Getting axons onto the right path: The role of transcription factors in axon guidance

Development

Volumn 134, Issue 3, 2007, Pages 439-448

  Butler, Samantha J ^a   Tear, Guy ^b  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

EPHRIN RECEPTOR; HOX PROTEIN; LIM PROTEIN; ROUNDABOUT RECEPTOR; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR POU; TRANSCRIPTION FACTOR RUNX;

CELL NUCLEUS; DROSOPHILA; EMBRYO DEVELOPMENT; EXTRACELLULAR SPACE; INNERVATION; MICROENVIRONMENT; MOTONEURON; NERVE GROWTH; NERVOUS SYSTEM FUNCTION; NONHUMAN; OLFACTORY SYSTEM; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN FUNCTION; RETINA; REVIEW; SENSORY NERVE; SIGNAL TRANSDUCTION; VERTEBRATE;

ANIMALS; AXONS; DROSOPHILA; DROSOPHILA PROTEINS; HOMEODOMAIN PROTEINS; MODELS, NEUROLOGICAL; NERVE TISSUE PROTEINS; NERVOUS SYSTEM; TRANSCRIPTION FACTORS; VERTEBRATES;

VERTEBRATA;

EID: 33847410600     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.02762     Document Type: Review

References (79)

1. Barbieri, A. M., Lupo, G., Bulfone, A., Andreazzoli, M., Mariani, M., Fougerousse, F., Consalez, G. G., Borsani, G., Beckmann, J. S., Barsacchi, G. et al. (1999). A homeobox gene, vax2, controls the patterning of the eye dorsoventral axis. Proc. Natl. Acad Sci. USA 96, 10729-10734.
2. Brittis, P. A., Lu, Q. and Flanagan, J. G. (2002). Axonal protein synthesis provides a mechanism for localized regulation at an intermediate target. Cell 110, 223-235.
3. Broihier, H. T., Kuzin, A., Zhu, Y., Odenwald, W. and Skeath, J. B. (2004). Drosophila homeodomain protein Nkx6 coordinates motoneuron subtype identity and axonogenesis. Development 131, 5233-5242.
4. Brown, A. G. (1981). Organization in the Spinal Cord. Berlin, Heidelberg, New York: Springer Verlag.
5. Brunet, I., Weinl, C., Piper, M., Trembleau, A., Volovitch, M., Harris, W., Prochiantz, A. and Holt, C. (2005). The transcription factor Engrailed-2 guides retinal axons. Nature 438, 94-98.
6. Campbell, D. S. and Holt, C. E. (2001). Chemotropic responses of retinal growth cones mediated by rapid local protein synthesis and degradation. Neuron 32, 1013-1026.
7. Certel, S. J. and Thor, S. (2004). Specification of Drosophila motoneuron identity by the combinatorial action of POU and LIM-HD factors. Development 131, 5429-5439.
8. Chan, S. S. Y., Zheng, H., Su, M. W., Wilk, R., Killeen, M. T., Hedgecock, E. M. and Culotti, J. G. (1996). UNC-40, a C-elegans homolog of DCC (Deleted in Colorectal Cancer), is required in motile cells responding to UNC-6 netrin cues. Cell 87, 187-195.
9. 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.
10. Chen, A. I., de Nooij, J. C. and Jessell, T. M. (2006a). Graded activity of transcription factor Runx3 specifies the laminar termination pattern of sensory axons in the developing spinal cord. Neuron 49, 395-408.
11. Chen, C. L., Broom, D. C., Liu, Y., de Nooij, J. C., Li, Z., Cen, C., Samad, O. A., Jessell, T. M., Woolf, C. J. and Ma, Q. (2006b). Runx1 determines nociceptive sensory neuron phenotype and is required for thermal and neuropathic pain. Neuron 49, 365-377.
12. Crowner, D., Madden, K., Goeke, S. and Giniger, E. (2002). Iola regulates midline crossing of CNS axons in Drosophila. Development 129, 1317-1325.
