The ATPase Cycle Mechanism of the DEAD-box rRNA Helicase, DbpA

Journal of Molecular Biology

Volumn 377, Issue 1, 2008, Pages 193-205

  Henn, Arnon ^a   Cao, Wenxiang ^a   Hackney, David D ^b   De La Cruz, Enrique M ^a  

^a YALE UNIVERSITY   (United States)

^b CARNEGIE MELLON UNIVERSITY   (United States)

Author keywords

ATPase; DEAD box protein; helicase; kinetics; RNA

Indexed keywords

ADENOSINE TRIPHOSPHATASE; DBPA ENYME; DEAD BOX PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; ENZYME ACTIVITY; ENZYME ANALYSIS; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HYDROLYSIS; KINETICS; PRIORITY JOURNAL; RNA BINDING; STEADY STATE;

EID: 39649096274     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2007.12.046     Document Type: Article

References (45)

1. Cordin O., Banroques J., Tanner N.K., and Linder P. The DEAD-box protein family of RNA helicases. Gene 367 (2006) 17-37
2. Henn A., Medalia O., Shi S.P., Steinberg M., Franceschi F., and Sagi I. 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. USA 98 (2001) 5007-5012
3. Mohr S., Matsuura M., Perlman P.S., and Lambowitz A.M. A DEAD-box protein alone promotes group II intron splicing and reverse splicing by acting as an RNA chaperone. Proc. Natl Acad. Sci. USA 103 (2006) 3569-3574
4. Fairman M.E., Maroney P.A., Wang W., Bowers H.A., Gollnick P., Nilsen T.W., and Jankowsky E. Protein displacement by DExH/D "RNA helicases" without duplex unwinding. Science 304 (2004) 730-734
5. Linder P., Lasko P.F., Ashburner M., Leroy P., Nielsen P.J., Nishi K., et al. Birth of the D-E-A-D box. Nature 337 (1989) 121-122
6. Rocak S., and Linder P. DEAD-box proteins: the driving forces behind RNA metabolism. Nat. Rev. Mol. Cell Biol. 5 (2004) 232-241
7. Diges C.M., and Uhlenbeck O.C. Escherichia coli DbpA is an RNA helicase that requires hairpin 92 of 23S rRNA. EMBO J. 20 (2001) 5503-5512
8. Yang Q., and Jankowsky E. The DEAD-box protein Ded1 unwinds RNA duplexes by a mode distinct from translocating helicases. Nat. Struct. Mol. Biol. 13 (2006) 981-986
9. Tijerina P., Bhaskaran H., and Russell R. Nonspecific binding to structured RNA and preferential unwinding of an exposed helix by the CYT-19 protein, a DEAD-box RNA chaperone. Proc. Natl Acad. Sci. USA 103 (2006) 16698-16703
10. Linder P. Dead-box proteins: a family affair-active and passive players in RNP-remodeling. Nucleic Acids Res. 34 (2006) 4168-4180
11. Diges C.M., and Uhlenbeck O.C. Escherichia coli DbpA is a 3′→5′ RNA helicase. Biochemistry 44 (2005) 7903-7911
12. Tsu C.A., and Uhlenbeck O.C. Kinetic analysis of the RNA-dependent adenosinetriphosphatase activity of DbpA, an Escherichia coli DEAD protein specific for 23S ribosomal RNA. Biochemistry 37 (1998) 16989-16996
13. Fuller-Pace F.V., Nicol S.M., Reid A.D., and Lane D.P. DbpA: a DEAD box protein specifically activated by 23S rRNA. EMBO J. 12 (1993) 3619-3626
14. von Hippel P.H., and Delagoutte E. A general model for nucleic acid helicases and their "coupling" within macromolecular machines. Cell 104 (2001) 177-190
15. Lohman T.M., and Bjornson K.P. Mechanisms of helicase-catalyzed DNA unwinding. Annu. Rev. Biochem. 65 (1996) 169-214
16. Tomko E.J., Fischer C.J., Niedziela-Majka A., and Lohman T.M. A nonuniform stepping mechanism for E. coli UvrD monomer translocation along single-stranded DNA. Mol. Cell 26 (2007) 335-347
17. Lorsch J.R., and Herschlag D. The DEAD box protein eIF4A.1. A minimal kinetic and thermodynamic framework reveals coupled binding of RNA and nucleotide. Biochemistry 37 (1998) 2180-2193
18. von Hippel P.H., and Delagoutte E. Macromolecular complexes that unwind nucleic acids. BioEssays 25 (2003) 1168-1177
19. Talavera M.A., Matthews E.E., Eliason W.K., Sagi I., Wang J., Henn A., and De La Cruz E.M. Hydrodynamic characterization of the DEAD-box RNA helicase DbpA. J. Mol. Biol. 355 (2006) 697-707
20. Robblee J.P., Cao W., Henn A., Hannemann D.E., and De La Cruz E.M. Thermodynamics of nucleotide binding to actomyosin V and VI: a positive heat capacity change accompanies strong ADP binding. Biochemistry 44 (2005) 10238-10249
