Erg is a crucial regulator of endocardial-mesenchymal transformation during cardiac valve morphogenesis

Development (Cambridge)

Volumn 139, Issue 21, 2012, Pages 3973-3985

  Vijayaraj, Preethi ^a   Le Bras, Alexandra ^a   Mitchell, Nora ^a   Kondo, Maiko ^b   Juliao, Saul ^a   Wasserman, Meredith ^a   Beeler, David ^a   Spokes, Katherine ^a   Aird, William C ^a   Scott Baldwin, H ^b   Oettgen, Peter ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

EMT; EnMT; Erg isoforms; Ets factor; Snail1 (Snai1); Snail2 (Snai2); Valve morphogenesis

Indexed keywords

SNAIL1 PROTEIN; SNAIL2 PROTEIN; TRANSCRIPTION FACTOR ERG; TRANSCRIPTION FACTOR SNAIL; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; BINDING SITE; CARTILAGE CELL; CELL CULTURE; CHROMATIN IMMUNOPRECIPITATION; EMBRYO DEVELOPMENT; ENDOCARDIAL MESENCHYMAL TRANSFORMATION; EPITHELIAL MESENCHYMAL TRANSITION; EX VIVO STUDY; EXON; GENE LOCUS; GENETIC ANALYSIS; GENOTYPE; HEART DEVELOPMENT; HEART LEFT VENTRICLE OUTFLOW TRACT; HEART RIGHT VENTRICLE OUTFLOW TRACT; HEART VALVE; KNOCKOUT MOUSE; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ANIMALS; ENDOCARDIUM; GENOTYPE; HEART VALVES; MESODERM; MICE; MICE, KNOCKOUT; MORPHOGENESIS; ONCOGENE PROTEINS; TRANSCRIPTION FACTORS;

EID: 84867242355     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.081596     Document Type: Article

References (65)

