Structural and functional dynamics of an integral membrane protein complex modulated by lipid headgroup charge

Journal of Molecular Biology

Volumn 418, Issue 5, 2012, Pages 379-389

  Li, Ji ^a   James, Zachary M ^a   Dong, Xiaoqiong ^a   Karim, Christine B ^a   Thomas, David D ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

Author keywords

electrostatic interactions; EPR; FRET; phospholamban; SERCA

Indexed keywords

ANION; CATION; LIPID; PHOSPHOLAMBAN; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE;

ARTICLE; BINDING AFFINITY; CYTOPLASM; ELECTRON SPIN RESONANCE; EQUILIBRIUM CONSTANT; FLUORESCENCE RESONANCE ENERGY TRANSFER; INHIBITION KINETICS; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN STRUCTURE; STATIC ELECTRICITY; T LYMPHOCYTE;

EID: 84862814385     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2012.02.011     Document Type: Article

References (44)

1. Sachs, J. N. & Engelman, D. M. (2006). Introduction to the membrane protein reviews: the interplay of structure, dynamics, and environment in membrane protein function. Annu. Rev. Biochem. 75, 707-712. (Pubitemid 44118049)
2. McLaughlin, S. & Murray, D. (2005). Plasma membrane phosphoinositide organization by protein electrostatics. Nature, 438, 605-611. (Pubitemid 41740564)
3. Tada, M. & Inui, M. (1983). Regulation of calcium transport by the ATPase-phospholamban system. J. Mol. Cell. Cardiol. 15, 565-575. (Pubitemid 13016799)
4. Cantilina, T., Sagara, Y., Inesi, G. & Jones, L. R. (1993). Comparative studies of cardiac and skeletal sarcoplasmic reticulum ATPases. Effect of a phospholamban antibody on enzyme activation by Ca2+. J. Biol. Chem. 268, 17018-17025. (Pubitemid 23236927)
5. Simmerman, H. K. & Jones, L. R. (1998). Phospholamban: protein structure, mechanism of action, and role in cardiac function. Physiol. Rev. 78, 921-947. (Pubitemid 28491945)
6. MacLennan, D. H. & Kranias, E. G. (2003). Phospholamban: a crucial regulator of cardiac contractility. Nat. Rev., Mol. Cell Biol. 4, 566-577. (Pubitemid 36773408)
7. Cornea, R. L., Jones, L. R., Autry, J. M. & Thomas, D. D. (1997). Mutation and phosphorylation change the oligomeric structure of phospholamban in lipid bilayers. Biochemistry, 36, 2960-2967. (Pubitemid 27138580)
8. Zamoon, J., Mascioni, A., Thomas, D. D. & Veglia, G. (2003). NMR solution structure and topological orientation of monomeric phospholamban in dodecylphosphocholine micelles. Biophys. J. 85, 2589-2598. (Pubitemid 37210804)
9. Karim, C. B., Kirby, T. L., Zhang, Z., Nesmelov, Y. & 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. USA, 101, 14437-14442. (Pubitemid 39346767)
10. Karim, C. B., Zhang, Z.,Howard, E.C., Torgersen, K. D. & Thomas, D. D. (2006). Phosphorylation-dependent conformational switch in spin-labeled phospholamban bound to SERCA. J. Mol. Biol. 358, 1032-1040.
11. Traaseth, N. J., Shi, L., Verardi, R., Mullen, D. G., Barany, G. & Veglia, G. (2009). Structure and topology of monomeric phospholamban in lipid membranes determined by a hybrid solution and solid-state NMR approach. Proc. Natl Acad. Sci. USA, 106, 10165-10170.
12. 15N heteronuclear NMR spectroscopy shows four dynamic domains for phospholamban reconstituted in dodecylphosphocholine micelles. Biophys. J. 87, 1205-1214.
13. Metcalfe, E. E., Traaseth,N. J.&Veglia,G. (2005). Serine 16 phosphorylation induces an order-to-disorder transition in monomeric phospholamban. Biochemistry, 44, 4386-4396. (Pubitemid 40403980)
14. Toyoshima, C., Nakasako, M., Nomura, H. & Ogawa, H. (2000). Crystal structure of the calcium pump of sarcoplasmic reticulum at 2.6 Å resolution. Nature, 405, 647-655. (Pubitemid 30428644)
15. 2+-ATPase: design of a perfect chemi-osmotic pump. Q. Rev. Biophys. 43, 501-566.
16. 2+ATPase. Proc. Natl Acad. Sci. USA, 100, 467-472.
17. 2+, but not by phospholamban phosphorylation, vanadate, or thapsigargin, and are enhanced by ATP. J. Biol. Chem. 275, 15034-15038.
18. 2+-ATPase by protein kinase A and by anti-phospholamban monoclonal antibody 2D12. J. Biol. Chem. 282, 20968-20976.
19. Kirby, T. L., Karim, C. B. & Thomas, D. D. (2004). Electron paramagnetic resonance reveals a large-scale conformational change in the cytoplasmic domain of phospholamban upon binding to the sarcoplasmic reticulum Ca-ATPase. Biochemistry, 43, 5842-5852. (Pubitemid 38623618)
20. Zamoon, J., Nitu, F., Karim, C., Thomas, D. D. & Veglia, G. (2005). Mapping the interaction surface of a membrane protein: unveiling the conformational switch of phospholamban in calcium pump regulation. Proc. Natl Acad. Sci. USA, 102, 4747-4752. (Pubitemid 40471525)
