Abstract
Postaggregation Dictyostelium discoideum cells contain 2000-3000 mRNA species that are absent from pre-aggregation cells. These aggregation-dependent sequences compose 30% of the mass of the late mRNA and represent the transcription products of an additional 11% of the single-copy genome. By analysis of mutants that are blocked at different stages of differentiation, we show that induction of expression of these genes is correlated with the formation of tight cell—cell contacts that resist EDTA. In particular, mutants that exhibit chemotaxis and aggregate to form loose mounds but do not form cell—cell contacts that resist EDTA fail to induce these late mRNA and protein species. By contrast, mutants that form normal contacts but progress no further through development do express the late mRNA species. Thus, interactions at the cell surface are involved in developmental induction of a large group of coregulated mRNAs. We have employed two independent assays for these developmentally regulated mRNAs: hybridization of gel-separated RNAs to cloned nuclear DNAs and hybridization of mRNA to a cDNA probe specific for the population of 2000-3000 regulated sequences.
Keywords: contact sites A, aggregation-dependent mRNAs
Full text
PDF




Images in this article
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Alton T. H., Lodish H. F. Developmental changes in messenger RNAs and protein synthesis in Dictyostelium discoideum. Dev Biol. 1977 Oct 1;60(1):180–206. doi: 10.1016/0012-1606(77)90118-x. [DOI] [PubMed] [Google Scholar]
- Alton T. H., Lodish H. F. Synthesis of developmentally regulated proteins in Dictyostelium discoideum which are dependent on continued cell-cell interaction. Dev Biol. 1977 Oct 1;60(1):207–216. doi: 10.1016/0012-1606(77)90119-1. [DOI] [PubMed] [Google Scholar]
- Beug H., Katz F. E., Gerisch G. Dynamics of antigenic membrane sites relating to cell aggregation in Dictyostelium discoideum. J Cell Biol. 1973 Mar;56(3):647–658. doi: 10.1083/jcb.56.3.647. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Blumberg D. D., Lodish H. F. Changes in the complexity of nuclear RNA during development of Dictyostelium discoideum. Dev Biol. 1981 Jan 15;81(1):74–80. doi: 10.1016/0012-1606(81)90349-3. [DOI] [PubMed] [Google Scholar]
- Blumberg D. D., Lodish H. F. Changes in the messenger RNA population during differentiation of dictyostelium discoideum. Dev Biol. 1980 Aug;78(2):285–300. doi: 10.1016/0012-1606(80)90337-1. [DOI] [PubMed] [Google Scholar]
- Blumberg D. D., Lodish H. F. Complexity of nuclear and polysomal RNAs in growing Dictyostelium discoideum cells. Dev Biol. 1980 Aug;78(2):268–284. doi: 10.1016/0012-1606(80)90336-x. [DOI] [PubMed] [Google Scholar]
- Bordier C., Loomis W. F. The major developmentally regulated protein complex in membranes of Dictyostelium. J Biol Chem. 1978 Jul 25;253(14):5133–5139. [PubMed] [Google Scholar]
- Boudreau R. J., Drummond G. I. A modified assay of 3':5'-cyclic-AMP phosphodiesterase. Anal Biochem. 1975 Feb;63(2):388–399. doi: 10.1016/0003-2697(75)90361-9. [DOI] [PubMed] [Google Scholar]
- Brackenbury R., Sussman M. Mutant of Dictyostelium discoideum defective in cell contact regulation of enzyme expression. Cell. 1975 Apr;4(4):347–351. doi: 10.1016/0092-8674(75)90155-5. [DOI] [PubMed] [Google Scholar]
- Chung S., Landfear S. M., Blumberg D. D., Cohen N. S., Lodish H. F. Synthesis and stability of developmentally regulated dictyostelium mRNAs are affected by cell--cell contact and cAMP. Cell. 1981 Jun;24(3):785–797. doi: 10.1016/0092-8674(81)90104-5. [DOI] [PubMed] [Google Scholar]
- Coukell M. B. Parasexual genetic analysis of aggregation-deficient mutants of Dictyostelium discoideum. Mol Gen Genet. 1975 Dec 29;142(2):119–135. doi: 10.1007/BF00266094. [DOI] [PubMed] [Google Scholar]
- Frazier W. A., Rosen S. D., Reitherman R. W., Barondes S. H. Purification and comparison of two developmentally regulated lectins from Dictyostelium discoideum. Discoidin I and II. J Biol Chem. 1975 Oct 10;250(19):7714–7721. [PubMed] [Google Scholar]
