The mRNA-destabilizing protein tristetraprolin is suppressed in many cancers, altering tumorigenic phenotypes and patient prognosis

Cancer Research

Volumn 69, Issue 12, 2009, Pages 5168-5176

  Brennan, Sarah E ^a   Kuwano, Yuki ^b   Alkharouf, Nadim ^c   Blackshear, Perry J ^d   Gorospe, Myriam ^b   Wilson, Gerald M ^a,e  

^a UNIVERSITY OF MARYLAND GREENEBAUM CANCER CENTER   (United States)

^b NATIONAL INSTITUTE ON AGING   (United States)

^c TOWSON UNIVERSITY   (United States)

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

^e UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN D; HUR PROTEIN; MESSENGER RNA; TIA 1 PROTEIN; TRISTETRAPROLIN; UNCLASSIFIED DRUG; VASCULOTROPIN;

ADVANCED CANCER; ANIMAL CELL; APOPTOSIS; ARTICLE; BREAST CANCER; CANCER MORTALITY; CANCER RECURRENCE; CARCINOGENESIS; CELL PROLIFERATION; CELL STRUCTURE; CELL TYPE; CONTROLLED STUDY; DNA MICROARRAY; GENE EXPRESSION REGULATION; GENE REPRESSION; HELA CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; MAJOR CLINICAL STUDY; MOUSE; NONHUMAN; PHENOTYPIC VARIATION; PRIORITY JOURNAL; PROGNOSIS; PROSTATE CANCER;

APOPTOSIS; CELL PROLIFERATION; DNA, COMPLEMENTARY; GENE EXPRESSION PROFILING; HELA CELLS; HUMANS; NEOPLASMS; PHENOTYPE; PROGNOSIS; RNA, MESSENGER; TRISTETRAPROLIN; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 67449132368     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-08-4238     Document Type: Article

References (40)

