The structural basis for phospholamban inhibition of the calcium pump in sarcoplasmic reticulum

Journal of Biological Chemistry

Volumn 288, Issue 42, 2013, Pages 30181-30191

  Akin, Brandy L ^a   Hurley, Thomas D ^a   Chen, Zhenhui ^a   Jones, Larry R ^a  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARDIAC CONTRACTILITY; KEY REGULATORS; PHOSPHOLAMBAN; SARCOPLASMIC RETICULUM; STRUCTURAL BASIS;

BIOCHEMISTRY; BIOLOGY;

CALCIUM;

CALCIUM ION; DIVALENT CATION; PHOSPHOLAMBAN; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; BINDING SITE; CALCIUM BINDING; COMPLEX FORMATION; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME CONFORMATION; ENZYME INHIBITION; HEART MUSCLE CONTRACTILITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN STRUCTURE; SARCOPLASMIC RETICULUM;

CALCIUM ATPASE; CALCIUM TRANSPORT; CRYSTAL STRUCTURE; PHOSPHOLAMBAN; PROTEIN CROSS-LINKING; PROTEIN CRYSTALLIZATION; SARCOLIPIN; SARCOPLASMIC RETICULUM (SR); SERCA;

ANIMALS; BINDING SITES; CALCIUM; CALCIUM-BINDING PROTEINS; DOGS; HUMANS; MULTIPROTEIN COMPLEXES; MUSCLE, SKELETAL; MYOCARDIAL CONTRACTION; MYOCARDIUM; PROTEIN STRUCTURE, QUATERNARY; RABBITS; SARCOPLASMIC RETICULUM; SARCOPLASMIC RETICULUM CALCIUM-TRANSPORTING ATPASES; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84885968069     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.501585     Document Type: Article

References (48)

