LATS-YAP/TAZ controls lineage specification by regulating TGFβ signaling and Hnf4α expression during liver development

Nature Communications

Volumn 7, Issue , 2016, Pages

  Lee, Da Hye ^a   Park, Jae Oh ^a   Kim, Tae Shin ^a   Kim, Sang Kyum ^b   Kim, Tack Hoon ^a   Kim, Min Chul ^a   Park, Gun Soo ^a   Kim, Jeong Hwan ^c   Kuninaka, Shinji ^d   Olson, Eric N ^e   Saya, Hideyuki ^d   Kim, Seon Young ^c   Lee, Ho ^f   Lim, Dae Sik ^a  

^a Korea Advanced Institute of Science and Technology (KAIST)   (South Korea)

^b Yonsei University College of Medicine   (South Korea)

^c Korea Research Institute of Bioscience and Biotechnology (KRIBB)   (South Korea)

^d KEIO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^e UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^f National Cancer Center   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

HEPATOCYTE NUCLEAR FACTOR 4ALPHA; LATS1 KINASE; LATS2 KINASE; NOTCH RECEPTOR; PROTEIN; PROTEIN P53; TAZ PROTEIN; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; YAP PROTEIN; HEPATOCYTE NUCLEAR FACTOR 4; HNF4A PROTEIN, MOUSE; LATS1 PROTEIN, MOUSE; LATS2 PROTEIN, MOUSE; PHOSPHOPROTEIN; PROTEIN SERINE THREONINE KINASE; SIGNAL TRANSDUCING ADAPTOR PROTEIN; TAZ PROTEIN, MOUSE; TRANSCRIPTION FACTOR; TUMOR SUPPRESSOR PROTEIN; YAP PROTEIN, MOUSE;

ANATOMY; CELL ORGANELLE; ENZYME; GENE EXPRESSION; GENETIC ANALYSIS; GENETIC DIFFERENTIATION; RODENT;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BILIARY EPITHELIUM CELL; CELL DIFFERENTIATION; CELL FATE; CELL LINEAGE; CELL PROLIFERATION; CONTROLLED STUDY; EMBRYO; EPITHELIUM CELL; FIBROBLAST; FORCE; GENE REPRESSION; LIVER CELL; LIVER DEVELOPMENT; MOUSE; NONHUMAN; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; ANIMAL; CELL AGING; EMBRYOLOGY; FEMALE; KNOCKOUT MOUSE; LIVER; METABOLISM; NEWBORN; PHYSIOLOGY; PREGNANCY; PRIMARY CELL CULTURE; UPREGULATION;

MUS;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; ANIMALS, NEWBORN; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLULAR SENESCENCE; FEMALE; HEPATOCYTE NUCLEAR FACTOR 4; LIVER; MICE; MICE, KNOCKOUT; PHOSPHOPROTEINS; PREGNANCY; PRIMARY CELL CULTURE; PROTEIN-SERINE-THREONINE KINASES; TRANSCRIPTION FACTORS; TRANSFORMING GROWTH FACTOR BETA; TUMOR SUPPRESSOR PROTEIN P53; TUMOR SUPPRESSOR PROTEINS; UP-REGULATION;

EID: 84977176795     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms11961     Document Type: Article

References (70)

