Hdac1 regulates differentiation of bipotent liver progenitor cells during regeneration via Sox9b and Cdk8. Gastroenterology 156(1):187–202. https://doi.org/10.1053/j.gastro.2018.09.039

Kordes, C., Sawitza, I., Götze, S., Herebian, D., and Häussinger, D. 2014. Hepatic stellate cells contribute to progenitor cells and liver regeneration. Journal of Clinical Investigation 124(12):5503–5515. https://doi.org/10.1172/JCI74119

Kordes, C. and Haussinger, D. 2013. Hepatic stem cell niches. The Journal of Clinical Investigation 123(5):1874–1880. https://doi.org/10.1172/JCI66027

Kowalik, M. A., Sulas, P., Ledda-Columbano G. M., Giordano, S., Columbano, A., and Perra, A. 2015. Cytokeratin-19 positivity is acquired along cancer progression and does not predict cell origin in rat hepatocarcinogenesis. Oncotarget 6(36):38749–38763. https://doi.org/10.18632/oncotarget.5501

Kremer, N. Sh. 2004. Probability theory and mathematical statistics: textbook. 550 p., Iuniti-Dana Publ., Moscow. (In Russian)

Leão, T., Siqueira, M., Marcondes, S., Franco-Belussi, L., De Oliveira, C., and Fernandes, C. E. 2021. Comparative liver morphology associated with the hepatosomatic index in five Neotropical anuran species. The Anatomical Record 304(4):860–871. https://doi.org/10.1002/ar.24540

Lebedeva, E. I. 2021. Role of CK19-positive cells of portal zones in thioacetamidine-induced rat liver cirrhosis. Cytology 63(4):379–389. https://doi.org/10.31857/S0041377121040052

Lemaigre, F. P. 2015. Determining the fate of hepatic cells by lineage tracing: facts and pitfalls. Hepatology 61(6):2100-3. https://doi.org/10.1002/hep.27659

Li, J., Xin, J., Zhang, L., Wu, J., Jiang, L., Zhou, Q., Li, J., Guo, J., Cao, H., and Li, L. 2014. Human hepatic progenitor cells express hematopoietic cell markers CD45 and CD109. International Journal of Medical Sciences 11(1):65–79. https://doi.org/10.7150/ijms.7426

Li, W., Yang, L., He, Q., Hu, C., Zhu, L., Ma, X., Ma, X., Bao, S., Li, L., Chen, Y., Deng, X., Zhang, X., Cen, J., Zhang, L., Wang, Z., Xie, W. F., Li, H., Li, Y., Hui, L. A. 2019. A homeostatic Arid1a-dependent permissive chromatin state licenses hepatocyte responsiveness to liver-injury-associated YAP signaling. Cell Stem Cell 25(1):54–68. https://doi.org/10.1016/j.stem.2019.06.008

Litzgus, J. D. and Hopkins, W. A. 2003. Effect of temperature on metabolic rate of the mud turtle (Kinosternon subrubrum). Thermal Biology 28(8):595–600. https://doi.org/10.1016/j.jtherbio.2003.08.005

López-Luque, J. and Fabregat, I. 2018. Revisiting the liver: from development to regeneration — what we ought to know! The International Journal of Developmental Biology 62(6-7-8):441–451. https://doi.org/10.1387/ijdb.170264JL

Ma, Z., Li, F., Chen, L., Gu, T., Zhang, Q., Qu, Y., Xu, M., Cai, X., and Lu, L. 2019. Autophagy promotes hepatic differentiation of hepatic progenitor cells by regulating the Wnt/β-catenin signaling pathway. Journal of Molecular Histology 50(1):75–90. https://doi.org/10.1007/s10735-018-9808-x

Mancino, M. G., Carpino, G., Onori, P., Franchitto, A., Alvaro, D., and Gaudio, E. 2007. Hepatic “stem” cells: State of the art. Italian Journal of Anatomy and Embryology 112(2):93–109.

