Adult Mouse Liver Contains Two Distinct Populations of Cholangiocytes

Stem Cell Reports

Volumn 9, Issue 2, 2017, Pages 478-489

  Li, Bin ^a   Dorrell, Craig ^a   Canaday, Pamela S ^a   Pelz, Carl ^a   Haft, Annelise ^a   Finegold, Milton ^c   Grompe, Markus ^a,b  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^c TEXAS CHILDREN S HOSPITAL   (United States)

Author keywords

bile duct; biliary tree; cholangiocyte; clonogenic assay; liver; liver regeneration; organoid; progenitor

Indexed keywords

CELL SURFACE MARKER; RNA; TRANSCRIPTOME; BIOLOGICAL MARKER;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BILE DUCT; CELL HETEROGENEITY; CHOLANGIOCYTE; CLONOGENESIS; CYTOPLASM; EPITHELIUM; FLUORESCENCE ACTIVATED CELL SORTING; FLUORESCENCE IN SITU HYBRIDIZATION; GENE EXPRESSION; LIVER; MOUSE; NONHUMAN; PRIORITY JOURNAL; ANIMAL; CELL CULTURE; CELL SURVIVAL; CFU COUNTING; CYTOLOGY; FLOW CYTOMETRY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; IMMUNOPHENOTYPING; INTRAHEPATIC BILE DUCT; KNOCKOUT MOUSE; LIVER REGENERATION; MALE; METABOLISM; ORGANOID; PHENOTYPE; TRANSPLANTATION;

ANIMALS; BILE DUCTS, INTRAHEPATIC; BIOMARKERS; CELL SURVIVAL; CELLS, CULTURED; COLONY-FORMING UNITS ASSAY; FLOW CYTOMETRY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; IMMUNOPHENOTYPING; LIVER; LIVER REGENERATION; MALE; MICE; MICE, KNOCKOUT; ORGANOIDS; PHENOTYPE; TRANSCRIPTOME;

EID: 85021821600     PISSN: 22136711     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.stemcr.2017.06.003     Document Type: Article

References (40)

