Design of λ Cro fold: Solution structure of a monomeric variant of the de novo protein

Journal of Molecular Biology

Volumn 354, Issue 4, 2005, Pages 801-814

  Isogai, Yasuhiro ^a,b   Ito, Yutaka ^b,c,f   Ikeya, Teppei ^d,f   Shiro, Yoshitsugu ^a   Ota, Motonori ^e  

^a RIKEN HARIMA INSTITUTE   (Japan)

^b Japan Science and Technology Agency   (Japan)

^c RIKEN   (Japan)

^d NATIONAL INSTITUTE OF ADVANCED INDUSTRIAL SCIENCE AND TECHNOLOGY AIST   (Japan)

^e TOKYO INSTITUTE OF TECHNOLOGY   (Japan)

^f TOKYO METROPOLITAN UNIVERSITY   (Japan)

Author keywords

de novo protein design; Knowledge based potential function; NMR; Solution structure; Cro

Indexed keywords

BACTERIOPHAGE LAMBDA CRO PROTEIN; DE NOVO PROTEIN; DNA BINDING PROTEIN; PROTEIN SUBUNIT; UNCLASSIFIED DRUG;

ALPHA HELIX; AMINO ACID SEQUENCE; ARTICLE; BETA SHEET; CARBOXY TERMINAL SEQUENCE; DIMERIZATION; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ENGINEERING; PROTEIN FOLDING; PROTEIN PROCESSING; PROTEIN STABILITY; PROTEIN STRUCTURE; PROTEIN VARIANT; SEQUENCE ANALYSIS; STRUCTURAL PROTEOMICS;

ENTEROBACTERIA PHAGE LAMBDA;

EID: 28444491969     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2005.10.005     Document Type: Article

References (74)

