The kakapo mutation affects terminal arborization and central dendritic sprouting of Drosophila motorneurons

Journal of Cell Biology

Volumn 143, Issue 5, 1998, Pages 1283-1294

  Prokop, Andreas ^a,b   Uhler, Jay ^a   Roote, John ^a   Bate, Michael ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b JOHANNES GUTENBERG UNIVERSITY   (Germany)

Author keywords

Cytoskeleton; Dendrites; Drosophila; Microtubules; Neuromuscular junction

Indexed keywords

CYTOSKELETON PROTEIN; KAKAPO; MEMBRANE PROTEIN; MICROTUBULE ASSOCIATED PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL SIZE; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; CUTICLE; DENDRITE; DROSOPHILA; ECTODERM; EMBRYO; EPIDERMIS CELL; GENE MUTATION; MICROTUBULE; MOTONEURON; NERVE CELL GROWTH; NEUROMUSCULAR SYNAPSE; NONHUMAN; POLYTENE CHROMOSOME; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SENSORY NERVE;

ALLELES; ANIMALS; CYTOSKELETAL PROTEINS; CYTOSKELETON; DENDRITES; DROSOPHILA; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, INSECT; INSECT PROTEINS; MEMBRANE PROTEINS; MICROSCOPY, ELECTRON; MICROTUBULES; MOTOR NEURONS; MUTATION; NERVE TISSUE PROTEINS; NEUROMUSCULAR JUNCTION; SYNAPSES;

ANIMALIA; HEXAPODA; STRIGOPS HABROPTILUS;

EID: 0032583166     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.143.5.1283     Document Type: Article

References (56)

