Axon sorting in the optic tract requires HSPG synthesis by ext2 (dackel) and extl3 (boxer)

Neuron

Volumn 44, Issue 6, 2004, Pages 947-960

  Lee, Jeong Soo ^a   Von Der Hardt, Sophia ^b   Rusch, Melissa A ^c   Stringer, Sally E ^c   Stickney, Heather L ^d   Talbot, William S ^d   Geisler, Robert ^b   Nüsslein Volhard, Christiane ^b   Selleck, Scott B ^c   Chien, Chi Bin ^a   Roehl, Henry ^b,e  

^a UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^b MAX PLANCK INSTITUTE FOR DEVELOPMENTAL BIOLOGY   (Germany)

^c UNIVERSITY OF MINNESOTA   (United States)

^d STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY OF SHEFFIELD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOSYLTRANSFERASE; PROTEOHEPARAN SULFATE;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; GENE FUNCTION; GENE OVEREXPRESSION; GENETIC CODE; IMMUNOHISTOCHEMISTRY; MOLECULAR CLONING; NERVE FIBER; NONHUMAN; OPTIC TRACT; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; RETINA GANGLION CELL; SYNTHESIS; TOPOGRAPHY; ZEBRA FISH;

ANIMALS; AXONS; HEPARAN SULFATE PROTEOGLYCANS; MOLECULAR SEQUENCE DATA; N-ACETYLGLUCOSAMINYLTRANSFERASES; RETINAL GANGLION CELLS; VISUAL PATHWAYS; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 10444270932     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuron.2004.11.029     Document Type: Article

References (70)

