Robo2 is required for Slit-mediated intraretinal axon guidance

Developmental Biology

Volumn 335, Issue 2, 2009, Pages 418-426

  Thompson, Hannah ^a,b   Andrews, William ^c   Parnavelas, John G ^c   Erskine, Lynda ^a,d  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b ROYAL VETERINARY COLLEGE   (United Kingdom)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

^d UNIVERSITY OF ABERDEEN   (United Kingdom)

Author keywords

Axon guidance; Development; Growth cone; Retina; Retinal ganglion cell; Robo; Slit; Visual system

Indexed keywords

ROBO2 PROTEIN; ROUNDABOUT RECEPTOR; SLIT PROTEIN; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EMBRYO; EMBRYO POLARITY; EYE DEVELOPMENT; MOUSE; NERVE FIBER GROWTH; NONHUMAN; OPTIC DISK; OPTIC NERVE FIBER; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETINA GANGLION CELL; SIGNAL TRANSDUCTION;

MUS; VERTEBRATA;

ANIMALS; AXONS; CELL POLARITY; IN SITU HYBRIDIZATION; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; MICE, INBRED C57BL; NERVE TISSUE PROTEINS; RECEPTORS, IMMUNOLOGIC; RETINAL GANGLION CELLS;

EID: 70350233259     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2009.09.034     Document Type: Article

References (53)

