Systematic analysis of AU-Rich element expression in cancer reveals common functional clusters regulated by key RNA-Binding proteins

Cancer Research

Volumn 76, Issue 14, 2016, Pages 4068-4080

  Hitti, Edward ^a   Bakheet, Tala ^a   Al Souhibani, Norah ^a   Moghrabi, Walid ^a   Al Yahya, Suhad ^a   Al Ghamdi, Maha ^a   Al Saif, Maher ^a   Shoukri, Mohamed M ^a   Lanczky, Andras ^b   Grepin, Renaud ^d   Gyorffy, Balazs ^b,c   Pages, Gilles ^e   Khabar, Khalid S A ^a  

^a KING FAISAL SPECIALIST HOSPITAL AND RESEARCH CENTER   (Saudi Arabia)

^b Lendület Cancer Biomarker Research Group   (Hungary)

^c SEMMELWEIS UNIVERSITY   (Hungary)

^d CENTRE SCIENTIFIQUE DE MONACO   (Monaco)

^e UNIVERSITÉ CÔTE D'AZUR   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ELAV LIKE PROTEIN 1; HISTONE H3; MESSENGER RNA; RNA BINDING PROTEIN; TRISTETRAPROLIN; ADENINE; ELAVL1 PROTEIN, HUMAN; URIDINE; ZFP36 PROTEIN, HUMAN;

ARTICLE; AU RICH ELEMENT; BREAST CANCER; BREAST CANCER CELL LINE; CDC6 GENE; CELL CYCLE ARREST; CENPA GENE; CENPE GENE; CONTROLLED STUDY; DISTANT METASTASIS FREE SURVIVAL; GENE; GENE EXPRESSION; HISTONE PHOSPHORYLATION; HUMAN; KIF11 GENE; KIF18A GENE; MITOSIS; NCAPG GENE; NEK2 GENE; NUF2 GENE; OVERALL SURVIVAL; PBK GENE; POLYADENYLATION; PRC1 GENE; PRIORITY JOURNAL; RECURRENCE FREE SURVIVAL; SOLID TUMOR; TOP2A GENE; CELL CYCLE CHECKPOINT; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; NEOPLASM; TUMOR CELL LINE;

ADENINE; CELL CYCLE CHECKPOINTS; CELL LINE, TUMOR; ELAV-LIKE PROTEIN 1; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; NEOPLASMS; POLYADENYLATION; RNA, MESSENGER; RNA-BINDING PROTEINS; TRISTETRAPROLIN; URIDINE;

EID: 84978435483     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-15-3110     Document Type: Article

References (49)

