Heterogeneity and stochastic growth regulation of biliary epithelial cells dictate dynamic epithelial tissue remodeling

eLife

Volumn 5, Issue 2016JULY, 2016, Pages

  Kamimoto, Kenji ^a   Kaneko, Kota ^a   Kok, Cindy Yuet Yin ^a   Okada, Hajime ^a   Miyajima, Atsushi ^a   Itoh, Tohru ^a  

^a UNIVERSITY OF TOKYO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

EPITHELIUM CELL; GROWTH REGULATION; HUMAN; STEM CELL; STOCHASTIC MODEL; ANIMAL; DISEASE MODEL; EPITHELIUM; INJURIES; LIVER; MOUSE; PHYSIOLOGY; REGENERATION; THEORETICAL MODEL;

ANIMALS; DISEASE MODELS, ANIMAL; EPITHELIAL CELLS; EPITHELIUM; LIVER; MICE; MODELS, THEORETICAL; REGENERATION;

EID: 84979582031     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.15034     Document Type: Article

References (44)

1. Barker N, Bartfeld S, Clevers H. 2010. Tissue-resident adult stem cell populations of rapidly self-renewing organs. Cell Stem Cell 7: 656-670. doi: 10.1016/j.stem.2010.11.016
2. De Minicis S, Kisseleva T, Francis H, Baroni GS, Benedetti A, Brenner D, Alvaro D, Alpini G, Marzioni M. 2013. Liver carcinogenesis: rodent models of hepatocarcinoma and cholangiocarcinoma. Digestive and Liver Disease 45: 450-459. doi: 10.1016/j.dld.2012.10.008
3. Dorrell C, Erker L, Schug J, Kopp JL, Canaday PS, Fox AJ, Smirnova O, Duncan AW, Finegold MJ, Sander M, Kaestner KH, Grompe M. 2011. Prospective isolation of a bipotential clonogenic liver progenitor cell in adult mice. Genes & Development 25: 1193-1203. doi: 10.1101/gad.2029411
4. Doupé DP, Klein AM, Simons BD, Jones PH. 2010. The ordered architecture of murine ear epidermis is maintained by progenitor cells with random fate. Developmental Cell 18: 317-323. doi: 10.1016/j.devcel.2009. 12.016
5. Driessens G, Beck B, Caauwe A, Simons BD, Blanpain C. 2012. Defining the mode of tumour growth by clonal analysis. Nature 488: 527-530. doi: 10.1038/nature11344
6. Duncan AW, Dorrell C, Grompe M. 2009. Stem cells and liver regeneration. Gastroenterology 137: 466-481. doi: 10.1053/j.gastro.2009.05.044
7. Edwards JR, Diamantakos EA, Peuler JD, Lamar PC, Prozialeck WC. 2007. A novel method for the evaluation of proximal tubule epithelial cellular necrosis in the intact rat kidney using ethidium homodimer. BMC Physiology 7: 1. doi: 10.1186/1472-6793-7-1
8. Enver T, Pera M, Peterson C, Andrews PW. 2009. Stem cell states, fates, and the rules of attraction. Cell Stem Cell 4: 387-397. doi: 10.1016/j.stem.2009.04.011
9. Etzrodt M, Endele M, Schroeder T. 2014. Quantitative single-cell approaches to stem cell research. Cell Stem Cell 15: 546-558. doi: 10.1016/j.stem.2014.10.015
10. Gouw AS, Clouston AD, Theise ND. 2011. Ductular reactions in human liver: diversity at the interface. Hepatology 54: 1853-1863. doi: 10.1002/hep.24613
11. Grompe M. 2014. Liver stem cells, where art thou? Cell Stem Cell 15: 257-258. doi: 10.1016/j.stem.2014.08.004
12. Hara K, Nakagawa T, Enomoto H, Suzuki M, Yamamoto M, Simons BD, Yoshida S. 2014. Mouse spermatogenic stem cells continually interconvert between equipotent singly isolated and syncytial states. Cell Stem Cell 14: 658-672. doi: 10.1016/j.stem.2014.01.019
13. Ishikawa T, Factor VM, Marquardt JU, Raggi C, Seo D, Kitade M, Conner EA, Thorgeirsson SS. 2012. Hepatocyte growth factor/c-met signaling is required for stem-cell-mediated liver regeneration in mice. Hepatology 55: 1215-1226. doi: 10.1002/hep.24796
