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. 1980 Jun 1;85(3):910–915. doi: 10.1083/jcb.85.3.910

Evidence for a pronounced secretion of cyclic AMP by Tetrahymena

PMCID: PMC2111456  PMID: 6248569

Abstract

The unicellular eukaryote Tetrahymena pyriformis secretes significant amounts of cyclic AMP into its external medium. Cells transferred from growth medium into any of the following three different non-nutrient media: (a) 5 mM phosphate buffer containing 47 mM NaCl and 1 mM MgSO4, (b) 10 mM Tris, or (c) 1.3 mM Tris containing 1 mM citrate and 1 mM Ca(OH)2, released to the outside almost 60--80% of the total cyclic AMP produced during 2--5 h of incubation. Tris-citrate-Ca+2 medium was chosen for further experiments because of its minimal nonspecific interference in the cyclic AMP radioimmunoassay. The identity of the secreted material recognized as cyclic AMP by radioimmunoassay was confirmed by demonstrating its almost complete hydrolysis with commerical beef heart phosphodiesterase. Furthermore, the radioimmunoassay-active material in the concentrated medium co- chromatographed on paper with [3H]cyclic AMP, as judged by assay of the eluted material. After resuspending cells in Tris-citrate-Ca2+ medium, the extracellular concentration of cyclic AMP rose steadily over a 5-h period, reaching a level equvalent to approximately 35--50 pmol cyclic AMP/10(6) cells vs. an internal cyclic AMP quantity at 5 h of 8--10 pmol/10(6) cells. After 5 h, the level of extracellular cyclic AMP reached a plateau. There was no degradation or uptake of external cyclic AMP by the cells during this period.

