Axon guidance at the midline: of mice and flies

Current Opinion in Neurobiology

Volumn 20, Issue 1, 2010, Pages 79-85

  Evans, Timothy A ^a   Bashaw, Greg J ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN; EPHRIN A4; EPHRIN B3; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; NETRIN; RETINOIC ACID INDUCIBLE PROTEIN I; ROUNDABOUT RECEPTOR; SLIT PROTEIN; SONIC HEDGEHOG PROTEIN; STEM CELL FACTOR; WNT PROTEIN;

BRAIN DEVELOPMENT; CELL SURFACE; DOWN REGULATION; NERVE FIBER; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; RNA INTERFERENCE; SIGNAL TRANSDUCTION; SPINAL CORD; THALAMUS MIDLINE NUCLEUS;

ANIMALS; AXONS; BODY PATTERNING; CELL MOVEMENT; DROSOPHILA; MICE; NERVE GROWTH FACTORS; NERVE TISSUE PROTEINS; NEUROGENESIS;

EID: 76749140017     PISSN: 09594388     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.conb.2009.12.006     Document Type: Review

References (34)

1. 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
2. Moore S.W., Tessier-Lavigne M., and Kennedy T.E. Netrins and their receptors. Adv Exp Med Biol 621 (2007) 17-31
3. O'Donnell M., Chance R.K., and Bashaw G.J. Axon growth and guidance: receptor regulation and signal transduction. Annu Rev Neurosci 32 (2009) 383-412
4. Kennedy T.E., Wang H., Marshall W., and Tessier-Lavigne M. Axon guidance by diffusible chemoattractants: a gradient of netrin protein in the developing spinal cord. J Neurosci 26 (2006) 8866-8874
5. Brankatschk M., and Dickson B.J. Netrins guide Drosophila commissural axons at short range. Nat Neurosci 9 (2006) 188-194
6. Charron F., Stein E., Jeong J., McMahon A.P., and Tessier-Lavigne M. The morphogen sonic hedgehog is an axonal chemoattractant that collaborates with netrin-1 in midline axon guidance. Cell 113 (2003) 11-23
7. Augsburger A., Schuchardt A., Hoskins S., Dodd J., and Butler S. BMPs as mediators of roof plate repulsion of commissural neurons. Neuron 24 (1999) 127-141
8. Okada A., Charron F., Morin S., Shin D.S., Wong K., Fabre P.J., Tessier-Lavigne M., and McConnell S.K. Boc is a receptor for sonic hedgehog in the guidance of commissural axons. Nature 444 (2006) 369-373
9. Yam P.T., Langlois S.D., Morin S., and Charron F. Sonic hedgehog guides axons through a noncanonical. Src-family-kinase-dependent signaling pathway. Neuron 62 (2009) 349-362. In this paper, a comprehensive series of experiments demonstrate that the role of Shh in promoting commissural axon attraction to the floor plate is independent of its role in regulating gene expression through the Gli transcription factors. Instead, the authors show using a combination of in vitro coculture experiments and in vivo genetic manipulations that Shh controls growth cone turning by regulating the asymmetric activation of Src family tyrosine kinases.
10. Yamauchi K., Phan K.D., and Butler S.J. BMP type I receptor complexes have distinct activities mediating cell fate and axon guidance decisions. Development 135 (2008) 1119-1128
11. ••].
12. ••].
13. •] suggests that DSCAM can also promote midline crossing independently of Netrin.
14. Hattori D., Millard S.S., Wojtowicz W.M., and Zipursky S.L. Dscam-mediated cell recognition regulates neural circuit formation. Annu Rev Cell Dev Biol 24 (2008) 597-620
15. Keleman K., Rajagopalan S., Cleppien D., Teis D., Paiha K., Huber L.A., Technau G.M., and Dickson B.J. Comm sorts robo to control axon guidance at the Drosophila midline. Cell 110 (2002) 415-427
16. Keleman K., Ribeiro C., and Dickson B.J. Comm function in commissural axon guidance: cell-autonomous sorting of Robo in vivo. Nat Neurosci 8 (2005) 156-163
17. Gilestro G.F. Redundant mechanisms for regulation of midline crossing in Drosophila. PLoS ONE 3 (2008) e3798
18. Yang L., Garbe D.S., and Bashaw G.J. A frazzled/DCC-dependent transcriptional switch regulates midline axon guidance. Science 324 5929 (2009) 944-947. This paper reports that besides mediating attraction in response to Netrin, the Drosophila Fra receptor functions independently of Netrin to regulate the mRNA expression of Commissureless, a key regulator of midline repulsion. Genetic evidence suggests that this dual function of Fra promotes midline crossing by coupling attraction to the downregulation of Slit repulsion.
