Down syndrome cell adhesion molecule (DSCAM) associates with uncoordinated-5C (UNC5C) in netrin-1-mediated growth cone collapse

Journal of Biological Chemistry

Volumn 287, Issue 32, 2012, Pages 27126-27138

  Purohit, Anish A ^a   Li, Weiquan ^b   Qu, Chao ^a   Dwyer, Trisha ^a   Shao, Qiangqiang ^a   Guan, Kun Liang ^c   Liu, Guofa ^a  

^a UNIVERSITY OF TOLEDO   (United States)

^b UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AXON GROWTH; BIFUNCTIONAL; BRAIN TISSUE; CELL ADHESION MOLECULES; CEREBELLAR GRANULE CELLS; CEREBELLAR NEURONS; COLORECTAL CANCER; COMPLEX FORMATIONS; CORTICAL NEURONS; DOMINANT-NEGATIVE MUTANTS; DOWN SYNDROME; EXTRACELLULAR ENVIRONMENTS; GROWTH CONES; NEURONAL GROWTH CONES; SIGNALING MOLECULES; SRC-FAMILY KINASE; TYROSINE PHOSPHORYLATION;

AMINO ACIDS; BRAIN; CELLS; CYTOLOGY; GRANULATION; MAMMALS; PHOSPHORYLATION;

NEURONS;

CELL ADHESION MOLECULE; DOWN SYNDROME CELL ADHESION MOLECULE; NETRIN 1; P21 ACTIVATED KINASE 1; PROTEIN FAK; PROTEIN KINASE FYN; PROTEIN TYROSINE KINASE; SHORT HAIRPIN RNA; TYROSINE; UNCLASSIFIED DRUG; UNCOORDINATED 5C PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CELL; BRAIN TISSUE; CEREBELLUM; COMPLEX FORMATION; CONTROLLED STUDY; EMBRYO; ENZYME INHIBITION; GENE SILENCING; GRANULE CELL; GROWTH CONE; INTRACELLULAR SIGNALING; MOUSE; NERVE FIBER GROWTH; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PERINATAL PERIOD; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; TISSUE INJURY;

ANIMALS; BLOTTING, WESTERN; CELL ADHESION MOLECULES; CELLS, CULTURED; DNA PRIMERS; GROWTH CONES; MICE; NERVE GROWTH FACTORS; RECEPTORS, CELL SURFACE; SIGNAL TRANSDUCTION; SRC-FAMILY KINASES; TUMOR SUPPRESSOR PROTEINS;

EID: 84864532040     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.340174     Document Type: Article

References (73)

