Numb family proteins are essential for cardiac morphogenesis and progenitor differentiation

Development (Cambridge)

Volumn 141, Issue 2, 2014, Pages 281-295

  Zhao, Chen ^a   Guo, Hua ^a   Li, Jingjing ^a   Myint, Thomas ^a   Pittman, William ^a   Yang, Le ^a   Zhong, Weimin ^b   Schwartz, Robert J ^c   Schwarz, John J ^a   Singer, Harold A ^a   Tallquist, Michelle D ^d   Wu, Mingfu ^a  

^a ALBANY MEDICAL COLLEGE   (United States)

^b YALE UNIVERSITY   (United States)

^c UNIVERSITY OF HOUSTON   (United States)

^d UNIVERSITY OF HAWAII   (United States)

Author keywords

Cardiac morphogenesis; Cardiac progenitor cell; Mouse; Numb family proteins

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR 1C; IRX3 PROTEIN; IRX4 PROTEIN; IRX5 PROTEIN; MESSENGER RNA; MYH11 PROTEIN; MYH6 PROTEIN; MYH7 PROTEIN; MYL2 PROTEIN; NOTCH1 RECEPTOR; NUMB PROTEIN; NUMB1 PROTEIN; PROTEIN; TNNT2 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; ENDOCYTOSIS; HEART; HEART DEVELOPMENT; HEART MUSCLE CELL; IMMUNOFLUORESCENCE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; STEM CELL; SURVIVAL; WESTERN BLOTTING;

EID: 84891545176     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.093690     Document Type: Article

References (113)

1. Ai, D., Fu, X., Wang, J., Lu, M. F., Chen, L., Baldini, A., Klein, W. H. and Martin, J. F. (2007). Canonical Wnt signaling functions in second heart field to promote right ventricular growth. Proc. Natl. Acad. Sci. USA 104, 9319-9324.
2. Bao, Z. Z., Bruneau, B. G., Seidman, J. G., Seidman, C. E. and Cepko, C. L. (1999). Regulation of chamber-specific gene expression in the developing heart by Irx4. Science 283, 1161-1164.
3. Beres, B. J., George, R., Lougher, E. J., Barton, M., Verrelli, B. C., McGlade, C. J., Rawls, J. A. and Wilson-Rawls, J. (2011). Numb regulates Notch1, but not Notch3, during myogenesis. Mech. Dev. 128, 247-257.
4. Black, B. L. (2007). Transcriptional pathways in second heart field development. Semin. Cell Dev. Biol. 18, 67-76.
5. Boucher, P., Gotthardt, M., Li, W. P., Anderson, R. G. and Herz, J. (2003). LRP: role in vascular wall integrity and protection from atherosclerosis. Science 300, 329-332.
6. Breckenridge, R. A., Anderson, R. H. and Elliott, P. M. (2007). Isolated left ventricular non-compaction: the case for abnormal myocardial development. Cardiol. Young 17, 124-129.
7. Briggs, L. E., Kakarla, J. and Wessels, A. (2012). The pathogenesis of atrial and atrioventricular septal defects with special emphasis on the role of the dorsal mesenchymal protrusion. Differentiation 84, 117-130.
8. Bruneau, B. G. (2008). The developmental genetics of congenital heart disease. Nature 451, 943-948.
9. Bruneau, B. G., Bao, Z. Z., Fatkin, D., Xavier-Neto, J., Georgakopoulos, D., Maguire, C. T., Berul, C. I., Kass, D. A., Kuroski-de Bold, M. L., de Bold, A. J. et al. (2001). Cardiomyopathy in Irx4-deficient mice is preceded by abnormal ventricular gene expression. Mol. Cell. Biol. 21, 1730-1736.
10. Buckingham, M., Meilhac, S. and Zaffran, S. (2005). Building the mammalian heart from two sources of myocardial cells. Nat. Rev. Genet. 6, 826-835.