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Selected References

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  1. Allewell N. M., Oles J., Wolfe J. A physicochemical analysis of conjugation in Tetrahymena pyriformis. Exp Cell Res. 1976 Feb;97(2):394–405. doi: 10.1016/0014-4827(76)90631-5. [DOI] [PubMed] [Google Scholar]
  2. Bonner J. T., Hall E. M., Noller S., Oleson F. B., Jr, Roberts A. B. Synthesis of cyclic AMP and phosphodiesterase in various species of cellular slime molds and its bearing on chemotaxis and differentiation. Dev Biol. 1972 Dec;29(4):402–409. doi: 10.1016/0012-1606(72)90080-2. [DOI] [PubMed] [Google Scholar]
  3. Bruns P. J., Palestine R. F. Costimulation in Tetrahymena pyriformis: a developmental interaction between specially prepared cells. Dev Biol. 1975 Jan;42(1):75–83. doi: 10.1016/0012-1606(75)90315-2. [DOI] [PubMed] [Google Scholar]
  4. Brunton L. L., Mayer S. E. Extrusion of cyclic AMP from pigeon erythrocytes. J Biol Chem. 1979 Oct 10;254(19):9714–9720. [PubMed] [Google Scholar]
  5. DAVOREN P. R., SUTHERLAND E. W. THE EFFECT OF L-EPINEPHRINE AND OTHER AGENTS ON THE SYNTHESIS AND RELEASE OF ADENOSINE 3',5'-PHOSPHATE BY WHOLE PIGEON ERYTHROCYTES. J Biol Chem. 1963 Sep;238:3009–3015. [PubMed] [Google Scholar]
  6. Dickinson J. R., Graves M. G., Swoboda B. E. Cyclic AMP metabolism in the cell cycle of Tetrahymena pyriformis. FEBS Lett. 1976 Jun 1;65(2):152–154. doi: 10.1016/0014-5793(76)80468-1. [DOI] [PubMed] [Google Scholar]
  7. HAMBURGER K., ZEUTHEN E. Synchronous divisions in Tetrahymena pyriformis as studied in an inorganic medium; the effect of 2,4-dinitrophenol. Exp Cell Res. 1957 Dec;13(3):443–453. doi: 10.1016/0014-4827(57)90074-5. [DOI] [PubMed] [Google Scholar]
  8. Hanna M. H., Klein C., Cox E. Cyclic nucleotides and cyclic nucleotide phosphodiesterase during development of Polysphondylium violaceum. Exp Cell Res. 1979 Sep;122(2):265–271. doi: 10.1016/0014-4827(79)90303-3. [DOI] [PubMed] [Google Scholar]
  9. Hausmann K. Extrusive organelles in protists. Int Rev Cytol. 1978;52:197–276. doi: 10.1016/s0074-7696(08)60757-3. [DOI] [PubMed] [Google Scholar]
  10. Hood E. E., Armour S., Ownby J. D., Handa A. K., Bressan R. A. Effect of nitrogen starvation on the level of adenosine 3',5'-monophosphate in Anabaena variabilis. Biochim Biophys Acta. 1979 Dec 3;588(2):193–200. doi: 10.1016/0304-4165(79)90202-2. [DOI] [PubMed] [Google Scholar]
  11. Kelly L. A., Butcher R. W. The effects of epinephrine and prostaglandin E-1 on cyclic adenosine 3':5'-monophosphate levels in WI-38 fibroblasts. J Biol Chem. 1974 May 25;249(10):3098–3102. [PubMed] [Google Scholar]
  12. Konijn T. M., Van De Meene J. G., Bonner J. T., Barkley D. S. The acrasin activity of adenosine-3',5'-cyclic phosphate. Proc Natl Acad Sci U S A. 1967 Sep;58(3):1152–1154. doi: 10.1073/pnas.58.3.1152. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Nandini-Kishore S. G., Thompson G. A., Jr Increased levels of adenosine 3',5'-cyclic monophosphate in Tetrahymena stimulated by glucose and mediated by Ca2+ and epinephrine. Proc Natl Acad Sci U S A. 1979 Jun;76(6):2708–2711. doi: 10.1073/pnas.76.6.2708. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Nelsen E. M., Debault L. E. Transformation in Tetrahymena pyriformis: description of an inducible phenotype. J Protozool. 1978 Feb;25(1):113–119. doi: 10.1111/j.1550-7408.1978.tb03880.x. [DOI] [PubMed] [Google Scholar]
  15. Nelsen E. M. Transformation in Tetrahymena thermophila. Development of an inducible phenotype. Dev Biol. 1978 Sep;66(1):17–31. doi: 10.1016/0012-1606(78)90270-1. [DOI] [PubMed] [Google Scholar]
  16. Peterkofsky A., Gazdar C. Glucose and the metabolism of adenosine 3':5'-cyclic monophosphate in Escherichia coli. Proc Natl Acad Sci U S A. 1971 Nov;68(11):2794–2798. doi: 10.1073/pnas.68.11.2794. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Rindler M. J., Bashor M. M., Spitzer N., Saier M. H., Jr Regulation of adenosine 3':5'-monophosphate efflux from animal cells. J Biol Chem. 1978 Aug 10;253(15):5431–5436. [PubMed] [Google Scholar]
  18. Rosen O. M. Interaction of cyclic GMP and cyclic AMP with a cyclic nucleotide phosphodiesterase of the frog erythrocyte. Arch Biochem Biophys. 1970 Aug;139(2):447–449. doi: 10.1016/0003-9861(70)90498-4. [DOI] [PubMed] [Google Scholar]
  19. Rozensweig Z., Kindler S. H. Epinephrine and serotonin activation of adenyl cyclase from Tetrahymena pyriformis. FEBS Lett. 1972 Sep 15;25(2):221–223. doi: 10.1016/0014-5793(72)80489-7. [DOI] [PubMed] [Google Scholar]
  20. Steiner A. L., Kipnis D. M., Utiger R., Parker C. Radioimmunoassay for the measurement of adenosine 3',5'-cyclic phosphate. Proc Natl Acad Sci U S A. 1969 Sep;64(1):367–373. doi: 10.1073/pnas.64.1.367. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Thompson G. A., Jr Studies of membrane formation in Tetrahymena pyriformis. I. Rates of phospholipid biosynthesis. Biochemistry. 1967 Jul;6(7):2015–2022. doi: 10.1021/bi00859a020. [DOI] [PubMed] [Google Scholar]
  22. Van Houten J. Membrane potential changes during chemokinesis in Paramecium. Science. 1979 Jun 8;204(4397):1100–1103. doi: 10.1126/science.572085. [DOI] [PubMed] [Google Scholar]
  23. Voichick J., Elson C., Granner D., Shrago E. Relationship of adenosine 3',5'-monophosphate to growth and metabolism of Tetrahymena pyriformis. J Bacteriol. 1973 Jul;115(1):68–72. doi: 10.1128/jb.115.1.68-72.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]

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