Manco, R., Clerbaux, L.-A., Verhulst, S., Nader, M. B., Sempoux, C., Ambroise, J., Bearzatto, B., Gala, J. L., Horsmans, Y., van Grunsven, L., Desdouets, C., and Leclercq, I. 2019. Reactive cholangiocytes differentiate into proliferative hepatocytes with efficient DNA repair in mice with chronic liver injury. Hepatology 70(6):1180–1191. https://doi.org/10.1016/j.jhep.2019.02.003

Mederacke, I., Hsu, C. C., Troeger, J. S., Huebener, P., Mu, X., Dapito, D. H., Pradere, J.-P., and Schwabe, R. F. 2013. Fate tracing reveals hepatic stel-late cells as dominant contributors to liver fibrosis independent of its aetiology. Nature Communications 4(1):e2823. https://doi.org/10.1038/ncomms3823

Michalopoulos, G. K. and Bhushan, B. 2021. Liver regeneration: biological and pathological mechanisms and implications. Nature Reviews Gastroenterology and Hepatology 18(1):40–55. https://doi.org/10.1038/s41575-020-0342-4

Mishhenko, V. A., Petrova, I. M., and Medvedeva, S. Ju. 2017. General histology: Teaching manual. Ed. by V. A. Mishhenko. 84 p. Izdatel'stvo Ural'skogo universiteta Publ., Ekaterinburg. (In Russian)

Miyajima, A., Tanaka, M., and Itoh, T. 2014. Stem/progenitor cells in liver development, homeostasis, regeneration and reprogramming. Cell Stem Cell 14(5):562–574. https://doi.org/10.1016/j.stem.2014.04.010

Nelson, D. M., Smith, S. D., Furesz, T. C., Sadovsky, Y., Ganapathy, V., Parvin, C. A., and Smith, C. H. 2003. Hypoxia reduces expression and function of system A amino acid transporters in cultured term human trophoblasts. American Journal of Physiology: Cell Physiology 284(2):310–315. https://doi.org/10.1152/ajpcell.00253.2002

Oderberg, I. M. and Goessling, W. 2023. Biliary epithelial cells are facultative liver stem cells during liver regeneration in adult zebrafish. JCI Insight 8(1):e163929. https://doi.org/10.1172/jci.insight.163929

Okabe, M., Tsukahara, Y., Tanaka, M., Suzuki, K., Saito, S., Kamiya, Y., Tsujimura, T., Nakamura, K., and Miyajima, A. 2009. Potential hepatic stem cells reside in EpCAM+ cells of normal and injured mouse liver. Development 136(11):1951–1960. https://doi.org/10.1242/dev.031369

Omori, N., Omori, M., Evarts, R. P., Teramoto, T., Miller, M. J., Hoang, T. N., and Thorgeirsson, S. S. 1997. Partial cloning of rat CD34 cDNA and expression during stem cell-dependent liver regeneration in the adult rat. Hepatology 26(3):720–727. https://doi.org/10.1002/hep.510260325

Onishhenko, N. A, Ljundup, A. V, Deev, R. V, Shagidulin, M. Ju., and Krasheninnikov, M. E. 2011. Sinusoidal liver cells and bone marrow cells as components of the common functional system for regulation of recovery morphogenesis of healthy and damaged liver. Kletochnaia transplantologiia i tkanevaia inzheneriia 2(6):78–92. (In Russian)

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., Ono, N., Shalek, A. K., van Oudenaarden, A., and Camargo, F. D. 2019. Single-cell analysis of the liver epithelium reveals dynamic heterogeneity and an essential role for YAP in homeostasis and regeneration. Cell Stem Cell 25(1):23–38. https://doi.org/10.1016/j.stem.2019.04.004

