Structural and dynamic basis of phospholamban and sarcolipin inhibition of Ca2+-ATPase

Biochemistry

Volumn 47, Issue 1, 2008, Pages 3-13

  Traaseth, Nathaniel J ^a   Ha, Kim N ^a   Verardi, Raffaello ^b   Shi, Lei ^a   Buffy, Jarrod J ^b   Masterson, Larry R ^a   Veglia, Gianluigi ^a,b  

^a University of Minnesota   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ENZYMATIC REACTION; PHOSPHOLAMBAN (PLN); SARCOLIPIN (SLN);

CALCIUM; METAL IONS; MUSCLE; NUCLEAR MAGNETIC RESONANCE; PHOSPHORYLATION; RELAXATION PROCESSES;

ENZYME ACTIVITY;

CALCIUM; MEMBRANE PROTEIN; PHOSPHOLAMBAN; SARCOLIPIN; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE; UNCLASSIFIED DRUG;

CALCIUM TRANSPORT; ENZYME INHIBITION; ENZYME REGULATION; ENZYME STRUCTURE; HUMAN; MUSCLE RELAXATION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; SARCOPLASMIC RETICULUM; SHORT SURVEY; SOLID STATE;

CALCIUM; CALCIUM-BINDING PROTEINS; CALCIUM-TRANSPORTING ATPASES; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, MOLECULAR; MUSCLE PROTEINS; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN STRUCTURE, SECONDARY; PROTEOLIPIDS;

EID: 37849007303     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi701668v     Document Type: Short Survey

References (62)

