Summary
We analysed the expression of two genes encoding two different cysteine proteinases which show a high degree of homology and are regulated differentially during Dictyostelium discoideum development. While absent from growing vegetative cells, the two specific messengers RNAs appear at an early stage of development but accumulate in the polysomes at different later stages of development. The message coding for cysteine proteinase I reaches its maximum level after the aggregative period while cysteine proteinase II mRNA reaches its maximum during the culmination stage. At these times they represent 1% and 0.7%, respectively, of cellular mRNA and belong to the most abundant class of mRNAs.
No accumulation of the two messages elsewhere than in the polyribosomes was observed in the cytoplasm of the cells, whatever the stage of development analysed. Results of analysis of the nuclear levels of RNA complementary to the two genes are in agreement with the relative transcription rates determined by in vitro transcription of nuclei isolated at different stages. The combined results of these measurements demonstrate that the expression of the cysteine proteinase I and II genes is mainly under transcriptional control. However, the difference between the RNA synthetic rate in the nucleus and the accumulation of the mRNA in the cytoplasm, indicates an additional post-transcriptional regulation for the cysteine proteinase II gene.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Affara NA, Robert B, Jacquet M, Buckingham ME, Gros F (1980) Changes in gene expression during myogenic differentiation. J Mol Biol 140:441–458
Alton TH, Lodish HF (1977) Translational control of protein synthesis during the early stages of differentiation of the slime mold Dictyostelium discoideum. Cell 12:301–310
Batts-Young B, Lodish HF, Jacobson A (1980) Similarity of the primary sequences of ribosomal RNAs isolated from vegetative and developing cells of Dictyostelium discoideum. Dev Biol 78:352–364
Blumberg DD, Lodish HF (1980) Changes in the messenger RNA population during differentiation of Dictyostelium discoideum. Dev Biol 78:285–300
Bogdanovsky-Sequeval D, Ayala J, Mathieu M, Presse F, Felenbok B (1984) Characterization and regulation of the expression of a cloned sequence derived from a post aggregation regulated mRNA of Dictyostelium discoideum. Biol Cell 50:217–222
Charlesworth MC, Parish RW (1975) The isolation of nucleic and basic nucleoproteins from the cellular slime mold Dictyostelium discoideum. Eur J Biochem 54:307–316
Charlesworth MC, Parish RW (1977) Further studies on basic nucleoproteins from the cellular slime mold Dictyostelium discoideum. Eur J Biochem 75:241–250
Darnell JE (1982) Variety on the level of gene control in eukaryotic cells. Nature 297:365–371
Gal A, Nahon JL, Sala-Trepat JM (1983) Detection of rare RNA species in a complex RNA population by blot hybridization techniques: a comparative survey. Anal Biochem 132:190–194
Guyette WA, Matusik RJ, Rosen JM (1979) Prolactin mediated transcriptional and post-transcriptional control of casein gene expression. Cell 17:1013–1023
Jacobson A (1976) Analysis of messenger RNA transcription in Dictyostelium discoideum or slime mold messenger RNA: how to find it and what to do with it once you have got it. In: Last JA (ed) Methods in molecular biology, vol 8. Marcel Dekker Inc, New York, p 161–209
Jacobson A, Firtel RA, Lodish HF (1974a) Synthesis of messenger and ribosomal RNA precursors in isolated nucleic of the cellular slime mold. J Mol Biol 82:213–230
Jacobson A, Firtel RA, Lodish HF (1974b) Transcription of poly(dT) sequences in the genome of the cellular slime mold Dictyostelium discoideum. Proc Natl Acad Sci USA 71:1608–1611
Jacquet M, Part D, Felenbok B (1981) Changes in the polyadenylated messenger RNA population during development of Dictyostelium discoideum. Dev Biol 81:155–166
