Pioneer longitudinal axons navigate using floor plate and Slit/Robo signals

Development

Volumn 135, Issue 22, 2008, Pages 3643-3653

  Farmer, W Todd ^a   Altick, Amy L ^a   Nural, Hikmet Feyza ^a   Dugan, James P ^a   Kidd, Thomas ^a   Charron, Frédéric ^b   Mastick, Grant S ^a  

^a UNIVERSITY OF NEVADA   (United States)

^b CLIN RESEARCH INSTITUTE OF MONTREAL   (Canada)

Author keywords

Axon guidance; Floor plate; Hindbrain; Longitudinal axon; Robo; Slit

Indexed keywords

ROUNDABOUT RECEPTOR; ROUNDABOUT RECEPTOR 1; ROUNDABOUT RECEPTOR 2; SLIT PROTEIN; SLIT1 PROTEIN; SLIT2 PROTEIN; UNCLASSIFIED DRUG; IMMUNOGLOBULIN RECEPTOR; KRUPPEL LIKE FACTOR; NERVE PROTEIN; ROBO2 PROTEIN, MOUSE; SIGNAL PEPTIDE; SLIT HOMOLOG 2 PROTEIN; SLIT1 PROTEIN, MOUSE; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR GLI2;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CHICK EMBRYO; CONTROLLED STUDY; EMBRYO; GENE DELETION; MOUSE; MOUSE MUTANT; NERVE FIBER GROWTH; NERVE PROJECTION; NERVE TRACT; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RHOMBENCEPHALON; SIGNAL TRANSDUCTION; ANIMAL; BRAIN; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MUTATION; NERVE FIBER; PHYSIOLOGY; PRENATAL DEVELOPMENT; TRANSGENIC ANIMAL;

MUS;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; AXONS; BRAIN; CHICK EMBRYO; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEDGEHOG PROTEINS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MICE; MUTATION; NERVE TISSUE PROTEINS; RECEPTORS, IMMUNOLOGIC; SIGNAL TRANSDUCTION;

EID: 59149092374     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.023325     Document Type: Article

References (70)

