Interaction of heparins and dextran sulfates with a mesoscopic protein nanopore

Biophysical Journal

Volumn 97, Issue 11, 2009, Pages 2894-2903

  Teixeira, Luciana R ^a   Merzlyak, Petr G ^b   Valeva, Angela ^c   Krasilnikov, Oleg V ^a  

^a FEDERAL UNIVERSITY OF PERNAMBUCO   (Brazil)

^b Institute of Bioorganic Chemistry Uzbekistan Academy of Sciences   (Uzbekistan)

^c JOHANNES GUTENBERG UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA HEMOLYSIN; DEXTRAN SULFATE; HEPARIN; ION CHANNEL; LIPOSOME; POLYANION;

ARTICLE; IC 50; ION CONDUCTANCE; NANOPORE; PROTEIN INTERACTION; SITE DIRECTED MUTAGENESIS; STAPHYLOCOCCUS AUREUS;

STAPHYLOCOCCUS AUREUS;

EID: 72549099597     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2009.09.019     Document Type: Article

References (44)

1. Olenina, L. V., T. I. Kuzmina, B. N. Sobolev, T. E. Kuraeva, E. F. Kolesanova, et al. 2005. Identification of glycosaminoglycan-binding sites within hepatitis C virus envelope glycoprotein E2*. J. Viral Hepat. 12:584-593. (Pubitemid 41532489)
2. Hurst, R. E., R. M. Moldwin, and S. G. Mulholland. 2007. Bladder defense molecules, urothelial differentiation, urinary biomarkers, and interstitial cystitis. Urology. 69:S17-S23.
3. Vannucchi, S., M. Ruggiero, and V. Chiarugi. 1985. Complexing of heparin with phosphatidylcholine - a possible supramolecular assembly of plasma heparin. Biochem. J. 227:57-65. (Pubitemid 15086945)
4. Sagrista, M. L., M. Mora, and M. A. De Madariaga. 2000. Surface modified liposomes by coating with charged hydrophilic molecules. Cell. Mol. Biol. Lett. 5:19-33.
5. Suppiramaniam, V., T. Vaithianathan, K. Manivannan, M. Dhanasekaran, K. Parameshwaran, et al. 2006. Modulatory effects of dextran sulfate and fucoidan on binding and channel properties of AMPA receptors isolated from rat brain. Synapse. 60:456-464. (Pubitemid 44380157)
6. Van, V. D., D. P. Wall, and K. G. Johnson. 2006. Heparan sulfate proteoglycans and the emergence of neuronal connectivity. Curr. Opin. Neurobiol. 16:40-51.
7. Chicoine, L. M., V. Suppiramaniam, T. Vaithianathan, G. Gianutsos, and B. A. Bahr. 2004. Sulfate- and size-dependent polysaccharide modulation of AMPA receptor properties. J. Neurosci. Res. 75: 408-416.
8. Zschornig, O., W. Richter, G. Paasche, and K. Arnold. 2000. Cation-mediated interaction of dextran sulfate with phospholipid vesicles: binding, vesicle surface polarity, leakage and fusion. Colloid Polym. Sci. 278:637-646.
9. Song, L., M. R. Hobaugh, C. Shustak, S. Cheley, H. Bayley, et al. 1996. Structure of staphylococcal α-hemolysin, a heptameric transmembrane pore. Science. 274:1859-1866. (Pubitemid 26424757)
10. Krasilnikov, O. V., P. G. Merzlyak, L. N. Yuldasheva, C. G. Rodrigues, S. Bhakdi, et al. 2000. Electrophysiological evidence for heptameric stoichiometry of ion channels formed by Staphylococcus aureus α-toxin in planar lipid bilayers. Mol. Microbiol. 37:1372-1378.
11. Movileanu, L., S. Cheley, S. Howorka, O. Braha, and H. Bayley. 2001. Location of a constriction in the lumen of a transmembrane pore by targeted covalent attachment of polymer molecules. J. Gen. Physiol. 117:239-251.
12. Ernst, S., G. Venkataraman, V. Sasisekharan, R. Langer, C. L. Cooney, et al. 1998. Pyranose ring flexibility. Mapping of physical data for iduronate in continuous conformational space. J. Am. Chem. Soc. 120: 2099-2107.
13. Gray, G. S., and M. Kehoe. 1984. Primary sequence of the α-toxin gene from Staphylococcus aureus wood 46. Infect. Immun. 46:615-618.
14. Valeva, A., J. Pongs, S. Bhakdi, and M. Palmer. 1997. Staphylococcal α-toxin: the role of the N-terminus in formation of the heptameric pore - a fluorescence study. Biochim. Biophys. Acta. 1325:281-286.
15. Mueller, P., D. O. Rudin, H. T. Tien, and W. C. Wescot. 1963. Methods for formation of single bimolecular lipid membranes in aqueous solution. J. Phys. Chem. 67:534-535.
16. Montal, M., and P. Mueller. 1972. Formation of bimolecular membranes from lipid monolayers and a study of their electrical properties. Proc. Natl. Acad. Sci. USA. 69:3561-3566.
17. Krasilnikov, O. V., V. I. Ternovsky, R. Z. Sabirov, R. K. Zaripova, and B. A. Tashmukhamedov. 1986. Cation-anion selectivity of staphylotoxin channels in lipid bilayer. Biofizika. 31:606-610.
18. Krasilnikov, O. V., P. G. Merzlyak, R. Z. Sabirov, V. I. Ternovsky, and R. K. Zaripova. 1988. Influence of pH on the potential-dependence of staphylococcal toxin channels functioning in phosphatidylcholine bilayer. Ukr. Biokhim. Zh. 60:60-66.
