Home LiteratureArticle Details
PMID: 9628881 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

RNA stabilization by the AU-rich element binding protein, HuR, an ELAV protein.

The EMBO journal ·Vol. 17 ·No. 12 ·1998-06-15 ·Pages 3461-70

Peng SS, Chen CY, Xu N, Shyu AB

Abstract

An important paradigm for post-transcriptional regulation is the control of cytoplasmic mRNA stability mediated by AU-rich elements (AREs) in the 3' untranslated region of transcripts encoding oncoproteins, cytokines and transcription factors. While many RNA-binding proteins have been shown to bind to AREs in vitro, neither the functional consequences nor the physiological significance of their interactions are known. Here we demonstrate a role for the embryonic lethal abnormal visual (ELAV) RNA-binding protein HuR in mRNA turnover in vivo. The ELAV family of RNA-binding proteins is highly conserved in vertebrates. In humans, there are four members; HuR is expressed in all proliferating cells, whereas Hel-N1, HuC and HuD are expressed in terminally differentiated neurons. We show that elevation of cytoplasmic HuR levels inhibits c-fos ARE-mediated RNA decay but has little effect on rapid decay directed by c-jun ARE. It appears that HuR has little effect on deadenylation but delays onset of decay of the RNA body and slows down its subsequent decay. We also show that HuR can be induced to redistribute from the nucleus to the cytoplasm and that this redistribution is associated with an altered function. Modulation of the ARE-mediated decay pathway through controlling distribution of the ELAV proteins between nucleus and cytoplasm may be a mechanism by which cell growth and differentiation is regulated.