1. Hanahan D, Weinberg RA. The hallmarks of cancer. Cell 2000;100:57-70. (Pubitemid 30046295)
2. Chen CYA, Shyu AB. AU-rich elements: characterization and importance in mRNA degradation. Trends Biochem Sci 1995;20:465-470
3. Guhaniyogi J, Brewer G. Regulation of mRNA stability in mammalian cells. Gene 2001;265:11-23. (Pubitemid 32209246)
4. Barreau C, Paillard L, Osborne HB. AU-rich elements and associated factors: are there unifying principles? Nucleic Acids Res 2005;33:7138-7150
5. Zhang T, Kruys V, Huez G, Gueydan C. AU-rich element-mediated translational control: complexity and multiple activities of trans-acting factors. Biochem Soc Trans 2002;30:952-958 (Pubitemid 36002387)
6. Gouble A, Grazide S, Meggetto F, Mercier P, Delsol G, Morello D. A new player in oncogenesis: AUF1/hnRNPD overexpression leads to tumorigenesis in transgenic mice. Cancer Res 2002;62:1489-1495 (Pubitemid 34407812)
7. 2 is mediated by enhanced cyclin D1 mRNA turnover. Mol Cell Biol 2000;20:7903-7913
8. Denkert C, Weichert W, Winzer KJ, et al. Expression of the ELAV-like protein HuR is associated with higher tumor grade and increased cyclooxygenase-2 expression in human breast carcinoma. Clin Cancer Res 2004;10:5580-5586 (Pubitemid 39100499)
9. Stoecklin G, Gross B, Ming XF, Moroni C. A novel mechanism of tumor suppression by destabilizing AU-rich growth factor mRNA. Oncogene 2003;22:3554-3561 (Pubitemid 36765315)
10. 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;18:4648-4658 (Pubitemid 350060189)
11. Tian Q, Streuli M, Saito H, Schlossman SF, Anderson P. A polyadenylate binding protein localized to the granules of cytolytic lymphocytes induces DNA fragmentation in target cells. Cell 1991;67:629-639 (Pubitemid 121001476)
12. Blackshear PJ. Tristetraprolin and other CCCH tandem zinc-finger proteins in the regulation of mRNA turnover. Biochem Soc Trans 2002;30:945-952 (Pubitemid 36002386)
13. Brewer BY, Malicka J, Blackshear PJ, Wilson GM. RNA sequence elements required for high affinity binding by the zinc finger domain of tristetraprolin: conformational changes coupled to the bipartite nature of AU-rich mRNA-destabilizing motifs. J Biol Chem 2004;279:27870-27877 (Pubitemid 38900055)
14. Lai WS, Parker JS, Grissom SF, Stumpo DJ, Blackshear PJ. Novel mRNA targets for tristetraprolin (TTP) identified by global analysis of stabilized transcripts in TTP-deficient fibroblasts. Mol Cell Biol 2006;26:9196-9208 (Pubitemid 44904416)
15. Suzuki A, Tsutomi Y, Akahane K, Araki T, Miura M. Resistance to Fas-mediated apoptosis: activation of caspase 3 is regulated by cell cycle regulator p21WAF1 and IAP gene family ILP. Oncogene 1998;17:931-939 (Pubitemid 28425403)
16. Lal A, Mazan-Mamczarz K, Kawai T, Yang X, Martindale JL, Gorospe M. Concurrent versus individual binding of HuR and AUF1 to common labile target mRNAs. EMBO J 2004;23:3092-3102 (Pubitemid 39093603)
17. Carrick DM, Blackshear PJ. Comparative expression of tristetraprolin (TTP) family member transcripts in normal human tissues and cancer cell lines. Arch Biochem Biophys 2008;462:278-285
18. Rhodes DR, Kalyana-Sundaram S, Mahavisno V, et al. Oncomine 3.0: genes, pathways, and networks in a collection of 18,000 cancer gene expression profiles. Neoplasia 2007;9:166-180 (Pubitemid 46318375)
19. Lal A, Lash AE, Altschul SF, et al. A public database for gene expression in human cancers. Cancer Res 1999;59:5403-5407 (Pubitemid 29526444)
20. Lai WS, Kennington EA, Blackshear PJ. Interactions of CCCH zinc finger proteins with mRNA: non-binding tristetraprolin mutants exert an inhibitory effect on degradation of AU-rich element-containing mRNAs. J Biol Chem 2002;277:9606-9613 (Pubitemid 34953050)
21. Johnson BA, Geha M, Blackwell TK. Similar but distinct effects of the tristetraprolin/TIS11 immediate-early proteins on cell survival. Oncogene 2000;19:1657-1664 (Pubitemid 30200967)
22. Jarvis WD, Turner AJ, Povirk LF, Traylor RS, Grant S. Induction of apoptotic DNA fragmentation and cell death in HL-60 promyelocytic leukemia cells by pharmacological inhibitors of protein kinase C. Cancer Res 1994;54:1707-1714 (Pubitemid 24116174)
23. Boulares AH, Yakovlev AG, Ivanova V, et al. Role of poly(ADP-ribose) polymerase (PARP) cleavage in apoptosis. Caspase 3-resistant PARP mutant increases rates of apoptosis in transfected cells. J Biol Chem 1999;274:22932-22940 (Pubitemid 129529118)
24. Jordan P, Carmo-Fonseca M. Molecular mechanisms involved in cisplatin cytotoxicity. Cell Mol Life Sci 2000;57:1229-1235 (Pubitemid 30663480)
25. Suswam E, Li Y, Zhang X, et al. Tristetraprolin downregulates interleukin-8 and vascular endothelial growth factor in malignant glioma cells. Cancer Res 2008;68:674-682 (Pubitemid 351206742)
26. Taylor GA, Carballo E, Lee DM. A pathogenic role for TNFα in the syndrome of cachexia, arthritis, and autoimmunity resulting from tristetraprolin (TTP) deficiency. Immunity 1996;4:445-454 (Pubitemid 26354654)
27. Miller LD, Smeds J, George J, et al. An expression signature for p53 status in human breast cancer predicts mutation status, transcriptional effects, and patient survival. Proc Natl Acad Sci U S A 2005;102:13550-13555 (Pubitemid 41420886)
28. Yu YP, Landsittel D, Jing L, et al. Gene expression alterations in prostate cancer predicting tumor aggression and preceding development of malignancy. J Clin Oncol 2004;22:2790-2799 (Pubitemid 41079896)
29. Bakheet T, Williams BRG, Khabar KSA. ARED 3.0: the large and diverse AU-rich transcriptome. Nucleic Acids Res 2006;34:D111-4.
30. Carmeliet P. VEGF as a key mediator of angiogenesis in cancer. Oncology 2005;69 Suppl 3:4-10. (Pubitemid 41680947)
31. Charlot JF, Prétet JL, Mougin C. Mitochondrial translocation of p53 and mitochondrial membrane potential (DYm) dissipation are early events in staurosporine-induced apoptosis of wild type and mutated p53 epithelial cells. Apoptosis 2004;9:333-343 (Pubitemid 38981507)
32. Wang Y, Zhang B, Peng X, Perpetua M, Harbrecht BG. Bcl-XL prevents staurosporine-induced hepatocyte apoptosis by restoring protein kinase B/mitogen-activated protein kinase activity and mitochondrial integrity. J Cell Physiol 2007;215:676-683
33. Stoecklin G, Tenebaum SA, Mayo T, et al. Genome-wide analysis identifies interleukin-10 mRNA as target of tristetraprolin. J Biol Chem 2008;283:11689-11699
34. Li L, Deng B, Xing G, et al. PACT is a negative regulator of p53 and essential for cell growth and embryonic development. Proc Natl Acad Sci U S A 2007;104:7951-7956 (Pubitemid 47185857)
35. Yang J, Siqueira MF, Behl Y, Alikhani M, Graves DT. The transcription factor ST18 regulates proapoptotic and proinflammatory gene expression in fibroblasts. FASEB J 2008;22:3956-3967
36. Wilson GM, Brewer G. The search for trans-acting factors controlling messenger RNA decay. Prog Nucleic Acids Res Mol Biol 1999;62:257-291
37. Fialcowitz EJ, Brewer BY, Keenan BP, Wilson GM. A hairpin-like structure within an AU-rich mRNA-destabilizing element regulates trans-factor binding selectivity and mRNA decay kinetics. J Biol Chem 2005;280:22406-22417 (Pubitemid 40827896)
38. Lopez de Silanes I, Galban S, Martindale JL, et al. Identification and functional outcome of mRNAs associated with RNA-binding protein TIA-1. Mol Cell Biol 2005;25:9520-9531 (Pubitemid 41507852)
39. Lee SK, Kim SB, Kim JS, et al. Butyrate response factor 1 enhances cisplatin sensitivity in human head and neck squamous cell carcinoma cell lines. Int J Cancer 2005;117:32-40. (Pubitemid 41262757)
40. Elston CW, Ellis IO. Pathological prognostic factors in breast cancer. I. The value of histological grade in breast cancer: experience from a large study with long-term follow-up. Histopathology 1991;19:403-410