Sonic Hedgehog regulates its own receptor on postcrossing commissural axons in a glypican1-dependent manner

Neuron

Volumn 79, Issue 3, 2013, Pages 478-491

  Wilson, Nicole H ^a   Stoeckli, Esther T ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

GLYPICAN 1; HEDGEHOG INTERACTING PROTEIN; MESSENGER RNA; RECEPTOR; SONIC HEDGEHOG PROTEIN; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; AXON GUIDANCE; BRAIN COMMISSURE; CHICK EMBRYO; CONTROLLED STUDY; EMBRYO; GENE EXPRESSION; GENE INTERACTION; GROWTH CONE; NERVE FIBER; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; AXONS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BODY PATTERNING; CARRIER PROTEINS; CERCOPITHECUS AETHIOPS; CHICK EMBRYO; COS CELLS; FUNCTIONAL LATERALITY; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLYPICANS; GREEN FLUORESCENT PROTEINS; HEDGEHOGS; IMMUNOPRECIPITATION; MEMBRANE GLYCOPROTEINS; MICRORNAS; MOLECULAR SEQUENCE DATA; MUTATION; NEURAL TUBE; SPINAL CORD;

EID: 84881499818     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2013.05.025     Document Type: Article

References (56)

1. Augsburger A., Schuchardt A., Hoskins S., Dodd J., Butler S. BMPs as mediators of roof plate repulsion of commissural neurons. Neuron 1999, 24:127-141.
2. Barik S. Megaprimer PCR. Methods Mol. Biol. 2002, 192:189-196.
3. Beckett K., Franch-Marro X., Vincent J.-P. Glypican-mediated endocytosis of Hedgehog has opposite effects in flies and mice. Trends Cell Biol. 2008, 18:360-363.
4. Bijlsma M.F., Damhofer H., Roelink H. Hedgehog-stimulated chemotaxis is mediated by smoothened located outside the primary cilium. Sci. Signal. 2012, 5:ra60.
5. Bonneh-Barkay D., Shlissel M., Berman B., Shaoul E., Admon A., Vlodavsky I., Carey D.J., Asundi V.K., Reich-Slotky R., Ron D. Identification of glypican as a dual modulator of the biological activity of fibroblast growth factors. J.Biol. Chem. 1997, 272:12415-12421.
6. Bourikas D., Pekarik V., Baeriswyl T., Grunditz A., Sadhu R., Nardó M., Stoeckli E.T. Sonic hedgehog guides commissural axons along the longitudinal axis of the spinal cord. Nat. Neurosci. 2005, 8:297-304.
7. Briscoe J., Chen Y., Jessell T.M., Struhl G. A hedgehog-insensitive form of patched provides evidence for direct long-range morphogen activity of sonic hedgehog in the neural tube. Mol. Cell 2001, 7:1279-1291.
8. Buttitta L., Mo R., Hui C.-C., Fan C.-M. Interplays of Gli2 and Gli3 and their requirement in mediating Shh-dependent sclerotome induction. Development 2003, 130:6233-6243.
9. Capurro M.I., Xu P., Shi W., Li F., Jia A., Filmus J. Glypican-3 inhibits Hedgehog signaling during development by competing with patched for Hedgehog binding. Dev. Cell 2008, 14:700-711.
10. Chan J.A., Balasubramanian S., Witt R.M., Nazemi K.J., Choi Y., Pazyra-Murphy M.F., Walsh C.O., Thompson M., Segal R.A. Proteoglycan interactions with Sonic Hedgehog specify mitogenic responses. Nat. Neurosci. 2009, 12:409-417.
11. Charron F., Stein E., Jeong J., McMahon A.P., Tessier-Lavigne M. The morphogen sonic hedgehog is an axonal chemoattractant that collaborates with netrin-1 in midline axon guidance. Cell 2003, 113:11-23.
12. Chédotal A. Further tales of the midline. Curr. Opin. Neurobiol. 2011, 21:68-75.
13. Chuang P.-T., McMahon A.P. Vertebrate Hedgehog signalling modulated by induction of a Hedgehog-binding protein. Nature 1999, 397:617-621.
14. Condron B. Gene expression is required for correct axon guidance. Curr. Biol. 2002, 12:1665-1669.
15. Das R.M., Van Hateren N.J., Howell G.R., Farrell E.R., Bangs F.K., Porteous V.C., Manning E.M., McGrew M.J., Ohyama K., Sacco M.A., et al. A robust system for RNA interference in the chicken using a modified microRNA operon. Dev. Biol. 2006, 294:554-563.
16. Domanitskaya E., Wacker A., Mauti O., Baeriswyl T., Esteve P., Bovolenta P., Stoeckli E.T. Sonic hedgehog guides post-crossing commissural axons both directly and indirectly by regulating Wnt activity. J.Neurosci. 2010, 30:11167-11176.
