Hemoglobin binding to phospholipid membranes as revealed by pyrene fluorescence study
Keywords:
hemoglobin, model membranes, protein-lipid complexes, pyrene, fluorescence spectroscopy
Abstract
In this work hemoglobin (Hb) association with lipid bilayers was investigated using fluorescent probe
pyrene. Model membranes were prepared from zwitterionic lipid phosphatidylcholine (PC), anionic lipid
phosphatidylglycerol (PG) and cholesterol (Chol). Hb-lipid binding was followed by the pyrene
fluorescence quenching. Hb-induced decrease of pyrene monomer fluorescence was followed by the
increase of relative intensities of vibronic bands. Presumably, Hb penetration into the bilayer increases
the space between neighbouring lipids and promotes water penetration into the membrane core. Pyrene
excimer emission quenching was interpreted in terms of resonance energy transfer. The greatest depth of
Hb penetration into the lipid bilayer was observed in PC vesicles. In Chol-containing liposomes sterol
condensing effect prevents deep protein penetration into the membrane. PG has an ability to stabilize lipid
bilayers due to the ordered state of its lipid tails and H-bonding interactions between lipid molecules. This
also can prevent Hb access to the inner membrane regions.
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References
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33. Levitt M., Perutz M.F. Aromatic rings act as hydrogen bond acceptors // J. Mol. Biol. – 1988. – V. 201. – P. 751–754.
34. Wong-ekkabut J., Xu Z., Triampo W., Tang I-M., Tieleman D.P., Monticelli L. Effect of lipid peroxidation on the properties of lipid bilayers: a molecular dynamics study // Biophys. J. – 2007. – V. 93. – P. 4225–4236.
35. Galla H.-J., Hartmann W., Theilen U., Sackmann E. On two dimensional passive random walk in lipid bilayers and fluid pathways in biomembranes // J. Membr. Biol. – 1979. – V. 48. – P. 215-236.
2. Szundi I., Szelényi J.G., Breuer J.H., Bérczi A. Interactions of haemoglobin with erythrocyte membrane phospholipids in monomolecular lipid layers // Biochim. Biophys. Acta. – 1980. – V. 595(1). – P. 41-46.
3. Chang T.M.S. Future generation of red blood cell substitutes // J. Internal Medicine. – 2003. – V. 253. – P. 527-535.
4. Goorha B.Y.K., Deb M.P., Chatterjee L.C.T., Dhot C.P.S., Prasad B.R.S. Artifical Blood // MJAFI. – 2003. – V. 59. – P. 45-50.
5. Szebeni J., Di Iorio E.E., Winterhalter K.H. Encapsulation of hemoglobin in phospholipid liposomes: characterization and stability // Biochemistry. – 1985. – V. 24. – P. 2827-2832.
6. Ioffe V., Gorbenko G.P. Lysozyme effect on structural state of model membranes as revealed by pyrene excimerization studies // Biophys. Chem. – 2005. – V. 114. – P. 199-204.
7. Tuominen E.K.J., Zhu K., Wallace C.J.A., Clark-Lewis I., Craig D.B., Rytömaa M., Kinnunen P.K.J. ATP induces a conformational change in lipid-bound cytochrome c // J. Biol. Chem. – 2001. – V. 276(22). – P. 19356-19362.
8. Duportail G., Lianos P. Fluorescence probing of vesicles using pyrene and pyrene derivatives, in Vesicles, edited by Rosoff M., Marcel Dekker, Inc: New York, 1996.
9. Nakajima A. Solvent effect on the vibrational structures of the fluorescence and absorption spectra of pyrene // Bull. Chem. Soc. Jpn. – 1971. – V. 44. – P. 3272-3277.
10. Kaprovich D.S., Blanchard G.J. Relating the polarity-dependent fluorescence response of pyrene to vibronic coupling. Achieving a fundamental understanding of the py polarity scale // J. Phys. Chem. – 1995. – V. 99. – P. 3951-3958.
11. Kalyanasundaram K., Thomas J.K. Environmental effects on vibronic band intensities in pyrene monomer fluorescence and their application in studies of micellar systems // J. Am. Chem. Soc. – 1977. – V. 99. – P. 2039-2044.
12. Galla H.-J., Sackmann E. Lateral diffusion in the hydrophobic region of membranes: use of pyrene excimers as optical probes // Biochim. Biophys. Acta. – 1974. – V. 339. – P. 103-115.
13. Birks J.B., Lumb M.D., Munro I.H. Excimer fluorescence. V. Influence of solvent viscosity and temperature // Proc. R. Soc. London, Ser. A. – 1964. – V. 280. – P. 289-297.
14. Hoff B., Strandberg E., Ulrich A.S., Tieleman D.P., Posten C. 2H-NMR study and molecular dynamics simulation of the location, alignment, and mobility of pyrene in POPC bilayers // Biophys. J. – 2005. – V. 88. – P. 1818–1827.
