Three Drosophila EXT genes shape morphogen gradients through synthesis of heparan sulfate proteoglycans

Development

Volumn 131, Issue 1, 2004, Pages 73-82

  Takei, Yuki ^a   Ozawa, Yutakahiko ^a   Sato, Makoto ^a   Watanabe, Akira ^a   Tabata, Tetsuya ^a  

^a UNIVERSITY OF TOKYO   (Japan)

Author keywords

Brother of ttv; Decapentaplegic; Drosophila; EXT genes; Gradient formation; Hedgehog; Morphogen; Sister of ttv; Tout velu; Wingless

Indexed keywords

DROSOPHILA PROTEIN; GLYCOSYLTRANSFERASE; MORPHOGEN; PROTEOHEPARAN SULFATE; SONIC HEDGEHOG PROTEIN; WNT1 PROTEIN;

ALLELE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; BIOACCUMULATION; BIOSYNTHESIS; CONCENTRATION RESPONSE; CONTROLLED STUDY; DROSOPHILA; EMBRYO; EMBRYO PATTERN FORMATION; ENZYME ACTIVITY; FORELIMB; GENE FUNCTION; GENE IDENTIFICATION; GENE MUTATION; GENE STRUCTURE; GENETIC CODE; GENETIC SCREENING; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN SYNTHESIS; PROTEIN TRANSPORT; REVIEW; SENSITIVITY ANALYSIS; SIGNAL TRANSDUCTION;

AMINO ACID SEQUENCE; ANIMALS; CONSERVED SEQUENCE; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEPARAN SULFATE PROTEOGLYCANS; MALE; MOLECULAR SEQUENCE DATA; MORPHOGENESIS; MUTATION; PROTO-ONCOGENE PROTEINS; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID;

ANIMALIA; ARACHNIDA; ERINACEIDAE; HEXAPODA; RAPHIA FRATER;

EID: 1342341864     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.00913     Document Type: Review

References (60)

