Skip to main content
NCBI home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1992 Sep 1;89(17):8025–8029. doi: 10.1073/pnas.89.17.8025

ATP-driven Ca2+/H+ antiport in acid vesicles from Dictyostelium.

E K Rooney 1, J D Gross 1
PMCID: PMC49848  PMID: 1387710

Abstract

Amoebae of the cellular slime mold Dictyostelium discoideum possess an extensive and dynamic endomembrane system that includes many types of acidic vacuoles. A light membrane fraction from Dictyostelium, rich in vacuolar-type H(+)-ATPase, has been described [Padh, H., Lavasa, M. & Steck, T.L. (1989) J. Cell Biol. 108, 865-874]. Here, we show that this "acidosomal" fraction also contains a high-affinity vanadate-sensitive Ca2+ uptake activity that is stimulated by the pH gradient formed by the H(+)-ATPase. We attribute this Ca2+ uptake to the presence of a H(+)-countertransporting Ca(2+)-ATPase, pumping Ca2+ into an acidic compartment.

Full text

PDF
8025

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Blackford S., Rea P. A., Sanders D. Voltage sensitivity of H+/Ca2+ antiport in higher plant tonoplast suggests a role in vacuolar calcium accumulation. J Biol Chem. 1990 Jun 15;265(17):9617–9620. [PubMed] [Google Scholar]
  2. Bowman E. J., Siebers A., Altendorf K. Bafilomycins: a class of inhibitors of membrane ATPases from microorganisms, animal cells, and plant cells. Proc Natl Acad Sci U S A. 1988 Nov;85(21):7972–7976. doi: 10.1073/pnas.85.21.7972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Brüne B., Ullrich V. Different calcium pools in human platelets and their role in thromboxane A2 formation. J Biol Chem. 1991 Oct 15;266(29):19232–19237. [PubMed] [Google Scholar]
  4. Europe-Finner G. N., Newell P. C. Inositol 1,4,5-triphosphate induces calcium release from a non- mitochondrial pool in amoebae of Dictyostelium. Biochim Biophys Acta. 1986 Aug 1;887(3):335–340. doi: 10.1016/0167-4889(86)90163-1. [DOI] [PubMed] [Google Scholar]
  5. Feit I. N., Bonner J. T., Suthers H. B. Regulation of the anterior-like cell state by ammonia in Dictyostelium discoideum. Dev Genet. 1990;11(5-6):442–446. doi: 10.1002/dvg.1020110519. [DOI] [PubMed] [Google Scholar]
  6. Gross J. D., Bradbury J., Kay R. R., Peacey M. J. Intracellular pH and the control of cell differentiation in Dictyostelium discoideum. Nature. 1983 May 19;303(5914):244–245. doi: 10.1038/303244a0. [DOI] [PubMed] [Google Scholar]
  7. Gross J. D., Peacey M. J., von Strandmann R. P. Plasma membrane proton pump inhibition and stalk cell differentiation in Dictyostelium discoideum. Differentiation. 1988 Jul;38(2):91–98. doi: 10.1111/j.1432-0436.1988.tb00202.x. [DOI] [PubMed] [Google Scholar]
  8. Levy D., Seigneuret M., Bluzat A., Rigaud J. L. Evidence for proton countertransport by the sarcoplasmic reticulum Ca2(+)-ATPase during calcium transport in reconstituted proteoliposomes with low ionic permeability. J Biol Chem. 1990 Nov 15;265(32):19524–19534. [PubMed] [Google Scholar]
  9. Miller A. J., Vogg G., Sanders D. Cytosolic calcium homeostasis in fungi: roles of plasma membrane transport and intracellular sequestration of calcium. Proc Natl Acad Sci U S A. 1990 Dec;87(23):9348–9352. doi: 10.1073/pnas.87.23.9348. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Milne J. L., Coukell M. B. Identification of a high-affinity Ca2+ pump associated with endocytotic vesicles in Dictyostelium discoideum. Exp Cell Res. 1989 Nov;185(1):21–32. doi: 10.1016/0014-4827(89)90033-5. [DOI] [PubMed] [Google Scholar]
  11. Nolta K. V., Padh H., Steck T. L. Acidosomes from Dictyostelium. Initial biochemical characterization. J Biol Chem. 1991 Sep 25;266(27):18318–18323. [PubMed] [Google Scholar]
  12. Ohsumi Y., Anraku Y. Calcium transport driven by a proton motive force in vacuolar membrane vesicles of Saccharomyces cerevisiae. J Biol Chem. 1983 May 10;258(9):5614–5617. [PubMed] [Google Scholar]
