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PMID: 9582286 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

The DEAH-box protein PRP22 is an ATPase that mediates ATP-dependent mRNA release from the spliceosome and unwinds RNA duplexes.

The EMBO journal ·Vol. 17 ·No. 10 ·1998-05-15 ·Pages 2926-37

Wagner JD, Jankowsky E, Company M, Pyle AM, Abelson JN

Abstract

Of the proteins required for pre-mRNA splicing, at least four, the DEAH-box proteins, are closely related due to the presence of a central 'RNA helicase-like' region, and extended homology through a large portion of the protein. A major unresolved question is the function of these proteins. Indirect evidence suggests that several of these proteins are catalysts for important structural rearrangements in the spliceosome. However, the mechanism for the proposed alterations is presently unknown. We present evidence that PRP22, a DEAH-box protein required for mRNA release from the spliceosome, unwinds RNA duplexes in a concentration- and ATP-dependent manner. This demonstrates that PRP22 can modify RNA structure directly. We also show that the PRP22-dependent release of mRNA from the spliceosome is an ATP-dependent process and that recombinant PRP22 is an ATPase. Non-hydrolyzable ATP analogs did not substitute for ATP in the RNA-unwinding reaction, suggesting that ATP hydrolysis is required for this reaction. Specific mutation of a putative ATP phosphate-binding motif in the recombinant protein eliminated the ATPase and RNA-unwinding capacity. Significantly, these data suggest that the DEAH-box proteins act directly on RNA substrates within the spliceosome.

