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References

  1. Brennan SE, 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.
    CrossRef
  2. Cha HJ, Lee HH, Chae SW, Cho WJ, Kim YM, Choi HJ, et al. 2011. Tristetraprolin downregulates the expression of both VEGF and COX-2 in human colon cancer. Hepatogastroenterology 58: 790-795.
  3. Chen CY, Shyu AB. 1995. AU-rich elements: characterization and importance in mRNA degradation. Trends Biochem. Sci. 20: 465-470.
    CrossRef
  4. DeGregori J, Kowalik T, Nevins JR. 1995. Cellular targets for activation by the E2F1 transcription factor include DNA synthesis- and G1/S-regulatory genes. Mol. Cell Biol. 15:4215-4224.
  5. Gorgoulis VG, Zacharatos P, Mariatos G, Kotsinas A, Bouda M, Kletsas D, et al. 2002. Transcription factor E2F-1 acts as a growth-promoting factor and is associated with adverse prognosis in non-small cell lung carcinomas. J. Pathol. 198:142-156.
    CrossRef
  6. Helin K, Wu CL, Fattaey AR, Lees JA, Dynlacht BD, Ngwu C, H arlow E. 1 993. H eterodimerization o f the t ranscription factors E2F-1 and DP-1 leads to cooperative trans-activation. Genes Dev. 7: 1850-1861.
    CrossRef
  7. Iwamoto M, Banerjee D, Menon LG, Jurkiewicz A, Rao PH, Kemeny NE, et al. 2004. Overexpression of E2F-1 in lung and liver metastases of human colon cancer is associated with gene amplification. Cancer Biol. Ther. 3: 395-399.
    CrossRef
  8. Kim CW, Kim HK, Vo MT, Lee HH, Kim HJ, Min YJ, et al. 2010. Tristetraprolin controls the stability of cIAP2 mRNA through binding to the 3'UTR of cIAP2 mRNA. Biochem. Biophys. Res. Commun. 400: 46-52.
    CrossRef
  9. Kim CW, Vo MT, Kim HK, Lee HH, Yoon NA, Lee BJ, et al. 2012. Ectopic over-expression of tristetraprolin in human cancer cells promotes biogenesis of let-7 by down-regulation of Lin28. Nucleic Acids Res. 40: 3856-3869.
    CrossRef
  10. Kim HK, Kim CW, Vo MT, Lee HH, Lee JY, Yoon NA, et al. 2012. Expression of proviral integration site for Moloney murine leukemia virus 1 (Pim-1) is post-transcriptionally regulated by tristetraprolin in cancer cells. J. Biol. Chem. 287:28770-28778.
    CrossRef
  11. Lee HH, Kim WT, Kim DH, Park JW, Kang TH, Chung JW, Leem SH. 2013. Tristetraprolin suppresses AHRR expression through mRNA destabilization. FEBS Lett. 587: 1518-1523.
    CrossRef
  12. Lee HH, Son YJ, Lee WH, Park YW, Chae SW, Cho WJ, et al. 2010. Tristetraprolin regulates expression of VEGF and tumorigenesis in human colon cancer. Int. J. Cancer 126:1817-1827.
  13. Lee HH, Vo MT, Kim HJ, Lee UH, Kim CW, Kim HK, et al. 2010. Stability of the LATS2 tumor suppressor gene is regulated by tristetraprolin. J. Biol. Chem. 285: 17329-17337.
    CrossRef
  14. Lee HH, Yoon NA, Vo MT, Kim CW, Woo JM, Cha HJ, et al. 2012. Tristetraprolin down-regulates IL-17 through mRNA destabilization. FEBS Lett. 586: 41-46.
    CrossRef
  15. Lee JY, Kim HJ, Yoon NA, Lee WH, Min YJ, Ko BK, et al. 2013. Tumor suppressor p53 plays a key role in induction of both tristetraprolin and let-7 in human cancer cells. Nucleic Acids Res. 41: 5614-5625.
    CrossRef
  16. Pierce AM, Fisher SM, Conti CJ, Johnson DG. 1998. Deregulated expression of E2F1 induces hyperplasia and cooperates with ras in skin tumor development. Oncogene 16: 1267-1276.
    CrossRef
  17. Pierce AM, Gimenez-Conti IB, Schneider-Broussard R, Martinez LA, Conti CJ, Johnson DG. 1998. Increased E2F1 activity induces skin tumors in mice heterozygous and nullizygous for p53. Proc. Natl. Acad. Sci. USA 95: 8858-8863.
    CrossRef
  18. Raghavan A, Robison RL, McNabb J, Miller CR, Williams DA, Bohjanen PR. 2001. HuA and tristetraprolin are induced following T cell activation and display distinct but overlapping RNA binding specificities. J. Biol. Chem. 276:47958-47965.
  19. Shim J, Lim H, Yates R, Karin M. 2002. Nuclear export of NF90 is required for interleukin-2 mRNA stabilization. Mol. Cell 10: 1331-1344.
    CrossRef
  20. Wikonkal NM, Remenyik E, Knezevic D, Zhang W, Liu M, Zhao H, et al. 2003. Inactivating E2f1 reverts apoptosis resistance and cancer sensitivity in Trp53-deficient mice. Nat. Cell Biol. 5: 655-660.
    CrossRef
  21. Zhang SY, Liu SC, Al-Saleem LF, Holloran D, Babb J, Guo X, Klein-Szanto AJ. 2000. E2F-1: a proliferative marker of breast neoplasia. Cancer Epidemiol. Biomarkers Prev. 9: 395401.
  22. Zhang SY, Liu SC, Johnson DG, Klein-Szanto AJ. 2000. E2F1 gene transfer enhances invasiveness of human head and neck carcinoma cell lines. Cancer Res. 60: 5972-5976.

