Distinct roles for Robo2 in the regulation of axon and dendrite growth by retinal ganglion cells

Mechanisms of Development

Volumn 127, Issue 1-2, 2010, Pages 36-48

  Hocking, Jennifer C ^a   Hehr, Carrie L ^a   Bertolesi, Gabriel E ^a   Wu, Jane Y ^b   McFarlane, Sarah ^a  

^a UNIVERSITY OF CALGARY   (Canada)

^b NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Axon guidance; Dendrite branching; Growth cone; Retina; Robo3; Slit proteins; Xenopus

Indexed keywords

CELL RECEPTOR; GROWTH FACTOR; PROTEIN ROBO2; PROTEIN ROBO3; PROTEIN SLIT1; ROUNDABOUT RECEPTOR; SLIT PROTEIN; SLIT2 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DENDRITE; EMBRYO; FEMALE; NERVE CELL GROWTH; NERVE CELL STIMULATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; RETINA BIPOLAR GANGLION CELL; RETINA DEVELOPMENT; RETINA GANGLION CELL; SIGNAL TRANSDUCTION; XENOPUS LAEVIS;

ANIMALS; AXONS; DENDRITES; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, DOMINANT; GREEN FLUORESCENT PROTEINS; GROWTH CONES; IN SITU HYBRIDIZATION; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; NERVE TISSUE PROTEINS; OLIGONUCLEOTIDES; RECEPTORS, IMMUNOLOGIC; RETINA; RETINAL GANGLION CELLS; SIGNAL TRANSDUCTION; XENOPUS LAEVIS; XENOPUS PROTEINS;

XENOPUS LAEVIS;

EID: 73649101691     PISSN: 09254773     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mod.2009.11.002     Document Type: Article

References (63)

