Hippo signaling is required for Notch-dependent smooth muscle differentiation of neural crest

Development (Cambridge)

Volumn 142, Issue 17, 2015, Pages 2962-2971

  Manderfield, Lauren J ^a   Aghajanian, Haig ^a   Engleka, Kurt A ^a   Lim, Lillian Y ^a   Liu, Feiyan ^a   Jain, Rajan ^a   Li, Li ^a   Olson, Eric N ^b   Epstein, Jonathan A ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

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

Author keywords

Hippo signaling; Jagged1; Mouse; Neural crest; Notch signaling; Taz; Vascular development; Yap

Indexed keywords

IMMUNOGLOBULIN J RECOMBINATION SIGNAL SEQUENCE BINDING PROTEIN; JAGGED1; NOTCH RECEPTOR; PROTEIN; PROTEIN HIPPO; PROTEIN TAZ; PROTEIN YAP; UNCLASSIFIED DRUG; DNA BINDING PROTEIN; HIPPO PROTEIN, MOUSE; PHOSPHOPROTEIN; PROTEIN BINDING; PROTEIN SERINE THREONINE KINASE; SIGNAL TRANSDUCING ADAPTOR PROTEIN; TAZ PROTEIN, MOUSE; TEAD1 PROTEIN, MOUSE; TRANSCRIPTION FACTOR; YAP PROTEIN, MOUSE;

ANIMAL TISSUE; AORTA ARCH; ARTICLE; CELL DIFFERENTIATION; CHROMATIN; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; ENHANCER REGION; HUMAN; HUMAN CELL; MESENCHYME; MOUSE; NEURAL CREST; NEURAL CREST CELL; NEURAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER; TRANSCRIPTION INITIATION; VASCULAR SMOOTH MUSCLE; ANIMAL; CHEMISTRY; CYTOLOGY; GENE DELETION; GENETIC TRANSCRIPTION; HEK293 CELL LINE; MESODERM; METABOLISM; PROTEIN TERTIARY STRUCTURE; SMOOTH MUSCLE; THORACIC AORTA;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; AORTA, THORACIC; CELL DIFFERENTIATION; DNA-BINDING PROTEINS; GENE DELETION; HEK293 CELLS; HUMANS; MESODERM; MICE; MUSCLE, SMOOTH; MYOCYTES, SMOOTH MUSCLE; NEURAL CREST; PHOSPHOPROTEINS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTEIN-SERINE-THREONINE KINASES; RECEPTORS, NOTCH; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 84940775012     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.125807     Document Type: Article

References (43)

