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PMID: 12773550 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Cotranscriptional processing of Drosophila histone mRNAs.

Molecular and cellular biology ·Vol. 23 ·No. 12 ·2003-06-00 ·Pages 4046-55

Adamson TE, Price DH

Abstract

The 3' ends of metazoan histone mRNAs are generated by specialized processing machinery that cleaves downstream of a conserved stem-loop structure. To examine how this reaction might be influenced by transcription, we used a Drosophila melanogaster in vitro system that supports both processes. In this system the complete synthesis of histone mRNA, including transcription initiation and elongation, followed by 3' end formation, occurred at a physiologically significant rate. Processing of free transcripts was efficient and occurred with a t(1/2) of less than 1 min. Divalent cations were not required, but nucleoside triphosphates (NTPs) stimulated the rate of cleavage slightly. Isolated elongation complexes encountered a strong arrest site downstream of the mature histone H4 3' end. In the presence of NTPs, transcripts in these arrested complexes were processed at a rate similar to that of free RNA. Removal of NTPs dramatically reduced this rate, potentially due to concealment of the U7 snRNP binding element. The arrest site was found to be a conserved feature located 32 to 35 nucleotides downstream of the processing site on the H4, H2b, and H3 genes. The significance of the newly discovered arrest sites to our understanding of the coupling between transcription and RNA processing on the one hand and histone gene expression on the other is discussed.

