Fluorescence energy transfer study of the lipid bilayer interactions with truncated apolipoprotein a-i mutants

  • M. S. Girych V. N. Karazin Kharkiv National University
  • I. L. Maliyov V. N. Karazin Kharkiv National University
  • M. V. Romanova V. N. Karazin Kharkiv National University
  • G. P. Gorbenko V. N. Karazin Kharkiv National University
  • E. Adachi Institute of Health Biosciences and Graduate School of Pharmaceutical Sciences, The University of Tokushima
  • C. Mizuguchi Institute of Health Biosciences and Graduate School of Pharmaceutical Sciences, The University of Tokushima
  • J. G. Molotkovsky Institute of Bioorganic Chemistry, Russian Academy of Sciences
  • H. Saito Institute of Health Biosciences and Graduate School of Pharmaceutical Sciences, The University of Tokushima
Keywords: Förster resonance energy transfer, lipid bilayer, Thioflavin T, apolipoprotein A-I.

Abstract

Förster resonance energy transfer (FRET) between anthrylvinyl-labeled phosphatidylcholine (AV-PC) as
a donor and Thioflavin T (ThT) as an acceptor has been employed to explore the binding of N-terminal
fragments of wild (A83) and amyloidogenic variants of apolipoprotein A-I (apoA-I) with substitution
mutations G26R, G26R/W@8, G26R/W@50 and G26R/W@72 to the model membranes composed of
phosphatidylcholine (PC). Analysis of the experimental data in terms of 2D FRET model combined with
the partition model revealed that ThT distance from the lipid bilayer center falls in the range 1.7-2.5 nm,
suggesting that the dye is located in the interfacial membrane region, at the level of phospholipid
headgroups, while partition coefficient characterizing ThT distribution between the aqueous and lipid
phases was estimated to be ca. 4×102. Interaction of monomeric apoA-I N-terminal fragments with PC
liposomes resulted in the increase of AV-ThT FRET efficiency, while this parameter displayed
ambiguous behavior upon membrane binding of fibrillar apoA-I mutants. These findings were
rationalized in terms of the existence of discrete lipid-binding sites within the fibril structure. It was
demonstrated that FRET technique can be employed for ascertaining specific modes of fibril-membrane
interactions.

Downloads

Download data is not yet available.

Author Biographies

M. S. Girych, V. N. Karazin Kharkiv National University

4 Svobody Sq., 61022, Kharkiv, Ukraine

I. L. Maliyov, V. N. Karazin Kharkiv National University

4 Svobody Sq., 61022, Kharkiv, Ukraine

M. V. Romanova, V. N. Karazin Kharkiv National University

4 Svobody Sq., 61022, Kharkiv, Ukraine

G. P. Gorbenko, V. N. Karazin Kharkiv National University

4 Svobody Sq., 61022, Kharkiv, Ukraine

E. Adachi, Institute of Health Biosciences and Graduate School of Pharmaceutical Sciences, The University of Tokushima


1-78-1 Shomachi, Tokushima 770-8505, Japan

C. Mizuguchi, Institute of Health Biosciences and Graduate School of Pharmaceutical Sciences, The University of Tokushima

1-78-1 Shomachi, Tokushima 770-8505, Japan

J. G. Molotkovsky, Institute of Bioorganic Chemistry, Russian Academy of Sciences

Institute of Bioorganic Chemistry, Russian Academy of Sciences

H. Saito, Institute of Health Biosciences and Graduate School of Pharmaceutical Sciences, The University of Tokushima

1-78-1 Shomachi, Tokushima 770-8505, Japan

References

1. Chiti F. Protein misfolding, functional amyloid, and human disease / F. Chiti, C. M. Dobson // Annu. Rev. Biochem. – 2006. – V. 75. – P. 333–366.

2. Stefani M. Generic cell dysfunction in neurodegenerative disorders: role of surfaces in early protein misfolding, aggregation, and aggregate cytotoxicity / M. Stefani // Neuroscientist. – 2007. – V. 13(5). – P. 519–531.

3. Greenwald J. Biology of Amyloid: Structure, Function, and Regulation / J. Greenwald, R. Riek // Structure. – 2010. – V. 18. – P. 1244–1260.

4. Kinnunen P. K. J. Amyloid formation on lipid membrane surfaces / P. K. J. Kinnunen // Open Biol. J. – 2009. – V. 2. – P. 163–175.

5. The two-fold aspect of the interplay of amyloidogenic proteins with lipid membranes / A. Relini, O. Cavalleri, R. Rolandi, A. Gliozzi // Chem. Phys. Lipids. – 2009. – V. 158(1). – P. 1–9.

