cAMP controls cytosolic Ca2+ levels in Dictyostelium discoideum

Lusche, Daniel F.; Bezares-Roder, Karen; Happle, Kathrin; Schlatterer, Christina

doi:10.1186/1471-2121-6-12

Cited by 17 publications

(8 citation statements)

References 36 publications

(47 reference statements)

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“…A parsimonious explanation of the propagation of pausing behavior from animal to animal is that ELP secreted from each pausing animal evoked ELP secretion in adjacent animals. Propagation of waves of secretion across groups of cells that have receptors for the signal they secrete is well known from work on the social amoeba Dictyostelium ( Robertson et al, 1972 ; Devreotes and Steck, 1979 ; Dormann et al, 2002 ; Lusche et al, 2005 ), for instance.…”

Section: Discussionmentioning

confidence: 99%

Neuropeptidergic integration of behavior in Trichoplax adhaerens, an animal without synapses

Senatore

Reese

Smith

2017

Journal of Experimental Biology

118

129

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Trichoplax adhaerens is a flat, millimeter-sized marine animal that adheres to surfaces and grazes on algae. Trichoplax displays a repertoire of different feeding behaviors despite the apparent absence of a true nervous system with electrical or chemical synapses. It glides along surfaces to find food, propelled by beating cilia on cells at its ventral surface, and pauses during feeding by arresting ciliary beating. We found that when endomorphin-like peptides are applied to an animal, ciliary beating is arrested, mimicking natural feeding pauses. Antibodies against these neuropeptides label cells that express the neurosecretory proteins and voltage-gated calcium channels implicated in regulated secretion. These cells are embedded in the ventral epithelium, where they comprise only 4% of the total, and are concentrated around the edge of the animal. Each bears a cilium likely to be chemosensory and used to detect algae. Trichoplax pausing during feeding or spontaneously in the absence of food often induce their neighbors to pause as well, even neighbors not in direct contact. Pausing behavior propagates from animal to animal across distances much greater than the signal that diffuses from just one animal, so we presume that the peptides secreted from one animal elicit secretion from nearby animals. Signal amplification by peptide-induced peptide secretion explains how a small number of sensory secretory cells lacking processes and synapses can evoke a wave of peptide secretion across the entire animal to globally arrest ciliary beating and allow pausing during feeding.

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Section: Discussionmentioning

confidence: 99%

Neuropeptidergic integration of behavior in Trichoplax adhaerens, an animal without synapses

Senatore

Reese

Smith

2017

Journal of Experimental Biology

118

129

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“…However, iplA-null cells might still have very low Ca 2+ influx that complicates the conclusion of Ca 2+ independence [167]. Furthermore, Ca 2+ chelation reduces cell spreading and lowers speed during chemotaxis, and extracellular Ca 2+ can improve cAMP-mediated migration at certain concentrations [168-171]. Interestingly, similar concentrations of Ca 2+ can induce improvements in cell migration in the absence of cAMP, suggesting that most of the effects on chemotaxis are due to changes in migration.…”

Section: Chemotactic Network Of Dictyostelium and Leukocytesmentioning

confidence: 99%

Moving towards a paradigm: common mechanisms of chemotactic signaling in Dictyostelium and mammalian leukocytes

Artemenko

Lampert

Devreotes

2014

Cell. Mol. Life Sci.

178

221

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Chemotaxis, or directed migration of cells along a chemical gradient, is a highly coordinated process that involves gradient sensing, motility, and polarity. Most of our understanding of chemotaxis comes from studies of cells undergoing amoeboid-type migration, in particular the social amoeba Dictyostelium discoideum and leukocytes. In these amoeboid cells the molecular events leading to directed migration can be conceptually divided into four interacting networks: receptor/G protein, signal transduction, cytoskeleton, and polarity. The signal transduction network occupies a central position in this scheme as it receives direct input from the receptor/G protein network, as well as feedback from the cytoskeletal and polarity networks. Multiple overlapping modules within the signal transduction network transmit the signals to the actin cytoskeleton network leading to biased pseudopod protrusion in the direction of the gradient. The overall architecture of the networks, as well as the individual signaling modules are remarkably conserved between Dictyostelium and mammalian leukocytes, and the similarities and differences between the two systems are the subject of this review.

