Cell speed, persistence and information transmission during signal relay and collective migration

McCann, Colin; Kriebel, Paul W.; Parent, Carole A.; Losert, Wolfgang

doi:10.1242/jcs.060137

Cited by 89 publications

(99 citation statements)

References 53 publications

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“…Single cells were identified by their size and tracked from frame to frame by finding the maximum overlap with the next image. Cell tracks that persisted for more than 60 frames and displaced at least one cell length were used to compute chemotaxis index (CI) and speed for each tracked cells (31). The CI is defined as the ratio of a cell motion in the imposed gradient direction over the total cell motion.…”

Section: Methodsmentioning

confidence: 99%

Direct Biochemical Measurements of Signal Relay during Dictyostelium Development

Das

Rericha

Bagorda

et al. 2011

Journal of Biological Chemistry

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Upon starvation, individual Dictyostelium discoideum cells enter a developmental program that leads to collective migration and the formation of a multicellular organism. The process is mediated by extracellular cAMP binding to the G proteincoupled cAMP receptor 1, which initiates a signaling cascade leading to the activation of adenylyl cyclase A (ACA), the synthesis and secretion of additional cAMP, and an autocrine and paracrine activation loop. The release of cAMP allows neighboring cells to polarize and migrate directionally and form characteristic chains of cells called streams. We now report that cAMP relay can be measured biochemically by assessing ACA, ERK2, and TORC2 activities at successive time points in development after stimulating cells with subsaturating concentrations of cAMP. We also find that the activation profiles of ACA, ERK2, and TORC2 change in the course of development, with later developed cells showing a loss of sensitivity to the relayed signal. We examined mutants in PKA activity that have been associated with precocious development and find that this loss in responsiveness occurs earlier in these mutants. Remarkably, we show that this loss in sensitivity correlates with a switch in migration patterns as cells transition from streams to aggregates. We propose that as cells proceed through development, the cAMP-induced desensitization and down-regulation of cAMP receptor 1 impacts the sensitivities of chemotactic signaling cascades leading to changes in migration patterns.The directed migration of individual cells or chains or sheets of cells requires cells to transduce external cues into internal signals that regulate cytoskeletal reorganization and cell polarity. Signal transduction is important during development where the transition from single to collective cell migration is regulated by multiple external cues (1). Cell-cell communication, a process that can be manifested through the relay of external chemical signals (2, 3), is critical for a wide range of developmental processes including the survival of the social amoebae Dictyostelium discoideum.Upon starvation, Dictyostelium cells enter a developmental program leading to the transition from cells operating individually to groups of cells operating as a population. Aggregation of starving cells is controlled by signaling centers that emit periodic pulses of 3Ј-5Ј-cAMP. This process is mediated by the binding of extracellular cAMP to the G protein-coupled receptor cAR1, 3 which initiates a signaling cascade leading to, among other things, the activation of ACA (4). When ACA is first activated, rapid cAMP synthesis leads to a burst in internal cAMP levels. Although part of the synthesized cAMP remains inside cells to activate PKA and regulate gene expression, the majority of it is rapidly secreted (5-7). The secreted cAMP binds to cAR1 and, in an autocrine and paracrine amplification step, results in the production and secretion of more cAMP (2, 3). For a spatially extended cell population, the stimulated release of cAMP result...

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Section: Methodsmentioning

confidence: 99%

Direct Biochemical Measurements of Signal Relay during Dictyostelium Development

Das

Rericha

Bagorda

et al. 2011

Journal of Biological Chemistry

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“…We also tested whether nhe1 Ϫ cells also lost chemotactic orientation in a simple phosphate buffer solution, DBϪDC, used by McCann et al (55), which contained 15 mM Na ϩ (Table 1). The chemotactic index of nhe1 Ϫ cells in this solution was negligible (ϩ0.04 Ϯ 0.29; n ϭ 63), and the percent positive chemotaxis was 61%.…”