1. −/− mice. Nat. Biotechnol. 25 (2007), 903–910.
2. Barker, N., van Es, J.H., Kuipers, J., Kujala, P., van den Born, M., Cozijnsen, M., Haegebarth, A., Korving, J., Begthel, H., Peters, P.J., et al. Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 449 (2007), 1003–1007.
3. Barker, N., Huch, M., Kujala, P., van de Wetering, M., Snippert, H.J., van Es, J.H., Sato, T., Stange, D.E., Begthel, H., van den Born, M., et al. Lgr5(+ve) stem cells drive self-renewal in the stomach and build long-lived gastric units in vitro. Cell Stem Cell 6 (2010), 25–36.
4. Boquest, A.C., Shahdadfar, A., Fronsdal, K., Sigurjonsson, O., Tunheim, S.H., Collas, P., Brinchmann, J.E., Isolation and transcription profiling of purified uncultured human stromal stem cells: alteration of gene expression after in vitro cell culture. Mol. Biol. Cell 16 (2005), 1131–1141.
5. Brazill, D.T., Caprette, D.R., Myler, H.A., Hatton, R.D., Ammann, R.R., Lindsey, D.F., Brock, D.A., Gomer, R.H., A protein containing a serine-rich domain with vesicle fusing properties mediates cell cycle-dependent cytosolic pH regulation. J. Biol. Chem. 275 (2000), 19231–19240.
6. Dorrell, C., Erker, L., Lanxon-Cookson, K.M., Abraham, S.L., Victoroff, T., Ro, S., Canaday, P.S., Streeter, P.R., Grompe, M., Surface markers for the murine oval cell response. Hepatology 48 (2008), 1282–1291.
7. 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., et al. Prospective isolation of a bipotential clonogenic liver progenitor cell in adult mice. Genes Dev. 25 (2011), 1193–1203.
8. Dorrell, C., Tarlow, B., Wang, Y., Canaday, P.S., Haft, A., Schug, J., Streeter, P.R., Finegold, M.J., Shenje, L.T., Kaestner, K.H., et al. The organoid-initiating cells in mouse pancreas and liver are phenotypically and functionally similar. Stem Cell Res. 13 (2014), 275–283.
9. Duncan, A.W., Dorrell, C., Grompe, M., Stem cells and liver regeneration. Gastroenterology 137 (2009), 466–481.
10. Erker, L., Azuma, H., Lee, A.Y., Guo, C., Orloff, S., Eaton, L., Benedetti, E., Jensen, B., Finegold, M., Willenbring, H., et al. Therapeutic liver reconstitution with murine cells isolated long after death. Gastroenterology 139 (2010), 1019–1029.
11. Espanol-Suner, R., Carpentier, R., Van Hul, N., Legry, V., Achouri, Y., Cordi, S., Jacquemin, P., Lemaigre, F., Leclercq, I.A., Liver progenitor cells yield functional hepatocytes in response to chronic liver injury in mice. Gastroenterology 143 (2012), 1564–1575.e7.
12. Evarts, R.P., Nagy, P., Nakatsukasa, H., Marsden, E., Thorgeirsson, S.S., In vivo differentiation of rat liver oval cells into hepatocytes. Cancer Res. 49 (1989), 1541–1547.
13. Flanagan, D.J., Phesse, T.J., Barker, N., Schwab, R.H., Amin, N., Malaterre, J., Stange, D.E., Nowell, C.J., Currie, S.A., Saw, J.T., et al. Frizzled7 functions as a Wnt receptor in intestinal epithelial Lgr5(+) stem cells. Stem Cell Reports 4 (2015), 759–767.
14. Font-Burgada, J., Shalapour, S., Ramaswamy, S., Hsueh, B., Rossell, D., Umemura, A., Taniguchi, K., Nakagawa, H., Valasek, M.A., Ye, L., et al. Hybrid periportal hepatocytes regenerate the injured liver without giving rise to cancer. Cell 162 (2015), 766–779.
15. Golding, M., Sarraf, C.E., Lalani, E.N., Anilkumar, T.V., Edwards, R.J., Nagy, P., Thorgeirsson, S.S., Alison, M.R., Oval cell differentiation into hepatocytes in the acetylaminofluorene-treated regenerating rat liver. Gastroenterology 110 (1996), 1182–1190.
16. Goss, A.M., Tian, Y., Tsukiyama, T., Cohen, E.D., Zhou, D., Lu, M.M., Yamaguchi, T.P., Morrisey, E.E., Wnt2/2b and beta-catenin signaling are necessary and sufficient to specify lung progenitors in the foregut. Dev. Cell 17 (2009), 290–298.
17. Gouon-Evans, V., Boussemart, L., Gadue, P., Nierhoff, D., Koehler, C.I., Kubo, A., Shafritz, D.A., Keller, G., BMP-4 is required for hepatic specification of mouse embryonic stem cell-derived definitive endoderm. Nat. Biotechnol. 24 (2006), 1402–1411.
18. Grompe, M., Liver stem cells, where art thou?. Cell Stem Cell 15 (2014), 257–258.
19. Grozdanov, P.N., Yovchev, M.I., Dabeva, M.D., The oncofetal protein glypican-3 is a novel marker of hepatic progenitor/oval cells. Lab. Invest. 86 (2006), 1272–1284.
20. Huch, M., Dorrell, C., Boj, S.F., van Es, J.H., Li, V.S., van de Wetering, M., Sato, T., Hamer, K., Sasaki, N., Finegold, M.J., et al. In vitro expansion of single Lgr5+ liver stem cells induced by Wnt-driven regeneration. Nature 494 (2013), 247–250.