  13. Padh H., Lavasa M., Steck T. L. Characterization of a vacuolar proton ATPase in Dictyostelium discoideum. Biochim Biophys Acta. 1989 Jul 10;982(2):271–278. doi: 10.1016/0005-2736(89)90064-3. [DOI] [PubMed] [Google Scholar]
  14. Padh H., Lavasa M., Steck T. L. Endosomes are acidified by association with discrete proton-pumping vacuoles in Dictyostelium. J Biol Chem. 1991 Mar 25;266(9):5514–5520. [PubMed] [Google Scholar]
  15. Padh H., Lavasa M., Steck T. L. Prelysosomal acidic vacuoles in Dictyostelium discoideum. J Cell Biol. 1989 Mar;108(3):865–874. doi: 10.1083/jcb.108.3.865. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Peterson G. L. A simplification of the protein assay method of Lowry et al. which is more generally applicable. Anal Biochem. 1977 Dec;83(2):346–356. doi: 10.1016/0003-2697(77)90043-4. [DOI] [PubMed] [Google Scholar]
  17. Pietrobon D., Di Virgilio F., Pozzan T. Structural and functional aspects of calcium homeostasis in eukaryotic cells. Eur J Biochem. 1990 Nov 13;193(3):599–622. doi: 10.1111/j.1432-1033.1990.tb19378.x. [DOI] [PubMed] [Google Scholar]
  18. Rooney E. K., Lee A. G. Binding of hydrophobic drugs to lipid bilayers and to the (Ca2+ + Mg2+)-ATPase. Biochim Biophys Acta. 1983 Jul 27;732(2):428–440. doi: 10.1016/0005-2736(83)90060-3. [DOI] [PubMed] [Google Scholar]
  19. Ruben L., Hutchinson A., Moehlman J. Calcium homeostasis in Trypanosoma brucei. Identification of a pH-sensitive non-mitochondrial calcium pool. J Biol Chem. 1991 Dec 25;266(36):24351–24358. [PubMed] [Google Scholar]
  20. Schindler J., Sussman M. Ammonia determines the choice of morphogenetic pathways in Dictyostelium discoideum. J Mol Biol. 1977 Oct 15;116(1):161–169. doi: 10.1016/0022-2836(77)90124-3. [DOI] [PubMed] [Google Scholar]
  21. Serrano R. Characterization of the plasma membrane ATPase of Saccharomyces cerevisiae. Mol Cell Biochem. 1978 Nov 30;22(1):51–63. doi: 10.1007/BF00241470. [DOI] [PubMed] [Google Scholar]
  22. Shorte S. L., Collingridge G. L., Randall A. D., Chappell J. B., Schofield J. G. Ammonium ions mobilize calcium from an internal pool which is insensitive to TRH and ionomycin in bovine anterior pituitary cells. Cell Calcium. 1991 Apr;12(4):301–312. doi: 10.1016/0143-4160(91)90004-x. [DOI] [PubMed] [Google Scholar]
  23. Thévenod F., Dehlinger-Kremer M., Kemmer T. P., Christian A. L., Potter B. V., Schulz I. Characterization of inositol 1,4,5-trisphosphate-sensitive (IsCaP) and -insensitive (IisCaP) nonmitochondrial Ca2+ pools in rat pancreatic acinar cells. J Membr Biol. 1989 Jul;109(2):173–186. doi: 10.1007/BF01870856. [DOI] [PubMed] [Google Scholar]
  24. Thévenod F., Schulz I. H+-dependent calcium uptake into an IP3-sensitive calcium pool from rat parotid gland. Am J Physiol. 1988 Oct;255(4 Pt 1):G429–G440. doi: 10.1152/ajpgi.1988.255.4.G429. [DOI] [PubMed] [Google Scholar]
  25. Virk S. S., Kirk C. J., Shears S. B. Ca2+ transport and Ca2+-dependent ATP hydrolysis by Golgi vesicles from lactating rat mammary glands. Biochem J. 1985 Mar 15;226(3):741–748. doi: 10.1042/bj2260741. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Warren G. B., Toon P. A., Birdsall N. J., Lee A. G., Metcalfe J. C. Reconstitution of a calcium pump using defined membrane components. Proc Natl Acad Sci U S A. 1974 Mar;71(3):622–626. doi: 10.1073/pnas.71.3.622. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Watts D. J., Ashworth J. M. Growth of myxameobae of the cellular slime mould Dictyostelium discoideum in axenic culture. Biochem J. 1970 Sep;119(2):171–174. doi: 10.1042/bj1190171. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Zhang G. H., Kraus-Friedmann N. The effects of Mg2+ on rat liver microsomal Ca2+ sequestration. Cell Calcium. 1990 Jun-Jul;11(6):397–403. doi: 10.1016/0143-4160(90)90051-u. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES