This Article
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Mann, S K
Right arrow Articles by Firtel, R A
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Mann, S K
Right arrow Articles by Firtel, R A

 Previous Article  |  Next Article 

Mol Cell Biol. 1987 January; 7(1): 458-469

Cyclic AMP regulation of early gene expression in Dictyostelium discoideum: mediation via the cell surface cyclic AMP receptor.

S K Mann and R A Firtel

ABSTRACT

We examined two sets of genes expressed early in the developmental cycle of Dictyostelium discoideum that appear to be regulated by cyclic AMP (cAMP). The transcripts of both sets of genes were not detectable in vegetative cells. During normal development on filter pads, RNA complementary to these genes could be detected at about 2 h, peaked around 6 to 8 h, and decreased gradually thereafter. Expression of these genes upon starvation in shaking culture was stimulated by pulsing the cells with nanomolar levels of cAMP, a condition that mimics the in vivo pulsing during normal aggregation. Expression was inhibited by caffeine or by continuous levels of cAMP, a condition found later in development when in vivo expression of these genes decreased. The inhibition of caffeine could be overcome by pulsing cells with cAMP. These results suggest that the expression is mediated via the cell surface cAMP receptor, but does not require a rise in intracellular cAMP. mRNA from a gene of the second class was induced upon starvation, peaked by 2.5 h of development, and then declined. In contrast to the other genes, its expression was maintained by continuous levels of cAMP and repressed by cAMP pulses. These and other results on a number of classes of developmentally regulated genes indicates that changing levels of cAMP, acting via the cell surface cAMP receptor, are involved in controlling these groups of genes. We also examined the structure and partial sequence of the cAMP pulse-induced genes. The two tandemly duplicated M3 genes were almost continuously homologous over the sequenced portion of the protein-coding region except for a region near the N-terminal end. The two M3 genes had regions of homology in the 5' flanking sequence and showed slight homology to the same regions in gene D2, another cAMP pulse-induced gene. D2 showed extremely significant homology over its entire sequenced length to an acetylcholinesterase. The results presented here and by others suggest that expression of many early genes in D. discoideum is regulated via the cell surface cAMP receptor. We expect that many of these genes may play essential roles in early Dictyostelium development and could code for elements of the cAMP signal transduction pathway involved in aggregation.

Mol Cell Biol. 1987 January; 7(1): 458-469




This article has been cited by other articles:

