The stability and dynamics of ribosomal protein L9: Investigations of a molecular strut by amide proton exchange and circular dichroism

Journal of Molecular Biology

Volumn 268, Issue 2, 1997, Pages 482-493

  Lillemoen, Jarle ^a   Cameron, Christopher S ^a   Hoffman, David W ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

Amide proton exchange; L9; Protein stability; Ribosomal protein; RNA binding

Indexed keywords

RIBOSOME PROTEIN; RNA BINDING PROTEIN;

ARTICLE; CIRCULAR DICHROISM; GEOBACILLUS STEAROTHERMOPHILUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN RNA BINDING; PROTEIN STABILITY; PROTON NUCLEAR MAGNETIC RESONANCE; PROTON TRANSPORT; RIBOSOME;

GEOBACILLUS STEAROTHERMOPHILUS;

EID: 0031547962     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1997.0982     Document Type: Article

References (46)

1. Aboul-ela F., Karn J., Varani G. The structure of the human immunodeficiency virus type-1 TAR RNA reveals the principles of RNA recognition by Tat protein. J. Mol. Biol. 253:1995;313-332.
2. Adamski F. M., Atkins J. F., Gesteland R. F. Ribosomal protein L9 interactions with 23 S rRNA: the use of translational bypass assay to study the effect of amino acid substitutions. J. Mol. Biol. 261:1996;357-371.
3. Babu Y. S., Bugg C. E., Cook W. J. Structure of calmodulin refined at 2.2 Å resolution. J. Mol. Biol. 204:1988;191-204.
4. Bai Y., Milne J. S., Mayne L., Englander S. W. Primary effects on peptide group hydrogen exchange. Proteins: Struct. Funct. Genet. 17:1993;75-86.
5. Bai Y., Englander J. J., Mayne L., Milne J. S., Englander S. W. Thermodynamic parameters from hydrogen exchange measurements. Methods in Enzymology. 1995a;Academic Press, New York.
6. Bai Y., Sosnick T. R., Mayne L., Englander S. W. Protein folding intermediates: native-state hydrogen exchange. Science. 269:1995b;192-197.
7. 15N relaxation using inverse detected two-dimensional NMR spectroscopy: the central helix is flexible. Biochemistry. 31:1992;5269-5278.
8. 13C-heteronuclear NMR. J. Biomol. NMR. 6:1995;375-389.
9. Betz S. F., Marmorino J. L., Saunders A. J., Doyle D. F., Young G. B., Pielak G. P. Unusual effects of an engineered disulfide on global and local protein stability. Biochemistry. 35:1996;7422-7428.
10. Biou V., Shu F., Ramakrishnan V. X-ray crystallography shows that translational initiation factor IF3 consists of two compact alpha/beta domains linked by an alpha helix. EMBO J. 14:1996;4056-4064.
11. Brimacombe R., Gornicki P., Greuer B., Mitchell P., Osswald M., Rinke-Appel J., Schüler D., Stade K. The three-dimensional structure and function of Escherichia coli ribosomal RNA, as studied by cross-linking techniques. Biochim. Biophys. Acta. 1050:1990;8-13.
12. Ferrin T. E., Huang C. C., Jarvis L. E., Langridge R. The MIDAS display system. J. Mol. Graph. 6:1988;13-27.
13. Forsén S., Hoffman R. A. A new method for study of the moderately rapid chemical exchange rates employing nuclear magnetic double resonance. Acta. Chem. Scand. 17:1963;1787.
14. Greenfield N. Methods to estimate the conformation of proteins and polypeptides from circular dichroism data. Anal. Biochem. 235:1996;1-10.
15. Herbst K. L., Nichols L. M., Gesteland R. F., Weiss R. B. A mutation in ribosomal protein L9 affects ribosomal hopping during translation of gene 60 from bacteriophage T4. Proc. Natl Acad. Sci. USA. 91:1994;12525-12529.
16. Hoffman D. W., Query C. Q., Golden B. L., White S. W., Keene J. D. RNA-binding domain of the A protein of the U1 small nuclear ribonucleoprotein analyzed by NMR spectroscopy is structurally similar to ribosomal proteins. Proc. Natl Acad. Sci. USA. 88:1991;2495-2499.
17. Hoffman D. W., Davies C., Gerchman S. E., Kycia J. H., Porter S. J., White S. W., Ramakrishnan V. Crystal structure of prokaryotic ribosomal protein L9: a bi-lobed RNA binding protein. EMBO J. 13:1994;205-212.
18. Hoffman D. W., Cameron C. S., Davies C., White S. W., Ramakrishnan V. Ribosomal Protein L9: a structure determination by the combined use of X-ray crystallography and NMR spectroscopy. J. Mol. Biol. 264:1996;1058-1071.
19. Howe P. W. A., Nagai K., Neuhaus D., Varani G. NMR studies of U1 snRNA recognition by the N-terminal RNP domain of the human U1A protein. EMBO J. 13:1994;3873-3881.
20. Huang C. C., Pettersen E. F., Klein T. E., Ferrin T. E., Longridge R. Conic: a fast renderer for space filling molecules with shadows. J. Mol. Graph. 9:1991;230-236.
