Structure and dynamics of the iron responsive element RNA: Implications for binding of the RNA by iron regulatory binding proteins

Journal of Molecular Biology

Volumn 274, Issue 1, 1997, Pages 72-83

  Addess, Kenneth J ^a   Basilion, James P ^b   Klausner, Richard D ^b   Rouault, Tracey A ^b   Pardi, Arthur ^a  

^a UNIVERSITY OF COLORADO   (United States)

^b EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

Author keywords

Hairpin loops and bulges; Iron regulation; IRP; NMR structure; RNA structure

Indexed keywords

FERRITIN; IRON REGULATORY FACTOR; MESSENGER RNA; RNA BINDING PROTEIN; TRANSFERRIN RECEPTOR;

ARTICLE; CONTROLLED STUDY; MOLECULAR DYNAMICS; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN RNA BINDING; RNA CONFORMATION; RNA SEQUENCE; RNA STRUCTURE;

EID: 0030660482     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1997.1377     Document Type: Article

References (71)

1. Allain F. H., Gubser C. C., Howe P. W., Nagai K., Neuhaus D., Varani G. Specificity of ribonucleoprotein interaction determined by RNA folding during complex formulation. Nature. 380:1996;646-650.
2. Altona C. Conformational analysis of nucleic acids. Determination of backbone geometry of single-helical RNA and DNA in aqueous solution. Rec. Trav. Chim. Pays-Bas. 101:1982;413-432.
3. Aziz N., Munro H. N. Iron regulates ferritin mRNA translation through a segment of its 5′ untranslated region. Proc. Natl Acad. Sci. USA. 84:1987;8478-8482.
4. Barton H. A., Eisenstein R. S., Bomford A., Munro H. N. Determinants of the interaction between the iron-responsive element-binding protein and its binding site in rat L-ferritin mRNA. J. Biol. Chem. 265:1990;7000-7008.
5. Basilion J. P., Rouault T. A., Massinople C. M., Klausner R. D., Burgess W. H. The iron-responsive element-binding protein: localization of the RNA-binding site to the aconitase active-site cleft. Proc. Natl Acad. Sci. USA. 91:1994;574-578.
6. Batey R. T., Inada M., Kujawinski E., Puglisi J. D., Williamson J. R. Preparation of isotopically labeled ribonucleotides for multidimensional NMR spectroscopy of RNA. Nucl. Acids Res. 20:1992;4515-4523.
7. Battiste J. L., Tan R., Frankel A. D., Williamson J. R. Binding of an HIV Rev peptide to Rev responsive element RNA induces formation of purine-purine base pairs. Biochemistry. 33:1994;2741-2747.
8. 13C-heteronuclear NMR. J. Biomol. NMR. 6:1995;375-389.
9. Beaumont C., Leneuve P., Devaux I., Scoazec J. Y., Berthier M., Loiseau M. N., Grandchamp B., Bonneau D. Mutation in the iron responsive element of the L ferritin mRNA in a family with dominant hyperferritinaemia and cataract. Nature Genet. 11:1995;444-446.
10. Bettany A. J., Eisenstein R. S., Munro H. N. Mutagenesis of the iron-regulatory element further defines a role for RNA secondary structure in the regulation of ferritin and transferrin receptor expression. J. Biol. Chem. 267:1992;16531-16537.
11. Binder R., Horowitz J. A., Basilion J. P., Koeller D. M., Klausner R. D., Harford J. B. Evidence that the pathway of transferrin receptor messenger-RNA degradation involves an endonucleolytic cleavage within the 3′ UTR and does not involve poly(A) tail shortening. EMBO J. 13:1994;1969-1980.
12. 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.
13. Brünger, A. T. 1992, X-PLOR, Version 3.1: A System for X-ray Crystallography and NMR, Yale University Press, New Haven, CT.