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“…30,31 In particular, the molecular circuit regulating Dictyostelium chemotaxis along cAMP gradients has been modelled as three interconnected modules involving intracellular calcium (Ca 2+ ), inositol 1,4,5-triphosphate (IP 3 ) and the G protein-coupled receptor cAR1, 24,26,[32][33][34][35] as shown in Fig. 1.…”

Section: A New Model For Camp Oscillations In Dictyostelium Exhibits mentioning

confidence: 99%

“…[24][25][26][27], we have considered cAMP production and degradation to be dependent on the level of intracellular Ca 2+ , which in turn is determined by a balance of fluxes into the cytoplasm from extracellular medium and endoplasmic reticulum (ER) and fluxes mostly generated by the membrane pumps compensating Ca 2+ leaks across the plasma and ER membranes. IP 3 is synthesised by Ca 2+ -dependent and G protein-dependent phospholipase C (PLC).…”

Section: A New Model For Camp Oscillations In Dictyostelium Exhibits mentioning

confidence: 99%

“…22 and 23. While the above computational studies have significantly advanced our understanding of various aspects of Dictyostelium behaviour, there are a range of questions that still require further elucidation. It has been shown experimentally that the levels of intracellular Ca 2+ and cAMP in Dictyostelium are tightly interconnected [24][25][26][27] and a number of experiments involving the application of calmidazolium (R24571), a calmodulin (CaM) inhibitor, to Dictyostelium have demonstrated a dramatic impact on the light scattering oscillations 26,28 which are one of the major characteristics of aggregation. 26,29 Ca 2+ has also been shown to be directly involved in cell migration via the stretch-activated Ca 2+ channels (SAC)s. 1 Previously developed models for Dictyostelium signalling and aggregation do not allow these phenomena to be investigated, however, as they all omit one or more of the networks involved.…”

Section: Introductionmentioning

confidence: 99%

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Computational modelling suggests dynamic interactions between Ca2+, IP3 and G protein-coupled modules are key to robust Dictyostelium aggregation

et al. 2009

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Under conditions of starvation, Dictyostelium cells begin a programme of development during which they aggregate to form a multicellular structure by chemotaxis, guided by propagating waves of cyclic AMP that are relayed robustly from cell to cell. In this paper, we develop and analyse a new model for the intracellular and extracellular cAMP dependent processes that regulate Dictyostelium migration. The model allows, for the first time, a quantitative analysis of the dynamic interactions between calcium, IP 3 and G protein-dependent modules that are shown to be key to the generation of robust cAMP oscillations in Dictyostelium cells. The model provides a mechanistic explanation for the transient increase in cytosolic free Ca 2+ concentration seen in recent experiments with the application of the calmodulin inhibitor calmidazolium (R24571) to Dictyostelium cells, and also allows elucidation of the effects of varying both the conductivity of stretch-activated channels and the concentration of external phosphodiesterase on the oscillatory regime of an individual cell. A rigorous analysis of the robustness of the new model shows that interactions between the different modules significantly reduce the sensitivity of the resulting cAMP oscillations to variations in the kinetics of different Dictyostelium cells, an essential requirement for the generation of the spatially and temporally synchronised chemoattractant cAMP waves that guide Dictyostelium aggregation.

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cAMP controls cytosolic Ca2+ levels in Dictyostelium discoideum

Cited by 17 publications

References 36 publications

Neuropeptidergic integration of behavior in Trichoplax adhaerens, an animal without synapses

Neuropeptidergic integration of behavior in Trichoplax adhaerens, an animal without synapses

Moving towards a paradigm: common mechanisms of chemotactic signaling in Dictyostelium and mammalian leukocytes

Computational modelling suggests dynamic interactions between Ca2+, IP3 and G protein-coupled modules are key to robust Dictyostelium aggregation

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