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A correlation between secondary structure and rheological properties of low-density lipoproteins at air/water interfaces

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Abstract

The secondary structure of apolipoprotein B-100 is studied within the bulk phase and at the air/water interface. In these “in viro” experiments, infrared reflection absorption spectroscopy (IRRAS) study was performed at the air/water interface while circular dichroism (CD) was conducted in the bulk phase. In the bulk phase, the conformational structure containing a significant amount of β–structure, whereas varying amount of α-helix, unordered structures, and β-sheet were observed at the air/water interface depending on the low-density lipoprotein (LDL) film interfacial pressure. The present IRRAS results demonstrate the importance of interfacial pressure-induced structural conformations on the apoB-100. A correlation between the secondary structure of the apoB-100 protein and the monomolecular film elasticity at the air/water interface was also established. The orientation of apoB-100 with respect to the LDL film-normal was found to depend on the interfacial pressure exhibited by the monomolecular film. These results may shed light on LDL’s pivotal role in the progression of atherosclerotic coronary artery disease as demonstrated previously by clinical trials.

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References

  1. Atkinson, D., Deckelbaum, R.J., Small, D.M., Shipley, G.G.: Structure of human plasma low-density lipoproteins: molecular organization of the central core. Proc. Natl. Acad. Sci. U. S. A. 74, 1042–1046 (1977)

    Article  ADS  Google Scholar 

  2. Deckelbaum, R.J., Shipley, G.G., Small, D.M.: Structure and interactions of lipids in human plasma low-density lipoproteins. J. Biol. Chem. 252, 744–754 (1977)

    Google Scholar 

  3. Ginsburg, G.S., Walsh, M.T., Small, D.M., Atkinson, D.: Reassembled plasma low-density lipoproteins phospholipid-cholesterol ester-apoproteins B complexes. J. Biol. Chem. 259, 6667–6673 (1984)

    Google Scholar 

  4. Coronado-Gray, A., Antwerpen, R.: The physical state of the LDL core influences the conformation of apolipoprotein B-100 on lipoprotein surface. FEBS Lett. 533, 21–24 (2003)

    Article  Google Scholar 

  5. Yabg, C.-Y., Gu, Z.-W., Weng, S.-A., Kim, T.W., Chen, S.-H., Pownall, H.J., Sharp, P.M., Liu, S.-W., Li, W.-H., Gotto, A.M., Chan, L.: Structure of apolipoprotein B-100 of human low-density lipoproteins. Arteriosclerosis. 9, 96–108 (1989)

    Article  Google Scholar 

  6. Titov, V.N.: Conformation of apolipoprotein B-100—structure and functional classification of low-density lipoproteins. Biokhimiia. 61, 3–23 (1996)

    Google Scholar 

  7. Ross, R.: The pathogenesis of atherosclerosis: a perspective for the 1990s. Nature. 362, 801–809 (1993)

    Article  ADS  Google Scholar 

  8. Steinberg, D., Parthasarathy, S., Carew, T.E., Khoo, J.C., Witztum, J.L.: Beyond cholesterol. Modifications of low-density lipoprotein that increase its atherogenicity. N. Engl. J. Med. 320, 915–924 (1989)

    Article  Google Scholar 

  9. Yavuzer, S., et al.: Endothelial damage in white coat hypertension: role of lectin-like oxidized low-density lipoprotein-1. J. Hum. Hypertens. 29, 92–98 (2015)

    Article  Google Scholar 

  10. Takeda, S., Subagyo, A., Hui, S.P., Fuda, H., Shrestha, R., Sueoka, K., Chiba, H.: Elastic modulus of low-density lipoprotein as potential indicator of its oxidation. Ann. Clin. Biochem. 14, 1–8 (2015)

    Google Scholar 

  11. Segrest, J.P., Jones, M.K., De Loof, H., Dashti, N.: Structure of apolipoproteins B-100 in low-density lipoproteins. J. Lipid Res. 42, 1346–1367 (2001)

