Analyzing ATP Utilization by DEAD-Box RNA Helicases Using Kinetic and Equilibrium Methods

Abdelhaleem, 2004, Do human RNA helicases have a role in cancer?, Biochim. Biophys. Acta, 1704, 37 Akao, 2009, A role of DEAD-Box RNA helicase rck/p54 in cancer cells, Curr. Drug Ther., 4, 29, 10.2174/157488509787081912 Antao, 1991, A thermodynamic study of unusually stable RNA and DNA hairpins, Nucleic Acids Res., 19, 5901, 10.1093/nar/19.21.5901 Attri, 2005, Composition gradient static light scattering: A new technique for rapid detection and quantitative characterization of reversible macromolecular hetero-associations in solution, Anal. Biochem., 346, 132, 10.1016/j.ab.2005.08.013 Barshop, 1983, Analysis of numerical methods for computer simulation of kinetic processes: Development of KINSIM—A flexible, portable system, Anal. Biochem., 130, 134, 10.1016/0003-2697(83)90660-7 Bizebard, 2004, Studies on three E. coli DEAD-box helicases point to an unwinding mechanism different from that of model DNA helicases, Biochemistry, 43, 7857, 10.1021/bi049852s Brune, 1994, Direct, real-time measurement of rapid inorganic phosphate release using a novel fluorescent probe and its application to actomyosin subfragment 1 ATPase, Biochemistry, 33, 8262, 10.1021/bi00193a013 Brune, 1998, Mechanism of inorganic phosphate interaction with phosphate binding protein from Escherichia coli, Biochemistry, 37, 10370, 10.1021/bi9804277 Bujalowski, 2011, Macromolecular competition titration method: Accessing thermodynamics of the unmodified macromolecule-ligand interactions through spectroscopic titrations of fluorescent analogs, Methods Enzymol., 488, 17, 10.1016/B978-0-12-381268-1.00002-1 Cao, 2011, Mechanism of Mss116 ATPase reveals functional diversity of DEAD-box proteins, J. Mol. Biol., 409, 399, 10.1016/j.jmb.2011.04.004 Chao, 2006, DDX3, a DEAD box RNA helicase with tumor growth-suppressive property and transcriptional regulation activity of the p21waf1/cip1 promoter, is a candidate tumor suppressor, Cancer Res., 66, 6579, 10.1158/0008-5472.CAN-05-2415 Charter, 2006, A generic, homogenous method for measuring kinase and inhibitor activity via adenosine 5′-diphosphate accumulation, J. Biomol. Screen., 11, 390, 10.1177/1087057106286829 Chen, 2008, DEAD-box proteins can completely separate an RNA duplex using a single ATP, Proc. Natl. Acad. Sci. U. S. A., 105, 20203, 10.1073/pnas.0811075106 Collins, 2009, The DEXD/H-box RNA helicase DDX19 is regulated by an alpha-helical switch, J. Biol. Chem., 284, 10296, 10.1074/jbc.C900018200 Cordin, 2006, The DEAD-box protein family of RNA helicases, Gene, 367, 17, 10.1016/j.gene.2005.10.019 Cornish-Bowden, 2004 De La Cruz, 2009, Kinetic and equilibrium analysis of the myosin ATPase, Methods Enzymol., 455, 157, 10.1016/S0076-6879(08)04206-7 De La Cruz, 1994, Transient kinetic analysis of rhodamine phalloidin binding to actin filaments, Biochemistry, 33, 14387, 10.1021/bi00252a003 De La Cruz, 1995, Nucleotide-free actin: Stabilization by sucrose and nucleotide binding kinetics, Biochemistry, 34, 5452, 10.1021/bi00016a016 De La Cruz, 1996, Kinetics and thermodynamics of phalloidin binding to actin filaments from three divergent species, Biochemistry, 35, 14054, 