Skip to main content
PMC home page
Biophysical Journal logoLink to Biophysical Journal
. 1997 Nov;73(5):2603–2614. doi: 10.1016/S0006-3495(97)78290-0

Effects of dipalmitoylglycerol and fatty acids on membrane structure and protein kinase C activity.

E M Goldberg 1, R Zidovetzki 1
PMCID: PMC1181163  PMID: 9370455

Abstract

The individual and combined effects of the saturated diacylglycerol (DAG) dipalmitin (DP) and saturated or polyunsaturated unesterified fatty acids (PUFAs) on both the structure of phosphatidylcholine/phosphatidylserine (PC/PS; 4:1 mol/mol) bilayers and on protein kinase C (PKC) activity were studied using 2H nuclear magnetic resonance (NMR) and enzyme activity assays. In the absence of DP, PUFAs only slightly activated PKC whereas palmitic acid had no effect. In the absence of fatty acids, DP induced lateral phase separation of the bilayer into liquid-crystalline and gel phases. Under these conditions virtually all DP was sequestered into the gel phase and no activation of PKC was observed. The addition of polyunsaturated arachidonic or docosahexaenoic acids to the DP-containing bilayers significantly increased the relative amounts of DP and other lipid components in the liquid-crystalline phase, correlating with a dramatic increase in PKC activity. Furthermore, the effect was greater with PS, resulting in an enrichment of PS in the liquid-crystalline domains. In the presence of DP, palmitic acid did not decrease the amount of gel phase lipid and had no effect on PKC activity. The results explain the observed lack of PKC-activating capacity of long-chain saturated DAGs as due to the sequestration of DAG into gel domains wherein it is complexed with phospholipids and thus not available for the required interaction with the enzyme.

Full text

PDF
2603

Selected References

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

  1. Ahkong Q. F., Fisher D., Tampion W., Lucy J. A. The fusion of erythrocytes by fatty acids, esters, retinol and alpha-tocopherol. Biochem J. 1973 Sep;136(1):147–155. doi: 10.1042/bj1360147. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Andreasen T. J., McNamee M. G. Inhibition of ion permeability control properties of acetylcholine receptor from Torpedo californica by long-chain fatty acids. Biochemistry. 1980 Sep 30;19(20):4719–4726. doi: 10.1021/bi00561a027. [DOI] [PubMed] [Google Scholar]
  3. Anel A., Richieri G. V., Kleinfeld A. M. Membrane partition of fatty acids and inhibition of T cell function. Biochemistry. 1993 Jan 19;32(2):530–536. doi: 10.1021/bi00053a018. [DOI] [PubMed] [Google Scholar]
  4. Arnold R. S., Cornell R. B. Lipid regulation of CTP: phosphocholine cytidylyltransferase: electrostatic, hydrophobic, and synergistic interactions of anionic phospholipids and diacylglycerol. Biochemistry. 1996 Jul 30;35(30):9917–9924. doi: 10.1021/bi960397c. [DOI] [PubMed] [Google Scholar]
  5. Baudier J., Delphin C., Grunwald D., Khochbin S., Lawrence J. J. Characterization of the tumor suppressor protein p53 as a protein kinase C substrate and a S100b-binding protein. Proc Natl Acad Sci U S A. 1992 Dec 1;89(23):11627–11631. doi: 10.1073/pnas.89.23.11627. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bazzi M. D., Nelsestuen G. L. Role of substrate in imparting calcium and phospholipid requirements to protein kinase C activation. Biochemistry. 1987 Apr 7;26(7):1974–1982. doi: 10.1021/bi00381a029. [DOI] [PubMed] [Google Scholar]
