Detergent properties influence the stability of the glycophorin a transmembrane helix dimer in lysophosphatidylcholine micelles

Biophysical Journal

Volumn 103, Issue 12, 2012, Pages 2455-2464

  Stangl, Michael ^a   Veerappan, Anbazhagan ^a,b   Kroeger, Anja ^c   Vogel, Peter ^a   Schneider, Dirk ^a  

^a JOHANNES GUTENBERG UNIVERSITY   (Germany)

^b SASTRA UNIVERSITY   (India)

^c MAX PLANCK INSTITUTE FOR POLYMER RESEARCH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

DETERGENT; GLYCOPHORIN; LYSOPHOSPHATIDYLCHOLINE;

AMINO ACID SEQUENCE; ARTICLE; CELL MEMBRANE; CHEMICAL PHENOMENA; CHEMISTRY; DOSE RESPONSE; DRUG EFFECT; HUMAN; MICELLE; MOLECULAR GENETICS; PROTEIN MULTIMERIZATION; PROTEIN SECONDARY STRUCTURE;

AMINO ACID SEQUENCE; CELL MEMBRANE; DETERGENTS; DOSE-RESPONSE RELATIONSHIP, DRUG; GLYCOPHORIN; HUMANS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; LYSOPHOSPHATIDYLCHOLINES; MICELLES; MOLECULAR SEQUENCE DATA; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, SECONDARY;

EID: 84871315983     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2012.11.004     Document Type: Article

References (50)