MeSH Terms
Animals Biochemical Phenomena Biochemistry Cell Line Cell Nucleus/metabolism DNA/metabolism Drosophila melanogaster/metabolism Gene Expression Regulation Histones/metabolism Kinetics Models, Biological Models, Genetic Polymerase Chain Reaction RNA/metabolism RNA Polymerase II/chemistry RNA, Messenger/metabolism Time Factors Transcription, Genetic
Chemicals
Histones RNA, Messenger RNA DNA RNA Polymerase II
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Adamson Todd E
Department of Biochemistry, University of Iowa, Iowa City, Iowa 52242, USA.
Price David H
References (60)
60 references, click to expand
  1. P-TEFb, a cyclin-dependent kinase controlling elongation by RNA polymerase II.
    Mol Cell Biol. 2000 Apr;20(8):2629-34 PMID: 10733565
  2. DSIF, a novel transcription elongation factor that regulates RNA polymerase II processivity, is composed of human Spt4 and Spt5 homologs.
    Genes Dev. 1998 Feb 1;12(3):343-56 PMID: 9450929
  3. Identification of multiple cyclin subunits of human P-TEFb.
    Genes Dev. 1998 Mar 1;12(5):755-62 PMID: 9499409
  4. Identification of a cyclin subunit required for the function of Drosophila P-TEFb.
    J Biol Chem. 1998 May 29;273(22):13855-60 PMID: 9593731
  5. RNA polymerase II is an essential mRNA polyadenylation factor.
    Nature. 1998 Sep 3;395(6697):93-6 PMID: 9738505
  6. Two Xenopus proteins that bind the 3' end of histone mRNA: implications for translational control of histone synthesis during oogenesis.
    Mol Cell Biol. 1999 Jan;19(1):835-45 PMID: 9858606
  7. NELF, a multisubunit complex containing RD, cooperates with DSIF to repress RNA polymerase II elongation.
    Cell. 1999 Apr 2;97(1):41-51 PMID: 10199401
  8. Terminal exon definition occurs cotranscriptionally and promotes termination of RNA polymerase II.
    Mol Cell. 1999 Mar;3(3):371-8 PMID: 10198639
  9. Stem-loop binding protein facilitates 3'-end formation by stabilizing U7 snRNP binding to histone pre-mRNA.
    Mol Cell Biol. 1999 May;19(5):3561-70 PMID: 10207079
  10. Phosphorylated RNA polymerase II stimulates pre-mRNA splicing.
    Genes Dev. 1999 May 15;13(10):1234-9 PMID: 10346811
  11. Specific transcriptional pausing activates polyadenylation in a coupled in vitro system.
    Mol Cell. 1999 May;3(5):593-600 PMID: 10360175
  12. Formation of the 3' end of histone mRNA.
    Gene. 1999 Oct 18;239(1):1-14 PMID: 10571029
  13. Drosophila stem loop binding protein coordinates accumulation of mature histone mRNA with cell cycle progression.
    Genes Dev. 2001 Jan 15;15(2):173-87 PMID: 11157774
  14. Multiple transcript cleavage precedes polymerase release in termination by RNA polymerase II.
    Cell. 2001 Jun 1;105(5):669-81 PMID: 11389836
  15. Coordination between transcription and pre-mRNA processing.
    FEBS Lett. 2001 Jun 8;498(2-3):179-82 PMID: 11412852
  16. A highly purified RNA polymerase II elongation control system.
    J Biol Chem. 2001 Nov 9;276(45):42601-9 PMID: 11553615
  17. Regulation of RNA polymerase II activity by CTD phosphorylation and cell cycle control.
    J Cell Physiol. 2002 Feb;190(2):160-9 PMID: 11807820
  18. Structure of the histone mRNA hairpin required for cell cycle regulation of histone gene expression.
    RNA. 2002 Jan;8(1):29-46 PMID: 11871659
  19. Developmental control of histone mRNA and dSLBP synthesis during Drosophila embryogenesis and the role of dSLBP in histone mRNA 3' end processing in vivo.
    Mol Cell Biol. 2002 Apr;22(7):2267-82 PMID: 11884612
  20. Integrating mRNA processing with transcription.
    Cell. 2002 Feb 22;108(4):501-12 PMID: 11909521
  21. The mRNA assembly line: transcription and processing machines in the same factory.
    Curr Opin Cell Biol. 2002 Jun;14(3):336-42 PMID: 12067656
  22. 3' end processing of Drosophila melanogaster histone pre-mRNAs: requirement for phosphorylated Drosophila stem-loop binding protein and coevolution of the histone pre-mRNA processing system.
    Mol Cell Biol. 2002 Sep;22(18):6648-60 PMID: 12192062
  23. Functional coupling of capping and transcription of mRNA.
    Mol Cell. 2002 Sep;10(3):599-609 PMID: 12408827
  24. The organization of the histone genes in Drosophila melanogaster: functional and evolutionary implications.
    Cold Spring Harb Symp Quant Biol. 1978;42 Pt 2:1047-51 PMID: 98262
  25. A Drosophila RNA polymerase II transcription factor contains a promoter-region-specific DNA-binding activity.
    Cell. 1984 Feb;36(2):357-69 PMID: 6537904
  26. The 3' end of drosophila histone H3 mRNA is produced by a processing activity in vitro.
    Cell. 1984 Sep;38(2):423-9 PMID: 6432343
  27. Genetic complementation in the Xenopus oocyte: co-expression of sea urchin histone and U7 RNAs restores 3' processing of H3 pre-mRNA in the oocyte.
    EMBO J. 1986 Jul;5(7):1675-82 PMID: 2943587
  28. Compensatory mutations suggest that base-pairing with a small nuclear RNA is required to form the 3' end of H3 messenger RNA.
    Nature. 1986 Oct 30-Nov 5;323(6091):777-81 PMID: 3022153
  29. Fractionation of transcription factors for RNA polymerase II from Drosophila Kc cell nuclear extracts.
    J Biol Chem. 1987 Mar 5;262(7):3244-55 PMID: 3818640
  30. RNA 3' processing regulates histone mRNA levels in a mammalian cell cycle mutant. A processing factor becomes limiting in G1-arrested cells.
    EMBO J. 1987 Jun;6(6):1721-6 PMID: 3608992
  31. Heat-labile regulatory factor is required for 3' processing of histone precursor mRNAs.
