Endoderm convergence controls subduction of the myocardial precursors during heart-tube formation

Development (Cambridge)

Volumn 142, Issue 17, 2015, Pages 2928-2940

  Ye, Ding ^a   Xie, Huaping ^a   Hu, Bo ^a   Lin, Fang ^b  

^a UNIVERSITY OF IOWA   (United States)

^b INSTITUTE OF HYDROBIOLOGY   (China)

Author keywords

Endoderm convergence; In vivo imaging; Myocardial migration; S1pr2 G 13; Subduction

Indexed keywords

FIBRONECTIN; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; SPHINGOSINE 1 PHOSPHATE RECEPTOR; ZEBRAFISH PROTEIN;

ANIMAL TISSUE; ARTICLE; CELL MIGRATION; CONTROLLED STUDY; EMBRYO; ENDODERM; HEART DEVELOPMENT; HEART MUSCLE CELL; MESODERM; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; SIGNAL TRANSDUCTION; STEM CELL; ANIMAL; CELL MOTION; CYTOLOGY; EMBRYOLOGY; EPITHELIUM; HEART; HEART MUSCLE; METABOLISM; MORPHOGENESIS; ORGANOGENESIS; ZEBRA FISH;

ANIMALS; BODY PATTERNING; CELL MOVEMENT; ENDODERM; EPITHELIUM; FIBRONECTINS; GTP-BINDING PROTEIN ALPHA SUBUNITS, G12-G13; HEART; MESODERM; MYOCARDIUM; ORGANOGENESIS; RECEPTORS, LYSOSPHINGOLIPID; SIGNAL TRANSDUCTION; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84940777760     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.113944     Document Type: Article

References (60)