10.1021/bi961047t De La Cruz, 2000, ADP inhibition of myosin V ATPase activity, Biophys. J., 79, 1524, 10.1016/S0006-3495(00)76403-4 Del Campo, 2009, Structure of the Yeast DEAD box protein Mss116p reveals two wedges that crimp RNA, Mol. Cell, 35, 598, 10.1016/j.molcel.2009.07.032 Diges, 2001, Escherichia coli DbpA is an RNA helicase that requires hairpin 92 of 23S rRNA, EMBO J., 20, 5503, 10.1093/emboj/20.19.5503 Ding, 2004, Sfold web server for statistical folding and rational design of nucleic acids, Nucleic Acids Res., 32, W135, 10.1093/nar/gkh449 Doma, 2007, RNA quality control in eukaryotes, Cell, 131, 660, 10.1016/j.cell.2007.10.041 Furch, 1998, Modulation of actin affinity and actomyosin adenosine triphosphatase by charge changes in the myosin motor domain, Biochemistry, 37, 6317, 10.1021/bi972851y Godbout, 2007, Role of DEAD box 1 in retinoblastoma and neuroblastoma, Future Oncol., 3, 575, 10.2217/14796694.3.5.575 Grimsley, 2003, Spectrophotometric determination of protein concentration, Curr. Protoc. Protein Sci., 33, 3.1.1, 10.1002/0471140864.ps0301s33 Gutfreund, 1995 Hackney, 2012, Oxygen isotopic exchange probes of ATP hydrolysis by RNA helicases, Methods Enzymol., 511, 65, 10.1016/B978-0-12-396546-2.00003-6 Henn, 2005, Vertebrate myosin VIIb is a high duty ratio motor adapted for generating and maintaining tension, J. Biol. Chem., 280, 39665, 10.1074/jbc.M507667200 Henn, 2001, Visualization of unwinding activity of duplex RNA by DbpA, a DEAD box helicase, at single-molecule resolution by atomic force microscopy, Proc. Natl. Acad. Sci. U. S. A., 98, 5007, 10.1073/pnas.071372498 Henn, 2008, The ATPase cycle mechanism of the DEAD-box rRNA helicase, DbpA, J. Mol. Biol., 377, 193, 10.1016/j.jmb.2007.12.046 Henn, 2010, Pathway of ATP utilization and duplex rRNA unwinding by the DEAD-box helicase, DbpA, Proc. Natl. Acad. Sci. U. S. A., 107, 4046, 10.1073/pnas.0913081107 Henn, 2012, ATP utilization and RNA conformational rearrangement by DEAD-box proteins, Annu. Rev. Biophys., 41, 11.1, 10.1146/annurev-biophys-050511-102243 Herschlag, 1995, RNA chaperones and the RNA folding problem, J. Biol. Chem., 270, 20871, 10.1074/jbc.270.36.20871 Hilbert, 2009, The mechanism of ATP-dependent RNA unwinding by DEAD box proteins, Biol. Chem., 390, 1237, 10.1515/BC.2009.135 Hiratsuka, 1983, New ribose-modified fluorescent analogs of adenine and guanine nucleotides available as subtrates for various enzymes, Biochim. Biophys. Acta, 742, 496, 10.1016/0167-4838(83)90267-4 Howard, 2001 Iost, 1999, Ded1p, a DEAD-box protein required for translation initiation in Saccharomyces cerevisiae, is an RNA helicase, J. Biol. Chem., 274, 17677, 10.1074/jbc.274.25.17677 Jarmoskaite, 2011, DEAD box proteins as RNA helicases and chaperones, WIREs: RNA, 2, 135, 10.1002/wrna.50 Jezewska, 2005, Binding of six nucleotide cofactors to the hexameric helicase RepA protein of plasmid RSF1010. 