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. 1997 Feb;113(2):535–548. doi: 10.1104/pp.113.2.535

Distinction between Endoplasmic Reticulum-Type and Plasma Membrane-Type Ca2+ Pumps (Partial Purification of a 120-Kilodalton Ca2+-ATPase from Endomembranes).

I Hwang 1, D M Ratterman 1, H Sze 1
PMCID: PMC158170  PMID: 12223624

Abstract

Two biochemical types of Ca2+-pumping ATPases were distinguished in membranes that were isolated from carrot (Daucus carota) suspension-cultured cells. One type hydrolyzed GTP nearly as well as ATP, was stimulated by calmodulin, and was resistant to cyclopiazonic acid. This plasma membrane (PM)-type pump was associated with PMs and endomembranes, including vacuolar membranes and the endoplasmic reticulum (ER). Another pump ("ER-type") that was associated mainly with the ER hydrolyzed ATP preferentially, was insensitive to calmodulin, and was inhibited partially by cyclopiazonic acid, a blocker of the animal sarcoplasmic/ER Ca2+ pump. Oxalate stimulation of Ca2+ accumulation by ER-type, but not PM-type, pump(s) indicated a separation of the two types on distinct compartments. An endomembrane 120-kD Ca2+ pump was partially purified by calmodulin-affinity chromatography. The purified polypeptide bound calmodulin reacted with antibodies to a calmodulin-stimulated Ca2+ pump from cauliflower and displayed [32P]phosphoenzyme properties that are characteristic of PM-type Ca2+ pumps. The purified ATPase corresponded to a phosphoenzyme and a 120-kD calmodulin-binding protein on endomembranes. Another PM-type pump was suggested by a 127-kD PM-associated protein that bound calmodulin. Thus, both ER- and PM-type Ca2+ pumps coexist in most plant tissues, and each type can be distinguished from another by a set of traits, even in partially purified membranes.

