Calmodulin and Son of sevenless dependent signaling pathways regulate midline crossing of axons in the Drosophila CNS

Development

Volumn 127, Issue 9, 2000, Pages 1991-2000

  Fritz, Janice L ^a   Vanberkum, Mark F A ^a  

^a WAYNE STATE UNIVERSITY   (United States)

Author keywords

Axon guidance; Calmodulin; CNS; Drosophila; Repulsion; Sos

Indexed keywords

CALMODULIN; CELL SURFACE PROTEIN; PROTEIN; SON OF SEVENLESS PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; DEVELOPMENTAL GENETICS; DROSOPHILA; EMBRYO; GENE DISRUPTION; MUTANT; NERVE FIBER GROWTH; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ANIMALS; AXONS; CALMODULIN; CENTRAL NERVOUS SYSTEM; DROSOPHILA; DROSOPHILA PROTEINS; HISTOCYTOCHEMISTRY; MEMBRANE PROTEINS; MUTATION; NERVE TISSUE PROTEINS; RECEPTORS, IMMUNOLOGIC; SIGNAL TRANSDUCTION; SON OF SEVENLESS PROTEIN, DROSOPHILA;

ANIMALIA; HEXAPODA; INSECTA;

EID: 0034121556     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (65)

1. Archer, F. R., Doherty, P., Collins, D, and Bolsover, S. R. (1999). CAMs and FGF cause a local submembrane calcium signal promoting axon outgrowth without a rise in bulk calcium concentration. Eur. J. Neurosci. 11, 3565-3573.
2. Avery, L. and Wasserman, S. (1992). Ordering gene function: the interpretation of epistasis in regulatory hierarchies. Trends Genet. 8, 312-316.
3. Bandtlow, C. E. and Loschinger, J. (1997). Developmental changes in neuronal responsiveness to the CNS myelin-associated neurite growth inhibitor NI-35/250. Eur. J. Neurosci. 9, 2743-2752.
4. Bandtlow, C. E., Schmidt, M. K, Hassinger, T. D., Schwab, M. E. and Kater, S. B. (1993). Role of intracellular calcium in NI-35-evoked collapse of neuronal growth cones. Science 259, 80-83.
5. Bashaw, G. J. and Goodman, C. S. (1999). Chimeric axon guidance receptors: the cytoplasmic domains of slit and netrin receptors specify attraction versus repulsion. Cell 97, 917-926.
6. Bonfini, L., Karlovich, C. A., Dasgupta, C. and Banerjee, U. (1992). The Son of sevenless gene product: a putative activator of Ras. Science 255, 603-606.
7. Brose, K., Bland, K. S., Wang, K. H., Arnott, D., Henzel, W., Goodman, C. S., Tessier-Lavigne, M. and Kidd, T. (1999). Slit proteins hind Robo receptors and have an evolutionarily conserved role in repulsive axon guidance. Cell 96, 795-806.
8. Cook, G., Tannahill, D. and Keynes, R. (1998). Axon guidance to and from choice points. Curr. Opin. Neurobiol. 8, 64-72.
9. Culotti, J. G. and Merz, D. C. (1998). DCC and netrins. Curr. Opin. Cell Biol. 10, 609-613.
10. Desai, C. J., Garrity, P. A., Keshishian, H., Zipursky, S. L., and Zinn, K. (1999). The Drosophila SH2-SH3 adapter protein Dock is expressed in embryonic axons and facilitates synapse formation by the RP3 motoneuron. Development 126, 1527-1535.
11. Doherty, P. and Walsh, F. S. (1996). CAM-FGF receptor i[nteractions: A model for axonal growth. Mol. Cell Neurosci. 8, 99-111.
12. Elkins, T., Zinn, K., McAllister, L., Hoffmann, F. M. and Goodman, C. S. (1990). Genetic analysis of a Drosophila neural cell adhesion molecule: interaction of fasciclin I and Abelson tyrosine kinase mutations. Cell 60, 565-575.
13. Finkbeiner, S. and Greenberg, M. K. (1996). Ca(2+)-dependent routes to Ras: mechanisms for neuronal survival, differentiation, and plasticity? Neuron 16, 233-236.
14. Flanagan, J. G. and Van Vactor, D. (1986). Through the looking glass: axon guidance at the midline choice point. Cell 92, 429-432.
15. Gallo, G. and Letourneau, P. C. (1999). Axon guidance: A balance of signals sets axons on the right track. Curr. Biol. 9, R490-492.
16. Garrity, P. A., Rao, Y., Salecker, I., McGlade, J., Pawson, T. and Zipursky, S. L. (1996). Drosophila photoreceptor axon guidance and targeting requires the dreadlocks SH2/SH3 adapter protein. Cell 85, 639-650.
17. Gertler, F. B., Comer, A. R., Juang, J. L., Ahern, S. M., Clark, M. J., Liebl, E. C. and Hoffmann, F. M. (1995). enabled, a dosage-sensitive suppressor of mutations in the Drosophila Ab1 tyrosine kinase, encodes an Ab1 substrate with SH3 domain-binding properties. Genes Dev. 9, 521-533.
18. Goldberg, D. J. and Grabham, P. W. (1999). Braking news: calcium in the growth cone. Neuron 22, 423-425.