1. Nord, Alex S. et al. Rapid and pervasive changes in genome-wide enhancer usage during mammalian development. Cell 155, 1521-1531 (2013).
2. Zhu, J. et al. Genome-wide chromatin state transitions associated with developmental and environmental cues. Cell 152, 642-654 (2013).
3. Zhao, R. & Duncan, S. A. Embryonic development of the liver. Hepatology 41, 956-967 (2005).
4. Si-Tayeb, K., Lemaigre, F. P. & Duncan, S. A. Organogenesis and development of the liver. Dev. Cell 18, 175-189 (2010).
5. Carpentier, R. et al. Embryonic ductal plate cells give rise to cholangiocytes, periportal hepatocytes, and adult liver progenitor cells. Gastroenterology 141, 1432-1438.e1434 (2011).
6. Boulter, L., Lu, W.-Y. & Forbes, S. J. Differentiation of progenitors in the liver: a matter of local choice. J. Clin. Invest. 123, 1867-1873 (2013).
7. Diehl, A. M. & Chute, J. Underlying potential: cellular and molecular determinants of adult liver repair. J. Clin. Invest. 123, 1858-1860 (2013).
8. Yamashita, T. & Wang, X. W. Cancer stem cells in the development of liver cancer. J. Clin. Invest. 123, 1911-1918 (2013).
9. Camargo, F. D. et al. YAP1 increases organ size and expands undifferentiated progenitor cells. Curr. Biol. 17, 2054-2060 (2007).
10. Irvine, K. D. & Harvey, K. F. Control of organ growth by patterning and hippo signaling in Drosophila. Cold Spring Harb. Perspect. Biol. 7, a019224 (2015).
11. Lee, J. H. et al. A crucial role of WW45 in developing epithelial tissues in the mouse. EMBO J. 27, 1231-1242 (2008).
12. Mo, J. S., Park, H. W. & Guan, K. L. The Hippo signaling pathway in stem cell biology and cancer. EMBO Rep. 15, 642-656 (2014).
13. Pan, D. Hippo signaling in organ size control. Genes Dev. 21, 886-897 (2007).
14. Varelas, X. The Hippo pathway effectors TAZ and YAP in development, homeostasis and disease. Development 141, 1614-1626 (2014).
15. Hansen, C. G., Moroishi, T. & Guan, K.-L. YAP and TAZ: a nexus for Hippo signaling and beyond. Trends Cell Biol. 25, 499-513 (2015).
16. Kim, M.-C., Kim, T.-S., Kim, T. & Lim, D.-S. in The Hippo Signaling Pathway and Cancer (eds Oren, M. & Aylon, Y.) 225-247 (Springer New York, 2013).
17. Johnson, R. & Halder, G. The two faces of Hippo: targeting the Hippo pathway for regenerative medicine and cancer treatment. Nat. Rev. Drug Discov. 13, 63-79 (2014).
18. Moroishi, T., Hansen, C. G. & Guan, K.-L. The emerging roles of YAP and TAZ in cancer. Nat. Rev. Cancer 15, 73-79 (2015).
19. Lee, K.-P. et al. The Hippo-Salvador pathway restrains hepatic oval cell proliferation, liver size, and liver tumorigenesis. Proc. Natl Acad. Sci. USA 107, 8248-8253 (2010).
20. Benhamouche, S. et al. Nf2/Merlin controls progenitor homeostasis and tumorigenesis in the liver. Genes Dev. 24, 1718-1730 (2010).
21. Dong, J. et al. Elucidation of a universal size-control mechanism in Drosophila and mammals. Cell 130, 1120-1133 (2007).
22. Zhang, N. et al. The Merlin/NF2 tumor suppressor functions through the yap oncoprotein to regulate tissue homeostasis in mammals. Dev. Cell 19, 27-38 (2010).
23. Lu, L. et al. Hippo signaling is a potent in vivo growth and tumor suppressor pathway in the mammalian liver. Proc. Natl Acad. Sci. USA 107, 1437-1442 (2010).
24. Yi, C. et al. The p130 isoform of angiomotin is required for yap-mediated hepatic epithelial cell proliferation and tumorigenesis. Sci. Signal. 6, ra77-ra77 (2013).
25. Song, H. et al. Mammalian Mst1 and Mst2 kinases play essential roles in organ size control and tumor suppression. Proc. Natl Acad. Sci. USA 107, 1431-1436 (2010).
