Solid-state 2H and 15N NMR studies of side-chain and backbone dynamics of phospholamban in lipid bilayers: Investigation of the N27A mutation

Biochimica et Biophysica Acta - Biomembranes

Volumn 1798, Issue 2, 2010, Pages 210-215

  Chu, Shidong ^a   Coey, Aaron T ^a   Lorigan, Gary A ^a  

^a MIAMI UNIVERSITY   (United States)

Author keywords

Dynamics; Phospholamban; Phospholipid membrane; Solid state NMR

Indexed keywords

ADENOSINE TRIPHOSPHATASE (CALCIUM); PHOSPHOLAMBAN;

ARTICLE; CONTROLLED STUDY; DEUTERON NUCLEAR MAGNETIC RESONANCE; LIPID BILAYER; MOLECULAR DYNAMICS; MUTATION; NITROGEN NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; WILD TYPE;

AMINO ACID SUBSTITUTION; ANIMALS; CALCIUM-BINDING PROTEINS; HUMANS; MUTATION, MISSENSE; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; SARCOPLASMIC RETICULUM CALCIUM-TRANSPORTING ATPASES;

EID: 74249090971     PISSN: 00052736     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamem.2009.09.025     Document Type: Article

References (45)

1. Simmerman H.K., and Jones L.R. Phospholamban: protein structure, mechanism of action, and role in cardiac function. Physiol. Rev. 78 (1998) 921-947
2. MacLennan D.H., and Kranias E.G. Phospholamban: a crucial regulator of cardiac contractility. Nat. Rev. Mol. Cell Biol. 4 (2003) 566-577
3. Wegener A.D., Simmerman H.K., Lindemann J.P., and Jones L.R. Phospholamban phosphorylation in intact ventricles. Phosphorylation of serine 16 and threonine 17 in response to beta-adrenergic stimulation, J. Biol. Chem. 264 (1989) 11468-11474
4. Karim C.B., Stamm J.D., Karim J., Jones L.R., and Thomas D.D. Cysteine reactivity and oligomeric structure of phospholamban and its mutants. Biochemistry 37 (1998) 12074-12081
5. Kimura Y., Kurzydlowski K., Tada M., and MacLennan D.H. Phospholamban inhibitory function is activated by depolymerization. J. Biol. Chem. 272 (1997) 15061-15064
6. Cornea R.L., Jones L.R., Autry J.M., and Thomas D.D. Mutation and phosphorylation change the oligomeric structure of phospholamban in lipid bilayers. Biochemistry 36 (1997) 2960-2967
7. 2+-ATPase and the pentameric form of phospholamban in two-dimensional co-crystals. Biophys. J. 90 (2006) 4213-4223
8. In: Ramamoorthy A. (Ed). NMR Spectroscopy of Biological Solids (2005), CRC/Taylor and Francis Group, Boca Raton
9. McDermott A. Structure and dynamics of membrane proteins by magic angle spinning solid-state NMR. Annu. Rev. Biophys. 38 (2009) 385-403
10. Page R.C., Li C., Hu J., Gao F.P., and Cross T.A. Lipid bilayers: an essential environment for the understanding of membrane proteins. Magn. Reson. Chem. 45 (2007) S2-S11
11. Karim C.B., Kirby T.L., Zhang Z.W., Nesmelov Y., and Thomas D.D. 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 (2004) 14437-14442
12. Zamoon J., Mascioni A., Thomas D.D., and Veglia G. NMR solution structure and topological orientation of monomeric phospholamban in dodecylphosphocholine micelles. Biophys. J 85 (2003) 2589-2598
13. Traaseth N.J., Verardi R., Torgersen K.D., Karim C.B., Thomas D.D., and Veglia G. Spectroscopic validation of the pentameric structure of phospholamban. Proc. Natl. Acad. Sci. U.S.A. 104 (2007) 14676-14681
14. 2+-ATPase. Biochemistry 47 (2008) 3-13
15. Oxenoid K., and Chou J.J. The structure of phospholamban pentamer reveals a channel-like architecture in membranes. Proc. Natl. Acad. Sci. U.S.A. 102 (2005) 10870-10875
16. Andronesi O.C., Becker S., Seidel K., Heise H., Young H.S., and Baldus M. Determination of membrane protein structure and dynamics by magic-angle-spinning solid-state NMR spectroscopy. J. Am. Chem. Soc. 127 (2005) 12965-12974