19. Gomez, T. M. and Spitzer, N. C. (1999). In vivo regulation of axon extension and pathtinding by growth-cone calcium transients. Nature 397, 350-355.
20. Harris, R., Sabatelli, L. M. and Seeger, M. A. (1996). Guidance cues at the Drosophila CNS midline: identification and characterization of two Drosophila Netrin/UNC-6 homologs. Neuron 17, 217-228.
21. Heiman, R. G., Atkinson, R. C., Andruss, B. F., Bolduc, C., Kovalick, G. E. and Beckingham, K. (1996). Spontaneous avoidance behavior in Drosophila null for calmodulin expression. Proc. Natl. Acad. Sci. USA 93, 2420-2425.
22. Hidalgo, A. and Brand, A. H. (1997). Targeted neuronal ablation: the role of pioneer neurons in guidance and fasciculation in the CNS of Drosophila. Development 124, 3253-3262.
23. 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.
24. Hopker, V. H., Shewan, D., Tessier-Lavigne, M, Poo, M. and Holt, C. (1999). Growth-cone attraction to netrin-1 is converted to repulsion by laminin-1. Nature 401, 69-73.
25. Hu, S., Sonnenfeld, M., Stahl, S. and Crews, S. T. (1998). Midline Fasciclin: a Drosophila Fasciclin-1-related membrane protein localized to the CNS midline cells and trachea. J. Neurobiol. 35, 77-93.
26. Hummel, T., Schimmelpfeng, K. and Klambt, C. (1999). Commissure formation in the embryonic CNS of Drosophila. Development 126, 771-779.
27. Karlovich, C. A., Bonfini, L., McCollam, L., Rogge, R. D., Daga, A., Czech, M. P. and Banerjee, U. (1995). In vivo functional analysis of the Ras exchange factor son of sevenless. Science 268, 576-579.
28. Kaufmann, N., Wills, Z. P. and Van Vaclor, D. (1998). Drosophila Rac1 controls motor axon guidance. Development 125, 453-461.
29. 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.
30. 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.
31. Kidd, T., Brose, K., Mitchell, K. J., Fetter, R. D., Tessier-Lavigne, M., Goodman, C. S. and Tear, G. (1998a). Roundabout controls axon crossing of the CNS midline and defines a novel subfamily of evolutionary conserved guidance receptors. Cell 92, 205-215.
32. Kidd, T., Russell, C., Goodman, C. S. and Tear, G. (1998b) Dosage-sensitive and complementary functions of roundabout and commissureless control axon crossing of the CNS midline. Neuron 20, 25-33.
33. Kovalick, G. E. and Beckingham, K. (1992). Calmodulin transcription is limited to the nervous system during Drosophila embryogenesis. Dev. Biol. 150, 33-46.
34. Lev, S., Moreno, H., Martinez, R., Canoll, P., Peles, E., Musacchio, J. M., Plowman, G. D., Rudy, B. and Schlessinger, J. (1995). Protein tyrosine kinase PYK2 involved in Ca(2+)-induced regulation of ion channel and MAP kinase functions. Nature 376, 737-745.
35. Li, H. S., Chen, J. H., Wu, W., Fagaly, T., Zhou, L., Yuan, W., Dupuis, S., Jiang, Z. H., Nash, W., Gick, C. et al. (1999). Vertebrate slit, a secreted ligand for the transmembrane protein roundabout, is a repellent for olfactory-bulb axons. Cell 96, 807-818.
36. Lin, C. H., Espreafico, E. M., Mooseker, M. S. and Forscher, P. (1996). Myosin drives retrograde F-actin flow in neuronal growth cones. Neuron 16, 769-782.
37. Lin, D. M., Fetter, R. D., Kopczynski, C., Grenningloh, G. and Goodman, C. S. (1994). Genetic analysis of Fasciclin II in Drosophila: defasciculation, refasciculation, and altered fasciculation. Neuron 13, 1055-1069.
38. Loschinger, J., Bandtlow, C. E., Jung, J., Klostermann, S., Schwab, M. E., Bonhoeffer, F. and Kater, S. B. (1997). Retinal axon growth cone responses to different environmental cues are mediated by different second-messenger systems. J. Neurobiol. 33, 825-834.
39. Lu, X., Chou, T. B., Williams, N. G., Roberts, T. and Perrimon, N. (1993). Control of cell fate determination by p21ras/Ras1, an essential component of torso signaling in Drosophila. Genes Dev. 7, 621-632.
40. Luo, L., Liao, Y. J., Jan, L. Y. and Jan, Y. N. (1994). Distinct morphogenetic functions of similar small GTPases: Drosophila Drac 1 is involved in axonal outgrowth and myoblast fusion. Genes Dev. 8, 1787-1802.
41. Ming, G., Song, H., Berninger, B., Inagaki, N., Tessier-Lavigne, M. and Poo, M. (1999). Phospholipase C-gamma and phosphoinositide 3-kinase mediate cytoplasmic signaling in nerve growth cone guidance. Neuron 23, 139-148.
