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Development 136 (5): 803-812

Steroids initiate a signaling cascade that triggers rapid sporulation in Dictyostelium

Christophe Anjard, Yongxuan Su, and William F. Loomis*

Center for Molecular Genetics, Division of Biological Sciences, University of California San Diego, La Jolla, CA 92093, USA.

* Author for correspondence (e-mail: wloomis{at}ucsd.edu)

Accepted for publication 4 January 2009.

Abstract: Encapsulation of prespore cells of Dictyostelium discoideum is controlled by several intercellular signals to ensure appropriate timing during fruiting body formation. Acyl-CoA-binding protein, AcbA, is secreted by prespore cells and processed by the prestalk protease TagC to form the 34 amino acid peptide SDF-2 that triggers rapid encapsulation. AcbA is secreted when {gamma}-aminobutyric acid (GABA) is released from prespore cells and binds to GrlE, a G protein-coupled receptor (GPCR). Analysis of SDF-2 production in mutant strains lacking G{alpha} subunits and GPCRs, either as pure populations or when mixed with other mutant strains, uncovered the non-cell-autonomous roles of GrlA, G{alpha}4 and G{alpha}7. We found that G{alpha}7 is essential for the response to GABA and is likely to be coupled to GrlE. GrlA-null and G{alpha}4-null cells respond normally to GABA but fail to secrete it. We found that they are necessary for the response to a small hydrophobic molecule, SDF-3, which is released late in culmination. Pharmacological inhibition of steroidogenesis during development blocked the production of SDF-3. Moreover, the response to SDF-3 could be blocked by the steroid antagonist mifepristone, whereas hydrocortisone and other steroids mimicked the effects of SDF-3 when added in the nanomolar range. It appears that SDF-3 is a steroid that elicits rapid release of GABA by acting through the GPCR GrlA, coupled to G protein containing the G{alpha}4 subunit. SDF-3 is at the head of the cascade that amplifies the signal for encapsulation to ensure the rapid, synchronous formation of spores.

Key Words: Steroids • SDF-2 • SDF-3 • G protein-coupled receptor • GrlA


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