The Drosophila Wnt5 protein mediates selective axon fasciculation in the embryonic central nervous system

Developmental Biology

Volumn 272, Issue 2, 2004, Pages 362-375

  Fradkin, Lee G ^a   Van Schie, Martijn ^a   Wouda, Rene R ^a   De Jong, Anja ^a   Kamphorst, Jessica T ^a   Radjkoemar Bansraj, Monique ^a   Noordermeer, Jasprina N ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Axon fasciculation; CNS; Commissural axon tracts; Drosophila; Longitudinal axon tracts; Wnt genes

Indexed keywords

GLYCOPROTEIN; UNCLASSIFIED DRUG; WNT 5 PROTEIN; WNT PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; DROSOPHILA; EMBRYO; FASCICULATION; NERVE FIBER; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION;

EID: 3342926026     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ydbio.2004.04.034     Document Type: Article

References (79)

1. Albagli O., Klaes A., Ferreira E., Leprince D., Klambt C. Function of ets genes is conserved between vertebrates and Drosophila. Mech. Dev. 59:1996;29-40
2. Araujo S.J., Tear G. Axon guidance mechanisms and molecules: lessons from invertebrates. Nat. Rev. Neurosci. 4:2003;910-922
3. Baker J.C., Beddington R.S., Harland R.M. Wnt signaling in Xenopus embryos inhibits bmp4 expression and activates neural development. Genes Dev. 13:1999;3149-3159
4. Bate C.M. Pioneer neurones in an insect embryo. Nature. 260:1976;54-56
5. Battye R., Stevens A., Jacobs J.R. Axon repulsion from the midline of the Drosophila CNS requires slit function. Development. 126:1999;2475-2481
6. Bellen H.J., Levis R.W., Liao G., He Y., Carlson J.W., Tsang G., Evans-Holm M., Hiesinger P.R., Schulze K.L., Rubin G.M., Hoskins R.A., Spradling A.C. The BDGP gene disruption project: single transposon insertions associated with 40% of Drosophila genes. Genetics. 2004;. (in press)
7. Benveniste R.J., Thor S., Thomas J.B., Taghert P.H. Cell type-specific regulation of the Drosophila FMRF-NH2 neuropeptide gene by Apterous, a LIM homeodomain transcription factor. Development. 125:1998;4757-4765
8. Bhat K.M. Frizzled and frizzled 2 play a partially redundant role in wingless signaling and have similar requirements to wingless in neurogenesis. Cell. 95:1998;1027-1036
9. Bonkowsky J.L., Yoshikawa S., O'Keefe D.D., Scully A.L., Thomas J.B. Axon routing across the midline controlled by the Drosophila Derailed receptor. Nature. 402:1999;540-544
10. Bopp D., Bell L.R., Cline T.W., Schedl P. Developmental distribution of female-specific sex-lethal proteins in Drosophila melanogaster. Genes Dev. 5:1991;403-415
11. Brand A.H., Perrimon N. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development. 118:1993;401-415
12. Budnik V., Koh Y.H., Guan B., Hartmann B., Hough C., Woods D., Gorczyca M. Regulation of synapse structure and function by the Drosophila tumor suppressor gene dlg. Neuron. 17:1996;627-640
13. Cadigan K.M., Nusse R. Wnt signaling: a common theme in animal development. Genes Dev. 11:1997;3286-3305
14. Callahan C.A., Muralidhar M.G., Lundgren S.E., Scully A.L., Thomas J.B. Control of neuronal pathway selection by a Drosophila receptor protein-tyrosine kinase family member. Nature. 376:1995;171-174
15. Castelo-Branco G., Wagner J., Rodriguez F.J., Kele J., Sousa K., Rawal N., Pasolli H.A., Fuchs E., Kitajewski J., Arenas E. Differential regulation of midbrain dopaminergic neuron development by Wnt-1, Wnt-3a, and Wnt-5a. Proc. Natl. Acad. Sci. U. S. A. 100:2003;12747-12752