14. Kaneko K, Kamimoto K, Miyajima A, Itoh T. 2015. Adaptive remodeling of the biliary architecture underlies liver homeostasis. Hepatology 61: 2056-2066. doi: 10.1002/hep.27685
15. Ke MT, Fujimoto S, Imai T. 2013. SeeDB: a simple and morphology-preserving optical clearing agent for neuronal circuit reconstruction. Nature Neuroscience 16: 1154-1161. doi: 10.1038/nn.3447
16. Kok CY, Cunningham SC, Carpenter KH, Dane AP, Siew SM, Logan GJ, Kuchel PW, Alexander IE. 2013. Adeno- associated virus-mediated rescue of neonatal lethality in argininosuccinate synthetase-deficient mice. Molecular Therapy 21: 1823-1831. doi: 10.1038/mt.2013.139
17. Lu WY, Bird TG, Boulter L, Tsuchiya A, Cole AM, Hay T, Guest RV, Wojtacha D, Man TY, Mackinnon A, Ridgway RA, Kendall T, Williams MJ, Jamieson T, Raven A, Hay DC, Iredale JP, Clarke AR, Sansom OJ, Forbes SJ. 2015. Hepatic progenitor cells of biliary origin with liver repopulation capacity. Nature Cell Biology 17: 971-983. doi: 10.1038/ncb3203
18. Madisen L, Zwingman TA, Sunkin SM, Oh SW, Zariwala HA, Gu H, Ng LL, Palmiter RD, Hawrylycz MJ, Jones AR, Lein ES, Zeng H. 2010. A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nature Neuroscience 13: 133-140. doi: 10.1038/nn.2467
19. Michalopoulos GK, Barua L, Bowen WC. 2005. Transdifferentiation of rat hepatocytes into biliary cells after bile duct ligation and toxic biliary injury. Hepatology 41: 535-544. doi: 10.1002/hep.20600
20. Michalopoulos GK, Khan Z. 2015. Liver Stem Cells: Experimental Findings and Implications for Human Liver Disease. Gastroenterology 149: 876-882. doi: 10.1053/j.gastro.2015.08.004
21. Michalopoulos GK. 2014. The liver is a peculiar organ when it comes to stem cells. American Journal of Pathology 184: 1263-1267. doi: 10.1016/j.ajpath.2014.02.020
22. Miyajima A, Tanaka M, Itoh T. 2014. Stem/progenitor cells in liver development, homeostasis, regeneration, and reprogramming. Cell Stem Cell 14: 561-574. doi: 10.1016/j.stem.2014.04.010
23. Nagahama Y, Sone M, Chen X, Okada Y, Yamamoto M, Xin B, Matsuo Y, Komatsu M, Suzuki A, Enomoto K, Nishikawa Y. 2014. Contributions of hepatocytes and bile ductular cells in ductular reactions and remodeling of the biliary system after chronic liver injury. American Journal of Pathology 184: 3001-3012. doi: 10.1016/j. ajpath.2014.07.005
24. O’Neill A, Schaffer DV. 2004. The biology and engineering of stem-cell control. Biotechnology and Applied Biochemistry 40: 5-16. doi: 10.1042/BA20030195
25. Okabe M, Tsukahara Y, Tanaka M, Suzuki K, Saito S, Kamiya Y, Tsujimura T, Nakamura K, Miyajima A. 2009. Potential hepatic stem cells reside in EpCAM+ cells of normal and injured mouse liver. Development 136: 1951-1960. doi: 10.1242/dev.031369
26. Osterwalder M, Galli A, Rosen B, Skarnes WC, Zeller R, Lopez-Rios J. 2010. Dual RMCE for efficient re- engineering of mouse mutant alleles. Nature Methods 7: 893-895. doi: 10.1038/nmeth.1521
27. Rountree CB, Barsky L, Ge S, Zhu J, Senadheera S, Crooks GM. 2007. A CD133-expressing murine liver oval cell population with bilineage potential. Stem Cells 25: 2419-2429. doi: 10.1634/stemcells.2007-0176
28. Samoilov MS, Price G, Arkin AP. 2006. From fluctuations to phenotypes: the physiology of noise. Science’s STKE 2006: re17. doi: 10.1126/stke.3662006re17
29. Sekiya S, Suzuki A. 2012. Intrahepatic cholangiocarcinoma can arise from Notch-mediated conversion of hepatocytes. Journal of Clinical Investigation 122: 3914-3918. doi: 10.1172/JCI63065