    Google Scholar 

  12. Scanu, A., Hirz, R., Pollard, H.: On thermal dependence of conformation of human serum low- and high-density lipoproteins (LDL and HDL) and their apoproteins. Biophys. J. 9, A148 (1969)

    Google Scholar 

  13. Dauphas, S., et al.: Structures and rheological properties of hen egg yolk low-density lipoprotein layers spread at air-water interface at pH 3 and 7. Colloids Surf. B: Biointerfaces. 57, 124–133 (2007)

    Article  Google Scholar 

  14. Sneck, M., et al.: Conformational changes of apoB-100 in SMase-modified LDL mediate formation of large aggregates at acidic pH. J. Lipid Res. 53, 1832–1839 (2012)

    Article  Google Scholar 

  15. Ollila, S., Lamberg, A., Lehtivaara, M., Koivuniemi, A., Sysi-Aho, Vattulainen, I.: Interfacial tension and surface pressure of high-density lipoprotein, low-density lipoprotein, and related lipid droplets. Biophys. J. 103, 1236–1244 (2012)

    Article  ADS  Google Scholar 

  16. Chhatriwalla, A.K., et al.: Low level of low-density lipoprotein cholesterol and blood pressure and progression of coronary atherosclerosis. J Am. Coll. Cardiol. 53, 1110–1115 (2009)

    Article  Google Scholar 

  17. Toshima, S., et al.: Circulating oxidized low-density lipoprotein levels: a biochemical rich for coronary heart disease. Arterioscler. Thromb. Vasc. Biol. 20, 2243–2247 (2000)

    Article  Google Scholar 

  18. Mendelsohn, R., Guangru, M., Flach, C.R.: Infrared reflection-absorption spectroscopy: principles and applications to lipid-protein interaction in Langmuir films. Biochim. Biophys. Acta 1798, 788–800 (2010)

    Article  Google Scholar 

  19. Wang, X., Zhang, Y., Wu, J., Wang, M., Cui, G., Li, J., Brezesinski, G.: Dynamical and morphological studies on the adsorption and penetration of human serum albumin into phospholipid monolayers at the air/water interface. Colloids Surf. B: Biointerfaces 23, 339–347 (2002)

    Article  Google Scholar 

  20. Wallace, B.A., Whitmore, L.: Protein secondary structure analyses from circular dichroism spectroscopy: methods and reference database. Biopolymers 89, 392–400 (2008)

    Article  Google Scholar 

  21. Li, W., Haung, X.-J., Vienken, J., Xu, Z.-K., Groth, T.: Bioinspired multiple-interaction model revealed in adsorption of low-density lipoprotein to surface containing saccharide and alkanesulfonate. Langmuir 29, 8363–8369 (2013)

  22. Schnitzer, E., Pinchuk, I., Bor, A., Fainaru, M., Lichtenberg, D.: The effect of albumin on copper-induced LDL oxidation. Biochim. Biophys. Acta 1344, 300–311 (1997)

    Article  Google Scholar 

  23. Parasassi, T., Bittolo-Bon, G., Brunelli, R., Cazzolato, G., Krasnowska, E.K., Mei, G., Sevanian, A., Ursini, F.: Loss of apoB-100 secondary structure and conformation in Hydroperoxide rich, electronegative LDL. Free Radic. Biol. Med. 31, 82–89 (2001)

    Article  Google Scholar 

  24. Brunelli, R., Mei, G., Krasnowska, E.K., Pierucci, F., Zichella, L., Ursini, F., Parasassi, T.: Estradiol enhances the resistance of LDL to oxidation by stabilizing apoB-100 conformation. Biochemistry 39, 13897–13903 (2000)

    Article  Google Scholar 

  25. Bolanos-Garcia, V.M., Ramos, S., Castillo, R., Xicohtencatl-Cortes, J., Mas-Oliva, J.: Monolayers of apolipoproteins at the air/water Interface. J. Phys. Chem. 105, 5757–5765 (2001)

    Article  Google Scholar 

  26. Martinet, V., Saulnier, P., Beaumal, V., Courthaudon, C.P., Anton, M.: Surface properties of hen egg yolk low-density lipoproteins spread at the air–water interface. Colloids Surf. B: Biointerfaces 31, 185–194 (2003)

