Neurite extension in central neurons: A novel role for the receptor tyrosine kinases Ror1 and Ror2

Journal of Cell Science

Volumn 118, Issue 2, 2005, Pages 433-446

  Paganoni, Sabrina ^a   Ferreira, Adriana ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Antisense; Microtubule associated proteins; Neurite elongation and branching; Receptor tyrosine kinases; siRNA

Indexed keywords

ANTISENSE OLIGONUCLEOTIDE; MICROTUBULE ASSOCIATED PROTEIN 2; MICROTUBULE ASSOCIATED PROTEIN 5; PROTEIN TYROSINE KINASE; ROR1 PROTEIN; ROR2 PROTEIN; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; ASTROCYTE; BRAIN DEVELOPMENT; BRAIN NERVE CELL; CELL ELONGATION; CELL STRUCTURE; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; HIPPOCAMPUS; HUMAN; HUMAN CELL; MODULATION; NERVE CELL NETWORK; NERVE FIBER GROWTH; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RNA INTERFERENCE; UPREGULATION;

ANIMALS; ASTROCYTES; CELL LINE; CELL SURVIVAL; HUMANS; MICE; MICROTUBULE-ASSOCIATED PROTEINS; NEURITES; NEURONS; OLIGONUCLEOTIDES, ANTISENSE; PHENOTYPE; RECEPTOR PROTEIN-TYROSINE KINASES; RECEPTORS, CELL SURFACE; RNA INTERFERENCE; SIGNAL TRANSDUCTION;

EID: 14044263637     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.01622     Document Type: Article

References (69)