1. Brose K., Bland K.S., Wang K.H., Arnott D., Henzel W., Goodman C.S., Tessier-Lavigne M., and Kidd T. Slit proteins bind Robo receptors and have an evolutionarily conserved role in repulsive axon guidance. Cell 96 (1999) 795-806
2. Campbell D.S., Stringham S.A., Timm A., Xiao T., Law M.Y., Baier H., Nonet M.L., and Chien C.B. Slit1a inhibits retinal ganglion cell arbourization and synaptogenesis via Robo2-dependent and -independent pathways. Neuron 55 (2007) 231-245
3. Camurri L., Mambetisaeva E., Davies D., Parnavelas J., Sundaresan V., and Andrews W. Evidence for the existence of two Robo3 isoforms with divergent biochemical properties. Mol. Cell. Neurosci. 30 (2005) 485-493
4. Challa A.K., Beattie C.E., and Seeger M.A. Identification and characterization of roundabout orthologs in zebrafish. Mech. Dev. 101 (2001) 249-253
5. Chalupa L.M., and Gunhan E. Development of On and Off retinal pathways and retinogeniculate projections. Prog. Retin. Eye Res. 23 (2004) 31-51
6. Chen J.H., Wu W., Li H.S., Fagaly T., Zhou L., Wu J.Y., and Rao Y. Embryonic expression and extracellular secretion of Xenopus slit. Neuroscience 96 (2000) 231-236
7. Chen Y.Y., Hehr C.L., Atkinson-Leadbeater K., Hocking J.C., and McFarlane S. Targeting of retinal axons requires the metalloproteinase ADAM10. J. Neurosci. 27 (2007) 8448-8456
8. Cohen-Cory S., and Fraser S.E. BDNF in the development of the visual system of Xenopus. Neuron 12 (1994) 747-761
9. Connor R.M., and Key B. Expression and role of Roundabout-1 in embryonic Xenopus forebrain. Dev. Dyn. 225 (2002) 22-34
10. Cornel E., and Holt C. Precocious pathfinding, retinal axons can navigate in an axonless brain. Neuron 9 (1992) 1001-1011
11. Devine C.A., and Key B. Robo-Slit interactions regulate longitudinal axon pathfinding in the embryonic vertebrate brain. Dev. Biol. 313 (2008) 371-383
12. Dickson B.J., and Gilestro G.F. Regulation of commissural axon pathfinding by slit and its Robo receptors. Annu. Rev. Cell Dev. Biol. 22 (2006) 651-675
13. Dimitova S., Reissaus A., and Tavosanis G. Slit and Robo regulate dendrite branching and elongation of space-filling neurons in Drosophila. Dev. Biol. 324 (2008) 18-30
14. Englund C., Steneberg P., Falileeva L., Xylourgidis N., and Samakovlis C. Attractive and repulsive functions of Slit are mediated by different receptors in the Drosophila trachea. Development 129 (2002) 4941-4951
15. Erskine L., and Herrera E. The retinal ganglion cell axon's journey: insights into molecular mechanisms of axon guidance. Dev. Biol. 308 (2007) 1-14
16. Erskine L., Williams S.E., Brose K., Kidd T., Rachel R.A., Goodman C.S., Tessier-Lavigne M., and Mason C.A. Retinal ganglion cell axon guidance in the mouse optic chiasm: expression and function of robos and slits. J. Neurosci. 20 (2000) 4975-4982
17. Fricke C., Lee J.S., Geiger-Rudolph S., Bonhoeffer F., and Chien C.B. Astray, a zebrafish roundabout homolog required for retinal axon guidance. Science 292 (2001) 507-510
18. Furrer M.P., Kim S., Wolf B., and Chiba A. Robo and Frazzled/DCC mediate dendritic guidance at the CNS midline. Nat. Neurosci. 6 (2003) 223-230
19. Furrer M.P., Vasenkova I., Kamiyama D., Rosado Y., and Chiba A. Slit and Robo control the development of dendrites in Drosophila CNS. Development 134 (2007) 3795-3804
20. Gascon E., Dayer A.G., Sauvain M.O., Potter G., Jenny B., De Roo M., Zgraggen E., Demaurex N., Muller D., and Kiss J.Z. GABA regulates dendritic growth by stabilizing lamellipodia in newly generated interneurons of the olfactory bulb. J. Neurosci. 26 (2006) 12956-12966
21. Haas K., Jensen K., Sin W.C., Foa L., and Cline H.T. Targeted electroporation in Xenopus tadpoles in vivo - from single cells to the entire brain. Differentiation 70 (2002) 148-154
22. Harland R.M. In situ hybridization: an improved whole-mount method for Xenopus embryos. Methods Cell Biol. 36 (1991) 685-695
