Investigating Structural Changes in the Lipid Bilayer upon Insertion of the Transmembrane Domain of the Membrane-Bound Protein Phospholamban Utilizing 31P and 2H Solid-State NMR Spectroscopy

Biophysical Journal

Volumn 86, Issue 3, 2004, Pages 1564-1573

  Dave, Paresh C ^a   Tiburu, Elvis K ^a   Damodaran, Krishnan ^a   Lorigan, Gary A ^a  

^a MIAMI UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DEUTERIUM; PHOSPHOLAMBAN; PHOSPHORUS 31;

ARTICLE; LIPID BILAYER; MEMBRANE BINDING; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PEPTIDE ANALYSIS; PHOSPHORUS NUCLEAR MAGNETIC RESONANCE; PROTEIN PURIFICATION; PROTEIN STRUCTURE;

INSERTION SEQUENCES;

EID: 1542345586     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(04)74224-1     Document Type: Article

References (70)

1. Arora, A., and L. K. Tamm. 2001. Biophysical approaches to membrane protein structure determination. Curr. Opin. Struct. Biol. 11:540-547.
2. Auger, M. 1997. Membrane structure and dynamics as viewed by solid-state NMR spectroscopy. Biophys. Chem. 68:233-241.
3. Barre, P., O. Zschoring, K. Arnold, and D. Huster. 2003. Structural and dynamical changes of the bindin B18 peptide upon binding to lipid membranes. Biochemistry. 42:8377-8386.
4. Bloom, M., E. Evans, and O. G. Mouritsen. 1991. Physical properties of the fluid lipid-bilayer component of cell membrane: a perspective. Q. Rev. Biophys. 24:293-397.
5. Brunner, E., J. Ogle, M. Wenzler, and H. R. Kalbitzer. 2000. Molecular alignment of proteins in bicellar solutions: Quantitative evaluation of effects induced in 2D COSY spectra. Biochem. Biophys. Res. Commun. 272:694-698.
6. 31P NMR line shapes. Biochim. Biophys. Acta. 1980:63-69.
7. Cavagnero, S., H. J. Dyson, and P. E. Wright. 1999. Improved low pH bicelle system for orienting macromolecules over a wide temperature range. J. Biomol. NMR. 13:387-391.
8. Cross, T. A. 1997. Solid-state nuclear magnetic resonance characterization of gramicidin channel structure. Methods Enzymol. 289:672-696.
9. Cullis, P. R., and B. de Kruijff. 1979. Lipid polymorphism and the functional roles of lipids in biological membranes. Biochim. Biophys. Acta. 559:399-420.
10. 2H NMR studies. Solid State Nucl. Magn. Reson. 24:328-339.
11. Davis, J. H. 1979. Deuterium magnetic resonance study of the gel and liquid crystalline phases of dipalmitoyl phosphatidylcholine. Biophys. J. 27:339-358.
12. Davis, J. H., K. R. Jeffrey, M. Bloom, and M. I. Valic. 1976. Quadrupolar echo deuteron magnetic resonance spectroscopy in ordered hydrocarbon chains. Chem. Phys. Lett. 42:390-394.
13. de Kruijff, B., and P. R. Cullis. 1980. Cytochrome-c specifically induces non-bilayer structures in cardiolipin-containing model membranes. Biochim. Biophys. Acta. 902:477-490.
14. Dempsey, C. E., N. J. P. Ryba, and A. Watts. 1986. Evidence from deuterium nuclear magnetic resonance for the temperature dependent reversible self association of erythrocyte band-3 in dimyristoylphosphatidylcholine bilayers. Biochemistry. 25:2180-2187.
15. Dufourc, E. J., E. J. Parish, S. Chitrakorn, and I. C. P. Smith. 1984. Structural and dynamical details of cholesterol-lipid interaction as revealed by deuterium NMR. Biochemistry. 23:6062-6071.
