Nodal mutant eXtraembryonic ENdoderm (XEN) stem cells upregulate markers for the anterior visceral endoderm and impact the timing of cardiac differentiation in mouse embryoid bodies

Biology Open

Volumn 1, Issue 3, 2012, Pages 208-219

  Liu, Wenrui ^a   Brown, Kemar ^a   Legros, Stephanie ^a   Foley, Ann C ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

Cardiomyocyte differentiation; Extraembryonic endoderm (XEN) stem cells; Mouse ES cells; Nodal

Indexed keywords

EID: 84964575980     PISSN: None     EISSN: 20466390     Source Type: Journal    
DOI: 10.1242/bio.2012038     Document Type: Article

References (52)

1. Abu-Issa, R. and Kirby, M. L. (2007). Heart field: from mesoderm to heart tube. Annu. Rev. Cell Dev. Biol. 23, 45-68.
2. Arai, A., Yamamoto, K. and Toyama, J. (1997). Murine cardiac progenitor cells require visceral embryonic endoderm and primitive streak for terminal differentiation. Dev. Dyn. 210, 344-353.
3. Artus, J., Panthier, J. J. and Hadjantonakis, A. K. (2010). A role for PDGF signaling in expansion of the extra-embryonic endoderm lineage of the mouse blastocyst. Development 137, 3361-3372.
4. Artus, J., Douvaras, P., Piliszek, A., Isern, J., Baron, M. H. and Hadjantonakis, A. K. (2012). BMP4 signaling directs primitive endoderm-derived XEN cells to an extraembryonic visceral endoderm identity. Dev. Biol. 361, 245-262.
5. Black, B. L. (2007). Transcriptional pathways in second heart field development. Semin. Cell Dev. Biol. 18, 67-76.
6. Brennan, J., Lu, C. C., Norris, D. P., Rodriguez, T. A., Beddington, R. S. and Robertson, E. J. (2001). Nodal signalling in the epiblast patterns the early mouse embryo. Nature 411, 965-969.
7. Brown, K., Doss, M. X., Legros, S., Artus, J., Hadjantonakis, A. K. and Foley, A. (2010a). eXtraembryonic ENdoderm (XEN) Cells Produce Factors that Activate Heart Formation. PLoS ONE 5, e13446.
8. Brown, K., Legros, S., Artus, J., Doss, M. X., Khanin, R., Hadjantonakis, A. K. and Foley, A. (2010b). A comparative analysis of extra-embryonic endoderm cell lines. PLoS ONE 5, e12016.
9. Bu, L., Jiang, X., Martin-Puig, S., Caron, L., Zhu, S., Shao, Y., Roberts, D. J., Huang, P. L., Domian, I. J. and Chien, K. R. (2009). Human ISL1 heart progenitors generate diverse multipotent cardiovascular cell lineages. Nature 460, 113-117.
10. 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.
11. Camus, A., Perea-Gomez, A., Moreau, A. and Collignon, J. (2006). Absence of Nodal signaling promotes precocious neural differentiation in the mouse embryo. Dev. Biol. 295, 743-755.
12. Collignon, J., Varlet, I. and Robertson, E. J. (1996). Relationship between asymmetric nodal expression and the direction of embryonic turning. Nature 381, 155-158.
13. David, N. B. and Rosa, F. M. (2001). Cell autonomous commitment to an endodermal fate and behaviour by activation of Nodal signalling. Development 128, 3937-3947.
14. Dyer, L. A. and Kirby, M. L. (2009). The role of secondary heart field in cardiac development. Dev. Biol. 336, 137-144.
15. Foley, A. C., Korol, O., Timmer, A. M. and Mercola, M. (2007). Multiple functions of Cerberus cooperate to induce heart downstream of Nodal. Dev. Biol. 303, 57-65.
16. Fullilove, S. L. (1970). Heart induction: distribution of active factors in newt endoderm. J. Exp. Zool. 175, 323-326.
17. Granier, C., Gurchenkov, V., Perea-Gomez, A., Camus, A., Ott, S., Papanayotou, C., Iranzo, J., Moreau, A., Reid, J., Koentges, G. et al. (2011). Nodal cis-regulatory elements reveal epiblast and primitive endoderm heterogeneity in the periimplantation mouse embryo. Dev. Biol. 349, 350-362.