1. Afelik, S. and Jensen, J. (2013). Notch signaling in the pancreas: patterning and cell fate specification. Wiley Interdiscip. Rev. Dev. Biol. 2, 531-544.
2. Andersson, E. R. and Lendahl, U. (2014). Therapeutic modulation of Notch signalling — are we there yet? Nat. Rev. Drug Discov. 13, 357-378.
3. Connor, D. A. (2001). Mouse embryo fibroblast (MEF) feeder cell preparation. Curr. Protoc. Mol. Biol. Chapter 23:Unit 23.2.
4. Djiane, A., Zaessinger, S., Babaoğ lan, A. B. and Bray S. J. (2014). Notch inhibits Yorkie activity in Drosophila wing discs. PLoS ONE 9, e106211.
5. Gao, T., Zhou, D., Yang, C., Singh, T., Penzo-Méndez A., Maddipati R., Tzatsos A., Bardeesy N., Avruch J. and Stanger B. Z. (2013). Hippo signaling regulates differentiation and maintenance in the exocrine pancreas. Gastroenterology 144, 1543-1553.
6. Heallen, T., Zhang, M., Wang, J., Bonilla-Claudio, M., Klysik, E., Johnson, R. L. and Martin, J. F. (2011). Hippo pathway inhibits Wnt signaling to restrain cardiomyocyte proliferation and heart size. Science 332, 458-461.
7. High, F. A. and Epstein, J. A. (2008). The multifaceted role of Notch in cardiac development and disease. Nat. Rev. Genet. 9, 49-61.
8. High, F. A., Zhang, M., Proweller, A., Tu, L., Parmacek, M. S., Pear, W. S. and Epstein, J. A. (2007). An essential role for Notch in neural crest during cardiovascular development and smooth muscle differentiation. J. Clin. Invest. 117, 353-363.
9. High, F. A., Lu, M. M., Pear, W. S., Loomes, K. M., Kaestner, K. H. and Epstein, J. A. (2008). Endothelial expression of the Notch ligand Jagged1 is required for vascular smooth muscle development. Proc. Natl. Acad. Sci. USA 105, 1955-1959.
10. Jarriault, S., Brou, C., Logeat, F., Schroeter, E. H., Kopan, R. and Israel, A. (1995). Signalling downstream of activated mammalian Notch. Nature 377, 355-358.
11. Jiang, X., Rowitch, D. H., Soriano, P., McMahon, A. P. and Sucov, H. M. (2000). Fate of the mammalian cardiac neural crest. Development 127, 1607-1616.
12. Li, X., Zhang, X., Leathers, R., Makino, A., Huang, C., Parsa, P., Macias, J., Yuan, J. X.-J., Jamieson, S. W. and Thistlethwaite, P. A. (2009). Notch3 signaling promotes the development of pulmonary arterial hypertension. Nat. Med. 15, 1289-1297.
13. Li, Y., Hibbs, M. A., Gard, A. L., Shylo, N. A. and Yun, K. (2012). Genome-wide analysis of N1ICD/RBPJ targets in vivo reveals direct transcriptional regulation of Wnt, SHH, and hippo pathway effectors by Notch1. Stem Cells 30, 741-752.
14. Li, Y.-W., Shen, H., Frangou, C., Yang, N., Guo, J., Xu, B., Bshara, W., Shepherd, L., Zhu, Q.,Wang, J. et al. (2015). Characterization of TAZ domains important for the induction of breast cancer stem cell properties and tumorigenesis. Cell Cycle 14, 146-156.
15. Madisen, L., Zwingman, T. A., Sunkin, S. M., Oh, S. W., Zariwala, H. A., Gu, H., Ng, L. L., Palmiter, R. D., Hawrylycz, M. J., Jones, A. R. et al. (2010). A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nat. Neurosci. 13, 133-140.
16. Makita, R., Uchijima, Y., Nishiyama, K., Amano, T., Chen, Q., Takeuchi, T., Mitani, A., Nagase, T., Yatomi, Y., Aburatani, H. et al. (2008). Multiple renal cysts, urinary concentration defects, and pulmonary emphysematous changes in mice lacking TAZ. Am. J. Physiol. Renal Physiol. 294, F542-F553.
17. Manderfield, L. J., High, F. A., Engleka, K. A., Liu, F., Li, L., Rentschler, S. and Epstein, J. A. (2012). Notch activation of Jagged1 contributes to the assembly of the arterial wall. Circulation 125, 314-323.
18. Manderfield, L. J., Engleka, K. A., Aghajanian, H., Gupta, M., Yang, S., Li, L., Baggs, J. E., Hogenesch, J. B., Olson, E. N. and Epstein, J. A. (2014). Pax3 and hippo signaling coordinate melanocyte gene expression in neural crest. Cell Rep. 9, 1885-1895.
19. Mead, T. J. and Yutzey, K. E. (2012). Notch pathway regulation of neural crest cell development in vivo. Dev. Dyn. 241, 376-389.
20. Mo, J.-S., Park, H.W. and Guan, K.-L. (2014). The Hippo signaling pathway in stem cell biology and cancer. EMBO Rep. 15, 642-656.
21. Murakami, M., Nakagawa, M., Olson, E. N. and Nakagawa, O. (2005). A WW domain protein TAZ is a critical coactivator for TBX5, a transcription factor implicated in Holt-Oram syndrome. Proc. Natl. Acad. Sci. USA 102, 18034-18039.
22. Neto-Silva, R. M., de Beco, S. and Johnston, L. A. (2010). Evidence for a growthstabilizing regulatory feedback mechanism between Myc and Yorkie, the Drosophila homolog of Yap. Dev. Cell 19, 507-520.
23. Oka, T., Mazack, V. and Sudol, M. (2008). Mst2 and Lats kinases regulate apoptotic function of Yes kinase-associated protein (YAP). J. Biol. Chem. 283, 27534-27546.
