Transplacental delivery of the Wnt antagonist Frzb1 inhibits development of caudal paraxial mesoderm and skeletal myogenesis in mouse embryos

Development

Volumn 126, Issue 19, 1999, Pages 4247-4255

  Borello, Ugo ^a   Coletta, Marcello ^a   Tajbakhsh, Shahragim ^b   Leyns, Luc ^c   De Robertis, Eddy M ^c   Buckingham, Margaret ^b   Cossu, Giulio ^a  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b INSTITUT PASTEUR   (France)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Frzb1; Myf5 activation; MyoD; Myogenic induction; Wnt

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DEATH; CONTROLLED STUDY; DEVELOPMENTAL GENETICS; EMBRYO; EMBRYO DEVELOPMENT; EXPLANT; EXPRESSION VECTOR; FETOMATERNAL TRANSFUSION; MESODERM; MOUSE; MUSCLE DEVELOPMENT; NEURAL TUBE; NONHUMAN; NOTOCHORD; PLACENTAL TRANSFER; PRIORITY JOURNAL; SKELETAL MUSCLE; SOMITE;

ANIMALS; BONE AND BONES; CARRIER PROTEINS; CELL DIFFERENTIATION; DNA-BINDING PROTEINS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLYCOPROTEINS; IN SITU HYBRIDIZATION; MESODERM; MICE; MUSCLE PROTEINS; MYOD PROTEIN; MYOGENIC REGULATORY FACTOR 5; PLACENTA; PREGNANCY; PROTEINS; PROTO-ONCOGENE PROTEINS; SOMITES; TRANS-ACTIVATORS; TRANSFECTION; WNT PROTEINS; ZEBRAFISH PROTEINS;

EID: 0032710482     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (48)

