Orientation and oligomerization specificity of the Bcr coiled-coil oligomerization domain

Biochemistry

Volumn 44, Issue 49, 2005, Pages 16246-16256

  Taylor, Christina M ^a   Keating, Amy E ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; CELL MEMBRANES; CRYSTAL ORIENTATION; DISEASES; POLYMERIZATION; PROTEINS;

CELLULAR TRANSFORMATION; CYSTEINE; OLIGOMERIZATION;

OLIGOMERS;

BCR ABL PROTEIN; DISULFIDE; IMATINIB; PROTEIN KINASE INHIBITOR;

ACUTE LYMPHOBLASTIC LEUKEMIA; ARTICLE; CELL TRANSFORMATION; CHRONIC MYELOID LEUKEMIA; CIRCULAR DICHROISM; DRUG TARGETING; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; LEUKEMIA; LEUKEMOGENESIS; MALIGNANT TRANSFORMATION; OLIGOMERIZATION; PRIORITY JOURNAL; STOICHIOMETRY; TEMPERATURE; ULTRACENTRIFUGATION;

AMINO ACID SEQUENCE; CIRCULAR DICHROISM; DIMERIZATION; FUSION PROTEINS, BCR-ABL; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, SECONDARY; SEQUENCE ALIGNMENT;

EID: 28944446279     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi051493t     Document Type: Article

References (77)

