Identification of RNA-binding surfaces in iron regulatory protein-1

EMBO Journal

Volumn 18, Issue 21, 1999, Pages 6073-6083

  Kaldy, Pierre ^a   Menotti, Eric ^a   Moret, Rémy ^a   Kühn, Lukas C ^a  

^a SWISS INST FOR EXP CANCER RESEARCH   (Switzerland)

Author keywords

Iron regulatory protein; Iron responsive element; Mutagenesis; Post transcription regulation; RNA protein interaction

Indexed keywords

ACONITATE HYDRATASE; HYBRID PROTEIN; IRON REGULATORY FACTOR; MESSENGER RNA; MITOCHONDRIAL ENZYME; MUTANT PROTEIN; RNA BINDING PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; BINDING AFFINITY; BINDING SITE; CONTROLLED STUDY; ESCHERICHIA COLI; HUMAN; PRIORITY JOURNAL; PROTEIN RNA BINDING; SCATCHARD PLOT; STRUCTURE ACTIVITY RELATION;

ACONITATE HYDRATASE; AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; ESCHERICHIA COLI; FERRITINS; HUMANS; IRON REGULATORY PROTEIN 1; IRON REGULATORY PROTEIN 2; IRON-REGULATORY PROTEINS; IRON-SULFUR PROTEINS; MITOCHONDRIA; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTAGENESIS; MUTATION; PROTEIN BINDING; PROTEIN CONFORMATION; PROTO-ONCOGENE PROTEINS; RECOMBINANT FUSION PROTEINS; RNA, MESSENGER; RNA-BINDING PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; SWINE; WNT2 PROTEIN;

ESCHERICHIA COLI; SUIDAE;

EID: 0033230590     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/18.21.6073     Document Type: Article

References (58)

