Home LiteratureArticle Details
PMID: 15047853 Published · epublish English Comparative Study Journal Article Research Support, U.S. Gov't, Non-P.H.S. Research Support, U.S. Gov't, P.H.S.

Growth-regulated expression and G0-specific turnover of the mRNA that encodes URH49, a mammalian DExH/D box protein that is highly related to the mRNA export protein UAP56.

Nucleic acids research ·Vol. 32 ·No. 6 ·2004-00-00 ·Pages 1857-65

Pryor A, Tung L, Yang Z, Kapadia F, Chang TH, Johnson LF

Abstract

URH49 is a mammalian protein that is 90% identical to the DExH/D box protein UAP56, an RNA helicase that is important for splicing and nuclear export of mRNA. Although Saccharomyces cerevisiae and Drosophila express only a single protein corresponding to UAP56, mRNAs encoding URH49 and UAP56 are both expressed in human and mouse cells. Both proteins interact with the mRNA export factor Aly and both are able to rescue the loss of Sub2p (the yeast homolog of UAP56), indicating that both proteins have similar functions. UAP56 mRNA is more abundant than URH49 mRNA in many tissues, although in testes URH49 mRNA is much more abundant. UAP56 and URH49 mRNAs are present at similar levels in proliferating cultured cells. However, when the cells enter quiescence, the URH49 mRNA level decreases 3-6-fold while the UAP56 mRNA level remains relatively constant. The amount of URH49 mRNA increases to the level found in proliferating cells within 5 h when quiescent cells are growth-stimulated or when protein synthesis is inhibited. URH49 mRNA is relatively unstable (T(1/2) = 4 h) in quiescent cells, but is stabilized immediately following growth stimulation or inhibition of protein synthesis. In contrast, there is much less change in the content or stability of UAP56 mRNA following growth stimulation. Our observations suggest that in mammalian cells, two UAP56-like RNA helicases are involved in splicing and nuclear export of mRNA. Differential expression of these helicases may lead to quantitative or qualitative changes in mRNA expression.