1. Tessier-Lavigne, M., and Goodman, C. S. (1996) The molecular biology of axon guidance. Science 274, 1123-1133 (Pubitemid 26389268)
2. Dodd, J., and Jessell, T. M. (1988) Axon guidance and the patterning of neuronal projections in vertebrates. Science 242, 692-699
3. Guan, K. L., and Rao, Y. (2003) Signaling mechanisms mediating neuronal responses to guidance cues. Nat. Rev. Neurosci. 4, 941-956
4. Lai Wing, Sun, K., Correia, J. P., and Kennedy, T. E. (2011) Netrins: versatile extracellular cues with diverse functions. Development 138, 2153-2169
5. Zou, Y., and Lyuksyutova, A. I. (2007) Morphogens as conserved axon guidance cues. Curr. Opin. Neurobiol. 17, 22-28 (Pubitemid 46237742)
6. 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 (Pubitemid 20149756)
7. 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 (Pubitemid 19014437)
8. 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
9. 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 (Pubitemid 24250807)
10. 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 (Pubitemid 26358998)
11. Mitchell, K. J., Doyle, J. L., Serafini, T., Kennedy, T. E., Tessier-Lavigne, M., Goodman, C. S., and Dickson, B. J. (1996) Genetic analysis of Netrin genes in Drosophila: Netrins guide CNS commissural axons and peripheral motor axons. Neuron 17, 203-215 (Pubitemid 26296148)
12. 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 (Pubitemid 24250806)
13. 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 (Pubitemid 26358997)
14. Fearon, E. R., Cho, K. R., Nigro, J. M., Kern, S. E., Simons, J. W., Ruppert, J. M., Hamilton, S. R., Preisinger, A. C., Thomas, G., and Kinzler, K. W. (1990) Identification of a chromosome 18q gene that is altered in colorectal cancers. Science 247, 49-56
15. Cooper, H. M., Armes, P., Britto, J., Gad, J., and Wilks, A. F. (1995) Cloning of the mouse homologue of the deleted in colorectal cancer gene (mDCC) and its expression in the developing mouse embryo. Oncogene 11, 2243-2254 (Pubitemid 26008400)
16. 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., Simons, J., Bronson, R. T., Gordon, J. I., Tessier-Lavigne, M., and Weinberg, R. A. (1997) Phenotype of mice lacking functional Deleted in colorectal cancer (Dcc) gene. Nature 386, 796-804 (Pubitemid 27181247)
17. 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 (Pubitemid 27389932)
18. Meyerhardt, J. A., Look, A. T., Bigner, S. H., and Fearon, E. R. (1997) Identification and characterization of neogenin, a DCC-related gene. Oncogene 14, 1129-1136 (Pubitemid 27141914)
19. Andrews, G. L., Tanglao, S., Farmer, W. T., Morin, S., Brotman, S., Berberoglu, M. A., Price, H., Fernandez, G. C., Mastick, G. S., Charron, F., and Kidd, T. (2008) Dscam guides embryonic axons by Netrin-dependent and -independent functions. Development 135, 3839-3848
20. 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 (Pubitemid 351852917)
21. 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. U.S.A. 106, 2951-2956
22. 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 (Pubitemid 27181258)
23. 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 (Pubitemid 27181257)
24. Przyborski, S. A., Knowles, B. B., and Ackerman, S. L. (1998) Embryonic phenotype of Unc5h3 mutant mice suggests chemorepulsion during the formation of the rostral cerebellar boundary. Development 125, 41-50 (Pubitemid 28048452)
25. Engelkamp, D. (2002) Cloning of three mouse Unc5 genes and their expression patterns at mid-gestation. Mech. Dev. 118, 191-197