1. Baeg, G. H., Lin, X., Khare, N., Baumgartner, S. and Perrimon, N. (2001). Heparan sulfate proteoglycans are critical for the organization of the extracellular distribution of Wingless. Development 128, 87-94.
2. Basler, K. and Struhl, G. (1994). Compartment boundaries and the control of Drosophila limb pattern by hedgehog protein. Nature 368, 208-214.
3. Bellaiche, Y., The, I. and Perrimon, N. (1998). Tout-velu is a Drosophila homologue of the putative tumour suppressor EXT-1 and is needed for Hh diffusion. Nature 394, 85-88.
4. Bier, E. (2000). Drawing lines in the Drosophila wing: initiation of wing vein development. Curr. Opin. Genet. Dev. 10, 393-398.
5. Binari, R. C., Staveley, B. E., Johnson, W. A., Godavarti, R., Sasisekharan, R. and Manoukian, A. S. (1997). Genetic evidence that heparin-like glycosaminoglycans are involved in wingless signaling. Development 124, 2623-2632.
6. Capdevila, J. and Guerrero, I. (1994). Targeted expression of the signaling molecule decapentaplegic induces pattern duplications and growth alterations in Drosophila wings. EMBO J. 13, 4459-4468.
7. Chen, Y. and Struhl, G. (1996). Dual roles for Patched in sequestering and transducing Hedgehog. Cell 87, 553-563.
8. David, G., Bai, X. M., Van der Schueren, B., Cassiman, J. J. and Van den Berghe, H. (1992). Developmental changes in heparan sulfate expression: in situ detection with mAbs. J. Cell Biol. 119, 961-975.
9. Entchev, E. V., Schwabedissen, A. and Gonzalez-Gaitan, M. (2000). Gradient formation of the TGF-beta homolog Dpp. Cell 103, 981-991.
10. Fujise, M., Takeo, S., Kamimura, K., Matsuo, T., Algaki, T., Izumi, S. and Nakato, H. (2003). Dally regulates Dpp morphogen gradient formation in the Drosophila wing. Development 130, 1515-1522.
11. Gerlitz, O. and Basler, K. (2002). Wingful, an extracellular feedback inhibitor of Wingless. Genes Dev. 16, 1055-1059.
12. Giraldez, A. J., Copley, R. R. and Cohen, S. M. (2002). HSPG modification by the secreted enzyme Notum shapes the Wingless morphogen gradient. Dev. Cell 2, 667-676.
13. Greco, V., Hannus, M. and Eaton, S. (2001). Argosomes: a potential vehicle for the spread of morphogens through epithelia. Cell 106, 633-645.
14. Gurdon, J. B., Dyson, S. and St Johnston, D. (1998). Cells' perception of position in a concentration gradient. Cell 95, 159-162.
15. Hacker, U., Lin, X. and Perrimon, N. (1997). The Drosophila sugarless gene modulates Wingless signaling and encodes an enzyme involved in polysaccharide biosynthesis. Development 124, 3565-3573.
16. Haerry, T. E., Heslip, T. R., Marsh, J. L. and O'Connor, M. B. (1997). Defects in glucuronate biosynthesis disrupt Wingless signaling in Drosophila. Development 124, 3055-3064.
17. Han, C., Lin, X., Zhao, C., Opoka, R., Wang, K. and Lin, X. (2001). Identification of botv, a new segment polarity gene that encodes a protein of the putative tumor suppressor EXT family. In 42nd Annual Drosophila Research Conference (Washington, D.C., Program No. 411).
18. Han, C., Belenkaya, T., Lin, X., Opoka, R. and Lin, X. (2002). Functional analysis of EXT family of tumor suppressor genes in Drosophila. In 43rd Annual Drosophila Research Conference (San Diego, 2001 Program No. 582C).
19. Jackson, S. M., Nakato, H., Sugiura, M., Jannuzi, A., Oakes, R., Kaluza, V., Golden, C. and Selleck, S. B. (1997). dally, a Drosophila glypican, controls cellular responses to the TGF-beta-related morphogen, Dpp. Development 124, 4113-4120.
20. Kerszberg, M. and Wolpert, L. (1998). Mechanisms for positional signalling by morphogen transport: a theoretical study. J. Theor. Biol. 191, 103-114.
21. Kim, B. T., Kitagawa, H., Tamura Ji, J., Kusche-Gullberg, M., Lindahl, U. and Sugahara, K. (2002). Demonstration of a novel gene DEXT3 of Drosophila melanogaster as the essential N-acetylglucosamine transferase in the heparan sulfate biosynthesis: chain initiation and elongation. J. Biol. Chem. 277, 13659-13665.
22. Lawrence, P. A. and Struhl, G. (1996). Morphogens, compartments, and pattern: lessons from Drosophila? Cell 85, 951-961.
23. Lee, J. J., von Kessler, D. P., Parks, S. and Beachy, P. A. (1992). Secretion and localized transcription suggest a role in positional signaling for products of the segmentation gene hedgehog. Cell 71, 33-50.
24. Lin, X. and Perrimon, N. (1999). Dally cooperates with Drosophila Frizzled 2 to transduce Wingless signalling. Nature 400, 281-284.
25. Lin, X. and Perrimon, N. (2000). Role of heparan sulfate proteoglycans in cell-cell signaling in Drosophila. Matrix Biol. 19, 303-307.
26. Lin, X., Buff, E. M., Perrimon, N. and Michelson, A. M. (1999). Heparan sulfate proteoglycans are essential for FGF receptor signaling during Drosophila embryonic development. Development 126, 3715-3723.
27. McCormick, C., Duncan, G., Goutsos, K. T. and Tufaro, F. (2000). The putative tumor suppressors EXT1 and EXT2 form a stable complex that accumulates in the Golgi apparatus and catalyzes the synthesis of heparan sulfate. Proc. Natl. Acad. Sci. USA 97, 668-673.
28. McDowell, N., Gurdon, J. B. and Grainger, D. J. (2001). Formation of a functional morphogen gradient by a passive process in tissue from the early Xenopus embryo. Int. J. Dev. Biol. 45, 199-207.
29. Moline, M. M., Southern, C. and Bejsovec, A. (1999). Directionality of wingless protein transport influences epidermal patterning in the Drosophila embryo. Development 126, 4375-4384.