1. Khabar KS. Post-transcriptional control of cytokine gene expression in health and disease. J Interferon Cytokine Res 2014;34:215-9.
2. Halees AS, El-Badrawi R, Khabar KS. ARED Organism: expansion of ARED reveals AU-rich element cluster variations between human and mouse. Nucleic Acids Res 2008;36:D137-40.
3. Bakheet T, Frevel M, Williams BRG, Greer W, Khabar KSA. ARED: human AU-rich element-containing mRNA database reveals an unexpectedly diverse functional reportiore of encoded proteins. Nucleic Acids Res 2001;29:246-54.
4. Al-Souhibani N, Al-Ahmadi W, Hesketh JE, Blackshear PJ, Khabar KS. The RNA-binding zinc-finger protein tristetraprolin regulates AU-rich mRNAs involved in breast cancer-related processes. Oncogene 2010;29:4205-15.
5. Al-Souhibani N, Al-Ghamdi M, Al-Ahmadi W, Khabar KSA. Posttranscriptional control of the chemokine receptor CXCR4 expression in cancer cells. Carcinogenesis 2014;35:1983-92.
6. Essafi-Benkhadir K, Onesto C, Stebe E, Moroni C, Pages G. Tristetraprolin inhibits Ras-dependent tumor vascularization by inducing vascular endothelial growth factor mRNA degradation. Mol Biol Cell 2007;18:4648-58.
7. Devaney JM, Tosi LL, Fritz DT, Gordish-Dressman HA, Jiang S, Orkunoglu-Suer FE, et al. Differences in fat and muscle mass associated with a functional human polymorphism in a post-transcriptional BMP2 gene regulatory element. J Cell Biochem 2009;107:1073-82.
8. Balmer LA, Beveridge DJ, Jazayeri JA, Thomson AM, Walker CE, Leedman PJ. Identification of a novel AU-Rich element in the 30 untranslated region of epidermal growth factor receptor mRNA that is the target for regulated RNA-binding proteins. Mol Cell Biol 2001;21:2070-84.
9. Young LE, Dixon DA. Posttranscriptional regulation of cyclooxygenase 2 expression in colorectal cancer. Curr Colorectal Cancer Rep 2010;6: 60-7.
10. Hitti E, Iakovleva T, Brook M, Deppenmeier S, Gruber AD, Radzioch D, et al. Mitogen-activated protein kinase-activated protein kinase 2 regulates tumor necrosis factor mRNA stability and translation mainly by altering tristetraprolin expression, stability, and binding to adenine/uridine-rich element. Mol Cell Biol 2006;26:2399-407.
11. Tiedje C, Ronkina N, Tehrani M, Dhamija S, Laass K, Holtmann H, et al. The p38/MK2-driven exchange between tristetraprolin and HuR regulates AUrich element-dependent translation. PLoS Genet 2012;8:e1002977 .
12. Kratochvill F, Machacek C, Vogl C, Ebner F, Sedlyarov V, Gruber AR, et al. Tristetraprolin-driven regulatory circuit controls quality and timing of mRNA decay in inflammation. Mol Syst Biol 2011;7:560.
13. Sanduja S, Blanco FF, Young LE, Kaza V, Dixon DA. The role of tristetraprolin in cancer and inflammation. Front Biosci 2012;17:174-88.
14. Abdelmohsen K, Gorospe M. Posttranscriptional regulation of cancer traits by HuR. Wiley Interdiscip Rev RNA 2010;1:214-29.
15. Eberhardt W, Doller A, Pfeilschifter J. Regulation of the mRNA-binding protein HuR by posttranslational modification: spotlight on phosphorylation. Curr Protein Pept Sci 2012;13:380-90.
16. Brook M, Tchen CR, Santalucia T, McIlrath J, Arthur JS, Saklatvala J, et al. Posttranslational regulation of tristetraprolin subcellular localization and protein stability by p38 mitogen-activated protein kinase and extracellular signal-regulated kinase pathways. Mol Cell Biol 2006;26:2408-18.
17. Tchen CR, Brook M, Saklatvala J, Clark AR. The stability of tristetraprolin mRNA is regulated by mitogen-activated protein kinase p38 and by tristetraprolin itself. J Biol Chem 2004;279:32393-400.
18. Al-Ahmadi W, Al-Ghamdi M, Al-Haj L, Al-Saif M, Khabar KS. Alternative polyadenylation variants of the RNA binding protein, HuR: abundance, role of AU-rich elements and auto-Regulation. Nucleic Acids Res 2009;37:3612-24.
19. Dai W, Zhang G, Makeyev EV. RNA-binding protein HuR autoregulates its expression by promoting alternative polyadenylation site usage. Nucleic Acids Res 2012;40:787-800.
20. Mansfield KD, Keene JD. Neuron-specific ELAV/Hu proteins suppress HuR mRNA during neuronal differentiation by alternative polyadenylation. Nucleic Acids Res 2012;40:2734-46.
21. Al-Ahmadi W, Al-Ghamdi M, Al-Souhibani N, Khabar KS. miR-29a inhibition normalizes HuR over-expression and aberrant AU-rich mRNA stability in invasive cancer. J Pathol 2013;230:28-38.
22. Gebeshuber CA, Zatloukal K, Martinez J. miR-29a suppresses tristetraprolin, which is a regulator of epithelial polarity and metastasis. EMBO Rep 2009;10:400-5.
23. Curtis C, Shah SP, Chin SF, Turashvili G, Rueda OM, Dunning MJ, et al. The genomic and transcriptomic architecture of 2,000 breast tumours reveals novel subgroups. Nature 2012;486:346-52.
24. Al-Ahmadi W, Al-Haj L, Al-Mohanna FA, Silverman RH, Khabar KS. RNase L downmodulation of the RNA-binding protein, HuR, and cellular growth. Oncogene 2009;28:1782-91.
25. Hitti E, Al-Yahya S, Al-Saif M, Mohideen P, Mahmoud L, Polyak SJ, et al. A versatile ribosomal protein promoter-based reporter system for selective assessment of RNA stability and post-transcriptional control. RNA 2010;16:1245-55.