19. 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
20. Chen Z., Gore B.B., Long H., Ma L., and Tessier-Lavigne M. Alternative splicing of the Robo3 axon guidance receptor governs the midline switch from attraction to repulsion. Neuron 58 (2008) 325-332. In this study, the authors report the discovery that the divergent Robo receptor Rig1/Robo3 has dual functions in the control of midline crossing in the spinal cord. The authors demonstrate that the Robo3 locus is alternatively spliced to produce two isoforms that have distinct roles in precrossing versus postcrossing commissural axons. Robo3.1 promotes crossing by preventing premature responses to Slit, while Robo3.2 cooperates with the Robo1 receptor to prevent postcrossing commissural axons from re-entering the midline.
21. Di Meglio T., Nguyen-Ba-Charvet K.T., Tessier-Lavigne M., Sotelo C., and Chedotal A. Molecular mechanisms controlling midline crossing by precerebellar neurons. J Neurosci 28 (2008) 6285-6294
22. Gore B.B., Wong K.G., and Tessier-Lavigne M. Stem cell factor functions as an outgrowth-promoting factor to enable axon exit from the midline intermediate target. Neuron 57 (2008) 501-510. In this study a novel function for floor plate derived stem cell factor (SCF) and its neuronal receptor Kit is reported. Loss-of-function genetic experiments demonstrate that in the absence of SCF or Kit commissural axons accumulate at the contralateral edge of the floor plate. In vitro, SCF is shown to selectively promote the outgrowth of postcrossing commissural axons. Thus, in addition to midline repellants, the regulation of midline exit requires the outgrowth-promoting function of SCF.
23. 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
24. Garbe D.S., and Bashaw G.J. Independent functions of Slit-Robo repulsion and Netrin-Frazzled attraction regulate axon crossing at the midline in Drosophila. J Neurosci 27 (2007) 3584-3592
25. Zou Y., Stoeckli E., Chen H., and Tessier-Lavigne M. Squeezing axons out of the gray matter: a role for slit and semaphorin proteins from midline and ventral spinal cord. Cell 102 (2000) 363-375
26. Kullander K., Butt S.J., Lebret J.M., Lundfald L., Restrepo C.E., Rydstrom A., Klein R., and Kiehn O. Role of EphA4 and EphrinB3 in local neuronal circuits that control walking. Science 299 (2003) 1889-1892
27. ••].
28. ••].
29. ••].
30. ••] describe the characterization of the Rac-specific GTPase activating protein alpha2-chimaerin and its role in EphA4 receptor forward signaling. Knock-out of alpha2-chimaerin leads to phenotypes at the anatomical and behavioral levels that are indistinguishable from loss of either the ephrinB3 ligand or the EphA4 receptor. Specifically, alpha2-chimaerin is shown to be a key signaling molecule that regulates midline repulsion of axons of the corticospinal tract, as well as interneurons of the CPG. All three studies report biochemical and cell culture experiments that support the model that alpha2-chimaerin directly couples the EphA4 receptor to the regulation of Rac activity and is required for growth cone collapse. This is the clearest demonstration to date that an individual signaling molecule is required for all of the guidance activity of a specific receptor.
31. Stoeckli E.T. Longitudinal axon guidance. Curr Opin Neurobiol 16 (2006) 35-39
32. 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 midline commissural axon guidance. Neuron 42 (2004) 213-223
33. Farmer W.T., Altick A.L., Nural H.F., Dugan J.P., Kidd T., Charron F., and Mastick G.S. Pioneer longitudinal axons navigate using floor plate and Slit/Robo signals. Development 135 (2008) 3643-3653
34. Kastenhuber E., Kern U., Bonkowsky J.L., Chien C.B., Driever W., and Schweitzer J. Netrin-DCC, Robo-Slit, and heparan sulfate proteoglycans coordinate lateral positioning of longitudinal dopaminergic diencephalospinal axons. J Neurosci 29 (2009) 8914-8926