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Robust patterns in the stochastic organization of filopodia.

Husainy AN, Morrow AA, Perkins TJ, Lee JM - BMC Cell Biol. (2010)

Bottom Line: Filopodia are highly dynamic structures that show a rich diversity in appearance and behavior.While there are several mathematical models of filopodia initiation and growth, testing the capacity of these theoretical models in predicting empirical behavior has been hampered by a surprising shortage of quantitative data related to filopodia.Neither is it clear how quantitatively robust the cellular filopodial network is and how perturbations alter it.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Biochemistry, Microbiology & Immunology, University of Ottawa, 451 Smyth Road, Ottawa, Ontario K1H 8M5, Canada.

ABSTRACT

Background: Filopodia are actin-based cellular projections that have a critical role in initiating and sustaining directional migration in vertebrate cells. Filopodia are highly dynamic structures that show a rich diversity in appearance and behavior. While there are several mathematical models of filopodia initiation and growth, testing the capacity of these theoretical models in predicting empirical behavior has been hampered by a surprising shortage of quantitative data related to filopodia. Neither is it clear how quantitatively robust the cellular filopodial network is and how perturbations alter it.

Results: We have measured the length and interfilopodial separation distances of several thousand filopodia in the rodent cell line Rat2 and measured these parameters in response to genetic, chemical and physical perturbation. Our work shows that length and separation distance have a lognormal pattern distribution over their entire detection range (0.4 μm to 50 μm).

Conclusions: We find that the lognormal distribution of length and separation is robust and highly resistant to perturbation. We also find that length and separation are independent variables. Most importantly, our empirical data is not entirely in agreement with predictions made based on existing theoretical models and that filopodial size and separation are an order of magnitude larger than what existing models suggest.

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Filopodia length and distance separation are independent after perturbation. Graph of filopodial length and separation distance for PI4KIIIβ, Bradykinin and Poly-D-lysine perturbations. Identically coloured data points represent measurements from the same cell.
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Figure 6: Filopodia length and distance separation are independent after perturbation. Graph of filopodial length and separation distance for PI4KIIIβ, Bradykinin and Poly-D-lysine perturbations. Identically coloured data points represent measurements from the same cell.

Mentions: Lastly, we chose to analyze the relationship between length and separation distance in the perturbed cells. Figure 6 shows this relationship, plotted on a log-log scale, for all three perturbations. In the case of bradykinin and poly-D lysine, there was no obvious relationship between length and separation. In this respect, these two perturbations do not cause changes from the wild-type situation. In the case of PI4KIIIβ expression, there is a weak, albeit statistically significant, positive correlation (r~0.39). This appears to result from two individual cells (coloured black and purple) with very long and highly separated filopodia. Filopodia length and separation are not highly correlated in these two cells, but the magnitude of the length and separation measurements leads to an apparent correlation in the overall population. As such, we conclude that length and filopodial separation remain independent variables even following perturbation.


Robust patterns in the stochastic organization of filopodia.

Husainy AN, Morrow AA, Perkins TJ, Lee JM - BMC Cell Biol. (2010)

Filopodia length and distance separation are independent after perturbation. Graph of filopodial length and separation distance for PI4KIIIβ, Bradykinin and Poly-D-lysine perturbations. Identically coloured data points represent measurements from the same cell.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2992051&req=5

Figure 6: Filopodia length and distance separation are independent after perturbation. Graph of filopodial length and separation distance for PI4KIIIβ, Bradykinin and Poly-D-lysine perturbations. Identically coloured data points represent measurements from the same cell.
Mentions: Lastly, we chose to analyze the relationship between length and separation distance in the perturbed cells. Figure 6 shows this relationship, plotted on a log-log scale, for all three perturbations. In the case of bradykinin and poly-D lysine, there was no obvious relationship between length and separation. In this respect, these two perturbations do not cause changes from the wild-type situation. In the case of PI4KIIIβ expression, there is a weak, albeit statistically significant, positive correlation (r~0.39). This appears to result from two individual cells (coloured black and purple) with very long and highly separated filopodia. Filopodia length and separation are not highly correlated in these two cells, but the magnitude of the length and separation measurements leads to an apparent correlation in the overall population. As such, we conclude that length and filopodial separation remain independent variables even following perturbation.

Bottom Line: Filopodia are highly dynamic structures that show a rich diversity in appearance and behavior.While there are several mathematical models of filopodia initiation and growth, testing the capacity of these theoretical models in predicting empirical behavior has been hampered by a surprising shortage of quantitative data related to filopodia.Neither is it clear how quantitatively robust the cellular filopodial network is and how perturbations alter it.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Biochemistry, Microbiology & Immunology, University of Ottawa, 451 Smyth Road, Ottawa, Ontario K1H 8M5, Canada.

ABSTRACT

Background: Filopodia are actin-based cellular projections that have a critical role in initiating and sustaining directional migration in vertebrate cells. Filopodia are highly dynamic structures that show a rich diversity in appearance and behavior. While there are several mathematical models of filopodia initiation and growth, testing the capacity of these theoretical models in predicting empirical behavior has been hampered by a surprising shortage of quantitative data related to filopodia. Neither is it clear how quantitatively robust the cellular filopodial network is and how perturbations alter it.

Results: We have measured the length and interfilopodial separation distances of several thousand filopodia in the rodent cell line Rat2 and measured these parameters in response to genetic, chemical and physical perturbation. Our work shows that length and separation distance have a lognormal pattern distribution over their entire detection range (0.4 μm to 50 μm).

Conclusions: We find that the lognormal distribution of length and separation is robust and highly resistant to perturbation. We also find that length and separation are independent variables. Most importantly, our empirical data is not entirely in agreement with predictions made based on existing theoretical models and that filopodial size and separation are an order of magnitude larger than what existing models suggest.

Show MeSH
Related in: MedlinePlus