Matching catalytic activity to developmental function: Tolloid-related processes Sog in order to help specify the posterior crossvein in the Drosophila wing

Development

Volumn 132, Issue 11, 2005, Pages 2645-2656

  Serpe, Mihaela ^a   Ralston, Amy ^b   Blair, Seth S ^b   O'Connor, Michael B ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

18w; Bmp; Crossvein; Drosophila; Sog; Tolloid

Indexed keywords

BONE MORPHOGENETIC PROTEIN; DROSOPHILA PROTEIN; LIGAND; MUTANT PROTEIN; PROTEIN SOG; PROTEIN TOLLOID; PROTEINASE; PROTEINASE INHIBITOR; TOLLOID RELATED PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BINDING SITE; CATALYSIS; CONTROLLED STUDY; DEGRADATION KINETICS; DEVELOPMENTAL STAGE; DROSOPHILA; ENZYME ACTIVITY; ENZYME INHIBITION; IN VITRO STUDY; IN VIVO STUDY; INSECT DEVELOPMENT; LIMB BLOOD VESSEL; LIMB DEVELOPMENT; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN PROCESSING; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION;

ANIMALS; BLOTTING, WESTERN; BONE MORPHOGENETIC PROTEINS; DROSOPHILA; DROSOPHILA PROTEINS; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; METALLOENDOPEPTIDASES; MUTAGENESIS, SITE-DIRECTED; SIGNAL TRANSDUCTION; WING;

ANIMALIA; INSECTA;

EID: 21244431603     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.01838     Document Type: Article

References (53)

