The three-dimensional structures of two complexes between recombinant MS2 capsids and RNA operator fragments reveal sequence-specific protein-RNA interactions

Journal of Molecular Biology

Volumn 270, Issue 5, 1997, Pages 724-738

  Valegård, Karin ^a   Murray, James B ^b   Stonehouse, Nicola J ^b   Van Den Worm, Sjoerd ^a,c   Stockley, Peter G ^b   Liljas, Lars ^a  

^a UPPSALA UNIVERSITY   (Sweden)

^b UNIVERSITY OF LEEDS   (United Kingdom)

^c LEIDEN UNIVERSITY   (Netherlands)

Author keywords

Bacteriophage coat protein; Crystal structure; MS2; RNA stem loop; Virus assembly

Indexed keywords

ADENINE; COAT PROTEIN; CYTOSINE; DIMER; PHOSPHATE; PYRIMIDINE; RECOMBINANT PROTEIN; RNA; TYROSINE; URIDINE;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARTICLE; BINDING AFFINITY; COMPLEX FORMATION; CONTROLLED STUDY; CRYSTAL STRUCTURE; HYDROGEN BOND; NONHUMAN; OPERATOR; PRIORITY JOURNAL; PROTEIN RNA BINDING; STRUCTURE ACTIVITY RELATION; VIRUS CAPSID;

MIRIDAE;

EID: 0031213649     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1997.1144     Document Type: Article

References (59)