16. Chenn A., Walsh C.A. Regulation of cerebral cortical size by control of cell cycle exit in neural precursors. Science. 297:2002;365-369
17. Chu-LaGraff Q., Doe C.Q. Neuroblast specification and formation regulated by wingless in the Drosophila CNS. Science. 261:1993;1594-1597
18. Deshpande N., Dittrich R., Technau G.M., Urban J. Successive specification of Drosophila neuroblasts NB 6-4 and NB 7-3 depends on interaction of the segment polarity genes wingless, gooseberry and naked cuticle. Development. 128:2001;3253-3261
19. Dickson B.J. Molecular mechanisms of axon guidance. Science. 298:2002;1959-1964
20. Dittrich R., Bossing T., Gould A.P., Technau G.M., Urban J. The differentiation of the serotonergic neurons in the Drosophila ventral nerve cord depends on the combined function of the zinc finger proteins Eagle and Huckebein. Development. 124:1997;2515-2525
21. Dorsky R.I., Moon R.T., Raible D.W. Control of neural crest cell fate by the Wnt signalling pathway. Nature. 396:1998;370-373
22. Eberl D.F., Perkins L.A., Engelstein M., Hilliker A.J., Perrimon N. Genetic and developmental analysis of polytene section 17 of the X chromosome of Drosophila melanogaster. Genetics. 130:1992;569-583
23. Engels W.R., Preston C.R. Formation of chromosome rearrangements by P factors in Drosophila. Genetics. 107:1984;657-678
24. Evan G.I., Lewis G.K., Ramsay G., Bishop J.M. Isolation of monoclonal antibodies specific for human c-myc proto-oncogene product. Mol. Cell. Biol. 5:1985;3610-3616
25. Fambrough D., Goodman C.S. The Drosophila beaten path gene encodes a novel secreted protein that regulates defasciculation at motor axon choice points. Cell. 87:1996;1049-1058
26. Fradkin L.G., Noordermeer J.N., Nusse R. The Drosophila Wnt protein DWnt-3 is a secreted glycoprotein localized on the axon tracts of the embryonic CNS. Dev. Biol. 168:1995;202-213
27. Garcia-Castro M.I., Marcelle C., Bronner-Fraser M. Ectodermal Wnt function as a neural crest inducer. Science. 297:2002;848-851
28. Golembo M., Raz E., Shilo B.Z. The Drosophila embryonic midline is the site of Spitz processing, and induces activation of the EGF receptor in the ventral ectoderm. Development. 122:1996;3363-3370
29. Goodman C.S., Doe C.Q. Embryonic development of the Drosophila central nervous system. Bate C.M., Martinez Arias A. The Development of Drosophila melanogaster. 1993;1131-1206 Cold Spring Harbor Press
30. Hall A.C., Lucas F.R., Salinas P.C. Axonal remodeling and synaptic differentiation in the cerebellum is regulated by WNT-7a signaling. Cell. 100:2000;525-535
31. Harris R., Sabatelli L.M., Seeger M.A. Guidance cues at the Drosophila CNS midline: identification and characterization of two Drosophila Netrin/UNC-6 homologs. Neuron. 17:1996;217-228
32. Hidalgo A. Neuron-glia interactions during axon guidance in Drosophila. Biochem. Soc. Trans. 31:2003;50-55
33. Hidalgo A., Brand A.H. Targeted neuronal ablation: the role of pioneer neurons in guidance and fasciculation in the CNS of Drosophila. Development. 124:1997;3253-3262
34. Jacobs J.R. The midline glia of Drosophila: a molecular genetic model for the developmental functions of glia. Prog. Neurobiol. 62:2000;475-508
35. Kadowaki T., Wilder E., Klingensmith J., Zachary K., Perrimon N. The segment polarity gene porcupine encodes a putative multitransmembrane protein involved in Wingless processing. Genes Dev. 10:1996;3116-3128
36. Keleman K., Dickson B.J. Short- and long-range repulsion by the Drosophila Unc5 netrin receptor. Neuron. 32:2001;605-617
