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Eukaryotic Cell, April 2005, p. 775-786, Vol. 4, No. 4
1535-9778/05/$08.00+0     doi:10.1128/EC.4.4.775-786.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.

Intracellular Role of Adenylyl Cyclase in Regulation of Lateral Pseudopod Formation during Dictyostelium Chemotaxis

Vesna Stepanovic,1 Deborah Wessels,1 Karla Daniels,1 William F. Loomis,2 and David R. Soll1*

W. M. Keck Dynamic Image Analysis Facility, Department of Biological Sciences, The University of Iowa, Iowa City, Iowa,1 Department of Biology, University of California—San Diego, La Jolla, California2

Received 20 December 2004/ Accepted 7 February 2005

Cyclic AMP (cAMP) functions as the extracellular chemoattractant in the aggregation phase of Dictyostelium development. There is some question, however, concerning what role, if any, it plays intracellularly in motility and chemotaxis. To test for such a role, the behavior of null mutants of acaA, the adenylyl cyclase gene that encodes the enzyme responsible for cAMP synthesis during aggregation, was analyzed in buffer and in response to experimentally generated spatial and temporal gradients of extracellular cAMP. acaA– cells were defective in suppressing lateral pseudopods in response to a spatial gradient of cAMP and to an increasing temporal gradient of cAMP. acaA– cells were incapable of chemotaxis in natural waves of cAMP generated by majority control cells in mixed cultures. These results indicate that intracellular cAMP and, hence, adenylyl cyclase play an intracellular role in the chemotactic response. The behavioral defects of acaA– cells were surprisingly similar to those of cells of null mutants of regA, which encodes the intracellular phosphodiesterase that hydrolyzes cAMP and, hence, functions opposite adenylyl cyclase A (ACA). This result is consistent with the hypothesis that ACA and RegA are components of a receptor-regulated intracellular circuit that controls protein kinase A activity. In this model, the suppression of lateral pseudopods in the front of a natural wave depends on a complete circuit. Hence, deletion of any component of the circuit (i.e., RegA or ACA) would result in the same chemotactic defect.

* Corresponding author. Mailing address: 302 BBE, Department of Biological Sciences, The University of Iowa, Iowa City, IA 52242. Phone: (319) 335-1117. Fax: (319) 335-2772. E-mail: david-soll{at}uiowa.edu.

Eukaryotic Cell, April 2005, p. 775-786, Vol. 4, No. 4
1535-9778/05/$08.00+0     doi:10.1128/EC.4.4.775-786.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.



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