Opposite effects of adenosine on two types of cAMP‐induced gene expression in <i>Dictyostelium</i> indicate the involvement of at least two different intracellular pathways for the transduction of cAMP signals

Spek, Wouter; Drunen, Kees van; Eijk, Ronald van; Schaap, Pauline

doi:10.1016/0014-5793(88)80005-x

Cited by 20 publications

(8 citation statements)

References 21 publications

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“…We found that adenosine had no effect on the accumulation of any of the three developmentally regulated transcripts in monolayers of V12-M2 (data not shown). This result was surprising, since Schaap and coworkers recently reported that adenosine inhibited D19 mRNA accumulation and stimulated D11 mRNA accumulation in cyclic AMP-pulsed suspensions of NC4 cells [37]. However, since high concentrations of cyclic AMP have been shown to counteract the effects of adenosine [37, 431, our negative results might be explained by the high concentration of cyclic AMP that is required for stalk cell formation in the monolayers.…”

Section: The Effects Of Adenosine On Gene Expressionmentioning

confidence: 63%

The effects of presumptive morphogens on prestalk and prespore gene expression in monolayers of Dictyostelium discoideum

Kwong

1990

Differentiation

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Abstract. The effects of several presumptive morphogens on the expression of three developmentally regulated genes (Dll, D19 and pDd63) has been examined during the in vitro differentiation of strain V12‐M2 in cell suspensions and in cell monolayers. Adenosine had no effect on either prestalk or prespore gene expression in strain V12‐M2, either in monolayers or in suspensions, casting some doubt as to its importance as a morphogen. In addition, although it had been shown previously that elevated pH stimulated spore cell formation and inhibited stalk cell formation, there was a reduction in the amounts of mRNA corresponding to the prespore‐cell‐specific gene D19 and the prestalk‐cell‐specific gene pDd63 when monolayers of strain V12‐M2 were exposed to an elevated extracellular pH. Furthermore, although ammonia had been shown previously to have opposite effects on stalk and spore cell formation in monolayers, it had differential effects on D19 and pDd63 gene expression only at low concentrations. At higher concentrations, the expression of both genes was stimulated. Methylamine also affects stalk and spore cell formation in monolayers, but had only slight effects on the expression of the three genes. The expression of the prestalk‐cell‐enriched gene, Dll, was only slightly affected by elevated pH, ammonia or methylamine. These results illustrate the fact that conditions that affect terminal cell differentiation do not necessarily influence cell‐type‐specific gene expression and indicate hitherto unexpected complexities in the progression of gene expression during differentiation. During monolayer differentiation, the accumulation of the prespore‐cell‐specific D19 mRNA preceded the accumulation of the prestalk‐cell‐specific pDd63 mRNA by 2–4 h. When cyclic AMP was removed from monolayers that had already accumulated D19 mRNA, the subsequent accumulation of the prestalk specific pDd63 mRNA did not occur, indicating that the D19 and pDd63 genes require cyclic AMP for their expression at different times during development.

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Section: The Effects Of Adenosine On Gene Expressionmentioning

confidence: 63%

The effects of presumptive morphogens on prestalk and prespore gene expression in monolayers of Dictyostelium discoideum

Kwong

1990

Differentiation

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“…While positional information may not be essential in this initial patterning of prestalk A cells, it presumably is important in maintaining the pattern and in controlling Dd-ras and Dd63 expression later in development (this report ;Schaap 1986;Wang et al 1986Wang et al , 1988aWilliams et al 1987Williams et al , 1989. The stabilization and maintenance of this pattern would require the interplay of cAMP, DIF, adenosine, NHJ, and possibly other morphogens (Nestle and Sussman 1972;Williams et al 1984;Schaap 1986;Schaap and Wang 1986;Spek et al 1988;Wang et al 1988). It is possible that the cell sorting mechanism combined with the preferential expression of appropriate gene products initially establishes gradients that may be required to stabilize the spatial pattern established in the tipped aggregate.…”

Section: Discussionmentioning

confidence: 87%

“…Thus, it is possible that the cell cycle controls the initial, apparently random patterning of Dd-ras-and D(i63-expressing cells. Although all cells within the developing aggregate during aggregation receive the cAMP signal, they may respond differently due to differences in the cAMP-signaling pathways in the two cell types (see Spek et al 1988;Ginsberg and Kimmel 1989). These cells may then sort, possibly in response to cAMP signals, with the Ddras-expressing prestalk cells migrating toward the tip.…”

Section: Discussionmentioning

confidence: 99%

cAMP and cell sorting control the spatial expression of a developmentally essential cell-type-specific ras gene in Dictyostelium.