13. Dasen, J. S., Liu, J. P. and Jessell, T. M. (2003). Motor neuron columnar fate imposed by sequential phases of Hox-c activity. Nature 425, 926-933.
14. Dasen, J. S., Tice, B. C., Brenner-Morton, S. and Jessell, T. M. (2005). A Hox regulatory network establishes motor neuron pool identity and target-muscle connectivity. Cell 123, 477-491.
15. Dickson, B. (2002). Molecular mechanisms of axon guidance. Science 298, 1959-1964.
16. Eberhart, J., Swartz, M. E., Koblar, S. A., Pasquale, E. B. and Krull, C. E. (2002). EphA4 constitutes a population-specific guidance cue for motor neurons. Dev. Biol. 247, 89-101.
17. Erkman, L., Yates, P. A., McLaughlin, T., McEvilly, R. J., Whisenhunt, T., O'Connell, S. M., Krones, A. I., Kirby, M. A., Rapaport, D. H., Bermingham, J. R. et al. (2000). A POU domain transcription factor-dependent program regulates axon pathfinding in the vertebrate visual system. Neuron 28, 779-792.
18. Erskine, L., Williams, S. E., Brose, K., Kidd, T., Rachel, R. A., Goodman, C. S., Tessier-Lavigne, M. and Mason, C. A. (2000). Retinal ganglion cell axon guidance in the mouse optic chiasm: expression and function of robos and slits. J. Neurosci. 20, 4975-4982.
19. Forscher, P. and Smith, S. J. (1988). Actions of cytochalasins on the organization of actin filaments and microtubules in a neuronal growth cone. J. Cell Biol. 107, 1505-1516.
20. Friedman, G. C. and O'Leary, D. D. (1996). Retroviral misexpression of engrailed genes in the chick optic tectum perturbs the topographic targeting of retinal axons. J. Neurosci. 16, 5498-5509.
21. Fujioka, M., Lear, B. C., Landgraf, M., Yusibova, G. L., Zhou, J., Riley, K. M., Patel, N. H. and Jaynes, J. B. (2003). Even-skipped, acting as a repressor, regulates axonal projections in Drosophila. Development 130, 5385-5400.
22. Garbe, D. S. and Bashaw, G. J. (2004). Axon guidance at the midline: from mutants to mechanisms. Crit. Rev. Biochem. Mol. Biol. 39, 319-341.
23. Garces, A. and Thor, S. (2006). Specification of Drosophila aCC motoneuron identity by a genetic cascade involving even-skipped, grain and zfh1. Development 133, 1445-1455.
24. Goeke, S., Greene, E. A., Grant, P. K., Gates, M. A., Crowner, D., Aigaki, T. and Giniger, E. (2003). Alternative splicing of Iola generates 19 transcription factors controlling axon guidance in Drosophila. Nat Neurosci. 6, 917-924.
25. Hamelin, M., Zhou, Y., Su, M. W., Scott, I. M. and Culotti, J. G. (1993). Expression of the UNC-5 guidance receptor in the touch neurons of C. elegans steers their axons dorsally. Nature 364, 327-330.
26. Harris, W. A., Holt, C. E. and Bonhoeffer, F. (1987). Retinal axons with and without their somata, growing to and arborizing in the tectum of Xenopus embryos: a time-lapse video study of single fibres in vivo. Development 101, 123-133.
27. Herrera, E., Brown, L., Aruga, J., Rachel, R. A., Dolen, G., Mikoshiba, K., Brown, S. and Mason, C. A. (2003). Zic2 patterns binocular vision by specifying the uncrossed retinal projection. Cell 114, 545-557.
28. Herrera, E., Marcus, R., Li, S., Williams, S. E., Erskine, L., Lai, E. and Mason, C. (2004). Foxd1 is required for proper formation of the optic chiasm. Development 131, 5727-5739.
29. Hong, K., Hinck, L., Nishiyama, M., Poo, M. M., Tessier-Lavigne, M. and Stein, E. (1999). A ligand-gated association between cytoplasmic domains of UNC5 and DCC family receptors converts netrin-induced growth cone attraction to repulsion. Cell 97, 927-941.