21. Talavera M.A., and De La Cruz E.M. Equilibrium and kinetic analysis of nucleotide binding to the DEAD-box RNA helicase DbpA. Biochemistry 44 (2005) 959-970
22. Polach K.J., and Uhlenbeck O.C. Cooperative binding of ATP and RNA substrates to the DEAD/H protein DbpA. Biochemistry 41 (2002) 3693-3702
23. Hannemann D.E., Cao W., Olivares A.O., Robblee J.P., and De La Cruz E.M. Magnesium, ADP, and actin binding linkage of myosin V: evidence for multiple myosin V-ADP and actomyosin V-ADP states. Biochemistry 44 (2005) 8826-8840
24. Moore K.J., and Lohman T.M. Kinetic mechanism of adenine nucleotide binding to and hydrolysis by the Escherichia coli Rep monomer. 1. Use of fluorescent nucleotide analogues. Biochemistry 33 (1994) 14550-14564
25. Johnson K.A. Rapid kinetic analysis of mechanochemical adenosinetriphosphatases. Methods Enzymol. 134 (1986) 677-705
26. 18O]ATP species formation. Proc. Natl Acad. Sci. USA 76 (1979) 3646-3650
27. Olivares A.O., Chang W., Mooseker M.S., Hackney D.D., and De La Cruz E.M. The tail domain of myosin Va modulates actin binding to one head. J. Biol. Chem. 281 (2006) 31326-31336
28. Hackney D.D., Stempel K.E., and Boyer P.D. Oxygen-18 probes of enzymic reactions of phosphate compounds. Methods Enzymol. 64 (1980) 60-83
29. Wong I., and Lohman T.M. A two-site mechanism for ATP hydrolysis by the asymmetric Rep dimer P2S as revealed by site-specific inhibition with ADP-A1F4. Biochemistry 36 (1997) 3115-3125
30. Yengo C.M., De La Cruz E.M., Safer D., Ostap E.M., and Sweeney H.L. Kinetic characterization of the weak binding states of myosin V. Biochemistry 41 (2002) 8508-8517
31. De La Cruz E.M., Wells A.L., Rosenfeld S.S., Ostap E.M., and Sweeney H.L. The kinetic mechanism of myosin V. Proc. Natl Acad. Sci. USA 96 (1999) 13726-13731
32. Ingraham L.J., and Neidhardt F.C. Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology (1987), ASM Press, Washington, DC
33. Shi H., Cordin O., Minder C.M., Linder P., and Xu R.M. Crystal structure of the human ATP-dependent splicing and export factor UAP56. Proc. Natl Acad. Sci. USA 101 (2004) 17628-17633
34. Sengoku T., Nureki O., Nakamura A., Kobayashi S., and Yokoyama S. Structural basis for RNA unwinding by the DEAD-box protein Drosophila Vasa. Cell 125 (2006) 287-300
35. Henn A., Shi S.P., Zarivach R., Ben-Zeev E., and Sagi I. The RNA helicase DbpA exhibits a markedly different conformation in the ADP-bound state when compared with the ATP- or RNA-bound states. J. Biol. Chem. 277 (2002) 46559-46565
36. 2+ ion concentration, and ionic strength. J. Biol. Chem. 244 (1969) 3330-3342
37. Jencks W.P. The utilization of binding energy in coupled vectorial processes. Adv. Enzymol. Relat. Areas Mol. Biol. 51 (1980) 75-106
38. Xia T., SantaLucia Jr. J., Burkard M.E., Kierzek R., Schroeder S.J., Jiao X., et al. Thermodynamic parameters for an expanded nearest-neighbor model for formation of RNA duplexes with Watson-Crick base pairs. Biochemistry 37 (1998) 14719-14735
39. Tsu C.A., Kossen K., and Uhlenbeck O.C. The Escherichia coli DEAD protein DbpA recognizes a small RNA hairpin in 23S rRNA. RNA 7 (2001) 702-709
40. Gill S.C., and von Hippel P.H. Calculation of protein extinction coefficients from amino acid sequence data. Anal. Biochem. 182 (1989) 319-326
41. Henn A., and De La Cruz E.M. Vertebrate myosin VIIb is a high duty ratio motor adapted for generating and maintaining tension. J. Biol. Chem. 280 (2005) 39665-39676
42. De La Cruz E.M., Sweeney H.L., and Ostap E.M. ADP inhibition of myosin V ATPase activity. Biophys. J. 79 (2000) 1524-1529
43. Brune M., Hunter J.L., Corrie J.E., and Webb M.R. Direct, real-time measurement of rapid inorganic phosphate release using a novel fluorescent probe and its application to actomyosin subfragment 1 ATPase. Biochemistry 33 (1994) 8262-8271
44. Samizo K., Ishikawa R., Nakamura A., and Kohama K. A highly sensitive method for measurement of myosin ATPase activity by reversed-phase high-performance liquid chromatography. Anal. Biochem. 293 (2001) 212-215
45. Barshop B.A., Wrenn R.F., and Frieden C. Analysis of numerical methods for computer simulation of kinetic processes: development of KINSIM-a flexible, portable system. Anal. Biochem. 130 (1983) 134-145