37. Kidd T., Brose K., Mitchell K.J., Fetter R.D., Tessier-Lavigne M., Goodman C.S., Tear G. Roundabout controls axon crossing of the CNS midline and defines a novel subfamily of evolutionarily conserved guidance receptors. Cell. 92:1998;205-215
38. Kidd T., Bland K.S., Goodman C.S. Slit is the midline repellent for the robo receptor in Drosophila. Cell. 96:1999;785-794
39. Klambt C., Jacobs J.R., Goodman C.S. The midline of the Drosophila central nervous system: a model for the genetic analysis of cell fate, cell migration, and growth cone guidance. Cell. 64:1991;801-815
40. Klambt C., Hummel T., Menne T., Sadlowski E., Scholz H., Stollewerk A. Development and function of embryonic central nervous system glial cells in Drosophila. Dev. Genet. 18:1996;40-49
41. Knirr S., Azpiazu N., Frasch M. The role of the NK-homeobox gene slouch (S59) in somatic muscle patterning. Development. 126:1999;4525-4535
42. Krylova O., Herreros J., Cleverley K.E., Ehler E., Henriquez J.P., Hughes S.M., Salinas P.C. WNT-3, expressed by motoneurons, regulates terminal arborization of neurotrophin-3-responsive spinal sensory neurons. Neuron. 35:2002;1043-1056
43. Lin D.M., Fetter R.D., Kopczynski C., Grenningloh G., Goodman C.S. Genetic analysis of Fasciclin II in Drosophila: defasciculation, refasciculation, and altered fasciculation. Neuron. 13:1994;1055-1069
44. Lucas F.R., Salinas P.C. WNT-7a induces axonal remodeling and increases synapsin I levels in cerebellar neurons. Dev. Biol. 192:1997;31-44
45. Lundgren S.E., Callahan C.A., Thor S., Thomas J.B. Control of neuronal pathway selection by the Drosophila LIM homeodomain gene apterous. Development. 121:1995;1769-1773
46. 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. 8:1994;1787-1802
47. Manoukian A.S., Yoffe K.B., Wilder E.L., Perrimon N. The porcupine gene is required for wingless autoregulation in Drosophila. Development. 121:1995;4037-4044
48. Megason S.G., McMahon A.P. A mitogen gradient of dorsal midline Wnts organizes growth in the CNS. Development. 129:2002;2087-2098
49. Mitchell K.J., Doyle J.L., Serafini T., Kennedy T.E., Tessier-Lavigne M., Goodman C.S., Dickson B.J. Genetic analysis of Netrin genes in Drosophila: Netrins guide CNS commissural axons and peripheral motor axons. Neuron. 17:1996;203-215
50. Mueller B.K. Growth cone guidance: first steps towards a deeper understanding. Annu. Rev. Neurosci. 22:1999;351-388
51. Muroyama Y., Fujihara M., Ikeya M., Kondoh H., Takada S. Wnt signaling plays an essential role in neuronal specification of the dorsal spinal cord. Genes Dev. 16:2002;548-553
52. Nagaso H., Murata T., Day N., Yokoyama K.K. Simultaneous detection of RNA and protein by in situ hybridization and immunological staining. J. Histochem. Cytochem. 49:2001;1177-1182
53. Noordermeer J., Klingensmith J., Perrimon N., Nusse R. Dishevelled and armadillo act in the wingless signalling pathway in Drosophila. Nature. 367:1994;80-83
54. Noordermeer J.N., Kopczynski C.C., Fetter R.D., Bland K.S., Chen W.Y., Goodman C.S. 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. 21:1998;991-1001
55. Nose A., Umeda T., Takeichi M. Neuromuscular target recognition by a homophilic interaction of connectin cell adhesion molecules in Drosophila. Development. 124:1997;1433-1441
56. Packard M., Koo E.S., Gorczyca M., Sharpe J., Cumberledge S., Budnik V. The Drosophila Wnt, wingless, provides an essential signal for pre- and postsynaptic differentiation. Cell. 111:2002;319-330
57. Patapoutian A., Reichardt L.F. Roles of Wnt proteins in neural development and maintenance. Curr. Opin. Neurobiol. 10:2000;392-399
