Direct binding of TUBB3 with DCC couples netrin-1 signaling to intracellular microtubule dynamics in axon outgrowth and guidance

Journal of Cell Science

Volumn 126, Issue 14, 2013, Pages 3070-3081

  Qu, Chao ^a   Dwyer, Trisha ^a   Shao, Qiangqiang ^a   Yang, Tao ^a   Huang, Huai ^a   Liu, Guofa ^a  

^a UNIVERSITY OF TOLEDO   (United States)

Author keywords

Axon guidance; DCC; Microtubule dynamics; Netrin; Signal transduction; TUBB3

Indexed keywords

BETA TUBULIN; DCC RECEPTOR; NETRIN 1; RECEPTOR; SMALL INTERFERING RNA; TUBB3 PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BRAIN CELL; GROWTH CONE; IN VITRO STUDY; MICROTUBULE; MOLECULAR DYNAMICS; NERVE FIBER GROWTH; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN INTERACTION; SIGNAL TRANSDUCTION;

AXON GUIDANCE; DCC; MICROTUBULE DYNAMICS; NETRIN; SIGNAL TRANSDUCTION; TUBB3;

ANIMALS; AXONS; CELL GROWTH PROCESSES; CHICK EMBRYO; GENE KNOCKDOWN TECHNIQUES; HEK293 CELLS; HUMANS; INTRACELLULAR SPACE; MICE; MICROTUBULES; NERVE GROWTH FACTORS; NEURONS; PROTEIN BINDING; PROTEIN TRANSPORT; RECEPTORS, CELL SURFACE; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; SPINAL CORD; TRANSGENES; TUBULIN; TUMOR SUPPRESSOR PROTEINS;

EID: 84880675455     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.122184     Document Type: Article

References (51)