30. Siminovitch L, McCulloch EA, Till JE. 1963. The distribution of colony-forming cells among spleen colonies. Journal of Cellular and Comparative Physiology 62: 327-336. doi: 10.1002/jcp.1030620313
31. Spencer SL, Cappell SD, Tsai FC, Overton KW, Wang CL, Meyer T. 2013. The proliferation-quiescence decision is controlled by a bifurcation in CDK2 activity at mitotic exit. Cell 155: 369-383. doi: 10.1016/j.cell.2013.08.062
32. Suzuki A, Sekiya S, Onishi M, Oshima N, Kiyonari H, Nakauchi H, Taniguchi H. 2008. Flow cytometric isolation and clonal identification of self-renewing bipotent hepatic progenitor cells in adult mouse liver. Hepatology 48: 1964-1978. doi: 10.1002/hep.22558
33. Takase HM, Itoh T, Ino S, Wang T, Koji T, Akira S, Takikawa Y, Miyajima A. 2013. FGF7 is a functional niche signal required for stimulation of adult liver progenitor cells that support liver regeneration. Genes & Development 27: 169-181. doi: 10.1101/gad.204776.112
34. Takashima Y, Terada M, Kawabata M, Suzuki A. 2015. Dynamic three-dimensional morphogenesis of intrahepatic bile ducts in mouse liver development. Hepatology 61: 1003-1011. doi: 10.1002/hep.27436
35. Tanimizu N, Nishikawa M, Saito H, Tsujimura T, Miyajima A. 2003. Isolation of hepatoblasts based on the expression of Dlk/Pref-1. Journal of Cell Science 116: 1775-1861. doi: 10.1242/jcs.00388
36. Tanimizu N, Nishikawa Y, Ichinohe N, Akiyama H, Mitaka T. 2014. Sry HMG box protein 9-positive (Sox9+) epithelial cell adhesion molecule-negative (EpCAM-) biphenotypic cells derived from hepatocytes are involved in mouse liver regeneration. Journal of Biological Chemistry 289: 7589-7598. doi: 10.1074/jbc.M113.517243
37. Tarlow BD, Finegold MJ, Grompe M. 2014b. Clonal tracing of Sox9+ liver progenitors in mouse oval cell injury. Hepatology 60: 278-289. doi: 10.1002/hep.27084
38. Tarlow BD, Pelz C, Naugler WE, Wakefield L, Wilson EM, Finegold MJ, Grompe M. 2014a. Bipotential adult liver progenitors are derived from chronically injured mature hepatocytes. Cell Stem Cell 15: 605-618. doi: 10.1016/ j.stem.2014.09.008
39. Teta M, Rankin MM, Long SY, Stein GM, Kushner JA. 2007. Growth and regeneration of adult beta cells does not involve specialized progenitors. Developmental Cell 12: 817-826. doi: 10.1016/j.devcel.2007.04.011
40. Till JE, McCulloch EA, Siminovitch L. 1964. A stochastic model of stem cell proliferation, based on the growth of spleen colony-forming cells. Proceedings of the National Academy of Sciences of the United States of America 51: 29-36. doi: 10.1073/pnas.51.1.29
41. Yanger K, Knigin D, Zong Y, Maggs L, Gu G, Akiyama H, Pikarsky E, Stanger BZ. 2014. Adult hepatocytes are generated by self-duplication rather than stem cell differentiation. Cell Stem Cell 15: 340-349. doi: 10.1016/j. stem.2014.06.003
42. Yanger K, Zong Y, Maggs LR, Shapira SN, Maddipati R, Aiello NM, Thung SN, Wells RG, Greenbaum LE, Stanger BZ. 2013. Robust cellular reprogramming occurs spontaneously during liver regeneration. Genes & Development 27: 719-724. doi: 10.1101/gad.207803.112
43. Yeh CN, Maitra A, Lee KF, Jan YY, Chen MF. 2004. Thioacetamide-induced intestinal-type cholangiocarcinoma in rat: an animal model recapitulating the multi-stage progression of human cholangiocarcinoma. Carcinogenesis 25: 631-636. doi: 10.1093/carcin/bgh037
44. Zhu L, Gibson P, Currle DS, Tong Y, Richardson RJ, Bayazitov IT, Poppleton H, Zakharenko S, Ellison DW, Gilbertson RJ. 2009. Prominin 1 marks intestinal stem cells that are susceptible to neoplastic transformation. Nature 457: 603-607. doi: 10.1038/nature07589