    Proc Natl Acad Sci U S A. 1987 Dec;84(24):8937-40 PMID: 2962194
  32. The stem-loop structure at the 3' end of histone mRNA is necessary and sufficient for regulation of histone mRNA stability.
    Mol Cell Biol. 1987 Dec;7(12):4557-9 PMID: 3437896
  33. Elongation by Drosophila RNA polymerase II. Transcription of 3'-extended DNA templates.
    J Biol Chem. 1988 Jul 15;263(20):9917-25 PMID: 2454924
  34. Properties of a Drosophila RNA polymerase II elongation factor.
    J Biol Chem. 1989 May 25;264(15):8963-9 PMID: 2722810
  35. Dynamic interaction between a Drosophila transcription factor and RNA polymerase II.
    Mol Cell Biol. 1989 Apr;9(4):1465-75 PMID: 2725511
  36. The efficiency of 3'-end formation contributes to the relative levels of different histone mRNAs.
    Mol Cell Biol. 1989 Aug;9(8):3499-508 PMID: 2796992
  37. Cell cycle-dependent regulation of histone precursor mRNA processing by modulation of U7 snRNA accessibility.
    Nature. 1990 Aug 16;346(6285):665-8 PMID: 1696685
  38. An intact histone 3'-processing site is required for transcription termination in a mouse histone H2a gene.
    Mol Cell Biol. 1991 Jan;11(1):497-509 PMID: 1986243
  39. Regulation of histone mRNA in the unperturbed cell cycle: evidence suggesting control at two posttranscriptional steps.
    Mol Cell Biol. 1991 May;11(5):2416-24 PMID: 2017161
  40. Stability of Drosophila RNA polymerase II elongation complexes in vitro.
    Mol Cell Biol. 1992 May;12(5):2067-77 PMID: 1373806
  41. Control of formation of two distinct classes of RNA polymerase II elongation complexes.
    Mol Cell Biol. 1992 May;12(5):2078-90 PMID: 1569941
  42. Histone 3' ends: essential and regulatory functions.
    Gene Expr. 1992;2(2):93-7 PMID: 1633440
  43. Variable effects of the conserved RNA hairpin element upon 3' end processing of histone pre-mRNA in vitro.
    Nucleic Acids Res. 1993 Apr 11;21(7):1569-75 PMID: 8479907
  44. Mechanism of DmS-II-mediated pause suppression by Drosophila RNA polymerase II.
    J Biol Chem. 1993 Sep 5;268(25):18762-70 PMID: 7689559
  45. The site of 3' end formation of histone messenger RNA is a fixed distance from the downstream element recognized by the U7 snRNP.
    EMBO J. 1994 May 15;13(10):2432-40 PMID: 8194533
  46. GreA-induced transcript cleavage in transcription complexes containing Escherichia coli RNA polymerase is controlled by multiple factors, including nascent transcript location and structure.
    J Biol Chem. 1994 Sep 2;269(35):22282-94 PMID: 8071355
  47. 3' end processing of mouse histone pre-mRNA: evidence for additional base-pairing between U7 snRNA and pre-mRNA.
    Nucleic Acids Res. 1994 Oct 11;22(20):4023-30 PMID: 7937126
  48. Purification of P-TEFb, a transcription factor required for the transition into productive elongation.
    J Biol Chem. 1995 May 26;270(21):12335-8 PMID: 7759473
  49. Decreasing the distance between the two conserved sequence elements of histone pre-messenger RNA interferes with 3' processing in vitro.
    RNA. 1995 Nov;1(9):905-14 PMID: 8548655
  50. The polyribosomal protein bound to the 3' end of histone mRNA can function in histone pre-mRNA processing.
    RNA. 1995 Nov;1(9):915-23 PMID: 8548656
  51. Efficient extraction and partial purification of the polyribosome-associated stem-loop binding protein bound to the 3' end of histone mRNA.
    Biochemistry. 1996 Feb 20;35(7):2146-56 PMID: 8652556
  52. Control of RNA polymerase II elongation potential by a novel carboxyl-terminal domain kinase.
    J Biol Chem. 1996 Oct 25;271(43):27176-83 PMID: 8900211
  53. The protein that binds the 3' end of histone mRNA: a novel RNA-binding protein required for histone pre-mRNA processing.
    Genes Dev. 1996 Dec 1;10(23):3028-40 PMID: 8957003
  54. Transcriptional termination and coupled polyadenylation in vitro.
    EMBO J. 2000 Jul 17;19(14):3770-7 PMID: 10899130
  55. Assembly of U7 small nuclear ribonucleoprotein particle and histone RNA 3' processing in Xenopus egg extracts.
    J Biol Chem. 2000 Aug 11;275(32):24284-93 PMID: 10827192
  56. Coupled in vitro synthesis and splicing of RNA polymerase II transcripts.
    RNA. 2000 Sep;6(9):1325-34 PMID: 10999609
  57. Participation of the C-terminal domain of RNA polymerase II in exon definition during pre-mRNA splicing.
    Mol Cell Biol. 2000 Nov;20(21):8290-301 PMID: 11027297
  58. Length suppression in histone messenger RNA 3'-end maturation: processing defects of insertion mutant premessenger RNAs can be compensated by insertions into the U7 small nuclear RNA.
    Proc Natl Acad Sci U S A. 1996 Dec 10;93(25):14659-64 PMID: 8962110
  59. Drosophila factor 2, an RNA polymerase II transcript release factor, has DNA-dependent ATPase activity.
    J Biol Chem. 1997 Dec 12;272(50):31902-7 PMID: 9395538
  60. Stem-loop binding protein, the protein that binds the 3' end of histone mRNA, is cell cycle regulated by both translational and posttranslational mechanisms.
    Mol Cell Biol. 2000 Jun;20(12):4188-98 PMID: 10825184
Article Info
Journal
Molecular and cellular biology
Abbr.
Mol Cell Biol
ISSN
0270-7306
DOI
10.1128/MCB.23.12.4046-4055.2003
Published
2003-06-00
Pages
4046-55
Language
English
Region
United States
NLM ID
8109087
PMCID
PMC156150
Subset
IM
Grants
NIGMS NIH HHS · R01 GM035500 · United States
NIGMS NIH HHS · GM35500 · United States
External Links
PubMed source DOI: 10.1128/MCB.23.12.4046-4055.2003 PMC Full Text View journal details
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