11. Cai, C. L., Liang, X., Shi, Y., Chu, P. H., Pfaff, S. L., Chen, J. and Evans, S. (2003). Isl1 identifies a cardiac progenitor population that proliferates prior to differentiation and contributes a majority of cells to the heart. Dev. Cell 5, 877-889.
12. Calderwood, D. A., Fujioka, Y., de Pereda, J. M., García-Alvarez, B., Nakamoto, T., Margolis, B., McGlade, C. J., Liddington, R. C. and Ginsberg, M. H. (2003). Integrin beta cytoplasmic domain interactions with phosphotyrosine-binding domains: a structural prototype for diversity in integrin signaling. Proc. Natl. Acad. Sci. USA 100, 2272-2277.
13. Chen, H., Shi, S., Acosta, L., Li, W., Lu, J., Bao, S., Chen, Z., Yang, Z., Schneider, M. D., Chien, K. R. et al. (2004). BMP10 is essential for maintaining cardiac growth during murine cardiogenesis. Development 131, 2219-2231.
14. Chen, H., Zhang, W., Li, D., Cordes, T. M., Mark Payne, R. and Shou, W. (2009). Analysis of ventricular hypertrabeculation and noncompaction using genetically engineered mouse models. Pediatr. Cardiol. 30, 626-634.
15. Chen, H., Zhang, W., Sun, X., Yoshimoto, M., Chen, Z., Zhu, W., Liu, J., Shen, Y., Yong, W., Li, D. et al. (2013). Fkbp1a controls ventricular myocardium trabeculation and compaction by regulating endocardial Notch1 activity. Development 140, 1946-1957.
16. Cheng, X., Huber, T. L., Chen, V. C., Gadue, P. and Keller, G. M. (2008). Numb mediates the interaction between Wnt and Notch to modulate primitive erythropoietic specification from the hemangioblast. Development 135, 3447-3458.
17. Colaluca, I. N., Tosoni, D., Nuciforo, P., Senic-Matuglia, F., Galimberti, V., Viale, G., Pece, S. and Di Fiore, P. P. (2008). NUMB controls p53 tumour suppressor activity. Nature 451, 76-80.
18. Conboy, I. M. and Rando, T. A. (2002). The regulation of Notch signaling controls satellite cell activation and cell fate determination in postnatal myogenesis. Dev. Cell 3, 397-409.
19. Cottage, C. T., Bailey, B., Fischer, K. M., Avitable, D., Collins, B., Tuck, S., Quijada, P., Gude, N., Alvarez, R., Muraski, J. et al. (2010). Cardiac progenitor cell cycling stimulated by pim-1 kinase. Circ. Res. 106, 891-901.
20. Croquelois, A., Domenighetti, A. A., Nemir, M., Lepore, M., Rosenblatt-Velin, N., Radtke, F. and Pedrazzini, T. (2008). Control of the adaptive response of the heart to stress via the Notch1 receptor pathway. J. Exp. Med. 205, 3173-3185.
21. Danielian, P. S., Muccino, D., Rowitch, D. H., Michael, S. K. and McMahon, A. P. (1998). Modification of gene activity in mouse embryos in utero by a tamoxifeninducible form of Cre recombinase. Curr. Biol. 8, 1323-1326.
22. Di Marcotullio, L., Ferretti, E., Greco, A., De Smaele, E., Po, A., Sico, M. A., Alimandi, M., Giannini, G., Maroder, M., Screpanti, I. et al. (2006). Numb is a suppressor of Hedgehog signalling and targets Gli1 for Itch-dependent ubiquitination. Nat. Cell Biol. 8, 1415-1423.
23. Duncan, A. W., Rattis, F. M., DiMascio, L. N., Congdon, K. L., Pazianos, G., Zhao, C., Yoon, K., Cook, J. M., Willert, K., Gaiano, N. et al. (2005). Integration of Notch and Wnt signaling in hematopoietic stem cell maintenance. Nat. Immunol. 6, 314-322.
