Wnt3a-mediated chemorepulsion controls movement patterns of cardiac progenitors and requires RhoA function

Development

Volumn 135, Issue 6, 2008, Pages 1029-1037

  Yue, Qiaoyun ^a   Wagstaff, Laura ^a   Yang, Xuesong ^b,c   Weijer, Cornelis ^b   Münsterberg, Andrea ^a  

^a UNIVERSITY OF EAST ANGLIA   (United Kingdom)

^b UNIVERSITY OF DUNDEE   (United Kingdom)

^c MEDICAL COLLEGE OF JINAN UNIVERSITY   (China)

Author keywords

Cardiac progenitors; Cell migration; Chemorepulsion; Chick; Wnt signalling

Indexed keywords

RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; WNT3A PROTEIN;

ANIMAL CELL; ARTICLE; CELL LINEAGE; CELL MIGRATION; CELL MOTION; CELL MUTANT; CELL SPECIFICITY; CONTROLLED STUDY; EMBRYO; EXPLANT; GASTRULA; HEART DEVELOPMENT; HEART MUSCLE CELL; IMMUNOHISTOCHEMISTRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; STEM CELL;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BASE SEQUENCE; CELL MOVEMENT; CHICK EMBRYO; DNA PRIMERS; EMBRYONIC STEM CELLS; GREEN FLUORESCENT PROTEINS; HEART; IN SITU HYBRIDIZATION; MICROSCOPY, VIDEO; MUTAGENESIS, SITE-DIRECTED; MYOBLASTS, CARDIAC; RHOA GTP-BINDING PROTEIN; SIGNAL TRANSDUCTION; WNT PROTEINS;

VERTEBRATA;

EID: 42549118076     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.015321     Document Type: Article

References (45)