17. Filmus J., Capurro M., Rast J. Glypicans. Genome Biol. 2008, 9:224.
18. Goodrich L.V., Johnson R.L., Milenkovic L., McMahon J.A., Scott M.P. Conservation of the hedgehog/patched signaling pathway from flies to mice: induction of a mouse patched gene by Hedgehog. Genes Dev. 1996, 10:301-312.
19. Hamburger V., Hamilton H.L. A series of normal stages in the development of the chick embryo. J.Morphol. 1951, 88:49-92.
20. Hu H. Cell-surface heparan sulfate is involved in the repulsive guidance activities of Slit2 protein. Nat. Neurosci. 2001, 4:695-701.
21. Hynes M., Ye W., Wang K., Stone D., Murone M., Sauvage Fd., Rosenthal A. The seven-transmembrane receptor smoothened cell-autonomously induces multiple ventral cell types. Nat. Neurosci. 2000, 3:41-46.
22. Islam S.M., Shinmyo Y., Okafuji T., Su Y., Naser I.B., Ahmed G., Zhang S., Chen S., Ohta K., Kiyonari H., et al. Draxin, a repulsive guidance protein for spinal cord and forebrain commissures. Science 2009, 323:388-393.
23. 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. 2004, 14:499-504.
24. Joset P., Wacker A., Babey R., Ingold E.A., Andermatt I., Stoeckli E.T., Gesemann M. Rostral growth of commissural axons requires the cell adhesion molecule MDGA2. Neural Dev. 2011, 6:22.
25. Kee N., Wilson N., De Vries M., Bradford D., Key B., Cooper H.M. Neogenin and RGMa control neural tube closure and neuroepithelial morphology by regulating cell polarity. J.Neurosci. 2008, 28:12643-12653.
26. Kennedy T.E., Serafini T., de la Torre J.R., Tessier-Lavigne M. Netrins are diffusible chemotropic factors for commissural axons in the embryonic spinal cord. Cell 1994, 78:425-435.
27. Kidd T., Russell C., Goodman C.S., Tear G. Dosage-sensitive and complementary functions of roundabout and commissureless control axon crossing of the CNS midline. Neuron 1998, 20:25-33.
28. Kim M.-S., Saunders A.M., Hamaoka B.Y., Beachy P.A., Leahy D.J. Structure of the protein core of the glypican Dally-like and localization of a region important for hedgehog signaling. Proc. Natl. Acad. Sci. USA 2011, 108:13112-13117.
29. Li F., Shi W., Capurro M., Filmus J. Glypican-5 stimulates rhabdomyosarcoma cell proliferation by activating Hedgehog signaling. J.Cell Biol. 2011, 192:691-704.
30. Long H., Sabatier C., Ma L., Plump A., Yuan W., Ornitz D.M., Tamada A., Murakami F., Goodman C.S., Tessier-Lavigne M. Conserved roles for Slit and Robo proteins in midline commissural axon guidance. Neuron 2004, 42:213-223.
31. Lyuksyutova A.I., Lu C.-C., Milanesio N., King L.A., Guo N., Wang Y., Nathans J., Tessier-Lavigne M., Zou Y. Anterior-posterior guidance of commissural axons by Wnt-frizzled signaling. Science 2003, 302:1984-1988.
32. Mauti O., Sadhu R., Gemayel J., Gesemann M., Stoeckli E.T. Expression patterns of plexins and neuropilins are consistent with cooperative and separate functions during neural development. BMC Dev. Biol. 2006, 6:32.
33. Nawabi H., Briançon-Marjollet A., Clark C., Sanyas I., Takamatsu H., Okuno T., Kumanogoh A., Bozon M., Takeshima K., Yoshida Y., et al. A midline switch of receptor processing regulates commissural axon guidance in vertebrates. Genes Dev. 2010, 24:396-410.
34. Niederkofler V., Baeriswyl T., Ott R., Stoeckli E.T. Nectin-like molecules/SynCAMs are required for post-crossing commissural axon guidance. Development 2010, 137:427-435.
35. Okada A., Charron F., Morin S., Shin D.S., Wong K., Fabre P.J., Tessier-Lavigne M., McConnell S.K. Boc is a receptor for sonic hedgehog in the guidance of commissural axons. Nature 2006, 444:369-373.
36. Oliver T.G., Grasfeder L.L., Carroll A.L., Kaiser C., Gillingham C.L., Lin S.M., Wickramasinghe R., Scott M.P., Wechsler-Reya R.J. Transcriptional profiling of the Sonic hedgehog response: a critical role for N-myc in proliferation of neuronal precursors. Proc. Natl. Acad. Sci. USA 2003, 100:7331-7336.
