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Two transmembrane signaling mechanisms control expression of the cAMP receptor gene CAR1 during Dictyostelium development.

ABSTRACT: Dictyostelium discoideum is among the best characterized organisms for the study of receptor/guanine nucleotide binding protein-mediated control of differentiation. Dictyostelium grow unicellularly but form fully differentiated multicellular organisms through a developmental program regulated by secreted cAMP activating specific cell-surface receptors. Dictyostelium respond differentially to cAMP at different developmental stages. During early development, expression of certain genes is induced by low-level oscillations of extracellular cAMP. Later, continuous, high cAMP concentrations will promote expression of specific genes in multicellular structures. Here, we show that the cAMP receptor gene CAR1, which is essential for development, utilizes two promoters that are activated at distinct stages of development and respond to different extracellular cAMP conditions. One promoter is active with low-level oscillations of cAMP; exposure to high cAMP concentrations will repress this promoter and induce a second promoter. The CAR1 mRNAs are alternatively spliced but encode identical proteins. Thus, through differential sensitivity to its own ligand, cAMP, two promoters and alternative splicing regulate CAR1 expression during Dictyostelium development.

SUBMITTER: Louis JM

PROVIDER: S-EPMC46848 | biostudies-other | 1993 Jul

REPOSITORIES: biostudies-other

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Two transmembrane signaling mechanisms control expression of the cAMP receptor gene CAR1 during Dictyostelium development.

Louis J M JM Saxe C L CL Kimmel A R AR

Proceedings of the National Academy of Sciences of the United States of America 19930701 13

Dictyostelium discoideum is among the best characterized organisms for the study of receptor/guanine nucleotide binding protein-mediated control of differentiation. Dictyostelium grow unicellularly but form fully differentiated multicellular organisms through a developmental program regulated by secreted cAMP activating specific cell-surface receptors. Dictyostelium respond differentially to cAMP at different developmental stages. During early development, expression of certain genes is induced ...[more]

PMID: 8392183

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Project description:Cyclic AMP (cAMP) is an important intracellular signaling molecule for many G protein-mediated signaling pathways but the specificity of cAMP signaling in cells with multiple signaling pathways is not well-understood. In Dictyostelium, at least two different G protein signaling pathways, mediated by the G?2 and G?4 subunits, are involved with cAMP accumulation, spore production, and chemotaxis and the stimulation of these pathways results in the activation of ERK2, a mitogen-activated protein kinase that can down regulate the cAMP-specific phosphodiesterase RegA. The regA gene was disrupted in g?2(?) and g?4(?) cells to determine if the absence of this phosphodiesterase rescues the development of these G protein mutants as it does for erk2(?) mutants. There gA(?) mutation had no major effects on developmental morphology but enriched the distribution of the G? mutant cells to the prespore/prestalk border in chimeric aggregates. The loss of RegA function had no effect on G?4- mediated folate chemotaxis. However, the regA gene disruption in g?4(?) cells, but not in g?2(?) cells, resulted in a substantial rescue and acceleration of spore production. This rescue in sporulation required cell autonomous signaling because the precocious sporulation could not be induced through intercellular signaling in chimeric aggregates. However, intercellular signals from regA(?) strains increased the expression of the prestalk gene ecmB and accelerated the vacuolization of stalk cells. Intercellular signaling from the g?4(?)regA(?) strain did not induce ecmA gene expression indicating cell-type specificity in the promotion of prestalk cell development. regA gene disruption in a G?4(HC) (G?4 overexpression) strain did not result in precocious sporulation or stalk cell development indicating that elevated G?4 subunit expression can mask regA(?) associated phenotypes even when provided with wild-type intercellular signaling. These findings indicate that the G?2 and G?4-mediated pathways provide different contributions to the development of spores and stalk cells and that the absence of RegA function can bypass some but not all defects in G protein regulated spore development.

Dataset Information

Two transmembrane signaling mechanisms control expression of the cAMP receptor gene CAR1 during Dictyostelium development.

Publications

Two transmembrane signaling mechanisms control expression of the cAMP receptor gene CAR1 during Dictyostelium development.

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