1. Acampora, D., Avantaggiato, V., Tuorto, F., Briata, P., Corte, G. and Simeone, A. (1998). Visceral endoderm-restricted translation of Otx1 mediates recovery of Otx2 requirements for specification of anterior neural plate and normal gastrulation. Development 125, 5091-5104.
2. Bhanot, P., Brink, M., Samos, C. H., Hsieh, J. C., Wang, Y., Macke, J. P., Andrew, D., Nathans, J. and Nusse, R. (1996). A new member of the frizzled family from Drosophila function as a Wingless receptor. Nature 382, 225-230.
3. Borycki, A. G., Mendham, L. and Emerson, C. P. Jr (1998). Control of somite patterning by Sonic hedgehog and its downstream signal response genes. Development 125, 777-790.
4. Borycki, A. G., Brunk, B., Tajbakhsh, S., Buckingham, M. and Emerson, C. P. Jr (1999). Sonic hedgehog controls epaxial muscle determination through Myf5 activation. Development 126, 4053-4063.
5. Boussif, O., Lezoualc'h, F., Zanta, M. A., Mergny, M. D., Scherman, D., Demeneix, B. and Behr, J. P. (1995). A versatile vector for gene and oligonucleotide transfer into cells in culture and in vivo: polyethylenimine. Proc. Natl. Acad. Sci. USA 92, 7297-7301.
6. Candia, A. F., Hu, J., Crosby, J., Lalley, P. A., Noden, D., Nadeau, J. H. and Wright, C. V. (1992). Mox-1 and Mox-2 define a novel homeobox gene subfamily and are differentially expressed during early mesodermal patterning in mouse embryos. Development 116, 1123-1136.
7. Capdevila, J., Tabin, C. and Johnson, R. L. (1998). Control of dorsoventral somite patterning by Wnt-1 and beta-catenin. Dev. Biol. 193, 182-194.
8. Christian, J. L. and Moon, R. T. (1993). Interactions between Xwnt-8 and Spemann organizer signaling pathways generate dorsoventral pattern in the embryonic mesoderm of Xenopus. Genes Dev. 7, 13-28.
9. Cossu, G., Kelly, R., Di Donna, S., Vivarelli, E. and Buckingham, M. (1995). Myoblast differentiation during mammalian somitogenesis is dependent upon a community effect. Proc. Natl. Acad. Sci. USA 92, 2254-2258.
10. Cossu, G., Kelly, R., Tajbakhsh, S., Di Donna, S., Vivarelli, E. and Buckingham, M. (1996). Activation of different myogenic pathways: Myf-5 is induced by the neural tube and MyoD by the dorsal ectoderm in mouse paraxial mesoderm. Development 122, 429-437.
11. Dailey, L. and Basilico, C. (1985). Sequences in the polyomavirus DNA regulatory region involved in viral DNA replication and early gene expression. J. Virol. 54, 739-749.
12. Fan, C. M. and Tessier-Lavigne, M. (1994). Patterning of mammalian somites by surface ectoderm and notochord: evidence for sclerotome induction by a hedgehog homolog. Cell 79, 1175-1186.
13. Fleischman, R. A. and Mintz, B. (1979). Prevention of genetic anemias in mice by microinjection of normal hematopoietic stem cells into the fetal placenta. Proc. Natl. Acad. Sci. USA 76, 5736-5740.
14. Goulding, M. D., Chalepakis, G., Deutsch, U., Erselius, J. R. and Gruss, P. (1991). Pax-3, a novel murine DNA binding protein expressed during early neurogenesis. EMBO J. 10, 1135-1147.
15. Graham, A., Heyman, I. and Lumsden, A. (1993). Even-numbered rhombomeres control the apoptotic elimination of neural crest cells from odd-numbered rhombomeres in the chick hindbrain. Development 119, 233-245.
16. Hirsinger, E., Duprez, D., Jouve, C., Malapert, P., Cooke, J. and Pourquie, O. (1997). Noggin acts downstream of Wnt and Sonic Hedgehog to antagonize BMP4 in avian somite patterning. Development 124, 4605-4614.
17. Hoang, B. H., Thomas, J. T., Abdul-Karim, F. W., Correia, K. M., Conlon, R. A., Luyten F. P. and Ballock, R. T. (1998). Expression pattern of two Frizzled-related genes, Frzb1 and Sfrp-1, during mouse embryogenesis suggests a role for modulating action of Wnt family members. Dev. Dyn. 212, 364-372.
18. 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.
19. Houzelstein, D. and Tajbakhsh, S. (1998). Increased in situ hybridisation sensitivity using non-radioactive probes after staining for β-galactosidase activity. Technical Tips online T01600.
20. Ikeya, M., Lee, S. M., Johnson, J. E., McMahon, A. P. and Takada, S. (1997). Wnt signalling required for expansion of neural crest and CNS progenitors. Nature 389, 966-970.
21. Ikeya, M. and Takada, S. (1998). Wnt signaling from the dorsal neural tube is required for the formation of the mediam dermomyotome. Development 125, 4969-4976.
22. Jones, C. M., Lyons, K. M. and Hogan B. L. (1991). Involvement of Bone Morphogenetic Protein-4 (BMP-4) and Vgr-1 in morphogenesis and neurogenesis in the mouse. Development 111, 531-542.
23. Koishi, K., Zhang, M., McLennan, I. S. and Harris, A. J. (1995). MyoD protein accumulates in satellite cells and is neurally regulated in regenerating myotubes and skeletal muscle fibers. Dev. Dyn. 202, 244-254.