1. Fujii, J., Ueno, A., Kitano, K., Tanaka, S., Kadoma, M., and Tada, M. (1987) Complete Complementary DNA-Derived Amino Acid Sequence of Canine Cardiac Phospholamban, J. Clin. Invest. 79, 301-304.
2. Wegener, A. D., Simmerman, H. K., Lindemann, J. P., and Jones, L. R. (1989) Phospholamban Phosphorylation in Intact Ventricles. Phosphorylation of Serine 16 and Threonine 17 in Response to β-Adrenergic Stimulation, J. Biol. Chem. 264, 11468-11474.
3. Mundina-Weilenmann, C., Vittone, L., Ortale, M., de Cingolani, G. C., and Mattiazzi, A. (1996) Immunodetection of Phosphorylation Sites Gives New Insights into the Mechanisms Underlying Phospholamban Phosphorylation in the Intact Heart, J. Biol. Chem. 271, 33561-33567.
4. Chu, G., Lester, J. W., Young, K. B., Luo, W., Zhai, J., and Kranias, E. G. (2000) A Single Site (Ser16) Phosphorylation in Phospholamban is Sufficient in Mediating its Maximal Cardiac Responses to β-Agonists, J. Biol. Chem. 275, 38938-38943.
5. Wawrzynow, A., Theibert, J. L., Murphy, C., Jona, I., Martonosi, A., and Collins, J. H. (1992) Sarcolipin, the "Proteolipid" of Skeletal Muscle Sarcoplasmic Reticulum, is a Unique, Amphipathic, 31-Residue Peptide, Arch. Biochem. Biophys. 298, 620-623.
6. Odermatt, A., Taschner, P. E., Scherer, S. W., Beatty, B., Khanna, V. K., Cornblath, D. R., Chaudhry, V., Yee, W. C., Schrank, B., Karpati, G., Breuning, M. H., Knoers, N., and MacLennan, D. H. (1997) Characterization of the Gene Encoding Human Sarcolipin (SLN), a Proteolipid Associated with SERCA1: Absence of Structural Mutations in Five Patients with Brody Disease, Genomics 45, 541-553.
7. Gayan-Ramirez, G., Vanzeir, L., Wuytack, F., and Decramer, M. (2000) Corticosteroids Decrease mRNA Levels of SERCA Pumps, Whereas they Increase Sarcolipin mRNA in the Rat Diaphragm, J. Physiol. 524 (Part 2), 387-397.
8. Minamisawa, S., Wang, Y., Chen, J., Ishikawa, Y., Chien, K. R., and Matsuoka, R. (2003) Atrial Chamber-Specific Expression of Sarcolipin is Regulated during Development and Hypertrophic Remodeling, J. Biol. Chem. 278, 9570-9575.
9. Babu, G. J., Bhupathy, P., Carnes, C. A., Billman, G. E., and Periasamy, M. (2007) Differential Expression of Sarcolipin Protein during Muscle Development and Cardiac Pathophysiology, J. Mol. Cell. Cardiol. 43, 215-222.
10. Maclennan, D. H., Yip, C. C., Iles, and Seeman, P. (1972) Isolation of Sarcoplasmic Reticulum Proteins, Cold Spring Harbor Symp. Quant. Biol. 37, 469-478.
11. 2+-ATPase, J. Biol. Chem. 273, 12360-12369.
12. Uemura, N., Ohkusa, T., Hamano, K., Nakagome, M., Hori, H., Shimizu, M., Matsuzaki, M., Mochizuki, S., Minamisawa, S., and Ishikawa, Y. (2004) Down-Regulation of Sarcolipin mRNA Expression in Chronic Atrial Fibrillation, Eur. J. Clin. Invest. 34, 723-730.
13. Gramolini, A. O., Trivieri, M. G., Oudit, G. Y., Kislinger, T., Li, W., Patel, M. M., Emili, A., Kranias, E. G., Backx, P. H., and Maclennan, D. H. (2006) Cardiac-Specific Overexpression of Sarcolipin in Phospholamban Null Mice Impairs Myocyte Function that is Restored by Phosphorylation, Proc. Natl. Acad. Sci. U.S.A. 103, 2446-2451.
14. Toyoshima, C., Nakasako, M., Nomura, H., and Ogawa, H. (2000) Crystal Structure of the Calcium Pump of Sarcoplasmic Reticulum at 2.6 Å Resolution, Nature 405, 647-655.
15. Toyoshima, C., and Nomura, H. (2002) Structural Changes in the Calcium Pump Accompanying the Dissociation of Calcium, Nature 418, 605-611.
16. Toyoshima, C., and Mizutani, T. (2004) Crystal Structure of the Calcium Pump with a Bound ATP Analogue, Nature 430, 529-535.
17. Toyoshima, C., Nomura, H., and Tsuda, T. (2004) Lumenal Gating Mechanism Revealed in Calcium Pump Crystal Structures with Phosphate Analogues, Nature 432, 361-368.
18. Olesen, C., Sorensen, T. L., Nielsen, R. C., Moller, J. V., and Nissen, P. (2004) Dephosphorylation of the Calcium Pump Coupled to Counterion Occlusion, Science 306, 2251-2255.
19. Sorensen, T. L., Moller, J. V., and Nissen, P. (2004) Phosphoryl Transfer and Calcium Ion Occlusion in the Calcium Pump, Science 304, 1672-1675.
20. 2+-ATPase by Cryoelectron Microscopy, Biophys. J. 81, 884-894.
21. 2+ ATPase, Proc. Natl. Acad. Sci. U.S.A. 100, 467-472.
22. 2+-ATPase (SERCA) by Binding to Transmembrane Helices Alone or in Association with Phospholamban, Proc. Natl. Acad. Sci. U.S.A. 100, 5040-5045.
23. Hutter, M. C., Krebs, J., Meiler, J., Griesinger, C., Carafoli, E., and Helms, V. (2002) A Structural Model of the Complex Formed by Phospholamban and the Calcium Pump of Sarcoplasmic Reticulum obtained by Molecular Mechanics, ChemBioChem 3, 1200-1208.
24. Buck, B., Zamoon, J., Kirby, T. L., DeSilva, T. M., Karim, C., Thomas, D., and Veglia, G. (2003) Overexpression, Purification, and Characterization of Recombinant Ca-ATPase Regulators for High-Resolution Solution and Solid-State NMR Studies, Protein Expression Purif. 30, 253-261.
25. Buffy, J. J., Buck-Koehntop, B. A., Porcelli, F., Traaseth, N. J., Thomas, D. D., and Veglia, G. (2006) Defining the Intramembrane Binding Mechanism of Sarcolipin to Calcium ATPase using Solution NMR Spectroscopy, J. Mol. Biol. 358, 420-429.
26. 2+-ATPase Complex, J. Mol. Biol. 358, 1041-1050.
