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Citations to this article

Altered expression of the mRNA stability factor HuR promotes cyclooxygenase-2 expression in colon cancer cells
Dan A. Dixon, … , Guy A. Zimmerman, Stephen M. Prescott
Dan A. Dixon, … , Guy A. Zimmerman, Stephen M. Prescott
Published December 1, 2001
Citation Information: J Clin Invest. 2001;108(11):1657-1665. https://doi.org/10.1172/JCI12973.
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Article

Altered expression of the mRNA stability factor HuR promotes cyclooxygenase-2 expression in colon cancer cells

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Abstract

Cyclooxygenase-2 (COX-2) expression is normally tightly regulated. However, constitutive overexpression plays a key role in colon carcinogenesis. To understand the molecular nature of enhanced COX-2 expression detected in colon cancer, we examined the ability of the AU-rich element–containing (ARE-containing) 3′ untranslated region (3′UTR) of COX-2 mRNA to regulate rapid mRNA decay in human colon cancer cells. In tumor cells displaying enhanced growth and tumorigenicity that is correlated with elevated COX-2, vascular endothelial growth factor (VEGF), and IL-8 protein levels, the corresponding mRNAs were transcribed constitutively and turned over slowly. The observed mRNA stabilization is owing to defective recognition of class II-type AREs present within the COX-2, VEGF, and IL-8 3′UTRs; c-myc mRNA, containing a class I ARE decayed rapidly in the same cells. Correlating with cellular defects in mRNA stability, the RNA-binding of trans-acting cellular factors was altered. In particular, we found that the RNA-stability factor HuR binds to the COX-2 ARE, and overexpression of HuR, as detected in tumors, results in elevated expression of COX-2, VEGF, and IL-8. These findings demonstrate the functional significance rapid mRNA decay plays in controlling gene expression and show that dysregulation of these trans-acting factors can lead to overexpression of COX-2 and other angiogenic proteins, as detected in neoplasia.

Authors

Dan A. Dixon, Neal D. Tolley, Peter H. King, L. Burt Nabors, Thomas M. McIntyre, Guy A. Zimmerman, Stephen M. Prescott

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Citations to this article (196)

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N Embade, D Fernández-Ramos, M Varela-Rey, N Beraza, M Sini, VG de Juan, A Woodhoo, N Martínez-López, B Rodríguez-Iruretagoyena, FJ Bustamante, AB de la Hoz, A Carracedo, DP Xirodimas, MS Rodríguez, SC Lu, JM Mato, ML Martínez-Chantar
Hepatology 2012
β-Catenin recognizes a specific RNA motif in the cyclooxygenase-2 mRNA 3′-UTR and interacts with HuR in colon cancer cells
I Kim, H Kwak, HK Lee, S Hyun, S Jeong
Nucleic Acids Research 2012
The novel tumor suppressor NOL7 post-transcriptionally regulates thrombospondin-1 expression
CL Doçi, G Zhou, MW Lingen
Oncogene 2012
Mechanistic and pharmacological issues of aspirin as an anticancer agent
M Dovizio, S Tacconelli, C Sostres, E Ricciotti, P Patrignani
Pharmaceuticals (Basel, Switzerland) 2012
Cyclooxygenase-2 is a target of microRNA-16 in human hepatoma cells
NA Andrieu, O Motiño, R Mayoral, CL Izquierdo, A Fernández-Alvarez, L Boscá, M Casado, P Martín-Sanz
PloS one 2012
The RNA-Binding Protein Musashi1: A Major Player in Intestinal Epithelium Renewal and Colon Cancer Development
M Plateroti, PR de Araujo, AE da Silva, LO Penalva
Current Colorectal Cancer Reports 2012
Tristetraprolin Impairs Myc-Induced Lymphoma and Abolishes the Malignant State
RJ Rounbehler, M Fallahi, C Yang, MA Steeves, W Li, JR Doherty, FX Schaub, S Sanduja, DA Dixon, PJ Blackshear, JL Cleveland
Cell 2012
HuR thermal stability is dependent on domain binding and upon phosphorylation
RM Scheiba, Á Aroca, I Díaz-Moreno
European Biophysics Journal 2012
Perspectives on the ARE as it turns 25 years old
D Beisang, PR Bohjanen
Wiley interdisciplinary reviews. RNA 2012
Prospects for Chemoprevention of Colorectal Neoplasia
AT Chan, E Detering
Prospects for Chemoprevention of Colorectal Neoplasia 2012
HuR function in disease.
