Dynamic regulation of axon guidance

Nature Neuroscience

Volumn 4, Issue 11s, 2001, Pages 1169-1176

  Yu, Timothy W ^a   Bargmann, Cornelia I ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL SURFACE RECEPTOR; NERVE GROWTH FACTOR;

ANIMAL; CELL COMMUNICATION; CELL DIFFERENTIATION; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; GROWTH CONE; HUMAN; METABOLISM; NERVE TRACT; NERVOUS SYSTEM; PHYSIOLOGY; PRENATAL DEVELOPMENT; REVIEW; ULTRASTRUCTURE;

ANIMALS; CELL COMMUNICATION; CELL DIFFERENTIATION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GROWTH CONES; HUMANS; NERVE GROWTH FACTORS; NERVOUS SYSTEM; NEURAL PATHWAYS; RECEPTORS, CELL SURFACE;

EID: 0035514195     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn748     Document Type: Article

References (101)

1. Tessier-Lavigne, M. & Goodman, C. S. The molecular biology of axon guidance. Science 274, 1123–1133 (1996).
2. Culotti, J. G. & Merz, D. C. DCC and netrins. Curr. Opin. Cell. Biol. 10, 609–613 (1998).
3. Van Vactor, D. & Flanagan, J. G. The middle and the end: slit brings guidance and branching together in axon pathway selection. Neuron 22, 649–652 (1999).
4. Guthrie, S. Axon guidance: starting and stopping with slit. Curr. Biol. 9, R432–435 (1999).
5. Tamagnone, L. & Comoglio, P. M. Signalling by semaphorin receptors: cell guidance and beyond. Trends Cell Biol. 10, 377–383 (2000).
6. Raper, J. A. Semaphorins and their receptors in vertebrates and invertebrates. Curr. Opin. Neurobiol. 10, 88–94 (2000).
7. Flanagan, J. G. & Vanderhaeghen, P. The ephrins and Eph receptors in neural development. Annu. Rev. Neurosci. 21, 309–345 (1998).
8. Wilkinson, D. G. Multiple roles of EPH receptors and ephrins in neural development. Nature Rev. Neurosci. 2, 155–164 (2001).
9. Hedgecock, E. M., Culotti, J. G. & Hall, D. H. The unc-5, unc-6, and unc-40 genes guide circumferential migrations of pioneer axons and mesodermal cells on the epidermis in C. elegans. Neuron 4, 61–85 (1990).
10. Ackerman, S. L. et al. The mouse rostral cerebellar malformation gene encodes an UNC-5-like protein. Nature 386, 838–842 (1997).
11. Zallen, J. A., Kirch, S. A. & Bargmann, C. I. Genes required for axon pathfinding and extension in the C. elegans nerve ring. Development 126, 3679–3692 (1999).
12. Kramer, S. G., Kidd, T., Simpson, J. H. & Goodman, C. S. Switching repulsion to attraction: changing responses to slit during transition in mesoderm migration. Science 292, 737–740 (2001).
13. Behar, O., Golden, J. A., Mashimo, H., Schoen, F. J. & Fishman, M. C. Semaphorin III is needed for normal patterning and growth of nerves, bones and heart. Nature 383, 525–528 (1996).
14. Wadsworth, W. G., Bhatt, H. & Hedgecock, E. M. Neuroglia and pioneer neurons express UNC-6 to provide global and local netrin cues for guiding migrations in C. elegans. Neuron 16, 35–46 (1996).
15. Yuan, W. et al. 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 (1999).
16. Luo, Y. et al. A family of molecules related to collapsin in the embryonic chick nervous system. Neuron 14, 1131–1140 (1995).
17. Giger, R. J., Pasterkamp, R. J., Heijnen, S., Holtmaat, A. J. & Verhaagen, J. Anatomical distribution of the chemorepellent semaphorin III/collapsin-1 in the adult rat and human brain: predominant expression in structures of the olfactory-hippocampal pathway and the motor system. J. Neurosci. Res. 52, 27–42 (1998).
