 |
Previous Article | Next Article 
Volume 17, Number 20,
Issue of October 15, 1997
pp. 7796-7804
Copyright ©1997 Society for Neuroscience
Pathfinding by Identified Zebrafish Motoneurons in the Absence of
Muscle Pioneers
Received March 24, 1997; revised July 28, 1997; accepted July 30, 1997.
Ellie Melançon1,
Dennis W. C. Liu2,
Monte Westerfield1, and
Judith S. Eisen1
1 Institute of Neuroscience, University of Oregon,
Eugene, Oregon 97403-1254, and 2 Howard Hughes Medical
Institute, Chevy Chase, Maryland 20815-6789
To identify the cellular cues that guide zebrafish neuronal growth
cones to their targets, we examined interactions between identified
motor growth cones and identified muscle fibers and tested whether
these fibers were required for growth cone navigation. Caudal primary
motoneurons (CaPs) and middle primary motoneurons (MiPs) are identified
motoneurons that innervate cell-specific regions of the myotome. Growth
cones of both cells initially extend along a common pathway and then
pause at a set of identified muscle fibers, called muscle pioneers,
before diverging along cell-specific pathways. Muscle pioneers are
intermediate targets of both CaP and MiP (; ); both motoneurons extend their growth cones
directly to the muscle pioneers on which the first functional
neuromuscular contacts form, suggesting that muscle pioneers may
provide guidance information to these growth cones. We tested this idea
by ablating muscle pioneers and observing the resulting motor axonal
trajectories. Both CaP and MiP ultimately formed normal axonal arbors
after muscle pioneer ablation, showing that muscle pioneers are
unnecessary for formation of correct axonal trajectories; however,
although final cellular morphology was correct in the absence of muscle pioneers, MiP growth cones branched abnormally or extended ventrally beyond the common pathway. Ablation of CaP and the muscle pioneers together increased the aberrant behavior of the MiP growth cone. Our
results provide evidence that an intermediate target, the muscle
pioneers, affects motor axonal extension without altering target
choice, suggesting that other cues also contribute to proper pathway
navigation.
Key words:
acetylcholine receptors;
neuromuscular junctions;
axogenesis;
zebrafish motoneurons;
muscle pioneers;
pathway
navigation
This article has been cited by other articles:

|
 |

|
 |
 
K.-L. Boon, S. Xiao, M. L. McWhorter, T. Donn, E. Wolf-Saxon, M. T. Bohnsack, C. B. Moens, and C. E. Beattie
Zebrafish survival motor neuron mutants exhibit presynaptic neuromuscular junction defects
Hum. Mol. Genet.,
October 1, 2009;
18(19):
3615 - 3625.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. L. van Leeuwen, T. van der Meulen, H. Schipper, and S. Kranenbarg
A functional analysis of myotomal muscle-fibre reorientation in developing zebrafish Danio rerio
J. Exp. Biol.,
April 15, 2008;
211(8):
1289 - 1304.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Sato-Maeda, M. Obinata, and W. Shoji
Position fine-tuning of caudal primary motoneurons in the zebrafish spinal cord
Development,
January 15, 2008;
135(2):
323 - 332.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. J. Kim, I-H. Liu, Y. Song, J.-A. Lee, W. Halfter, R. J. Balice-Gordon, E. Linney, and G. J. Cole
Agrin is required for posterior development and motor axon outgrowth and branching in embryonic zebrafish
Glycobiology,
February 1, 2007;
17(2):
231 - 247.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. A. Hutchinson and J. S. Eisen
Islet1 and Islet2 have equivalent abilities to promote motoneuron formation and to specify motoneuron subtype identity
Development,
June 1, 2006;
133(11):
2137 - 2147.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Sato-Maeda, H. Tawarayama, M. Obinata, J. Y. Kuwada, and W. Shoji
Sema3a1 guides spinal motor axons in a cell- and stage-specific manner in zebrafish
Development,
March 1, 2006;
133(5):
937 - 947.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. Brennan, M. Mangoli, C. E. F. Dyer, and R. Ashworth
Acetylcholine and calcium signalling regulates muscle fibre formation in the zebrafish embryo
J. Cell Sci.,
November 15, 2005;
118(22):
5181 - 5190.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T. van der Meulen, H. Schipper, J. L. van Leeuwen, and S. Kranenbarg
Effects of decreased muscle activity on developing axial musculature in nicb107 mutant zebrafish (Danio rerio)
J. Exp. Biol.,
October 1, 2005;
208(19):
3675 - 3687.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. Winkler, C. Eggert, D. Gradl, G. Meister, M. Giegerich, D. Wedlich, B. Laggerbauer, and U. Fischer
Reduced U snRNP assembly causes motor axon degeneration in an animal model for spinal muscular atrophy
Genes & Dev.,
October 1, 2005;
19(19):
2320 - 2330.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. L. Lefebvre, F. Ono, C. Puglielli, G. Seidner, C. Franzini-Armstrong, P. Brehm, and M. Granato
Increased neuromuscular activity causes axonal defects and muscular degeneration
Development,
June 1, 2004;
131(11):
2605 - 2618.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
I. T. Shepherd, J. Pietsch, S. Elworthy, R. N. Kelsh, and D. W. Raible
Roles for GFR{alpha}1 receptors in zebrafish enteric nervous system development
Development,
January 1, 2004;
131(1):
241 - 249.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. L. McWhorter, U. R. Monani, A. H.M. Burghes, and C. E. Beattie
Knockdown of the survival motor neuron (Smn) protein in zebrafish causes defects in motor axon outgrowth and pathfinding
J. Cell Biol.,
September 1, 2003;
162(5):
919 - 932.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. R. Svoboda, S. Vijayaraghavan, and R. L. Tanguay
Nicotinic Receptors Mediate Changes in Spinal Motoneuron Development and Axonal Pathfinding in Embryonic Zebrafish Exposed to Nicotine
J. Neurosci.,
December 15, 2002;
22(24):
10731 - 10741.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. A. Cornell and J. S. Eisen
Delta/Notch signaling promotes formation of zebrafish neural crest by repressing Neurogenin 1 function
Development,
January 6, 2002;
129(11):
2639 - 2648.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. R. Buss and P. Drapeau
Physiological Properties of Zebrafish Embryonic Red and White Muscle Fibers During Early Development
J Neurophysiol,
September 1, 2000;
84(3):
1545 - 1557.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. C. LEKVEN, K. A. HELDE, C. J. THORPE, R. ROOKE, and R. T. MOON
Reverse genetics in zebrafish
Physiol Genomics,
March 14, 2000;
2(2):
37 - 48.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T. J. Diefenbach, P. B. Guthrie, and S. B. Kater
Stimulus History Alters Behavioral Responses of Neuronal Growth Cones
J. Neurosci.,
February 15, 2000;
20(4):
1484 - 1494.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. Beattie, E Melancon, and J. Eisen
Mutations in the stumpy gene reveal intermediate targets for zebrafish motor axons
Development,
January 6, 2000;
127(12):
2653 - 2662.
[Abstract]
[PDF]
|
 |
|

|
 |

|
 |
 
J Zeller and M Granato
The zebrafish diwanka gene controls an early step of motor growth cone migration
Development,
January 8, 1999;
126(15):
3461 - 3472.
[Abstract]
[PDF]
|
 |
|
|

|