Srikantan S, Gorospe M
2012
The role of tristetraprolin in cancer and inflammation.
Sanduja S, Blanco FF, Young LE, Kaza V, Dixon DA
2012
Deep sequencing reveals direct targets of gammaherpesvirus-induced mRNA decay and suggests that multiple mechanisms govern cellular transcript escape
K Clyde, BA Glaunsinger
PloS one 2011
Integrin α3β1 as a breast cancer target
S Subbaram, CM DiPersio
Expert Opinion on Therapeutic Targets 2011
mRNA stability alterations mediated by HuR are necessary to sustain the fast growth of glioma cells
F Bolognani, AI Gallani, L Sokol, DS Baskin, N Meisner-Kober
Journal of Neuro-Oncology 2011
The mRNA-Binding Protein HuR is Regulated in the Menstrual Cycle and Repressed in Ectopic Endometrium
FS Karipcin, TA Ensari, UA Kayisli, E Guzel, CB Kallen, E Seli
Reproductive Sciences 2011
The mRNA stability factor HuR inhibits microRNA-16 targeting of COX-2
LE Young, AE Moore, L Sokol, N Meisner-Kober, DA Dixon
Molecular cancer research : MCR 2011
Chemokine transcripts as targets of the RNA-binding protein HuR in human airway epithelium
J Fan, FT Ishmael, X Fang, A Myers, C Cheadle, SK Huang, U Atasoy, M Gorospe, C Stellato
Journal of immunology (Baltimore, Md. : 1950) 2011
MicroRNA and AU-rich element regulation of prostaglandin synthesis
AE Moore, LE Young, DA Dixon
Cancer and Metastasis Reviews 2011
Coordinate Regulation of GATA-3 and Th2 Cytokine Gene Expression by the RNA-Binding Protein HuR
C Stellato, MM Gubin, JD Magee, X Fang, J Fan, DM Tartar, J Chen, GM Dahm, R Calaluce, F Mori, GA Jackson, V Casolaro, CL Franklin, U Atasoy
Journal of immunology (Baltimore, Md. : 1950) 2011
11-Oxoeicosatetraenoic Acid Is a Cyclooxygenase-2/15-Hydroxyprostaglandin Dehydrogenase-Derived Antiproliferative Eicosanoid
X Liu, S Zhang, JS Arora, NW Snyder, SJ Shah, IA Blair
Chemical Research in Toxicology 2011
The RNA-binding Protein HuR Opposes the Repression of ERBB-2 Gene Expression by MicroRNA miR-331-3p in Prostate Cancer Cells
MR Epis, A Barker, KM Giles, DJ Beveridge, PJ Leedman
The Journal of biological chemistry 2011
RNAi-based strategies for cyclooxygenase-2 inhibition in cancer
A Strillacci, C Griffoni, MC Valerii, G Lazzarini, V Tomasi, E Spisni
Journal of biomedicine & biotechnology 2010
Role of RNA-Binding Proteins in Colorectal Carcinogenesis
S Anant, CW Houchen, V Pawar, S Ramalingam
Current Colorectal Cancer Reports 2010
Reduced nuclear export of HuR mRNA by HuR is linked to the loss of HuR in replicative senescence
J Yi, N Chang, X Liu, G Guo, L Xue, T Tong, M Gorospe, W Wang
Nucleic Acids Research 2010
Selective cyclooxygenase-2 silencing mediated by engineered E. coli and RNA interference induces anti-tumour effects in human colon cancer cells
A Strillacci, C Griffoni, G Lazzarini, MC Valerii, SD Molfetta, F Rizzello, M Campieri, MP Moyer, V Tomasi, E Spisni
British Journal of Cancer 2010
Inflammation: cytokines and RNA-based regulation
DJ Stumpo, WS Lai, PJ Blackshear
Wiley Interdisciplinary Reviews - RNA 2010
Post-transcriptional regulation of cancer traits by HuR
K Abdelmohsen, M Gorospe
Wiley interdisciplinary reviews. RNA 2010
HuR expression is a marker of poor prognosis in renal cell carcinoma
H Ronkainen, MH Vaarala, P Hirvikoski, A Ristimäki
Tumor Biology 2010
Post-transcriptional control during chronic inflammation and cancer: a focus on AU-rich elements