21. Nesmelov, Y. E., Karim, C. B., Song, L., Fajer, P. G. & Thomas, D. D. (2007). Rotational dynamics of phospholamban determined by multifrequency electron paramagnetic resonance. Biophys. J. 93, 2805-2812. (Pubitemid 47607816)
22. Kast, D., Espinoza-Fonseca, L. M., Yi, C. & Thomas, D. D. (2010). Phosphorylation-induced structural changes in smooth muscle myosin regulatory light chain. Proc. Natl Acad. Sci. USA, 107, 8207-8212.
23. Hunter, G. W., Negash, S. & Squier, T. C. (1999). Phosphatidylethanolamine modulates Ca-ATPase function and dynamics. Biochemistry, 38, 1356-1364.
24. Reddy, L. G., Cornea, R. L.,Winters, D. L.,McKenna, E. & Thomas, D. D. (2003). Defining the molecular components of calcium transport regulation in a reconstituted membrane system. Biochemistry, 42, 4585-4592. (Pubitemid 36457628)
25. Mueller, B., Karim, C. B., Negrashov, I. V., Kutchai, H. & Thomas, D. D. (2004). Direct detection of phospholamban and sarcoplasmic reticulum Ca-ATPase interaction in membranes using fluorescence resonance energy transfer. Biochemistry, 43, 8754-8765. (Pubitemid 38880046)
26. Lockamy, E. L., Cornea, R. L., Karim, C. B. & Thomas, D. D. (2011). Functional and physical competition between phospholamban and its mutants provides insight into the molecular mechanism of gene therapy for heart failure. Biochem. Biophys. Res. Commun. 408, 388-392.
27. Birmachu, W., Nisswandt, F. L. & Thomas, D. D. (1989). Conformational transitions in the calcium adenosinetriphosphatase studied by time-resolved fluorescence resonance energy transfer. Biochemistry, 28, 3940-3947. (Pubitemid 19125446)
28. Muretta, J. M., Kyrychenko, A., Ladokhin, A. S., Kast, D. J., Gillispie, G. D. & Thomas, D. D. (2010). Highperformance time-resolved fluorescence by direct waveform recording. Rev. Sci. Instrum. 81, 103101.
29. Agafonov, R. V., Negrashov, I. V., Tkachev, Y. V., Blakely, S. E., Titus, M. A., Thomas, D. D. & Nesmelov, Y. E. (2009). Structural dynamics of the myosin relay helix by time-resolved EPR and FRET. Proc. Natl Acad. Sci. USA, 106, 21625-21630.
30. Lakowicz, J. R. (1999). Principles of Fluorescence Spectroscopy, 2nd edit. Kluwer Academic/Plenum Press, New York, NY.
31. 2+-ATPase by tuning phospholamban structural dynamics. J. Biol. Chem. 282, 37205-37214.
32. Karim, C. B., Marquardt, C. G., Stamm, J. D., Barany, G. & Thomas, D. D. (2000). Synthetic null-cysteine phospholamban analogue and the corresponding transmembrane domain inhibit the Ca-ATPase. Biochemistry, 39, 10892-10897.
33. Gustavsson, M., Traaseth, N. J., Karim, C. B., Lockamy, E. L., Thomas, D. D. & Veglia, G. (2011). Lipidmediated folding/unfolding of phospholamban as a regulatory mechanism for the sarcoplasmic reticulum Ca(2+)-ATPase. J. Mol. Biol. 408, 755-765.
34. Gustavsson, M., Traaseth, N. J. & Veglia, G. (2011). Probing ground and excited states of phospholamban in model and native lipid membranes by magic angle spinning NMR spectroscopy. Biochim. Biophys. Acta, 1818, 146-153.
35. Bick, R. J., Buja, L. M., Van Winkle, W. B. & Taffet, G. E. (1998). Membrane asymmetry in isolated canine cardiac sarcoplasmic reticulum: comparison with skeletal muscle sarcoplasmic reticulum. J. Membr. Biol. 164, 169-175. (Pubitemid 28336994)
36. Cornea, R. L. & Thomas, D. D. (1994). Effects of membrane thickness on the molecular dynamics and enzymatic activity of reconstituted Ca-ATPase. Biochemistry, 33, 2912-2920. (Pubitemid 24103351)
37. Sonntag, Y., Musgaard, M., Olesen, C., Schiott, B., Moller, J. V., Nissen, P. & Thogersen, L. (2011). Mutual adaptation of a membrane protein and its lipid bilayer during conformational changes. Nat. Commun. 2, 304.
38. Hughes, E., Clayton, J. C. & Middleton, D. A. (2009). Cytoplasmic residues of phospholamban interact with membrane surfaces in the presence of SERCA: a new role for phospholipids in the regulation of cardiac calcium cycling? Biochim. Biophys. Acta, 1788, 559-566.
39. Lee, A. G. (2003). Lipid-protein interactions in biological membranes: a structural perspective. Biochim. Biophys. Acta, 1612, 1-40.
40. 2+-ATPase/ phospholamban complex. Biochemistry, 50, 10367-10374.
41. Guo, X. & Huang, L. (2011). Recent advances in nonviral vectors for gene delivery. Acc. Chem. Res. in press. doi:10.1021/ar200151m.
42. Kunze, A., Svedhem, S. & Kasemo, B. (2009). Lipid transfer between charged supported lipid bilayers and oppositely charged vesicles. Langmuir, 25, 5146-5158.
43. Karim, C. B., Zhang, Z. & Thomas, D. D. (2007). Synthesis of TOAC spin-labeled proteins and reconstitution in lipid membranes. Nat. Protoc. 2, 42-49. (Pubitemid 47044699)
44. Reddy, L. G., Autry, J. M., Jones, L. R. & 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.