Expression of proviral integration site for moloney murine leukemia virus 1 (Pim-1) is post-transcriptionally regulated by tristetraprolin in cancer cells

Journal of Biological Chemistry

Volumn 287, Issue 34, 2012, Pages 28770-28778

  Kim, Hong Kyeung ^a   Kim, Chae Won ^a   Vo, Mai Tram ^a   Lee, Hyun Hee ^a   Lee, Ji Young ^a   Yoon, Nal Ae ^a   Lee, Chae Yeong ^a   Moon, Chang Hoon ^b   Min, Young Joo ^b   Park, Jeong Woo ^a   Cho, Wha Ja ^b  

^a University of Ulsan   (South Korea)

^b University of Ulsan College of Medicine   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

AU-RICH ELEMENTS; CANCER CELLS; CELL-CYCLE PROGRESSION; HUMAN CANCER; HUMAN CANCER CELLS; INHIBITORY EFFECT; MRNA STABILITY; MURINE LEUKEMIA VIRUS; OVER-EXPRESSION; TRISTETRAPROLIN; TUMOR SUPPRESSION;

AMINO ACIDS; CELL DEATH; DISEASES; GROWTH KINETICS; PHOSPHORYLATION; VIRUSES;

CELL GROWTH;

COMPLEMENTARY DNA; MESSENGER RNA; PROTEIN KINASE PIM 1; PROTEIN P21; PROTEIN P27; SMALL INTERFERING RNA; TRISTETRAPROLIN;

3' UNTRANSLATED REGION; ARTICLE; CANCER CELL CULTURE; CELL CYCLE; CELL GROWTH; CELL STRAIN LNCAP; CONTROLLED STUDY; DOWN REGULATION; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; MALE; ONCOGENE; PIM 1 GENE; PRIORITY JOURNAL; PROSTATE CARCINOMA; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; PROTO ONCOGENE; RNA STABILITY; TRANSCRIPTION REGULATION;

3' UNTRANSLATED REGIONS; GENE EXPRESSION REGULATION, NEOPLASTIC; HELA CELLS; HUMANS; NEOPLASMS; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-PIM-1; RNA STABILITY; RNA, NEOPLASM; TRISTETRAPROLIN;

EID: 84865237099     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.376483     Document Type: Article

References (44)