24. Rayon, T., Menchero, S., Nieto, A., Xenopoulos, P., Crespo, M., Cockburn, K., Cañon S., Sasaki H., Hadjantonakis A.-K., de la Pompa, J. L. et al. (2014). Notch and hippo converge on Cdx2 to specify the trophectoderm lineage in the mouse blastocyst. Dev. Cell 30, 410-422.
25. Robinson, D.R., Kalyana-Sundaram, S., Wu, Y.-M., Shankar, S., Cao, X., Ateeq, B., Asangani, I. A., Iyer, M., Maher, C. A., Grasso, C. S. et al. (2011). Functionally recurrent rearrangements of the MAST kinase and Notch gene families in breast cancer. Nat. Med. 17, 1646-1651.
26. Russ, W. P., Lowery, D. M., Mishra, P., Yaffe, M. B. and Ranganathan, R. (2005). Natural-like function in artificial WW domains. Nature 437, 579-583.
27. Strano, S., Munarriz, E., Rossi, M., Castagnoli, L., Shaul, Y., Sacchi, A., Oren, M., Sudol, M., Cesareni, G. and Blandino, G. (2001). Physical interaction with Yes-associated protein enhances p73 transcriptional activity. J. Biol. Chem. 276, 15164-15173.
28. Stylianou, S., Clarke, R. B. and Brennan, K. (2006). Aberrant activation of notch signaling in human breast cancer. Cancer Res. 66, 1517-1525.
29. Taniguchi, K., Wu, L.-W., Grivennikov, S. I., de Jong, P. R., Lian, I., Yu, F.-X., Wang, K., Ho, S. B., Boland, B. S., Chang, J. T. et al. (2015). A gp130–Src–YAP module links inflammation to epithelial regeneration. Nature 519, 57-62.
30. Tschaharganeh, D. F., Chen, X., Latzko, P., Malz, M., Gaida, M. M., Felix, K., Ladu, S., Singer, S., Pinna, F., Gretz, N. et al. (2013). Yes-associated protein upregulates Jagged-1 and activates the Notch pathway in human hepatocellular carcinoma. Gastroenterology 144, 1530-1542.
31. Varelas, X. (2014). The Hippo pathway effectors TAZ and YAP in development, homeostasis and disease. Development 141, 1614-1626.
32. Villanueva, A., Alsinet, C., Yanger, K., Hoshida, Y., Zong, Y., Toffanin, S., Rodriguez-Carunchio, L., Solé M., Thung S., Stanger B. Z. et al. (2012). Notch signaling is activated in human hepatocellular carcinoma and induces tumor formation in mice. Gastroenterology 143, 1660-1669.e7.
33. Von Gise, A., Lin, Z., Schlegelmilch, K., Honor, L. B., Pan, G. M., Buck, J. N., Ma, Q., Ishiwata, T., Zhou, B., Camargo, F. D. et al. (2012). YAP1, the nuclear target of Hippo signaling, stimulates heart growth through cardiomyocyte proliferation but not hypertrophy. Proc. Natl. Acad. Sci. USA 109, 2394-2399.
34. Wang, X., Hu, G., Gao, X., Wang, Y., Zhang, W., Harmon, E. Y., Zhi, X., Xu, Z., Lennartz, M. R., Barroso, M. et al. (2012). The induction of yes-associated protein expression after arterial injury is crucial for smooth muscle phenotypic modulation and neointima formation. Arterioscler. Thromb. Vasc. Biol. 32, 2662-2669.
35. Wang, Y., Hu, G., Liu, F., Wang, X., Wu, M., Schwarz, J. J. and Zhou, J. (2014). Deletion of yes-associated protein (YAP) specifically in cardiac and vascular smooth muscle cells reveals a crucial role for YAP in mouse cardiovascular development. Circ. Res. 114, 957-965.
36. Weng, A. P., Millholland, J. M., Yashiro-Ohtani, Y., Arcangeli, M. L., Lau, A., Wai, C., Del Bianco, C., Rodriguez, C. G., Sai, H., Tobias, J. et al. (2006). c-Myc is an important direct target of Notch1 in T-cell acute lymphoblastic leukemia/lymphoma. Genes Dev. 20, 2096-2109.
37. Xie, C., Guo, Y., Zhu, T., Zhang, J., Ma, P. X. and Chen, Y. E. (2012). Yap1 protein regulates vascular smooth muscle cell phenotypic switch by interaction with myocardin. J. Biol. Chem. 287, 14598-14605.
38. Xin, M., Kim, Y., Sutherland, L. B., Qi, X., McAnally, J., Schwartz, R. J., Richardson, J. A., Bassel-Duby, R. and Olson, E. N. (2011). Regulation of insulin-like growth factor signaling by Yap governs cardiomyocyte proliferation and embryonic heart size. Sci. Signal. 4, ra70.
39. Xin, M., Kim, Y., Sutherland, L. B., Murakami, M., Qi, X., McAnally, J., Porrello, E. R., Mahmoud, A. I., Tan, W., Shelton, J. M. et al. (2013). Hippo pathway effector Yap promotes cardiac regeneration. Proc. Natl. Acad. Sci. USA 110, 13839-13844.
40. 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, 1324-1338.
41. Yu, F.-X., Zhang, Y., Park, H.W., Jewell, J. L., Chen, Q., Deng, Y., Pan, D., Taylor, S. S., Lai, Z.-C. and Guan, K.-L. (2013). Protein kinase A activates the Hippo pathway to modulate cell proliferation and differentiation. Genes Dev. 27, 1223-1232.
42. Zender, L., Spector, M. S., Xue, W., Flemming, P., Cordon-Cardo, C., Silke, J., Fan, S.-T., Luk, J. M., Wigler, M., Hannon, G. J. et al. (2006). Identification and validation of oncogenes in liver cancer using an integrative oncogenomic approach. Cell 125, 1253-1267.
43. Zhao, B., Kim, J., Ye, X., Lai, Z.-C. and Guan, K.-L. (2009). Both TEAD-binding and WW domains are required for the growth stimulation and oncogenic transformation activity of yes-associated protein. Cancer Res. 69, 1089-1098.