1. Anderson, M. K., Hernandez-Hoyos, G., Diamond, R. A. and Rothenberg, E. V. (1999). Precise developmental regulation of Ets family transcription factors during specification and commitment to the T cell lineage. Development 126, 3131-3148.
2. Armstrong, E. J. and Bischoff, J. (2004). Heart valve development: endothelial cell signaling and differentiation. Circ. Res. 95, 459-470.
3. Baltzinger, M., Mager-Heckel, A. M. and Remy, P. (1999). Xl erg: expression pattern and overexpression during development plead for a role in endothelial cell differentiation. Dev. Dyn. 216, 420-433.
4. Bartram, U., Molin, D. G., Wisse, L. J., Mohamad, A., Sanford, L. P., Doetschman, T., Speer, C. P., Poelmann, R. E. and Gittenberger-de Groot, A. C. (2001). Double-outlet right ventricle and overriding tricuspid valve reflect disturbances of looping, myocardialization, endocardial cushion differentiation, and apoptosis in TGF-beta(2)-knockout mice. Circulation 103, 2745-2752.
5. Ben-Porath, I., Thomson, M. W., Carey, V. J., Ge, R., Bell, G. W., Regev, A. and Weinberg, R. A. (2008). An embryonic stem cell-like gene expression signature in poorly differentiated aggressive human tumors. Nat. Genet. 40, 499-507.
6. Birdsey, G. M., Dryden, N. H., Amsellem, V., Gebhardt, F., Sahnan, K., Haskard, D. O., Dejana, E., Mason, J. C. and Randi, A. M. (2008). Transcription factor Erg regulates angiogenesis and endothelial apoptosis through VE-cadherin. Blood 111, 3498-3506.
7. Butcher, J. T. and Markwald, R. R. (2007). Valvulogenesis: the moving target. Philos. Trans. R. Soc. Lond. B Biol. Sci. 362, 1489-1503.
8. Buttice, G., Duterque-Coquillaud, M., Basuyaux, J. P., Carrere, S., Kurkinen, M. and Stehelin, D. (1996). Erg, an Ets-family member, differentially regulates human collagenase1 (MMP1) and stromelysin1 (MMP3) gene expression by physically interacting with the Fos/Jun complex. Oncogene 13, 2297-2306.
9. Cai, X., Nomura-Kitabayashi, A., Cai, W., Yan, J., Christoffels, V. M. and Cai, C. L. (2011). Myocardial Tbx20 regulates early atrioventricular canal formation and endocardial epithelial-mesenchymal transition via Bmp2. Dev. Biol. 360, 81-90.
10. Camenisch, T. D., Molin, D. G., Person, A., Runyan, R. B., Gittenberger-de Groot, A. C., McDonald, J. A. and Klewer, S. E. (2002a). Temporal and distinct TGFbeta ligand requirements during mouse and avian endocardial cushion morphogenesis. Dev. Biol. 248, 170-181.
11. Camenisch, T. D., Schroeder, J. A., Bradley, J., Klewer, S. E. and McDonald, J. A. (2002b). Heart-valve mesenchyme formation is dependent on hyaluronanaugmented activation of ErbB2-ErbB3 receptors. Nat. Med. 8, 850-855.
12. Carey, M. F., Peterson, C. L. and Smale, S. T. (2009). Chromatin immunoprecipitation (ChIP). Cold Spring Harb. Protoc. 2009, pdb prot5279.
13. Chen, H. Q., Zhang, X. C., Huang, S. L., Cai, Y., Wu, B. Y., Zhou, D. H. and Huang, K. (2008). [BMP-4 and VEGF promote development of hematopoietic stem cells during the embryoid body formation from embryonic stem cells]. Zhongguo Shi Yan Xue Ye Xue Za Zhi 16, 855-858.
14. Colas, E., Muinelo-Romay, L., Alonso-Alconada, L., Llaurado, M., Monge, M., Barbazan, J., Gonzalez, M., Schoumacher, M., Pedrola, N., Ertekin, T. et al. (2012). ETV5 cooperates with LPP as a sensor of extracellular signals and promotes EMT in endometrial carcinomas. Oncogene (in press).
15. DeLaughter, D. M., Saint-Jean, L., Baldwin, H. S. and Barnett, J. V. (2011). What chick and mouse models have taught us about the role of the endocardium in congenital heart disease. Birth Defects Res. A Clin. Mol. Teratol. 91, 511-525.
