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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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Related in: MedlinePlus

Experimentally and theoretically predicted symmetry breaking in neurons with different neurite counts.Each color series indicates a different neurite count, as listed in the legend. A, Experimental measurements of neuronal polarity as a function of time and neurite count. Dashed lines separate data from different discrete time points. Bars indicate mean plus/minus SE, and neurite counts at each time point are only shown if at least 3 neurons had that neurite count at that time point. B–D, Computationally predicted polarity vs. time curves for neurons with different neurite counts using the Samuels (B), Fivaz (C), and Toriyama (D) models. E, Computationally predicted polarity vs. time curves for neurons with different neurite counts using a modified version of the Fivaz model in which HRas expression is independent of neurite count. The original Fivaz model, in which HRas expression increases with neurite count, is shown in C.
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pone-0054905-g003: Experimentally and theoretically predicted symmetry breaking in neurons with different neurite counts.Each color series indicates a different neurite count, as listed in the legend. A, Experimental measurements of neuronal polarity as a function of time and neurite count. Dashed lines separate data from different discrete time points. Bars indicate mean plus/minus SE, and neurite counts at each time point are only shown if at least 3 neurons had that neurite count at that time point. B–D, Computationally predicted polarity vs. time curves for neurons with different neurite counts using the Samuels (B), Fivaz (C), and Toriyama (D) models. E, Computationally predicted polarity vs. time curves for neurons with different neurite counts using a modified version of the Fivaz model in which HRas expression is independent of neurite count. The original Fivaz model, in which HRas expression increases with neurite count, is shown in C.

Mentions: We next experimentally determined whether neurons with different neurite counts polarize synchronously or asynchronously. At each time point, with the lone exception at 40.5 h after plating, we observed no statistical difference among the polarities of neurons with different neurite counts (p > 0.05 by ANOVA, Fig. 3A). We also found that there was no significant correlation (p > 0.01 by Pearson correlation) between neurite count and polarity at any of the time points, including the 40.5 h time point.


Synchronous symmetry breaking in neurons with different neurite counts.

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

Experimentally and theoretically predicted symmetry breaking in neurons with different neurite counts.Each color series indicates a different neurite count, as listed in the legend. A, Experimental measurements of neuronal polarity as a function of time and neurite count. Dashed lines separate data from different discrete time points. Bars indicate mean plus/minus SE, and neurite counts at each time point are only shown if at least 3 neurons had that neurite count at that time point. B–D, Computationally predicted polarity vs. time curves for neurons with different neurite counts using the Samuels (B), Fivaz (C), and Toriyama (D) models. E, Computationally predicted polarity vs. time curves for neurons with different neurite counts using a modified version of the Fivaz model in which HRas expression is independent of neurite count. The original Fivaz model, in which HRas expression increases with neurite count, is shown in C.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0054905-g003: Experimentally and theoretically predicted symmetry breaking in neurons with different neurite counts.Each color series indicates a different neurite count, as listed in the legend. A, Experimental measurements of neuronal polarity as a function of time and neurite count. Dashed lines separate data from different discrete time points. Bars indicate mean plus/minus SE, and neurite counts at each time point are only shown if at least 3 neurons had that neurite count at that time point. B–D, Computationally predicted polarity vs. time curves for neurons with different neurite counts using the Samuels (B), Fivaz (C), and Toriyama (D) models. E, Computationally predicted polarity vs. time curves for neurons with different neurite counts using a modified version of the Fivaz model in which HRas expression is independent of neurite count. The original Fivaz model, in which HRas expression increases with neurite count, is shown in C.
Mentions: We next experimentally determined whether neurons with different neurite counts polarize synchronously or asynchronously. At each time point, with the lone exception at 40.5 h after plating, we observed no statistical difference among the polarities of neurons with different neurite counts (p > 0.05 by ANOVA, Fig. 3A). We also found that there was no significant correlation (p > 0.01 by Pearson correlation) between neurite count and polarity at any of the time points, including the 40.5 h time point.

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