1. Abad-Zapatero C., Abdel-Meguid S. S., Johnson J. E., Leslie A. G. W., Rayment I., Rossmann M. G., Suck D., Tsukihara T. Structure of southern bean mosaic virus at 2.8 Å resolution. Nature. 286:1980;33-39.
2. Baidya N., Uhlenbeck O. C. The role of 2′-hydroxyl groups in an RNA-protein interaction. Biochemistry. 34:1995;12363-12368.
3. Beckett D., Uhlenbeck O. C. Ribonucleoprotein complexes of R17 coat protein and a translation operator analog. J. Mol. Biol. 204:1988;927-938.
4. Beckett D., Wu H.-N., Uhlenbeck O. C. Roles of operator and non-operator RNA sequences in bacteriophage R17 capsid assembly. J. Mol. Biol. 204:1988;939-947.
5. Biou V., Yaremchuk A., Tukalo M., Cusack S. The 2.9 Å structure of T. thermophilus seryl-tRNA synthetase complexed with tRNASer. Science. 263:1994;1404-1410.
6. Borer P. N., Lin Y., Wang S., Roggenbuck M. W., Gott J. M., Uhlenbeck O. C., Pelczer I. Proton NMR and structural features of a 24-nucleotide RNA hairpin. Biochemistry. 34:1995;6488-6503.
7. Brünger A. T. X-PLOR Manual. 1990;Yale University, New Haven.
8. Carey J., Cameron V., de Haseth P. L., Uhlenbeck O. C. Sequence-specific interaction of R17 coat protein with its RNA binding site. Biochemistry. 22:1983;2601-2610.
9. Asprecognition by its cognate class II aminoacyl-tRNA synthetase. Nature. 362:1993;181-184.
10. Engh R., Huber R. Accurate bond and angle parameters for X-ray protein structure refinement. Acta Crystallog. sect. A. 38:1991;392-400.
11. Fiers W. Structure and function of RNA bacteriophages. Comprehensive Virology. 1979;Plenum Publishing Corporation, New York.
12. Fiers W., Contreras R., Duerinck F., Haegeman G., Iserentant D., Merregaert J., Min Jou W., Molemans F., Raeymaekers A., Vandenberghe A., Volckaert G., Ysebaert M. Complete nucloetide sequence of bacteriophage MS2 RNA: primary and secondary structure of the replicase gene. Nature. 260:1976;500-507.
13. Frey P., Sammons D. Bond order and charge localization in nucleoside phosphorothioates. Science. 228:1985;541-545.
14. Golmohammadi R., Valegård K., Fridborg K., Liljas L. The refined structure of bacteriophage MS2 at 2.8 Å resolution. J. Mol. Biol. 234:1993;620-639.
15. Golmohammadi R., Fridborg K., Bundule M., Valegård K., Liljas L. The crystal structure of bacteriophage Qβ at 3.5 Å resolution. Structure. 4:1996;543-554.
16. Gott J. M., Wilhelm L. J., Uhlenbeck O. C. RNA binding properties of the coat protein from bacteriophage GA. Nucl. Acids Res. 19:1991;6499-6503.
17. Gott J. M., Pan T., LeCuyer K. A., Uhlenbeck O. C. Using circular permutation analysis to redefine the R17 coat protein binding site. Biochemistry. 32:1993;13399-13404.
18. Groebe D. R., Uhlenbeck O. C. Characterization of RNA hairpin loop stability. Nucl. Acids Res. 16:1987;11725-11734.
19. Gutell R. R., Weiser B., Woese C. R., Noller H. F. Comparative anatomy of 16-S-like ribosomal RNA. Progr. Nucl. Acid Res. Mol. Biol. 32:1985;155-216.
20. Harrison S. C., Olson A. J., Schutt C. E., Winkler F. K., Bricogne G. Tomato bushy stunt virus at 2.9 Å resolution. Nature. 276:1978;368-373.
21. Hogle J. M., Maeda A., Harrison S. C. Structure and assembly of turnip crinkle virus. I. X-ray crystallographic structure analysis at 3.2 Å resolution. J. Mol. Biol. 191:1986;625-638.
22. Hohn T. The assembly of protein particles of the RNA bacteriophage fr in the absence of RNA. Biochem. Biophys. Res. Commun. 36:1969a;7-17.
23. Hohn T. Role of RNA in the assembly process of bacteriophage fr. J. Mol. Biol. 43:1969b;191-200.
24. Hosur M. V., Schmidt T., Tucker R. C., Johnson J. E., Gallagher T. M., Selling B. H., Rueckert R. R. Structure of an insect virus at 3.0 Å resolution. Proteins: Struct. Funct. Genet. 2:1987;167-176.
25. Hung P. P., Ling C. M., Overby L. R. Self-assembly of Qβ and MS2 phage particles: possible function of initiation complexes. Science. 166:1969;1638-1640.
26. Jones T. A., Zou J.-Y., Cowan S. W., Kjeldgaard M. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallog. sect. A. 47:1991;110-119.
27. Kleywegt G. J., Brünger A. T. Cross-validation in crystallography. Structure. 4:1996;899-903.
28. Kleywegt G. J., Jones T. A. Halloween . Masks and Bones. Bailey S., Hubbard R., Waller D. From First Map to Final Model. Proceedings of the CCP4 Study Weekend. 1994;SERC Daresbury Laboratory, Daresbury.
29. Kraulis P. J. Molscript: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallog. 24:1991;946-950.
30. Liljas L., Fridborg K., Valegård K., Bundule M., Pumpens P. Crystal structure of bacteriophage fr capsids at 3.5 Å resolution. J. Mol. Biol. 244:1994;279-290.
31. Lim F., Peabody D. S. Mutations that increase the affinity of a translational repressor for RNA. Nucl. Acids Res. 22:1994;3748-3752.