27. Kimura, Y., Kurzydlowski, K., Tada, M., and MacLennan, D. H. (1997) Phospholamban Inhibitory Function is Activated by Depolymerization, J. Biol. Chem. 272, 15061-15064.
28. 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.
29. Zamoon, J., Mascioni, A., Thomas, D. D., and Veglia, G. (2003) NMR Solution Structure and Topological Orientation of Monomeric Phospholamban in Dodecylphosphocholine Micelles, Biophys. J. 85, 2589-2598.
30. 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.
31. Lambeth, S., Schmid, H., Muenchbach, M., Vorherr, T., Krebs, J., Carafoli, E., and Griesinger, C. (2000) NMR Solution Structure of Phospholamban, Helv. Chim. Acta 83, 2141-2152.
32. 15N Heteronuclear NMR Spectroscopy shows Four Dynamic Domains for Phospholamban Reconstituted in Dodecylphosphocholine Micelles, Biophys. J. 87, 1205-1214.
33. Metcalfe, E. E., Traaseth, N. J., and Veglia, G. (2005) Serine 16 Phosphorylation Induces an Order-to-Disorder Transition in Monomeric Phospholamban, Biochemistry 44, 4386-4396.
34. 2+ Uptake as a Primary Cause of Heart Failure, Cardiovasc. Res. 56, 248-259.
35. Oxenoid, K., and Chou, J. J. (2005) The Structure of Phospholamban Pentamer Reveals a Channel-Like Architecture in Membranes, Proc. Natl. Acad. Sci. U.S.A. 102, 10870-10875.
36. Traaseth, N. T., Verardi, R., Torgersen, K. D., Karim, C. B., Thomas, D. D., and Veglia, G. (2007) Spectroscopic Validation of the Pentameric Structure of Phospholamban, Proc. Natl. Acad. Sci. U.S.A. 104, 14676-14681.
37. Mascioni, A., Karim, C., Barany, G., Thomas, D. D., and Veglia, G. (2002) Structure and Orientation of Sarcolipin in Lipid Environments, Biochemistry 41, 475-482.
38. Opella, S. J. (1997) NMR and Membrane Proteins, Nat. Struct. Biol. 4 (Suppl.), 845-848.
39. Baldus, M. (2006) Molecular Interactions Investigated by Multi-Dimensional Solid-State NMR, Curr. Opin. Struct. Biol. 16, 618-623.
40. 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.
41. Wu, C. H., Ramamoorthy, A., and Opella, S. J. (1994) High-Resolution Heteronuclear Dipolar Solid-State NMR Spectroscopy, J. Magn. Reson. 109, 270-272.
42. Traaseth, N. J., Buffy, J. J., Zamoon, J., and Veglia, G. (2006) Structural Dynamics and Topology of Phospholamban in Oriented Lipid Bilayers using Multidimensional Solid-State NMR, Biochemistry 45, 13827-13834.
43. 19F-Labeled Tryptophan in Gramicidin A in Oriented Membranes, Biophys. J. 83, 3336-3350.
44. 15N Solid-State NMR Spectroscopy, J. Am. Chem. Soc. 126, 16676-16683.
45. Park, S. H., Mrse, A. A., Nevzorov, A. A., De Angelis, A. A., and Opella, S. J. (2006) Rotational Diffusion of Membrane Proteins in Aligned Phospholipid Bilayers by Solid-State NMR Spectroscopy, J. Magn. Reson. 178, 162-165.
46. Andronesi, O. C., Becker, S., Seidel, K., Heise, H., Young, H. S., and Baldus, M. (2005) Determination of Membrane Protein Structure and Dynamics by Magic-Angle-Spinning Solid-State NMR Spectroscopy, J. Am. Chem. Soc. 127, 12965-12974.
47. Hughes, E., Clayton, J. C., and Middleton, D. A. (2005) Probing the Oligomeric State of Phospholamban Variants in Phospholipid Bilayers from Solid-State NMR Measurements of Rotational Diffusion Rates, Biochemistry 44, 4055-4066.
48. 2H, and REDOR Solid-State NMR Spectroscopy, Biochim. Biophys. Acta 1758, 772-780.
49. Buffy, J. J., Traaseth, N. J., Mascioni, A., Gor'kov, P. L., Chekmenev, E. Y., Brey, W. W., and Veglia, G. (2006) Two-Dimensional Solid-State NMR Reveals Two Topologies of Sarcolipin in Oriented Lipid Bilayers, Biochemistry 45, 10939-10946.
50. 2+-ATPase and the Pentameric Form of Phospholamban in Two-Dimensional Co-Crystals, Biophys. J. 90, 4213-4223.
51. Tatulian, S. A., Jones, L. R., Reddy, L. G., Stokes, D. L., and Tamm, L. K. (1995) Secondary Structure and Orientation of Phospholamban Reconstituted in Supported Bilayers from Polarized Attenuated Total Reflection FTIR Spectroscopy, Biochemistry 34, 4448-4456.
52. Arkin, I. T., Rothman, M., Ludlam, C. F., Aimoto, S., Engelman, D. M., Rothschild, K. J., and Smith, S. O. (1995) Structural Model of the Phospholamban Ion Channel Complex in Phospholipid Membranes, J. Mol. Biol. 248, 824-834.
53. 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.
54. Robia, S. L., Flohr, N. C., and Thomas, D. D. (2005) Phospholamban Pentamer Quaternary Conformation Determined by inGel Fluorescence Anisotropy, Biochemistry 44, 4302-4311.
55. Simmerman, H. K., 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.
56. 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.
57. Zamoon, J., Nitu, F., Karim, C., Thomas, D. D., and 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. U.S.A. 102, 4747-4752.
58. 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.
59. Wagner, G., Pardi, A., and Wuthrich, K. (1983) Hydrogen Bond Length and Proton NMR Chemical Shifts in Proteins, J. Am. Chem. Soc. 105, 5948-5949.
60. 2+-ATPase Isoform of Cardiac Sarcoplasmic Reticulum, J. Biol. Chem. 273, 14238-14241.
61. 2+ ATPase (SERCA) Catalytic Cycle, Biochemistry 45, 13769-13778.
62. Ha, K. N., Traaseth, N. J., Verardi, R., Zamoon, J., Cembran, A., Karim, C. B., Thomas, D. D., Veglia, G. (2007) Controlling the Inhibition of the Sarcoplasmic Ca2+-ATPase by Tuning Phospholamban Structural Dynamics, J. Biol. Chem. E-pub Sep. 30, 2007.