16. Epand, R. M. 1998. Lipid polymorphism and protein-lipid interactions. Biochim. Biophys. Acta. 1376:353-368.
17. Fujii, J., A. Ueno, K. Kitano, S. Tanaka, M. Kadoma, and M. Tada. 1987. Characterization of structural unit of phospholamban by amino acid sequencing and electropherotic analysis. Biochem. Biophys. Res. Commun. 138:1044-1050.
18. Hallock, K. J., D. K. Lee, and A. Ramamoorthy. 2003. MSI-78, an analogue of the magainin antimicrobial peptides, disrupts lipid structure via positive curvature strain. Biophys. J. 84:3052-3060.
19. 31P solid-state NMR spectroscopy investigation. Biochemistry. 39:13106-13114.
20. Henzler Wildman, K. A., D. K. Lee, and A. Ramamoorthy. 2003. Mechanism of lipid bilayer disruption by the human antimicrobial peptide, LL-37. Biochemistry. 42:6545-6558.
21. Hori, Y., M. Demura, T. Niidome, H. Aoyagi, and T. Asakura. 1999. Orientational behavior of phospholipid membranes with mastoparan studied by 31P solid state NMR. FEBS Lett. 455:228-232.
22. 2H NMR and molecular dynamics simulations. J. Am. Chem. Soc. 124:298-309.
23. Huster, D., K. Arnold, and K. Garwrisch. 1998. Influence of docosahexaenoic acid and cholesterol on lateral lipid organization. Biochemistry. 37:17299-17308.
24. Huster, D., X. Yao, K. Jakes, and M. Hong. 2002. Conformational changes of colicin Ia channel-forming domain upon membrane binding: a solid-state NMR study. Biochim. Biophys. Acta. 1561:159-170.
25. Jones, D. T., W. R. Taylor, and J. M. Thormon. 1994. A model recognition approach to the prediction of all-helical membrane protein structure and topology. Biochemistry. 33:3038-3049.
26. 2H-nuclear magnetic resonance. Biophys. J. 56:1037-1041.
27. Lemmon, M. A., and D. M. Engelman. 1994a. Specificity and promiscuity in membrane helix interactions. FEBS Lett. 346:17-20.
28. Lemmon, M. A., and D. M. Engelman. 1994b. Specificity and promiscuity in membrane helix interactions. Q. Rev. Biophys. 27:157-218.
29. 31P NMR spectroscopic study of the effect of transmembrane a-helical peptides on the lamellar-reversed hexagonal phase transition of phosphatidylethanolamine model membranes. Biochemistry. 40:760-768.
30. Long, J. R., J. L. Dindot, H. Zebroski, S. Kiihne, R. H. Clark, A. A. Campbell, P. S. Stayton, and G. P. Drobny. 1998. A peptide that inhibits hydroxyapatite growth is in an extended conformation on the crystal surface. Proc. Natl. Acad. Sci. USA. 95:12083-12087.
31. Long, J. R., W. J. Shaw, P. S. Stayton, and G. P. Drobny. 2001. Structure and dynamics of hydrated statherin on hydroxyapatite as determined by solid-state NMR. Biochemistry. 40:15451-15455.
32. Marassi, F. M., C. Ma, H. Gratkowski, S. K. Straus, K. Strebel, M. Orblatt-Montal, M. Montal, and S. J. Opella. 1999. Correlation of the structural and functional domains in the membrane protein Vpu from HIV-1. Proc. Natl. Acad. Sci. USA. 96:14336-14341.
33. Marassi, F. M., and S. J. Opella. 1998. NMR structural studies of membrane proteins. Curr. Opin. Struct. Biol. 8:640-648.
34. 2H solid-state NMR. Biophys. J. 85:328-339.
35. Mascioni, A., C. Karim, J. Zamoon, D. D. Thomas, and G. Vegila. 2002a. Solid-state NMR and rigid body molecular dynamics to determine domain orientations of monomeric phospholamban. J. Am. Chem. Soc. 124:9392-9393.