1. Andrews W., Barber M., Hernadez-Miranda L.R., Xian J., Rakic S., Sundaresan V., Rabbitts T.H., Pannell R., Rabbitts P., Thompson H., Erskine L., Murakami F., and Parnavelas J.G. The role of Slit-Robo signaling in the generation, migration and morphological differentiation of cortical interneurons. Dev. Biol. 313 (2008) 648-658
2. Avci H.X., Zelina P., Thelen K., and Pollerberg G.E. Role of cell adhesion molecule DM-GRASP in growth and orientation of retinal ganglion cell axons. Dev. Biol. 271 (2004) 291-305
3. Bao Z.Z. Intraretinal projection of retinal ganglion cell axons as a model system for studying axon navigation. Brain Res. 1992 (2008) 165-177
4. Birgbauer E., Cowan C.A., Sretavan D.W., and Henkemeyer M. Kinase independent function of EphB receptors in retinal axon pathfinding to the optic disc from dorsal but not ventral retina. Development 127 (2000) 1231-1241
5. Birgbauer E., Oster S.F., Severin C.G., and Sretavan D.W. Retinal axon growth cones respond to EphB extracellular domain as inhibitory guidance cues. Development 128 (2001) 3041-3048
6. Brittis P.A., and Silver J. Multiple factors govern intraretinal axon guidance: a time-lapse study. Mol. Cell. Neurosci. 6 (1995) 413-432
7. Brittis P.A., Canning D.R., and Silver J. Chondroitin sulfate as a regulator of neuronal patterning in the retina. Science 255 (1992) 733-736
8. Brittis P.A., Lemmon V., Rutishauser U., and Silver J. Unique changes of ganglion cell growth cone behavior following cell adhesion molecule perturbations: a time-lapse study of the living retina. Mol. Cell. Neurosci. 6 (1995) 433-449
9. 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
10. Deiner M.S., Kennedy T.E., Fazeli A., Serafini T., Tessier-Lavigne M., and Sretavan D.W. Netrin-1 and DCC mediate axon guidance locally at the optic disc: loss of function leads to optic nerve hypoplasia. Neuron 19 (1997) 575-589
11. Erskine L., and Herrera E. The retinal axon journey: insights into molecular mechanisms of axons guidance. Dev. Biol. 308 (2007) 1-14
12. Erskine L., and Thompson H. Intra-retinal axon guidance. In: Chalupa L.M., and Williams R.W. (Eds). Eye, Retina and Visual System of the Mouse (2008), MIT Press, Cambridge, Massachusetts 379-388
13. 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
14. 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
15. Höpker V.H., Shewan D., Tessier-Lavigne M., Poo M.M., and Holt C. Growth cone attraction to netrin-1 is converted to repulsion by laminin-1. Nature 401 (1999) 69-73
16. Huminiecki L., and Bicknell R. In silico cloning of novel endothelial-specific genes. Genome Res. 10 (2000) 1796-1806
17. Hussain S.A., Piper M., Fukuhara N., Strochlic L., Cho G., Howitt J.A., Ahmed Y., Powell A.K., Turnbull J.E., Holt C.E., and Hohenester E. A molecular mechanism for heparan sulfate dependence of slit-robo signaling. J. Biol. Chem. 281 (2006) 39693-39698
18. Hutson L.D., and Chien C.-B. Pathfinding and error correction by retinal axons: the role of astray/robo2. Neuron 33 (2002) 205-217
19. Inatani M., Irie F., Plump A.S., Tessier-Lavigne M., and Yamaguchi Y. Mammalian brain morphogenesis and midline axon guidance require heparan sulfate. Science 302 (2003) 1044-1046
20. Kidd T., Brose K., Mitchell K.J., Fetter R.D., Tessier-Lavigne M., Goodman C.S., and Tear G. Roundabout controls axon crossing of the CNS midline and defines a novel subfamily of evolutionarily conserved guidance receptors. Cell 92 (1998) 205-215
21. Kidd T., Bland K.S., and Goodman C.S. Slit is the midline repellent for the robo receptor in Drosophila. Cell 96 (1999) 785-794
22. Kolpak A., Zhang J., and Bao Z.Z. Sonic hedgehog has a dual effect on the growth of retinal ganglion axons depending on its concentration. J. Neurosci. 25 (2005) 3432-3441
23. Koshiba-Takeuchi K., Takeuchi J.K., Matsumoto K., Momose T., Uno K., Hoepker V., Ogura K., Takahashi N., Nakamura H., Yasuda K., and Oaura T. Tbx5 and the retinotectum projection. Science 287 (2000) 134-137
24. Liu J., Wilson S., and Reh T. BMP receptor 1b is required for axon guidance and cell survival in the developing retina. Dev. Biol. 256 (2003) 34-48
25. Long H., Sabatier C., Ma L., Plump A., Yuan W., Ornitz D.M., Tamada A., Murakami F., Goodman C.S., and Tessier-Lavigne M. Conserved roles for Slit and Robo proteins in commissural axon guidance. Neuron 42 (2004) 213-223
26. López-Bendito G., Flames N., Ma L., Fouquet C., Di Meglio T., Chedotal A., Tessier-Lavigne M., and Marin O. Robo1 and Robo2 cooperate to control the guidance of major axonal tracts in the mammalian forebrain. J. Neurosci. 27 (2007) 3395-3407