26. 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 (Pubitemid 29375051)
27. Killeen, M., Tong, J., Krizus, A., Steven, R., Scott, I., Pawson, T., and Culotti, J. (2002) UNC-5 function requires phosphorylation of cytoplasmic tyrosine 482, but its UNC-40-independent functions also require a region between the ZU-5 and death domains. Dev. Biol. 251, 348-366 (Pubitemid 35373754)
28. Keleman, K., and Dickson, B. J. (2001) Short- and long-range repulsion by the Drosophila Unc5 netrin receptor. Neuron 32, 605-617 (Pubitemid 33145195)
29. Chen, B. E., Kondo, M., Garnier, A., Watson, F. L., Püettmann- Holgado, R., Lamar, D. R., and Schmucker, D. (2006) The molecular diversity of Dscam is functionally required for neuronal wiring specificity in Drosophila. Cell 125, 607-620
30. Hummel, T., Vasconcelos, M. L., Clemens, J. C., Fishilevich, Y., Vosshall, L. B., and Zipursky, S. L. (2003) Axonal targeting of olfactory receptor neurons in Drosophila is controlled by Dscam. Neuron 37, 221-231 (Pubitemid 36143818)
31. Schmucker, D., Clemens, J. C., Shu, H., Worby, C. A., Xiao, J., Muda, M., Dixon, J. E., and Zipursky, S. L. (2000) Drosophila Dscam is an axon guidance receptor exhibiting extraordinary molecular diversity. Cell 101, 671-684
32. Wang, J., Zugates, C. T., Liang, I. H., Lee, C. H., and Lee, T. (2002) Drosophila Dscam is required for divergent segregation of sister branches and suppresses ectopic bifurcation of axons. Neuron 33, 559-571 (Pubitemid 34188432)
33. Zhu, H., Hummel, T., Clemens, J. C., Berdnik, D., Zipursky, S. L., and Luo, L. (2006) Dendritic patterning by Dscam and synaptic partner matching in the Drosophila antennal lobe. Nat. Neurosci. 9, 349-355 (Pubitemid 43290964)
34. Zhan, X. L., Clemens, J. C., Neves, G., Hattori, D., Flanagan, J. J., Hummel, T., Vasconcelos, M. L., Chess, A., and Zipursky, S. L. (2004) Analysis of Dscam diversity in regulating axon guidance in Drosophila mushroom bodies. Neuron 43, 673-686 (Pubitemid 39179727)
35. Fuerst, P. G., Bruce, F., Tian, M., Wei, W., Elstrott, J., Feller, M. B., Erskine, L., Singer, J. H., and Burgess, R. W. (2009) DSCAM and DSCAML1 function in self-avoidance in multiple cell types in the developing mouse retina. Neuron 64, 484-497
36. Fuerst, P. G., Koizumi, A., Masland, R. H., and Burgess, R. W. (2008) Neurite arborization and mosaic spacing in the mouse retina require DSCAM. Nature 451, 470-474 (Pubitemid 351158890)
37. Yamagata, M., and Sanes, J. R. (2008) Dscam and Sidekick proteins direct lamina-specific synaptic connections in vertebrate retina. Nature 451, 465-469 (Pubitemid 351158882)
38. Kruger, R. P., Lee, J., Li, W., and Guan, K. L. (2004) Mapping netrin receptor binding reveals domains of Unc5 regulating its tyrosine phosphorylation. J. Neurosci. 24, 10826-10834 (Pubitemid 39602394)
39. Li, W., and Guan, K. L. (2004) The Down syndrome cell adhesion molecule (DSCAM) interacts with and activates Pak. J. Biol. Chem. 279, 32824-32831 (Pubitemid 39014742)
40. 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 (Pubitemid 39426242)
41. Liu, G., Li, W., Gao, X., Li, X., Jürgensen, C., Park, H. T., Shin, N. Y., Yu, J., He, M. L., Hanks, S. K., Wu, J. Y., Guan, K. L., and Rao, Y. (2007) p130CAS is required for netrin signaling and commissural axon guidance. J. Neurosci. 27, 957-968 (Pubitemid 46174517)
42. 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 (Pubitemid 30232588)
