Hydrophobic imbalance in the cytoplasmic domain of phospholamban is a determinant for lethal dilated cardiomyopathy

Journal of Biological Chemistry

Volumn 287, Issue 20, 2012, Pages 16521-16529

  Ceholski, Delaine K ^a   Trieber, Catharine A ^a   Young, Howard S ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CARDIOLOGY; HYDROPHOBICITY;

AMINO ACID SUBSTITUTION; CYTOPLASMIC DOMAINS; DILATED CARDIOMYOPATHY; DOMINANT NEGATIVE; LOSS-OF-FUNCTION MUTANTS; MYOCARDIAL CONTRACTILITY; PHOSPHOLAMBAN; WILD TYPES;

CELL PROLIFERATION;

ALANINE; ARGININE; CYSTEINE; LEUCINE; PHOSPHOLAMBAN; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE; THREONINE;

AMINO ACID SUBSTITUTION; ANIMAL TISSUE; ARTICLE; CONGESTIVE CARDIOMYOPATHY; CONTROLLED STUDY; CYTOPLASM; EMBRYO; ENZYME INHIBITION; ENZYME REGULATION; HETEROZYGOSITY; HUMAN; HUMAN CELL; HYDROPHOBICITY; LETHALITY; LOSS OF FUNCTION MUTATION; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; WILD TYPE;

EID: 84860863765     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.360859     Document Type: Article

References (56)