KS Khabar
Cellular and Molecular Life Sciences 2010
Posttranscriptional Regulation of Cyclooxygenase 2 Expression in Colorectal Cancer
LE Young, DA Dixon
Current Colorectal Cancer Reports 2010
APOBEC-1-mediated RNA editing
V Blanc, NO Davidson
Wiley Interdisciplinary Reviews Systems Biology and Medicine 2010
Tandem Phosphorylation of Serines 221 and 318 by Protein Kinase Cδ Coordinates mRNA Binding and Nucleocytoplasmic Shuttling of HuR
A Doller, K Schlepckow, H Schwalbe, J Pfeilschifter, W Eberhardt
Molecular and cellular biology 2010
miR-519 suppresses tumor growth by reducing HuR levels
Abdelmohsen K, Kim MM, Srikantan S, Mercken EM, Brennan SE, Wilson GM, de Cabo R, Gorospe M
Cell cycle (Georgetown, Tex.) 2010
Nucleotide‐binding domain of phosphoglycerate kinase 1 reduces tumor growth by suppressing COX‐2 expression
Ho M, Tang S, Ng WV, Yang W, Leu SJ, Lin Y, Feng C, Sung J, Sun K
Cancer Science 2010
Essential role of the RNA regulatory factor HuR in progenitor cell survival
Mallika Ghosh, Hector Leonardo Aguila, Jason Michaud, Youxi Ai, Ming-Tao Wu, Annabrita Hemmes, Ari Ristimaki, Caiying Guo, Henry Furneaux, Timothy Hla
Journal of Clinical Investigation 2009
Pulmonary surfactant: an immunological perspective
ZC Chroneos, Z Sever-Chroneos, VL Shepherd
Cellular physiology and biochemistry : international journal of experimental cellular physiology, biochemistry, and pharmacology 2009
Angiotensin II Induces Renal Plasminogen Activator Inhibitor-1 and Cyclooxygenase-2 Expression Post-Transcriptionally via Activation of the mRNA-Stabilizing Factor Human-Antigen R
A Doller, S Gauer, E Sobkowiak, H Geiger, J Pfeilschifter, W Eberhardt
The American Journal of Pathology 2009
Alternative polyadenylation variants of the RNA binding protein, HuR: abundance, role of AU-rich elements and auto-Regulation
W Al-Ahmadi, M Al-Ghamdi, L Al-Haj, M Al-Saif, KS Khabar
Nucleic Acids Research 2009
Cytoplasmic Expression of HuR is Related to Cyclooxygenase-2 Expression in Colon Cancer
SJ Lim, SH Lee, SH Joo, JY Song, SI Choi
Cancer Research and Treatment 2009
HuR and TTP: Two RNA Binding Proteins That Deliver Message From the 3′ End
S Anant, CW Houchen
Gastroenterology 2009
The mRNA Binding Proteins HuR and Tristetraprolin Regulate Cyclooxygenase 2 Expression During Colon Carcinogenesis
LE Young, S Sanduja, K Bemis–Standoli, EA Pena, RL Price, DA Dixon
Gastroenterology 2009
The p38 MAPK pathway inhibits tristetraprolin-directed decay of interleukin-10 and pro-inflammatory mediator mRNAs in murine macrophages
C Tudor, FP Marchese, E Hitti, A Aubareda, L Rawlinson, M Gaestel, PJ Blackshear, AR Clark, J Saklatvala, JL Dean
FEBS Letters 2009
Reduced Expression of an RNA-binding Protein by Prolactin Leads to Translational Silencing of Programmed Cell Death Protein 4 and Apoptosis in Newt Spermatogonia
K Eto, K Eda, M Hayano, S Goto, K Nagao, T Kawasaki, H Kashimura, H Tarui, O Nishimura, K Agata, S Abe
The Journal of biological chemistry 2009
Analysis of Nitric Oxide-Stabilized mRNAs in Human Fibroblasts Reveals HuR-Dependent Heme Oxygenase 1 Upregulation
Y Kuwano, A Rabinovic, S Srikantan, M Gorospe, B Demple
Molecular and cellular biology 2009
The mRNA decay factor tristetraprolin (TTP) induces senescence in human papillomavirus-transformed cervical cancer cells by targeting E6-AP ubiquitin ligase.
