Computational design of a water-soluble analog of phospholamban

Protein Science

Volumn 12, Issue 2, 2003, Pages 337-348

  Slovic, Avram M ^a   Summa, Christopher M ^a   Lear, James D ^a   Degrado, William F ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Computational methods; Phospholamban; Protein design; Water soluble membrane protein

Indexed keywords

AMINO ACID; ISOPROTEIN; MEMBRANE PROTEIN; MUTANT PROTEIN; PHOSPHOLAMBAN;

AQUEOUS SOLUTION; ARTICLE; CALCULATION; CONFORMATIONAL TRANSITION; ELECTRIC POTENTIAL; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY; PROTEIN STRUCTURE; SOLUBILITY; STRUCTURE ANALYSIS; TECHNIQUE;

ALGORITHMS; AMINO ACID SEQUENCE; CALCIUM-BINDING PROTEINS; CIRCULAR DICHROISM; COMPUTER-AIDED DESIGN; DRUG DESIGN; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; PEPTIDE FRAGMENTS; PHOSPHORYLATION; PROTEIN DENATURATION; PROTEIN ENGINEERING; PROTEIN STRUCTURE, QUATERNARY; SOLUBILITY; THERMODYNAMICS; WATER;

EID: 0037305504     PISSN: 09618368     EISSN: None     Source Type: Journal    
DOI: 10.1110/ps.0226603     Document Type: Article

References (67)

