Are microtubules the 'nerves' of the cell?

[See ref 10, ref 20 ]

A most important required step towards the concept of an 'intelligent' cell is to identify the specific structures and mechanisms which mediated between the light detection at the cell center on one hand and the extension of specific pseudopodia at the peripheral cellular cortex on the other. The mediator mechanism could not be explained by diffusible, chemical signals. Such signals would travel into every possible direction and, thus, would not be able to specify a particular direction for the extension of a pseudopodium. Therefore, the signals had to be confined to individual tracks that connected the cell center with specific locations of the cell periphery. The most promising candidate for this function seemed to be the microtubules.

As shown in the micrograph above, the microtubules radiate away from the center of the centrosome. Originating at this center they lead unbranchingly to the cellular cortex which contains the autonomously motile microplast domains. The situation is very reminiscent of nerves connecting the brain (centrosome) to a set of muscles (microplasts). The image shows some fuzzy spots in the center which are grazing sections of the microtubule organizing centers near the centrioles which we consider the eyes of the cell.

Another line of arguments to support microtubules as good candidates for cellular 'nerves' comes from experiments that interfere with microtubules: If anti-microtubular drugs are given to the cell it can still move all parts of its body, but the remarkable coordination of the typical shape changes is lost. This led to the following question. Are any signals, indeed, propagated along the microtubules to the cell cortex in response to pulsating near-infrared light? If so, how can they be detected?

Experimental strategies to identify changes of microtubules during a putative signal transmission.

Signal transmission is unlikely to drastically change the microtubule structure.

If microtubules, indeed, conduct such signals one could hardly expect them to cause structural changes of the microtubules drastic enough to be visible in a microscope. Such an expectation would be analogous to the search for structural changes of the optical nerve every time the retina transmits images to the brain. Nevertheless, for several years I tried but failed to find any direct effects of pulsating near-infrared light signals on microtubules or other cytoskeletal components.

Signal transmission may alter the effectiveness of anti-microtubular drugs.

Consequently, I took an indirect approach. If the putative signals themselves had no direct effect on the structure of microtubules, I hypothesized that they might enhance or diminish the effects of some other agent that was known to change the structure of microtubules. For example, it seemed possible that the traveling signals were strong enough to alter the speed of disassembly of microtubules which were exposed to an anti-microtubular drug. Therefore, I measured the stability of cytoplasmic microtubules in the presence of nocodazole while exposing the entire cell culture to pulsating near-infrared signals.

Disassembly of cytoplasmic asters ('DCA') of CV1 cells.

Therefore, I wrote a program to measure the microtubules in a cell while they were disassembled by the anti-microtubular drug nocodazole. The figure below shows a typical example of the way the program turns the fluorescent patterns of microtubules (panel a) into a set of labeled pixels (panel b) that can be counted.

The experiments used an epithelial cell line called CV1 cells. They were exposed to pulsating infrared light while at the same time the microtubules were disassembled by nocodazole. I found that pulsating infrared light accelerated the disassembly of the microtubules or, to put it another way, it destabilized them. The figure below shows microtubules being disassembled by nocodazole in the dark (panel a) and in the presence of pulsating infrared light (panel b).

Obviously, there are fewer microtubules in panel b: the disassembly by nocodazole has progressed further due to the light pulses. It is easy to show that heating of the cells has nothing to do with it. For example the describeed destabilization of the microtubules is strictly wavelength dependent, as shown in the spectrum below.

Wavelength dependence of the destabilization of the microtubules of CV1 cells (ordinate percent difference between unirradiated and irradiated cells; rectangular pulses; pulse length = 1 [s]; intensity = 4 [µW]; average sample size: 2340 cells/ data point (range 1270 - 5060 cells/ data point). The error bars show the errors of the mean.
The spectrum is remarkably similar to the action spectrum of the cellular detection of infrared light sources.

Significance for cell intelligence:

In response to exogenous signals the centrosome may send destabilizing signals along its radial array of microtubules.
Neither microtubules nor the drug (nocodazole) are sensitive to infrared light. If the light pulses destabilized the microtubules it had to be an indirect effect caused by some other cellular component which is light sensitive and connected to the microtubules. Based on our previous data, this component had to be the pair of centrioles embedded inside the centrosome. In other words, after receiving the light pulses the centrosome destabilizes the radial array of microtubules which run towards the cell cortex which, in turn , will subsequently extend special pseudopodia to the light sources. Therefore, it seems that the observed destabilization is the signal that is propagated along the microtubles like along 'nerves'.

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