1. Wang, Z., Bhattacharya, N., Weaver, M., Petersen, K., Meyer, M., Gapter, L., and Magnuson, N. S. (2001) Pim-1: a serine/threonine kinase with a role in cell survival, proliferation, differentiation, and tumorigenesis. J. Vet. Sci. 2, 167-179
2. Bachmann, M., and Möröy, T. (2005) The serine/threonine kinase Pim-1. Int. J. Biochem. Cell Biol. 37, 726-730
3. Brault, L., Gasser, C., Bracher, F., Huber, K., Knapp, S., and Schwaller, J. (2010) PIM serine/threonine kinases in the pathogenesis and therapy of hematologic malignancies and solid cancers. Haematologica 95, 1004-1015
4. Zhang, Y., Wang, Z., Li, X., and Magnuson, N. S. (2008) Pim kinase-dependent inhibition of c-Myc degradation. Oncogene 27, 4809-4819
5. Wang, Z., Bhattacharya, N., Mixter, P. F., Wei, W., Sedivy, J., and Magnuson, N. S. (2002) Phosphorylation of the cell cycle inhibitor p21Cip1/WAF1 by Pim-1 kinase. Biochim. Biophys. Acta 1593, 45-55 (Pubitemid 35335911)
6. Zhang, Y., Wang, Z., and Magnuson, N. S. (2007) Pim-1 kinase-dependent phosphorylation of p21Cip1/WAF1 regulates its stability and cellular localization in H1299 cells. Mol. Cancer Res. 5, 909-922 (Pubitemid 47416668)
7. Morishita, D., Katayama, R., Sekimizu, K., Tsuruo, T., and Fujita, N. (2008) Pim kinases promote cell cycle progression by phosphorylating and downregulating p27Kip1 at the transcriptional and post-transcriptional levels. Cancer Res. 68, 5076-5085
8. van Lohuizen, M., Verbeek, S., Krimpenfort, P., Domen, J., Saris, C., Radaszkiewicz, T., and Berns, A. (1989) Predisposition to lymphomagenesis in pim-1 transgenic mice: cooperation with c-myc and N-myc in murine leukemia virus-induced tumors. Cell 56, 673-682 (Pubitemid 19065532)
9. Zippo, A., De Robertis, A., Serafini, R., and Oliviero, S. (2007) PIM-1-dependent phosphorylation of histone H3 at serine 10 is required for MYC-dependent transcriptional activation and oncogenic transformation. Nat. Cell Biol. 9, 932-944 (Pubitemid 47190448)
10. Nosaka, T., Kawashima, T., Misawa, K., Ikuta, K., Mui, A. L., and Kitamura, T. (1999) STAT5 as a molecular regulator of proliferation, differentiation, and apoptosis in hematopoietic cells. EMBO J. 18, 4754-4765 (Pubitemid 29415529)
11. Kim, K. T., Baird, K., Ahn, J. Y., Meltzer, P., Lilly, M., Levis, M., and Small, D. (2005) Pim-1 is up-regulated by constitutively activated FLT3 and plays a role in FLT3-mediated cell survival. Blood 105, 1759-1767 (Pubitemid 40223700)
12. Meeker, T. C., Nagarajan, L., ar-Rushdi, A., and Croce, C. M. (1987) Cloning and characterization of the human PIM-1 gene: a putative oncogene related to the protein kinases. J. Cell. Biochem. 35, 105-112
13. Dhanasekaran, S. M., Barrette, T. R., Ghosh, D., Shah, R., Varambally, S., Kurachi, K., Pienta, K. J., Rubin, M. A., and Chinnaiyan, A. M. (2001) Delineation of prognostic biomarkers in prostate cancer. Nature 412, 822-826 (Pubitemid 32801464)
14. Chiang, W. F., Yen, C. Y., Lin, C. N., Liaw, G. A., Chiu, C. T., Hsia, Y. J., and Liu, S. Y. (2006) Up-regulation of a serine/threonine kinase proto-oncogene Pim-1 in oral squamous cell carcinoma. Int. J. Oral Maxillofac. Surg. 35, 740-745
15. Warnecke-Eberz, U., Bollschweiler, E., Drebber, U., Metzger, R., Baldus, S. E., Hölscher, A. H., and Mönig, S. (2009) Prognostic impact of protein overexpression of the proto-oncogene PIM-1 in gastric cancer. Anticancer Res. 29, 4451-4455
