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Autonomous right-screw rotation of growth cone filopodia drives neurite turning.

Tamada A, Kawase S, Murakami F, Kamiguchi H - J. Cell Biol. (2010)

Bottom Line: We have developed a technique for monitoring three-dimensional motility of growth cone filopodia and demonstrate that an individual filopodium rotates on its own longitudinal axis in the right-screw direction from the viewpoint of the growth cone body.Furthermore, we provide evidence that the unidirectional rotation of filopodia causes deflected neurite elongation, most likely via asymmetric positioning of the filopodia onto the substrate.Although the growth cone itself has been regarded as functionally symmetric, our study reveals the asymmetric nature of growth cone motility.

View Article: PubMed Central - HTML - PubMed

Affiliation: Laboratory for Neuronal Growth Mechanisms, RIKEN Brain Science Institute, Wako, Saitama 351-0198, Japan. tamada@brain.riken.jp

ABSTRACT
The direction of neurite elongation is controlled by various environmental cues. However, it has been reported that even in the absence of any extrinsic directional signals, neurites turn clockwise on two-dimensional substrates. In this study, we have discovered autonomous rotational motility of the growth cone, which provides a cellular basis for inherent neurite turning. We have developed a technique for monitoring three-dimensional motility of growth cone filopodia and demonstrate that an individual filopodium rotates on its own longitudinal axis in the right-screw direction from the viewpoint of the growth cone body. We also show that the filopodial rotation involves myosins Va and Vb and may be driven by their spiral interactions with filamentous actin. Furthermore, we provide evidence that the unidirectional rotation of filopodia causes deflected neurite elongation, most likely via asymmetric positioning of the filopodia onto the substrate. Although the growth cone itself has been regarded as functionally symmetric, our study reveals the asymmetric nature of growth cone motility.

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Correlation between filopodial dynamics and neurite turning. (A) A scatter plot of the curvature of neurites (data in Fig. 6 E) versus the angular velocity of filopodia (data in Fig. 5 A) expressing the indicated transgene products. The correlation was statistically significant (P < 0.05). (B) A scatter plot of the curvature of neurites (data in Fig. 6 E) versus the velocity of filopodia (data in Fig. 5 B). The correlation was statistically significant (P < 0.01). (A and B) The broken lines show the linear regression fit of the data. (C) A scatter plot of the curvature of neurites (data in Fig. 6 E) versus the length of neurites (data in Fig. 6 F). The correlation was not statistically significant (P = 0.47).
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fig7: Correlation between filopodial dynamics and neurite turning. (A) A scatter plot of the curvature of neurites (data in Fig. 6 E) versus the angular velocity of filopodia (data in Fig. 5 A) expressing the indicated transgene products. The correlation was statistically significant (P < 0.05). (B) A scatter plot of the curvature of neurites (data in Fig. 6 E) versus the velocity of filopodia (data in Fig. 5 B). The correlation was statistically significant (P < 0.01). (A and B) The broken lines show the linear regression fit of the data. (C) A scatter plot of the curvature of neurites (data in Fig. 6 E) versus the length of neurites (data in Fig. 6 F). The correlation was not statistically significant (P = 0.47).

Mentions: To test whether right-screw filopodial rotation is associated with rightward neurite turning on 2D substrates, we analyzed the relationship between these two forms of motile behavior. We compared the neurite curvature (Fig. 6 E) with either the filopodial angular velocity (Fig. 5 A) or the filopodial velocity (Fig. 5 B). There was a linear correlation between the filopodial angular velocity and the neurite curvature (Fig. 7 A), indicating that a neurite turns more sharply when filopodia rotate more quickly. We also found a linear correlation between the filopodial velocity and the neurite curvature (Fig. 7 B), with the velocity values reflecting not only the rotation but also the random movement of filopodia. These results are consistent with our hypothesis that the right-screw rotation of filopodia drives the rightward turning of neurites on 2D substrates.


Autonomous right-screw rotation of growth cone filopodia drives neurite turning.

