Interpretation of a BMP activity gradient in Drosophila embryos depends on synergistic signaling by two type I receptors, SAX and TKV

Cell

Volumn 95, Issue 4, 1998, Pages 495-506

  Nguyen, Minh ^a   Park, Sangbin ^a   Marqués, Guillermo ^b   Arora, Kavita ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b INSTITUTO CAJAL   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN;

ARTICLE; DROSOPHILA; EMBRYO; EMBRYO DEVELOPMENT; EMBRYO PATTERN FORMATION; GENE EXPRESSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; SIGNAL TRANSDUCTION;

HEXAPODA;

EID: 0032514852     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0092-8674(00)81617-7     Document Type: Article

References (48)

1. Aono, A., Hazama, M., Notoya, K., Taketomi, S., Yamasaki, H., Tsukuda, R., Sasaki, S., and Fujisawa, Y. (1995). Potent ectopic bone-inducing activity of bone morphogenetic protein-4/7 heterodimer. Biochem. Biophys. Res. Commun. 210, 670-677.
2. Arora, K., and Nüsslein-Volhard, C. (1992). Altered mitotic domains reveal fate map changes in Drosophila embryos mutant for zygotic dorsoventral patterning genes. Development 114, 1003-1024.
3. Arora, K., Levine, M., and O'Connor, M. (1994). The screw gene encodes a ubiquitously expressed member of the TGFβ family required for specification of dorsal cell fates in the Drosophila embryo. Genes Dev. 8, 2588-2601.
4. Biehs, B., François, V., and Bier, E. (1996). The Drosophila short gastrulation gene prevents Dpp from autoactivating and suppressing neurogenesis in the neuroectoderm. Genes Dev. 10, 2922-2934.
5. Brand, A.H., and Perrimon, N. (1993). Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118, 401-415.
6. Brummel, T.J., Twombly, V., Marqués, G., Wrana, J.L., Newfeld, S.J., Attisano, L., Massagué, J., O'Connor, M.B., and Gelbart, W.M. (1994). Characterization and relationship of Dpp receptors encoded by the saxophone and thick veins genes in Drosophila. Cell 78, 251-261.
7. Burke, R., and Basler, K. (1996). Dpp receptors are autonomously required for cell proliferation in the entire developing Drosophila wing. Development 122, 2261-2269.
8. Derynck, R., and Feng, X.-H. (1997). TGFβ receptor signaling. Biochim. Biophys. Acta 1333, F105-F150.
9. Ferguson, E.L., and Anderson, K.V. (1992a). decapentaplegic acts as a morphogen to organize dorsal-ventral pattern in the Drosophila embryo. Cell 71, 451-461.
10. Ferguson, E.L., and Anderson, K.V. (1992b). Localized enhancement and repression of the activity of the TGFβ family member, decapentaplegic, is necessary for dorsal-ventral pattern formation in the Drosophila embryo. Development 114, 583-597.
11. François, V., Solloway, M., O'Neill, J.W., Emery, J., and Bier, E. (1994). Dorsal-ventral patterning of the Drosophila embryo depends on a putative negative growth factor encoded by the short gastrulation gene. Genes Dev. 8, 2602-2616.
12. Gelbart, W.M. (1989). The decapentaplegic gene: a TGFβ homolog controlling pattern formation in Drosophila. Development 107 (Suppl.), 65-74.
13. Haerry, T.E., Khalsa, O., O'Connor, M.B., and Wharton, K.A. (1998). Synergistic signaling by two BMP ligands through the SAX and TKV receptors controls wing growth and patterning in Drosophila. Development 125, 3977-3987.
14. Heldin, C.-H., Miyazono, K., and ten Dijke, P. (1997). TGFβ signaling from cell membrane to nucleus through SMAD proteins. Nature 390, 465-471.