1. Sawyers, C. L. (1999) Chronic myeloid leukemia, N. Engl. J. Med. 340, 1330-1340.
2. Catovsky, D. (1979) Ph1-positive acute leukaemia and chronic granulocytic leukaemia: one or two diseases? Br. J. Haematol. 42, 493-498.
3. Smith, K. M., Yacobi, R., and Van Etten, R. A. (2003) Autoinhibition of Bcr-Abl through its SH3 domain, Mol. Cell 12, 27-37.
4. Nardi, V., Azam, M., and Daley, G. Q. (2004) Mechanisms and implications of imatinib resistance mutations in BCR-ABL, Curr. Opin. Hematol. 11, 35-43.
5. McWhirter, J. R., Galasso, D. L., and Wang, J. Y. (1993) A coiled-coil oligomerization domain of Bcr is essential for the transforming function of Bcr-Abl oncoproteins, Mol. Cell. Biol. 13, 7587-7595.
6. Beissert, T., Puccetti, E., Bianchini, A., Guller, S., Boehrer, S., Hoelzer, D., Ottmann, O. G., Nervi, C., and Ruthardt, M. (2003) Targeting of the N-terminal coiled coil oligomerization interface of BCR interferes with the transformation potential of BCR-ABL and increases sensitivity to STI571, Blood 102, 2985-2993.
7. Burkhard, P., Stetefeld, J., and Strelkov, S. V. (2001) Coiled coils: a highly versatile protein folding motif, Trends Cell Biol. 11, 82-88.
8. Mason, J. M., and Arndt, K. M. (2004) Coiled coil domains: stability, specificity, and biological implications, ChemBioChem 5, 170-176.
9. O'Shea, E. K., Klemm, J. D., Kim, P. S., and Alber, T. (1991) X-ray structure of the GCN4 leucine zipper, a two-stranded, parallel coiled coil, Science 254, 539-544.
10. Bussiere, D. E., Bastia, D., and White, S. W. (1995) Crystal structure of the replication terminator protein from B. subtilis at 2.6 Å, Cell 80, 651-660.
11. Peterson, C. L. (1994) The SMC family: novel motor proteins for chromosome condensation? Cell 79, 389-392.
12. Saitoh, N., Goldberg, I., and Earnshaw, W. C. (1995) The SMC proteins and the coming of age of the chromosome scaffold hypothesis, BioEssays 17, 759-766.
13. Hirano, T., and Mitchison, T. J. (1994) A heterodimeric coiled-coil protein required for mitotic chromosome condensation in vitro, Cell 79, 449-458.
14. Melby, T. E., Ciampaglio, C. N., Briscoe, G., and Erickson, H. P. (1998) The symmetrical structure of structural maintenance of chromosomes (SMC) and MukB proteins: long, antiparallel coiled coils, folded at a flexible hinge, J. Cell Biol. 142, 1595-1604.
15. Lowe, J., Cordell, S. C., and van den Ent, F. (2001) Crystal structure of the SMC head domain: an ABC ATPase with 900 residues antiparallel coiled-coil inserted, J. Mol Biol. 306, 25-35.
16. Koshiba, T., Detmer, S. A., Kaiser, J. T., Chen, H., McCaffery, J. M., and Chan, D. C. (2004) Structural basis of mitochondrial tethering by mitofusin complexes, Science 305, 858-862.
17. Bonifacino, J. S., and Glick, B. S. (2004) The mechanisms of vesicle budding and fusion, Cell 116, 153-166.
18. Sutton, R. B., Fasshauer, D., Jahn, R., and Brunger, A. T. (1998) Crystal structure of a SNARE complex involved in synaptic exocytosis at 2.4 Å resolution, Nature 395, 347-353.
19. Eckert, D. M., and Kim, P. S. (2001) Mechanisms of viral membrane fusion and its inhibition, Annu. Rev. Biochem. 70,777-810.
20. O'Shea, E. K., Rutkowski, R., and Kim, P. S. (1992) Mechanism of specificity in the Fos-Jun oncoprotein heterodimer, Cell 68, 699-708.
21. O'Shea, E. K., Lumb, K. J., and Kim, P. S. (1993) Peptide ′Velcro*′: design of a heterodimeric coiled coil, Curr. Boil. 3, 658-667.
22. Hendsch, Z. S., Nohaile, M. J., Sauer, R. T., and Tidor, B. (2001) Preferential heterodimer formation via undercompensated electrostatic interactions, J. Am. Chem. Soc. 123, 1264-1265.
23. Ali, M. H., Taylor, C. M., Grigoryan, G., Alien, K. N., Imperiali, B., and Keating, A. E. (2005) Design of a heterospecific, tetrameric, 21-residue miniprotein with mixed alpha/beta structure, Structure 13, 225-234.
24. Nohaile, M. J., Hendsch, Z. S., Tidor, B., and Sauer, R. T. (2001) Altering dimerization specificity by changes in surface electrostatics, Proc. Natl. Acad. Sci. U.S.A. 98, 3109-3114.
25. Lumb, K. J., and Kim, P. S. (1995) A buried polar interaction imparts structural uniqueness in a designed heterodimeric coiled coil, Biochemistry 34, 8642-8648.
26. Gonzalez, L., Jr., Woolfson, D. N., and Alber, T. (1996) Buried polar residues and structural specificity in the GCN4 leucine zipper, Nat. Struct. Biol. 3, 1011-1018.
27. Akey, D. L., Malashkevich, V. N., and Kim, P. (2001) Buried polar residues in coiled-coil interfaces, Biochemistry 40, 6352-6360.
28. Harbury, P. B., Zhang, 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.