24. Frise, E., Knoblich, J. A., Younger-Shepherd, S., Jan, L. Y. and Jan, Y. N. (1996). The Drosophila Numb protein inhibits signaling of the Notch receptor during cellcell interaction in sensory organ lineage. Proc. Natl. Acad. Sci. USA 93, 11925-11932.
25. Garg, V., Muth, A. N., Ransom, J. F., Schluterman, M. K., Barnes, R., King, I. N., Grossfeld, P. D. and Srivastava, D. (2005). Mutations in NOTCH1 cause aortic valve disease. Nature 437, 270-274.
26. Grego-Bessa, J., Luna-Zurita, L., del Monte, G., Bolós, V., Melgar, P., Arandilla, A., Garratt, A. N., Zang, H., Mukouyama, Y. S., Chen, H. et al. (2007). Notch signaling is essential for ventricular chamber development. Dev. Cell 12, 415-429.
27. Gulino, A., Di Marcotullio, L. and Screpanti, I. (2010). The multiple functions of Numb. Exp. Cell Res. 316, 900-906.
28. Guo, M., Jan, L. Y. and Jan, Y. N. (1996). Control of daughter cell fates during asymmetric division: interaction of Numb and Notch. Neuron 17, 27-41.
29. Habara-Ohkubo, A. (1996). Differentiation of beating cardiac muscle cells from a derivative of P19 embryonal carcinoma cells. Cell Struct. Funct. 21, 101-110.
30. Han, Z. and Bodmer, R. (2003). Myogenic cells fates are antagonized by Notch only in asymmetric lineages of the Drosophila heart, with or without cell division. Development 130, 3039-3051.
31. Hellström, M., Phng, L. K., Hofmann, J. J., Wallgard, E., Coultas, L., Lindblom, P., Alva, J., Nilsson, A. K., Karlsson, L., Gaiano, N. et al. (2007). Dll4 signalling through Notch1 regulates formation of tip cells during angiogenesis. Nature 445, 776-780.
32. Hoffman, J. I. and Kaplan, S. (2002). The incidence of congenital heart disease. J. Am. Coll. Cardiol. 39, 1890-1900.
33. Hoffmann, A. D., Peterson, M. A., Friedland-Little, J. M., Anderson, S. A. and Moskowitz, I. P. (2009). sonic hedgehog is required in pulmonary endoderm for atrial septation. Development 136, 1761-1770.
34. Holtwick, R., Gotthardt, M., Skryabin, B., Steinmetz, M., Potthast, R., Zetsche, B., Hammer, R. E., Herz, J. and Kuhn, M. (2002). Smooth muscle-selective deletion of guanylyl cyclase-A prevents the acute but not chronic effects of ANP on blood pressure. Proc. Natl. Acad. Sci. USA 99, 7142-7147.
35. Ilagan, R., Abu-Issa, R., Brown, D., Yang, Y. P., Jiao, K., Schwartz, R. J., Klingensmith, J. and Meyers, E. N. (2006). Fgf8 is required for anterior heart field development. Development 133, 2435-2445.
36. Ito, T., Kwon, H. Y., Zimdahl, B., Congdon, K. L., Blum, J., Lento, W. E., Zhao, C., Lagoo, A., Gerrard, G., Foroni, L. et al. (2010). Regulation of myeloid leukaemia by the cell-fate determinant Musashi. Nature 466, 765-768.
37. Jenni, R., Rojas, J. and Oechslin, E. (1999). Isolated noncompaction of the myocardium. N. Engl. J. Med. 340, 966-967.
38. Kelly, R. G. (2012). The second heart field. Curr. Top. Dev. Biol. 100, 33-65.
39. Kelly, R. G. and Buckingham, M. E. (2002). The anterior heart-forming field: voyage to the arterial pole of the heart. Trends Genet. 18, 210-216.
40. Kelly, R. G., Brown, N. A. and Buckingham, M. E. (2001). The arterial pole of the mouse heart forms from Fgf10-expressing cells in pharyngeal mesoderm. Dev. Cell 1, 435-440.
