Notum homolog plays a novel role in primary motor innervation

Journal of Neuroscience

Volumn 33, Issue 5, 2013, Pages 2177-2187

  Cantu, Jorge A ^a   Flowers, G Parker ^a   Topczewski, Jacek ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLINERGIC RECEPTOR; PROTEIN NOTUM 2; UNCLASSIFIED DRUG; ZEBRAFISH PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR; CONTROLLED STUDY; EMBRYO; GENE OVEREXPRESSION; GENE SILENCING; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; INNERVATION; MOTONEURON; MOTOR PERFORMANCE; NERVE FIBER GROWTH; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY; ZEBRA FISH;

ANIMALS; AXONS; CELL MOVEMENT; GROWTH CONES; HYDROLASES; MOTOR NEURONS; MUSCLE, SKELETAL; WNT SIGNALING PATHWAY; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84873027989     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3694-12.2013     Document Type: Article

References (73)

1. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403-410. CrossRef Medline
2. Ayers KL, Gallet A, Staccini-Lavenant L, Thérond PP (2010) The long-range activity of Hedgehog is regulated in the apical extracellular space by the glypican Dally and the hydrolase Notum. Dev Cell 18:605-620. CrossRef Medline
3. Beckett K, Franch-Marro X, Vincent JP (2008) Glypican-mediated endocytosis of Hedgehog has opposite effects in flies and mice. Trends Cell Biol 18:360-363. CrossRef Medline
4. Benowitz LI, Yin Y (2007) Combinatorial treatments for promoting axon regeneration in the CNS: strategies for overcoming inhibitory signals and activating neurons' intrinsic growth state. Dev Neurobiol 67:1148-1165. CrossRef Medline
5. Bulow HE, Tjoe N, Townley RA, Didiano D, van Kuppevelt TH, Hobert O (2008) Extracellular sugar modifications provide instructive and cellspecific information for axon-guidance choices. Curr Biol 18:1978-1985. CrossRef Medline
6. Capurro MI, Xu P, Shi W, Li F, Jia A, Filmus J (2008) Glypican-3 inhibits Hedgehog signaling during development by competing with Patched for Hedgehog binding. Developmental Cell 14:700-711. CrossRef Medline
7. Currie PD, Ingham PW (1996) Induction of a specific muscle cell type by a hedgehog-like protein in zebrafish. Nature 382:452-455. CrossRef Medline
8. Dickson BJ (2002) Molecular mechanisms of axon guidance. Science 298: 1959-1964. CrossRef Medline
9. Dolez M, Nicolas JF, Hirsinger E (2011) Laminins, via heparan sulfate proteoglycans, participate in zebrafish myotome morphogenesis by modulating the pattern of Bmp responsiveness. Development 138:97-106. CrossRef Medline
10. Du SJ, Devoto SH, Westerfield M, Moon RT (1997) Positive and negative regulation of muscle cell identity by members of the hedgehog and TGF- beta gene families. J Cell Biol 139:145-156. CrossRef Medline
11. Eisen JS (1999) Patterning motoneurons in the vertebrate nervous system. Trends Neurosci 22:321-326. CrossRef Medline
12. Eisen JS, Pike SH, Romancier B (1990) An identified motoneuron with variable fates in embryonic zebrafish. J Neurosci 10:34-43. Medline
13. Ekker M, Wegner J, Akimenko MA, Westerfield M (1992) Coordinate embryonic expression of three zebrafish engrailed genes. Development 116: 1001-1010. Medline
14. Feldner J, Becker T, Goishi K, Schweitzer J, Lee P, Schachner M, Klagsbrun M, Becker CG (2005) Neuropilin-1a is involved in trunk motor axon outgrowth in embryonic zebrafish. Dev Dyn 234:535-549. CrossRef Medline
15. Feldner J, Reimer MM, Schweitzer J, Wendik B, Meyer D, Becker T, Becker CG (2007) PlexinA3 restricts spinal exit points and branching of trunk motor nerves in embryonic zebrafish. J Neurosci 27:4978-4983. CrossRef Medline