29. Efimov, A. V., and Kondratova, M. S. (2003) A comparative analysis of interhelical polar interactions of various alpha-helix packings in proteins, Mol. Biol. (Moscow) 37, 515-521.
30. Bolon, D. N., and Mayo, S. L. (2001) Polar residues in the protein core of Escherichia coli thioredoxin are important for fold specificity, Biochemistry 40, 10047-10053.
31. Hendsch, Z. S., and Tidor, B. (1994) Do salt bridges stabilize proteins? A continuum electrostatic analysis, Protein Sci. 3, 211-226.
32. Rozwarski, D. A., Gronenborn, A. M., Clore, G. M., Bazan, J. F., Bohm, A., Wlodawer, A., Hatada, M., and Karplus, P. A. (1994) Structural comparisons among the short-chain helical cytokines, Structure 2, 159-173.
33. Oakley, M. G., and Hollenbeck, J. J. (2001) The design of antiparallel coiled coils, Curr. Opin. Struct. Biol. 11, 450-457.
34. Walshaw, J., and Woolfson, D. N. (2001) Socket: a program for identifying and analysing coiled-coil motifs within protein structures, J. Mol. Biol. 307, 1427-1450.
35. Gernert, K. M., Surles, M. C., Labean, T. H., Richardson, J. S., and Richardson, D. C. (1995) The Alacoil: a very tight, antiparallel coiled-coil of helices, Protein Sci. 4, 2252-2260.
36. Schnarr, N. A., and Kennan, A. J. (2004) Strand orientation by steric matching: a designed antiparallel coiled-coil trimer. J. Am. Chem. Soc. 126, 14447-14451.
37. Betz, S. F., and DeGrado, W. F. (1996) Controlling topology and native-like behavior of de novo-designed peptides: design and characterization of antiparallel four-stranded coiled coils, Biochemistry 35, 6955-6962.
38. Gurnon, D. G., Whitaker, J. A., and Oakley, M. G. (2003) Design and characterization of a homodimeric antiparallel coiled coil, J. Am. Chem. Soc. 125, 7518-7519.
39. Monera, O., Zhou, N., Lavigne, P., Kay, C., and Hodges, R. (1996) Formation of parallel and antiparallel coiled-coils controlled by the relative positions of alanine residues in the hydrophobic core, J. Biol. Chem. 271, 3995-4001.
40. Oakley, M. G., and Kim, P. S. (1998) A buried polar interaction can direct the relative orientation of helices in a coiled coil, Biochemistry 37, 12603-12610.
41. Monera, O. D., Zhou, N. E., Kay, C. M., and Hodges, R. S. (1993) Comparison of antiparallel and parallel two-stranded alpha-helical coiled-coils. Design, synthesis, and characterization, J. Biol. Chem. 268, 19218-19227.
42. Monera, O., Kay, C., and Hodges, R. (1994) Electrostatic interactions control the parallel and antiparallel orientation of α-helical chains in two-stranded α-helical coiled-coils, Biochemistry 33, 3862-3871.
43. McClain, D. L., Binfet, J. P., and Oakley, M. G. (2001) Evaluation of the energetic contribution of interhelical Coulombic interactions for coiled coil helix orientation specificity, J. Mol Biol, 313, 371-383.
44. McClain, D. L., Woods, H. L., and Oakley, M. G. (2001) Design and characterization of a heterodimeric coiled coil that forms exclusively with an antiparallel relative helix orientation, J. Am. Chem. Soc. 123, 3151-3152.
45. Ghosh, I., Hamilton, A, and Regan, L. (2000) Antiparallel leucine zipper-directed protein reassembly: application to the green fluorescent protein, J. Am. Chem. Soc. 122, 5658-5659.
46. Wolf, E., Kim, P. S., and Berger, B. (1997) MultiCoil: a program for predicting two- and three-stranded coiled coils, Protein Sci. 6, 1179-1189.
47. Woolfson, D. N., and Alber, T. (1995) Predicting oligomerization states of coiled coils, Protein Sci 4, 1596-1607.
48. Akey, D. L., Malashkevich, V. N., and Kim, P. S. (2001) Buried polar residues in coiled-coil interfaces, Biochemistry 40, 6352-6360.
49. Campbell, K. M., and Lumb, K. J. (2002) Complementation of buried lysine and surface polar residues in a designed heterodimeric coiled coil, Biochemistry 41, 7169-7175.
50. McClain, D. L., Gurnon, D. G., and Oakley, M. G. (2002) Importance of potential interhelical salt-bridges involving interior residues for coiled-coil stability and quaternary structure, J. Mol. Biol. 324, 257-270.
51. Zhao, X., Ghaffari, S., Lodish, H., Malashkevich, V. N., and Kim, P. S. (2002) Structure of the Bcr-Abl oncoprotein oligomerization domain, Nat. Struct. Biol. 9, 117-120.
52. Yan, Y., Winograd, E., Viel, A., Cronin, T., Harrison, S. C., and Branton, D. (1993) Crystal structure of the repetitive segments of spectrin, Science 262, 2027-2030.
53. Lovejoy, B., Choe, S., Cascio, D., McRorie, D. K., DeGrado, W. F., and Eisenberg, D. (1993) Crystal structure of a synthetic triple-stranded alpha-helical bundle, Science 259, 1288-1293.
