Rapid kinetics of iron responsive element (IRE) RNA/iron regulatory protein 1 and IRE-RNA/eIF4F complexes respond differently to metal ions

Nucleic Acids Research

Volumn 42, Issue 10, 2014, Pages 6567-6577

  Khan, Mateen A ^a   Ma, Jia ^a   Walden, William E ^b   Merrick, William C ^c   Theil, Elizabeth C ^d,e   Goss, Dixie J ^a  

^a CITY UNIVERSITY OF NEW YORK   (United States)

^b UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^c CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d Childeren's Hospital Oakland Research Institute   (United States)

^e NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACONITATE HYDRATASE; FERRITIN; INITIATION FACTOR 4F; IRON REGULATORY PROTEIN 1; MANGANESE; MESSENGER RNA; METAL ION; MITOCHONDRIAL ENZYME; POTASSIUM ION;

ARTICLE; CHEMICAL REACTION KINETICS; CODON; COMPLEX FORMATION; CONTROLLED STUDY; CRYSTAL STRUCTURE; DISSOCIATION CONSTANT; IONIC STRENGTH; IRON RESPONSIVE ELEMENT; MOLECULAR EVOLUTION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN RNA BINDING; PROTEIN STABILITY; RNA SEQUENCE; SUBSTITUTION REACTION;

ACONITATE HYDRATASE; ANIMALS; EUKARYOTIC INITIATION FACTOR-4F; FERRITINS; IRON; IRON REGULATORY PROTEIN 1; KINETICS; MANGANESE; POTASSIUM; RABBITS; REGULATORY SEQUENCES, RIBONUCLEIC ACID; RNA, MESSENGER;

EID: 84903138875     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku248     Document Type: Article

References (54)