1. C.M. Franzin, P. Teriete, and F.M. Marassi Structural similarity of a membrane protein in micelles and membranes J. Am. Chem. Soc. 129 2007 8078 8079 (Pubitemid 47035115)
2. A. Veerappan, and F. Cymer D. Schneider The tetrameric α-helical membrane protein GlpF unfolds via a dimeric folding intermediate Biochemistry 50 2011 10223 10230
3. R.A. Melnyk, A.W. Partridge, and C.M. Deber Retention of native-like oligomerization states in transmembrane segment peptides: application to the Escherichia coli aspartate receptor Biochemistry 40 2001 11106 11113 (Pubitemid 32847978)
4. S.L. Federkeil, and T.L. Winstone R.J. Turner Examination of EmrE conformational differences in various membrane mimetic environments Biochem. Cell Biol. 81 2003 61 70 (Pubitemid 37378252)
5. J.J. Chou, and J.D. Kaufman A. Bax Micelle-induced curvature in a water-insoluble HIV-1 Env peptide revealed by NMR dipolar coupling measurement in stretched polyacrylamide gel J. Am. Chem. Soc. 124 2002 2450 2451 (Pubitemid 34251754)
6. N. Grigorieff, and T.A. Ceska R. Henderson Electron-crystallographic refinement of the structure of bacteriorhodopsin J. Mol. Biol. 259 1996 393 421 (Pubitemid 26179019)
7. S. Faham, and J.U. Bowie Bicelle crystallization: a new method for crystallizing membrane proteins yields a monomeric bacteriorhodopsin structure J. Mol. Biol. 316 2002 1 6 (Pubitemid 34729261)
8. E. Pebay-Peyroula, and G. Rummel E.M. Landau X-ray structure of bacteriorhodopsin at 2.5 Ångstroms from microcrystals grown in lipidic cubic phases Science 277 1997 1676 1681 (Pubitemid 27446232)
9. J. Koehler, and E.S. Sulistijo C.R. Sanders Lysophospholipid micelles sustain the stability and catalytic activity of diacylglycerol kinase in the absence of lipids Biochemistry 49 2010 7089 7099
10. M. le Maire, P. Champeil, and J.V. Moller Interaction of membrane proteins and lipids with solubilizing detergents Biochim. Biophys. Acta 1508 2000 86 111
11. G.G. Privé Detergents for the stabilization and crystallization of membrane proteins Methods 41 2007 388 397 (Pubitemid 46400529)
12. A.G. Therien, and C.M. Deber Interhelical packing in detergent micelles. Folding of a cystic fibrosis transmembrane conductance regulator construct J. Biol. Chem. 277 2002 6067 6072 (Pubitemid 34968392)
13. P.J. Booth, and P. Curnow Folding scene investigation: membrane proteins Curr. Opin. Struct. Biol. 19 2009 8 13
14. J.U. Bowie Solving the membrane protein folding problem Nature 438 2005 581 589 (Pubitemid 41740561)
15. J.L. Popot, and D.M. Engelman Membrane protein folding and oligomerization: the two-stage model Biochemistry 29 1990 4031 4037 (Pubitemid 20145635)
16. K.R. MacKenzie, J.H. Prestegard, and D.M. Engelman A transmembrane helix dimer: structure and implications Science 276 1997 131 133 (Pubitemid 27161261)
17. D. Langosch, and B. Brosig H.J. Fritz Dimerization of the glycophorin A transmembrane segment in membranes probed with the ToxR transcription activator J. Mol. Biol. 263 1996 525 530 (Pubitemid 26382072)
18. S.O. Smith, and D. Song S. Aimoto Structure of the transmembrane dimer interface of glycophorin A in membrane bilayers Biochemistry 40 2001 6553 6558 (Pubitemid 32552780)
19. D. Schneider, and D.M. Engelman Motifs of two small residues can assist but are not sufficient to mediate transmembrane helix interactions J. Mol. Biol. 343 2004 799 804 (Pubitemid 39345944)
20. M.A. Lemmon, and J.M. Flanagan D.M. Engelman Sequence specificity in the dimerization of transmembrane α-helices Biochemistry 31 1992 12719 12725 (Pubitemid 23027049)
21. A.K. Doura, and K.G. Fleming Complex interactions at the helix-helix interface stabilize the glycophorin A transmembrane dimer J. Mol. Biol. 343 2004 1487 1497 (Pubitemid 39387839)
22. C. Finger, and T. Volkmer D. Schneider The stability of transmembrane helix interactions measured in a biological membrane J. Mol. Biol. 358 2006 1221 1228
23. V. Anbazhagan, and D. Schneider The membrane environment modulates self-association of the human GpA TM domain - implications for membrane protein folding and transmembrane signaling Biochim. Biophys. Acta 1798 2010 1899 1907
24. H. Hong, and J.U. Bowie Dramatic destabilization of transmembrane helix interactions by features of natural membrane environments J. Am. Chem. Soc. 133 2011 11389 11398
25. L.E. Fisher, D.M. Engelman, and J.N. Sturgis Detergents modulate dimerization, but not helicity, of the glycophorin A transmembrane domain J. Mol. Biol. 293 1999 639 651 (Pubitemid 29512062)