1. Baier H., Klostermann S., Trowe T., Karlstrom R.O., Nusslein-Volhard C., Bonhoeffer F. Genetic dissection of the retinotectal projection. Development. 123:1996;415-425
2. Bandtlow C.E., Zimmermann D.R. Proteoglycans in the developing brain. new conceptual insights for old proteins Physiol. Rev. 80:2000;1267-1290
3. Bellaiche Y., The I., Perrimon N. Tout-velu is a Drosophila homologue of the putative tumour suppressor EXT-1 and is needed for Hh diffusion. Nature. 394:1998;85-88
4. Bink R.J., Habuchi H., Lele Z., Dolk E., Joore J., Rauch G.J., Geisler R., Wilson S.W., den Hertog J., Kimata K., Zivkovic D. Heparan sulfate 6-o-sulfotransferase is essential for muscle development in zebrafish. J. Biol. Chem. 278:2003;31118-31127
5. Bornemann D.J., Duncan J.E., Staatz W., Selleck S., Warrior R. Abrogation of heparan sulfate synthesis in Drosophila disrupts the Wingless, Hedgehog and Decapentaplegic signaling pathways. Development. 131:2004;1927-1938
6. Bülow H.E., Hobert O. Differential sulfations and epimerization define heparan sulfate specificity in nervous system development. Neuron. 41:2004;723-736
7. Busse M., Kusche-Gullberg M. In vitro polymerization of heparan sulfate backbone by the EXT proteins. J. Biol. Chem. 278:2003;41333-41337
8. Capdevila J., Izpisua Belmonte J.C. Patterning mechanisms controlling vertebrate limb development. Annu. Rev. Cell Dev. Biol. 17:2001;87-132
9. Chan S.O., Guillery R.W. Changes in fiber order in the optic nerve and tract of rat embryos. J. Comp. Neurol. 344:1994;20-32
10. Chien C.-B., Cornel E.M., Holt C.E. Absence of topography in precociously innervated tecta. Development. 121:1995;2621-2631
11. Chung K.Y., Leung K.M., Lin L., Chan S.O. Heparan sulfate proteoglycan expression in the optic chiasm of mouse embryos. J. Comp. Neurol. 436:2001;236-247
12. David G., Bai X.M., Van der Schueren B., Cassiman J.J., Van den Berghe H. Developmental changes in heparan sulfate expression. in situ detection with mAbs J. Cell Biol. 119:1992;961-975
13. Duncan G., McCormick C., Tufaro F. The link between heparan sulfate and hereditary bone disease. finding a function for the EXT family of putative tumor suppressor proteins J. Clin. Invest. 108:2001;511-516
14. Fricke C., Lee J.S., Geiger-Rudolph S., Bonhoeffer F., Chien C.B. astray, a zebrafish roundabout homolog required for retinal axon guidance. Science. 292:2001;507-510
15. Fujisawa H. Retinotopic analysis of fiber pathways in the regenerating retinotectal system of the adult newt cynops Pyrrhogaster. Brain Res. 206:1981;27-37
16. Geisler R. Tübingen map of the zebrafish genome. http://wwwmap.tuebingen.mpg.de/:2002
17. Grandel H., Schulte-Merker S. The development of the paired fins in the zebrafish (Danio rerio). Mech. Dev. 79:1998;99-120
18. Grandel H., Draper B.W., Schulte-Merker S. dackel acts in the ectoderm of the zebrafish pectoral fin bud to maintain AER signaling. Development. 127:2000;4169-4178
19. Halfter W. A heparan sulfate proteoglycan in developing avian axonal tracts. J. Neurosci. 13:1993;2863-2873
20. Han C., Belenkaya T.Y., Khodoun M., Tauchi M., Lin X. Distinct and collaborative roles of Drosophila EXT family proteins in morphogen signalling and gradient formation. Development. 131:2004;1563-1575
21. Hoffman-Kim D., Lander A.D., Jhaveri S. Patterns of chondroitin sulfate immunoreactivity in the developing tectum reflect regional differences in glycosaminoglycan biosynthesis. J. Neurosci. 18:1998;5881-5890
22. Hu H. Cell-surface heparan sulfate is involved in the repulsive guidance activities of Slit2 protein. Nat. Neurosci. 4:2001;695-701
23. Hutson L.D., Chien C.B. Pathfinding and error correction by retinal axons. the role of astray/robo2 Neuron. 33:2002;205-217
24. Inatani M., Irie F., Plump A.S., Tessier-Lavigne M., Yamaguchi Y. Mammalian brain morphogenesis and midline axon guidance require heparan sulfate. Science. 302:2003;1044-1046
25. Inoue A., Takahashi M., Hatta K., Hotta Y., Okamoto H. Developmental regulation of islet-1 mRNA expression during neuronal differentiation in embryonic zebrafish. Dev. Dyn. 199:1994;1-11
26. Irie A., Yates E.A., Turnbull J.E., Holt C.E. Specific heparan sulfate structures involved in retinal axon targeting. Development. 129:2002;61-70
