In vivo manipulation of heparan sulfate structure and its effect on Drosophila development

Glycobiology

Volumn 21, Issue 5, 2011, Pages 607-618

  Kamimura, Keisuke ^a,b   Maeda, Nobuaki ^b   Nakato, Hiroshi ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

^b TOKYO METROPOLITAN INSTITUTE OF MEDICAL SCIENCE   (Japan)

Author keywords

Decapentaplegic; Drosophila; heparan sulfate proteoglycan; heparan sulfate modifying enzyme; Wingless

Indexed keywords

BONE MORPHOGENETIC PROTEIN; DISACCHARIDE; ENZYME; HEPARAN SULFATE; HEPARAN SULFATE MODIFYING ENZYME; PROTEOHEPARAN SULFATE; UNCLASSIFIED DRUG; WNT PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CHEMICAL MODIFICATION; CHEMICAL STRUCTURE; CONTROLLED STUDY; DROSOPHILA; ENZYME ACTIVITY; IN VIVO STUDY; INSECT DEVELOPMENT; LETHALITY; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TRANSGENIC ORGANISM;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; CARBOHYDRATE EPIMERASES; CELL PROLIFERATION; DROSOPHILA; DROSOPHILA PROTEINS; HEPARAN SULFATE PROTEOGLYCANS; HYBRIDIZATION, GENETIC; PHENOTYPE; RECOMBINANT PROTEINS; SIGNAL TRANSDUCTION; SULFOTRANSFERASES; TRANSGENES; WING; WNT1 PROTEIN;

ANIMALIA;

EID: 79953847208     PISSN: 09596658     EISSN: 14602423     Source Type: Journal    
DOI: 10.1093/glycob/cwq202     Document Type: Article

References (35)

