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Developmental genetics of the C. elegans pharyngeal neurons NSML and NSMR.

Axäng C, Rauthan M, Hall DH, Pilon M - BMC Dev. Biol. (2008)

Bottom Line: We found that the three NSM processes are differently sensitive to mutations.By studying the effects of nearly forty different mutations we have learned that the different NSM processes require different genes for their proper guidance and use both growth cone dependent and growth cone independent mechanisms for establishing their proper trajectories.Together with the guidance of the M2 neuron, this is the second case of a pharyngeal neuron establishing one of its processes using an unexpected mechanism.

View Article: PubMed Central - HTML - PubMed

Affiliation: Dept, Cell and Molecular Biology, Göteborg University, Box 462, S-405 30, Sweden. axang@chalmers.se

ABSTRACT

Background: We are interested in understanding how the twenty neurons of the C. elegans pharynx develop in an intricate yet reproducible way within the narrow confines of the embryonic pharyngeal primordium. To complement an earlier study of the pharyngeal M2 motorneurons, we have now examined the effect of almost forty mutations on the morphology of a bilateral pair of pharyngeal neurosecretory-motor neurons, the NSMs.

Results: A careful description of the NSM morphology led to the discovery of a third, hitherto unreported process originating from the NSM cell body and that is likely to play a proprioceptive function. We found that the three NSM processes are differently sensitive to mutations. The major dorsal branch was most sensitive to mutations that affect growth cone guidance and function (e.g. unc-6, unc-34, unc-73), while the major sub-ventral branch was more sensitive to mutations that affect components of the extracellular matrix (e.g. sdn-1). Of the tested mutations, only unc-101, which affects an adaptin, caused the loss of the newly described thin minor process. The major processes developed synaptic branches post-embryonically, and these exhibited activity-dependent plasticity.

Conclusion: By studying the effects of nearly forty different mutations we have learned that the different NSM processes require different genes for their proper guidance and use both growth cone dependent and growth cone independent mechanisms for establishing their proper trajectories. The two major NSM processes develop in a growth cone dependent manner, although the sub-ventral process relies more on substrate adhesion. The minor process also uses growth cones but uniquely develops using a mechanism that depends on the clathrin adaptor molecule UNC-101. Together with the guidance of the M2 neuron, this is the second case of a pharyngeal neuron establishing one of its processes using an unexpected mechanism.

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Morphology of the NSM neurons. (A) Cartoon of one NSM neuron, NSML (B) Flattened stack of confocal images of an adult worm expressing pTPH-1::GFP. The main structures shown in panels A and B are the cell body (red circle; filled triangle), the major sub-ventral (blue; filled arrow) and dorsal (green; open triangle) and the minor (red line; open arrow) processes. The scale bar represents 20 μm.
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Figure 1: Morphology of the NSM neurons. (A) Cartoon of one NSM neuron, NSML (B) Flattened stack of confocal images of an adult worm expressing pTPH-1::GFP. The main structures shown in panels A and B are the cell body (red circle; filled triangle), the major sub-ventral (blue; filled arrow) and dorsal (green; open triangle) and the minor (red line; open arrow) processes. The scale bar represents 20 μm.

Mentions: Pharyngeal expression of the pTPH-1::GFP reporter is limited to the NSM neurons in larvae and adults; outside the pharynx, expression is also seen in the nerve ring and some other extra-pharyngeal neurons e.g. HSN, ADF (Fig. 1). During embryogenesis, expression of pTPH-1::GFP within the pharyngeal primordium can first be observed at approximately 300 min. of development (Fig. 2). When the pharyngeal primordium begins to elongate at two-fold stage, strong expression of the pTPH-1::GFP reporter is observed both in the muscle cells of the procorpus and metacorpus. In the late three-fold stage, as the pharynx elongates and matures, pharyngeal expression of the pTPH-1::GFP reporter becomes restricted to the NSM neurons; pharyngeal muscle expression weakens and eventually disappears completely by the time of hatching [7]. Because of the embryonic expression of pTPH-1::GFP in pharyngeal muscles, the NSM processes have already established their trajectories by the time that they can be unambiguously scored using this reporter. It is therefore not possible to directly study the NSM neurons as they are developing using the pTPH-1::GFP reporter, although it is useful to examine the final morphology of these neurons. Note that none of the mutants tested in the course of the present study affected the levels of pTPH-1::GFP expression (see below).