Tamada A, Kawase S, Murakami F, Kamiguchi H - J. Cell Biol. (2010)

Correlation between filopodial dynamics and neurite turning. (A) A scatter plot of the curvature of neurites (data in Fig. 6 E) versus the angular velocity of filopodia (data in Fig. 5 A) expressing the indicated transgene products. The correlation was statistically significant (P < 0.05). (B) A scatter plot of the curvature of neurites (data in Fig. 6 E) versus the velocity of filopodia (data in Fig. 5 B). The correlation was statistically significant (P < 0.01). (A and B) The broken lines show the linear regression fit of the data. (C) A scatter plot of the curvature of neurites (data in Fig. 6 E) versus the length of neurites (data in Fig. 6 F). The correlation was not statistically significant (P = 0.47).
© Copyright Policy - openaccess
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC2819689&req=5

fig7: Correlation between filopodial dynamics and neurite turning. (A) A scatter plot of the curvature of neurites (data in Fig. 6 E) versus the angular velocity of filopodia (data in Fig. 5 A) expressing the indicated transgene products. The correlation was statistically significant (P < 0.05). (B) A scatter plot of the curvature of neurites (data in Fig. 6 E) versus the velocity of filopodia (data in Fig. 5 B). The correlation was statistically significant (P < 0.01). (A and B) The broken lines show the linear regression fit of the data. (C) A scatter plot of the curvature of neurites (data in Fig. 6 E) versus the length of neurites (data in Fig. 6 F). The correlation was not statistically significant (P = 0.47).
Mentions: To test whether right-screw filopodial rotation is associated with rightward neurite turning on 2D substrates, we analyzed the relationship between these two forms of motile behavior. We compared the neurite curvature (Fig. 6 E) with either the filopodial angular velocity (Fig. 5 A) or the filopodial velocity (Fig. 5 B). There was a linear correlation between the filopodial angular velocity and the neurite curvature (Fig. 7 A), indicating that a neurite turns more sharply when filopodia rotate more quickly. We also found a linear correlation between the filopodial velocity and the neurite curvature (Fig. 7 B), with the velocity values reflecting not only the rotation but also the random movement of filopodia. These results are consistent with our hypothesis that the right-screw rotation of filopodia drives the rightward turning of neurites on 2D substrates.

Bottom Line: We have developed a technique for monitoring three-dimensional motility of growth cone filopodia and demonstrate that an individual filopodium rotates on its own longitudinal axis in the right-screw direction from the viewpoint of the growth cone body.Furthermore, we provide evidence that the unidirectional rotation of filopodia causes deflected neurite elongation, most likely via asymmetric positioning of the filopodia onto the substrate.Although the growth cone itself has been regarded as functionally symmetric, our study reveals the asymmetric nature of growth cone motility.

View Article: PubMed Central - HTML - PubMed

Affiliation: Laboratory for Neuronal Growth Mechanisms, RIKEN Brain Science Institute, Wako, Saitama 351-0198, Japan. tamada@brain.riken.jp

ABSTRACT
The direction of neurite elongation is controlled by various environmental cues. However, it has been reported that even in the absence of any extrinsic directional signals, neurites turn clockwise on two-dimensional substrates. In this study, we have discovered autonomous rotational motility of the growth cone, which provides a cellular basis for inherent neurite turning. We have developed a technique for monitoring three-dimensional motility of growth cone filopodia and demonstrate that an individual filopodium rotates on its own longitudinal axis in the right-screw direction from the viewpoint of the growth cone body. We also show that the filopodial rotation involves myosins Va and Vb and may be driven by their spiral interactions with filamentous actin. Furthermore, we provide evidence that the unidirectional rotation of filopodia causes deflected neurite elongation, most likely via asymmetric positioning of the filopodia onto the substrate. Although the growth cone itself has been regarded as functionally symmetric, our study reveals the asymmetric nature of growth cone motility.

Show MeSH
Related in: MedlinePlus