Sanduja S, Kaza V, Dixon DA
Aging 2009
MicroRNA-125a represses cell growth by targeting HuR in breast cancer.
Guo X, Wu Y, Hartley RS
RNA biology 2009
The aryl hydrocarbon receptor attenuates tobacco smoke-induced cyclooxygenase-2 and prostaglandin production in lung fibroblasts through regulation of the NF-kappaB family member RelB
CJ Baglole, SB Maggirwar, TA Gasiewicz, TH Thatcher, RP Phipps, PJ Sime
The Journal of biological chemistry 2008
Post-transcriptional control of CCAAT/enhancer-binding protein beta (C/EBPbeta) expression: formation of a nuclear HuR-C/EBPbeta mRNA complex determines the amount of message reaching the cytosol
J Cherry, H Jones, VA Karschner, PH Pekala
The Journal of biological chemistry 2008
Translation regulatory factor RBM3 is a proto-oncogene that prevents mitotic catastrophe
SM Sureban, S Ramalingam, G Natarajan, R May, D Subramaniam, KS Bishnupuri, AR Morrison, BK Dieckgraefe, DJ Brackett, RG Postier, CW Houchen, S Anant
Oncogene 2008
TGF-β1 reduces the heterogeneity of astrocytic cyclooxygenase-2 and nitric oxide synthase-2 gene expression in a stimulus-independent manner
ME Hamby, JA Hewett, SJ Hewett
Prostaglandins & Other Lipid Mediators 2008
Posttranscriptional regulation of IL-13 in T cells: Role of the RNA-binding protein HuR
V Casolaro, X Fang, B Tancowny, J Fan, F Wu, S Srikantan, SY Asaki, UD Fanis, SK Huang, M Gorospe, UX Atasoy, C Stellato
Journal of Allergy and Clinical Immunology 2008
Distinct Roles of Heterogeneous Nuclear Ribonuclear Protein K and microRNA-16 in Cyclooxygenase-2 RNA Stability Induced by S100b, a Ligand of the Receptor for Advanced Glycation End Products
N Shanmugam, MA Reddy, R Natarajan
The Journal of biological chemistry 2008
Posttranslational Modification of the AU-Rich Element Binding Protein HuR by Protein Kinase Cδ Elicits Angiotensin II-Induced Stabilization and Nuclear Export of Cyclooxygenase 2 mRNA
A Doller, ES Akool, A Huwiler, R Müller, HH Radeke, J Pfeilschifter, W Eberhardt
Molecular and cellular biology 2008
Oncogenic Ras and Transforming Growth Factor-β Synergistically Regulate AU-Rich Element–Containing mRNAs during Epithelial to Mesenchymal Transition
CL Kanies, JJ Smith, C Kis, C Schmidt, S Levy, KS Khabar, J Morrow, N Deane, DA Dixon, RD Beauchamp
Molecular cancer research : MCR 2008
AUF1 and HuR Proteins Stabilize Interleukin-8 mRNA in Human Saliva
Palanisamy V, Park NJ, Wang J, Wong DT
Journal of dental research 2008
Protecting the stress response, guarding the MKP-1 mRNA
Kuwano Y, Gorospe M
Cell cycle (Georgetown, Tex.) 2008
Specific trans-acting proteins interact with auxiliary RNA polyadenylation elements in the COX-2 3'-UTR
T Hall-Pogar, S Liang, LK Hague, CS Lutz
RNA (New York, N.Y.) 2007
Insulin-like growth factor-I induces cyclooxygenase-2 expression via PI3K, MAPK and PKC signaling pathways in human ovarian cancer cells
Z Cao, LZ Liu, DA Dixon, JZ Zheng, B Chandran, BH Jiang