Developmental genetics of the C. elegans pharyngeal neurons NSML and NSMR.

Axäng C, Rauthan M, Hall DH, Pilon M - BMC Dev. Biol. (2008)

Morphology of the NSM neurons. (A) Cartoon of one NSM neuron, NSML (B) Flattened stack of confocal images of an adult worm expressing pTPH-1::GFP. The main structures shown in panels A and B are the cell body (red circle; filled triangle), the major sub-ventral (blue; filled arrow) and dorsal (green; open triangle) and the minor (red line; open arrow) processes. The scale bar represents 20 μm.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2375884&req=5

Figure 1: Morphology of the NSM neurons. (A) Cartoon of one NSM neuron, NSML (B) Flattened stack of confocal images of an adult worm expressing pTPH-1::GFP. The main structures shown in panels A and B are the cell body (red circle; filled triangle), the major sub-ventral (blue; filled arrow) and dorsal (green; open triangle) and the minor (red line; open arrow) processes. The scale bar represents 20 μm.
Mentions: Pharyngeal expression of the pTPH-1::GFP reporter is limited to the NSM neurons in larvae and adults; outside the pharynx, expression is also seen in the nerve ring and some other extra-pharyngeal neurons e.g. HSN, ADF (Fig. 1). During embryogenesis, expression of pTPH-1::GFP within the pharyngeal primordium can first be observed at approximately 300 min. of development (Fig. 2). When the pharyngeal primordium begins to elongate at two-fold stage, strong expression of the pTPH-1::GFP reporter is observed both in the muscle cells of the procorpus and metacorpus. In the late three-fold stage, as the pharynx elongates and matures, pharyngeal expression of the pTPH-1::GFP reporter becomes restricted to the NSM neurons; pharyngeal muscle expression weakens and eventually disappears completely by the time of hatching [7]. Because of the embryonic expression of pTPH-1::GFP in pharyngeal muscles, the NSM processes have already established their trajectories by the time that they can be unambiguously scored using this reporter. It is therefore not possible to directly study the NSM neurons as they are developing using the pTPH-1::GFP reporter, although it is useful to examine the final morphology of these neurons. Note that none of the mutants tested in the course of the present study affected the levels of pTPH-1::GFP expression (see below).

Bottom Line: We found that the three NSM processes are differently sensitive to mutations.By studying the effects of nearly forty different mutations we have learned that the different NSM processes require different genes for their proper guidance and use both growth cone dependent and growth cone independent mechanisms for establishing their proper trajectories.Together with the guidance of the M2 neuron, this is the second case of a pharyngeal neuron establishing one of its processes using an unexpected mechanism.

View Article: PubMed Central - HTML - PubMed

Affiliation: Dept, Cell and Molecular Biology, Göteborg University, Box 462, S-405 30, Sweden. axang@chalmers.se

ABSTRACT

Background: We are interested in understanding how the twenty neurons of the C. elegans pharynx develop in an intricate yet reproducible way within the narrow confines of the embryonic pharyngeal primordium. To complement an earlier study of the pharyngeal M2 motorneurons, we have now examined the effect of almost forty mutations on the morphology of a bilateral pair of pharyngeal neurosecretory-motor neurons, the NSMs.

Results: A careful description of the NSM morphology led to the discovery of a third, hitherto unreported process originating from the NSM cell body and that is likely to play a proprioceptive function. We found that the three NSM processes are differently sensitive to mutations. The major dorsal branch was most sensitive to mutations that affect growth cone guidance and function (e.g. unc-6, unc-34, unc-73), while the major sub-ventral branch was more sensitive to mutations that affect components of the extracellular matrix (e.g. sdn-1). Of the tested mutations, only unc-101, which affects an adaptin, caused the loss of the newly described thin minor process. The major processes developed synaptic branches post-embryonically, and these exhibited activity-dependent plasticity.

Conclusion: By studying the effects of nearly forty different mutations we have learned that the different NSM processes require different genes for their proper guidance and use both growth cone dependent and growth cone independent mechanisms for establishing their proper trajectories. The two major NSM processes develop in a growth cone dependent manner, although the sub-ventral process relies more on substrate adhesion. The minor process also uses growth cones but uniquely develops using a mechanism that depends on the clathrin adaptor molecule UNC-101. Together with the guidance of the M2 neuron, this is the second case of a pharyngeal neuron establishing one of its processes using an unexpected mechanism.

Show MeSH
Related in: MedlinePlus