16. Xu, D., Allsop, S. A., Witherspoon, S. M., Snider, J. L., Yeh, J. J., Fiordalisi, J. J., White, C. D., Williams, D., Cox, A. D., and Baines, A. T. (2011) The oncogenic kinase Pim-1 is modulated by K-Ras signaling and mediates transformed growth and radioresistance in human pancreatic ductal adenocarcinoma cells. Carcinogenesis 32, 488-495
17. Guo, S., Mao, X., Chen, J., Huang, B., Jin, C., Xu, Z., and Qiu, S. (2010) Overexpression of Pim-1 in bladder cancer. J Exp. Clin. Cancer Res. 29, 161
18. Adam, M., Pogacic, V., Bendit, M., Chappuis, R., Nawijn, M. C., Duyster, J., Fox, C. J., Thompson, C. B., Cools, J., and Schwaller, J. (2006) Targeting PIM kinases impairs survival of hematopoietic cells transformed by kinase inhibitor-sensitive and kinase inhibitor-resistant forms of Fms-like tyrosine kinase 3 and BCR/ABL. Cancer Res. 66, 3828-3835
19. Hu, X. F., Li, J., Vandervalk, S., Wang, Z., Magnuson, N. S., and Xing, P. X. (2009) PIM-1-specific mAb suppresses human and mouse tumor growth by decreasing PIM-1 levels, reducing Akt phosphorylation, and activating apoptosis. J. Clin. Invest. 119, 362-375
20. Blanco-Aparicio, C., Collazo, A. M., Oyarzabal, J., Leal, J. F., Albarán, M. I., Lima, F. R., Pequeño, B., Ajenjo, N., Becerra, M., Alfonso, P., Reymundo, M. I., Palacios, I., Mateos, G., Quiñones, H., Corrionero, A., Carnero, A., Pevarello, P., Lopez, A. R., Fominaya, J., Pastor, J., and Bischoff, J. R. (2011) Pim-1 kinase inhibitor ETP-45299 suppresses cellular proliferation and synergizes with PI3K inhibition. Cancer Lett. 300, 145-153
21. Lin, Y. W., Beharry, Z. M., Hill, E. G., Song, J. H., Wang, W., Xia, Z., Zhang, Z., Aplan, P. D., Aster, J. C., Smith, C. D., and Kraft, A. S. (2010) A small molecule inhibitor of Pim protein kinases blocks the growth of precursor T-cell lymphoblastic leukemia/lymphoma. Blood 115, 824-833
22. Amaravadi, R., and Thompson, C. B. (2005) The survival kinases Akt and Pim as potential pharmacological targets. J. Clin. Invest. 115, 2618-2624 (Pubitemid 41434384)
23. Cuypers, H. T., Selten, G., Quint, W., Zijlstra, M., Maandag, E. R., Boelens, W., van Wezenbeek, P., Melief, C., and Berns, A. (1984) Murine leukemia virus-induced T-cell lymphomagenesis: integration of proviruses in a distinct chromosomal region. Cell 37, 141-150 (Pubitemid 14079845)
24. Selten, G., Cuypers, H. T., Boelens, W., Robanus-Maandag, E., Verbeek, J., Domen, J., van Beveren, C., and Berns, A. (1986) The primary structure of the putative oncogene pim-1 shows extensive homology with protein kinases. Cell 46, 603-611 (Pubitemid 16022415)
25. Wingett, D., Reeves, R., and Magnuson, N. S. (1991) Stability changes in pim-1 proto-oncogene mRNA after mitogen stimulation of normal lymphocytes. J. Immunol. 147, 3653-3659
26. Shyu, A. B., and Wilkinson, M. F. (2000) The double lives of shuttling mRNA-binding proteins. Cell 102, 135-138
27. Blackshear, P. J. (2002) Tristetraprolin and other CCCH tandem zincfinger proteins in the regulation of mRNA turnover. Biochem. Soc. Trans. 30, 945-952
28. Chen, C. Y., Gherzi, R., Ong, S. E., Chan, E. L., Raijmakers, R., Pruijn, G. J., Stoecklin, G., Moroni, C., Mann, M., and Karin, M. (2001) AU-binding proteins recruit the exosome to degrade ARE-containing mRNAs. Cell 107, 451-464 (Pubitemid 33152781)
29. Brennan, S. E., Kuwano, Y., Alkharouf, N., Blackshear, P. J., Gorospe, M., and Wilson, G. M. (2009) The mRNA-destabilizing protein tristetraprolin is suppressed in many cancers, altering tumorigenic phenotypes and patient prognosis. Cancer Res. 69, 5168-5176
30. Young, L. E., Sanduja, S., Bemis-Standoli, K., Pena, E. A., Price, R. L., and Dixon, D. A. (2009) The mRNA-binding proteins HuR and tristetraprolin regulate cyclooxygenase-2 expression during colon carcinogenesis. Gastroenterology 136, 1669-1679