1. Amano, S., Scott, I. C., Takahara, K., Koch, M., Champliaud, M. F., Gerecke, D. R., Keene, D. R., Hudson, D. L., Nishiyama, T., Lee, S. et al. (2000). Bone morphogenetic protein 1 is an extracellular processing enzyme of the laminin 5 γ2 chain. J. Biol. Chem. 275, 22728-22735.
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. Ashe, H. L. and Levine, M. (1999). Local inhibition and long-range enhancement of Dpp signal transduction by Sog. Nature 398, 427-431.
4. Barr, P. J. (1991). Mammalian subtilisins: the long-sought dibasic processing endoproteases. Cell 66, 1-3.
5. Binnerts, M. E., Wen, X., Cante-Barrett, K., Bright, J., Chen, H. T., Asundi, V., Sattari, P., Tang, T., Boyle, B., Funk, W. et al. (2004). Human Crossveinless-2 is a novel inhibitor of bone morphogenetic proteins. Biochem. Biophys. Res. Commun. 315, 272-280.
6. Blader, P., Rastegar, S., Fisher, N. and Strahle, U. (1997). Cleavage of the BMP-4 antagonist chordin by zebrafish tolloid. Science 278, 1937-1940.
7. Bode, W., Gomis-Ruth, F. X., Huber, R., Zwilling, R. and Stöcker, W. (1992). Structure of astacin and implication for activation of astacins and zinc-ligation of collagenases. Nature 368, 164-167.
8. Bond, J. S. and Beynon, R. J. (1995). The astacin family of metalloendopeptidases. Protein Sci. 4, 1247-1261.
9. 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.
10. Bunch, T. A., Grinblat, Y. and Goldstein, L. S. (1988). Characterization and use of the Drosophila metallothionein promoter in cultured Drosophila melanogaster cells. Nucleic Acids Res. 16, 1043-1061.
11. Childs, S. R. and O'Connor, M. B. (1994). Two domains of the tolloid protein contribute to its unusual genetic interaction with decapentaplegic. Dev. Biol. 162, 209-220.
12. Clark, T. G., Conway, S. J., Scott, I. C., Labosky, P. A., Winnier, G., Bundy, J., Hogan, B. L. and Greenspan, D. S. (1999). The mammalian Tolloid-like gene, Tll1, is necessary for normal septation and positioning of the heart. Development 126, 2631-2642.
13. Coffinier, C., Keptura, N., Tran, U., Geissert, D. and De Robertis, E. M. (2002). Mouse Crossveinless-2 is the vertebrate homolog of a Drosophila extracellular regulator of BMP signaling. Mech. Dev. 119, S179-S184.
14. Conley, C. A., Silburn, R., Singer, M. A., Ralston, A., Rohwer-Nutter, D., Olson, D. J., Gelbart, W. and Blair, S. S. (2000). Crossveinless 2 contains cysteme-rich domains and is required for high levels of BMP-like activity during the formation of the cross veins in Drosophila. Development 127, 3947-3959.
15. Connors, S. A., Trout, J., Ekker, M. and Mullins, M. C. (1999). The role of Tolloid/mini fin in dorsoventral pattern formation of the zebrafish embryo. Development 126, 3119-3130.
16. 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.
17. Eldar, A., Dorfman, R., Weiss, D., Ashe, H., Shilo, B. Z. and Barkai, N. (2002). Robustness of the BMP morphogen gradient in Drosophila embryonic patterning. Nature 419, 304-308.
18. Ferguson, E. L. and Anderson, K. V. (1992). 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.
19. Finelli, A. L., Xie, T., Bossie, C. A., Blackman, R. K. and Padgett, R. W. (1995). The tolkin gene is a tolloid BMP-1 homologue that is essential for Drosophila development. Genetics 141, 271-281.
20. François, V. and Bier, E. (1995). Xenopus chordin and Drosophila short gastrulation genes encode homologous proteins functioning in dorsal-ventral axis formation. Cell 80, 19-20.
21. François, V., Solloway, M., O'Neil, 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.
22. 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.
23. Hishida, R., Ishihara, T., Kondo, K. and Katsura, I. (1996). hch-1, a gene required for normal hatching and normal migration of a neuroblast in C. elegans, encodes a protein related to Tolloid and BMP-1. EMBO J. 15, 4111-4122.
24. Holley, S. A., Jackson, P. D., Sasai, Y., Lu, B., De Robertis, E. M., Hoffmann, 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.
25. Jürgens, G., Wieschaus, E., Nüsslein-Volhard, C. and Klunding, H. (1984). Mutations affecting the pattern of the larval cuticle in Drosophila melanogaster. II. Zygotic loci on the thirdchromosome. Roux's Arch. Develop. Biol. 193, 283-295.
26. Kamimura, M., Matsumoto, K., Koshiba-Takeuchi, K. and Ogura, T. (2004). Vertebrate crossveinless 2 is secreted and acts as an extracellular modulator of the BMP signaling cascade. Dev. Dyn. 230, 434-445.
27. Kessler, E., Takahara, K., Biniaminov, L., Brusel, M. and Greenspan, D. S. (1996). Bone morphogenetic protein-1: the type I procollagen C-proteinase. Science 271, 360-362.
28. Khalsa, O., Yoon, J. W., Torres-Schumann, S. and Wharton, K. A. (1998). TGF-beta/BMP superfamily members, Gbb-60A and Dpp, cooperate to provide pattern information and establish cell identity in the Drosophila wing. Development 125, 2723-2734.
29. Marqués, G., Musacchio, M., Shimell, M. J., Wünnerberg-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.
30. Mason, E. D., Konrad, K. D., Webb, C. D. and Marsh, J. L. (1994). Dorsal midline fate in Drosophila embryos requires twisted gastrulation, a gene encoding a secreted protein related to human connective tissue growth factor. Genes Dev. 8, 1489-501.
