Studies on three E. coli DEAD-box helicases point to an unwinding mechanism different from that of model DNA helicases

Biochemistry

Volumn 43, Issue 24, 2004, Pages 7857-7866

  Bizebard, Thierry ^a   Ferlenghi, Ilaria ^a,c   Iost, Isabelle ^b   Dreyfus, Marc ^b  

^a LABORATOIRE D ENZYMOLOGIE ET BIOCHIMIE STRUCTURALES   (France)

^b ECOLE NORMALE SUPÉRIEURE   (France)

^c CHIRON VACCINES   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINETRIPHOSPHATE; DNA; HYDROLYSIS; PROTEINS; RNA;

BIOLOGICAL SPECIFICITY; EQUIVOCAL UNWINDING ACTIVITY;

BIOCHEMISTRY;

ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; BACTERIAL ENZYME; BACTERIAL PROTEIN; DEAD BOX PROTEIN; DOUBLE STRANDED RNA; HELICASE; OLIGORIBONUCLEOTIDE; PROTEIN CSDA; PROTEIN RHLE; PROTEIN SRMB; RNA; UNCLASSIFIED DRUG;

ARTICLE; BASE PAIRING; ENZYME MECHANISM; ENZYME SPECIFICITY; ESCHERICHIA COLI; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN HYDROLYSIS; PROTEIN STRUCTURE; RNA METABOLISM;

ADENOSINE TRIPHOSPHATASES; BASE SEQUENCE; CLONING, MOLECULAR; DNA PRIMERS; ESCHERICHIA COLI; RNA HELICASES;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 2942754127     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi049852s     Document Type: Article

References (45)

