Home LiteratureArticle Details
PMID: 12944492 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Selective degradation of AU-rich mRNAs promoted by the p37 AUF1 protein isoform.

Molecular and cellular biology ·Vol. 23 ·No. 18 ·2003-09-00 ·Pages 6685-93

Sarkar B, Xi Q, He C, Schneider RJ

Abstract

An AU-rich element (ARE) consisting of repeated canonical AUUUA motifs confers rapid degradation to many cytokine mRNAs when present in the 3' untranslated region. Destabilization of mRNAs with AREs (ARE-mRNAs) is consistent with the interaction of ARE-binding proteins such as tristetraprolin and the four AUF1 isoforms. However, the association of the AUF1-mRNA interaction with decreased ARE-mRNA stability is correlative and has not been directly tested. We therefore determined whether overexpression of AUF1 isoforms promotes ARE-mRNA destabilization and whether AUF1 isoforms are limiting components for ARE-mRNA decay. We show that the p37 AUF1 isoform and, to a lesser extent, the p40 isoform possess ARE-mRNA-destabilizing activity when overexpressed. Surprisingly, overexpressed p37 AUF1 also destabilized reporter mRNAs containing a noncanonical but AU-rich 3' untranslated region. Since overexpressed p37 AUF1 could interact in vivo with the AU-rich reporter mRNA, AUF1 may be involved in rapid turnover of mRNAs that lack canonical AREs. Moreover, overexpression of p37 AUF1 restored the ability of cells to rapidly degrade ARE-mRNAs when that ability was saturated and inhibited by overexpression of ARE-mRNAs. Finally, activation of ARE-mRNA decay often involves a translation-dependent step, which was eliminated by overexpression of p37 AUF1. These data indicate that the p37 AUF1 isoform and, to some extent, the p40 isoform are limiting factors that facilitate rapid decay of AU-rich mRNAs.

