Zebrafish unplugged reveals a role for muscle-specific kinase homologs in axonal pathway choice

Nature Neuroscience

Volumn 7, Issue 12, 2004, Pages 1303-1309

  Zhang, Jing ^a,b   Lefebvre, Julie L ^a   Zhao, Shuxia ^a   Granato, Michael ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PHOSPHOTRANSFERASE; CHOLINERGIC RECEPTOR; HOMEODOMAIN PROTEIN; MUSK PROTEIN, HUMAN; PROTEIN TYROSINE KINASE; UNPLUGGED PROTEIN, ZEBRAFISH; ZEBRAFISH PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; ENVIRONMENT; GENE LOCUS; GENETIC CODE; GENETIC TRANSCRIPTION; MAMMAL; MOLECULAR CLONING; NERVE FIBER; NEUROMUSCULAR SYNAPSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; RNA SPLICING; SEQUENCE HOMOLOGY; SYNAPTOGENESIS; ZEBRA FISH; ANIMAL; GENETICS; MOLECULAR GENETICS; MUTATION; NERVE TRACT; PHYSIOLOGY;

AMINO ACID SEQUENCE; ANIMALS; AXONS; HOMEODOMAIN PROTEINS; MOLECULAR SEQUENCE DATA; MUTATION; NEURAL PATHWAYS; RECEPTOR PROTEIN-TYROSINE KINASES; RECEPTORS, CHOLINERGIC; SEQUENCE HOMOLOGY, AMINO ACID; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 13744260786     PISSN: 10976256     EISSN: None     Source Type: Journal    
DOI: 10.1038/nn1350     Document Type: Article

References (48)

