Abstract
Hyperosmotic shock, induced by raising the NaCl concentration of Dunaliella salina medium from 1.71 to 3.42 M, elicited a rapid decrease of nearly one-third in whole cell volume and in the volume of intracellular organelles. The decrease in cell volume was accompanied by plasmalemma infolding without overall loss of surface area. This contrasts with the dramatic increase in plasmalemma surface area after hypoosmotic shock (Maeda, M., and G. A. Thompson. 1986. J. Cell Biol. 102:289-297). Although plasmalemma surface area remained constant after hyperosmotic shock, the nucleus, chloroplast, and mitochondria lost membrane surface area, apparently through membrane fusion with the endoplasmic reticulum. Thus the endoplasmic reticulum serves as a reservoir for excess membrane during hyperosmotic stress, reversing its role as membrane donor to the same organelles during hypoosmotically induced cell expansion. Hyperosmotic shock also induced rapid changes in phospholipid metabolism. The mass of phosphatidic acid dropped to 56% of control and that of phosphatidylinositol 4,5-bisphosphate rose to 130% of control within 4 min. Further analysis demonstrated that within 10 min after hyperosmotic shock, there was 2.5-fold increase in phosphatidylcholine turnover, a twofold increase in lysophosphatidylcholine mass, a four-fold increase in lysophosphatidate mass, and an elevation in free fatty acids to 124% of control, all observations suggesting activation of phospholipase A. The observed biophysical and biochemical phenomena are likely to be causally interrelated in providing mechanisms for successful accommodation to such severe osmotic extremes.
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Selected References
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- Anderson K. E., Whitlon D. S., Mueller G. C. Role of fatty acid structure in the reversible activation of phosphatidylcholine synthesis in lymphocytes. Biochim Biophys Acta. 1985 Jul 9;835(2):360–368. doi: 10.1016/0005-2760(85)90292-9. [DOI] [PubMed] [Google Scholar]
- BARTLETT G. R. Phosphorus assay in column chromatography. J Biol Chem. 1959 Mar;234(3):466–468. [PubMed] [Google Scholar]
- Cornell R., Vance D. E. Translocation of CTP: phosphocholine cytidylyltransferase from cytosol to membranes in HeLa cells: stimulation by fatty acid, fatty alcohol, mono- and diacylglycerol. Biochim Biophys Acta. 1987 May 13;919(1):26–36. doi: 10.1016/0005-2760(87)90214-1. [DOI] [PubMed] [Google Scholar]
- Dise C. A., Goodman D. B., Rasmussen H. Selective stimulation of erythrocyte membrane phospholipid fatty acid turnover associated with decreased cell volume. J Biol Chem. 1980 Jun 10;255(11):5201–5207. [PubMed] [Google Scholar]
- Einspahr K. J., Peeler T. C., Thompson G. A., Jr Rapid changes in polyphosphoinositide metabolism associated with the response of Dunaliella salina to hypoosmotic shock. J Biol Chem. 1988 Apr 25;263(12):5775–5779. [PubMed] [Google Scholar]
- Gordon-Kamm W. J., Steponkus P. L. Lamellar-to-hexagonalII phase transitions in the plasma membrane of isolated protoplasts after freeze-induced dehydration. Proc Natl Acad Sci U S A. 1984 Oct;81(20):6373–6377. doi: 10.1073/pnas.81.20.6373. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jolles J., Wirtz K. W., Schotman P., Gispen W. H. Pituitary hormones influence polyphosphoinositide metabolism in rat brain. FEBS Lett. 1979 Sep 1;105(1):110–114. doi: 10.1016/0014-5793(79)80897-2. [DOI] [PubMed] [Google Scholar]
