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PMID: 11720287 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Cellular mutants define a common mRNA degradation pathway targeting cytokine AU-rich elements.

RNA (New York, N.Y.) ·Vol. 7 ·No. 11 ·2001-11-00 ·Pages 1578-88

Stoecklin G, Stoeckle P, Lu M, Muehlemann O, Moroni C

Abstract

To functionally classify AU-rich elements (AREs) from six different cytokine mRNAs, we made use of two previously described HT1080-derived cellular mutants (slowA, slowC) that lack a function required for the rapid degradation of interleukin-3 (IL-3) mRNA. Here we show that the defect is specific for ARE-containing mRNAs, whereas nonsense-mediated decay is intact. Degradation of beta-globin reporter transcripts mediated by the AREs of IL-3, GM-CSF, and TNFalpha, as well as by the structurally different and less potent AREs of IL-2 and IL-6, is impaired in both mutants. All these reporter transcripts are also sensitive to decay induced by ectopic expression of the RNA-binding protein tristetraprolin in the slowC background. Thus, we concluded that the mutants slowA and slowC define a common mRNA degradation pathway that targets cytokine AREs. In NIH3T3 cells, this decay pathway becomes incapacitated by upstream signaling from p38 MAP- or PI3-kinases, which independently stabilize cytokine ARE-containing transcripts. In contrast, c-fos ARE-directed mRNA degradation proceeds through a different pathway not affected by these kinases.