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Article

Research article

J. Microbiol. Biotechnol. 2014; 24(2): 287-294

Published online February 28, 2014 https://doi.org/10.4014/jmb.1309.09070

Copyright © The Korean Society for Microbiology and Biotechnology.

Tristetraprolin Regulates Prostate Cancer Cell Growth Through Suppression of E2F1

Hyun Hee Lee 1, Se-Ra Lee 1 and Sun-Hee Leem 1*

Department of Biological Sciences, Dong-A University, Busan 604-714, Republic of Korea

Received: September 25, 2013; Accepted: October 15, 2013

Abstract

The transcription factor E2F1 is active during G1 to S transition and is involved in the cell
cycle and progression. A recent study reported that increased E2F1 is associated with DNA
damage and tumor development in several tissues using transgenic models. Here, we show
that E2F1 expression is regulated by tristetraprolin (TTP) in prostate cancer. Overexpression of
TTP decreased the stability of E2F1 mRNA and the expression level of E2F1. In contrast,
inhibition of TTP using siRNA increased the E2F1 expression. E2F1 mRNA contains three
AREs within the 3’UTR, and TTP destabilized a luciferase mRNA that contained the E2F1
mRNA 3’UTR. Analyses of point mutants of the E2F1 mRNA 3’UTR demonstrated that ARE2
was mostly responsible for the TTP-mediated destabilization of E2F1 mRNA. RNA EMSA
revealed that TTP binds directly to the E2F1 mRNA 3’UTR of ARE2. Moreover, treatment with
siRNA against TTP increased the proliferation of PC3 human prostate cancer cells. Taken
together, these results demonstrate that E2F1 mRNA is a physiological target of TTP and
suggests that TTP controls proliferation as well as migration and invasion through the
regulation of E2F1 mRNA stability.

