Synergistic signaling by two BMP ligands through the SAX and TKV receptors controls wing growth and patterning in Drosophila

Development

Volumn 125, Issue 20, 1998, Pages 3977-3987

  Haerry, Theodor E ^a,b   Khalsa, Ongkar ^c   O'Connor, Michael B ^a,b   Wharton, Kristi A ^c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

^c BROWN UNIVERSITY   (United States)

Author keywords

Activated receptor; BMP; Dominant negative receptor; Morphogen

Indexed keywords

BONE MORPHOGENETIC PROTEIN; LIGAND; MORPHOGEN; RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; DEVELOPMENTAL GENETICS; DROSOPHILA; EMBRYO; EMBRYO PATTERN FORMATION; FORELIMB; IMAGINAL DISC; LIMB DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ANIMALS; BODY PATTERNING; DIFFUSION; DNA-BINDING PROTEINS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, INSECT; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; INSECT PROTEINS; MODELS, BIOLOGICAL; NERVE TISSUE PROTEINS; PHENOTYPE; PROTEIN-SERINE-THREONINE KINASES; RECEPTORS, CELL SURFACE; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; SEQUENCE DELETION; SIGNAL TRANSDUCTION; T-BOX DOMAIN PROTEINS; TRANSFORMING GROWTH FACTOR BETA; WING;

ANIMALIA; HEXAPODA;

EID: 0031766027     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (42)

