Kota Miura
Zoologisches Institut, Universität München, Germany,
Miura@zi.biologie.uni-muenchen.de
Amoebae of the cellular slime mould Dictyostelium discoideum normally live as single cells in forest litter and feed on bacteria. Starvation induces the transition from the unicellular stage to the multicellular stage. Chemotactic aggregation of up to 100,000 cells forms a multicellular mass which behaves as a single organism and ultimately transforms into a fruiting body consisting of a stalk and a spore head. Beginning 4 to 6 hours after removal of the food source individual amoebae start to aggregate in response to periodic cAMP (adenosine 3',5'-monophosphate) signals initiated at the center of aggregation and transmitted outward from cell to cell as a travelling wave of cAMP. In turn, these cAMP waves direct the coordinated inward movement of the amoebae by chemotaxis. Aggregation results in the formation of a migrating slug. During the slug stage, up to 10^5 cells coordinate their movement and migrate as a single organism. Slugs have a cylindrical shape with tip and tail; their morphological polarity corresponds to the polarity of migration. A large body of results suggest that cyclic AMP-mediated cell-cell signaling is the mechanism coordinating multicellular movement. Waves of cyclic AMP generated at the anterior tip propagate towards the tail and induce the chemotactic movement of cells toward the tip. Slugs exhibit highly sensitive environmental reactions: phototaxis, chemotaxis and thermotaxis. Although many studies have investigated how Dictyostelium slugs move toward a light source, the mechanism of phototaxis is still unclear. It has been known that slugs turn towards the light at the anterior end. In addition, previous research identified mutations and drug treatments that interfere with phototaxis but the strategy for analyzing phototaxis has been limited to low resolution both temporarily and spatially. Methods have been developed in my research to analyze phototactic behavior on two different scales, the slug level and cellular level. The analyses revealed dynamic features of slug behavior during phototaxis which have not been previously described. Following light irradiation slugs moved with approximately 50 percent higher speed; they showed prominent serpentine movement of their tip as if they were scanning and correcting migration direction; they elongated and decreased the diameter of their body; and their tip remained lifted off the substrate for long periods. The analysis of cell movement during phototactic turning showed that the cell movement pattern was unlike any predicted from earlier hypotheses. Some cells in the anterior zone moved away from the light source across the slug, thus increasing the volume on the 'dark' side ('asymmetric cell accumulation') and bending the anterior zone like a lever-arm toward the light source. Furthermore, it was discovered that light irradiation enhances secretion of cyclic AMP from the slug and that light interferes with cyclic AMP cell-cell signaling during other multicellular stages as well. A model for phototaxis has been proposed based on these results. Laterally irradiated light is focused on the distal side of the slug by a lens effect and locally induces cyclic AMP release. Some cells accumulate chemotactically on the side away from the light source and cause a bending of the anterior zone towards the light source. Since cell movement within the slug is organized by cyclic AMP waves, light induced cyclic AMP release interferes with the endogenous signaling pattern. The consequence is an overall change in the shape and the behavior of slug.