Cell-cell contact elicits cAMP secretion and alters cAMP signaling in Dictyostelium discoideum

Abstract

Abstract Cell-cell contact and cAMP regulate Dictyostelium discoideum development. Aggregation-competent D. discoideum amoebae respond to cell-cell contact by secreting cAMP and altering the amount of cAMP secreted after stimulation by extracellular cAMP. cAMP-stimulated cAMP secretion is called cAMP signaling. Depending upon experimental conditions, the cAMP signaling response following cell-cell contact can be enhanced or inhibited. The two contact-induced responses are elicited by Enterobacter aerogenes-amoebal and amoebal-amoebal contact. Latex beads, charged or neutral, elicit amoebal secretion of cAMP but do not alter the magnitude of a subsequent cAMP signaling response. These results suggest that the stimulus which leads to the secretion of cAMP may be a mechanical one such as a contact-induced deformation of the plasma membrane. A more specific interaction must be necessary to alter the magnitude of the cAMP signaling response. Examination of the temperature-dependence of cAMP signaling, phagocytosis, contact-elicited cAMP secretion, and contact-induced alterations of cAMP signaling suggests that the contact-induced responses are not the result of enhanced amoebal sensitivity to cAMP, nor are they a result of phagocytosis. A mutant of D. discoideum, which is unable to (1) phagocytose charged particles, (2) cohere to other amoebae, or (3) adhere to plastic, secretes cAMP upon particle-amoebal contact. This mutant does not alter the magnitude of its cAMP signaling response following bacterialamoebal contact. These four phenotypes revert coordinately, suggesting that they are linked. Contact-induced cAMP secretion and the alteration in the responsiveness of amoebae to external cAMP demonstrate a relationship between cAMP and cell-cell contact, the two known regulators of Dictyostelium discoideum development. These results suggest that the reversal of Dictyostelium development following refeeding may be facilitated by a bacterial-amoebal contact-induced inhibition of cAMP signaling. Amoebal-amoebal contact might coordinate Dictyostelium discoideum development by altering cAMP levels.