Julien J, Bogdanovsky-Sequeval D, Felenbok B, Jacquet M (1984) Expression of a spore specific gene in Dictyostelium discoideum. Cell Differ 15:37–42
Landfear SM, Lefebvre PA, Chung S, Lodish HF (1982) Transcriptional control of gene expression during development of Dictyostelium discoideum. Mol Cell Biol 2:1417–1426
Loomis WF (1982) The development of Dictyostelium discoideum. Academic Press Inc, New York
Ma GCl, Firtel RA (1978) Regulation of the synthesis of 2 carbohydrate binding proteins in Dictyostelium discoideum. J Biol Chem 253:3924–3932
Mangiarotti G, Chung S, Zucker C, Lodish HF (1981) Selection and analysis of cloned developmentally regulated Dictyostelium discoideum genes by hybridization-competition. Nucleic Acids Res 9:947–963
Mangiarotti G, Giorda R, Ceccarelli A, Perlo C (1985) mRNA stabilization control: the expression of a class of developmentally regulated genes in Dictyostelium discoideum. Proc Natl Acad Sci USA 82:5786–5790
Maniatis R, Fritsch EF, Sambrook J (1982) Molecular cloning. Cold Spring Harbor Laboratory, New York
Margolskee JP, Lodish HF (1980) The regulation of the synthesis of actin and two other proteins induced early in Dictyostelium discoideum development. Dev Biol 74:50–64
Nahon JL, Gal A, Frain M, Sell S, Sala-Trepat JM (1982) No evidence for post-transcriptional control of albumin and α-fetoprotein gene expression in developing rat liver and neoplasia. Nucleic Acids Res 10:1895–1911
North MJ (1982) Comparative biochemistry of the proteinases of eukaryotic micro-organisms. Microbiol Rev 46:308–340
North MJ (1985) Cysteine proteinases of cellular slime moulds. Biochem Soc Trans 13:288–290
F'Farrell PH (1975) High resolution two-dimensional electrophoresis of proteins. J Biol Chem 250:4007–4021
Pelham RB, Jackson RJ (1976) An efficient mRNA-dependent translation system from reticulocyte lysates. Eur J Biochem 67:247–256
Presse F, Bogdanovsky-Sequeval D, Mathieu M, Felenbok B (1986) Structural analysis of a developmentally regulated sequence encoding for a cysteine proteinase in Dictyostelium discoideum. Mol Gen Genet 203:324–332
Rigby PWJ, Dieckmann M, Rhodes C, Berg P (1977) Labeling deoxyribonucleic acid to high specific activity in vitro by nick translation with DNA polymerase I. J Mol Biol 113:237–251
Rowekamp W, Poole S, Firtel RA (1980) Analysis of the multigene family coding the developmentally regulated carbohydrate binding protein discoidin i in D. discoideum. Cell 20:495–505
Takio K, Towatari T, Katunuma N, Teller DC, Titani K (1983) Homology of amino acid sequences of rat liver cathepsins B and H with that of papain. Proc Natl Acad Sci USA 80:3666–3670
Vieira J, Messing J (1982) The pUC plasmids, an M13mp7-derived system for insertion mutagenesis and sequencing with synthetic universal primers. Gene 19:259–268
Williams JG, Lloyd MM (1979a) Changes in the abundance of polyadenylated RNA during slime mould development measured using cloned molecular hybridization probes. J Mol Biol 129:19–35
Williams JG, Lloyd MM, Levine JM (1979b) Characterization and transcription analysis of a cloned sequence derived from a major developmentally regulated mRNA of D. discoideum. Cell 17:903–913
Williams JG, North MJ, Mahbubani H (1985) A developmentally regulated cysteine proteinase in Dictyostelium discoideum. EMBO J 4:999–1006
Wolfgang N, Firtel RA (1985) High copy number transformants and co-transformation in Dictyostelium. Gene, in press
Author information
Authors and Affiliations
Additional information
Communicated by W. Gajewski
Rights and permissions
About this article
Cite this article
Presse, F., Bogdanovsky-Sequeval, D., Mathieu, M. et al. Analysis of the expression of two genes of Dictyostelium discoideum which code for developmentally regulated cysteine proteinases. Molec Gen Genet 203, 333–340 (1986). https://doi.org/10.1007/BF00333976
Received:
Issue Date:
DOI: https://doi.org/10.1007/BF00333976