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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 distribution is unimodal and best fits a lognormal model. (A) Histogram of all the filopodia lengths (n = 1,682), and independent experiments 1, 2 and 3 with n = 745, n = 573 and n = 364 respectively. (B) Empirical cumulative distribution functions (CDFs) of lengths with the lognormal and other statistical models for all the experiments combined and each independent experiment 1, 2 and 3. (C) Empirical PDFs and CDFs of filopodia lengths for 53 cells.
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Figure 2: Filopodia length distribution is unimodal and best fits a lognormal model. (A) Histogram of all the filopodia lengths (n = 1,682), and independent experiments 1, 2 and 3 with n = 745, n = 573 and n = 364 respectively. (B) Empirical cumulative distribution functions (CDFs) of lengths with the lognormal and other statistical models for all the experiments combined and each independent experiment 1, 2 and 3. (C) Empirical PDFs and CDFs of filopodia lengths for 53 cells.

Mentions: We compiled filopodia length measurements from three independent experiments. We counted filopodia from a total of 52 Rat2 cells (experiment 1 = 25; experiment 2 = 18; experiment 3 = 10). The total number of filopodia was 1,682 (experiment 1 = 745; experiment 2 = 573; experiment 3 = 364). As shown in Figure 2A, filopodia distribution in the total data set is unimodal with a mean of 2.70 μm. The length distribution of the individual experiments was also unimodal with a respective mean of 2.79 μm, 2.49 μm, and 2.84 μm for Experiments 1, 2 and 3. Approximately 82% of the filopodia fall within the range of 1 μm to 10 μm in length.


Robust patterns in the stochastic organization of filopodia.

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

Filopodia length distribution is unimodal and best fits a lognormal model. (A) Histogram of all the filopodia lengths (n = 1,682), and independent experiments 1, 2 and 3 with n = 745, n = 573 and n = 364 respectively. (B) Empirical cumulative distribution functions (CDFs) of lengths with the lognormal and other statistical models for all the experiments combined and each independent experiment 1, 2 and 3. (C) Empirical PDFs and CDFs of filopodia lengths for 53 cells.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 2: Filopodia length distribution is unimodal and best fits a lognormal model. (A) Histogram of all the filopodia lengths (n = 1,682), and independent experiments 1, 2 and 3 with n = 745, n = 573 and n = 364 respectively. (B) Empirical cumulative distribution functions (CDFs) of lengths with the lognormal and other statistical models for all the experiments combined and each independent experiment 1, 2 and 3. (C) Empirical PDFs and CDFs of filopodia lengths for 53 cells.
Mentions: We compiled filopodia length measurements from three independent experiments. We counted filopodia from a total of 52 Rat2 cells (experiment 1 = 25; experiment 2 = 18; experiment 3 = 10). The total number of filopodia was 1,682 (experiment 1 = 745; experiment 2 = 573; experiment 3 = 364). As shown in Figure 2A, filopodia distribution in the total data set is unimodal with a mean of 2.70 μm. The length distribution of the individual experiments was also unimodal with a respective mean of 2.79 μm, 2.49 μm, and 2.84 μm for Experiments 1, 2 and 3. Approximately 82% of the filopodia fall within the range of 1 μm to 10 μm in length.

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