Cellular Signalling 2007
Beyond the 3' end: experimental validation of extended transcript isoforms
V Moucadel, F Lopez, T Ara, P Benech, D Gautheret
Nucleic Acids Research 2007
Regulation of Intracellular Cyclooxygenase Levels by Gene Transcription and Protein Degradation
YJ Kang, UR Mbonye, CJ DeLong, M Wada, WL Smith
Progress in Lipid Research 2007
Intramural delivery of Sirolimus prevents vascular remodeling following balloon injury
M Buerke, M Guckenbiehl, H Schwertz, U Buerke, M Hilker, H Platsch, J Richert, S Bomm, GA Zimmerman, S Lindemann, U Mueller-Werdan, K Werdan, H Darius, AS Weyrich
Biochimica et Biophysica Acta (BBA) - Proteins & Proteomics 2007
Cyclooxygenase-2 transactivates the epidermal growth factor receptor through specific E-prostanoid receptors and Tumor Necrosis Factor-α converting enzyme
MA Al-Salihi, SC Ulmer, T Doan, CD Nelson, T Crotty, SM Prescott, DM Stafforini, MK Topham
Cellular Signalling 2007
Protein Kinase Cα-dependent Phosphorylation of the mRNA-stabilizing Factor HuR: Implications for Posttranscriptional Regulation of Cyclooxygenase-2
A Doller, A Huwiler, R Müller, HH Radeke, J Pfeilschifter, W Eberhardt, MP Wickens
Molecular biology of the cell 2007
Mutant Cu/Zn-Superoxide Dismutase Associated with Amyotrophic Lateral Sclerosis Destabilizes Vascular Endothelial Growth Factor mRNA and Downregulates Its Expression
L Lu, L Zheng, L Viera, E Suswam, Y Li, X Li, AG Estevez, PH King
The Journal of neuroscience : the official journal of the Society for Neuroscience 2007
Apigenin Prevents UVB-Induced Cyclooxygenase 2 Expression: Coupled mRNA Stabilization and Translational Inhibition
X Tong, RT Dross, A Abu-Yousif, AR Morrison, JC Pelling
Molecular and cellular biology 2007
Expression of Cyclooxygenase-2 in Platelet-Monocyte Interactions Occurs via Combinational Regulation Involving Adhesion and Cytokine Signaling
Dan A. Dixon, Neal D. Tolley, Kristi Bemis-Standoli, Mark L. Martinez, Andrew S. Weyrich, Jason D. Morrow, Stephen M. Prescott, and Guy A. Zimmerman
Journal of Clinical Investigation 2006
Endotoxic shock in AUF1 knockout mice mediated by failure to degrade proinflammatory cytokine mRNAs
JY Lu, N Sadri, RJ Schneider
Genes & development 2006
AU-rich elements and associated factors: are there unifying principles?
C Barreau, L Paillard, HB Osborne
Nucleic Acids Research 2006
Beta-Catenin stabilizes cyclooxygenase-2 mRNA by interacting with AU-rich elements of 3'-UTR
HK Lee, S Jeong
Nucleic Acids Research 2006
Derepression of the Her-2 uORF is mediated by a novel post-transcriptional control mechanism in cancer cells
A Mehta, CR Trotta, SW Peltz
Genes & development 2006
Imaging Cyclooxygenase-2 (Cox-2) Gene Expression in Living Animals with a Luciferase Knock-in Reporter Gene
T Ishikawa, NK Jain, MM Taketo, HR Herschman
Molecular Imaging and Biology 2006
Cyclooxygenases in hepatocellular carcinoma.