1. Direct evidence of cooperative interactions between the nucleotide-binding sites of a hexameric helicase, Biochemistry, 44, 3865, 10.1021/bi048037+ Johnson, 1986, Rapid kinetic analysis of mechanochemical adenosinetriphosphatases, Methods Enzymol., 134, 677, 10.1016/0076-6879(86)34129-6 Johnson, 1992, Transient-state kinetic analysis of enzyme reaction pathways, 1, 10.1016/S1874-6047(08)60019-0 Johnson, 1995, Rapid quench kinetic analysis of polymerases, adenosinetriphosphatases, and enzyme intermediates, Methods Enzymol., 249, 38, 10.1016/0076-6879(95)49030-2 Johnson, 2003, Introduction to kinetic analysis of enzyme systems, 1 Johnson, 2009, Fitting enzyme kinetic data with KinTek Global Kinetic Explorer, Methods Enzymol., 467, 601, 10.1016/S0076-6879(09)67023-3 Johnson, 2009, FitSpace Explorer: An algorithm to evaluate multidimensional parameter space in fitting kinetic data, Anal. Biochem., 387, 30, 10.1016/j.ab.2008.12.025 Johnson, 2009, Global Kinetic Explorer: A new computer program for dynamic simulation and fitting of kinetic data, Anal. Biochem., 387, 20, 10.1016/j.ab.2008.12.024 Klostermeier, 2009, A novel dimerization motif in the C-terminal domain of the Thermus thermophilus DEAD box helicase Hera confers substantial flexibility, Nucleic Acids Res., 37, 421, 10.1093/nar/gkn947 Kossen, 2002, The carboxy-terminal domain of the DExDH protein YxiN is sufficient to confer specificity for 23S rRNA, J. Mol. Biol., 324, 625, 10.1016/S0022-2836(02)01140-3 Lakowicz, 2006 Le Hir, 2008, Structural insights into the exon junction complex, Curr. Opin. Struct. Biol., 18, 112, 10.1016/j.sbi.2007.11.002 Lebowitz, 2002, Modern analytical ultracentrifugation in protein science: A tutorial review, Protein Sci., 11, 2067, 10.1110/ps.0207702 Linder, 2011, From unwinding to clamping—The DEAD box RNA helicase family, Nat. Rev. Mol. Cell Biol., 12, 505, 10.1038/nrm3154 Liu, 2008, ATP hydrolysis is required for DEAD-box protein recycling but not for duplex unwinding, Proc. Natl. Acad. Sci. U. S. A., 105, 20209, 10.1073/pnas.0811115106 Lohman, 2008, Non-hexameric DNA helicases and translocases: Mechanisms and regulation, Nat. Rev. Mol. Cell Biol., 9, 391, 10.1038/nrm2394 Lorsch, 1998, The DEAD box protein eIF4A. 1. A minimal kinetic and thermodynamic framework reveals coupled binding of RNA and nucleotide, Biochemistry, 37, 2180, 10.1021/bi972430g Lucius, 2006, The Escherichia coli PriA helicase has two nucleotide-binding sites differing dramatically in their affinities for nucleotide cofactors. 1. Intrinsic affinities, cooperativities, and base specificity of nucleotide cofactor binding, Biochemistry, 45, 7202, 10.1021/bi051826m Mallam, 2011, Solution structures of DEAD-box RNA chaperones reveal conformational changes and nucleic acid tethering by a basic tail, Proc. Natl. Acad. Sci. U. S. A., 108, 12254, 10.1073/pnas.1109566108 Marintchev, 2009, Topology and regulation of the human eIF4A/4G/4H helicase complex in translation initiation, Cell, 136, 447, 10.1016/j.cell.2009.01.014 Montpetit, 2011, A conserved mechanism of DEAD-box ATPase activation by nucleoporins and InsP6 in mRNA export, Nature, 472, 238, 10.1038/nature09862 Murphy, 1997, Static and dynamic light scattering of biological macromolecules: What can we learn?, Curr. Opin. Biotechnol., 8, 25, 10.1016/S0958-1669(97)80153-X Pan, 2010, Roles of DEAD-box proteins in RNA and RNP Folding, RNA Biol., 7, 667, 10.4161/rna.7.6.13571 Polach, 2002, Cooperative binding of ATP and RNA substrates to the DEAD/H protein DbpA, Biochemistry, 41, 3693, 10.1021/bi012062n