1. 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. U.S.A., 85, 2171-2175.
2. Mullner, E.W., Neupert, B. and Kuhn, L.C. (1989) A specific mRNA binding factor regulates the iron-dependent stability of cytoplasmic transferrin receptor mRNA. Cell, 58, 373-382.
3. Henderson, B.R., Seiser, C. and Kuhn, L.C. (1993) Characterization of a second RNA-binding protein in rodents with specificity for iron-responsive elements. J. Biol. Chem., 268, 27327-27334.
4. 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.
5. 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.
6. Gray, N.K., Pantopoulos, K., Dandekar, T., Ackrell, B.A. and Hentze, M.W. (1996) Translational regulation of mammalian and Drosophila citric acid cycle enzymes via iron-responsive elements. Proc. Natl. Acad. Sci. U.S.A., 93, 4925-4930.
7. Dandekar, T., Stripecke, R., Gray, N.K., Goossen, B., Constable, A., Johansson, H.E. and Hentze, M.W. (1991) Identification of a novel iron-responsive element in murine and human erythroid delta-aminolevulinic acid synthase mRNA. EMBO J., 10, 1903-1909.
8. Hentze, M.W. and Kuhn, L.C. (1996) Molecular control of vertebrate iron metabolism: mRNA-based regulatory circuits operated by iron, nitric oxide, and oxidative stress. Proc. Natl. Acad. Sci. U.S.A., 93, 8175-8182.
9. Theil, E.C. (1994) Iron regulatory elements (IREs): a family of mRNA non-coding sequences. Biochem. J., 304 (Pt 1), 1-11.
10. Piccinelli, P. and Samuelsson, T. (2007) Evolution of the iron-responsive element. RNA, 13, 952-966.
11. Wallander, M.L., Leibold, E.A. and Eisenstein, R.S. (2006) Molecular control of vertebrate iron homeostasis by iron regulatory proteins. Biochim. Biophys. Acta, 1763, 668-689.
12. Rouault, T.A. (2006) The role of iron regulatory proteins in mammalian iron homeostasis and disease. Nat. Chem. Biol., 2, 406-414.
13. Leipuviene, R. and Theil, E.C. (2007) The family of iron responsive RNA structures regulated by changes in cellular iron and oxygen. Cell. Mol. Life Sci., 64, 2945-2955.
14. Muckenthaler, M.U., Galy, B. and Hentze, M.W. (2008) Systemic iron homeostasis and the iron-responsive element/iron-regulatory protein (IRE/IRP) regulatory network. Annu. Rev. Nutr., 28, 197-213.
15. Goforth, J.B., Anderson, S.A., Nizzi, C.P. and Eisenstein, R.S. (2010) Multiple determinants within iron-responsive elements dictate iron regulatory protein binding and regulatory hierarchy. RNA, 16, 154-169.
16. Ma, J., Haldar, S., Khan, M.A., Sharma, S.D., Merrick, W.C., Theil, E.C. and Goss, D.J. (2012) Fe2+ binds iron responsive element-RNA, selectively changing protein-binding affinities and regulating mRNA repression and activation. Proc. Natl. Acad. Sci. U.S.A., 109, 8417-8422.
17. 2+ sensing by iron-responsive messenger RNA:repressor complexes weakens binding. J. Biol. Chem., 284, 30122-30128.
18. Shenvi, C.L., Dong, K.C., Friedman, E.M., Hanson, J.A. and Cate, J.H. (2005) Accessibility of 18S rRNA in human 40S subunits and 80S ribosomes at physiological magnesium ion concentrations-implications for the study of ribosome dynamics. RNA, 11, 1898-1908.
19. Wang, B., Wilkinson, K.A. and Weeks, K.M. (2008) Complex ligand-induced conformational changes in tRNA(Asp) revealed by single-nucleotide resolution SHAPE chemistry. Biochemistry, 47, 3454-3461.
20. Oshikane, H., Sheppard, K., Fukai, S., Nakamura, Y., Ishitani, R., Numata, T., Sherrer, R.L., Feng, L., Schmitt, E., Panvert, M. et al. (2006) Structural basis of RNA-dependent recruitment of glutamine to the genetic code. Science, 312, 1950-1954.
21. Koculi, E., Thirumalai, D. and Woodson, S.A. (2006) Counterion charge density determines the position and plasticity of RNA folding transition states. J. Mol. Biol., 359, 446-454.
22. Vicens, Q., Paukstelis, P.J., Westhof, E., Lambowitz, A.M. and Cech, T.R. (2008) Toward predicting self-splicing and protein-facilitated splicing of group I introns. RNA, 14, 2013-2029.
23. Nelson, J.A. and Uhlenbeck, O.C. (2008) Hammerhead redux: does the new structure fit the old biochemical data? RNA, 14, 605-615.
24. Adilakshmi, T., Bellur, D.L. and Woodson, S.A. (2008) Concurrent nucleation of 16S folding and induced fit in 30S ribosome assembly. Nature, 455, 1268-1272.
25. Vogt, M., Lahiri, S., Hoogstraten, C.G., Britt, R.D. and DeRose, V.J. (2006) Coordination environment of a site-bound metal ion in the hammerhead ribozyme determined by 15N and 2H ESEEM spectroscopy. J. Am. Chem. Soc., 128, 16764-16770.
26. Brantl, S. (2007) Metal sensing by RNA in bacteria: exception or rule? ACS Chem. Biol., 2, 656-660.
27. Lipfert, J., Das, R., Chu, V.B., Kudaravalli, M., Boyd, N., Herschlag, D. and Doniach, S. (2007) Structural transitions and thermodynamics of a glycine-dependent riboswitch from Vibrio cholerae. J. Mol. Biol., 365, 1393-1406.
28. Coppins, R.L., Hall, K.B. and Groisman, E.A. (2007) The intricate world of riboswitches. Curr. Opin. Microbiol., 10, 176-181.