18. Itoh, A., Miyabayashi, T., Ohno, M. & Sakano, S. Cloning and expressions of three mammalian homologues of Drosophila slit suggest possible roles for Slit in the formation and maintenance of the nervous system. Brain Res. Mol. Brain Res. 62, 175–186 (1998).
19. Nakagawa, S. et al. Ephrin-B regulates the ipsilateral routing of retinal axons at the optic chiasm. Neuron 25, 599–610 (2000).
20. Nash, B., Colavita, A., Zheng, H., Roy, P. J. & Culotti, J. G. The forkhead transcription factor UNC-130 is required for the graded spatial expression of the UNC-129 TGF-beta guidance factor in C. elegans. Genes Dev. 14, 2486–2500 (2000).
21. Su, M. et al. Regulation of the UNC-5 netrin receptor initiates the first reorientation of migrating distal tip cells in Caenorhabditis elegans. Development 127, 585–594 (2000).
22. Brown, A. et al. Topographic mapping from the retina to the midbrain is controlled by relative but not absolute levels of EphA receptor signaling. Cell 102, 77–88 (2000).
23. Retaux, S. & Harris, W. A. Engrailed and retinotectal topography. Trends Neurosci. 19, 542–546 (1996).
24. Rhinn, M., Dierich, A., Le Meur, M. & Ang, S. Cell autonomous and non-cell autonomous functions of Otx2 in patterning the rostral brain. Development 126, 4295–4304 (1999).
25. Schulte, D. & Cepko, C. L. Two homeobox genes define the domain of EphA3 expression in the developing chick retina. Development 127, 5033–5045 (2000).
26. Baran, R., Aronoff, R. & Garriga, G. The C. elegans homeodomain gene unc- 42 regulates chemosensory and glutamate receptor expression. Development 126, 2241–2251 (1999).
27. Erkman, L. et al. A POU domain transcription factor–dependent program regulates axon pathfinding in the vertebrate visual system. Neuron 28, 779–792 (2000).
28. Much, J. W., Slade, D. J., Klampert, K., Garriga, G. & Wightman, B. The fax-1 nuclear hormone receptor regulates axon pathfinding and neurotransmitter expression. Development 127, 703–712 (2000).
29. Thor, S., Andersson, S. G., Tomlinson, A. & Thomas, J. B. A LIM homeodomain combinatorial code for motor-neuron pathway selection. Nature 397, 76–80 (1999).
30. Lundgren, S. E., Callahan, C. A., Thor, S. & Thomas, J. B. Control of neuronal pathway selection by the Drosophila LIM homeodomain gene apterous. Development 121, 1769–1773 (1995).
31. Thor, S. & Thomas, J. B. The Drosophila islet gene governs axon pathfinding and neurotransmitter identity. Neuron 18, 397–409 (1997).
32. Landgraf, M., Roy, S., Prokop, A., VijayRaghavan, K. & Bate, M. even-skipped determines the dorsal growth of motor axons in Drosophila. Neuron 22, 43–52 (1999).
33. Hartmann, B., Hirth, F., Walldorf, U. & Reichert, H. Expression, regulation and function of the homeobox gene empty spiracles in brain and ventral nerve cord development of Drosophila. Mech. Dev. 90, 143–153 (2000).
34. Kania, A., Johnson, R. L. & Jessell, T. M. Coordinate roles for LIM homeobox genes in directing the dorsoventral trajectory of motor axons in the vertebrate limb. Cell 102, 161–173 (2000).
35. Seeger, M., Tear, G., Ferres-Marco, D. & Goodman, C. S. Mutations affecting growth cone guidance in Drosophila: genes necessary for guidance toward or away from the midline. Neuron 10, 409–426 (1993).
36. Kidd, T., Russell, C., Goodman, C. S. & Tear, G. Dosage-sensitive and complementary functions of roundabout and commissureless control axon crossing of the CNS midline. Neuron 20, 25–33 (1998).
37. Tear, G. et al. commissureless controls growth cone guidance across the CNS midline in Drosophila and encodes a novel membrane protein. Neuron 16, 501–514 (1996).