1. Alvares, L. E., Schubert, F. R., Thorpe, C., Mootoosamy, R. C., Cheng, L., Parkyn, G., Lumsden, A. and Dietrich, S. (2003). Intrinsic, Hox-dependent cues determine the fate of skeletal muscle precursors. Dev. Cell 5, 379-390.
2. Brand, T. (2003). Heart development: molecular insights into cardiac specification and early morphogenesis. Dev. Biol. 258, 1-19.
3. Chapman, S. C., Collignon, J., Schoenwolf, G. C. and Lumsden, A. (2001). Improved method for chick whole-embryo culture using a filter paper carrier. Dev. Dyn. 220, 284-289.
4. Chapman, S. C., Schubert, F. R., Schoenwolf, G. C. and Lumsden, A. (2002). Analysis of spatial and temporal gene expression patterns in blastula and gastrula stage chick embryos. Dev. Biol. 245, 187-199.
5. Chuai, M., Zeng, W., Yang, X., Boychenko, V., Glazier, J. A. and Weijer, C. J. (2006). Cell movement during chick primitive streak formation. Dev Biol. 296, 137-149.
6. Cui, C., Yang, X., Chuai, M., Glazier, J. A. and Weijer, C. J. (2005). Analysis of tissue flow patterns during primitive streak formation in the chick embryo. Dev. Biol. 294, 37-47.
7. Dormann, D. and Weijer, C. J. (2003). Chemotactic cell movement during development. Curr. Opin. Genet. Dev. 13, 358-364.
8. Eisenberg, C. A. and Eisenberg, L. M. (1999). WNT11 promotes cardiac tissue formation of early mesoderm. Dev. Dyn. 216, 45-58.
9. Eisenberg, C. A., Gourdie, R. G. and Eisenberg, L. M. (1997). Wnt-11 is expressed in early avian mesoderm and required for the differentiation of the quail mesoderm cell line QCE-6. Development 124, 525-536.
10. Endo, Y., Wolf, V., Muraiso, K., Kamijo, K., Soon, L., Uren, A., Barshishat-Kupper, M. and Rubin, J. S. (2005). Wnt-3a-dependent cell motility involves RhoA activation and is specifically regulated by dishevelled-2. J. Biol. Chem. 280, 777-786.
11. Garcia-Martinez, V. and Schoenwolf, G. C. (1993). Primitive-streak origin of the cardiovascular system in avian embryos. Dev. Biol. 159, 706-719.
12. Hamburger, V. and Hamilton, H. L. (1951). A series of normal stages in the development of the chick embryo. J. Morphol. 88, 49-92.
13. Hatada, Y. and Stern, C. D. (1994). A fate map of the epiblast of the early chick embryo. Development 120, 2879-2889.
14. Hillier, L. W., Miller, W., Birney, E., Warren, W., Hardison, R. C., Ponting, C. P., Bork, P., Burt, D. W., Groenen, M. A., Delany, M. E. et al. (2004). Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution. Nature 432, 695-716.
15. Hoppler, S., Brown, J. D. and Moon, R. T. (1996). Expression of a dominant-negative Wnt blocks induction of MyoD in Xenopus embryos. Genes Dev. 10, 2805-2817.
16. Itasaki, N., Bel-Vialar, S. and Krumlauf, R. (1999). 'Shocking' developments in chick embryology: electroporation and in ovo gene expression. Nat. Cell Biol. 1, E203-E207.
17. Kaarbo, M., Crane, D. I. and Murrell, W. G. (2003). RhoA is highly up-regulated in the process of early heart development of the chick and important for normal embryogenesis. Dev. Dyn. 227, 35-47.
18. Kirby, M. L., Lawson, A., Stadt, H. A., Kumiski, D. H., Wallis, K. T., McCraney, E., Waldo, K. L., Li, Y. X. and Schoenwolf, G. C. (2003). Hensen's node gives rise to the ventral midline of the foregut: implications for organizing head and heart development. Dev. Biol. 253, 175-188.
19. Leslie, N. R., Yang, X., Downes, C. P. and Weijer, C. J. (2007). Ptdlns(3,4,5)P(3)-dependent and -independent roles for PTEN in the control of cell migration. Curr. Biol. 17, 115-125.
20. Lickert, H., Kutsch, S., Kanzler, B., Tamai, Y., Taketo, M. M. and Kemler, R. (2002). Formation of multiple hearts in mice following deletion of beta-catenin in the embryonic endoderm. Dev. Cell 3, 171-181.
21. Lyuksyutova, A. I., Lu, C. C., Milanesio, N., King, L. A., Guo, N., Wang, Y., Nathans, J., Tessier-Lavigne, M. and Zou, Y. (2003). Anterior-posterior guidance of commissural axons by Wnt-frizzled signaling. Science 302, 1984-1988.
22. 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.
23. Matsui, T., Raya, A., Kawakami, Y., Callol-Massot, C., Capdevila, J., Rodriguez-Esteban, C. and Izpisua Belmonte, J. C. (2005). Noncanonical Wnt signaling regulates midline convergence of organ primordia during zebrafish development. Genes Dev. 19, 164-175.
24. Momose, T., Tonegawa, A., Takeuchi, J., Ogawa, H., Umensono, K. and Yasuda, K. (1999). Efficient targeting of gene expression in chick embryos by microelectroporation. Dev. Growth Differ. 41, 335-344.
25. Münsterberg, A. E., Kitajewski, J., Bumcrot D. A., McMahon, A. P. and Lassar, A. B. (1995). Combinatorial signaling by Sonic hedgehog and Wnt family members induces myogenic bHLH gene expression in the somite. Genes Dev. 9, 2911-2922.
26. Naito, A. T., Shiojima, L., Akazawa, H., Hidaka, K., Morisaki, T., Kikuchi, A. and Komuro, I. (2006). Developmental stage-specific biphasic roles of Wnt/beta-catenin signaling in cardiomyogenesis and hematopoiesis. Proc. Natl. Acad. Sci. USA 103, 19812-19817.
27. Nakamura, T., Sano, M., Songyang, Z. and Schneider, M. D. (2003). A Wnt- and beta -catenin-dependent pathway for mammalian cardiac myogenesis. Proc. Natl. Acad. Sci. USA 100, 5834-5839.
28. Niswander, L., Jeffrey, S., Martin, G. R. and Tickle, C. (1994). A positive feedback loop coordinates growth and patterning in the vertebrate limb. Nature 371, 609-612.
29. Ridley, A. J. and Hall, A. (1992). The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors. Cell 70, 389-399.
30. Rosenquist, G. C. (1970). Location and movements of cardiogenic cells in the chick embryo: the heart-forming portion of the primitive streak. Dev. Biol. 22, 461-475.
31. Schmidt, M., Tanaka, M. and Munsterberg, A. (2000). Expression of (beta)-catenin in the developing chick myotome is regulated by myogenic signals. Development 127, 4105-4113.
32. Schmidt, M., Patterson, M., Farrell, E. and Münsterberg, A. (2004). Dynamic expression of Lef/Tcf family members and β-catenin during chick gastrulation, neurulation and early limb development. Dev. Dyn. 229, 703-707.
33. Schmitt, A. M., Shi, J., Wolf, A. M., Lu, C. C., King, L. A. and Zou, Y. (2006). Wnt-Ryk signalling mediates medial-lateral retinotectal topographic mapping. Nature 439, 31-37.
34. Schneider, V. A. and Mercola, M. (2001). Wnt antagonism initiates cardiogenesis in Xenopus laevis. Genes Dev. 15, 304-315.
35. Schultheiss, T. M., Burch, J. B. and Lassar, A. B. (1997). A role for bone morphogenetic proteins in the induction of cardiac myogenesis. Genes Dev. 11, 451-462.
36. Skromne, I. and Stern, C. D. (2001). Interactions between Wnt and Vg1 signalling pathways initiate primitive streak formation in the chick embryo. Development 128, 2915-2927.
37. Stalsberg, H. and DeHaan, R. L. (1969). The precardiac areas and formation of the tubular heart in the chick embryo. Dev. Biol. 19, 128-159.
38. Tzahor, E. and Lassar, A. B. (2001). Wnt signals from the neural tube block ectopic cardiogenesis. Genes Dev. 15, 255-260.
39. 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.
40. Vijayaragavan, K. and Bhatia, M. (2007). Early cardiac development: a Wnt beat away. Proc. Natl. Acad. Sci. USA 104, 9549-9550.
41. Wei, L., Roberts, W., Wang, L., Yamada, M., Zhang, S., Zhao, Z., Rivkees, S. A., Schwartz, R. J. and Imanaka-Yoshida, K. (2001). Rho kinases play an obligatory role in vertebrate embryonic organogenesis. Development 128, 2953-2962.
42. Yang, X., Dormann, D., Munsterberg, A. E. and Weijer, C. J. (2002). Cell movement patterns during gastrulation in the chick are controlled by positive and negative chemotaxis mediated by FGF4 and FGF8. Dev. Cell 3, 425-437.
43. Yoshikawa, S., McKinnon, R. D., Kokel, M. and Thomas, J. B. (2003). Wnt-mediated axon guidance via the Drosophila Derailed receptor. Nature 422, 583-588.
44. Yutzey, K. E. and Kirby, M. L. (2002). Wherefore heart thou? Embryonic origins of cardiogenic mesoderm. Dev. Dyn. 223, 307-320.
45. Zamir, E. A., Czirok, A., Cui, C., Little, C. D. and Rongish, B. J. (2006). Mesodermal cell displacements during avian gastrulation are due to both individual cell-autonomous and convective tissue movements. Proc. Natl. Acad. Sci. USA 103, 19806-19811.