1. Agarwala, S. and Ragsdale, C. W. (2002). A role for midbrain arcs in nucleogenesis. Development 129, 5779-5788.
2. Agarwala, S., Sanders, T. A. and Ragsdale, C. W. (2001). Sonic hedgehog control of size and shape in midbrain pattern formation. Science 291, 2147-2150.
3. Ahsan, M., Riley, K. L. and Schubert, F. R. (2007). Molecular mechanisms in the formation of the medial longitudinal fascicle. J. Anat. 211, 177-187.
4. Andrews, W., Liapi, A., Plachez, C., Camurri, L., Zhang, J., Mori, S., Murakami, F., Parnavelas, J. G., Sundaresan, V. and Richards, L. J. (2006). Robo1 regulates the development of major axon tracts and interneuron migration in the forebrain. Development 133, 2243-2252.
5. Bagri, A., Marin, O., Plump, A. S., Mak, J., Pleasure, S. J., Rubenstein, J. L. and Tessier-Lavigne, M. (2002). Slit proteins prevent midline crossing and determine the dorsoventral position of major axonal pathways in the mammalian forebrain. Neuron 33, 233-248.
6. Bourikas, D., Pekarik, V., Baeriswyl, T., Grunditz, A., Sadhu, R., Nardo, M. and Stoeckli, E. T. (2005). Sonic hedgehog guides commissural axons along the longitudinal axis of the spinal cord. Nat. Neurosci. 8, 297-304.
7. Brose, K., Bland, K. S., Wang, K. H., Arnott, D., Henzel, W., Goodman, C. S., Tessier-Lavigne, M. and Kidd, T. (1999). Slit proteins bind Robo receptors and have an evolutionarily conserved role in repulsive axon guidance. Cell 96, 795-806.
8. Charron, F. and Tessier-Lavigne, M. (2005). Novel brain wiring functions for classical morphogens: a role as graded positional cues in axon guidance. Development 132, 2251-2262.
9. Charron, F., Stein, E., Jeong, J., McMahon, A. P. and Tessier-Lavigne, M. (2003). The morphogen sonic hedgehog is an axonal chemoattractant that collaborates with netrin-1 in midline axon guidance. Cell 113, 11-23.
10. Chedotal, A., Pourquie, O. and Sotelo, C. (1995). Initial tract formation in the brain of the chick embryo: selective expression of the BEN/SC1/DM-GRASP cell adhesion molecule. Eur. J. Neurosci. 7, 198-212.
11. Chitnis, A. B. and Kuwada, J. Y. (1991). Elimination of a brain tract increases errors in pathfinding by follower growth cones in the zebrafish embryo. Neuron 7, 277-285.
12. Colamarino, S. A. and Tessier-Lavigne, M. (1995). The role of the floor plate in axon guidance. Annu. Rev. Neurosci. 18, 497-529.
13. Devine, C. A. and Key, B. (2008). Robo-Slit interactions regulate longitudinal axon pathfinding in the embryonic vertebrate brain. Dev. Biol. 313, 371-383.
14. Easter, S. S., Jr, Ross, L. S. and Frankfurter, A. (1993). Initial tract formation in the mouse brain. J. Neurosci. 13, 285-299.
15. Easter, S. S., Jr, Burrill, J., Marcus, R. C., Ross, L. S., Taylor, J. S. and Wilson, S. W. (1994). Initial tract formation in the vertebrate brain. Prog. Brain Res. 102, 79-93.
16. Englund, C., Steneberg, P., Falileeva, L., Xylourgidis, N. and Samakovlis, C. (2002). Attractive and repulsive functions of Slit are mediated by different receptors in the Drosophila trachea. Development 129, 4941-4951.
17. Fouquet, C., Di Meglio, T., Ma, L., Kawasaki, T., Long, H., Hirata, T., Tessier-Lavigne, M., Chedotal, A. and Nguyen-Ba-Charvet, K. T. (2007). Robo1 and robo2 control the development of the lateral olfactory tract. J. Neurosci. 27, 3037-3045.
18. Fujisawa, K., Wrana, J. L. and Culotti, J. G. (2007). The slit receptor EVA-1 coactivates a SAX-3/Robo mediated guidance signal in C. elegans. Science 317, 1934-1938.
19. Garbe, D. S. and Bashaw, G. J. (2007). Independent functions of Slit-Robo repulsion and Netrin-Frazzled attraction regulate axon crossing at the midline in Drosophila. J. Neurosci. 27, 3584-3592.
20. Glover, J. C. and Petursdottir, G. (1991). Regional specificity of developing reticulospinal, vestibulospinal, and vestibulo-ocular projections in the chicken embryo. J. Neurobiol. 22, 353-376.
21. Grieshammer, U., Le, M., Plump, A. S., Wang, F., Tessier-Lavigne, M. and Martin, G. R. (2004). SLIT2-mediated ROBO2 signaling restricts kidney induction to a single site. Dev. Cell 6, 709-717.
22. Hao, J. C., Yu, T. W., Fujisawa, K., Culotti, J. G., Gengyo-Ando, K., Mitani, S., Moulder, G., Barstead, R., Tessier-Lavigne, M. and Bargmann, C. I. (2001). C. elegans slit acts in midline, dorsal-ventral, and anterior-posterior guidance via the SAX-3/Robo receptor. Neuron 32, 25-38.
23. Hatta, K. (1992). Role of the floor plate in axonal patterning in the zebrafish CNS. Neuron 9, 629-642.
24. Hivert, B., Liu, Z., Chuang, C. Y., Doherty, P. and Sundaresan, V. (2002). Robo1 and Robo2 are homophilic binding molecules that promote axonal growth. Mol. Cell Neurosci. 21, 534-545.