1. Kaprielian, Z., Runko, E. & Imondi, R. Axon guidance at the midline choice point. Dev. Dyn. 221, 154-181 (2001).
2. Giger, R.J. & Kolodkin, A.L. Silencing the siren: guidance cue hierarchies at the CNS midline. Cell 105, 1-4 (2001).
3. Shirasaki, R. & Pfaff, S.L. Transcriptional codes and the control of neuronal identity. Annu. Rev. Neurosci. 25, 251-281 (2002).
4. Landmesser, L.T. The acquisition of motoneuron subtype identity and motor circuit formation. Int. J. Dev. Neurosci. 19, 175-182 (2001).
5. Lance-Jones, C. & Landmesser, L. Pathway selection by chick lumbosacral motoneurons during normal development. Proc. R. Soc. Lond. B Biol. Sci. 214, 1-18 (1981).
6. Tosney, K.W. & Landmesser, L.T. Pattern and specificity of axonal outgrowth following varying degrees of chick limb bud ablation. J. Neurosci. 4, 2518-2527 (1984).
7. Ferns, M.J. & Hollyday, M. Motor innervation of dorsoventrally reversed wings in chick/quail chimeric embryos. J. Neurosci. 13, 2463-2476 (1993).
8. Helmbacher, F., Schneider-Maunoury, S., Topilko, P., Tiret, L. & Charnay, P. Targeting of the EphA4 tyrosine kinase receptor affects dorsal/ventral pathfinding of limb motor axons. Developmental 127, 3313-3324 (2000).
9. Kania, A. & Jessell, T.M. Topographic motor projections in the limb imposed by LIM homeodomain protein regulation of ephrin-A:EphA interactions. Neuron 38, 581-596 (2003).
10. Beattie, C.E. Control of motor axon guidance in the zebrafish embryo. Brain Res. Bull. 53, 489-500 (2000).
11. Bernhardt, R.R., Goerlinger, S., Roos, M. & Schachner, M. Anterior-posterior subdivision of the somite in embryonic zebrafish: implications for motor axon guidance. Dev. Dyn. 213, 334-347 (1998).
12. Eisen, J.S., Myers, P.Z. & Westerfield, M. Pathway selection by growth-cones of identified motoneurons in live zebra fish embryos. Nature 320, 269-271 (1986).
13. Felsenfeld, A.L., Curry, M. & Kimmel, C.B. The fub-1 mutation blocks initial myofibril formation in zebrafish muscle pioneer cells. Dev. Biol. 148, 23-30 (1991).
14. Melançon, E., Liu, D.W.C., Westerfield, M. & Eisen, J.S. Pathfinding by identified zebrafish motorneurons in the absence of muscle pioneers. J. Neurosci. 17, 7796-7804 (1997).
15. Zhang, J. & Granato, M. The zebrafish unplugged gene controls motor axon pathway selection. Development 127, 2099-2111 (2000).
16. Zeller, J. & Granato, M. The zebrafish diwanka gene controls an early step of motor growth cone migration. Development 126, 3461-3472 (1999).
17. Devoto, S.H., Melancon, E., Eisen, J.S. & Westerfield, M. Identification of separate slow and fast muscle precursor cells in vivo, prior to somite formation. Development 122, 3371-3380 (1996).
18. Forrester, W.C. The Ror receptor tyrosine kinase family. Cell Mol. Life Sci. 59, 83-96 (2002).
19. Burden, S.J. Building the vertebrate neuromuscular synapse. J. Neurobiol. 53, 501-511 (2002).
20. Sanes, J.R. & Lichtman, J.W. Induction, assembly, maturation and maintenance of a postsynaptic apparatus. Nat. Rev. Neurosci. 2, 791-805 (2001).
21. Zhang, J., Malayaman, S., Davis, C. & Granato, M. A dual role for the zebrafish unplugged gene in motor axon pathfinding and pharyngeal development. Dev. Biol. 240, 560-573. (2001).
22. Gautam, M. et al. Defective neuromuscular synaptogenesis in agrin-deficient mutant mice. Cell 85, 525-535 (1996).
23. Gautam, M. et al. Failure of postsynaptic specialization to develop at neuromuscular junctions of rapsyn-deficient mice. Nature 377, 232-236 (1995).
24. DeChiara, T.M. et al. The receptor tyrosine kinase MuSK is required for neuromuscular junction formation in vivo. Cell 85, 501-512 (1996).
25. Coers, C. Structure and organization of the myoneural junction. Int. Rev. Cytol. 22, 239-267 (1967).
26. Westerfield, M., McMurray, J.V. & Eisen, J.S. Identified motoneurons and their innervation of axial muscles in the zebrafish. J. Neurosci. 6, 2267-2277 (1986).
27. Ono, F., Shcherbatko, A., Higashijima, S., Mandel, G. & Brehm, P. The zebrafish motility mutant twitch once reveals new roles for rapsyn in synaptic function. J. Neurosci. 22, 6491-6498 (2002).
28. Draper, B.W., Morcos, P.A. & Kimmel, C.B. Inhibition of zebrafish fgf8 pre-mRNA splicing with morpholino oligos: a quantifiable method for gene knockdown. Genesis 30, 154-156 (2001).
29. Nasevicius, A. & Ekker, S.C. Effective targeted gene 'knockdown' in zebrafish. Nat. Genet. 26, 216-220 (2000).
30. Du, S.J., Gao, J. & Anyangwe, V. Muscle-specific expression of myogenin in zebrafish embryos is controlled by multiple regulatory elements in the promoter. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 134, 123-134 (2003).
31. Chung, K.Y., Taylor, J.S., Shum, D.K. & Chan, S.O. Axon routing at the optic chiasm after enzymatic removal of chondroitin sulfate in mouse embryos. Development 127, 2673-2683 (2000).
32. Walz, A., Anderson, R.B., Irie, A., Chien, C.B. & Holt, C.E. Chondroitin sulfate disrupts axon pathfinding in the optic tract and alters growth cone dynamics. J. Neurobiol. 53, 330-342 (2002).
33. Karlstrom, R.O., Talbot, W.S. & Schier, A.F. Comparative synteny cloning of zebrafish you-too: mutations in the Hedgehog target gli2 affect ventral forebrain patterning. Genes Dev. 13, 388-393 (1999).
34. Du, S.J. & Dienhart, M. Gli2 mediation of hedgehog signals in slow muscle induction in zebrafish. Differentiation 67, 84-91 (2001).
35. Zeller, J. et al. Migration of zebrafish spinal motor nerves into the periphery requires multiple myotome-derived cues. Dev. Biol. 252, 241-256 (2002).
36. Hwang, H.Y., Olson, S.K., Esko, J.D. & Horvitz, H.R. Caenorhabditis elegans early embryogenesis and vulval morphogenesis require chondroitin biosynthesis. Nature 423, 439-443 (2003).
37. Kitagawa, H., Uyama, T. & Sugahara, K. Molecular cloning and expression of a human chondroitin synthase. J. Biol. Chem. 276, 38721-38726 (2001).
38. Landgraf, M., Baylies, M. & Bate, M. Muscle founder cells regulate defasciculation and targeting of motor axons in the Drosophila embryo. Curr. Biol. 9, 589-592 (1999).
39. Hesser, B.A., Sander, A. & Witzemann, V. Identification and characterization of a novel splice variant of MuSK. FEBS Lett. 442, 133-137 (1999).
40. Zhou, H., Glass, D.J., Yancopoulos, G.D. & Sanes, J.R. Distinct domains of MuSK mediate its abilities to induce and to associate with postsynaptic specializations. J. Cell Biol. 146, 1133-1146 (1999).
41. Hikasa, H., Shibata, M., Hiratani, I. & Taira, M. The Xenopus receptor tyrosine kinase Xror2 modulates morphogenetic movements of the axial mesoderm and neuroectoderm via Wnt signaling. Development 129, 5227-5239 (2002).
42. Oishi, I. et al. The receptor tyrosine kinase Ror2 is involved in non-canonical Wnt5a/JNK signalling pathway. Genes Cells 8, 645-654 (2003).
43. Moeller, C., Swindell, E.G., Kispert, A. & Eichele, G. Carboxypeptidase Z (CPZ) modulates Wnt signaling and regulates the development of skeletal elements in the chicken. Development 130, 5103-5111 (2003).
44. Yoshikawa, S., McKinnon, R.D., Kokel, M. & Thomas, J.B. Wnt-mediated axon guidance via the Drosophila Derailed receptor. Nature 422, 583-588 (2003).
45. Lyuksyutova, A.I. et al. Anterior-posterior guidance of commissural axons by Wnt-frizzled signaling. Science 302, 1984-1988 (2003).
46. Mullins, M.C., Hammerschmidt, M., Haffter, P. &. Nüsslein- Volhard, C. Large-scale mutagenesis in the zebrafish: in search of genes controlling development in a vertebrate. Curr. Biol. 4, 189-202 (1994).
47. Odenthal, J. & Nusslein-Volhard, C. Forkhead domain genes in zebrafish. Dev. Genes Evol. 208, 245-258 (1998).
48. Downes, G.B., Waterbury, J.A. & Granato, M. Rapid in vivo labeling of identified zebrafish neurons. Genesis 34, 196-202 (2002).