  • Katoh, M., Chen, G., Roberge, E., Shaulsky, G., Kuspa, A. (2007). Developmental Commitment in Dictyostelium discoideum. Eukaryot Cell 6: 2038-2045 [Abstract] [Full Text]  
  • Zhang, M., Goswami, M., Hereld, D. (2005). Constitutively Active G Protein-coupled Receptor Mutants Block Dictyostelium Development. Mol. Biol. Cell 16: 562-572 [Abstract] [Full Text]  
  • Iranfar, N., Fuller, D., Loomis, W. F. (2003). Genome-Wide Expression Analyses of Gene Regulation during Early Development of Dictyostelium discoideum. Eukaryot Cell 2: 664-670 [Abstract] [Full Text]  
  • Chien, S., Chung, C. Y., Sukumaran, S., Osborne, N., Lee, S., Ellsworth, C., McNally, J. G., Firtel, R. A. (2000). The Dictyostelium LIM Domain-containing Protein LIM2 Is Essential for Proper Chemotaxis and Morphogenesis. Mol. Biol. Cell 11: 1275-1291 [Abstract] [Full Text]  
  • Chung, C. Y., Firtel, R. A. (1999). Paka, a Putative Pak Family Member, Is Required for Cytokinesis and the Regulation of the Cytoskeleton in Dictyostelium discoideum Cells during Chemotaxis. JCB 147: 559-576 [Abstract] [Full Text]  
  • Lee, S., Parent, C. A., Insall, R., Firtel, R. A. (1999). A Novel Ras-interacting Protein Required for Chemotaxis and Cyclic Adenosine Monophosphate Signal Relay in Dictyostelium. Mol. Biol. Cell 10: 2829-2845 [Abstract] [Full Text]  
  • Gamper, M., Kim, E., Howard, P. K., Ma, H., Hunter, T., Firtel, R. A. (1999). Regulation of Dictyostelium Protein-tyrosine Phosphatase-3 (PTP3) through Osmotic Shock and Stress Stimulation and Identification of pp130 as a PTP3 Substrate. J. Biol. Chem. 274: 12129-12138 [Abstract] [Full Text]  
  • Mohanty, S, Jermyn, K., Early, A, Kawata, T, Aubry, L, Ceccarelli, A, Schaap, P, Williams, J., Firtel, R. (1999). Evidence that the Dictyostelium Dd-STATa protein is a repressor that regulates commitment to stalk cell differentiation and is also required for efficient chemotaxis. Development 126: 3391-3405 [Abstract]  
  • Guo, K, Anjard, C, Harwood, A, Kim, H., Newell, P., Gross, J. (1999). A myb-related protein required for culmination in Dictyostelium. Development 126: 2813-2822 [Abstract]  
  • Otsuka, H., Van Haastert, P. J.M. (1998). A novel Myb homolog initiates Dictyostelium development by induction of adenylyl cyclase expression. Genes Dev. 12: 1738-1748 [Abstract] [Full Text]  
  • Mu, X, Lee, B, Louis, J., Kimmel, A. (1998). Sequence-specific protein interaction with a transcriptional enhancer involved in the autoregulated expression of cAMP receptor 1 in Dictyostelium. Development 125: 3689-3698 [Abstract]  
  • Han, Z, Firtel, R. (1998). The homeobox-containing gene Wariai regulates anterior-posterior patterning and cell-type homeostasis in Dictyostelium. Development 125: 313-325 [Abstract]  
  • Lee, S, Escalante, R, Firtel, R. (1997). A Ras GAP is essential for cytokinesis and spatial patterning in Dictyostelium. Development 124: 983-996 [Abstract]  
  • Hadwiger, J., Natarajan, K, Firtel, R. (1996). Mutations in the Dictyostelium heterotrimeric G protein alpha subunit G alpha5 alter the kinetics of tip morphogenesis. Development 122: 1215-1224 [Abstract]  
  • Gaskins, C, Clark, A M, Aubry, L, Segall, J E, Firtel, R A (1996). The Dictyostelium MAP kinase ERK2 regulates multiple, independent developmental pathways.. Genes Dev. 10: 118-128 [Abstract]  
  • Dynes, J L, Clark, A M, Shaulsky, G, Kuspa, A, Loomis, W F, Firtel, R A (1994). LagC is required for cell-cell interactions that are essential for cell-type differentiation in Dictyostelium.. Genes Dev. 8: 948-958 [Abstract]  
  • Schnitzler, G R, Fischer, W H, Firtel, R A (1994). Cloning and characterization of the G-box binding factor, an essential component of the developmental switch between early and late development in Dictyostelium.. Genes Dev. 8: 502-514 [Abstract]  
  • Dharmawardhane, S, Cubitt, A., Clark, A., Firtel, R. (1994). Regulatory role of the G alpha 1 subunit in controlling cellular morphogenesis in Dictyostelium. Development 120: 3549-3561 [Abstract]  
  • Desbarats, L, Brar, S., Siu, C. (1994). Involvement of cell-cell adhesion in the expression of the cell cohesion molecule gp80 in Dictyostelium discoideum. J. Cell Sci. 107: 1705-1712 [Abstract]  
  • Jain, R, Yuen, I S, Taphouse, C R, Gomer, R H (1992). A density-sensing factor controls development in Dictyostelium.. Genes Dev. 6: 390-400 [Abstract]  
  • Cubitt, A.B., Carrel, F., Dharmawardhane, S., Gaskins, C., Hadwiger, J., Howard, P., Mann, S.K.O., Okaichi, K., Zhou, K., Firtel, R.A. (1992). Molecular Genetic Analysis of Signal Transduction Pathways Controlling Multicellular Development in Dictyostelium. Cold Spring Harb Symp Quant Biol 57: 177-192 [Abstract]  
  • Hadwiger, J A, Firtel, R A (1992). Analysis of G alpha 4, a G-protein subunit required for multicellular development in Dictyostelium.. Genes Dev. 6: 38-49 [Abstract]  
  • Sun, T J, Devreotes, P N (1991). Gene targeting of the aggregation stage cAMP receptor cAR1 in Dictyostelium.. Genes Dev. 5: 572-582 [Abstract]  
  • Saxe, C L, Johnson, R L, Devreotes, P N, Kimmel, A R (1991). Expression of a cAMP receptor gene of Dictyostelium and evidence for a multigene family.. Genes Dev. 5: 1-8 [Abstract]  
  • Esch, R K, Firtel, R A (1991). cAMP and cell sorting control the spatial expression of a developmentally essential cell-type-specific ras gene in Dictyostelium.. Genes Dev. 5: 9-21 [Abstract]  
  • Haberstroh, L, Firtel, R A (1990). A spatial gradient of expression of a cAMP-regulated prespore cell-type-specific gene in Dictyostelium.. Genes Dev. 4: 596-612 [Abstract]  
  • Hjorth, A L, Pears, C, Williams, J G, Firtel, R A (1990). A developmentally regulated trans-acting factor recognizes dissimilar G/C-rich elements controlling a class of cAMP-inducible Dictyostelium genes.. Genes Dev. 4: 419-432 [Abstract]  
  • Firtel, R A, Chapman, A L (1990). A role for cAMP-dependent protein kinase A in early Dictyostelium development.. Genes Dev. 4: 18-28 [Abstract]  
  • Devreotes, P (1989). Dictyostelium discoideum: a model system for cell-cell interactions in development. Science 245: 1054-1058 [Abstract]  
  • Hjorth, A L, Khanna, N C, Firtel, R A (1989). A trans-acting factor required for cAMP-induced gene expression in Dictyostelium is regulated developmentally and induced by cAMP.. Genes Dev. 3: 747-759 [Abstract]  
  • Klein, P., Sun, T., Saxe, C. 3rd, Kimmel, A., Johnson, R., Devreotes, P. (1988). A chemoattractant receptor controls development in Dictyostelium discoideum. Science 241: 1467-1472 [Abstract]  
  • Kumagai, A., Mann, S.K.O., Pupillo, M., Pitt, G., Devreotes, P.N., Firtel, R.A. (1988). A Molecular Analysis of G Proteins and Control of Early Gene Expression by the Cell-surface cAMP Receptor in Dictyostelium. Cold Spring Harb Symp Quant Biol 53: 675-685 [Abstract]  


Copyright © 2009 by the American Society for Microbiology.   For an alternate route to Journals.ASM.org, visit: http://intl-journals.asm.org | More Info»