43. Bartoe, J. L., McKenna, W. L., Quan, T. K., Stafford, B. K., Moore, J. A., Xia, J., Takamiya, K., Huganir, R. L., and Hinck, L. (2006) Protein interacting with C-kinase 1/protein kinase Calpha-mediated endocytosis converts netrin-1-mediated repulsion to attraction. J. Neurosci. 26, 3192-3205
44. Barlow, G. M., Micales, B., Chen, X. N., Lyons, G. E., and Korenberg, J. R. (2002) Mammalian DSCAMs: roles in the development of the spinal cord, cortex, and cerebellum? Biochem. Biophys. Res. Commun. 293, 881-891 (Pubitemid 34694124)
45. Guijarro, P., Simó, S., Pascual, M., Abasolo, I., Del Rio, J. A., and Soriano, E. (2006) Netrin1 exerts a chemorepulsive effect on migrating cerebellar interneurons in a Dcc-independent way. Mol. Cell Neurosci. 33, 389-400 (Pubitemid 44820856)
46. Hata, K., Kaibuchi, K., Inagaki, S., and Yamashita, T. (2009) Unc5B associates with LARG to mediate the action of repulsive guidance molecule. J. Cell Biol. 184, 737-750
47. Ren, X. R., Ming, G. L., Xie, Y., Hong, Y., Sun, D. M., Zhao, Z. Q., Feng, Z., Wang, Q., Shim, S., Chen, Z. F., Song, H. J., Mei, L., and Xiong, W. C. (2004) Focal adhesion kinase in netrin-1 signaling. Nat. Neurosci. 7, 1204-1212 (Pubitemid 39426240)
48. 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., Rao, Y., Hong, K., and Guan, K. L. (2004) Activation of FAK and Src are receptor-proximal events required for netrin signaling. Nat. Neurosci. 7, 1213-1221 (Pubitemid 39426241)
49. 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 (Pubitemid 39565149)
50. Shekarabi, M., Moore, S. W., Tritsch, N. X., Morris, S. J., Bouchard, J. F., and Kennedy, T. E. (2005) Deleted in colorectal cancer binding netrin-1 mediates cell substrate adhesion and recruits Cdc42, Rac1, Pak1, and N-WASP into an intracellular signaling complex that promotes growth cone expansion. J. Neurosci. 25, 3132-3141 (Pubitemid 40463548)
51. Li, W., Aurandt, J., Jürgensen, C., Rao, Y., and Guan, K. L. (2006) FAK and Src kinases are required for netrin-induced tyrosine phosphorylation of UNC5. J. Cell Sci. 119, 47-55 (Pubitemid 43169297)
52. Tang, X., Jang, S. W., Okada, M., Chan, C. B., Feng, Y., Liu, Y., Luo, S. W., Hong, Y., Rama, N., Xiong, W. C., Mehlen, P., and Ye, K. (2008) Netrin-1 mediates neuronal survival through PIKE-L interaction with the dependence receptor UNC5B. Nat. Cell Biol. 10, 698-706 (Pubitemid 351772935)
53. Matthews, B. J., Kim, M. E., Flanagan, J. J., Hattori, D., Clemens, J. C., Zipursky, S. L., and Grueber, W. B. (2007) Dendrite self-avoidance is controlled by Dscam. Cell 129, 593-604
54. Hughes, M. E., Bortnick, R., Tsubouchi, A., Bäumer, P., Kondo, M., Uemura, T., and Schmucker, D. (2007) Homophilic Dscam interactions control complex dendrite morphogenesis. Neuron 54, 417-427 (Pubitemid 46659811)
55. Soba, P., Zhu, S., Emoto, K., Younger, S., Yang, S. J., Yu, H. H., Lee, T., Jan, L. Y., and Jan, Y. N. (2007) Drosophila sensory neurons require Dscam for dendritic self-avoidance and proper dendritic field organization. Neuron 54, 403-416 (Pubitemid 46659807)
56. Hattori, D., Millard, S. S., Wojtowicz, W. M., and Zipursky, S. L. (2008) Dscam-mediated cell recognition regulates neural circuit formation. Annu. Rev. Cell Dev. Biol. 24, 597-620
57. Agarwala, K. L., Nakamura, S., Tsutsumi, Y., and Yamakawa, K. (2000) Down syndrome cell adhesion molecule DSCAM mediates homophilic intercellular adhesion. Brain Res. Mol. Brain Res. 79, 118-126 (Pubitemid 30495535)
58. Yamakawa, K., Huot, Y. K., Haendelt, M. A., Hubert, R., Chen, X. N., Lyons, G. E., and Korenberg, J. R. (1998) DSCAM: a novel member of the immunoglobulin superfamily maps in a Down syndrome region and is involved in the development of the nervous system. Hum. Mol. Genet 7, 227-237 (Pubitemid 28048538)
