Three-dimensional scroll waves organize Dictyostelium slugs.

Abstract

To test the hypothesis that periodic signals and chemotaxis direct later morphogenesis in Dictyostelium discoideum, we investigated cell behavior and cell movement in slugs. Trails of neutral red-stained prestalk and anterior-like cells were recorded by high-resolution digital image processing. Neutral red-stained anterior-like cells in the prespore zone of slugs move straight forward in the direction of slug migration and, furthermore, show coherent periodic cell movement. In contrast, cells in the prestalk zone move along completely different trajectories. Prestalk cells move perpendicular to the direction of slug migration; that is, they rotate around the tip. The cell movement data show that the chemotactic signal in the slug propagates as a three-dimensional scroll wave in the prestalk zone and as a planar wave in the prespore zone. The different behavior of prestalk and prespore cells is most likely caused by a difference in the oscillatory properties of the two cell types. We provide evidence that the slug stage of Dictyostelium behaves like an excitable system and that a (twisted) scroll wave organizes slug formation and migration.The cellular slime mold Dictyostelium discoideum is well suited to the study of cellular communication and the role of biological oscillations in spatiotemporal pattern formation. During the life cycle, solitary amoebae collect to form a multicellular organism. This aggregation process is well characterized and occurs by chemotaxis to periodic cAMP signals initiated by the aggregation center (1). The cAMP pulses, generated and secreted by cells in the aggregation center, are detected and amplified by the monolayer of surrounding cells. This leads to the outward propagation of cAMP waves. The signal propagates as expanding concentric rings or, more often, as spirals (2). These waves direct the cells toward the aggregation center via chemotaxis toward increasing cAMP concentrations. Signal propagation can be detected by direct autoradiographic determination of the spatial variation in cAMP concentration (3) or as an optical density wave caused by periodic cell shape changes associated with chemotactic cell movement (4, 5). After 20-30 waves, cells collect in bifurcating aggregation streams, in which optical density waves are no longer visible. Therefore little is known about signal propagation during multicellular development. Up to 105 cells collect into a compact aggregate (mound),where they begin to differentiate into three major cell types, prestalk, prespore, and anterior-like cells. The cells differentiate in random positions and then undergo chemotactic cell sorting (6, 7). The prestalk cells collect on top of the mound and form a distinct morphological structure (the tip).As soon as a tip is formed, the mound elongates and forms the slug, which then falls over and starts to migrate. The foremost 20% of the slug including the tip consists of prestalk cells, while the remainder is formed by prespore cells. Anterior-like cells are found scattered throughout the presp...

Negative Tension of Scroll Wave Filaments and Turbulence in Three-Dimensional Excitable Media and Application in Cardiac Dynamics

“…Scroll waves have been observed in many excitable systems, e.g., in the Belousov-Zhabotinsky chemical reaction (Winfree 1973), in the slug phase of the life cycle of slime molds (Siegert and Weijer 1992), and in the ventricles of the heart during cardiac arrhythmias (Pertsov and Jalife 2002). Numerous modeling studies of scroll waves have been performed using analytical and numerical methods.…”

Phototaxis during the slug stage of Dictyostelium discoideum: a model study

“…The ¢rst cells to sort out are the prestalk A cells, which form the tip and are the source of the cAMP waves (Williams et al 1989;Siegert & Weijer 1992). Therefore in all simulations a slug is initiated with a tip consisting of oscillatory prestalk cells.…”

The G alpha subunit G alpha 4 couples to pterin receptors and identifies a signaling pathway that is essential for multicellular development in Dictyostelium.

“…These include cAMP, which interacts with guanine nucleotide-binding protein (G protein)-coupled cell surface receptors, and differentiation-inducing factor (DIF), which may interact with a putative intracellular DIF-binding protein (1)(2)(3)(4)(5). cAMP plays an essential role as the chemotactic agent controlling aggregation and cell sorting and regulates aggregation-stage and prestalk-and prespore-specific gene expression (1)(2)(3)(4)(5)(6)(7)(8)(9). Other factors, including NH' and adenosine, have also been proposed to regulate various aspects of morphogenesis, possibly by affecting cAMP-and DIF-mediated pathways (10).…”