41. Kisanuki, Y. Y., Hammer, R. E., Miyazaki, J., Williams, S. C., Richardson, J. A. and Yanagisawa, M. (2001). Tie2-Cre transgenic mice: a new model for endothelial celllineage analysis in vivo. Dev. Biol. 230, 230-242.
42. Kratsios, P., Catela, C., Salimova, E., Huth, M., Berno, V., Rosenthal, N. and Mourkioti, F. (2010). Distinct roles for cell-autonomous Notch signaling in cardiomyocytes of the embryonic and adult heart. Circ. Res. 106, 559-572.
43. Krieger, J. R., Taylor, P., Gajadhar, A. S., Guha, A., Moran, M. F. and McGlade, C. J. (2013). Identification and selected reaction monitoring (SRM) quantification of endocytosis factors associated with Numb. Mol. Cell. Proteomics 12, 499-514.
44. Kwon, C., Arnold, J., Hsiao, E. C., Taketo, M. M., Conklin, B. R. and Srivastava, D. (2007). Canonical Wnt signaling is a positive regulator of mammalian cardiac progenitors. Proc. Natl. Acad. Sci. USA 104, 10894-10899.
45. Kwon, C., Cheng, P., King, I. N., Andersen, P., Shenje, L., Nigam, V. and Srivastava, D. (2011). Notch post-translationally regulates β-catenin protein in stem and progenitor cells. Nat. Cell Biol. 13, 1244-1251.
46. Lechler, T. and Fuchs, E. (2005). Asymmetric cell divisions promote stratification and differentiation of mammalian skin. Nature 437, 275-280.
47. Li, L., Miano, J. M., Mercer, B. and Olson, E. N. (1996). Expression of the SM22alpha promoter in transgenic mice provides evidence for distinct transcriptional regulatory programs in vascular and visceral smooth muscle cells. J. Cell Biol. 132, 849-859.
48. Li, H. S., Wang, D., Shen, Q., Schonemann, M. D., Gorski, J. A., Jones, K. R., Temple, S., Jan, L. Y. and Jan, Y. N. (2003). Inactivation of Numb and Numblike in embryonic dorsal forebrain impairs neurogenesis and disrupts cortical morphogenesis. Neuron 40, 1105-1118.
49. Lin, L., Cui, L., Zhou, W., Dufort, D., Zhang, X., Cai, C. L., Bu, L., Yang, L., Martin, J., Kemler, R. et al. (2007). Beta-catenin directly regulates Islet1 expression in cardiovascular progenitors and is required for multiple aspects of cardiogenesis. Proc. Natl. Acad. Sci. USA 104, 9313-9318.
50. Luxán, G., Casanova, J. C., Martínez-Poveda, B., Prados, B., D'Amato, G., MacGrogan, D., Gonzalez-Rajal, A., Dobarro, D., Torroja, C., Martinez, F. et al. (2013). Mutations in the NOTCH pathway regulator MIB1 cause left ventricular noncompaction cardiomyopathy. Nat. Med. 19, 193-201.
51. McBurney, M. W. and Rogers, B. J. (1982). Isolation of male embryonal carcinoma cells and their chromosome replication patterns. Dev. Biol. 89, 503-508.
52. McCright, B., Gao, X., Shen, L., Lozier, J., Lan, Y., Maguire, M., Herzlinger, D., Weinmaster, G., Jiang, R. and Gridley, T. (2001). Defects in development of the kidney, heart and eye vasculature in mice homozygous for a hypomorphic Notch2 mutation. Development 128, 491-502.
53. McGill, M. A. and McGlade, C. J. (2003). Mammalian numb proteins promote Notch1 receptor ubiquitination and degradation of the Notch1 intracellular domain. J. Biol. Chem. 278, 23196-23203.
54. McGill, M. A., Dho, S. E., Weinmaster, G. and McGlade, C. J. (2009). Numb regulates post-endocytic trafficking and degradation of Notch1. J. Biol. Chem. 284, 26427-26438.