23. Harris W.A., Holt C.E., and Bonhoeffer F. Retinal axons with and without their somata, growing to and arbourizing in the tectum of Xenopus embryos: a time-lapse video study of single fibres in vivo. Development 101 (1987) 123-133
24. Harris W.A., and Messersmith S.L. Two cellular inductions involved in photoreceptor determination in the Xenopus retina. Neuron 9 (1992) 357-372
25. Huang S., and Moody S.A. Dual expression of GABA or serotonin and dopamine in Xenopus amacrine cells is transient and may be regulated by laminar cues. Vis. Neurosci. 15 (1998) 969-977
26. Hiscock J., and Straznicky C. Neuropeptide Y- and substance P-like immunoreactive amacrine cells in the retina of the developing Xenopus laevis. Brain Res. Dev. Brain Res. 54 (1990) 105-113
27. Hivert B., Liu Z., Chuang C.Y., Doherty P., and Sundaresan V. Robo1 and Robo2 are homophilic binding molecules that promote axonal growth. Mol. Cell. Neurosci. 21 (2002) 534-545
28. Hocking J.C., Hehr C.L., Chang R.Y., Johnston J., and McFarlane S. TGFbeta ligands promote the initiation of retinal ganglion cell dendrites in vitro and in vivo. Mol. Cell. Neurosci. 37 (2008) 247-260
29. Hocking J.C., and McFarlane S. Expression of Bmp ligands and receptors in the developing Xenopus retina. Int. J. Dev. Biol. 51 (2007) 161-165
30. Holt C.E. A single-cell analysis of early retinal ganglion cell differentiation in Xenopus, from soma to axon tip. J. Neurosci. 9 (1989) 3123-3145
31. Hutson L.D., and Chien C.B. Pathfinding and error correction by retinal axons: the role of astray/robo2. Neuron 33 (2002) 205-217
32. Hutson L.D., Jurynec M.J., Yeo S.Y., Okamoto H., and Chien C.B. Two divergent slit1 genes in zebrafish. Dev. Dyn. 228 (2003) 358-369
33. Jen J.C., Chan W.M., Bosley T.M., Wan J., Carr J.R., Rub U., Shattuck D., Salamon G., Kudo L.C., Ou J., et al. Mutations in a human ROBO gene disrupt hindbrain axon pathway crossing and morphogenesis. Science 304 (2004) 1509-1513
34. Jin Z., Zhang J., Klar A., Chedotal A., Rao Y., Cepko C.L., and Bao Z.Z. Irx4-mediated regulation of Slit1 expression contributes to the definition of early axonal paths inside the retina. Development 130 (2003) 1037-1048
35. Lee J.S., Ray R., and 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. Lennox K.A., Sabel J.L., Johnson M.J., Moreira B.G., Fletcher C.A., Rose S.D., Behlke M.A., Laikhter A.L., Walder J.A., and Dagle J.M. Characterization of modified antisense oligonucleotides in Xenopus laevis embryos. Oligonucleotides 16 (2006) 26-42
37. Li H.S., Chen J.H., Wu W., Fagaly T., Zhou L., Yuan W., Dupuis S., Jiang Z.H., Nash W., Gick C., et al. Vertebrate slit, a secreted ligand for the transmembrane protein roundabout, is a repellent for olfactory bulb axons. Cell 96 (1999) 807-818
38. Lilienbaum A., Reszka A.A., Horwitz A.F., and Holt C.E. Chimeric integrins expressed in retinal ganglion cells impair process outgrowth in vivo. Mol. Cell. Neurosci. 6 (1995) 139-152
39. Lohmann C., Myhr K.L., and Wong R.O. Transmitter-evoked local calcium release stabilizes developing dendrites. Nature 418 (2002) 177-181
40. Lom B., Cogen J., Sanchez A.L., Vu T., and Cohen-Cory S. Local and target-derived brain-derived neurotrophic factor exert opposing effects on the dendritic arbourization of retinal ganglion cells in vivo. J. Neurosci. 22 (2002) 7639-7649
41. Lom B., and Cohen-Cory S. Brain-derived neurotrophic factor differentially regulates retinal ganglion cell dendritic and axonal arbourization in vivo. J. Neurosci. 19 (1999) 9928-9938
42. Ma L., and Tessier-Lavigne M. Dual branch-promoting and branch-repelling actions of Slit/Robo signalling on peripheral and central branches of developing sensory axons. J. Neurosci. 27 (2007) 6843-6851
43. McFarlane S., McNeill L., and Holt C.E. FGF signalling and target recognition in the developing Xenopus visual system. Neuron 15 (1995) 1017-1028
44. Miyashita T., Yeo S.Y., Hirate Y., Segawa H., Wada H., Little M.H., Yamada T., Takahashi N., and Okamoto H. PlexinA4 is necessary as a downstream target of Islet2 to mediate Slit signalling for promotion of sensory axon branching. Development 131 (2004) 3705-3715
