Multiple signal transduction pathways regulate discoidin I gene expression in Dictyostelium discoideum

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The expression of the discoidin I genes in Dictyostelium discoideum is regulated by the concerted action of the extracellular factors cyclic adenosine monophosphate (cAMP), folate, prestarvation factor (PSF) and conditioned media factor (CMF). However, the pathways by which these signals are transduced and the interactions between the pathways have been unexplored so far. We have analysed wild-type and mutant cells with defined lesions in signal transduction to elucidate these regulatory processes, and shown that different pathways are used for the down-regulation and induction of these genes. The cAMP receptor cARI is required for the cAMP-mediated down-regulation of discoidin I gene expression but not for the induction of discoidin I expression during development. Surprisingly, induction of the discoidin I genes requires Gα2, the G-protein subunit which is generally believed to couple to cARI, to control the expression of cAMP-inducible genes. Thus, our data suggest that Gα2 interacts with different receptors to regulate gene expression in early development. Furthermore, the analysis shows that discoidin induction in bacterially grown cells occurs in two sequential steps. The first is a low basal induction which occurs in late log-phase growth prior to starvation. PSF can induce the basal level, and the induction is independent of Gα2. The developmental induction following starvation is much stronger, dependent on Gα2 and probably signaled by CMF, which is secreted at that time. We also demonstrate that the growth history of the cells has a major influence on the pattern of gene expression and on the choice of the signal transduction pathway that is used to induce the discoidin I genes. Overall, these studies reveal complex regulatory interactions between the stimulatory and inhibitory signaling pathways controlling the expression of the discoidin I gene family.