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The calcium uptake of the rat heart sarcoplasmic reticulum is altered by dietary lipid

Summary

Small amounts of dietary n-3 fatty acids can have dramatic physiological effects, including the reduction of plasma triglycerides and an elevation of cellular eicosapentanoic (EPA) and docosahexanoic acids (DHA) at the expense of arachidonic acid (AA). We investigated the effects of alterations in the fatty acid compositions of cardiac sarcoplasmic reticulum (CSR) produced by dietary manipulation on the calcium pump protein that is required for energy dependent calcium transport. CSR was isolated from rats fed menhaden oil, which is rich in n-3 fatty acids, and from control animals that were given corn oil. Relative to control membranes, those isolated from rats fed menhaden oil, had a lower content of saturated phospholipids, an increased DHA/AA ratio, and an increased ratio of n-3 to n-6 fatty acids. These changes were associated with a 30% decrease in oxalate-facilitated, ATP-dependent calcium uptake and concomitant decreased Ca-ATPase activity in the membranes from the animals fed menhaden oil. In contrast, there was no alteration in active pump sites as measured by phosphoenzyme formation. Thus, the CSR Ca-ATPase function can be altered by dietary interventions that change the composition, and possibly structure, of the phospholipid membranes thereby affecting enzyme turnover.

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References

  1. Bakardjieva, A., Galla, H.J., Helmreich, E.J.M. 1979. Modulation of theβ-receptor adenylate cyclase interactions in cultured Chang liver cells by phospholipid enrichment.Biochemistry 18:3016–3023

  2. Bick, R.J., Youker, K.A., Pownall, H.J., Van Winkle, W.B., Entman, M.L. 1991. Unsaturated aminophospholipids are preferentially retained by the fast skeletal muscle CaATPase during detergent solubilization.Arch. Biochem. Biophys. 286:346–352

  3. Blasie, J.K., Pascolini, D., Asturias, F., Herbette, L.G., Pierce, D., Scarpa, A. 1990. Large-scale structural changes in the sarcoplasmic reticulum ATPase appear essential for calcium transport.Biophys. J. 58:687–693

  4. Brandl, C.J., Green, N.M., Korczak, B., MacLennan, D.H. 1984. Two Ca21 ATPase genes: Homologies and mechanistic implications of deduced amino acids sequences.Cell 44:597–607

  5. Cheng, K-H., Lepock, J.R., Hui, S.W., Yeagle, P.L. 1986. The role of cholesterol in the activity of reconstituted Ca-ATPase vesicles containing unsaturated phosphatidylethanolamine.J. Biol. Chem. 261:5081–5087

  6. Croset, M., Black, J.M., Swanson, J.E., Kinsella, J.E., 1989. Effects of dietary n-3 polyunsaturated fatty acids on phospholipid composition and calcium transport in more cardiac sarcoplasmic reticulum.Lipids 24:278–285

  7. Croset, M., Kinsella, J.E. 1989. Changes in phospholipid fatty acid composition of mouse cardiac organelles after feeding graded amounts of docosahexanoate in the presence of high levels of linoleate. Effect on cardiac ATPase activities.Ann. Nut. Metab. 33:125–142

  8. Dillmann, W.H. 1990. Biochemical basis of thyroid hormone action in the heart.Amer. J. Med. 88:626–630

  9. East, M., Lee, A.G. 1982. Lipid selectivity of the Calcium and Magnesium ion dependent adenosinetriphosphatase, studied with fluorescence quenching by a brominated phospholipid.Biochemistry 21:4144–4151

  10. Fiehn, W., Hasselbach, W. 1970. The effect of phospholipase A on the calcium transport and the role of unsaturated fatty acids in ATPase activity of sarcoplasmic vesicles.Eur. J. Biochem. 13:510–518

  11. Fritsche, K.L., Johnston, P.V. 1988. Rapid autoxidation of Fish Oil in diets without added antioxidants.J. Nutrition 118:425–426

  12. Gould, G.W., McWhirter, J.M., Lee, M., East A.G. 1987. Effects of diet on the function of sarcoplasmic reticulum.Biochem. J. 245:751–755

  13. Gudbjarnason, S. 1990. What is the function of docosahexanoic acid in heart muscle membranes?J. Appl. Cardiol. 5:13–21

  14. Hidalgo, C., de la Fuente, M., Gonzalez, M.E. 1986. Role of lipids in sarcoplasmic reticulum: a higher lipid content is required to sustain phosphoenzyme decomposition than phosphoenzyme formation.Arch. Biochem. Biophys. 247:365–371

  15. Hidalgo, C., Petrucci, D.A., Vergara, C. 1982. Uncoupling of Ca2+ transport in sarcoplasmic reticulum as a result of labeling lipid amino groups and inhibition of Ca2+ ATPase activity by modification of lysine residues of the Ca2+ ATPase polypeptide.J. Biol. Chem. 257:208–214