29. Noeske, J., Schwalbe, H. and Wohnert, J. (2007) Metal-ion binding and metal-ion induced folding of the adenine-sensing riboswitch aptamer domain. Nucleic Acids Res., 35, 5262-5273.
30. Martick, M., Horan, L.H., Noller, H.F. and Scott, W.G. (2008) A discontinuous hammerhead ribozyme embedded in a mammalian messenger RNA. Nature, 454, 899-902.
31. Ke, Y., Sierzputowska-Gracz, H., Gdaniec, Z. and Theil, E.C. (2000) Internal loop/bulge and hairpin loop of the iron-responsive element of ferritin mRNA contribute to maximal iron regulatory protein 2 binding and translational regulation in the iso-iron-responsive element/iso-iron regulatory protein family. Biochemistry, 39, 6235-6242.
32. Walden, W.E., Selezneva, A.I., Dupuy, J., Volbeda, A., Fontecilla-Camps, J.C., Theil, E.C. and Volz, K. (2006) Structure of dual function iron regulatory protein 1 complexed with ferritin IRE-RNA. Science, 314, 1903-1908.
33. Wang, Y.H., Lin, P.N., Sczekan, S.R., McKenzie, R.A. and Theil, E.C. (1991) 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, 56-61.
34. Ciftan, S.A., Theil, E.C. and Thorp, H.H. (1998) Oxidation of guanines in the iron-responsive element RNA: similar structures from chemical modification and recent NMR studies. Chem. Biol., 5, 679-687.
35. Tibodeau, J.D., Fox, P.M., Ropp, P.A., Theil, E.C. and Thorp, H.H. (2006) The up-regulation of ferritin expression using a small-molecule ligand to the native mRNA. Proc. Natl. Acad. Sci. U.S.A., 103, 253-257.
36. 2+ speciation and oxidative stress resistance in yeast cells with electron-nuclear double resonance spectroscopy. Proc. Natl. Acad. Sci. U.S.A., 107, 15335-15339.
37. 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.
38. Harrell, C.M., McKenzie, A.R., Patino, M.M., Walden, W.E. and Theil, E.C. (1991) 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. U.S.A., 88, 4166-4170.
39. Erlitzki, R., Long, J.C. and Theil, E.C. (2002) Multiple, conserved iron-responsive elements in the 3'-untranslated region of transferrin receptor mRNA enhance binding of iron regulatory protein 2. J. Biol. Chem., 277, 42579-42587.
40. Grifo, J.A., Tahara, S.M., Morgan, M.A., Shatkin, A.J. and Merrick, W.C. (1983) New initiation factor activity required for globin mRNA translation. J. Biol. Chem., 258, 5804-5810.
41. Ke, Y., Wu, J., Leibold, E.A., Walden, W.E. and Theil, E.C. (1998) Loops and bulge/loops in iron-responsive element isoforms influence iron regulatory protein binding. Fine-tuning of mRNA regulation? J. Biol. Chem., 273, 23637-23640.
42. Bradford, M.M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem., 72, 248-254.
43. Khan, M.A., Yumak, H. and Goss, D.J. (2009) Kinetic mechanism for the binding of eIF4F and tobacco Etch virus internal ribosome entry site RNA: effects of eIF4B and poly(A)-binding protein. J. Biol. Chem., 284, 35461-35470.
44. 7G cap analogue to wheat germ eIFiso4F and eIFiso4F. PABP. Biochemistry, 44, 4510-4516.
45. Carberry, S.E., Darzynkiewicz, E. and Goss, D.J. (1991) A comparison of the binding of methylated cap analogues to wheat germ protein synthesis initiation factors 4F and (iso)4F. Biochemistry, 30, 1624-1627.
46. Khan, M.A., Miyoshi, H., Ray, S., Natsuaki, T., Suehiro, N. and Goss, D.J. (2006) Interaction of genome-linked protein (VPg) of turnip mosaic virus with wheat germ translation initiation factors eIFiso4E and eIFiso4F. J. Biol. Chem., 281, 28002-28010.
47. Khan, M.A., Miyoshi, H., Gallie, D.R. and Goss, D.J. (2008) Potyvirus genome-linked protein, VPg, directly affects wheat germ in vitro translation: interactions with translation initiation factors eIF4F and eIFiso4F. J. Biol. Chem., 283, 1340-1349.
48. Wickiser, J.K., Cheah, M.T., Breaker, R.R. and Crothers, D.M. (2005) The kinetics of ligand binding by an adenine-sensing riboswitch. Biochemistry, 44, 13404-13414.
49. Gray, N.K. and Hentze, M.W. (1994) Iron regulatory protein prevents binding of the 43S translation pre-initiation complex to ferritin and eALAS mRNAs. EMBO J., 13, 3882-3891.
50. Katsamba, P.S., Myszka, D.G. and Laird-Offringa, I.A. (2001) Two functionally distinct steps mediate high affinity binding of U1A protein to U1 hairpin II RNA. J. Biol. Chem., 276, 21476-21481.
51. Walden, W.E., Selezneva, A. and Volz, K. (2012) Accommodating variety in iron-responsive elements: Crystal structure of transferrin receptor 1 B IRE bound to iron regulatory protein 1. FEBS Lett., 586, 32-35.
52. 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.
53. Breuer, W., Epsztejn, S. and Cabantchik, Z.I. (1995) Iron acquired from transferrin by K562 cells is delivered into a cytoplasmic pool of chelatable iron(II). J. Biol. Chem., 270, 24209-24215.
54. Roth, A. and Breaker, R.R. (2009) The structural and functional diversity of metabolite-binding riboswitches. Annu. Rev. Biochem., 78, 305-334.