Fluorescence approach to evaluating conformational changes upon binding of β-spectrin ankyrin-binding domain mutants with the lipid bilayer

General Physiology and Biophysics

Volumn 28, Issue 3, 2009, Pages 283-293

  Pazdzior, Grzegorz ^a   Chorzalska, Anna ^b   Czogalla, Aleksander ^b   Borowik, Tomasz ^a   Sikorski, Aleksander F ^b,c   Langner, Marek ^a,c  

^a WROCLAW UNIVERSITY OF TECHNOLOGY   (Poland)

^b UNIVERSITY OF WROC AW   (Poland)

^c Academic Centre for the Biotechnology of Lipid Aggregates   (Poland)

Author keywords

Ankyrin binding domain; Fluorescence; Liposomes; Quenching; Spectrin

Indexed keywords

AMINOPHOSPHOLIPID; ANKYRIN; LIPOSOME; MEMBRANE PHOSPHOLIPID; MEMBRANE PROTEIN; MUTANT PROTEIN; SPECTRIN; SPECTRIN BETA SUBUNIT; TRYPTOPHAN; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CELL MEMBRANE; CONFORMATIONAL TRANSITION; EVALUATION; FLUORESCENCE; LIPID BILAYER; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN LIPID INTERACTION; QUALITATIVE ANALYSIS;

ALGORITHMS; ANIMALS; ANKYRINS; BINDING SITES; FLUORESCENCE; LIPID BILAYERS; LIPOSOMES; MEMBRANE POTENTIALS; MODELS, CHEMICAL; MODELS, MOLECULAR; MUTATION; PROTEIN CONFORMATION; RECOMBINANT PROTEINS; SPECTRIN; SPECTRUM ANALYSIS; TRYPTOPHAN; WATER;

EID: 72949086465     PISSN: 02315882     EISSN: None     Source Type: Journal    
DOI: 10.4149/gpb_2009_03_283     Document Type: Article

References (42)