  7. Bechinger B., Seelig J. Interaction of electric dipoles with phospholipid head groups. A 2H and 31P NMR study of phloretin and phloretin analogues in phosphatidylcholine membranes. Biochemistry. 1991 Apr 23;30(16):3923–3929. doi: 10.1021/bi00230a017. [DOI] [PubMed] [Google Scholar]
  8. Bolen E. J., Sando J. J. Effect of phospholipid unsaturation on protein kinase C activation. Biochemistry. 1992 Jun 30;31(25):5945–5951. doi: 10.1021/bi00140a034. [DOI] [PubMed] [Google Scholar]
  9. Buchner K. Protein kinase C in the transduction of signals toward and within the cell nucleus. Eur J Biochem. 1995 Mar 1;228(2):211–221. [PubMed] [Google Scholar]
  10. Cevc G., Seddon J. M., Hartung R., Eggert W. Phosphatidylcholine-fatty acid membranes. I. Effects of protonation, salt concentration, temperature and chain-length on the colloidal and phase properties of mixed vesicles, bilayers and nonlamellar structures. Biochim Biophys Acta. 1988 May 24;940(2):219–240. doi: 10.1016/0005-2736(88)90197-6. [DOI] [PubMed] [Google Scholar]
  11. Chen S. G., Murakami K. Synergistic activation of type III protein kinase C by cis-fatty acid and diacylglycerol. Biochem J. 1992 Feb 15;282(Pt 1):33–39. doi: 10.1042/bj2820033. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Cheng K. H., Ruymgaart L., Liu L. I., Somerharju P., Sugar I. P. Intramolecular excimer kinetics of fluorescent dipyrenyl lipids: 2. DOPE/DOPC membranes. Biophys J. 1994 Aug;67(2):914–921. doi: 10.1016/S0006-3495(94)80553-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Chien K. R., Han A., Sen A., Buja L. M., Willerson J. T. Accumulation of unesterified arachidonic acid in ischemic canine myocardium. Relationship to a phosphatidylcholine deacylation-reacylation cycle and the depletion of membrane phospholipids. Circ Res. 1984 Mar;54(3):313–322. doi: 10.1161/01.res.54.3.313. [DOI] [PubMed] [Google Scholar]
  14. Cornell R. B. Regulation of CTP:phosphocholine cytidylyltransferase by lipids. 2. Surface curvature, acyl chain length, and lipid-phase dependence for activation. Biochemistry. 1991 Jun 18;30(24):5881–5888. doi: 10.1021/bi00238a011. [DOI] [PubMed] [Google Scholar]
  15. Das S., Rand R. P. Modification by diacylglycerol of the structure and interaction of various phospholipid bilayer membranes. Biochemistry. 1986 May 20;25(10):2882–2889. doi: 10.1021/bi00358a022. [DOI] [PubMed] [Google Scholar]
  16. Davis J. H. Deuterium magnetic resonance study of the gel and liquid crystalline phases of dipalmitoyl phosphatidylcholine. Biophys J. 1979 Sep;27(3):339–358. doi: 10.1016/S0006-3495(79)85222-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Davis J. H. The description of membrane lipid conformation, order and dynamics by 2H-NMR. Biochim Biophys Acta. 1983 Mar 21;737(1):117–171. doi: 10.1016/0304-4157(83)90015-1. [DOI] [PubMed] [Google Scholar]
  18. De Boeck H., Zidovetzki R. Effects of diacylglycerols on the structure of phosphatidylcholine bilayers: a 2H and 31P NMR study. Biochemistry. 1989 Sep 5;28(18):7439–7446. doi: 10.1021/bi00444a043. [DOI] [PubMed] [Google Scholar]
  19. Dekker L. V., Parker P. J. Protein kinase C--a question of specificity. Trends Biochem Sci. 1994 Feb;19(2):73–77. doi: 10.1016/0968-0004(94)90038-8. [DOI] [PubMed] [Google Scholar]