1. Aigner, L. and Caroni, P. (1995). Absence of persistent spreading, branching, and adhesion in GAP-43-depleted growth cones. J. Cell Biol. 128, 647-660.
2. Al-Shawi, R., Ashton, S. V., Underwood, C. and Simons, J. P. (2001). Expression of the Ror1 and Ror2 receptor tyrosine kinase genes during mouse development. Dev. Genes Evol. 211, 161-171.
3. Avila, J., Dominguez, J. and Diaz-Nido, J. (1994). Regulation of microtubule dynamics by microtubule-associated protein expression and phosphorylation during neuronal development. Int. J. Dev. Biol. 38, 13-25.
4. Black, M. M., Slaughter, T. and Fischer, I. (1994). Microtubule-associated protein 1b (MAP1b) is concentrated in the distal region of growing axons. J. Neurosci. 14, 857-870.
5. Bose, C. M., Qiu, D., Bergamaschi, A., Gravante, B., Bossi, M., Villa, A., Rupp, F. and Malgaroli, A. (2000). Agrin controls synaptic differentiation in hippocampal neurons. J. Neurosci. 20, 9086-9095.
6. Bottenstein, J. E. and Sato, G. H. (1979). Growth of a rat neuroblastoma cell line in serum-free supplemented medium. Proc. Natl. Acad. Sci. USA 76, 514-517.
7. Burden, S. J. (2000). Wnts as retrograde signals for axon and growth cone differentiation. Cell 100, 495-497.
8. Burgess, R. W., Skarnes, W. C. and Sanes, J. R. (2000). Agrin isoforms with distinct amino termini: differential expression, localization, and function. J. Cell Biol. 151, 41-52.
9. Caceres, A. and Kosik, K. S. (1990). Inhibition of neurite polarity by tau antisense oligonucleotides in primary cerebellar neurons. Nature 343, 461-463.
10. Caceres, A., Mautino, J. and Kosik, K. S. (1992). Suppression of MAP2 in cultured cerebellar macroneurons inhibits minor neurite formation. Neuron 9, 607-618.
11. Carman, C. V., Som, T., Kim, C. M. and Benovic, J. L. (1998). Binding and phosphorylation of tubulin by G protein-coupled receptor kinases. J. Biol. Chem. 273, 20308-20316.
12. Coffey, E. T., Akerman, K. E. and Courtney, M. J. (1997). Brain derived neurotrophic factor induces a rapid upregulation of synaptophysin and tau proteins via the neurotrophin receptor TrkB in rat cerebellar granule cells. Neurosci. Lett. 227, 177-180.
13. Cohen, N. A., Kaufmann, W. E., Worley, P. F. and Rupp, F. (1997). Expression of agrin in the developing and adult rat brain. Neuroscience 76, 581-596.
14. Craig, A. M. and Banker, G. A. (1994). Neuronal polarity. Annu. Rev. Neurosci. 17, 267-310.
15. Davies, A. M. (2000). Neurotrophins: neurotrophic modulation of neurite growth. Curr. Biol. 10, R198-R200.
16. Dickson, B. J. (2002). Molecular mechanisms of axon guidance. Science 298, 1959-1964.
17. Dotti, C. G., Sullivan, C. A. and Banker, G. A. (1988). The establishment of polarity by hippocampal neurons in culture. J. Neurosci. 8, 1454-1468.
18. Elbashir, S. M., Harborth, J., Lendeckel, W., Yalcin, A., Weber, K. and Tuschl, T. (2001a). Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature 411 494-498.
19. Elbashir, S. M., Martinez, J., Patkaniowska, A., Lendeckel, W. and Tuschl, T. (2001b). Functional anatomy of siRNAs for mediating efficient RNAi in Drosophila melanogaster embryo lysate. EMBO J. 20, 6877-6888.
20. Eto, M., Bock, R., Brautigan, D. L. and Linden, D. J. (2002). Cerebellar long-term synaptic depression requires PKC-mediated activation of CPI-17, a myosin/moesin phosphatase inhibitor. Neuron 36, 1145-1158.
21. Ferreira, A. (1999). Abnormal synapse formation in agrin-depleted hippocampal neurons. J. Cell Sci. 112, 4729-4738.
22. Ferreira, A., Busciglio, J. and Caceres, A. (1989). Microtubule formation and neurite growth in cerebellar macroneurons which develop in vitro: evidence for the involvement of the microtubule-associated proteins, MAP-1a, HMW-MAP2 and Tau. Brain Res. Dev. Brain Res. 49, 215-228.
23. Ferreira, A., Kosik, K. S., Greengard, P. and Han, H. Q. (1994). Aberrant neurites and synaptic vesicle protein deficiency in synapsin II-depleted neurons. Science 264, 977-979.
24. Ferreira, A., Kao, H. T., Feng, J., Rapoport, M. and Greengard, P. (2000). Synapsin III: developmental expression, subcellular localization, and role in axon formation. J. Neurosci. 20, 3736-3744.
25. Fink, C. C., Bayer, K. U., Myers, J. W., Ferrell, J. E., Jr, Schulman, H. and Meyer, T. (2003). Selective regulation of neurite extension and synapse formation by the beta but not the alpha isoform of CaMKII. Neuron 39, 283-297.