1. Arora, K., Levine, M. and O'Connor, M. (1994). The screw gene encodes a ubiquitously expressed member of the TGF-β family required for specification of dorsal cell fates in the Drosophila embryo. Genes Dev. 8, 2588-2601.
2. 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.
3. Brummel, T. J., Twombly, V., Marques, G., Wrana, J. L., Newfeld, S. J., Attisano, L., Massague, 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.
4. Burke, R. and Basler, K. (1996). Dpp receptors are autonomously required for cell proliferation in the entire developing Drosophila wing. Development 122, 2261-2269.
5. Casanova, J. and Struhl, G. (1993). The torso receptor localizes as well as transduces the spatial signal specifying terminal body pattern in Drosophila. Nature 362, 152-155.
6. Chen, X., Weisberg, E., Fridmacher, V., Watanabe, M., Naco, G. and Whitman, M. (1997). Smad4 and FAST-1 in the assembly of activin- responsive factor. Nature 389, 85-89.
7. Chen, Y. and Struhl, G. (1996), Dual roles for patched in sequestering and transducing Hedgehog. Cell 87, 553-563.
8. Chen, Y., Riese, M. J., Killinger, M. A. and Hoffmann, F. M. (1998). A genetic screen for modifiers of Drosophila decapentaplegic signaling identifies mutations in punt, Mothers against dpp and the BMP-7 homologue, 60A. Development 125, 1759-1768
9. Cornell, R. A. and Kimelmanm, D. (1994). Combinatorial signaling in development. BioEssays 16, 577-581.
10. de Celis, J. F. (1997). Expression and function of decapentaplegic and thick veins during the differentiation of the veins in the Drosophila wing. Development 124, 1007-1018.
11. de Celis, J. F., Barrio, R. and Kafatos, F. C. (1996). A gene complex acting downstream of dpp in Drosophila wing morphogenesis. Nature 381, 421-424.
12. Doctor, J. S., Jackson, P. D., Rashka, K. E., Visalli, M. and Hoffmann, F. M. (1992). Sequence, biochemical characterization and developmental expression of a new member of the TGF-beta superfamily in Drosophila melanogaster. Dev. Biol. 151, 491-505.
13. Fainsod, A., Deissler, K., Yelin, R., Marom, K., Epstein, M., Pillemer, G., Steinbeisser, H. and Blum, M. (1997). The dorsalizing and neural inducing gene follistatin is an antagonist of BMP-4. Mech. Dev. 63, 39-50.
14. Ferguson, E. L. and Anderson, K. V. (1992). Decapentaplegic acts as a morphogen to organize dorsal-ventral pattern in the Drosophila embryo. Cell 71, 451-461.
15. Gelbart, W. M. (1989). The decapentaplegic gene: A TGF-β homolog controlling pattern formation in Drosophila. Development 107 (supplement), 65-74.
16. Grimm, S. and Pflugfelder, G. O. (1996). Control of the gene optomotor- blind in Drosophila wing development by decapentaplegic and wingless. Science 211, 1601-1604.
17. Haerry, T. E., Heslip, T. R., Marsh, J. L. and O'Conn or, M. B. (1997). Defects in glucuronate biosynthesis disrupt Wingless signaling in Drosophila. Development 124, 3055-3064.
18. Heldin, C. H., Miyazono, K. and ten Dijke, P. (1997). TGF-beta signalling from cell membrane to nucleus through SMAD proteins. Nature 390, 465-471.
19. Hogan, B. L. (1996). Bdflte morphogenetic proteins: multifunctional regulators of vertebrate development. Genes Dev. 10, 1580-1594.
20. Jackson, S., Nakato, H., Suglura, M., Jannuzi, A., Oakes, R., Kaluza, V., Golden, C. and Selleck, S. (1997). dally, a Drosophila glypican, controls cellular responses to the TGF-β-related morphogen, Dpp. Development 124 (supplement), 4113-4120.
21. Khalsa, O., Yoon, J.-W., Torres-Schumann, S. and Wharton, K. A. (1998). TGF-β/BMP superfamily members, Gbb-60A and Dpp signal in a synergistic manner to pattern the Drosophila wing. Development (in press).
22. Kim, J., Johnson, K., Chen, H. J., Carroll, S. and Laughon, A. (1997). Drosophila Mad binds to DNA and directly mediates activation of vestigial by Decapentaplegic. Nature 388, 304-308.
23. Kingsley, D. M. (1994). The TGF-β superfamily: new members, new receptors and new genetic tests of function in different organisms. Genes Dev. 8, 133-146.
24. Kretzschmar, M., Liu, F., Hata, A., Doody, J. and Massague, J. (1997). The TGF-beta family mediator Smad1 is phosphorylated directly and activated functionally by the BMP receptor kinase. Genes Dev. 11, 984-995.
25. 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 [see comments] [published erratum appears in Nature 1996, July 4, 382, 93]. Nature 381, 387-393.
26. Letsou, A., Arora, K., Wrana, J. L., Simin, K., Twonbly, V., Jamal, J., Staehling-Hampton, K., Hoffmann, F. M., Gelbart, W. M., Massague, J. and O'Connor, M. B. (1995). Dpp signaling in Drosophila is mediated by the punt gene product: a dual ligand binding type II receptor of the TGF-β receptor family. Cell 80, 899-908.
27. Liu, F., Ventura, F., Doody, J. and Massagué, J. (1995). Human type II receptor for bone morphogenic proteins (BMPs): Extension of the two-kinase receptor model to the BMPs. Mol, Cell. Biol. 15, 3479-3486.
28. Massagué, J., Hata, A. and Liu, F. (1997). TGF-β signalling through the Smad pathway. Trends Cell Biol, 7, 187-192.
29. 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.
30. Nellen, D., Burke, R., Struhl, G. and Basler, K. (1996). Direct and long- range action of a DPP morphogen gradient. Cell 85, 357-368.
31. Neumann, C. and Cohen, S. (1997). Morphogens and pattern formation. BioEssays 19, 721-729.
32. Nguyen, T., Jamal, J., Shimell, M. J., Arora, K. and O'Connor, M. B. (1994), Characterization of tolloid-related-1: a BMP-1-like product that is required during larval and pupal stages of Drosophila development. Dev. Biol. 166, 569-586.
33. 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.
34. Piccolo, S., Sasai, Y., Lu, B. and De Robertis, E. M. (1996). Dorsoventral patterning in Xenopus: inhibition of ventral signals by direct binding of chordin to BMP-4. Cell 86, 589-598.
35. Ruberte, E., Marty, T., Neuen, 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.
36. Singer, M., Penton, A., Twombly, V., Hoffmann, F. and Gelbart, W. (1997). Signaling through both type I DPP receptors is required for anterior- posterior patterning of the entire Drosophila wing. Development 124 (supplement), 79-89.
37. Sturtevant, M. A., Biehs, B., Marin, E. and Bier, E. (1997). The spalt gene links the A/P compartment boundary to a linear adult structure in the Drosophila wing. Development 124, 21-32.
38. Wharton, K. A., Ray, R. P. and Gelbart, W. M. (1993). An activity gradient of decapentataplegic is necessary for the specification of dorsal pattern elements in the Drosophila embryo. Development 117, 807-822.
39. Wharton, K. A., Thomsen, G. H. and Gelbart, W. M. (1991). Drosophila 60A gene, another transforming growth factor beta family member, is closely related to human bone morphogenetic proteins. Proc. Nat, Acad. Sci. USA 88, 9214-9218.
40. Xie, T., Finelli, A. L. and Padgett, R. W. (1994). The Drosophila saxophone. gene: a serine-threonine kinase receptor of the TGF-β superfamily. Science 263, 1756-1759.
41. Zhang, Y., Feng, X., We, R. and Derynck, R. (1996). Receptor-associated Mad homologues synergize as effectors of the TGF-β response. Nature. 383, 168-172.
42. Zou, H., Wieser, R., Massague, J. and Niswander, L. (1997). Distinct roles of type I bone morphogenetic protein receptors in the formation and differentiation of cartilage. Genes Dev. 11, 2191-2203.