1. Angau-Petit, D., P. Toth, O. Rogero, L. Faille, F.J. Tejedor, and A. Ferrús. 1998. Enhanced neurotransmitter release is associated with reduction of neuronal branching in a Drosophila mutant overexpressing frequenin. Eur. J. Neurosci. 10:423-434.
2. Arcaro, K.F., and G.A. Lnenicka. 1995. Intrinsic differences in axonal growth from crayfish fast and slow motorneurons. Dev. Biol. 168:272-283.
3. Ashburner, M., J. Faithfull, T. Littlewood, G. Richards, S. Smith, V. Velissariou, and R.C. Woodruff. 1980. Report of new mutants - Drosophila melanogaster. Dros. Info. Service. 55:193-195.
4. Avila, J., J. Domínguez, and J. Díaz-Nido. 1994. Regulation of microtubule dynamics by microtubule-associated protein expression and phosphorylation during neuronal development. Int. J. Dev. Biol. 38:13-25.
5. Bate, M. 1993. The mesoderm and its derivatives. In The Development of Drosophila melanogaster. M. Bate and A. Martínez Arias, editors. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY. 1013-1090.
6. Bate, M., and K. Broadie. 1995. Wiring by fly: the neuromuscular system of the Drosophila embryo. Neuron. 15:513-525.
7. Bentley, D., and T.P. O'Connor. 1994. Cytoskeletal events in growth cone steering. Curr. Opin. Neurobiol. 4:43-48.
8. Bodmer, R., and Y.N. Jan. 1987. Morphological differentiation of the embryonic peripheral neurons in Drosophila. Roux's Arch. Dev. Biol. 196:69-77.
9. Broadie, K., A. Prokop, H.J. Bellen, C.J. O'Kane, K.L. Schulze, and S.T. Sweeney. 1995. Syntaxin or synaptobrevin function downstream of vesicle docking in Drosophila. Neuron. 15:663-673.
10. Broadie, K.S., and M. Bate. 1993. Development of the embryonic neuromuscular synapse of Drosophila melanogaster. J. Neurosci. 13:144-166.
11. Buttgereit, D., D. Leiss, F. Michiels, and R. Renkawitz-Pohl. 1991. During Drosophila embryogenesis the β1 tubulin gene is specifically expressed in the nervous system and the apodemes. Mech. Dev. 33:107-118.
12. Caceres, A., J. Mautino, and K.S. Kosik. 1992. Suppression of MAP2 in cultured cerebellar macroneurons inhibits minor neurite formation. Neuron. 9:607-618.
13. Caceres, A., S. Potrebic, and K.S. Kosik. 1991. The effect of tau antisense oligonucleotides on neurite formation of cultured cerebellar macroneurons. J. Neurosci. 11:1515-1523.
14. Canal, I., A. Acebes, and A. Ferrús. 1998. Single neuron mosaics of the Drosophila gigas mutant project beyond normal targets and modify behaviour. J. Neurosci. 18:999-1008.
15. Carlson, S.D., S.L. Hilgers, and J.L. Juang. 1997. Ultrastructure and bloodnerve barrier of chordotonal organs in the Drosophila embryo. J. Neurocytol. 26:377-388.
16. Caroni, P. 1997. Intrinsic neuronal determinants that promote axonal sprouting and elongation. Bioessays. 19:767-775.
17. Cartaud, A., M.A. Ludosky, F.S. Tomé, H. Collin, F. Stetzkowski-Marden, T.S. Khurana, L.M. Kunkel, M. Fardeau, J.P. Changeux, and J. Cartaud. 1992. Localisation of dystrophin and dystrophin-related protein at the electromotor synapse and neuromuscular junction in Torpedo marmorata. Neuroscience. 48:995-1003.
18. Challacombe, J.F.S., D.M. Snow, and P.C. Letourneau. 1996. Actin filament bundles are required for microtubule reorientation during growth cone turning to avoid an inhibitory guidance cue. J. Cell Sci. 109:2031-2040.
19. Challacombe, J.F., D.M. Snow, and P.C. Letourneau. 1997. Dynamic microtubule ends are required for growth cone turning to avoid an inhibitory guidance cue. J. Neurosci. 17:3085-3095.
20. Dinsmore, J., and F. Solomon. 1991. Inhibition of MAP-2 expression affects both morphological and cell division phenotypes of neuronal differentiation. Neuron. 9:607-618.
21. Eberl, D.F., A.J. Hilliker, C.B. Sharp, and S.N. Trusis-Coulter. 1989. Further observations on the nature of radiation-induced chromosomal interchanges recovered from Drosophila sperm. Genome. 32:847-855.
22. Fuchs, E., and D.W. Cleveland. 1998. A structural scaffolding of intermediate filaments in health and disease. Science. 279:514-519.
23. Fujita, S.C., S.L. Zipursky, S. Benzer, A. Ferrús, and S.L. Shotwell. 1982. Monoclonal antibodies against the Drosophila nervous system. Proc. Natl. Acad. Sci. USA. 79:7929-7933.
24. González-Gaitán, M., and H. Jäckle. 1997. Role of Drosophila α-adaptin in presynaptic vesicle recycling. Cell. 88:767-776.
25. Goodman, C.S., and C.Q. Doe. 1993. Embryonic development of the Drosophila central nervous system. In The Development of Drosophila melanogaster. M. Bate and A. Martínez Arias, editors. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY. 1131-1206.
26. Gregory, S.L., and N.H. Brown. 1998. kakapo, a gene required for adhesion between cell layers in Drosophila, encodes a large cytoskeletal linker protein related to plectin and dystrophin. J. Cell Biol. 143:1271-1282.
27. Grenningloh, G., E.J. Rehm, and C.S. Goodman. 1991. Genetic analysis of growth cone guidance in Drosophila: fasciclin II functions as a neuronal recognition molecule. Cell. 67:45-57.
28. Guo, L., L. Degenstein, J. Dowling, Q.-C. Yu, R. Wollmann, B. Perman and E. Fuchs. 1995. Gene targeting of BPAG1: abnormalities in mechanical strength and cell migration in stratified squamous epithelia and severe neurologic degeneration. Cell. 81:233-243.
