Regulation of discoidin I gene expression in dictyostelium discoideum by cell‐cell contact and cAMP

Berger, Edward A.; Bozzone, Donna M.; Berman, Marcia B.; Morgenthaler, J.; Clark, Junebug

doi:10.1002/jcb.240270408

Cited by 12 publications

(9 citation statements)

References 33 publications

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“…Several other genes such as discoidin have been shown to be induced by pulses and repressed by constant high cAMP (Berger et al, 1985). Now that we know that these genes are controlled by GataC and that this transcription factor is only active for a brief period after extracellular cAMP goes up, it is clear why they are pulse dependent.…”

Section: Early Developmental Signalsmentioning

confidence: 99%

“…However, when the cells become close-packed in the center of the aggregate and the cAMP generated by each cell is immediately added to the total, the concentration stays at a constant high level. Many of the early genes are repressed by this level of cAMP, while others that accumulate during later stages are induced (Berger et al, 1985; Kimmel, 1987; Iranfar, Fuller and Loomis, 2006). …”

Section: Early Developmental Signalsmentioning

confidence: 99%

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Cell signaling during development of Dictyostelium

Loomis

2014

Developmental Biology

158

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Continuous communication between cells is necessary for development of any multicellular organism and depends on the recognition of secreted signals. A wide range of molecules including proteins, peptides, amino acids, nucleic acids, steroids and polylketides are used as intercellular signals in plants and animals. They are also used for communication in the social amoeba Dictyostelium discoideum when the solitary cells aggregate to form multicellular structures. Many of the signals are recognized by surface receptors that are seven-transmembrane proteins coupled to trimeric G proteins, which pass the signal on to components within the cytoplasm. Dictyostelium cells have to judge when sufficient cell density has been reached to warrant transition from growth to differentiation. They have to recognize when exogenous nutrients become limiting, and then synchronously initiate development. A few hours later they signal each other with pulses of cAMP that regulate gene expression as well as direct chemotactic aggregation. They then have to recognize kinship and only continue developing when they are surrounded by close kin. Thereafter, the cells diverge into two specialized cell types, prespore and prestalk cells, that continue to signal each other in complex ways to form well proportioned fruiting bodies. In this way they can proceed through the stages of a dependent sequence in an orderly manner without cells being left out or directed down the wrong path.

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Section: Early Developmental Signalsmentioning

confidence: 99%

Section: Early Developmental Signalsmentioning

confidence: 99%

Cell signaling during development of Dictyostelium

Loomis

2014

Developmental Biology

158

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“…Because of this relationship between cAMP signaling and cohesion, cohesion should participate in the regulation of cellular cAMP concentrations. In support of this conclusion, it has been reported that intracellular levels of cAMP drop severalfold when D. discoideum aggregates are disaggregated and cAMP levels remain low if the cells are maintained in a disaggregated state (1). Therefore, the transcription and stability of developmentally regulated mRNA species may also be regulated, through alterations in cAMP levels, by the degree of cohesion within the aggregate.…”

Section: Discussionmentioning

confidence: 80%

“…Genes whose induction is correlated with aggregation and the formation of tight cell-cell contact are not induced in mutants that only form loose mounds (3). A mRNA species that disappears upon the formation of tight cell-cell contacts is overexpressed in mutants that only form loose mounds (1). Because the mutants that only form loose mounds do not show contact-mediated modulation of mRNA levels, it appears that tight cell-cell contact and not just close proximity is necessary for proper regulation of developmental gene expression.…”

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confidence: 99%

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Dictyostelium discoideum lipids modulate cell-cell cohesion and cyclic AMP signaling.

Fontana¹,

Luo²,

Phillips³

1991

Mol. Cell. Biol.

