Effects of decreased muscle activity on developing axial musculature in<i>nicb107</i>mutant zebrafish (<i>Danio rerio</i>)

Meulen, Talitha van der; Schipper, H.; Leeuwen, J.L. van; Kranenbarg, S.

doi:10.1242/jeb.01826

Cited by 21 publications

(14 citation statements)

References 64 publications

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“…They were approximately the same size as the sop mutants and nicotine-exposed wild-type larvae. We conclude that the size reduction reported in this paper may not be related to muscle degeneration or abnormal axonal pathfinding, but may simply be an effect of prolonged paralysis consistent with observations of van der Muelen et al, 2005.…”

Section: Discussionsupporting

confidence: 85%

“…or wild-type larvae. This size reduction has been reported by another group studying the nic1 mutant zebrafish (van der Muelen et al, 2005), and is not likely related to axonal pathfinding errors or degenerated muscle because in the sop mutants, muscle and motoneuron axons are present and appear normal (our work and Ono et al, 2001). In nicotine-exposed wild-type larvae, the motoneuron axons and muscle are altered.…”

Section: Discussionsupporting

confidence: 84%

“…This phenotype was apparent in sop −/− larvae as well as nicotine-exposed wild-type larvae. This reduction in size along the dorsal/ventral axis has also been reported for another paralytic mutant nic b107/b107 , also known as the nic1 mutant (van der Muelen et al, 2005). At the cross section-level, white muscle fibers of sop −/− larvae appeared very similar to white muscle fibers in stage matched sop sibling larvae, or wild-type larvae (Figs.…”

Section: Resultssupporting

confidence: 75%

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Uncoupling nicotine mediated motoneuron axonal pathfinding errors and muscle degeneration in zebrafish

Welsh

Tanguay

Svoboda

2009

Toxicology and Applied Pharmacology

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Zebrafish embryos offer a unique opportunity to investigate the mechanisms by which nicotine exposure impacts early vertebrate development. Embryos exposed to nicotine become functionally paralyzed by 42 hpf suggesting that the neuromuscular system is compromised in exposed embryos. We previously demonstrated that secondary spinal motoneurons in nicotine-exposed embryos were delayed in development and that their axons made pathfinding errors (Svoboda, K.R., Vijayaraghaven, S., Tanguay, R.L., 2002. Nicotinic receptors mediate changes in spinal motoneuron development and axonal pathfinding in embryonic zebrafish exposed to nicotine. J. Neurosci. 22, 10731–10741). In that study, we did not consider the potential role that altered skeletal muscle development caused by nicotine exposure could play in contributing to the errors in spinal motoneuron axon pathfinding. In this study, we show that an alteration in skeletal muscle development occurs in tandem with alterations in spinal motoneuron development upon exposure to nicotine. The alteration in the muscle involves the binding of nicotine to the muscle-specific AChRs. The nicotine-induced alteration in muscle development does not occur in the zebrafish mutant (sofa potato, [sop]), which lacks muscle-specific AChRs. Even though muscle development is unaffected by nicotine exposure in sop mutants, motoneuron axonal pathfinding errors still occur in these mutants, indicating a direct effect of nicotine exposure on nervous system development.

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Section: Discussionsupporting

confidence: 85%

Section: Discussionsupporting

confidence: 84%

Section: Resultssupporting

confidence: 75%

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Uncoupling nicotine mediated motoneuron axonal pathfinding errors and muscle degeneration in zebrafish

Welsh

Tanguay

Svoboda

2009

Toxicology and Applied Pharmacology

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“…Pseudohelical muscle fibre arrangements are generated despite the immobility ( Van der Meulen et al, 2005). Although the initial development of curved muscle fibre trajectories does not depend on active muscle, the architectural fine tuning in later stages (2·d.p.f.…”

Section: Effects Of Immobility On Muscle-fibre Arrangementmentioning

confidence: 99%

A functional analysis of myotomal muscle-fibre reorientation in developing zebrafishDanio rerio