1. Addess, K.J., Basilion, J.P., Klausner, R.D., Rouault, T.A. and Pardi, A. (1997) Structure and dynamics of the iron responsive element RNA: implications for binding of the RNA by iron regulatory binding proteins. J. Mol. Biol., 274, 72-83.
2. Basilion, J.P., Kennedy, M.C., Beinert, H., Massinople, C.M., Klausner, R.D. and Rouault, T.A. (1994a) Overexpression of iron-responsive element-binding protein and its analytical characterization as the RNA-binding form, devoid of an iron-sulfur cluster. Arch. Biochem. Biophys., 311, 517-522.
3. Basilion, J.P., Rouault, T.A., Massinople, C.M., Klausner, R.D. and Burgess, W.H. (1994b) The iron-responsive element-binding protein: localization of the RNA-binding site to the aconitase active-site cleft. Proc. Natl Acad. Sci. USA, 91, 574-578.
4. Beinert, H., Kennedy, M.C. and Stout, C.D. (1996) Aconitase as iron-sulfur protein, enzyme and iron-regulatory protein. Chem. Rev., 96, 2335-2373.
5. Binder, R., Horowitz, J.A., Basilion, J.P., Koeller, D.M., Klausner, R.D. and Harford, J.B. (1994) Evidence that the pathway of transferrin receptor mRNA degradation involves an endonucleolytic cleavage within the 3′ UTR and does not involve poly(A) tail shortening. EMBO J., 13, 1969-1980.
6. Biou, V., Yaremchuk, A., Tukalo, M. and Cusack, S. (1994) The 2.9 Å crystal structure of T. thermophilus seryl-tRNA synthetase complexed with tRNASer. Science, 263, 1404-1410.
7. Burd, C.G. and Dreyfuss, G. (1994) Conserved structures and diversity of functions of RNA-binding proteins. Science, 265, 615-621.
8. Bycroft, M., Grünert, S., Murzin, A.G., Proctor, M. and St Johnston, D. (1995) NMR solution structure of a dsRNA binding domain from Drosophila staufen protein reveals homology to the N-terminal domain of ribosomal protein S5. EMBO J., 14, 3563-3571.
9. Casey, J.L., Hentze, M.W., Koeller, D.M., Caughman, S.W., Rouault, T.A., Klausner, R.D. and Harford, J.B. (1988) Iron-responsive elements: regulatory RNA sequences that control mRNA levels and translation. Science, 240, 924-928.
10. Drapier, J.-C. and Hibbs, J.B., Jr (1986) Murine cytotoxic activated macrophages inhibit aconitase in tumor cells. Inhibition involves the iron-sulfur prosthetic group and is reversible. J. Clin. Invest., 78, 790-797.
11. Emery-Goodman, A., Hirling, H., Scarpellino, L., Henderson, B. and Kühn, L.C. (1993) Iron regulatory factor expressed from recombinant baculovirus: conversion between the RNA-binding apoprotein and Fe-S cluster containing aconitase. Nucleic Acids Res., 21, 1457-1461.
12. Frishman, D. and Hentze, M.W. (1996) Conservation of aconitase residues revealed by multiple sequence analysis. Implications for structure/function relationships. Eur. J. Biochem., 239, 197-200.
13. Gdaniec, Z., Sierzputowska-Gracz, H. and Theil, E.C. (1998) Iron regulatory element and internal loop/bulge structure for ferritin mRNA studied by cobalt (III) hexammine binding, molecular modeling and NMR spectroscopy. Biochemistry, 37, 1505-1512.
14. Gray, N.K., Quick, S., Goossen, B., Constable, A., Hirling, H., Kühn, L.C. and Hentze, M.W. (1993) Recombinant iron regulatory factor functions as an iron-responsive-element-binding protein, a translational repressor and an aconitase. A functional assay for translational repression and direct demonstration of the iron switch. Eur. J. Biochem., 218, 657-667.
15. Guo, B., Yu, Y. and Leibold, E.A. (1994) Iron regulates cytoplasmic levels of a novel iron-responsive element-binding protein without aconitase activity. J. Biol. Chem., 269, 24252-24260.
16. Guo, B., Brown, F.M., Phillips, J.D., Yu, Y. and Leibold, E.A. (1995) Characterization and expression of iron regulatory protein 2 (IRP2). Presence of multiple IRP2 transcripts regulated by intracellular iron levels. J. Biol. Chem., 270, 16529-16535.
17. Haile, D.J., Rouault, T.A., Tang, C.K., Chin, J., Harford, J.B. and Klausner, R.D. (1992) Reciprocal control of RNA-binding and aconitase activity in the regulation of the iron-responsive element binding protein: role of the iron-sulfur cluster. Proc. Natl Acad. Sci. USA, 89, 7536-7540.