  20. Dill K. A., Flory P. J. Molecular organization in micelles and vesicles. Proc Natl Acad Sci U S A. 1981 Feb;78(2):676–680. doi: 10.1073/pnas.78.2.676. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Epand R. M. Diacylglycerols, lysolecithin, or hydrocarbons markedly alter the bilayer to hexagonal phase transition temperature of phosphatidylethanolamines. Biochemistry. 1985 Dec 3;24(25):7092–7095. doi: 10.1021/bi00346a011. [DOI] [PubMed] [Google Scholar]
  22. Epand R. M., Epand R. F., Ahmed N., Chen R. Promotion of hexagonal phase formation and lipid mixing by fatty acids with varying degrees of unsaturation. Chem Phys Lipids. 1991 Jan-Feb;57(1):75–80. doi: 10.1016/0009-3084(91)90051-c. [DOI] [PubMed] [Google Scholar]
  23. Epand R. M., Lester D. S. The role of membrane biophysical properties in the regulation of protein kinase C activity. Trends Pharmacol Sci. 1990 Aug;11(8):317–320. doi: 10.1016/0165-6147(90)90234-y. [DOI] [PubMed] [Google Scholar]
  24. Epand R. M. The relationship between the effects of drugs on bilayer stability and on protein kinase C activity. Chem Biol Interact. 1987;63(3):239–247. doi: 10.1016/0009-2797(87)90044-5. [DOI] [PubMed] [Google Scholar]
  25. Fagnou D. D., Tuchek J. M. The biochemistry of learning and memory. Mol Cell Biochem. 1995 Aug-Sep;149-150:279–286. doi: 10.1007/BF01076589. [DOI] [PubMed] [Google Scholar]
  26. Fields A. P., Tyler G., Kraft A. S., May W. S. Role of nuclear protein kinase C in the mitogenic response to platelet-derived growth factor. J Cell Sci. 1990 May;96(Pt 1):107–114. doi: 10.1242/jcs.96.1.107. [DOI] [PubMed] [Google Scholar]
  27. Gheriani-Gruszka N., Almog S., Biltonen R. L., Lichtenberg D. Hydrolysis of phosphatidylcholine in phosphatidylcholine-cholate mixtures by porcine pancreatic phospholipase A2. J Biol Chem. 1988 Aug 25;263(24):11808–11813. [PubMed] [Google Scholar]
  28. Go M., Sekiguchi K., Nomura H., Kikkawa U., Nishizuka Y. Further studies on the specificity of diacylglycerol for protein kinase C activation. Biochem Biophys Res Commun. 1987 Apr 29;144(2):598–605. doi: 10.1016/s0006-291x(87)80008-6. [DOI] [PubMed] [Google Scholar]
  29. Goldberg E. M., Lester D. S., Borchardt D. B., Zidovetzki R. Effects of diacylglycerols and Ca2+ on structure of phosphatidylcholine/phosphatidylserine bilayers. Biophys J. 1994 Feb;66(2 Pt 1):382–393. doi: 10.1016/s0006-3495(94)80788-x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Goldberg E. M., Lester D. S., Borchardt D. B., Zidovetzki R. Effects of diacylglycerols on conformation of phosphatidylcholine headgroups in phosphatidylcholine/phosphatidylserine bilayers. Biophys J. 1995 Sep;69(3):965–973. doi: 10.1016/S0006-3495(95)79970-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Gruner S. M. Intrinsic curvature hypothesis for biomembrane lipid composition: a role for nonbilayer lipids. Proc Natl Acad Sci U S A. 1985 Jun;82(11):3665–3669. doi: 10.1073/pnas.82.11.3665. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Hamilton J. A., Cistola D. P. Transfer of oleic acid between albumin and phospholipid vesicles. Proc Natl Acad Sci U S A. 1986 Jan;83(1):82–86. doi: 10.1073/pnas.83.1.82. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Hannun Y. A., Loomis C. R., Merrill A. H., Jr, Bell R. M. Sphingosine inhibition of protein kinase C activity and of phorbol dibutyrate binding in vitro and in human platelets. J Biol Chem. 1986 Sep 25;261(27):12604–12609. [PubMed] [Google Scholar]