14. Butt J., Kim H. Y., Basilion J. P., Cohen S., Iwai K., Philpott C. C., Altschul S., Klausner R. D., Rouault T. A. Differences in the RNA binding sites of iron regulatory proteins and potential target diversity. Proc. Natl Acad. Sci. USA. 93:1996;4345-4349.
15. Dieckmann T., Suzuki E., Nakamura G. K., Feigon J. Solution structure of an ATP-binding RNA aptamer reveals a novel fold. RNA. 2:1996;628-640.
16. Girelli D., Corrocher R., Bisceglia L., Olivieri O., Defranceschi L., Zelante L., Gasparini P. Molecular-basis for the recently described hereditary hyperferritinemia cataract syndrome: a mutation in the iron-responsive element of ferritin L-subunit gene (the Verona Mutation). Blood. 86:1995;4050-4053.
17. Gray N. K., Hentze M. W. Iron regulatory protein prevents binding of the 43 S translation pre-initiation complex to ferritin and eALAS messenger-RNAs. EMBO J. 13:1994;3882-3891.
18. Guo B., Yu Y., Leibold E. A. Iron regulates cytoplasmic levels of a novel iron-responsive element-binding protein without aconitase activity. J. Biol. Chem. 269:1994;24252-24260.
19. Haile D. J., Hentze M. W., Rouault T. A., Harford J. B., Klausner R. D. Regulation of interaction of the iron-responsive element binding protein with iron-responsive RNA elements. Mol. Cell. Biol. 9:1989;5055-5061.
20. Harrell C. M., McKenzie A. R., Patino M. M., Walden W. E., Theil E. C. Ferritin mRNA: interactions of iron regulatory element with translational regulator protein P-90 and the effect on base-paired flanking regions. Proc. Natl Acad. Sci. USA. 88:1991;4166-4170.
21. Henderson B. R., Menotti E., Bonnard C., Kuhn L. C. Optimal sequence and structure of iron-responsive elements. Selection of RNA stem-loops with high affinity for iron regulatory factor. J. Biol. Chem. 269:1994;17481-17489.
22. Henderson B. R., Menotti E., Kuhn L. C. Iron regulatory proteins 1 and 2 bind distinct sets of RNA target sequences. J. Biol. Chem. 271:1996;4900-4908.
23. Hentze M. W., Kuhn L. C. Molecular control of vertebrate iron metabolism: mRNA-based regulatory circuits operated by iron, nitric oxide, and oxidative stress. Proc. Natl Acad. Sci. USA. 93:1996;8175-8182.
24. Hentze M. W., Caughman S. W., Rouault T. A., Barriocanal J. G., Dancis A., Harford J. B., Klausner R. D. Identification of the iron-responsive element for the translational regulation of human ferritin mRNA. Science. 238:1987;1570-1573.
25. Jaffrey S. R., Haile D. J., Klausner R. D., Harford J. B. The interaction between the iron-responsive element binding protein and its cognate RNA is highly dependent upon both RNA sequence and structure. Nucl. Acids Res. 21:1993;4627-4631.
26. Jiang F., Kumar R. A., Jones R. A., Patel D. J. Structural basis of RNA folding and recognition in an AMP-RNA aptamer complex. Nature. 382:1996;183-186.
27. Jucker F. M., Heus H. A., Yip P. F., Moors E. H. M., Pardi A. A network of heterogeneous hydrogen bonds in GNRA tetraloops. J. Mol. Biol. 264:1996;968-980.
28. Kennedy M. C., Mendemueller L., Blondin G. A., Beinert H. Purification and characterization of cytosolic aconitase from beef-liver and its relationship to the iron-responsive element binding-protein. Proc. Natl Acad. Sci. USA. 89:1992;11730-11734.
29. Kikinis Z., Eisenstein R. S., Bettany A. J., Munro H. N. Role of RNA secondary structure of the iron-responsive element in translational regulation of ferritin synthesis. Nucl. Acids Res. 23:1995;4190-4195.