32. Lim F., Spingola M., Peabody D. S. Altering the RNA binding specificity of a translational repressor. J. Biol. Chem. 269:1994;9006-9010.
33. Lowary P. T., Uhlenbeck O. C. An RNA mutation that increases the affinity of an RNA-protein interaction. Nucl. Acids Res. 15:1987;10483-10493.
34. Mastico R. A., Talbot S. J., Stockley P. G. Multiple presentation of foreign peptides on the surface of an RNA-free spherical bacteriophage capsid. J. Gen. Virol. 74:1993;541-548.
35. Matthews K., Cole R. D. Shell formation by capsid protein of f2 bacteriophage. J. Mol. Biol. 65:1972;1-15.
36. Milligan J. F., Uhlenbeck O. C. Determination of RNA-protein contacts using thiophosphate substitutions. Biochemistry. 28:1989;2849-2855.
37. Murray J. B., Collier A. K., Arnold J. R. P. A general purification procedure for chemically synthesized oligoribonucleotides. Anal. Biochem. 218:1994;177-184.
38. Ni C.-Z., Syed R., Kodandapani R., Wickersham J., Peabody D. S., Ely K. R. Crystal structure of the MS2 coat protein dimer: implications for RNA binding and virus assembly. Structure. 3:1995;255-263.
39. Oubridge C., Ito N., Evans P. R., Teo C.-H., Nagai K. Crystal structure of the U1A protein RNA binding domain complexed with an RNA hairpin at 1.92 Å resolution. Nature. 372:1994;432-438.
40. Parkinson G., Vojtechovsky J., Clowney L., Brünger A. T., Berman H. M. New parameters for the refinement of nucleic acid-containing structures. Acta Crystallog. sect. D. 52:1996;57-64.
41. Peabody D. S. The RNA binding site of bacteriophage MS2 coat protein. EMBO J. 12:1993;595-600.
42. Peabody D. S., Ely K. R. Control of translational repression by protein-protein interactions. Nucl. Acids Res. 20:1992;1649-1655.
43. Peattie D. A., Douthwaite S., Garrett R. A., Noller H. F. A "bulged" double helix in a RNA-protein contact site. Proc. Natl Acad. Sci. USA. 78:1981;7331-7335.
44. Romaniuk P. J., Lowary P. T., Wu H. N., Stormo G., Uhlenbeck O. C. RNA binding site of R17 coat protein. Biochemistry. 26:1987;1563-1568.
45. Rould M. A., Perona J. J., Steitz T. A. Structural basis of anticodon loop recognition by glutaminyl-tRNA synthetase. Nature. 352:1991;213-218.
46. Schubert D., Frank H. Properties of particles aggregated from protein subunits of bacteriophage fr. Virology. 43:1971;41-50.
47. Spahr P. F., Farber M., Gesteland R. Binding site on R17 RNA for coat protein. Nature. 222:1969;455-458.
48. Stockley P. G., Stonehouse N. J., Walton C., Walters D. A., Medina G., Macedo M. B., Hill H. R., Goodman S. T. S., Talbot S. J., Tewary H. K., Golmohammadi R., Liljas L., Valegård K. Molecular mechanism of RNA-phage morphogenesis. Biochem. Soc. Trans. 21:1993;627-633.
49. Stockley P. G., Stonehouse N. J., Valegård K. Molecular mechanism of RNA phage morphogenesis. Int. J. Biochem. 26:1994;1249-1260.
50. Stockley P. G., Stonehouse N. J., Murray J. B., Goodman S. T. S., Talbot S. J., Adams C. J., Liljas L., Valegård K. Probing sequence-specific RNA recognition by the bacteriophage MS2 coat protein. Nucl. Acids Res. 23:1995;2512-2518.
51. Stonehouse N. J., Stockley P. G. Effects of amino acid substitutions on the thermal stability of MS2 capsids lacking genomic RNA. FEBS Letters. 334:1993;355-359.
52. Stonehouse N. J., Valegård K., Golmohammadi R., van den Worm S., Walton C., Stockley P. G., Liljas L. Crystal structure of MS2 capsids with mutations in the subunit FG loop. J. Mol. Biol. 256:1996;330-339.
53. Talbot S. J., Goodman S., Bates S. R. E., Fishwick C. W. G., Stockley P. G. Use of synthetic oligoribonucleotides to probe RNA-protein interactions in the MS2 translational operator complex. Nucl. Acids Res. 18:1990;3521-3528.
54. Valegård K., Liljas L., Fridborg K., Unge T. The three-dimensional structure of the bacterial virus MS2. Nature. 345:1990;36-41.
55. Valegård K., Murray J. B., Stockley P. G., Stonehouse N. J., Liljas L. Crystal structure of an RNA bacteriophage coat protein-operator complex. Nature. 371:1994;623-626.
56. Westhof E., Dumas P., Moras D. Restrained refinement of two crystalline forms of yeast aspartic acid and phenylalanine transfer RNA crystals. Acta Crystallog. sect. A. 44:1988;112-123.
57. Witherell G. W., Gott J. M., Uhlenbeck O. C. Specific interaction between RNA phage coat proteins and RNA. Progr. Nucl. Acid Res. Mol. Biol. 40:1991;185-220.
58. Wu H. N., Uhlenbeck O. C. Role of a bulged A residue in a specific RNA-protein interaction. Biochemistry. 26:1987;8221-8227.
59. Zengel J. M., Lindahl L. Diverse mechanisms for regulating ribosomal protein synthesis in Escherichia coli. Progr. Nucl. Acid Res. Mol. Biol. 47:1994;331-370.