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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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Bright-field micrographs of four different neurons.Neurite count (N) and polarity (P) using Eq. (1) are also indicated for each neuron. A and B show examples of neurons with two neurites that are relatively more (A) or less (B) polarized. C and D similarly show neurons with many neurites that are relatively more (C) or less (D) polarized. The image in A was taken 28.5 h after plating, and B–D were taken at 52.5 h after plating. All scale bars are 25 µm.
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pone-0054905-g001: Bright-field micrographs of four different neurons.Neurite count (N) and polarity (P) using Eq. (1) are also indicated for each neuron. A and B show examples of neurons with two neurites that are relatively more (A) or less (B) polarized. C and D similarly show neurons with many neurites that are relatively more (C) or less (D) polarized. The image in A was taken 28.5 h after plating, and B–D were taken at 52.5 h after plating. All scale bars are 25 µm.

Mentions: We measured neurite lengths and polarities in two hundred E18 rat hippocampal neurons, cultured on glass coated with poly-D-lysine and laminin, at nine different time points over the course of two days. We introduce the following metric to quantify neuronal polarity of neurons with multiple neurites (see Methods):(1)where N is the neurite count, and x­i is the relative length of neurite i. Fig. 1 shows four different neurons, as well as their neurite counts and their polarities calculated using Eq. (1). For a discussion and justification of this metric, see the Materials and Methods section. We also verified that the neurons were functionally polarizing over this time scale by performing an immunocytochemical stain for axonal and dendritic markers (Fig. S1).


Synchronous symmetry breaking in neurons with different neurite counts.

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

Bright-field micrographs of four different neurons.Neurite count (N) and polarity (P) using Eq. (1) are also indicated for each neuron. A and B show examples of neurons with two neurites that are relatively more (A) or less (B) polarized. C and D similarly show neurons with many neurites that are relatively more (C) or less (D) polarized. The image in A was taken 28.5 h after plating, and B–D were taken at 52.5 h after plating. All scale bars are 25 µm.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0054905-g001: Bright-field micrographs of four different neurons.Neurite count (N) and polarity (P) using Eq. (1) are also indicated for each neuron. A and B show examples of neurons with two neurites that are relatively more (A) or less (B) polarized. C and D similarly show neurons with many neurites that are relatively more (C) or less (D) polarized. The image in A was taken 28.5 h after plating, and B–D were taken at 52.5 h after plating. All scale bars are 25 µm.
Mentions: We measured neurite lengths and polarities in two hundred E18 rat hippocampal neurons, cultured on glass coated with poly-D-lysine and laminin, at nine different time points over the course of two days. We introduce the following metric to quantify neuronal polarity of neurons with multiple neurites (see Methods):(1)where N is the neurite count, and x­i is the relative length of neurite i. Fig. 1 shows four different neurons, as well as their neurite counts and their polarities calculated using Eq. (1). For a discussion and justification of this metric, see the Materials and Methods section. We also verified that the neurons were functionally polarizing over this time scale by performing an immunocytochemical stain for axonal and dendritic markers (Fig. S1).

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