1. 2+-ATPase activity in guinea pig ventricles. J. Biol. Chem. 258, 464-471
2. Simmerman, H. K., and Jones, L. R. (1998) Phospholamban. Protein structure, mechanism of action, and role in cardiac function. Physiol. Rev. 78, 921-947
3. Young, H. S., and Stokes, D. L. (2004) The mechanics of calcium transport. J. Membr. Biol. 198, 55-63
4. 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 -adrenergic stimulation. J. Biol. Chem. 264, 11468-11474
5. 2+ pump revealed by intermolecular thiol cross-linking. J. Biol. Chem. 277, 28319-28329
6. 2+ ATPase. Proc. Natl. Acad. Sci. U.S.A. 100, 467-472
7. 2+ pump revealed with use of heterobifunctional cross-linking agents. J. Biol. Chem. 278, 48348-48356
8. 2+ pump of cardiac sarcoplasmic reticulum. J. Biol. Chem. 280, 10530-10539
9. 2+ pump of cardiac sarcoplasmic reticulum to probe spatial and functional interactions within the transmembrane domain. J. Biol. Chem. 281, 14163-14172
10. 2+ for binding to SERCA2a by stabilizing a unique nucleotide-dependent conformational state. J. Biol. Chem. 285, 28540-28552
11. Lytton, J., Westlin, M., and Hanley, M. R. (1991) Thapsigargin inhibits the sarcoplasmic or endoplasmic reticulum Ca-ATPase family of calcium pumps. J. Biol. Chem. 266, 17067-17071
12. 2+ transport ATPases by thapsigargin. J. Biol. Chem. 267, 12606-12613
13. 2+)- ATPase. J. Biol. Chem. 253, 1643-1653
14. 2+-ATPase. J. Biol. Chem. 270, 9390-9397
15. 2+-ATPase. J. Biotechnol. 124, 704-716
16. 2+-ATPase 2a (SERCA2a) protein binding interactions in human cardiac sarcoplasmic reticulum vesicles using chemical cross-linking. J. Biol. Chem. 287, 7582-7593
17. Otwinowski, Z., and Minor, W. (1997) Processing of x-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326
18. Jensen, A. M., Sørensen, T. L., Olesen, C., Møller, J. V., and Nissen, P. (2006) Modulatory and catalytic modes of ATP binding by the calcium pump. EMBO J. 25, 2305-2314
19. McCoy, A. J., Grosse-Kunstleve, R. W., Adams, P. D., Winn, M. D., Storoni, L. C., and Read, R. J. (2007) Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674
20. Emsley, P., Lohkamp, B., Scott, W. G., and Cowtan, K. (2010) Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486-501
21. Murshudov, G. N., Vagin, A. A., and Dodson, E. J. (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53, 240-255
22. Painter, J., and Merritt, E. A. (2006) Optimal description of a protein structure in terms of multiple groups undergoing TLS motion. Acta Crystallogr. D Biol. Crystallogr. 62, 439-450
23. 2+-ATPase by protein kinase A and by anti-phospholamban monoclonal antibody 2D12. J. Biol. Chem. 282, 20968-20976
24. Toyoshima, C., and Nomura, H. (2002) Structural changes in the calcium pump accompanying the dissociation of calcium. Nature 418, 605-611
25. 2+-ATPase (SERCA1a). Biochem. Biophys. Res. Commun. 391, 1067-1069
26. 2+-ATPase of sarcoplasmic reticulum. Arch. Biochem. Biophys. 476, 3-11
27. Gorski, P. A., Glaves, J. P., Vangheluwe, P., and Young, H. S. (2013) Sarco- (endo)plasmic reticulum calcium ATPase (SERCA) inhibition by sarcolipin is encoded in its luminal tail. J. Biol. Chem. 288, 8456-8467
28. Jones, L. R., Simmerman, H. K., Wilson, W. W., Gurd, F. R., and Wegener, A. D. (1985) Purification and characterization of phospholamban from canine cardiac sarcoplasmic reticulum. J. Biol. Chem. 260, 7721-7730
29. Mueller, B., Karim, C. B., Negrashov, I. V., Kutchai, H., and Thomas, D. D. (2004) Direct detection of phospholamban and sarcoplasmic reticulum Ca-ATPase interaction in membranes using florescence resonance energy transfer. Biochemistry 43, 8754-8765
30. Li, J., Bigelow, D. J., and Squier, T. C. (2004) Conformational changes within the cytoplasmic portion of phospholamban upon release of Ca- ATPase inhibition. Biochemistry 43, 3870-3879
31. Bidwell, P., Blackwell, D. J., Hou, Z., Zima, A. V., and Robia, S. L. (2011) Phospholamban binds with differential affinity to calcium pump conformers. J. Biol. Chem. 286, 35044-35050
32. Kimura, Y., Kurzydlowski, K., Tada, M., and MacLennan, D. H. (1997) Phospholamban inhibitory function is activated by depolymerization. J. Biol. Chem. 272, 15061-15064
33. 2+-ATPase forms a functional interaction site with phospholamban. Evidence for physical interactions at other sites. J. Biol. Chem. 274, 32855-32862
34. 2+-ATPase of sarcoplasmic reticulum. J. Biol. Chem. 267, 2767-2774
35. 2+-ATPase isoform of cardiac sarcoplasmic reticulum. J. Biol. Chem. 273, 14238-14241
36. 2+ pump and phospholamban in Spodoptera frugiperda (Sf21) cells reveals new insights on ATPase regulation. J. Biol. Chem. 272, 15872-15880
37. 2+ pump of cardiac sarcoplasmic reticulum. J. Biol. Chem. 275, 41487-41494
38. 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
39. Simmerman, H. K., Collins, J. H., Theibert, J. L., Wegener, A. D., and Jones, L. R. (1986) Sequence analysis of phospholamban. Identification of phosphorylation sites and two major structural domains. J. Biol. Chem. 261, 13333-13341
40. 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
41. 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
42. 2+-ATPase. J. Biol. Chem. 288, 10759-10765
43. +- bound E1 state. Nature 495, 260-264
44. Winther, A. M., Bublitz, M., Karlsen, J. L., Møller, J. V., Hansen, J. B., Nissen, P., and Buch-Pedersen, M. J. (2013) The sarcolipin-bound calcium pump stabilizes calcium sites exposed to the cytoplasm. Nature 495, 265-269
45. 2+ ATPase (SERCA) is distinct from phospholamban protein, and only sarcolipin can promote uncoupling of the SERCA pump. J. Biol. Chem. 288, 6881-6889
46. 2+- ATPase. J. Biol. Chem. 273, 12360-12369
47. Lytton, J., Westlin, M., Burk, S. E., Shull, G. E., and MacLennan, D. H. (1992) Functional comparisons between isoforms of the sarcoplasmic or endoplasmic reticulum family of calcium pumps. J. Biol. Chem. 267, 14483-14489
48. 2+ pump of sarcoplasmic reticulum. Nature 342, 90-92