31. Lee, H. H., Son, Y. J., Lee, W. H., Park, Y. W., Chae, S. W., Cho, W. J., Kim, Y. M., Choi, H. J., Choi, D. H., Jung, S. W., Min, Y. J., Park, S. E., Lee, B. J., Cha, H. J., and Park, J. W. (2010) Tristetraprolin regulates expression of VEGF and tumorigenesis in human colon cancer. Int. J. Cancer 126, 1817-1827
32. Lee, H. H., Vo, M. T., Kim, H. J., Lee, U. H., Kim, C. W., Kim, H. K., Ko, M. S., Lee, W. H., Cha, S. J., Min, Y. J., Choi, D. H., Suh, H. S., Lee, B. J., Park, J. W., and Cho, W. J. (2010) Stability of the LATS2 tumor suppressor gene is regulated by tristetraprolin. J. Biol. Chem. 285, 17329-17337
33. Domen, J., Von Lindern, M., Hermans, A., Breuer, M., Grosveld, G., and Berns, A. (1987) Comparison of the human and mouse PIM-1 cDNAs: nucleotide sequence and immunological identification of the in vitro synthesized PIM-1 protein. Oncogene Res. 1, 103-112 (Pubitemid 18041731)
34. Saris, C. J., Domen, J., and Berns, A. (1991) The pim-1 oncogene encodes two related serine/threonine protein kinases by alternative initiation at AUG and CUG. EMBO J. 10, 655-664 (Pubitemid 21905520)
35. Carballo, E., Lai, W. S., and Blackshear, P. J. (1998) Feedback inhibition of macrophage tumor necrosis factor-α production by tristetraprolin. Science 281, 1001-1005 (Pubitemid 28399252)
36. Lilly, M., and Kraft, A. (1997) Enforced expression of the Mr 33,000 Pim-1 kinase enhances factor-independent survival and inhibits apoptosis in murine myeloid cells. Cancer Res. 57, 5348-5355 (Pubitemid 27516373)
37. Shah, N., Pang, B., Yeoh, K. G., Thorn, S., Chen, C. S., Lilly, M. B., and Salto-Tellez, M. (2008) Potential roles for the PIM-1 kinase in human cancer - a molecular and therapeutic appraisal. Eur. J. Cancer 44, 2144-2151
38. Bullock, A. N., Debreczeni, J. E., Fedorov, O. Y., Nelson, A., Marsden, B. D., and Knapp, S. (2005) Structural basis of inhibitor specificity of the human proto-oncogene proviral insertion site in Moloney murine leukemia virus (PIM-1) kinase. J. Med. Chem. 48, 7604-7614 (Pubitemid 41698801)
39. Cheney, I. W., Yan, S., Appleby, T., Walker, H., Vo, T., Yao, N., Hamatake, R., Hong, Z., and Wu, J. Z. (2007) Identification and structure-activity relationships of substituted pyridones as inhibitors of Pim-1 kinase. Bioorg. Med. Chem. Lett. 17, 1679-1683 (Pubitemid 46274341)
40. Holder, S., Zemskova, M., Zhang, C., Tabrizizad, M., Bremer, R., Neidigh, J. W., and Lilly, M. B. (2007) Characterization of a potent and selective small molecule inhibitor of the PIM-1 kinase. Mol. Cancer Ther. 6, 163-172 (Pubitemid 46206679)
41. Scott, M. T., Ingram, A., and Ball, K. L. (2002) PDK1-dependent activation of atypical PKC leads to degradation of the p21 tumor modifier protein. EMBO J. 21, 6771-6780 (Pubitemid 36014549)
42. Li, Y., Dowbenko, D., and Lasky, L. A. (2002) AKT/PKB phosphorylation of p21Cip/WAF1 enhances protein stability of p21Cip/WAF1 and promotes cell survival. J. Biol. Chem. 277, 11352-11361 (Pubitemid 34952901)
43. Coleman, M. L., Marshall, C. J., and Olson, M. F. (2003) Ras promotes p21Waf1/Cip1 protein stability via a cyclin D1-imposed block in protea-some- mediated degradation. EMBO J. 22, 2036-2046 (Pubitemid 36565529)
44. Jascur, T., Brickner, H., Salles-Passador, I., Barbier, V., El Khissiin, A., Smith, B., Fotedar, R., and Fotedar, A. (2005) Regulation of p21WAF1/CIP1 stability by WISp39, a Hsp90-binding TPR protein. Mol. Cell 17, 237-249 (Pubitemid 40138618)