1. Linder, P., Lasko, P. F., Ashburner, M., Leroy, P., Nielsen, P. J., Nishi, K., Schnier, J., and Slonimski, P. P. (1989) Birth of the D-E-A-D box, Nature 337, 121-122.
2. Tanner, N. K., and Linder, P. (2001) DExD/H box RNA helicases: from generic motors to specific dissociation functions, Mol. Cell 8, 251-262.
3. Tanner, N. K., Cordin, O., Banroques, J., Doère, M., and Linder, P. (2003) The Q motif: a newly identified motif in DEAD box helicases may regulate ATP binding and hydrolysis, Mol. Cell 11, 127-138.
4. Silverman, E., Edwalds-Gilbert, G., and Lin, R. J. (2003) DExD/H-box proteins and their partners: helping RNA helicases unwind, Gene 312, 1-16.
5. de la Cruz, J., Kressler, D., and Linder, P. (1999) Unwinding RNA in Saccharomyces cerevisiae: DEAD-box proteins and related families, Trends Biochem. Sci. 24, 192-198.
6. Gorbalenya, A. E., and Koonin, E. V. (1993) Helicases: amino acid sequence comparisons and structure-function relationships, Curr. Opin. Struct. Biol. 3, 419-429.
7. Caruthers, J. M., and McKay, D. B. (2002) Helicase structure and mechanism, Curr. Opin. Struct. Biol. 12, 123-133.
8. Singleton, M. R., and Wigley, D. B. (2002) Modularity and specialization in superfamily 1 and 2 helicases, J. Bacteriol. 184, 1819-1826.
9. Korolev, S., Hsieh, J., Gauss, G. H., Lohman, T. M., and Waksman, G. (1997) Major domain swiveling revealed by the crystal structures of complexes of E. coli Rep helicase bound to single-stranded DNA and ADP, Cell 90, 635-647.
10. Velankar, S. S., Soultanas, P., Dillingham, M. S., Subramanya, H. S., and Wigley, D. B. (1999) Crystal structures of complexes of PcrA DNA helicase with a DNA substrate indicate an inchworm mechanism, Cell 97, 75-84.
11. Soultanas, P., Dillingham, M. S., Wiley, P., Webb, M. R., and Wigley, D. B. (2000) Uncoupling DNA translocation and helicase activity in PcrA: direct evidence for an active mechanism, EMBO J. 19, 3799-3810.
12. Rocak, S., and Linder, P. (2004) DEAD-box proteins: The driving forces behind RNA metabolism, Nat. Rev. Mol. Cell Biol. 5, 232-241.
13. Diges, C. M., and Uhlenbeck, O. C. (2001) Escherichia coli DbpA is an RNA helicase that requires hairpin 92 of 23S rRNA, EMBO J. 20, 5503-5512.
14. Rogers, G. W. J., Richter, N. J., and Merrick, W. C. (1999) Biochemical and kinetic characterization of the RNA helicase activity of Eukaryotic Initiation Factor 4A, J. Biol. Chem. 274, 12236-12244.
15. Lorsch, J. R., and Herschlag, D. (1998) The DEAD box protein eIF4A. 1. A minimal kinetic and thermodynamic framework reveals coupled binding of RNA and nucleotide, Biochemistry 37, 2180-2193.
16. Vanzo, N. F., Li, Y. S., Py, B., Blum, E., Higgins, C. F., Raynal, L. C., Krisch, H. M., and Carpousis, A. J. (1998) Ribonuclease E organizes the protein interactions in the Escherichia coli RNA degradosome, Genes Dev. 12, 2770-2781.
17. Rogers, G. W. J., Richter, N. J., Lima, W. F., and Merrick, W. C. (2001) Modulation of the helicase activity of eIF4A by eIF4B, eIF4H, and eIF4F, J. Biol. Chem. 276, 30914-30922.
18. Kossen, K., Karginov, F. V., and Uhlenbeck, O. C. (2002) The carboxy-terminal domain of the DExD/H protein YxiN is sufficient to confer specificity for 23S rRNA, J. Mol. Biol. 324, 625-636.
19. Rogers, G. W. J., Lima, W. F., and Merrick, W. C. (2001) Further characterization of the helicase activity of eIF4A. Substrate specificity, J. Biol. Chem. 276, 12598-12608.
20. Du, M. X., Johnson, R. B., Sun, X. L., Staschke, K. A., Colacino, J., and Wang, Q. M. (2002) Comparative characterization of two DEAD-box RNA helicases in superfamily II: human translation initiation factor 4A and hepatitis C virus nonstructural protein 3 (NS3) helicase, Biochem. J. 363, 147-155.
21. Fuller-Pace, F. V., Nicol, S. M., Reid, A. D., and Lane, D. P. (1993) DbpA: a DEAD-box protein specifically activated by 23S rRNA, EMBO J. 12, 3619-3626.
22. Khemici, V., and Carpousis, A. J. (2004) The RNA degradosome and poly(A) polymerase of Escherichia coli are required in vivo for the degradation of small mRNA decay intermediates containing REP-stabilizers, Mol. Microbiol. 51, 777-790.