Planas-Paz, L., Sun, T., Pikiolek, M., Cochran, N. R., Bergling, S., Orsini, V., Yang, Z., Sigoillot, F., Jetzer, J., Syed, M., Neri, M., Schuierer, S., Morelli, L., Hoppe, P. S., Schwarzer, W., Cobos, C. M., Alford, J. L., Zhang, L., Cuttat, R., Waldt, A., Carballido-Perrig, N., Nigsch, F., Kinzel, B., Nicholson, T. B., Yang, Y., Mao, X., Terracciano, L. M., Russ, C., Reece-Hoyes, J. S., Gubser Keller, C., Sailer, A. W., Bouwmeester, T., Greenbaum, L. E., Lugus, J. J., Cong, F., McAllister, G., Hoffman, G. R., Roma, G., and Tchorz, J. S. 2019. YAP, but not RSPO-LGR4/5, signaling in biliary epithelial cells promotes a ductular reaction in response to liver injury. Cell Stem Cell 25(1):39–53. https://doi.org/10.1016/j.stem.2019.04.005

Pritchard, J. B. 2002. Comparative models and biological stress. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology 283(4):807–809. https://doi.org/10.1152/ajpregu.00415.2002

Raven, A., Lu, W.-Y., Man, T. Y., Ferreira-Gonzalez, S., O’Duibhir, E., Dwyer, B. J., Thomson, J. P., Meehan, R. R., Bogorad, R., Koteliansky, V., Kotel-evtsev, Y., Ffrench-Constant, C., Boulter, L., and Forbes, S. J. 2017. Cholangiocytes act as facultative liver stem cells during impaired hepatocyte regeneration. Nature 547(7663):350–354. https://doi.org/10.1038/nature23015

Rome, L. C. and Swank, D. M. 2001. The influence of thermal acclimation on power production during swimming. In vivo stimulation and length change pattern of scup red muscle. Journal of Experimental Biology 204(Pt 3):409–418. https://doi.org/10.1242/jeb.204.3.409

Russell, J. O., Lu, W.-Y., Okabe, H., Abrams, M., Oertel, M., Poddar, M., Singh, S., Forbes, S. J., and Monga, S. P. 2019. Hepatocyte-specific β-catenin deletion during severe liver injury provokes cholangiocytes to differentiate into hepatocytes. Hepatology 69(2):742–759. https://doi.org/10.1002/hep.30270

Sackett, S. D., Li, Z., Hurtt, R., Gao, Y., Wells, R. G., Brondell, K., Kaestner, K. H., and Greenbaum, L. E. 2009. Foxl1 is a marker of bipotential hepatic progenitor cells in mice. Hepatology 49(3):920–929. https://doi.org/10.1002/hep.22705

Schaub, J. R., Malato, Y., Gormond, C., and Willenbring, H. 2014. Evidence against a stem cell origin of new hepatocytes in a common mouse model of chronic liver injury. Cell Reports 8(4):933–939. https://doi.org/10.1016/j.celrep.2014.07.003

Schleucher, E. and Withers, P. С. 2002. Metabolic and thermal physiology of pigeons and doves. Physiological and Biochemical Zoology 75(5):439–450. https://doi.org/10.1086/342803

Scholz, H., 2002. Adaptational responses to hypoxia. American Journal of Physiology Regulatory, Integrative and Comparative Physiology 282(6):1541–1543. https://doi.org/10.1152/ajpregu.00136.2002

Shahbazov, V. G., 2001. Ecological and Biophysical Genetics: selected works. 435 p. Shtrikh Publ., Kharkiv. (In Russian)

Shin, D. and Monga, S. P. 2013. Cellular and molecular basis of liver development. Comprehensive Physiology 3(2):799–815. https://doi.org/10.1152/10.1002/cphy.c120022

Stanger, B. Z. 2015. Cellular homeostasis and repair in the mammalian liver. Annual Review of Physiology 77:179–200. https://doi.org/10.1146/annurev-physiol-021113-170255