25. Holmes, G. P., Negus, K., Burridge, L., Raman, S., Algar, E., Yamada, T. and Little, M. H. (1998). Distinct but overlapping expression patterns of two vertebrate slit homologs implies functional roles in CNS development and organogenesis. Mech. Dev. 79, 57-72.
26. Hutson, L. D. and Chien, C. B. (2002). Pathfinding and error correction by retinal axons: the role of astray/robo2. Neuron 33, 205-217.
27. Imondi, R. and Kaprielian, Z. (2001). Commissural axon pathfinding on the contralateral side of the floor plate: a role for B-class ephrins in specifying the dorsoventral position of longitudinally projecting commissural axons. Development 128, 4859-4871.
28. 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. (2004). Mutations in a human ROBO gene disrupt hindbrain axon pathway crossing and morphogenesis. Science 304, 1509-1513.
29. Kadison, S. R., Murakami, F., Matise, M. P. and Kaprielian, Z. (2006). The role of floor plate contact in the elaboration of contralateral commissural projections within the embryonic mouse spinal cord. Dev. Biol. 296, 499-513.
30. Kennedy, T. E., Serafini, T., de la Torre, J. R. and Tessier-Lavigne, M. (1994). Netrins are diffusible chemotropic factors for commissural axons in the embryonic spinal cord. Cell 78, 425-435.
31. Kidd, T., Brose, K., Mitchell, K. J., Fetter, R. D., Tessier-Lavigne, M., Goodman, C. S. and 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.
32. Kidd, T., Russell, C., Goodman, C. S. and Tear, G. (1998b). Dosage-sensitive and complementary functions of roundabout and commissureless control axon crossing of the CNS midline. Neuron 20, 25-33.
33. Kidd, T., Bland, K. S. and Goodman, C. S. (1999). Slit is the midline repellent for the robo receptor in Drosophila. Cell 96, 785-794.
34. Kramer, S. G., Kidd, T., Simpson, J. H. and Goodman, C. S. (2001). Switching repulsion to attraction: changing responses to slit during transition in mesoderm migration. Science 292, 737-740.
35. Lebel, M., Mo, R., Shimamura, K. and Hui, C. C. (2007). Gli2 and Gli3 play distinct roles in the dorsoventral patterning of the mouse hindbrain. Dev. Biol. 302, 345-355.
36. Long, H., Sabatier, C., Ma, L., Plump, A., Yuan, W., Ornitz, D. M., Tamada, A., Murakami, F., Goodman, C. S. and Tessier-Lavigne, M. (2004). Conserved roles for Slit and Robo proteins in midline commissural axon guidance. Neuron 42, 213-223.
37. Lopez-Bendito, G., Flames, N., Ma, L., Fouquet, C., Di Meglio, T., Chedotal, A., Tessier-Lavigne, M. and Marin, O. (2007). Robo1 and Robo2 cooperate to control the guidance of major axonal tracts in the mammalian forebrain. J. Neurosci. 27, 3395-3407.
38. Lyuksyutova, A. I., Lu, C. C., Milanesio, N., King, L. A., Guo, N., Wang, Y., Nathans, J., Tessier-Lavigne, M. and Zou, Y. (2003). Anterior-posterior guidance of commissural axons by Wnt-frizzled signaling. Science 302, 1984-1988.
39. Mambetisaeva, E. T., Andrews, W., Camurri, L., Annan, A. and Sundaresan, V. (2005). Robo family of proteins exhibit differential expression in mouse spinal cord and Robo-Slit interaction is required for midline crossing in vertebrate spinal cord. Dev. Dyn. 233, 41-51.
40. Mastick, G. S. and Easter, S. S., Jr (1996). Initial organization of neurons and tracts in the embryonic mouse fore- and midbrain. Dev. Biol. 173, 79-94.
41. Mastick, G. S. and Andrews, G. L. (2001). Pax6 regulates the identity of embryonic diencephalic neurons. Mol. Cell Neurosci. 17, 190-207.
42. Mastick, G. S., Davis, N. M., Andrew, G. L. and Easter, S. S., Jr (1997). Pax-6 functions in boundary formation and axon guidance in the embryonic mouse forebrain. Development 124, 1985-1997.
43. Matise, M. P., Epstein, D. J., Park, H. L., Platt, K. A. and Joyner, A. L. (1998). Gli2 is required for induction of floor plate and adjacent cells, but not most ventral neurons in the mouse central nervous system. Development 125, 2759-2770.
44. Matise, M. P., Lustig, M., Sakurai, T., Grumet, M. and Joyner, A. L. (1999). Ventral midline cells are required for the local control of commissural axon guidance in the mouse spinal cord. Development 126, 3649-3659.
45. Mo, R., Freer, A. M., Zinyk, D. L., Crackower, M. A., Michaud, J., Heng, H. H., Chik, K. W., Shi, X. M., Tsui, L. C., Cheng, S. H. et al. (1997). Specific and redundant functions of Gli2 and Gli3 zinc finger genes in skeletal patterning and development. Development 124, 113-123.
46. Molle, K. D., Chedotal, A., Rao, Y., Lumsden, A. and Wizenmann, A. (2004). Local inhibition guides the trajectory of early longitudinal tracts in the developing chick brain. Mech. Dev. 121, 143-156.
47. Nural, H. F. and Mastick, G. S. (2004). Pax6 guides a relay of pioneer longitudinal axons in the embryonic mouse forebrain. J. Comp. Neurol. 479, 399-409.