15. Hogan, B.L. (1996). Bone morphogenetic proteins: multifunctional regulators of vertebrate development. Genes Dev. 10, 1580-1594.
16. Holley, S.A., Jackson, P.D., Sasai, Y., Lu, B., DeRobertis, E.M., Hoffman, F.M., and Ferguson, E.L. (1995). A conserved system for dorsal-ventral patterning in insects and vertebrates involving sog and chordin. Nature 376, 249-253.
17. Holley, S.A., Neul, J.L., Attisano, L., Wrana, J.L., Sasai, Y., O'Connor, M.B., De Robertis, E.M., and Ferguson, E.L. (1996). The Xenopus dorsalizing factor noggin ventralizes Drosophila embryos by preventing DPP from activating its receptor. Cell 86, 607-617.
18. Hoodless, P.A., Haerry, T., Abdollah, S., Stapleton, M., O'Connor, M.B., Attisano, L., and Wrana, J.L. (1996). MADR1, a MAD-related protein that functions in BMP2 signaling pathways. Cell 85, 489-500.
19. Irish, V.F., and Gelbart, W.M. (1987). The decapentaplegic gene is required for dorsal-ventral patterning of the Drosophila embryo. Genes Dev. 1, 868-879.
20. Jiang, J., and Levine, M. (1993). Binding affinities and cooperative interactions with bHLH activators delimit threshold responses to the dorsal gradient morphogen. Cell 72, 741-752.
21. Kretzschmar, M., and Massagué, J. (1998). SMADs: mediators and regulators of TGFβ signaling. Curr. Opin. Genet. Dev. 8, 103-111.
22. Lawrence, P.A., and Struhl, G. (1996). Morphogens, compartments, and pattern: lessons from Drosophila? Cell 85, 951-961.
23. Lecuit, T., Brook, W.J., Ng, M., Calleja, M., Sun, H., and Cohen, S.M. (1996). Two distinct mechanisms for long-range patterning by Decapentaplegic in the Drosophila wing. Nature 381, 1387-1393.
24. Letsou, A., Arora, K., Wrana, J.L., Simin, K., Twombly, V., Jamal, J., Staehling-Hampton, K., Hoffman, F.M., Gelbart, W.M., Massagué, J., and O'Connor, M.B. (1995). Drosophila Dpp signaling is mediated by the punt gene product: a dual ligand binding type II receptor of the TGFβ receptor family. Cell 80, 899-908.
25. Marqués, G., Musacchio, M., Shimell, M.J., Wünnenberg-Stapleton, K., Cho, K.W.Y., and O'Connor, M.B. (1997). Production of a DPP activity gradient in the early Drosophila embryo through the opposing actions of the SOG and TLD proteins. Cell 91, 417-426.
26. Massagué, J. (1990). The transforming growth factor-β family. Annu. Rev. Cell Biol. 6, 597-641.
27. Nellen, D., Affolter, M., and Basler, K. (1994). Receptor serine/threonine kinases implicated in the control of Drosophila body pattern by decapentaplegic. Cell 78, 225-237.
28. Nellen, D., Burke, R., Struhl, G., and Basler, K. (1996). Direct and long-range action of a DPP morphogen gradient. Cell 85, 357-368.
29. Neul, J.L., and Ferguson, E.L. (1998). Spatially restricted activation of the SAX receptor by SCW modulates DPP/TKV signaling in Drosophila dorsal-ventral patterning. Cell 95, this issue, 483-494.
30. Neumann, C., and Cohen, S. (1997). Morphogens and pattern formation. Bioessays 19, 721-729.
31. Newfeld, S.J., Mehra, A., Singer, M.A., Wrana, J.L., Attisano, L., and Gelbart, W.M. (1997). Mothers against dpp participates in a DPP/ TGF-beta responsive serine-threonine kinase signal transduction cascade. Development 124, 3167-3176.
32. Padgett, R.W., Johnston, R.D.S., and Gelbart, W.M. (1987). A transcript from a Drosophila pattern gene predicts a protein homologous to the transforming growth factor-β family. Nature 325, 81-84.