- Geltosky J. E., Siu C. H., Lerner R. A. Glycoproteins of the plasma membrane of Dictyostelium discoideum during development. Cell. 1976 Jul;8(3):391–396. doi: 10.1016/0092-8674(76)90151-3. [DOI] [PubMed] [Google Scholar]
- Geltosky J. E., Weseman J., Bakke A., Lerner R. A. Identification of a cell surface glycoprotein involved in cell aggregation in D. discoideum. Cell. 1979 Oct;18(2):391–398. doi: 10.1016/0092-8674(79)90058-8. [DOI] [PubMed] [Google Scholar]
- Henderson E. J. The cyclic adenosine 3':5'-monophosphate receptor of Dictyostelium discoideum. Binding characteristics of aggregation-competent cells and variation of binding levels during the life cycle. J Biol Chem. 1975 Jun 25;250(12):4730–4736. [PubMed] [Google Scholar]
- Hoffman S., McMahon D. The effects of inhibition of development in Dictyostelium discoideum on changes in plasma membrane composition and topography. Arch Biochem Biophys. 1978 Apr 15;187(1):12–24. doi: 10.1016/0003-9861(78)90002-4. [DOI] [PubMed] [Google Scholar]
- Huesgen A., Gerisch G. Solubilized contact sites a from cell membranes of Dictyostelium discoideum. FEBS Lett. 1975 Aug 1;56(1):46–49. doi: 10.1016/0014-5793(75)80108-6. [DOI] [PubMed] [Google Scholar]
- Jaffe A. R., Swan A. P., Garrod D. R. A ligand-receptor model for the cohesive behaviour of Dictyostelium discoideum axenic cells. J Cell Sci. 1979 Jun;37:157–167. doi: 10.1242/jcs.37.1.157. [DOI] [PubMed] [Google Scholar]
- Landfear S. M., Lodish H. F. A role for cyclic AMP in expression of developmentally regulated genes in Dictyostelium discoideum. Proc Natl Acad Sci U S A. 1980 Feb;77(2):1044–1048. doi: 10.1073/pnas.77.2.1044. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Loomis W. F. Biochemistry of Aggregation in Dictyostelium. A review. Dev Biol. 1979 May;70(1):1–12. doi: 10.1016/0012-1606(79)90002-2. [DOI] [PubMed] [Google Scholar]
- Loomis W. F., Jr Acetylglucosaminidase, an early enzyme in the development of Dictyostelium discoideum. J Bacteriol. 1969 Mar;97(3):1149–1154. doi: 10.1128/jb.97.3.1149-1154.1969. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mangiarotti G., Chung S., Zuker C., Lodish H. F. Selection and analysis of cloned developmentally-regulated Dictyostelium discoideum genes by hybridization-competition. Nucleic Acids Res. 1981 Feb 25;9(4):947–963. doi: 10.1093/nar/9.4.947. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Margolskee J. P., Froshauer S., Skrinska R., Lodish H. F. The effects of cell density and starvation on early developmental events in Dictyostelium discoideum. Dev Biol. 1980 Feb;74(2):409–421. doi: 10.1016/0012-1606(80)90442-x. [DOI] [PubMed] [Google Scholar]
- Margolskee J. P., Lodish H. F. Half-lives of messenger RNA species during growth and differentiation of Dictyostelium discoideum. Dev Biol. 1980 Jan;74(1):37–49. doi: 10.1016/0012-1606(80)90051-2. [DOI] [PubMed] [Google Scholar]
- Margolskee J. P., Lodish H. F. The regulation of the synthesis of actin and two other proteins induced early in Dictyostelium discoideum development. Dev Biol. 1980 Jan;74(1):50–64. doi: 10.1016/0012-1606(80)90052-4. [DOI] [PubMed] [Google Scholar]
- Marin F. T., Goyette-Boulay M., Rothman F. G. Regulation of development in Dictyostelium discoideum. III. Carbohydrate-specific intercellular interactions in early development. Dev Biol. 1980 Dec;80(2):301–312. doi: 10.1016/0012-1606(80)90406-6. [DOI] [PubMed] [Google Scholar]
- Müller K., Gerisch G. A specific glycoprotein as the target site of adhesion blocking Fab in aggregating Dictyostelium cells. Nature. 1978 Aug 3;274(5670):445–449. doi: 10.1038/274445a0. [DOI] [PubMed] [Google Scholar]
- Newell P. C., Franke J., Sussman M. Regulation of four functionally related enzymes during shifts in the developmental program of Dictyostelium discoideum. J Mol Biol. 1972 Feb 14;63(3):373–382. doi: 10.1016/0022-2836(72)90434-2. [DOI] [PubMed] [Google Scholar]
- Newell P. C., Longlands M., Sussman M. Control of enzyme synthesis by cellular interaction during development of the cellular slime mold Dictyostelium discoideum. J Mol Biol. 1971 Jun 14;58(2):541–554. doi: 10.1016/0022-2836(71)90370-6. [DOI] [PubMed] [Google Scholar]
