The RNA-binding zinc-finger protein tristetraprolin regulates AU-rich mRNAs involved in breast cancer-related processes

Oncogene

Volumn 29, Issue 29, 2010, Pages 4205-4215

  Al Souhibani, N ^a   Al Ahmadi, W ^a   Hesketh, J E ^b   Blackshear, P J ^c   Khabar, K S A ^a  

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

^b NEWCASTLE UNIVERSITY   (United Kingdom)

^c NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

Author keywords

AU rich elements; posttranscriptional control; RNA stability; RNA binding proteins; tristetraprolin

Indexed keywords

MATRIX METALLOPROTEINASE; MESSENGER RNA; RNA BINDING PROTEIN; TRISTETRAPROLIN; UROKINASE RECEPTOR; ZINC FINGER PROTEIN;

ANIMAL CELL; ARTICLE; BREAST CANCER; CONTROLLED STUDY; FIBROBLAST; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; UPREGULATION;

3' UNTRANSLATED REGIONS; ANIMALS; BREAST; BREAST NEOPLASMS; CELL LINE, TUMOR; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MATRIX METALLOPROTEINASE 1; MICE; NEOPLASM INVASIVENESS; RECEPTORS, UROKINASE PLASMINOGEN ACTIVATOR; RNA, MESSENGER; TRISTETRAPROLIN; UROKINASE-TYPE PLASMINOGEN ACTIVATOR;

EID: 77954952745     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2010.168     Document Type: Article

References (45)