  27. Johs, A., Hammel, M., Waldner, I., May, P.R., Laggner, P., Prassl, R.: Modular structure of solubilized human apolipoprotein B-100 - low resolution model revealed by small angle neutron scattering. J. Biol. Chem. 281, 19732–19739 (2006)

    Article  Google Scholar 

  28. Sakurai, T., et al.: Measurement of single low-density lipoprotein particles by atomic force microscopy. Ann. Clin. Biochem. 50, 564–570 (2013)

    Article  Google Scholar 

  29. Barth, A.: Infrared spectroscopy of proteins. Biochim. Biophys. Acta 1767, 1073–1101 (2007)

    Article  Google Scholar 

  30. Chieze, L., et al.: Fluid and condensed ApoA-I/phospholipid monolayers provide insights into ApoA-I membrane insertion. J. Mol. Biol. 410, 60–75 (2011)

    Article  Google Scholar 

  31. Domon, M.M., Nasir, M.N., Pikula, S., Besson, F.: Influence of the 524-VAAEIL-529 sequence of annexins A6 in their interfacial behavior and interaction with lipid monolayers. J. Colloid Interface Sci. 403, 99–104 (2013)

    Article  ADS  Google Scholar 

  32. Gallego-Nicasio, J., et al.: Structural changes of low-density lipoproteins with Cu2+ and glucose induced oxidation. Biopolymers 72, 514–520 (2003)

    Article  Google Scholar 

  33. Byler, D.M., Susi, H.: Examination of the secondary structure of proteins by deconvolved FTIR spectra. Biopolymers. 25, 469–487 (1986)

    Article  Google Scholar 

  34. Olinger, J.M., Hill, D.M., Jakobson, R.J., Brody, R.S.: Fourier transform infrared studies of ribonuclease in H2O and 2H2O solutions. Biochim. Biophys. Acta 869, 89–98 (1986)

    Article  Google Scholar 

  35. Herzyk, E., Lee, D.C., Dunn, R.C., Bruckdorfer, K.R., Chapman, D.: Changes in the secondary structure of apolipoprotein B-100 after Cu2+-catalysed oxidation of human low-density lipoproteins monitored by Fourier transform infrared spectroscopy. Biochim. Biophys. Acta 922, 145–154 (1987)

    Article  Google Scholar 

  36. Goormaghtigh, E., et al.: Evaluation of the secondary structure of apo B-100 in low-density lipoprotein (LDL) by infrared spectroscopy. Biochim. Biophys. Acta 1006, 147–150 (1989)

    Article  Google Scholar 

  37. De Loof, H., Rosseneu, M., Yang, C.Y., Li, W.H., Gotto, A.M., Chan, L.: Human apolipoprotein B: analysis of internal repeats and homology with other apolipoproteins. J. Lipid Res. 28, 1455–1465 (1987)

    Google Scholar 

  38. Kriško, A., Stjepanović, G., Pifat, G., Ruysschaert, J.M., Goormaghtigh, E.: Detection of apolipoprotein B100 early conformational changes during oxidation. Biochim. Biophys. Acta 1768, 2923–2930 (2007)

    Article  Google Scholar 

  39. Blume, K., Dietrich, K., Lilienthal, S., Ternes, W., Drotleff, A.M.: Exploring the relationship between protein secondary structures, temperature-dependent viscosities, and technological treatments in egg yolk and LDL by FTIR and rheology. Food Chem. 173, 584–593 (2015)

    Article  Google Scholar 

Download references

Acknowledgements

I would like to thank Prof. Dr. Thomas Fischer (University of Bayreuth, Germany) for the generous hospitality to carry out the experiments in his laboratory. The financial support from DFG and Hashemite University are gratefully acknowledged.

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Correspondence to Ziad Khattari.

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Khattari, Z. A correlation between secondary structure and rheological properties of low-density lipoproteins at air/water interfaces. J Biol Phys 43, 381–395 (2017). https://doi.org/10.1007/s10867-017-9458-3

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