55. Mellgren, A. M., Smith, C. L., Olsen, G. S., Eskiocak, B., Zhou, B., Kazi, M. N., Ruiz, F. R., Pu, W. T. and Tallquist, M. D. (2008). Platelet-derived growth factor receptor beta signaling is required for efficient epicardial cell migration and development of two distinct coronary vascular smooth muscle cell populations. Circ. Res. 103, 1393-1401.
56. Mishra, R., Vijayan, K., Colletti, E. J., Harrington, D. A., Matthiesen, T. S., Simpson, D., Goh, S. K., Walker, B. L., Almeida-Porada, G., Wang, D. et al. (2011). Characterization and functionality of cardiac progenitor cells in congenital heart patients. Circulation 123, 364-373.
57. Mizutani, K., Yoon, K., Dang, L., Tokunaga, A. and Gaiano, N. (2007). Differential Notch signalling distinguishes neural stem cells from intermediate progenitors. Nature 449, 351-355.
58. Mjaatvedt, C. H., Nakaoka, T., Moreno-Rodriguez, R., Norris, R. A., Kern, M. J., Eisenberg, C. A., Turner, D. and Markwald, R. R. (2001). The outflow tract of the heart is recruited from a novel heart-forming field. Dev. Biol. 238, 97-109.
59. Moore, J. C., Spijker, R., Martens, A. C., de Boer, T., Rook, M. B., van der Heyden, M. A., Tertoolen, L. G. and Mummery, C. L. (2004). A P19Cl6 GFP reporter line to quantify cardiomyocyte differentiation of stem cells. Int. J. Dev. Biol. 48, 47-55.
60. Moses, K. A., DeMayo, F., Braun, R. M., Reecy, J. L. and Schwartz, R. J. (2001). Embryonic expression of an Nkx2-5/Cre gene using ROSA26 reporter mice. Genesis 31, 176-180.
61. Mummery, C., Ward, D., van den Brink, C. E., Bird, S. D., Doevendans, P. A., Opthof, T., Brutel de la Riviere, A., Tertoolen, L., van der Heyden, M. and Pera, M. (2002). Cardiomyocyte differentiation of mouse and human embryonic stem cells. J. Anat. 200, 233-242.
62. Muzumdar, M. D., Tasic, B., Miyamichi, K., Li, L. and Luo, L. (2007). A global double-fluorescent Cre reporter mouse. Genesis 45, 593-605.
63. Niikura, Y., Tabata, Y., Tajima, A., Inoue, I., Arai, K. and Watanabe, S. (2006). Zebrafish Numb homologue: phylogenetic evolution and involvement in regulation of left-right asymmetry. Mech. Dev. 123, 407-414.
64. Nishimura, T. and Kaibuchi, K. (2007). Numb controls integrin endocytosis for directional cell migration with aPKC and PAR-3. Dev. Cell 13, 15-28.
65. Oka, T., Maillet, M., Watt, A. J., Schwartz, R. J., Aronow, B. J., Duncan, S. A. and Molkentin, J. D. (2006). Cardiac-specific deletion of Gata4 reveals its requirement for hypertrophy, compensation, and myocyte viability. Circ. Res. 98, 837-845.
66. Olson, E. N. (2006). Gene regulatory networks in the evolution and development of the heart. Science 313, 1922-1927.
67. Park, E. J., Ogden, L. A., Talbot, A., Evans, S., Cai, C. L., Black, B. L., Frank, D. U. and Moon, A. M. (2006). Required, tissue-specific roles for Fgf8 in outflow tract formation and remodeling. Development 133, 2419-2433.
68. Petersen, P. H., Zou, K., Hwang, J. K., Jan, Y. N. and Zhong, W. (2002). Progenitor cell maintenance requires numb and numblike during mouse neurogenesis. Nature 419, 929-934.
