Biomechanical Events in the Production of Ciliary Movement

Abstract

Ciliary motility consists of a repetitive series of bends that are formed and propagated along the ciliary axoneme. It is clear that the axoneme, the cytoskeletal core of each motile cilium, that consists of the classic 9 + 2 arrangement of microtubules (cf. Sugrue et al., 1991), is responsible for the production of bending and bend propagation. The form of beat in living cilia is matched by that produced by isolated axonemes reactivated by ATP, sometimes with great fidelity. Cilia are found on many different cells of a great variety of single and multicellular organisms. They come in many lengths, ranging from about 5 to over 500 μm and numbers ranging from 1 to about 200 per cell. However, the diameter of the 9 + 2 axoneme is always the same, about 0.2 μm, suggesting that this is an important parameter for the production of motility. Ciliary bending is also variable, both with regard to amplitude and timing, and the same organelle can exhibit quite different kinds of beat, varying specifically in beat frequency, in overall form or in the spatial direction of net force production. An elegant example is given by sea urchin embryo cilia which spontaneously beat in two different directions - normal and reversed, and whose beat can be recorded and analyzed at high time resolution (Mogami et al., 1993). A second example is given by Chlamydomonas, whose so-called ‘flagella’ beat normally with a ciliary breast stroke, but which reverse, for example during a photophobic response, to beat with what is in effect, undulatory motion. In both of these examples, the motile mechanism of the axoneme remains unchanged, but it is controlled in specific ways, to give the appropriate changes in timing and bend amplitude. The controls work by means of second messengers, notably Ca²⁺ or cAMP, which act directly on axonemal constituents. Any explanation of the mechanism of motility needs to explain how it is possible to change flexural into undulatory motion and back again, or to change the direction of the effective stroke for a short while on a single cilium.