30. Klausner R. D., Rouault T. A., Harford J. B. Regulating the fate of mRNA: the control of cellular iron metabolism. Cell. 72:1993;19-28.
31. Kraulis P. J. MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallog. 24:1991;946-950.
32. Kumar A., Ernst R. R., Wüthrich K. A two-dimensional nuclear Overhauser enhancement (2D NOE) experiment for the elucidation of complete proton-proton cross-relaxation networks in biological macromolecules. Biochem. Biophys. Res. Commun. 95:1980;1-6.
33. Laing L. G., Hall K. B. A model of the iron responsive element RNA hairpin loop structure determined from NMR and thermodynamic data. Biochemistry. 35:1996;13586-13596.
34. Lauble H., Kennedy M. C., Beinert H., Stout C. D. Crystal-structures of aconitase with isocitrate and nitroisocitrate bound. Biochemistry. 31:1992;2735-2748.
35. 31P coupling constants in isotopically labeled RNA. FEBS Letters. 362:1995;156-160.
36. Luisi B. F., Xu W. X., Otwinowski Z., Freedman L. P., Yamamoto K. R., Sigler P. B. Crystallographic analysis of the interaction of the glucocorticoid receptor with DNA. Nature. 352:1991;497-505.
37. Milligan J. F., Groebe D. R., Witherell G. W., Uhlenbeck O. C. Oligoribonucleotide synthesis using T7 RNA polymerase and synthetic DNA templates. Nucl. Acids Res. 15:1987;8783-8789.
38. Mueller L., Legault P., Pardi A. Improved RNA structure determination by detection of NOE contacts to exchange-broadened amino protons. J. Am. Chem. Soc. 117:1995;11043-11048.
39. 15N labeled nucleic acids. J. Mol. Biol. 232:1993;1141-1156.
40. 15N labelled RNAs for heteronuclear multi-dimensional NMR studies. Nucl. Acids Res. 20:1992;4507-4513.
41. Otwinowski Z., Schevitz R. W., Zhang R. G., Lawson C. L., Joachimiak A., Marmorstein R. Q., Luisi B. F., Sigler P. B. Crystal structure of trp repressor/operator complex at atomic resolution. Nature. 335:1988;321-329.
42. Pardi A. Multidimensional heteronuclear NMR experiments for structure determination of isotopically labeled RNA. Methods Enzymol. 261:1995;350-380.
43. Pavletich N. P., Pabo C. O. Zinc finger-DNA recognition: crystal structure of a Zif268-DNA complex at 2.1 Å Science. 252:1991;809-817.
44. 1H-NMR studies of the high-affinity rev binding-site of the rev responsive element of HIV-1 messenger-RNA: base pairing in the core binding-element. Biochemistry. 33:1994;5357-5366.
45. Philpott C. C., Haile D., Rouault T. A., Klausner R. D. Modification of a free Fe-S cluster cysteine residue in the active iron-responsive element-binding protein prevents RNA binding. J. Biol. Chem. 268:1993;17655-17658.
46. Philpott C. C., Klausner R. D., Rouault T. A. The bifunctional iron-responsive element binding protein/cytosolic aconitase: the role of active-site residues in ligand binding and regulation. Proc. Natl Acad. Sci. USA. 91:1994;7321-7325.
47. Piotto M., Saudek V., Sklenar V. Gradient-tailored excitation for single-quantum NMR-spectroscopy of aqueous-solutions. J. Biomol. NMR. 2:1992;661-665.
48. Puglisi J. D., Chen L., Frankel A. D., Williamson J. R. Role of RNA structure in arginine recognition of TAR RNA. Proc. Natl Acad. Sci. USA. 90:1993;3680-3684.
49. 1H NMR spectra of proteins via double quantum filtering. Biochem. Biophys. Res. Commun. 117:1983;479-485.
50. Robbins A. H., Stout C. D. Structure of activated aconitase: formation of the [4Fe-4S] cluster in the crystal. Proc. Natl Acad. Sci. USA. 86:1989;3639-3643.