38. Kidd, T. et al. Roundabout controls axon crossing of the CNS midline and defines a novel subfamily of evolutionarily conserved guidance receptors. Cell 92, 205–215 (1998).
39. Hornberger, M. R. et al. Modulation of EphA receptor function by coexpressed ephrinA ligands on retinal ganglion cell axons. Neuron 22, 731–742 (1999).
40. Dutting, D., Handwerker, C. & Drescher, U. Topographic targeting and pathfinding errors of retinal axons following overexpression of ephrinA ligands on retinal ganglion cell axons. Dev. Biol. 216, 297–311 (1999).
41. Feldheim, D. A. et al. Genetic analysis of ephrin-A2 and ephrin-A5 shows their requirement in multiple aspects of retinocollicular mapping. Neuron 25, 563–574 (2000).
42. Holmberg, J., Clarke, D. L. & Frisen, J. Regulation of repulsion versus adhesion by different splice forms of an Eph receptor. Nature 408, 203–206 (2000).
43. Castellani, V., Yue, Y., Gao, P. P., Zhou, R. & Bolz, J. Dual action of a ligand for Eph receptor tyrosine kinases on specific populations of axons during the development of cortical circuits. J Neurosci. 18, 4663–4672 (1998).
44. Galko, M. J. & Tessier-Lavigne, M. Function of an axonal chemoattractant modulated by metalloprotease activity. Science 289, 1365–1367 (2000).
45. Hattori, M., Osterfield, M. & Flanagan, J. G. Regulated cleavage of a contactmediated axon repellent. Science 289, 1360–1365 (2000).
46. Hiramoto, M., Hiromi, Y., Giniger, E. & Hotta, Y. The Drosophila Netrin receptor Frazzled guides axons by controlling Netrin distribution. Nature 406, 886–889 (2000).
47. Brose, K. et al. Slit proteins bind Robo receptors and have an evolutionarily conserved role in repulsive axon guidance. Cell 96, 795–806 (1999).
48. Lander, A. D. Mechanisms by which molecules guide axons. Curr. Opin. Cell Biol. 2, 907–913 (1990).
49. Tanaka, E. & Sabry, J. Making the connection: cytoskeletal rearrangements during growth cone guidance. Cell 83, 171–176 (1995).
50. Nobes, C. D. & Hall, A. Rho, rac, and cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia. Cell 81, 53–62 (1995).
51. Luo, L., Liao, Y. J., Jan, L. Y. & Jan, Y. N. Distinct morphogenetic functions of similar small GTPases: Drosophila Drac1 is involved in axonal outgrowth and myoblast fusion. Genes Dev. 8, 1787–1802 (1994).
52. Zipkin, I. D., Kindt, R. M. & Kenyon, C. J. Role of a new Rho family member in cell migration and axon guidance in C. elegans. Cell 90, 883–894 (1997).
53. Steven, R. et al. UNC-73 activates the Rac GTPase and is required for cell and growth cone migrations in C. elegans. Cell 92, 785–795 (1998).
54. Luo, L. Trio quartet in D. (melanogaster). Neuron 26, 1–2 (2000).
55. Shamah, S. M. et al. EphA receptors regulate growth cone dynamics through the novel guanine nucleotide exchange factor ephexin. Cell 105, 233–244 (2001).
56. Mueller, B. K. Growth cone guidance: first steps towards a deeper understanding. Annu. Rev. Neurosci. 22, 351–388 (1999).
57. Song, H. & Poo, M. The cell biology of neuronal navigation. Nat Cell Biol. 3, E81–E88 (2001).
58. Wightman, B. et al. The C. elegans gene vab-8 guides posteriorly directed axon outgrowth and cell migration. Development 122, 671–682 (1996).
59. Wolf, F. W., Hung, M. S., Wightman, B., Way, J. & Garriga, G. vab-8 is a key regulator of posteriorly directed migrations in C. elegans and encodes a novel protein with kinesin motor similarity. Neuron 20, 655–666 (1998).