6. Stefani M. Biochemical and biophysical features of both oligomer⁄fibril and cell membrane in amyloid cytotoxicity / M. Stefani // FEBS J. – 2010. – V. 277(22). – P. 4602–4613.

7. Komoda T. The HDL Handbook. Biological Functions and Clinical Implications / T. Komoda. Academic Press, 2010.

8. Ramirez-Alvarado M. Protein Misfolding Diseases: Current and Emerging Principles and Therapies / M. Ramirez-Alvarado, J. W. Kelly, C. M. Dobson. – John Wiley & Sons, Inc., 2010.

9. Sarantseva S. Amyloidosis - Mechanisms and Prospects for Therapy / S. Sarantseva // Intech., 2011.

10. Dual role of an N-terminal amyloidogenic mutation in apolipoprotein A-I: destabilization of helix bundle and enhancement of fibril formation / E. Adachi, H. Nakajima, C. Mizuguchi [et al.] // J. Biol. Chem. – 2013. – V. 288. – P. 2848–2856.

11. Groenning M. Binding mode of Thioflavin T and other molecular probes in the context of amyloid fibrils—current status / M. Groenning // J. Chem. Biol. – 2010. – V. 3(1). – P. 1–18.

12. Bergelson L. Lipid-specific fluorescent probes in studies of biological membranes / L. Bergelson, J. Molotkovsky, Y. Manevich // Chem. Phys. Lipids. – 1985. – V. 37. – P. 165–195.

13. Lakowicz J. R. Principles of fluorescence spectroscopy / J. R. Lakowicz. Springer: New York., 2006.

14. Bulychev A. A. Current methods of biophysical studies / A. A. Bulychev, V. N. Verchoturov, B. A. Gulaev. Vyschaya shkola. Moscow., 1998.

15. Fung B.K. Surface density determination in membranes by fluorescence energy transfer / B. K. Fung, L. Stryer // Biochemistry. – 1978. – V. 17. – P. 5241–5248.

16. Effect of cholesterol on bilayer location of the class A peptide Ac-18A-NH2 as revealed by fluorescence resonance energy transfer / G. Gorbenko, T. Handa, H. Saito [et al.] // Eur. Biophys. J. 2003. – V. 32(8). – P. 703–709.

17. Dale R. The orientational freedom of molecular probes. The orientation factor in intramolecular energy transfer / R. Dale, J. Eisinger, W. Blumberg // Biophys. J. – 1979. – V. 26. – P. 161–193.

18. Differential study of phosphatidylcholine and sphingomyelin in human high-density lipoproteins with lipid-specific fluorescent probes / J. Molotkovsky, E. Manevich, E. Gerasimova [et al.] // Eur. J. Biochem. – 1982. – V. 122. – P. 573–579.

19. Structure of apolipoprotein A-I N terminus on nascent high density lipoproteins / J. O. Lagerstedt, G. Cavigiolio, M. S. Budamagunta [et al.] // J Biol Chem. – 2011. – V. 286. – P. 2966–2975.

20. Effects of the Iowa and Milano mutations on apolipoprotein A-I structure and dynamics determined by hydrogen exchange and mass spectrometry / P. S. Chetty, M. Ohshiro, H. Saito [et al.] // Biochemistry. – 2012. – V. 51(44). – P. 8993–9001.

21. Effects of a lipid environment on the fibrillogenic pathway of the N-terminal polypeptide of human apolipoprotein A-I, responsible for in vivo amyloid fibril formation / D. M. Monti, F. Guglielmi, M. Monti [et al.] // European Biophysics Journal. – 2010. – V. 39. – P. 1289–1299.

22. Babenko V. Thioflavin T forms a non-fluorescent complex with α-helical poly-L-glutamic acid / V. Babenko, W. Dzwolak // Chem. Commun. – 2011. – V. 47. – P. 10686–10688.

23. Solar M. Comparative analysis of nanomechanics of protein filaments under lateral loading / M. Solar, M. J. Buehler // Nanoscale. – 2012. – V. 21(4). – P. 1177–1183.

24. Robert T. Solid State NMR Studies of Amyloid Fibril Structure / T. Robert // Annu. Rev. Phys. Chem. – 2011. – V. 62. – P. 279–299.
Cited
How to Cite
Girych, M. S., Maliyov, I. L., Romanova, M. V., Gorbenko, G. P., Adachi, E., Mizuguchi, C., Molotkovsky, J. G., & Saito, H. (1). Fluorescence energy transfer study of the lipid bilayer interactions with truncated apolipoprotein a-i mutants. Biophysical Bulletin, 1(29). Retrieved from https://periodicals.karazin.ua/biophysvisnyk/article/view/2327