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During Dictyostelium discoideum development, cell-cell communication is mediated through cyclic AMP (cAMP)-induced cAMP synthesis and secretion (cAMP signaling) and cell-cell contact. Cell-cell contact elicits cAMP secretion and modulates the magnitude of a subsequent cAMP signaling response (D. R. Fontana and P. L. Price, Differentiation 41:184-192, 1989), demonstrating that cell-cell contact and cAMP signaling are not independent events. To identify components involved in the contact-mediated modulation of cAMP signaling, amoebal membranes were added to aggregation-competent amoebae in suspension. The membranes from aggregation-competent amoebae inhibited cAMP signaling at all concentrations tested, while the membranes from vegetative amoebae exhibited a concentration-dependent enhancement or inhibition of cAMP signaling. Membrane lipids inhibited cAMP signaling at all concentrations tested. The lipids abolished cAMP signaling by blocking cAMP-induced adenylyl cyclase activation. The membrane lipids also inhibited amoeba-amoeba cohesion at concentrations comparable to those which inhibited cAMP signaling. The phospholipids and neutral lipids decreased cohesion and inhibited the cAMP signaling response. The glycolipid/sulfolipid fraction enhanced cohesion and cAMP signaling. Caffeine, a known inhibitor of cAMP-induced adenylyl cyclase activation, inhibited amoeba-amoeba cohesion. These studies demonstrate that endogenous lipids are capable of modulating amoeba-amoeba cohesion and cAMP-induced activation of the adenylyl cyclase. These results suggest that cohesion may modulate cAMP-induced adenylyl cyclase activation. Because the complete elimination of cohesion is accompanied by the complete elimination of cAMP signaling, these results further suggest that cohesion may be necessary for cAMP-induced adenylyl cyclase activation in D. discoideum.The well-defined life cycle of Dictyostelium discoideum makes it an excellent model system in which to study the mechanisms through which extracellular signals regulate differentiation and morphogenesis. D. discoideum grows as an amoeboid cell in the presence of an adequate supply of its bacterial food source. Following starvation, approximately 105 amoebae aggregate into a mound. Subsequent stages of morphogenesis result in the formation of a pseudoplasmodium and then a fruiting body (for an overview of the life cycle, see reference 4).After the initiation of development, the acquisition of aggregation competence involves the synthesis of a cell surface cyclic AMP (cAMP) receptor (20), an increase in the rate of synthesis of a phosphodiesterase (22), and an increase in adenylyl cyclase activity (25). When amoebae are aggregation competent, cAMP binds to the surface cAMP receptor, causing a transient activation of the adenylyl cyclase and the subsequent secretion of cAMP (9). This response to extracellular cAMP is called cAMP signaling or cAMP relay. cAMP signaling and chemotaxis to cAMP result in the organized aggregation of amoebae into mounds (43).The mechanism of recep...

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Contact alters cAMP metabolism in aggregation‐competent Dictyostelium amoebae

Fontana

Price

1988

Dev. Genet.

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cAMP and cell-cell contact are involved in the coordination of differentiation and morphogenesis in Dictyostelium discoideum. The experiments described in this paper establish a relationship between cAMP and cell-cell contact. Contact between Enterobacter aerogenes and aggregation-competent Dictyostelium amoebae and contact between Dictyostelium amoebae themselves results in the transient secretion of cAMP and an alteration in the amount of cAMP secreted in response to subsequent stimulation by cAMP, i.e., an alteration in magnitude of a cAMP relay response. The subsequent cAMP relay response can be enhanced or diminished depending upon the number of contacts formed and the concentration of cAMP present at the time of contact. Latex beads are capable of evoking cAMP secretion. However, the bead/amoebal contact is unable to alter the magnitude of a subsequent response to cAMP. This suggests that a nonspecific interaction via cell-cell contact elicits transient cAMP secretion in aggregation-competent Dictyostelium amoebae. The two responses to cell-cell contact are distinct from each other and distinct from the cAMP relay response. 1) The dose-response curves for the responses to Enterobacter contact are clearly different. 2) Contact with latex beads can elicit cAMP secretion but not alter the magnitude of a subsequent cAMP relay response. 3) The temperature dependences of the contact-induced responses and the cAMP relay response show that only the contact-induced cAMP secretion is inhibited at 12 and 15 degrees C, while only the cAMP relay response is inhibited at 28 degrees C. A 4-second application of cAMP at the time that contact is initiated enhances both contact-induced responses. Whether the relationship between these two developmental regulators is important for the regulation of Dictyostelium development has yet to be established.

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Regulation of discoidin I gene expression in dictyostelium discoideum by cell‐cell contact and cAMP

Cited by 12 publications

References 33 publications

Cell signaling during development of Dictyostelium

Cell signaling during development of Dictyostelium

Dictyostelium discoideum lipids modulate cell-cell cohesion and cyclic AMP signaling.

Contact alters cAMP metabolism in aggregation‐competent Dictyostelium amoebae

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