26. L.E. Fisher, D.M. Engelman, and J.N. Sturgis Effect of detergents on the association of the glycophorin A transmembrane helix Biophys. J. 85 2003 3097 3105 (Pubitemid 37345797)
27. V. Anbazhagan, F. Cymer, and D. Schneider Unfolding a transmembrane helix dimer: a FRET study in mixed micelles Arch. Biochem. Biophys. 495 2010 159 164
28. K.R. MacKenzie, and K.G. Fleming Association energetics of membrane spanning α-helices Curr. Opin. Struct. Biol. 18 2008 412 419
29. L. Columbus, and J. Lipfert S.A. Lesley Mixing and matching detergents for membrane protein NMR structure determination J. Am. Chem. Soc. 131 2009 7320 7326
30. M. Merzlyakov, L. Chen, and K. Hristova Studies of receptor tyrosine kinase transmembrane domain interactions: the EmEx-FRET method J. Membr. Biol. 215 2007 93 103 (Pubitemid 47282676)
31. M. Merzlyakov, and K. Hristova Förster resonance energy transfer measurements of transmembrane helix dimerization energetics Methods Enzymol. 450 2008 107 127
32. L. Whitmore, and B.A. Wallace DICHROWEB, an online server for protein secondary structure analyses from circular dichroism spectroscopic data Nucleic Acids Res. 32 Web Server issue 2004 W668 W673
33. L. Whitmore, and B.A. Wallace Protein secondary structure analyses from circular dichroism spectroscopy: methods and reference databases Biopolymers 89 2008 392 400
34. P. Palladino, F. Rossi, and R. Ragone Effective critical micellar concentration of a zwitterionic detergent: a fluorimetric study on n-dodecyl phosphocholine J. Fluoresc. 20 2010 191 196
35. N.J. Turro, and A. Yekta Luminescent probes for detergent solutions. A simple procedure for determination of the mean aggregation number of micelles J. Am. Chem. Soc. 100 1978 5951 5952
36. M. Wolszczak, and J. Miller Characterization of non-ionic surfactant aggregates by fluorometric techniques J. Photochem. Photobiol. Chem. 147 2002 45 54
37. A. Kroeger, and J. Belack G. Wegner Supramolecular structures in aqueous solutions of rigid polyelectrolytes with monovalent and divalent counterions Macromolecules 39 2006 7098 7106 (Pubitemid 44625948)
38. P. Wu, and L. Brand Resonance energy transfer: methods and applications Anal. Biochem. 218 1994 1 13 (Pubitemid 24124740)
39. G. Vitiello, and D. Ciccarelli G. D'Errico Microstructural characterization of lysophosphatidylcholine micellar aggregates: the structural basis for their use as biomembrane mimics J. Colloid Interface Sci. 336 2009 827 833
40. B.D. Adair, and D.M. Engelman Glycophorin A helical transmembrane domains dimerize in phospholipid bilayers: a resonance energy transfer study Biochemistry 33 1994 5539 5544 (Pubitemid 24162990)
41. E. Li, M. You, and K. Hristova Sodium dodecyl sulfate-polyacrylamide gel electrophoresis and Förster resonance energy transfer suggest weak interactions between fibroblast growth factor receptor 3 (FGFR3) transmembrane domains in the absence of extracellular domains and ligands Biochemistry 44 2005 352 360 (Pubitemid 40095737)
42. Y. Asaoka, and K. Yoshida Y. Nishizuka Potential role of phospholipase A2 in HL-60 cell differentiation to macrophages induced by protein kinase C activation Proc. Natl. Acad. Sci. USA 90 1993 4917 4921 (Pubitemid 23182946)
43. Y. Sasaki, Y. Asaoka, and Y. Nishizuka Potentiation of diacylglycerol-induced activation of protein kinase C by lysophospholipids. Subspecies difference FEBS Lett. 320 1993 47 51 (Pubitemid 23089154)
44. M. Okita, and D.C. Gaudette B.J. Holub Elevated levels and altered fatty acid composition of plasma lysophosphatidylcholine(lysoPC) in ovarian cancer patients Int. J. Cancer 71 1997 31 34 (Pubitemid 27158406)
45. L.A. Taylor, and J. Arends U. Massing Plasma lyso-phosphatidylcholine concentration is decreased in cancer patients with weight loss and activated inflammatory status Lipids Health Dis. 6 2007 17
46. V.P. Skipski, and M. Barclay F.M. Archibald Lipid composition of human serum lipoproteins Biochem. J. 104 1967 340 352
47. A.G. Lee Lipid-protein interactions in biological membranes: a structural perspective Biochim. Biophys. Acta 1612 2003 1 40 (Pubitemid 36555684)
48. T.K. Nyholm, S. Ozdirekcan, and J.A. Killian How protein transmembrane segments sense the lipid environment Biochemistry 46 2007 1457 1465
49. H.W. Huang Deformation free energy of bilayer membrane and its effect on gramicidin channel lifetime Biophys. J. 50 1986 1061 1070 (Pubitemid 17205992)
50. K.S. Mineev, and E.V. Bocharov A.S. Arseniev Dimeric structure of the transmembrane domain of glycophorin a in lipidic and detergent environments Acta Naturae 3 2011 90 98