Esch¹,

Firtel²

1991

Genes Dev.

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The Dictyostelium ras gene {Dd-ras) is expressed at a low level in vegetative cells, is not expressed between the onset of development and aggregation, and is then re-expressed in the multicellular aggregate stages from the distal, now cAMP-responsive, promoter and from two more proximal promoters. Expression of activated Dd-ras (Gi2^ T12) (Reymond et al. 1986) results in an abnormal developmental phenotype with the formation of aggregates having multiple tips and an inhibition of further development. In this report we investigate the spatial expression of Dd-ras by fusing the 5'-flanking region to the Escherichia coli lacZ gene and by staining aggregates for p-galactosidase (P-gal) activity. We show that fusions using 5'-flanking sequences that include all promoters are expressed in -10-20% of the cells randomly scattered within the early aggregate. Our data indicate that these p-gal-expressing cells migrate to newly formed tips of aggregates and localize in the region that becomes the prestalk zone. Staining is also seen in the very posterior of the organism. The anterior staining appears to be specific for the prestalk A population, and p-gal activity is subsequently present in stalk cells as developmental proceeds. When only the two more proximal promoters are used to drive lacZ expression, localized staining is seen in the anterior prestalk region, although it is weaker than with the construct carrying all promoters. Moreover, staining is not seen in the posterior domain in the first finger stage, suggesting differences in the spatial expression from the different promoters. Staining is also observed in some cells within the prespore region, which could be anterior-like cells. The pattern of Dd-ras/lacZ staining during tip formation suggests a directed, spiral pattern of cell migration, possibly in response to the proposed spiral gradient of cAMP within the developing aggregate. The pattern of Dd-ras is consistent with the abnormal developmental phenotype caused by expressing an activated Dd-ras Thrjj gene and suggests an essential role for Dd-ras in controlling spatial differentiation.

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“…It was subsequently reported that the application of adenosine to pseudoplasmodia decreased the number of prespore cells, while addition of adenosine deaminase had the opposite effect ). In addition, adenosine stimulated prestalk cell enriched gene expression and inhibited prespore cell specific gene expression in shaken suspensions of NC-4 (Spek et al 1988). This data is consistent with the idea that adenosine stimulates the stalk cell pathway of differentiation at the expense of the prespore cell pathway.…”

Section: Adenosinementioning

confidence: 97%

Potential morphogens involved in pattern formation during Dictyostelium differentiation

Gross¹

1991

Biochem. Cell Biol.

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Upon starvation, Dictyostelium amoebae aggregate together and then differentiate into either the stalk or spore cells that, respectively, form the stalk and sorus of the fruiting body. During differentiation, the prestalk and prespore cells become spatially segregated in a clearly defined developmental pattern. Several low molecular weight molecules that influence cell type determination during in vitro differentiation have been identified. The possible role of these molecules as morphogens, responsible for the formation of the developmental pattern, is discussed.

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Opposite effects of adenosine on two types of cAMP‐induced gene expression in Dictyostelium indicate the involvement of at least two different intracellular pathways for the transduction of cAMP signals

Cited by 20 publications

References 21 publications

The effects of presumptive morphogens on prestalk and prespore gene expression in monolayers of Dictyostelium discoideum

The effects of presumptive morphogens on prestalk and prespore gene expression in monolayers of Dictyostelium discoideum

cAMP and cell sorting control the spatial expression of a developmentally essential cell-type-specific ras gene in Dictyostelium.

Potential morphogens involved in pattern formation during Dictyostelium differentiation

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