The cyclic nucleotide phosphodiesterase gene of Dictyostelium discoideum utilizes alternate promoters and splicing for the synthesis of multiple mRNAs.

Podgorski, Gregory J.; Franke, Jakob; Faure, M; Kessin, Richard H.

doi:10.1128/mcb.9.9.3938

Cited by 34 publications

(27 citation statements)

References 34 publications

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“…These results show that the ecmA promoter has a modular structure, as do the promoters of the ecmB gene and the cAMP phosphodiesterase gene (Podgorski et al, 1989;Faure et al, 1990;Ceccarelli et al, 1991). This form of promoter organisation may be common to genes expressed in development, perhaps because it allows the fine tuning of expression patterns in response to inductive signals.…”

Section: Analysis Of the Ecma Promotermentioning

confidence: 81%

Two distinct populations of prestalk cells within the tip of the migratory Dictyostelium slug with differing fates at culmination

Early¹,

Gaskell²,

Traynor³

et al. 1993

Trends in Genetics

141

126

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Section: Analysis Of the Ecma Promotermentioning

confidence: 81%

Two distinct populations of prestalk cells within the tip of the migratory Dictyostelium slug with differing fates at culmination

Early¹,

Gaskell²,

Traynor³

et al. 1993

Trends in Genetics

141

126

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“…The developmentally regulated changes in size of the CARl RNAs could result from alternative transcriptional initiation sites or alternative splicing. The Dictyostelium phosphodiesterase gene encodes multiple sized mRNAs, and recent evidence indicates the presence of both stage-specific initiation and splice sites (Podgorski et al 1989;Faure et al 1990). …”

Section: Carl Mrna Length Heterogeneitymentioning

confidence: 99%

Expression of a cAMP receptor gene of Dictyostelium and evidence for a multigene family.

Saxe¹,

Johnson²,

Devreotes³

et al. 1991

Genes Dev.

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We have previously reported the cloning of cDNAs for a Dictyostelium cell-surface cAMP receptor that is a member of the family of G-protein-linked receptors. Here, we report the organization and the developmental expression of this cAMP receptor gene, designated CARl. CARl is a single copy gene that contains two intervening sequences. CARl mRNA levels are low in growing cells, rise to peak expression at 5-10 hr of development when the cAMP signaling system is maximally active, and decrease as development proceeds. At 5 hr the predominant mRNA species is -1.9 kb, by 10 hr the mRNA is heterogeneous with sizes of -1.9-2.1 kb, but during culmination only the 2.1 kb mRNA is detected. The variety of mRNA sizes results from differences in 5'-untranslated regions. Studies using developmental mutants with aberrant cAMP-signaling patterns indicate that pulsatile action of cAMP promotes maximal expression of CARl during early development. Low stringency hybridization of CARl probes to genomic DNA detects additional, related sequences, suggesting that there are several genes that encode a family of structurally similar receptors. Multiple functions previously attributed to the cAMP receptor instead may be fulfilled by distinct receptor subtypes encoded by specific genes.

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“…To understand the origin of these two mRNAs and to identify the factors and the second messenger pathways involved in the induction of the 2.4-kb mRNA, we have studied the structure of the phosphodiesterase gene. We have reported the complete sequence of the gene and demonstrated the existence of two promoters responsible for the transcription of the 1.9-and 2.4-kb mRNAs (37). These two mRNAs have the same coding sequence but differ in their 5' untranslated sequences, which are derived from two different exons.…”

mentioning

confidence: 99%

“…Most of the enzymes and chemicals were the same as those used in previous work (37), except that the Taq polymerase was purchased from Beckman Instruments, Inc.…”

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confidence: 99%

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The cyclic nucleotide phosphodiesterase gene of Dictyostelium discoideum contains three promoters specific for growth, aggregation, and late development.

Faure¹,

Franke²,

Hall³

et al. 1990

Mol. Cell. Biol.

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The cyclic nucleotide phosphodiesterase (phosphodiesterase) plays essential roles throughout the development of Dictyostelium discoideum. It is crucial to cellular aggregation and to postaggregation morphogenesis. The phosphodiesterase gene is transcribed into three mRNAs, containing the same coding sequence connected to different 5' untranslated sequences, that accumulate at different times during the life cycle. A 1.9-kilobase (kb) mRNA is specific for growth, a 2.4-kb mRNA is specific for aggregation, and a 2.2-kb mRNA is specific for late development and is only expressed in prestalk cells. Hybridization of RNA isolated from cells at various stages of development with different upstream regions of the gene indicated separate promoters for each of the three mRNAs. The existence of specific promoters was confirmed by fusing the three putative promoter regions to the chloramphenicol acetyltransferase reporter gene, and the analysis of transformants containing these constructs. The three promoters are scattered within a 4.1-kilobase pair (kbp) region upstream of the initiation codon. The late promoter is proximal to the coding sequence, the growth-specific promoter has an initiation site that is 1.9 kbp upstream of the ATG codon, and the aggregation-specific promoter has an initiation site 3 kbp upstream.When Dictyostelium discoideum amoebae are deprived of nutrients, they initiate a developmental program that results in the formation of a multicellular organism composed of differentiated cell types. The aggregation process that takes place early in development is driven by chemotaxis toward cyclic AMP (cAMP) (6), and one of the earliest events in development is the elaboration of the biochemical apparatus required for chemotaxis toward cAMP (for reviews see references 7, 18, and 23). Soon after starvation, the cells synthesize an adenylate cyclase, a cell surface cAMP receptor, an extracellular phosphodiesterase, and a specific phosphodiesterase inhibitor. These proteins, among others, function coordinately to allow the cells to aggregate by chemotaxis. Cells secrete pulses of cAMP every 5 to 6 min, and neighboring cells respond by moving toward elevated concentrations of cAMP and by emitting cAMP to create a relay. The binding of cAMP to cell surface receptors activates second messenger cascades involving G proteins (27) that lead to a variety of cellular events (for reviews, see references 13 and 20), including the chemotactic response and the regulation of genes specific for development. The cAMP receptor is down regulated and phosphorylated upon constant stimulation by cAMP (25,53), and this results in the adaptation of cellular responses (52). The cyclic nucleotide phosphodiesterase (phosphodiesterase) acts outside the cell to reduce cAMP levels, limiting saturation and down regulation of the receptor. The phosphodiesterase exists in membrane-bound and free extracellular forms (30, 47). Its activity is regulated at the gene level (16) and is controlled at the protein level by a specific inhibitor (15). A m...

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The cyclic nucleotide phosphodiesterase gene of Dictyostelium discoideum utilizes alternate promoters and splicing for the synthesis of multiple mRNAs.

Cited by 34 publications

References 34 publications

Two distinct populations of prestalk cells within the tip of the migratory Dictyostelium slug with differing fates at culmination

Two distinct populations of prestalk cells within the tip of the migratory Dictyostelium slug with differing fates at culmination

Expression of a cAMP receptor gene of Dictyostelium and evidence for a multigene family.

The cyclic nucleotide phosphodiesterase gene of Dictyostelium discoideum contains three promoters specific for growth, aggregation, and late development.

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