18. Holtzinger, A., Rosenfeld, G. E. and Evans, T. (2010). Gata4 directs development of cardiac-inducing endoderm from ES cells. Dev. Biol. 337, 63-73.
19. Jacobson, A. G. (1960). Influences of ectoderm and endoderm on heart differentiation in the newt. Dev. Biol. 2, 138-154.
20. Julio, M. K., Alvarez, M. J., Galli, A., Chu, J., Price, S. M., Califano, A. and Shen, M. M. (2011). Regulation of extra-embryonic endoderm stem cell differentiation by Nodal and Cripto signaling. Development 138, 3885-3895.
21. 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.
22. Kolossov, E., Lu, Z., Drobinskaya, I., Gassanov, N., Duan, Y., Sauer, H., Manzke, O., Bloch, W., Bohlen, H., Hescheler, J. et al. (2005). Identification and characterization of embryonic stem cell-derived pacemaker and atrial cardiomyocytes. FASEB J. 19, 577-579.
23. Kunath, T., Arnaud, D., Uy, G. D., Okamoto, I., Chureau, C., Yamanaka, Y., Heard, E., Gardner, R. L., Avner, P. and Rossant, J. (2005). Imprinted Xinactivation in extra-embryonic endoderm cell lines from mouse blastocysts. Development 132, 1649-1661.
24. Lough, J. and Sugi, Y. (2000). Endoderm and heart development. Dev. Dyn. 217, 327-342.
25. Madabhushi, M. and Lacy, E. (2011). Anterior Visceral Endoderm Directs Ventral Morphogenesis and Placement of Head and Heart via BMP2 Expression. Dev. Cell 21, 907-919.
26. Marvin, M. J., Di Rocco, G., Gardiner, A., Bush, S. M. and Lassar, A. B. (2001). Inhibition of Wnt activity induces heart formation from posterior mesoderm. Genes Dev. 15, 316-327.
27. Meilhac, S. M., Esner, M., Kelly, R. G., Nicolas, J. F. and Buckingham, M. E. (2004). The clonal origin of myocardial cells in different regions of the embryonic mouse heart. Dev. Cell 6, 685-698.
28. Mesnard, D., Guzman-Ayala, M. and Constam, D. B. (2006). Nodal specifies embryonic visceral endoderm and sustains pluripotent cells in the epiblast before overt axial patterning. Development 133, 2497-2505.
29. Moretti, A., Caron, L., Nakano, A., Lam, J. T., Bernshausen, A., Chen, Y., Qyang, Y., Bu, L., Sasaki, M., Martin-Puig, S. et al. (2006). Multipotent embryonic isl1+ progenitor cells lead to cardiac, smooth muscle, and endothelial cell diversification. Cell 127, 1151-1165.
30. Mummery, C., Ward-van Oostwaard, D., Doevendans, P., Spijker, R., van den Brink, S., Hassink, R., van der Heyden, M., Opthof, T., Pera, M., de la Riviere, A. B. et al. (2003). Differentiation of human embryonic stem cells to cardiomyocytes: role of coculture with visceral endoderm-like cells. Circulation 107, 2733-2740.
31. Nascone, N. and Mercola, M. (1995). An inductive role for the endoderm in Xenopus cardiogenesis. Development 121, 515-523.
32. Nijmeijer, R. M., Leeuwis, J. W., DeLisio, A., Mummery, C. L. and Chuva de Sousa Lopes, S. M. (2009). Visceral endoderm induces specification of cardiomyocytes in mice. Stem Cell Res. 3, 170-178.
33. Norris, D. P., Brennan, J., Bikoff, E. K. and Robertson, E. J. (2002). The Foxh1-dependent autoregulatory enhancer controls the level of Nodal signals in the mouse embryo. Development 129, 3455-3468.
34. Orts-Llorca, F. and Gil, D. R. (1965). Influence of the endoderm on heart differentiation. Roux's Arch. EntwMech. Org. 156, 368-370.
35. Prall, O. W., Menon, M. K., Solloway, M. J., Watanabe, Y., Zaffran, S., Bajolle, F., Biben, C., McBride, J. J., Robertson, B. R., Chaulet, H. et al. (2007). An Nkx2-5/Bmp2/Smad1 negative feedback loop controls heart progenitor specification and proliferation. Cell 128, 947-959.
36. Qyang, Y., Martin-Puig, S., Chiravuri, M., Chen, S., Xu, H., Bu, L., Jiang, X., Lin, L., Granger, A., Moretti, A. et al. (2007). The renewal and differentiation of Isl1+ cardiovascular progenitors are controlled by a Wnt/beta-catenin pathway. Cell Stem Cell 1, 165-179.