69. Petersen, P. H., Zou, K., Krauss, S. and Zhong, W. (2004). Continuing role for mouse Numb and Numbl in maintaining progenitor cells during cortical neurogenesis. Nat. Neurosci. 7, 803-811.
70. Petersen, P. H., Tang, H., Zou, K. and Zhong, W. (2006). The enigma of the numb-Notch relationship during mammalian embryogenesis. Dev. Neurosci. 28, 156-168.
71. Rasin, M. R., Gazula, V. R., Breunig, J. J., Kwan, K. Y., Johnson, M. B., Liu-Chen, S., Li, H. S., Jan, L. Y., Jan, Y. N., Rakic, P. et al. (2007). Numb and Numbl are required for maintenance of cadherin-based adhesion and polarity of neural progenitors. Nat. Neurosci. 10, 819-827.
72. Rhyu, M. S., Jan, L. Y. and Jan, Y. N. (1994). Asymmetric distribution of numb protein during division of the sensory organ precursor cell confers distinct fates to daughter cells. Cell 76, 477-491.
73. Rochais, F., Mesbah, K. and Kelly, R. G. (2009). Signaling pathways controlling second heart field development. Circ. Res. 104, 933-942.
74. Salcini, A. E., Confalonieri, S., Doria, M., Santolini, E., Tassi, E., Minenkova, O., Cesareni, G., Pelicci, P. G. and Di Fiore, P. P. (1997). Binding specificity and in vivo targets of the EH domain, a novel protein-protein interaction module. Genes Dev. 11, 2239-2249.
75. Samsa, L. A., Yang, B. and Liu, J. (2013). Embryonic cardiac chamber maturation: trabeculation, conduction, and cardiomyocyte proliferation. Am. J. Med. Genet. C Semin. Med. Genet. 163C, 157-168.
76. Sanalkumar, R., Dhanesh, S. B. and James, J. (2010). Non-canonical activation of Notch signaling/target genes in vertebrates. Cell. Mol. Life Sci. 67, 2957-2968.
77. Santolini, E., Puri, C., Salcini, A. E., Gagliani, M. C., Pelicci, P. G., Tacchetti, C. and Di Fiore, P. P. (2000). Numb is an endocytic protein. J. Cell Biol. 151, 1345-1352.
78. Schwenk, F., Baron, U. and Rajewsky, K. (1995). A cre-transgenic mouse strain for the ubiquitous deletion of loxP-flanked gene segments including deletion in germ cells. Nucleic Acids Res. 23, 5080-5081.
79. Smith, A. G. (2001). Embryo-derived stem cells: of mice and men. Annu. Rev. Cell Dev. Biol. 17, 435-462.
80. Snarr, B. S., O'Neal, J. L., Chintalapudi, M. R., Wirrig, E. E., Phelps, A. L., Kubalak, S. W. and Wessels, A. (2007a). Isl1 expression at the venous pole identifies a novel role for the second heart field in cardiac development. Circ. Res. 101, 971-974.
81. Snarr, B. S., Wirrig, E. E., Phelps, A. L., Trusk, T. C. and Wessels, A. (2007b). A spatiotemporal evaluation of the contribution of the dorsal mesenchymal protrusion to cardiac development. Dev. Dyn. 236, 1287-1294.
82. Sorkin, A. (2004). Cargo recognition during clathrin-mediated endocytosis: a team effort. Curr. Opin. Cell Biol. 16, 392-399.
83. Spana, E. P. and Doe, C. Q. (1996). Numb antagonizes Notch signaling to specify sibling neuron cell fates. Neuron 17, 21-26.
84. Stankunas, K., Hang, C. T., Tsun, Z. Y., Chen, H., Lee, N. V., Wu, J. I., Shang, C., Bayle, J. H., Shou, W., Iruela-Arispe, M. L. et al. (2008). Endocardial Brg1 represses ADAMTS1 to maintain the microenvironment for myocardial morphogenesis. Dev. Cell 14, 298-311.
85. Traub, L. M. (2003). Sorting it out: AP-2 and alternate clathrin adaptors in endocytic cargo selection. J. Cell Biol. 163, 203-208.