16. Felsenfeld AL, Curry M, Kimmel CB (1991) The fub-1 mutation blocks initial myofibril formation in zebrafish muscle pioneer cells. Dev Biol 148: 23-30. CrossRef Medline
17. Fetcho JR, O'Malley DM (1995) Visualization of active neural circuitry in the spinal cord of intact zebrafish. J Neurophysiol 73:399-406. Medline
18. Filmus J, Capurro M, Rast J (2008) Glypicans. Genome Biol 9:224. CrossRef Medline
19. Flanagan-Steet H, Fox MA, Meyer D, Sanes JR (2005) Neuromuscular synapses can form in vivo by incorporation of initially aneural postsynaptic specializations. Development 132:4471-4481. CrossRef Medline
20. Flowers GP, Topczewska JM, Topczewski J (2012) A zebrafish Notum homolog specifically blocks the Wnt/ -catenin signaling pathway. Development 139:2416-2425. CrossRef Medline
21. Gerlitz O, Basler K (2002) Wingful, an extracellular feedback inhibitor of Wingless. Genes Dev 16:1055-1059. CrossRef Medline
22. Giráldez AJ, Copley RR, Cohen SM (2002) HSPG modification by the secreted enzyme Notum shapes the Wingless morphogen gradient. Dev Cell 2:667-676. CrossRef Medline
23. Glasgow E, Tomarev SI (1998) Restricted expression of the homeobox gene prox 1 in developing zebrafish. Mech Dev 76:175-178. CrossRef Medline
24. Grisaru S, Cano-Gauci D, Tee J, Filmus J, Rosenblum ND (2001) Glypican-3 modulates BMP- and FGF-mediated effects during renal branching morphogenesis. Dev Biol 231:31-46. CrossRef Medline
25. Gumienny TL, MacNeil LT, Wang H, de Bono M, Wrana JL, Padgett RW (2007) Glypican LON-2 is a conserved negative regulator of BMP-like signaling in Caenorhabditis elegans. Curr Biol 17:159-164. CrossRef Medline
26. Hale LA, Fowler DK, Eisen JS (2011) Netrin signaling breaks the equivalence between two identified zebrafish motoneurons revealing a new role of intermediate targets. PloS One 6:e25841. CrossRef Medline
27. Hatta K, Bremiller R, Westerfield M, Kimmel CB (1991) Diversity of expression of engrailed-like antigens in zebrafish. Development 112:821-832. Medline
28. Hilario JD, Rodino-Klapac LR, Wang C, Beattie CE (2009) Semaphorin 5A is a bifunctional axon guidance cue for axial motoneurons in vivo. Dev Biol 326:190-200. CrossRef Medline
29. Hilario JD, Wang C, Beattie CE (2010) Collagen XIXa1 is crucial for motor axon navigation at intermediate targets. Development 137:4261-4269. CrossRef Medline
30. Jing L, Lefebvre JL, Gordon LR, Granato M (2009) Wnt signals organize synaptic prepattern and axon guidance through the zebrafish unplugged/ MuSK receptor. Neuron 61:721-733. CrossRef Medline
31. Johnson KG, Ghose A, Epstein E, Lincecum J, O'Connor MB, Van Vactor D (2004) Axonal heparan sulfate proteoglycans regulate the distribution and efficiency of the repellent slit during midline axon guidance. Curr Biol 14:499-504. CrossRef Medline
32. Kantor DB, Chivatakarn O, Peer KL, Oster SF, Inatani M, Hansen MJ, Flanagan JG, Yamaguchi Y, Sretavan DW, Giger RJ, Kolodkin AL (2004) Semaphorin 5A is a bifunctional axon guidance cue regulated by heparan and chondroitin sulfate proteoglycans. Neuron 44:961-975. CrossRef Medline
33. Karlstrom R, Talbot WS, Schier AF (1999) Comparative synteny cloning of zebrafish you-too: mutations in the Hedgehog target gli2 affect ventral forebrain patterning. Genes Dev 13:388-393. CrossRef
34. Kim MJ, Liu IH, Song Y, Lee JA, Halfter W, Balice-Gordon RJ, Linney E, Cole GJ (2007) Agrin is required for posterior development and motor axon outgrowth and branching in embryonic zebrafish. Glycobiology 17:231-247. CrossRef Medline
35. Kimmel CB, Patterson J, Kimmel RO (1974) The development and behavioral characteristics of the startle response in the zebra fish. Dev Psychobiol 7:47-60. CrossRef Medline