Keywords: ARE-binding protein, TTP, E2F1, prostate cancer, gene regulation

References

  1. Brennan SE, 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.
    CrossRef
  2. Cha HJ, Lee HH, Chae SW, Cho WJ, Kim YM, Choi HJ, et al. 2011. Tristetraprolin downregulates the expression of both VEGF and COX-2 in human colon cancer. Hepatogastroenterology 58: 790-795.
  3. Chen CY, Shyu AB. 1995. AU-rich elements: characterization and importance in mRNA degradation. Trends Biochem. Sci. 20: 465-470.
    CrossRef
  4. DeGregori J, Kowalik T, Nevins JR. 1995. Cellular targets for activation by the E2F1 transcription factor include DNA synthesis- and G1/S-regulatory genes. Mol. Cell Biol. 15:4215-4224.
  5. Gorgoulis VG, Zacharatos P, Mariatos G, Kotsinas A, Bouda M, Kletsas D, et al. 2002. Transcription factor E2F-1 acts as a growth-promoting factor and is associated with adverse prognosis in non-small cell lung carcinomas. J. Pathol. 198:142-156.
    CrossRef
  6. Helin K, Wu CL, Fattaey AR, Lees JA, Dynlacht BD, Ngwu C, H arlow E. 1 993. H eterodimerization o f the t ranscription factors E2F-1 and DP-1 leads to cooperative trans-activation. Genes Dev. 7: 1850-1861.
    CrossRef
  7. Iwamoto M, Banerjee D, Menon LG, Jurkiewicz A, Rao PH, Kemeny NE, et al. 2004. Overexpression of E2F-1 in lung and liver metastases of human colon cancer is associated with gene amplification. Cancer Biol. Ther. 3: 395-399.
    CrossRef
  8. Kim CW, Kim HK, Vo MT, Lee HH, Kim HJ, Min YJ, et al. 2010. Tristetraprolin controls the stability of cIAP2 mRNA through binding to the 3'UTR of cIAP2 mRNA. Biochem. Biophys. Res. Commun. 400: 46-52.
    CrossRef
  9. Kim CW, Vo MT, Kim HK, Lee HH, Yoon NA, Lee BJ, et al. 2012. Ectopic over-expression of tristetraprolin in human cancer cells promotes biogenesis of let-7 by down-regulation of Lin28. Nucleic Acids Res. 40: 3856-3869.
    CrossRef
  10. Kim HK, Kim CW, Vo MT, Lee HH, Lee JY, Yoon NA, et al. 2012. Expression of proviral integration site for Moloney murine leukemia virus 1 (Pim-1) is post-transcriptionally regulated by tristetraprolin in cancer cells. J. Biol. Chem. 287:28770-28778.
    CrossRef
  11. Lee HH, Kim WT, Kim DH, Park JW, Kang TH, Chung JW, Leem SH. 2013. Tristetraprolin suppresses AHRR expression through mRNA destabilization. FEBS Lett. 587: 1518-1523.
    CrossRef
  12. Lee HH, Son YJ, Lee WH, Park YW, Chae SW, Cho WJ, et al. 2010. Tristetraprolin regulates expression of VEGF and tumorigenesis in human colon cancer. Int. J. Cancer 126:1817-1827.
  13. Lee HH, Vo MT, Kim HJ, Lee UH, Kim CW, Kim HK, et al. 2010. Stability of the LATS2 tumor suppressor gene is regulated by tristetraprolin. J. Biol. Chem. 285: 17329-17337.
    CrossRef
  14. Lee HH, Yoon NA, Vo MT, Kim CW, Woo JM, Cha HJ, et al. 2012. Tristetraprolin down-regulates IL-17 through mRNA destabilization. FEBS Lett. 586: 41-46.
    CrossRef
  15. Lee JY, Kim HJ, Yoon NA, Lee WH, Min YJ, Ko BK, et al. 2013. Tumor suppressor p53 plays a key role in induction of both tristetraprolin and let-7 in human cancer cells. Nucleic Acids Res. 41: 5614-5625.
    CrossRef
  16. Pierce AM, Fisher SM, Conti CJ, Johnson DG. 1998. Deregulated expression of E2F1 induces hyperplasia and cooperates with ras in skin tumor development. Oncogene 16: 1267-1276.
    CrossRef
  17. Pierce AM, Gimenez-Conti IB, Schneider-Broussard R, Martinez LA, Conti CJ, Johnson DG. 1998. Increased E2F1 activity induces skin tumors in mice heterozygous and nullizygous for p53. Proc. Natl. Acad. Sci. USA 95: 8858-8863.
    CrossRef
  18. Raghavan A, Robison RL, McNabb J, Miller CR, Williams DA, Bohjanen PR. 2001. HuA and tristetraprolin are induced following T cell activation and display distinct but overlapping RNA binding specificities. J. Biol. Chem. 276:47958-47965.
  19. Shim J, Lim H, Yates R, Karin M. 2002. Nuclear export of NF90 is required for interleukin-2 mRNA stabilization. Mol. Cell 10: 1331-1344.
    CrossRef
  20. Wikonkal NM, Remenyik E, Knezevic D, Zhang W, Liu M, Zhao H, et al. 2003. Inactivating E2f1 reverts apoptosis resistance and cancer sensitivity in Trp53-deficient mice. Nat. Cell Biol. 5: 655-660.
    CrossRef
  21. Zhang SY, Liu SC, Al-Saleem LF, Holloran D, Babb J, Guo X, Klein-Szanto AJ. 2000. E2F-1: a proliferative marker of breast neoplasia. Cancer Epidemiol. Biomarkers Prev. 9: 395401.
  22. Zhang SY, Liu SC, Johnson DG, Klein-Szanto AJ. 2000. E2F1 gene transfer enhances invasiveness of human head and neck carcinoma cell lines. Cancer Res. 60: 5972-5976.