15. Vanderkooi J.M., Callis J.B. Pyrene. A probe of lateral diffusion in the hydrophobic region of membranes // Biochemistry. – 1974. – V. 13(19). – P. 4000-4006.
16. Mui B., Chow L., Hope M.J. Extrusion technique to generate liposomes of defined size // Meth. Enzymol. – 2003. – V. 367. – P. 3–14.
17. Lakowicz J.R. Principles of fluorescent spectroscopy, Springer: Singapore, 2006, 954 p.
18. Szebeni J., Hauser H., Eskelson C.D., Watson R.R., Winterhalter K.H. Interaction of hemoglobin derivatives with liposomes. Membrane cholesterol protects against the changes of hemoglobin // Biochemistry. – 1988. – V. 27. – P. 6425-6434.
19. Fu X., Xu S., Wang Z. Kinetics of lipid oxidation and off-odor formation in silver carp mince: the effect of lipoxigenase and hemoglobin // Food Res. Int. – 2009. – V. 42. – P. 85-90.
20. Pitcher III W.H., Huestis W.H. Preparation and analysis of small unilamellar phospholipid vesicles of a uniform size // Biochem. Biophys. Res. Commun. – 2002. – V. 296. – P. 1352-1355.
21. Abugo O.O., Balagopalakrishna C., Rifkind J.M., Rudolph A.S., Hess J.R., Macdonald V.M. Direct measurements of hemoglobin interaction with liposomes using EPR spectroscopy // Artif. Cells, Blood Substitutes, Immobilization Biotechnol. – 2001. – V. 29(1). – P. 5-18.
22. Di Giulio A., Bonamore A. Globin interactions with lipids and membranes // Methods Enzymol. – 2008. – V. 436. – P. 239-253.
23. Xi J., Guo R., Guo X. Interactions of hemoglobin with lecithin liposomes // Colloid Polym. Sci. – 2006. – V. 284. – P. 1139–1145.
24. Pitcher III W.H., Keller S.L., Huestis W.H. Interaction of nominally soluble proteins with phospholipid monolayers at the air–water interface // Biochim. Biophys. Acta. – 2002. – V. 1564. – P. 107– 113.
25. Ушакова И.П., Серебренникова Г.А., Евстигнеева Р.П. Обратимые переносчики кислорода на основе липосомальных форм производных гема и гемоглобина // Биологические мембраны. – 1987. – Т. 4(6). – C. 565-589.
26. Datta P., Chakrabarty S., Chakrabarty A., Chakrabarti A. Membrane interactions of hemoglobin variants, HbA, HbE, HbF and globin subunits of HbA: effects of aminophospholipids and cholesterol // Biochim. Biophys. Acta. – 2008. – V. 1778. – P. 1-9.
27. Ушакова И.П., Василенко И.А., Серебренникова Г.А., Евстигнеева Р.П. Изучение взаимодействия метгемоглобина с фосфолипидными бислойными мембранами методом флуоресценции // Биоорг. химия. – 1981. – Т. 7(4). – С. 613-627.
28. Gornicki A. The influence of oxidative stress on microviscosity of hemoglobin-containing liposomes // Gen. Physiol. Biophys. – 2003. – V. 22. – P. 121-127.
29. Elmore D.E. Molecular dynamics simulation of a phosphatidylglycerol membrane // FEBS Lett. – 2006. – V. 580. – P. 144–148.
30. Murzyn K., Rog T., Pasenkiewicz-Gierula M. Phosphatidylethanolamine-phosphatidylglycerol bilayer as a model of the inner bacterial membrane // Biophys. J. – 2005. – V. 88. – P. 1091–1103.
31. Tedeschi C., Mohwald H., Kirstein S. Polarity of layer-by-layer deposited polyelectrolyte films as determined by pyrene fluorescence // J. Am. Chem. Soc. – 2001. – V. 123. – P. 954-960.
32. Dougherty D.A. Cation-p interactions in chemistry and biology: a new view of benzene, Phe, Tyr and Trp // Science. – 1996. – V. 271. – P. 163–168.
33. Levitt M., Perutz M.F. Aromatic rings act as hydrogen bond acceptors // J. Mol. Biol. – 1988. – V. 201. – P. 751–754.
34. Wong-ekkabut J., Xu Z., Triampo W., Tang I-M., Tieleman D.P., Monticelli L. Effect of lipid peroxidation on the properties of lipid bilayers: a molecular dynamics study // Biophys. J. – 2007. – V. 93. – P. 4225–4236.
35. Galla H.-J., Hartmann W., Theilen U., Sackmann E. On two dimensional passive random walk in lipid bilayers and fluid pathways in biomembranes // J. Membr. Biol. – 1979. – V. 48. – P. 215-236.
Cited
How to Cite
Kutsenko, O. K., Gorbenko, G. P., & Trusova, V. M. (1). Hemoglobin binding to phospholipid membranes as revealed by pyrene fluorescence study. Biophysical Bulletin, 1(26). Retrieved from https://periodicals.karazin.ua/biophysvisnyk/article/view/2710
Section
Cell biophysics
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