Skip to main content
Biophysical Journal logoLink to Biophysical Journal
. 1998 Feb;74(2 Pt 1):869–878. doi: 10.1016/S0006-3495(98)74010-X

Surface properties of native human plasma lipoproteins and lipoprotein models.

J B Massey 1, H J Pownall 1
PMCID: PMC1302566  PMID: 9533698

Abstract

Plasma lipoprotein surface properties are important but poorly understood determinants of lipoprotein catabolism. To elucidate the relation between surface properties and surface reactivity, the physical properties of surface monolayers of native lipoproteins and lipoprotein models were investigated by fluorescent probes of surface lipid fluidity, surface lateral diffusion, and interfacial polarity, and by their reactivity to Naja melanoleuca phospholipase A2 (PLA2). Native lipoproteins were human very low, low-, and subclass 3 high-density lipoproteins (VLDL, LDL, and HDL3); models were 1-palmitoyl-2-oleoyl-sn-glycero-3-phosphocholine (POPC) or its ether analog in single-bilayer vesicles, large and small microemulsions of POPC and triolein, and reassembled HDL (apolipoprotein A-I plus phospholipid). Among lipoproteins, surface lipid fluidity increased in the order HDL3 < LDL < VLDL, varying inversely with their (protein + cholesterol)/phospholipid ratios. Models resembled VLDL in fluidity. Both lateral mobility in the surface monolayer and polarity of the interfacial region were lower in native lipoproteins than in models. Among native lipoproteins and models, increased fluidity in the surface monolayer was associated with increased reactivity to PLA2. Addition of cholesterol (up to 20 mol%) to models had little effect on PLA2 activity, whereas the addition of apolipoprotein C-III stimulated it. Single-bilayer vesicles, phospholipid-triolein microemulsions, and VLDL have surface monolayers that are quantitatively similar, and distinct from those of LDL and HDL3. Surface property and enzymatic reactivity differences between lipoproteins and models were associated with differences in surface monolayer protein and cholesterol contents. Thus differences in the surface properties that regulate lipolytic reactivity are a predictable function of surface composition.

Full Text

The Full Text of this article is available as a PDF (119.5 KB).