- Okamoto K., Takeuchi I. Changes in activities of two developmentally regulated enzymes induced by disaggregation of the pseudoplasmodia of Dictyostelium discoideum. Biochem Biophys Res Commun. 1976 Sep 20;72(2):739–746. doi: 10.1016/s0006-291x(76)80101-5. [DOI] [PubMed] [Google Scholar]
- Pearson W. R., Davidson E. H., Britten R. J. A program for least squares analysis of reassociation and hybridization data. Nucleic Acids Res. 1977 Jun;4(6):1727–1737. doi: 10.1093/nar/4.6.1727. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ray J., Shinnick T., Lerner R. A mutation altering the function of a carbohydrate binding protein blocks cell-cell cohesion in developing Dictyostelium discoideum. Nature. 1979 May 17;279(5710):215–221. doi: 10.1038/279215a0. [DOI] [PubMed] [Google Scholar]
- Reitherman R. W., Rosen S. D., Frasier W. A., Barondes S. H. Cell surface species-specific high affinity receptors for discoidin: developmental regulation in Dictyostelium discoideum. Proc Natl Acad Sci U S A. 1975 Sep;72(9):3541–3545. doi: 10.1073/pnas.72.9.3541. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rosen S. D., Kafka J. A., Simpson D. L., Barondes S. H. Developmentally regulated, carbohydrate-binding protein in Dictyostelium discoideum. Proc Natl Acad Sci U S A. 1973 Sep;70(9):2554–2557. doi: 10.1073/pnas.70.9.2554. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rosen S. D., Kaur J., Clark D. L., Pardos B. T., Frazier W. A. Purification and characterization of multiple species (isolectins) of a slime mold lectin implicated in intercellular adhesion. J Biol Chem. 1979 Oct 10;254(19):9408–9415. [PubMed] [Google Scholar]
- Shinnick T. M., Lerner R. A. The cbpA gene: role of the 26,000-dalton carbohydrate-binding protein in intercellular cohesion of developing Dictyostelium discoideum cells. Proc Natl Acad Sci U S A. 1980 Aug;77(8):4788–4792. doi: 10.1073/pnas.77.8.4788. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Siu C. H., Lerner R. A., Ma G., Firtel R. A., Loomis W. F. Developmentally regulated proteins of the plasma membrane of Dictyostelium discoideum. The carbohydrate-binding protein. J Mol Biol. 1976 Jan 15;100(2):157–178. doi: 10.1016/s0022-2836(76)80146-5. [DOI] [PubMed] [Google Scholar]
- Smart J. E., Hynes R. O. Developmentally regulated cell surface alterations in Dictyostelium discoideum. Nature. 1974 Sep 27;251(5473):319–321. doi: 10.1038/251319a0. [DOI] [PubMed] [Google Scholar]
- Steinemann C., Parish R. W. Evidence that a developmentally regulated glycoprotein is target of adhesion-blocking Fab in reaggregating Dictyostelium. Nature. 1980 Aug 7;286(5773):621–623. doi: 10.1038/286621a0. [DOI] [PubMed] [Google Scholar]
- Weeks G. Studies of the cell surface of Dictyostelium discoideum during differentiation. The binding of 125I-concanavalin A to the cell surface. J Biol Chem. 1975 Sep 10;250(17):6706–6710. [PubMed] [Google Scholar]
- Wilcox D. K., Sussman M. Defective cell cohesivity expressed late in the development of a Dictyostelium discoideum mutant. Dev Biol. 1981 Feb;82(1):102–112. doi: 10.1016/0012-1606(81)90432-2. [DOI] [PubMed] [Google Scholar]
- Williams J. G., Lloyd M. M. Changes in the abundance of polyadenylated RNA during slime mould development measured using cloned molecular hybridization probes. J Mol Biol. 1979 Mar 25;129(1):19–35. doi: 10.1016/0022-2836(79)90056-1. [DOI] [PubMed] [Google Scholar]
- Williams J. G., Lloyd M. M., Devine J. M. Characterization and transcription analysis of a cloned sequence derived from a major developmentally regulated mRNA of D. discoideum. Cell. 1979 Aug;17(4):903–913. doi: 10.1016/0092-8674(79)90330-1. [DOI] [PubMed] [Google Scholar]
- Williams J. G., Tsang A. S., Mahbubani H. A change in the rate of transcription of a eukaryotic gene in response to cyclic AMP. Proc Natl Acad Sci U S A. 1980 Dec;77(12):7171–7175. doi: 10.1073/pnas.77.12.7171. [DOI] [PMC free article] [PubMed] [Google Scholar]