Home LiteratureArticle Details
PMID: 12885872 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Regulation of cyclooxygenase-2 expression by the translational silencer TIA-1.

The Journal of experimental medicine ·Vol. 198 ·No. 3 ·2003-08-04 ·Pages 475-81

Dixon DA, Balch GC, Kedersha N, Anderson P, Zimmerman GA, Beauchamp RD, Prescott SM

Abstract

The cyclooxygenase-2 (COX-2) enzyme catalyzes the rate-limiting step of prostaglandin formation in inflammatory states, and COX-2 overexpression plays a key role in carcinogenesis. To understand the mechanisms regulating COX-2 expression, we examined its posttranscriptional regulation mediated through the AU-rich element (ARE) within the COX-2 mRNA 3'-untranslated region (3'UTR). RNA binding studies, performed to identify ARE-binding regulatory factors, demonstrated binding of the translational repressor protein TIA-1 to COX-2 mRNA. The significance of TIA-1-mediated regulation of COX-2 expression was observed in TIA-1 null fibroblasts that produced significantly more COX-2 protein than wild-type fibroblasts. However, TIA-1 deficiency did not alter COX-2 transcription or mRNA turnover. Colon cancer cells demonstrated to overexpress COX-2 through increased polysome association with COX-2 mRNA also showed defective TIA-1 binding both in vitro and in vivo. These findings implicate that TIA-1 functions as a translational silencer of COX-2 expression and support the hypothesis that dysregulated RNA-binding of TIA-1 promotes COX-2 expression in neoplasia.

MeSH Terms
Animals Cyclooxygenase 2 Fibroblasts/cytology,metabolism Gene Expression Regulation, Enzymologic Humans Isoenzymes/genetics,metabolism Membrane Proteins/genetics,metabolism Mice Poly(A)-Binding Proteins Prostaglandin-Endoperoxide Synthases/genetics,metabolism Protein Binding Protein Biosynthesis Proteins RNA Processing, Post-Transcriptional RNA, Messenger/metabolism RNA-Binding Proteins/genetics,metabolism Silencer Elements, Transcriptional T-Cell Intracellular Antigen-1 Tumor Cells, Cultured
Chemicals
Isoenzymes Membrane Proteins Poly(A)-Binding Proteins Proteins RNA, Messenger RNA-Binding Proteins T-Cell Intracellular Antigen-1 TIA1 protein, human Tia1 protein, mouse Cyclooxygenase 2 PTGS2 protein, human Prostaglandin-Endoperoxide Synthases
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Dixon Dan A
Surgical Oncology Research Laboratory, Department of Surgery, Vanderbilt University Medical Center, Nashville, TN 37232-2733, USA. dan.dixon@vanderbilt.edu
Balch Glen C
Kedersha Nancy
Anderson Paul
Zimmerman Guy A
Beauchamp R Daniel
Prescott Stephen M
References (21)
21 references, click to expand
  1. Ultraviolet-induced cross-linking of RNA to proteins in vivo.
    Methods Enzymol. 1989;180:410-8 PMID: 2515420
  2. TIA-1 is a translational silencer that selectively regulates the expression of TNF-alpha.
    EMBO J. 2000 Aug 1;19(15):4154-63 PMID: 10921895
  3. 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
  4. RNA-binding proteins TIA-1 and TIAR link the phosphorylation of eIF-2 alpha to the assembly of mammalian stress granules.
    J Cell Biol. 1999 Dec 27;147(7):1431-42 PMID: 10613902
  5. Stressful initiations.
    J Cell Sci. 2002 Aug 15;115(Pt 16):3227-34 PMID: 12140254
  6. Transforming growth factor-beta1 enhances Ha-ras-induced expression of cyclooxygenase-2 in intestinal epithelial cells via stabilization of mRNA.
    J Biol Chem. 2000 Mar 3;275(9):6628-35 PMID: 10692471
  7. A new player in oncogenesis: AUF1/hnRNPD overexpression leads to tumorigenesis in transgenic mice.
    Cancer Res. 2002 Mar 1;62(5):1489-95 PMID: 11888925
  8. Colorectal cancer prevention and treatment by inhibition of cyclooxygenase-2.
    Nat Rev Cancer. 2001 Oct;1(1):11-21 PMID: 11900248
  9. Post-transcriptional control of cyclooxygenase-2 gene expression. The role of the 3'-untranslated region.
    J Biol Chem. 2000 Apr 21;275(16):11750-7 PMID: 10766797
  10. Altered expression of the mRNA stability factor HuR promotes cyclooxygenase-2 expression in colon cancer cells.
    J Clin Invest. 2001 Dec;108(11):1657-65 PMID: 11733561
  11. Misregulated posttranscriptional checkpoints: inflammation and tumorigenesis.
    J Exp Med. 2001 Jan 15;193(2):F1-4 PMID: 11208868
  12. AU-rich element-mediated translational control: complexity and multiple activities of trans-activating factors.
    Biochem Soc Trans. 2002 Nov;30(Pt 6):952-8 PMID: 12440953
  13. Regulation of COX-2 expression in human cancers.
    Prog Exp Tumor Res. 2003;37:52-71 PMID: 12795048
  14. The apoptosis-promoting factor TIA-1 is a regulator of alternative pre-mRNA splicing.
    Mol Cell. 2000 Nov;6(5):1089-98 PMID: 11106748
  15. HuA and tristetraprolin are induced following T cell activation and display distinct but overlapping RNA binding specificities.
    J Biol Chem. 2001 Dec 21;276(51):47958-65 PMID: 11602610
  16. Is cyclooxygenase-2 the alpha and the omega in cancer?
    J Clin Invest. 2000 Jun;105(11):1511-3 PMID: 10841506
  17. 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
  18. Translational control of cytokine expression by 3' UA-rich sequences.
    Biochimie. 1994;76(9):862-6 PMID: 7880903
  19. Intron-exon organization and chromosomal localization of the human TIA-1 gene.
    J Immunol. 1994 May 15;152(10):4937-45 PMID: 8176212
  20. 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
  21. Translational control mediated by UA-rich sequences.
    Enzyme. 1990;44(1-4):193-202 PMID: 2133651
Article Info
Journal
The Journal of experimental medicine
Abbr.
J Exp Med
ISSN
0022-1007
Published
2003-08-04
Epub
2003-00-28
Pages
475-81
Language
English
Region
United States
NLM ID
2985109R
PMCID
PMC2194089
Subset
IM
Grants
NIAID NIH HHS · R01 AI50167 · United States
NIAID NIH HHS · R56 AI033600 · United States
NIAID NIH HHS · R01 AI033600 · United States
NCI NIH HHS · P30 CA68485 · United States
NCI NIH HHS · P01 CA73992 · United States
NCI NIH HHS · CA42014 · United States
NIAID NIH HHS · AI33600 · United States
NCI NIH HHS · P01 CA77839 · United States
NCI NIH HHS · P01 CA077839 · United States
NIAID NIH HHS · R01 AI050167 · United States
NCI NIH HHS · P30 CA068485 · United States
NIDDK NIH HHS · DK-52334 · United States
NCI NIH HHS · P01 CA073992 · United States
NIDDK NIH HHS · R01 DK052334 · United States
NCI NIH HHS · P30 CA042014 · 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