36. Mascioni, A., C. Karim, G. Barany, D. D. Thomas, and G. Vegila. 2002b. Structure and orientation of sacrolipin in lipid environments. Biochemistry. 41:475-482.
37. Massiot, D., F. Fayon, M. Capron, I. King, S. Le Calve, B. Alonso, J. O. Durand, B. Bujoli, Z. Gan, and G. Hoatson. 2002. Modelling one- and two-dimensional solid-state NMR spectra. Magn. Reson. Chem. 40: 70-76.
38. McCabe, M. A., and S. R. Wassall. 1995. Fast-Fourier-transform dePaking. J. Magn. Reson. B. 106:80-82.
39. McCabe, M. A., and S. R. Wassall. 1997. Rapid deconvolution of NMR powder spectra by weighted fast Fourier transformation. Solid State Nucl. Magn. Reson. 10:53-61.
40. Morrow, M. R., and C. W. M. Grant. 2000. The EGF-receptor transmembrane domain: peptide-peptide interactions in fluid bilayer membranes. Biophys. J. 79:2024-2032.
41. Nakazawa, Y., and T. Asakura. 2003. Structure determination of a peptide model of the repeated helical domain in Samia cynthia ricini silk fibroin before spinning by a combination of advanced solid-state NMR methods. J. Am. Chem. Soc. 125:7230-7237.
42. Nezil, F. A., and M. Bloom. 1992. Combined influence of cholesterol and synthetic amphiphilic peptides upon bilayer thickness in model membranes. Biophys. J. 61:1176-1183.
43. Nicholson, L. K., and T. A. Cross. 1989. Gramicidin cation channel: an experimental determination of the right-handed helix sense and verification of beta-type hydrogen bonding. Biochemistry. 28:9379-9385.
44. Ottiger, M., and A. Bax. 1999. Bicelle-based liquid crystals for NMR-measurement of dipolar couplings at acidic and basic pH values. J. Biomol. NMR. 13:187-191.
45. 31P NMR: the effects of a peripheral protein on collective lipid fluctuations. Solid State Nucl. Magn. Reson. 8:55-64.
46. Pinheiro, T. J. T., and A. Watts. 1994a. Lipid specificity in the interaction of cytochrome-c with anionic phospholipid-bilayers revealed by solid-state P-31 NMR. Biochemistry. 33:2451-2458.
47. Pinheiro, T. J. T., and A. Watts. 1994b. Resolution of individual lipids in mixed phospholipid membranes and specific lipid-cytochrome c interactions by magic-angle spinning solid-state P-31 NMR. Biochemistry. 33:2459-2467.
48. 2H NMR. Biochemistry. 35:12591-12601.
49. Sanders, C. R., and J. P. Schwonek. 1992. Characterization of magnetically orientable bilayers in mixtures of dihexanoylphosphatidylcholine and dimyristoylphosphatidylcholine by solid-state NMR. Biochemistry. 31:8898-8905.
50. 31P Nuclear magnetic resonance and the head group structure of phospholipids in membranes. Biochim. Biophys. Acta. 515:105-140.
51. Seelig, J., and W. Niederberger. 1974. Deuterium-labeled lipids as structural probes in liquid crystalline bilayers. A deuterium magnetic resonance. J. Am. Chem. Soc. 96:2069-2072.
52. Seelig, A., and J. Seelig. 1974. The dynamic structure of fatty acyl chains in a phosphatidylcholine bilayer measured by deuterium magnetic resonance. Biochemistry. 13:4839-4845.
53. Sharpe, S., K. R. Barber, C. W. M. Grant, D. Goodyear, and M. R. Morrow. 2002a. Organization of model helical peptides in lipid bilayers: insight into the behavior of single-span protein transmembrane domains. Biophys. J. 83:345-358.