Pyle, 2008, Translocation and unwinding mechanisms of RNA and DNA helicases, Annu. Rev. Biophys., 37, 317, 10.1146/annurev.biophys.37.032807.125908 Ramasawmy, 2006, BAT1, a putative anti-inflammatory gene, is associated with chronic Chagas cardiomyopathy, J. Infect. Dis., 193, 1394, 10.1086/503368 Reuter, 2010, RNAstructure: Software for RNA secondary structure prediction and analysis, BMC Bioinformatics, 11, 129, 10.1186/1471-2105-11-129 Robblee, 2005, Thermodynamics of nucleotide binding to actomyosin V and VI: A positive heat capacity change accompanies strong ADP binding, Biochemistry, 44, 10238, 10.1021/bi050232g Rogers, 1999, Biochemical and kinetic characterization of the RNA helicase activity of eukaryotic initiation factor 4A, J. Biol. Chem., 274, 12236, 10.1074/jbc.274.18.12236 Rogers, 2001, Modulation of the helicase activity of eIF4A by eIF4B, eIF4H, and eIF4F, J. Biol. Chem., 19, 30914, 10.1074/jbc.M100157200 Sahni, 2010, UAP56 is an important regulator of protein synthesis and growth in cardiomyocytes, Biochem. Biophys. Res. Commun., 393, 106, 10.1016/j.bbrc.2010.01.093 Schroeder, 2004, Strategies for RNA folding and assembly, Nat. Rev. Mol. Cell Biol., 5, 908, 10.1038/nrm1497 Sengoku, 2006, Structural basis for RNA unwinding by the DEAD-box protein Drosophila Vasa, Cell, 125, 287, 10.1016/j.cell.2006.01.054 Seol, 2004, Elastic properties of a single-stranded charged homopolymeric ribonucleotide, Phys. Rev. Lett., 93, 118102, 10.1103/PhysRevLett.93.118102 Seol, 2007, Stretching of homopolymeric RNA reveals single-stranded helices and base-stacking, Phys. Rev. Lett., 98, 158103, 10.1103/PhysRevLett.98.158103 Talavera, 2005, Equilibrium and kinetic analysis of nucleotide binding to the DEAD-box RNA helicase DbpA, Biochemistry, 44, 959, 10.1021/bi048253i Talavera, 2006, Hydrodynamic characterization of the DEAD-box RNA helicase DbpA, J. Mol. Biol., 355, 697, 10.1016/j.jmb.2005.10.058 Thomä, 2003, What to do if there is no signal: Using competition experiments to determine binding parameters, 153 Tsu, 1998, Kinetic analysis of the RNA-dependent adenosinetriphosphatase activity of DbpA, an Escherichia coli DEAD protein specific for 23S ribosomal RNA, Biochemistry, 37, 16989, 10.1021/bi981837y Tsu, 2001, The Escherichia coli DEAD protein DbpA recognizes a small RNA hairpin in 23S rRNA, RNA, 7, 702, 10.1017/S1355838201010135 Wang, 2006, The domain of the Bacillus subtilis DEAD-box helicase YxiN that is responsible for specific binding of 23S rRNA has an RNA recognition motif fold, RNA, 12, 959, 10.1261/rna.5906 Webb, 2003, A fluorescent sensor to assay inorganic phosphate, 131 Weirich, 2006, Activation of the DExD/H-box protein Dbp5 by the nuclear-pore protein Gle1 and its coactivator InsP6 is required for mRNA export, Nat. Cell Biol., 8, 668, 10.1038/ncb1424 Woodson, 2010, Taming free energy landscapes with RNA chaperones, RNA Biol., 7, 677, 10.4161/rna.7.6.13615 Wyman, 1990 Yang, 2006, The DEAD-box protein Ded1 unwinds RNA duplexes by a mode distinct from translocating helicases, Nat. Struct. Mol. Biol., 13, 981, 10.1038/nsmb1165 Zimmerle, 1989, Analysis of progress curves by simulations generated by numerical integration, Biochem. J., 258, 381, 10.1042/bj2580381