Rapid differential transport of Nodal and Lefty on sulfated proteoglycan-rich extracellular matrix regulates left-right asymmetry in Xenopus

Development

Volumn 138, Issue 3, 2011, Pages 475-485

  Marjoram, Lindsay ^a   Wright, Christopher ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

ECM; Left right asymmetry; Lefty; Nodal; Sulfated proteoglycans; Xenopus

Indexed keywords

CHONDROITIN SULFATE; LEFT RIGHT DETERMINATION FACTOR; PROTEIN NODAL; PROTEOGLYCAN;

ANIMAL EXPERIMENT; ARTICLE; AUTOREGULATION; CONTROLLED STUDY; EMBRYO; EXTRACELLULAR MATRIX; MESODERM; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; SOMITE; XENOPUS;

ANIMALS; BLOTTING, WESTERN; BODY PATTERNING; EMBRYO, NONMAMMALIAN; EXTRACELLULAR MATRIX; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; LEFT-RIGHT DETERMINATION FACTORS; MESODERM; NODAL PROTEIN; PROTEOGLYCANS; XENOPUS; XENOPUS PROTEINS;

EID: 78751505793     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.056010     Document Type: Article

References (57)

1. Aw, S. and Levin, M. (2009). Is left-right asymmetry a form of planar cell polarity? Development 136, 355-366.
2. Belenkaya, T. Y., Han, C., Yan, D., Opoka, R. J., Khodoun, M., Liu, H. and Lin, X. (2004). Drosophila Dpp morphogen movement is independent of dynaminmediated endocytosis but regulated by the glypican members of heparan sulfate proteoglycans. Cell 119, 231-244.
3. Bernfield, M., Gotte, M., Park, P. W., Reizes, O., Fitzgerald, M. L., Lincecum, J. and Zako, M. (1999). Functions of cell surface heparan sulfate proteoglycans. Annu. Rev. Biochem. 68, 729-777.
4. Bowes, J., Snyder, K., Segerdell, E., Jarabek, C., Azam, K., Zorn, A. and Vize, P. (2010). Xenbase: gene expression and improved integration. Nucleic Acids Res. 38, D607-D612.
5. Branford, W. W. and Yost, H. J. (2002). Lefty-dependent inhibition of Nodal-and Wnt-responsive organizer gene expression is essential for normal gastrulation. Curr. Biol. 12, 2136-2141.
6. Casey, B. (1998). Two rights make a wrong: human left-right malformations. Hum. Mol. Genet. 7, 1565-1571.
7. Casey, B. and Hackett, B. P. (2000). Left-right axis malformations in man and mouse. Curr. Opin. Genet. Dev. 10, 257-261.
8. Cha, Y., Takahashi, S. and Wright, C. (2006). Cooperative non-cell and cell autonomous regulation of Nodal gene expression and signaling by Lefty/Antivin and Brachyury in Xenopus. Dev. Biol. 290, 246-264.
9. Chen, Y. and Schier, A. F. (2001). The zebrafish Nodal signal Squint functions as a morphogen. Nature 411, 607-610.
10. Cui, Y., Hackenmiller, R., Berg, L., Jean, F., Nakayama, T., Thomas, G. and Christian, J. L. (2001). The activity and signaling range of mature BMP-4 is regulated by sequential cleavage at two sites within the prodomain of the precursor. Genes Dev. 15, 2797-2802.
11. Davis, N., Kurpios, N., Sun, X., Gros, J., Martin, J. and Tabin, C. (2008). The chirality of gut rotation derives from left-right asymmetric changes in the architecture of the dorsal mesentery. Dev. Cell 15, 134-145.
12. Deimling, S. J. and Drysdale, T. A. (2009). Retinoic acid regulates anteriorposterior patterning within the lateral plate mesoderm of Xenopus. Mech. Dev. 126, 913-923.
13. Dzamba, B. J., Jakab, K. R., Marsden, M., Schwartz, M. A. and DeSimone, D. W. (2009). Cadherin adhesion, tissue tension, and noncanonical Wnt signaling regulate fibronectin matrix organization. Dev. Cell 16, 421-432.
14. García-García, M. J. and Anderson, K. V. (2003). Essential role of glycosaminoglycans in Fgf signaling during mouse gastrulation. Cell 114, 727-737.
15. Guo, Z. and Wang, Z. (2009). The glypican Dally is required in the niche for the maintenance of germline stem cells and short-range BMP signaling in the Drosophila ovary. Development 136, 3627-3635.