54. Sharpe, S., K. R. Barber, C. W. M. Grant, and M. R. Morrow. 2002b. Evidence of a tendency to self-association of the transmembrane domain of ErbB-2 in fluid phospholipid bilayers. Biochemistry. 41:2341-2352.
55. Shaw, W. J., J. R. Long, J. L. Dindot, A. A. Campbell, P. S. Stayton, and G. P. Drobny. 2000. Determination of statherin N-terminal peptide conformation on hydroxyapatite crystals. J. Am. Chem. Soc. 122:1709-1716.
56. Simmerman, H. K. B., J. H. Collins, J. L. Theibert, A. D. Wegner, and L. R. Jones. 1986. Sequence analysis of phospholamban: identification of phosphorylation sites and two major structural domains. J. Biol. Chem. 261:13333-13341.
57. Simmerman, H. K. B., and L. R. Jones. 1998. Phospholamban: protein structure, mechanism of action, and role in cardiac function. Physiol. Rev. 78:921-947.
58. Simmerman, H. K. B., Y. M. Kobayashi, J. M. Autry, and L. R. Jones. 1996. A leucine zipper stabilizes the pentameric membrane domain of phospholamban and forms a coiled-coil pore structure. J. Biol. Chem. 271:5941-5946.
59. Singer, S. L., and G. L. Nicolson. 1972. The fluid mosaic model of the structure of cell membranes. Science. 175:720-731.
60. Smith, I. C. P., and I. H. Ekiel. 1984. Phosphorus-31 NMR of phospholipids in membranes, Chapter 5. In Phosphorus-31 NMR. D. G. Gorenstein, editor. Academic Press, New York. 447-475.
61. Stockson, G. W., C. F. Polnaszek, A. P. Tulloch, F. Hasan, and I. C. P. Hasan. 1976. Molecular motion and order in single bilayer vesicles and multilamellar dispersions of egg lecithin and lecithin-cholesterol mixtures. A deuterium nuclear magnetic resonance study of specifically labeled lipids. Biochemistry. 15:954-966.
62. 2+-ATPase and phospholamban. Curr. Opin. Struct. Biol. 7:550-558.
63. Strandberg, E., T. Sparrman, and G. Lindblom. 2001. Phase diagrams of systems with cationic a-helical membrane-spanning model peptides and dioleoylphosphatidylcholine. Adv. Colloid Interface Sci. 89-90:239-261.
64. Tiburu, E. K., P. C. Dave, J. F. Vanlerberghe, T. B. Cardon, R. E. Minto, and G. A. Lorigan. 2003. An improved synthetic and purification procedure for the hydrophobic segment of the transmembrane peptide phospholamban. Anal. Biochem. 318:146-151.
65. Vold, R. R., R. S. Prosser, and A. J. Deese. 1997. Isotropic solutions of phospholipid bicelles: a new membrane mimetic for high-resolution NMR studies of polypeptides. J. Biomol. NMR. 9:329-335.
66. Watts, A. 1981. Protein-lipid interactions: do the spectroscopists now agree? Nature. 294:512-513.
67. Watts, A. 1993. Magnetic resonance studies of phospholipid-protein interactions in bilayers. In Phospholipids Handbook. G. Cevc, editor. Marcel Dekker, New York. 687-744.
68. Watts, A. 1998. Solid-state NMR approaches for studying the interaction of peptides and proteins with membranes. Biochim. Biophys. Acta. 1376:297-318.
69. Yao, Q., L. T. L. Chen, J. Li, K. Brungardt, T. C. Squier, and D. J. Bigelow. 2001. Oligomeric interactions between phospholamban molecules regulate Ca-ATPase activity in functionally reconstituted membranes. Biochemistry. 40:6406-6413.
70. Ying, W., S. E. Irvine, R. A. Beekman, D. J. Siminovitch, and S. O. Smith. 2000. Deuterium NMR reveals helix packing interactions in phospholamban. J. Am. Chem. Soc. 122:11125-11128.