26. Al-Saif M, Khabar KS. UU/UA dinucleotide frequency reduction in coding regions results in increased mRNA stability and protein expression. Mol Ther 2012;20:954-9.
27. al-Haj L, Al-Ahmadi W, Al-Saif M, Demirkaya O, Khabar KS. Cloning-free regulated monitoring of reporter and gene expression. BMC Mol Biol 2009;10:20.
28. Griseri P, Bourcier C, Hieblot C, Essafi-Benkhadir K, Chamorey E, Touriol C, et al. A synonymous polymorphism of the Tristetraprolin (TTP) gene, an AU-rich mRNA-binding protein, affects translation efficiency and response to Herceptin treatment in breast cancer patients. Hum Mol Genet 2011;20:4556-68.
29. Gyorffy B, Lanczky A, Eklund AC, Denkert C, Budczies J, Li Q, et al. An online survival analysis tool to rapidly assess the effect of 22,277 genes on breast cancer prognosis using microarray data of 1,809 patients. Breast Cancer Res Treat 2010;123:725-31.
30. Mihaly Z, Kormos M, Lanczky A, Dank M, Budczies J, Szasz MA, et al. A meta-analysis of gene expression-based biomarkers predicting outcome after tamoxifen treatment in breast cancer. Breast Cancer Res Treat 2013;140:219-32.
31. Nigg EA. Mitotic kinases as regulators of cell division and its checkpoints. Nat Rev Mol Cell Biol 2001;2:21-32.
32. Lee HH, Lee SR, Leem SH. Tristetraprolin regulates prostate cancer cell growth through suppression of E2F1. J Microbiol Biotechnol 2014;24: 287-94.
33. Marderosian M, Sharma A, Funk AP, Vartanian R, Masri J, Jo OD, et al. Tristetraprolin regulates Cyclin D1 and c-Myc mRNA stability in response to rapamycin in an Akt-dependent manner via p38 MAPK signaling. Oncogene 2006;25:6277-90.
34. Milke L, Schulz K, Weigert A, Sha W, Schmid T, Brüne B. Depletion of tristetraprolin in breast cancer cells increases interleukin-16 expression and promotes tumor infiltration with monocytes/macrophages. Carcinogenesis 2013;34:850-7.
35. Kim CW, Vo MT, Kim HK, Lee HH, Yoon NA, Lee BJ, et al. Ectopic overexpression of tristetraprolin in human cancer cells promotes biogenesis of let-7 by down-regulation of Lin28. Nucleic Acids Res 2012;40:3856-69.
36. Nabors LB, Gillespie GY, Harkins L, King PH. HuR, a RNA stability factor, is expressed in malignant brain tumors and binds to adenine- and uridinerich elements within the 30 untranslated regions of cytokine and angiogenic factor mRNAs. Cancer Res 2001;61:2154-61.
37. Niesporek S, Kristiansen G, Thoma A, Weichert W, Noske A, Buckendahl AC, et al. Expression of the ELAV-like protein HuR in human prostate carcinoma is an indicator of disease relapse and linked to COX-2 expression. Int J Oncol 2008;32:341-7.
38. Wang J, Zhao W, Guo Y, Zhang B, Xie Q, Xiang D, et al. The expression of RNA-binding protein HuR in non-small cell lung cancer correlates with vascular endothelial growth factor-C expression and lymph node metastasis. Oncology 2009;76:420-9.
39. Yi X, Zhou Y, Zheng W, Chambers SK. HuR expression in the nucleus correlates with high histological grade and poor disease-free survival in ovarian cancer. Aust N Z J Obstet Gynaecol 2009;49:93-8.
40. Yuan Z, Sanders AJ, Ye L, Jiang WG. HuR, a key post-transcriptional regulator, and its implication in progression of breast cancer. Histol Histopathol 2010;25:1331-40.
41. Mazan-Mamczarz K, Hagner PR, Corl S, Srikantan S, Wood WH, Becker KG, et al. Post-transcriptional gene regulation by HuR promotes a more tumorigenic phenotype. Oncogene 2008;27:6151-63.
42. Mukherjee N, Corcoran DL, Nusbaum JD, Reid DW, Georgiev S, Hafner M, et al. Integrative regulatory mapping indicates that the RNA-binding protein HuR couples pre-mRNA processing and mRNA stability. Mol Cell 2011;43:327-39.
43. Zhu H, Zhou H-L, Hasman RA, Lou H. Hu proteins regulate polyadenylation by blocking sites containing U-rich sequences. J Biol Chem 2007;282:2203-10.
44. Tiedje C, Holtmann H, Gaestel M. The role of mammalian MAPK signaling in regulation of cytokine mRNA stability and translation. J Interferon Cytokine Res 2014;34:220-32.
45. Dai W, Li W, Hoque M, Li Z, Tian B, Makeyev EV. A post-transcriptional mechanism pacing expression of neural genes with precursor cell differentiation status. Nat Commun 2015;6:7576.
46. Suswam E, Li Y, Zhang X, Gillespie GY, Li X, Shacka JJ, et al. Tristetraprolin down-regulates interleukin-8 and vascular endothelial growth factor in malignant glioma cells. Cancer Res 2008;68: 674-82.
47. Griseri P, Pages G. Control of pro-angiogenic cytokine mRNA half-life in cancer: the role of AU-rich elements and associated proteins. J Interferon Cytokine Res 2014;34:242-54.
48. Van Tubergen EA, Banerjee R, Liu M, Vander Broek R, Light E, Kuo S, et al. Inactivation or loss of TTP promotes invasion in head and neck cancer via transcript stabilization and secretion of MMP9, MMP2, and IL-6. Clin Cancer Res 2013;19:1169-79.
49. Kakuguchi W, Kitamura T, Kuroshima T, Ishikawa M, Kitagawa Y, Totsuka Y, et al. HuR knockdown changes the oncogenic potential of oral cancer cells. Mol Cancer Res 2010;8:520-8.