21. Huch, M., Gehart, H., van Boxtel, R., Hamer, K., Blokzijl, F., Verstegen, M.M., Ellis, E., van Wenum, M., Fuchs, S.A., de Ligt, J., et al. Long-term culture of genome-stable bipotent stem cells from adult human liver. Cell 160 (2015), 299–312.
22. Kamimoto, K., Kaneko, K., Kok, C.Y., Okada, H., Miyajima, A., Itoh, T., Heterogeneity and stochastic growth regulation of biliary epithelial cells dictate dynamic epithelial tissue remodeling. Elife, 5, 2016, 10.7554/eLife.15034.
23. Koo, B.K., Clevers, H., Stem cells marked by the R-spondin receptor LGR5. Gastroenterology 147 (2014), 289–302.
24. Langmead, B., Trapnell, C., Pop, M., Salzberg, S.L., Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol., 10, 2009, R25.
25. Lim, E., Wu, D., Pal, B., Bouras, T., Asselin-Labat, M.L., Vaillant, F., Yagita, H., Lindeman, G.J., Smyth, G.K., Visvader, J.E., Transcriptome analyses of mouse and human mammary cell subpopulations reveal multiple conserved genes and pathways. Breast Cancer Res., 12, 2010, R21.
26. Liu, D., Wang, Y., Jia, Z., Wang, L., Wang, J., Yang, D., Song, J., Wang, S., Fan, Z., Demethylation of IGFBP5 by histone demethylase KDM6B promotes mesenchymal stem cell-mediated periodontal tissue regeneration by enhancing osteogenic differentiation and anti-inflammation potentials. Stem Cells 33 (2015), 2523–2536.
27. Love, M.I., Huber, W., Anders, S., Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol., 15, 2014, 550.
28. Mahmoud, L., Al-Saif, M., Amer, H.M., Sheikh, M., Almajhdi, F.N., Khabar, K.S., Green fluorescent protein reporter system with transcriptional sequence heterogeneity for monitoring the interferon response. J. Virol. 85 (2011), 9268–9275.
29. Miyajima, A., Tanaka, M., Itoh, T., Stem/progenitor cells in liver development, homeostasis, regeneration, and reprogramming. Cell Stem Cell 14 (2014), 561–574.
30. Mootha, V.K., Lindgren, C.M., Eriksson, K.F., Subramanian, A., Sihag, S., Lehar, J., Puigserver, P., Carlsson, E., Ridderstrale, M., Laurila, E., et al. PGC-1alpha-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat. Genet. 34 (2003), 267–273.
31. Paku, S., Schnur, J., Nagy, P., Thorgeirsson, S.S., Origin and structural evolution of the early proliferating oval cells in rat liver. Am. J. Pathol. 158 (2001), 1313–1323.
32. Schaub, J.R., Malato, Y., Gormond, C., Willenbring, H., Evidence against a stem cell origin of new hepatocytes in a common mouse model of chronic liver injury. Cell Rep. 8 (2014), 933–939.
33. Snow, G.E., Kasper, A.C., Busch, A.M., Schwarz, E., Ewings, K.E., Bee, T., Spinella, M.J., Dmitrovsky, E., Freemantle, S.J., Wnt pathway reprogramming during human embryonal carcinoma differentiation and potential for therapeutic targeting. BMC Cancer, 9, 2009, 383.
34. Subramanian, A., Tamayo, P., Mootha, V.K., Mukherjee, S., Ebert, B.L., Gillette, M.A., Paulovich, A., Pomeroy, S.L., Golub, T.R., Lander, E.S., et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl. Acad. Sci. USA 102 (2005), 15545–15550.
35. Tarlow, B.D., Finegold, M.J., Grompe, M., Clonal tracing of Sox9(+) liver progenitors in mouse oval cell injury. Hepatology 60 (2014), 278–289.
36. Tarlow, B.D., Pelz, C., Naugler, W.E., Wakefield, L., Wilson, E.M., Finegold, M.J., Grompe, M., Bipotential adult liver progenitors are derived from chronically injured mature hepatocytes. Cell Stem Cell 15 (2014), 605–618.
37. Wang, B., Zhao, L., Fish, M., Logan, C.Y., Nusse, R., Self-renewing diploid Axin2(+) cells fuel homeostatic renewal of the liver. Nature 524 (2015), 180–185.
38. 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., Robust cellular reprogramming occurs spontaneously during liver regeneration. Genes Dev. 27 (2013), 719–724.
39. Zhang, M.Z., Mai, W., Li, C., Cho, S.Y., Hao, C., Moeckel, G., Zhao, R., Kim, I., Wang, J., Xiong, H., et al. PKHD1 protein encoded by the gene for autosomal recessive polycystic kidney disease associates with basal bodies and primary cilia in renal epithelial cells. Proc. Natl. Acad. Sci. USA 101 (2004), 2311–2316.
40. Zhao, N., Nizzi, C.P., Anderson, S.A., Wang, J., Ueno, A., Tsukamoto, H., Eisenstein, R.S., Enns, C.A., Zhang, A.S., Low intracellular iron increases the stability of matriptase-2. J. Biol. Chem. 290 (2015), 4432–4446.