59. Matthews, B. J., and Grueber, W. B. (2011) Dscam1-mediated self-avoidance counters netrin-dependent targeting of dendrites in Drosophila. Curr. Biol. 21, 1480-1487
60. Islam, S. M., Shinmyo, Y., Okafuji, T., Su, Y., Naser, I. B., Ahmed, G., Zhang, S., Chen, S., Ohta, K., Kiyonari, H., Abe, T., Tanaka, S., Nishinakamura, R., Terashima, T., Kitamura, T., and Tanaka, H. (2009) Draxin, a repulsive guidance protein for spinal cord and forebrain commissures. Science 323, 388-393
61. Ahmed, G., Shinmyo, Y., Ohta, K., Islam, S. M., Hossain, M., Naser, I. B., Riyadh, M. A., Su, Y., Zhang, S., Tessier-Lavigne, M., and Tanaka, H. (2011) Draxin inhibits axonal outgrowth through the netrin receptor DCC. J. Neurosci. 31, 14018-14023
62. Williams, M. E., Wu, S. C., McKenna, W. L., and Hinck, L. (2003) Surface expression of the netrin receptor UNC5H1 is regulated through a protein kinase C-interacting protein/protein kinase-dependent mechanism. J. Neurosci. 23, 11279-11288 (Pubitemid 37549683)
63. Tong, J., Killeen, M., Steven, R., Binns, K. L., Culotti, J., and Pawson, T. (2001) Netrin stimulates tyrosine phosphorylation of the UNC-5 family of netrin receptors and induces Shp2 binding to the RCM cytodomain. J. Biol. Chem. 276, 40917-40925
64. Lucanic, M., Kiley, M., Ashcroft, N., L'Etoile, N., and Cheng, H. J. (2006) The Caenorhabditis elegans P21-activated kinases are differentially required for UNC-6/netrin-mediated commissural motor axon guidance. Development 133, 4549-4559 (Pubitemid 46017829)
65. Huang, X., Cheng, H. J., Tessier-Lavigne, M., and Jin, Y. (2002) MAX-1, a novel PH/MyTH4/FERM domain cytoplasmic protein implicated in netrin-mediated axon repulsion. Neuron 34, 563-576 (Pubitemid 34628753)
66. Li, X., Saint-Cyr-Proulx, E., Aktories, K., and Lamarche-Vane, N. (2002) Rac1 and Cdc42 but not RhoA or Rho kinase activities are required for neurite outgrowth induced by the Netrin-1 receptor DCC (deleted in colorectal cancer) in N1E-115 neuroblastoma cells. J. Biol. Chem. 277, 15207-15214 (Pubitemid 34952600)
67. Shekarabi, M., and Kennedy, T. E. (2002) The netrin-1 receptor DCC promotes filopodia formation and cell spreading by activating Cdc42 and Rac1. Mol. Cell Neurosci. 19, 1-17 (Pubitemid 34113693)
68. 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
69. Briançon-Marjollet, A., Ghogha, A., Nawabi, H., Triki, I., Auziol, C., Fromont, S., Piché, C., Enslen, H., Chebli, K., Cloutier, J. F., Castellani, V., Debant, A., and Lamarche-Vane, N. (2008) Trio mediates netrin-1-induced Rac1 activation in axon outgrowth and guidance. Mol. Cell. Biol. 28, 2314-2323 (Pubitemid 351429977)
70. Forsthoefel, D. J., Liebl, E. C., Kolodziej, P. A., and Seeger, M. A. (2005) The Abelson tyrosine kinase, the Trio GEF and Enabled interact with the Netrin receptor Frazzled in Drosophila. Development 132, 1983-1994 (Pubitemid 40691786)
71. Watari-Goshima, N., Ogura, K., Wolf, F. W., Goshima, Y., and Garriga, G. (2007) C. elegans VAB-8 and UNC-73 regulate the SAX-3 receptor to direct cell and growth-cone migrations. Nat. Neurosci. 10, 169-176 (Pubitemid 46174841)
72. Moore, S. W., Correia, J. P., Lai Wing Sun, K., Pool, M., Fournier, A. E., and Kennedy, T. E. (2008) Rho inhibition recruitsDCCto the neuronal plasma membrane and enhances axon chemoattraction to netrin 1. Development 135, 2855-2864
73. Bagrodia, S., and Cerione, R. A. (1999) Pak to the future. Trends Cell Biol. 9, 350-355 (Pubitemid 29447715)