Cell-cell contact elicits cAMP secretion and alters cAMP signaling in Dictyostelium discoideum

Fontana, Donna R.; Price, Pamela L.

doi:10.1111/j.1432-0436.1989.tb00746.x

Cited by 13 publications

(10 citation statements)

References 38 publications

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“…Thus, cell-cell contact might exert its effect on transcription and mRNA stability by altering cAMP levels within the aggregate. In support of this hypothesis, we have demonstrated that cell-cell contact elicits cAMP secretion from aggregation-competent amoebae and alters the amount of cAMP secreted by the amoebae during a subsequent cAMP signaling response (12,13).…”

supporting

confidence: 54%

“…We have previously shown that cell-cell contact elicits cAMP secretion and alters the magnitude of a subsequent cAMP signaling response (12,13). These observations plus the localization of the adenylyl cyclase in a detergentresistant fraction led us to suggest that the membrane skeleton was involved in the regulation of D. discoideum adenylyl cyclase activity.…”

Section: Discussionmentioning

confidence: 90%

“…Examination of the dose-response curves for the inhibition of cAMP signaling and cohesion by the neutral lipid fraction and by caffeine showed a quantitative correlation between the inhibition of cAMP signaling and the inhibition of cohesion. While it is possible that the lipid fractions and the caffeine exert their effects on a cellular component or function which in turn alters both cohesion and cAMP signaling, because it has been directly demonstrated that cell-cell contact alters the magnitude of a subsequent cAMP signaling response (12,13), these data strongly suggest that it is cell-cell cohesion which determines the magnitude of the D. discoideum cAMP signaling response.…”

Section: Discussionmentioning

confidence: 99%

“…This complex dose-response curve suggests that the membranes from vegetative amoebae contain at least two components capable of altering a subsequent cAMP signaling response, one stimulatory and the other inhibitory. In addition to altering a subsequent cAMP signaling response, cell-cell contact and cell-bead contact elicit cAMP secretion (13). Membrane addition alone, without the addition of cAMP, did not elicit cAMP secretion, demonstrating that membranes cannot replace cells in eliciting both of the contact-induced responses.…”

mentioning

confidence: 95%

“…Because caffeine interferes with the isotope dilution method described above, when the bovine muscle protein was used, the inhibition of cAMP signaling by caffeine was measured by a perfusion technique (9,11,13,42). Briefly, amoebae were labeled with [3H]adenosine and allowed to develop to aggregation competence.…”

mentioning

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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supporting

confidence: 54%

Section: Discussionmentioning

confidence: 90%

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 95%

mentioning

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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Cell‐cell contact mediates cAMP secretion in Dictyostelium discoideum

1991

Self Cite

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Cyclic adenosine 3':5' monophosphate (cAMP) and cell-cell contact regulate developmental gene expression in Dictyostelium discoideum. Developing D. discoideum amoebae synthesize and secrete cAMP following the binding of cAMP to their surface cAMP receptor, a response called cAMP signaling. We have demonstrated two responses of developing D. discoideum amoebae to cell-cell contact. Cell-cell contact elicits cAMP secretion and alters the amount of cAMP secreted in a subsequent cAMP signaling response. Depending upon experimental conditions, bacterial-amoebal contact and amoebal-amoebal contact can enhance or diminish the amount of cAMP secreted during a subsequent cAMP signaling response. We have hypothesized that cell-cell contact regulates D. discoideum development by altering cellular and extracellular levels of cAMP. To begin testing this hypothesis, these responses were further characterized. The two responses to cell-cell contact are independent, i.e., they can each occur in the absence of the other. The responses to cell-cell contact also have unique temperature dependences when compared to each other, cAMP signaling, and phagocytosis. This suggests that these four responses have unique steps in their transduction mechanisms. The secretion of cAMP in response to cell-cell contact appears to be a non-specific response; contact between D. discoideum amoebae and Enterobacter aerogenes, latex beads, or other amoebae elicits cAMP secretion. Despite the apparent similarities of the effects of bacterial-amoebal and amoebal-amoebal contact on the cAMP signaling response, this contact-induced response appears to be specific. Latex beads addition does not alter the magnitude of a subsequent cAMP signaling response.(ABSTRACT TRUNCATED AT 250 WORDS)

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Changes in the interior surface of newly mesodermalized ectoderm and its contact activity with competent ectoderm in the newtCynops (Amphibia)

Suzuki

Miyagawa

Kuwana

1991

Roux's Arch Dev Biol

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The presumptive ectoderm (pE) ofCynops gastrulae was artificially mesodermalized by contact with teleost swimbladder. The newly mesodermalized ectoderm (mE) acquired the capacity for neural induction (Suzuki et al. 1986a). SEM observations revealed that the mE cells altered their cellular profiles immediately after mesodermalization. The characteristics of the cell surface and the cell architecture became similar to those of invaginated mesoderm cells. There were distinct differences in the cellular contact between mE-pE and pE-pE combinations. The mE-pE combinations kept close contact at their interior surfaces, while the pE-pE combinations did not keep contact. Both TEM and SEM observations also indicated that there were tight contacts between mE and pE cells. These findings suggest that neural-inducing activity of the newly mesodermalized ectoderm cells is coupled with acquisition of cellular affinity toward the interior surface of competent ectoderm cells, and probably requires close cell contacts.

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Cell-cell contact elicits cAMP secretion and alters cAMP signaling in Dictyostelium discoideum

Cited by 13 publications

References 38 publications

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

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

Cell‐cell contact mediates cAMP secretion in Dictyostelium discoideum

Changes in the interior surface of newly mesodermalized ectoderm and its contact activity with competent ectoderm in the newtCynops (Amphibia)

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