1. Dellefave, L., and McNally, E. M. (2010) The genetics of dilated cardiomyopathy. Curr. Opin. Cardiol. 25, 198-204
2. Kirchberber, M. A., Tada, M., and Katz, A. M. (1975) Phospholamban. A regulatory protein of the cardiac sarcoplasmic reticulum. Recent Adv. Stud. Cardiac Struct. Metab. 5, 103-115
3. 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 (Pubitemid 17006915)
4. MacLennan, D. H., and Kranias, E. G. (2003) Phospholamban. A crucial regulator of cardiac contractility. Nat. Rev. Mol. Cell Biol. 4, 566-577 (Pubitemid 36773408)
5. 2+-ATPase in failing and nonfailing human myocardium. Circ. Res. 75, 434-442
6. Meyer, M., Schillinger, W., Pieske, B., Holubarsch, C., Heilmann, C., Posival, H., Kuwajima, G., Mikoshiba, K., Just, H., and Hasenfuss, G. (1995) Alterations of sarcoplasmic reticulum proteins in failing human dilated cardiomyopathy. Circulation 92, 778-784
7. Minamisawa, S., Sato, Y., Tatsuguchi, Y., Fujino, T., Imamura, S., Uetsuka, Y., Nakazawa, M., and Matsuoka, R. (2003) Mutation of the phospholamban promoter associated with hypertrophic cardiomyopathy. Biochem. Biophys. Res. Commun. 304, 1-4 (Pubitemid 36434184)
8. Haghighi, K., Chen, G., Sato, Y., Fan, G. C., He, S., Kolokathis, F., Pater, L., Paraskevaidis, I., Jones, W. K., Dorn, G. W., 2nd, Kremastinos, D. T., and Kranias, E. G. (2008) A human phospholamban promoter polymorphism in dilated cardiomyopathy alters transcriptional regulation by glucocorticoids. Hum. Mutat. 29, 640-647 (Pubitemid 351614588)
9. Haghighi, K., Kolokathis, F., Pater, L., Lynch, R. A., Asahi, M., Gramolini, A. O., Fan, G. C., Tsiapras, D., Hahn, H. S., Adamopoulos, S., Liggett, S. B., Dorn, G. W., 2nd, MacLennan, D. H., Kremastinos, D. T., and Kranias, E. G. (2003) Human phospholamban null results in lethal dilated cardiomyopathy revealing a critical difference between mouse and human. J. Clin. Invest. 111, 869-876 (Pubitemid 37074962)
10. Landstrom, A. P., Adekola, B. A., Bos, J. M., Ommen, S. R., and Ackerman, M. J. (2011) PLN-encoded phospholamban mutation in a large cohort of hypertrophic cardiomyopathy cases. Summary of the literature and implications for genetic testing. Am. Heart J. 161, 165-171
11. Schmitt, J. P., Kamisago, M., Asahi, M., Li, G. H., Ahmad, F., Mende, U., Kranias, E. G., MacLennan, D. H., Seidman, J. G., and Seidman, C. E. (2003) Dilated cardiomyopathy and heart failure caused by a mutation in phospholamban. Science 299, 1410-1413 (Pubitemid 36254657)
12. DeWitt, M. M., MacLeod, H. M., Soliven, B., and McNally, E. M. (2006) Phospholamban R14 deletion results in late-onset, mild, hereditary dilated cardiomyopathy. J. Am. Coll. Cardiol. 48, 1396-1398 (Pubitemid 44436827)
13. Haghighi, K., Kolokathis, F., Gramolini, A. O., Waggoner, J. R., Pater, L., Lynch, R. A., Fan, G. C., Tsiapras, D., Parekh, R. R., Dorn, G. W., 2nd, MacLennan, D. H., Kremastinos, D. T., and Kranias, E. G. (2006) A mutation in the human phospholamban gene, deleting arginine 14, results in lethal, hereditary cardiomyopathy. Proc. Natl. Acad. Sci. U.S.A. 103, 1388-1393 (Pubitemid 43191175)
14. Posch, M. G., Perrot, A., Geier, C., Boldt, L. H., Schmidt, G., Lehmkuhl, H. B., Hetzer, R., Dietz, R., Gutberlet, M., Haverkamp, W., and Ozcelik, C. (2009) Genetic deletion of arginine 14 in phospholamban causes dilated cardiomyopathy with attenuated electrocardiographic R amplitudes. Heart Rhythm 6, 480-486
15. Medeiros, A., Biagi, D. G., Sobreira, T. J., de Oliveira, P. S., Negrão, C. E., Mansur, A. J., Krieger, J. E., Brum, P. C., and Pereira, A. C. (2011) Mutations in the human phospholamban gene in patients with heart failure. Am. Heart J. 162, 1088-1095.e1
16. Rapti, K., Chaanine, A. H., and Hajjar, R. J. (2011) Targeted gene therapy for the treatment of heart failure. Can. J. Cardiol. 27, 265-283
17. 2+-ATPase regulation and phosphorylation by protein kinase A. Proc. Natl. Acad. Sci. U.S.A. 108, 2735-2740
18. 2+-ATPase regulatory proteins for high-resolution structural studies. Protein Expr. Purif. 40, 118-125
19. Trieber, C. A., Douglas, J. L., Afara, M., and Young, H. S. (2005) The effects of mutation on the regulatory properties of phospholamban in co-reconstituted membranes. Biochemistry 44, 3289-3297 (Pubitemid 40321999)
20. Eletr, S., and Inesi, G. (1972) Phospholipid orientation in sarcoplasmic reticulum membranes. Spin-label ESR and proton NMR studies. Biochim. Biophys. Acta 282, 174-179
21. Stokes, D. L., and Green, N. M. (1990) Three-dimensional crystals of Ca- ATPase from sarcoplasmic reticulum. Symmetry and molecular packing. Biophys. J. 57, 1-14 (Pubitemid 20033741)
22. 2+-ATPase by cryoelectron microscopy. Biophys. J. 81, 884-894
23. 2+/calmodulin- dependent protein kinase. J. Biol. Chem. 271, 14964-14970
24. Ferrington, D. A., Yao, Q., Squier, T. C., and Bigelow, D. J. (2002) Comparable levels of Ca-ATPase inhibition by phospholamban in slow-twitch skeletal and cardiac sarcoplasmic reticulum. Biochemistry 41, 13289 -13296
25. Negash, S., Chen, L. T., Bigelow, D. J., and Squier, T. C. (1996) Phosphorylation of phospholamban by cAMP-dependent protein Kinase enhances interactions between Ca-ATPase polypeptide chains in cardiac sarcoplasmic reticulum membranes. Biochemistry 35, 11247-11259 (Pubitemid 26299297)