51. Rouault T. A., Stout C. D., Kaptain S., Harford J. B., Klausner R. D. Structural relationship between an iron-regulated RNA-binding protein (IRE-BP) and aconitase: functional implications. Cell. 64:1991;881-883.
52. Rouault T. A., Haile D. J., Downey W. E., Philpott C. C., Tang C., Samaniego F., Chin J., Paul I., Orloff D., Harford J. B. et al. An iron-sulfur cluster plays a novel regulatory role in the iron-responsive element binding protein. Biometals. 5:1992;131-140.
53. Saenger W. Principles of Nucleic Acid Structure. 1984;Springer-Verlag, New York.
54. Samaniego F., Chin J., Iwai K., Rouault T. A., Klausner R. D. Molecular characterization of a second iron-responsive element binding protein, iron regulatory protein 2. Structure, function, and post-translational regulation. J. Biol. Chem. 269:1994;30904-30910.
55. Schalinkse K. L., Anderson S. L., Tuazon P. T., Chen O. S., Kennedy M. C., Eisenstein R. S. The iron-sulfur cluster of iron regulatory protein 1 modulates the accessibility of RNA binding and phosphorylation sites. Biochemistry. 36:1997;3950-3958.
56. 13C-labeled oligonucleotides. J. Biomol. NMR. 4:1994;631-644.
57. Sierzputowska-Gracz H., McKenzie R. A., Theil E. C. The importance of a single G in the hairpin loop of the iron responsive element (IRE) in ferritin mRNA for structure: an NMR spectroscopy study. Nucl. Acids Res. 23:1995;146-153.
58. Simorre J.-P., Zimmermann G. R., Pardi A., Farmer B. T. I. I., Mueller L. Triple resonance HNNCCH experiments for correlating exchangeable and nonexchangeable cytidine and uridine base protons in RNA. J. Biomol. NMR. 6:1995;427-432.
59. 15N-labeled RNA. J. Am. Chem. Soc. 118:1996a;5316-5317.
60. 15N-labeled RNA with an HNC-TOCSY-CH experiment. J. Biomol. NMR. 7:1996b;153-156.
61. Sklenár V., Bax A. Spin-echo water suppression for the generation of pure-phase two-dimensional NMR spectra. J. Magn. Reson. 74:1987;469-479.
62. Swenson G. R., Walden W. E. Localization of an RNA-binding element of the iron-responsive element-binding protein within a proteolytic fragment containing iron coordination ligands. Nucl. Acids Res. 22:1994;2627-2633.
63. Theil E. C. Iron regulatory elements (IREs): a family of mRNA non-coding sequences. Biochem. J. 304:1994;1-11.
64. Varani, Tinoco. RNA structure and NMR spectroscopy. Quart. Rev. Biophys. 24:1991;479-532.
65. Valegard K., Murray J. B., Stockley P. G., Stonehouse N. J., Liljas L. Crystal structure of a bacteriophage-RNA coat protein-operator complex. Nature. 371:1994;623-626.
66. Wang Y. H., Sczekan S. R., Theil E. C. Structure of the 5′ untranslated regulatory region of ferritin mRNA studied in solution. Nucl. Acids Res. 18:1990;4463-4468.
67. Wang Y. H., Lin P. N., Sczekan S. R., McKenzie R. A., Theil E. C. Ferritin mRNA probed, near the iron regulatory region, with protein and chemical (1,10-phenanthroline-Cu) nucleases. A possible role for base-paired flanking regions. Biol. Met. 4:1991;56-61.
68. Wüthrich K. NMR of Proteins and Nucleic Acids. 1986;John Wiley & Sons, New York.
69. αcarbons. J. Am. Chem. Soc. 116:1994;8266-8278.
70. Zheng L., Kennedy M. C., Beinrt H., Zalkin H. Mutational analysis of active-site residues in pig-heart aconitase. J. Biol. Chem. 267:1992;7895-7903.
71. Zimmermann G. R., Jenison R. D., Wick C. L., Simorre J.-P., Pardi A. Interlocking structural motifs mediate molecular discrimination by a theophylline-binding RNA. Nature-Struct. Biol. 4:1997;644-649.