1. Arkin, I.T., Adams, P.D., MacKenzie, K.R., Lemmon, M.A., Brünger, A.T., and Engelman, D.M. 1994. Structural organization of the pentameric transmembrane α-helices of phospholamban, a cardiac ion channel. EMBO J. 13: 4757-4764.
2. 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.
3. Boice, J.A., Dieckmann, G.R., DeGrado, W.F., and Fairman, R. 1996. Thermodynamic analysis of a designed three-stranded coiled coil. Biochemistry 35: 14480-14485.
4. Bowie, J.U. 1997. Helix packing in membrane proteins. J. Mol. Biol., 272: 780-789.
5. 2+ affinity by phospholamban in transgenic hearts overexpressing a non-phosphorylatable form of phospholamban. J. Biol. Chem. 275: 12129-12135.
6. Brooks, I.S., Soneson, K.K., and Hensley, P. 1993. Development and use of a mac based data-analysis package for equilibrium sedimentation data from the analytical ultracentrifuge. Biophys. J. 64: a244.
7. Cantilina, T., Sagara, Y., Inesi, G., and Jones, L.R. 1993. Comparative studies of cardiac and skeletal sarcoplasmic reticulum ATPases: Effect of a phospholambn antibody on enzyme activation. J. Biol. Chem. 268: 17018-17025.
8. Chakrabartty, A., Schellman, J.A., and Baldwin, R.L. 1991. Large differences in the helix propensities of alanine and glycine. Nature 351: 586-588.
9. Chu, G.X., Lester, J.W., Young, K.B., Luo, W.S., Zhai, J., and Kranias, E.G. 2000. A single site (Ser(16)) phosphorylation in phospholamban is sufficient in mediating its maximal cardiac responses to β-agonists. J. Biol. Chem. 275: 38938-38943.
10. 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.
11. 2+ pump of cardiac sarcoplasmic reticulum. J. Biol. Chem. 275: 41487-41494.
12. Crick, F. 1953. The packing of α-helices: Simple coiled-coils. Acta Crystallogr. 6: 689-697.
13. Dieckmann, G.R. and DeGrado, W.F. 1997. Modeling transmembrane helical oligomers. Curr. Opin. Struct. Biol. 7: 486-494.
14. Eilers, M., Patel, A.B., Liu, W., and Smith, S.O. 2002. Comparison of helix interactions in membrane and soluble α-bundle proteins. Biophys. J. 82: 2702-2736.
15. Fauchere, J.-L. and Pliska, V. 1983. Hydrophobic parameters p of amino acid side chains from the partitioning of N-aceyl-amino acid amides. Eur. J. Med. Chem. 18: 369-375.
16. Frank, S., Kammerer, R.A., Hellstern, S., Pegoraro, S., Stetefeld, J., Lustig, A., Moroder, L., and Engel, J. 2000. Toward a high-resolution structure of phospholamban: Design of soluble transmembrane domain mutants. Biochemistry 39: 6825-6831.
17. Fujii, J., Kadoma, M., Tada, M., Toda, H., and Sakiyama, F. 1986. Characterization of structural unit of phospholamban by amino acid sequencing and electrophoretic analysis. Biochem. Biophys. Res. Commun. 138: 1044-1050.
18. 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.
19. Harbury, P.B., Zheng, T., Kim, P.S., and Alber, T. 1993. A switch between two-, three-, and four-stranded coiled coils in GCN4 leucine zipper mutants. Science 262: 1401-1407.
20. Harrer, J.M. and Kranias, E.G. 1994. Characterization of the molecular form of cardiac phospholamban. Mol. Cell. Biochem. 140: 185-193.
21. Hill, R.B. and DeGrado, W.F. 1998. Solution structure of α2D, a nativelike de novo designed protein. J. Am. Chem. Soc. 120: 1138-1145.
22. Hill, R.B. and DeGrado, W.F. 2000. A polar, solvent-exposed residue can be essential for native protein structure. Struct. Fold. Design 8: 471-479.
23. Hill, R.B., Hong, J-K., and DeGrado, W.F. 1999. Hydrogen bonding cluster can specify the unique conformation of a protein. J. Am. Chem. Soc. 122: 746-747.
24. Hubbard, J.A., Maclachlan, L.K., Meenan, E., Salter, C.J., Reid, D.G., Lahouratate, P., Humphries, J., Stevens, N., Bell, D., Neville, W.A., et al. 1994. Conformation of the cytoplasmic domain of phospholamban by NMR and CD. J. Mol. Membr. Biol. 11: 263-269.
25. 2+ transport as studied by reconstitution of cardiac sarcoplasmic reticulum. J. Biol. Chem. 261: 1794-1800.
26. 2+ transport ATPase of cardiac sarcoplasmic-reticulum. J. Biol. Chem. 268: 11486-11488.
27. Jones, L.R., Simmerman, H.K.B., Wilson, W.W., Gurd, F.R.N., and Wegener, A.D. 1985. Purification and characterization of phospholamban from canine cardiac sarcoplasmic reticulum. J. Biol. Chem. 260: 7721-7730.
28. Kharakoz, D.P. 1997. Partial volumes and compressibilities of extended polypeptide chains in aqueous solution: Additivity scheme and implication of protein unfolding at normal and high pressure. Biochemistry 36: 10276-10285.
29. Kimura, Y., Kurzydlowski, K., Tada, M., and MacLennan, D.H. 1997. Phospholamban inhibitory function is activated by depolymerization. J. Biol. Chem. 272: 15061-15064.
30. Kirchberger, M.A., Borchman, D., and Ckasinathan, C. 1986. Proteolytic activation of the canine cardiac sarcoplasmic reticulum calcium pump. Biochemistry 25: 5484-5492.
31. 2+-selective channels in lipid bilayers. J. Biol. Chem. 263: 18364-18368.
32. Krylov, D., Mikhailenko, I., and Vinson, C. 1994. A thermodynamic scale for leucine zipper stability and dimerization specificity: e and g interhelical interactions. EMBO J. 13: 2849-2861.
33. Laue, T., Shaw, B.D., Ridgeway, T.M., and Pelletier, S.L. 1992. Computeraided interpretation of analytical sedimentation data for proteins. The Royal Society of Chemistry, Cambridge, UK.
34. Lee, C. and Subbiah, S. 1991. Prediction of protein side-chain conformation by packing optimization. J. Mol. Biol. 217: 373-388.
35. Li, H., Cocco, M.J., Steitz, T.A., and Engelman, D.E. 2001. Conversion of phospholamban into a soluble pentameric helical bundle. Biochemistry 40: 6636-6645.
36. Li, M., Cornea, R.L., Autry, J.M., Jones, L.R., and Thomas, D.D. 1998. Phosphorylation-induced structural change in phospholamban and its mutants, detected by intrinsic fluorescence. Biochemistry 37: 7869-7877.
