Functional coordination of microtubule-based and actin-based motility in melanophores

The fish melanophore has been considered the exemplar of microtubule-based organelle transport. In this system, a radial array of uniformly polarized microtubules [1] provides a framework on which dynein-related and kinesin-related motors drive pigment granules toward the minus or plus ends, respectively [2-4]. Stimulation of minus-end motors accounts satisfactorily for aggregation of granules at the cell center. Rapid dispersion is clearly microtubule-dependent; however, the uniform distribution of granules throughout the cytoplasm is paradoxical because stimulation of plus-end motors is predicted to drive the granules to the cell margin. This paradox suggested that the transport system was incompletely understood. Here, we report the discovery of a microtubule-independent motility system in fish melanophores. The system is based on actin filaments and is required for achieving uniform distribution of pigment granules. When it is abrogated, granules accumulate at the cell's margin as predicted for microtubule plus-end motors acting alone. The results presented here demonstrate the functional coordination of microtubule and actin filament systems, a finding that may be of general significance for organelle motility in cytoplasm.