Mechano-electrical vibrations of microtubules—Link to subcellular morphology
Introduction
In spite of tremendous merit of biochemical approach, our understanding to how does the organism develop and regulate its shape and maintain its functionality is still vague. Thus, while new genetic signalling and regulation pathways are being discovered, underlying mechanism, which maintain biochemical processes extraordinarily organised in time and space, remains unknown. It is, nevertheless, evident that whatever these pathways and background mechanisms are they must result in a force acting on a matter. For that reason, we believe, the issue of morphogenesis is indeed also an issue of physics, as may be supported by works on self-organisation (Karsenti, 2008, Lehn, 2002), although they have not yet exceeded systems of several supramolecules and broader time span. Large scale coherence of biological systems, together with extraordinary variability, suggests itself an action of mechanism with longer rage than that of chemical interactions driven by thermal fluctuations. In following we will hypothesise that oscillating electric field generated by mechanical oscillations of electrically polar structures in cells – particularly microtubules – may play significant role in morphogenesis and physiology.
The reason why do we focus on oscillating electric field instead of electrostatic one is that electrostatics of biomaterials is already well explored and understood (Simonson, 2003). And more importantly, oscillating electric field seems to be more efficient for signal propagation and long range interactions under physiological conditions (Cifra et al., 2010a) because, in contrast to electrostatic field, the screening by ions takes place to lesser extent at higher frequencies.
Spontaneous mechanical oscillations of biocomponents on different levels, to which we devote Section 2, were predicted and experimentally proven. As almost all proteins and protein-composed structures are electrically polar, mechanical oscillations of the charge bound in their structure will generate oscillating electric field. Mechanical oscillations themselves have morphogenetic significance (see Kruse and Riveline, 2011 and Section 3 of this paper) but coupled electric field may potentiate this relevance even more (see Section 4). We demonstrate this idea on the conformation of two microtubules, for which we calculated electric field generated by axial longitudinal vibrations of each micrtotubule. Namely we analyse the intensity of electric field and its possibility to act on molecules under physiological conditions (Section 5). Results presented here expand on our previous work dedicated to microtubule vibrations (Cifra et al., 2010b, Havelka et al., 2011a).
Section snippets
Spontaneous mechanical oscillations in cells
In this section, starting with brief introduction to the topic, we review the phenomenon of spontaneous mechanical oscillations in cells on different levels.
Mechanics of biological object – whether it is a protein, organelle, cell, or a tissue – has gained importance since measurement and manipulation of biological samples on the scale of micro and nanometres has became technologically feasible. Besides measurement of passive mechanical properties and question of how do cells actively respond
Role of mechanical oscillations in morphogenesis
There is no doubt about the function of oscillations of specialised cells like cardiomyocytes, hair cells or others. The importance of oscillations of specialised sub cellular structures, like axoneme, is well understood too. However, there is a plenty of oscillations on both cellular and sub cellular level which biological relevance (or even generating mechanism) is not clear. This is, for instance, the case of oscillations of yeast's cell wall (Pelling et al., 2004a, Pelling et al., 2004b),
Electrical oscillations in living matter
Existence of electric field is coupled to electric charge. Almost all proteins are electrically polar4 and electrostatic properties of proteins oftentimes play essential role in their function. Interaction between proteins or protein–ligand interactions are often of electrostatic nature because they involve
Mechano-electrical vibrations of microtubules
Microtubules (MTs) constitute important part of eukaryotic cytoskeleton. In contrast to the skeleton of a body, cytoskeleton is not only a mechanical support of the cell but also an active network responsible for self-organisation of a cell. MTs are present in a cell most frequently in the form of single cylindrical tubes (inner diameter 17 nm and outer diameter 25 nm) consisting of 13 protofilaments (see Fig. 2). More complicated shapes are also possible; however, the protofilament is their
Implications for experiments
The very first thought of results presented here naturally leads to the possibility of their experimental verification. As we have already mentioned, no experimental work unifying mechanical and electrical vibrations of supramolecules has been published yet. In the case of electrical oscillations, there have however been reports of resonant interaction of MTs with external oscillating electric field. This indicates the existence of oscillation states in MTs alone (Sahu et al., in press).
Some
Conclusions
In this paper, we reviewed spontaneous mechanical oscillations in cells and discussed them as a feeding of mechano-electrical vibrations of microtubule. We demonstrated calculations of generated oscillating electric field and we speculated about its role in morphogenesis. The model we used is simplified, and also very special case of physical reality. Our results however, together with recent experimental findings (Sahu et al., in press), indicate that the effect of generated electric field is
Contributions
OK designed the research and wrote the paper and DH performed calculations.
Acknowledgments
We would like to thank M. Cifra, D. Fels, and J. Pokorný for valuable discussions and suggestions which helped us to improve the manuscript.
Research presented in this paper was supported by the Czech Science Foundation, GA CR, grant no. P102/11/0649, and the Grant Agency of the Czech Technical University in Prague, grant nos. SGS10/179/OHK3/2T/13 and SGS12/071/OHK3/1T/13.
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