60. Bashaw, G. J., Kidd, T., Murray, D., Pawson, T. & Goodman, C. S. Repulsive axon guidance: Abelson and Enabled play opposing roles downstream of the roundabout receptor. Cell 101, 703–715 (2000).
61. Sun, Q., Bahri, S., Schmid, A., Chia, W. & Zinn, K. Receptor tyrosine phosphatases regulate axon guidance across the midline of the Drosophila embryo. Development 127, 801–812 (2000).
62. Hong, K., Nishiyama, M., Henley, J., Tessier-Lavigne, M. & Poo, M. Calcium signalling in the guidance of nerve growth by netrin-1. Nature 403, 93–98 (2000).
63. Zheng, J. Q. Turning of nerve growth cones induced by localized increases in intracellular calcium ions. Nature 403, 89–93 (2000).
64. Ming, G. L. et al. cAMP-dependent growth cone guidance by netrin-1. Neuron 19, 1225–1235 (1997).
65. Song, H. et al. Conversion of neuronal growth cone responses from repulsion to attraction by cyclic nucleotides. Science 281, 1515–1518 (1998).
66. Polleux, F., Giger, R. J., Ginty, D. D., Kolodkin, A. L. & Ghosh, A. Patterning of cortical efferent projections by semaphorin–neuropilin interactions. Science 282, 1904–1906 (1998).
67. Polleux, F., Morrow, T. & Ghosh, A. Semaphorin 3A is a chemoattractant for cortical apical dendrites. Nature 404, 567–573 (2000).
68. Davis, S. et al. Ligands for EPH-related receptor tyrosine kinases that require membrane attachment or clustering for activity. Science 266, 816–819 (1994).
69. Bruckner, K. & Klein, R. Signaling by Eph receptors and their ephrin ligands. Curr. Opin. Neurobiol. 8, 375–382 (1998).
70. Smalla, M. et al. Solution structure of the receptor tyrosine kinase EphB2 SAM domain and identification of two distinct homotypic interaction sites. Protein Sci. 8, 1954–1961 (1999).
71. Stapleton, D., Balan, I., Pawson, T. & Sicheri, F. The crystal structure of an Eph receptor SAM domain reveals a mechanism for modular dimerization. Nature Struct. Biol. 6, 44–49 (1999).
72. Thanos, C. D., Goodwill, K. E. & Bowie, J. U. Oligomeric structure of the human EphB2 receptor SAM domain. Science 283, 833–836 (1999).
73. Kullander, K. et al. Kinase-dependent and kinase-independent functions of EphA4 receptors in major axon tract formation in vivo. Neuron 29, 73–84 (2001).
74. Schlessinger, J. Cell signaling by receptor tyrosine kinases. Cell 103, 211–225 (2000).
75. Stein, E., Zou, Y., Poo, M. & Tessier-Lavigne, M. Binding of DCC by netrin-1 to mediate axon guidance independent of adenosine A2B receptor activation. Science 291, 1976–1982 (2001).
76. Tamagnone, L. et al. Plexins are a large family of receptors for transmembrane, secreted, and GPI-anchored semaphorins in vertebrates. Cell 99, 71–80 (1999).
77. Takahashi, T. et al. Plexin–neuropilin-1 complexes form functional semaphorin–3A receptors. Cell 99, 59–69 (1999).
78. Takahashi, T. & Strittmatter, S. M. Plexin-A1 autoinhibition by the plexin sema domain. Neuron 29, 429–439 (2001).
79. Nakamura, F., Tanaka, M., Takahashi, T., Kalb, R. G. & Strittmatter, S. M. Neuropilin-1 extracellular domains mediate semaphorin D/III-induced growth cone collapse. Neuron 21, 1093–1100 (1998).
80. He, Z. & Tessier-Lavigne, M. Neuropilin is a receptor for the axonal chemorepellent Semaphorin III. Cell 90, 739–751 (1997).
81. Kitsukawa, T. et al. Neuropilin–semaphorin III/D-mediated chemorepulsive signals play a crucial role in peripheral nerve projection in mice. Neuron 19, 995–1005 (1997).