16. Hamada, H. (2008). Breakthroughs and future challenges in left-right patterning. Dev. Growth Diff. 50, S71-S78.
17. Hecksher-Sørensen, J., Watson, R. P., Lettice, L. A., Serup, P., Eley, L., De Angelis, C., Ahlgren, U. and Hill, R. E. (2004). The splanchnic mesodermal plate directs spleen and pancreatic laterality, and is regulated by Bapx1/Nkx3.2. Development 131, 4665-4675.
18. Hemmati-Brivanlou, A. and Thomsen, G. H. (1995). Ventral mesodermal patterning in Xenopus embryos: expression patterns and activities of BMP-2 and BMP-4. Dev. Genet. 17, 78-89.
19. Horne-Badovinac, S., Rebagliati, M. and Stainier, D. Y. R. (2003). A cellular framework for gut-looping morphogenesis in zebrafish. Science 302, 662-665.
20. Itoh, K. and Sokol, S. Y. (1994). Heparan sulfate proteoglycans are required for mesoderm formation in Xenopus embryos. Development 120, 2703-2711.
21. Jing, X., Zhou, S., Wang, W. and Chen, Y. (2006). Mechanisms underlying longand short-range nodal signaling in Zebrafish. Mech. Dev. 123, 388-394.
22. Jones, C. M., Armes, N. and Smith, J. C. (1996). Signalling by TGF-beta family members: short-range effects of Xnr-2 and BMP-4 contrast with the long-range effects of activin. Curr. Biol. 6, 1468-1475.
23. Kramer, K. L. and Yost, H. J. (2002). Ectodermal syndecan-2 mediates left-right axis formation in migrating mesoderm as a cell-nonautonomous Vg1 cofactor. Dev. Cell 2, 115-124.
24. Kramer, K. L., Barnette, J. E. and Yost, H. J. (2002). PKCgamma regulates syndecan-2 inside-out signaling during Xenopus left-right development. Cell 111, 981-990.
25. Kucenas, S., Takada, N., Park, H.-C., Woodruff, E., Broadie, K. and Appel, B. (2008). CNS-derived glia ensheath peripheral nerves and mediate motor root development. Nat. Neurosci. 11, 143-151.
26. Le Good, J. A., Joubin, K., Giraldez, A. J., Ben-Haim, N., Beck, S., Chen, Y., Schier, A. F. and Constam, D. B. (2005). Nodal stability determines signaling range. Curr. Biol. 15, 31-36.
27. Lowe, L. A., Supp, D. M., Sampath, K., Yokoyama, T., Wright, C. V., Potter, S. S., Overbeek, P. and Kuehn, M. R. (1996). Conserved left-right asymmetry of nodal expression and alterations in murine situs inversus. Nature 381, 158-161.
28. Lugemwa, F. N. and Esko, J. D. (1991). Estradiol beta-D-xyloside, an efficient primer for heparan sulfate biosynthesis. J. Biol. Chem. 266, 6674-6677.
29. Massagué, J. (1998). TGF-beta signal transduction. Annu. Rev. Biochem. 67, 753-791.
30. McDowell, N., Zorn, A. M., Crease, D. J. and Gurdon, J. B. (1997). Activin has direct long-range signalling activity and can form a concentration gradient by diffusion. Curr. Biol. 7, 671-681.
31. Meier, S. (1979). Development of the chick embryo mesoblast. Formation of the embryonic axis and establishment of the metameric pattern. Dev. Biol. 73, 24-45.
32. Nakamura, T., Mine, N., Nakaguchi, E., Mochizuki, A., Yamamoto, M., Yashiro, K., Meno, C. and Hamada, H. (2006). Generation of robust left-right asymmetry in the mouse embryo requires a self-enhancement and lateralinhibition system. Dev. Cell 11, 495-504.
33. Nieuwkoop, P. D. and Faber, J. (1967). Normal Table of Xenopus laevis: A Systematical and Chronological Survey of the Development from the Fertilized Egg till the End of Metamorphosis. Amsterdam: North-Holland Publishing Company.
34. Ohi, Y. and Wright, C. (2007). Anteriorward shifting of asymmetric Xnr1 expression and contralateral communication in left-right specification in Xenopus. Dev. Biol. 301, 447-463.
35. Ohkawara, B., Iemura, S.-i., ten Dijke, P. and Ueno, N. (2002). Action range of BMP is defined by its N-terminal basic amino acid core. Curr. Biol. 12, 205-209.