30. Inoue, K., Ozaki, S., Shiga, T., Ito, K., Masuda, T., Okado, N., Iseda, T., Kawaguchi, S., Ogawa, M., Bae, S. C. et al. (2002). Runx3 controls the axonal projection of proprioceptive dorsal root ganglion neurons. Nat. Neurosci. 5, 946-954.
31. Jin, Z., Zhang, J., Klar, A., Chedotal, A., Rao, Y., Cepko, C. L. and Bao, Z. Z. (2003). Irx4-mediated regulation of Slit1 expression contributes to the definition of early axonal paths inside the retina. Development 130, 1037-1048.
32. Kaminker, J. S., Canon, J., Salecker, I. and Banerjee, U. (2002). Control of photoreceptor axon target choice by transcriptional repression of Runt. Nat. Neurosci. 5, 746-750.
33. Kania, A. and Jessell, T. M. (2003). Topographic motor projections in the limb imposed by LIM homeodomain protein regulation of ephrin-A:EphA interactions. Neuron 38, 581-596.
34. Kania, A., Johnson, R. L. and Jessell, T. M. (2000). Coordinate roles for LIM homeobox genes in directing the dorsoventral trajectory of motor axons in the vertebrate limb. Cell 102, 161-173.
35. Keino-Masu, K., Masu, M., Hinck, L., Leonardo, E. D., Chan, S. S. Y., Culotti,J. G. and Tessier-Lavigne, M. (1996). Deleted in Colorectal Cancer (DCC) encodes a netrin receptor. Cell 87, 175-185.
36. Keleman, K. and Dickson, B. J. (2001). Short- and long-range repulsion by the Drosophila Unc5 netrin receptor. Neuron 32, 605-617.
37. Keleman, K., Rajagopalan, S., Cleppien, D., Teis, D., Paiha, K., Huber, L. A., Technau. G. M. and Dickson, B. J. (2002). Comm sorts robo to control axon guidance at the Drosophila midline. Cell 110, 415-427.
38. Keleman, K., Ribeiro, C. and Dickson, B. J. (2005). Comm function in commissural axon guidance: cell-autonomous sorting of Robo in vivo. Nat Neurosci. 8, 156-163.
39. Kidd, T., Russell, C., Goodman, C. S. and Tear, G. (1998a). Dosage-sensitive and complementary functions of roundabout and commissureless control axon crossing of the CNS midline. Neuron 20, 25-33.
40. Kidd, T., Brose, K., Mitchell, K. J., Fetter, R. D., Tessier-Lavigne, M., Goodman, C. S. and Tear, G. (19981b). Roundabout controls axon crossing of the CNS midline and defines a novel subfamily of evolutionarily conserved guidance receptors. Cell 92, 205-215.
41. 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.
42. Kolodziej, P. A., Timpe, L. C., Mitchell, K. J., Fried, S. R., Goodman, C. S., Jan, L. Y. and Jan, Y. N. (1996). frazzled encodes a Drosophila member of the DCC immunoglobulin subfamily and is required for CNS and motor axon guidance. Cell 87, 197-204.
43. Komiyama, T., Johnson, W. A., Luo, L. and Jefferis, G. S. (2003). From lineage to wiring specificity. POU domain transcription factors control precise connections of Drosophila olfactory projection neurons. Cell 112, 157-167.
44. Koshiba-Takeuchi, K., Takeuchi, J. K., Matsumoto, K., Momose, T., Uno, K., Hoepker, V., Ogura, K., Takahashi, N., Nakamura, H., Yasuda, K. et al. (2000). Tbx5 and the retinotectum projection. Science 287, 134-137.
45. Kramer, I., Sigrist, M., de Nooij, J. C., Taniuchi, I., Jessell, T. M. and Arber, S. (2006). A role for Runx transcription factor signaling in dorsal root ganglion sensory neuron diversificaion. Neuron 49, 379-393.