1. Ackerman, S. L., Kozak, L. P., Przyborski, S. A., Rund, L. A., Boyer, B. B. and Knowles, B. B. (1997). The mouse rostral cerebellar malformation gene encodes an UNC-5-like protein. Nature 386, 838-842.
2. Alcántara, S., Ruiz, M., De Castro, F., Soriano, E. and Sotelo, C. (2000). Netrin 1 acts as an attractive or as a repulsive cue for distinct migrating neurons during the development of the cerebellar system. Development 127, 1359-1372.
3. Buck, K. B. and Zheng, J. Q. (2002). Growth cone turning induced by direct local modification of microtubule dynamics. J. Neurosci. 22, 9358-9367.
4. Colamarino, S. A. and Tessier-Lavigne, M. (1995). The axonal chemoattractant netrin-1 is also a chemorepellent for trochlear motor axons. Cell 81, 621-629.
5. Dent, E. W. and Gertler, F. B. (2003). Cytoskeletal dynamics and transport in growth cone motility and axon guidance. Neuron 40, 209-227.
6. Dent, E. W., Barnes, A. M., Tang, F. and Kalil, K. (2004). Netrin-1 and semaphorin 3A promote or inhibit cortical axon branching, respectively, by reorganization of the cytoskeleton. J. Neurosci. 24, 3002-3012.
7. Dent, E. W., Gupton, S. L. and Gertler, F. B. (2011). The growth cone cytoskeleton in axon outgrowth and guidance. Cold Spring Harb. Perspect. Biol. 3.
8. Fazeli, A., Dickinson, S. L., Hermiston, M. L., Tighe, R. V., Steen, R. G., Small, C. G., Stoeckli, E. T., Keino-Masu, K., Masu, M., Rayburn, H. et al. (1997). Phenotype of mice lacking functional Deleted in colorectal cancer (Dcc) gene. Nature 386, 796-804.
9. Finger, J. H., Bronson, R. T., Harris, B., Johnson, K., Przyborski, S. A. and Ackerman, S. L. (2002). The netrin 1 receptors Unc5h3 and Dcc are necessary at multiple choice points for the guidance of corticospinal tract axons. J. Neurosci. 22, 10346-10356.
10. Gitai, Z., Yu, T. W., Lundquist, E. A., Tessier-Lavigne, M. and Bargmann, C. I. (2003). The netrin receptor UNC-40/DCC stimulates axon attraction and outgrowth through enabled and, in parallel, Rac and UNC-115/AbLIM. Neuron 37, 53-65.
11. Guan, K. L. and Rao, Y. (2003). Signalling mechanisms mediating neuronal responses to guidance cues. Nat. Rev. Neurosci. 4, 941-956.
12. Hedgecock, E. M., Culotti, J. G. and Hall, D. H. (1990). 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.
13. 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.
14. Ishii, N., Wadsworth, W. G., Stern, B. D., Culotti, J. G. and Hedgecock, E. M. (1992). UNC-6, a laminin-related protein, guides cell and pioneer axon migrations in C. elegans. Neuron 9, 873-881.
15. Jaglin, X. H., Poirier, K., Saillour, Y., Buhler, E., Tian, G., Bahi-Buisson, N., Fallet-Bianco, C., Phan-Dinh-Tuy, F., Kong, X. P., Bomont, P. et al. (2009). Mutations in the beta-tubulin gene TUBB2B result in asymmetrical polymicrogyria. Nat. Genet. 41, 746-752.
16. Kalil, K. and Dent, E. W. (2005). Touch and go: guidance cues signal to the growth cone cytoskeleton. Curr. Opin. Neurobiol. 15, 521-526.
17. Katsetos, C. D., Legido, A., Perentes, E. and Mörk, S. J. (2003). Class III beta-tubulin isotype: a key cytoskeletal protein at the crossroads of developmental neurobiology and tumor neuropathology. J. Child Neurol. 18, 851-866, discussion 867.
18. Keays, D. A., Tian, G., Poirier, K., Huang, G.-J., Siebold, C., Cleak, J., Oliver, P. L., Fray, M., Harvey, R. J., Molnár, Z. et al. (2007). Mutations in alpha-tubulin cause abnormal neuronal migration in mice and lissencephaly in humans. Cell 128, 45-57.
19. Keeling, S. L., Gad, J. M. and Cooper, H. M. (1997). Mouse Neogenin, a DCC-like molecule, has four splice variants and is expressed widely in the adult mouse and during embryogenesis. Oncogene 15, 691-700.
20. Keino-Masu, K., Masu, M., Hinck, L., Leonardo, E. D., Chan, S. S., Culotti, J. G. and Tessier-Lavigne, M. (1996). Deleted in Colorectal Cancer (DCC) encodes a netrin receptor. Cell 87, 175-185.
21. 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.
22. Kolodkin, A. L. and Tessier-Lavigne, M. (2011). Mechanisms and molecules of neuronal wiring: a primer. Cold Spring Harb. Perspect. Biol. 3.
23. 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.
24. Lai Wing Sun, K., Correia, J. P. and Kennedy, T. E. (2011). Netrins: versatile extracellular cues with diverse functions. Development 138, 2153-2169.
25. Leonardo, E. D., Hinck, L., Masu, M., Keino-Masu, K., Ackerman, S. L. and Tessier-Lavigne, M. (1997). Vertebrate homologues of C. elegans UNC-5 are candidate netrin receptors. Nature 386, 833-838.