48. Oberg, K. C., Pira, C. U., Revelli, J. P., Ratz, B., Aguilar-Cordova, E. and Eichele, G. (2002). Efficient ectopic gene expression targeting chick mesoderm. Dev. Dyn. 224, 291-302.
49. Okada, A., Charron, F., Morin, S., Shin, D. S., Wong, K., Fabre, P. J., Tessier-Lavigne, M. and McConnell, S. K. (2006). Boc is a receptor for sonic hedgehog in the guidance of commissural axons. Nature 444, 369-373.
50. Rajagopalan, S., Nicolas, E., Vivancos, V., Berger, J. and Dickson, B. J. (2000a). Crossing the midline: roles and regulation of Robo receptors. Neuron 28, 767-777.
51. Rajagopalan, S., Vivancos, V., Nicolas, E. and Dickson, B. J. (2000b). Selecting a longitudinal pathway: Robo receptors specify the lateral position of axons in the Drosophila CNS. Cell 103, 1033-1045.
52. Roelink, H., Augsburger, A., Heemskerk, J., Korzh, V., Norlin, S., Ruiz i Altaba, A., Tanabe, Y., Placzek, M., Edlund, T., Jessell, T. M. et al. (1994). Floor plate and motor neuron induction by vhh-1, a vertebrate homolog of hedgehog expressed by the notochord. Cell 76, 761-775.
53. Rothberg, J. M., Jacobs, J. R., Goodman, C. S. and Artavanis-Tsakonas, S. (1990). slit: an extracellular protein necessary for development of midline glia and commissural axon pathways contains both EGF and LRR domains. Genes Dev. 4, 2169-2187.
54. Ruiz i Altaba, A., Jessell, T. M. and Roelink, H. (1995). Restrictions to floor plate induction by hedgehog and winged-helix genes in the neural tube of frog embryos. Mol. Cell Neurosci. 6, 106-121.
55. Sabatier, C., Plump, A. S., Le, M., Brose, K., Tamada, A., Murakami, F., Lee, E. Y. and Tessier-Lavigne, M. (2004). The divergent Robo family protein rig1/Robo3 is a negative regulator of slit responsiveness required for midline crossing by commissural axons. Cell 117, 157-169.
56. Seeger, M., Tear, G., Ferres-Marco, D. and Goodman, C. S. (1993). Mutations affecting growth cone guidance in Drosophila: genes necessary for guidance toward or away from the midline. Neuron 10, 409-426.
57. Serafini, T., Kennedy, T. E., Galko, M. J., Mirzayan, C., Jessell, T. M. and Tessier-Lavigne, M. (1994). The netrins define a family of axon outgrowth-promoting proteins homologous to C. elegans UNC-6. Cell 78, 409-424.
58. Serafini, T., Colamarino, S. A., Leonardo, E. D., Wang, H., Beddington, R., Skarnes, W. C. and Tessier-Lavigne, M. (1996). Netrin-1 is required for commissural axon guidance in the developing vertebrate nervous system. Cell 87, 1001-1014.
59. Simpson, J. H., Bland, K. S., Fetter, R. D. and Goodman, C. S. (2000a). Short-range and long-range guidance by Slit and its Robo receptors: a combinatorial code of Robo receptors controls lateral position. Cell 103, 1019-1032.
60. Simpson, J. H., Kidd, T., Bland, K. S. and Goodman, C. S. (2000b). Short-range and long-range guidance by slit and its Robo receptors. Robo and Robo2 play distinct roles in midline guidance. Neuron 28, 753-766.
61. Stein, E. and 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.
62. Sundaresan, V., Mambetisaeva, E., Andrews, W., Annan, A., Knoll, B., Tear, G. and Bannister, L. (2004). Dynamic expression patterns of Robo (Robo1 and Robo2) in the developing murine central nervous system. J. Comp. Neurol. 468, 467-481.
63. Tamada, A., Shirasaki, R. and Murakami, F. (1995). Floor plate chemoattracts crossed axons and chemorepels uncrossed axons in the vertebrate brain. Neuron 14, 1083-1093.
64. Taylor, J. S. (1991). The early development of the frog retinotectal projection. Development Suppl. 2, 95-104.
65. Tessier-Lavigne, M., Placzek, M., Lumsden, A. G., Dodd, J. and Jessell, T. M. (1988). Chemotropic guidance of developing axons in the mammalian central nervous system. Nature 336, 775-778.
66. Wilson, S. W., Ross, L. S., Parrett, T. and Easter, S. S., Jr (1990). The development of a simple scaffold of axon tracts in the brain of the embryonic zebrafish, Brachydanio rerio. Development 108, 121-145.
67. Wolman, M. A., Liu, Y., Tawarayama, H., Shoji, W. and Halloran, M. C. (2004). Repulsion and attraction of axons by semaphorin3D are mediated by different neuropilins in vivo. J. Neurosci. 24, 8428-8435.
68. Wolman, M. A., Sittaramane, V. K., Essner, J. J., Yost, H. J., Chandrasekhar, A. and Halloran, M. C. (2008). Transient axonal glycoprotein-1 (TAG-1) and laminin-alpha1 regulate dynamic growth cone behaviors and initial axon direction in vivo. Neural Develop. 3, 6.
69. Yuan, W., Zhou, L., Chen, J. H., Wu, J. Y., Rao, Y. and Ornitz, D. M. (1999). The mouse SLIT family: secreted ligands for ROBO expressed in patterns that suggest a role in morphogenesis and axon guidance. Dev. Biol. 212, 290-306.
70. Zou, Y., Stoeckli, E., Chen, H. and 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.