86. Uemura, T., Shepherd, S., Ackerman, L., Jan, L. Y. and Jan, Y. N. (1989). numb, a gene required in determination of cell fate during sensory organ formation in Drosophila embryos. Cell 58, 349-360.
87. Ueno, S., Weidinger, G., Osugi, T., Kohn, A. D., Golob, J. L., Pabon, L., Reinecke, H., Moon, R. T. and Murry, C. E. (2007). Biphasic role for Wnt/beta-catenin signaling in cardiac specification in zebrafish and embryonic stem cells. Proc. Natl. Acad. Sci. USA 104, 9685-9690.
88. Umans, L., Cox, L., Tjwa, M., Bito, V., Vermeire, L., Laperre, K., Sipido, K., Moons, L., Huylebroeck, D. and Zwijsen, A. (2007). Inactivation of Smad5 in endothelial cells and smooth muscle cells demonstrates that Smad5 is required for cardiac homeostasis. Am. J. Pathol. 170, 1460-1472.
89. Varadkar, P., Kraman, M., Despres, D., Ma, G., Lozier, J. and McCright, B. (2008). Notch2 is required for the proliferation of cardiac neural crest-derived smooth muscle cells. Dev. Dyn. 237, 1144-1152.
90. Venkatesh, D. A., Park, K. S., Harrington, A., Miceli-Libby, L., Yoon, J. K. and Liaw, L. (2008). Cardiovascular and hematopoietic defects associated with Notch1 activation in embryonic Tie2-expressing populations. Circ. Res. 103, 423-431.
91. Verdi, J. M., Schmandt, R., Bashirullah, A., Jacob, S., Salvino, R., Craig, C. G., Program, A. E., Lipshitz, H. D. and McGlade, C. J. (1996). Mammalian NUMB is an evolutionarily conserved signaling adapter protein that specifies cell fate. Curr. Biol. 6, 1134-1145.
92. Verzi, M. P., McCulley, D. J., De Val, S., Dodou, E. and Black, B. L. (2005). The right ventricle, outflow tract, and ventricular septum comprise a restricted expression domain within the secondary/anterior heart field. Dev. Biol. 287, 134-145.
93. Vincent, S. D. and Buckingham, M. E. (2010). How to make a heart: the origin and regulation of cardiac progenitor cells. Curr. Top. Dev. Biol. 90, 1-41.
94. Vitelli, F., Morishima, M., Taddei, I., Lindsay, E. A. and Baldini, A. (2002). Tbx1 mutation causes multiple cardiovascular defects and disrupts neural crest and cranial nerve migratory pathways. Hum. Mol. Genet. 11, 915-922.
95. Waldo, K. L., Kumiski, D. H., Wallis, K. T., Stadt, H. A., Hutson, M. R., Platt, D. H. and Kirby, M. L. (2001). Conotruncal myocardium arises from a secondary heart field. Development 128, 3179-3188.
96. Wang, Z., Sandiford, S., Wu, C. and Li, S. S. (2009). Numb regulates cell-cell adhesion and polarity in response to tyrosine kinase signalling. EMBO J. 28, 2360-2373.
97. Ward, C., Stadt, H., Hutson, M. and Kirby, M. L. (2005). Ablation of the secondary heart field leads to tetralogy of Fallot and pulmonary atresia. Dev. Biol. 284, 72-83.
98. Watanabe, Y., Kokubo, H., Miyagawa-Tomita, S., Endo, M., Igarashi, K., Aisaki, K., Kanno, J. and Saga, Y. (2006). Activation of Notch1 signaling in cardiogenic mesoderm induces abnormal heart morphogenesis in mouse. Development 133, 1625-1634.
99. Webb, S., Qayyum, S. R., Anderson, R. H., Lamers, W. H. and Richardson, M. K. (2003). Septation and separation within the outflow tract of the developing heart. J. Anat. 202, 327-342.