MeSH Terms
3' Untranslated Regions/metabolism 3T3 Cells Animals Base Sequence Codon, Nonsense Cytokines/genetics DNA-Binding Proteins Enzyme Activation Granulocyte-Macrophage Colony-Stimulating Factor/genetics Humans Immediate-Early Proteins/metabolism Interleukin-2/genetics Interleukin-3/genetics Interleukin-4/genetics Interleukin-6/genetics Mice Mitogen-Activated Protein Kinases/metabolism Molecular Sequence Data Mutagenesis Phosphatidylinositol 3-Kinases/metabolism RNA RNA Stability RNA, Messenger/metabolism RNA-Binding Proteins/metabolism Response Elements Tristetraprolin Tumor Cells, Cultured Tumor Necrosis Factor-alpha/genetics Zinc Fingers p38 Mitogen-Activated Protein Kinases
Chemicals
3' Untranslated Regions Codon, Nonsense Cytokines DNA-Binding Proteins Immediate-Early Proteins Interleukin-2 Interleukin-3 Interleukin-6 RNA, Messenger RNA-Binding Proteins Tristetraprolin Tumor Necrosis Factor-alpha ZFP36 protein, human Zfp36 protein, mouse Interleukin-4 RNA Granulocyte-Macrophage Colony-Stimulating Factor Phosphatidylinositol 3-Kinases Mitogen-Activated Protein Kinases p38 Mitogen-Activated Protein Kinases
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Stoecklin G
Institute of Medical Microbiology, University of Basel, Switzerland.
Stoeckle P
Lu M
Muehlemann O
Moroni C
References (52)
52 references, click to expand
  1. The cap-to-tail guide to mRNA turnover.
    Nat Rev Mol Cell Biol. 2001 Apr;2(4):237-46 PMID: 11283721
  2. Regulation of cyclooxygenase 2 mRNA stability by the mitogen-activated protein kinase p38 signaling cascade.
    Mol Cell Biol. 2000 Jun;20(12):4265-74 PMID: 10825190
  3. Aberrant c-myc RNAs of Burkitt's lymphoma cells have longer half-lives.
    EMBO J. 1985 Dec 30;4(13B):3717-25 PMID: 3004968
  4. Identification of a common nucleotide sequence in the 3'-untranslated region of mRNA molecules specifying inflammatory mediators.
    Proc Natl Acad Sci U S A. 1986 Mar;83(6):1670-4 PMID: 2419912
  5. 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
  6. Rapid cytoplasmic turnover of c-myc mRNA: requirement of the 3' untranslated sequences.
    Mol Cell Biol. 1987 Dec;7(12):4513-21 PMID: 3325826
  7. Cloning of tetradecanoyl phorbol ester-induced 'primary response' sequences and their expression in density-arrested Swiss 3T3 cells and a TPA non-proliferative variant.
    Oncogene. 1987;1(3):263-70 PMID: 3330774
  8. 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
  9. GM-CSF and oncogene mRNA stabilities are independently regulated in trans in a mouse monocytic tumor.
    Cell. 1988 Dec 23;55(6):1115-22 PMID: 3060261
  10. 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
  11. Regulation of lymphokine messenger RNA stability by a surface-mediated T cell activation pathway.
    Science. 1989 Apr 21;244(4902):339-43 PMID: 2540528
  12. Regulation of interleukin 3 mRNA expression in mast cells occurs at the posttranscriptional level and is mediated by calcium ions.
    Proc Natl Acad Sci U S A. 1990 Jan;87(2):777-81 PMID: 2105489
  13. Advanced mammalian gene transfer: high titre retroviral vectors with multiple drug selection markers and a complementary helper-free packaging cell line.
    Nucleic Acids Res. 1990 Jun 25;18(12):3587-96 PMID: 2194165
  14. Rapid insulin-stimulated accumulation of an mRNA encoding a proline-rich protein.
    J Biol Chem. 1990 Sep 25;265(27):16556-63 PMID: 2204625
  15. Role of AUUU sequences in stabilization of granulocyte-macrophage colony-stimulating factor RNA in stimulated cells.
    Blood. 1991 Oct 15;78(8):2005-12 PMID: 1717077
  16. Stability changes in pim-1 proto-oncogene mRNA after mitogen stimulation of normal lymphocytes.
    J Immunol. 1991 Nov 15;147(10):3653-9 PMID: 1940364
  17. Cyclosporin A inhibits growth of autocrine tumour cell lines by destabilizing interleukin-3 mRNA.
    Nature. 1994 May 19;369(6477):239-42 PMID: 8183344
  18. Rearrangement of CCND1 (BCL1/PRAD1) 3' untranslated region in mantle-cell lymphomas and t(11q13)-associated leukemias.
    Blood. 1994 Jun 15;83(12):3689-96 PMID: 8204893
  19. A truncated cyclin D1 gene encodes a stable mRNA in a human breast cancer cell line.
    Oncogene. 1994 Jul;9(7):1925-9 PMID: 8208539
  20. 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
  21. Multiple instability-regulating sites in the 3' untranslated region of the urokinase-type plasminogen activator mRNA.
    Mol Cell Biol. 1994 Jul;14(7):4920-8 PMID: 8007988
  22. Functional hierarchy of AUUUA motifs in mediating rapid interleukin-3 mRNA decay.
    J Biol Chem. 1994 Nov 18;269(46):28591-7 PMID: 7961806
  23. AUUUA is not sufficient to promote poly(A) shortening and degradation of an mRNA: the functional sequence within AU-rich elements may be UUAUUUA(U/A)(U/A).
    Mol Cell Biol. 1994 Dec;14(12):7984-95 PMID: 7969138
  24. 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
  25. The nonamer UUAUUUAUU is the key AU-rich sequence motif that mediates mRNA degradation.
    Mol Cell Biol. 1995 Apr;15(4):2219-30 PMID: 7891716
  26. Degradation of mRNA in eukaryotes.
    Cell. 1995 Apr 21;81(2):179-83 PMID: 7736570
  27. AU-rich elements: characterization and importance in mRNA degradation.
    Trends Biochem Sci. 1995 Nov;20(11):465-70 PMID: 8578590
  28. 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
  29. 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
  30. Impaired interleukin-3 mRNA decay in autocrine mast cell tumors after transient calcium ionophore stimulation.
    Growth Factors. 1996;13(1-2):99-110 PMID: 8804994
  31. Interrelationships of the pathways of mRNA decay and translation in eukaryotic cells.
    Annu Rev Biochem. 1996;65:693-739 PMID: 8811193
  32. A splicing-dependent regulatory mechanism that detects translation signals.
    EMBO J. 1996 Nov 1;15(21):5965-75 PMID: 8918474
  33. A cytokine mRNA-destabilizing element that is structurally and functionally distinct from A+U-rich elements.
    Proc Natl Acad Sci U S A. 1996 Nov 26;93(24):13721-5 PMID: 8943001
  34. T cell receptor (TCR) mini-gene mRNA expression regulated by nonsense codons: a nuclear-associated translation-like mechanism.
    J Exp Med. 1997 Mar 17;185(6):985-92 PMID: 9091590
  35. A negative role for phosphoinositide 3-kinase in T-cell antigen receptor function.
    Curr Biol. 1997 May 1;7(5):285-93 PMID: 9115394
  36. 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
  37. 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
  38. RNA stabilization by the AU-rich element binding protein, HuR, an ELAV protein.
    EMBO J. 1998 Jun 15;17(12):3461-70 PMID: 9628881
  39. Stabilization of interleukin-2 mRNA by the c-Jun NH2-terminal kinase pathway.
    Science. 1998 Jun 19;280(5371):1945-9 PMID: 9632395
  40. Feedback inhibition of macrophage tumor necrosis factor-alpha production by tristetraprolin.
    Science. 1998 Aug 14;281(5379):1001-5 PMID: 9703499
  41. c-jun N-terminal kinase is involved in AUUUA-mediated interleukin-3 mRNA turnover in mast cells.
    EMBO J. 1998 Oct 15;17(20):6039-48 PMID: 9774347
  42. A perfect message: RNA surveillance and nonsense-mediated decay.
    Cell. 1999 Feb 5;96(3):307-10 PMID: 10025395
  43. Control of mRNA decay by heat shock-ubiquitin-proteasome pathway.
    Science. 1999 Apr 16;284(5413):499-502 PMID: 10205060
  44. Evidence that tristetraprolin binds to AU-rich elements and promotes the deadenylation and destabilization of tumor necrosis factor alpha mRNA.
    Mol Cell Biol. 1999 Jun;19(6):4311-23 PMID: 10330172
  45. mRNA surveillance in eukaryotes: kinetic proofreading of proper translation termination as assessed by mRNP domain organization?
    RNA. 1999 Jun;5(6):711-9 PMID: 10376871
  46. CD28-Mediated regulation of mRNA stability requires sequences within the coding region of the IL-2 mRNA.
    J Immunol. 1999 Jul 1;163(1):120-9 PMID: 10384107
  47. 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
  48. 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
  49. 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
  50. Somatic mRNA turnover mutants implicate tristetraprolin in the interleukin-3 mRNA degradation pathway.
    Mol Cell Biol. 2000 Jun;20(11):3753-63 PMID: 10805719
  51. Nucleolin and YB-1 are required for JNK-mediated interleukin-2 mRNA stabilization during T-cell activation.
    Genes Dev. 2000 May 15;14(10):1236-48 PMID: 10817758
  52. Parallel and independent regulation of interleukin-3 mRNA turnover by phosphatidylinositol 3-kinase and p38 mitogen-activated protein kinase.
    Mol Cell Biol. 2001 Sep;21(17):5778-89 PMID: 11486017
Article Info
Journal
RNA (New York, N.Y.)
Abbr.
RNA
ISSN
1355-8382
Published
2001-11-00
Pages
1578-88
Language
English
Region
United States
NLM ID
9509184
PMCID
PMC1370200
Subset
IM
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