45. Niclou S.P., Jia L., and Raper J.A. Slit2 is a repellent for retinal ganglion cell axons. J. Neurosci. 20 (2000) 4962-4974
46. Nieuwkoop, P.D., Faber, J., 1994. Normal Table of Xenopus laevis.
47. Piper M., Anderson R., Dwivedy A., Weinl C., van Horck F., Leung K.M., Cogill E., and Holt C. Signalling mechanisms underlying Slit2-induced collapse of Xenopus retinal growth cones. Neuron 49 (2006) 215-228
48. Plachez C., Andrews W., Liapi A., Knoell B., Drescher U., Mankoo B., Zhe L., Mambetisaeva E., Annan A., Bannister L., Parnavelas J.G., Richards L.J., and Sundaresan V. Robos are required for the correct targeting of retinal ganglion cell axons in the visual pathway of the brain. Mol. Cell. Neurosci. 37 (2008) 719-730
49. Plump A.S., Erskine L., Sabatier C., Brose K., Epstein C.J., Goodman C.S., Mason C.A., and Tessier-Lavigne M. Slit1 and Slit2 cooperate to prevent premature midline crossing of retinal axons in the mouse visual system. Neuron 33 (2002) 219-232
50. Polleux F., Morrow T., and Ghosh A. Semaphorin 3A is a chemoattractant for cortical apical dendrites. Nature 404 (2000) 567-573
51. Rayborn M.E., Sarthy P.V., Lam D.M., and Hollyfield J.G. The emergence, localization, and maturation of neurotransmitter systems during development of the retina in Xenopus laevis: II. Glycine. J. Comp. Neurol. 195 (1981) 585-593
52. Riehl R., Johnson K., Bradley R., Grunwald G.B., Cornel E., Lilienbaum A., and Holt C.E. Cadherin function is required for axon outgrowth in retinal ganglion cells in vivo. Neuron 17 (1996) 837-848
53. Ringstedt T., Braisted J.E., Brose K., Kidd T., Goodman C., Tessier-Lavigne M., and O'Leary D.D. Slit inhibition of retinal axon growth and its role in retinal axon pathfinding and innervation patterns in the diencephalon. J. Neurosci. 20 (2000) 4983-4991
54. Sabatier C., Plump A.S., Le M., Brose K., Tamada A., Murakami F., Lee E.Y., and Tessier-Lavigne M. The divergent Robo family protein rig-1/Robo3 is a negative regulator of slit responsiveness required for midline crossing by commissural axons. Cell 117 (2004) 157-169
55. Stein E., and Tessier-Lavigne M. Hierarchical organization of guidance receptors: silencing of netrin attraction by slit through a Robo/DCC receptor complex. Science 291 (2001) 1928-1938
56. Suli A., Mortimer N., Shepherd I., and Chien C.B. Netrin/DCC signalling controls contralateral dendrites of octavolateralis efferent neurons. J. Neurosci. 26 (2006) 13328-13337
57. Thompson H., Barker D., Camand O., and Erskine L. Slits contribute to the guidance of retinal ganglion cell axons in the mammalian optic tract. Dev. Biol. 296 (2006) 476-484
58. Thompson H., Camand O., Barker D., and Erskine L. Slit proteins regulate distinct aspects of retinal ganglion cell axon guidance within dorsal and ventral retina. J. Neurosci. 26 (2006) 8082-8091
59. Wang K.H., Brose K., Arnott D., Kidd T., Goodman C.S., Henzel W., and Tessier-Lavigne M. Biochemical purification of a mammalian slit protein as a positive regulator of sensory axon elongation and branching. Cell 96 (1999) 771-784
60. Whitford K.L., Marillat V., Stein E., Goodman C.S., Tessier-Lavigne M., Chedotal A., and Ghosh A. Regulation of cortical dendrite development by Slit-Robo interactions. Neuron 33 (2002) 47-61
61. Wong R.O., and Ghosh A. Activity-dependent regulation of dendritic growth and patterning. Nat. Rev. Neurosci. 3 (2002) 803-812
62. Yeo S.Y., Miyashita T., Fricke C., Little M.H., Yamada T., Kuwada J.Y., Huh T.L., Chien C.B., and Okamoto H. Involvement of Islet-2 in the Slit signalling for axonal branching and defasciculation of the sensory neurons in embryonic zebrafish. Mech. Dev. 121 (2004) 315-324
63. Yuan W., Zhou L., Chen J.H., Wu J.Y., Rao Y., and Ornitz D.M. The mouse SLIT family: secreted ligands for ROBO expressed in patterns that suggest a role in morphogenesis and axon guidance. Dev. Biol. 212 (1999) 290-306