Pigmented cells in vertebrate dermis are being studied by several laboratories as a model for intracellular organelle transport. Fish and amphibians possess specialized cells, called melanophores, which contain hundreds of melanin-filled pigment granules, termed melanosomes. The sole function of these cells is pigment aggregation in the center of the cell or dispersion throughout the cytoplasm. This alternative transport of pigment allows the animal to effect color changes important for camouflage and social interactions. Melanophores transport their pigment in response to extracellular cues: neurotransmitters in the case of fish and hormonal stimuli in the case of frogs. In both cases, melanosome dispersion is induced by elevation of intracellular cAMP levels, while aggregation is triggered by depression of cAMP. The regulatory mechanisms downstream of these second-messengers are poorly understood.

Early studies of pigment transport in melanophores established a role for microtubules. Reconstitution of melanosome motility along microtubules in vitro demonstrated the presence of two distinct motor activities of opposite polarity. Using a dominant negative approach, our laboratory subsequently identified the microtubule plus-end directed motor responsible for pigment dispersion as the heterotrimeric Kinesin-2 (formerly kinesin-II or KRP85/95) (Tuma et al., 1998). Cytoplasmic dynein has also been shown to carry melanosomes to the cell center during aggregation (Nilsson and Wallin, 1997).

It was recently demonstrated that pigment in fish melanophores is transported along actin filaments in vivo and that filamentous actin and melanosomes are closely associated (Rodionov. et al., 1998). Concurrently, our laboratory reconstituted melanosome motility along actin filaments in vitro and tentatively identified the motor attached to melanosomes as myosin V (Rogers and Gelfand, 1998). The model that has evolved from these observations is that melanosomes are transported across long distances via microtubules in both types of cells, while actin-based transport is probably utilized to achieve uniform distribution of pigment throughout the cell. Work with melanophores points to cooperation between microtubule- and actin-based transport for several types of organelles.

Mammalian melanocytes also produce melanosomes but, unlike melanophores, pigment in these cells is transported to the cell periphery for subsequent exocytosis to surrounding epithelial cells. Analysis of dilute, a naturally occurring mouse mutant exhibiting coat-color defects, showed that the unconventional myosin, myosin V, is essential for melanosome movement. Recently, video microscopic analysis revealed that a microtubule-based component is involved in pigment transport in melanocytes (Wu et al., 1998), as in melanophores. These findings underscore the importance of interplay between actin- and microtubule-based organelle motility.

Contributed by V. Gelfand and S. Rogers

Recent references

Nilsson, H. and Wallin, M. 1997. Evidence for several roles of dynein in pigment transport in melanophores. Cell Motil. Cytoskel. 38: 397-409.

Tuma, M., Zill, A., LeBot, N., Vernos, I., and Gelfand, V. 1998. Heterotrimeric kinesin II is the motor responsible for pigment dispersion in Xenopus melanophores. J. Cell Biol. 143: 1547-1558.

Wu, X., B. Bowers, K. Rao, Q. Wei, and J. Hammer. 1998. Visualization of melanosome dynamics within wild-type and dilute melanocytes suggests a paradigm for myosin V function in vivo. J. Cell Biol. 143:1899-1918.

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