Independent functions of slit-robo repulsion and Netrin-Frazzled attraction regulate axon crossing at the midline in Drosophila

Journal of Neuroscience

Volumn 27, Issue 13, 2007, Pages 3584-3592

  Garbe, David S ^a   Bashaw, Greg J ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Attraction; Axon guidance; DCC Frazzled; Midline; Netrin; Repulsion; Robo; Slit

Indexed keywords

FRA RECEPTOR; MUTANT PROTEIN; NETRIN; RECEPTOR PROTEIN; ROUNDABOUT RECEPTOR; SLIT PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; DROSOPHILA; NERVE CELL; NERVE FIBER; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION;

ANIMALS; AXONS; BODY PATTERNING; DROSOPHILA; DROSOPHILA PROTEINS; GENE EXPRESSION; MUTATION; NERVE TISSUE PROTEINS; RECEPTORS, CELL SURFACE; RECEPTORS, IMMUNOLOGIC;

EID: 34047156566     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0301-07.2007     Document Type: Article

References (42)

1. Bashaw GJ, Goodman CS (1999) Chimeric axon guidance receptors: the cytoplasmic domains of slit and netrin receptors specify attraction versus repulsion. Cell 97:917-926.
2. Bashaw GJ, Kidd T, Murray D, Pawson T, Goodman CS (2000) Repulsive axon guidance: Abelson and Enabled play opposing roles downstream of the roundabout receptor. Cell 101:703-715.
3. Bhat KM (2005) Slit-roundabout signaling neutralizes netrin-Frazzled- mediated attractant cue to specify the lateral positioning of longitudinal axon pathways. Genetics 170:149-159.
4. Bossing T, Udolph G, Doe CQ, Technau GM (1996) The embryonic central nervous system lineages of Drosophila melanogaster. I. Neuroblast lineages derived from the ventral half of the neuroectoderm. Dev Biol 179:41-64.
5. Brankatschk M, Dickson BJ (2006) Netrins guide Drosophila commissural axons at short range. Nat Neurosci 9:188-194.
6. Brose K, Tessier-Lavigne M (2000) Slit proteins: key regulators of axon guidance, axonal branching, and cell migration. Curr Opin Neurobiol 10:95-102.
7. Brose K, Bland KS, Wang KH, Arnott D, Henzel W, Goodman CS, Tessier-Lavigne M, Kidd T (1999) Slit proteins bind Robo receptors and have an evolutionarily conserved role in repulsive axon guidance. Cell 96:795-806.
8. Dickson BJ (2001) Rho GTPases in growth cone guidance. Curr Opin Neurobiol 11:103-110.
9. Dittrich R, Bossing T, Gould AP, Technau GM, Urban J (1997) The differentiation of the serotonergic neurons in the Drosophila ventral nerve cord depends on the combined function of the zinc finger proteins Eagle and Huckebein. Development 124:2515-2525.
10. Forsthoefel DJ, Liebl EC, Kolodziej PA, Seeger MA (2005) The Abelson tyrosine kinase, the Trio GEF and Enabled interact with the Netrin receptor Frazzled in Drosophila. Development 132:1983-1994.
11. Garbe D, Bashaw G (2004) Axon guidance at the midline: from mutants to mechanisms. Crit Rev Biochem Mol Biol 39:319-341.
12. Garbe DS, Das A, Dubreuil RR, Bashaw GJ (2006) beta-Spectrin functions independently of Ankyrin to regulate the establishment and maintenance of axon connections in the Drosophila embryonic CNS. Development 134:273-284.
13. Hao JC, Yu TW, Fujisawa K, Culotti JG, Gengyo-Ando K, Mitani S, Moulder G, Barstead R, Tessier-Lavigne M, Bargmann CI (2001) C. elegans slit acts in midline, dorsal-ventral, and anterior-posterior guidance via the SAX-3/Robo receptor. Neuron 32:25-38.
14. Harris R, Sabatelli LM, Seeger MA (1996) Guidance cues at the Drosophila CNS midline: identification and characterization of two Drosophila Netrin/UNC-6 homologs. Neuron 17:217-228.
15. Higashijima S, Shishido E, Matsuzaki M, Saigo K (1996) eagle, a member of the steroid receptor gene superfamily, is expressed in a subset of neuroblasts and regulates the fate of their putative progeny in the Drosophila CNS. Development 122:527-536.
16. Hiramoto M, Hiromi Y (2006) ROBO directs axon crossing of segmental boundaries by suppressing responsiveness to relocalized Netrin. Nat Neurosci 9:58-66.
17. Hiramoto M, Hiromi Y, Giniger E, Hotta Y (2000) The Drosophila Netrin receptor Frazzled guides axons by controlling Netrin distribution. Nature 406:886-889.
18. Hummel T, Schimmelpfeng K, Klambt C (1999) Commissure formation in the embryonic CNS of Drosophila. Development 126:771-779.
19. Keleman K, Rajagopalan S, Cleppien D, Teis D, Paiha K, Huber LA, Technau GM, Dickson BJ (2002) Comm sorts robo to control axon guidance at the Drosophila midline. Cell 110:415-427.