16. Dickson, M. C., Martin, J. S., Cousins, F. M., Kulkarni, A. B., Karlsson, S. and Akhurst, R. J. (1995). Defective haematopoiesis and vasculogenesis in transforming growth factor-beta 1 knock out mice. Development 121, 1845-1854.
17. Eisenberg, L. M. and Markwald, R. R. (1995). Molecular regulation of atrioventricular valvuloseptal morphogenesis. Circ. Res. 77, 1-6.
18. Ellett, F., Kile, B. T. and Lieschke, G. J. (2009). The role of the ETS factor erg in zebrafish vasculogenesis. Mech. Dev. 126, 220-229.
19. Fafeur, V., Tulasne, D., Queva, C., Vercamer, C., Dimster, V., Mattot, V., Stehelin, D., Desbiens, X. and Vandenbunder, B. (1997). The ETS1 transcription factor is expressed during epithelial-mesenchymal transitions in the chick embryo and is activated in scatter factor-stimulated MDCK epithelial cells. Cell Growth Differ. 8, 655-665.
20. Findlay, V. J., Turner, D. P., Yordy, J. S., McCarragher, B., Shriver, M. R., Szalai, G., Watson, P. M., Larue, A. C., Moussa, O. and Watson, D. K. (2011). Prostate-derived ETS factor regulates epithelial-to-mesenchymal transition through both SLUG-dependent and independent mechanisms. Genes Cancer 2, 120-129.
21. Grego-Bessa, J., Luna-Zurita, L., del Monte, G., Bolos, 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.
22. Habets, P. E., Moorman, A. F., Clout, D. E., van Roon, M. A., Lingbeek, M., van Lohuizen, M., Campione, M. and Christoffels, V. M. (2002). Cooperative action of Tbx2 and Nkx2.5 inhibits ANF expression in the atrioventricular canal: implications for cardiac chamber formation. Genes Dev. 16, 1234-1246.
23. Hasegawa, Y., Abe, M., Yamazaki, T., Niizeki, O., Shiiba, K., Sasaki, I. and Sato, Y. (2004). Transcriptional regulation of human angiopoietin-2 by transcription factor Ets-1. Biochem. Biophys. Res. Commun. 316, 52-58.
24. Hewett, P. W., Nishi, K., Daft, E. L. and Clifford Murray, J. (2001). Selective expression of erg isoforms in human endothelial cells. Int. J. Biochem. Cell Biol. 33, 347-355.
25. Higashino, F., Yoshida, K., Noumi, T., Seiki, M. and Fujinaga, K. (1995). Etsrelated protein E1A-F can activate three different matrix metalloproteinase gene promoters. Oncogene 10, 1461-1463.
26. Iwamoto, M., Higuchi, Y., Koyama, E., Enomoto-Iwamoto, M., Kurisu, K., Yeh, H., Abrams, W. R., Rosenbloom, J. and Pacifici, M. (2000). Transcription factor ERG variants and functional diversification of chondrocytes during limb long bone development. J. Cell Biol. 150, 7-40.
27. Iwamoto, M., Higuchi, Y., Enomoto-Iwamoto, M., Kurisu, K., Koyama, E., Yeh, H., Rosenbloom, J. and Pacifici, M. (2001). The role of ERG (ets related gene) in cartilage development. Osteoarthritis Cartilage 9 Suppl. A, S41-S47.
28. Iwamoto, M., Tamamura, Y., Koyama, E., Komori, T., Takeshita, N., Williams, J. A., Nakamura, T., Enomoto-Iwamoto, M. and Pacifici, M. (2007). Transcription factor ERG and joint and articular cartilage formation during mouse limb and spine skeletogenesis. Dev. Biol. 305, 40-51.
29. Kaartinen, V., Voncken, J. W., Shuler, C., Warburton, D., Bu, D., Heisterkamp, N. and Groffen, J. (1995). Abnormal lung development and cleft palate in mice lacking TGF-beta 3 indicates defects of epithelialmesenchymal interaction. Nat. Genet. 11, 415-421.
30. Kalluri, R. (2009). EMT: when epithelial cells decide to become mesenchymal-like cells. J. Clin. Invest. 119, 1417-1419.
31. Kola, I., Brookes, S., Green, A. R., Garber, R., Tymms, M., Papas, T. S. and Seth, A. (1993). The Ets1 transcription factor is widely expressed during murine embryo development and is associated with mesodermal cells involved in morphogenetic processes such as organ formation. Proc. Natl. Acad. Sci. USA 90, 7588-7592.