MeSH Terms
ATP-Binding Cassette Transporters Active Transport, Cell Nucleus Adenosine Triphosphatases/genetics Animals Cell Division Cell Nucleus/metabolism Conserved Sequence DEAD-box RNA Helicases Gene Expression Regulation Genetic Complementation Test HeLa Cells Humans Male Mice Nuclear Proteins/metabolism RNA Helicases/genetics,metabolism,physiology RNA Stability RNA, Messenger/metabolism RNA-Binding Proteins/metabolism Resting Phase, Cell Cycle Transcription Factors/metabolism
Chemicals
ALYREF protein, human ATP-Binding Cassette Transporters Nuclear Proteins RNA, Messenger RNA-Binding Proteins Refbp1 protein, mouse Transcription Factors Adenosine Triphosphatases DDX39A protein, human DDX39B protein, human RNA-dependent ATPase DEAD-box RNA Helicases RNA Helicases
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Pryor Anne
The Ohio State Biochemistry Program, The Ohio State University, Columbus, OH 43210, USA.
Tung Luh
Yang Zhe
Kapadia Fehmida
Chang Tien-Hsien
Johnson Lee F
References (57)
57 references, click to expand
  1. HEL/UAP56 binds cotranscriptionally to the Balbiani ring pre-mRNA in an intron-independent manner and accompanies the BR mRNP to the nuclear pore.
    Curr Biol. 2002 May 14;12(10):859-62 PMID: 12015125
  2. DExD/H box RNA helicases: from generic motors to specific dissociation functions.
    Mol Cell. 2001 Aug;8(2):251-62 PMID: 11545728
  3. The mRNA assembly line: transcription and processing machines in the same factory.
    Curr Opin Cell Biol. 2002 Jun;14(3):336-42 PMID: 12067656
  4. Comprehensive proteomic analysis of the human spliceosome.
    Nature. 2002 Sep 12;419(6903):182-5 PMID: 12226669
  5. Nutritional control of mRNA stability is mediated by a conserved AU-rich element that binds the cytoplasmic shuttling protein HuR.
    J Biol Chem. 2002 Nov 1;277(44):41539-46 PMID: 12196519
  6. Stable mRNP formation and export require cotranscriptional recruitment of the mRNA export factors Yra1p and Sub2p by Hpr1p.
    Mol Cell Biol. 2002 Dec;22(23):8241-53 PMID: 12417727
  7. A quantitative analysis of intron effects on mammalian gene expression.
    RNA. 2003 May;9(5):607-17 PMID: 12702819
  8. The interplay of nuclear mRNP assembly, mRNA surveillance and export.
    Trends Cell Biol. 2003 Jun;13(6):319-27 PMID: 12791298
  9. The Ref/Aly proteins are dispensable for mRNA export and development in Caenorhabditis elegans.
    RNA. 2003 Jul;9(7):881-91 PMID: 12810921
  10. Yeast RNA helicases of the DEAD-box family involved in translation initiation.
    Biol Cell. 2003 May-Jun;95(3-4):157-67 PMID: 12867080
  11. Cell-specific and hormone-regulated expression of gonadotropin-regulated testicular RNA helicase gene (GRTH/Ddx25) resulting from alternative utilization of translation initiation codons in the rat testis.
    J Biol Chem. 2003 Jul 25;278(30):27796-803 PMID: 12734186
  12. Pre-mRNA splicing: awash in a sea of proteins.
    Mol Cell. 2003 Jul;12(1):5-14 PMID: 12887888
  13. Regulation of A + U-rich element-directed mRNA turnover involving reversible phosphorylation of AUF1.
    J Biol Chem. 2003 Aug 29;278(35):33029-38 PMID: 12819195
  14. Splicing enhances translation in mammalian cells: an additional function of the exon junction complex.
    Genes Dev. 2004 Jan 15;18(2):210-22 PMID: 14752011
  15. Regulation of histone mRNA production and stability in serum-stimulated mouse 3T6 fibroblasts.
    Mol Cell Biol. 1983 Nov;3(11):1920-9 PMID: 6656760
  16. Regulation of c-myc transcription and mRNA abundance by serum growth factors and cell contact.
    J Biol Chem. 1986 Jul 15;261(20):9161-6 PMID: 3722193
  17. Expression of a set of growth-related immediate early genes in BALB/c 3T3 cells: coordinate regulation with c-fos or c-myc.
    Proc Natl Acad Sci U S A. 1987 Mar;84(5):1182-6 PMID: 3469660
  18. Complexity of the early genetic response to growth factors in mouse fibroblasts.
    Mol Cell Biol. 1988 May;8(5):2140-8 PMID: 2898731
  19. Removal of poly(A) and consequent degradation of c-fos mRNA facilitated by 3' AU-rich sequences.
    Nature. 1988 Nov 24;336(6197):396-9 PMID: 3194021
  20. The protein encoded by a murine male germ cell-specific transcript is a putative ATP-dependent RNA helicase.
    Cell. 1989 May 19;57(4):549-59 PMID: 2720782
  21. Yeast vectors for the controlled expression of heterologous proteins in different genetic backgrounds.
    Gene. 1995 Apr 14;156(1):119-22 PMID: 7737504
  22. mRNA decay mediated by two distinct AU-rich elements from c-fos and granulocyte-macrophage colony-stimulating factor transcripts: different deadenylation kinetics and uncoupling from translation.
    Mol Cell Biol. 1995 Oct;15(10):5777-88 PMID: 7565731
  23. The transcriptional elongation inhibitor 5,6-dichloro-1-beta-D-ribofuranosylbenzimidazole inhibits transcription factor IIH-associated protein kinase.
    J Biol Chem. 1995 Oct 13;270(41):23922-5 PMID: 7592583
  24. U2AF65 recruits a novel human DEAD box protein required for the U2 snRNP-branchpoint interaction.
    Genes Dev. 1997 Jul 15;11(14):1864-72 PMID: 9242493
  25. Mechanical devices of the spliceosome: motors, clocks, springs, and things.
    Cell. 1998 Feb 6;92(3):315-26 PMID: 9476892
  26. Dbp5p, a cytosolic RNA helicase, is required for poly(A)+ RNA export.
