Efficiency of organelle capture by microtubules as a function of centrosome nucleation capacity: general theory and the special case of polyspermia

Transport of organelles along microtubules is essential for the cell metabolism and morphogenesis. The presented analysis derives the probability that an organelle of a given size comes in contact with the microtubule aster. The question is asked how this measure of functionality of the microtubule...

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Bibliographic Details
Published in:PloS one 2012-05, Vol.7 (5), p.e37675-e37675
Main Author: Maly, Ivan V
Format: Article
Language:English
Subjects:
Algorithms
Analysis
Beroe ovata
Biology
Cell cycle
Centrosome - metabolism
Computer Science
Cytoskeleton
Design of experiments
Eggs
Female
Fertilization
Fertilization - physiology
Humans
Male
Metabolism
Microscopy
Microsurgery
Microtubules
Microtubules - metabolism
Models, Biological
Morphogenesis
Nonlinear systems
Nucleation
Organelles
Organelles - metabolism
Physics
Physiological aspects
Polymerization
Pronucleus
Proteins
Sperm
Spermatozoa - metabolism
Stochastic models
Transport
Tubulin
Xenopus
Zygote - metabolism
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Summary:Transport of organelles along microtubules is essential for the cell metabolism and morphogenesis. The presented analysis derives the probability that an organelle of a given size comes in contact with the microtubule aster. The question is asked how this measure of functionality of the microtubule aster is controlled by the centrosome. A quantitative model is developed to address this question. It is shown that for the given set of cellular parameters, such as size and total tubulin content, a centrosome nucleation capacity exists that maximizes the probability of the organelle capture. The developed general model is then applied to the capture of the female pronucleus by microtubules assembled on the sperm centrosome, following physiologically polyspermic fertilization. This application highlights an unintuitive reflection of nonlinearity of the nucleated polymerization of the cellular pool of tubulin. The prediction that the sperm centrosome should lower its nucleation capacity in the face of the competition from the other sperm is a stark illustration of the new optimality principle. Overall, the model calls attention to the capabilities of the centrosomal pathway of regulation of the transport-related functionality of the microtubule cytoskeleton. It establishes a quantitative and conceptual framework that can guide experiment design and interpretation.
ISSN:1932-6203
1932-6203
DOI:10.1371/journal.pone.0037675