1. A.G. Murzin, S.E. Brenner, T. Hubbard, and C. Chothia SCOP: a structural classification of proteins database for the investigation of sequences and structures J. Mol. Biol. 247 1995 536 540
2. A. Bateman, L. Coin, R. Durbin, R.D. Finn, V. Hollich, and S. Griffiths-Jones The Pfam protein families database Nucl. Acids Res. 32 2004 D138 D141
3. J.R. Desjarlais, and T.M. Handel New strategies in protein design Curr. Opin. Biotechnol. 6 1995 460 466
4. J.W. Bryson, S.F. Betz, H.S. Lu, D.J. Suich, H.X. Zhou, K.T. O'Neil, and W.F. DeGrado Protein design: a hierarchic approach Science 270 1995 935 941
5. M.H. Cordes, A.R. Davidson, and R.T. Sauer Sequence space, folding and protein design Curr. Opin. Struct. Biol. 6 1996 3 10
6. T.P. Quinn, N.B. Tweedy, R.W. Williams, J.S. Richardson, and D.C. Richardson Betadoublet: de novo design, synthesis, and characterization of a beta-sandwich protein Proc. Natl Acad. Sci. USA 91 1994 8747 8751
7. R.B. Hill, and W.F. DeGrado Solution structure of alpha D-2, a nativelike de novo designed protein J. Am. Chem. Soc. 120 1998 1138 1145
8. B.R. Gibney, F. Rabanal, J.J. Skalicky, A.J. Wand, and P.L. Dutton Iterative protein redesign J. Am. Chem. Soc. 121 1999 4952 4960
9. Y. Isogai, M. Ota, T. Fujisawa, H. Izuno, M. Mukai, H. Nakamura, T. Iizuka, and K. Nishikawa Design and synthesis of a globin fold Biochemistry 38 1999 7431 7443
10. S. Roy, and M.H. Hecht Cooperative thermal denaturation of proteins designed by binary patterning of polar and nonpolar amino acids Biochemistry 39 2000 4603 4607
11. S.A. Marshall, and S.L. Mayo Achieving stability and conformational specificity in designed proteins via binary patterning J. Mol. Biol. 305 2001 619 631
12. B.I. Dahiyat, and S.L. Mayo De novo protein design: fully automated sequence selection Science 278 1997 82 87
13. B. Kuhlman, G. Dantas, G.C. Ireton, G. Varani, B.L. Stoddard, and D. Baker Design of a novel globular protein fold with atomic-level accuracy Science 302 2003 1364 1368
14. B. Kuhlman, and D. Baker Native protein sequences are close to optimal for their structures Proc. Natl Acad. Sci. USA 97 2000 10383 10388
15. M. Ota, S. Kanaya, and K. Nishikawa Desk-top analysis of the structural stability of various point mutations introduced into ribonuclease H J. Mol. Biol. 248 1995 733 738
16. M. Ota, Y. Isogai, and K. Nishikawa Knowledge-based potential defined for a rotamer library to design protein sequences Protein Eng. 14 2001 557 564
17. H.M. Berman, J. Westbrook, Z. Feng, G. Gilliland, T.N. Bhat, and H. Weissig The protein data bank Nucl. Acids Res. 28 2000 235 242
18. Y. Isogai, A. Ishii, T. Fujisawa, M. Ota, and K. Nishikawa Redesign of artificial globins: effects of residue replacements at hydrophobic sites on the structural properties Biochemistry 39 2000 5683 5690
19. Y. Isogai, M. Ota, A. Ishii, M. Ishida, and K. Nishikawa Identification of amino acids involved in protein structural uniqueness: implication for de novo protein design Protein Eng. 15 2002 555 560
20. W.F. Anderson, D.H. Ohlendorf, Y. Takeda, and B.W. Matthews Structure of the cro repressor from bacteriophage lambda and its interaction with DNA Nature 290 1981 754 758
21. W.F. Anderson, Y. Takeda, D.H. Ohlendorf, and B.W. Matthews Proposed alpha-helical super-secondary structure associated with protein DNA recognition J. Mol. Biol. 159 1982 745 751
22. T.A. Steitz, D.H. Ohlendorf, D.B. McKay, W.F. Anderson, and B.W. Matthews Structural similarity in the DNA-binding domains of catabolite gene activator and cro repressor proteins Proc. Natl Acad. Sci. USA 79 1982 3097 3100
23. D.H. Ohlendorf, W.F. Anderson, M. Lewis, C.O. Pabo, and B.W. Matthews Comparison of the structures of cro and lambda repressor proteins from bacteriophage lambda J. Mol. Biol. 169 1983 757 769
24. Y. Takeda, D.H. Ohlendorf, W.F. Anderson, and B.W. Matthews DNA-binding proteins Science 221 1983 1020 1026