100. Weiford, B. C., Subbarao, V. D. and Mulhern, K. M. (2004). Noncompaction of the ventricular myocardium. Circulation 109, 2965-2971.
101. Wilson, A., Ardiet, D. L., Saner, C., Vilain, N., Beermann, F., Aguet, M., Macdonald, H. R. and Zilian, O. (2007). Normal hemopoiesis and lymphopoiesis in the combined absence of numb and numblike. J. Immunol. 178, 6746-6751.
102. Wu, B., Zhang, Z., Lui, W., Chen, X., Wang, Y., Chamberlain, A. A., Moreno-Rodriguez, R. A., Markwald, R. R., O'Rourke, B. P., Sharp, D. J. et al. (2012). Endocardial cells form the coronary arteries by angiogenesis through myocardialendocardial VEGF signaling. Cell 151, 1083-1096.
103. Wu, M., Kwon, H. Y., Rattis, F., Blum, J., Zhao, C., Ashkenazi, R., Jackson, T. L., Gaiano, N., Oliver, T. and Reya, T. (2007). Imaging hematopoietic precursor division in real time. Cell Stem Cell 1, 541-554.
104. Wu, M., Smith, C. L., Hall, J. A., Lee, I., Luby-Phelps, K. and Tallquist, M. D. (2010). Epicardial spindle orientation controls cell entry into the myocardium. Dev. Cell 19, 114-125.
105. Xu, K., Chong, D. C., Rankin, S. A., Zorn, A. M. and Cleaver, O. (2009). Rasip1 is required for endothelial cell motility, angiogenesis and vessel formation. Dev. Biol. 329, 269-279.
106. Xu, K., Sacharidou, A., Fu, S., Chong, D. C., Skaug, B., Chen, Z. J., Davis, G. E. and Cleaver, O. (2011). Blood vessel tubulogenesis requires Rasip1 regulation of GTPase signaling. Dev. Cell 20, 526-539.
107. Yang, X., Klein, R., Tian, X., Cheng, H. T., Kopan, R. and Shen, J. (2004). Notch activation induces apoptosis in neural progenitor cells through a p53-dependent pathway. Dev. Biol. 269, 81-94.
108. Yang, J., Bücker, S., Jungblut, B., Böttger, T., Cinnamon, Y., Tchorz, J., Müller, M., Bettler, B., Harvey, R., Sun, Q. Y. et al. (2012). Inhibition of Notch2 by Numb/Numblike controls myocardial compaction in the heart. Cardiovasc. Res. 96, 276-285.
109. Zhang, W., Chen, H., Qu, X., Chang, C. P. and Shou, W. (2013). Molecular mechanism of ventricular trabeculation/compaction and the pathogenesis of the left ventricular noncompaction cardiomyopathy (LVNC). Am. J. Med. Genet. C Semin. Med. Genet. 163C, 144-156.
110. Zhong, W., Feder, J. N., Jiang, M. M., Jan, L. Y. and Jan, Y. N. (1996). Asymmetric localization of a mammalian numb homolog during mouse cortical neurogenesis. Neuron 17, 43-53.
111. Zhong, W., Jiang, M. M., Weinmaster, G., Jan, L. Y. and Jan, Y. N. (1997). Differential expression of mammalian Numb, Numblike and Notch1 suggests distinct roles during mouse cortical neurogenesis. Development 124, 1887-1897.
112. Zhou, B., Ma, Q., Rajagopal, S., Wu, S. M., Domian, I., Rivera-Feliciano, J., Jiang, D., von Gise, A., Ikeda, S., Chien, K. R. et al. (2008). Epicardial progenitors contribute to the cardiomyocyte lineage in the developing heart. Nature 454, 109-113.
113. Zilian, O., Saner, C., Hagedorn, L., Lee, H. Y., Säuberli, E., Suter, U., Sommer, L. and Aguet, M. (2001). Multiple roles of mouse Numb in tuning developmental cell fates. Curr. Biol. 11, 494-501.