37. Roessler, E., Pei, W., Ouspenskaia, M. V., Karkera, J. D., Velez, J. I., Banerjee-Basu, S., Gibney, G., Lupo, P. J., Mitchell, L. E., Towbin, J. A. et al. (2009). Cumulative ligand activity of NODAL mutations and modifiers are linked to human heart defects and holoprosencephaly. Mol. Genet. Metab. 98, 225-234.
38. Sater, A. K. and Jacobson, A. G. (1989). The specification of heart mesoderm occurs during gastrulation in Xenopus laevis. Development 105, 821-830.
39. Schneider, V. A. and Mercola, M. (1999). Spatially distinct head and heart inducers within the Xenopus organizer region. Curr. Biol. 9, 800-809.
40. Stary, M., Pasteiner, W., Summer, A., Hrdina, A., Eger, A. and Weitzer, G. (2005). Parietal endoderm secreted SPARC promotes early cardiomyogenesis in vitro. Exp. Cell Res. 310, 331-343.
41. Stennard, F. A., Costa, M. W., Lai, D., Biben, C., Furtado, M. B., Solloway, M. J., McCulley, D. J., Leimena, C., Preis, J. I., Dunwoodie, S. L. et al. (2005). Murine T-box transcription factor Tbx20 acts as a repressor during heart development, and is essential for adult heart integrity, function and adaptation. Development 132, 2451-2462.
42. Sugi, Y. and Lough, J. (1994). Anterior endoderm is a specific effector of terminal cardiac myocyte differentiation of cells from the embryonic heart forming region. Dev. Dyn. 200, 155-162.
43. Takahashi, T., Lord, B., Schulze, P. C., Fryer, R. M., Sarang, S. S., Gullans, S. R. and Lee, R. T. (2003). Ascorbic acid enhances differentiation of embryonic stem cells into cardiac myocytes. Circulation 107, 1912-1916.
44. Takaoka, K., Yamamoto, M. and Hamada, H. (2011). Origin and role of distal visceral endoderm, a group of cells that determines anterior-posterior polarity of the mouse embryo. Nat. Cell Biol. 13, 743-752.
45. Tonegawa, A., Moriya, M., Tada, M., Nishimatsu, S., Katagiri, C. and Ueno, N. (1996). Heart formative factor(s) is localized in the anterior endoderm of early Xenopus neurula. Roux's Arch. Dev. Biol. 205, 282-289.
46. Torres-Padilla, M. E., Richardson, L., Kolasinska, P., Meilhac, S. M., Luetke-Eversloh, M. V. and Zernicka-Goetz, M. (2007). The anterior visceral endoderm of the mouse embryo is established from both preimplantation precursor cells and by de novo gene expression after implantation. Dev. Biol. 309, 97-112.
47. Varlet, I., Collignon, J. and Robertson, E. J. (1997). nodal expression in the primitive endoderm is required for specification of the anterior axis during mouse gastrulation. Development 124, 1033-1044.
48. 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.
49. Waldo, K. L., Hutson, M. R., Ward, C. C., Zdanowicz, M., Stadt, H. A., Kumiski, D., Abu-Issa, R. and Kirby, M. L. (2005). Secondary heart field contributes myocardium and smooth muscle to the arterial pole of the developing heart. Dev. Biol. 281, 78-90.
50. Yamamoto, M., Saijoh, Y., Perea-Gomez, A., Shawlot, W., Behringer, R. R., Ang, S. L., Hamada, H. and Meno, C. (2004). Nodal antagonists regulate formation of the anteroposterior axis of the mouse embryo. Nature 428, 387-392.
51. Yuasa, S., Itabashi, Y., Koshimizu, U., Tanaka, T., Sugimura, K., Kinoshita, M., Hattori, F., Fukami, S., Shimazaki, T., Ogawa, S. et al. (2005). Transient inhibition of BMP signaling by Noggin induces cardiomyocyte differentiation of mouse embryonic stem cells. Nat. Biotechnol. 23, 607-611.
52. Zaffran, S., Kelly, R. G., Meilhac, S. M., Buckingham, M. E. and Brown, N. A. (2004). Right ventricular myocardium derives from the anterior heart field. Circ. Res. 95, 261-268.