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Relationships between cell-cell interactions, cAMP, and gene expression in a developmental mutant of Dictyostelium
D M Bozzone1, R E Kohnken, E A Berger
1Cell Biology Group, Worcester Foundation for Experimental Biology, Shrewsbury, Massachusetts 91545.
Abstract:
Previous work has led us to propose that close cell-cell associations during D. discoideum development serve as a signal to deactivate expression of discoidin I mRNA, and that intracellular cAMP serves as a mediator of this regulatory pathway. This model is based in part on the failure of a morphogenetic mutant, EB-21, to deactivate discoidin I expression under conditions where these cells fail to acquire cell-cell cohesiveness and hence remain as single cells, unlike the wild type strain which forms multicellular aggregates. Here we show that the failure of EB-21 to express specific cohesiveness depends on developmental conditions, and that under conditions where close cell-cell associations are allowed to form, discoidin I mRNA expression is deactivated normally. Furthermore, in both wild type and EB-21 there is a close correlation between formation close cell-cell associations and elevation of intracellular cAMP under different developmental conditions. Additional analyses of the biological behavior of EB-21 indicate that it acquires a normal cAMP chemotactic signal-response system, and that the morphogenetic defect cannot be corrected by co-development with wild type cells. The results are discussed in terms of possible relationships between cell-cell interactions, cAMP metabolism, and developmental gene expression in this organism.
Insights
Cell-cell interactions in Dictyostelium discoideum development signal the deactivation of discoidin I mRNA. This process is mediated by intracellular cyclic adenosine monophosphate (cAMP) and is crucial for proper multicellular development.
Area of Science:
- Cellular and Molecular Biology
- Developmental Biology
- Biochemistry
Background:
- Previous research suggested cell-cell associations deactivate discoidin I mRNA via intracellular cyclic adenosine monophosphate (cAMP).
- A mutant, EB-21, failed to deactivate discoidin I expression when cell cohesion was absent, supporting the model.
Purpose of the Study:
- To investigate the role of cell-cell associations and intracellular cAMP in discoidin I mRNA regulation during Dictyostelium discoideum development.
- To clarify the developmental defect in the EB-21 mutant.
Main Methods:
- Analysis of discoidin I mRNA expression under varying developmental conditions.
- Assessment of intracellular cAMP levels in wild type and mutant strains.
- Evaluation of the EB-21 mutant's chemotaxis and ability to aggregate with wild type cells.
Main Results:
- The EB-21 mutant's failure to deactivate discoidin I expression was condition-dependent; normal deactivation occurred when cell-cell associations formed.
- A strong correlation was observed between cell-cell associations and elevated intracellular cAMP in both wild type and EB-21.
- EB-21 exhibited normal cAMP chemotaxis but its developmental defect was not rescued by co-development with wild type cells.
Conclusions:
- Close cell-cell associations are essential for deactivating discoidin I mRNA expression during Dictyostelium discoideum development.
- Intracellular cAMP acts as a mediator in this regulatory pathway, linking cell interactions to gene expression.
- The EB-21 mutant's defect is intrinsic and related to cell cohesion, not the cAMP signaling pathway itself.