19. Szoka, F., and D. Papahadjopoulos. 1980. Comparative properties and methods of preparation of lipid vesicles (liposomes). Annu. Rev. Biophys. Bioeng. 9:467-508.
20. Ruso, J. M., L. Besada, P. Martinez-Landeira, L. Seoane, G. Prieto, et al. 2003. Interactions between liposomes and cations in aqueous solution. J. Liposome Res. 13:131-145. (Pubitemid 36597237)
21. Guex, N., and M. C. Peitsch. 1997. SWISS-MODEL and the Swiss-PDBViewer: an environment for comparative protein modeling. Electrophoresis. 18:2714-2723. (Pubitemid 28059943)
22. Krasilnikov, O. V., P. G. Merzlyak, L. N. Yuldasheva, and M. F. Capistrano. 2005. Protein electrostriction: a possibility of elastic deformation of the α-hemolysin channel by the applied field. Eur. Biophys. J. 34:997-1006.
23. Rabenstein, D. L. 2002. Heparin and heparan sulfate: structure and function. Nat. Prod. Rep. 19:312-331.
24. Mulloy, B., M. J. Forster, C. Jones, and D. B. Davies. 1993. NMR and molecular-modeling studies of the solution conformation of heparin. Biochem. J. 293:849-858. (Pubitemid 23244575)
25. Larm, O., B. Lindberg, and S. Svensson. 1971. Studies on length of side chains of dextran elaborated by Leuconostoc mesenteroides Nrrl B-512. Carbohydr. Res. 20:39-48.
26. Bovey, F. A. 1959. Enzymatic polymerization. 1. Molecular weight and branching during the formation of dextran. J. Polym. Sci. 35:167-182.
27. Krasilnikov, O. V., P. G. Merzlyak, L. N. Yuldasheva, C. G. Rodrigues, and R. A. Nogueira. 1999. Heparin influence on α-staphylotoxin formed channel. Biochim. Biophys. Acta. 1417:167-182.
28. Bangham, A. D. 1968. Membrane models with phospholipids. Prog. Biophys. Mol. Biol. 18:29-95.
29. Davenport, J. B. 1971. Physical chemistry of lipids. In Biochemistry and Methodology of Lipids. A. R. Johnson and J. B. Davenport, editors. Wiley-Interscience, New York. 47-83.
30. Huster, D., and K. Arnold. 1998. Ca2+-mediated interaction between dextran sulfate and dimyristoyl-sn-glycero-3-phosphocholine surfaces studied by H-2 nuclear magnetic resonance. Biophys. J. 75:909-916. (Pubitemid 28357531)
31. Hattori, T., K. Kimura, E. Seyrek, and P. L. Dubin. 2001. Binding of bovine serum albumin to heparin determined by turbidimetric titration and frontal analysis continuous capillary electrophoresis. Anal. Biochem. 295:158-167.
32. Kragh-Hansen, U., and H. Vorum. 1993. Quantitative analyses of the interaction between calcium ions and human serum-albumin. Clin. Chem. 39:202-208.
33. Yokouchi, Y., T. Tsunoda, T. Imura, H. Yamauchi, S. Yokoyama, et al. 2001. Effect of adsorption of bovine serum albumin on liposomal membrane characteristics. Colloids Surf. B Biointerfaces. 20:95-103.
34. Mulloy, B., and M. J. Forster. 2000. Conformation and dynamics of heparin and heparan sulfate. Glycobiology. 10:1147-1156.
35. De Felice, L. J. 1981. Introduction to Membrane Noise. Plenum Press, New York.
36. Hall, J. E. 1975. Access resistance of a small circular pore. J. Gen. Physiol. 66:531-532.
37. Mangan, P. S., and M. Colombini. 1987. Ultrasteep voltage dependence in a membrane channel. Proc. Natl. Acad. Sci. USA. 84:4896-4900.
38. Burger, K., F. Gaizer, M. Pekli, G. T. Nagy, and J. Siemroth. 1984. The effect of cations on the calcium-ion coordination of heparin. Inorg. Chim. Acta Bioinorg. Chem. 92:173-176.
39. 2+ ions. On the role of the phospholipid head groups. Cell Biol. Int. Rep. 14:353-360.
40. Steffan, G., S. Wulff, and H. J. Galla. 1994. Divalent cation-dependent interaction of sulfated polysaccharides with phosphatidylcholine and mixed phosphatidylcholine phosphatidylglycerol liposomes. Chem. Phys. Lipids. 74:141-150.
41. McLaughlin, S. 1977. Electrostatic potentials at membrane-solution interfaces. In Current Topics in Membranes and Transport. F. Bronner and A. Kleinzeller, editors. Academic Press, New York-London. 71-144.
42. Valeva, A., N. Hellmann, I. Walev, D. Strand, M. Plate, et al. 2006. Evidence that clustered phosphocholine head groups serve as sites for binding and assembly of an oligomeric protein pore. J. Biol. Chem. 281:26014-26021.
43. Aguilella-Arzo, M., J. Cervera, P. Ramirez, and S. Mafe. 2006. Blocking of an ion channel by a highly charged drug: modeling the effects of applied voltage, electrolyte concentration, and drug concentration. Phys. Rev. 73:041914.
44. Karginov, V. A., E. M. Nestorovich, F. Schmidtmann, T. M. Robinson, A. Yohannes, et al. 2007. Inhibition of S-aureus α-hemolysin and B. anthracis lethal toxin by β-cyclodextrin derivatives. Bioorg. Med. Chem. 15:5424-5431.