- Kent C. Stimulation of phospholipid metabolism in embryonic muscle cells treated with phospholipase C. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4474–4478. doi: 10.1073/pnas.76.9.4474. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kitajima Y., Thompson G. A., Jr Tetrahymena strives to maintain the fluidity interrelationships of all its membranes constant. Electron microscope evidence. J Cell Biol. 1977 Mar;72(3):744–755. doi: 10.1083/jcb.72.3.744. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lynch D. V., Thompson G. A. Chloroplast Phospholipid Molecular Species Alterations during Low Temperature Acclimation in Dunaliella. Plant Physiol. 1984 Feb;74(2):198–203. doi: 10.1104/pp.74.2.198. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lynch D. V., Thompson G. A. Low Temperature-Induced Alterations in the Chloroplast and Microsomal Membranes of Dunaliella salina. Plant Physiol. 1982 Jun;69(6):1369–1375. doi: 10.1104/pp.69.6.1369. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lynch D. V., Thompson G. A. Microsomal Phospholipid Molecular Species Alterations during Low Temperature Acclimation in Dunaliella. Plant Physiol. 1984 Feb;74(2):193–197. doi: 10.1104/pp.74.2.193. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Maeda M., Thompson G. A., Jr On the mechanism of rapid plasma membrane and chloroplast envelope expansion in Dunaliella salina exposed to hypoosmotic shock. J Cell Biol. 1986 Jan;102(1):289–297. doi: 10.1083/jcb.102.1.289. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Menashe M., Romero G., Biltonen R. L., Lichtenberg D. Hydrolysis of dipalmitoylphosphatidylcholine small unilamellar vesicles by porcine pancreatic phospholipase A2. J Biol Chem. 1986 Apr 25;261(12):5328–5333. [PubMed] [Google Scholar]
- Okimasu E., Sasaki J., Utsumi K. Stimulation of phospholipase A2 activity by high osmotic pressure on cholesterol-containing phospholipid vesicles. FEBS Lett. 1984 Mar 12;168(1):43–48. doi: 10.1016/0014-5793(84)80203-3. [DOI] [PubMed] [Google Scholar]
- Pelech S. L., Cook H. W., Paddon H. B., Vance D. E. Membrane-bound CTP:phosphocholine cytidylyltransferase regulates the rate of phosphatidylcholine synthesis in HeLa cells treated with unsaturated fatty acids. Biochim Biophys Acta. 1984 Oct 4;795(3):433–440. doi: 10.1016/0005-2760(84)90169-3. [DOI] [PubMed] [Google Scholar]
- Pelech S. L., Pritchard P. H., Brindley D. N., Vance D. E. Fatty acids promote translocation of CTP:phosphocholine cytidylyltransferase to the endoplasmic reticulum and stimulate rat hepatic phosphatidylcholine synthesis. J Biol Chem. 1983 Jun 10;258(11):6782–6788. [PubMed] [Google Scholar]
- Romero G., Thompson K., Biltonen R. L. The activation of porcine pancreatic phospholipase A2 by dipalmitoylphosphatidylcholine large unilamellar vesicles. Analysis of the state of aggregation of the activated enzyme. J Biol Chem. 1987 Oct 5;262(28):13476–13482. [PubMed] [Google Scholar]
- Rouser G., Fkeischer S., Yamamoto A. Two dimensional then layer chromatographic separation of polar lipids and determination of phospholipids by phosphorus analysis of spots. Lipids. 1970 May;5(5):494–496. doi: 10.1007/BF02531316. [DOI] [PubMed] [Google Scholar]
- Ryals P. E., Thompson G. A., Jr Alterations of the composition and size of the free fatty acid pool of Tetrahymena responding to low-temperature stress. Biochim Biophys Acta. 1987 Jun 2;919(2):122–131. doi: 10.1016/0005-2760(87)90198-6. [DOI] [PubMed] [Google Scholar]
- Sekar M. C., Hokin L. E. The role of phosphoinositides in signal transduction. J Membr Biol. 1986;89(3):193–210. doi: 10.1007/BF01870664. [DOI] [PubMed] [Google Scholar]
- Weinhold P. A., Rounsifer M. E., Williams S. E., Brubaker P. G., Feldman D. A. CTP:phosphorylcholine cytidylyltransferase in rat lung. The effect of free fatty acids on the translocation of activity between microsomes and cytosol. J Biol Chem. 1984 Aug 25;259(16):10315–10321. [PubMed] [Google Scholar]
- Whitlon D. S., Anderson K. E., Mueller G. C. Analysis of the effects of fatty acids and related compounds on the synthesis of phosphatidylcholine in lymphocytes. Biochim Biophys Acta. 1985 Jul 9;835(2):369–377. doi: 10.1016/0005-2760(85)90293-0. [DOI] [PubMed] [Google Scholar]