27. Lu W., van Eerde A.M., Fan X., Quintero-Rivera F., Kulkarni S., Ferguson H., Kim H.G., Fan Y., Xi Q., Sanlaville D., Andrews W., Sundaresan V., Bi W., Yan J., Giltay J.C., Wijmenga C., de Jong T.P., Feather S.A., Woolf A.S., Rao Y., Lupski J.R., Eccles M.R., Quade B.J., Guseall J.F., Morton C.C., and Maas R.L. Disruption of ROBO2 is associated with urinary tract anomalies and confers risk of vesicoureteral reflux. Am. J. Hum. Genet. 80 (2007) 616-632
28. Monnier P.P., Beck S.G., Bolz J., and Henke-Fahle S. The polysialic acid moiety of the neural cell adhesion molecule is involved in intraretinal guidance of retinal ganglion cell axons. Dev. Biol. 229 (2001) 1-14
29. Niclou S.P., Jia L., and Raper J.A. Slit2 is a repellent for retinal ganglion cell axons. J. Neurosci. 20 (2000) 4962-4974
30. Oster S.F., Bodeker M.O., He F., and Sretavan D.W. Invariant Sema5A inhibition serves an ensheathing function during optic nerve development. Development 130 (2003) 775-784
31. Ott H., Bastmeyer M., and Stuermer C.A. Neurolin, the goldfish homolog of DM-GRASP, is involved in retinal axon pathfinding to the optic disk. J. Neurosci. 18 (1998) 3363-3372
32. 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
33. 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
34. 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
35. Pollerberg G.E., and Beck-Sickinger A. A functional role for the middle extracellular region of the neural cell adhesion molecule (NCAM) in axonal fasciculation and orientation. Dev. Biol. 156 (1993) 324-340
36. Pratt T., Conway C.D., Tian N.M., Price D.J., and Mason J.O. Heparan sulphation patterns generated by distinct heparan sulfotransferase enzymes direct distinct aspects of retinal axon guidance at the optic chiasm. J. Neurosci. 26 (2006) 6911-6923
37. Rajagopalan S., Nicolas E., Vivancos V., Berger J., and Dickson B.J. Crossing the midline: roles and regulation of Robo receptors. Neuron 28 (2000) 767-777
38. Rajagopalan S., Vivancos V., Nicolas E., and Dickson B.J. Selecting a longitudinal pathway: Robo receptors specify the lateral position of axons in the Drosophila CNS. Cell 103 (2000) 1033-1045
39. 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
40. Rothberg J.M., Jacobs J.R., Goodman C.S., and Artavanis-Tsakonas S. Slit: an extracellular protein necessary for development of midline glia and commissural axon pathways contains both EGF and LRR domains. Genes Dev. 4 (1990) 2169-2187
41. Sabatier C., Plump A.S., Le Ma., 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
42. Sakuta H., Suzuki R., Takahashi H., Kato A., Shintani T., Lemura Si., Yamamoto T.S., Ueno N., and Noda M. Ventropin: aBMP-4 antagonist expressed in a double gradient pattern in the retina. Science 293 (2001) 111-116
43. Schulte D., Furukawa T., Peters M.A., Kozak C.A., and Cepko C.L. Misexpression of the Emx-related homeobox genes cVax and mVax2 ventralizes the retina and perturbs the retinotectal map. Neuron 24 (1999) 541-553
44. Seeger M., Tear G., Ferres-Marco D., and Goodman C.S. Mutations affecting growth cone guidance in Drosophila: genes necessary for guidance toward or away from the midline. Neuron 10 (1993) 409-426
45. Simpson J.H., Kidd T., Bland K.S., and Goodman C.S. Short-range and long-range guidance by slit and its Robo receptors. Robo and Robo2 play distinct roles in midline guidance. Neuron 28 (2000) 753-766
46. Simpson J.H., Bland K.S., Fetter R.D., and Goodman C.S. Short-range and long-range guidance by Slit and its Robo receptors: a combinatorial code of Robo receptors controls lateral position. Cell 103 (2000) 1019-1032
47. Thanos S. Genesis, neurotrophic responsiveness, and apoptosis of a pronounced direct connection between the two eyes of the chick embryo: a natural error or a meaningful developmental event?. J. Neurosci. 19 (1999) 3900-3917
48. 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
49. 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
50. Weiner J.A., Koo S.J., Nicolas S., Fraboulet S., Pfaff S.L., Pourquié O., and Sanes J.R. Axon fasciculation defects and retinal dysplasias in mice lacking the immunoglobulin superfamily adhesion molecule BEN/ALCAM/SC1. Mol. Cell. Neurosci. 27 (2004) 59-69
51. Yuan S.S., Cox L.A., Dasika G.K., and Lee E.Y. Cloning and functional studies of a novel gene aberrantly expressed in RB-deficient embryos. Dev. Biol. 207 (1999) 62-75
52. Zhang J., Jin Z., and Bao Z.Z. Disruption of gradient expression of Zic3 resulted in abnormal intraretinal axon projection. Development 131 (2004) 1553-1562
53. Zelina P., Avci H.X., Thelen K., and Pollerberg G.E. The cell adhesion molecule NrCAM is crucial for growth cone behaviour and pathfinding of retinal ganglion cell axons. Development 132 (2005) 3609-3618