Selected References

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

  1. Atkinson D., Small D. M. Recombinant lipoproteins: implications for structure and assembly of native lipoproteins. Annu Rev Biophys Biophys Chem. 1986;15:403–456. doi: 10.1146/annurev.bb.15.060186.002155. [DOI] [PubMed] [Google Scholar]
  2. BARTLETT G. R. Phosphorus assay in column chromatography. J Biol Chem. 1959 Mar;234(3):466–468. [PubMed] [Google Scholar]
  3. Barenholz Y., Cohen T., Haas E., Ottolenghi M. Lateral organization of pyrene-labeled lipids in bilayers as determined from the deviation from equilibrium between pyrene monomers and excimers. J Biol Chem. 1996 Feb 9;271(6):3085–3090. doi: 10.1074/jbc.271.6.3085. [DOI] [PubMed] [Google Scholar]
  4. Barenholz Y., Gibbes D., Litman B. J., Goll J., Thompson T. E., Carlson R. D. A simple method for the preparation of homogeneous phospholipid vesicles. Biochemistry. 1977 Jun 14;16(12):2806–2810. doi: 10.1021/bi00631a035. [DOI] [PubMed] [Google Scholar]
  5. Bhamidipati S. P., Hamilton J. A. Hydrolysis of a phospholipid in an inert lipid matrix by phospholipase A2: a 13C NMR study. Biochemistry. 1989 Aug 8;28(16):6667–6672. doi: 10.1021/bi00442a020. [DOI] [PubMed] [Google Scholar]
  6. Cunningham B. A., Tsujita T., Brockman H. L. Enzymatic and physical characterization of diacylglycerol-phosphatidylcholine interactions in bilayers and monolayers. Biochemistry. 1989 Jan 10;28(1):32–40. doi: 10.1021/bi00427a006. [DOI] [PubMed] [Google Scholar]
  7. DeBose C. D., Roberts M. F. The interaction of dialkyl ether lecithins with phospholipase A2 (Naja naja naja). J Biol Chem. 1983 May 25;258(10):6327–6334. [PubMed] [Google Scholar]
  8. Derksen A., Small D. M. Interaction of ApoA-1 and ApoE-3 with triglyceride-phospholipid emulsions containing increasing cholesterol concentrations. Model of triglyceride-rich nascent and remnant lipoproteins. Biochemistry. 1989 Jan 24;28(2):900–906. doi: 10.1021/bi00428a074. [DOI] [PubMed] [Google Scholar]
  9. Fenske D. B., Chana R. S., Parmar Y. I., Treleaven W. D., Cushley R. J. Structure and motion of phospholipids in human plasma lipoproteins. A 31P NMR study. Biochemistry. 1990 Apr 24;29(16):3973–3981. doi: 10.1021/bi00468a026. [DOI] [PubMed] [Google Scholar]
  10. HAVEL R. J., EDER H. A., BRAGDON J. H. The distribution and chemical composition of ultracentrifugally separated lipoproteins in human serum. J Clin Invest. 1955 Sep;34(9):1345–1353. doi: 10.1172/JCI103182. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Handa T., Saito H., Tanaka I., Kakee A., Tanaka K., Miyajima K. Lateral interactions of pig apolipoprotein A-1 with egg yolk phosphatidylcholine and with cholesterol in mixed monolayers at the triolein-saline interface. Biochemistry. 1992 Feb 11;31(5):1415–1420. doi: 10.1021/bi00120a018. [DOI] [PubMed] [Google Scholar]
  12. Ibdah J. A., Lund-Katz S., Phillips M. C. Kinetics and mechanism of transfer of reduced and carboxymethylated apolipoprotein A-II between phospholipid vesicles. Biochemistry. 1990 Apr 10;29(14):3472–3479. doi: 10.1021/bi00466a008. [DOI] [PubMed] [Google Scholar]
  13. Ibdah J. A., Lund-Katz S., Phillips M. C. Molecular packing of high-density and low-density lipoprotein surface lipids and apolipoprotein A-I binding. Biochemistry. 1989 Feb 7;28(3):1126–1133. doi: 10.1021/bi00429a029. [DOI] [PubMed] [Google Scholar]
  14. Jain M. K., Egmond M. R., Verheij H. M., Apitz-Castro R., Dijkman R., De Haas G. H. Interaction of phospholipase A2 and phospholipid bilayers. Biochim Biophys Acta. 1982 Jun 14;688(2):341–348. doi: 10.1016/0005-2736(82)90345-5. [DOI] [PubMed] [Google Scholar]
  15. Jonas A. Lecithin-cholesterol acyltransferase in the metabolism of high-density lipoproteins. Biochim Biophys Acta. 1991 Jul 30;1084(3):205–220. doi: 10.1016/0005-2760(91)90062-m. [DOI] [PubMed] [Google Scholar]
  16. Jonas A. Synthetic substrates of lecithin: cholesterol acyltransferase. J Lipid Res. 1986 Jul;27(7):689–698. [PubMed] [Google Scholar]
  17. Jonas A., Zorich N. L., Kézdy K. E., Trick W. E. Reaction of discoidal complexes of apolipoprotein A-I and various phosphatidylcholines with lecithin cholesterol acyltransferase. Interfacial effects. J Biol Chem. 1987 Mar 25;262(9):3969–3974. [PubMed] [Google Scholar]