46. Labrador, J. P., O'Keefe, D., Yoshikawa, S., McKinnon, R. D., Thomas, J. B. and Bashaw, G. J. (2005). The homeobox transcription factor even-skipped regulates netrin-receptor expression to control dorsal motor-axon projections in Drosophila. Curr. Biol. 15, 1413-1419.
47. Landgraf, M. and Thor, S. (2006). Development of Drosophila motoneurons: specification and morphology Semin. Cell Dev. Biol. 17, 3-11.
48. Landgraf, M., Roy, S., Prokop, A., VijayRaghavan, K. and Bate, M. (1999). even-skipped determines the dorsal growth of motor axons in Drosophila. Neuron 22, 43-52.
49. Layden, M. J., Odden, J. P., Schmid, A., Garces, A., Thor, S. and Doe, C. Q. (2006). Zfh1, a somatic motor neuron transcription factor, regulates axon exit from the CNS. Dev. Biol. 291, 253-263.
50. Leung, K. M., van Horck, F. P., Lin, A. C., Allison, R., Standart, N. and Holt, C. E. (2006). Asymmetrical beta-actin mRNA translation in growth cones mediates attractive turning to netrin-1. Nat. Neurosci. 9, 1247-1256.
51. Levanon, D., Bettoun, D., Harris-Cerruti, C., Woolf, E., Negreanu, V., Eilam, R., Bernstein, Y., Goldenberg, D., Xiao, C., Fliegauf, M. et al. (2002). The Runx3 transcription factor regulates development and survival of TrkC dorsal root ganglia neurons. EMBO J. 21, 3454-3463.
52. Logan, C., Wizenmann, A., Drescher, U, Monschau, B., Bonhoeffer, F., and Lumsden, A. (1996). Rostral optic tectum acquires caudal characteristics following ectopic engrailed expression. Curr. Biol. 6, 1006-1014.
53. McLaughlin, T., and O'Leary, D. D. (2005). Molecular radients and development of retinotopic maps. Annu. Rev. Neurosci. 28, 327-355.
54. Mu, X., Silos-Santiago, I., Carroll, S. L. and Snider, W. D. (1993). Neurotrophin receptor genes are expressed in distinct patterns in developing dorsal root ganglia. J. Neurosci. 13, 4029-4041.
55. Mu, X., Beremand, P. D., Zhao, S., Pershad, R., Sun, H., Scarpa, A., Liang, S., Thomas, T. L. and Klein, W. H. (2004). Discrete gene sets depend on POU domain transcription factor Brn3b/Brn-3.2/POU4f2 for their expression in the mouse embryonic retina. Development 131, 1197-1210.
56. Mull, S. H., Hindges, R., O'Leary, D. D., Lemke, G. and Bertuzzi, S. (2002). The homeodomain protein Vax2 patterns the dorsoventral and nasotemporal axes of the eye. Development 129, 797-804.
57. Myat, A., Henry, P., McCabe, V., Flintoft, L., Rotin, D. and Tear, G. (2002). Drosophila Nedd4, an ubiquitin ligase, is recruited by Commissureless to control cell surface levels of the Roundabout receptor Neuron 35, 447-459.
58. Oster, S. F. and Sretavan, D. W. (2003). Connecting the eye to the brain: the molecular basis of ganglion cell axon guidance. Br. J. Ophthalmol. 87, 639-645.
59. Pak, W., Hindges, R., Lim, Y. S., Pfaff, S. L. and O'Leary, D. D. (2004). Magnitude of binocular vision controlled by islet-2 repression of a genetic program that specifies laterality of retinal axon pathfinding. Cell 119, 567-578.
60. Sanchez-Soriano, N. and Prokop, A. (2005). The influence of pioneer neurons on a growing motor nerve in Drosophila requires the neural cell adhesion molecule homolog Fasciclinll. J. Neurosci. 25, 78-87.
61. Schmid, A., Chiba, A. and Doe, C. Q. (1999). Clonal analysis of Drosophila embryonic neuroblasts: neural cell types, axon projections and muscle targets. Development 126, 4653-4699.