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Selected References

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  1. Askerlund P., Evans D. E. Reconstitution and Characterization of a Calmodulin-Stimulated Ca-Pumping ATPase Purified from Brassica oleracea L. Plant Physiol. 1992 Dec;100(4):1670–1681. doi: 10.1104/pp.100.4.1670. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Askerlund P. Modulation of an Intracellular Calmodulin-Stimulated Ca2+-Pumping ATPase in Cauliflower by Trypsin (The Use of Calcium Green-5N to Measure Ca2+ Transport in Membrane Vesicles). Plant Physiol. 1996 Mar;110(3):913–922. doi: 10.1104/pp.110.3.913. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bergeron J. J., Brenner M. B., Thomas D. Y., Williams D. B. Calnexin: a membrane-bound chaperone of the endoplasmic reticulum. Trends Biochem Sci. 1994 Mar;19(3):124–128. doi: 10.1016/0968-0004(94)90205-4. [DOI] [PubMed] [Google Scholar]
  4. Briskin D. P. Ca-translocating ATPase of the plant plasma membrane. Plant Physiol. 1990 Oct;94(2):397–400. doi: 10.1104/pp.94.2.397. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Buckhout T. J. Characterization of Ca Transport in Purified Endoplasmic Reticulum Membrane Vesicles from Lepidium sativum L. Roots. Plant Physiol. 1984 Dec;76(4):962–967. doi: 10.1104/pp.76.4.962. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bush D. R., Sze H. Calcium transport in tonoplast and endoplasmic reticulum vesicles isolated from cultured carrot cells. Plant Physiol. 1986 Feb;80(2):549–555. doi: 10.1104/pp.80.2.549. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Camacho P., Lechleiter J. D. Increased frequency of calcium waves in Xenopus laevis oocytes that express a calcium-ATPase. Science. 1993 Apr 9;260(5105):226–229. doi: 10.1126/science.8385800. [DOI] [PubMed] [Google Scholar]
  8. Carafoli E. Calcium pump of the plasma membrane. Physiol Rev. 1991 Jan;71(1):129–153. doi: 10.1152/physrev.1991.71.1.129. [DOI] [PubMed] [Google Scholar]
  9. Carafoli E. The Ca2+ pump of the plasma membrane. J Biol Chem. 1992 Feb 5;267(4):2115–2118. [PubMed] [Google Scholar]
  10. Chen F. H., Ratterman D. M., Sze H. A Plasma Membrane-Type Ca2+-ATPase of 120 Kilodaltons on the Endoplasmic Reticulum from Carrot (Daucus carota) Cells (Properties of the Phosphorylated Intermediate). Plant Physiol. 1993 Jun;102(2):651–661. doi: 10.1104/pp.102.2.651. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Dupont F. M., Bush D. S., Windle J. J., Jones R. L. Calcium and proton transport in membrane vesicles from barley roots. Plant Physiol. 1990 Sep;94(1):179–188. doi: 10.1104/pp.94.1.179. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Ferrol N., Bennett A. B. A Single Gene May Encode Differentially Localized Ca2+-ATPases in Tomato. Plant Cell. 1996 Jul;8(7):1159–1169. doi: 10.1105/tpc.8.7.1159. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hsieh W. L., Pierce W. S., Sze H. Calcium-pumping ATPases in vesicles from carrot cells : stimulation by calmodulin or phosphatidylserine, and formation of a 120 kilodalton phosphoenzyme. Plant Physiol. 1991 Dec;97(4):1535–1544. doi: 10.1104/pp.97.4.1535. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Kincaid R. L., Billingsley M. L., Vaughan M. Preparation of fluorescent, cross-linking, and biotinylated calmodulin derivatives and their use in studies of calmodulin-activated phosphodiesterase and protein phosphatase. Methods Enzymol. 1988;159:605–626. doi: 10.1016/0076-6879(88)59058-4. [DOI] [PubMed] [Google Scholar]
  15. Maeshima M. Characterization of the major integral protein of vacuolar membrane. Plant Physiol. 1992 Apr;98(4):1248–1254. doi: 10.1104/pp.98.4.1248. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Perez-Prat E., Narasimhan M. L., Binzel M. L., Botella M. A., Chen Z., Valpuesta V., Bressan R. A., Hasegawa P. M. Induction of a Putative Ca-ATPase mRNA in NaCl-Adapted Cells. Plant Physiol. 1992 Nov;100(3):1471–1478. doi: 10.1104/pp.100.3.1471. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Rasi-Caldogno F., Carnelli A., De Michelis M. I. Identification of the Plasma Membrane Ca2+-ATPase and of Its Autoinhibitory Domain. Plant Physiol. 1995 May;108(1):105–113. doi: 10.1104/pp.108.1.105. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Rasi-Caldogno F., Carnelli A., De Michelis M. I. Plasma Membrane Ca-ATPase of Radish Seedlings : II. Regulation by Calmodulin. Plant Physiol. 1992 Mar;98(3):1202–1206. doi: 10.1104/pp.98.3.1202. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Rudolph H. K., Antebi A., Fink G. R., Buckley C. M., Dorman T. E., LeVitre J., Davidow L. S., Mao J. I., Moir D. T. The yeast secretory pathway is perturbed by mutations in PMR1, a member of a Ca2+ ATPase family. Cell. 1989 Jul 14;58(1):133–145. doi: 10.1016/0092-8674(89)90410-8. [DOI] [PubMed] [Google Scholar]
  20. Schatzmann H. J. The calcium pump of the surface membrane and of the sarcoplasmic reticulum. Annu Rev Physiol. 1989;51:473–485. doi: 10.1146/annurev.ph.51.030189.002353. [DOI] [PubMed] [Google Scholar]
  21. Seidler N. W., Jona I., Vegh M., Martonosi A. Cyclopiazonic acid is a specific inhibitor of the Ca2+-ATPase of sarcoplasmic reticulum. J Biol Chem. 1989 Oct 25;264(30):17816–17823. [PubMed] [Google Scholar]
  22. Tekamp P. A., Valenzuela P., Maynard T., Bell G. I., Rutter W. J. Specific gene transcription in yeast nuclei and chromatin by added homologous RNA polymerases I and II. J Biol Chem. 1979 Feb 10;254(3):955–963. [PubMed] [Google Scholar]
  23. Thomson L. J., Xing T., Hall J. L., Williams L. E. Investigation of the Calcium-Transporting ATPases at the Endoplasmic Reticulum and Plasma Membrane of Red Beet (Beta vulgaris). Plant Physiol. 1993 Jun;102(2):553–564. doi: 10.1104/pp.102.2.553. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Weber K., Osborn M. The reliability of molecular weight determinations by dodecyl sulfate-polyacrylamide gel electrophoresis. J Biol Chem. 1969 Aug 25;244(16):4406–4412. [PubMed] [Google Scholar]
  25. Wimmers L. E., Ewing N. N., Bennett A. B. Higher plant Ca(2+)-ATPase: primary structure and regulation of mRNA abundance by salt. Proc Natl Acad Sci U S A. 1992 Oct 1;89(19):9205–9209. doi: 10.1073/pnas.89.19.9205. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. van Engelen F. A., Sterk P., Booij H., Cordewener J. H., Rook W., van Kammen A., de Vries S. C. Heterogeneity and cell type-specific localization of a cell wall glycoprotein from carrot suspension cells. Plant Physiol. 1991 Jul;96(3):705–712. doi: 10.1104/pp.96.3.705. [DOI] [PMC free article] [PubMed] [Google Scholar]

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