36. Kimmel CB, Warga RM, Schilling TF (1990) Origin and organization of the zebrafish fate map. Development 108:581-594. Medline
37. Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF (1995) Stages of embryonic development of the zebrafish. Dev Dyn 203:253-310. CrossRef Medline
38. Krauss S, Concordet JP, Ingham PW (1993) A functionally conserved homolog of the Drosophila segment polarity gene hh is expressed in tissues with polarizing activity in zebrafish embryos. Cell 75:1431-1444. CrossRef Medline
39. Kreuger J, Perez L, Giráldez AJ, Cohen SM (2004) Opposing activities of Dally-like glypican at high and low levels of Wingless morphogen activity. Dev Cell 7:503-512. CrossRef Medline
40. Kwan KM, Fujimoto E, Grabher C, Mangum BD, Hardy ME, Campbell DS, Parant JM, Yost HJ, Kanki JP, Chien CB (2007) The Tol2kit: a multisite gateway-based construction kit for Tol2 transposon transgenesis constructs. Dev Dyn 236:3088-3099. CrossRef Medline
41. Lee JS, von der Hardt S, Rusch MA, Stringer SE, Stickney HL, Talbot WS, Geisler R, Nusslein-Volhard C, Selleck SB, Chien CB, Roehl H (2004) Axon sorting in the optic tract requires HSPG synthesis by ext2 (dackel) and extl3 (boxer). Neuron 44:947-960. CrossRef Medline
42. Lee P, Goishi K, Davidson AJ, Mannix R, Zon L, Klagsbrun M (2002) Neuropilin-1 is required for vascular development and is a mediator of VEGF-dependent angiogenesis in zebrafish. Proc Natl Acad Sci U S A 99:10470-10475. CrossRef Medline
43. Lefebvre JL, Jing L, Becaficco S, Franzini-Armstrong C, Granato M (2007) Differential requirement for MuSK and dystroglycan in generating patterns of neuromuscular innervation. Proc Natl Acad Sci U S A 104:2483-2488. CrossRef Medline
44. Liang Y, Annan RS, Carr SA, Popp S, Mevissen M, Margolis RK, Margolis RU (1999) Mammalian homologues of the Drosophila slit protein are ligands of the heparan sulfate proteoglycan glypican-1 in brain. J Biol Chem 274:17885-17892. CrossRef Medline
45. Liu DW, Westerfield M (1988) Function of identified motoneurones and co-ordination of primary and secondary motor systems during zebra fish swimming. J Physiol 403:73-89. Medline
46. Matsumoto Y, Irie F, Inatani M, Tessier-Lavigne M, Yamaguchi Y (2007) Netrin-1/DCC signaling in commissural axon guidance requires cellautonomous expression of heparan sulfate. J Neurosci 27:4342-4350. CrossRef Medline
47. Melancon E, Liu DW, Westerfield M, Eisen JS (1997) Pathfinding by identified zebrafish motoneurons in the absence of muscle pioneers. J Neurosci 17:7796-7804. Medline
48. Myers PZ, Eisen JS, Westerfield M (1986) Development and axonal outgrowth of identified motoneurons in the zebrafish. J Neurosci 6:2278-2289. Medline
49. Nakano Y, Kim HR, Kawakami A, Roy S, Schier AF, Ingham PW (2004) Inactivation of dispatched 1 by the chameleon mutation disrupts Hedgehog signalling in the zebrafish embryo. Dev Biol 269:381-392. CrossRef Medline
50. Nardini M, Dijkstra BW (1999) α/β Hydrolase fold enzymes: the family keeps growing. Curr Opin Struct Biol 9:732-737. CrossRef Medline
51. Nasevicius A, Ekker SC (2000) Effective targeted gene /'knockdown/' in zebrafish. Nat Genet 26:216-220. CrossRef Medline
52. O'Connor TP (1999) Intermediate targets and segmental pathfinding. Cell Mol Life Sci 55:1358-1364. CrossRef
53. Petersen CP, Reddien PW (2011) Polarized notum activation at wounds inhibits Wnt function to promote planarian head regeneration. Science 332:852-855. CrossRef Medline
