MT Sensory Transduction Atema

Several authors have discussed the transduction of sensory information by the mechanical distortion of cilia: membrane covered centriole-like structures which protude from cells. Lowenstein, Osborne, and Warshall (1964) suggested that the "kinocilium" of the hair cells in the inner ear served as motile cilia in reverse. They reasoned that motile cilia produced movement using chemical energy provided by ATP hydrolysis, so mechanoreceptor cilia should transduce mechanical deformation caused by environmental stimuli to provide the cell with "patterns of chemical energy representing information." Lettvin and Gestalind

(1965) also proposed that receptor cilia operated "by virtue of transmitting mechanical signals to the base of the cilium."

Biologist Jelle Atema (1973) of the Wood's Hole Oceanographic Institute, whose work had focused on acoustical perception at the cellular level, also linked microtubules and sensory transduction. Noting common cilia-like structure in sensory receptor organelles among a wide variety of organisms, Atema proposed that sensory cilia conveyed environmental information to the rest of the cell. He suggested that transduction occurred by propagated conformational changes in the microtubule subunits which constituted these cilia. He argued that microtubules were active functional units in reception and transduction of sensory information.

Atema reviewed conformational changes in MT tubulin subunit dimers observed by a variety of authors and suggested that these occurred under physiological conditions. For example, oscillations of sperm flagella are apparently not controlled by their cell membrane but rather are direct properties of their microtubules in the presence of ATP (Lindemann and Rikmensboel, 1972). Atema concluded that a sequence of subunit conformational changes is likely to occur in microtubules. In motor cilia and flagella, the distortion would originate at the base of the structure and be propagated distally, resulting in wavelike or whiplike motions which propel the organism. In sensory cilia, the distortion apparently originates near the distal end of the ciliary MT and propagates in either direction or at least proximally towards the cell body. There the signal may propagate via either an excitable membrane or through the anchoring basal body and cytoskeleton. Because mechanical deformation and/or local chemical distortion are sufficient stimuli to start a propagating signal in sensory cilia, Atema's microtubule theory assumed that distortion of tubulin conformation by any number of sources was sufficient to propagate a conformational wave. Thus light energy, chemical bond energy, and mechanical forces could be transduced by sensory cilia.

Atema's view of MT information processing was an "all or none" propagation by allosteric conformational changes along tubulin protofilaments. His was the first theory to look beyond the global behavior of cilia to consider conformational effects in tubulin components. Subsequent theories became more elaborate to consider localized analog functions, switching, and collective neighbor interactions among MT subunits.

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