    EMBO J. 1998 May 1;17(9):2651-62 PMID: 9564047
  27. RNA stabilization by the AU-rich element binding protein, HuR, an ELAV protein.
    EMBO J. 1998 Jun 15;17(12):3461-70 PMID: 9628881
  28. RNA unwinding in U4/U6 snRNPs requires ATP hydrolysis and the DEIH-box splicing factor Brr2.
    Curr Biol. 1998 Jul 16;8(15):847-55 PMID: 9705931
  29. An RNA switch at the 5' splice site requires ATP and the DEAD box protein Prp28p.
    Mol Cell. 1999 Jan;3(1):55-64 PMID: 10024879
  30. Dbp5, a DEAD-box protein required for mRNA export, is recruited to the cytoplasmic fibrils of nuclear pore complex via a conserved interaction with CAN/Nup159p.
    EMBO J. 1999 Aug 2;18(15):4332-47 PMID: 10428971
  31. The p38 MAP kinase pathway signals for cytokine-induced mRNA stabilization via MAP kinase-activated protein kinase 2 and an AU-rich region-targeted mechanism.
    EMBO J. 1999 Sep 15;18(18):4969-80 PMID: 10487749
  32. Quantitative studies of the growth of mouse embryo cells in culture and their development into established lines.
    J Cell Biol. 1963 May;17:299-313 PMID: 13985244
  33. Iron-regulatory proteins, iron-responsive elements and ferritin mRNA translation.
    Int J Biochem Cell Biol. 1999 Oct;31(10):1139-52 PMID: 10582343
  34. UV-Induced stabilization of c-fos and other short-lived mRNAs.
    Mol Cell Biol. 2000 May;20(10):3616-25 PMID: 10779351
  35. The protein Aly links pre-messenger-RNA splicing to nuclear export in metazoans.
    Nature. 2000 Sep 21;407(6802):401-5 PMID: 11014198
  36. Two closely related human nuclear export factors utilize entirely distinct export pathways.
    Mol Cell. 2001 Aug;8(2):397-406 PMID: 11545741
  37. Pre-mRNA splicing and mRNA export linked by direct interactions between UAP56 and Aly.
    Nature. 2001 Oct 11;413(6856):644-7 PMID: 11675789
  38. Splicing factor Sub2p is required for nuclear mRNA export through its interaction with Yra1p.
    Nature. 2001 Oct 11;413(6856):648-52 PMID: 11675790
  39. The DExH/D box protein HEL/UAP56 is essential for mRNA nuclear export in Drosophila.
    Curr Biol. 2001 Oct 30;11(21):1716-21 PMID: 11696332
  40. The protein Mago provides a link between splicing and mRNA localization.
    EMBO Rep. 2001 Dec;2(12):1119-24 PMID: 11743026
  41. NXF1/p15 heterodimers are essential for mRNA nuclear export in Drosophila.
    RNA. 2001 Dec;7(12):1768-80 PMID: 11780633
  42. The mammalian exosome mediates the efficient degradation of mRNAs that contain AU-rich elements.
    EMBO J. 2002 Jan 15;21(1-2):165-74 PMID: 11782436
  43. A new quantitative method of real time reverse transcription polymerase chain reaction assay based on simulation of polymerase chain reaction kinetics.
    Anal Biochem. 2002 Mar 1;302(1):52-9 PMID: 11846375
  44. Integrating mRNA processing with transcription.
    Cell. 2002 Feb 22;108(4):501-12 PMID: 11909521
  45. A conserved mRNA export machinery coupled to pre-mRNA splicing.
    Cell. 2002 Feb 22;108(4):523-31 PMID: 11909523
  46. An extensive network of coupling among gene expression machines.
    Nature. 2002 Apr 4;416(6880):499-506 PMID: 11932736
  47. In vitro mutagenesis and plasmid shuffling: from cloned gene to mutant yeast.
    Methods Enzymol. 1991;194:302-18 PMID: 2005795
  48. High-level expression in male germ cells of murine P68 RNA helicase mRNA.
    Life Sci. 1993;52(11):917-26 PMID: 8445986
  49. Human cyclin D1 encodes a labile nuclear protein whose synthesis is directly induced by growth factors and suppressed by cyclic AMP.
    J Cell Sci. 1993 Feb;104 ( Pt 2):545-55 PMID: 8389378
  50. Absolute quantification of mRNA using real-time reverse transcription polymerase chain reaction assays.
    J Mol Endocrinol. 2000 Oct;25(2):169-93 PMID: 11013345
  51. The spliceosome deposits multiple proteins 20-24 nucleotides upstream of mRNA exon-exon junctions.
    EMBO J. 2000 Dec 15;19(24):6860-9 PMID: 11118221
  52. Identification and characterization of yUAP/Sub2p, a yeast homolog of the essential human pre-mRNA splicing factor hUAP56.
    Genes Dev. 2001 Jan 1;15(1):30-5 PMID: 11156602
  53. Multiple roles for the yeast SUB2/yUAP56 gene in splicing.
    Genes Dev. 2001 Jan 1;15(1):36-41 PMID: 11156603
  54. Deletion of MUD2, the yeast homolog of U2AF65, can bypass the requirement for sub2, an essential spliceosomal ATPase.
    Genes Dev. 2001 Jan 1;15(1):42-9 PMID: 11156604
  55. Specific alterations of U1-C protein or U1 small nuclear RNA can eliminate the requirement of Prp28p, an essential DEAD box splicing factor.
    Mol Cell. 2001 Jan;7(1):227-32 PMID: 11172727
  56. The exon-exon junction complex provides a binding platform for factors involved in mRNA export and nonsense-mediated mRNA decay.
    EMBO J. 2001 Sep 3;20(17):4987-97 PMID: 11532962
  57. TREX is a conserved complex coupling transcription with messenger RNA export.
    Nature. 2002 May 16;417(6886):304-8 PMID: 11979277
Article Info
Journal
Nucleic acids research
Abbr.
Nucleic Acids Res
ISSN
1362-4962
Published
2004-00-00
Epub
2004-00-26
Pages
1857-65
Language
English
Region
England
NLM ID
0411011
PMCID
PMC390356
Subset
IM
Grants
NCI NIH HHS · P30 CA016058 · United States
NCI NIH HHS · CA16058 · United States
NIGMS NIH HHS · GM29356 · United States
NIGMS NIH HHS · GM48752 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com