23. Py, B., Higgins, C. F., Krish, H. M., and Carpousis, A. J. (1996) A DEAD-box RNA helicase in the Escherichia coli RNA degradosome, Nature 381, 169-172.
24. Miczak, A., Kaberdin, V. R., Wei, C. L., and Lin-Chao, S. (1996) Proteins associated with RNase E in a multicomponent ribonucleolytic complex, Proc. Natl. Acad. Sci. U.S.A. 93, 3865-3869.
25. Jones, P. G., Mitta, M., Kim, Y., Jiang, W., and Inouye, M. (1996) Cold-shock induces a major ribosomal-associated protein that unwinds double-stranded RNA in Escherichia coli, Proc. Natl. Acad. Sci. U.S.A. 93, 76-80.
26. Charollais, J., Dreyfus, M., and Iost, I. (2004) CsdA, A cold-shock RNA helicase from Escherichia coli, is involved in the biogenesis of 50S ribosomal subunit, Nucleic Acids Res., in press.
27. Iost, I., and Dreyfus, M. (1994) mRNAs can be stabilized by DEAD-box proteins, Nature 372, 193-196.
28. Charollais, J., Pflieger, D., Vinh, J., Dreyfus, M., and Iost, I. (2003) The DEAD-box RNA helicase SrmB is involved in the assembly of 50S ribosomal subunits in Escherichia coli, Mol. Microbiol. 48, 1253-1265.
29. Nishi, K., Morel-Deville, F., Hershey, J. W. B., Leighton, T., and Schnier, J. (1988) An eIF-4A-like protein is a suppressor of an Escherichia coli mutant defective in 50S ribosomal subunit assembly, Nature 336, 496-498.
30. Raynal, L. C., and Carpousis, A. J. (1999) Poly(A) polymerase I of Escherichia coli: characterization of the catalytic domain, an RNA binding site, and regions for the interaction with proteins involved in mRNA degradation, Mol. Microbiol. 32, 765-775.
31. Bessman, M. J. (1963) Deoxynucleotide monophosphate kinases, Methods Enzymol. 6, 166-176.
32. Iost, I., Dreyfus, M., and Linder, P. (1999) Dedlp, a DEAD-box protein required for translation initiation in Saccharomyces cerevisiae, is a RNA helicase, J. Biol. Chem. 274, 17677-17683.
33. Peck, M. L., and Herschlag, D. (1999) Effects of oligonucleotide length and atomic composition on stimulation of the ATPase activity of translation initiation factor eIF4A, RNA 5, 1210-1221.
34. Pause, A., and Sonenberg, N. (1992) Mutational analysis of a DEAD box RNA helicase - the mammalian translation initiation factor eIF-4A, EMBO J. 11, 2643-2654.
35. Kim, J. L., Morgenstern, K. A., Griffith, J. P., Dwyer, M. D., Thomson, J. A., Murcko, M. A., Lin, C., and Caron, P. R. (1998) Hepatitis C virus NS3 RNA helicase domain with a bound oligonucleotide: the crystal structure provides insights into the mode of unwinding, Structure 6, 89-100.
36. Levin, M. K., and Patel, S. S. (2002) Helicase from hepatitis C virus, energetics of DNA binding, J. Biol. Chem. 277, 29377-29385.
37. Story, R. M., Li, H., and Abelson, J. N. (2000) Crystal structure of a DEAD box protein of the hyperthermophile Methanococcus jannaschii, Proc. Natl. Acad. Sci. U.S.A. 98, 1465-1470.
38. Huang, Y., and Liu, Z. R. (2002) The ATPase, RNA unwinding and RNA binding activities of recombinant p68 RNA helicase, J. Biol. Chem. 277, 12810-12815.
39. Lee, C. G. (2002) RH70, a bidirectional RNA helicase, co-purifies with UlsnRNP, J. Biol. Chem. 277, 39679-39683.
40. Flores-Rozas, H., and Hurwitz, J. (1993) Characterization of a new RNA helicase from nuclear extracts of HeLa cells which translocates in the 5′ to 3′ direction, J. Biol. Chem. 268, 21372-21383.
41. Yu, E., and Owttrim, G. W. (2000) Characterization of the cold stress-induced cyanobacterial DEAD-box protein CrhC as an RNA helicase, Nucleic Acids Res. 28, 3926-3934.
42. Singleton, M. R., Scaife, S., and Wigley, D. B. (2001) Structural analysis of DNA replication fork reversal by RecG, Cell 107, 79-89.
43. Mahdi, A. A., Briggs, G. S., Sharples, G. J., Wen, Q., and Lloyd, R. G. (2003) A model for dsDNA translocation revealed by a structural motif common to RecG and Mfd proteins, EMBO J. 22, 724-734.
44. Jankowsky, E., Gross, C. H., Shuman, S., and Pyle, A. M. (2001) Active disruption of an RNA-protein interaction by a DExH/D RNA helicase, Science 291, 121-124.
45. Bateman, A., Bimey, E., Cerruti, L., Durbin, R., Etwiller, L., Eddy, S. R., Griffiths-Jones, S., Howe, K. L., Marshall, M., and Sonnhammer, E. L. (2002) The Pfam Protein Families Database, Nucleic Acids Res. 30, 276-280.