EMBO J 11(8): 2849-2854
DIF-1 induces its own breakdown in Dictyostelium.
Abstract
DIF-1 is a novel chlorinated alkyl phenone which induces differentiation of prestalk cells in Dictyostelium discoideum. It is broken down and inactivated by a cytoplasmic enzyme, DIF-1 3(5)-dechlorinase (hereafter referred to as DIF-1 dechlorinase), which is found only in prestalk cells. We show that DIF-1 dechlorinase levels are induced at least 50-fold when cells are treated with DIF-1. This response is rapid--enzyme activity doubles within 15 min and is fully induced within an hour--and occurs early in development, before other prestalk markers can be induced by DIF-1. Maximum inducibility is seen towards the end of aggregation, when DIF-1 dechlorinase is barely detectable in uninduced cells. The dose-dependence reveals a threshold concentration of DIF-1 (15 nM) below which almost no response is seen. Cyclic AMP, which is the chemoattractant during aggregation and plays a key role in later development, suppresses the induction of DIF-1 dechlorinase by DIF-1. We conclude that induction of DIF-1 dechlorinase is one of the first steps on the developmental pathway which leads to prestalk cell differentiation, and suggest that the resulting negative feedback on DIF-1 levels is an important part of the mechanism by which cells decide whether to become prestalk or prespore cells.
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- Kay RR. Gene expression in Dictyostelium discoidium: mutually antagonistic roles of cyclic-AMP and ammonia. J Embryol Exp Morphol. 1979 Aug;52:171–182. [PubMed] [Google Scholar]
- Kay RR, Jermyn KA. A possible morphogen controlling differentiation in Dictyostelium. Nature. 1983 May 19;303(5914):242–244. [PubMed] [Google Scholar]
- Kay RR, Garrod D, Tilly R. Requirement for cell differentiation in Dictyostelium discoideum. Nature. 1978 Jan 5;271(5640):58–60. [PubMed] [Google Scholar]
- Kimmel AR. Different molecular mechanisms for cAMP regulation of gene expression during Dictyostelium development. Dev Biol. 1987 Jul;122(1):163–171. [PubMed] [Google Scholar]
- Kay RR, Berks M, Traynor D. Morphogen hunting in Dictyostelium. Development. 1989;107 (Suppl):81–90. [PubMed] [Google Scholar]
- Klein C. cAMP-independent oscillations of adenylate cyclase in Dictyostelium discoideum. Dev Biol. 1980 Oct;79(2):500–507. [PubMed] [Google Scholar]
- Kopachik W, Oohata A, Dhokia B, Brookman JJ, Kay RR. Dictyostelium mutants lacking DIF, a putative morphogen. Cell. 1983 Jun;33(2):397–403. [PubMed] [Google Scholar]
- Kopachik WJ, Dhokia B, Kay RR. Selective induction of stalk-cell-specific proteins in Dictyostelium. Differentiation. 1985;28(3):209–216. [PubMed] [Google Scholar]
- Kwong L, Xie YJ, Daniel J, Robbins SM, Weeks G. A Dictyostelium morphogen that is essential for stalk cell formation is generated by a subpopulation of prestalk cells. Development. 1990 Sep;110(1):303–310. [PubMed] [Google Scholar]
- Meinhardt H. A model for the prestalk/prespore patterning in the slug of the slime mold Dictyostelium discoideum. Differentiation. 1983;24(3):191–202. [PubMed] [Google Scholar]
- Morris HR, Taylor GW, Masento MS, Jermyn KA, Kay RR. Chemical structure of the morphogen differentiation inducing factor from Dictyostelium discoideum. Nature. 328(6133):811–814. [PubMed] [Google Scholar]
- Morris HR, Masento MS, Taylor GW, Jermyn KA, Kay RR. Structure elucidation of two differentiation inducing factors (DIF-2 and DIF-3) from the cellular slime mould Dictyostelium discoideum. Biochem J. 1988 Feb 1;249(3):903–906.[PMC free article] [PubMed] [Google Scholar]
- Struhl G, Struhl K, Macdonald PM. The gradient morphogen bicoid is a concentration-dependent transcriptional activator. Cell. 1989 Jun 30;57(7):1259–1273. [PubMed] [Google Scholar]
- Town CD, Gross JD, Kay RR. Cell differentiation without morphogenesis in Dictyostelium discoideum. Nature. 1976 Aug 19;262(5570):717–719. [PubMed] [Google Scholar]
- Traynor D, Kay RR. The DIF-1 signaling system in Dictyostelium. Metabolism of the signal. J Biol Chem. 1991 Mar 15;266(8):5291–5297. [PubMed] [Google Scholar]
- Watts DJ, Ashworth JM. Growth of myxameobae of the cellular slime mould Dictyostelium discoideum in axenic culture. Biochem J. 1970 Sep;119(2):171–174.[PMC free article] [PubMed] [Google Scholar]
- Wilcox M, Mitchison GJ, Smith RJ. Pattern formation in the blue-green alga, Anabaena. I. Basic mechanisms. J Cell Sci. 1973 May;12(3):707–723. [PubMed] [Google Scholar]
- Williams JG, Ceccarelli A, McRobbie S, Mahbubani H, Kay RR, Early A, Berks M, Jermyn KA. Direct induction of Dictyostelium prestalk gene expression by DIF provides evidence that DIF is a morphogen. Cell. 1987 Apr 24;49(2):185–192. [PubMed] [Google Scholar]
- Williams JG, Duffy KT, Lane DP, McRobbie SJ, Harwood AJ, Traynor D, Kay RR, Jermyn KA. Origins of the prestalk-prespore pattern in Dictyostelium development. Cell. 1989 Dec 22;59(6):1157–1163. [PubMed] [Google Scholar]
- Berks M, Kay RR. Combinatorial control of cell differentiation by cAMP and DIF-1 during development of Dictyostelium discoideum. Development. 1990 Nov;110(3):977–984. [PubMed] [Google Scholar]
- Brookman JJ, Town CD, Jermyn KA, Kay RR. Developmental regulation of a stalk cell differentiation-inducing factor in Dictyostelium discoideum. Dev Biol. 1982 May;91(1):191–196. [PubMed] [Google Scholar]
- Brookman JJ, Jermyn KA, Kay RR. Nature and distribution of the morphogen DIF in the Dictyostelium slug. Development. 1987 May;100(1):119–124. [PubMed] [Google Scholar]
- Early AE, Williams JG. A Dictyostelium prespore-specific gene is transcriptionally repressed by DIF in vitro. Development. 1988 Jul;103(3):519–524. [PubMed] [Google Scholar]
- Gerisch G. Cyclic AMP and other signals controlling cell development and differentiation in Dictyostelium. Annu Rev Biochem. 1987;56:853–879. [PubMed] [Google Scholar]
- Green JB, Smith JC. Graded changes in dose of a Xenopus activin A homologue elicit stepwise transitions in embryonic cell fate. Nature. 1990 Sep 27;347(6291):391–394. [PubMed] [Google Scholar]
- Insall R, Kay RR. A specific DIF binding protein in Dictyostelium. EMBO J. 1990 Oct;9(10):3323–3328.[PMC free article] [PubMed] [Google Scholar]
- Jermyn KA, Duffy KT, Williams JG. A new anatomy of the prestalk zone in Dictyostelium. Nature. 1989 Jul 13;340(6229):144–146. [PubMed] [Google Scholar]