1. Aleksandrova, A., Czirok, A., Kosa, E., Galkin, O., Cheuvront, T. J. and Rongish, B. J. (2015). The endoderm and myocardium join forces to drive early heart tube assembly. Dev. Biol. 404, 40-54.
2. Andrée B., Duprez D., Vorbusch B., Arnold H.-H. and Brand T. (1998). BMP-2 induces ectopic expression of cardiac lineage markers and interferes with somite formation in chicken embryos. Mech. Dev. 70, 119-131.
3. Arnold J. S., Werling, U., Braunstein, E. M., Liao, J., Nowotschin, S., Edelmann, W., Hebert, J. M. and Morrow, B. E. (2006). Inactivation of Tbx1 in the pharyngeal endoderm results in 22q11DS malformations. Development 133, 977-987.
4. Arrington, C. B. and Yost, H. J. (2009). Extra-embryonic syndecan 2 regulates organ primordia migration and fibrillogenesis throughout the zebrafish embryo. Development 136, 3143-3152.
5. Bakkers, J. (2011). Zebrafish as a model to study cardiac development and human cardiac disease. Cardiovasc. Res. 91, 279-288.
6. Bénazéraf B., Francois, P., Baker, R. E., Denans, N., Little, C. D. and Pourquié O. (2010). A random cell motility gradient downstream of FGF controls elongation of an amniote embryo. Nature 466, 248-252.
7. Bussmann, J., Bakkers, J. and Schulte-Merker, S. (2007). Early endocardial morphogenesis requires Scl/Tal1. PLoS Genet. 3, e140.
8. Carvalho, L., Stuhmer, J., Bois, J. S., Kalaidzidis, Y., Lecaudey, V. and Heisenberg, C.-P. (2009). Control of convergent yolk syncytial layer nuclear movement in zebrafish. Development 136, 1305-1315.
9. Choe, C. P., Collazo, A., Trinh le, A., Pan, L., Moens, C. B. and Crump, J. G. (2013). Wnt-dependent epithelial transitions drive pharyngeal pouch formation. Dev. Cell 24, 296-309.
10. Cui, C., Cheuvront, T. J., Lansford, R. D., Moreno-Rodriguez, R. A., Schultheiss, T. M. and Rongish, B. J. (2009). Dynamic positional fate map of the primary heart-forming region. Dev. Biol. 332, 212-222.
11. 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.
12. Evans, S. M., Yelon, D., Conlon, F. L. and Kirby, M. L. (2010). Myocardial lineage development. Circ. Res. 107, 1428-1444.
13. Garavito-Aguilar, Z. V., Riley, H. E. and Yelon, D. (2010). Hand2 ensures an appropriate environment for cardiac fusion by limiting Fibronectin function. Development 137, 3215-3220.
14. Guner-Ataman, B., Paffett-Lugassy, N., Adams, M. S., Nevis, K. R., Jahangiri, L., Obregon, P., Kikuchi, K., Poss, K. D., Burns, C. E. and Burns, C. G. (2013). Zebrafish second heart field development relies on progenitor specification in anterior lateral plate mesoderm and nkx2.5 function. Development 140, 1353-1363.
15. Haack, T., Schneider, M., Schwendele, B. and Renault, A. D. (2014). Drosophila heart cell movement to the midline occurs through both cell autonomous migration and dorsal closure. Dev. Biol. 396, 169-182.
16. Holtzman, N. G., Schoenebeck, J. J., Tsai, H.-J. and Yelon, D. (2007). Endocardium is necessary for cardiomyocyte movement during heart tube assembly. Development 134, 2379-2386.
17. Huang, C. J., Tu, C. T., Hsiao, C. D., Hsieh, F. J. and Tsai, H. J. (2003). Germ-line transmission of a myocardium-specific GFP transgene reveals critical regulatory elements in the cardiac myosin light chain 2 promoter of zebrafish. Dev. Dyn. 228, 30-40.
18. Kawahara, A., Nishi, T., Hisano, Y., Fukui, H., Yamaguchi, A. and Mochizuki, N. (2009). The sphingolipid transporter spns2 functions in migration of zebrafish myocardial precursors. Science 323, 524-527.
19. Kimmel, C. B., Ballard, W. W., Kimmel, S. R., Ullmann, B. and Schilling, T. F. (1995). Stages of embryonic development of the zebrafish. Dev. Dyn. 203, 253-310.
20. Kupperman, E., An, S., Osborne, N.,Waldron, S. and Stainier, D. Y. R. (2000). A sphingosine-1-phosphate receptor regulates cell migration during vertebrate heart development. Nature 406, 192-195.
21. Kwan, K. M., Fujimoto, E., Grabher, C., Mangum, B. D., Hardy, M. E., Campbell, D. S., Parant, J. M., Yost, H. J., Kanki, J. P. and Chien, C.-B. (2007). The Tol2kit: a multisite gateway-based construction kit for Tol2 transposon transgenesis constructs. Dev. Dyn. 236, 3088-3099.
22. Lecuit, T., Lenne, P.-F. and Munro, E. (2011). Force generation, transmission, and integration during cell and tissue morphogenesis. Annu. Rev. Cell Dev. Biol. 27, 157-184.
23. Lin, F., Sepich, D. S., Chen, S., Topczewski, J., Yin, C., Solnica-Krezel, L. and Hamm, H. (2005). Essential roles of Ga12/13 signaling in distinct cell behaviors driving zebrafish convergence and extension gastrulation movements. J. Cell. Biol. 169, 777-787.
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. Maretto, S., Mü ller, P.-S., Aricescu A. R., Cho K. W. Y., Bikoff E. K. and Robertson E. J. (2008). Ventral closure, headfold fusion and definitive endoderm migration defects in mouse embryos lacking the fibronectin leucine-rich transmembrane protein FLRT3. Dev. Biol. 318, 184-193.
27. Matsui, T., Raya, Á., Callol-Massot, C., Kawakami, Y., Oishi, I., Rodriguez- Esteban, C. and Belmonte, J. C. I. (2007). miles-apart-Mediated regulation of cell–fibronectin interaction and myocardial migration in zebrafish. Nat. Clin. Pract. Cardiovasc. Med. 4 Suppl. 1, S77-S82.
28. Miller, C. J. and Davidson, L. A. (2013). The interplay between cell signalling and mechanics in developmental processes. Nat. Rev. Genet. 14, 733-744.
29. Mizoguchi, T., Verkade, H., Heath, J. K., Kuroiwa, A. and Kikuchi, Y. (2008). Sdf1/Cxcr4 signaling controls the dorsal migration of endodermal cells during zebrafish gastrulation. Development 135, 2521-2529.
30. Muto, A., Calof, A. L., Lander, A. D. and Schilling, T. F. (2011). Multifactorial origins of heart and gut defects in nipbl-deficient zebrafish, a model of Cornelia de Lange Syndrome. PLoS Biol. 9, e1001181.
