Probing the oligomeric state of phospholamban variants in phospholipid bilayers from solid-state NMR measurements of rotational diffusion rates

Biochemistry

Volumn 44, Issue 10, 2005, Pages 4055-4066

  Hughes, Eleri ^a   Clayton, Jonathan C ^a   Middleton, David A ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CELLS; DIFFUSION IN LIQUIDS; DIMERS; MEMBRANES; MICELLES; MONOMERS; NUCLEAR MAGNETIC RESONANCE; OLIGOMERS; POLARIZATION; PROTEINS;

DIPOLAR COUPLINGS; PHOSPHOLAMBAN (PLB); SARCOPLASMIC RETICULUM (SR); SODIUM DODECYL SULFATE (SDS);

PHOSPHOLIPIDS;

ALANINE; CYSTEINE; DIMER; DIMYRISTOYLPHOSPHATIDYLCHOLINE; MEMBRANE PROTEIN; MONOMER; MUTANT PROTEIN; OLIGOMER; PHOSPHOLE DERIVATIVE;

ARTICLE; CARBON NUCLEAR MAGNETIC RESONANCE; CELL HETEROGENEITY; GEL; PHOSPHOLIPID BILAYER; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; SOLID STATE;

ALANINE; AMINO ACID SEQUENCE; CALCIUM-BINDING PROTEINS; CARBON ISOTOPES; CYSTEINE; DEUTERIUM EXCHANGE MEASUREMENT; DIMYRISTOYLPHOSPHATIDYLCHOLINE; ELECTROPHORESIS, POLYACRYLAMIDE GEL; LIPID BILAYERS; MAGNETIC RESONANCE SPECTROSCOPY; MEMBRANE PROTEINS; MODELS, CHEMICAL; MOLECULAR SEQUENCE DATA; PHOSPHOLIPIDS; PHOSPHORUS ISOTOPES; THERMODYNAMICS; VARIATION (GENETICS);

MUS;

EID: 14844354134     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi0482351     Document Type: Article

References (36)