Section: K ؉ Facilitation and Chemotactic Orientation Are Defective Imentioning

confidence: 99%

Nhe1 Is Essential for Potassium but Not Calcium Facilitation of Cell Motility and the Monovalent Cation Requirement for Chemotactic Orientation in Dictyostelium discoideum

et al. 2011

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In Dictyostelium discoideum, extracellular K ؉ or Ca 2؉ at a concentration of 40 or 20 mM, respectively, facilitates motility in the absence or presence of a spatial gradient of chemoattractant. Facilitation results in maximum velocity, cellular elongation, persistent translocation, suppression of lateral pseudopod formation, and myosin II localization in the posterior cortex. A lower threshold concentration of 15 mM K ؉ or Na or 5 mM Ca 2؉ is required for chemotactic orientation. Although the common buffer solutions used by D. discoideum researchers to study chemotaxis contain sufficient concentrations of cations for chemotactic orientation, the majority contain insufficient levels to facilitate motility. Here it has been demonstrated that Nhe1, a plasma membrane protein, is required for K ؉ but not Ca 2؉ facilitation of cell motility and for the lower K ؉ but not Ca 2؉ requirement for chemotactic orientation.Extracellular Ca 2ϩ and K ϩ , ubiquitous in the soluble environment of cells, both free-living and in multicellular organisms (5,15,21,36,56,79,80,84,91), have long been known to affect the motility of cells ranging in complexity from bacterial to human (7,8,19,25,31,60,62,65,98). In Dictyostelium discoideum, which serves as a powerful model for studying animal cell motility (4,6,20,34,41,42,43,45,50,82,87,86,92,98), either extracellular K ϩ or Ca 2ϩ at an optimum concentration of 40 mM or 20 mM, respectively, enhances most aspects of basic cell motility in the absence of chemoattractant, including cell elongation, uropod formation, the suppression of lateral pseudopod formation, velocity, directional persistence, and localization of myosin II in the posterior cell cortex (51, 78). These facilitating concentrations of K ϩ or Ca 2ϩ cannot be replaced with other monovalent or divalent cations (51) and are within the range of the soluble concentrations of the two cations found in soil (1,5,32,44,49,56) and manure (9, 66, 83), two common niches in which soil amoebae thrive (12,27,35,67,71). These concentrations of K ϩ and Ca 2ϩ are close to those found to be optimum for enhancing the motility of a variety of other animal cells. For instance, 9 mM Ca 2ϩ has been found to be optimum for flagellated sea urchin sperm motility (99), and Ca 2ϩ ranging in concentration from 1 to 10 mM has been found optimum for vertebrate cell motility (28,58,63). Concentrations of K ϩ greater than 100 mM have been found to be optimum for the polarization and motility of human polymorphonuclear leukocytes (52, 69).The surface molecules and mechanisms regulating K ϩ and Ca 2ϩ facilitation in D. discoideum have not been elucidated. However, Patel and Barber (64) reported a defective behavioral phenotype for cells of the nhe1 null mutant in a facilitating concentration of K ϩ that was strikingly similar to the behavior of wild-type cells in a nonfacilitating concentration of K ϩ (51). Nhe1 is a plasma membrane protein related to cation/H ϩ exchangers (64). We therefore tested the possibility that Nhe1 mediated K ϩ facilitation. First, t...

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“…In fact, most of these systems display both types of behavior, e.g. fish switch between migration and rotation (milling) [2,15], and, depending on environmental conditions, slime molds [6,16,17] and bacteria [18][19][20] will migrate or rotate. For example, the slime mold Dictyostelium discoideum (or Dicty) will collectively migrate if food is scarce, but transitions to a vortex to form a fruiting body as a last resort [21].…”

Section: Introductionmentioning

confidence: 99%

Collective dynamics of soft active particles

et al. 2015

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We present a model of soft active particles that leads to a rich array of collective behavior found also in dense biological swarms of bacteria and other unicellular organisms. Our model uses only local interactions, such as Vicsek-type nearest-neighbor alignment, short-range repulsion, and a local boundary term. Changing the relative strength of these interactions leads to migrating swarms, rotating swarms, and jammed swarms, as well as swarms that exhibit run-and-tumble motion, alternating between migration and either rotating or jammed states. Interestingly, although a migrating swarm moves slower than an individual particle, the diffusion constant can be up to three orders of magnitude larger, suggesting that collective motion can be highly advantageous, for example, when searching for food.

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Cell speed, persistence and information transmission during signal relay and collective migration

Cited by 89 publications

References 53 publications

Direct Biochemical Measurements of Signal Relay during Dictyostelium Development

Direct Biochemical Measurements of Signal Relay during Dictyostelium Development

Nhe1 Is Essential for Potassium but Not Calcium Facilitation of Cell Motility and the Monovalent Cation Requirement for Chemotactic Orientation in Dictyostelium discoideum

Collective dynamics of soft active particles

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