24. Labarca, C. and Paigen, K. (1980). A simple, rapid and sensitive DNA assay procedure. Anal. Biochem. 102, 344-352.
25. Leimeister, C., Bach A. and Gessler, M. (1998). Developmental expression patterns of mouse sFRP genes encoding members of the secreted frizzled related protein family. Mech. Dev. 75, 29-42.
26. Leyns, L., Bouwmeester, T., Kim, S. H., Piccolo, S. and De Robertis, E. M. (1997). Frzb1 is a secreted antagonist of Wnt signaling expressed in the Spemann organizer. Cell 88, 747-756.
27. Liu, A., Joiner, A. L. and Turnbull, D. H. (1998). Alteration of limb and brain patterning in early mouse embryos by ultrasound-guided injection of Shh-expressing cells. Mech. Dev. 75, 107-115.
28. Marcelle, C., Stark, M. R. and Bronner-Fraser, M. (1997). Coordinate actions of BMPs, Wnts, Shh and noggin mediate patterning of the dorsal somite. Development 124, 3955-3963.
29. Maroto, M., Reshef, R., Münsterberg, A. E., Koester, S., Goulding, M. and Lassar, A. B. (1997). Ectopic Pax-3 activates MyoD and Myf-5 expression in embryonic mesoderm and neural tissue. Cell 89, 139-148.
30. Mayr, T., Deutsch, U., Kühl, M., Drexler, H. C., Lottspeich, F., Deutzmann, R., Wedlich, D. and Risau, W. (1997). Fritz: a secreted frizzled-related protein that inhibits Wnt activity. Mech. Dev. 63, 109-125.
31. McMahon, J. A., Takada, S., Zimmerman, L. B., Fan, C. M., Harland, R. M. and McMahon, A. P. (1998). Noggin-mediated antagonism of BMP signaling is required for growth and patterning of the neural tube and somite. Genes Dev. 12, 1438-1452.
32. Melkonyan, H. S., Chang, W. C., Shapiro, J. P., Mahadevappa, M., Fitzpatrick, P. A., Kiefer, M. C., Tomei, L. D. and Umansky, S. R. (1997). SARPs: a family of secreted apoptosis-related proteins. Proc. Natl. Acad. Sci. USA 94, 13636-13641.
33. 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.
34. Ordahl, C. P. (1993). Myogenic lineages within the developing somite. In Molecular Basis of Morphogenesis (ed. M. Bernfield), pp. 165-176. New York: Wiley-Liss.
35. Pourquie, O., Fan, C. M., Coltey, M., Hirsinger, E., Watanabe, Y., Breant, C., Francis-West, P., Brickell, P., Tessier-Lavigne, M. and Le Douarin, N. M. (1996). Lateral and axial signals involved in avian somite patterning: a role for BMP4. Cell 84, 461-471.
36. Salvatori, G., Lattanzi, L., Coletta, M., Aguanno, S., Vivarelli, E., Kelly, R., Ferrari, G., Harris, A. J., Mavilio, F., Molinaro, M. and Cossu, G. (1995). Myogenic conversion of mammalian fibroblasts induced by differentiating muscle cells. J. Cell Sci. 108, 2733-2739.
37. Schmidt, C., Christ, B., Patel, K. and Brand-Saberi, B. (1998). Experimental induction of BMP-4 expression leads to apoptosis in the paraxial and lateral plate mesoderm. Dev. Biol. 202, 253-263.
38. Sokol, S. Y. (1996). Analysis of Dishevelled signaling pathways during Xenopus development. Curr. Biol. 6, 1456-1467.
39. Stern, H. M., Brown, A. M. and Hauschka, S. D. (1995). Myogenesis in paraxial mesoderm: preferential induction by dorsal neural tube and by cells expressing Wnt-1. Development 121, 3675-3686.
40. Tajbakhsh, S., Vivarelli, E., Cusella-De Angelis, G., Rocancourt, D., Buckingham, M. and Cossu, G. (1994). A population of myogenic cells derived from the mouse neural tube. Neuron 13, 813-821.
41. Tajbakhsh, S., Rocancourt, D. and Buckingham, M. (1996). Muscle progenitor cells failing to respond to positional cues adopt non-myogenic fates in Myf-5 null mice. Nature 384, 266-270.
42. Tajbakhsh, S., Rocancourt, D., Cossu, G. and Buckingham, M. (1997) Redefining the genetic hierarchies controlling skeletal myogenesis: Pax3 and Myf-5 act upstream of MyoD. Cell 89, 127-138.
43. Tajbakhsh, S., Borello, U., Vivarelli, E., Kelly, R., Papkoff, J., Duprez, D., Buckingham, M. and Cossu G. (1998). Differential activation of Myf5 and MyoD by different Wnts in explants of mouse paraxial mesoderm and the later activation of myogenesis in the absence of Myf5. Development 125, 4155-4162
44. Takada, S., Stark, K. L., Shea, M. J., Vassileva, G., McMahon, J. A. and McMahon, A. P. (1994). Wnt-3a regulates somite and tailbud formation in the mouse embryo. Genes Dev. 8, 174-189.
45. Wang, S., Krinks, M., Lin, K., Luyten, F. P. and Moos, M. Jr (1997). Frzb, a secreted protein expressed in the Spemann organizer, binds and inhibits Wnt-8. Cell 88, 757-766.
46. Wodarz, A. and Nusse, R. (1998). Mechanisms of Wnt signaling in development. Ann. Rev. Cell. Dev. Biol. 14, 59-88.
47. Yamaguchi, T. P., Bradley, A., McMahon, A. P. and Jones, S. (1999). A Wnt5a pathway underlies outgrowth of multiple structures in the vertebrate embryo. Development 126, 1211-1223.
48. Zimmerman, L. B., De Jesus-Escobar, J. M. and Harland, R. M. (1996) The Spemann organizer signal noggin binds and inactivates bone morphogenetic protein 4. Cell 86, 599-606.