26. Forrester, W. C. (2002). The Ror receptor tyrosine kinase family. Cell Mol. Life Sci. 59, 83-96.
27. Forrester, W. C., Dell, M., Perens, E. and Garriga, G. (1999). A C. elegans Ror receptor tyrosine kinase regulates cell motility and asymmetric cell division. Nature 400, 881-885.
28. Fukumitsu, H., Ohashi, A., Nitta, A., Nomoto, H. and Furukawa, S. (1997). BDNF and NT-3 modulate expression and threonine phosphorylation of microtubule-associated protein 2 analogues, and alter their distribution in the developing rat cerebral cortex. Neurosci. Lett. 238, 107-110.
29. Gautam, M., Noakes, P. G., Moscoso, L., Rupp, E., Scheller, R. H., Merlie, J. P. and Sanes, J. R. (1996). Defective neuromuscular synaptogenesis in agrin-deficient mutant mice. Cell 85, 525-535.
30. Glass, D. J., Bowen, D. C., Stitt, T. N., Radziejewski, C., Bruno, J., Ryan, T. E., Gies, D. R., Shah, S., Mattsson, K., Burden, S. J. et al. (1996). Agrin acts via a MuSK receptor complex. Cell 85, 513-523.
31. Gonzalez-Billault, C., Engelke, M., Jimenez-Mateos, E. M., Wandosell, F., Caceres, A. and Avila, J. (2002). Participation of structural micrombule-associated proteins (MAPs) in the development of neuronal polarity. J. Neurosci. Res. 67, 713-719.
32. Goslin, K. and Banker, G. A. (1991). Rat hippocampal neurons in low-density culture. In: Culturing nerve cells (ed. G. A. Banker and K. Goslin), pp. 251-283. Cambridge, MA: The MIT Press.
33. Hall, A. C., Lucas, F. R. and Salinas, P. C. (2000). Axonal remodeling and synaptic differentiation in the cerebellum is regulated by WNT-7a signaling. Cell 100, 525-535.
34. Heldin, C. H. (1995). Dimerization of cell surface receptors in signal transduction. Cell 80, 213-223.
35. Higuchi, H., Yamashita, T., Yoshikawa, H. and Tohyama, M. (2003). Functional inhibition of the p75 receptor using a small interfering RNA. Biochem. Biophys. Res. Commun. 301, 804-809.
36. Hikasa, H., Shibata, M., Hiratani, I. and Taira, M. (2002). The Xenopus receptor tyrosine kinase Xror2 modulates morphogenetic movements of the axial mesoderm and neuroectoderm via Wnt signaling. Development 129, 5227-5239.
37. Holgado, A. and Ferreira, A. (2000). Synapse formation proceeds independently of dendritic elongation in cultured hippocampal neurons. J. Neurobiol. 43, 121-131.
38. Huang, E. J. and Reichardt, L. F. (2003). Trk receptors: roles in neuronal signal transduction. Annu. Rev. Biochem. 72, 609-642.
39. Ji, R. R., Bose, C. M., Lesuisse, C., Qiu, D., Huang, J. C., Zhang, Q. and Rupp, F. (1998). Specific agrin isoforms induce cAMP response element binding protein phosphorylation in hippocampal neurons. J. Neurosci. 18, 9695-9702.
40. Kadowaki, T., Fujita-Yamaguchi, Y., Nishida, E., Takaku, F., Akiyama, T., Kathuria, S., Akanuma, Y. and Kasuga, M. (1985). Phosphorylation of tubulin and microtubule-associated proteins by the purified insulin receptor kinase. J. Biol. Chem. 260, 4016-4020.
41. Klein, R. (2001). Excitatory Eph receptors and adhesive ephrin ligands. Curr. Opin. Cell Biol. 13, 196-203.
42. Koga, M., Take-uchi, M., Tameishi, T. and Ohshima, Y. (1999). Control of DAF-7 TGF-(alpha) expression and neuronal process development by a receptor tyrosine kinase KIN-8 in Caenorhabditis elegans. Development 126, 5387-5398.
43. Krichevsky, A. M. and Kosik, K. S. (2002). RNAi functions in cultured mammalian neurons. Proc. Natl. Acad. Sci. USA 99, 11926-11929.
44. Krylova, O., Herreros, J., Cleverley, K. E., Ehler, E., Henriquez, J. P., Hughes, S. M. and Salinas, P. C. (2002). WNT-3, expressed by motoneurons, regulates terminal arborization of neurotrophin-3-responsive spinal sensory neurons. Neuron 35, 1043-1056.
45. Labelle, C. and Leclerc, N. (2000). Exogenous BDNF, NT-3 and NT-4 differentially regulate neurite outgrowth in cultured hippocampal neurons. Brain Res. Dev. Brain Res. 123, 1-11.
46. Laemmli, U. K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227 680-685.
47. Mantych, K. B. and Ferreira, A. (2001). Agrin differentially regulates the rates of axonal and dendritic elongation in cultured hippocampal neurons. J. Neurosci. 21, 6802-6809.
48. Masiakowski, P. and Carroll, R. D. (1992). A novel family of cell surface receptors with tyrosine kinase-like domain. J. Biol. Chem. 267, 26181-26190.