MeSH Terms
Animals Base Sequence Cell Line Cycloheximide/pharmacology Gene Expression Regulation Heterogeneous Nuclear Ribonucleoprotein D0 Heterogeneous-Nuclear Ribonucleoprotein D/drug effects,genetics,metabolism Humans Mice Molecular Sequence Data Protein Biosynthesis Protein Isoforms RNA Stability RNA, Messenger/drug effects,metabolism
Chemicals
HNRNPD protein, human Heterogeneous Nuclear Ribonucleoprotein D0 Heterogeneous-Nuclear Ribonucleoprotein D Hnrpd protein, mouse Protein Isoforms RNA, Messenger Cycloheximide
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Sarkar Bedabrata
Department of Microbiology, New York University School of Medicine, 550 First Avenue, New York, NY 10016, USA.
Xi Qiaoran
He Cheng
Schneider Robert J
References (54)
54 references, click to expand
  1. Developmental regulation of RNA transcript destabilization by A + U-rich elements is AUF1-dependent.
    J Biol Chem. 1999 Nov 26;274(48):33973-8 PMID: 10567360
  2. Nuclear proteins that bind the pre-mRNA 3' splice site sequence r(UUAG/G) and the human telomeric DNA sequence d(TTAGGG)n.
    Mol Cell Biol. 1993 Jul;13(7):4301-10 PMID: 8321232
  3. Testosterone and dihydrotestosterone regulate AUF1 isoforms in a tissue-specific fashion in the mouse.
    Am J Physiol Endocrinol Metab. 2000 Jan;278(1):E50-7 PMID: 10644536
  4. 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
  5. Hypoxic stabilization of vascular endothelial growth factor mRNA by the RNA-binding protein HuR.
    J Biol Chem. 1998 Mar 13;273(11):6417-23 PMID: 9497373
  6. Structure and genomic organization of the human AUF1 gene: alternative pre-mRNA splicing generates four protein isoforms.
    Genomics. 1998 Mar 1;48(2):195-202 PMID: 9521873
  7. 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
  8. RNA stabilization by the AU-rich element binding protein, HuR, an ELAV protein.
    EMBO J. 1998 Jun 15;17(12):3461-70 PMID: 9628881
  9. Developmental expression of AUF1 and HuR, two c-myc mRNA binding proteins.
    Oncogene. 1998 Jul 2;16(26):3413-21 PMID: 9692549
  10. ELAV proteins stabilize deadenylated intermediates in a novel in vitro mRNA deadenylation/degradation system.
    Genes Dev. 1999 Jan 15;13(2):188-201 PMID: 9925643
  11. The search for trans-acting factors controlling messenger RNA decay.
    Prog Nucleic Acid Res Mol Biol. 1999;62:257-91 PMID: 9932457
  12. Heterogeneous nuclear ribonucleoprotein D0B is a sequence-specific DNA-binding protein.
    Biochem J. 1999 Mar 1;338 ( Pt 2):417-25 PMID: 10024518
  13. Control of mRNA decay by heat shock-ubiquitin-proteasome pathway.
    Science. 1999 Apr 16;284(5413):499-502 PMID: 10205060
  14. Unraveling a cytoplasmic role for hnRNP D in the in vivo mRNA destabilization directed by the AU-rich element.
    Genes Dev. 1999 Jul 15;13(14):1884-97 PMID: 10421639
  15. hnRNP A2 and hnRNP L bind the 3'UTR of glucose transporter 1 mRNA and exist as a complex in vivo.
    Biochem Biophys Res Commun. 1999 Aug 11;261(3):646-51 PMID: 10441480
  16. Evidence that tristetraprolin is a physiological regulator of granulocyte-macrophage colony-stimulating factor messenger RNA deadenylation and stability.
    Blood. 2000 Mar 15;95(6):1891-9 PMID: 10706852
  17. HuR binding to cytoplasmic mRNA is perturbed by heat shock.
    Proc Natl Acad Sci U S A. 2000 Mar 28;97(7):3073-8 PMID: 10737787
  18. Interactions of CCCH zinc finger proteins with mRNA. Binding of tristetraprolin-related zinc finger proteins to Au-rich elements and destabilization of mRNA.
    J Biol Chem. 2000 Jun 9;275(23):17827-37 PMID: 10751406
  19. Differential expression and localization of the mRNA binding proteins, AU-rich element mRNA binding protein (AUF1) and Hu antigen R (HuR), in neoplastic lung tissue.
    Mol Carcinog. 2000 Jun;28(2):76-83 PMID: 10900464
  20. Regulation of the Epstein-Barr virus C promoter by AUF1 and the cyclic AMP/protein kinase A signaling pathway.
    J Virol. 2000 Sep;74(17):8166-75 PMID: 10933728
  21. Complex contribution of the 3'-untranslated region to the expressional regulation of the human inducible nitric-oxide synthase gene. Involvement of the RNA-binding protein HuR.
    J Biol Chem. 2000 Aug 25;275(34):26040-9 PMID: 10859327
  22. ARED: human AU-rich element-containing mRNA database reveals an unexpectedly diverse functional repertoire of encoded proteins.
    Nucleic Acids Res. 2001 Jan 1;29(1):246-54 PMID: 11125104
  23. A novel mRNA-decapping activity in HeLa cytoplasmic extracts is regulated by AU-rich elements.
    EMBO J. 2001 Mar 1;20(5):1134-43 PMID: 11230136
  24. Regulation of mRNA stability in mammalian cells.
    Gene. 2001 Mar 7;265(1-2):11-23 PMID: 11255003
  25. Versatile role for hnRNP D isoforms in the differential regulation of cytoplasmic mRNA turnover.
    Mol Cell Biol. 2001 Oct;21(20):6960-71 PMID: 11564879
  26. Ubiquitin-dependent mechanism regulates rapid turnover of AU-rich cytokine mRNAs.
