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Synchronous symmetry breaking in neurons with different neurite counts.

Wissner-Gross ZD, Scott MA, Steinmeyer JD, Yanik MF - PLoS ONE (2013)

Bottom Line: However, the effects of neurite count in neuronal symmetry breaking have never been studied.We also show that despite the significant differences among the previously proposed models, they all agree with our experimental findings when the expression levels of the proteins responsible for symmetry breaking increase with neurite count.Consistent with these results, we observe that the expression levels of two of these proteins, HRas and shootin1, significantly correlate with neurite count.

View Article: PubMed Central - PubMed

Affiliation: Department of Physics, Harvard University, Cambridge, Massachusetts, USA.

ABSTRACT
As neurons develop, several immature processes (i.e., neurites) grow out of the cell body. Over time, each neuron breaks symmetry when only one of its neurites grows much longer than the rest, becoming an axon. This symmetry breaking is an important step in neurodevelopment, and aberrant symmetry breaking is associated with several neuropsychiatric diseases, including schizophrenia and autism. However, the effects of neurite count in neuronal symmetry breaking have never been studied. Existing models for neuronal polarization disagree: some predict that neurons with more neurites polarize up to several days later than neurons with fewer neurites, while others predict that neurons with different neurite counts polarize synchronously. We experimentally find that neurons with different neurite counts polarize synchronously. We also show that despite the significant differences among the previously proposed models, they all agree with our experimental findings when the expression levels of the proteins responsible for symmetry breaking increase with neurite count. Consistent with these results, we observe that the expression levels of two of these proteins, HRas and shootin1, significantly correlate with neurite count. This coordinated symmetry breaking we observed among neurons with different neurite counts may be important for synchronized polarization of neurons in developing organisms.

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Neurite sprouting in developing neurons.A, Mean neurite count as a function of time. The solid line is an exponential fit to the data, constrained to include the origin. Error bars are SE. B, Neurite count distribution at the final measured time point 52.5 h after plating. The solid line is a simulated distribution using the exponential fit from A to calculate the sprouting rate and assumes random neurite sprouting independent of neurite count. Error bars are SE.
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pone-0054905-g004: Neurite sprouting in developing neurons.A, Mean neurite count as a function of time. The solid line is an exponential fit to the data, constrained to include the origin. Error bars are SE. B, Neurite count distribution at the final measured time point 52.5 h after plating. The solid line is a simulated distribution using the exponential fit from A to calculate the sprouting rate and assumes random neurite sprouting independent of neurite count. Error bars are SE.

Mentions: The Samuels, Fivaz, and Toriyama models all assume that neurite count does not change throughout the polarization process. However, we observed that new neurites sprouted while the neurons were breaking symmetry. We specifically found that neurite sprouting occurred in an exponentially decaying fashion, with a characteristic time of approximately 32 h and an asymptotic mean neurite count of approximately 8.0 (Fig. 4A).


Synchronous symmetry breaking in neurons with different neurite counts.

Wissner-Gross ZD, Scott MA, Steinmeyer JD, Yanik MF - PLoS ONE (2013)

Neurite sprouting in developing neurons.A, Mean neurite count as a function of time. The solid line is an exponential fit to the data, constrained to include the origin. Error bars are SE. B, Neurite count distribution at the final measured time point 52.5 h after plating. The solid line is a simulated distribution using the exponential fit from A to calculate the sprouting rate and assumes random neurite sprouting independent of neurite count. Error bars are SE.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3569465&req=5

pone-0054905-g004: Neurite sprouting in developing neurons.A, Mean neurite count as a function of time. The solid line is an exponential fit to the data, constrained to include the origin. Error bars are SE. B, Neurite count distribution at the final measured time point 52.5 h after plating. The solid line is a simulated distribution using the exponential fit from A to calculate the sprouting rate and assumes random neurite sprouting independent of neurite count. Error bars are SE.
Mentions: The Samuels, Fivaz, and Toriyama models all assume that neurite count does not change throughout the polarization process. However, we observed that new neurites sprouted while the neurons were breaking symmetry. We specifically found that neurite sprouting occurred in an exponentially decaying fashion, with a characteristic time of approximately 32 h and an asymptotic mean neurite count of approximately 8.0 (Fig. 4A).

Bottom Line: However, the effects of neurite count in neuronal symmetry breaking have never been studied.We also show that despite the significant differences among the previously proposed models, they all agree with our experimental findings when the expression levels of the proteins responsible for symmetry breaking increase with neurite count.Consistent with these results, we observe that the expression levels of two of these proteins, HRas and shootin1, significantly correlate with neurite count.

View Article: PubMed Central - PubMed

Affiliation: Department of Physics, Harvard University, Cambridge, Massachusetts, USA.

ABSTRACT
As neurons develop, several immature processes (i.e., neurites) grow out of the cell body. Over time, each neuron breaks symmetry when only one of its neurites grows much longer than the rest, becoming an axon. This symmetry breaking is an important step in neurodevelopment, and aberrant symmetry breaking is associated with several neuropsychiatric diseases, including schizophrenia and autism. However, the effects of neurite count in neuronal symmetry breaking have never been studied. Existing models for neuronal polarization disagree: some predict that neurons with more neurites polarize up to several days later than neurons with fewer neurites, while others predict that neurons with different neurite counts polarize synchronously. We experimentally find that neurons with different neurite counts polarize synchronously. We also show that despite the significant differences among the previously proposed models, they all agree with our experimental findings when the expression levels of the proteins responsible for symmetry breaking increase with neurite count. Consistent with these results, we observe that the expression levels of two of these proteins, HRas and shootin1, significantly correlate with neurite count. This coordinated symmetry breaking we observed among neurons with different neurite counts may be important for synchronized polarization of neurons in developing organisms.

Show MeSH
Related in: MedlinePlus