26. Li, W., Lee, J., Vikis, H. G., Lee, S. H., Liu, G., Aurandt, J., Shen, T. L., Fearon, E. R., Guan, J. L., Han, M. et al. (2004). Activation of FAK and Src are receptorproximal events required for netrin signaling. Nat. Neurosci. 7, 1213-1221.
27. Li, X., Gao, X., Liu, G., Xiong, W., Wu, J. and Rao, Y. (2008). Netrin signal transduction and the guanine nucleotide exchange factor DOCK180 in attractive signaling. Nat. Neurosci. 11, 28-35.
28. Liu, G., Beggs, H., Jürgensen, C., Park, H. T., Tang, H., Gorski, J., Jones, K. R., Reichardt, L. F., Wu, J. and Rao, Y. (2004). Netrin requires focal adhesion kinase and Src family kinases for axon outgrowth and attraction. Nat. Neurosci. 7, 1222-1232.
29. Liu, G., Li, W., Gao, X., Li, X., Jü rgensen, C., Park, H. T., Shin, N. Y., Yu, J., He, M. L., Hanks, S. K. et al. (2007). p130CAS is required for netrin signaling and commissural axon guidance. J. Neurosci. 27, 957-968.
30. Liu, G., Li, W., Wang, L., Kar, A., Guan, K. L., Rao, Y. and Wu, J. Y. (2009). DSCAM functions as a netrin receptor in commissural axon pathfinding. Proc. Natl. Acad. Sci. USA 106, 2951-2956.
31. Lowery, L. A. and Van Vactor, D. (2009). The trip of the tip: understanding the growth cone machinery. Nat. Rev. Mol. Cell Biol. 10, 332-343.
32. Ly, A., Nikolaev, A., Suresh, G., Zheng, Y., Tessier-Lavigne, M. and Stein, E. (2008). DSCAM is a netrin receptor that collaborates with DCC in mediating turning responses to netrin-1. Cell 133, 1241-1254.
33. Marsh, L. and Letourneau, P. C. (1984). Growth of neurites without filopodial or lamellipodial activity in the presence of cytochalasin B. J. Cell Biol. 99, 2041-2047.
34. Meriane, M., Tcherkezian, J., Webber, C. A., Danek, E. I., Triki, I., McFarlane, S., Bloch-Gallego, E. and Lamarche-Vane, N. (2004). Phosphorylation of DCC by Fyn mediates Netrin-1 signaling in growth cone guidance. J. Cell Biol. 167, 687-698.
35. Poirier, K., Saillour, Y., Bahi-Buisson, N., Jaglin, X. H., Fallet-Bianco, C., Nabbout, R., Castelnau-Ptakhine, L., Roubertie, A., Attie-Bitach, T., Desguerre, I. et al. (2010). Mutations in the neuronal ß-tubulin subunit TUBB3 result in malformation of cortical development and neuronal migration defects. Hum. Mol. Genet. 19, 4462-4473.
36. Purohit, A. A., Li, W., Qu, C., Dwyer, T., Shao, Q., Guan, K.-L. and Liu, G. (2012). Down syndrome cell adhesion molecule (DSCAM) associates with uncoordinated-5C (UNC5C) in netrin-1-mediated growth cone collapse. J. Biol. Chem. 287, 27126-27138.
37. Qu, C., Li, W., Shao, Q., Dwyer, T., Huang, H., Yang, T. and Liu, G. (2013). c-Jun N-terminal kinase 1 (JNK1) is required for coordination of netrin signaling in axon guidance. J. Biol. Chem. 288, 1883-1895.
38. Sbalzarini, I. F. and Koumoutsakos, P. (2005). Feature point tracking and trajectory analysis for video imaging in cell biology. J. Struct. Biol. 151, 182-195.
39. Sengottuvel, V., Leibinger, M., Pfreimer, M., Andreadaki, A. and Fischer, D. (2011). Taxol facilitates axon regeneration in the mature CNS. J. Neurosci. 31, 2688-2699.
40. 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.
41. 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.
42. 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.
43. Stein, E., Zou, Y., Poo, M. and Tessier-Lavigne, M. (2001). Binding of DCC by netrin-1 to mediate axon guidance independent of adenosine A2B receptor activation. Science 291, 1976-1982.
44. Suter, D. M. and Forscher, P. (2000). Substrate-cytoskeletal coupling as a mechanism for the regulation of growth cone motility and guidance. J. Neurobiol. 44, 97-113.
45. Suter, D. M., Schaefer, A. W. and Forscher, P. (2004). Microtubule dynamics are necessary for SRC family kinase-dependent growth cone steering. Curr. Biol. 14, 1194-1199.
46. Tanaka, E. and Kirschner, M. W. (1995). The role of microtubules in growth cone turning at substrate boundaries. J. Cell Biol. 128, 127-137.
47. Tanaka, E. and Sabry, J. (1995). Making the connection: cytoskeletal rearrangements during growth cone guidance. Cell 83, 171-176.
48. 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.
49. Tischfield, M. A., Baris, H. N., Wu, C., Rudolph, G., Van Maldergem, L., He, W., Chan, W. M., Andrews, C., Demer, J. L., Robertson, R. L. et al. (2010). Human TUBB3 mutations perturb microtubule dynamics, kinesin interactions, and axon guidance. Cell 140, 74-87.
50. Vitriol, E. A. and Zheng, J. Q. (2012). Growth cone travel in space and time: the cellular ensemble of cytoskeleton, adhesion, and membrane. Neuron 73, 1068-1081.
51. Yu, J.-Y., DeRuiter, S. L. and Turner, D. L. (2002). RNA interference by expression of short-interfering RNAs and hairpin RNAs in mammalian cells. Proc. Natl. Acad. Sci. USA 99, 6047-6052.