20. Kidd T, Brose K, Mitchell KJ, Fetter RD, Tessier-Lavigne M, Goodman CS, Tear G (1998a) Roundabout controls axon crossing of the CNS midline and defines a novel subfamily of evolutionarily conserved guidance receptors. Cell 92:205-215.
21. Kidd T, Russell C, Goodman CS, Tear G (1998b) Dosage sensitive and complementary functions of Roundabout and Commissureless control axon crossing of the CNS midline. Neuron 20:25-33.
22. Kidd T, Bland KS, Goodman CS (1999) Slit is the midline repellent for the robo receptor in Drosophila. Cell 96:785-794.
23. Kolodziej PA, Timpe LC, Mitchell KJ, Fried SR, Goodman CS, Jan LY, Jan YN (1996) frazzled encodes a Drosophila member of the DCC immunoglobulin subfamily and is required for CNS and motor axon guidance. Cell 87:197-204.
24. Lin DM, Fetter RD, Kopczynski C, Grenningloh G, Goodman CS (1994) Genetic analysis of fasciclin II in Drosophila: defasciculation, refasciculation, and altered fasciculation. Neuron 13:1055-1069.
25. Long H, Sabatier C, Ma L, Plump A, Yuan W, Ornitz DM, Tamada A, Murakami F, Goodman CS, Tessier-Lavigne M (2004) Conserved roles for Slit and Robo proteins in midline commissural axon guidance. Neuron 42:213-223.
26. Mitchell KJ, Doyle JL, Serafini T, Kennedy TE, Tessier-Lavigne M, Goodman CS, Dickson BJ (1996) Genetic analysis of Netrin genes in Drosophila: Netrins guide CNS commissural axons and peripheral motor axons. Neuron 17:203-215.
27. O'Keefe DD, Thor S, Thomas JB (1998) Function and specificity of LIM domains in Drosophila nervous system and wing development. Development 125:3915-3923.
28. Rajagopalan S, Nicolas E, Vivancos V, Berger J, Dickson BJ (2000) Crossing the midline: roles and regulation of Robo receptors. Neuron 28:767-777.
29. Sabatier C, Plump AS, Le M, Brose K, Tamada A, Murakami F, Lee EY, Tessier-Lavigne M (2004) The divergent Robo family protein rig-1/Robo3 is a negative regulator of slit responsiveness required for midline crossing by commissural axons. Cell 117:157-169.
30. Schmid A, Chiba A, Doe CQ (1999) Clonal analysis of Drosophila embryonic neuroblasts: neural cell types, axon projections and muscle targets. Development 126:4653-4689.
31. Schmidt H, Rickert C, Bossing T, Vef O, Urban J, Technau GM (1997) The embryonic central nervous system lineages of Drosophila melanogaster. II. Neuroblast lineages derived from the dorsal part of the neuroectoderm. Dev Biol 189:186-204.
32. Serafini T, Kennedy TE, Galko MJ, Mirzayan C, Jessell TM, Tessier-Lavigne M (1994) The netrins define a family of axon outgrowth-promoting proteins homologous to C. elegans UNC-6. Cell 78:409-424.
33. Serafini T, Colamarino SA, Leonardo ED, Wang H, Beddington R, Skarnes WC, Tessier-Lavigne M (1996) Netrin-1 is required for commissural axon guidance in the developing vertebrate nervous system. Cell 87:1001-1014.
34. Shirasaki R, Katsumata R, Murakami F (1998) Change in chemoattractant responsiveness of developing axons at an intermediate target. Science 279:105-107.
35. Simpson JH, Kidd T, Bland KS, Goodman CS (2000) Short-range and longrange guidance by slit and its Robo receptors. Robo and Robo2 play distinct roles in midline guidance. Neuron 28:753-766.
36. Stein E, Tessier-Lavigne M (2001) Hierarchical organization of guidance receptors: silencing of netrin attraction by slit through a Robo/DCC receptor complex. Science 291:1928-1938.
37. Tear G, Harris R, Sutaria S, Kilomanski K, Goodman CS, Seeger MA (1996) commissureless controls growth cone guidance across the CNS midline in Drosophila and encodes a novel membrane protein. Neuron 16:501-514.
38. Tessier-Lavigne M, Goodman CS (1996) The molecular biology of axon guidance. Science 274:1123-1133.
39. Winberg ML, Mitchell KJ, Goodman CS (1998) Genetic analysis of the mechanisms controlling target selection: complementary and combinatorial functions of netrins, semaphorins, and IgCAMs. Cell 93:581-591.
40. Yu TW, Bargmann CI (2001) Dynamic regulation of axon guidance. Nat Neurosci 4 [Suppl]:1169-1176.
41. Yu TW, Hao JC, Lim W, Tessier-Lavigne M, Bargmann CI (2002) Shared receptors in axon guidance: SAX-3/Robo signals via UNC-34/Enabled and a Netrin-independent UNC-40/DCC function. Nat Neurosci 5:1147-1154.
42. Zou Y, Stoeckli E, Chen H, Tessier-Lavigne M (2000) Squeezing axons out of the gray matter: a role for slit and semaphorin proteins from midline and ventral spinal cord. Cell 102:363-375.