Cervello M, Montalto G
World Journal of Gastroenterology 2006
Enhanced proliferation of cultured human vascular smooth muscle cells linked to increased function of RNA-binding protein HuR
R Pullmann, M Juhaszova, IL de Silanes, T Kawai, K Mazan-Mamczarz, MK Halushka, M Gorospe
The Journal of biological chemistry 2005
Alternative polyadenylation of cyclooxygenase-2
T Hall-Pogar, H Zhang, B Tian, CS Lutz
Nucleic Acids Research 2005
Allellic variants in regulatory regions of cyclooxygenase-2: association with advanced colorectal adenoma
IU Ali, BT Luke, M Dean, P Greenwald
British Journal of Cancer 2005
Involvement of KSRP in the post-transcriptional regulation of human iNOS expression-complex interplay of KSRP with TTP and HuR
K Linker, A Pautz, M Fechir, T Hubrich, J Greeve, H Kleinert
Nucleic Acids Research 2005
Neuronal ELAV proteins enhance mRNA stability by a PKCalpha-dependent pathway
A Pascale, M Amadio, G Scapagnini, C Lanni, M Racchi, A Provenzani, S Govoni, DL Alkon, A Quattrone
Proceedings of the National Academy of Sciences 2005
Novel DNA-binding properties of the RNA-binding protein TIAR
EA Suswam, YY Li, H Mahtani, PH King
Nucleic Acids Research 2005
Antiapoptotic function of RNA-binding protein HuR effected through prothymosin alpha
A Lal, T Kawai, X Yang, K Mazan-Mamczarz, M Gorospe
The EMBO Journal 2005
RNA-Binding Protein HuR Is Required for Stabilization of SLC11A1 mRNA and SLC11A1 Protein Expression
YZ Xu, SD Marco, I Gallouzi, M Rola-Pleszczynski, D Radzioch
Molecular and cellular biology 2005
Mechanism and clinical significance of cyclooxygenase-2 expression in gastric cancer.
Wang BC, Guo CQ, Sun C, Sun QL, Liu GY, Li DG
World Journal of Gastroenterology 2005
Cyclooxygenase-2 and its role in colorectal cancer development
D Wendum, J Masliah, G Trugnan, JF Fljou
Virchows Archiv 2004
Dynamic antagonism between RNA-binding protein CUGBP2 and cyclooxygenase-2-mediated prostaglandin E2 in radiation damage
N Murmu, J Jung, D Mukhopadhyay, CW Houchen, TE Riehl, WF Stenson, AR Morrison, T Arumugam, BK Dieckgraefe, S Anant
Proceedings of the National Academy of Sciences 2004
Roles of AUF1 isoforms, HuR and BRF1 in ARE-dependent mRNA turnover studied by RNA interference
I Raineri, D Wegmueller, B Gross, U Certa, C Moroni
Nucleic Acids Research 2004
Structural and functional dissection of a conserved destabilizing element of cyclo-oxygenase-2 mRNA: evidence against the involvement of AUF-1 [AU-rich element/poly(U)-binding/degradation factor-1], AUF-2, tristetraprolin, HuR (Hu antigen R) or FBP1 (far-upstream-sequence-element-binding protein 1)
G Sully, JL Dean, R Wait, L Rawlinson, T Santalucia, J Saklatvala, AR Clark
Biochemical Journal 2004
Global analysis of HuR-regulated gene expression in colon cancer systems of reducing complexity.
López de Silanes I, Fan J, Galbán CJ, Spencer RG, Becker KG, Gorospe M
Gene expression 2004
Regulation of Cyclooxygenase-2 Expression by the Translational Silencer TIA-1
DA Dixon, GC Balch, N Kedersha, P Anderson, GA Zimmerman, RD Beauchamp, SM Prescott
Journal of Experimental Medicine 2003
Nitric Oxide Increases the Decay of Matrix Metalloproteinase 9 mRNA by Inhibiting the Expression of mRNA-Stabilizing Factor HuR
ES Akool, H Kleinert, FM Hamada, MH Abdelwahab, U Förstermann, J Pfeilschifter, W Eberhardt
Molecular and cellular biology 2003
Chronic Ethanol Exposure Increases the Binding of HuR to the TNFα 3′-Untranslated Region in Macrophages
MR McMullen, E Cocuzzi, M Hatzoglou, LE Nagy
The Journal of biological chemistry 2003
Developmental expression of functional cyclooxygenases in zebrafish
T Grosser, S Yusuff, E Cheskis, MA Pack, GA FitzGerald
Proceedings of the National Academy of Sciences 2002
ELAV/Hu proteins inhibit p27 translation via an IRES element in the p27 5'UTR
M Kullmann, U Göpfert, B Siewe, L Hengst
Genes & development 2002

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