  34. Hanski E., Rimon G., Levitzki A. Adenylate cyclase activation by the beta-adrenergic receptors as a diffusion-controlled process. Biochemistry. 1979 Mar 6;18(5):846–853. doi: 10.1021/bi00572a017. [DOI] [PubMed] [Google Scholar]
  35. Heimburg T., Würz U., Marsh D. Binary phase diagram of hydrated dimyristoylglycerol-dimyristoylphosphatidylcholine mixtures. Biophys J. 1992 Nov;63(5):1369–1378. doi: 10.1016/S0006-3495(92)81714-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Holte L. L., Peter S. A., Sinnwell T. M., Gawrisch K. 2H nuclear magnetic resonance order parameter profiles suggest a change of molecular shape for phosphatidylcholines containing a polyunsaturated acyl chain. Biophys J. 1995 Jun;68(6):2396–2403. doi: 10.1016/S0006-3495(95)80422-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Hoover R. L., Lynch R. D., Karnovsky M. J. Decrease in adhesion of cells cultured in polyunsaturated fatty acids. Cell. 1977 Sep;12(1):295–300. doi: 10.1016/0092-8674(77)90207-0. [DOI] [PubMed] [Google Scholar]
  38. Huang H. W., Goldberg E. M., Zidovetzki R. Ceramide induces structural defects into phosphatidylcholine bilayers and activates phospholipase A2. Biochem Biophys Res Commun. 1996 Mar 27;220(3):834–838. doi: 10.1006/bbrc.1996.0490. [DOI] [PubMed] [Google Scholar]
  39. Ido M., Sekiguchi K., Kikkawa U., Nishizuka Y. Phosphorylation of the EGF receptor from A431 epidermoid carcinoma cells by three distinct types of protein kinase C. FEBS Lett. 1987 Jul 13;219(1):215–218. doi: 10.1016/0014-5793(87)81219-x. [DOI] [PubMed] [Google Scholar]
  40. Israelachvili J. N., Marcelja S., Horn R. G. Physical principles of membrane organization. Q Rev Biophys. 1980 May;13(2):121–200. doi: 10.1017/s0033583500001645. [DOI] [PubMed] [Google Scholar]
  41. Jain M. K., Berg O. G. The kinetics of interfacial catalysis by phospholipase A2 and regulation of interfacial activation: hopping versus scooting. Biochim Biophys Acta. 1989 Apr 3;1002(2):127–156. doi: 10.1016/0005-2760(89)90281-6. [DOI] [PubMed] [Google Scholar]
  42. Jain M. K., Jahagirdar D. V. Action of phospholipase A2 on bilayers. Effect of inhibitors. Biochim Biophys Acta. 1985 Apr 11;814(2):319–326. doi: 10.1016/0005-2736(85)90451-1. [DOI] [PubMed] [Google Scholar]
  43. Jarrell H. C., Byrd R. A., Smith I. C. Analysis of the composition of mixed lipid phases by the moments of 2H NMR spectra. Biophys J. 1981 Jun;34(3):451–463. doi: 10.1016/S0006-3495(81)84862-X. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Kantor H. L., Prestegard J. H. Fusion of phosphatidylcholine bilayer vesicles: role of free fatty acid. Biochemistry. 1978 Aug 22;17(17):3592–3597. doi: 10.1021/bi00610a027. [DOI] [PubMed] [Google Scholar]
  45. Karnovsky M. J., Kleinfeld A. M., Hoover R. L., Klausner R. D. The concept of lipid domains in membranes. J Cell Biol. 1982 Jul;94(1):1–6. doi: 10.1083/jcb.94.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Kishimoto A., Takai Y., Mori T., Kikkawa U., Nishizuka Y. Activation of calcium and phospholipid-dependent protein kinase by diacylglycerol, its possible relation to phosphatidylinositol turnover. J Biol Chem. 1980 Mar 25;255(6):2273–2276. [PubMed] [Google Scholar]
  47. Kiss Z. Regulation of phospholipase D by protein kinase C. Chem Phys Lipids. 1996 May 24;80(1-2):81–102. doi: 10.1016/0009-3084(96)02547-9. [DOI] [PubMed] [Google Scholar]