32. Loughran, S. J., Kruse, E. A., Hacking, D. F., de Graaf, C. A., Hyland, C. D., Willson, T. A., Henley, K. J., Ellis, S., Voss, A. K., Metcalf, D. et al. (2008). The transcription factor Erg is essential for definitive hematopoiesis and the function of adult hematopoietic stem cells. Nat. Immunol. 9, 810-819.
33. Lukashev, M. E. and Werb, Z. (1998). ECM signalling: orchestrating cell behaviour and misbehaviour. Trends Cell Biol. 8, 37-41.
34. Ma, Q. J., Gu, X. Q., Cao, X., Zhao, J., Kong, X. B., Li, Y. X. and Cai, S. Y. (2005). Effect of beta radiation on TGF-beta1 and bFGF expression in hyperplastic prostatic tissues. Asian J. Androl. 7, 49-54.
35. Marin-Padilla, M. (1985). Early vascularization of the embryonic cerebral cortex: Golgi and electron microscopic studies. J. Comp. Neurol. 241, 237-249.
36. Maroulakou, I. G., Papas, T. S. and Green, J. E. (1994). Differential expression of ets-1 and ets-2 proto-oncogenes during murine embryogenesis. Oncogene 9, 1551-1565.
37. McKeown, S. J., Lee, V. M., Bronner-Fraser, M., Newgreen, D. F. and Farlie, P. G. (2005). Sox10 overexpression induces neural crest-like cells from all dorsoventral levels of the neural tube but inhibits differentiation. Dev. Dyn. 233, 430-444.
38. Niessen, K. and Karsan, A. (2008). Notch signaling in cardiac development. Circ. Res. 102, 1169-1181.
39. Niessen, K., Fu, Y., Chang, L., Hoodless, P. A., McFadden, D. and Karsan, A. (2008). Slug is a direct Notch target required for initiation of cardiac cushion cellularization. J. Cell Biol. 182, 315-325.
40. Nikolova-Krstevski, V., Yuan, L., Le Bras, A., Vijayaraj, P., Kondo, M., Gebauer, I., Bhasin, M., Carman, C. V. and Oettgen, P. (2009). ERG is required for the differentiation of embryonic stem cells along the endothelial lineage. BMC Dev. Biol. 9, 72.
41. Person, A. D., Klewer, S. E. and Runyan, R. B. (2005). Cell biology of cardiac cushion development. Int. Rev. Cytol. 243, 287-335.
42. Pimanda, J. E., Chan, W. Y., Donaldson, I. J., Bowen, M., Green, A. R. and Gottgens, B. (2006). Endoglin expression in the endothelium is regulated by Fli- 1, Erg, and Elf-1 acting on the promoter and a -8-kb enhancer. Blood 107, 4737-4745.
43. Raghow, R. (1994). The role of extracellular matrix in postinflammatory wound healing and fibrosis. FASEB J. 8, 823-831.
44. Remy, P. and Baltzinger, M. (2000). The Ets-transcription factor family in embryonic development: lessons from the amphibian and bird. Oncogene 19, 6417-6431.
45. Risau, W. and Wolburg, H. (1990). Development of the blood-brain barrier. Trends Neurosci. 13, 174-178.
46. Runyan, R. B. and Markwald, R. R. (1983). Invasion of mesenchyme into threedimensional collagen gels: a regional and temporal analysis of interaction in embryonic heart tissue. Dev. Biol. 95, 108-114.
47. Saint-Germain, N., Lee, Y. H., Zhang, Y., Sargent, T. D. and Saint-Jeannet, J. P. (2004). Specification of the otic placode depends on Sox9 function in Xenopus. Development 131, 1755-1763.
48. Sanford, L. P., Ormsby, I., Gittenberger-de Groot, A. C., Sariola, H., Friedman, R., Boivin, G. P., Cardell, E. L. and Doetschman, T. (1997). TGFbeta2 knockout mice have multiple developmental defects that are nonoverlapping with other TGFbeta knockout phenotypes. Development 124, 2659-2670.
49. Schachterle, W., Rojas, A., Xu, S. M. and Black, B. L. (2012). ETS-dependent regulation of a distal Gata4 cardiac enhancer. Dev. Biol. 361, 439-449.