MeSH Terms
Adenosine Triphosphatases/genetics,metabolism Adenosine Triphosphate/metabolism DEAD-box RNA Helicases Fungal Proteins/genetics,metabolism Genetic Complementation Test Hydrolysis Mutation Phenotype RNA Helicases RNA Splicing RNA Splicing Factors RNA, Double-Stranded RNA, Messenger/metabolism RNA, Small Nuclear Recombinant Fusion Proteins/genetics,metabolism Ribonucleoprotein, U4-U6 Small Nuclear/genetics Saccharomyces cerevisiae Proteins Spliceosomes
Chemicals
Fungal Proteins RNA Splicing Factors RNA, Double-Stranded RNA, Messenger RNA, Small Nuclear Recombinant Fusion Proteins Ribonucleoprotein, U4-U6 Small Nuclear Saccharomyces cerevisiae Proteins Adenosine Triphosphate Adenosine Triphosphatases PRP22 protein, S cerevisiae DEAD-box RNA Helicases RNA Helicases
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Wagner J D
Division of Biology, California Institute of Technology, Pasadena, CA 91125, USA.
Jankowsky E
Company M
Pyle A M
Abelson J N
References (43)
43 references, click to expand
  1. A new RNA helicase isolated from HeLa cells that catalytically translocates in the 3' to 5' direction.
    J Biol Chem. 1992 Mar 5;267(7):4398-407 PMID: 1537828
  2. The DEAH-box splicing factor Prp16 unwinds RNA duplexes in vitro.
    Curr Biol. 1998 Apr 9;8(8):441-51 PMID: 9550699
  3. The purified yeast pre-mRNA splicing factor PRP2 is an RNA-dependent NTPase.
    EMBO J. 1992 Jun;11(6):2319-26 PMID: 1534753
  4. A dominant negative mutation in a spliceosomal ATPase affects ATP hydrolysis but not binding to the spliceosome.
    Mol Cell Biol. 1992 Aug;12(8):3540-7 PMID: 1385854
  5. A conformational rearrangement in the spliceosome is dependent on PRP16 and ATP hydrolysis.
    EMBO J. 1992 Dec;11(13):5033-9 PMID: 1464325
  6. Distantly related sequences in the alpha- and beta-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold.
    EMBO J. 1982;1(8):945-51 PMID: 6329717
  7. The "spliceosome": yeast pre-messenger RNA associates with a 40S complex in a splicing-dependent reaction.
    Science. 1985 May 24;228(4702):963-7 PMID: 3890181
  8. Splicing of yeast nuclear pre-mRNA in vitro requires a functional 40S spliceosome and several extrinsic factors.
    Genes Dev. 1987 Mar;1(1):7-18 PMID: 3322937
  9. Spliceosome assembly in yeast.
    Genes Dev. 1987 Nov;1(9):1014-27 PMID: 2962902
  10. Spliceosomal RNA U6 is remarkably conserved from yeast to mammals.
    Nature. 1988 Jul 21;334(6179):213-8 PMID: 3041282
  11. Two related superfamilies of putative helicases involved in replication, recombination, repair and expression of DNA and RNA genomes.
    Nucleic Acids Res. 1989 Jun 26;17(12):4713-30 PMID: 2546125
  12. Isolation and characterization of pre-mRNA splicing mutants of Saccharomyces cerevisiae.
    Genes Dev. 1989 Aug;3(8):1206-16 PMID: 2676722
  13. Bidirectional RNA helicase activity of eucaryotic translation initiation factors 4A and 4F.
    Mol Cell Biol. 1990 Mar;10(3):1134-44 PMID: 2304461
  14. Use of T7 RNA polymerase to direct expression of cloned genes.
    Methods Enzymol. 1990;185:60-89 PMID: 2199796
  15. The yeast PRP2 protein, a putative RNA-dependent ATPase, shares extensive sequence homology with two other pre-mRNA splicing factors.
    Nucleic Acids Res. 1990 Nov 11;18(21):6447 PMID: 2147058
  16. RNA splicing. Alive with DEAD proteins.
    Nature. 1991 Feb 7;349(6309):463-4 PMID: 1825133
  17. Requirement of the RNA helicase-like protein PRP22 for release of messenger RNA from spliceosomes.
    Nature. 1991 Feb 7;349(6309):487-93 PMID: 1992352
  18. PRP16 is an RNA-dependent ATPase that interacts transiently with the spliceosome.
    Nature. 1991 Feb 7;349(6309):494-9 PMID: 1825134
  19. The isolation and characterization of an RNA helicase from nuclear extracts of HeLa cells.
    J Biol Chem. 1991 Jun 5;266(16):10358-67 PMID: 1709930
  20. U4 small nuclear RNA dissociates from a yeast spliceosome and does not participate in the subsequent splicing reaction.
    Mol Cell Biol. 1991 Nov;11(11):5571-7 PMID: 1833635
  21. Pre-mRNA splicing within an assembled yeast spliceosome requires an RNA-dependent ATPase and ATP hydrolysis.
    Proc Natl Acad Sci U S A. 1993 Feb 1;90(3):888-92 PMID: 8430102
  22. Stages in the second reaction of pre-mRNA splicing: the final step is ATP independent.
    Genes Dev. 1993 Feb;7(2):320-9 PMID: 8436300
  23. Escherichia coli rep helicase unwinds DNA by an active mechanism.
    Biochemistry. 1993 Jul 13;32(27):6815-20 PMID: 8392863
  24. The splicing factor PRP2, a putative RNA helicase, interacts directly with pre-mRNA.
    EMBO J. 1994 Feb 15;13(4):888-97 PMID: 8112302
  25. RNA-RNA interactions in the spliceosome: unraveling the ties that bind.
    Cell. 1994 Jul 15;78(1):1-4 PMID: 7518355
  26. Specificity of Prp24 binding to RNA: a role for Prp24 in the dynamic interaction of U4 and U6 snRNAs.
    RNA. 1995 Apr;1(2):132-45 PMID: 7585243
  27. Vaccinia virus RNA helicase: nucleic acid specificity in duplex unwinding.
    J Virol. 1996 Apr;70(4):2615-9 PMID: 8642695
  28. A human RNA helicase-like protein, HRH1, facilitates nuclear export of spliced mRNA by releasing the RNA from the spliceosome.
    Genes Dev. 1996 Apr 15;10(8):997-1007 PMID: 8608946
  29. A DEAD-box RNA helicase in the Escherichia coli RNA degradosome.
    Nature. 1996 May 9;381(6578):169-72 PMID: 8610017
  30. An RNA-dependent ATPase associated with U2/U6 snRNAs in pre-mRNA splicing.
    Nature. 1996 Jun 20;381(6584):709-13 PMID: 8649518
  31. Requirement for SLU7 in yeast pre-mRNA splicing is dictated by the distance between the branchpoint and the 3' splice site.
    RNA. 1996 Jul;2(7):707-17 PMID: 8756413
  32. Mechanisms of helicase-catalyzed DNA unwinding.
    Annu Rev Biochem. 1996;65:169-214 PMID: 8811178
  33. p72: a human nuclear DEAD box protein highly related to p68.
    Nucleic Acids Res. 1996 Oct 1;24(19):3739-47 PMID: 8871553
  34. Crystal structure of a DExx box DNA helicase.
    Nature. 1996 Nov 28;384(6607):379-83 PMID: 8934527
  35. Spliceosome activation by PRP2 ATPase prior to the first transesterification reaction of pre-mRNA splicing.
    Mol Cell Biol. 1996 Dec;16(12):6810-9 PMID: 8943336
  36. The Saccharomyces cerevisiae Prp5 protein has RNA-dependent ATPase activity with specificity for U2 small nuclear RNA.
    J Biol Chem. 1996 Dec 27;271(52):33261-7 PMID: 8969184
  37. Virus-encoded RNA helicases.
    J Virol. 1997 Apr;71(4):2583-90 PMID: 9060609
  38. The yeast tRNA splicing endonuclease: a tetrameric enzyme with two active site subunits homologous to the archaeal tRNA endonucleases.
    Cell. 1997 Jun 13;89(6):849-58 PMID: 9200603
  39. Molecular analysis of the SNF2/SWI2 protein family member MOT1, an ATP-driven enzyme that dissociates TATA-binding protein from DNA.
    Mol Cell Biol. 1997 Aug;17(8):4842-51 PMID: 9234740
  40. A conformational switch in Escherichia coli 16S ribosomal RNA during decoding of messenger RNA.
    Science. 1997 Aug 29;277(5330):1262-7 PMID: 9271564
  41. Prp43: An RNA helicase-like factor involved in spliceosome disassembly.
    Proc Natl Acad Sci U S A. 1997 Oct 28;94(22):11798-802 PMID: 9342317
  42. Mechanical devices of the spliceosome: motors, clocks, springs, and things.
    Cell. 1998 Feb 6;92(3):315-26 PMID: 9476892
  43. D-E-A-D protein family of putative RNA helicases.
    Mol Microbiol. 1992 Feb;6(3):283-91 PMID: 1552844
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
Published
1998-05-15
Pages
2926-37
Language
English
Region
England
NLM ID
8208664
PMCID
PMC1170633
Subset
IM
Grants
NIGMS NIH HHS · GM17595-01 · United States
NIGMS NIH HHS · GM32637 · United States
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