1. Abrams JM, White K, Fessler LI, Steller H. (1993) Programmed cell death during Drosophila embryogenesis. Development. 117:29-43. (Pubitemid 23094155)
2. Akiyama T, Kamimura K, Firkus C, Takeo S, Shimmi O, Nakato H. (2008) Dally regulates Dpp morphogen gradient formation by stabilizing Dpp on the cell surface. Dev Biol. 313:408-419. (Pubitemid 350298327)
3. Belenkaya TY, Han C, Yan D, Opoka RJ, Khodoun M, Liu H, Lin X. (2004) Drosophila Dpp morphogen movement is independent of dynamin-mediated endocytosis but regulated by the glypican members of heparan sulfate proteoglycans. Cell. 119:231-244. (Pubitemid 39360905)
4. Brand AH, Perrimon N. (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development. 118:401-415. (Pubitemid 23214028)
5. Bullock SL, Fletcher JM, Beddington RS, Wilson VA. (1998) Renal agenesis in mice homozygous for a gene trap mutation in the gene encoding heparan sulfate 2-sulfotransferase. Genes Dev. 12:1894-1906. (Pubitemid 28304341)
6. Burke R, Basler K. (1996) Dpp receptors are autonomously required for cell proliferation in the entire developing Drosophila wing. Development. 122:2261-2269. (Pubitemid 26235825)
7. Couso JP, Bishop SA, Martinez Arias A. (1994) The wingless signalling pathway and the patterning of the wing margin in Drosophila. Development. 120:621-636. (Pubitemid 24071204)
8. De Celis JF. (2003) Pattern formation in the Drosophila wing: The development of the veins. Bioessays. 25:443-451. (Pubitemid 36565682)
9. Esko JD, Selleck SB. (2002) Order out of chaos: assembly of ligand binding sites in heparan sulfate. Annu Rev Biochem. 71:435-471. (Pubitemid 34800227)
10. Fujise M, Takeo S, Kamimura K, Matsuo T, Aigaki T, Izumi S, Nakato H. (2003) Dally regulates Dpp morphogen gradient formation in the Drosophila wing. Development. 130:1515-1522. (Pubitemid 36527513)
11. Gallet A, Staccini-Lavenant L, Therond PP. (2008) Cellular trafficking of the glypican Dally-like is required for full-strength Hedgehog signaling and wingless transcytosis. Dev Cell. 14:712-725. (Pubitemid 351622609)
12. Gorsi B, Stringer SE. (2007) Tinkering with heparan sulfate sulfation to steer development. Trends Cell Biol. 17:173-177. (Pubitemid 46507809)
13. Habuchi H, Nagai N, Sugaya N, Atsumi F, Stevens RL, Kimata K. (2007) Mice deficient in heparan sulfate 6-O-sulfotransferase-1 exhibit defective heparan sulfate biosynthesis, abnormal placentation, and late embryonic lethality. J Biol Chem. 282:15578-15588.
14. Han C, Belenkaya TY, Khodoun M, Tauchi M, Lin X, Lin X. (2004) Distinct and collaborative roles of Drosophila EXT family proteins in morphogen signalling and gradient formation. Development. 131:1563-1575. (Pubitemid 38559283)
15. Holmborn K, Ledin J, Smeds E, Eriksson I, Kusche-Gullberg M, Kjellen L. (2004) Heparan sulfate synthesized by mouse embryonic stem cells deficient in NDST1 and NDST2 is 6-O-sulfated but contains no N-sulfate groups. J Biol Chem. 279:42355-42358. (Pubitemid 39372115)
16. Jackson SM, Nakato H, Sugiura M, Jannuzi A, Oakes R, Kaluza V, Golden C, Selleck SB. (1997) dally, a Drosophila glypican, controls cellular responses to the TGF-beta-related morphogen, Dpp. Development. 124:4113-4120. (Pubitemid 27483336)
17. Kamimura K, Koyama T, Habuchi H, Ueda R, Masu M, Kimata K, Nakato H. (2006) Specific and flexible roles of heparan sulfate modifications in Drosophila FGF signaling. J Cell Biol. 174:773-778. (Pubitemid 44373727)
18. Kinoshita A, Sugahara K. (1999) Microanalysis of glycosaminoglycan- derived oligosaccharides labeled with a fluorophore 2-aminobenzamide by high-performance liquid chromatography: application to disaccharide composition analysis and exosequencing of oligosaccharides. Anal Biochem. 269:367-378. (Pubitemid 29201038)
19. Kirkpatrick CA, Dimitroff BD, Rawson JM, Selleck SB. (2004) Spatial regulation of Wingless morphogen distribution and signaling by Dally-like protein. Dev Cell. 7:513-523. (Pubitemid 39341837)
20. Kirkpatrick CA, Selleck SB. (2007) Heparan sulfate proteoglycans at a glance. J Cell Sci. 120:1829-1832. (Pubitemid 46979773)
21. Kleinschmit A, Koyama T, Dejima K, Hayashi Y, Kamimura K, Nakato H. (2010) Drosophila heparan sulfate 6-O endosulfatase regulates Wingless morphogen gradient formation. Dev Biol. 345:204-214.
22. Kreuger J, Perez L, Giraldez AJ, Cohen SM. (2004) Opposing activities of Dally-like glypican at high and low levels of Wingless morphogen activity. Dev Cell. 7:503-512. (Pubitemid 39341836)
23. Kreuger J, Spillmann D, Li JP, Lindahl U. (2006) Interactions between heparan sulfate and proteins: the concept of specificity. J Cell Biol. 174:323-327. (Pubitemid 44156762)
24. Li JP, Gong F, Hagner-McWhirter A, Forsberg E, Abrink M, Kisilevsky R, Zhang X, Lindahl U. (2003) Targeted disruption of a murine glucuronyl C5-epimerase gene results in heparan sulfate lacking L-iduronic acid and in neonatal lethality. J Biol Chem. 278:28363-28366. (Pubitemid 36935735)
25. Martin-Castellanos C, Edgar BA. (2002) A characterization of the effects of Dpp signaling on cell growth and proliferation in the Drosophila wing. Development. 129:1003-1013. (Pubitemid 34874124)
26. Merry CL, Bullock SL, Swan DC, Backen AC, Lyon M, Beddington RS, Wilson VA, Gallagher JT. (2001) The molecular phenotype of heparan sulfate in the Hs2st-/- mutant mouse. J Biol Chem. 276:35429-35434.
27. Nakato H, Futch TA, Selleck SB. (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.
28. Nakato H, Kimata K. (2002) Heparan sulfate fine structure and specificity of proteoglycan functions. Biochim Biophys Acta. 1573:312-318. (Pubitemid 35335440)
29. Pinhal MA, Smith B, Olson S, Aikawa J, Kimata K, Esko JD. (2001) Enzyme interactions in heparan sulfate biosynthesis: uronosyl 5-epimerase and 2-O-sulfotransferase interact in vivo. Proc Natl Acad Sci USA. 98:12984-12989. (Pubitemid 33054083)
30. Presto J, Thuveson M, Carlsson P, Busse M, Wilen M, Eriksson I, Kusche-Gullberg M, Kjellen L. (2008) Heparan sulfate biosynthesis enzymes EXT1 and EXT2 affect NDST1 expression and heparan sulfate sulfation. Proc Natl Acad Sci USA. 105:4751-4756. (Pubitemid 351753818)
31. Strigini M, Cohen SM. (2000) Wingless gradient formation in the Drosophila wing. Curr Biol. 10:293-300. (Pubitemid 30186132)
32. Sugaya N, Habuchi H, Nagai N, Ashikari-Hada S, Kimata K. (2008) 6-O-sulfation of heparan sulfate differentially regulates various fibroblast growth factor-dependent signalings in culture. J Biol Chem. 283:10366-10376.
33. Takeo S, Akiyama T, Firkus C, Aigaki T, Nakato H. (2005) Expression of a secreted form of Dally, a Drosophila glypican, induces overgrowth pheno-type by affecting action range of Hedgehog. Dev Biol. 284:204-218. (Pubitemid 41096735)
34. Toyoda H, Kinoshita-Toyoda A, Selleck SB. (2000) Structural analysis of gly-cosaminoglycans in Drosophila and Caenorhabditis elegans and demonstration that tout-velu, a Drosophila gene related to EXT tumor suppressors, affects heparan sulfate in vivo. J Biol Chem. 275:2269-2275. (Pubitemid 30081981)
35. Tsuda M, Kamimura K, Nakato H, Archer M, Staatz W, Fox B, Humphrey M, Olson S, Futch T, Kaluza V, Siegfried E, Stam L, Selleck SB. (1999) The cell-surface proteoglycan Dally regulates Wingless signalling in Drosophila. Nature. 400:276-280. (Pubitemid 29334144)