  18. Joubert F. J., Van der Walt S. J. Naja melanoleuca (forest cobra) venom. Purification and some properties of phospholipases A. Biochim Biophys Acta. 1975 Feb 27;379(2):317–328. doi: 10.1016/0005-2795(75)90140-3. [DOI] [PubMed] [Google Scholar]
  19. Lund-Katz S., Phillips M. C. Packing of cholesterol molecules in human low-density lipoprotein. Biochemistry. 1986 Apr 8;25(7):1562–1568. doi: 10.1021/bi00355a016. [DOI] [PubMed] [Google Scholar]
  20. Mantulin W. W., Massey J. B., Gotto A. M., Jr, Pownall H. J. Reassembled model lipoproteins. Lipid dynamics in recombinants of human apolipoprotein A-II and dimyristoylphosphatidylcholine. J Biol Chem. 1981 Nov 10;256(21):10815–10819. [PubMed] [Google Scholar]
  21. Massey J. B., Bick D. H., Pownall H. J. Spontaneous transfer of monoacyl amphiphiles between lipid and protein surfaces. Biophys J. 1997 Apr;72(4):1732–1743. doi: 10.1016/S0006-3495(97)78819-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Massey J. B., Pao Q., Van Winkle W. B., Pownall H. J. Interaction of human plasma lecithin:cholesterol acyltransferase and venom phospholipase A2 with apolipoprotein A-I recombinants containing nonhydrolyzable diether phosphatidylcholines. J Biol Chem. 1985 Sep 25;260(21):11719–11723. [PubMed] [Google Scholar]
  23. Massey J. B., She H. S., Gotto A. M., Jr, Pownall H. J. Lateral distribution of phospholipid and cholesterol in apolipoprotein A-I recombinants. Biochemistry. 1985 Dec 3;24(25):7110–7116. doi: 10.1021/bi00346a014. [DOI] [PubMed] [Google Scholar]
  24. Massey J. B., She H. S., Pownall H. J. Interfacial properties of model membranes and plasma lipoproteins containing ether lipids. Biochemistry. 1985 Nov 19;24(24):6973–6978. doi: 10.1021/bi00345a033. [DOI] [PubMed] [Google Scholar]
  25. McKeone B. J., Massey J. B., Knapp R. D., Pownall H. J. Apolipoproteins C-I, C-II, and C-III: kinetics of association with model membranes and intermembrane transfer. Biochemistry. 1988 Jun 14;27(12):4500–4505. doi: 10.1021/bi00412a042. [DOI] [PubMed] [Google Scholar]
  26. McLean L. R., Jackson R. L. Interaction of lipoprotein lipase and apolipoprotein C-II with sonicated vesicles of 1,2-ditetradecylphosphatidylcholine: comparison of binding constants. Biochemistry. 1985 Jul 16;24(15):4196–4201. doi: 10.1021/bi00336a057. [DOI] [PubMed] [Google Scholar]
  27. Mims M. P., Morrisett J. D. Lipolysis of phospholipids in model cholesteryl ester rich lipoproteins and related systems: effect of core and surface lipid phase state. Biochemistry. 1988 Jul 12;27(14):5290–5295. doi: 10.1021/bi00414a051. [DOI] [PubMed] [Google Scholar]
  28. Ohnishi T., Yokoyama S. Activation of human plasma lipid transfer protein by apolipoproteins. Biochemistry. 1993 May 18;32(19):5029–5035. doi: 10.1021/bi00070a009. [DOI] [PubMed] [Google Scholar]
  29. Pal R., Petri W. A., Jr, Ben-Yashar V., Wagner R. R., Barenholz Y. Characterization of the fluorophore 4-heptadecyl-7-hydroxycoumarin: a probe for the head-group region of lipid bilayers and biological membranes. Biochemistry. 1985 Jan 29;24(3):573–581. doi: 10.1021/bi00324a005. [DOI] [PubMed] [Google Scholar]
  30. Parasassi T., Di Stefano M., Loiero M., Ravagnan G., Gratton E. Cholesterol modifies water concentration and dynamics in phospholipid bilayers: a fluorescence study using Laurdan probe. Biophys J. 1994 Mar;66(3 Pt 1):763–768. doi: 10.1016/s0006-3495(94)80852-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Parks J. S., Thuren T. Y., Schmitt J. D. Inhibition of lecithin:cholesterol acyltransferase activity by synthetic phosphatidylcholine species containing eicosapentaenoic acid or docosahexaenoic acid in the sn-2 position. J Lipid Res. 1992 Jun;33(6):879–887. [PubMed] [Google Scholar]
  32. Patsch J. R., Gotto A. M., Jr, Olivercrona T., Eisenberg S. Formation of high density lipoprotein2-like particles during lipolysis of very low density lipoproteins in vitro. Proc Natl Acad Sci U S A. 1978 Sep;75(9):4519–4523. doi: 10.1073/pnas.75.9.4519. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Pownall H. J., Pao Q., Massey J. B. Acyl chain and headgroup specificity of human plasma lecithin:cholesterol acyltransferase. Separation of matrix and molecular specificities. J Biol Chem. 1985 Feb 25;260(4):2146–2152. [PubMed] [Google Scholar]