Siapati, E. K., Roubelakis, M. G., and Vassilopoulos, G. 2011. Liver-derived progenitor cells: isolation and characterization. Methods in Molecular Biology 763:131–142. https://doi.org/10.1007/978-1-61779-108-4_10

So, J., Kim, A., Lee, S.-H., and Shin, D. 2020. Liver progenitor cell-driven liver regeneration. Experimental and Molecular Medicine 52(8):1230–1238. https://doi.org/10.1038/s12276-020-0483-0

So, J., Kim, M., Lee, S.-H., Ko, S., Lee, D. A., Park, H., Azuma, M., Parsons, M. J., Prober, D., and Shin, D. 2020. Attenuating the epidermal growth factor receptor–extracellular signal-regulated kinase–sex-determining region Y-box 9 axis promotes liver progenitor cell-mediated liver regeneration in Zebrafish. Hepatology 73(4):1494–1508. https://doi.org/10.1002/hep.31437

Stueck, A. E. and Wanless, I. R. 2015. Hepatocyte buds derived from progenitor cells repopulate regions of parenchymal extinction in human cirrhosis. Hepatology 61(5):1696–1707. https://doi.org/10.1002/hep.27706

Sun, T., Pikiolek, M., Orsini, V., Bergling, S., Holwerda, S., Morelli, L., Hoppe, P. S., Planas-Paz, L., Yang, Y., Ruffner, H., Bouwmeester, T., Lohmann, F., Terracciano, L. M., Roma, G., Cong, F., and Tchorz, J. S. 2020. AXIN2(+) Pericentral hepatocytes have limited contributions to liver homeostasis and regeneration. Cell Stem Cell 26(1):97–107. https://doi.org/10.1016/j.stem.2019.10.011

Suzuki, A., Sekiya, S., Onishi, M., Oshima, N., Kiyonari, H., Nakauchi, H., and Taniguchi, H. 2008. Flow cytometric isolation and clonal identification of self-renewing bipotent hepatic progenitor cells in adult mouse liver. Hepatology 48(6):1964–1978. https://doi.org/10.1002/hep.22558

Swiderska-Syn, M., Syn, W. K., Xie, G., Krüger, L., Machado, M. V., Karaca, G., Michelotti, G. A., Choi, S. S., Premont, R. T., and Diehl, A. M. 2014. Myo-fibroblastic cells function as progenitors to regenerate murine livers after partial hepatectomy. Gut 63(8):1333–1344. https://doi.org/10.1136/gutjnl-2013-305962

Szücs, A., Paku, S., Sebestyén, E., Nagy, P., and Dezső, K. 2020. Postnatal, ontogenic liver growth accomplished by biliary/oval cell proliferation and differentiation. PLoS ONE 15(5):e0233736. https://doi.org/10.1371/journal.pone.0233736

Tarlow, B. D., Pelz, C., Naugler, W. E., Wakefield, L., Wilson, E. M., Finegold, M. J., and Grompe, M. 2014. Bipotential adult liver progenitors are derived from chronically injured mature hepatocytes. Cell Stem Cell 15(5):605–618. https://doi.org/10.1016/j.stem.2014.09.008

Tarlow, B. D., Finegold, M. J., and Grompe, M. 2014. Clonal tracing of Sox9+ liver progenitors in mouse oval cell injury. Hepatology 60(1):278–289. https://doi.org/10.1002/hep.27084

Tatematsu, M., Ho, R. H., Kaku, T., Ekem, J. K., and Farber, E. 1984. Studies on the proliferation and fate of oval cells in the liver of rats treated with 2-acetylaminofluorene and partial hepatectomy. The American Journal of Pathology 114(3):418–430.