    Proc Natl Acad Sci U S A. 2002 Feb 19;99(4):1842-6 PMID: 11842200
  27. Correlation between intrinsic mRNA stability and the affinity of AUF1 (hnRNP D) and HuR for A+U-rich mRNAs.
    Mol Cell Biochem. 2002 Mar;232(1-2):1-11 PMID: 12030365
  28. Translation is required to remove Y14 from mRNAs in the cytoplasm.
    Curr Biol. 2002 Jul 9;12(13):1060-7 PMID: 12121612
  29. Alternate exon insertion controls selective ubiquitination and degradation of different AUF1 protein isoforms.
    Nucleic Acids Res. 2002 Jul 15;30(14):3052-8 PMID: 12136087
  30. Lactate dehydrogenase is an AU-rich element-binding protein that directly interacts with AUF1.
    J Biol Chem. 2002 Sep 20;277(38):35738-45 PMID: 12107167
  31. NF-kappaB regulates the expression of the human complement receptor 2 gene.
    J Immunol. 2002 Dec 1;169(11):6236-43 PMID: 12444129
  32. A conserved AU sequence from the 3' untranslated region of GM-CSF mRNA mediates selective mRNA degradation.
    Cell. 1986 Aug 29;46(5):659-67 PMID: 3488815
  33. 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
  34. Regulation of c-myc mRNA stability in vitro by a labile destabilizer with an essential nucleic acid component.
    Mol Cell Biol. 1989 May;9(5):1996-2006 PMID: 2747642
  35. 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
  36. An A + U-rich element RNA-binding factor regulates c-myc mRNA stability in vitro.
    Mol Cell Biol. 1991 May;11(5):2460-6 PMID: 1901943
  37. Evidence for instability of mRNAs containing AUUUA motifs mediated through translation-dependent assembly of a > 20S degradation complex.
    Genes Dev. 1992 Oct;6(10):1927-39 PMID: 1398070
  38. Selective destabilization of short-lived mRNAs with the granulocyte-macrophage colony-stimulating factor AU-rich 3' noncoding region is mediated by a cotranslational mechanism.
    Mol Cell Biol. 1993 Mar;13(3):1971-80 PMID: 8382780
  39. 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
  40. 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
  41. Enhanced stability of interleukin-2 mRNA in MLA 144 cells. Possible role of cytoplasmic AU-rich sequence-binding proteins.
    J Biol Chem. 1994 Feb 18;269(7):5377-83 PMID: 8106521
  42. LR1 regulates c-myc transcription in B-cell lymphomas.
    Proc Natl Acad Sci U S A. 1994 May 24;91(11):4915-9 PMID: 8197157
  43. Rapid mRNA degradation mediated by the c-fos 3' AU-rich element and that mediated by the granulocyte-macrophage colony-stimulating factor 3' AU-rich element occur through similar polysome-associated mechanisms.
    Mol Cell Biol. 1995 Jul;15(7):3796-804 PMID: 7540719
  44. The UUAG-specific RNA binding protein, heterogeneous nuclear ribonucleoprotein D0. Common modular structure and binding properties of the 2xRBD-Gly family.
    J Biol Chem. 1995 Sep 22;270(38):22167-75 PMID: 7673195
  45. Rapid degradation of AU-rich element (ARE) mRNAs is activated by ribosome transit and blocked by secondary structure at any position 5' to the ARE.
    Mol Cell Biol. 1995 Nov;15(11):6331-40 PMID: 7565786
  46. Cloning and characterization of HuR, a ubiquitously expressed Elav-like protein.
    J Biol Chem. 1996 Apr 5;271(14):8144-51 PMID: 8626503
  47. Regulation of the mRNA-binding protein AUF1 by activation of the beta-adrenergic receptor signal transduction pathway.
    J Biol Chem. 1996 Apr 5;271(14):8493-501 PMID: 8626551
  48. AUF1 binding affinity to A+U-rich elements correlates with rapid mRNA degradation.
    J Biol Chem. 1996 May 24;271(21):12179-84 PMID: 8647811
  49. A pathogenetic role for TNF alpha in the syndrome of cachexia, arthritis, and autoimmunity resulting from tristetraprolin (TTP) deficiency.
    Immunity. 1996 May;4(5):445-54 PMID: 8630730
  50. Turnover and translation of in vitro synthesized messenger RNAs in transfected, normal cells.
    J Biol Chem. 1996 Aug 16;271(33):19871-6 PMID: 8702698
  51. Increased granulocyte-macrophage colony-stimulating factor mRNA instability in cord versus adult mononuclear cells is translation-dependent and associated with increased levels of A + U-rich element binding factor.
    Blood. 1996 Oct 15;88(8):2889-97 PMID: 8874185
  52. Adhesion-dependent regulation of an A+U-rich element-binding activity associated with AUF1.
    Mol Cell Biol. 1997 Jul;17(7):3898-906 PMID: 9199324
  53. Structural determinants in AUF1 required for high affinity binding to A + U-rich elements.
    J Biol Chem. 1997 Oct 31;272(44):27635-43 PMID: 9346902
  54. HuR regulates p21 mRNA stabilization by UV light.
    Mol Cell Biol. 2000 Feb;20(3):760-9 PMID: 10629032
Article Info
Journal
Molecular and cellular biology
Abbr.
Mol Cell Biol
ISSN
0270-7306
Published
2003-09-00
Pages
6685-93
Language
English
Region
United States
NLM ID
8109087
PMCID
PMC193711
Subset
IM
Grants
NIGMS NIH HHS · R01 GM060428 · United States
NCI NIH HHS · T32 CA009161 · United States
NCI NIH HHS · 5T32 CA 09161 · United States
NIGMS NIH HHS · GM 60428 · 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