1. An X., Guo X., Sum H., Morrow J., Gratzer W., Mohandas N. (2004): Phosphatidylserine binding sites in erythroid spectrin: location and implications for membrane stability. Biochemistry 43, 310-315; doi:10.1021/bi035653h
2. Bennett V., Branton D. (1977): Selective association of spectrin with the cytoplasmic surface of human erythrocyte plasma membranes. Quantitative determination with purified (32P) spectrin. J. Biol. Chem. 252,2753-2763
3. Bennett V., Stenbuck P. J. (1979): The membrane attachment protein for spectrin is associated with band 3 in human erythrocyte membranes. Nature 280, 468-473; doi:10.1038/280468a0 (Pubitemid 9234557)
4. Bennett V., Stenbuck P. J. (1980): Association between ankyrin and the cytoplasmic domain of band 3 isolated from the human erythrocyte membrane. J. Biol. Chem. 255, 6424-6432
5. Bialkowska K., Zembron A., Sikorski A. F. (1994): Ankyrin inhibits binding of erythrocyte spectrin to phospholipid vesicles. Biochim. Biophys. Acta 1191,21-26; doi:10.1016/0005-2736(94)90228-90233
6. Bok E., Plażuk E., Hryniewicz-Jankowska A., Chorzalska A., Szmaj A., Dubielecka P. M., Stebelska K., Diakowski W., Lisowski M., Langner M., Sikorski A. F. (2007): The lipid-binding role of the βll-spectrin ankyrin-binding domain. Cell Biol. Int. 31, 1482-1494; doi:10.1016/ j.cellbi.2007.06.014
7. Burstein E. A., Vedenkin N., Ivkova M. N. (1973): Fluorescence and location of tryptophan residues in protein molecules. Photochem. Photobiol. 18,263-279; doi:10.1111/j.1751-1097.1973.tb06422.x
8. Byers T. J., Branton D. (1985): Visualization of the protein associations in the erythrocyte membrane skeleton. Proc. Natl. Acad. Sci. U. S. A. 82, 6153-6157; doi:10.1073/ pnas.82.18.6153
9. Callis P. R., Liu T. Q. (2004): Quantitative prediction of fluorescence quantum yields for tryptophan in proteins. J. Phys. Chem. B 108,4248-4259; doi:10.1021/jp0310551
10. Chattopadhyay A., London E. (1987): Parallax method for direct measurement of membrane penetration depth utilizing fluorescence quenching by spin-labeled phospholipids. Biochemistry 26, 39-45; doi:10.1021/bi00375a006
11. Czogalla A., Grzymajlo K., Jezierski A., Sikorski A. F. (2008): Phospholipid-induced structural changes to an erythroid β-spectrin ankyrin-dependent lipid-binding site. Biochim. Biophys. Acta 1778, 2612-2620; doi: 10.1016/ j.bbamem.2008.07.020
12. Czogalla A., Jaszewski A. R., Diakowski W., Bok E., Jezierski A., Sikorski A. F. (2007): Structural insight into an ankyrin-sensitive lipid-binding site of erythroid β-spectrin. Mol. Membr. Biol. 24, 215-224; doi: 10.1080/ 09687860601102427
13. Diakowski W., Prychidny A., Swistak M., Nietubyc M., Bialkowska K., Szopa J., Sikorski A. F. (1999): Brain spectrin (fodrin) interacts with phospholipids as revealed by intrinsic fluorescence quenching and monolayer experiments. Biochem. J. 338, 83-90; doi:10.1042/0264-6021:3380083
14. Discher D. E., Carl P. (2001): New insights into red cell network structure, elasticity, and spectrin unfolding - a current review. Cell. Mol. Biol. Lett. 6, 593-606
15. Djinovic-Carugo K., Young P., Gautel M., Saraste M. (1999): Structure of the alpha-actinin rod: molecular basis for cross-linking of actin filaments. Cell 98, 537-546; doi:10.1016/S0092-8674(00)81981-9 (Pubitemid 29402490)
16. Grum V. L., Li D., MacDonald R. L., Mondragon A. (1999): Structures of two repeats of spectrin suggest models of flexibility. Cell 98, 523-535; doi:10.1016/S0092-8674(00)81980-81987
17. Grzybek M., Chorzalska A., Bok E., Hryniewicz-Jankowska A., Czogalla A., Diakowski W, Sikorski A. F. (2006): Spectrin-phospholipid interactions. Existence of multiple kinds of binding sites? Chem. Phys. Lipids 141,133-141; doi:10.1016/j.chemphyslip.2006.02.008
18. Hartwig J. H. (1995): Actin-binding proteins. 1: Spectrin super family. Protein Profile 2, 703-800
19. Hemming N. J., Anstee D. J., Staricoff M. A., Tanner M. J., Mohandas N. (1995): Identification of the membrane attachment sites for protein 4.1 in the human erythrocyte. J. Biol. Chem. 270, 5360-5366; doi:10.1074/jbc.270.10.5360
20. Hryniewicz-Jankowska A., Bok E., Dubielecka P., Chorzalska A., Diakowski W., Jezierski A., Lisowski M., Sikorski A. F. (2004): Mapping of an ankyrin-sensitive, phos- phatidylethanolamine/phosphatidylcholine mono- and bi-layer binding site in erythroid β-spectrin. Biochem. J. 382, 677-685; doi:10.1042/BJ20040358