31. Narita, N., Bielinska, M. and Wilson, D. B. (1997). Wild-type endoderm abrogates the ventral developmental defects associated with GATA-4 deficiency in the mouse. Dev. Biol. 189, 270-274.
32. Nascone, N. and Mercola, M. (1995). An inductive role for the endoderm in Xenopus cardiogenesis. Development 121, 515-523.
33. Osborne, N., Brand-Arzamendi, K., Ober, E. A., Jin, S.-W., Verkade, H., Holtzman, N. G., Yelon, D. and Stainier, D. Y. R. (2008). The spinster homolog, two of hearts, is required for sphingosine 1-phosphate signaling in zebrafish. Curr. Biol. 18, 1882-1888.
34. Reiter, J. F., Alexander, J., Rodaway, A., Yelon, D., Patient, R., Holder, N. and Stainier, D. Y. R. (1999). Gata5 is required for the development of the heart and endoderm in zebrafish. Genes Dev. 13, 2983-2995.
35. Rosenquist, G. C. (1970). Cardia bifida in chick embryos: anterior and posterior defects produced by transplanting tritiated thymidine-labeled grafts medial to the heart-forming regions. Teratology 3, 135-142.
36. Sakaguchi, T., Kikuchi, Y., Kuroiwa, A., Takeda, H. and Stainier, D. Y. R. (2006). The yolk syncytial layer regulates myocardial migration by influencing extracellular matrix assembly in zebrafish. Development 133, 4063-4072.
37. Schultheiss, T. M., Xydas, S. and Lassar, A. B. (1995). Induction of avian cardiac myogenesis by anterior endoderm. Development 121, 4203-4214.
38. Shoji, W. and Sato-Maeda, M. (2008). Application of heat shock promoter in transgenic zebrafish. Dev. Growth Differ. 50, 401-406.
39. Shook, D. R., Majer, C. and Keller, R. (2002). Urodeles remove mesoderm from the superficial layer by subduction through a bilateral primitive streak. Dev. Biol. 248, 220-239.
40. Shook, D. R., Majer, C. and Keller, R. (2004). Pattern and morphogenesis of presumptive superficial mesoderm in two closely related species, Xenopus laevis and Xenopus tropicalis. Dev. Biol. 270, 163-185.
41. Staudt, D. and Stainier, D. (2012). Uncovering the molecular and cellular mechanisms of heart development using the zebrafish. Annu. Rev. Genet. 46, 397-418.
42. Trinh, L. A. and Stainier, D. Y. R. (2004). Fibronectin regulates epithelial organization during myocardial migration in zebrafish. Dev. Cell 6, 371-382.
43. Trinh, L. A., Yelon, D. and Stainier, D. Y. R. (2005). Hand2 regulates epithelial formation during myocardial differentiation. Curr. Biol. 15, 441-446.
44. Varner, V. D. and Taber, L. A. (2012). Not just inductive: a crucial mechanical role for the endoderm during heart tube assembly. Development 139, 1680-1690.
45. Villefranc, J. A., Amigo, J. and Lawson, N. D. (2007). Gateway compatible vectors for analysis of gene function in the zebrafish. Dev. Dyn. 236, 3077-3087.
46. Wong, K. S., Rehn, K., Palencia-Desai, S., Kohli, V., Hunter, W., Uhl, J. D., Rost, M. S. and Sumanas, S. (2012). Hedgehog signaling is required for differentiation of endocardial progenitors in zebrafish. Dev. Biol. 361, 377-391.
47. Woo, S., Housley, M. P., Weiner, O. D. and Stainier, D. Y. R. (2012). Nodal signaling regulates endodermal cell motility and actin dynamics via Rac1 and Prex1. J. Cell Biol. 198, 941-952.
48. Xu, H., Ye, D., Behra, M., Burgess, S., Chen, S. and Lin, F. (2014). Gb1 controls collective cell migration by regulating the protrusive activity of leader cells in the posterior lateral line primordium. Dev. Biol. 385, 316-327.
49. Ye, D. and Lin, F. (2013). S1pr2/Gα13 signaling controls myocardial migration by regulating endoderm convergence. Development 140, 789-799.
50. Yelon, D., Horne, S. A. and Stainier, D. Y. R. (1999). Restricted expression of cardiac myosin genes reveals regulated aspects of heart tube assembly in zebrafish. Dev. Biol. 214, 23-37.
51. Yelon, D., Ticho, B., Halpern, M. E., Ruvinsky, I., Ho, R. K., Silver, L. M. and Stainier, D. Y. (2000). The bHLH transcription factor hand2 plays parallel roles in zebrafish heart and pectoral fin development. Development 127, 2573-2582.
52. Yin, C., Kikuchi, K., Hochgreb, T., Poss, K. D. and Stainier, D. Y. (2010). Hand2 regulates extracellular matrix remodeling essential for gut-looping morphogenesis in zebrafish. Dev. Cell 18, 973-984.
53. Zamir, E. A., Rongish, B. J., Little, C. D. and Hogan, B. (2008). The ECM moves during primitive streak formation—computation of ECM versus cellular motion. PLoS Biol. 6, e247.
54. Zhou, Y., Cashman, T. J., Nevis, K. R., Obregon, P., Carney, S. A., Liu, Y., Gu, A., Mosimann, C., Sondalle, S., Peterson, R. E. et al. (2011). Latent TGF-β binding protein 3 identifies a second heart field in zebrafish. Nature 474, 645-648.
55. Barthel, L. K. and Raymond, P. A. (1990). Improved method for obtaining 3-microns cryosections for immunocytochemistry. J Histochem Cytochem 38, 1383-1388.
56. Lin, F., Sepich, D. S., Chen, S., Topczewski, J., Yin, C., Solnica-Krezel, L. and Hamm, H. (2005). Essential roles of Ga12/13 signaling in distinct cell behaviors driving zebrafish convergence and extension gastrulation movements. J Cell Biol 169, 777-787.
57. Megason, S. G. (2009). In toto imaging of embryogenesis with confocal time-lapse microscopy. Meth Mol Biol 546, 317-332.
58. Thisse, C. and Thisse, B. (2008). High-resolution in situ hybridization to whole-mount zebrafish embryos. Nature Protocols 3, 59-69.
59. Trinh, L. A. and Stainier, D. Y. (2004). Fibronectin regulates epithelial organization during myocardial migration in zebrafish. Dev Cell 6, 371-382.
60. Ye, D. and Lin, F. (2013). S1pr2/Ga13 signaling controls myocardial migration by regulating endoderm convergence. Development 140, 789-799.