MeSH Terms
3T3 Cells Animals Antigens, Surface Cell Nucleus/metabolism Cytoplasm/metabolism ELAV Proteins ELAV-Like Protein 1 Genes, fos/physiology Genes, jun/physiology Humans Mice RNA Processing, Post-Transcriptional RNA, Messenger/metabolism RNA-Binding Proteins/metabolism Ribonucleoproteins/metabolism
Chemicals
Antigens, Surface ELAV Proteins ELAV-Like Protein 1 ELAVL1 protein, human RNA, Messenger RNA-Binding Proteins Ribonucleoproteins
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Peng S S
Department of Biochemistry and Molecular Biology, University of Texas Houston Health Science Center Medical School, Houston, TX 77030, USA.
Chen C Y
Xu N
Shyu A B
References (43)
43 references, click to expand
  1. The c-fos transcript is targeted for rapid decay by two distinct mRNA degradation pathways.
    Genes Dev. 1989 Jan;3(1):60-72 PMID: 2496006
  2. Overexpression of HuR, a nuclear-cytoplasmic shuttling protein, increases the in vivo stability of ARE-containing mRNAs.
    EMBO J. 1998 Jun 15;17(12):3448-60 PMID: 9628880
  3. Two distinct destabilizing elements in the c-fos message trigger deadenylation as a first step in rapid mRNA decay.
    Genes Dev. 1991 Feb;5(2):221-31 PMID: 1899842
  4. Transcription-dependent and transcription-independent nuclear transport of hnRNP proteins.
    Science. 1991 Jul 19;253(5017):312-4 PMID: 1857966
  5. Tight control of gene expression in mammalian cells by tetracycline-responsive promoters.
    Proc Natl Acad Sci U S A. 1992 Jun 15;89(12):5547-51 PMID: 1319065
  6. U-rich sequence-binding proteins (URBPs) interacting with a 20-nucleotide U-rich sequence in the 3' untranslated region of c-fos mRNA may be involved in the first step of c-fos mRNA degradation.
    Mol Cell Biol. 1992 Jul;12(7):2931-40 PMID: 1620106
  7. Association of heterogeneous nuclear ribonucleoprotein A1 and C proteins with reiterated AUUUA sequences.
    J Biol Chem. 1993 Apr 25;268(12):8881-7 PMID: 8473331
  8. Hel-N1: an autoimmune RNA-binding protein with specificity for 3' uridylate-rich untranslated regions of growth factor mRNAs.
    Mol Cell Biol. 1993 Jun;13(6):3494-504 PMID: 8497264
  9. Purification, characterization, and cDNA cloning of an AU-rich element RNA-binding protein, AUF1.
    Mol Cell Biol. 1993 Dec;13(12):7652-65 PMID: 8246982
  10. Interplay of two functionally and structurally distinct domains of the c-fos AU-rich element specifies its mRNA-destabilizing function.
    Mol Cell Biol. 1994 Jan;14(1):416-26 PMID: 7903419
  11. A novel strategy for the immunological tagging of cDNA constructs.
    Gene. 1993 Dec 27;137(1):139-43 PMID: 7506688
  12. Purification of an AU-rich RNA binding protein from Sarcophaga peregrina (flesh fly) and its identification as a Thiolase.
    J Biochem. 1993 Sep;114(3):432-7 PMID: 7904267
  13. Cyclosporin A inhibits growth of autocrine tumour cell lines by destabilizing interleukin-3 mRNA.
    Nature. 1994 May 19;369(6477):239-42 PMID: 8183344
  14. Selective degradation of early-response-gene mRNAs: functional analyses of sequence features of the AU-rich elements.
    Mol Cell Biol. 1994 Dec;14(12):8471-82 PMID: 7969180
  15. Selection of a subset of mRNAs from combinatorial 3' untranslated region libraries using neuronal RNA-binding protein Hel-N1.
    Proc Natl Acad Sci U S A. 1994 Nov 8;91(23):11207-11 PMID: 7972035
  16. Glyceraldehyde-3-phosphate dehydrogenase selectively binds AU-rich RNA in the NAD(+)-binding region (Rossmann fold).
    J Biol Chem. 1995 Feb 10;270(6):2755-63 PMID: 7531693
  17. AUH, a gene encoding an AU-specific RNA binding protein with intrinsic enoyl-CoA hydratase activity.
    Proc Natl Acad Sci U S A. 1995 Mar 14;92(6):2051-5 PMID: 7892223
  18. A conserved family of elav-like genes in vertebrates.
    Proc Natl Acad Sci U S A. 1995 May 9;92(10):4557-61 PMID: 7753842
  19. 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
  20. Short- and long-term mechanisms of tau regulation in PC12 cells.
    J Cell Sci. 1995 Aug;108 ( Pt 8):2857-64 PMID: 7593325
  21. mRNA stability in mammalian cells.
    Microbiol Rev. 1995 Sep;59(3):423-50 PMID: 7565413
  22. When cells stop making sense: effects of nonsense codons on RNA metabolism in vertebrate cells.
    RNA. 1995 Jul;1(5):453-65 PMID: 7489507
  23. AU-rich elements: characterization and importance in mRNA degradation.
    Trends Biochem Sci. 1995 Nov;20(11):465-70 PMID: 8578590
  24. Purification and properties of HuD, a neuronal RNA-binding protein.
    J Biol Chem. 1996 May 10;271(19):11518-24 PMID: 8626712
  25. Cloning and characterization of HuR, a ubiquitously expressed Elav-like protein.
    J Biol Chem. 1996 Apr 5;271(14):8144-51 PMID: 8626503
  26. Functional characterization of a non-AUUUA AU-rich element from the c-jun proto-oncogene mRNA: evidence for a novel class of AU-rich elements.
    Mol Cell Biol. 1996 Apr;16(4):1490-9 PMID: 8657122
  27. From transcript to protein.
    Cell. 1996 Jun 28;85(7):963-72 PMID: 8674124
  28. Interrelationships of the pathways of mRNA decay and translation in eukaryotic cells.
    Annu Rev Biochem. 1996;65:693-739 PMID: 8811193
  29. Hel-N1/Hel-N2 proteins are bound to poly(A)+ mRNA in granular RNP structures and are implicated in neuronal differentiation.
    J Cell Sci. 1996 Mar;109 ( Pt 3):579-89 PMID: 8907704
  30. Ectopic expression of Hel-N1, an RNA-binding protein, increases glucose transporter (GLUT1) expression in 3T3-L1 adipocytes.
    Mol Cell Biol. 1997 Feb;17(2):954-62 PMID: 9001249
  31. Two different RNA binding activities for the AU-rich element and the poly(A) sequence of the mouse neuronal protein mHuC.
    Nucleic Acids Res. 1996 Dec 15;24(24):4895-901 PMID: 9016658
  32. The Elav-like proteins bind to a conserved regulatory element in the 3'-untranslated region of GAP-43 mRNA.
    J Biol Chem. 1997 Mar 7;272(10):6593-8 PMID: 9045688
  33. A hierarchy of Hu RNA binding proteins in developing and adult neurons.
    J Neurosci. 1997 May 1;17(9):3024-37 PMID: 9096138
  34. Nucleocytoplasmic transport: signals, mechanisms and regulation.
    Nature. 1997 Apr 24;386(6627):779-87 PMID: 9126736
  35. Life and death in the cytoplasm: messages from the 3' end.
    Curr Opin Genet Dev. 1997 Apr;7(2):220-32 PMID: 9115434
  36. Identification of HuR as a protein implicated in AUUUA-mediated mRNA decay.
    EMBO J. 1997 Apr 15;16(8):2130-9 PMID: 9155038
  37. Nuclear export of proteins and RNAs.
    Curr Opin Cell Biol. 1997 Jun;9(3):420-9 PMID: 9159083
  38. Modulation of the fate of cytoplasmic mRNA by AU-rich elements: key sequence features controlling mRNA deadenylation and decay.
    Mol Cell Biol. 1997 Aug;17(8):4611-21 PMID: 9234718
  39. The Elav-like proteins bind to AU-rich elements and to the poly(A) tail of mRNA.
    Nucleic Acids Res. 1997 Sep 15;25(18):3564-9 PMID: 9278474
  40. Sequential expression and role of Hu RNA-binding proteins during neurogenesis.
    Development. 1997 Sep;124(17):3449-60 PMID: 9310339
  41. Embryonic lethal abnormal visual RNA-binding proteins involved in growth, differentiation, and posttranscriptional gene expression.
    Am J Hum Genet. 1997 Aug;61(2):273-8 PMID: 9311730
  42. A broader role for AU-rich element-mediated mRNA turnover revealed by a new transcriptional pulse strategy.
    Nucleic Acids Res. 1998 Jan 15;26(2):558-65 PMID: 9421516
  43. Regulation of lymphokine messenger RNA stability by a surface-mediated T cell activation pathway.
    Science. 1989 Apr 21;244(4902):339-43 PMID: 2540528
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
Published
1998-06-15
Pages
3461-70
Language
English
Region
England
NLM ID
8208664
PMCID
PMC1170682
Subset
IM
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