18. Henderson, B.R., Seiser, C. and Kühn, L.C. (1993) Characterization of a second RNA-binding protein in rodents with specificity for iron-responsive elements. J. Biol. Chem., 268, 27327-27334.
19. Henderson, B.R., Menotti, E., Bonnard, C. and Kühn, L.C. (1994) Optimal sequence and structure of iron-responsive elements. Selection of RNA stem-loops with high affinity for iron regulatory factor. J. Biol. Chem., 269, 17481-17489.
20. Henderson, B.R., Menotti, E. and Kühn, L.C. (1996) Iron regulatory proteins 1 and 2 bind distinct sets of RNA target sequences. J. Biol. Chem., 271, 4900-4908.
21. Hentze, M.W. and Kühn, L.C. (1996) Molecular control of vertebrate iron metabolism - mRNA-based regulatory circuits operated by iron, nitric oxide andoxidative stress. Proc. Natl Acad. Sci. USA, 93, 8175-8182.
22. Hentze, M.W., Rouault, T.A., Harford, J.B. and Klausner, R.D. (1989) Oxidation-reduction and the molecular mechanism of a regulatory RNA-protein interaction. Science, 244, 357-359.
23. Hirling, H., Emery-Goodman, A., Thompson, N., Neupert, B., Seiser, C. and Kühn, L.C. (1992) Expression of active iron regulatory factor from a full-length human cDNA by in vitro transcription/translation. Nucleic Acids Res., 20, 33-39.
24. Hirling, H., Henderson, B.R. and Kühn, L.C. (1994) Mutational analysis of the [4Fe-4S]-cluster converting iron regulatory factor from its RNA-binding form to cytoplasmic aconitase. EMBO J., 13, 453-461.
25. Kenan, D.J., Query, C.C. and Keene, J.D. (1991) RNA recognition: towards identifying determinants of specificity. Trends Biochem. Sci., 16, 214-220.
26. Kennedy, M.C, Mende-Mueller, L., Blondin, G.A. and Beinert, H. (1992) 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, 11730-11734.
27. Klausner, R.D., Rouault, T.A. and Harford, J.B. (1993) Regulating the fate of mRNA: The control of cellular iron metabolism. Cell, 72, 19-28.
28. Koeller, D.M., Casey, J.L., Hentze, M.W., Gerhardt, E.M., Chan, L.-N., Klausner, R.D. and Harford, J.B. (1989) A cytosolic protein binds to structural elements within the iron regulatory region of the transferrin receptor mRNA. Proc. Natl Acad. Sci. USA, 86, 3574-3578.
29. Kunkel, T.A., Roberts, J.D. and Zakour, R.A. (1987) Rapid and efficient site-specific mutagenesis without phenotypic selection. Methods Enzymol., 154, 367-382.
30. Laing, L.G. and Hall, K.B. (1996) A model of the iron responsive element RNA hairpin loop structure determined from NMR and thermodynamic data. Biochemistry, 35, 13586-13596.
31. Leibold, E.A. and Munro, H.N. (1988) Cytoplasmic protein binds in vitro to a highly conserved sequence in the 5′ untranslated region of ferritin heavy- and light-subunit mRNAs. Proc. Natl Acad. Sci. USA, 85, 2171-2175.
32. Müllner, E.W. and Kühn, L.C. (1988) A stem-loop in the 3′ untranslated region mediates iron-dependent regulation of transferrin receptor mRNA stability in the cytoplasm. Cell, 53, 815-825.
33. Müllner, E.W., Neupert, B. and Kühn, L.C. (1989) A specific mRNA-binding factor regulates the iron-dependent stability of cytoplasmic transferrin receptor mRNA. Cell. 58, 373-382.
34. Musco, G., Stier, G., Joseph, C., Castiglione Morelli, M.A., Nilges, M., Gibson, T.J. and Pastore, A. (1996) Three-dimensional structure and stability of the KH domain: molecular insights into the fragile X syndrome. Cell, 85, 237-245.
35. Nagai, K. (1996) RNA-protein complexes. Curr. Opin. Struct. Biol., 6, 53-61.
36. Neupert, B., Menotti, E. and Kühn, L.C. (1995) A novel method to identify nucleic acid binding sites in proteins by scanning mutagenesis - application to iron regulatory protein. Nucleic Acids Res., 23, 2579-2583.
37. Oubridge, C., Ito, N., Evans, P.R., Teo, C.H. and Nagai, K. (1994) Crystal structure at 1.92 Å resolution of the RNA-binding domain of the U1A spliceosomal protein complexed with an RNA hairpin. Nature, 372, 432-438.
38. Patino, M.M. and Walden, W.E. (1992) Cloning of a functional cDNA for the rabbit ferritin mRNA repressor protein. Demonstration of a tissue-specific pattern of expression. J. Biol. Chem., 267, 19011-19016.