37. Louis, C.F., Maffitt, M., and Jarvis, B. 1982. Factors that modify the molecularsize of phospholamban, the 23,000-Dalton cardiac sarcoplasmic-reticulum phosphoprotein. J. Biol. Chem. 257: 5182-5186.
38. Lumb, K.J. and Kim, P.S. 1998. A buried polar interaction imparts structural uniqueness in a designed heterodimeric coiled coil. Biochemistry 37: 10342.
39. Malashkevich, V.N., Kammerer, R.A., Efimov, V.P., Schulthess, T., and Engel, J. 1996. The crystal structure of a five-stranded coiled coil in COMP: A prototype ion channel? Science 274: 761-765.
40. Mortishiresmith, R.J., Pitzenberger, S.M., Burke, C.J., Middaugh, C.R., Garsky, V.M., and Johnson, R.G. 1995. Solution structure of the cytoplasmic domain of phospholamban-phosphorylation leads to a local perturbation in secondary structure. Biochemistry 34: 7603-7613.
41. Muñoz, V. and Serrano, L. 1994. Elucidating the folding problem of helical peptides using empirical parameters. Nature 1: 399-409.
42. -. 1995. Elucidating the folding problem of helical peptides using empirical parameters. II. Helix macrodipole effects and rational modification of the helical content of natural peptides. J. Mol. Biol. 245: 275-296.
43. North, B., Summa, C.M., Ghirlanda, G., and DeGrado, W.F. 2001. D(n)-symmetrical tertiary templates for the design of tubular proteins. J. Mol. Biol. 311: 1081-1090.
44. O'Neil, K.T. and DeGrado, W.F. 1990. A thermodynamic scale for the helixforming tendencies of the commonly occurring amino acids. Science 250: 646-651.
45. Plank, B., Pifl, C., Hellmann, G., Wyskovsky, W., Hoffmann, R., and Suko, J. 1983. Correlation between calmodulin-dependent increase in the rate of calcium transport and calmodulin-dependent phosphorylation of cardiac sarcoplasmic reticulum. Eur. J. Biochem. 136: 215-221.
46. Quirk, P.G., Patchell, V.B., Colyer, J., Drago, G.A., and Gao, Y. 1996. Conformational effects of serine phosphorylation in phospholamban peptides. Eur. J. Biochem. 263: 85-91.
47. 2+-ATPase. J. Biol. Chem. 270: 9390-9397.
48. Rees, D.C., DeAntonio, L., and Eisenberg, D. 1989. Hydrophobic organization of membrane proteins. Science 245: 510-513.
49. Sabine, F., Kammerer, R.A., Hellstern, S., Pegoraro, S., Stetefeld, J., Lustig, A., Moroder, L., and Engel, J. 2000. Toward a high-resolution structure of phospholamban: Design of soluble transmembrane domain mutants. Biochemistry 39: 6825-6831.
50. 2+ uptake in mammalian ventricular myocytes. Am. J. Physiol. 261: H1344-H1349.
51. Simmerman, H.K., Lovelace, D.E., and Jones, L.R. 1989. Secondary structure of detergent-solubilized phospholamban, a phosphorylatable, oligomeric protein of cardiac sarcoplasmic reticulum. Biochim. Biophys. Acta. 997: 322-329.
52. Simmerman, H.K.B., Collins, J.H., Theibert, J.L., Wegener, A.D., and Jones, L.R. 1986. Sequence-analysis of phospholamban - Identification of phosphorylation sites and 2 major structural domains. J. Biol. Chem. 261: 3333-3341.
53. Simmerman, H.K.B., 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.
54. Stevens, T.J. and Arkin, I.T. 2000. Do more complex organisms have a greater proportion of membrane proteins in their genomes? Proteins 39: 417-420.
55. Summa, C.M., Rosenblatt, M.M., Hong, J.-K., Lear, J.D., and DeGrado, W.F. 2002. Computational de novo design, and characterization of an A2B2 diiron protein. J. Mol. Biol. (in press).
56. 2+ pump and blocking of phospholamban phosphorylation and dephosphorylation by a phospholamban monoclonal antibody. J. Biol. Chem. 261: 7018-7023.
57. Tada, M. and Inui, M. 1983. Regulation of calcium transport by the ATPasephospholamban system. J. Mol. Cell. Cardiol. 15: 565-575.
58. Terzi, E., Poteur, L., and Trifilieff, E. 1992. Evidence for a phosphorylation-indiced conformational change in phospholamban cytoplasmic domain by CD analysis. FEBS Lett. 309: 413-416.
59. Torres, J., Adams, P.D., and Arkin, I.T. 2000. Use of a new label, 13C-18O, in the determination of a structural model of phospholamban in a lipid bilayer. Spatial restraints resolve the ambiguity arising from interpretations of mutagenesis data. J. Mol. Biol. 300: 677-685.
60. 2+-ATPase of cardiac sarcoplasmic-reticulum are critical for functional association with phospholamban. J. Biol. Chem. 269: 22929-22932.
61. Villegas, V., Viguera, A.R., Aviles, F.X., and Serrano, L. 1996. Stabilization of proteins by rational design of α-helix stability using helix-coil transition theory. Fold. Design 1: 29-34.
62. Vorherr, T., Chiesi, M., Schwaller, R., and Carafoli, E. 1992. Regulation of the calcium ion pump of sarcoplasmic reticulum: Reversible inhibition by phospholamban and by the calmodulin binding domain of the plasma membrane calcium ion pump. Biochemistry 31: 371-376.
63. Watanabe, Y., Kijima, Y., Kadoma, M., Tada, M., and Tagaki, T. 1991. Molecular weight determination of phospholamban oligomer in the presence of sodium dodecyl sulfate: Application of low-angle laserlight scattering photometry. J. Biochem. 110: 40-45.
64. 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.
65. Wegener, A.D., Simmerman, H.K., Liepnieks, J., and Jones, L.R. 1986. Proteolytic cleavage of phospholamban purified from canine cardiac sarcoplasmic reticulum vesicles. Generation of a low resolution model of phospholamban structure. J. Biol. Chem. 261: 5154-5159.
66. Wegener, A.D., Simmerman, H.B.K., Liepnieks, J., and Jones, L.R. 1989. Phospholamban phosphorylation in intact ventricles: Phosphorylation of serine 16 and threonine 17 in response to b-adrenergic stimulation. J. Biol. Chem. 264: 11468-11474.
67. Zhao, S., Goodsell, D.S., and Olson, A.J. 2001. Analysis of a data set of paired uncomplexed protein structures: New metrics for side-chain flexibility and model evaluation. Proteins 43: 271-279.