31. 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.
32. Piccolo, S., Agius, E., Lu, B., Goodman, S., Dale, E. and De Robertis, E. M. (1997). Cleavage of Chordin by Xolloid metalloprotease suggest a role for proteolytic processing in the regulation of Spemann organizer activity. Cell 91, 407-416.
33. Posakony, L. G., Raftery, L. A. and Gelbart, W. M. (1990). Wing formation in Drosophila melanogaster requires decapentaplegic gene function along the anterior-posterior compartment boundary. Mech. Dev. 33, 69-82.
34. Ralston, A. and Blair, S. S. (2005). Long-range dpp signaling is regulated to restrict BMP signaling to a crossvein competent zone. Dev. Biol. 280, 187-200.
35. Ray, R. P. and Wharton, K. A. (2001). Context-dependent relationships between the BMPs gbb and dpp during development of the Drosophila wing imaginal disk. Development 128, 3913-3925.
36. Ross, J. J., Shimmi, O., Vilmos, P., Petryk, A., Kim, H., Gaudenz, K., Hermanson, S., Ekker, S. C., O'Connor, M. B. and Marsh, J. L. (2001). Twisted gastrulation is a conserved extracellular BMP antagonist. Nature 410, 479-483.
37. Scott, I. C., Blitz, I. L., Pappano, W. N., Imamura, Y., Clark, T. G., Steiglitz, B. M., Thomas, C. L., Mass, S. A., Takahara, K., Cho, K. W. Y. et al. (1999). Mammalian BMP-1/tolloid-related metalloproteinases, including novel family member mammalian tolloid-like 2, have differential enzymatic activities and distributions of expression relevant to patterning and skeletogenesis. Dev. Biol. 213, 283-300.
38. Scott, I. C., Imamura, Y., Pappano, W. N., Troedel, J. M., Recklies, A. D., Roughley, P. J. and Greenspan, D. S. (2000). Bone morphogenetic protein-1 processes probiglycan. J. Biol. Chem. 275, 30504-30511.
39. 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 morphogenetic protein 1. Cell 67, 469-481.
40. Shimmi, O. and O'Connor, M. B. (2003). Physical properties of Tld, Sog, Tsg and Dpp protein interactions are predicted to help create a sharp boundary in BMP signals during dorsoventral patterning of the Drosophila embryo. Development 130, 4673-4682.
41. Shimmi, O., Umulis, D., Othmar, H. and O'Connor, M. B. (2005a). Facilitated Transport of a Dpp/Scw heterodimer by Sog/Tsg leads to robust patterning of the Drosophila blastoderm Embryo. Cell 120 (in press).
42. Shimmi, O., Ralston, A., Blair, S. S. and O'Connor, M. B. (2005b). The crossveinless gene encodes a new member of the Twisted gastrulation family of BMP-binding proteins which, with Short gastrulation, promotes BMP signaling in the crossveins of the Drosophila wing. Dev. Biol. (in press).
43. Srinivasan, S., Rashka, K. E. and Bier, E. (2002). Creation of a Sog morphogen gradient in the Drosophila embryo. Dev. Cell. 2, 91-101.
44. Suzuki, N., Labosky, P. A., Furuta, Y., Hargett, L., Dunn, R., Fogo, A. B., Takahara, K., Peters, D. M., Greenspan, D. S. and Hogan, B. L. (1996). Failure of ventral body wall closure in mouse embryos lacking a procollagen C-proteinase encoded by BMP1, a mammalian gene related to Drosophila tolloid. Development 122, 3587-3595.
45. Uzel, M. I., Scott, I. C., Babakhanlou-Chase, H., Palamankumbura, A. H., Pappano, W. N., Hong, H.-H., Greenspan, D. S. and Trackman, P. C. (2001). Multiple bone morphogenetic protein 1-related mammalian metalloproteinases process pro-lysyl oxidase at the correct physiological site and control lysyl oxidase activation in mouse embryo fibroblast cultures. J. Biol. Chem. 276, 22537-22543.
46. Vilmos, P., Sousa-Neves, R., Lukacsovich, T. and Marsh, J. L. (2005). crossveinless defines a new family of Twisted-gastrulation-like modulators of bone morphogenetic protein signaling. EMBO Rep. 6, 262-267.
47. Wang, Y.-C. and Ferguson, E. L. (2005). Spatial bistability of Dpp-receptor interactions during Drosophila dorsal-ventral patterning. Nature 434, 229-234.
48. Wharton, K. A., Cook, J. M., Torres-Schumann, S., de Castro, K., Borod, E. and Phillips, D. A. (1999). Genetic analysis of the bone morphogenetic protein-related gene, gbb, identifies multiple requirements during Drosophila development. Genetics 152, 629-640.
49. Wolfman, N. M., McPherron, A. C., Pappano, W. N., Davies, M. V., Song, K., Tomkinson, K. N., Wright, J. F., Zhao, L., Sebald, S. M., Lee, S.-J. and Greenspan, D. S. (2003). Activation of latent myostatin by the BMP-1/tolloid family of metalloproteinases. PNAS 100, 15842-15846.
50. Wozney, J. M., Rosen, V., Celeste, A. J., Mitsock, L. M., Whitters, M. J., Kriz, R. W., Hewick, R. M. and Wang, E. A. (1988). Novel regulators of bone formation: molecular clones and activities. Science 242, 1528-1534.
51. Yu, K., Sturtevant, M. A., Biehs, B., Francois, 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.
52. Yu, K., Shrinivasan, S., Shimmi, O., Biehs, B., Rashka, K. E., Kimelman, D., O'Connor, M. B. and Bier, E. (2000). Processing of the Drosophila Sog protein creates a novel BMP inhibitory activity. Development 127, 2143-2154.
53. Yu, K., Kang, K. H., Pyati, U., Srinivasan, S., Kimelman, D. and Bier, E. (2004). Cysteine repeat domains adjacent sequences determine distinct bone morphogenetic protein modulating activities of the Drosophila Sog protein. Genetics 166, 1323-1336.