54. Rawson JM, Dimitroff B, Johnson KG, Rawson JM, Ge X, Van Vactor D, Selleck SB (2005) The heparan sulfate proteoglycans Dally-like and syndecan have distinct functions in axon guidance and visual-system assembly in Drosophila. Curr Biol 15:833-838. CrossRef Medline
55. Rhiner C, Hengartner MO (2006) Sugar antennae for guidance signals: syndecans and glypicans integrate directional cues for navigating neurons. ScientificWorldJournal 6:1024-1036. CrossRef Medline
56. Ronca F, Andersen JS, Paech V, Margolis RU (2001) Characterization of Slit protein interactions with glypican-1. J Biol Chem 276:29141-29147. CrossRef Medline
57. Saint-Amant L, Drapeau P (1998) Time course of the development of motor behaviors in the zebrafish embryo. J Neurobiol 37:622-632. CrossRef Medline
58. Sato-Maeda M, Tawarayama H, Obinata M, Kuwada JY, Shoji W (2006) Sema3a1 guides spinal motor axons in a celland stage-specific manner in zebrafish. Development 133:937-947. CrossRef Medline
59. Schneider VA, Granato M (2006) The myotomal diwanka (lh3) glycosyltransferase and type XVIII collagen are critical for motor growth cone migration. Neuron 50:683-695. CrossRef Medline
60. Song HH, Shi W, Xiang YY, Filmus J (2005) The loss of glypican-3 induces alterations in Wnt signaling. J Biol Chem 280:2116-2125. CrossRef Medline
61. Summerton J, Weller D (1997) Morpholino antisense oligomers: design, preparation, and properties. Antisense Nucleic Acid Drug Dev 7:187-195. CrossRef Medline
62. Tan K, Duquette M, Liu JH, Zhang R, Joachimiak A, Wang JH, Lawler J (2006) The Structures of the thrombospondin-1 N-terminal domain and its complex with a synthetic pentameric heparin. Structure 14:33-42. CrossRef Medline
63. Tessier-Lavigne M, Goodman CS (1996) The molecular biology of axon guidance. Science 274:1123-1133. CrossRef Medline
64. Thisse C, Thisse B (2008) High-resolution in situ hybridization to wholemount zebrafish embryos. Nat Protoc 3:59-69. CrossRef Medline
65. Topczewski J, Sepich DS, Myers DC, Walker C, Amores A, Lele Z, Hammerschmidt M, Postlethwait J, Solnica-Krezel L (2001) The zebrafish glypican knypek controls cell polarity during gastrulation movements of convergent extension. Dev Cell 1:251-264. CrossRef Medline
66. Torisu Y, Watanabe A, Nonaka A, Midorikawa Y, Makuuchi M, Shimamura T, Sugimura H, Niida A, Akiyama T, Iwanari H, Kodama T, Zeniya M, Aburatani H (2008) Human homolog of NOTUM, overexpressed in hepatocellular carcinoma, is regulated transcriptionally by -catenin/ TCF. Cancer Sci 99:1139-1146. CrossRef Medline
67. Traister A, Shi W, Filmus J (2008) Mammalian Notum induces the release of glypicans and other GPI-anchored proteins from the cell surface. Biochem J 410:503-511. CrossRef Medline
68. Villefranc JA, Amigo J, Lawson ND (2007) Gateway compatible vectors for analysis of gene function in the zebrafish. Dev Dyn 236:3077-3087. CrossRef Medline
69. Westerfield M, McMurray JV, Eisen JS (1986) Identified motoneurons and their innervation of axial muscles in the zebrafish. J Neurosci 6:2267-2277. Medline
70. Yaron A, Zheng B (2007) Navigating their way to the clinic: Emerging roles for axon guidance molecules in neurological disorders and injury. Dev Neurobiol 67:1216-1231. CrossRef Medline
71. Yee CS, Chandrasekhar A, Halloran MC, Shoji W, Warren JT, Kuwada JY (1999) Molecular cloning, expression, and activity of zebrafish semaphorin Z1a. Brain Res Bull 48:581-593. CrossRef Medline
72. Zhang J, Granato M (2000) The zebrafish unplugged gene controls motor axon pathway selection. Development 127:2099-2111. Medline
73. Zhang J, Lefebvre JL, Zhao S, Granato M (2004) Zebrafish unplugged reveals a role for muscle-specific kinase homologs in axonal pathway choice. Nat Neurosci 7:1303-1309. CrossRef Medline