  48. Klausner R. D., Kleinfeld A. M., Hoover R. L., Karnovsky M. J. Lipid domains in membranes. Evidence derived from structural perturbations induced by free fatty acids and lifetime heterogeneity analysis. J Biol Chem. 1980 Feb 25;255(4):1286–1295. [PubMed] [Google Scholar]
  49. Lafleur M., Cullis P. R., Bloom M. Modulation of the orientational order profile of the lipid acyl chain in the L alpha phase. Eur Biophys J. 1990;19(2):55–62. doi: 10.1007/BF00185086. [DOI] [PubMed] [Google Scholar]
  50. Lapetina E. G., Reep B., Ganong B. R., Bell R. M. Exogenous sn-1,2-diacylglycerols containing saturated fatty acids function as bioregulators of protein kinase C in human platelets. J Biol Chem. 1985 Feb 10;260(3):1358–1361. [PubMed] [Google Scholar]
  51. Leray V., Hubert P., Burgun C., Staedel C., Crémel G. Reconstitution studies of lipid effects on insulin-receptor kinase activation. Eur J Biochem. 1993 Apr 1;213(1):277–284. doi: 10.1111/j.1432-1033.1993.tb17760.x. [DOI] [PubMed] [Google Scholar]
  52. Lester D. S. In vitro linoleic acid activation of protein kinase C. Biochim Biophys Acta. 1990 Sep 24;1054(3):297–303. doi: 10.1016/0167-4889(90)90100-r. [DOI] [PubMed] [Google Scholar]
  53. Lewis R. E., Czech M. P. Phospholipid environment alters hormone-sensitivity of the purified insulin receptor kinase. Biochem J. 1987 Dec 15;248(3):829–836. doi: 10.1042/bj2480829. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Lucas M., Sánchez-Margalet V. Protein kinase C involvement in apoptosis. Gen Pharmacol. 1995 Sep;26(5):881–887. doi: 10.1016/0306-3623(94)00295-x. [DOI] [PubMed] [Google Scholar]
  55. López-García F., Villalaín J., Gómez-Fernández J. C., Quinn P. J. The phase behavior of mixed aqueous dispersions of dipalmitoyl derivatives of phosphatidylcholine and diacylglycerol. Biophys J. 1994 Jun;66(6):1991–2004. doi: 10.1016/S0006-3495(94)80992-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Marassi F. M., Macdonald P. M. Response of the phosphatidylcholine headgroup to membrane surface charge in ternary mixtures of neutral, cationic, and anionic lipids: a deuterium NMR study. Biochemistry. 1992 Oct 20;31(41):10031–10036. doi: 10.1021/bi00156a024. [DOI] [PubMed] [Google Scholar]
  57. Mayer L. D., Hope M. J., Cullis P. R., Janoff A. S. Solute distributions and trapping efficiencies observed in freeze-thawed multilamellar vesicles. Biochim Biophys Acta. 1985 Jul 11;817(1):193–196. doi: 10.1016/0005-2736(85)90084-7. [DOI] [PubMed] [Google Scholar]
  58. McCallum C. D., Epand R. M. Insulin receptor autophosphorylation and signaling is altered by modulation of membrane physical properties. Biochemistry. 1995 Feb 14;34(6):1815–1824. doi: 10.1021/bi00006a001. [DOI] [PubMed] [Google Scholar]
  59. McLaughlin A. C., Cullis P. R., Hemminga M. A., Hoult D. I., Radda G. K., Ritchie G. A., Seeley P. J., Richards R. E. Application of 31P NMR to model and biological membrane systems. FEBS Lett. 1975 Sep 15;57(2):213–218. doi: 10.1016/0014-5793(75)80719-8. [DOI] [PubMed] [Google Scholar]
  60. McLaughlin S., Mulrine N., Gresalfi T., Vaio G., McLaughlin A. Adsorption of divalent cations to bilayer membranes containing phosphatidylserine. J Gen Physiol. 1981 Apr;77(4):445–473. doi: 10.1085/jgp.77.4.445. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Mitaku S., Jippo T., Kataoka R. Thermodynamic properties of the lipid bilayer transition. Pseudocritical phenomena. Biophys J. 1983 May;42(2):137–144. doi: 10.1016/S0006-3495(83)84379-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Mori T., Takai Y., Yu B., Takahashi J., Nishizuka Y., Fujikura T. Specificity of the fatty acyl moieties of diacylglycerol for the activation of calcium-activated, phospholipid-dependent protein kinase. J Biochem. 1982 Feb;91(2):427–431. doi: 10.1093/oxfordjournals.jbchem.a133714. [DOI] [PubMed] [Google Scholar]