Leeuwen

Meulen

Schipper

et al. 2008

Journal of Experimental Biology

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SUMMARYThe fast muscle fibres in the anterior trunk of teleost fish are primarily responsible for large amplitude undulatory swimming motions. Previous theoretical studies suggested that the near-helical arrangement of these fibres results in a (fairly) uniform distribution of fibre strain and work output during swimming. However, the underlying simplifications of these studies precluded unequivocal support for this hypothesis. We studied the fast muscle-fibre reorientation and the concomitant myotomal strain variance in a body segment near the anus during larval and juvenile development in the zebrafish. From 2 to 4 days post fertilization (d.p.f.), the measured angles between the muscle fibres and the longitudinal axis of the zebrafish were small. Yet, onset of a near-helical muscle-fibre arrangement was recognized. Juveniles of 51·d.p.f. have larger mean fibre angles and already possess the near-helical pattern of adult teleosts. We present a model that computes the distribution of the strain along the muscle fibres from measured muscle-fibre orientations, body curvature and prescribed tissue deformations. We selected the most extreme body curvatures, which only occur during fast starts and turning manoeuvres. Using the model, we identified the (nonlinear) tissue deformations that yield the least variance in the muscle-fibre strain. We show that simple beam theory cannot reliably predict the strain distribution: it results in very small strains and negligible work output of the most medial fibres. In our model, we avoided these functional limitations by adding a shear deformation to the simple beam deformation. At 2·d.p.f., the predicted variance in the muscle-fibre strain for the shear deformation optimized for strain uniformity is fairly small, due to the small variation in the fibre distances to the medial plane that is caused by the relatively large spinal cord and notochord. The predicted minimal strain variance increases sharply from 2·d.p.f. to 3·d.p.f., remains relatively large at 4·d.p.f., but decreases again considerably at 15 and 39·d.p.f. The 51·d.p.f. stage exhibits the smallest variance in the fibre strains (for the identified optimal deformation), in spite of the widely varying muscle-fibre distances to the medial plane. The non-linear nature of the body deformations with the least strain variance implies an interesting optimization constraint: the juvenile muscle-fibre arrangement results in small predicted spatial strain variations at large-amplitude body curvatures, at the (modest) expense of a large coefficient of variation for small curvatures. We conclude that larval fish rapidly change their muscle-fibre orientations (probably in response to mechanical signals). Within the theoretically examined plausible range of deformations, the closest correspondence to a uniform strain field was found for the juvenile stage. Supplementary material available online at

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“…For example, muscle contractions could stimulate stretch-activated channels on the muscles or the skin, which in turn could alter secretion or regulate localization of an extracellular guidance molecule expressed in a dorsal-ventral gradient. Interestingly, the mRNA expression of collagen 1α2 in the skin is altered in the chrna1 (nic-1) mutant (van der Meulen et al, 2005), although it is unknown if collagen 1α2 affects peripheral RB axon direction. We also found that CSPG expression is reduced in chrna1 (nic-1) mutants, suggesting that muscle activity can somehow affect CSPG levels.…”

Section: Discussionmentioning

confidence: 99%

Muscle Contractions Guide Rohon–Beard Peripheral Sensory Axons

Paulus

Willer²,

Willer³

et al. 2009

J. Neurosci.

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Multiple molecular cues guide neuronal axons to their targets during development. Previous studies in vitro have shown that mechanical stimulation also can affect axon growth; however, whether mechanical force contributes to axon guidance in vivo is unknown. We investigated the role of muscle contractions in the guidance of zebrafish peripheral Rohon-Beard (RB) sensory axons in vivo. We analyzed several mutants that affect muscle contraction through different molecular pathways, including a new mutant allele of the titin a (pik) gene, mutants that affect the hedgehog signaling pathway, and a nicotinic acetylcholine receptor mutant. We found RB axon defects in these mutants, the severity of which appeared to correlate with the extent of muscle contraction loss. These axons extend between the muscle and skin and normally have ventral trajectories and repel each other on contact. RB peripheral axons in muscle mutants extend longitudinally instead of ventrally, and the axons fail to repel one another on contact. In addition, we showed that limiting muscle movements by embedding embryos in agarose caused similar defects in peripheral RB axon guidance. This work suggests that the mechanical forces generated by muscle contractions are necessary for proper sensory axon pathfinding in vivo.

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Effects of decreased muscle activity on developing axial musculature innicb107mutant zebrafish (Danio rerio)

Cited by 21 publications

References 64 publications

Uncoupling nicotine mediated motoneuron axonal pathfinding errors and muscle degeneration in zebrafish

Uncoupling nicotine mediated motoneuron axonal pathfinding errors and muscle degeneration in zebrafish

A functional analysis of myotomal muscle-fibre reorientation in developing zebrafishDanio rerio

Muscle Contractions Guide Rohon–Beard Peripheral Sensory Axons

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