37. Parra L.M., Zou Y. Sonic hedgehog induces response of commissural axons to Semaphorin repulsion during midline crossing. Nat. Neurosci. 2010, 13:29-35.
38. Parsons B.D., Schindler A., Evans D.H., Foley E. A direct phenotypic comparison of siRNA pools and multiple individual duplexes in a functional assay. PLoS ONE 2009, 4:e8471.
39. Rawson J.M., Dimitroff B., Johnson K.G., Rawson J.M., Ge X., Van Vactor D., Selleck S.B. The heparan sulfate proteoglycans Dally-like and Syndecan have distinct functions in axon guidance and visual-system assembly in Drosophila. Curr. Biol. 2005, 15:833-838.
40. Rikin A., Rosenfeld G.E., McCartin K., Evans T. A reverse genetic approach to test functional redundancy during embryogenesis. J.Vis. Exp. 2010, 42:e2020.
41. Ronca F., Andersen J.S., Paech V., Margolis R.U. Characterization of Slit protein interactions with glypican-1. J.Biol. Chem. 2001, 276:29141-29147.
42. Sánchez-Camacho C., Bovolenta P. Emerging mechanisms in morphogen-mediated axon guidance. Bioessays 2009, 31:1013-1025.
43. Smart A.D., Course M.M., Rawson J., Selleck S., Van Vactor D., Johnson K.G. Heparan sulfate proteoglycan specificity during axon pathway formation in the Drosophila embryo. Dev. Neurobiol. 2011, 71:608-618.
44. Stoeckli E.T., Landmesser L.T. Axonin-1, Nr-CAM, and Ng-CAM play different roles in the invivo guidance of chick commissural neurons. Neuron 1995, 14:1165-1179.
45. Tenzen T., Allen B.L., Cole F., Kang J.-S., Krauss R.S., McMahon A.P. The cell surface membrane proteins Cdo and Boc are components and targets of the Hedgehog signaling pathway and feedback network in mice. Dev. Cell 2006, 10:647-656.
46. Williams E.H., Pappano W.N., Saunders A.M., Kim M.-S., Leahy D.J., Beachy P.A. Dally-like core protein and its mammalian homologues mediate stimulatory and inhibitory effects on Hedgehog signal response. Proc. Natl. Acad. Sci. USA 2010, 107:5869-5874.
47. Wilson N.H., Key B. Neogenin interacts with RGMa and netrin-1 toguide axons within the embryonic vertebrate forebrain. Dev. Biol. 2006, 296:485-498.
48. Wilson N.H., Stoeckli E.T. Cell type specific, traceable gene silencing for functional gene analysis during vertebrate neural development. Nucleic Acids Res. 2011, 39:e133.
49. Wilson N.H., Stoeckli E.T. In ovo electroporation of miRNA-based plasmids in the developing neural tube and assessment of phenotypes by DiI injection in open-book preparations. J.Vis. Exp. 2012, 68:e4384.
50. Yam P.T., Langlois S.D., Morin S., Charron F. Sonic hedgehog guides axons through a noncanonical, Src-family-kinase-dependent signaling pathway. Neuron 2009, 62:349-362.
51. Yam P.T., Kent C.B., Morin S., Farmer W.T., Alchini R., Lepelletier L., Colman D.R., Tessier-Lavigne M., Fournier A.E., Charron F. 14-3-3 proteins regulate a cell-intrinsic switch from sonic hedgehog-mediated commissural axon attraction to repulsion after midline crossing. Neuron 2012, 76:735-749.
52. Yan D., Wu Y., Yang Y., Belenkaya T.Y., Tang X., Lin X. The cell-surface proteins Dally-like and Ihog differentially regulate Hedgehog signaling strength and range during development. Development 2010, 137:2033-2044.
53. Yang L., Garbe D.S., Bashaw G.J. A frazzled/DCC-dependent transcriptional switch regulates midline axon guidance. Science 2009, 324:944-947.
54. Zhang X., Liu C., Nestor K.E., McFarland D.C., Velleman S.G. The effect of glypican-1 glycosaminoglycan chains on turkey myogenic satellite cell proliferation, differentiation, and fibroblast growth factor 2 responsiveness. Poult. Sci. 2007, 86:2020-2028.
55. Zheng L., Baumann U., Reymond J.L. An efficient one-step site-directed and site-saturation mutagenesis protocol. Nucleic Acids Res. 2004, 32:e115.
56. Zou Y., Stoeckli E., Chen H., Tessier-Lavigne M. Squeezing axons out of the gray matter: a role for slit and semaphorin proteins from midline and ventral spinal cord. Cell 2000, 102:363-375.