  63. Mosior M., McLaughlin S. Peptides that mimic the pseudosubstrate region of protein kinase C bind to acidic lipids in membranes. Biophys J. 1991 Jul;60(1):149–159. doi: 10.1016/S0006-3495(91)82038-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Mosior M., Newton A. C. Mechanism of interaction of protein kinase C with phorbol esters. Reversibility and nature of membrane association. J Biol Chem. 1995 Oct 27;270(43):25526–25533. doi: 10.1074/jbc.270.43.25526. [DOI] [PubMed] [Google Scholar]
  65. Murakami K., Chan S. Y., Routtenberg A. Protein kinase C activation by cis-fatty acid in the absence of Ca2+ and phospholipids. J Biol Chem. 1986 Nov 25;261(33):15424–15429. [PubMed] [Google Scholar]
  66. Murakami K., Routtenberg A. Direct activation of purified protein kinase C by unsaturated fatty acids (oleate and arachidonate) in the absence of phospholipids and Ca2+. FEBS Lett. 1985 Nov 18;192(2):189–193. doi: 10.1016/0014-5793(85)80105-8. [DOI] [PubMed] [Google Scholar]
  67. Nakamura S., Nishizuka Y. Lipid mediators and protein kinase C activation for the intracellular signaling network. J Biochem. 1994 Jun;115(6):1029–1034. doi: 10.1093/oxfordjournals.jbchem.a124451. [DOI] [PubMed] [Google Scholar]
  68. Newton A. C. Protein kinase C: structure, function, and regulation. J Biol Chem. 1995 Dec 1;270(48):28495–28498. doi: 10.1074/jbc.270.48.28495. [DOI] [PubMed] [Google Scholar]
  69. Nichol C. P., Davis J. H., Weeks G., Bloom M. Quantitative study of the fluidity of Escherichia coli membranes using deuterium magnetic resonance. Biochemistry. 1980 Feb 5;19(3):451–457. doi: 10.1021/bi00544a008. [DOI] [PubMed] [Google Scholar]
  70. Nishizuka Y. Studies and perspectives of protein kinase C. Science. 1986 Jul 18;233(4761):305–312. doi: 10.1126/science.3014651. [DOI] [PubMed] [Google Scholar]
  71. Orly J., Schramm M. Fatty acids as modulators of membrane functions: catecholamine-activated adenylate cyclase of the turkey erythrocyte. Proc Natl Acad Sci U S A. 1975 Sep;72(9):3433–3437. doi: 10.1073/pnas.72.9.3433. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. Quinn P. J., Takahashi H., Hatta I. Characterization of complexes formed in fully hydrated dispersions of dipalmitoyl derivatives of phosphatidylcholine and diacylglycerol. Biophys J. 1995 Apr;68(4):1374–1382. doi: 10.1016/S0006-3495(95)80310-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  73. Ray T. K., Skipski V. P., Barclay M., Essner E., Archibald F. M. Lipid composition of rat liver plasma membranes. J Biol Chem. 1969 Oct 25;244(20):5528–5536. [PubMed] [Google Scholar]
  74. 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]
  75. Sandermann H., Jr, Duncan T. M. Lipid-dependent membrane enzymes. Kinetic modelling of the activation of protein kinase C by phosphatidylserine. Biochim Biophys Acta. 1991 Nov 4;1069(2):235–240. doi: 10.1016/0005-2736(91)90130-z. [DOI] [PubMed] [Google Scholar]