  34. Prendergast F. G., Haugland R. P., Callahan P. J. 1-[4-(Trimethylamino)phenyl]-6-phenylhexa-1,3,5-triene: synthesis, fluorescence properties, and use as a fluorescence probe of lipid bilayers. Biochemistry. 1981 Dec 22;20(26):7333–7338. doi: 10.1021/bi00529a002. [DOI] [PubMed] [Google Scholar]
  35. Reijngoud D. J., Phillips M. C. Mechanism of dissociation of human apolipoprotein A-I from complexes with dimyristoylphosphatidylcholine as studied by guanidine hydrochloride denaturation. Biochemistry. 1982 Jun 8;21(12):2969–2976. doi: 10.1021/bi00541a026. [DOI] [PubMed] [Google Scholar]
  36. Rosseneu M., Taveirne M. J., Caster H., Van Biervliet J. P. Hydrolysis of very-low-density lipoproteins labeled with a fluorescent triacylglycerol: 1,3-dioleoyl-2-(4-pyrenylbutanoyl)glycerol. Eur J Biochem. 1985 Oct 1;152(1):195–198. doi: 10.1111/j.1432-1033.1985.tb09182.x. [DOI] [PubMed] [Google Scholar]
  37. Sassaroli M., Vauhkonen M., Perry D., Eisinger J. Lateral diffusivity of lipid analogue excimeric probes in dimyristoylphosphatidylcholine bilayers. Biophys J. 1990 Feb;57(2):281–290. doi: 10.1016/S0006-3495(90)82530-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Shen B. W., Scanu A. M., Kézdy F. J. Structure of human serum lipoproteins inferred from compositional analysis. Proc Natl Acad Sci U S A. 1977 Mar;74(3):837–841. doi: 10.1073/pnas.74.3.837. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Sparks D. L., Davidson W. S., Lund-Katz S., Phillips M. C. Effect of cholesterol on the charge and structure of apolipoprotein A-I in recombinant high density lipoprotein particles. J Biol Chem. 1993 Nov 5;268(31):23250–23257. [PubMed] [Google Scholar]
  40. Straume M., Litman B. J. Influence of cholesterol on equilibrium and dynamic bilayer structure of unsaturated acyl chain phosphatidylcholine vesicles as determined from higher order analysis of fluorescence anisotropy decay. Biochemistry. 1987 Aug 11;26(16):5121–5126. doi: 10.1021/bi00390a034. [DOI] [PubMed] [Google Scholar]
  41. Tajima S., Yokoyama S., Yamamoto A. Effect of lipid particle size on association of apolipoproteins with lipid. J Biol Chem. 1983 Aug 25;258(16):10073–10082. [PubMed] [Google Scholar]
  42. Vauhkonen M., Sassaroli M., Somerharju P., Eisinger J. Lateral diffusion of phospholipids in the lipid surface of human low-density lipoprotein measured with a pyrenyl phospholipid probe. Eur J Biochem. 1989 Dec 22;186(3):465–471. doi: 10.1111/j.1432-1033.1989.tb15230.x. [DOI] [PubMed] [Google Scholar]
  43. Vauhkonen M., Somerharju P. Parinaroyl and pyrenyl phospholipids as probes for the lipid surface layer of human low density lipoproteins. Biochim Biophys Acta. 1989 Aug 21;984(1):81–87. doi: 10.1016/0005-2736(89)90345-3. [DOI] [PubMed] [Google Scholar]
  44. Vauhkonen M., Somerharju P. The surface lipid layer of human low density lipoprotein probed by dipyrenyl phospholipids. Chem Phys Lipids. 1990 Feb;52(3-4):207–216. doi: 10.1016/0009-3084(90)90116-9. [DOI] [PubMed] [Google Scholar]
  45. Vist M. R., Davis J. H. Phase equilibria of cholesterol/dipalmitoylphosphatidylcholine mixtures: 2H nuclear magnetic resonance and differential scanning calorimetry. Biochemistry. 1990 Jan 16;29(2):451–464. doi: 10.1021/bi00454a021. [DOI] [PubMed] [Google Scholar]
  46. Weber G., Farris F. J. Synthesis and spectral properties of a hydrophobic fluorescent probe: 6-propionyl-2-(dimethylamino)naphthalene. Biochemistry. 1979 Jul 10;18(14):3075–3078. doi: 10.1021/bi00581a025. [DOI] [PubMed] [Google Scholar]
  47. Wetterau J. R., Jonas A. Factors affecting the size of complexes of dipalmitoylphosphatidylcholine with human apolipoprotein A-I. J Biol Chem. 1983 Feb 25;258(4):2637–2643. [PubMed] [Google Scholar]
  48. Yokoyama S., Kawai Y., Tajima S., Yamamoto A. Behavior of human apolipoprotein E in aqueous solutions and at interfaces. J Biol Chem. 1985 Dec 25;260(30):16375–16382. [PubMed] [Google Scholar]
  49. Zhang F., Kamp F., Hamilton J. A. Dissociation of long and very long chain fatty acids from phospholipid bilayers. Biochemistry. 1996 Dec 17;35(50):16055–16060. doi: 10.1021/bi961685b. [DOI] [PubMed] [Google Scholar]

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

RESOURCES