62. Schulte, D. and Cepko, C. L. (2000). Two homeobox genes define the domain of EphA3 expression in the developing chick retina. Development 127, 5033-5045.
63. Schulte, D., Furukawa, T., Peters, M. A., Kozak, C. A. and Cepko, C. L. (1999). Misexpression of the Ennx-related homeobox genes cVax and mVax2 ventralizes the retina and perturbs the retinotectal map. Neuron 24, 541-553.
64. Seth, A., Culverwell, J., Walkowicz, M., Toro, S., Rick, J. M., Neuhauss, S. C., Varga, Z. M. and Karlstrom, R. O. (2006). belladonna/ (Ihx2) is required for neural patterning and midline axon guidance in the zebrafish forebrain. Development 133, 725-735.
65. Sharma, K., Sheng, H. Z., Lettieri, K., Li, H., Karavanov, A., Potter, S., Westphal, H. and Pfaff, S. L. (1998). LIM homeodomain factors Lhx3 and Lhx4 assign subtype identities for motor neurons. Cell 95, 817-828.
66. Shaw, G. and Bray, D. (1977). Movement and extension of isolated growth cones. Exp. Cell Res, 104, 55-62.
67. Shirasaki, R., Lewcock, J. W., Lettieri, K. and Pfaff, S. L. (2006). FGF as a target-derived chemoattractant for developing motor axons genetically programmed by the LIM code. Neuron 50, 841-853.
68. Solano, R. J., Mugat, B., Martin, D., Girard, F., Huibant, J. M., Ferraz, C., Jacq, B., Demaille, J. and Maschat, F. (2003). Genome-wide identification of in vivo Drosophila Engrailed-binding DNA fragments and related target genes. Development 130, 1243-1254.
69. Song, H. J., Ming, G. L. and Poo, M. M. (1997). cAMP-induced switching in turning direction of nerve growth cones [published erratum appears in Nature (1997) Sep 25;389(6649):412]. Nature 388, 275-279.
70. Song, H., Ming, G., He, Z., Lehmann, M., McKerracher, L., Tessier-Lavigne, M. and Poo, M. (1998). Conversion of neuronal growth cone responses from repulsion to attraction by cyclic nucleotides. Science 281, 1515-1518.
71. Stoeckli, E. T. and Landmesser, L. T. (1998). Axon guidance at choice points. Curr. Opin. Neurobiol. 8, 73-79.
72. Takahashi, H., Shintani, T, Sakuta, H. and Noda, M. (2003). CBF1 controls the retinotectal topographical map along the anteroposterior axis through multiple mechanisms. Development 130, 5203-5215.
73. Tanabe, Y. and Jessell, T. M. (1996). Diversity and pattern in the developing spinal cord. Science 274, 1115-1123.
74. Tear, G. (1999). Axon guidance at the central nervous system midline. Cell Mol. Life Sci. 55, 1365-1376.
75. Thor, S., Andersson, S. G., Tomlinson, A. and Thomas, J. B. (1999). A LIM-homeodomain combinatorial code for motor-neuron pathway selection. Nature 397, 76-80.
76. Tsuchida, T. Ensini, M., Morton, S. B., Baldassare, M., Edlund, T., Jessell, T. M. and Pfaff, S. L. (1994). Topographic organization of embryonic motor neurons defined by expression of LIM homeobox genes. Cell 79, 957-970.
77. Wang, S. W., Gan, L., Martin, S. E. and Klein, W. H. (2000). Abnormal polarization and axon outgrowth in retinal ganglion cells lacking the POU-domain transcription factor Brn-3b. Mol. Cell. Neurosci. 16, 141-156.
78. Wu, K. Y., Hengst, U., Cox, L. J., Macosko, E. Z., Jeromin, A., Urquhart, E. R. and Jaffrey, S. R. (2005). Local translation of RhoA regulates growth cone collapse. Nature 436, 1020-1024.
79. Yu, T. W. and Bargmann, C. I. (2001). Dynamic regulation of axon guidance. Nat. Neurosci. 4 Suppl, 1169-1176.