  76. Sando J. J., Chertihin O. I. Activation of protein kinase C by lysophosphatidic acid: dependence on composition of phospholipid vesicles. Biochem J. 1996 Jul 15;317(Pt 2):583–588. doi: 10.1042/bj3170583. [DOI] [PMC free article] [PubMed] [Google Scholar]
  77. Sasaki Y., Asaoka Y., Nishizuka Y. Potentiation of diacylglycerol-induced activation of protein kinase C by lysophospholipids. Subspecies difference. FEBS Lett. 1993 Mar 29;320(1):47–51. doi: 10.1016/0014-5793(93)81655-j. [DOI] [PubMed] [Google Scholar]
  78. Schachter J. B., Lester D. S., Alkon D. L. Synergistic activation of protein kinase C by arachidonic acid and diacylglycerols in vitro: generation of a stable membrane-bound, cofactor-independent state of protein kinase C activity. Biochim Biophys Acta. 1996 Oct 24;1291(2):167–176. doi: 10.1016/0304-4165(96)00063-3. [DOI] [PubMed] [Google Scholar]
  79. Scherer P. G., Seelig J. Electric charge effects on phospholipid headgroups. Phosphatidylcholine in mixtures with cationic and anionic amphiphiles. Biochemistry. 1989 Sep 19;28(19):7720–7728. doi: 10.1021/bi00445a030. [DOI] [PubMed] [Google Scholar]
  80. Scherer P. G., Seelig J. Structure and dynamics of the phosphatidylcholine and the phosphatidylethanolamine head group in L-M fibroblasts as studied by deuterium nuclear magnetic resonance. EMBO J. 1987 Oct;6(10):2915–2922. doi: 10.1002/j.1460-2075.1987.tb02595.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  81. Schorn K., Marsh D. Lipid chain dynamics and molecular location of diacylglycerol in hydrated binary mixtures with phosphatidylcholine: spin label ESR studies. Biochemistry. 1996 Mar 26;35(12):3831–3836. doi: 10.1021/bi952688b. [DOI] [PubMed] [Google Scholar]
  82. Schramm M., Eisenkraft B., Barkai E. Cold-induced leakage of amylase from the zymogen granule and sealing of its membrane by specific lipids. Biochim Biophys Acta. 1967 Feb 1;135(1):44–52. doi: 10.1016/0005-2736(67)90006-5. [DOI] [PubMed] [Google Scholar]
  83. Seddon J. M. Structure of the inverted hexagonal (HII) phase, and non-lamellar phase transitions of lipids. Biochim Biophys Acta. 1990 Feb 28;1031(1):1–69. doi: 10.1016/0304-4157(90)90002-t. [DOI] [PubMed] [Google Scholar]
  84. Seelig J. Deuterium magnetic resonance: theory and application to lipid membranes. Q Rev Biophys. 1977 Aug;10(3):353–418. doi: 10.1017/s0033583500002948. [DOI] [PubMed] [Google Scholar]
  85. Sekiguchi K., Tsukuda M., Ase K., Kikkawa U., Nishizuka Y. Mode of activation and kinetic properties of three distinct forms of protein kinase C from rat brain. J Biochem. 1988 May;103(5):759–765. doi: 10.1093/oxfordjournals.jbchem.a122343. [DOI] [PubMed] [Google Scholar]
  86. Sen A., Isac T. V., Hui S. W. Bilayer packing stress and defects in mixed dilinoleoylphosphatidylethanolamine and palmitoyloleoylphosphatidylcholine and their susceptibility to phospholipase A2. Biochemistry. 1991 May 7;30(18):4516–4521. doi: 10.1021/bi00232a021. [DOI] [PubMed] [Google Scholar]
  87. Senisterra G., Epand R. M. Dual modulation of protein kinase C activity by sphingosine. Biochem Biophys Res Commun. 1992 Sep 16;187(2):635–640. doi: 10.1016/0006-291x(92)91242-i. [DOI] [PubMed] [Google Scholar]
  88. Senisterra G., Epand R. M. Role of membrane defects in the regulation of the activity of protein kinase C. Arch Biochem Biophys. 1993 Jan;300(1):378–383. doi: 10.1006/abbi.1993.1051. [DOI] [PubMed] [Google Scholar]