39. Peyret, P., Perez, P. and Alric, M. (1995) Structure, genomic organization and expression of the Arabidopsis thaliana aconitase gene: plant aconitase shows significant homology with mammalian iron-responsive element-binding protein. J. Biol. Chem., 270, 8131-8137.
40. Philpott, C.C, Rouault, T.A. and Klausner, R.D. (1991) Sequence and expression of the murine iron-responsive element binding protein. Nucleic Acids Res., 19, 6333.
41. Philpott, C.C, Haile, D., Rouault, T.A. and Klausner, R.D. (1993) Modification of a free Fe-S cluster cysteine residue in the active iron-responsive element-binding protein prevents RNA binding. J. Biol. Chem., 268, 17655-17658.
42. Philpott, C.C., Klausner, R.D. and Rouault, T.A. (1994) 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, 7321-7325.
43. Prodromou, C., Artymiuk, P.J. and Guest, J.R. (1992) The aconitase of Escherichia coli. Nucleotide sequence of the aconitase gene and amino acid sequence similarity with mitochondrial aconitases, the iron-responsive-element-binding protein and isopropylmalate isomerases. Eur. J. Biochem., 204, 599-609.
44. Robbins, A.H. and Stout, C.D. (1989) The structure of aconitase. Proteins, 5, 289-312.
45. Rothenberger, S., Müllner, E.W. and Kühn, L.C. (1990) The mRNA-binding protein which controls ferritin and transferrin receptor expression is conserved during evolution. Nucleic Acids Res., 18, 1175-1179.
46. Rouault, T.A., Tang, C.K., Kaptain, S., Burgess, W.H., Haile, D.J., Samaniego, F., McBride, O.W., Harford, J.B. and Klausner, R.D. (1990) Cloning of the cDNA encoding an RNA regulatory protein: the human iron-responsive element-binding protein. Proc. Natl Acad. Sci. USA, 87, 7958-7962.
47. Rouault, T.A., Stout, C.D., Kaptain, S., Harford, J.B. and Klausner, R.D. (1991) Structural relationship between an iron-regulated RNA-binding protein (IRE-BP) and aconitase: functional implications. Cell, 64, 881-883.
48. Rouault, T.A. et al. (1992) An iron-sulfur cluster plays a novel regulatory role in the iron-responsive element binding protein. BioMetals, 5, 131-140.
49. Samaniego, F., Chin, J., Iwai, K., Rouault, T.A. and Klausner, R.D. (1994) Molecular characterization of a second iron-responsive element binding protein, iron regulatory protein 2: structure, function and post-translational regulations. J. Biol. Chem., 269, 30904-30910.
50. Sanger, F., Nicklen, S. and Coulson, A.R. (1977) DNA sequencing with chain-terminating inhibitors. Proc. Natl Acad. Sci. USA, 74, 5463-5467.
51. Schalinske, K.L., Anderson, S.A., Tuazon, P.T., Chen, O.S., Kennedy, M.C. and Eisenstein, R.S. (1997) The iron-sulfur cluster of iron regulatory protein 1 modulates the accessibility of RNA binding and phosphorylation sites. Biochemistry, 36, 3950-3958.
52. Schlegl, J., Gegout, V., Schlager, B., Hentze, M.W., Westhof, E., Ehresmann, C., Ehresmann, B. and Romby, P. (1997) Probing the structure of the regulatory region of human transferrin receptor messenger RNA and its interaction with iron regulatory protein-1. RNA, 3, 1159-1172.
53. Siomi, H., Choi, M., Siomi, M.C., Nussbaum, R.L. and Dreyfuss, G. (1994) Essential role for KH domains in RNA binding: impaired RNA binding by a mutation in the KH domain of FMR1 that causes fragile X syndrome. Cell, 77, 33-39.
54. Smith, D.B. and Johnson, K.S. (1988) Single-step purification of polypeptides expressed in Escherichia coli as fusions with glutathione S-transferase. Gene, 67, 31-40.
55. Uhlenbeck, O.C., Pardi, A. and Feigon, J. (1997) RNA structure comes of age. Cell, 90, 833-840.
56. Valegard, K., Murray, J.B., Stockley, P.G., Stonehouse, N.J. and Liljas, L. (1994) Crystal structure of an RNA bacteriophage coat protein-operator complex. Nature, 371, 623-626.
57. Yu, Y., Radisky, E. and Leibold, E.A. (1992) The iron-responsive element binding protein. Purification, cloning and regulation in rat liver. J. Biol. Chem., 267, 19005-19010.
58. Zheng, L., Andrews, P.C, Hermodson, M.A., Dixon, J.E. and Zalkin, H. (1990) Cloning and structural characterization of porcine heart aconitase. J. Biol. Chem., 265, 2814-2821.