50. Schwachtgen, J. L., Janel, N., Barek, L., Duterque-Coquillaud, M., Ghysdael, J., Meyer, D. and Kerbiriou-Nabias, D. (1997). Ets transcription factors bind and transactivate the core promoter of the von Willebrand factor gene. Oncogene 15, 3091-3102.
51. Stenvers, K. L., Tursky, M. L., Harder, K. W., Kountouri, N., Amatayakul- Chantler, S., Grail, D., Small, C., Weinberg, R. A., Sizeland, A. M. and Zhu, H. J. (2003). Heart and liver defects and reduced transforming growth factor beta2 sensitivity in transforming growth factor beta type III receptor-deficient embryos. Mol. Cell. Biol. 23, 4371-4385.
52. Tahtakran, S. A. and Selleck, M. A. (2003). Ets-1 expression is associated with cranial neural crest migration and vasculogenesis in the chick embryo. Gene Expr. Patterns 3, 455-458.
53. Taoudi, S., Bee, T., Hilton, A., Knezevic, K., Scott, J., Willson, T. A., Collin, C., Thomas, T., Voss, A. K., Kile, B. T. et al. (2011). ERG dependence distinguishes developmental control of hematopoietic stem cell maintenance from hematopoietic specification. Genes Dev. 25, 251-262.
54. Theveneau, E., Duband, J. L. and Altabef, M. (2007). Ets-1 confers cranial features on neural crest delamination. PLoS ONE 2, e1142.
55. Timmerman, L. A., Grego-Bessa, J., Raya, A., Bertran, E., Perez-Pomares, J. M., Diez, J., Aranda, S., Palomo, S., McCormick, F., Izpisua-Belmonte, J. C. et al. (2004). Notch promotes epithelial-mesenchymal transition during cardiac development and oncogenic transformation. Genes Dev. 18, 99-115.
56. Vijayaraj, P., Sohl, G. and Magin, T. M. (2007). Keratin transgenic and knockout mice: functional analysis and validation of disease-causing mutations. Methods Mol. Biol. 360, 203-251.
57. Vlaeminck-Guillem, V., Carrere, S., Dewitte, F., Stehelin, D., Desbiens, X. and Duterque-Coquillaud, M. (2000). The Ets family member Erg gene is expressed in mesodermal tissues and neural crests at fundamental steps during mouse embryogenesis. Mech. Dev. 91, 331-335.
58. Wasylyk, B., Hahn, S. L. and Giovane, A. (1993). The Ets family of transcription factors. Eur. J. Biochem. 211, 7-18.
59. Werb, Z. (1997). ECM and cell surface proteolysis: regulating cellular ecology. Cell 91, 439-442.
60. Werb, Z. and Chin, J. R. (1998). Extracellular matrix remodeling during morphogenesis. Ann. N. Y. Acad. Sci. 857, 110-118.
61. Wu, B., Wang, Y., Lui, W., Langworthy, M., Tompkins, K. L., Hatzopoulos, A. K., Baldwin, H. S. and Zhou, B. (2011). Nfatc1 coordinates valve endocardial cell lineage development required for heart valve formation. Circ. Res. 109, 183-192.
62. Yamamoto, H., Flannery, M. L., Kupriyanov, S., Pearce, J., McKercher, S. R., Henkel, G. W., Maki, R. A., Werb, Z. and Oshima, R. G. (1998). Defective trophoblast function in mice with a targeted mutation of Ets2. Genes Dev. 12, 315-326.
63. Yu, J., Yu, J., Mani, R. S., Cao, Q., Brenner, C. J., Cao, X., Wang, X., Wu, L., Li, J., Hu, M. et al. (2010). An integrated network of androgen receptor, polycomb, and TMPRSS2-ERG gene fusions in prostate cancer progression. Cancer Cell 17, 443-454.
64. Yuan, L., Nikolova-Krstevski, V., Zhan, Y., Kondo, M., Bhasin, M., Varghese, L., Yano, K., Carman, C. V., Aird, W. C. and Oettgen, P. (2009). Antiinflammatory effects of the ETS factor ERG in endothelial cells are mediated through transcriptional repression of the interleukin-8 gene. Circ. Res. 104, 1049-1057.
65. Yuan, L., Le Bras, A., Sacharidou, A., Itagaki, K., Zhan, Y., Kondo, M., Carman, C. V., Davis, G. E. and Aird, W. C. (2012). ETS-related gene (ERG) controls endothelial cell permeability via transcriptional regulation of the claudin 5 (CLDN5) gene. J. Biol. Chem. 287, 6582-6591.