26. Zhou, D. et al. Mst1 and Mst2 maintain hepatocyte quiescence and suppress hepatocellular carcinoma development through inactivation of the Yap1 oncogene. Cancer Cell 16, 425-438 (2009).
27. Yimlamai, D. et al. Hippo pathway activity influences liver cell fate. Cell 157, 1324-1338 (2014).
28. Crestani, M., Sadeghpour, A., Stroup, D., Galli, G. & Chiang, J. Y. L. Transcriptional activation of the cholesterol 7a-hydroxylase gene (CYP7A) by nuclear hormone receptors. J. Lipid Res. 39, 2192-2200 (1998).
29. Tchorz, J. S. et al. Notch2 signaling promotes biliary epithelial cell fate specification and tubulogenesis during bile duct development in mice. Hepatology 50, 871-879 (2009).
30. Antoniou, A. et al. Intrahepatic bile ducts develop according to a new mode of tubulogenesis regulated by the transcription factor SOX9. Gastroenterology 136, 2325-2333 (2009).
31. Hofmann, J. J. et al. Jagged1 in the portal vein mesenchyme regulates intrahepatic bile duct development: insights into Alagille syndrome. Development 137, 4061-4072 (2010).
32. Kodama, Y., Hijikata, M., Kageyama, R., Shimotohno, K. & Chiba, T. The role of notch signaling in the development of intrahepatic bile ducts. Gastroenterology 127, 1775-1786 (2004).
33. Nguyen, Q., Anders, R. A., Alpini, G. & Bai, H. Yes-associated protein in the liver: regulation of hepatic development, repair, cell fate determination and tumorigenesis. Dig. Liver Dis. 47, 826-835 (2015).
34. Bai, H. et al. Yes-associated protein regulates the hepatic response after bile duct ligation. Hepatology 56, 1097-1107 (2012).
35. Zhang, N. et al. The Merlin/NF2 tumor suppressor functions through the YAP oncoprotein to regulate tissue homeostasis in mammals. Dev. Cell 19, 27-38 (2010).
36. Fiorotto, R. et al. Notch signaling regulates tubular morphogenesis during repair from biliary damage in mice. J. Hepatol. 59, 124-130 (2013).
37. Clotman, F. et al. Control of liver cell fate decision by a gradient of TGFb signaling modulated by Onecut transcription factors. Genes Dev. 19, 1849-1854 (2005).
38. Takayama, K. et al. CCAAT/enhancer binding protein-mediated regulation of TGFb receptor 2 expression determines the hepatoblast fate decision. Development 141, 91-100 (2014).
39. Seth, A. et al. Prox1 ablation in hepatic progenitors causes defective hepatocyte specification and increases biliary cell commitment. Development 141, 538-547 (2014).
40. Park, Y. N. & Roncalli, M. Large liver cell dysplasia: a controversial entity. J. Hepatol. 45, 734-743 (2006).
41. Harada, N. et al. Hepatocarcinogenesis in mice with b-catenin and Ha-Ras gene mutations. Cancer Res. 64, 48-54 (2004).
42. Kyrmizi, I. et al. Plasticity and expanding complexity of the hepatic transcription factor network during liver development. Genes Dev. 20, 2293-2305 (2006).
43. Cebola, I. et al. TEAD and YAP regulate the enhancer network of human embryonic pancreatic progenitors. Nat. Cell Biol. 17, 615-626 (2015).
44. Alder, O. et al. Hippo signaling influences HNF4A and FOXA2 enhancer switching during hepatocyte differentiation. Cell Rep. 9, 261-271 (2014).
45. Beyer, Tobias A. et al. Switch enhancers interpret TGF-β and hippo signaling to control cell fate in human embryonic stem cells. Cell Rep. 5, 1611-1624 (2013).
46. Zhu, Y. et al. Brahma regulates the Hippo pathway activity through forming complex with Yki-Sd and regulating the transcription of Crumbs. Cell. Signal. 27, 606-613 (2015).
47. Kim, M., Kim, T., Johnson, R. L. & Lim, D. S. Transcriptional co-repressor function of the hippo pathway transducers YAP and TAZ. Cell Rep. 11, 270-282 (2015).