27. Johnson K.G., Ghose A., Epstein E., Lincecum J., O'Connor M.B., Van Vactor D. Axonal heparan sulfate proteoglycans regulate the distribution and efficiency of the repellent Slit during midline axon guidance. Curr. Biol. 14:2004;499-504
28. Karlstrom R.O., Trowe T., Klostermann S., Baier H., Brand M., Crawford A.D., Grunewald B., Haffter P., Hoffmann H., Meyer S.U., et al. Zebrafish mutations affecting retinotectal axon pathfinding. Development. 123:1996;427-438
29. Kim B.T., Kitagawa H., Tamura J., Saito T., Kusche-Gullberg M., Lindahl U., Sugahara K. Human tumor suppressor EXT gene family members EXTL1 and EXTL3 encode α1,4- N-acetylglucosaminyltransferases that likely are involved in heparan sulfate/ heparin biosynthesis. Proc. Natl. Acad. Sci. USA. 98:2001;7176-7181
30. Kim B.T., Kitagawa H., Tamura Ji J., Kusche-Gullberg M., Lindahl U., Sugahara K. 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. 277:2002;13659-13665
31. Kim B.T., Kitagawa H., Tanaka J., Tamura J., Sugahara K. In vitro heparan sulfate polymerization. crucial roles of core protein moieties of primer substrates in addition to the EXT1-EXT2 interaction J. Biol. Chem. 278:2003;41618-41623
32. Kitagawa H., Egusa N., Tamura J.I., Kusche-Gullberg M., Lindahl U., Sugahara K. rib-2, a Caenorhabditis elegans homolog of the human tumor suppressor EXT genes encodes a novel α1,4-N-acetylglucosaminyltransferase involved in the biosynthetic initiation and elongation of heparan sulfate. J. Biol. Chem. 276:2001;4834-4838
33. Ledin J., Staatz W., Li J.P., Gotte M., Selleck S., Kjellen L., Spillmann D. Heparan sulfate structure in mice with genetically modified heparan sulfate production. J. Biol. Chem. 279:2004;42732-42741
34. Lee J.S., Chien C.B. When sugars guide axons. new lessons from HSPG mutants Nat. Rev. Genetics. in press:2004
35. Lee J.S., Ray R., Chien C.B. Cloning and expression of three zebrafish roundabout homologs suggest roles in axon guidance and cell migration. Dev. Dyn. 221:2001;216-230
36. Leung K.M., Taylor J.S., Chan S.O. Enzymatic removal of chondroitin sulphates abolishes the age-related axon order in the optic tract of mouse embryos. Eur. J. Neurosci. 17:2003;1755-1767
37. Lewis K.E., Concordet J.P., Ingham P.W. Characterisation of a second patched gene in the zebrafish Danio rerio and the differential response of patched genes to Hedgehog signalling. Dev. Biol. 208:1999;14-29
38. Liang Y., Annan R.S., Carr S.A., Popp S., Mevissen M., Margolis R.K., Margolis R.U. Mammalian homologues of the Drosophila slit protein are ligands of the heparan sulfate proteoglycan glypican-1 in brain. J. Biol. Chem. 274:1999;17885-17892
39. Lin X., Wei G., Shi Z., Dryer L., Esko J.D., Wells D.E., Matzuk M.M. Disruption of gastrulation and heparan sulfate biosynthesis in EXT1-deficient mice. Dev. Biol. 224:2000;299-311
40. Lind T., Tufaro F., McCormick C., Lindahl U., Lidholt K. The putative tumor suppressors EXT1 and EXT2 are glycosyltransferases required for the biosynthesis of heparan sulfate. J. Biol. Chem. 273:1998;26265-26268
41. Masai I., Lele Z., Yamaguchi M., Komori A., Nakata A., Nishiwaki Y., Wada H., Tanaka H., Nojima Y., Hammerschmidt M., et al. N-cadherin mediates retinal lamination, maintenance of forebrain compartments and patterning of retinal neurites. Development. 130:2003;2479-2494
42. McCormick C., Duncan G., Goutsos K.T., Tufaro F. 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. 97:2000;668-673
43. McFarlane S., McNeill L., Holt C.E. FGF signaling and target recognition in the developing Xenopus visual system. Neuron. 15:1995;1017-1028
44. McFarlane S., Cornel E., Amaya E., Holt C.E. Inhibition of FGF receptor activity in retinal ganglion cell axons causes errors in target recognition. Neuron. 17:1996;245-254
45. McLaughlin T., Hindges R., O'Leary D.D. Regulation of axial patterning of the retina and its topographic mapping in the brain. Curr. Opin. Neurobiol. 13:2003;57-69
46. Morio H., Honda Y., Toyoda H., Nakajima M., Kurosawa H., Shirasawa T. EXT gene family member rib-2 is essential for embryonic development and heparan sulfate biosynthesis in Caenorhabditis elegans. Biochem. Biophys. Res. Commun. 301:2003;317-323
47. Neff M.M., Turk E., Kalishman M. Web-based primer design for single nucleotide polymorphism analysis. Trends Genet. 18:2002;613-615
48. Nybakken K., Perrimon N. Heparan sulfate proteoglycan modulation of developmental signaling in Drosophila. Biochim. Biophys. Acta. 1573:2002;280-291