58. Patel N.H. Imaging neuronal subsets and other cell types in whole-mount Drosophila embryos and larvae using antibody probes. Methods Cell Biol. 44:1994;445-487
59. Pipes G.C., Lin Q., Riley S.E., Goodman C.S. The Beat generation: a multigene family encoding IgSF proteins related to the Beat axon guidance molecule in Drosophila. Development. 128:2001;4545-4552
60. Rajagopalan S., Nicolas E., Vivancos V., Berger J., Dickson B.J. Crossing the midline: roles and regulation of Robo receptors. Neuron. 28:2000;767-777
61. 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. 103:2000;1033-1045
62. Rincon-Limas D.E., Lu C.H., Canal I., Calleja M., Rodriguez-Esteban C., Izpisua-Belmonte J.C., Botas J. Conservation of the expression and function of apterous orthologs in Drosophila and mammals. Proc. Natl. Acad. Sci. U. S. A. 96:1999;2165-2170
63. Scholz H., Sadlowski E., Klaes A., Klambt C. Control of midline glia development in the embryonic Drosophila CNS. Mech. Dev. 62:1997;79-91
64. Shiga Y., Tanaka-Matakatsu M., Hayashi S. A nuclear GFP/beta- galactosidase fusion protein as a marker for morphogenesis in living Drosophila. Dev. Growth Differ. 38:1996;99-106
65. Siegfried E., Wilder E.L., Perrimon N. Components of wingless signalling in Drosophila. Nature. 367:1994;76-80
66. 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. 103:2000;1019-1032
67. 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. 28:2000;753-766
68. Speicher S., Garcia-Alonso L., Carmena A., Martin-Bermudo M.D., de la Escalera S., Jimenez F. Neurotactin functions in concert with other identified CAMs in growth cone guidance in Drosophila. Neuron. 20:1998;221-233
69. Tanaka K., Kitagawa Y., Kadowaki T. Drosophila segment polarity gene product porcupine stimulates the posttranslational N-glycosylation of wingless in the endoplasmic reticulum. J. Biol. Chem. 277:2002;12816-12823
70. Tautz D., Pfeifle C. A non-radioactive in situ hybridization method for the localization of specific RNAs in Drosophila embryos reveals translational control of the segmentation gene hunchback. Chromosoma. 98:1989;81-85
71. Tessier-Lavigne M., Goodman C.S. The molecular biology of axon guidance. Science. 274:1996;1123-1133
72. Tower J., Karpen G.H., Craig N., Spradling A.C. Preferential transposition of Drosophila P elements to nearby chromosomal sites. Genetics. 133:1993;347-359
73. Vactor D.V., Sink H., Fambrough D., Tsoo R., Goodman C.S. Genes that control neuromuscular specificity in Drosophila. Cell. 73:1993;1137-1153
74. van den Heuvel M., Harryman-Samos C., Klingensmith J., Perrimon N., Nusse R. Mutations in the segment polarity genes wingless and porcupine impair secretion of the wingless protein. EMBO J. 12:1993;5293-5302
75. van Vactor D. Adhesion and signaling in axonal fasciculation. Curr. Opin. Neurobiol. 8:1998;80-86
76. Wieschaus E., Nusslein-Volhard C. Looking at embryos. Roberts Drosophila: A Practical Approach. 1986;IRL Press, Oxford, UK
77. Wilson S.I., Rydstrom A., Trimborn T., Willert K., Nusse R., Jessell T.M., Edlund T. The status of Wnt signalling regulates neural and epidermal fates in the chick embryo. Nature. 411:2001;325-330
78. Yoshikawa S., McKinnon R.D., Kokel M., Thomas J.B. Wnt-mediated axon guidance via the Drosophila Derailed receptor. Nature. 422:2003;583-588
79. Zipursky S.L., Venkatesh T.R., Teplow D.B., Benzer S. Neuronal development in the Drosophila retina: monoclonal antibodies as molecular probes. Cell. 36:1984;15-26