48. Gao, T. et al. Hippo signaling regulates differentiation and maintenance in the exocrine pancreas. Gastroenterology 144, 1543-1553.e1541 (2013).
49. Zhou, D. et al. Mst1 and Mst2 protein kinases restrain intestinal stem cell proliferation and colonic tumorigenesis by inhibition of Yes-associated protein (Yap) overabundance. Proc. Natl Acad. Sci. USA 108, E1312-E1320 (2011).
50. Tschaharganeh, D. F. et al. Yes-associated protein up-regulates Jagged-1 and activates the NOTCH pathway in human hepatocellular carcinoma. Gastroenterology 144, 1530-1542.e1512 (2013).
51. Williams, M. J., Clouston, A. D. & Forbes, S. J. Links between hepatic fibrosis, ductular reaction, and progenitor cell expansion. Gastroenterology 146, 349-356 (2014).
52. Gressner, O. A. & Gao, C. Monitoring fibrogenic progression in the liver. Clin. Chim. Acta 433, 111-122 (2014).
53. Matallanas, D. et al. Mutant K-Ras activation of the proapoptotic MST2 pathway is antagonized by wild-type K-Ras. Mol. Cell 44, 893-906 (2011).
54. Vigneron, A. M., Ludwig, R. L. & Vousden, K. H. Cytoplasmic ASPP1 inhibits apoptosis through the control of YAP. Genes Dev. 24, 2430-2439 (2010).
55. Aylon, Y. et al. The Lats2 tumor suppressor augments p53-mediated apoptosis by promoting the nuclear proapoptotic function of ASPP1. Genes Dev. 24, 2420-2429 (2010).
56. Celton-Morizur, S. & Desdouets, C. Polyploidization and Cancer (ed. Poon, R. Y. C.) 123-135 (Springer New York, 2010).
57. Stanger, B. Z. Cellular homeostasis and repair in the mammalian liver. Annu. Rev. Physiol. 77, 179-200 (2015).
58. Ehmer, U. et al. Organ size control is dominant over Rb family inactivation to restrict proliferation in vivo. Cell Rep. 8, 371-381 (2014).
59. Fitamant, J. et al. YAP inhibition restores hepatocyte differentiation in advanced HCC, leading to tumor regression. Cell Rep. 10, 1692-1707 (2015).
60. Su, T. et al. Two-signal requirement for growth-promoting function of Yap in hepatocytes. Elife 4, e02948 (2015).
61. Hansen, C. G., Moroishi, T. & Guan, K. L. YAP and TAZ: a nexus for Hippo signaling and beyond. Trends Cell Biol. 25, 499-513 (2015).
62. Roskams, T. & Desmet, V. Embryology of extra- and intrahepatic bile ducts, the ductal plate. Anat. Rec. 291, 628-635 (2008).
63. Das, A. et al. Stromal-epithelial crosstalk regulates kidney progenitor cell differentiation. Nat. Cell Biol. 15, 1035-1044 (2013).
64. Chiyoda, T. et al. LATS1/WARTS phosphorylates MYPT1 to counteract PLK1 and regulate mammalian mitotic progression. J. Cell Biol. 197, 625-641 (2012).
65. Kim, M. et al. cAMP/PKA signalling reinforces the LATS-YAP pathway to fully suppress YAP in response to actin cytoskeletal changes. EMBO J. 32, 1543-1555 (2013).
66. Oh, S. et al. Crucial role for Mst1 and Mst2 kinases in early embryonic development of the mouse. Mol. Cell Biol. 29, 6309-6320 (2009).
67. Chung, C. et al. Hippo-Foxa2 signaling pathway plays a role in peripheral lung maturation and surfactant homeostasis. Proc. Natl Acad. Sci. USA 110, 7732-7737 (2013).
68. Giovannini, M. et al. Conditional biallelic Nf2 mutation in the mouse promotes manifestations of human neurofibromatosis type 2. Genes Dev. 14, 1617-1630 (2000).
69. Xin, M. et al. Hippo pathway effector Yap promotes cardiac regeneration. Proc. Natl Acad. Sci. USA 110, 13839-13844 (2013).
70. Xin, M. et al. Regulation of insulin-like growth factor signaling by Yap governs cardiomyocyte proliferation and embryonic heart size. Sci. Signal. 4, ra70 (2011).