54. O'Neil, K. T., and DeGrado, W. F. (1990) A thermodynamic scale for the helix-forming tendencies of the commonly occurring amino acids, Science 250, 646-651.
55. Liu, J., and Lu, M. (2002) An alanine-zipper structure determined by long-range intermolecular interactions, J. Biol. Chem. 277, 48708-48713.
56. Liu, Y., and Eisenberg, D. (2002) 3D domain swapping: as domains continue to swap, Protein Sci. 11, 1285-1299.
57. Harbury, P. B., Tidor, B., and Kim, P. S. (1995) Repacking protein cores with backbone freedom: structure prediction for coiled coils, Proc. Natl. Acad. Sci. U.S.A. 92, 8408-8412.
58. Crick, F. H. C. (1953) The packing of a-helices: simple coiled coils, Acta Crystallogr. 6, 689-697.
59. Edelhoch, H. (1967) Spectroscopic determination of tryptophan and tyrosine in proteins, Biochemistry 6, 1948-1954.
60. Johnson, M. L., Correia, J. C., Yphantis, D. A., and Halvorson, H. R. (1981) Analysis of data from the analytical ultracentrifuge by nonlinear least-squares techniques, Biophys. J. 36, 575-588.
61. Schuck, P. (2003) On the analysis of protein self-association by sedimentation velocity analytical ultracentrifugation, Anal. Biochem. 320, 104-124.
62. Vistica, J., Dam, J., Balbo, A., Yikilmaz, E., Mariuzza, R. A., Roualt, T. A., and Schuck, P. (2004) Sedimentation equilibrium analysis of protein interactions with global implicit mass conservation constraints and systematic noise decomposition, Anal. Biochem. 326, 234-256.
63. Laue, T. M., Shah, B. D., Ridgeway, T. M., and Pelletier, S. L. (1992) Computer aided interpretation of analytical sedimentation data for proteins, in Analytical Ultracentrifugation in Biochemistry and Polymer Science, pp 90-125, Royal Society of Chemistry, Cambridge, U.K.
64. O'Shea, E. K., Rutkowski, R., Stafford, W. F. d., and Kim, P. S. (1989) Preferential heterodimer formation by isolated leucine zippers from fos and jun, Science 245, 646-648.
65. Zhou, N. E., Zhu, B. Y., Kay, C. M., and Hodges, R. S. (1992) The two-stranded alpha-helical coiled-coil is an ideal model for studying protein stability and subunit interactions, Biopolymers 32, 419-426.
66. Hu, J. C., O'Shea, E. K., Kim, P. S., and Sauer, R. T. (1990) Sequence requirements for coiled-coils: analysis with lambda repressor-GCN4 leucine zipper fusions, Science 250, 1400-1403.
67. Dunbrack, R. L., Jr., and Karplus, M. (1993) Backbone-dependent rotamer library for proteins. Application to side-chain prediction, J. Mol. Biol. 230, 543-574.
68. Havranek, J. J., and Harbury, P. B. (2003) Automated design of specificity in molecular recognition, Nat. Struct. Biol. 10, 45-52.
69. Pokala, N., and Handel, T. M. (2005) Energy functions for protein design: adjustment with protein-protein complex affinities, models for the unfolded state, and negative design of solubility and specificity, J. Mol. Biol. 347, 203-227.
70. Park, S., Yang, X., and Saven, J. G. (2004) Advances in computational protein design, Curr. Opin. Struct. Biol. 14, 487-494.
71. 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 A(2)B(2) diiron protein, J. Mol. Biol. 321, 923-938.
72. Nautiyal, S., Woolfson, D. N., King, D. S., and Alber, T. (1995) A designed heterotrimeric coiled coil, Biochemistry 34, 11645-11651.
73. Campbell, K. M., Sholders, A. J., and Lumb, K. J. (2002) Contribution of buried lysine residues to the oligomerization specificity and stability of the fos coiled coil, Biochemistry 41, 4866-4871.
74. Monera, O., Sonnichsen, F., Hicks, L., Kay, C., and Hodges, R. (1996) The relative positions of alanine residues in the hydrophobic core control the formation of two-stranded or four-stranded alpha-helical coiled-coils, Protein Eng. 9, 353-363.
75. Acharya, A., Ruvinov, S. B., Gal, J., Moll, J. R., and Vinson, C. (2002) A heterodimerizing leucine zipper coiled coil system for examining the specificity of a position interactions: amino acids I, V, L, N, A, and K, Biochemistry 41, 14122-14131.
76. Moitra, J., Szilak, L., Krylov, D., and Vinson, C. (1997) Leucine is the most stabilizing aliphatic amino acid in the d position of a dimeric leucine zipper coiled coil, Biochemistry 36, 12567-12573.
77. Laue, T. M., Shah, B. D., Ridgeway, T. M., and Pelletier, S. L. (1992) Computer-aided interpretation of analytical sedimentation data for proteins, in Analytical Ultracentrifugation in Biochemistry and Polymer Science (Harding, S. E., Rowe, A. J., and Horton, J. C., Eds.) pp 90-125, Royal Society of Chemistry, Cambridge, U.K.