25. A.K.M.M. Mollah, M.A. Aleman, R.A. Albright, and M.C. Mossing Core packing defects in an engineered Cro monomer corrected by combinatorial mutagenesis Biochemistry 35 1996 743 748
26. P.B. Rupert, A.K. Mollah, M.C. Mossing, and B.W. Matthews The structural basis for enhanced stability and reduced DNA binding seen in engineered second-generation Cro monomers and dimers J. Mol. Biol. 296 2000 1079 1090
27. M.C. Mossing, and R.T. Sauer Stable, monomeric variants of lambda Cro obtained by insertion of a designed beta-hairpin sequence Science 250 1990 1712 1715
28. A.A. Pakula, V.B. Young, and R.T. Sauer Bacteriophage lambda cro mutations: effects on activity and intracellular degradation Proc. Natl Acad. Sci. USA 83 1986 8829 8833
29. W.A. Lim, and R.T. Sauer Alternative packing arrangements in the hydrophobic core of lambda repressor Nature 339 1989 31 36
30. J.U. Bowie, J.F. Reidhaar-Olson, W.A. Lim, and R.T. Sauer Deciphering the message in protein sequences: tolerance to amino acid substitutions Science 247 1990 1306 1310
31. B.M. Brown, and R.T. Sauer Tolerance of Arc repressor to multiple-alanine substitutions Proc. Natl Acad. Sci. USA 96 1999 1983 1988
32. R. Jana, T.R. Hazbun, A.K. Mollah, and M.C. Mossing A folded monomeric intermediate in the formation of lambda Cro dimer-DNA complexes J. Mol. Biol. 273 1997 402 416
33. A.J. Hubbard, L.P. Bracco, S.J. Eisenbeis, R.B. Gayle, G. Beaton, and M.H. Caruthers Role of the Cro repressor carboxy-terminal domain and flexible dimer linkage in operator and nonspecific DNA binding Biochemistry 29 1990 9241 9249
34. D.H. Ohlendorf, D.E. Tronrud, and B.W. Matthews Refined structure of Cro repressor protein from bacteriophage lambda suggests both flexibility and plasticity J. Mol. Biol. 280 1998 129 136
35. R.A. Albright, and B. Matthews Crystal structure of lambda-Cro bound to a consensus operator at 3.0 Å resolution J. Mol. Biol. 280 1996 137 151
36. S.F. Altschul, T.L. Madden, A.A. Schaffer, J. Zhang, Z. Zhang, W. Miller, and D.J. Lipman Gapped BLAST and PSI-BLAST: a new generation of protein database search programs Nucl. Acids Res. 25 1997 3389 3402
37. K.A. Dill, S. Bromberg, K. Yue, K.M. Fiebig, D.P. Yee, P.D. Thomas, and H.S. Chan Principles of protein folding, a perspective from simple exact models Protein Sci. 4 1995 561 602
38. K. Furukawa, M. Oda, and H. Nakamura A small engineered protein lacks structural uniqueness by increasing the side-chain conformational entropy Proc. Natl Acad. Sci. USA 93 1996 13583 13588
39. D.A. Parsell, and R.T. Sauer The structural stability of a protein is an important determinant of its proteolytic susceptibility in Escherichia coli J. Biol. Chem. 264 1989 7590 7595
40. J.K. Myers, C.N. Pace, and J.M. Scholtz Denaturant m values and heat capacity changes: relation to changes in accessible surface areas of protein unfolding Protein Sci. 4 1995 2138 2148
41. 13C chemical shift data J. Biomol. NMR 4 1994 171 180
42. R.A. Albright, M.C. Mossing, and B. Matthews High-resolution structure of an engineered Cro monomer shows changes in conformation relative to the native dimer Biochemistry 35 1996 735 742
43. M.C. Mossing Solution structure and dynamics of a designed monomeric variant of the lambda Cro repressor Protein Sci. 7 1998 983 993
44. P.J. Fleming, and F.M. Richards Protein packing: dependence on protein size, secondary structure and amino acid composition J. Mol. Biol. 299 2000 487 498
45. K. Yutani, K. Ogasahara, T. Tsujita, and Y. Sugino Dependence of conformational stability on hydrophobicity of the amino acid residue in a series of variant proteins substituted at a unique position of tryptophan synthase alpha subunit Proc. Natl Acad. Sci. USA 84 1987 4441 4444
46. M. Matsumura, W.J. Becktel, and B.W. Matthews Hydrophobic stabilization in T4 lysozyme determined directly by multiple substitutions of Ile 3 Nature 334 1998 406 410