36. Oki, S., Hashimoto, R., Okui, Y., Shen, M. M., Mekada, E., Otani, H., Saijoh, Y. and Hamada, H. (2007). Sulfated glycosaminoglycans are necessary for Nodal signal transmission from the node to the left lateral plate in the mouse embryo. Development 134, 3893-3904.
37. Pohl, B. S., Rössner, A. and Knöchel, W. (2005). The Fox gene family in Xenopus laevis: FoxI2, FoxM1 and FoxP1 in early development. Int. J. Dev. Biol. 49, 53-58.
38. Ramsdell, A. (2005). Left-right asymmetry and congenital cardiac defects: Getting to the heart of the matter in vertebrate left-right axis determination. Dev. Biol. 288, 1-20.
39. Raya, Á. and Belmonte, J. C. I. (2006). Left-right asymmetry in the vertebrate embryo: from early information to higher-level integration. Nat. Rev. Genet. 7, 283-293.
40. Sakuma, R., Ohnishi, Yi, Y.-i., Meno, C., Fujii, H., Juan, H., Takeuchi, J., Ogura, T., Li, E., Miyazono, K. and Hamada, H. (2002). Inhibition of Nodal signalling by Lefty mediated through interaction with common receptors and efficient diffusion. Genes Cells 7, 401-412.
41. Sampath, K., Cheng, A. M., Frisch, A. and Wright, C. V. (1997). Functional differences among Xenopus nodal-related genes in left-right axis determination. Development 124, 3293-3302.
42. Schier, A. F. (2003). Nodal signaling in vertebrate development. Annu. Rev. Cell Dev. Biol. 19, 589-621.
43. Scholpp, S. and Brand, M. (2004). Endocytosis controls spreading and effective signaling range of Fgf8 protein. Curr. Biol. 14, 1834-1841.
44. Schweickert, A., Weber, T., Beyer, T., Vick, P., Bogusch, S., Feistel, K. and Blum, M. (2007). Cilia-driven leftward flow determines laterality in Xenopus. Curr. Biol. 17, 60-66.
45. Sive, H. L., Grainger, R. M. and Harland, R. M. (2000). Early Development of Xenopus laevis: A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
46. Slack, J. M. and Tannahill, D. (1992). Mechanism of anteroposterior axis specification in vertebrates. Lessons from the amphibians. Development 114, 285-302.
47. Stevens, R. L. and Austen, K. F. (1982). Effect of p-nitrophenyl-beta-D- xyloside on proteoglycan and glycosaminoglycan biosynthesis in rat serosal mast cell cultures. J. Biol. Chem. 257, 253-259.
48. Tabin, C. (2006). The key to left-right asymmetry. Cell 127, 27-32.
49. Turing, A. M. (1990). The chemical basis of morphogenesis. 1953. Bull. Math. Biol. 52, 119-153.
50. Wallingford, J. B., Rowning, B. A., Vogeli, K. M., Rothbacher, U., Fraser, S. E. and Harland, R. M. (2000). Dishevelled controls cell polarity during Xenopus gastrulation. Nature 405, 81-85.
51. Wang, X. and Yost, H. J. (2008). Initiation and propagation of posterior to anterior (PA) waves in zebrafish left-right development. Dev. Dyn. 237, 3640-3647.
52. Westmoreland, J. J., Takahashi, S. and Wright, C. V. E. (2007). Xenopus Lefty requires proprotein cleavage but not N-linked glycosylation to inhibit Nodal signaling. Dev. Dyn. 236, 2050-2061.
53. Williams, P. H., Hagemann, A., González-Gaitán, M. and Smith, J. C. (2004). Visualizing long-range movement of the morphogen Xnr2 in the Xenopus embryo. Curr. Biol. 14, 1916-1923.
54. Wright, C. V. (2001). Mechanisms of left-right asymmetry: what's right and what's left? Dev. Cell 1, 179-186.
55. Yamamoto, M., Mine, N., Mochida, K., Sakai, Y., Saijoh, Y., Meno, C. and Hamada, H. (2003). Nodal signaling induces the midline barrier by activating Nodal expression in the lateral plate. Development 130, 1795-1804.
56. Yost, H. J. (1990). Inhibition of proteoglycan synthesis eliminates left-right asymmetry in Xenopus laevis cardiac looping. Development 110, 865-874.
57. Yu, S. R., Burkhardt, M., Nowak, M., Ries, J., Petrasek, Z., Scholpp, S., Schwille, P. and Brand, M. (2009). Fgf8 morphogen gradient forms by a source-sink mechanism with freely diffusing molecules. Nature 461, 533-536.