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. 1998 Feb 15;330(Pt 1):139–147. doi: 10.1042/bj3300139

Oscillating response to a purine nucleotide disrupted by mutation in Paramecium tetraurelia.

J L Mimikakis 1, D L Nelson 1, R R Preston 1
PMCID: PMC1219119  PMID: 9461502

Abstract

The purine nucleotide GTP, when added extracellularly, induces oscillations in the swimming behaviour of the protist Paramecium tetraurelia. For periods as long as 10 min the cell swims backwards and forwards repetitively. The oscillations in swimming behaviour are driven by changes in membrane potential of the cell, which in turn are caused by periodic activation of inward Mg2+- and Na+-specific currents. We screened for and isolated mutants that are defective in this response, exploiting the fact that the net result of GTP on a population of cells is repulsion. One mutant, GTP-insensitive (gin A), is not repelled by GTP. In addition, GTP fails to induce repetitive backwards swimming in gin A mutants, although they swim backwards normally in response to other stimuli. GTP fails to evoke oscillations in membrane potential or Mg2+ and Na+ currents in the mutant, although the Mg2+ and Na+ conductances are not themselves measurably affected. A small, oscillating Ca2+ current induced by GTP in the wild type, which might be part of the mechanism that generates oscillations, is also missing from gin A cells. To our knowledge, gin A is the first example of a mutant defective in a purinergic response. We discuss the possibility that the gin A lesion affects the oscillator itself.

