The Onset of Collective Behavior in Social Amoebae

Abstract

In the social amoebae Dictyostelium discoideum, periodic synthesis and release of extracellular cyclic AMP (cAMP) guides cell aggregation and commitment to form fruiting bodies. It is unclear whether these oscillations represent an intrinsic property of individual cells or if they only exist as a population-level phenomenon. Here we show by live-cell imaging of intact cell populations that pulses originate from a discrete location despite constant exchange of cells to and from the region. In a perfusion chamber, both isolated single cells and cell populations switch from quiescence to rhythmic activity depending on the level of extracellular cAMP. A quantitative analysis shows that stochastic pulsing of individual cells below the threshold concentration of extracellular cAMP plays a critical role in the onset of collective behavior.

Progress and perspectives in signal transduction, actin dynamics, and movement at the cell and tissue level: lessons fromDictyostelium

“…These processes have been modelled to a great extent and the main features are understood in some considerable detail [32,[81][82][83][84][85][86] ( figure 10). Initially, the cAMP waves were measured in fixed time points using an ingenious isotope dilution strategy, but more recently it has been possible to measure the cAMP waves dynamically using dedicated FRET constructs [87,88]. Interesting questions that can now be started to be resolved are what is the exact mechanism of cAMP amplification in single cells?…”

Migration of cells in a social context

“…These studies revealed useful information on cell migration, but because in general the relevant interactions in a social context and their relative importance are not established, migratory behavior of cells in a social context remains as one of the major unresolved problems in biology (30). Furthermore, striking social effects such as highly sensitive collective responses in a number of sensing systems [e.g., quorum sensing (31,32) and onset of collective behavior in Dictyostelium discoideum (33)] mediated by increased levels of cell-secreted signals in higher cell density indicate that mechanical links are not necessary for collective behavior. At the subcellular level, many types of nonswimming motile cells involved in multicellular biology [e.g., fibroblasts, Dictyostelium, and neutrophils (13,14,(16)(17)(18)] have been found to transmit traction force to the substrate by intracellularly polymerizing their cytoskeletons in dynamically formed membrane protrusions known as pseudopodia.…”

Organization of early frog embryos by chemical waves emanating from centrosomes

“…It requires an excitable medium that locally amplifies a chemical state so the state can propagate through the medium faster than diffusion. Familiar examples include the Belousov-Zhabotinsky reaction [5], action potential in neurons [6], calcium waves during fertilization [7] and cAMP waves in a population of Dictyostelium cells [8,9]. Microtubule organization and cell cycle progression are not normally considered as chemical waves, apart from a few notable exceptions [10 -13].…”