Theise, N. D., Badve, S., Saxena, R., Henegariu, O., Sell, S., Crawford, J. M., and Krause, D. S. 2000. Derivation of hepatocytes from bone marrow cells in mice after radiation-induced myeloablation. Hepatology 31(1):235–240. https://doi.org/10.1002/hep.510310135

Tirnitz-Parker, J. E., Viebahn, C. S., Jakubowski, A., Klopcic, B. R., Olynyk, J. K., Yeoh, G. C., and Knight, B. 2010. Tumor necrosis factor-like weak inducer of apoptosis is a mitogen for liver progenitor cells. Hepatology 52(1):291–302. https://doi.org/10.1002/hep.23663

Vestentoft, P. S. 2013. Development and molecular composition of the hepatic progenitor cell niche. Danish Medical Journal 60(5):B4640.

Vinogradov, A. E. 2005. Duplicity genic the collector pf dust is satisfied also with sample CpG concerning expression in a human genome: Size against breadth. Trend in Genetics 21(12):639–643. https://doi.org/10.1016/j.tig.2005.09.002

Voejkov, V. L. 2001. The beneficial role of reactive oxygen species. https://www.ikar.udm.ru/sb/sb24-1.html

Wang, S., Miller, S. R., Ober, E. A., and Sadler, K. C. 2017. Making it new again: insight into liver development, regeneration, and disease from Zebrafish research. Current Topics in Developmental Biology 124:161–195. https://doi.org/10.1016/bs.ctdb.2016.11.012

Wang, B., Zhao, L., Fish, M., Logan, C. Y., and Nusse, R. 2015. Self-renewing diploid Axin2+ cells fuel homeostatic renewal of the liver. Nature 524(7564):180–185. https://doi.org/10.1038/nature14863

Wei, Y., Wang, Y. G., Jia, Y., Li, L., Yoon, J., Zhang, S., Wang, Z., Zhang, Y., Zhu, M., Sharma, T., Lin, Y. H., Hsieh, M. H., Albrecht, J. H., Le, P. T., Rosen, C. J., Wang, T., and Zhu, H. 2021. Liver homeostasis is maintained by midlobular zone 2 hepatocytes. Science 371(6532):eabb1625. https://doi.org/10.1126/science.abb1625

Yanger, K., Zong, Y., Maggs, L. R., Shapira, S. N., Maddipati, R., Aiello, N. M., Thung, S. N., Wells, R. G., Greenbaum, L. E., and Stanger, B. Z. 2013. Robust cellular reprogramming occurs spontaneously during liver regeneration. Genes and Development 27(7):719–724. https://doi.org/10.1101/gad.207803.112

Yanger, K., Knigin, D., Zong, Y., Maggs, L., Gu, G., Akiyama, H., Pikarsky, E., and Stanger, B. Z. 2014. Adult hepatocytes are generated by self-duplication rather than stem cell differentiation. Cell Stem Cell 15(3):340–349. https://doi.org/10.1016/j.stem.2014.06.003

Yimlamai, D., Christodoulou, C., Galli, G. G., Yanger, K., Pepe-Mooney, B., Gurung, B., Shrestha, K., Cahan, P., Stanger, B. Z., and Camargo, F. D. 2014. Hippo pathway activity influences liver cell fate. Cell 157(6):1324–1338. https://doi.org/10.1016/j.cell.2014.03.060

Yin, D.-Z., Cai, J.-Y., Zheng, Q.-Ch., Chen, Z.-W., Zhao, J.-X., and Yuan, Y.-N. 2014. Mouse A6-positive hepatic oval cells derived from embryonic stem cells. Journal of Huazhong University of Science and Technology 34(1):1–9. https://doi.org/10.1007/s11596-014-1223-2

Young, B., Woodford, P., and O’Dowd, G. 2013. Wheater’s functional histology: A Text and Colour Atlas. 6th ed. 464 p. Churchill Living-stone, London.

Zhang, L., Theise, N., Chua, M., and Reid, L. M. 2008. The stem cell niche of human livers: Symmetry between development and regeneration. Hepatology 48(5):1598–1607. https://doi.org/10.1002/hep.22516