26. Warren, G. B., Toon, P. A., Birdsall, N. J., Lee, A. G., and Metcalfe, J. C. (1974) Reconstitution of a calcium pump using defined membrane components. Proc. Natl. Acad. Sci. U.S.A. 71, 622-626
27. Inesi, G., Kurzmack, M., and Lewis, D. (1988) Kinetic and equilibrium characterization of an energy-transducing enzyme and its partial reactions. Methods Enzymol. 157, 154-190 (Pubitemid 19020272)
28. Cantilina, T., Sagara, Y., Inesi, G., and Jones, L. R. (1993) Comparative studies of cardiac and skeletal sarcoplasmic reticulum ATPases. Effect of phospholamban antibody on enzyme activation. J. Biol. Chem. 268, 17018-17025 (Pubitemid 23236927)
29. Trieber, C. A., Afara, M., and Young, H. S. (2009) Effects of phospholamban transmembrane mutants on the calcium affinity, maximal activity, and cooperativity of the sarcoplasmic reticulum calcium pump. Biochemistry 48, 9287-9296
30. Toyofuku, T., Kurzydlowski, K., Tada, M., and MacLennan, D. H. (1994) Amino acids Glu-2 to Ile-18 in the cytoplasmic domain of phospholamban are essential for functional association with the Ca-ATPase of sarcoplasmic reticulum. J. Biol. Chem. 269, 3088-3094
31. Hou, Z., and Robia, S. L. (2010) Relative affinity of calcium pump isoforms for phospholamban quantified by fluorescence resonance energy transfer. J. Mol. Biol. 402, 210-216
32. Reddy, L. G., Autry, J. M., Jones, L. R., and Thomas, D. D. (1999) Coreconstitution of phospholamban mutants with the Ca-ATPase reveals dependence of inhibitory function on phospholamban structure. J. Biol. Chem. 274, 7649-7655
33. 2+ ATPase. Proc. Natl. Acad. Sci. U.S.A. 100, 467-472
34. 2+-ATPase and the pentameric form of phospholamban in two-dimensional co-crystals. Biophys. J. 90, 4213- 4223
35. 2+-ATPase/phospholamban complex. Biochemistry 50, 10367-10374
36. Glaves, J. P., Trieber, C. A., Ceholski, D. K., Stokes, D. L., and Young, H. S. (2011) Phosphorylation and mutation of phospholamban alter physical interactions with the sarcoplasmic reticulum calcium pump. J. Mol. Biol. 405, 707-723
37. Reddy, L. G., Jones, L. R., Cala, S. E., O'Brian, J. J., Tatulian, S. A., and Stokes, D. L. (1995) Functional reconstitution of recombinant phospholamban with rabbit skeletal Ca-ATPase. J. Biol. Chem. 270, 9390-9397
38. Louis, C. F., Turnquist, J., and Jarvis, B. (1987) Phospholamban stoichiometry in canine cardiac muscle sarcoplasmic reticulum. Neurochem. Res. 12, 937-941 (Pubitemid 18020296)
39. Colyer, J., and Wang, J. H. (1991) Dependence of cardiac sarcoplasmic reticulum calcium pump activity on the phosphorylation status of phospholamban. J. Biol. Chem. 266, 17486-17493 (Pubitemid 21907964)
40. 2+ affinity by phospholamban in transgenic hearts overexpressing a non-phosphorylatable form of phospholamban. J. Biol. Chem. 275, 12129-12135
41. 2+ uptake in human failing left ventricular myocardium. J. Heart Lung Transplant. 21, 366-373
42. Deleted in proof
43. 2+-dependent ATPase following phosphorylation by cAMP-dependent protein kinase. Biochem. J. 351, 195-205
44. Karim, C. B., Zhang, Z., Howard, E. C., Torgersen, K. D., and Thomas, D. D. (2006) Phosphorylation-dependent conformational switch in spin-labeled phospholamban bound to SERCA. J. Mol. Biol. 358, 1032-1040
45. Traaseth, N. J., Thomas, D. D., and Veglia, G. (2006) Effects of Ser-16 phosphorylation on the allosteric transitions of phospholamban/Ca2+- ATPase complex. J. Mol. Biol. 358, 1041-1050 (Pubitemid 44382448)
46. Kimura, Y., Kurzydlowski, K., Tada, M., and MacLennan, D. H. (1997) Phospholamban inhibitory function is enhanced by depolymerization. J. Biol. Chem. 272, 15061-15064 (Pubitemid 27255517)
47. Grünig, E., Tasman, J. A., Kücherer, H., Franz, W., Kübler, W., and Katus, H. A. (1998) Frequency and phenotypes of familial dilated cardiomyopathy. J. Am. Coll. Cardiol. 31, 186-194 (Pubitemid 28064741)
48. 2+ binding to site I of the cardiac Ca2+ pump is sufficient to dissociate phospholamban. J. Biol. Chem. 285, 3253-3260
49. Akin, B. L., and Jones, L. R. (2012) Characterizing phospholamban to SERCA2a binding interactions in human cardiac sarcoplasmic reticulum vesicles using chemical cross-linking. J. Biol. Chem. 287, 7582-7593
50. 2+ pump of sarcoplasmic reticulum. Nature 342, 90-92
51. 2+-ATPase by protein kinase A and by anti-phospholamban monoclonal antibody 2D12. J. Biol. Chem. 282, 20968-20976
52. Fowler, C., Huggins, J. P., Hall, C., Restall, C. J., and Chapman, D. (1989) The effects of calcium, temperature, and phospholamban phosphorylation on the dynamics of the calcium-stimulated ATPase of canine cardiac sarcoplasmic reticulum. Biochim. Biophys. Acta 980, 348 -356
53. 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
54. Lockamy, E. L., Cornea, R. L., Karim, C. B., and 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
55. 2+ pump of cardiac sarcoplasmic reticulum. J. Biol. Chem. 280, 10530-10539
56. Liu, L. P., and Deber, C. M. (1998) Guidelines for membrane protein engineering derived from de novo designed model peptides. Biopolymers 47, 41-62