1. Al-Ahmadi W, Al-Ghamdi M, Al-Haj L, Al-Saif M, Khabar KS. (2009a). Alternative polyadenylation variants of the RNA binding protein, HuR: abundance, role of AU-rich elements and auto-regulation. Nucl Acids Res 37: 3612-3624.
2. Al-Ahmadi W, Al-Haj L, Al-Mohanna FA, Silverman RH, Khabar KS. (2009b). RNase L downmodulation of the RNA-binding protein, HuR, and cellular growth. Oncogene 28: 1782-1791.
3. Asyali MH, Shoukri MM, Demirkaya O, Khabar KSA. (2004). Assessment of reliability of microarray data and estimation of signal thresholds using mixture modeling. Nucl Acids Res 32: 2323-2335.
4. Bacac M, Stamenkovic I. (2008). Metastatic cancer cell. Annu Rev Pathol: Mech Dis 3: 221-247.
5. Blackshear PJ. (2002). Tristetraprolin and other CCCH tandem zinc-finger proteins in the regulation of mRNA turnover. Biochem Soc Trans 30: 945-952.
6. Brennan CM, Kuwano Y, Alkharouf N, Blackshear PJ, Gorospe M, Wilson GM. (2009). The mRNA-destabilizing protein tristetraprolin is suppressed in many cancers, altering tumorigenic phenotypes and patient prognosis. Cancer Res 69: 5168-5176.
7. Carballo E, Lai WS, Blackshear PJ. (1998). Feedback inhibition of macrophage tumor necrosis factor-{alpha} production by tristetra-prolin. Science 281: 1001-1005.
8. Carballo E, Lai WS, Blackshear PJ. (2000). Evidence that tristetra-prolin is a physiological regulator of granulocyte-macrophage colony stimulating factor messenger RNA deadenylation and stability. Blood 95: 1891-1899.
9. Christensen L, Wiborg Simonsen AC, Heeqaard CW, Moestrup SK, Andersen JA, Andreasen P. (1996). Immunohistochemical localization of urokinase-type plasminogen activator, type-1 plasminogen-activator inhibitor, urokinase receptor and alpha(2)-macroglobulin receptor in human breast carcinomas. Int J Cancer 66: 441-452.
10. Dass K, Ahmad A, Azmi AS, Sarkar SH, Sarkar FH. (2008). Evolving role of uPA/uPAR system in human cancers. Cancer Treat Rev 34: 122-136.
11. de Silanes IL, Fan J, Yang X, Zonderman AB, Potapova O, Pizer ES et al. (2003). Role of the RNA-binding protein HuR in colon carcinogenesis. Oncogene 22: 7146-7154.
12. Denkert C, Weichert W, Pest S, Koch I, Licht D, Kobel M et al. (2004). Overexpression of the embryonic-lethal abnormal vision-like protein HuR in ovarian carcinoma is a prognostic factor and is associated with increased cyclooxygenase 2 expression. Cancer Res 64: 189-195.
13. DuBois RN, McLane MW, Ryder K, Lau LF, Nathans D. (1990). A growth factor-inducible nuclear protein with a novel cysteine/histidine repetitive sequence. J Biol Chem 265: 19185-19191.
14. Essafi-Benkhadir K, Onesto C, Stebe E, Moroni C, Pages G. (2007). Tristetraprolin inhibits Ras-dependent tumor vascularization by inducing vascular endothelial growth factor mRNA degradation. Mol Biol Cell 18: 4648-4658.
15. Fini ME, Plucinska IM, Mayer AS, Gross RH, Brinckerhoff CE. (1987). A gene for rabbit synovial cell collagenase: member of a family of metalloproteinases that degrade the connective tissue matrix. Biochemistry 26: 6157-6165.
16. Fisher JL, Field CL, Zhou H, Harris TL, Henderson MA, Choong PF. (2000). Urokinase plasminogen activator system gene expression is increased in human breast carcinoma and its bone metastases-a comparison of normal breast tissue, non-invasive and invasive carcinoma and osseous metastases. Breast Cancer Res Treat 61: 1-12.
17. Gebeshuber CA, Zatloukal K, Martinez J. (2009). miR-29a suppresses tristetraprolin, which is a regulator of epithelial polarity and metastasis. EMBO J Rep 10: 400-405.
18. Heinonen M, Fagerholm R, Aaltonen K, Kilpivaara O, Aittomaki K, Blomqvist C et al. (2007). Prognostic role of HuR in hereditary breast cancer. Clin Cancer Res 13: 6959-6963.
19. Iwata H, Kobayashi S, Iwase H, Masaoka A, Fujimoto N, Okada Y. (1996). Production of matrix metalloproteinases and tissue inhibitors of metalloproteinases in human breast carcinomas. Jpn J Cancer Res 87: 602-611.
20. Khabar KS, Al-Haj L, Al-Zoghaibi F, Marie M, Dhalla M, Polyak SJ et al. (2004). Expressed gene clusters associated with cellular sensitivity and resistance towards anti-viral and anti-proliferative actions of interferon. J Mol Biol 342: 833-846.
21. Kleiner DE, Stetler-Stevenenson W. (1999). Matrix metalloproteinases and metastasis. Cancer Chemother Pharmacol 43: S42-S51.
22. Lai WS, Carballo E, Strum JR, Kennington EA, Phillips RS, Blackshear PJ. (1999). Evidence that tristetraprolin binds to AU-rich elements and promotes the deadenylation and destabilization of tumor necrosis factor alpha mRNA. Mol Cell Biol 19: 4311-4323.
23. Lai WS, Carballo E, Thorn JM, Kennington EA, Blackshear PJ. (2000). 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 275: 17827-17837.