1. Arkin, I. T., Adams, P. D., Brunger, A. T., Smith, S. O., and Engelman, D. M. (1997) Structural perspectives of phospholamban, a helical transmembrane pentamer, Annu. Rev. Biophys. Biomol. Struct. 26, 157-179.
2. Wegener, A. D., and Jones, L. R. (1984) Phosphorylation-induced mobility shift in phospholamban in sodium dodecyl sulfate-polyacrylamide gels - Evidence for a protein-structure consisting of multiple identical phosphorylatable subunits, J. Biol. Chem. 259, 1834-1841.
3. Cornea, R. L., Jones, L. R., Autry, J. M., and Thomas, D. D. (1997) Mutation and phosphorylation change the oligomeric structure of phospholamban in lipid bilayers, Biochemistry 36, 2960-2967.
4. Li, M., Reddy, L. G., Bennett, R., Silva, N. D., Jones, L. R., and Thomas, D. D. (1999) A fluorescence energy transfer method for analyzing protein oligomeric structure: Application to phospholamban, Biophys. J. 76, 2587-2599.
5. Reddy, L. G., Autry, J. M., Jones, L. R., and Thomas, D. D. (1999) Co-reconstitution of phospholamban mutants with the Ca-ATPase reveals dependence of inhibitory function on phospholamban structure, J. Biol. Chem. 274, 7649-7655.
6. 2+ pump and phospholamban in Spodoptera frugiperda (Sf21) cells reveals new insights on ATPase regulation, J. Biol. Chem. 272, 15872-15880.
7. Kimura, Y., Kurzydlowski, K., Tada, M., and MacLennan, D. H. (1997) Phospholamban inhibitory function is activated by depolymerization, J. Biol. Chem. 272, 15061-15064.
8. Arkin, I. T., Adams, P. D., Mackenzie, K. R., Lemmon, M. A., Brunger, A. T., and Engelman, D. M. (1994) Structural organization of the pentameric transmembrane alpha-helices of phospholamban, a cardiac ion-channel, EMBO J. 13, 4757-4764.
9. Mayer, E. J., McKenna, E., Garsky, V. M., Burke, C. J., Mach, H., Middaugh, C. R., Sardana, M., Smith, J. S., and Johnson, R. G. (1996) Biochemical and biophysical comparison of native and chemically synthesized phospholamban and a monomeric phospholamban analog, J. Biol. Chem. 271, 1669-1677.
10. Karim, C. B., Stamm, J. D., Karim, J., Jones, L. R., and Thomas, D. D. (1998) Cysteine reactivity and oligomeric structures of phospholamban and its mutants, Biochemistry 37, 12074-12081.
11. Pollesello, P., Annila, A., and Ovaska, M. (1999) Structure of the 1-36 amino-terminal fragment of human phospholamban by nuclear magnetic resonance and modeling of the phospholamban pentamer, Biophys. J. 76, 1784-1795.
12. Simmerman, H. K. B., Kobayashi, Y. M., Autry, J. M., and Jones, L. R. (1996) A leucine zipper stabilizes the pentameric membrane domain of phospholamban and forms a coiled-coil pore structure, J. Biol. Chem. 271, 5941-5946.
13. Torres, J., Adams, P. D., and Arkin, I. T. (2000) Use of a new label C-13=O-18 in the determination of a structural model of phospholamban in a lipid bilayer. Spatial restraints resolve the ambiguity arising from interpretations of mutagenesis data, J. Mol. Biol. 300, 677-685.
14. Ying, W., and Smith, S. O. (2000) Deuterium NMR reveals helix packing interactions in phospholamban, Biophys. J. 78, 924.
15. Reddy, L. G., Jones, L. R., and Thomas, D. D. (1999) Depolymerization of phospholamban in the presence of calcium pump: A fluorescence energy transfer study, Biochemistry 38, 3954-3962.
16. Ying, W., Irvine, S. E., Beekman, R. A., Siminovitch, D. J., and Smith, S. O. (2000) Deuterium NMR reveals helix packing interactions in phospholamban, J. Am. Chem. Soc. 122, 11125-11128.
17. Smith, S. O., Kawakami, T., Liu, W., Ziliox, M., and Aimoto, S. (2001) Helical structure of phospholamban in membrane bilayers, J. Mol. Biol. 313, 1139-1148.
18. Mascioni, A., Karim, C., Zamoon, J., Thomas, D. D., and Veglia, G. (2002) Solid-state NMR and rigid body molecular dynamics to determine domain orientations of monomeric phospholamban, J. Am. Chem. Soc. 124, 9392-9393.
19. Karim, C. B., Marquardt, C. G., Stamm, J. D., Barany, G., and Thomas, D. D. (2000) Synthetic null-cysteine phospholamban analogue and the corresponding transmembrane domain inhibit the Ca-ATPase, Biochemistry 39, 10892-10897.
20. Laemmli, U. K. (1970) Nature 227, 680-685.
21. Schagger, H., and von Jagow, G. (1987) Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa, Anal. Biochem. 166, 368-379.
22. Dzandu, J. K., Johnson, J. F., and Wise, G. E. (1988) Sodium dodecyl-sulfate gel-electrophoresis - Staining of polypeptides using heavy-metal salts, Anal. Biochem. 174, 157-167.
23. Hong, M., Gross, J. D., and Griffin, R. G. (1997) Site-resolved determination of peptide torsion angle phi from the relative orientations of backbone N-H and C-H bonds by solid-state NMR, J. Phys. Chem. B 101, 5869-5874.
24. Bennett, A. E., Rienstra, C. M., Auger, M., Lakshmi, K. V., and Griffin, R. G. (1995) Heteronuclear decoupling in rotating solids, J. Chem. Phys. 103, 6951-6958.
25. Levitt, M. H., Raleigh, D. P., Creuzet, F., and Griffin, R. G. (1990) Theory and simulations of homonuclear spin pair systems in rotating solids, J. Chem. Phys. 92, 6347-6364.
26. Davis, J. H., Jeffrey, K. R., Bloom, M., Valic, M. I., and Higgs, T. P. (1976) Quadrupolar echo deuteron magnetic resonance spectroscopy in ordered hydrocarbon chains, Chem. Phys. Lett. 42, 390-394.
27. Esmann, M., Horvath, L. I., and Marsh, D. (1987) Saturation-transfer electron-spin resonance studies on the mobility of spin-labeled sodium and potassium-ion activated adenosine-triphosphatase in membranes from Squalus acanthias. Biochemistry 26, 8675-8683.
28. Petrache, H. I., Dodd, S. W., and Brown, M. F. (2000) Area per lipid and acyl length distributions in fluid phosphatidylcholines determined by H-2 NMR spectroscopy, Biophys. J. 79, 3172-3192.
29. Wittebort, R. J., Olejniczak, E. T., and Griffin, R. G. (1987) Analysis of deuterium nuclear-magnetic-resonance line-shapes in anisotropic media, J. Chem. Phys. 86, 5411-5420.
30. Smith, S. A., Levante, T. O., Meier, B. H., and Ernst, R. R. (1994) Computer-simulations in magnetic-Resonance-an object-oriented programming approach, J. Magn. Reson., Ser. A 106, 75-105.
31. Hellstern, S., Pegoraro, S., Karim, C. B., Lustig, A., Thomas, D. D., Moroder, L., and Engel, J. (2001) Sarcolipin, the shorter homologue of phospholamban, forms oligomeric structures in detergent micelles and in liposomes, J. Biol. Chem. 276, 30845-30852.
32. Huster, D., Xiao, L. S., and Hong, M. (2001) Solid-state NMR investigation of the dynamics of the soluble and membrane-bound colicin Ia channel-forming domain, Biochemistry 40, 7662-7674.
33. Sharpe, S., Barber, K. R., and Grant, C. W. M. (2002) Evidence of a tendency to self-association of the transmembrane domain of ErbB-2 in fluid phospholipid bilayers, Biochemistry 41, 2341-2352.
34. Wang, Y., and Jardetsky, O. (2002) Probability based protein secondary structure identification using combined NMR chemical-shift data, Protein Sci. 11, 852-861.
35. Ludlam, C. F. C., Arkin, I. T., Liu, X. M., Rothman, M. S., Rath, P., Aimoto, S., Smith, S. O., Engelman, D. M., and Rothschild, K. J. (1996) Fourier transform infrared spectroscopy and site-directed isotope labeling as a probe of local secondary structure in the transmembrane domain of phospholamban, Biophys. J. 70, 1728-1736.
36. Karim, C. B., Kirby, T. L., Zhang, Z., Nesmelov, Y., and Thomas, D. D. (2004) Phospholamban structural dynamics in lipid bilayers probed by a spin label rigidly coupled to the peptide backbone, Proc. Natl. Acad. Sci. U.S.A. 101, 14437-14442.