17. 2+-ATPase-bound phospholamban in lipid bilayers by solid-state nuclear magnetic resonance (NMR) spectroscopy. Biochemistry 47 (2008) 4369-4376
18. Hughes E., Clayton J.C., and Middleton D.A. Probing the oligomeric state of phospholamban variants in phospholipid bilayers from solid-state NMR measurements of rotational diffusion rates. Biochemistry 44 (2005) 4055-4066
19. Opella S.J. Protein dynamics by solid state nuclear magnetic resonance. Methods Enzymol 131 (1986) 327-361
20. Krushelnitskya A., and Reichertb D. Solid-state NMR and protein dynamics. Prog. Nucl. Magn. Reson. Spectrosc. 47 (2005) 1-25
21. Hong M. Structure, topology, and dynamics of membrane peptides and proteins from solid-state NMR spectroscopy. J. Phys. Chem. B 111 (2007) 10340-10351
22. 2+-ATPase isoform of cardiac sarcoplasmic reticulum. J. Biol. Chem. 273 (1998) 14238-14241
23. 2+ uptake as a primary cause of heart failure. Cardiovasc. Res. 56 (2002) 248-259
24. Zhai J., Schmidt A.G., Hoit B.D., Kimura Y., MacLennan D.H., and Kranias E.G. Cardiac-specific overexpression of a superinhibitory pentameric phospholamban mutant enhances inhibition of cardiac function in vivo. J. Biol. Chem. 275 (2000) 10538-10544
25. 15N solid-state NMR spectroscopy. Biochemistry 43 (2004) 13899-13909
26. 2H, and REDOR solid-state NMR spectroscopy. Biochim. Biophys. Acta-Biomembranes 1758 (2006) 772-780
27. 13C solid-state NMR spectroscopic study. Biochemistry 45 (2006) 13312-13322
28. 13C heteronuclear dipolar solid-state NMR spectroscopy. J. Magn. Reson. 178 (2006) 283-287
29. 15N solid-state NMR spectroscopy. Biochemistry 46 (2007) 11695-11706
30. 15N solid-state NMR spectroscopy. Protein Sci 16 (2007) 2345-2349
31. Wegener A.D., and Jones L.R. 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 (1984) 1834-1841
32. Davis J.H., Jeffrey K.R., Bloom M., Valic M.I., and Higgs T.P. Quadrupole echo deuteron magnetic resonance spectroscopy in ordered hydrocarbon chains. Chem. Phys. Lett. 42 (1976) 390-394
33. Massiot D., Fayon F., Capron M., King I., Le Calvé S., Alonso B., Durand J.-O., Bujoli B., Gan Z., and Hoatson G. Modelling one- and two-dimensional solid-state NMR spectra. Magn. Reson. Chem. 40 (2002) 70-76
34. Tada M., Kirchberger M.A., and Katz A.M. Phosphorylation of a 22,000-dalton component of the cardiac sarcoplasmic reticulum by adenosine 3′:5′-monophosphate-dependent protein kinase. J. Biol. Chem. 250 (1975) 2640-2647
35. Vorherr T., Wrzosek A., Chiesi M., and Carafoli E. Total synthesis and functional properties of the membrane-intrinsic protein phospholamban. Protein Sci 2 (1993) 339-347
36. Arkin I.T., Rothman M., Ludlam C.F.C., Aimoto S., Engelman D.M., Rothschild K.J., and Smith S.O. Structural model of the phospholamban ion channel complex in phospholipid membranes. J. Mol. Biol. 248 (1995) 824-834
37. Seelig J. Deuterium magnetic resonance: theory and applications to lipid membranes. Q. Rev. Biophys. 10 (1977) 353-418
38. 2H-NMR. Biochim. Biophys. Acta 737 (1983) 117-171
39. Clayton J.C., Hughes E., and Middleton D.A. Spectroscopic studies of phospholamban variants in phospholipid bilayers. Biochem. Soc. Trans. 33 (2005) 913-915
40. Colnago L.A., Valentine K.G., and Opella S.J. Dynamics of fd coat protein in the bacteriophage. Biochemistry 26 (1987) 847-854
41. Kim S., and Cross T.A. Uniformity, ideality, and hydrogen bonds in transmembrane alpha-helices. Biophys J 83 (2002) 2084-2095
42. 2+ ATPase. Proc. Natl. Acad. Sci. U.S.A. 100 (2003) 467-472
43. 2+-ATPase. Biochem. Biophys. Res. Commun. 369 (2008) 188-194
44. 2+-ATPase superinhibition and cardiac remodeling. Circulation 113 (2006) 995-1004
45. 2+-ATPase by tuning phospholamban structural dynamics. J. Biol. Chem. 282 (2007) 37205-37214