21. Hvidt A., Nielsen S. O. Hydrogen exchange in proteins. Advan. Protein Chem. 21:1966;287-386.
22. Jeng M.-F., Dyson J. Comparison of the hydrogen-exchange behavior of reduced and oxidized Escherichia coli thioredoxin. Biochemistry. 34:1995;611-619.
23. Kraulis P. J. MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallog. 24:1991;946-950.
24. Mayo S. L., Baldwin R. L. Guanidinium chloride induction of partial unfolding in amide proton exchange in RNase A. Science. 262:1993;873-876.
25. Molday R. S., Englander S. W., Kallen R. G. Primary structure effects of peptide group hydrogen exchange. Biochemistry. 11:1972;150-158.
26. Nag B., Akella S. S., Cann P. A., Tewari D. S., Glitz D. G., Traut R. R. Monoclonal antibodies to Escherichia coli ribosomal proteins L9 and L10. J. Biol. Chem. 266:1991;22129-22135.
27. Nagai K., Oubridge C., Jessen T. M., Li J., Evans P. R. Crystal structure of the RNA-binding domain of the U1 small ribonucleoprotein A. Nature. 348:1990;515-520.
28. Noller H. F., Green R., Heilek G., Hoffarth V., Hüttenhofer A., Joseph S., Lee I., Lieberman K., Mankin A., Merryman C., Powers T., Puglisi E., Samaha R., Weiser B. Structure and function of ribosomal RNA. Biochem. Cell Biol. 73:1995;997-1009.
29. Oubridge C., Ito N., Evans P. E., Teo C. H., Nagai K. Crystal structure at 1.92 Å resolution of the RNA-binding domain of the U1A spliceosomal protein complexed with an RNA hairpin. Nature. 372:1994;432-438.
30. Peterson R. D., Bartel D. P., Szostak J. W., Horvath S. J., Feigon J. 1H NMR studies of the high-affinity Rev binding site of the rev responsive element of HIV-1 mRNA: base pairing in the core binding element. Biochemistry. 33:1994;5357-5366.
31. Plateau P., Guéron M. Exchangeable proton NMR without line distortion. J. Am. Chem. Soc. 104:1982;7310-7311.
32. Puglisi J. D., Chen L., Blanchard S., Frankel A. D. Solution structure of a bovine immunodeficiency virus Tat-TAR peptide-RNA complex. Science. 270:1995;1200-1203.
33. Ramakrishnan V., Davies C., Gerchman S. E., Golden B. L., Hoffman D. W., Jaishree T. N., Kycia J. H., Porter S., White S. W. Structures of prokaryotic ribosomal proteins: implications for RNA binding and evolution. Biochem. Cell Biol. 73:1995;979-986.
34. 2H and temperature. Biochemistry. 24:1985;7396-7407.
35. Roth H. E., Nierhaus K. H. Assembly map of the 50S subunit from Escherichia coli ribosomes, covering the proteins present in the first reconstituted intermediate particle. Eur. J. Biochem. 103:1980;95-98.
36. Samaha R. R., Green R., Noller H. F. A base pair between tRNA and 23 S rRNA in the peptidyl transferase centre of the ribosome. Nature. 377:1995;309-314.
37. Scholtz J. M., Qian H., York E. J., Stewart J. M., Baldwin R. L. Parameters of helix-coil transition theory for alanine-based peptides of varying chainlengths in water. Biopolymers. 31:1991;1463-1470.
38. Schulman B. A., Kim P. S. Hydrogen exchange in BPT1 variants that do not share a common disulphide bond. Protein Sci. 3735:1994;2226-2232.
39. 2+) calbindin D9k: the rates of amide proton exchange with solvent. J. Mol. Biol. 227:1992;1100-1117.
40. Spera S., Ikura M., Bax A. Measurement of the exchange rates of rapidly exchanging amide protons: application to the study of calmodulin and its complex with the myosin light chain kinase. J. Biomol. NMR. 1:1991;155-165.
41. Sreerama N., Woody R. W. Protein secondary structure from circular dichroism spectroscopy. Combining variable selection principle and cluster analysis with neural network, ridge regression and self-consistent methods. Biochemistry. 242:1994;497-507.
42. 13C isotope labeling of proteins with sodium acetate for NMR studies: application to human carbonic anhydrase II. Biochemistry. 30:1991;4491-4494.
43. Walleczek J., Redl B., Stöffler-Meilcke M., Stöffler G. Protein-protein cross-linking of the 50S ribosomal subunit of Escherichia coli using 2-iminothiolane. J. Biol. Chem. 264:1989;4231-4237.
44. Wishart D. S., Sykes B. D. Chemical shifts as a tool for structure determination. James T. L., Oppenheimer N. J. Methods in Enzymology. 1994;Academic Press, New York.
45. 15N chemical shift referencing in biomolecular NMR. J. Biomol. NMR. 6:1995;135-140.
46. Zuiderweg E. R. P. A proton-detected heteronuclear chemical-shift correlation experiment with improved resolution and sensitivity. J. Magn. Reson. 86:1990;346-352.