21. Karinch A. M., Zimmer W. E., Goodman S. R. (1990): The identification and sequence of the actin-binding domain of human red blood cell β-spectrin. J. Biol. Chem. 265, 11833-11840
22. Ladokhin A. S. (1999): Evaluation of lipid exposure of tryptophan residues in membrane peptides and proteins. Anal. Biochem. 276,65-71; doi:10.1006/abio.l999.4343
23. Ladokhin A. S., Jayasinghe S., White S. H. (2000): How to measure and analyze tryptophan fluorescence in membranes properties, and why bother? Anal. Biochem. 285, 235-245; doi:10.1006/abio.2000.4773
24. Lakowicz J. R. (1999): Principles of Fluorescence Spectroscopy. Kluwer Academic/Plenum Press, New York
25. Langner M., Kubica K. (1999): The electrostatics of lipid surfaces. Chem. Phys. Lipids 101,3-35; doi:10.1016/S0009-3084(99)00052-53
26. McLaughlin S. (1989): The electrostatic properties of membranes. Annu. Rev. Biophys. Biophys. Chem. 18, 113-136; doi:10.1146/annurev.bb.18.060189. 000553
27. Michalak K., Bobrowska M., Sikorski A. F. (1993): Interaction of bovine erythrocyte spectrin with aminophospholipid liposomes. Gen. Physiol. Biophys. 12, 163-170
28. Mouro-Chanteloup I, Delaunay J., Gane P., Nicolas V., Johansen M., Brown E. J., Peters L. L., Le Van Kim C. L., Cartron J. P., Colin Y. (2003): Evidence that the red cell skeleton protein 4.2 interacts with the Rh membrane complex member CD47. Blood 101,338-344; doi:10.1182/blood-2002-04-1285
29. Nagle J. F., Tristram-Nagle S. (2000): Structure of lipid bilayers. Biochim. Biophys. Acta 1469,159-195
30. Nicolas V., Le Van Kim C., Gane P., Birkenmeier C., Cartron J. P., Colin Y., Mouro-Chanteloup I. (2003): Rh-RhAG/ankyrin-R, a new interaction site between the membrane bilayer and the red cell skeleton, is impaired by Rh(null)-associated mutation. J. Biol. Chem. 278, 25526-25533; doi:10.1074/jbc.M302816200
31. Peters L. L., Birkenmeier C. S., Barker J. E. (1992): Fetal compensation of the hemolytic anemia in mice homozygous for the normoblastosis (nb) mutation. Blood 80,2122-2127
32. Pinder J. C., Chung A., Reid M. E., Gratzer W. B. (1993): Membrane attachment sites for the membrane cytoskeletal protein 4.1 of the red blood cell. Blood 82,3482-3488
33. Sahr K. E., Laurila P., Kotula L., Scarpa A. L., Coupai E., Leto T. L., Linnenbach A. J., Winkelmann J. C., Speicher D. W., Marchesi V. T. (1990): The complete cDNA and polypeptide sequences of human erythroid α-spectrin. J. Biol. Chem. 265,4434-4443
34. Sikorski A. F., Bialkowska K. (1996): Interactions of spectrins with membrane intrinsic domain. Cell. Mol. Biol. Lett. 1,97-104
35. Sikorski A. F., Czogalla A., Hryniewicz-Jankowska A., Bok E., Plazuk E., Diakowski W., Chorzalska A., Kolondra A., Langner M., Grzybek M. (2008): Interactions of erythroid and nonerythroid spectrins and other membranes skeletal proteins with lipid mono - and bilayers. In: Advances in Planar Lipid Bilayers and Liposomes, 6 (Ed. A. Leitmannova Liu), pp. 81-104, Elsevier, New York; doi:10.1016/S1554-4516(07)06004-8
36. Sikorski A. F., Michalak K., Bobrowska M. (1987): Interaction of spectrin with phospholipids. Quenching of spectrin intrinsic fluorescence by phospholipid suspensions. Biochim. Biophys. Acta 904, 55-60; doi:10.1016/0005-2736(87)90086-90091
37. Southgate C. D., Chishti A. H., Mitchell B., Yi S. J., Palek J. (1996): Targeted disruption of the murine band 3 gene results in spherocytosis and severe hemolytic anemia despite a normal membrane skeleton. Nat. Genet. 14, 227-230; doi:10.1038/ngl096-227
38. Winkelmann J. C., Chang J. G., Tse W. T., Scarpa A. L., Marchesi V. T., Forget B. G. (1990): Full-length sequence of the cDNA for human erythroid β-spectrin. J. Biol. Chem. 265,11827-11832
39. Yan Y., Winograd E., Viel A., Cronin T., Harrison S. C., Branton D. (1993): Crystal structure of the repetitive segments of spectrin. Science 262,2027-2030; doi:10.1126/science.8266097 (Pubitemid 24041880)
40. Yi S. J., Liu S. C, Derick L. H., Murray J., Barkeret J. E., Cho M. R., Palek J., Golan D. E. (1997): Red cell membrane skeleton of ankyrin-deficient nb/nb mice lack band 3 tetramers but contain normal skeletons. Biochemistry 36, 9596-9604; doi:10.1021/bi9704966
41. Yu J., Goodman S. R. (1979): Syndeins: the spectrin-binding protein(s) of the human erythrocyte membrane. Proc. Natl. Acad. Sci. U. S. A. 76, 2340-2344; doi: 10.1073/ pnas.76.5.2340
42. Zhang Z., Weed S. A., Gallagher P. G., Morrow J. S. (2001): Dynamic molecular modeling of pathogenic mutations in the spectrin self-association domain. Blood 98, 1645-1653; doi:10.1182/blood.V98.6.1645