42. Ming, G. L., Song, H. J., Berninger, B., Holt, C. E., Tessier-Lavigne, M. and Poo, M. M. (1997). cAMP-dependent growth cone guidance by netrin-1. Neuron 19, 1225-1235.
43. 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.
44. Murray, M. J. and Whitington, P. M. (1999). Effects of roundabout on growth cone dynamics, filopodial length, and growth cone morphology at the midline and throughout the neuropile. J. Neurosci. 19, 7901-7912.
45. Nguyen Ba-Charvet, K. T., Brose, K., Marillat, V., Kidd, T., Goodman, C. S., Tessier-Lavigne, M., Sotelo, C. and Chedotal, A. (1999). Slit2-mediated chemorepulsion and collapse of developing forebrain axons. Neuron 22, 463-473.
46. Nimnual, A. S., Yatsula, B. A. and Bar-Sagi, D. (1998). Coupling of Ras and Rac guanosine triphosphatases through the Ras exchanger Sos. Science 279, 560-563.
47. Noordermeer, J. N., Kopczynski, C. C., Fetter, R. D., Bland, K. S., Chen, W. Y. and Goodman, C. S. (1998). Wrapper, a novel member of the Ig superfamily, is expressed by midline glia and is required for them to ensheath commissural axons in Drosophila. Neuron 21, 991-1001.
48. Raabe, T., Olivier, J. P., Dickson, B., Liu, X., Gish, G. D., Pawson, T. and Hafen, E. (1995). Biochemical and genetic analysis of the Drk SH2/SH3 adaptor protein of Drosophila. EMBO J. 14, 2509-2518.
49. Rusanescu, G., Qi, H., Thomas, S. M., Brugge, J. S. and Halegoua, S. (1995). Calcium influx induces neurite growth through a Src-Ras signaling cassette. Neuron 15, 1415-1425.
50. Seeger, M., Tear, G., Ferres-Marco, D. and Goodman, C. S. (1993). Mutations affecting growth cone guidance in Drosophila: genes necessary for guidance toward or away from the midline. Neuron 10, 409-426.
51. 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.
52. Song, H. J., Ming, G. L. and Poo, M. M. (1997). cAMP-induced switching in turning direction of nerve growth cones. Nature 388, 275-279.
53. Song, H. J. and Poo, M. M. (1999). Signal transduction underlying growth cone guidance by diffusible factors. Curr. Opin. Neurobiol. 9, 355-363.
54. Suter, D. M. and Forscher, P. (1998). An emerging link between cytoskeletal dynamics and cell adhesion molecules in growth cone guidance. Curr. Opin. Neurobiol. 8, 106-116.
55. Takei, K., Shin, R. M., Inoue, T., Kato, K. and Mikoshiba, K. (1998). Regulation of nerve growth mediated by inositol 1,4,5-trisphosphate receptors in growth cones. Science 282, 1705-1708.
56. Tear, G., Harris, R., Sutaria, S., Kilomanski, K., Goodman, C. S. and Seeger, M. A. (1996). commissureless controls growth cone guidance across the CNS midline in Drosophila and encodes a novel membrane protein. Neuron 16, 501-514.
57. Tessier-Lavigne, M. and Goodman, C. S. (1996). The molecular biology of axon guidance. Science 274, 1123-1133.
58. Thomas, J. B. (1998). Axon guidance: crossing the midline. Curr. Biol. 8, R102-104.
59. VanBerkum, M. F. and Goodman, C. S. (1995). Targeted disruption of Ca(2+)-calmodulin signaling in Drosophila growth cones leads to stalls in axon extension and errors in axon guidance. Neuron 14, 43-56.
60. Wang, K. H., Brose, K., Arnott, D., Kidd, T., Goodman, C. S., Henzel, W. and Tessier-Lavigne, M. (1999). Biochemical purification of a mammalian slit protein as a positive regulator of sensory axon elongation and branching. Cell 96, 771-784.
61. Wang, Q. and Zheng, J. Q. (1998). cAMP-mediated regulation of neurotrophin-induced collapse of nerve growth cones. J. Neurosci. 18, 4973-4984.
62. Welnhofer, E. A., Zhao, L. and Cohan, C. S. (1999). Calcium influx alters actin bundle dynamics and retrograde flow in Helisoma growth cones. J. Neurosci. 19, 7971-7982.
63. Wills, Z., Bateman, J., Korey, C. A., Comer, A. and Van Vactor, D. (1999). The tyrosine kinase AbI and its substrate enabled collaborate with the receptor phosphatase Dlar to control motor axon guidance. Neuron 22, 301-312.
64. Xia, Z. and Storm, D. R. (1997). Calmodulin-regulated adenylyl cyclases and neuromodulation. Curr. Opin. Neurobiol. 1, 391-396.
65. Zheng, J, Q., Poo, M. M. and Connor, J. A. (1996). Calcium and chemotropic turning of nerve growth cones. Perspect. Dev. Neurobiol. 4, 205-213.