  89. Separovic F., Gawrisch K. Effect of unsaturation on the chain order of phosphatidylcholines in a dioleoylphosphatidylethanolamine matrix. Biophys J. 1996 Jul;71(1):274–282. doi: 10.1016/S0006-3495(96)79223-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  90. Shinomura T., Asaoka Y., Oka M., Yoshida K., Nishizuka Y. Synergistic action of diacylglycerol and unsaturated fatty acid for protein kinase C activation: its possible implications. Proc Natl Acad Sci U S A. 1991 Jun 15;88(12):5149–5153. doi: 10.1073/pnas.88.12.5149. [DOI] [PMC free article] [PubMed] [Google Scholar]
  91. Slater S. J., Kelly M. B., Taddeo F. J., Ho C., Rubin E., Stubbs C. D. The modulation of protein kinase C activity by membrane lipid bilayer structure. J Biol Chem. 1994 Feb 18;269(7):4866–4871. [PubMed] [Google Scholar]
  92. Streicher-Scott J., Lapidus R., Sokolove P. M. The reconstituted mitochondrial adenine nucleotide translocator: effects of lipid polymorphism. Arch Biochem Biophys. 1994 Dec;315(2):548–554. doi: 10.1006/abbi.1994.1535. [DOI] [PubMed] [Google Scholar]
  93. Stubbs C. D., Slater S. J. The effects of non-lamellar forming lipids on membrane protein-lipid interactions. Chem Phys Lipids. 1996 Jul 15;81(2):185–195. doi: 10.1016/0009-3084(96)02581-9. [DOI] [PubMed] [Google Scholar]
  94. Verkest V., McArthur M., Hamilton S. Fatty acid activation of protein kinase C: dependence on diacylglycerol. Biochem Biophys Res Commun. 1988 Apr 29;152(2):825–829. doi: 10.1016/s0006-291x(88)80112-8. [DOI] [PubMed] [Google Scholar]
  95. Walker J. M., Homan E. C., Sando J. J. Differential activation of protein kinase C isozymes by short chain phosphatidylserines and phosphatidylcholines. J Biol Chem. 1990 May 15;265(14):8016–8021. [PubMed] [Google Scholar]
  96. Westman J., Boulanger Y., Ehrenberg A., Smith I. C. Charge and pH dependent drug binding to model membranes. A 2H-NMR and light absorption study. Biochim Biophys Acta. 1982 Mar 8;685(3):315–328. doi: 10.1016/0005-2736(82)90073-6. [DOI] [PubMed] [Google Scholar]
  97. Wetsel W. C., Khan W. A., Merchenthaler I., Rivera H., Halpern A. E., Phung H. M., Negro-Vilar A., Hannun Y. A. Tissue and cellular distribution of the extended family of protein kinase C isoenzymes. J Cell Biol. 1992 Apr;117(1):121–133. doi: 10.1083/jcb.117.1.121. [DOI] [PMC free article] [PubMed] [Google Scholar]
  98. Wilschut J. C., Regts J., Westenberg H., Scherphof G. Action of phospholipases A2 on phosphatidylcholine bilayers. Effects of the phase transition, bilayer curvature and structural defects. Biochim Biophys Acta. 1978 Apr 4;508(2):185–196. doi: 10.1016/0005-2736(78)90324-3. [DOI] [PubMed] [Google Scholar]
  99. Wojtczak L. Effect of long-chain fatty acids and acyl-CoA on mitochondrial permeability, transport, and energy-coupling processes. J Bioenerg Biomembr. 1976 Dec;8(6):293–311. doi: 10.1007/BF00765158. [DOI] [PubMed] [Google Scholar]
  100. Zidovetzki R., Laptalo L., Crawford J. Effect of diacylglycerols on the activity of cobra venom, bee venom, and pig pancreatic phospholipases A2. Biochemistry. 1992 Aug 25;31(33):7683–7691. doi: 10.1021/bi00148a032. [DOI] [PubMed] [Google Scholar]
  101. Zidovetzki R., Lester D. S. The mechanism of activation of protein kinase C: a biophysical perspective. Biochim Biophys Acta. 1992 Apr 7;1134(3):261–272. doi: 10.1016/0167-4889(92)90185-e. [DOI] [PubMed] [Google Scholar]

Articles from Biophysical Journal are provided here courtesy of The Biophysical Society

RESOURCES