47. N.C. Gassner, W.A. Baase, and B.W. Matthews A test of the "jigsaw puzzle" model for protein folding by multiple methionine substitutions within the core of T4 lysozyme Proc. Natl Acad. Sci. USA 93 1996 12155 12158
48. D.D. Axe, N.W. Foster, and A.R. Fersht Active barnase variants with completely random hydrophobic cores Proc. Natl Acad. Sci. USA 93 1996 5590 5594
49. M.C. Mossing, J.U. Bowie, and R.T. Sauer A streptomycin selection for DNA-binding activity Methods Enzymol. 208 1991 604 619
50. S. Kirkpatrick, C.D. Gelatt, and M.P. Vecchi Optimization by simulated annealing Science 220 1983 671 680
51. J.W. Ponder, and M. Richards Tertiary templates for proteins. Use of packing criteria in the enumeration of allowed sequences for different structural classes J. Mol. Biol. 193 1987 775 791
52. M. Ota, and K. Nishikawa Assessment of pseudo-energy potentials by the best-five test: a new use of the three-dimensional profiles of proteins Protein Eng. 10 1997 339 351
53. M.J. Sippl Calculation of conformational ensembles from potentials of mean force. An approach to the knowledge-based prediction of local structures in globular proteins J. Mol. Biol. 213 1990 859 883
54. N. Metropolis, A.W. Rosenbluth, M.N. Rosenbluth, and A.H. Teller Equation of state calculations by fast computing machines J. Chem. Phys. 21 1953 1087 1092
55. M. Ishida, N. Dohmae, Y. Shiro, T. Oku, T. Iizuka, and Y. Isogai Design and synthesis of de novo cytochromes c Biochemistry 43 2004 9823 9833
56. J. Sambrook, and R.W. Russell Molecular Cloning: A Laboratory Manual 3rd edit., vol. 3, pp A2.2-A2.4 1991 Cold Spring Harbor Laboratory Press Cold Spring Harbor, NY
57. T.E. Creighton Proteins, Structures and Molecular Properties 2nd edit., pp. 14-17 1993 Freeman New York, NY
58. G. Ralston Introduction to Analytical Ultracentrifugation vol. 1, pp. 43-47 1993 Beckman Fullerton, CA
59. E.D. Laue, M.R. Mayger, J. Skilling, and J. Staunton Reconstruction of phase sensitive 2D NMR spectra by maximum entropy J. Magn. Reson. 68 1986 14 29
60. 1H 2D NMR spectra by interactive graphics J. Magn. Reson. 24 1989 627 633
61. P.J. Kraulis, P.J. Domaille, S.L. Campbell-Burk, T. Van Aken, and E.D. Laue Solution structure and dynamics of ras p21.GDP determined by heteronuclear three- and four-dimensional NMR spectroscopy Biochemistry 33 1994 3515 3531
62. S. Grzesiek, and A. Bax Correlating backbone amide and side chain resonances in larger proteins by multiple relayed triple resonance NMR J. Am. Chem. Soc. 114 1992 6291 6293
63. S. Grzesiek, and A. Bax An efficient experiment for sequential backbone assignment of medium-sized isotopically enriched proteins J. Magn. Reson. 99 1992 201 207
64. S. Grzesiek, and A. Bax Improved 3D triple-resonance NMR techniques applied to a 31-kDa protein J. Magn. Reson. 96 1992 432 440
65. 13C-labelled proteins J. Magn. Reson. 97 1992 213 217
66. 15N-enriched proteins J. Biomol. NMR 3 1993 185 204
67. 13C magnetization J. Magn. Reson. ser. B 101 1993 114 119
68. 15N-labelled proteins J. Biomol. NMR 3 1993 349 354
69. 13C-enriched proteins J. Magn. Reson. 88 1990 425 431
70. 15N-labelled proteins J. Am. Chem. Soc. 111 1989 1515 1517
71. P. Güntert, C. Mumenthaler, and K. Wüthrich Torsion angle dynamics for NMR structure calculation with the new program DYANA J. Mol. Biol. 273 1997 283 298
72. T. Herrmann, P. Güntert, and K. Wuthrich Protein NMR structure determination with automated NOE assignment using the new software CANDID and the torsion angle dynamics algorithm DYANA J. Mol. Biol. 319 2002 209 227
73. A.T. Brünger, P.D. Adams, G.M. Clore, W.L. DeLano, P. Gros, and R.W. Grosse-Kunstleve Crystallography and NMR system (CNS): a new software system for macromolecular structure determination Acta Crystallog. sect. D 54 1998 905 921
74. R.A. Laskowski, J.A. Rullmannn, M.W. MacArthur, R. Kaptein, and J.M. Thornton AQUA PROCHECK-NMR programs for checking the quality of protein structures solved by NMR J. Biomol. NMR 8 1996 477 486