82. Kolodkin, A. L. et al. Neuropilin is a semaphorin III receptor. Cell 90, 753–762 (1997).
83. Chen, H., Chedotal, A., He, Z., Goodman, C. S. & Tessier-Lavigne, M. Neuropilin-2, a novel member of the neuropilin family, is a high affinity receptor for the semaphorins Sema E and Sema IV but not Sema III. Neuron 19, 547–559 (1997).
84. Soker, S., Takashima, S., Miao, H. Q., Neufeld, G. & Klagsbrun, M. Neuropilin-1 is expressed by endothelial and tumor cells as an isoformspecific receptor for vascular endothelial growth factor. Cell 92, 735–745 (1998).
85. Whitaker, G. B., Limberg, B. J. & Rosenbaum, J. S. Vascular endothelial growth factor receptor-2 and neuropilin-1 form a receptor complex that is responsible for the differential signaling potency of vegf165 and vegf21. J. Biol. Chem. 276, 25520–25531 (2001).
86. Castellani, V., Chedotal, A., Schachner, M., Faivre-Sarrailh, C. & Rougon, G. Analysis of the L1-deficient mouse phenotype reveals cross-talk between Sema3A and L1 signaling pathways in axonal guidance. Neuron 27, 237–249 (2000).
87. Kidd, T., Bland, K. S. & Goodman, C. S. Slit is the midline repellent for the Robo receptor in Drosophila. Cell 96, 785–794 (1999).
88. Simpson, J. H., Kidd, T., Bland, K. S. & 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, 753–766 (2000).
89. Simpson, J. H., Bland, K. S., Fetter, R. D. & 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, 1019–1032 (2000).
90. Rajagopalan, S., Nicolas, E., Vivancos, V., Berger, J. & Dickson, B. J. Crossing the midline: roles and regulation of Robo receptors. Neuron 28, 767–777 (2000).
91. Rajagopalan, S., Vivancos, V., Nicolas, E. & Dickson, B. J. Selecting a longitudinal pathway: Robo receptors specify the lateral position of axons in the Drosophila CNS. Cell 103, 1033–1045 (2000).
92. Chan, S. S. et al. 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 (1996).
93. Corset, V. et al. Netrin-1-mediated axon outgrowth and cAMP production requires interaction with adenosine A2b receptor. Nature 407, 747–750 (2000).
94. Leung-Hagesteijn, C. et al. UNC-5, a transmembrane protein with immunoglobulin and thrombospondin type 1 domains, guides cell and pioneer axon migrations in C. elegans. Cell 71, 289–299 (1992).
95. Leonardo, E. D. et al. Vertebrate homologues of C. elegans UNC-5 are candidate netrin receptors. Nature 386, 833–838 (1997).
96. Hamelin, M., Zhou, Y., Su, M. W., Scott, I. M. & Culotti, J. G. Expression of the UNC-5 guidance receptor in the touch neurons of C. elegans steers their axons dorsally. Nature 364, 327–330 (1993).
97. Hong, K. et al. 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 (1999).
98. Colavita, A. & Culotti, J. G. Suppressors of ectopic UNC-5 growth cone steering identify eight genes involved in axon guidance in Caenorhabditis elegans. Dev. Biol. 194, 72–85 (1998).
99. Hopker, V. H., Shewan, D., Tessier-Lavigne, M., Poo, M. & Holt, C. Growthcone attraction to netrin-1 is converted to repulsion by laminin-121. Nature 401, 69–73 (1999).
100. Stein, E. & Tessier-Lavigne, M. Hierarchical organization of guidance receptors: silencing of netrin attraction by slit through a Robo/DCC receptor complex. Science 291, 1928–1938 (2001).
101. Lu, Q., Sun, E. E., Klein, R. S. & Flanagan, J. G. Ephrin-B reverse signaling is mediated by a novel PDZ–RGS protein and selectively inhibits G protein–coupled chemoattraction. Cell 105, 69–79 (2001)