33. Park, S., and Lim, J.K. (1995). A microinjection technique for ethanol-treated eggs and a mating scheme for detection of germ line transformants. Dros. Info. Senv. 76, 197-199.
34. Penton, A., Chen, Y., Staehling-Hampton, K., Wrana, J.L., Attisano, L., Szidonya, J., Cassill, J.A., Massagué, J., and Hoffmann, F.M. (1994). Identification of two bone morphogenetic protein type I receptors in Drosophila and evidence that Brk25D is a decapentaplegic receptor. Cell 78, 239-250.
35. Piccolo, S., Agius, E., Lu, B., Goodman, S., Dale, L., and De Robertis, E.M. (1997). Cleavage of Chordin by Xolloid metalloprotease suggests a role for proteolytic processing in the regulation of Spemann organizer activity. Cell 91, 407-416.
36. Raftery, L.A., Twombly, V., Wharton, K., and Gelbart, W.M. (1995). Genetic screens to identify elements of the decapentaplegic signaling pathway in Drosophila. Genetics 139, 241-254.
37. Ray, R.P., Arora, K., Nüsslein, V.C., and Gelbart, W.M. (1991). The control of cell fate along the dorsal-ventral axis of the Drosophila embryo. Development 113, 35-54.
38. Ruberte, E., Marty, T., Nellen, D., Affolter, M., and Basler, K. (1995). An absolute requirement for both the type II and type I receptors, punt and thick veins, for Dpp signaling in vivo. Cell 80, 889-897.
39. Sasai, Y., Lu, B., Steinbeisser, H., and De Robertis, E.M. (1995). Regulation of neural induction by the Chd and BMP4 antagonistic patterning signals in Xenopus. Nature 376, 333-336.
40. Schmidt, J., François, V., Bier, E., and Kimelman, D. (1995). Drosophila short gastrulation induces an ectopic axis in Xenopus: evidence for conserved mechanisms of dorsal-ventral patterning. Development 121, 4319-4328.
41. Shimell, M.J., Ferguson, E.L., Childs, S.R., and O'Connor, M.B. (1991). The Drosophila dorsal-ventral patterning gene tolloid is related to human bone morphogenetic protein 1. Cell 67, 469-481.
42. Singer, M.A., Penton, A., Twombly, V., Hoffmann, F.M., and Gelbart, W.M. (1997). Signaling through both type I Dpp receptors is required for anterior-posterior patterning of the entire Drosophila wing. Development 124, 79-89.
43. St. Johnston, R.D., and Gelbart, W.M. (1987). decapentaplegic transcripts are localized along the dorsal-ventral axis of the Drosophila embryo. EMBO J. 6, 2785-2791.
44. Suzuki, A., Kaneko, E., Maeda, J., and Ueno, N. (1997). Mesoderm induction by BMP4 and -7 heterodimers. Biochem. Biophys. Res. Commun. 232, 153-156.
45. Terracol, R., and Lengyel, J.A. (1994). The thick veins gene of Drosophila is required for dorsoventral polarity of the embryo. Genetics 138, 165-178.
46. Wharton, K.A., Ray, R.P., and Gelbart, W.M. (1993). An activity gradient of decapentaplegic is necessary for the specification of dorsal pattern elements in the Drosophila embryo. Development 117, 807-822.
47. Xie, T., Finelli, A.L., and Padgett, R.W. (1994). The Drosophila saxophone gene: a serine-threonine kinase receptor of the TGFβ super-family. Science 263, 1756-1759.
48. Yu, K., Sturtevant, M.A., Biehs, B., François, V., Padgett, R.W., Blackman, R.K., and Bier, E. (1996). The Drosophila decapentaplegic and short gastrulation genes function antagonistically during adult wing vein development. Development 122, 4033-4044.