49. Pedersen L.C., Dong J., Taniguchi F., Kitagawa H., Krahn J.M., Pedersen L.G., Sugahara K., Negishi M. Crystal structure of an α1,4-N- acetylhexosaminyltransferase (EXTL2), a member of the exostosin gene family involved in heparan sulfate biosynthesis. J. Biol. Chem. 278:2003;14420-14428
50. Picker A., Brennan C., Reifers F., Clarke J.D., Holder N., Brand M. Requirement for the zebrafish mid-hindbrain boundary in midbrain polarisation, mapping and confinement of the retinotectal projection. Development. 126:1999;2967-2978
51. Princivalle M., de Agostini A. Developmental roles of heparan sulfate proteoglycans. a comparative review in Drosophila, mouse and human Int. J. Dev. Biol. 46:2002;267-278
52. Ronca F., Andersen J.S., Paech V., Margolis R.U. Characterization of Slit protein interactions with glypican-1. J. Biol. Chem. 276:2001;29141-29147
53. Schilling T.F., Piotrowski T., Grandel H., Brand M., Heisenberg C.P., Jiang Y.J., Beuchle D., Hammerschmidt M., Kane D.A., Mullins M.C., et al. Jaw and branchial arch mutants in zebrafish I. branchial arches Development. 123:1996;329-344
54. Schlessinger J., Lax I., Lemmon M. Regulation of growth factor activation by proteoglycans. what is the role of the low affinity receptors? Cell. 83:1995;357-360
55. Scholes J.H. Nerve fibre topography in the retinal projection to the tectum. Nature. 278:1979;620-624
56. Senay C., Lind T., Muguruma K., Tone Y., Kitagawa H., Sugahara K., Lidholt K., Lindahl U., Kusche-Gullberg M. The EXT1/EXT2 tumor suppressors. catalytic activities and role in heparan sulfate biosynthesis EMBO Rep. 1:2000;282-286
57. Shanmugalingam S., Houart C., Picker A., Reifers F., Macdonald R., Barth A., Griffin K., Brand M., Wilson S.W. Ace/Fgf8 is required for forebrain commissure formation and patterning of the telencephalon. Development. 127:2000;2549-2561
58. Steigemann P., Molitor A., Fellert S., Jackle H., Vorbruggen G. Heparan sulfate proteoglycan syndecan promotes axonal and myotube guidance by slit/robo signaling. Curr. Biol. 14:2004;225-230
59. Stickney H.L., Schmutz J., Woods I.G., Holtzer C.C., Dickson M.C., Kelly P.D., Myers R.M., Talbot W.S. Rapid mapping of zebrafish mutations with SNPs and oligonucleotide microarrays. Genome Res. 12:2002;1929-1934
60. Straznicky C., Gaze R.M., Horder T.J. Selection of appropriate medial branch of the optic tract by fibres of ventral retinal origin during development and in regeneration. an autoradiographic study in Xenopus J. Embryol. Exp. Morphol. 50:1979;253-267
61. Stuermer C.A. Retinotopic organization of the developing retinotectal projection in the zebrafish embryo. J. Neurosci. 8:1988;4513-4530
62. Takei Y., Ozawa Y., Sato M., Watanabe A., Tabata T. Three Drosophila EXT genes shape morphogen gradients through synthesis of heparan sulfate proteoglycans. Development. 131:2004;73-82
63. Talbot W.S., Schier A.F. Positional cloning of mutated zebrafish genes. Methods Cell Biol. 60:1999;259-286
64. The I., Bellaiche Y., Perrimon N. Hedgehog movement is regulated through tout velu-dependent synthesis of a heparan sulfate proteoglycan. Mol. Cell. 4:1999;633-639
65. Toyoda H., Kinoshita-Toyoda A., Selleck S.B. Structural analysis of glycosaminoglycans 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. 275:2000;2269-2275
66. Trowe T., Klostermann S., Baier H., Granato M., Crawford A.D., Grunewald B., Hoffmann H., Karlstrom R.O., Meyer S.U., Muller B., et al. Mutations disrupting the ordering and topographic mapping of axons in the retinotectal projection of the zebrafish, Danio rerio. Development. 123:1996;439-450
67. Udin S.B., Fawcett J.W. Formation of topographic maps. Annu. Rev. Neurosci. 11:1988;289-327
68. van Eeden F.J., Granato M., Schach U., Brand M., Furutani-Seiki M., Haffter P., Hammerschmidt M., Heisenberg C.P., Jiang Y.J., Kane D.A., et al. Genetic analysis of fin formation in the zebrafish, Danio rerio. Development. 123:1996;255-262
69. Walz A., McFarlane S., Brickman Y.G., Nurcombe V., Bartlett P.F., Holt C.E. Essential role of heparan sulfates in axon navigation and targeting in the developing visual system. Development. 124:1997;2421-2430
70. Zak B.M., Crawford B.E., Esko J.D. Hereditary multiple exostoses and heparan sulfate polymerization. Biochim. Biophys. Acta. 1573:2002;346-355