30. Mullor, J. L., Calleja, M., Capdevila, J. and Guerrero, I. (1997). Hedgehog activity, independent of Decapentaplegic, participates in wing disc patterning. Development 124, 1227-1237.
31. Nakato, H., Futch, T. A. and Selleck, S. B. (1995). The division abnormally delayed (dally) gene: a putative integral membrane proteoglycan required for cell division patterning during postembryonic development of the nervous system in Drosophila. Development 121, 3687-3702.
32. Narayanan, R. and Ramaswami, M. (2001). Endocytosis in Drosophila: progress, possibilities, prognostications. Exp. Cell Res. 271, 28-35.
33. Neumann, C. and Cohen, S. (1997a). Morphogens; and pattern formation. BioEssays 19, 721-729.
34. Neumann, C. J. and Cohen, S. M. (1997b). Long-range action of Wingless organizes the dorsal-ventral axis of the Drosophila wing. Development 124, 871-880.
35. Panganiban, G., Sebring, A., Nagy, L. and Carroll, S. (1995). The development of crustacean limbs and the evolution of arthropods. Science 270, 1363-1366.
36. Pepinsky, R. B., Zeng, C., Wen, D., Rayhorn, P., Baker, D. P., Williams, K. P., Bixler, S. A., Ambrose, C. M., Garber, E. A., Miatkowski, K. et al. (1998). Identification of a palmitic acid-modified form of human Sonic hedgehog. J. Biol. Chem. 273, 14037-14045.
37. Perrimon, N. and Bernfield, M. (2000). Specificities of heparan sulphate proteoglycans in developmental processes. Nature 404, 725-728.
38. Persson, U., Izumi, H., Souchelnytskyi, S., Itoh, S., Grimsby, S., Engstrom, U., Heldin, C.-H., Funa, K. and ten Dijke, P. (1998). The L45 loop in type I receptors for TGF-β family members is a critical determinant in specifying Smad isoform activation. FEBS Lett. 434, 83-87.
39. Pfeiffer, S. and Vincent, J. P. (1999). Signalling at a distance: transport of Wingless in the embryonic epidermis of Drosophila. Semin. Cell Dev. Biol. 10, 303-309.
40. Porter, J. A., Young, K. E. and Beachy, P. A. (1996). Cholesterol modification of hedgehog signaling proteins in animal development. Science 274, 255-259.
41. Reichsman, F., Smith, L. and Cumberledge, S. (1996). Glycosaminoglycans can modulate extracellular localization of the wingless protein and promote signal transduction. J. Cell Biol. 135, 819-827.
42. Selleck, S. B. (2001). Genetic dissection of proteoglycan function in Drosophila and C. elegans. Semin. Cell Dev. Biol. 12, 127-134.
43. Senay, C., Lind, T., Muguruma, K., Tone, Y., Kitagawa, H., Sugahara, K., Lidholt, K., Lindahl, U. and Kusche-Gullberg, M. (2000). The EXT1/EXT2 tumor suppressors: catalytic activities and role in heparan sulfate biosynthesis. EMBO Rep. 1, 282-286.
44. Strigini, M. and Cohen, S. M. (1997). A Hedgehog activity gradient contributes to AP axial patterning of the Drosophila wing. Development 124, 4697-4705.
45. Strigini, M. and Cohen, S. M. (2000). Wingless gradient formation in the Drosophila wing. Curr. Biol. 10, 293-300.
46. 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.
47. Sugahara, K. and Kitagawa, H. (2000). Recent advances in the study of the biosynthesis and functions of sulfated glycosaminoglycans. Curr. Opin. Struct. Biol. 10, 518-527.
48. Tabata, T. (2001). Genetics of morphogen gradients. Nat. Rev. Genet. 2, 620-630.
49. Tabata, T. and Kornberg, T. B. (1994). Hedgehog is a signaling protein with a key role in patterning Drosophila imaginal discs. Cell 76, 89-102.
50. Thipale, J. and Keski-Oja, J. (1997). Growth factors in the extracellular matrix. FASEB J. 11, 51-59.
51. Tanimoto, H., Rob, S., ten Dijke, P. and Tabata, T. (2000). Hedgehog creates a gradient of DPP activity in Drosophila wing imaginal discs. Mol. Cell 5, 59-71.
52. Teleman, A. A. and Cohen, S. M. (2000). Dpp gradient formation in the Drosophila wing imaginal disc. Cell 103, 971-980.
53. The, I., Bellaiche, Y. and Perrimon, N. (1999). Hedgehog movement is regulated through tout velu-dependent synthesis of a heparan sulfate proteoglycan. Mol. Cell 4, 633-639.
54. Toyoda, H., Kinoshita-Toyoda, A., Fox, B. and Selleck, S. B. (2000). Structural analysis of glycosaminoglycans in animals bearing mutations in sugarless, sulfateless, and tout-velu. Drosophila homologues of vertebrate genes encoding glycosaminoglycan biosynthetic enzymes. J. Biol. Chem. 275, 21856-21861.
55. Tsuda, M., Kamimura, K., Nakato, H., Archer, M., Staatz, W., Fox, B., Humphrey, M., Olson, S., Futch, T., Kaluza, V. et al. (1999). The cell-surface proteoglycan Dally regulates Wingless signalling in Drosophila. Nature 400, 276-280.
56. Willert, K., Brown, J. D., Danenberg, E., Duncan, A. W., Weissman, I. L., Reya, T., Yates, J. R., 3rd and Nusse, R. (2003). Wnt proteins are lipid-modified and can act as stem cell growth factors. Nature 423, 448-452.
57. Wolpert, L. (1969). Positional information and the spatial pattern of cellular differentiation. J. Theor. Biol. 25, 1-47.
58. Xu, T. and Robin, G. M. (1993). Analysis of genetic mosaics in developing and adult Drosophila tissues. Development 117, 1223-1237.
59. Zecca, M., Basler, K. and Struhl, G. (1995). Sequential organizing activities of engrailed, hedgehog and decapentaplegic in the Drosophila wing. Development 121, 2265-2278.
60. Zecca, M., Basler, K. and Struhl, G. (1996). Direct and long-range action of a Wingless morphogen gradient. Cell 87, 833-844.