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Selected References

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  1. Berridge M. J. Calcium oscillations. J Biol Chem. 1990 Jun 15;265(17):9583–9586. [PubMed] [Google Scholar]
  2. Bootman M. D., Berridge M. J. The elemental principles of calcium signaling. Cell. 1995 Dec 1;83(5):675–678. doi: 10.1016/0092-8674(95)90179-5. [DOI] [PubMed] [Google Scholar]
  3. Clark K. D., Hennessey T. M., Nelson D. L. External GTP alters the motility and elicits an oscillating membrane depolarization in Paramecium tetraurelia. Proc Natl Acad Sci U S A. 1993 May 1;90(9):3782–3786. doi: 10.1073/pnas.90.9.3782. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Clark K. D., Hennessey T. M., Nelson D. L., Preston R. R. Extracellular GTP causes membrane-potential oscillations through the parallel activation of Mg2+ and Na+ currents in Paramecium tetraurelia. J Membr Biol. 1997 May 15;157(2):159–167. doi: 10.1007/s002329900225. [DOI] [PubMed] [Google Scholar]
  5. Dixon C. J., Cobbold P. H., Green A. K. Oscillations in cytosolic free Ca2+ induced by ADP and ATP in single rat hepatocytes display differential sensitivity to application of phorbol ester. Biochem J. 1995 Jul 1;309(Pt 1):145–149. doi: 10.1042/bj3090145. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Dubyak G. R., el-Moatassim C. Signal transduction via P2-purinergic receptors for extracellular ATP and other nucleotides. Am J Physiol. 1993 Sep;265(3 Pt 1):C577–C606. doi: 10.1152/ajpcell.1993.265.3.C577. [DOI] [PubMed] [Google Scholar]
  7. Eckert R. Bioelectric control of ciliary activity. Science. 1972 May 5;176(4034):473–481. doi: 10.1126/science.176.4034.473. [DOI] [PubMed] [Google Scholar]
  8. Edwards F. A., Gibb A. J., Colquhoun D. ATP receptor-mediated synaptic currents in the central nervous system. Nature. 1992 Sep 10;359(6391):144–147. doi: 10.1038/359144a0. [DOI] [PubMed] [Google Scholar]
  9. Evans R. J., Derkach V., Surprenant A. ATP mediates fast synaptic transmission in mammalian neurons. Nature. 1992 Jun 11;357(6378):503–505. doi: 10.1038/357503a0. [DOI] [PubMed] [Google Scholar]
  10. Francis J. T., Hennessey T. M. Chemorepellents in Paramecium and Tetrahymena. J Eukaryot Microbiol. 1995 Jan-Feb;42(1):78–83. doi: 10.1111/j.1550-7408.1995.tb01544.x. [DOI] [PubMed] [Google Scholar]
  11. Fredholm B. B., Abbracchio M. P., Burnstock G., Dubyak G. R., Harden T. K., Jacobson K. A., Schwabe U., Williams M. Towards a revised nomenclature for P1 and P2 receptors. Trends Pharmacol Sci. 1997 Mar;18(3):79–82. doi: 10.1016/s0165-6147(96)01038-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Harootunian A. T., Kao J. P., Tsien R. Y. Agonist-induced calcium oscillations in depolarized fibroblasts and their manipulation by photoreleased Ins(1,4,5)P3, Ca++, and Ca++ buffer. Cold Spring Harb Symp Quant Biol. 1988;53(Pt 2):935–943. doi: 10.1101/sqb.1988.053.01.108. [DOI] [PubMed] [Google Scholar]
  13. Hennessey T. M., Kim M. Y., Satir B. H. Lysozyme acts as a chemorepellent and secretagogue in Paramecium by activating a novel receptor-operated Ca++ conductance. J Membr Biol. 1995 Nov;148(1):13–25. doi: 10.1007/BF00234152. [DOI] [PubMed] [Google Scholar]
  14. Hinrichsen R. D. Calcium and calmodulin in the control of cellular behavior and motility. Biochim Biophys Acta. 1993 Dec 23;1155(3):277–293. doi: 10.1016/0304-419x(93)90010-a. [DOI] [PubMed] [Google Scholar]
  15. Hinrichsen R. D., Saimi Y., Hennessey T., Kung C. Mutants in paramecium tetraurelia defective in their axonemal response to calcium. Cell Motil. 1984;4(4):283–295. doi: 10.1002/cm.970040406. [DOI] [PubMed] [Google Scholar]
  16. Hinrichsen R. D., Saimi Y., Kung C. Mutants with altered Ca2+-channel properties in Paramecium tetraurelia: isolation, characterization and genetic analysis. Genetics. 1984 Nov;108(3):545–558. doi: 10.1093/genetics/108.3.545. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Kastritsis C. H., Salm A. K., McCarthy K. Stimulation of the P2Y purinergic receptor on type 1 astroglia results in inositol phosphate formation and calcium mobilization. J Neurochem. 1992 Apr;58(4):1277–1284. doi: 10.1111/j.1471-4159.1992.tb11339.x. [DOI] [PubMed] [Google Scholar]
  18. Kung C. Genic mutants with altered system of excitation in Paramecium aurelia. II. Mutagenesis, screening and genetic analysis of the mutants. Genetics. 1971 Sep;69(1):29–45. doi: 10.1093/genetics/69.1.29. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Lefort-Tran M., Aufderheide K., Pouphile M., Rossignol M., Beisson J. Control of exocytotic processes: cytological and physiological studies of trichocyst mutants in Paramecium tetraurelia. J Cell Biol. 1981 Feb;88(2):301–311. doi: 10.1083/jcb.88.2.301. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Meyer T., Stryer L. Calcium spiking. Annu Rev Biophys Biophys Chem. 1991;20:153–174. doi: 10.1146/annurev.bb.20.060191.001101. [DOI] [PubMed] [Google Scholar]
  21. Oertel D., Schein S. J., Kung C. Separation of membrane currents using a Paramecium mutant. Nature. 1977 Jul 14;268(5616):120–124. doi: 10.1038/268120a0. [DOI] [PubMed] [Google Scholar]
  22. Plattner H., Braun C., Klauke N., Länge S. Veratridine triggers exocytosis in Paramecium cells by activating somatic Ca channels. J Membr Biol. 1994 Nov;142(2):229–240. doi: 10.1007/BF00234945. [DOI] [PubMed] [Google Scholar]
  23. Preston R. R. A magnesium current in Paramecium. Science. 1990 Oct 12;250(4978):285–288. doi: 10.1126/science.2218533. [DOI] [PubMed] [Google Scholar]
  24. Preston R. R. Genetic dissection of Ca2(+)-dependent ion channel function in Paramecium. Bioessays. 1990 Jun;12(6):273–281. doi: 10.1002/bies.950120605. [DOI] [PubMed] [Google Scholar]
  25. Preston R. R., Kung C. Inhibition of Mg2+ current by single-gene mutation in Paramecium. J Membr Biol. 1994 May;139(3):203–213. doi: 10.1007/BF00232624. [DOI] [PubMed] [Google Scholar]
  26. Preston R. R., Kung C. Isolation and characterization of paramecium mutants defective in their response to magnesium. Genetics. 1994 Jul;137(3):759–769. doi: 10.1093/genetics/137.3.759. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Preston R. R., Saimi Y., Kung C. Calcium current activated upon hyperpolarization of Paramecium tetraurelia. J Gen Physiol. 1992 Aug;100(2):233–251. doi: 10.1085/jgp.100.2.233. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Richard E. A., Hinrichsen R. D., Kung C. A single gene mutation that affects a potassium conductance and resting membrane potential in Paramecium. J Neurogenet. 1985 Sep;2(4):239–252. doi: 10.3109/01677068509102321. [DOI] [PubMed] [Google Scholar]
  29. Saimi Y., Kung C. Behavioral genetics of Paramecium. Annu Rev Genet. 1987;21:47–65. doi: 10.1146/annurev.ge.21.120187.000403. [DOI] [PubMed] [Google Scholar]
  30. Stelly N., Mauger J. P., Claret M., Adoutte A. Cortical alveoli of Paramecium: a vast submembranous calcium storage compartment. J Cell Biol. 1991 Apr;113(1):103–112. doi: 10.1083/jcb.113.1.103. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Tomić M., Jobin R. M., Vergara L. A., Stojilkovic S. S. Expression of purinergic receptor channels and their role in calcium signaling and hormone release in pituitary gonadotrophs. Integration of P2 channels in plasma membrane- and endoplasmic reticulum-derived calcium oscillations. J Biol Chem. 1996 Aug 30;271(35):21200–21208. doi: 10.1074/jbc.271.35.21200. [DOI] [PubMed] [Google Scholar]
  32. Tsien R. W., Tsien R. Y. Calcium channels, stores, and oscillations. Annu Rev Cell Biol. 1990;6:715–760. doi: 10.1146/annurev.cb.06.110190.003435. [DOI] [PubMed] [Google Scholar]
  33. Vuorinen P., Wu X., Arvola P., Vapaatalo H., Pörsti I. Effects of P1 and P2Y purinoceptor antagonists on endothelium-dependent and -independent relaxations of rat mesenteric artery to GTP and guanosine. Br J Pharmacol. 1994 May;112(1):71–74. doi: 10.1111/j.1476-5381.1994.tb13031.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Weiss T., Gheber L., Shoshan-Barmatz V., Priel Z. Possible mechanism of ciliary stimulation by extracellular ATP: involvement of calcium-dependent potassium channels and exogenous Ca2+. J Membr Biol. 1992 May;127(3):185–193. doi: 10.1007/BF00231506. [DOI] [PubMed] [Google Scholar]
  35. Wright M. V., Elwess N., Van Houten J. Ca2+ transport and chemoreception in Paramecium. J Comp Physiol B. 1993;163(4):288–296. doi: 10.1007/BF00347779. [DOI] [PubMed] [Google Scholar]

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