  16. Holmes, R.P., Mahfouz, M., Travis, B.D., Yoss, N.L., Keenan, M.J. 1983. The effect of membrane lipid composition on the permeability of membranes to Ca2−.Ann. NY Acad, Sci. 414:44–56

  17. Horrocks, L.A. 1968. The alk-l-enyl group content of mammalian myelin phosphoglycerides by quantitative two-dimensional thin-layer chromatography.J. Lipid. Res. 9:469–472

  18. Johansson, A., Keigthly, C.A., Smith, G.A., Richards, C.D., Hesketh, T.R., Metcalfe, J.C. 1981. The effect of the bilayer thickness and n-alkanes on the activity of the (Ca2+ + Mg2−)dependent ATPase of sarcoplasmic reticulum.J. Biol. Chem. 256:1643–1650

  19. Lowry, O.H., Rosebrough, N.J., Farr, A.L., Randall, R.J. 1951. Protein measurement with the Folin phenol reagent.J. Biol. Chem. 193:265–275

  20. Martonosi, A. 1964. Role of phospholipids in ATPase activity and Ca transport of fragmented sarcoplasmic reticulum.Fed. Proc. 23:913–923

  21. Martonosi, A., Donley, J., Halpin, R.A. 1968. Sarcoplasmic Reticulum III. The role of phospholipids in the adeosine triphosphatase activity and Ca2+ transport.J. Biol. Chem. 243:61–70

  22. Meissner, G., Fleischer, S. 1972. The role of phospholipid in Ca2+-stimulated ATPase activity of sarcoplasmic reticulum.Biochim. Biophys. Acta 255:19–33

  23. Moore, B.M., Lentz, B.R., Meissner, G. 1978. Effects of sarcoplasmic reticulum Ca2+-ATPase on phospholipid bilayer fluidity: boundary lipid.Biochemistry 17:5248–5255

  24. Navarro, J., Toívio-Kinnucan, M., Racker, E. 1984. Effect of lipid composition on the calcium /adenosine 5′-triphosphate coupling ratio of the Ca2+-ATPase of sarcoplasmic reticulum.Biochemistry 23:130–136

  25. Pagani, E.D., Solaro, R.J. 1984. Coordination of cardiac myofibrillar and sarcotubular activities in rats exercised by swimming.Am. J. Physiol. 247:H909-H915

  26. Rouser, G., Siakotos, A.N., Fleischer, S. 1966. Quantitative analysis of phospholipids by thin-layer chromatography and phosphorus analysis of spots. Lipids1:85–86

  27. Shigekawa, M., Finegan, J.M., Katz, A.M. 1976. Calcium transport of canine cardiac sarcoplasmic reticulum. A comparison with that of rabbit fast skeletal muscle sarcoplasmic reticulum.J. Biol. Chem. 251:6894–6900

  28. Swanson, J.E., Lokesh, B.R. Kinsella, J.E. 1989. Ca2+ − Mg2+ ATPase of mouse cardiac sarcoplasmic reticulum is affected by membrane n-6 and n-3 polyunsaturated fatty acid content.J. Nutrition 119:364–372

  29. Tada, M., Yamada, M., Ohmori, F., Kiruya, T., Inui, M., Abe, H. 1980. Transient state kinetic studies of Ca2+-dependent ATPase and calcium transport by cardiac sarcoplasmic reticulum.J. Biol. Chem. 255:1985–1992

  30. Tada, M., Yamamoto, T., Tonomura, Y. 1978. Molecular mechanism of active calcium transport by sarcoplasmic reticulum.Physiol. Rev. 58:1–79

  31. Tate, C.A., Bick, R.J., Chu, A., Van Winkle, W.B., Entman, M.L. 1985. Nucleotide specficity of cardiac sarcoplasmic reticulum.J. Biol. Chem. 260:9618–9623

  32. Van Winkle, W.B., Bick R.J., Tucker, D.E., Tate, C.A., Entman, M. L. 1982. Evidence for membrane microheterogeneity in the sarcoplasmic reticulum of fast twitch skeletal muscle.J. Biol. Chem. 257:11689–11695

  33. Van Winkle, W.B., Tate, C.A., Bick, R.J., Entman, M.L. 1981. Substrate utilization by cardiac and skeletal muscle sarcoplasmic reticulum: evidence for a hydrolysis cycle not coupled to intermediate acyl-phosphate formation and calcium translocation.J. Biol. Chem. 256:2268–2276

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Taffet, G.E., Thu Pham, T., Bick, D.L.M. et al. The calcium uptake of the rat heart sarcoplasmic reticulum is altered by dietary lipid. J. Membrain Biol. 131, 35–42 (1993). https://doi.org/10.1007/BF02258532

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Key words

  • sarcoplasmic reticulum
  • diet fatty acids
  • phospholipids
  • calcium adenosine triphosphatase
  • turnover