49. McKay, S. E., Hislop, J., Scott, D., Bulloch, A. G., Kaczmarek, L. K., Carew, T. J. and Sossin, W. S. (2001). Aplysia ror forms clusters on the surface of identified neuroendocrine cells. Mol. Cell. Neurosci. 17, 821-841.
50. Mueller, B. K. (1999). Growth cone guidance: first steps towards a deeper understanding. Annu. Rev. Neurosci. 22 351-388.
51. Nishida, E., Hoshi, M., Miyata, Y., Sakai, H., Kadowaki, T., Kasuga, M., Saijo, S., Ogawara, H. and Akiyama, T. (1987). Tyrosine phosphorylation by the epidermal growth factor receptor kinase induces functional alterations in microtubule-associated protein 2. J. Biol. Chem. 262, 16200-16204.
52. Oishi, I., Sugiyama, S., Liu, Z. J., Yamamura, H., Nishida, Y. and Minami, Y. (1997). A novel Drosophila receptor tyrosine kinase expressed specifically in the nervous system. Unique structural features and implication in developmental signaling. J. Biol. Chem. 272, 11916-11923.
53. Oishi, I., Takeuchi, S., Hashimoto, R., Nagabukuro, A., Ueda, T., Liu, Z. J., Hatta, T., Akira, S., Matsuda, Y., Yamamura, H. et al. (1999). Spatiotemporally regulated expression of receptor tyrosine kinases, mRor1, mRor2, during mouse development: implications in development and function of the nervous system. Genes Cells 4 41-56.
54. Oishi, I., Suzuki, H., Onishi, N., Takada, R., Kani, S., Ohkawara, B., Koshida, I., Suzuki, K., Yamada, G., Schwabe, G. C. et al. (2003). The receptor tyrosine kinase Ror2 is involved in non-canonical Wnt5a/JNK signalling pathway. Genes Cells 8, 645-654.
55. Packard, M., Koo, E. S., Gorczyca, M., Sharpe, J., Cumberledge, S. and Budnik, V. (2002). The Drosopbila Wnt, wingless, provides an essential signal for pre- and postsynaptic differentiation. Cell 111, 319-330.
56. Paganoni, S. and Ferreira, A. (2003). Expression and subcellular localization of Ror tyrosine kinase receptors are developmentally regulated in cultured hippocampal neurons. J. Neurosci. Res. 73, 429-440.
57. Paganoni, S., Anderson, K. L. and Ferreira, A. (2004). Differential subcellular localization of Ror tyrosine kinase receptors in cultured astrocytes. Glia 46, 456-466.
58. Passafaro, M., Nakagawa, T., Sala, C. and Sheng, M. (2003). Induction of dendritic spines by an extracellular domain of AMPA receptor subunit GluR2. Nature 424, 677-681.
59. Patapoutian, A. and Reichardt, L. F. (2000). Roles of Wnt proteins in neural development and maintenance. Curr. Opin. Neurobiol. 10, 392-399.
60. San Jose, I., Vazquez, E., Garcia-Atares, N., Huerta, J. J., Vega, J. A. and Represa, J. (1997). Differential expression of microtubule associated protein MAP-2 in developing cochleovestibular neurons and its modulation by neurotrophin-3. Int. J. Dev. Biol. 41, 509-519.
61. Sanes, J. R. and Lichtman, J. W. (2001). Induction, assembly, maturation and maintenance of a postsynaptic apparatus. Nat. Rev. Neurosci. 2, 791-805.
62. Schlessinger, J. (2000). Cell signaling by receptor tyrosine kinases. Cell 103, 211-225.
63. Skaper, S. D., Moore, S. E. and Walsh, F. S. (2001). Cell signalling cascades regulating neuronal growth-promoting and inhibitory cues. Prog. Neurobiol. 65, 593-608.
64. Tanaka, E. and Sabry, J. (1995). Making the connection: cytoskeletal rearrangements during growth cone guidance. Cell 83 171-176.
65. Tao, H. W. and Poo, M. (2001). Retrograde signaling at central synapses. Proc. Natl. Acad. Sci. USA 98, 11009-11015.
66. Towbin, H., Staehelin, T. and Gordon, J. (1979). Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. USA 76, 4350-4354.
67. Valenzuela, D. M., Stitt, T. N., DiStefano, P. S., Rojas, E., Mattsson, K., Compton, D. L., Nunez, L., Park, J. S., Stark, J. L., Gies, D. R. et al. (1995). Receptor tyrosine kinase specific for the skeletal muscle lineage: expression in embryonic muscle, at the neuromuscular junction, and after injury. Neuron 15, 573-584.
68. Wilson, C., Goberdhan, D. C. and Steller, H. (1993). Dror, a potential neurotrophic receptor gene, encodes a Drosophila homolog of the vertebrate Ror family of Trk-related receptor tyrosine kinases. Proc. Natl. Acad. Sci. USA 90, 7109-7113.
69. Yoda, A., Oishi, I. and Minami, Y. (2003). Expression and function of the Ror-family receptor tyrosine kinases during development: lessons from genetic analyses of nematodes, mice, and humans. J. Recept. Signal. Transduct. Res. 23, 1-15.