24. Lai WS, Kennington EA, Blackshear PJ. (2002). Interactions of CCCH zinc finger proteins with mRNA. Non-binding tristetrapro-lin mutants exert an inhibitory effect on degradation of AU-rich element-containing mRNAs. J Biol Chem 277: 9606-9613.
25. Lai WS, Parker JS, Grissom SF, Stumpo DJ, Blackshear PJ. (2006). Novel mRNA targets for tristetraprolin (TTP) identified by global analysis of stabilized transcripts in TTP-deficient fibroblasts. Mol Cell Biol 26: 9196-9208.
26. Lai WS, Stumpo DJ, Blackshear PJ. (1990). Rapid insulin-stimulated accumulation of an mRNA encoding a proline-rich protein. J Biol Chem 265: 16556-16563.
27. Liotta LA. (1986). Tumor invasion and metastases\role of the extracellular matrix: Rhoads Memorial Award lecture. Cancer Res 46: 1-7.
28. Liotta LA, Tryggvason K, Garbisa S, Hart I, Foltz CM, Shafie S. (1980). Metastatic potential correlates with enzymatic degradation of basement membrane collagen. Nature 284: 67-68.
29. McPherson K, Steel CM, Dixon JM. (2000). ABC of breast diseases: breast cancer\epidemiology, risk factors, and genetics. Br Med J 321: 624-628.
30. Mrena J, Wiksten J-P, Thiel A, Kokkola A, Pohjola L, Lundin J et al. (2005). Cyclooxygenase-2 is an independent prognostic factor in gastric cancer and its expression is regulated by the messenger RNA stability factor HuR. Clin Cancer Res 11: 7362-7368.
31. Nanbu R, Menoud PA, Nagamine Y. (1994). Multiple instability-regulating sites in the 3' untranslated region of the urokinase-type plasminogen activator mRNA. Mol Cell Biol 14: 4920-4928.
32. Nanbu R, Montero L, D'Orazio D, Nagamine Y. (1997). Enhanced stability of urokinase-type plasminogen activator mRNA in metastatic breast cancer MDA-MB-231 cells and LLC-PK, cells down-regulated for protein kinase C correlation with cytoplasmic heterogeneous nuclear ribonucleoprotein C. Eur J Biochem 247: 169-174.
33. Quax PHA, van Leeuwen RTJ, Verspaget HW, Verheijen JH. (1990). Protein and messenger RNA levels of plasminogen activators and inhibitors analyzed in 22 human tumor cell lines. Cancer Res 50: 1488-1494.
34. Roldan AL, Cubellis MY, Masucci MT, Behrendt NL, Lund LR, Dano K et al. (1990). Cloning and expression of the receptor for human urokinase plasminogen activator, a central molecule in cell surface plasmin dependent proteolysis. EMBO J 9: 467-474.
35. Sawaoka H, Dixon DA, Oates JA, Boutaud O. (2003). Tristetraprolin binds to the 3'-untranslated region of cyclooxygenase-2 mRNA. A polyadenylation variant in a cancer cell line lacks the binding site. J Biol Chem 278: 13928-13935.
36. Shetty S, Kumar A, Idell S. (1997). Posttranscriptional regulation of urokinase receptor mRNA: identification of a novel urokinase receptor mRNA binding protein in human mesothelioma cells. Mol Cell Biol 17: 1075-1083.
37. Soslow RA, Dannenberg AJ, Rush D, Woerner BM, Khan KN, Masferrer J et al. (2000). COX-2 is expressed in human pulmonary, colonic, and mammary tumors. Cancer 89: 2637-2645.
38. Stoecklin G, Tenenbaum SA, Mayo T, Chittur SV, George AD, Baroni TE et al. (2008). Genome-wide analysis identifies interleukin-10 mRNA as target of tristetraprolin. J Biol Chem 283: 11689-11699.
39. Suswam E, Li Y, Zhang X, Gillespie GY, Li X, Shacka JJ et al. (2008). Tristetraprolin down-regulates interleukin-8 and vascular endothelial growth factor in malignant glioma cells. Cancer Res 68: 674-682.
40. Tran H, Maurer F, Nagamine Y. (2003). Stabilization of urokinase and urokinase receptor mRNAs by HuR is linked to its cytoplasmic accumulation induced by activated mitogen-activated protein kinase-activated protein kinase 2. Mol Cell Biol 23: 7177-7188.
41. Vincenti MP, Brinckerhoff CE. (2002). Transcriptional regulation of collagenase (MMP-1, MMP-13) genes in arthritis: integration of complex signaling pathways for the recruitment of gene-specific transcription factors. Arthritis Res 4: 157-164.
42. Vincenti MP, Coon CI, Lee O, Brinckerhoff CE. (1994). Regulation of collagenase gene expression by IL-1 requires transcriptional and post-transcriptional mechanisms. Nucl Acids Res 22: 4818-4827.
43. Vlasova IA, Tahoe NM, Fan D, Larsson O, Rattenbacher B, Sternjohn JR et al. (2008). Conserved GU-rich elements mediate mRNA decay by binding to CUG-binding protein 1. Mol Cell 29: 263-270.
44. Wang GJ, Collinge M, Blasi F, Pardi R, Bender JR. (1998). Posttranscriptional regulation of urokinase plasminogen activator receptor messenger RNA levels by leukocyte integrin engagement. Proc Natl Acad Sci USA 95: 6296-6301.
45. Young LE, Sanduja S, Bemis-Standoli K, Pena EA, Price RL, Dixon DA. (2009). The mRNA binding proteins HuR and tristetraprolin regulate cyclooxygenase 2 expression during colon carcinogenesis. Gastroenterology 136: 1669-1679.