29. Halpern, M.E., A. Chiba, J. Johansen, and H. Keshishian, H. 1991. Growth cone behaviour underlying the development of Stereotypic synaptic connections in Drosophila embryos. J. Neurosci. 11:3227-3238.
30. Hartenstein, V. 1988. Development of Drosophila larval sensory organs: spatiotemporal pattern of sensory neurons, peripheral axonal pathways and sensilla differentiation. Development (Camb.). 102:869-886.
31. Kopczynski, C.C., D.W. Davis, and C.S. Goodman. 1996. A neural tetraspanin, encoded by late bloomer, that facilitates synapse formation. Science. 271: 1876-1870.
32. Landgraf, M., T. Bossing, G.M. Technau, and M. Bate. 1997. The origin, location, and projection of the embryonic abdominal motorneurons of Drosophila. J. Neurosci. 17:9642-9655.
33. Landmesser, L., L. Dahm, J. Tang, and U. Rutishauser. 1990. Polysialic acid as a regulator of intramuscular nerve branching during embryonic development. Neuron. 4:655-667.
34. Lin, D.M., R.D. Fetter, C. Kopczynski, G. Grenningloh, and C.S. Goodman. 1994. Genetic analysis of fasciclin II in Drosophila: defasciculation, refasciculation, and altered fasciculation. Neuron. 13:1055-1069.
35. Littleton, J.T., H.J. Bellen, and M.S. Perin. 1993. Expression of synaptotagmin in Drosophila reveals transport and localization of synaptic vesicles in the synapse. Development (Camb.). 118:1077-1088.
36. Murphey, R.K., and C.A. Lemere. 1984. Competition controls the growth of an identified axonal arborization. Science. 224:1352-1355.
37. Nobes, C.D., and A. Hall. 1995. Rho, Rac, Cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia. Cell. 81:53-62.
38. Preston, C.R., J.A. Sved, and W.R. Engels. 1996. Flanking duplications and deletions associated with P-induced male recombination in Drosophila. Genetics. 144:1623-1638.
39. Prokop, A., M. Landgraf, E. Rushton, K. Broadie, and M. Bate. 1996. Presynaptic development at the Drosophila neuromuscular junction: the assembly and localisation of presynaptic active zones. Neuron. 17:617-626.
40. Prokop, A., M.D. Martín-Bermudo, M. Bate, and N. Brown. 1998. Absence of PS integrins or laminin A affects extracellular adhesion, but not intracellular assembly, of hemiadherens and neuromuscular junctions in Drosophila embryos. Dev. Biol. 196:58-76.
41. Prokop, A., and G.M. Technau. 1993. Cell transplantation. In Cellular Interactions in Development: A Practical Approach. D. Hartley, editor. Oxford University Press, London, UK. 33-57.
42. Prout, M., Z. Damania, J. Soong, D. Fristrom, and J.W. Fristrom. 1997. Autosomal mutations affecting adhesion between wing surfaces in Drosophila melanogaster. Genetics. 146:275-285.
43. Reddy, S., P. Jin, J. Trimarchi, P. Caruccio, R. Phillis, and R.K. Murphey. 1997. Mutant molecular motors disrupt neural circuits in Drosophila. J. Neurobiol. 33:711-723.
44. Ruegg, M.A., and J.L. Bixby. 1998. Agrin orchestrates synaptic differentiation at the vertebrate neuromuscular junction. Trends Neurosci. 21:22-27.
45. Sink, H., and P.M. Whitington. 1991. Pathfinding in the central nervous system and periphery by identified embryonic Drosophila motor axons. Development (Camb.). 112:307-316.
46. Smith, C.L. 1994. Cytoskeletal movements and substrate interactions during initiation of neurite outgrowth by sympathetic neurons in vitro. J. Neurosci. 14:384-398.
47. Speicher, S., L. Garcia-Alonso, A. Carmena, M.D. Martín-Bermudo, S. de la Escalera, and F. Jiménez. 1998. Neurotactin functions in concert with other identified CAMs in growth cone guidance in Drosophila. Neuron. 20:221-233.
48. Strumpf, D., and T. Volk. 1998. Kakapo, a novel Drosophila protein, is essential for the restricted localization of the neuregulin-like factor, Vein, at the muscle-tendon junctional site. J. Cell Biol. 143:1259-1270.
49. Suter, D.M., and P. Forscher. 1998. An emerging link between cytoskeletal dynamics and cell adhesion molecules in growth cone guidance. Curr. Opin. Neurobiol. 8:106-116.
50. Tepass, U., and V. Hartenstein. 1994. The development of cellular junctions in the Drosophila embryo. Dev. Biol. 161:563-596.
51. Tessier-Lavignc, M., and C.S. Goodman. 1996. The molecular biology of axon guidance. Science. 274:1123-1133.
52. Thomas, J.B., M.J. Bastiani, M. Bate, and C.S. Goodman. 1984. From grasshopper to Drosophila: a common plan for neural development. Nature. 310:203-206.
53. Thompson, C., C.-H. Lin, and P. Forscher. 1996. An Aplysia cell adhesion molecule associated with site-directed actin filament assembly in neuronal growth cones. J. Cell Sci. 109:2843-2854.
54. Van Vactor, D., H. Sink, D. Fambrough, R. Tsoo, and C.S. Goodman. 1993. Genes that control neuromuscular specificity in Drosophila. Cell. 73:1137-1153.
55. Yoshihara, M., M.B. Rheuben, and Y. Kidokoro. 1997. Transition from growth cone to functional motor nerve terminal in Drosophila embryo. J. Neurosci. 17:8408-8426.
56. Zinsmaier, K.E., K.K. Eberle, E. Buchner, N. Walter, and S. Benzer. 1994. Paralysis and early death in cysteine string protein mutants of Drosophila. Science. 263:977-980.